Intraspinal Variations of Nerve Roots [1st ed.] 978-3-030-01685-2, 978-3-030-01686-9

Table of contents :
Front Matter ....Pages i-ix
Front Matter ....Pages 1-1
The Composition and Structure of Peripheral Nerves (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 3-13
Injuries of the Peripheral Nerves (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 15-24
Neuropathies (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 25-30
Regeneration of Peripheral Nerves (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 31-38
Terminology (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 39-42
Front Matter ....Pages 43-43
General Description (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 45-51
Overlapping Innervations and Embryonic Explanations (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 53-59
Front Matter ....Pages 61-61
General Description (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 63-66
Our Observations and Results (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 67-101
Front Matter ....Pages 103-103
Connections Between Cervical Spinal Nerve Roots (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 105-110
Connections Between Ventral Rootlets and Dorsal Rootlets (Separately) in the Region of Lumbosacral Enlargement (Intumescentia Lumbosacralis) and Cauda Equina (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 111-117
Details of Relationship Between the Ventral and Dorsal Rootlets in the Region of Spinal Ganglion of the Lumbosacral Plexus (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 119-133
Front Matter ....Pages 135-135
General Description (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 137-145
Extradural Connections of the Lumbosacral Nerve Roots (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 147-153
Front Matter ....Pages 155-155
Axonal Pathways to Innervation Regions of the Upper Limbs (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 157-165
Axonal Pathways to the Innervation Regions of the Lower Limbs (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 167-171
Anastomoses Between the Individual Nerves and Inside Nerves (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 173-178
Conclusion (Viktor Matejčík, Zora Haviarová, Roman Kuruc, Andrej Šteňo, Juraj Šteňo)....Pages 179-181

Citation preview

Intraspinal Variations of Nerve Roots Viktor Matejčík Zora Haviarová Roman Kuruc Andrej Šteňo Juraj Šteňo

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Intraspinal Variations of Nerve Roots

Viktor Matejčík • Zora Haviarová Roman Kuruc • Andrej Šteňo • Juraj Šteňo

Intraspinal Variations of Nerve Roots

Viktor Matejčík Department of Neurosurgery Comenius University Bratislava Slovakia

Zora Haviarová Institute of Anatomy Comenius University Bratislava Slovakia

Roman Kuruc The Health Surveillance Authority Bratislava Slovakia

Andrej Šteňo Department of Neurosurgery Comenius University Bratislava Slovakia

Juraj Šteňo Department of Neurosurgery Comenius University Bratislava Slovakia

ISBN 978-3-030-01685-2    ISBN 978-3-030-01686-9 (eBook) https://doi.org/10.1007/978-3-030-01686-9 Library of Congress Control Number: 2018967962 © Springer Nature Switzerland AG 2019 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

A desire to help students and physicians to understand the complexity of the peripheral nervous system in relation to the diagnosis and treatment inspired us to write this book. It might be the illustrative enhancement in the context of the undergraduate study for students as well as for postgraduate education for doctors. Figures, though intricate at a glance, are sufficiently illustrative, helping a neurologist, neurosurgeon, and doctors of other specialties to illuminate in the memory anatomical variabilities of the intraspinal peripheral nervous system. References in the text were specified only where it was necessary. The extent of the monograph is not large, but it is meant to be a contribution to the knowledge of the full width of intraspinal anatomical variabilities. The book is based on the experience and specific work of the authors and the complement of the previous monographs dealing with the variability of the brachial and lumbosacral plexus. The structure of the peripheral nervous system and intraspinal variabilities due to their unpredictability can sometimes be associated with great complexity and even insolvability. Solutions cannot be formulated in the form of any mathematical expression or “formula”. We have to cope with a substantial reality: even though principles of the observed system are known and are relatively simple, it is impossible to calculate the future development of the system. Even behind this seemingly complicated natural beauty, one has to seek the repetition of simple rules. It appears that natural creations, including the construction of the human body, in many cases resemble a fractal approach. Bratislava, Slovakia Bratislava, Slovakia  Bratislava, Slovakia  Bratislava, Slovakia  Bratislava, Slovakia 

Viktor Matejčík Zora Haviarová Roman Kuruc Andrej Šteňo Juraj Šteňo

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Contents

Part I General Part 1 The Composition and Structure of Peripheral Nerves ��������������������������   3 References����������������������������������������������������������������������������������������������������  13 2 Injuries of the Peripheral Nerves ������������������������������������������������������������  15 References����������������������������������������������������������������������������������������������������  24 3 Neuropathies����������������������������������������������������������������������������������������������  25 References����������������������������������������������������������������������������������������������������  30 4 Regeneration of Peripheral Nerves����������������������������������������������������������  31 References����������������������������������������������������������������������������������������������������  38 5 Terminology������������������������������������������������������������������������������������������������  39 References����������������������������������������������������������������������������������������������������  42 Part II Vertebral Column and Spinal Cord 6 General Description ����������������������������������������������������������������������������������  45 References����������������������������������������������������������������������������������������������������  51 7 Overlapping Innervations and Embryonic Explanations����������������������  53 References����������������������������������������������������������������������������������������������������  59 Part III Intraspinal Connections of Nerve Roots 8 General Description ����������������������������������������������������������������������������������  63 References����������������������������������������������������������������������������������������������������  65 9 Our Observations and Results������������������������������������������������������������������  67 References���������������������������������������������������������������������������������������������������� 100

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Contents

Part IV Intradural Connections of Spinal Nerve Roots 10 Connections Between Cervical Spinal Nerve Roots�������������������������������� 105 References���������������������������������������������������������������������������������������������������� 110 11 Connections Between Ventral Rootlets and Dorsal Rootlets (Separately) in the Region of Lumbosacral Enlargement (Intumescentia Lumbosacralis) and Cauda Equina ������������������������������ 111 References���������������������������������������������������������������������������������������������������� 117 12 Details of Relationship Between the Ventral and Dorsal Rootlets in the Region of Spinal Ganglion of the Lumbosacral Plexus������������������������������������������������������������������������ 119 12.1 Intraspinal, Intradural, and Extradural Anomalies of Communicating Branches������������������������������������������������������������ 127 Part V Extradural Spinal Nerve Roots Connection 13 General Description ���������������������������������������������������������������������������������� 137 References���������������������������������������������������������������������������������������������������� 144 14 Extradural Connections of the Lumbosacral Nerve Roots�������������������� 147 References���������������������������������������������������������������������������������������������������� 152 Part VI Anastomoses in the Region of Plexuses 15 Axonal Pathways to Innervation Regions of the Upper Limbs ������������ 157 15.1 Ulnar Nerve�������������������������������������������������������������������������������������� 162 15.2 Median Nerve������������������������������������������������������������������������������������ 162 References���������������������������������������������������������������������������������������������������� 165 16 Axonal Pathways to the Innervation Regions of the Lower Limbs������������������������������������������������������������������������������������ 167 16.1 Obturator Nerve�������������������������������������������������������������������������������� 170 16.2 Sciatic Nerve ������������������������������������������������������������������������������������ 170 16.3 Tibial Nerve�������������������������������������������������������������������������������������� 171 16.4 Fibular Nerve������������������������������������������������������������������������������������ 171 References���������������������������������������������������������������������������������������������������� 171 17 Anastomoses Between the Individual Nerves and Inside Nerves���������� 173 17.1 Characteristics of the Macroscopic Structure of the Peripheral Nerves�������������������������������������������������������������������� 173 17.2 Anastomoses Inside the Nerves�������������������������������������������������������� 175 17.3 The Musculocutaneous Nerve���������������������������������������������������������� 176 17.4 Lumbosacral Plexus�������������������������������������������������������������������������� 177 References���������������������������������������������������������������������������������������������������� 178 18 Conclusion�������������������������������������������������������������������������������������������������� 179 References���������������������������������������������������������������������������������������������������� 181

Abbreviations

bilat. Bilateral C Cervical CNS Central nervous system CSF Cerebrospinal fluid CT Computed tomography dx. Dextra epi Epineurium FBSS Failed back surgery syndrome L Lumbar LIS Lumboischialgic syndrome LS Lumbosacral m. Musculus MRI Magnetic resonance imaging n. Nervus nn. Nervi PNS Peripheral nervous system PMG Perimyelography postfix. Postfixed prefix. Prefixed S Sacral sin. Sinistra T Thoracic

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Part I General Part

1

The Composition and Structure of Peripheral Nerves

The brain and its caudal continuation, the spinal cord, connect to the peripherals via the peripheral nervous system. In no system is such a large amount of functional capacity concentrated in such a small volume of tissue than in the cervical spine, which contains all structures that control the somatic functions and most of the visceral functions from the neck caudally. For a larger volume of connective tissue, peripheral nerves have less functional content. The spinal cord is surrounded by the meninges, which are continuing from the level of the foramen magnum down to the second lumbar vertebra, where the spinal dural sac ends blindly (Fig.  1.1). They are separated from the wall of the spinal canal by the epidural space containing fatty tissue and the venous plexus. Between the dura mater and the arachnoidea, there is a subdural space containing a clear film of fluid similar to lymph. The arachnoidea is a thin membrane and ends at the level of the second sacral vertebra. It is separated from the pia mater by subarachnoid space, which contains fine mesothelial septa and liquor cerebrospinalis, i.e. cerebrospinal fluid (CSF). Spinal nerve roots are surrounded by the arachnoid up to the site where they penetrate the dura mater. The pia mater is a thin layer of vascular connective tissue that closely adheres to the spinal cord and its nerve roots. Under the conus medullaris, it proceeds as thin filum terminale continuing caudally among the nerve roots of cauda equina, and then it penetrates through the terminal portion of the arachnoid and the dura mater to end blindly in connective tissue behind the first vertebra of the coccyx (Fig. 1.2). On each side, the pia mater is attached to the dura mater through 22 tooth-like triangular processes—denticulate ligaments. The spinal cord has two spindle-like thickenings: cervical enlargement (intumescentia cervicalis) and lumbosacral enlargement (intumescentia lumbosacralis). Cervical enlargement projects to the spine from C3 to T2 with a maximum at C5. Lumbosacral enlargement projects from T9 to L1 with a maximum at T12 [1].

© Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_1

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1  The Composition and Structure of Peripheral Nerves

Fibrotic ligament

Fig. 1.1  Dural sac has blind ends fixed by fibrotic connective tissue at the level of the second lumbar vertebra

The first four cervical segments of the spinal cord are positioned behind the vertebrae C1–C4. The C5–T1 segments of the spinal cord range from the fifth cervical to the second thoracic vertebra. The T2–T12 segments of the spinal cord are localized behind the second down to the ninth thoracic vertebra, and the L1–L4 segments lay behind the tenth to the twelfth thoracic vertebra. The L5–S2 segments are located behind the body of the first lumbar vertebra; the S3–S5 segments behind the L1–L2 intervertebral space (in women) or to the cranial half of the second lumbar vertebra (in men). There are 31 pairs of spinal nerves extending from a particular intervertebral foramen (except for the first one, which leaves the vertebral column between the atlas and occipital bone), and the last two nerves—S5 and Co1 that pass through the sacral hiatus. The spinal dura mater surrounds the ventral (efferent) and dorsal (afferent) spinal roots (except the root C1 that does not have a dorsal root) lying close to each other when passing through it, and then the roots combine and form the spinal nerve, and the spinal dura mater fuses with their epineurium (Fig. 1.3). On the ventrolateral and dorsolateral spinal cord periphery, there are longitudinal grooves: anterolateral sulcus and posterolateral sulcus (sulcus anterolateralis et sulcus posterolateralis), from which nerve fibres extend from the spinal cord as anterior rootlets (fila radicularia anteriora) and connect to form the ventral spinal roots. Likewise, the posterior rootlets (fila radicularia posterior) form the dorsal roots. Each sensitive root is divided into several branches—rootlets. The distribution of the ventral roots to the rootlets is less obvious and arises closer to the spinal cord.

1  The Composition and Structure of Peripheral Nerves

5

Filum terminale

Fig. 1.2  Insertion of terminal filum behind the first coccygeal vertebra

The bodies of afferent cells stored in the spinal ganglia expand the dorsal root. They are parts of the dorsal roots of all spinal nerves except for the root C1 and located in the intervertebral foramina through which the nerves leave the spinal canal as mixed spinal nerves containing afferent and efferent fibres. Ganglia of sacral nerves and coccygeal nerve are placed in the sacral canal. The dorsal nerve root is generally thicker than the ventral one. A fibrous sheath, from which fibrous septa extend inside, covers the surface of a ganglion. Nerve fibres extending through the axis of the ganglion are primarily the processes of large nerve cells stored in the ganglion. When projecting out of the sensitive nerve cells in the dorsal root ganglion, the processes of the nerve cells are protected by myelin sheaths. The only exception is a short section of the fibre at the exit from the nerve cell and close to its peripheral termination, where the myelin sheath is missing. The central axon passes through the dorsal root into the dorsal horn of the spinal cord. Some of the axons enter the spinal cord without branching, the others in two or more branches themselves. Some central processes and processes entering the spinal cord themselves exceeds the number of ganglion cells by 43% [2–4].

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1  The Composition and Structure of Peripheral Nerves Pia mater Arachnoidea Dorsal root

Dura Spinal ganglion

Liquor

Epineurium Ventral root

Root sac Root sleeve - sheath

Fig. 1.3  Anatomy of the intraspinal portion of formation of the nerve root, meninges, and root sheaths

About 30% of axons in the ventral roots are unmyelinated fibres of the dorsal root ganglia. It is believed that they provide nociceptive functions. A majority of axons in the ventral roots are motor fibres. In addition to myelinated fibres, also thin unmyelinated fibres pass through the ganglion, and backwardly sympathetic fibres accompany nutrient arteries. Vascularization of ganglia is richer than of peripheral nerves due to the presence of nerve cells, which require richer arterial blood supply than their fibres. It is provided by branches of segmental spinal arteries and tiny branches of spinal arteries that lead to the ganglion from the spinal cord along the dorsal and vertebral roots. In the intervertebral foramen, nerve roots are coated by the dural sac elongations forming the root sacs. They pass distally through separate openings or join the sheaths of a nerve root. The dura mater and the arachnoid invaginate each dorsal and ventral root forming two individual sleeves. Thus, arachnoid adhesions in the region of root isthmus prevent the subarachnoid fluid from passing into the root sleeves. Meningeal sheaths continue along the spinal nerves and form a strong epineural sleeve. In dural sac elongations, the roots are coated with root sleeves, pass through the subarachnoid space, and float in the cerebrospinal fluid (CSF). A normal function of axons depends on the CSF that ensures their movement in the fluid. Surroundings of the nerve fibres are directly exposed to the influence and composition of the cerebrospinal fluid.

1  The Composition and Structure of Peripheral Nerves

7

Many studies have demonstrated liquid penetration from the CSF to and from perineural spaces enveloping nerve roots. Thus, a pathological process in the CSF or leptomeninges can affect spinal roots. The perineurium serves as a barrier of the nerve against the surrounding area and the liquor. It divides into the subarachnoid space at the entry; a large portion passes outside between the dura mater and the arachnoid mater, but several layers continue over the nerve as part of the root sheath. The root sheath is composed of the outer layer corresponding to the arachnoid, and the inner layer corresponding to the perineurium. The outer layer consists of sparsely arranged cells and continues to the pia mater. The inner layer consists of tabular cells and is closely linked to the basal lamina. It is continuation of the perineurium. These anatomical relations are of clinical relevance, as the free root sheaths protect nerve root fibres from chemical and mechanical noxious agents. However, they do not protect against stretching forces, and they are not suitable for the suture. The delicate collagenous tissue, the endoneurium, enters the fascicles from the perineurium. Sometimes it forms septa within fascicles where thin vessels are located. Directly on the surface of nerve fibres, around the basal membrane and Schwann cells, the endoneurium constitutes the endoneurial tube. The endoneurium remains unchanged from the peripheral nerves and spinal roots to the spinal cord. Intraspinal nerve roots are susceptible to different mechanical forces because the amount and arrangement of connective tissue are different from the peripheral nerve. In intraspinal parts of typical spinal nerve roots, their fibres are arranged in parallel without changing the density of connective tissue. Therefore, they are much more vulnerable to stretching forces. Since they have no epineural cover, they are also more susceptible to compression. Adhesions that compress the nerve roots and reduce their mobility, as well as a loss of elastic connective tissue accompanied by venous congestion, arterial compression and direct pressure can cause a pathophysiological mechanism sufficient to cause the onset of radiculopathy. A connection between the peripheral and central nervous system represents a transitional zone, which plays an important role in nerve root avulsions. Generally, it is the site where the rupture of roots in traction traumas occurs. In the transitional zone, the growth of axons supports the tissue of the peripheral nervous system— PNS and inhibits the tissue of the central nerve tissue—CNS [5, 6]. After an injury, nerve cells are not able to grow through the transitional zone to or from the spinal cord as the transitional zone is a very effective barrier preventing regeneration, which is important for surgical treatment of the spinal cord and spinal nerve roots injuries. The transitional zone is characterized by the presence and projection of the CNS tissue from the spinal cord together with the PNS tissue in the most proximal portion of the root.

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1  The Composition and Structure of Peripheral Nerves

In the CNS portion of the root, the bodies of fibrous astrocytes and a dense network of their processes dominate. The occurrence of astrocytes is ten times higher than in the white matter glia limitans. The glia limitans is a thin membrane of astrocyte processes associated with the dorsal membrane enclosing the brain and spinal cord. It is the outermost layer of nerve tissue. It prevents the migration of neurons and neuroglia into the meninges. This membrane lies under the pia mater and the subpial space on the surface of the spinal cord. The bodies of fibrous astrocytes project their astrocyte processes distally between the nerve fibres by the CNS portion of the root. Astrocyte processes separate and surround the myelinated nerve fibres as sheaths. In this way, the myelinated fibres continue from endoneurial spaces of the PNS to the CNS portion of the root. They present themselves as numerous canals or sheaths of the nerve fibres in the transitional zone between the PNS and the CNS. An extensive reorganization of dorsal root nerve fibres occurs when they reach the root portion of the CNS. This part of the root acts as a sieve. It organizes fibres of the same size and function and prepares them for the entry into various nerve tracts in the spinal cord. The largest fibres are located in the centre of the root, while thin myelinated and unmyelinated fibres are arranged on the periphery of the root and concentrated to the ventrolateral zone of the rootlet. The redistribution of the thinnest nerve fibres to the surface of nerve roots is an anatomical basis for superficial rhizotomy utilized in the treatment of pain. Myelinated fibres change the type of the organization and location of Ranvier’s grooves in the transitional zone. The irregular basal membrane of Schwann cells forms the external border of the CNS. There is the transition between astrocytes and Schwann cells in places where nerve fibres pass from the PNS to the CNS compartment of the root, and it presents a direct contact between the cells of the CNS and PNS. There is no structural border between the CNS and PNS.  The relationship between the PNS and CNS is more a sort of chemical border based on the contact inhibition, which prevents the “invasion” of one tissue to another, for example, overgrowth of Schwann cells into the spinal cord. Peripheral nerves connect the central nervous system with the peripheral receptors and executive organs by the system of sensitive, motor, and autonomic fibres. They are of different diameters and can be myelinated or unmyelinated. The peripheral nerve transmits information in the form of nerve impulses. A basic nerve unit is a nerve axon—the process of a nerve cell, which ensures axoplasmic transport (Fig. 1.4). A wavy course of axons protects them from damage due to stretching. Axolemma, myelin sheath, Schwann cells, basal membrane, endoneurium, and perineurium surround an axon. The basal membrane (Schwann sheath) is a continuous outer membrane, which spans over the nodes of Ranvier, separating the extracellular space of the nerve from its intracellular space. On the outside of the basal membrane, each nerve fibre is surrounded by the endoneurium—supporting tissue, which is generally formed by two collagen lamellae.

1  The Composition and Structure of Peripheral Nerves

9 Terminal axon branching

Body of the nerve cell Myelin sheath Nucleus

Axon

Dendrites with dendritic spines

Fig. 1.4  Diagram of a nerve cell

More nerve fibres (axons) are grouped together into a bundle—fascicle. Separate fascicles contain a heterogeneous mix of myelinated and unmyelinated nerve fibres. Inside the bundle between the nerve fibres, there is the connective tissue—endoneurium. It contains mucopolysaccharides, collagen, reticulin, cells (fibroblasts, macrophages), and blood vessels. It passes into the terminal branching of the axon and forms the endoneurial tube in which the nerve fibre (axon and Schwann cells with myelin) is closed. The correct understanding of the endoneurial tube is fundamental for explaining most of the pathological conditions affecting peripheral nerves. All degenerative and regenerative processes take place in this anatomical structure. In intraspinal nerve roots, the endoneurial collagen is sparse unlike in extraforaminally localized nerves. Each fascicle contains on average 10,000 axons. It has an outer coat—perineurium (Fig. 1.5). The perineurium forms a morphological unit of the fascicle. The inner layer of perineurium consists of squamous cells, and the outer layer consists of collagen fibres. It also contains blood vessels connecting the endoneurial and epineural vascular networks. There is the connective tissue between fascicles—the inner epineurium. Microcirculation of each fascicle is localized in the sparse connective tissue of the epineurium that surrounds it. Intrinsic blood flow in the fascicle is provided through mesoneural vessels of the nerve (Fig. 1.6). Sufficient vascularization is important for the conduction of nerve impulses. Nerve ischaemia may manifest as pain and results in the impairment of conduction velocity. Blood supply to the peripheral nerves is usually provided by tiny branches originating from the nearest arterial trunk. A distinct fascial sheet located between the artery and the nerve represents a serious barrier preventing the development of any nourishing branches to the nerve. The venous blood outflow is arranged similarly to the arterial supply. From the subcutaneous nerves, blood flows mostly into muscle veins. Draining venules from the nerves may lead directly to the venous plexuses in the walls of the arteries running in the neurovascular bundles. Since the endoneurium has no lymphatic vessels, the perineural pressure is required for epineural lymphatic drainage. Lymphatic vessels usually follow the arterial supply and venous drainage from the nerve to regional lymphatic nodes, but their passage along the nerve to the subarachnoid space is also

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1  The Composition and Structure of Peripheral Nerves Nerve fascicles Epineurium

Nerve fiber

Perineurium

The vessel nourshing nerve

Endoneurium

Fig. 1.5  Schematic cross section of the peripheral nerve

Blood supply of mezoneuria Mesoneurium

Epineural arterioles

Epineural vessels

Fig. 1.6  The vascular system of the peripheral nerve is supplied by the arteries through the mesoneurium, epineural vascular plexuses, and a rich network of anastomotic vessels of different calibre, branches of which obliquely penetrate the perineurium. The perineural plexus is composed of arterioles, veins, and capillaries. Open communication with endoneurial capillary bed is in progress

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possible. In certain pathological conditions, this arrangement of the lymphatic system may prevent spreading of infection along nerves to the nerve roots and meninges. Thin unmyelinated vegetative fibres are part of the peripheral nerves, too. They enter nerves mostly together with arteries and are of vasomotor nature. They are located in the epineurium and the perineurium where nutritive arteries have still a well-developed tunica media composed of smooth muscles. Around the whole nerve, there is the outer epineurium that connects it through the mesoneurium with surrounding structures. The epineurium comprises the collagenelastin matrix with fibroblasts, blood vessels, and mastoid cells. The fat content has a protective function preventing fascicles from damage by compression. Endoneurium, perineurium, and epineurium form connective fibrous tissue of the peripheral nerve. They do not only connect but also isolate and separate one portion of the nerve from the other. The amount of connective tissue in the nerve depends on the age, type of the nerve, and its level. It varies from 25% to 85%. With age, the amount of connective tissue in the nerve rises. At the level of the brachial plexus, the amount of connective tissue ranges from 57% to 85%. Its amount is higher in parts of nerves where they cross joints or in the nerves with a larger number of small fascicles. Connective tissue is responsible for the strength and elasticity of nerve fascicles. Intraspinal roots are tiny, delicate, fragile, and highly vulnerable to trauma. Peripheral nerves, in contrast, are strong and more resistant to trauma. The fascicular plexus is an important cause of the variability of the connective tissue arrangement (Fig. 1.7). The greatest amount of myelinated fibres is by people of 20–30 years old. A total number of myelinated fibres in the brachial plexus in adults are from 120,000 to 150,000. The fifth cervical and the first thoracic nerve contains the lowest number of myelinated fibres—from 15,000 to 20,000. The eighth cervical nerve is the largest, comprising about 30,000 myelinated fibres. The largest number of motor fibres is in C5–C8, and the lowest in C7, and T1 nerve roots. The greatest number of sensory fibres is found in C7, then C6, and then in C8. From the age of 30, the number of myelinated fibres progressively decreases; only 32% of average content was observed in people over 80 years. Peripheral nerves can be classified as follows: (a) Monofascicular—having one large fascicle. (b) Oligofascicular—having several large fascicles. (c) Polyfascicular—containing many fascicles that can be grouped, or the pattern may be undetectable. Each fascicle in the nerve may move forward and backward through thin connective tissue that encloses it. This allows an independent movement related to adjacent

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Fig. 1.7  Fascicular plexus

fascicles and the outer surface of the nerve, and in the region of the girdle roots, trunks, fascicles, and terminal branches of the brachial and lumbosacral plexus related to surrounding structures. In the regions such as the shoulder, elbow, and wrist, which require great mobility of the nerve, the mesoneurium is longer and more complex and contains more blood vessels. When the tension of the nerve with the flexion in the joint releases, vessels undulate and contract as a harmonica. There is the increase in tension while moving, and the vessels in the mesoneurium straighten and adapt to the position of the nerve. It seems that the blood vessels in the mesoneurium are responsible for the retraction of the nerve terminals following cut wounds. It is proved by the retraction of the nerve after its innervations. In the case of complete interruption, each fascicle can move forward or backward. This explains why some fascicles form the image with characteristic refractions. The surrounding supporting tissue that keeps them in a straight position and stretched, if damaged, cannot provide its tasks. Because of the formation of connective tissue, these changes increase with the time passing between the accident and the reconstruction of the nerve. A greater amount of fibrous tissue decreases the chance of accurate treatment and favourable functional outcome. Peripheral nerves have considerable strength and elasticity due to the perineurium that maintains the integrity of nerve trunks on tension. A fibrous coat provides peripheral nerves with considerable strength and flexibility. After peripheral neurotomy, both stumps shorten and set apart. Tensile strength is high, i.e. in the sciatic nerve it is about 60–70 kg.

References

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References 1. Borovanský L. a kol.: Soustavná anatomie člověka. 1. vyd. Praha: Státní zdravotnické nakladatelství; 1960. p. 469. 2. Chung K, Coggeshall RE. The ratio of dorsal root ganglion cells to dorsal root axons in sacral segments of the cat. J Comp Neurol. 1984;225(1):24–30. 3. Guérin P, Obeid I, Bourghli A, Masquefa T, Luc S, Gille O, Pointillart V, Vital JM. The lumbosacral plexus: anatomic considerations for minimally invasive retroperitoneal transpsoas approach. Surg Radiol Anat. 2012;34(2):151–7. 4. Marzo JM, Simmons EH, Kallen F. Intradural connections between adjacent cervical spinal roots. Spine (Phila Pa 1976). 1987;12(10):964–8. 5. Carlstedt T.  Nerve fibre regeneration across the peripheral-central transitional zone. J Anat. 1997;190(Pt.1):51–6. 6. Carlstedt T, Cullheim S, Risling M, Ulfhake B. Nerve fibre regeneration across the PNS-CNS interface at the root-spinal cord junction. Brain Res Bull. 1989;22(1):93–102.

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Injuries of the Peripheral Nerves

Nerve damage caused by injury trauma can occur with varying severity requiring reconstructive surgery. From the neurosurgical point of view, contusion, partial neurotmesis, and neurotmesis are important. Surgically, they are performed by external neurolysis, internal neurolysis, epineural neurosuture, fascicular neurosuture, suture using autotransplant, and cross-anastomosis. The aim of reconstructive surgery is to achieve maximum motor and sensory functions in a denervated distal portion. The simplest form of reconstruction of a severed peripheral nerve is its direct reconstruction. Nerve grafts to bridge the gap between the two ends of a damaged peripheral nerve if they cannot be anastomosed without even minimum tension have to be used. Nerve injuries to the lower extremities are less frequent than to the upper extremities. The type of injury of peripheral nerves has a significant impact on the extent of recovery and quality of sensitive, sensory, and motor functions [1–4]. The restoration of nerve conduction is influenced by different factors. The prognosis of the results of reconstructive operations is more favourable in children than in adults. Presumably, a nerve growth factor plays an important role. If the injury is more peripheral, the chance for a successful result is better. The quality of reconstruction decreases due to the rising time from the injury to surgery. However, there is never a zero chance, and a degree of sensitivity, though protective, can be achieved even years after the injury. Nevertheless, this does not relate to motor functions. Following 2 or more years from a complete nerve injury, scarring of the muscle is so pronounced that the adjustment is unlikely. For a normal nerve function and regeneration activity, the condition of the local blood supply is important. If a longer portion (10–16 cm) of a peripheral nerve loses its blood supply, its central part becomes avascular. However, this segment of the nerve may temporarily act as a free nerve graft in the well-vascularized bed, as its circulation can be adjusted. Dripping of blood from the distal end of the nerve incision in time of surgery indicates maintaining of continuity in the vascular supply between the internal and external circulation.

© Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_2

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In the cases of nerve injuries associated with contusions, surgical reconstructions are more time-consuming than in the cases, when the second suture is required. The extent of scarring—formation of cicatricial tissue and subsequent intra- and extraneural compression—is responsible for ischemia and obstruction of the axonal flow. In Waller degeneration, axons and their coats degenerate. Degeneration occurs mainly post-traumatically when the axon is severed completely. In Waller degeneration, the body of the neuron responds to axon detachment by the creation of structural proteins and tries to restore the connection with receptors and effectors. The axons severed from the body of neurons disintegrate, and this process results in the proliferation of Schwann cells at the site of injury. Schwann cells line up and create the so-called Bungner bands. Along these bands, regenerating axons outgrow into the periphery. If the damage lasts longer or is to a larger extent, there arises the problem of the accurate navigation of axons caused by the atrophy of cells that are arranged in bands. Another function of Schwann cells is the production of molecules that act as a support of axonal regeneration and growth [5–7]. In axonal degeneration, the axon is afflicted, while the nerve coating is preserved. Axonal degeneration is a result of toxic, metabolic, and ischaemic effects or due to the trauma—compression, traction. An example of this disability is polyneuropathy. In polyneuropathies, the initial damage to the nerve in the distal portions occurs, which is followed by centripetal progression. In demyelination, the damage to the myelin sheath occurs, wherein the impulse conduction (reflecting on the EMG) is impaired. This results in denervation. In Waller and axonal degeneration (generally due to the damage to an axon), fibrillations are recorded on EMG.  It is caused by a spontaneous activity of the muscle fibres due to increased membrane excitability. Axonotmesis is characterized by disruption of axons but with preservation of the nerve coatings. A lesion is partly reversible. Longer exposure to pressure or tension can cause severance of axons. However, they can be regenerated, thanks to Schwann sheaths, if they are undamaged. Firstly, there is Wallerian degeneration lasting for about 3 weeks. Then the axon grows 1–2 mm/day. We can predict the time when the function can be restored. Another possibility of functional improvement is a connection through collaterals, so-called sprouting, in the terminal branching in the region of the neighbouring neuron and its axons. It sends fibres that undertake the innervation of muscle fibres of the severed axon. Functional adjustment is incomplete, especially in fine-tune motor movements. Clinically, the peripheral paralysis with muscular atrophy and degeneration of the distal portion of the nerve appears. Neurapraxia is transient impairment of a nervous function caused by pressure, cold, and occasionally hypoxia. The myelinated sheath is damaged without a lesion of anatomical continuity. It is reversible damage to the peripheral nerve. An example of this damage is numbness of the crural portion of the lower limb when there transient paresis occurs. Clinically, sensitivity is impaired (paraesthesia), and muscular atrophy or pathological activity at EMG is not present.

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The last type of nerve damage is the destruction of the cell body of a neuron. As the cell body is the main structure, it means the destruction of the whole cell. This occurs when nerve roots are avulsed from the anterior spinal horns due to an accident or in transverse spinal cord lesions that can result from trauma or inflammation. Nerve damage to brachial and lumbosacral plexuses can be caused by injury trauma and can occur with varying severity. Brachial plexus ensures sensory and motor innervation of the upper limb, except the trapezius muscle, which is the only muscle from the shoulder griddle not being innervated from the brachial plexus. The brachial plexus is a network of the anterior branches of the last four cervical nerve roots (C5, C6, C7, C8) and the first thoracic nerve root T1. These five nerve roots merge to form three trunks: • • • •

Superior—formed by merging the anterior branches of C5 and C6. Middle—formed by the anterior branch of C7. Inferior—formed by merging the anterior branches of C8 and T1. Each of these trunks is divided into two branches (divisions), anterior and posterior, which merge to form three fascicles: • Lateral—formed by merging the anterior branches of the superior and middle trunk. • Medial—formed by the anterior branch of the inferior trunk. • Posterior—formed by merging three posterior branches of three trunks. The total number of myelin fibres in the brachial plexus ranges from 120,000 to 150,000 in adults, and 25% of them innervates the shoulder girdle. The fifth cervical and the first thoracic nerve contain the smallest number of myelin fibres 15,000– 20,000. The eighth nerve is the biggest, containing approximately 30,000 myelin fibres. The largest number of motor fibres is found in C5, followed by C8, the smallest number in C7 and T1. Sensory fibres are mostly in C7, followed by C6 and then by C8. The fundamental nerves forming the brachial plexus (according to the mass of the anterior branches) are C6, C7, and C8. The majority of branches of the brachial plexus originates from fascicles. Attention was paid to the course, anastomosis, diameter or pure absence, as well as to the mechanism and morphological causes of some injuries. The root is the least resistant when leaving the spine. Motor roots have fewer fila radicularia and are thinner than sensory roots, so they are disrupted more frequently. The spinal nerve covering is firmly connected to the dural sack, so the tension is transferred to its vault into the intervertebral foramen, where C8 and T1 roots are freely mobile. The C5, C6, and C7 roots are located in the sulcus spinatus, firmly connected by fibrous tissue, and protect the intrathecal roots. They are located to be less vulnerable during traction, in contrast to the C8 and T1 roots, which are not fixed. So, during traction, superior roots are injured at a more distalperipheral location, and avulsion happens, their fixations must be disrupted, or the processus transversus vertebrae must be broken. The presence of avulsion fractures at this level highly suspects the nerve roots to be disrupted from the spine. The term

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“root” means the trunk root, not the spinal one, i.e. the pre-truncal part of the plexus, including the spinal nerve in the sulcus and the anterior branch of the spinal nerve towards the trunk variations, either supraclavicular or infraclavicular. Simultaneous participation of the C4 and T2 roots on the formation of the brachial plexus was not found. The plexus was not the same on both sides. No perfect symmetry existed in the majority of anatomical variations in the supraclavicular area. Variations at the level of fascicles were quite common, and the highest number of variations was found in the lateral fascicle. Variations at the level of terminal branches were found in 92% of cases. In the prefixed type, nerves receive more fibres from the upper nerves. The C4 root may markedly contribute to the suprascapular nerve or even to the axillary nerve; the radial nerve receives more fibres from C5. The same is observed in relation to the musculocutaneous nerve and others. The impairment of the upper nerves or trunks, such as the superior trunk, is associated with larger plegia on the periphery than the same impairment in the postfixed type. In the first case, the impairment of C5 may be associated not only with plegia of the deltoideus, biceps, and brachialis muscle but also with paralysis of extensors of the wrist, brachioradialis, and supinator and pronator teres muscle. The same impairment of C5 in the case of caudal location of the plexus may not or only partially reflect the function of the forearm muscles. The brachialis and the biceps muscle may be affected only partially. In the postfixed type, the T1 root may have many fibres typically carried in the C8, and contribution of T2 may be bigger. The C7 root gives a wide innervation of the limb and more or less contributes to the formation of all trunks of the upper limb. In the case of injury, not frequently, we primarily observe a diffuse loss of function without complete anaesthesia or paralysis of a significant muscle group. The C8 participates in innervation of fingers and thumb extensors. The T1 root does more or less the same and also partially contributes to the three main arm nerves, and in the case of injury, each of them may present with signs of impairment. Its contributions are on the forearm; therefore, the forearm muscles innervated from the radial, ulnar, and median nerves may be affected. The posterior fascicle innervates mostly extensors, the medial and lateral fascicles mostly flexors. The medial fascicle contributes to the innervation of the proprietary hand muscles innervated from the median nerve; the lateral fascicle contributes to the innervation of the sensory component of the median nerve. The presence of the Horner syndrome suggests an avulsion of the C8 and T1 roots, even when C5, C6, C7, and C8 are pulled out, the patient can move his arm. The mobility is caused by n. XI and cervical plexus in some cases. The biceps brachii muscle can restore its function even in a complete injury with a root avulsion. The C3, C4, and the phrenic nerve participate in innervation. Variations of the brachial plexus have clinical and surgical implications. Knowledge of anatomical variations can help to explain incomprehensible clinical signs. Some anatomical variations are important particularly for surgeons during plexus reconstruction. It is useful to consider not only these variations in plexus forming but also their relation to big vessels because the topographic relationship of fascicles and arteries may be variable and can cause difficulties in urgent operation. In the case of bilateral variations, the identical variations are not always present. In

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some cases, only after preparations of trunks and fascicles we determined the real origin of the terminal branches and the sparse fibrous tissue forming sleeves. Frequently multilayers are worth mentioning. It is most dominant in the area of trunk divisions and fascicles formation, especially the medial one, less in the area of terminal branches formation. Its role in these locations is presumably to prevent nerve injuries between the nerves themselves or between the nerves and vessels and bones during the motion of the upper limb. In several cases, we observed fibrotic changes in the tissue. The brachial plexus injury is not a single nerve injury but the injury of multiple nerve roots, trunks, fascicles, and branches, connected by complex anatomic relations. Usually, various types of nerve injuries occur not only at the same site but also along individual nerves at various levels. Severe injuries of the brachial plexus are associated with contemporary problems. Scalenus muscles may be interrupted, and fractures of the cervical processus transversus may be present. The most common cause of the brachial plexus injuries is traction injuries during car accidents. The main forces to brachial plexus injury above the clavicle are the following: 1 . Downward injuries of the superior trunk. 2. Traction of the abducted arm causes the inferior trunk injury. 3. Anteroposterior traction can selectively injure the C7 root; sudden traction may affect all roots. Injuries below the clavicle result from the arm dislocation or traction during fractures. When the arm is forced to hyperabduction, the axillary suprascapularis and musculocutaneous nerve are often disrupted at their first point of fixing. That is the quadrilateral space for the axillary nerve and the coracobrachialis muscle for the musculocutaneous nerve. The suprascapular nerve can be disrupted at the suprascapular sulcus or taken off the muscle. Both levels, above and below the scapulae, should be surgically examined because the injuries affect both levels quite frequently. The clinical pictures depend on the level of brachial plexus injury, histological type of injury, the time between the injury, and treatment and joint injuries on the same limb. Neurapraxia is present in the majority of brachial plexus injuries and can last up to 6 weeks; therefore, it is difficult to predict spontaneous recovery at the beginning. Examination of deep touch sensation is a useful part of the examination on the continuity of the nerve with no clinical signs of sensory or motor functions. It is performed by pressing the patient’s fingers at the line of nails together. The pain is transmitted by the smallest sensory fibres in the nerve. In an apparently numb finger, where even burn is not felt, some continuity may be present after this manoeuvre, and the thumb top reflects the C6 root via the median nerve and the lateral fascicle. The top of the middle finger relates to the C7 root via the median nerve and C7 branch to the lateral fascicle, and the last phalanx of the little finger relates to the C8 root via the ulnar nerve and the medial fascicle. These small nerve fibres are the least affected by the nerve compression due to injury and oedema and are functional even when the rest of fibres does not function. Neurapraxia may slow down or stop

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the transfer of nutrition in these fibres, so the loss of sensitivity up to 6 weeks after the injury is not a diagnostic sign of a nerve rupture. These small fibres are quite frequently functional, and the examination can be performed soon after the injury. No pain in the hand or limb suggests a root avulsion. When pain starts in an insensitive hand, it is a sign of deafferentation due to a root avulsion from the spine. In the postganglionary lesions, pain is rare. Dry skin in the anaesthetic area suggests preganglionic injury. The sensitivity of the inner side of the arm is usually normal, as it is innervated by the T2 and the intercostobrachial anastomoses, not from the brachial plexus. Root avulsion may cause a partial spine lesion. Brown-Sequard syndrome may be present, and the spine lesion and haematoma may cause the injury and partial paralysis of the intercostal nerves, which needs to be considered during the plexus reconstruction. In penetrating injuries, bleeding (mainly arterial) may cause its compression; a traumatic aneurysm can act similarly. The functional degree of nerve compression is compared to the loss of motor and sensory functions. If they do not correlate, more probably, it is nerve compression, not a nerve rupture. A reported examination after several hours or days can reflect changes in the clinical picture. The C8 and T1 avulsion and lesions close to the spinal nerves interrupt sympathetic preganglionic fibres, which cause Horner syndrome (vasodilatation, anhydrosis, and ptosis). Quite frequently, only miosis is observed, and the other symptoms are minimal. Generally, an isolated C7 lesion does not cause muscle paralysis because the proximal muscles innervated from C7 are also innervated from C6, and the lower muscles for C7 are also innervated from C8. In C7 injury, a sensory function is affected only minimally because it is covered from C6 and C8. When also the associated spinal nerves or trunk are affected, muscular paralysis and a sensory deficit are obvious. CT and MRI scans ensure useful preoperational information, but their sensitivity and specificity are not sufficient to prove continuity so far. Clinically, it is difficult to exclude vessel impairment, so all serious injuries of the brachial plexus should be examined by angiography, as the main nerves of the plexus are not available for transcutaneous stimulation. The fibres of the superior and middle trunk are found in deeper situated nerves and terminate more proximally, where they are not available for the neurophysiological examination. Most information is derived from the neurophysiological examinations of the hand and forearm via nerve fibres of the inferior trunk and medial fascicle. The interpretation of examinations may be difficult if more lesions affecting the spinal roots, plexus, and its branches are present. Although the imaging and neurophysiological examinations may give suggestions for the probable operational findings, they do not impact the decision to operate. The indication for operation is derived from the clinical examination, which can show a partial or complete lesion of the brachial plexus without the signs of improvement. The success of interventions depends on the correct decision whether or not to operate. This is true for surgery in general and also for surgical interventions on the peripheral nerves. There is a time limit until when denervated muscles can recover. In vessel injuries, avulsion of less elastic nerve muscles occurs. A direct wound bleeding requires an urgent revision of vessels in order to restore the circulation first and foremost; nerve compression caused by oedema or necrotized muscles

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should be removed. When the treatment of the affected artery is delayed for more than 8 h, a chance to restore the function is mostly lost due to increasing pressure in the fascial compartment and subsequent development of ischemic necrosis. If an experienced surgeon is needed, the majority of uncomplicated open nerve injuries can be safely delayed by 24 h without the vessel impairment. In stubbing injuries without the vessel injury, an emergency surgery should be performed in 2–3 days when there are no signs of root avulsion and vessel lesions, but a complete paralysis persists, and a delay for 2 months is acceptable. If there are no signs of recovery, the injury should be revised. On the other hand, if the recovery continues and all nerves show the signs of continuity, surgical revision may be delayed. If a dissociative paralysis (without a sensory deficit) is present, another delay for several weeks is acceptable. In some cases of an incomplete paralysis, it is better to wait up to 3 months for another possible improvement prior to a revision. Another factor in the timing of the operation is a halted recovery of some muscle groups with still significant residual deficit. When the deep touch sense is on the inferior trunk, only the superior trunk should be revised. However, when the deep touch is not present on the little finger, a revision of the whole plexus should be performed up to 3 months. Surgical intervention is indicated in the closed injuries of the brachial plexus when no recovery is observed, and no deep touch is present on fingers 2 months after the injury. Many surgeons discuss the timing of surgical intervention; most of them recommend the revisions up to 2 weeks. An early revision has more advantages than later revision, such as early identification of nerve disorders and early treatment by nerve graft of another type of reconstruction. The operation area is free from fibrous tissue; axons in the distal stump and neuromuscular connections continue in function for several days. The stimulation of the distal stump causes a motor reaction, which enables to identify a fascicle with motor function. If delayed, the intraneural fibrosis progresses. Suitable conditions for reconstruction should be used immediately; later they are lost. The patient should be informed about the prognosis, and the rehabilitation should be initiated on time. A disadvantage of an early operation is a difficult evaluation of the limb function. The surgeon’s knowledge about the degree of injury is limited. Therefore, the perioperative decision on continuity is difficult. But the problems associated with a late operation prevail over the disadvantages of an early operation. We do not recommend the observation time or examinations for more than 4  months if there are no signs of recovery. The cause to recover in this period is neurapraxia. Axonotmesis of roots or trunks may not show any signs of recovery up to 6 or 8 months. When the operational revision is delayed until this time, the results of reconstruction operations are poor. Therefore, in the cases of injuries above the clavicle, a decision to operate on should be made long before the expected recovery after axonotmesis. In the cases of C7 neurapraxia, the improvement of clinical signs may mislead and support a delay to the operation, although the superior trunk is interrupted. When operating later, the nerve on longer distances may be thinner and without sufficient vessel supply. If no gross anatomical changes are found on the nerve during revision, more or less a prompt recovery may be expected. In ischemic injuries, the resection of changed nerved pieces should be considered after monitoring the clinical course during first months after

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the operation, because recovery after decompression can be observed even in (apparently) markedly changed nerves. Operations last long, and it is necessary to prevent the knees and elbows from the pressure. In the operations on the neck, it is important to prevent air embolism. In acute lesions of the brachial plexus, when the liquor suddenly may be relapsed, one has to be prepared to change the position of the patient to prevent the occipital conus. The phrenic nerve is a C5 branch. Following it proximally, C5 is found. During operation, supraclavicular sensory nerves are found. Following them proximally, C4 can be identified. After C4 and C5 identification, the upper level of the brachial plexus is determined. Palpation can determine the carotid tubercle on the processus transversus of C6. The next step is C5 and C6 and superior trunk isolation. The roots suggested to be injured are examined proximally first. The scalenus anterior muscle may be transversally interrupted to identify roots of the brachial plexus; they should be followed to the foramen in order to identify the injury. The perioperative stimulation is useful to prove the function of the phrenic nerve; nerve roots can also transfer impulses during perioperative stimulation; the contracting muscles should be within the distribution of the injured nerve. It should be obvious that the impulse was not propagated to adjacent, frequently intact muscles or nerves. When vessel injury is suspected, the surgical intervention is aimed at proximal and distal control of the subclavian artery, which should be identified at least at the junction of the scalenus anterior muscle and the first rib. Before the preparation of the affected area, arterial circles are put around it. Next, the clavicle is isolated. During clavicle mobilization, all bone fragments or prominent bone tissue from the healing fracture is removed to prevent plexus compression. A clavicle is revised by a longitudinal section through the periosteum, which is removed. After its removal and making four holes into the bone, the clavicle is divided, and both ends are moved. The subclavius muscle and periosteum are interrupted at the most lateral side of the clavicle. Medium long segments of the artery and vein are found under the subclavius muscle longitudinally. Subsequently, it is easy to determine the spinal nerves of C7, the inferior trunk and spinal nerves of C8 and T1. The whole plexus is now approachable and, if needed, can be treated. In the revision of the infraclavicular part of the plexus, the section continues to the insertion of the pectoralis major muscle to the humerus. The musculopectoral line is identified, and both muscles are separated to visualize the cephalic vein and the insertion of the pectoralis minor muscle, fixing it to processus coracoideus approachable. The cephalic vein is cut proximally, and the insertion of the pectoralis minor muscle is interrupted from the processus coracoideus and moved medially. Subsequently, we can identify distal fascicules of the brachial plexus. The musculocutaneous nerve is the first nerve to be observed, as it is located laterally, right under the insertion of the pectoralis minor muscle. The lateral fascicle is located medially and deeper from this point. The posterior fascicle is right under the lateral fascicle. The medial fascicle is located medially under the axillary artery. The branches between the medial and lateral fascicle should be maintained during preparation. At the end of the operation, all structures crossing the brachial plexus should be maintained in order to preserve the soft tissue covering the plexus. In the supraclavicular part, it is the omohyoideus and major muscle. If one of the muscles mentioned

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above is contracted, it must be fixed after its prolongation, and also the clavicular insertion of the pectoralis major muscle. The clavicle is treated by plates. After careful haemostasis, the drainage is left for 2–4 days. The drainage is located not to be close to the nerve graft. Immobilization is maintained by the bandage for 3–4 days. The musculocutaneous nerve is one of the best nerves to repair, albeit that repair was attempted in extremely unfavourable cases with postischaemic fibrosis, after direct damage to the elbow flexor muscles, or after prolonged delay. Radial nerve—these results are not as good as one might expect in high lesions. As one might expect, recovery for the posterior interosseous nerve is usually good. Median and ulnar nerves. The effect of age and injury level are significant for these two nerves. Equally or even more so are the effects of the cause of injury and the delay between injury and repair. The results after repair of high median and ulnar nerve lesions are, on the whole, much more modest than those following more distal repairs, trunk nerves in the lower limb. Most injuries to trunk nerves in the lower limb occurred in “untidy” wounds (penetrating missiles being the main cause), and all were associated with fractures and dislocations. The associated arterial injury was common and had a particularly deleterious effect. The lesions of the lumbosacral plexus are less frequent peripheral lesions affecting the lower limb. The lumbar plexus is formed by the anterior rami of the L1–L4, with or without T12. The sacral plexus is formed by the anterior rami of S1–S3 with a contribution of S4 and a very important lumbosacral trunk formed by the L4 and L5. Depending on the presence of the T12, a high cranial prefixed plexus or low caudal plexus is mentioned. The borderline root, contributing to the plexus, is the L4, which in some cases contributes more to the lumbar plexus, and in the other cases to the sacral plexus. Its contribution to the respective plexus helps to characterize the whole plexus—as cranial prefixed or caudal postfixed plexus. Similarly to the upper limb, the trunks of the lower limb receive more fascicles from the higher located nerves in the high cranial type compared to the low caudal type. The lumbosacral plexus is the brachial plexus analogue. Variations are manifested on the periphery as a variable contribution of some nerves, including variable tissue innervation, like in the brachial plexus. However, there is not the same interest in variations of both plexuses. This can be explained by the fact that the injuries and variations as well are less frequent compared to the brachial plexus. Reconstruction operations of the lumbosacral plexus are extremely rare. The components of the lumbosacral plexus are spread to the lower limb like the brachial plexus to the upper limb. The lumbar nerves are spread similarly like the nerves from the medial and lateral fascicle of the brachial plexus and the sacral nerves similarly like the nerves from the posterior fascicle of the brachial plexus. Many variations of the lumbosacral plexus are beside the atypical clinical and electromyographic findings the source of diagnostic problems. It is important to understand which nerve functions are transmitted in the individual parts of the plexus. Simultaneously, it should be considered that due to varying connections between the plexus roots, muscle innervation can change independently to the root number entering the plexus.

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In the prefixed type, the nerve roots receive more fibres from the high spinal roots. The injuries of the high nerve roots or nerves are associated with a wider lesion on the periphery than the same injury affecting the postfixed type. In the postfixed type, the S3 can have many fibres normally carried in the S2, and the contribution of the S4 can be bigger. The lumbar structure forming the plexus is more distant than in the brachial plexus. Thus, in the lumbar plexus injuries, the neurological deficit is less severe. Mostly car accidents can cause the lumbar plexus injuries associated with root avulsion. Repairs of the common peroneal nerve can fail in the cases of ischaemic fibrosis in the anterolateral muscles of the leg. However, it is clear that the sciatic nerve has an undeservedly bad reputation. We have seen some impressive results from primary repair. We have not found pain and hypersensitivity to be a frequent complication of repair of the sciatic nerve, the tibial division of the posterior tibial nerve. Recovery into the small muscles was seen after primary repair in tidy wounds at the hip, but it was rarely seen in “untidy” wounds or after traction injuries. The femoral nerve—the results of repair of this nerve are disappointing. Significant pain and hypersensitivity were common. Arterial lesions often complicated the injury.

References 1. Learmonth JR. The principles of decompression in the treatment of certain diseases of peripheral nerves. Surg Clin North Am. 1933;13:905–13. 2. Millesi H, Rath T, Reihsner R, Zőch G. Microsurgical neurolysis: its anatomical and physiological basis and its classification. Microsurgery. 1993;14:430–9. 3. Samardžič D, Grujičič I, Rasulič L, Miličič B. Restoration of upper arm function in traction injuries to the brachial plexus. Acta Neurochir. 2002;144(4):327–35. 4. Stejskal L, Haninec P. Indikace k chirurgické rekonstrukci pažní pleteně. Elektrodiagnostika. Výsledky rekonstrukcí. Čes Sl Neurol Neurochir. 1997;60/93(3):126–33. 5. Bednařík J, Ambler Z, Růžička E. Klinická neurologie, Část speciální I, 1.vyd. Praha: Triton; 2010. p. 707. 6. Mráz P. Anatómia ľudského tela 2, 1.vyd. Bratislava: Slovak Akademic Press; 2005. p. 286. 7. Pfeifer J. Neurologie v rehabilitaci. 1.vyd. Praha: Grada Publishing; 2007. p. 352.

3

Neuropathies

Neuropathy is a general term for peripheral nerve involvement. Mononeuropathy is damage to a single nerve. The causes are mainly traumas in which a partial or total severance of the nerve is present. Closed traumas include damage by a traction mechanism that results in a rupture of several axons and interruption of their vascular supply. Another cause is nerve compression, especially when the myelin sheath is damaged. Polyneuropathy is damage to multiple peripheral nerves. The cause may be the system processes—infection, inflammation, immune or metabolic disorders, and toxic effects. Peripheral neuropathy is damage affecting the nerves, which may impair sensation, movement, gland or organ function, depending on the type of nerve affected. Neuropathy affecting just one nerve is called “mononeuropathy”, and neuropathy involving nerves in roughly the same areas on both sides of the body is called “polyneuropathy”. When two or more separate nerves in different areas of the body are affected, it is called “multiple mononeuropathy” [1–3]. Peripheral neuropathy may be chronic or acute. Acute neuropathies demand urgent diagnosis. Motor nerves, sensory nerves, or autonomic nerves may be affected. More than one type of nerve may be affected at the same time. Neuropathy may cause painful cramps, fasciculations (fine muscle twitching), muscle loss, bone degeneration, and changes in the skin, hair, and nails. Motor neuropathy may cause impaired balance and coordination or, most commonly, muscle weakness. Sensory neuropathy may cause numbness to touch and vibration, reduced position sense causing poorer coordination and balance, reduced sensitivity to temperature change and pain, spontaneous tingling or burning pain, or skin allodynia (severe pain from normally nonpainful stimuli, such as light touch), and autonomic neuropathy may produce diverse symptoms, depending on the affected glands and organs, but common symptoms are poor bladder control, abnormal blood pressure or heart rate, and reduced ability to sweat normally [2, 3].

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Peripheral neuropathy may be classified according to the number and distribution of nerves affected (mononeuropathy, mononeuritis multiplex, or polyneuropathy), the type of nerve fibre predominantly affected (motor, sensory, autonomic), or the process affecting the nerves, e.g. inflammation (neuritis), compression (compression neuropathy), and chemotherapy (chemotherapy-induced peripheral neuropathy). The most common cause of mononeuropathy is physical compression of the nerve known as compression neuropathy. Carpal tunnel syndrome and axillary nerve palsy are examples. Direct injury to a nerve, interruption of its blood supply resulting in ischaemia, or inflammation also may cause mononeuropathy. Polyneuropathy is a pattern of nerve damage that is quite different from mononeuropathy, often more serious and affecting more areas of the body. In the cases of polyneuropathy, many nerve cells in various parts of the body are affected, without regard to the nerve through which they pass; not all nerve cells are affected in any particular case. In distal axonopathy, one common pattern is that the cell bodies of neurons remain intact, but the axons are affected in proportion to their length, and the longest axons are the most affected. Diabetic neuropathy is the most common cause of this pattern. In demyelinating polyneuropathies, the myelin sheath around axons is damaged, which affects the ability of the axons to conduct electrical impulses. The third and least common pattern affects the cell bodies of neurons directly. This usually picks out either the motor neurons or the sensory neurons (known as sensory neuronopathy or dorsal root ganglionopathy). The effect of this is to cause symptoms in more than one part of the body, often symmetrically on the left and right side. As for any neuropathy, the chief symptoms include motor symptoms such as weakness or clumsiness of movement, and sensory symptoms such as unusual or unpleasant sensations such as tingling or burning, reduced ability to feel sensations such as texture or temperature, and impaired balance when standing or walking. In many polyneuropathies, these symptoms occur first and most severely in the feet. Autonomic symptoms also may occur, such as dizziness on standing up, erectile dysfunction, and difficulty controlling urination. Polyneuropathies are usually caused by processes that affect the body as a whole [4]. Diabetes and impaired glucose tolerance are the most common causes. Other causes relate to the particular type of polyneuropathy, and there are many different causes of each type, including inflammatory diseases, vitamin deficiencies, blood disorders, and toxins (including alcohol and certain prescribed drugs). Most types of polyneuropathy progress fairly slowly, over months or years, but rapidly progressive polyneuropathy also occurs. The treatment of polyneuropathies is aimed firstly at eliminating or controlling the cause, secondly at maintaining strength and physical function, and thirdly at controlling symptoms such as neuropathic pain. Mononeuritis multiplex is simultaneous or sequential involvement of individual noncontiguous nerve trunks [5, 6] either partially or completely, evolving over days to years and typically presenting with acute or subacute loss of sensory and motor function of individual nerves. The pattern involvement is asymmetric; however, as the disease progresses, deficit becomes more confluent and symmetrical, making it difficult to differentiate from polyneuropathy.

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Mononeuritis multiplex may cause pain, which is characterized as a deep, aching pain that is worse at night and frequently in the lower back, hip, or leg. Electrodiagnostic studies will show multifocal sensory-motor axonal neuropathy. Autonomic neuropathy is a form of polyneuropathy that affects the non-voluntary, non-sensory nervous system, affecting mostly the internal organs such as the bladder muscles, the cardiovascular system, the digestive tract, and the genital organs. These nerves are not under a person’s conscious control and function automatically. Autonomic nerve fibres form large collections in the thorax, abdomen, and pelvis outside the spinal cord. However, they have connections with the spinal cord and ultimately the brain. Most commonly, autonomic neuropathy is seen in persons with long-standing diabetes mellitus. Autonomic neuropathy is one cause of malfunction of the autonomic nervous system, but not the only one; some conditions affecting the brain or spinal cord also may cause similar symptoms to autonomic neuropathy. Compression neuropathies occur acutely (e.g. proximal radial nerve palsy, peroneal neuropathy at the fibular head) or more gradually (e.g. median neuropathy at the wrist, ulnar neuropathy at the elbow). Acute compressive neuropathies typically develop at sites where external pressure can compress the nerve against a harder surface, such as the radial nerve at the spiral groove of the humerus. Chronic neuropathies (e.g. entrapment neuropathies) occur where a nerve passes through tissue tunnels with a propensity to narrow with time, eventually entrapping the nerve itself. Acute neuropathies tend to manifest more with predominant motor manifestations, for instance, peroneal neuropathy—a foot drop, and radial neuropathy—a wrist drop; sensory disturbances are relatively mild. Entrapment neuropathies usually present with paraesthesia predating focal weakness by months and often years, as well as overshadowing it. Median neuropathies at the wrist initially are characterized by hand tingling at night or with various hand activities, particularly driving; only later in the course does weakness of the thumb, particularly the abductor pollicis brevis, become evident. Diabetes mellitus, myxedema, or, rarely, hereditary neuropathy with liability to pressure palsy makes nerves more susceptible to compression injury. Peripheral nerves are made up of many myelinated and unmyelinated nerve fibres originating from either the anterior horn cell (motor) or the posterior root ganglia (sensory) and travelling the nerve’s entire length. Nerve fibres are organized into fascicles, of which there are many within one peripheral nerve. Elements contained within the fascicles represent the endoneurium. The perineurium, a protective sheath of connective tissue, surrounds each fascicle. Schwann cells concentrically wrap their cytoplasmic processes around axons many times, creating the myelinated nerve fibre. Each nerve segment is associated with one adjacent Schwann cell. When many Schwann cells are lined up continuously, the entire nerve fibre becomes myelinated. An internode consists of one myelinated segment. Nodes of Ranvier represent areas lacking myelin, thus interrupting the internodal sections and containing high concentrations of voltage-gated sodium channels. Juxtaparanodal and

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paranodal regions are distinctive myelin folds at internode edges containing high concentrations of voltage-gated potassium channels. These areas are integral to conduction of action potentials down the axons. When nerve tissues are subjected to mechanical compression, some of the compressed tissues are displaced to sites of lower pressure. This is especially the case for acute compression neuropathies, such as proximal radial neuropathy and neuropathies secondary to tourniquet compression. With acute nerve compression, the damage is concentrated at the compression edges. The predominant injury at this level implies that the pressure gradient itself, rather than absolute pressure, is the critical factor for acute compression neuropathy. In the setting of experimental acute compression, the earliest histopathologic change is seen within just a few hours in an invagination of one paranodal segment into its adjacent paranode. Directed towards the uncompressed tissue, paranodal myelin, tethered to the axon, may be grossly distorted, resulting in invagination on one side and passive stretching on the other side. Longitudinal movement of the axon relative to the Schwann cell accompanies the paranodal myelin alterations. In extreme cases, myelin lamellae can be ruptured. These findings are reminiscent of intussusception of the bowel, suggesting that the pressure gradient between compressed and uncompressed nerve provides definitive forces causing axoplasm extrusion similar to toothpaste from a tube. The subsequent events of acute focal compression initially include an early combined extrusion of endoneurial fluid (the fluid between fibres), axonal fluid, cytoskeletal elements, and subsequently distortion of myelin and Schwann cell elements. A second slower phase is attributed to further endoneurial and axonal fluid extrusion, paranodal disruption, Schwann cell cytoplasm extrusion, and displacement of other tissue elements. Additional damage (e.g. of the cytoskeletal network) may occur at more extreme pressures or with protracted compression. Nodes of Ranvier are frequently obscured or lengthened because of displaced paranodal myelin. Classic nerve conduction studies provide a means to measure the magnitude of the nerve action potentials as well as focal conduction slowing. These findings correlate with the degree and duration of compression. Focal ischaemia may also contribute in some compression neuropathies, particularly in combination with the direct effects of pressure. Transient nerve block, for instance, when a limb goes to sleep for a few seconds, may be related to modest external pressures and/or may be primarily caused by focal ischaemia because no recognizable structural nerve pathology has been convincingly demonstrated. For more severe cases of acute compression, nerve fibre remyelination may occur weeks to months after resolution of the acute compression. The earliest histopathologic change observed in chronic nerve compression is an asymmetric distortion of the large myelinated fibre internodes; there is a tapering of the internodes at one side and swelling of the internodes at the other. A modified axoplasm accumulation occurs, possibly caused by interference of axon flow. The direction of tapering reverses on the other side of the compressive lesion. In contrast to the pathologic changes of acute nerve compression, there is no displacement of nodes of Ranvier. Subsequently, these myelinated fibre paranodal changes are

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followed by demyelination and remyelination, events probably occurring repeatedly during chronic compression. Ischaemia and endoneurial oedema also contribute to the pathology of nerves that sustain chronic compression; the modest pressure magnitudes develop, such as what occurs with median nerve compression in the carpal tunnel. The ischaemic hypothesis has focused on the transperineurial vascular system. This includes an intrafascicular circulation, composed mostly of capillaries running longitudinally within the endoneurium and an extrafascicular network within the epineurium, composed predominantly of venules and arterioles. The extrinsic vessels penetrate the relatively rigid perineurium to anastomose with the intrinsic circulation, and it is this transperineural vessel network that may be particularly susceptible to focal compression, especially because these vessels transverse the perineurium at oblique angles. These transperineurial vessels, especially the venules, are vulnerable to constriction caused by endoneurial oedema and elevated (intrinsic) endoneurial fluid pressure. Constriction of these vessels causes venous congestion, endoneurial capillary leakage, and elevated endoneurial fluid pressures. These effects introduce metabolic disturbances to the microenvironment, with subsequent damage to the peripheral nerve anatomy and nerve function. Thus, chronic external compression may induce ischaemia and endoneurial oedema with concomitantly elevated endoneurial fluid pressures. These two effects impair nerve function by altering the metabolic microenvironment as well as contributing to nerve injury by further constricting transperineurial venules. Thus, a precarious cycle of venous congestion, ischaemia, and metabolic disturbances is initiated that eventually leads to a miniature compartment syndrome. In the cases of median neuropathy at the wrist—carpal tunnel syndrome, it is thought that carpal tunnel pressures may rise to abnormal levels, increasing the endoneurial fluid pressure and thereby impairing the transperineurial microcirculation. Carpal tunnel pressure and consequently endoneurial fluid pressures probably rise significantly at night in the setting of carpal tunnel syndrome because the limb venous return is impeded by limb posture and reduced limb movement. Endoneurial oedema due to other causes, for instance, diabetes, further increases nerve susceptibility to compression. Moderately elevated pressures also disturb axonal transport. Retrograde axonal transport is critical for communication with the nerve cell body. Fast and slow anterograde axonal transport may also be reversibly impaired after compression. The blocking of axonal transport with compression is a graded effect, related to the magnitude and duration of compression. For example, the susceptibility to entrapment in diabetic polyneuropathy may be in part due to the combination of widespread endoneurial oedema (diabetes) and focal (entrapment) impairment of axonal flow. The gliding capacity of a perineural nerve is another important factor inherent to chronic compression neuropathies. This is particularly relevant at common sites of entrapment, such as the wrist and elbow. Gliding of nerves is necessary during movement of limbs and is made possible by conjunctiva-like adventitia that allows longitudinal excursion of a nerve trunk. Restriction of glide may occur with extraneural and intraneural fibrosis, especially at sites of entrapment, inducing nerve stretch lesions, oedema, inflammation, and further fibrosis. Stretch may contribute to nerve injury at common sites of entrapment, although it is unlikely to be

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the major factor in injury and is likely overshadowed by the consequences of direct pressure and perhaps ischaemia. A careful history and meticulous neurologic examination are essential for evaluation of mononeuropathies. Initially, one defines the precise motor and sensory deficits and next decides whether this fits an individual peripheral nerve’s anatomic distribution. This is relatively easily accomplished with acute nerve trauma, i.e. a laceration or gunshot wound. In contrast, mononeuropathies have a relatively ingravescent course characterized first by intermittent paraesthesia initially not producing a clinically definable functional loss. Patients with brachial or lumbosacral plexus lesions are less likely to have neck or back pain, rather pain within the affected extremity. Here the numbness may be more diffuse, and muscles are weakened within the distribution of multiple peripheral nerves/nerve roots. Numbness rather than pain is much more common with early mononeuropathies. The symptoms can help in diagnosis. Because sensory examination is the most subjective part of the neurologic examination, occasionally this is difficult to define clearly. Sometimes clinical neurologic examination is not precise enough to provide early diagnosis of mononeuropathies. Electrodiagnostic studies are the method of choice for defining the precise anatomic distribution of peripheral nerve damage. This includes nerve conduction studies (NCS) and needle EMG. Thus, it is possible to assess the quality of peripheral nerve conduction as well as whether there is damage to muscles specifically innervated by that nerve. NCS allow identification of the site of nerve damage whenever the nerve’s myelin is chronically damaged. Early signs of a carpal tunnel syndrome are best defined by sensory NCS, and later motor NCS, demonstrating prolongation of the time for nerve conduction across the wrist (distal latency). Motor NCS are especially useful for defining more proximal nerve blocks, i.e. at the elbow (ulnar nerve), midhumerus (radial nerve), and knee (fibular nerve).

References 1. Kassardjian CD, Dyck PJ, Davies JL, Carter RE, Dyck PJ. Does prediabetes cause small fiber sensory polyneuropathy? Does it matter? J Neurol Sci. 2015;355(1-2):196–8. 2. Hughes RA. Peripheral neuropathy. Clinical review. BMJ. 2002;324(7335):466–9. 3. Torpy JM, Kincaid JL, Glass RM.  JAMA patient page. Peripheral neuropathy. JAMA. 2010;303(15):1556. 4. Sugimoto K, Yasujima M, Yagihashi S. Role of advanced glycation end products in diabetic neuropathy. Curr Pharm Des. 2008;14(10):953–61. 5. Cioroiu CM, Brannagan TH. Peripheral neuropathy. Curr Geriatr Rep. 2014;3(2):83–90. 6. Watson JC, Dyck PJ. Peripheral neuropathy: a practical approach to diagnosis and symptom management. Mayo Clin Proc. 2015;90(7):940–51.

4

Regeneration of Peripheral Nerves

From the distal segment of a disrupted nerve, the newly formed axons grow. A precondition of peripheral nerve regeneration is a preserved endoneurial tube that acts as a conductor. Axons grow as the first, then myelin sheaths are formed, and gradually a functional regeneration occurs. In axonal denervation, the endoneurial tubes are preserved, but not in a traumatic injury. In axonal denervation, the regeneration occurs when neighbouring axons are stimulated to “sprouting,” and the newly formed axons innervate denervated muscles. To assess the course of regeneration, a so-called Tinel’s sign is used. It is performed by light tapping over the nerve trunk to elicit pain; a sensation of tingling (paraesthesia or dysesthesia) in the distribution area of the nerve occurs. This test serves as evidence of regeneration of sensitive nerve fibres. If there is no connection of the nerve, a neuroma forms at the proximal segment. In addition, an intraneural neuroma can arise. It can develop after severe trauma or in continued traumatization. The cause is the formation of connective tissue within the nerve. A nerve function is impaired and regeneration is impeded. Surgical reconstruction consists of the preparation and adaptation of damaged stubs of peripheral nerves microscopically up to a normal fascicular pattern (Fig. 4.1). Subsequently, they microsurgically adhere to the epi- and perineurium (Fig. 4.2). Very often, a good functional result can be achieved. In addition to early treatment, an experienced surgeon and a microsurgical technique are very important. The radial nerve (n. radialis) and the tibial nerve (n. tibialis) have the best regenerative capacity. Even in the cases of poorly regenerating nerves, such as fibular nerve (n. fibularis) and ulnar nerve (n. ulnaris), early treatment provides good results [1]. Comparing the results of direct nerve sutures with reconstructive surgical procedures using autografts (Fig. 4.3), no significant differences have been found. In the cases of avulsion of one or more roots from the spinal cord, a fully functional adaptation is not possible. In such cases, a transfer of nerve branches of a healthy nerve is used. This is a palliative method because the damaged spinal

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32 Fig. 4.1  Resection of damaged peripheral nerves

Fig. 4.2  Suture behind the epineurium

Fig. 4.3  Autotransplants of peripheral nerves

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segments are not linked to the peripherals. The success is determined by the function and structure of peripheral nerves. In the majority of brachial plexus lesions, it is a combined lesion, including several elements of the plexus with various degree of nerve impairment. It is a complex lesion with ruptures at various levels or nerve avulsion from muscles or nerve discontinuity for the majority of nerve injuries. Surgical treatment consists of neurolysis up to reconstruction operation. The operation usually starts with neurolysis, when a degree of impairment may be determined. Both actions are often needed at the revision. They may be dangerous for the life-maintaining structures in the area of arteries, veins, ductus thoracicus, lung peaks, airways, oesophagus, and thyroid gland. The safety is maintained by anatomical knowledge. A serious problem is a reconstruction in a fibrous transformation of surrounding structures. Gaps between the individual muscles are frequently filled with fibrous tissue. Surgical revision may start from the distal parts of the brachial plexus in the fossa axillaris by nerve identification. If they are normal, the revision continues proximally. If nerves are within the fibrous tissue, the peripheral nerves of the upper limb are evaluated, or the brachial plexus is revised distally to the pectoralis minor muscle and the deltopectoral sulcus. Although the confirmation of avulsion is preferably done by a direct revision of the roots, severe scarring may cause the operation very difficult, even hazardous in such cases. The surgeon can prepare the roots considering the CT and MRI findings. In preganglionic injuries, the nerve roots (especially the anterior one) are disrupted or taken off the spine with subsequent retrograde changes in the spine leading to the spine atrophy resulting from the impairment of motor and sensory fibres. So far, the reimplantation of the nerve roots to the spine is possible only exceptionally. It may come to reinnervation, but this condition has one major disadvantage: it never comes to the creation of specific paths to a particular muscle. The axonal structure on the periphery is considerably irregular which results in reciprocal reinnervation of not only various muscles but agonists and antagonists particularly. This leads to synthesis in the clinical picture. Therefore, if root avulsion is present, the reconstruction with nerve transfers is needed. The goal of neurotization is to achieve nerve continuity to the distal stump by a functional nerve graft. Nerve transfer should reach only the terminal branches because the transfer to the trunks or fascicles may lead to dispersion and loss of fibres. In adults, the extraplexal nerve transfer is more suitable than the intraplexal one. In the case of C5–C6 injuries, intraplexal nerve transfers have better results. Oberlin [2] described a method of distal neurotization when he performed a transfer of n. ulnaris motor fascicle for m. flexor carpi ulnaris on n. musculocutaneous. It came to the recovery of elbow flexion in the patients within less than 6  months—this can be explained by distal suture [2, 3]. Songcharoen [4] used a similar procedure in 2011 in the case of n. medianus, using the fascicle for m. pronator teres and m. flexor carpi radialis. There was not confirmed a concern that results would be worse due to the violation of n. medianus fibre parts in the case of brachial plexus injury [5]. Oberlin’s method is appropriate in the case of C5–C6 superior root injuries but only when a donor nerve is intact (normal hand mobility). The fascicle after opening

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the epineurium of a given nerve in the upper third of an arm is localized with electrical stimulation, and contraction of a followed muscle is monitored. Consequently, it is cut and its proximal stub is released in the length of several centimetres. After that, this stub is stitched with perineural technique on the branch for m. biceps brachii before entering the muscle and not on the trunk of n. musculocutaneous. Temporary disorders of sensitivity, as well as rare motor disability in the innervation nerve zone, were described as procedural complications. End-to-side anastomosis—a principle of this method is a connection of distal stub of a damaged nerve to the side of intact donor nerve which serves as axon donor. It is used in the cases when suitable nerves for standard neurotization are not available. Success on a cellular level is based on the knowledge that the axons are beside terminal branching able to split in their course—collateral branching [6, 7]. Successful reinnervation in the case of proximal injuries requires perineural window creation which does not lead to a functional deficit of the innervation area of donor nerve. The extraplexal nerve transfer might be C4, the accessory nerve, intercostal nerves, the cervical plexus, or the hypoglossal nerve. These are used for the transfer to the distal stumps, which lost their spinal roots due to avulsion. The order of importance is the following: the musculocutaneous, suprascapularis, axillary, thoracicus longus, pectoralis nerve, and radial nerve to triceps. The dissection of reconstruction is elbow flexion, abduction, and external rotation of the shoulder, improvement of long flexors of the hand, and the recovery of the sensation of the radial side of the hand. The neurotization of the musculocutaneous nerve has the following indications: 1 . C5–C6 avulsion or a total avulsion. 2. Up to 5 months after injury. 3. Elbow stiffness is not present. 4. A rib fracture is not present. 5. The age is under 50 years. The musculocutaneous nerve contains approximately 6000 nerve fibres. For the reinnervation, the intercostal nerves containing 1550 nerve fibres are used. In both nerves, 50% of fibres are motor ones. The musculocutaneous nerve is dissected from its motor point in the biceps muscle to the beginning of the lateral fascicle. The motor component of the intercostal nerves T4 and T5 is directly sutured with the motor part of the musculocutaneous nerve and the sensory component with the sensory part. When the intercostal nerve T6 is used, we need to insert a graft. The motor component of the T3 intercostal nerve is transferred by a direct connection of the nerve at the lower margin of the pectoralis major muscle. A bad arrangement of the nerve fascicles during suture can cause a loss of 50% of motor fibres and is responsible for their poor results of the nerve transfer. When using the accessory nerve, additional 2500 nerve fibres are available. In order to prevent the denervation of the trapezius muscle, the accessory nerve is prepared under its proximal branch. The impulses from all intercostal nerves are simultaneous. When two muscles are innervated from different intercostal nerves, they contract together. So, no antagonists should be

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neurotized by the same donor nerves. If the intercostal nerve is not suitable (multiple rib fractures, Brown-Sequard syndrome, paralysis of the diaphragm), the accessory of hypoglossal nerve may be used. Motor branches of the cervical plexus are used in the neurotization of the thoracicus longus nerve and the second intercostal nerve for the neurotization of the thoracodorsal nerve. The thoracolateral C7 transfer is reserved mainly for the neurotization of the free muscle graft because patients will not learn to coordinate impulses from the contralateral side. In the C7 avulsion, the surgical plan is different and depends on joint disorders. When no lesion is found, a transfer of the cervical sensory nerves to the C7 stump is performed. If the C5–T1 avulsion is present, it is better to neurotize the thoracicus longus nerve and later perform the arm arthrodesis. Reconstruction is very difficult. The hand deficit is bigger, or wrist extrusion or metacarpophalangeal extrusion is missing. The arthrodesis of the wrist will not solve the problems of moving the wrist. It is indicated only for cosmetic reasons in the cases with associated rupture of the superior trunk. The intraplexal nerve transfer can be achieved by distribution of fibres from the superior trunk to the distal stumps of C5, C6, and C7. But in cases of the inferior trunk or low spinal nerves injury, the grafts originating from the inferior trunk were distributed mostly to the intermedial trunk and the top parts of the inferior trunk due to the limited possible recovery of the C8 and T1. In the cases of the C7 rupture, an operation using a nerve graft is performed. Palsy of n. radialis within brachial plexus injury is usually insoluble due to a long reinnervation path with the exception of m. triceps which is not normally neurotized for its relatively minor significance in the case of severe injuries of the brachial plexus—the extremity falls in extension spontaneously. The condition is usually solved secondarily, using tendon transposition. The n. radialis on the forearm may also be solved by neurotization with branches from n. medianus and n. ulnaris. If the C7 is intact, the wrist extension may be sufficient, but the finger extension requires a transfer of the tendon from hand flexors. The potential benefit from the tendon transfer should be higher than weakness or loss of function at the side of tendon removal. The tendon transfer also causes weakness or loss of function at the other side, but it has to be smaller than the potential benefit. Muscles which were paralyzed after the nerve injury and recovered are not suitable for the tendon transfer because they have different power. More importantly, they do not have good independent control. The decision on the arthrodesis or tenodesis should be carefully considered. Generally, the wrist arthrodesis should be used to stabilize the wrist, so the effect of the function must be considered before the arthrodesis. Tenodesis on the hand may be useful if a squeeze of the hand is accurate. More rarely, in the cases of rupture of the root or distal parts during the reconstruction operation, the sural nerve is used. When the root injury is postganglionic, the root can be connected to the distal parts by suture or by nerve graft. A disadvantage of nerve graft is two more connection sites. The length of the graft more than 5 cm brings worse results. It is frequently ineffective due to a fibrous block at the level of distal suture or transplant necrosis, which prevents the growth of the regenerating axons. The velocity of the nerve fibre growth through the transplant is 1.5–2 times lower. If more grafts are needed, the median cutaneous nerve of the arm can also be used.

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Only nerves sized as cutaneous nerves are suitable as nerve grafts. In bigger nerve roots, ischaemic injury with necrosis and fibrotization can develop due to slow spontaneous revascularization in the centre. The brachial plexus injuries may also be associated with motor nerve avulsion from the muscles. The peripheral nerve rupture is usually located at the site of its terminal branching and neuromuscular junction. In such cases, in a direct neurotization nerve-muscle, the motor fibres can be transferred to the muscle directly or by a nerve graft. New motor discs are formed in the aneural part of the denervated muscle. Grafts from the sural nerve are connected to the original nerve or another nerve, if possible. The distal graft endings are divided into several fascicular groups and inserted into distal parts of impaired muscle via a longitudinal section performed as an atraumatic one. Nerve branches are implanted in a broad area to increase the volume of innervated muscle. The epineurium is sutured to the muscle fascia by 8.0 absorbable stitches. Fascicles remain in the muscle sulcus and do not need a suture. When bleeding occurs during the section in the muscle, a new section should be done at another site due to scarring. Depending on the character of the injury and the time from injury to operation, the results are frequently seen in several years (reconstruction operation). Crucial factors for the results of the reconstruction operation are the character and extent of the injury, the age of the patient, and the time from the injury to operation in all cases; vessel impairment worsens the prognosis of the plexus lesion. Not only the injury is more severe, but also the revision due to scarring is much complicated, especially after the vessel reconstruction. The vessel prosthesis may leak at the side of the anastomosis, leading to the formation of firm fibrous tissue, which subsequently surrounds nerve roots and an accident impairment of the prosthesis may cause uncontrolled bleeding. When evaluating the results, neurotrophic factors should be considered, which are more active and effective in children compared to adults. Good results of the plexus operations are in the case of neurolysis or the C5 and C6 treatment, while the treatment of the C8 and T1 is rarely successful. In the plexus avulsion, the operational results are much worse. In the avulsion of the superior roots, when the middle and inferior part of the plexus is in good condition, the function of the upper limb is reconstructed by improving the shoulder stability and restoring the elbow flexion. When a total avulsion is present, the results are much worse, and later wrist arthrodesis is needed. In a total avulsion, only a limited goal may be settled, such as medial arm abduction, shoulder stabilization via reinnervation of the external rotators, elbow flexion, and partial improvement of sensitivity of radial fingers. This goal can be achieved by neurotization of the suprascapularis, axillary, and musculocutaneous nerve by the motor nerves and the median nerve by the cervical sensory nerves. Sensory improvement up to 3 years partially corrects the defensive sensitivity of radial fingers for defence. When muscles show only partial recovery and their power is too small for a useful function, the mechanic situation may be improved by the insertion of tendon more distally. In other cases, the power may be improved by a combination of two simultaneously innervated muscles, such as the biceps and triceps muscle, to increase a mechanical effect. Under

4  Regeneration of Peripheral Nerves

37

these circumstances, an active extension is not possible, and the patient has to extend the elbow by decreasing the flexion power and using gravitation. Adult patients experience problems and difficulties in learning new functions, even a simple elbow flexion. The time needed to learn a new movement may be long. Another reconstruction via tendon transfer or other procedures should be reconsidered. If it is clear that the improvement of some function is not expected after the operation, the reconstruction plan—shoulder arthrodesis or the forearm tendon transfer—may start earlier. Positive results were not observed in operations after 9 months. The immobilization lasts for 1–2 weeks in the cases of neurolysis, 6 weeks in the cases of nerve grafts or after neurotization followed by physiotherapy. The patients leave the hospital 7–9 days after the operation. Rehabilitation and electrical stimulation begin 3 weeks after the operation. The lateral abduction at 90° and posterior shoulder flexion begin after 6 months, in order to prevent the rupture of nerve suture. Patients are regularly monitored every 3  months. Patients who are more than 15 months after the injury without an apparent improvement reach the “state” when no further improvement can be expected. Prophylactic tendon transfers for the wrist extension are valuable when done on time, even in the cases of further improvement of the function. In children, the recovery starts in 7–8 months after the nerve graft, but 24 months is the maximum for the innervation compatible with the useful recovery of the function. Further recovery continues up to 3 years. Common complications, such as haematoma, wound infection, and wound dehiscence, can jeopardize the results. Reconstruction operations are able to tolerate some of these complications quite well and still give an acceptable result. Another reason for the failure is fibrosis on the distal end of the nerve graft. End-to-end sutures may cause poor operational results. Because the sutures are teared up within several days after the operation, only nerve grafts in all supraclavicular injuries should be considered. More rarely, in the cases of rupture of the root or distal parts during the reconstruction operation, the sural nerve is used. When the root injury is postganglionic, the root can be connected to the distal parts by suture or by nerve graft. A disadvantage of nerve graft is the two more connection sites. The length of the graft more than 5 cm brings worse results. It is frequently ineffective due to a fibrous block at the level of distal suture or transplant necrosis, which prevents the growth of the regenerating axons. The velocity of the nerve fibre growth through the transplant is 1.5–2 times lower. If more grafts are needed, the median cutaneous nerve of the arm can also be used. Surgical reconstruction of peripheral nerves faces several difficulties, and a clinical outcome depends on several factors. The knowledge of anatomic variability in peripheral innervation is a prerequisite of successful reconstruction surgery of peripheral nerves depending on the following: the period between the injury and operation, patient’s age, length of autograft, location of the injury, and type of a nerve. A complete recovery of sensitive functions has not been observed in any of the patients over 40 years. In those cases, only the protective sensitivity was achieved. There were observed worse results for the reconstructive operation of n. fibularis.

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References 1. Waller A. On the sensory, motory and vasomotory symptoms resulting from refrigeration and compression of the ulnar and other nerves in man. Proc Roy Soc. 1862;12:89–103. 2. Oberlin C, Béal D, Leechavengvongs S, Salon A, Dauge MC, Sarcy JJ. Nerve transfer to biceps muscle using a part of ulnar nerve for C5-C6 avulsion of the brachial plexus: anatomical study and report of four cases. J Hand Surg [Am]. 1994;19(2):232–7. 3. Songcharoen P, Mahaisavariya B, Wongtrakul S, Lamsam C. Ipsilateral median nerve’s fascicle transfer for restoration of elbow flexion in root avulsion brachial plexus injury. J Thai Orthop Surg. 2001;26(2):93–5. 4. Haninec P, Sámal F, Tomás R, Houšťava L, Dubový P. Direct repair (nerve grafting), neurotization, and end-to-side neuropathy in the treatment of brachial plexus injury. J Neurosurg. 2007;106(3):391–9. 5. Nath RK, Lyons AB, Bietz G. Physiological and clinical advantages of median nerve fascicle transfer to the musculocutaneous nerve following brachial plexus root avulsion injury. J Neurosurg. 2006;105(6):830–4. 6. Brown JM, Shah MN, Mackinnon SE.  Distal nerve transfers: a biology-based rationale. Neurosurg Focus. 2009;26(2):E12. 7. Geuna S, Papalia I, Tos P. End-to-side (terminolateral) nerve regeneration: a challenge for neuroscientists coming from and intriguing nerve repair concept. Brain Res Rev. 2006;52(2):381–8.

5

Terminology

“Anatomy is said to be the basis of medicine”. Probably everyone agrees with that. However, ever since the earliest beginning of anatomy as a scientific discipline, there has been a problem of crucial importance: how to name the structures described in such a way that every student and every reader of anatomical literature can understand what is being referred to. That is because such a large number of different names, synonyms, and eponymic terms existed that even eminent experts could not decipher the expressions used to indicate the anatomical structures [1]. Knowledge of anatomical terminology and its correct use is an indispensable part of medical training. The Latin language forms the basis of anatomical terminology. The concise, apt, and comprehensible naming of anatomical units, organs, and their parts in conformity with the use of official international anatomical terms is the first precondition for communication so important in the practice of medicine. The creation of medical terminology is a gradual and ongoing process. From the philological point of view, it involves not only a merging of Latin and Greek elements, but also Arabic and, with the development of science and different fields of medicine, some words are taken from other languages as well. Anatomical terms are the basis of medical terminology. The development of science and technology is advancing at a rapid pace. New terms are created, and at the same time, many terms fall out of use. The movement in specialized (medical) vocabulary is far more rapid than in the basic vocabulary, and that is why there is such an urgent need to update anatomical terms [2]. The first attempt of radical reform and unification of anatomical terminology was Andreas Vesalius (1514–1564). Although Vesalius managed to introduce a certain degree of transparency and order into anatomical nomenclature, for various reasons, his system did not become firmly established. Nevertheless, the name of Vesalius is linked with the first systematic effort to remove anarchy and confusion in anatomical terminology. Unmistakable success in endeavour to achieve an international codification of anatomical terminology only came in the nineteenth century (the Basel Anatomical Nomenclature, BNA, 1895). In the twentieth century, it was modified and changed © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_5

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several times (the Jena Anatomical Nomenclature published in 1939, the Paris Anatomical Nomenclature, 1955), but even then not everyone was satisfied. At a congress in Rio de Janeiro in 1989, a Federative Committee of Anatomical Terminology (FCAT) was appointed in accordance with proposals from 56 national anatomical associations-members of the International Federation of Anatomical Associations (IFAA). The task of FCAT was “after consultations with all the members of IFAA to prepare an official nomenclature for anatomical disciplines”, because “anatomical terminology is the basis of medical terminology and it is important for doctors and scientist worldwide to use the same terms for each structure” (Whitmore, President of FCAT, in: Terminologia Anatomica, 1998). The outcome of the activities of FCAT was the publication of an official anatomical terminology, Terminologia Anatomica (TA, 1998). The publication gives the Latin terms (or in some cases Greek), which are obligatory (all of them, however, are included in the index as “Latin terms”), together with the correct English ones [1]. Terminologia Anatomica (TA 98; Thieme, Stuttgart), the successor to Nomina Anatomica as the international standard of human anatomical terminology, was first published as a book in 1998 and was recently reprinted (2011). The anatomical terms were listed according to systemic, topographical, and alphabetical rules, which influenced the typography of the book. Every term was given an identifying number (TA code). Since 2010 the image files of every page of the book are freely available on website: http://www.unifr.ch/ifaa/Public/EntryPage/HomePublic.html (generously hosted by the Université de Fribourg). The on-line TA98 consists of reports from this knowledge base. These reports include hierarchical and alphabetical indexes, near-facsimile pages of chapters and sections of TA98, individual pages for each entity, and individual pages for the analysis of the form and syntax of the Latin terms. The near-facsimile pages are conservatively corrected, but these corrections and the material added by the Informatics Working Group have not yet been approved by FIPAT or IFAA. Therefore, the published book remains the international standard of human anatomical terminology [3]. The Federative International Programme for Anatomical Terminology (FIPAT, the successor of FCAT) deals with the official international standard set of human anatomical terminologies. It is one of the six major fields of activity of the International Federation of Associations of Anatomists (IFAA), the world body of anatomy (the others are Education, Ethics and Humanities, Research, Supranational Projects, and Scientific Publications). The IFAA [http://www.ifaa.net] was founded in 1903, and its membership comprises anatomical societies and associations worldwide. It represents and coordinates all aspects of anatomy and the anatomical sciences. Up to now FIPAT publications and those of its predecessor (FCAT) were in book form. Terminologia Anatomica (TA), Terminologia Histologica (TH), and Terminologia Embryologica (TE) have been published in this format, in 1998, 2008, and 2013, respectively. Henceforth, however, the publications will be web-based (see below). The brief of FIPAT is to coordinate and support the preparation, revision, and publication of documents on the terminology of the anatomical sciences and biomorphology (as set out in the aims of the IFAA). The vision of FIPAT is to

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provide and develop the definitive anatomical terminology which constitutes the basic vocabulary at the core of the health sciences. FIPAT terminologies are designed to be flexible so as to enable continual refinement by making new introductions and by taking account of new developments, such as the continual generation of new terms in areas of clinical practice and of anatomical science (e.g. embryology and neuroscience). FIPAT protocols incorporate continual revision and reorganization in order to meet these challenges. Particular emphasis was given to expanding the content of clinical anatomical terms, to enhance the relevance of FIPAT for the clinical community. The neuroanatomical and sensory organ components were modified in exact accordance with Terminologia Neuroanatomica (TNA)—this new section was developed as a modification of the CNS, PNS, and Sensory Organ sections of TA. Major revisions were introduced, also in response to recent advances in molecular neuroscience. The relevant histological terms were merged. Terminologia Neuroanatomica currently can stand alone. It, including the blood supply to the CNS, is also to constitute verbatim a component of TA and should be again accessed through the website: http://fipat. library.dal.ca/tna/. Every official FIPAT term is in Latin, is ideally singular (except where it heads a list), and consists of the minimum number of words. Being in Latin, it provides the focal reference point which enables clear communication and provides the key link for translation into any vernacular. Latin has the unique advantage of being apolitical. The Latin subcommittee ensures a common and consistent approach across the terminologies. It aids all aspects of Latin naming and translation at an exacting standard. Whereas standardized English is extending widely and becoming the lingua franca of biomedical science, FIPAT takes account of the fact that clinical practice still uses and will continue to use national or regional languages. Hence the value of having Latin as the pivotal reference term is preferred. The FIPAT format is designed to facilitate translation into vernacular languages that use anatomy as the basis of their medical training and practice. Revised and new FIPAT documents are to be for the time being constituted in six columns, replacing the three-column arrangement which was standard in the publications. This arrangement enables unequivocal identification of the official Latin and English terms, of common synonyms in both English and Latin, and of eponyms. TNA is a recent revision of the terminology on the central nervous system (CNS; systema nervosum centrale), the peripheral nervous system (PNS; systema nervosum periphericum), and the sensory organs (organa sensuum). These were abstracted from the Terminologia Anatomica and the Terminologia Histologica and were extensively updated by the FIPAT Neuroanatomy Working Group and merged to form a Terminologia Neuroanatomica (TNA). Because of its clinical and functional significance, the TNA includes the blood supply to the CNS (vasa sanguinea encephali and vasa sanguinea medullae spinalis) to ensure it contains a more or less complete list of terms for the human nervous system. The document is divided into three chapters. The official FIPAT terms are in Latin. This enables translation into

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any vernacular, in the present instance English. The Latin terms have been reviewed by members of the FIPAT Latin Subcommittee [4]. The number of studies describing variabilities and anomalies in arrangements of intraspinal (both extradural and also intradural) spinal nerve courses raised as a result of multiple observed radiological or surgical findings influencing the actual treatment management. The authors usually refer these unusual findings as variations or anomalies, or in a case of found connecting branch, it is termed as anastomosis between nerve roots. This is not terminologically correct, because anastomosis refers usually to the connection between two tubular structures (having lumen, like vessels, intestines, ducts, etc.); in a case of constant nervous connection, it is more termed as ansa. The Federative International Programme for Anatomical Terminology (FIPAT) in its most recent update (February 2017) for such nervous connections (with proved nervous fibres presence) recommends the term “communicating branch(es)”. That is why we also prefer this terminology in this our book.

References 1. Holomáňová A, Brucknerová I. Anatomical terms I. (Anatomické názvy I. Latinsko-anglickoslovenský slovník). Bratislava: Elán; 2001., 94 p. isbn:80-85331-29-2. 2. Holomáňová A, Brucknerová I.  Anatomical terms III. (Anatomické názvy III.  Latinskoanglicko-slovenský slovník). Bratislava: Elán; 2003., 154 p. isbn:80-85331-39-X. 3. FCAT. Terminologia Anatomica. Stuttgart: Thieme; 1998. 4. FIPAT.  Terminologia neuroanatomica. FIPAT.library.dal.ca. Federative International Programme for Anatomical Terminology, February 2017.

Part II Vertebral Column and Spinal Cord

6

General Description

The vertebral column must combine great strength and flexibility and protect neural elements. Bones, ligaments, and muscles provide its stability and increase its strength. The vertebral column is flexible, as it has many closely stacked joints. Intervertebral discs make up about 25% of the spine length. Daily changes in the volume of a disc lead to a loss of its height in the evening. Dehydration of the disc causes a loss of height in older people. Ageing and degenerative changes also affect connective tissue—ligaments and osseous tissue of the spine. Any degenerative changes affecting the spinal canal or the neuroforamen can result in a radicular syndrome. All of these changes can cause nerve root angulation with the edge of neuroforamen, which results in a direct or axonal or myelin injury. In the early embryonic stage, the spinal cord fills the entire spinal canal, and its segments are at the height of individual vertebrae [1]. Bundles of root fibres are then short in all sections. Later, the rapid growth of the spine results in a relative shortening of the spinal cord, and spinal roots are extended, particularly in the caudal divisions. Lumbosacral nerve roots have almost a vertical course and pass in a considerable distance in the intrathecal space until they enter the corresponding nerve sleeve and leave the spinal canal below the pedicle of the corresponding vertebra. At the lumbar level, nerve roots are formed and leave the spinal canal passing around the medial part of the ipsilateral pedicle. Spinal nerves are formed slightly below the pedicle. Each spinal nerve lies at the lower end of the ipsilateral vertebra, i.e. above the intervertebral disc at that level. A ganglion of the dorsal root lies directly beneath the pedicle centre. There is limited space for a neurovascular bundle in the intervertebral foramen. The posterior portion of the intervertebral disc, the adjacent portion of the vertebral body, limit the intervertebral foramen along with the pedicles of two adjacent vertebrae, and posteriorly by articular processes and their articulation with the capsular ligament. The ligament covers the articular capsule and extends into the foramen (Figs. 6.1 and 6.2). © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_6

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6  General Description

Pedicle

Conus medullaris

Spinal ganglion

Cauda equina

Filum terminale

Fig. 6.1  Anatomy of roots of lumbosacral region, ventral view

In the intervertebral canal, the dura mater forms firm connections with pedicles, as well as with the posterior longitudinal ligament and with the capsule of the articular facet.

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47

Dura meter

Arachnoidea

Pia meter

Dorsal roots

Spinal ganglion Th12

a

Dorsal roots

Ventral nerve roots

L1

L2

L3

L4

L5

b Fig. 6.2 (a) Anatomy of roots of lumbosacral region, side view. (b) Lumbar nerves cross the intervertebral disc just above. The foramen and enter the foramen next to pedicles

Local fibrosis of nerve sleeves, hyperplasia, or fibrous adhesions can also be a result of mechanical forces and lead to nerve compression causing foraminal stenosis. This in cooperation with the restricted blood supply caused by vascular compression results in ischaemia. The spinal column is built up from alternating bony vertebrae and fibrocartilaginous discs, which are intimately connected by strong ligaments and supported by powerful musculotendinous masses. There are 33 vertebrae (7 cervical, 12 thoracic, 5 lumbar, 5 sacral, and 4 coccygeal), although the sacral and coccygeal vertebrae are usually fused to form the sacrum and coccyx. The increasing size of the vertebral bodies from above downward is related to the increasing weights and stresses borne by successive segments and the sacral vertebrae and fused to form a solid wedgeshaped base—the keystone in a bridge whose arches curve down toward the hip joints. The intervertebral discs act as elastic buffers to absorb the many mechanical shocks sustained by the spinal column. Only limited movements are possible

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between adjacent vertebrae, but the sum of these movements confers a considerable range of mobility, on the vertebral column as a whole. Flexion, extension, lateral bending, rotation, and circumduction are all possible, and these actions are freer in the cervical and lumbar regions than in the thoracic one. Such differences exist because the discs are thicker in the cervical and lumbar areas, the splinting effects produced by the thoracic cage are lacking, the cervical and lumbar spinous processes are shorter and less closely apposed, and articular processes are shaped and arranged differently. Human evolution from a quadrupedal to a bipedal posture was mainly affected. An upright posture greatly increases the load borne by the lower spinal joints by the tilting of the sacrum between the hip bones together with an increase in lumbosacral angulation, and also by minor adjustments of the anterior and posterior depths of various vertebrae and discs, an upright posture greatly increases the load borne by the lower spinal joints. Some static and dynamic imperfections remain and predispose to strain and backache. The vertebral canal extends through the entire length of the column and provides excellent protection for the spinal cord. The spinal vessels and nerves pass through intervertebral foramina formed by notches on the superior and inferior borders of the pedicles of adjacent vertebrae, bounded anteriorly by the corresponding intervertebral discs, and posteriorly by the joints between articular processes of adjoining vertebrae. Pathologic or traumatic conditions affecting any of these structures may produce pressure on the nerves or vessels they transmit. The spinal cord functions primarily in the transmissions of nerve signals from the motor cortex to the body and from the afferent fibres of the sensory neurons to the sensory cortex. It is also the centre for coordinating many reflexes and contains reflex arcs that can independently control reflexes and central pattern generators [2]. The vertebral column surrounds the spinal cord which travels within the spinal canal, formed from a central hole within each vertebra. The spinal cord is a part of the central nervous system that supplies nerves and receives information from the peripheral nervous system within the body. The spinal cord consists of grey and white matter and a central cavity, the central canal. Adjacent to each vertebra emerge spinal nerves. The spinal nerves provide sympathetic nervous supply to the body, with nerves emerging forming the sympathetic trunk and the splanchnic nerves. The spinal canal follows the different curves of the column; it is large and triangular in those parts of the column which enjoy the greatest freedom of movement (such as in the cervical and lumbar regions) and it is small and rounded in the thoracic region, where motion is more limited [3]. The spine is made of 33 individual bones stacked one on top of the other. This spinal column provides the main support for the body, allowing to stand upright, bend, and twist while protecting the spinal cord from injury. Strong muscles and bones, flexible tendons and ligaments, and sensitive nerves contribute to a healthy spine. Any of these structures affected by strain, injury, or disease can cause pain. When viewed from the side, an adult spine has a natural S-shaped curve. The cervical and lumbar regions have a slight concave curve, and the thoracic and sacral regions have a gentle convex curve. The curves work like a coiled spring to absorb shock, maintain balance, and allow a range of motion through the spinal column.

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The two main muscle groups that affect the spine are extensors and flexors. The extensor muscles enable us to stand up and lift objects. The extensors are attached to the back of the spine. The flexor muscles are in the front and include the abdominal muscles. These muscles enable to flex or bend forward and are important in lifting and controlling the arch in the lower back. The back muscles stabilize the spine. Only top 24 vertebrae are movable. The neck has the greatest range of motion because of two specialized vertebrae that connect to the skull. The first vertebra is the ring-shaped atlas that connects directly to the skull. This joint allows for the nodding or “yes” motion of the head. The second vertebra is the peg-shaped axis, which has a projection called the odontoid that atlas pivots around this joint allow for the side-to-side or “no” motion of the head. The main function of the thoracic spine is to hold the rib cage and protect the heart and lungs; the range of motion in the thoracic spine is limited. The main function of the lumbar spine is to bear the weight of the body. These vertebrae are much larger in size to absorb the stress of lifting and carrying heavy objects. The main function of the sacrum is to connect the spine to the hip bones. Together with the iliac bones, they form a ring called the pelvic girdle. Bones of the coccyx provide attachment for ligaments and muscles of the pelvic floor. Each vertebra in the spine is separated and cushioned by an intervertebral disc, keeping the bones from rubbing together. Discs are designed like a radial car tire. The outer ring called the annulus has crisscrossing fibrous bands, much like a tire tread. These bands attach between the bodies of each vertebra. Inside the disc is a gel-filled centre— nucleus much like a tire tube. Disc function resembles coiled springs. The crisscrossing fibres of the annulus pull the vertebral bodies together against the elastic resistance of the gel-filled nucleus. The nucleus acts like a ball-bearing when a person moves, allowing the vertebral bodies to roll over the incompressible gel. The gel-filled nucleus is composed mostly of fluid. This fluid absorbs during the night as a person lies down and is pushed out during the day as you move upright [4]. With age, discs increasingly lose the ability to reabsorb fluid and become brittle and flatter; this is why we get shorter as we grow older. Also, diseases, such as osteoarthritis and osteoporosis, cause bone spurs (osteophytes) to grow. Injury and strain can cause discs to bulge or herniate, a condition in which the nucleus is pushed out through the annulus to compress the nerve roots causing back pain. On the back of each vertebra are bony projections that form the vertebral arch. The arch is made of two supporting pedicles and two laminae. The hollow spinal canal contains the spinal cord, fat, ligaments, and blood vessels. Under each pedicle, a pair of spinal nerves exits the spinal cord and passes through the intervertebral foramen. Seven body processes arise from the vertebral arch to form the facet joints and processes for muscle attachment. The facet joints of the spine allow back motion. Each vertebra has four joint facets, one pair that connects to the vertebra above and one pair that connects to the vertebra below. Ligaments are strong fibrous bands that hold the vertebrae together, stabilize the spine, and protect the discs. The three major ligaments of the spine are the ligamentum flavum, anterior longitudinal ligament, and posterior longitudinal ligament.

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The ligaments are continuous bands that run from the top to the bottom of the spinal column along the vertebral bodies. They prevent excessive movement of the vertebral bones. The ligamentum flavum attaches between the lamina of each vertebra of the spinal cord. The nerve supply to the upper limb involves the fourth cervical to second thoracic spinal cord segments and that to the lower limb, the third lumbar to third sacral spinal cord segments. The spinal cord runs within the protective spinal canal from the brainstem to the first lumbar vertebra. At the end of the spinal cord, the cord fibres separate into the cauda equine and continue down through the spinal canal to the tailbone before branching off to the legs and feet. The spinal cord serves as an information highway, relaying messages from the cord between the brain and the body. Sometimes, the spinal cord can react without sending information to the brain. These particular pathways called spinal reflexes are designed to protect our body (from harm) immediately. The spinal cord is covered with the same three membranes as the brain, called meninges [5]. The inner membrane is the pia mater, which is intimately attached to the cord. The next membrane is the arachnoid mater. The outer membrane is the tough dura mater. Between these membranes are spaces. The space between the pia mater and arachnoid mater is the vast subarachnoid space, which surrounds the spinal cord and contains cerebrospinal fluid. The space between the dura mater and the bone is the epidural space. The cord is surrounded by dura, arachnoid, and pia mater, which are continuous with corresponding layers of the cerebral meninges at the foramen magnum. The spinal dura mater, unlike the cerebral, consists only of a meningeal layer that is not adherent to the vertebrae; it is separated from the boundaries of the vertebral canal by an epidural space containing fatty areolar tissue and many veins. The spinal and cranial subarachnoid spaces are continuous and contain cerebrospinal fluid. The pia mater closely invests the cord; on each side, it sends out a series of 22 triangular processes, the denticulate ligaments, which are attached to the dura mater and thus anchor the cord. The spinal cord is considerably shorter than the vertebral canal, the meninges, the cerebrospinal fluid, and the epidural fatty tissue and veins which combine in against jarring contacts with its bony and ligaments surroundings. These are 31 pairs (8 cervical, 12 thoracic, 5 lumbar, 5 sacral, and 1 coccygeal) of symmetrically arranged spinal nerves, attached to the cord in linear series by anterior and posterior nerve rootlets, or filaments, which coalesce to form the nerve roots. Each posterior spinal nerve root possesses an oval enlargement, the spinal (sensory) ganglion in early embryonic life, the cord as long as the vertebral canal, but as development proceeds, it logs behind the growth of the vertebral column. Consequently, the cord segments move upward in relation to the vertebrae, and the nerve roots, originally horizontal, assume an increasingly oblique direction from above downward as they proceed to their foramina of exit. In the adult, except in the upper cervical region, the cord segments lie at the varying distances above the corresponding vertebrae. For clinical purposes, it is customary to localize them in relation to the vertebral spinous processes. In the lower cervical region, the vertebral

References

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spines are one lower in number than the corresponding cord segments; in the upper thoracic region, two lower in number; and in the lower thoracic region, three lower in number. For example, the fourth thoracic spinous process is approximately level with the sixth thoracic cord segment. The lumbar, sacral, and coccygeal segments of the cord are crowded together and occupy the space approximately opposite the ninth thoracic to the first lumbar vertebrae. These alterations of the cord segments relative to the vertebral segments explain why the cervical enlargement (C4 to T2) lies approximately opposite the corresponding vertebrae, whereas the lumbar enlargement (L3 to S3) lies opposite the last three thoracic vertebrae. The nerve roots attached to the lower part of the cord descend to their points of exit as the cauda equine, named for their resemblance to the tail of a horse.

References 1. Kapeller K, Pospíšilová V.  Embryologický atlas. Martin: Osveta; 1996, 119 p. isbn:80-217-0549-3. 2. Alini M, Ito K, Nerlich AG, Boos N. Aging and pathological degeneration, aospine manual, vol. 1. Stuttgart: Thieme; 2007. p. 87–100. 3. Aebi M, Artel V. Degenerative spinal disease, aospine manual, vol. 2. Stuttgart: Thieme; 2007. p. 561–7. 4. Čihák R. Páteř. In: Anatomie 1. Praha: Grada; 2001. p. 89–123. 5. Neidlinger-Wilke C, Wilke HJ. The biology of intervertebral disc degeneration. In: Szpalski M, Gunzburg R, Rydevik B, Le Huec JC, Mayer H, editors. Surgery for Low Back Pain. Berlin, Heidelberg: Springer; 2010. p. 3–10. isbn:978-3-642-04547-9.

7

Overlapping Innervations and Embryonic Explanations

The importance of determining the spinal root segments is that according to the peripheral location of sensitivity changes and impairment of muscle innervations, the place of a pathological process affecting the spinal cord can be determined. The practical importance is in defining the areas of sensitivity innervated by individual nerves (areae nervinae), as well as determining the areas of the arrival of fibres of certain roots—segments (areae radiculares) (Figs. 7.1, 7.2, and 7.3). Both borders—areae nervinae and areae radiculares—overlay on the thorax, the abdomen, and the back, where the nerves maintain their segmentary arrangement. These are innervation regions of intercostal nerves and dorsal branches of the spinal nerves. On the head, neck, and limbs, areae nervinae have different borders than areae radiculares. Development of the nervous system can answer why. In the first weeks of embryonal development, the arrangement of the spinal nerves is simple. The dorsal mesoderm is divided into somites and in each somite enters a single root nerve of the relevant section of the spinal cord. Very soon, however, the cellular material of somites, from which the foundations of skeletal muscles and the fibrous part of the skin arise, grows, enlarges, and extends; the foundations of muscles are moved to other sites—especially in the areas of developing limbs. This also results in changes of nerve arrangement, which can be well demonstrated by the development of muscles. The basis for muscles, a myotome, is divided into the dorsal and ventral myomere. This is also reflected in the division of the nerve into the dorsal and ventral branch for the relevant region of the myotome. Epaxial muscles (autochthonous back muscles) arise from dorsal myomeres. They retain (after merging into longer muscles) their metameric arrangement. Thus, dorsal branches of spinal nerves retain the original simple segmental course [1, 2]. Hypaxial muscles arise from the ventral myomeres, and they preserve their metameric arrangement only on the thorax (intercostal muscles). In other parts of the body, the bases of definitive muscles are formed of materials of two or more adjacent myomeres, and when moving, they draw out relevant nerves. The course of a nerve then shows the path, along which the muscle moved and relocated from the original site. This development results in significant changes © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_7

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7  Overlapping Innervations and Embryonic Explanations

N. occipitalis N. occipitalis minor N. auricularis magnus Rr. posteriores nn. spinales cervicales

C2 C3 C4 C5

Nn. supraclaviculares N. cutaneus brachii lateralis

C6 C7

T1 T2 T3 T4 T5 T6 T7 T8 T9 T10 T11 T12 L1 L2 L3 L4 L5

N. cutaneus brachii medialis N. cutaneus brachii posterior Rr. posteriores nn. spinales thoracales Rr. laterales nn. intercostales N. cutaneus antebrachii lateralis N. cutaneus antebrachii posterior N. cutaneus antebrachii medialis N. radialis

C8

C6

C7 C8

S1

C8 C7

S2

S3 S4 S5

N. ulnaris L5

N. medianus

L1

N. iliohypogastricus N. cutaneus femoris lateralis N. cutaneus femoris posterior N. obturatorius

S2

S1

L2

N. cutaneus surea medialis N. saphenus

L3

S2 S1 N. cutaneus surae lateralis

L4

S1

N. suralis N. plantaris lateralis N. plantaris medialis

Fig. 7.1  Area nervorum et area radiculares—dorsal view

L5

L4

7  Overlapping Innervations and Embryonic Explanations

55

N. trigeminus r. ophthalmicus r. maxillaris r. mandibularis N. auricularis magnus N. cutaneus colli Nn. supraclaviculares

C2 C3 C4 C5 T1 T2 T3

N. cutaneus brachii lateralis N. cutaneus brachii medialis

T4 T5

Nn. intercostales

T1

T6

C6

T7 T8 T9

N. cutaneus antebrachii Iateralis N. cutaneus antebrachii medialis

C8

C5

T10 T11

N. iliohypogastricus N. radialis N medianus

C6

T12 L1

N. ulnaris

S2-3

C8 C7

L2

N. genitofemoralis N. cutaneus femoris lateralis N. femoralis N. obturatorius

L3

L4

N. cutaneus surae Iateralis

L5

N. saphenus L4

S1 N. peroneus superficialis N. suralis N tibialis N. peroneus profundus

Fig. 7.2  Area nervorum et area radiculares—ventral view

L5

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7  Overlapping Innervations and Embryonic Explanations

C1 2 3

Seg. cervicales (C1-C8)

4 5 6 7

C3 C4

Cervical nerves

C5 C6 C7 C8

T1

T1

2

T2

3

T3

4 Seg. thoracicae (T1-T12)

C1 C2

T4

5

T5

6

T6

Thoracic nerves

7

T7

8

T8

9

T9

10

T10

11

T11

12

Seg. lumbales (L1-L5)

T12 L1

Seg. sacrales (S1-S5)

2

Seg. coccygea

3

Cauda equina

Lumbar nerves

L1 L2 L3

Sacral nerves

4 L4 5 S1 2 3 4 5 Co

Fig. 7.3  Spinal segments, spinal roots, and nerves

L5 Coccygeal nerves S1 S2 S3 S4 S5 n. coccygeus

7  Overlapping Innervations and Embryonic Explanations

57

in the arrangement of ventral branches of the spinal nerves—as they exit from the spinal canal they link to each other, exchange root fibres, and form plexuses from which the relevant nerves are formed [3]. Virtually, each nerve extending from the plexus consists of fibres of several roots and conducts them to its innervation area. Conversely, fibres from a single root are again brought into its radicular zone through several nerves. Areae nervinae are easy to identify by the preparation of individual nerves to their finest peripheral branches. Their scope and size are presented on the skin and muscles. Areae radiculares form original horizontal bands that are regular in humans only on the thorax. Uneven growth causes that they are inclined differently and extend obliquely to the abdomen and vertically to the lower extremities. The borders of radicular zones are not exactly known, with the exception of places where they correspond with the areae nervinae because a detailed anatomical preparation of root fibres from places of their protrusion to the finest peripheral small branches is extremely complicated and has not been performed so far. Determining the root zones is mainly carried out on the basis of clinical observations in disorders of innervation. Nerves supplying neighbouring dermatomes overlap, so the interruption of one dorsal nerve root leads to hypaesthesia rather than anaesthesia. Damage to at least three spinal nerves or their dorsal roots results in complete anaesthesia of the skin in any area. The exception is the C2 nerve root. Its damage results in complete anaesthesia in the occipital areas of the skin. The degree and extent of the overlap depend on different types of sensitivity—it is greater for the tactile sensitivity and the temperature. The large muscles (particularly of the extremities) are innervated from several ventral nerve roots. Therefore, paresis occurs when one or more roots are damaged, but paralysis appears following a lesion of minimum two roots. 1. Individual radicular zones are overlapping. Each area of the skin is innervated from three nerves—one main and two neighbouring: cranial and caudal, positioned higher and lower. According to some clinical experience, even two roots cranially and two roots caudally intervene the main root. 2. In some individuals, the entire radicular zone is shifted upward or downward. This shifting presents a half to the whole segment (prefixed and postfixed type). 3. It is better to assume the site of disorder according to symptoms of the segment that is the most cranial. Segmental innervation of muscles is wiped over more than the skin innervation. The same rules apply to the motor innervation of muscles. Dorsal branches (rami dorsales) of spinal roots that are determined for back muscles and adjacent skin areas keep the segmental arrangement best. Afferent fibres are sensitive; they provide conduction of general sensitivity modalities—touch, vibration, and temperature. Sensory fibres carry impulses from specialized organs: eye, vestibulocochlear apparatus, olfactory, and gustatory analysers.

58

7  Overlapping Innervations and Embryonic Explanations

Sensitive nerve fibres are getting to all viscera from the spinal nerves. They conduct feelings of visceral pain. Indeed, there are also areae radiculares viscerales. The bowels and vermiform appendix are innervated bilaterally. Since a topographical position of internal organs varies considerably during development (descending of the diaphragm, heart, gonads), visceral root districts are found in a completely different site than the corresponding segmentary skin areas. One may understand why in the cases of acute abdominal diseases nociceptive stimuli from the abdominal region shoot brachially via phrenic nerve (n. phrenicus) (the same root innervation of C4 and C5). In the case of carcinoma of the sigmoid colon, pains are projecting via obturator nerve (n. obturatorius) to the knee region; in a case of prostatitis, symptoms of sciatica can appear. Efferent fibres are motor and autonomous. The motor fibres carry impulses to the striated muscles and autonomous fibres to the glands, smooth muscle cells, and the myocardium. Autonomous fibres belong to the sympathetic or parasympathetic system. Each spinal nerve is formed by two spinal roots. A posterior (dorsal) root contains somatosensory fibres carrying impulses to the spinal cord from the skin and musculoskeletal apparatus and viscerosensory fibres carrying impulses from the internal organs. Part of the dorsal root is a spinal node—ganglion (spinal ganglion). The anterior (ventral) root contains motor fibres innervating skeletal muscles (somatomotor fibres) as well as smooth muscles and glands (visceromotor fibres). While the bodies of somatomotor neurons are located in the ventral horns of the grey matter of the spinal cord, the bodies of visceromotor neurons are situated outside the central nervous system in the so-called autonomic (sympathetic or parasympathetic) ganglia. The ventral branches of spinal nerves are thinner than dorsal, except for the first and the second cervical nerve. All dorsal spinal nerve branches retain their segmentary arrangement. They separate from the trunk of spinal nerves immediately after their exit from the intervertebral foramen. They turn backward to back muscles and adjacent parts of the skin, where they are depleted. All dorsal branches (but not the first cervical, the fourth and fifth sacral and coccygeal nerves) divide into one medial and one lateral branch, after a short course. Superior clunial nerves (nn. clunium superiores) are sensitive branches from dorsal branches (rami dorsalis) of L1–L3 roots. They penetrate through the aponeurosis of wide back muscles and extend laterocaudally to the skin of the upper gluteal region. Medial branches (rami mediales) are mixed. They contain motor fibres for the back muscles and sensitive fibres for innervations of relevant skin areas. Sensitive fibres are declining caudally, so the last thoracic and all lumbar roots are almost exclusively motor ones. Lateral branches (rami laterales) are in the cervical and upper thoracic region motor; caudally (in the lower thoracic region and L1–L3), they contain sensitive fibres, i.e. they are mixed and thicker than the medial fibres; and in the region

References

59

L4–L5, they are motor again. Dorsal branches (rami dorsales) of five sacral nerves and one coccygeal nerve are sensitive, rather than thin; S1–S4 nerves are leaving the sacral spinal canal through dorsal sacral foramina (foramina sacralia dorsalia) and S5 and Co through the sacral hiatus. Middle clunial nerves (nn. clunium medii) are three small lateral branches from the dorsal branches (rami dorsales) of S1–S3 nerves. They break through the cranial part of the gluteus maximus muscle and innervate the skin in the sacral and adjacent gluteal region. The root S4 (depending on the type of the plexus) is mostly involved in the formation of pudendal nerve (n. pudendus), in the innervation of ischiococcygeal muscles of levator ani muscle and, partially, of the perineal region. S4 is emitting a small branch to S5-Co and participating in the formation of the upper and lower hypogastric plexus. The anococcygeal nerve (n. anococcygeus, branch of the Co nerve) innervates coccygeal muscles. They may receive fibres from S4 or S3, too. They are thin small nerve branches forming the plexus on coccygeus muscle. Dorsal branches of the last two sacral nerves are tiny and lie below multifidus muscle. They do not divide into medial and lateral branches, but they anastomose with the dorsal branch of the coccygeal nerve. They form a network—connections on the dorsal part of the sacrum. The fibres of this plexus supply the skin above the coccyx. Anococcygeal nerve (n. anococcygeus) extends from the plexus running around the sacrotuberal ligament between the anus and coccyx. In addition, several small branches innervate levator ani muscle and coccygeus muscle. In patients with fractures of the coccyx, defecation (due to squeezing of these nerves) is accompanied by stubborn pain.

References 1. Kapeller K, Pospíšilová V.  Embryologický atlas. Osveta: Martin; 1996. 199 p. isbn:80-217-0549-3. 2. Mráz P. Anatómia ľudského tela 2, 1.vyd. Bratislava: Slovak Akademic Press; 2005. 286 p. 3. Kapeller K, Pospíšilová V.  Embryológia človeka. Osveta: Martin; 2001. 370 p. isbn:80-8063-072-0.

Part III Intraspinal Connections of Nerve Roots

8

General Description

The aim of the presented work is to point out intraspinal anatomical variations of nerve roots and their interrelationships throughout the spinal canal, as well as their possible impact on the clinical picture. Very few studies have reported occasional intradural and extradural communications between adjacent roots [1, 2]. These studies mostly focus on lumbosacral and cervical regions, rarely the thoracic region. Additionally, such communications are primarily between the dorsal rootlets, while ventral root intercommunications have rarely been reported [3, 4]. To our knowledge, no study has reported interconnections between intradural and extradural nerve roots in the cervical, thoracic, or lumbosacral region in reference to a normal, prefixed, or postfixed type of brachial and lumbosacral plexuses. Most of the papers dealing with intraspinal variations of nerve roots took into consideration extradural anatomical variations of lumbosacral nerve roots [5–17]. Our work comprehensively evaluates a topic of intraspinal intradural and extradural variations of nerve roots. The presented study was undertaken to determine if there is any relationship between the level and concentration of root interconnections and significance of these variations for the formation of plexuses. The anatomical data collected from 43 cadavers with nerve root variations represent the basis of the report. Such data may be important for the diagnosis of radiculopathy and may help to improve understanding of nerve root injuries and other intrathecal pathological processes. Anatomical and surgical textbooks give almost no attention to the intradural communications between intradural roots. These communications are of significance in various neurosurgical procedures and clinical conditions. Knowledge of the specific anatomy and variations of this area is important. Brachial plexus is formed by contributions from C5 to T1, where the communications between the C4–C5 and C8–T1 may lead to misinterpretations of crucial roots. The communications of the roots may explain the clinical variations and overlapping sensory symptoms caused by nerve root compression. Further, physical examinations reveal unexpected results such as altered deep tendon reflexes or sensory dermatomes different from the expected segmental innervation pattern which may be produced by © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_8

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8  General Description

intradural communications between roots. Failure to identify these communications means missing their functional contributions. Clinicians should be aware of the communication between the dorsal rootlets of the spinal nerves in order to localize the level of pathology accurately on the basis of clinical signs and symptoms. Due to these communications, if a dorsal rootlet is injured, a small segment of the neighbouring rootlets may be injured as well. For this reason, clinical localization might occur one segment above or below the pathological condition. There is no fine imaging instrumentation yet to show these communications. They not only exist in cervical and lumbosacral rootlets but can also be present at all spinal levels and also should be taken into consideration during surgical procedures and diagnostic evaluations as well as in the treatment. The sacral nerve roots form a dense neural network around the conus medullaris with multiple interconnections and without the segmental separation typically encountered in the lumbar, thoracic, and cervical spinal cord. However, the roots are loosely organized into bundles by arachnoid membranes. Typically, nerve roots of different spinal cord segments are separated by interradicular gaps. At the level of conus medullaris, these gaps are no longer present and make orientation more difficult. No gaps were found at the level of conus medullaris. The ventral roots of S1–S5 consisted of fewer rootlets. In contrast, the dorsal roots typically had more rootlets with an overall decreasing number of rootlets from the rostral to the caudal direction. Also, other investigators of intradural anatomy have not found the ventral S5 root to be inconsistently present [18, 19]. They did not identify coccygeal roots. They found anastomoses frequently between dorsal roots and less frequently between ventral roots, but never found a bridge between the dorsal and ventral roots. Some investigators observed none of the anastomotic fibres extended beyond one spinal segment and no intersegmental anastomoses between the ventral roots [4]. Clinically, the high frequency of anastomoses in this anatomical region may translate into the loss of dermatomal organization with sequent misleading findings or symptoms in surgery; the presence of frequent anastomoses increases the density of the neural network around the conus medullaris and thus makes orientation as well as dissection more difficult. These data may help for intraoperative orientation. Furthermore, differences in root size may account for various effects of anaesthetics during epidural or spinal anaesthesia. In contrast to the extramedullary origin of the dorsal spinal roots, the ventral roots arise from motoneurons in the anterior spinal horn that never seems to undergo segmentation. These motoneurons, innervating a given skeletal muscle, are grouped in a slender columnar arrangement. In the anterior horn of the cervical and lumbar cords, the motoneuron columns are closely packed because of many skeletal muscles in the upper and lower extremities to be innervated. The intersegmental anastomoses at these levels suggest that the motoneuron columns formed much longer craniocaudal distribution than had previously been suspected [4]. It is not always possible to localize the level of cervical pathology accurately on the basis of clinical signs and symptoms. Intradural intersegmental connections between sensory rootlets occur frequently in the cervical region and have been shown to be clinically and surgically significant. Similar connections between

References

65

motor rootlets also have been noticed, but their incidence was not reported. Alteration of the deep tendon reflexes, muscle spasm, muscle weakness, and atrophy also may deviate from the expected pattern of innervation. Inconsistencies in the formation of nerve plexuses (i.e. pre- and postfixation of the brachial and lumbosacral plexuses and nerve root variations) and the final distribution of peripheral nerves are known to cause this deviation. Classical neuroanatomy teaches that the segmental nature of the spinal cord is evident where the posterior and anterior rootlets attach to the posterolateral and anterolateral sulci of the cord. The dermatomes in humans overlap to such an extent that resection of a single root produces no loss of sensibility. Pre- and postfixation of the brachial and lumbosacral plexuses shift the segmental innervation of the neck and upper extremity one level higher or one level lower. Intersegmental connections of anterior and posterior roots probably contribute to variation in dermatome pattern and motor innervation in the distribution of cervical nerves. Previous investigations have not commented on the incidence of anterior intradural connections between nerve rootlets. They may be important in spinal cord trauma and may be responsible for sparing of some motor function below the level of insult. For example, complete C5 quadriplegia may have some C6 motor function from intact rootlets originating from the spinal cord at C5, the connection between C5 and C6. The lumbosacral intrathecal anatomy is complex because of the density of nerve roots in the cauda equina. Space-occupying lesions, including disc herniation, trauma, and tumour, within the spinal canal may compromise the nerve roots causing severe clinical symptoms. The lumbosacral nerve roots innervate muscles that provide movement and allow the sensation of portions of the lower extremities as well as regulation of bladder function.

References 1. Arslan M, Cömert A, Açar Hİ, Özdemir M, Elhan A, Tekdemir İ, Tubbs RS, Attar A, Uğur HÇ. Lumbosacral intrathecal nerve roots: an anatomical study. Acta Neurochir. 2011;153:1435–42. 2. Tubbs RS, El-Zammar D, Loukas M, Cömert A, Cohen-Gadol AA.  Intradural cervical root adjacent interconnections in the normal, prefixed, and postfixed brachial plexus. J Neurosurg Spine. 2009;11:413–6. 3. Marzo JM, Simmons EH, Kallen F. Intradural connections between adjacent cervical spinal roots. Spine. 1987;12(10):964–8. 4. Moriishi J, Otani K, Tanaka K, Inoue S. The intersegmental anastomoses between spinal nerve roots. Anat Rec. 1989;224(1):110–6. 5. Boden SD, Davis DO, Dina TS, Patronas NJ, Wiesel SW. Abnormal magnetic-resonance scans of the lumbar spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg Am. 1990;72(3):403–8. 6. Burke SM, Safain MG, Kryzanski J, Riesenburger RI. Nerve root anomalies: implications for transforaminal lumbar interbody fusion surgery and a review of the Neidre and Macnab classification system. Neurosurg Focus. 2013;35(2):E9. 7. Chotigavanich C, Sawangnatra S.  Anomalies of the lumbosacral nerve roots. An anatomic investigation. Clin Orhop Relat Res. 1992;278:46–50.

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8. Haijiao W, Koti M, Smith FW, Wardlaw D. Diagnosis of lumbosacral nerve roots anomalies by magnetic resonance imaging. J Spinal Disord. 2001;14:143–9. 9. Kadish LJ, Simmons EH. Anomalies of the lumbosacral nerve roots. An anatomical investigation and myelographic study. J Bone Joint Surg (Br). 1984;66(3):411–6. 10. Kikuchi S, Hasue M, Nishiyama K, Ito T. Anatomic and clinical studies of radicular symptoms. Spine. 1984;9:23–30. 11. Neidre A, Macnab I. Anomalies of the lumbosacral nerve roots. Review of 16 cases and classification. Spine. 1983;8(3):294–9. 12. Postacchini F, Urso S, Ferro L.  Lumbosacral nerve-root anomalies. J Bone Joint Surg Am. 1982;64(5):721–9. 13. Rask MR. Anomalous lumbosacral nerve roots associated with spondylolisthesis. Surg Neurol. 1977;8(2):139–40. 14. Scarf FF, Dalman DE, Toleikis JR, Bunch WM. Dermatomal evoked potentials in the diagnosis of lumbar root entrapment. Sur Forum. 1981;32:489–91. 15. Solmaz B, Tatarli N, Ceylan D, Keleş E, Çavdar S. Intradural communications between dorsal rootlets of spinal nerves: their clinical significance. Acta Neurochir. 2015;157:1069–76. 16. Stambough JL, Balderston RA, Booth RE, Rothman RH.  Surgical management of sciatica involving anomalous lumbar nerve roots. J Spinal Disord. 1988;1(2):111–4; discussion 114–115. 17. Yilmaz T, Turan Y, Gulsen I, Dalbayrak S.  Co-occurrence of lumbar spondylolysis and lumbar disc herniation with lumbosacral nerve root anomaly. J Cardiovertebral Jun Spine. 2014;5:99–101. 18. Hauck EF, Wittkowski W, Bothe HW. Intradural microanatomy of the nerve roots S1–S5 at their origin from the conus medullaris. J Neurosurg Spine. 2008;9(2):207–12. 19. Mersdorf A, Schidt RA, Tanagha EA. Topographic–anatomical basis of sacral neurostimulation: neuroanatomical variations. J Urol. 1993;149(2):345–9.

9

Our Observations and Results

The anatomical study was carried out in 43 fresh cadavers without inherited or detected abnormalities, tumour diseases, orthopaedic deformities, and spinal operations within 24 h before the death. The study included 32 men (74.4%) aged 30–75  years and 11 women (25.6%) aged 45–77  years. The subjects had died a violent death, most often in car accidents, when the spine had not been damaged. In the prone position of the cadaver, the paravertebral muscles were separated from spinous processes and vertebral laminas on both sides from the cervico-cranial transition to the sacrum. Spinous processes were removed using bone punches and a Stryker saw. The vertebral laminas on both sides, as well as parts of articular processes, were removed with the Kerrison rongeur. Such “roofing off” allowed direct visualization of the spinal canal without damaging the spinal cord and nerve roots. This wide laminectomy from the cervico-cranial transition to the sacrum revealed the whole spinal canal and enabled to examine each cervical, thoracic, lumbar, and sacral nerve root from its protrusion out of the spinal cord to its exit from the spinal canal through the intervertebral foramen and sacral hiatus. Subsequently, a longitudinal incision of the dura mater was performed. The nerve roots were cut distally from the spinal ganglion to allow direct visualization of the spinal cord, conus medullaris, and spinal nerve roots. The exposed segments of the spinal cord and nerve roots were examined, followed, and explored, including a detailed examination of the intradural and extradural communicating branches (rami communicantes). All intradural and extradural communicating branches (rami communicantes) connecting nerve roots were excised and examined histologically aimed on proving the presence or absence of nervous tissue. The type of the plexus was defined by subtracting from the root C2. Enlargements (intumescentiae) had a different scale of shape and formation. Specification of the type of plexus was carried out on the basis of the formation of intradural and extradural roots. Normal anatomical locations of the cervical enlargement (intumescentia cervicalis) are the C4–T1 segment (C4–T1 vertebra level) and host the neurons providing axons for brachial plexus. Lumbosacral enlargements (intumescentia lumbosacralis) originating from L1–S3 spinal cord segments (T9–T12 vertebra level) give rise to the lumbosacral plexus. © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_9

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9  Our Observations and Results

In the normotype from the top of the cervical enlargement, the C6 root was retracted. In the prefixed type, the C5 root and, in the postfixed type, C7 and C8 roots were retracted. From the cranial part of lumbar enlargement in the normotype the L3 root, in the prefixed type the L2 root, and in the postfixed type L4 and L5 roots were retracted (Fig. 9.1). The determination of the type of plexus was easier on the basis of formation of intradural than extradural roots. Not always was possible to determine clearly the type of plexus. Bordering— transitional types with a tendency more to the prefixed or the postfixed type were present.

C2 C3 C4 C5

C5

C6 C7 C8

C7-C8

Th1 Th2 Th3 Th4 Th5 Th6 Th7 Th8 Th9 Th10 Th11 Th12 L1 L3

L2

L2

L4 L5 S1 S2 S3 S4 S5

Fig. 9.1  Scheme of normal, prefixed, and postfixed type

L4-L5

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9  Our Observations and Results

The normotype of intraspinal intradural and extradural formation of the brachial and lumbosacral plexus was dominant, present in 30 cases (69.8%) (Tables 9.1, 9.2, and 9.3). Variations of the formation were observed in 13 cases (30.2%). The prefixed type occurred in 9 cases (20.9%) (Figs. 9.2, 9.3, and 9.4) and postfixed type in 4 cases (9.3%) (Figs. 9.5, 9.6, and 9.7). The formation of the isolated prefixed or postfixed type of brachial and lumbosacral plexus was not observed. The frequency of intradural and extradural communicating branches between nerve roots showed variations among spinal levels. Table 9.1  Intraspinal intradural variations of nerve roots

Plexus type Number Normotype 30 Prefix. 9 type Postfix. 4 type Total 43

Rami communicantes between dorsal roots C T LS 12 – 30 3 2 9

Rami communicantes between ventral roots C T LS 1 1 6 1 – 2

Rami communicantes between dorsal and ventral roots C Th LS 1 – 6 – – 3

Multiple rami communicantes C T LS 6 – 30 1 1 9

2

–

4

–

–

1

1

–

1

–

–

4

17

2

43

2

1

9

2

0

10

7

1

43

Prefix. prefixed, Postfix. postfixed, C cervical, T thoracic, LS lumbosacral Table 9.2  Atypical spacing—intraspinal variations Common or close double spacing of roots Plexus type Number from one segment C T LS Normotype 30 2 2 15 Prefix. type 9 – – 5 Postfix. 4 1 – 2 type Total 43 3 2 22

Asymmetry of roots C T LS 2 1 22 3 1 5 2 1 4 7

Missing of ventral root C Th LS – – 4 – – 7 – – 2

3 31 0

0

Missing of both ventral and dorsal roots C T LS – – – – – 3 – – –

13 0

0 3

Extradural missing nerve root C T LS – – – – – 3 – – – – – 3

Aberrant root C T LS 1 – – – – – – – – 1 – –

Prefix. prefixed, Postfix. postfixed, C cervical, T thoracic, LS lumbosacral Table 9.3  Intraspinal extradural variations of nerve roots Atypical spacing of Plexus type Number roots C T LS Normotype 30 1 2 2 Prefix. type 9 1 – – Postfix. type 4 1 – 2 Total 43 3 2 4

Two roots leading to one neuroforamen C T LS – 2 1 – – – 1 – – 1 2 1

Extradural rami communicantes C T LS 4 1 1 – – 1 1 1 – 5 2 2

Prefix. prefixed, Postfix. postfixed, C cervical, T thoracic, LS lumbosacral

70

9  Our Observations and Results C2 C3 C4 C5 C6 C7 C8 T1 T2 T3 T4

sulcus medianus anterior

C6 C7

T5

ventral view

T6 T7 T8 T9 T10 T11 T12 L1 L2 L3 L4

L5

S1

S2

right

S5 Co Ft

S4

S3

left

Fig. 9.2  Ventral view, intradural communicating branch between the ventral roots C6 and C7. Complex formation of the roots of the lumbosacral plexus. Missing root L2 dx. Communicating branch between the dorsal roots S3 dx and S3 sin and communicating branch between the dorsal roots S1 and S2 sin and S1–S3 sin. Roots L4 and L5 thicker than roots S2 and S3. Missing anterior roots S3, S4, and S5

9  Our Observations and Results

71

T6 T7

sulcus medianus anterior

T8 T9 T10 T11 T12 L1

L3

L4

ventral view

L2

L5

S1

S2 S4

S3

S5 Co right

Ft

left

Fig. 9.3  Lumbosacral plexus, ventral view. Complex formation of the roots of the lumbosacral plexus. Missing root L2 dx. Communicating branch between the dorsal roots S3 dx and S3 sin and communicating branch between the dorsal roots S1 and S2 sin and S1–S3 sin. Roots L4 and L5 thicker than roots S2 and S3. Missing anterior roots S3, S4, and S5

The communicating branches were mostly concentrated in the lumbosacral regions (in all studied cadavers), followed by the cervical regions (28 times, 65.1%), and rarely in the thoracic region (4 times, 9.3%). The communicating branches between the dorsal roots prevailed in all cases. The presence of nervous tissue was histologically proved in all intradural communicating branches (Fig. 9.8).

72 Fig. 9.4  Prefixed type and asymmetry of roots, dorsal view. The root L4 and L5 thicker than the root S1

9  Our Observations and Results left

C2 C3 C4 C5 C6 C7 C8 T1

right

T2 T3 T4 T5 T6 T7 T8 T9 T10 T11 T12 L1 L2 L3 L4 L5 S1 S2 S3 S4

They occurred more frequently in variations of the formation of the plexus. In the prefixed type, we observed the absence of ventral roots S3, S4, and S5 and in three cases the absence of the dorsal root. In one case, the common spacing of the roots L1 and L2 on the left side was observed (Fig. 9.9). In one case we observed a double spacing of roots T1, T9, T11, T12, and L2 and in one case concurrently the spacing of two roots C8 and T1 on both sides. The ventral root L4 was thicker or of the same thickness as the ventral roots L5, S1, and S2. The thickness of the anterior branch of the root L3 was equal to the anterior branches of the roots L5 and S1. Communicating branch above 1–2 roots occurred in one case (Fig. 9.10). In one case, we observed communicating branches between the roots L2 and L3 bilaterally, accompanied by an anomaly of formation of the root L1.

9  Our Observations and Results

73

C2 C3 C4 C5 C6 C7 C8 T1 T2 T3

C4 C5

vent r al v i ew

T4 T5 T6 T7 T8 T9 T10 T11 T12 L1 L2 L3 L4

L5

S1

S2

right

S5 S4 Co Ft

S3

left

Fig. 9.5  Postfixed type, ventral view. The sleeve of roots C4–C5 sin, asymmetry of roots. Roots L3 and L4 were thinner and sacral roots S3 and S4 clearer. The assimilation of segments in the region of spacing of sacral roots. Close and distal communicating branches

74

9  Our Observations and Results T4 T5 T6 T7 T8 T9 T10

L1

Dorsal view

T11 T12

L2

L3

L4

L5

S1

S2 left

S3 S4

S5 Co Ft

right

Fig. 9.6  Dorsal view, asymmetry of roots. The roots L3 and L4 were thinner and sacral roots S3 and S4 clearer. The assimilation of segments in the region of spacing of sacral roots. Close and distal communicating branches

In one case we observed cross-communicating branch between dorsal roots S3 of the right side and S3 of the left side. The asymmetry of roots was more pronounced in the lumbosacral plexus (31 cases, 72.09%) (Fig. 9.11), particularly at the level of spacing of roots L4–S3, maximum at the level of S1–S2. Their atypical spacing; multiple communicating branches

9  Our Observations and Results Fig. 9.7  Postfixed type, dorsal view. Cervical enlargement—longer, flatter up to T2–T3, root T2 thicker

75

C2 C3 C4 C5 C6 C7 C8 T1 T2 T3 T4 T5

T6 T7 T8 T9

between dorsal sacral roots, at a short as well as a longer distance from the spinal cord (Figs. 9.12, 9.13, and 9.14); or the absence of the ventral root occurred in 13 cases (30.2%); the absence of ventral and dorsal roots occurred in 3 cases (7%); and communicating branches between the ventral and dorsal roots were observed in 10 cases (23.3%). Communicating branches only between ventral roots were present in 12 cases (27.9%), out of which there were 3 cases in the prefixed type. In eight cases (18.6%), the communicating branches were present between sacral and lumbar roots. In the cervical region, communicating branches between the dorsal roots prevailed (Fig. 9.15). Extradural anatomical variations occurred in 26 cases (60.5%). They were more frequent on the left side (in 13 cases, 30.2%), bilateral in 4 cases (9.3%). The asymmetry of roots was observed, too. It was more pronounced in the lumbosacral plexus, particularly at the level of the spacing of the roots L4–S3, maximum

76

9  Our Observations and Results

Fig. 9.8  Longitudinal section of the nerve with the perineurium, no inflammation, fibrosis, 200 × H&E

at the level of S1–S3 (Fig. 9.16). In 9 cases (20.9%), the atypical spacing, including four in the lumbosacral region, was observed. After an extradural course of different length, the nerve roots remained close to each other and in 4 cases (9.3%) left the spinal canal through one neuroforamen (Figs. 9.17 and 9.18): two cases of two roots in the thoracic region in one neuroforamen and one case of two roots in one neuroforamen in the cervical and lumbosacral regions. In two cases (4.65%), the absence of nerve roots (S3), and in one case the root (L2), on the right side occurred and in one case an aberrant root between roots of C2–C3 (Fig. 9.19). In nine cases (20.9%), extradural communicating branches between the nerve roots were observed (Figs. 9.20 and 9.21). Two adjacent nerve roots were connected by a communicating branch shortly after their exit from the dura. In one case, we observed right-left extradural cross-anastomosis in the lumbosacral area (Fig. 9.22). Multiple extradural communicating branches were observed in six cases (13.95%), including the simultaneous occurrence of multiple intradural and extradural ones in five cases (11.6%): in the cervical region in three cases (Figs. 9.23, 9.24, and 9.25) and in the lumbosacral region in two cases (Fig. 7.2). Communicating branches were mostly—in six cases—unilateral. The histological examination confirmed the presence of neural tissue inside them (Figs. 9.26 and 9.27). In the postfixed type, the roots L3 and L4 were thinner and sacral roots S3 and S4 more pronounced. Variations were observed at sacral levels from 0% [1] to 20–30% [2, 3]. We observed intradural communicating branches in all lumbosacral plexuses. Their number increased, especially among sacral roots.

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77

left

C3

right

C2

C4

C3 C4

C5 C6 C7

L1

L2 L1 L2

L3 L4 L5 S1

S1 S2-3

S4

S2-3 S4 S5

Fig. 9.9  Spacing of the roots L1 and L2 sin. With two spinal ganglia from one segment, dorsal view

In the cervical region, intradural communicating branches were less frequent—28 cadavers (65.1%). And in the thoracic region, they occurred rarely—four times (9.3%). Our results were evaluated in relation to the type of the plexus. Prefixation of the brachial plexus was more common than postfixation. Prefixation of the brachial plexus was reported in 28% of cases, while the postfixation was observed in 5% [4]. We found differences in 9 specimens (20.9%) that were prefixed and in 4 specimens (9.3%) that were postfixed. Intradural variations prevailed in their atypical formation in the lumbosacral region. Our findings have indicated that the location of variations throughout the whole segment of the spinal cord differs, as well as the form of variations. In some cases, they are few and they are located at a short distance from the spinal cord. In other cases, communicating branches are multiple; they flow further away from the spinal cord.

78

9  Our Observations and Results

right

left

T9 T10

L3 L4

sulcus medianus anterior

T11 T12

L5

L1

S1

L2 L3 L4 L5 S1

S2

S3

S2

S4 S5 S5 S4

S3

Fig. 9.10  Lumbosacral plexus, ventral view. Asymmetry of roots, anastomosis from ventral root L4 to the ventral root S1 l. sin. Multiple rami communicantes between the sacral roots S1, S2, and S3 sin. Roots S2 and S3 exit from the same segment, creating numerous communicating branches on left side

Interneural interconnections may cloud clinical interpretation [5–7]. Some patients with hernias of intervertebral discs do not have typical symptomatology characteristic for this type of the disease. In disc operations, sometimes, anatomical variations of nerve roots are found. This results in studying different types of variations by the examination of cervical, thoracic, lumbar, and sacral nerve roots in cadavers. The aetiology of these variations has to be elucidated. The most likely explanation of variations is that they result from defective migration of the nerve roots during the first 4  weeks of embryonic development [8, 9]. Embryologic evidence can account for the frequent occurrence of intradural anomalies. The presence of an unbroken ridge of neural crest tissue travelling along the length of the spinal cord may provide the means for neighbouring dorsal roots to intercommunicate during the development [4, 8, 9]. In the 4-mm embryo, the spinal ganglia develop processes, which are directed toward the spinal cord to become the dorsal roots. This period of dorsal root expansion and fusion with the spinal cord lasts up to the 10-mm stage and may depict the route by which connections between adjacent segments can be formed.

9  Our Observations and Results

79 C2 C3 C4 C5 C6 C7

left

right

C8 T1 T2 T3

L2

L1

T8 T9 T10 T12 T11

dorsal view

T4 T5 T6 T7

L3 L4

L5

S1

S2

S3 S4 S5 Co Ft

Fig. 9.11  Prefixed type, lumbosacral plexus, dorsal view. Asymmetry of roots, roots L4 and L5 thicker than S2 and S3. Missing anterior roots S3, S4, and S5

Moreover, the dorsal roots are much slower to form than their ventral counterparts and do not begin to separate until approximately the 30th day of the embryonic development [10]. This may be a reason for the occurrence of much fewer interconnections between the ventral roots. It would, to some extent, explain the fact that migrations are usually unilateral.

80

9  Our Observations and Results

right

C2 C3 C4 C5 C6 C7 C8 T1 T2 T3

left

T12

T4 T5 T6

L3 L4

sulcus medianus posterior

T7

L5

L2

T8 T9 T10 T11 T12 L1

L3 L4 L5

S1

S1 S2

S3 S2 S3 S4 S5Co Ft

Fig. 9.12  Multiple close and distant communicating branches between the roots of the lumbosacral plexus. Asymmetry of roots and the level of their spacing, assimilation of sacral segments; dorsal view

Most papers refer to extradural anomalies of lumbosacral nerve roots [11–18], what resulted in analysing and comparing mainly this part of our observations. Symptoms of radiculopathy may manifest by the extradural variations of lumbosacral nerve roots even in the cases of the absence of pressure on nerve roots [11, 14, 19, 20]. Some papers are based on surgical findings [21]; others are based on anatomical studies [14, 15]. Their incidence ranges from 1.3% found during the operation [11] to 26.7% detected by imaging methods before surgery [14, 15, 17, 22] and from 8.5% to 30% during the study of cadavers [11, 19]. They occur most frequently unilaterally at the level of L5–S1 [14, 23–26] and can be the cause of failure of intervertebral disc operations [25]. Atypical spacing of the two nerve roots is most frequently observed in the lumbosacral region [14, 26]. The occurrence of such disorders was observed in 30% of cadavers [15, 19, 21, 23, 25, 27].

9  Our Observations and Results

81 T11 T12

sulcus medianus anterior

L1

L2 L3 L4

L5

S1

S2

right

S4

S3

left

L5 S4 S5

S1 S3

S2

Fig. 9.13  Lumbosacral plexus, ventral view. Remote communicating branches of the sacral plexus, pronounced on the left side

We observed extradural variations in 26 cases (60.5%) and 10 cases (23.3%) of the lumbosacral plexus, usually with a dominant left-side prevalence. Atypical spacing of the two nerve roots occurred in our study in four cases (9.3%). In two cases, it was at the level of L5–S1, which is less frequent than in other reports [11, 14, 15, 18, 21, 25]. In two cases, there was the extradural absence of a nerve root at the S3 level on the right side. Extradural communicating branches between lumbosacral nerve roots were described in some studies, too [12, 14, 15, 25]. They reported the extradural communicating branches ranging from 1% to 25% of cases. In our study, it was in two cases (4.6%). Comparing our anatomical findings with previous results of other authors [20, 25, 27, 28], it appears that a percentage rate was lower and the types of extradural variations partially differ. We did not observe atypical spacing of nerve roots so frequently as (commonly) reported in other studies [11, 15, 28].

82

9  Our Observations and Results right

left

C2 C3 C4 C5 C6 C7 C8 T1 T2 T3 T4 T5 T6

C5 C6 C7 C8

sulcus medianus anterior

T7 T8

L1

T9 L2

T10 T11 T12

L5

L1 L2 L3 L4 L5 L5

S1

S1 S2

S3

S4 S5

Fig. 9.14  Lumbosacral communicating branches, prefixed type, dorsal view

This explains the importance of recognizing variations of nerve roots of different types, which may increase the number of successful operations [28, 29]. Variations of nerve roots can cause symptoms at more than one level due to the pressure, e.g. caused by the herniated disc. The pressure placed on an abnormally situated nerve root may give incorrect information about the level of hernia of the disc. Variations are the major cause of failure of surgical therapy and are particularly sensitive to the retraction of nerve roots. Discectomy is, therefore, more complicated. Nerve roots cannot be mobilized safely, and the possibility of their damaging increases [12, 13, 23]. Variations of roots occupy more space in the spinal canal, and so even a small bulging of an intervertebral disc may be the cause of symptoms. Variations themselves can cause pain.

9  Our Observations and Results Fig. 9.15  Dorsal view, communicating branch between the dorsal roots C2–C3 sin

83 left

right C2

C3

C5

C6

dorsal view

C4

C7

C8

The spinal cord moves during normal flexion and extension. Therefore, stronger traction forces may be produced with variations in nerve roots, as well as with normal movements of the spinal column [30]. Intradural and extradural nerve roots can be damaged by stretching [7, 31]. A stretch-induced nerve root injury may be related to changes in the length of the spinal canal and the length of nerve roots. The perineurium and endoneurium have considerable mechanical strength and protect neural tissues against mechanical forces. However, intrathecal nerve roots do not have such a protective sheath [7, 32]. Excessive flexion of the trunk during various surgical procedures may be one of the risk factors for injury of the tethered roots in the presence of intrathecal pathologies [6]. Therefore, intradural nerve roots are vulnerable to mechanical stretch, including operative manoeuvres and trauma. Interneural interconnections may cause symptoms at more than one level and may give an incorrect indication of the disc herniation level. Therefore, the results of decompression may be unsatisfactory [7]. The preoperative diagnosis of variations of nerve roots is difficult. Lack of preoperative vigilance can lead to iatrogenic damage to nerve roots. We believe that data obtained from anatomical dissection will be helpful to many surgeons. Our study is affected by some factors such as a strong regional focus and a small number of cadavers. This limitation affects the interpretation of our data quality and the ability to generalize our findings.

84 Fig. 9.16  Asymmetry of roots, dorsal view. Close spacing of the roots C2–C3 sin and roots S2–S3 sin

9  Our Observations and Results left

C2 C3 C4 C5 C6 C7 C8 T1 T2

right

T3 T4 T5 T6 T7 T8 T9 T10 T11 T12 L1 L2 L3 L4 L5 S1 S2 S3 S4 Co S5 Ft

We detected intraspinal intradural and extradural neuroanatomical variations of nerve roots and their interrelationships through the spinal canal with their potential impact on the clinical picture. Anatomical dissections revealed a higher incidence of intraspinal intradural variations mainly among sacral roots. Reliance of their incidence on the type of plexus was observed. These data may help to understand nerve root injuries according to various pathologies, such as disc herniation, space-occupying lesions, and trauma. We believe that the data obtained will be helpful for spinal surgeons in improving a success rate of spinal operations. In our works, we have repeatedly pointed to the importance of individuality in the analysis of the course and results of treatment of the peripheral nerve injuries.

9  Our Observations and Results Fig. 9.17  Atypical spacing of the root C5 dx. Dorsal view of the roots C6–C7 dx and C7–C8 sin is detected to one neuroforamen

85 left

right C2

C3 C4

C5

C6 C7

C8

T1

T2

dorsal view

Our attention was paid to the differences in topography. Not only our experience but also experience of other authors suggested instability of their formation. “Anomalies” and “variations” have been reported quite often, but sometimes we do not dare to say which of them are genuine anomalies and which are variations of the roots. In intraspinal changes, we more frequently talk about variations. Even though the obtained findings largely reflect the variability of the peripheral nervous system, they do not exhaust all the issues and demands of the practice. Generalization of acquired knowledge has allowed us to refine certain patterns of a macroscopic structure and topography of the peripheral nervous system. Clinical observations show the importance of awareness of anomalies and variability, without knowledge of which it is difficult to imagine the whole spectrum of clinical responses and their differences. We think that it is necessary to know not only one, so-called “standard” of the classics, but also show what life brings in the clinic every day and on which the

86

9  Our Observations and Results

Fig. 9.18  Two closely located roots directing into one neuroforamen, right (dorsal view)

whole varying pathology depends. Obtained observations may explain the difference between the clinical picture and generally accepted anatomical standards. A clinical picture not corresponding with the accepted “standards” naturally led some authors to a possibility of collateral innervations, communicating branches between the peripheral nerve roots and peripheral nerves. They assumed differences in the structure of nerves—increasing the number of the motor fibres to the detriment of the sensitive ones and vice versa. Clinical observations have shown extremely inconstant regions of specific nerve distributions. Surgeons could not be satisfied with the existing anatomical knowledge, and they were forced to seek explanations of their observations. Going back to the anatomical side of the question, which is probably crucial in this issue, the stereotype of statements of classic authors of monographs or complete

9  Our Observations and Results

87 C2 C3 C4 C5 C6 C7 C8 T1 T2 T3 T4

dorsal view

T5 T6 T7 T8 T9 T10 T11 T12 L1 L2 L3 L4 L5 S1

left

S3 S5 S4 Co Ft

S2 right

Fig. 9.19  Dorsal view, asymmetry of the roots. Aberrant root between the roots C2–C3 dx

88

9  Our Observations and Results C2 C3 C4 C5 C6 C7 C8 T1 T2 T3 T4 T5

C2 C3

C5 C6

dorsal view

T6

T12 L1

T7 T8 T9 T10 T11

L2 L3 L4 L5

S1

S2

S3 S4 left

S5 Co Ft

right

Fig. 9.20  Dorsal view, extradural communicating branch between the roots C5 and C6 dx. Intradural communicating branch between the roots C2 and C3 dx

decorrelation is surprising, particularly in comparison with works specifically dealing with the structure and formation of one nerve or innervations of the region as a whole. Confirmation of this issue is the existence of a large number of publications, as a rule, case reports, which describe “variations” of a particular nerve, usually without any complex analysis of the region. Some published works dealing with “variations” lead to the conclusion that the nervous system is in its structure extremely inconstant. We could agree with this

9  Our Observations and Results right

left C2 C3

C4

ventral view

sulcus medianus anterior

Fig. 9.21  Ventral view, extradural communicating branch between C5 and C6 dx. Intradural communicating branch between the roots C2 and C3 dx

89

C5 C6 C7 C8

L3 dorsal view

Fig. 9.22  Dorsal view, asymmetry of sacral roots, atypical spacing of the root S3 sin. Extradural communicating branch between S3 sin and S4 dx

L4

L5

S1 S2 S3

S3

S4

left

right

idea with one important objection—regardless of the apparent instability of anatomical connections, the almost complete absence of standards in the structure of the peripheral nervous system, a certain regularity can be observed. That does not consist in showing numerous variations of the individual peripheral nerves, but in the analysis of innervation areas as a whole, in the detection of the relationships

90 Fig. 9.23 Intradural communicating branch between the roots C5 and C6 dx. Extradural communicating branches between the roots C6–C7–C8 dx

9  Our Observations and Results

C3 C4 C5 dorsal view

C6 C7

C8 T1

left

right

left C2 C3

C4

C5

C6

C5

dorsal view

Fig. 9.24  Dorsal view, intradural communicating branch between the roots C2 and C3 dx. Extradural communicating branches between the roots C5 and C6 dx

right

C6

C7

among all nerve roots, which are in the particular stage involved in the innervation of the given area. Therefore, finding and reviewing all the nerves in any area as a whole, as well as the complex of nerves, open up wide possibilities to solve several important issues. The essential questions are connections between individual nerve roots, replacing one nerve by another one and shifting and overlapping of their territories.

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91

Fig. 9.25  Ventral view, intradural communicating branch between C3 and C4 sin. Extradural communicating branches between the roots C4–C5 dx and C6–C7–C8 dx

C2 C3 C4 C5

ventral view

C6 C7 C8 T1 T2 T3 T4 right

Fig. 9.26  Longitudinal section of the nerve, no inflammation, fibrosis, 200 × H&E

left

92

9  Our Observations and Results

Fig. 9.27  A nerve marked in the middle, around fibrosis, 200 × H&E

In the cervical and the lumbar segment of the spinal cord in particular, from which the nerves of the limbs originate, possible connections are more frequent between the roots, as those segments pass through the most significant changes. It is known that in the plexus region, the connections between individual nerves are most pronounced and some segments involved in forming plexuses are not stable. This is a result of complex transformation of the peripheral nervous system. Not only the number but also the level of segments of which the limbs and the nerves that innervate them are formed is important. The process of the limbs moving accompanied by “assimilation” of new segments is of great importance in the formation of plexuses. Extreme types of forming the brachial and lumbosacral plexuses—the prefixed and postfixed types—reveal differences at the site of formation of the limbs but also reflect peculiarities of this segmental origin. If some segments that are involved in forming the plexus are larger, commissures among peripheral nerves are observed in a higher number of cases, whereas the course of axons in these cases is particularly important. Developing (comparative) anatomical data indicate that median nerve (n. medianus), ulnar nerve (n. ulnaris), and musculocutaneous nerve (n. musculocutaneous) form one developmental unit. It is, therefore, natural that between these nerves there are connections depending, to a greater or lesser extent, on the degree of differentiation. In fact, in anthropoid monkeys, we always observe connections between median and ulnar nerves (n. medianus et n. ulnaris) in the proximal third of the forearm. For continuity and relations of these mentioned nerves, we can assume that one of the basic symptoms of delayed differentiation of the nerves of the upper limb is the presence of numerous commissures between the nerves mentioned above.

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93

Replacing one nerve by another one and overlapping of territories on the periphery are possible because of the common origin. Different numbers of segments are involved in the creation of the lumbosacral plexus in various representatives of vertebrates. In terms of localization of connections between the underlying nerves, we are interested in the source of their formation. The femoral (n. femoralis) and obturator nerves (n. obturatorius) are formed from a single trunk. The branches of the nerve extending in a different direction have a common origin. Likewise, other nerves of the lower extremity have much in common (tibial nerve and fibular nerves). The analysis of anatomical differences in terms of development-anatomical findings leads to the conclusion that the connections between the peripheral nerves, the transition of axons from one perineural sleeve to the other, and the formation of “plexuses” on the periphery were observed between genetically related nerves. In these nerves, the replacement of one nerve by another or connection of two nerves into one common trunk is possible. Comparative anatomical findings are also confirmed in embryology. Anatomical differences indicate that segmentation in the construction of various portions of the human body is also maintained. Segmentation is best preserved in the thoracic region. In other regions, segmentation is less pronounced. It is especially difficult in the head region that corresponds to the level of formation of the limbs. In the regions of the peripheral nervous system corresponding to the head and limbs—divisions formed of a large number of segments—the creation of complex connections is expected. It is known that each myotome or dermatome receives the bundles of nerve fibres from the corresponding segment and two adjacent segments. Therefore, every myotome and dermatome (Fig. 9.28) is connected with three neurotomes. This causes the formation of connections between individual nerve plexuses. Considering that the formation of the head and limbs involves a great number of segments, due to which we can expect great complexity in the course of axons to the end territories, therefore, in divisions with clear segmentation (thoracic division), the pathway of axons from the neurotome to the corresponding dermatome leads almost directly (Fig. 9.29)—there are no substantial shifts of myotomes and dermatomes. In this segment, the overlapping zones between the individual intercostal nerves are less pronounced than in other regions. A completely different picture is seen on the head and limbs. Here, due to difficult conversion of metameres and instability of levels of the limbs, individual districts of the skin, and particularly, muscles, are formed from two or three segments. However, in some segments—the face, hand—fist, foot, perianogenital region— a combination of three or more segments can be observed in a relatively small segment. The result of such multisegmentation is that individual portions of the skin and muscles receive axons from several neurotomes. Therefore, the pathways of axons to the end territories in the nerves of the head, limbs, and perianogenital region have great complexity. Connections observed in the region of plexuses and between the nerves of limbs indicate the complexity of transition of axons from the constitution of one nerve to the constitution of the other that results in the formation of connections

94

9  Our Observations and Results Neurotome

Dermatome

Fig. 9.28  Each myotome or dermatome receives nerve fibres from 3 neurotomes Thoracic segments

Inter

cos

tal

ner

ves

Territory innervations

Fig. 9.29  Combination of neurotomes in the thoracic region (intercostal nerves). The pathway of axons from the neurotome to the corresponding dermatome leads almost directly

9  Our Observations and Results

95

“arcs and circles” between the nerves of the extremities. The presence of connections suggests that each neurotome has its myotome and dermatome, but because of their complicated formation, the pathways of axons to the end innervation regions change. Therefore, on the periphery, we can observe that in one case only one nerve supplies a particular region and in the other part two and sometimes three nerves are involved in the innervations. In these cases, we can observe overlapping zones on the periphery. Obviously, in such cases, the pathways of axons to the end territories are unstable and differ in each particular case. Nevertheless, despite the great variability in the course of nerve fibres and comparing anatomical data, we can observe a certain regularity. Connections are generally observed among relative nerves, which are determined not only by a common origin of sources from which the individual nerves were formed during the phylogenetic development but also by their segmental togetherness. If groups of axons form two anatomically different nerves arising from the same spinal cord segment or from neighbouring ones, the pathways of their axons to the end territories are just as likely in the constitution of one or the other nerve. The transition of axons from the trunk of one nerve to the trunk of the other nerve on the periphery is possible. Therefore, the connections between nerves of the common origin will be more frequently observed on the periphery within the common segment. Figure 9.30 presents a case where the axons of several segments of the spinal cord lead to the innervation region in the constitution of one nerve. The course of the axons, in this case, is not complicated. A different situation is presented in Fig. 9.31, Fig. 9.30  A case where the axons of several segments of the spinal cord lead to the innervation region in the constitution of one nervethe course of axons is not complicated

Segments

Nerves

Territory innervations

96

9  Our Observations and Results

when the axons from segments of the spinal cord can expand to the corresponding regions of innervation on the periphery in the constitution of two nerves. In such cases, the course of the axons is complicated; connections between nerves, transitions of the axons from one nerve to the other, and the overlapping zones are inevitable. A common segmentary origin of the nerves determines a possibility of the replacement of one nerve by another one, extensions of the innervation region of one nerve over the other, and even mutual replacement of the nerves. The axons in one case can achieve their innervation regions in the constitution of one or the other nerve or in the constitution of both of them (Figs. 9.32 and 9.33). This implies that the pathways of axons, though unstable, are determined by a segmentary origin of the nerves. Thus, it is inevitable to examine not only one particular nerve but also the innervation of the region as a whole. The obtained data will bring us closer to solving the issues—in the constitution of which nerves the axons can travel to the region, as the complex arrangement of nerves involved in innervation of the region will be known. Such an approach helps us to identify important sites of anatomical peculiarities of the peripheral nervous system. Observing only an individual nerve, not only a general idea of innervation of the organ or region is lost, but also the analysis of the obtained results is more difficult. Segments

Nerves

Territory innervations

Fig. 9.31 The axons from the spinal cord segments can expand to the corresponding regions of innervations at the periphery in the constitution of two nerves- the courses of axons are complicated

n. musculocutaneus

C6

n. medianus

Outskirts

C7

n. ulnaris

Fig. 9.32  Pathways of axons to the end territories of innervations by nerves of the upper limb

C5

Segments C8

n. radialis

n. axillaris

Th1

9  Our Observations and Results 97

L2

n. femoralis

L3

L4

n. obturatorius

Outskirts

L5

Segments S1

Fig. 9.33  Pathways of axons to the end territories of innervations by nerves of the lower limb

n. cutaneus femoris lat.

L1

n. peroneus communis

S2

S3

n. tibialis

S4

S5

98 9  Our Observations and Results

9  Our Observations and Results

99

Based on a comprehensive approach, communicating branches between individual nerves and intraneural architecture become understandable. We distinguish three basic types of communicating branches: I. Intraspinal intersegmental communicating branches. II. Communicating branches in the region of plexuses. III. Communicating branches between individual nerves and within the nerves. The first group includes intraspinal intersegmental connections between the roots. Our findings indicate that the localization of these communicating branches in the whole segment of the spinal cord is different as well as their form and number. These connections represent the transition of the axons from one root to the other to make the connection between segments on the periphery (intersegmental connections). This group includes communicating branches occurring even within the borders of one root (Fig. 9.34). Fig. 9.34 Communicating branches between fascicles of the sensitive nerve visible after removing the epineurium—cells forming spinocerebellar ganglion (1) are scattered in the course of the individual fascicles (2) extending to the periphery 1

2

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Communicating branches of the second group are determined by the difference of plexuses and formation of the basic nerves of the extremities, as well as communicating branches of the third group. Their localization is determined by the differences in innervation of individual regions (skin, muscles, bones, joints) allowing us to talk about the complex of nerves of each region.

References 1. Solmaz B, Tatarli N, Ceylan D, Keleş E, Çavdar S. Intradural communications between dorsal rootlets of spinal nerves: their clinical significance. Acta Neurochir. 2015;157:1069–76. 2. Kapeller K, Pospíšilová V.  Embryologický atlas. Osveta: Martin; 1996, 119 p. isbn:80-217-0549-3. 3. Neidlinger-Wilke C, Wilke HJ. The biology of intervertebral disc degeneration. In: Szpalski M, Gunzburg R, Rydevik B, Le Huec JC, Mayer H, editors. Surgery for low back pain. Berlin, Heidelberg: Springer; 2010. p. 3–10. isbn:978-3-642-04547-9. 4. Tubbs RS, El-Zammar D, Loukas M, Cömert A, Cohen-Gadol AA. Intradural cervical root adjacent interconnections in the normal, prefixed, and postfixed brachial plexus. J Neurosurg Spine. 2009;11:413–6. 5. Arslan M, Cömert A, Açar Hİ, Ozdemir M, Elhan A, Tekdemir I, Tubbs RS, Uğur HÇ. Nerve root to lumbar disc relationships at the intervertebral foramen from a surgical viewpoint: an anatomical study. Clin Anat. 2012;25:218–23. 6. Arslan M, Cömert A, Açar Hİ, Özdemir M, Elhan A, Tekdemir İ, Tubbs RS, Attar A, Uğur HÇ. Lumbosacral intrathecal nerve roots: an anatomical study. Acta Neurochir. 2011;153:1435–42. 7. Kitab SA, Miele VJ, Lavelle WF, Benzel EC. Pathoanatomic basis for stretch-induced lumbar nerve root injury with a review of the literature. Neurosurgery. 2009;65:161–7; discussion 167–168. 8. Marieb EN, Mallat J.  Základy embryologie. Kapitola 3. In: Marieb EN, Mallat J, editors. Anatomie lidského těla. Brno: Computer Press a.s; 2005. p. 62–7. isbn:80-251-0066-9. 9. O'rahilly R, Müller F, Meyer DB. The human vertebral column at the end of the embryonic periods proper. 4. The sacrococcygeal region. J Anat. 1990;168:95–111. 10. Marzo JM, Simmons EH, Kallen F. Intradural connections between adjacent cervical spinal roots. Spine. 1987;12(10):964–8. 11. Burke SM, Safain MG, Kryzanski J, Riesenburger RI. Nerve root anomalies: implications for transforaminal lumbar interbody fusion surgery and a review of the Neidre and Macnab classification system. Neurosurg Focus. 2013;35(2):E9. 12. Chotigavanich C, Sawangnatra S.  Anomalies of the lumosacral nerve roots. An anatomic investigation. Clin Orhop Relat Res. 1992;278:46–50. 13. Haijiao W, Koti M, Smith FW, Wardlaw D. Diagnosis of lumbosacral nerve roots anomalies by magnetic resonance imaging. J Spinal Disord. 2001;14:143–9. 14. Kadish LJ, Simmons EH. Anomalies of the lumbosacral nerve roots. An anatomical investigation and myelographic study. J Bone Joint Surg (Br). 1984;66(3):411–6. 15. Postacchini F, Urso S, Ferro L.  Lumbosacral nerve-root anomalies. J Bone Joint Surg Am. 1982;64(5):721–9. 16. Rask MR. Anomalous lumbosacral nerve roots associated with spondylolisthesis. Surg Neurol. 1977;8(2):139–40. 17. Stambough JL, Balderston RA, Booth RE, Rothman RH.  Surgical management of sciatica involving anomalous lumbar nerve roots. J Spinal Disord. 1988;1(2):111–4; discussion 114–115 18. Yilmaz T, Turan Y, Gulsen I, Dalbayrak S.  Co-occurrence of lumbar spondylolysis and lumbar disc herniation with lumbosacral nerve root anomaly. J Cardiovertebral Jun Spine. 2014;5:99–101.

References

101

19. Bedeschi P, Bonola A. Anomalie di origine, di decorso di lungehezza e di diametro delle radici lombari e loro importanza nella patologia dell'ernia del disco. Reumatismo. 1956;8(5):266–80. 20. Boden SD, Davis DO, Dina TS, Patronas NJ, Wiesel SW. Abnormal magnetic-resonance scans of the lumbar spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg Am. 1990;72(3):403–8. 21. Goffin J, Plets C. Association of conjoined and anastomosed nerve roots in the lumbar region. A case report. Clin Neurol Neurosurg. 1987;89(2):117–20. 22. Kyoshima K, Nishiura I, Koyama T. Conjoined lumbosacral nerve roots—diagnosis by metrizamide myelography and metrizamide CT. No Shinkei Geka. 1986;14(7):865–71. Article in Japanese 23. Ethelberg S, Riishede J. Malformation of lumbar spinal roots and sheaths in the causation of low backache and sciatica. J Bone Joint Surg (Br). 1952;34-B(3):442–6. 24. Chin CH, Chew KC. Lumbosacral nerve root avulsion. Injury. 1997;28:674–8. 25. Neidre A, Macnab I. Anomalies of the lumbosacral nerve roots. Review of 16 cases and classification. Spine. 1983;8(3):294–9. 26. Zagnosi C. Reperto di un tipo non conosciuto di anastomosi nervosa delle radici spinali. Atti Soc Med Chir (Padova). 1949;27:48–52. 27. Scarf FF, Dalman DE, Toleikis JR, Bunch WM. Dermatomal evoked potentials in the diagnosis of lumbar root entrapment. Sur Forum. 1981;32:489–91. 28. Kikuchi S, Hasue M, Nishiyama K, Ito T. Anatomic and clinical studies of radicular symptoms. Spine. 1984;9:23–30. 29. Keegan JJ. Relations of nerve roots to abnormalities of lumbar and cervical portions of the spine. Arch Surg. 1947;55(3):246–70. 30. Transfeld EE, Simons EH. Functional and pathological biomechanics of the spinal cord: an in vivo study. Presented at the International Society for the Study of the Lumbar Spine Meeting, Toronto, June 7, 1982. 31. Petraco DM, Spivak JM, Cappadona JG, Kummer FJ, Neuwirth MG. An anatomic evaluation of L5 nerve stretch in spondylolisthesis reduction. Spine. 1996;21:1133–8; discussion 1139 32. Hasue M. Pain and the nerve root. An interdisciplinary approach. Spine. 1993;18:2053–8.

Part IV Intradural Connections of Spinal Nerve Roots

Connections Between Cervical Spinal Nerve Roots

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In the cervical region, depending on the type of the plexus, there may be observed commissures between various roots. We have observed connections between the dorsal roots C3–C8, less commonly communicating branches between the ventral roots. These communicating branches in anatomy generally reflect individual differences in dermatomes and myotomes with respect to the division of the cervical segments and spinal roots. The thickness of the nerve roots and the number of axons increase from the root C4–C5 to the root of C6–C7 and then decrease to the root T1. At some distance from the cervical spinal cord, nerve roots divide into several small branches that are divided into the thinner small branches—rootlets before entering the spinal cord. This part—back entering root zone—is a special part of the nervous system, the transition zone between the central and peripheral nervous system. Connections between dorsal roots tend to be arranged differently in the number and form. In some cases (Fig. 10.1), they are the same from the right, as well as from the left side [1, 2] to form the fibres extending from a caudally placed root to a cranially placed root. In other cases (Fig. 10.2), they are multiple and different in character. For example, individual small groups of fibres extend from a caudally placed root into a cranially placed root [1–3] and vice versa. Moreover, sometimes it is possible to observe the connection of two adjacent fibres of the roots into one that enters the spinal cord individually [2, 3]. Rarely, it is possible to see the transition of fibres from one root to the other one in the form of an “arch” [1]. A large number of intradural communicating branches between the roots in the diversity of their forms are generally identical with the asymmetry of the root that manifests as in the relation of the level of entry or exit of the roots and so in the relation of the number of fibres that constitute them. Comparing the findings of Figs. 10.1 and 10.2, in Fig. 10.2 we can see more significant asymmetry sometimes at such a rate that several roots are missing.

© Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_10

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Fig. 10.1 Communicating branches between the dorsal roots in the cervical part of the spinal cord

The communicating branches in the cervical region were less frequent than in the lumbosacral region. In a supinated prefixed type, the cervical enlargement (intumescentia cervicalis) was shorter; the peak was at the level of the deflecting root C5. The roots T1 and T2 were thin. Described differences indicate that in many cases the formation of cervical, brachial and lumbosacral plexuses can occur intradurally but also extradurally. We identify the anastomoses between the accessory nerve and the posterior roots of cervical nerves below the level of the C2 segment. The bridging fibres in the most common type of anastomoses were observed to connect the posterior roots of a cervical nerve with the spinal rootlets of the accessory nerve below the level of C2, which has been rarely reported, and also to suggest the possibility that the accessory nerve may innervate the trapezius muscle through the cervical nerves.

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Fig. 10.2 Multiple communicating branches between the dorsal roots in the cervical part of the spinal cord

The roots, from which n. accessorius is formed, leave from the cervical segment of the spinal cord. The spinal portion of n. accessorius is expressed in different ways. Various anastomoses between fascicles forming the cervical portion of n. accessorius and dorsal roots of the spinal cord have been observed (Figs. 10.3). In some cases (Fig. 10.3), the cervical portion of n. accessorius is made up of bundles of fibres resulting from the segment C1–C6; in other cases, fascicles of fibres leaving only to the extent of the cervical segments C1–C3 are forming the spinal portion of n. accessorius. Plexus cervicalis, brachialis, and n. accessorius are formed from the cervical portion of the spinal cord. In the region of cervical intumescence, we have observed anastomoses between dorsal roots and asymmetry of fascicles forming roots and connections between

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Fig. 10.3  In some cases fiber fascicles from C1–C3 are forming the spinal portion of the n. accessorius

them and n. accessorius as well. The form of anastomoses varies. We have observed (Fig.  10.4) that one of the bundles (1) penetrating the spinal cord, together with bundles of the dorsal roots, is connected with n. accessorius (2). Another time (Fig. 10.5), a bundle forming the dorsal root (1) is connected via a branch (2) with the trunk of n. accessorius (3). Figure  10.6 shows a bundle (1) joining the roots C3–C4 and connected to n. accessorius (2) via the anastomosing branch.

10  Connections Between Cervical Spinal Nerve Roots Fig. 10.4  In some cases, the cervical portion of n. accessorius is made up of bundles of fibres resulting from the segment C1–C6

Fig. 10.5  A bundle forming the dorsal root (1) is connected via a branch (2) with the trunk of n. accessorius

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Fig. 10.6  A bundle (1) joining the roots C3–C4 and connected to the n. accessorius (2) through the anastomosing branch

References 1. Haninec P, Houšťava L, Stejskal L, Smrčka V.  Chirurgická léčba poranění pažní pleteně. Výsledky a přehled literatury. Rehab Fyz Lék. 1998;5(2):61–4. 2. Kapeller K, Slováková D, Janovič J, Mikulaiová M, Mráz P, Polonyi J.  Sutúra periférneho nervu. Bratisl Lek Listy. 1980;74(3):249–360. 3. Šulla JI, Lukáč I, Šulla I.  Syndroma caudae equinae discogenes. Košice: Univerzita Pavla Jozefa Šafárika v Košiciach; 2009. 231 p. isbn:978-80-7097-769-9.

Connections Between Ventral Rootlets and Dorsal Rootlets (Separately) in the Region of Lumbosacral Enlargement (Intumescentia Lumbosacralis) and Cauda Equina

11

The communicating branches between the dorsal roots of the cervical and lumbar region and extension of the spinal cord tend to be various not only in the number and form but also in relation to the topography, which is associated in the lumbosacral region with the presence of cauda equina (Figs.  11.1 and 11.2). In some cases (Fig. 11.1), connections are only a few, and they are located at a short distance from the spinal cord [1, 2]. They are the fibres extending from the root located caudally to the root located more cranially. Asymmetry of the roots is obscure. In other cases (Fig. 11.2), communicating branches are multiple; they flow further away from the spinal cord and have a complex form. Figure 11.2 shows the fibres [1–6] leaving from caudally located roots into the cranially located roots that then disunite [7, 8]; sometimes they individually penetrate into the spinal cord. From the right communicating branches, they are at a great distance from the spinal cord [9–12] and connect not only neighbouring roots, but they also pass over one root [11]. In the presence of multiple communicating branches, significant asymmetry has also been observed. Described differences show that in many cases, the lumbosacral plexus is formed intradurally. That is why it is usually difficult to identify the location or association of roots to a particular spinal cord segment. Intradural intercommunications between adjacent nerve roots have received scant attention in the literature. Moreover, the pattern of these connections among individuals harbouring normal, pre- and postfixed brachial plexuses to our knowledge has not been explored. Being among pre- and postfixed brachial and lumbosacral plexuses, intercommunications between adjacent nerve roots were more or less equally distributed between the left and right side. These are mostly concentrated in lumbosacral regions followed by the cervical region and rarely in the thoracic region. Additionally, such communications are primarily between the dorsal rootlets, with ventral root intercommunications being rarely reported. To our knowledge, no study has related such intercommunications between adjacent dorsal and ventral roots in the cervical, thoracic, and lumbosacral region in reference to a normal, prefixed, or postfixed plexus. Only few interconnections © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_11

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Fig. 11.1 Close communicating branches between the dorsal roots of the spinal cord in the region of lumbosacral enlargement and cauda equina

overjumped more than one segment, and the diameter of roots in the lumbosacral region increased from L1 to S1 because of the increasing number of rootlets and then decreased toward S5. In all, the number of dorsal rootlets was greater compared to ventral rootlets. Several interneural connections were identified. They were rarely present between the lumbar nerve roots. Moreover, intercommunications were found more frequently between sacral roots around the conus medullaris. Many authors reported that roots are arranged in pairs, whereas in our study, the dorsal roots were especially in a sacral region composed of several subgroups, and their number varied. In one study ventral roots were variably composed. The dorsal and ventral roots had more rootlets with an increasing number of these in a rostral

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Fig. 11.2 Remote communicating branches between the dorsal roots of the spinal cord in the region of lumbosacral enlargement and cauda equina

to caudal direction in the lumbar region. Anastomoses appeared to be more frequent between the dorsal sacral nerve roots at origin from the conus medullaris. Based on our dissections, at lower levels of the distal spinal cord, lumbar and sacral roots are so crowded that it is very difficult to identify the limit of the segment of origin of a single root. Moreover, also anastomoses may affect the results of the procedure. Intersegmental anastomoses between the dorsal roots were commonly observed through the whole intersegmental levels of the spinal cord, but they were relatively few between ventral roots. Intradural intersegmental connections between sensory rootlets frequently occur. Similar connections between motor rootlets also have

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been noticed, but their incidence was not reported. These connections may provide a pathway for overlap of sensory dermatomes and motor innervation of the neck and upper extremity. When a cervical nerve root is injured, small segments of an adjacent root may be equally affected, and the process may be clinically localized one segment higher or lower than it actually is. This variation can potentially lead to misinterpretation of the segmental level of the cervical spinal root pathology. Motor rootlets had connections more frequently between sacral roots. There was no symmetry in those with multiple connections. No connection extended more than one level above or below. Histology examination of these connections revealed the presence of axons in every case. Intersegmental connections of anterior and posterior roots probably contribute to the variation in the distribution of cervical nerves. Previously, the incidence of anterior intradural connections between nerve rootlets was not commented on. They may be important in spinal cord trauma and may be responsible for sparing of some motor functions below the level of insult, for example. Complete C5 quadriplegia may have some C6 motor function from other rootlets originating from the spinal cord at C5. In the sacral region, the number of rootlets decreased in the rostrocaudal direction. Intersegmental nerve anastomoses may disturb the classic dermatomal and myotomal organization of the spinal cord and roots at this level. The nerve roots were identified from distal (dural sleeve) to proximal. Interradicular gaps in between sacral nerves roots were extremely uncommon. Most commonly we found the most caudal interradicular gap between L1 and L2. Anastomoses between the dorsal branches of the lumbosacral plexus. In some cases (Fig. 11.3) between the dorsal branches of the lumbar nerves from L1 to L5, especially from the right, a large number of connections are present. The form of connections varies. In other cases (Fig. 11.4), however, between the dorsal branches of the lumbar nerves, only isolated connections are found. The ventral roots S4, S5, and coccygeal roots were inconsistently present, depending on the type of plexus. In some cases, we found a bridge between the dorsal and ventral roots. Clinically, high frequency of anastomoses in this anatomical region may translate into the loss of dermatomal organization with subsequent misleading findings or symptoms. In surgery, the presence of frequent anastomoses increases the density of the neural network around the conus medullaris and thus makes orientation as well as dissection more difficult. Intradural nerve simulation might be less successful, considering the loss of strict segmental organization due to the numerous interconnections [13, 14].

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Fig. 11.3  In some cases between the dorsal branches of the lumbar nerves only isolated connections are found

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Fig. 11.4  In other cases between the dorsal branches of the lumbar nerves from L1 to L5 (especially from the right) a large number of connections are present

References

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References 1. Borovanský L. a kol.: Soustavná anatomie člověka. 1. vyd. Praha, Státní zdravotnické nakladatelství. 1960, 469 p. 2. Chung K, Coggeshall RE. The ratio of dorsal root ganglion cells to dorsal root axons in sacral segments of the cat. J Comp Neurol. 1984;225(1):24–30. 3. Carlstedt T. Nerve fibre regeneration across the peripheral-central transitional zone. J Anat. 1997;190(Pt. 1):51–6. 4. Carlstedt T, Cullheim S, Risling M, Ulfhake B. Nerve fibre regeneration across the PNS-CNS interface at the root-spinal cord junction. Brain Res Bull. 1989;22(1):93–102. 5. Guérin P, Obeid I, Bourghli A, Masquefa T, Luc S, Gille O, Pointillart V, Vital JM. The lumbosacral plexus: anatomic considerations for minimally invasive retroperitoneal transpsoas approach. Surg Radiol Anat. 2012;34(2):151–7. 6. Marzo JM, Simmons EH, Kallen F. Intradural connections between adjacent cervical spinal roots. Spine. 1987;12(10):964–8. 7. Kapeller K, Slováková D, Janovič J, Mikulaiová M, Mráz P, Polonyi J.  Sutúra periférneho nervu. Bratisl Lek Listy. 1980;74(3):249–360. 8. Šulla JI, Lukáč I, Šulla I.  Syndroma caudae equinae discogenes. Košice: Univerzita Pavla Jozefa Šafárika v Košiciach; 2009. 231 p. isbn:978-80-7097-769-9. 9. Haninec P, Houšťava L, Stejskal L, Smrčka V.  Chirurgická léčba poranění pažní pleteně. Výsledky a přehled literatury. Rehab Fyz Lék. 1998;5(2):61–4. 10. Haninec P, Kaiser R.  Operační léčba porenění plexus brachiális. Cesk Slov Neurol N. 2011;74/107(5):619–30. 11. Šteňo J, Nádvorník P. K neurosutúre pod ťahom. Rozhl Chir. 1991;60(7):502–4. 12. Šteňová J, Kubíková E, Šteno J. Topograficko-anatomické vzťahy chrbtice, mechy a miechových nervov, význam pre klinickú prax. Neurol Pre Prax. 2009;10(4):205–8. 13. Hauck EF, Wittkowski W, Bothe HW. Intradural microanatomy of the nerve roots S1-S5 at their origin from the conus medullaris. J Neurosurg Spine. 2008;9(2):207–12. 14. Tubbs RS, El-Zammar D, Loukas M, Cömert A, Cohen-Gadol AA. Intradural cervical root adjacent interconnections in the normal, prefixed, and postfixed brachial plexus. J Neurosurg Spine. 2009;11:413–6.

Details of Relationship Between the Ventral and Dorsal Rootlets in the Region of Spinal Ganglion of the Lumbosacral Plexus

12

In the region of spinal ganglia, fibres of the ventral and dorsal roots are so tightly interwoven that it is not possible to separate the motor and sensitive part using a conventional method of dissection. In some cases (Figs. 12.1 and 12.2), both roots macroscopically merge into one trunk proximally from the spinal ganglion before being divided. In the intratruncal preparations after removing the epineurium (Fig. 12.3), complicated enlacements between the fascicles of fibres can be seen. In other cases (Fig. 12.4), the roots are connected to a single trunk and form a mixed nerve distal from the spinal ganglion, particularly in the cervical and thoracic region (Fig. 12.5). In the cases where the root connection is macroscopically carried out within the ganglion (Figs. 12.6 and 12.7) during the intratruncal preparation (Fig. 12.8), we found a very complicated enlacement of sensitive and motor fibres, where the motor fibres are passing through the mass of the ganglion. Where the roots are connected proximally from the ganglia, they often leave through one opening in the dura mater, and they have a common cover. In other cases, it is possible to observe that the connection of the roots occurs distally from the ganglion and the roots with their covers leave the spinal dural sac separately, usually in the lower cervical and upper thoracic region (Fig. 12.9). Sometimes (Fig.  12.10), connections between the motor (2) and sensitive (1) roots of the spinal cord are observed. They often are rather complex. Doubling of spinal ganglia and the increase of the number of fibres forming roots also occur. Figure  12.11 shows the formation of two separate spinal ganglia, located in the course of two separate bundles of fibres that form (in this case) the dorsal root within the ganglion. Connections between bundles through “double exchange of fibres” can also be seen. The connection of the ventral root with dorsal roots is performed distally from the ganglion, while the ventral root breaks up into several separate branches connecting the branches of the dorsal roots.

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Fig. 12.1  Details of relations between the ventral and dorsal roots in the region of spinal ganglia

Fig. 12.2  (1) dorsal root, (2) ventral root

12  Details of Relationship Between the Ventral and Dorsal Rootlets in the Region… Fig. 12.3  In the trunks after removing the epineurium the complicated enlacements between the fascicles of fibres can be seen

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Fig. 12.4  Details of relations between the ventral and dorsal roots in the region of spinal ganglia

Fig. 12.5  In some cases the roots are connected to a single trunk and form a mixed nerve distal to the spinal ganglion (particularly in the cervical and thoracis regions)

12  Details of Relationship Between the Ventral and Dorsal Rootlets in the Region… Fig. 12.6  A case with the root connection macroscopically carried out within the ganglion (vertical view)

Fig. 12.7  A case with the root connection macroscopically carried out within the ganglion (horisontal view)

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Fig. 12.8  A case with the root connection macroscopically carried out within the ganglion - by the the further intratruncal preparation we found a very complicated enlacement of sensitive and motor fibres

12  Details of Relationship Between the Ventral and Dorsal Rootlets in the Region… Fig. 12.9  Details of relations between the ventral and dorsal roots in the region of spinal ganglia

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Fig. 12.10  The connections between the motor (2) and sensitive (1) roots of the spinal cord are often complicated

12.1  Intraspinal, Intradural, and Extradural Anomalies of Communicating Branches

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Fig. 12.11  Formation of the two separate spinal ganglia, located in the course of two separate fibre bundles, that form in this case the dorsal root within the ganglia

12.1 I ntraspinal, Intradural, and Extradural Anomalies of Communicating Branches Intradural communicating branches: Figs. 12.12 and 12.13. Intradural and extradural branching: Fig. 12.14. Extradural communicating branches: Figs.  12.15, 12.16, 12.17, 12.18, 12.19, 12.20, and 12.21. Intradural communicating branches and extradural branching: Fig. 12.22.

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Fig. 12.12 Intradural communicating branches

Fig. 12.13 Intradural communicating branches

12.1  Intraspinal, Intradural, and Extradural Anomalies of Communicating Branches Fig. 12.14  Intradural and extradural branching

Fig. 12.15 Extradural communicating branch

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Fig. 12.16 Extradural communicating branch

Fig. 12.17 Extradural communicating branches

12.1  Intraspinal, Intradural, and Extradural Anomalies of Communicating Branches Fig. 12.18 Extradural communicating branches. Two adjacent nerve roots are joined with vertical anastomosis; one neuroforamen is unoccupied

Fig. 12.19 Extradural communicating branches, extradural anomalies of the nerve roots origins

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Fig. 12.20 Extradural communicating branches

Fig. 12.21 Extradural communicating branches

12.1  Intraspinal, Intradural, and Extradural Anomalies of Communicating Branches Fig. 12.22 Intradural communicating branches and extradural branching

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Part V Extradural Spinal Nerve Roots Connection

General Description

13

Among the common extradural spinal nerve roots anomalies we have observed the cranial origin of the extradural nerve root (Fig.  13.1), or rather its caudal origin (Fig. 13.2), or the combination of cranial and caudal origins of closely connected nerve roots (Fig. 13.3), or connected nerve roots (Figs. 13.4 and 13.5). As the lumbosacral region is most frequently exposed especially due to frequent intervertebral disc hernias (and their management), this region deserves a more detailed analysis. To our knowledge, no study has reported occurring interconnections between extradural nerve roots in the cervical, thoracic, and lumbosacral region in reference to a normal, prefixed, or postfixed type of brachial and lumbosacral plexuses. Most of the papers dealt with extradural anatomical variations of lumbosacral nerve roots [1–17]. Extradural lumbosacral nerve root connections are a group of congenital anatomical variations. Various types of interconnections of the lumbosacral nerve roots have been documented in the available literature. Generally speaking, these variations may consist of a bifid, conoid structure of a transverse course or a characteristic anastomized appearance. Firstly, being described as an incidental finding during autopsies or surgical procedures performed for lumbar disc herniations and often asymptomatic, lumbosacral nerve root interconnections have been more frequently described in the last years due to advances made in radiological diagnosis. These variations were assessed on the basis of operative findings, neurological examination, and autopsy studies [11, 18]. The percentage incidence of these nerve root variations shows a range comprised between 0.3% and 30%, although the last figure may be overestimated. In any case, it is probable that interconnections of the lumbosacral nerve roots are more frequent than radiological reports seem to indicate. The roots most frequently involved by the anatomy are L5 and S1, accounting for 50% of the total number, while S2 variations of other roots are rare. An abnormal anastomosis between roots may persist either as a band of nerve fibres or as a complete distal union in a common sheath [18]. The operative management of these anomalies depends on the neurological problems and the clinical conditions existing in each individual case [19]. © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_13

137

138 Fig. 13.1  Cranial origin

Fig. 13.2  Caudal origin

13  General Description

13  General Description Fig. 13.3  Cranial origin

Fig. 13.4  Caudal origin

139

140

13  General Description

Fig. 13.5  The combination of cranial and caudal origins, closely connected to the nerve roots

Asymptomatic and accidentally diagnosed cases do not require treatment. Intervertebral disc herniations, associated with root variations (with or without bony alterations), have to be treated in order to relieve neurological signs and symptoms. In these cases, an adequate exposure of the roots involved to avoid persistent compression as well as to reduce any traction may be necessary, keeping in mind that hemilaminectomy with sufficient exposure of the intervertebral foramen or the lateral recess should be performed to avoid the alterations of stability and to ensure correct mobility of the lumbosacral spine. In fact, in the presence of nerve root variations, an extensive exposure by hemilaminectomy is necessary. It allows adequate visualization and mobilization of the involved roots and aids in the definition of the conjoined roots and their origin, thus avoiding the risk of laceration and excessive traction. Because possible concomitant spinal stenosis may often be associated with a herniated disc, unroofing of the lateral recess, foraminotomy, and medial facetectomy are necessary to obtain a proper decompression and mobilization of the roots. A careful inspection of the disc space is always recommended because a small disc protrusion, which usually causes the radicular symptoms, may be overlooked when the anomalous roots cover the intervertebral space. When the abnormal configuration and fixation of the roots (clearly depicted by CT and MRI) prevents an adequate exposure of the disc space on the involved side,

13  General Description

141

the removal of the herniated disc through a contralateral laminotomy may be advisable as a correct surgical treatment for patients with variations of lumbosacral nerve roots, and associated disc herniation or spinal stenosis results in clinical remission or improvement. A relatively high incidence of unsatisfactory postoperative results may be often due to some factors, such as a previous operation, accidental opening of the dura, or iatrogenic injury to the variations of nerve roots [19]. These unusual variations may be treated in the same way as other spinal extradural pathologies as long as correct diagnosis, clinical and prognostic evaluation, and surgical planning and management have been carefully performed. Variations of the lumbosacral nerve roots have been sporadically documented in medical literature. Some failures in lumbar disc surgery may be caused by variations of the lumbosacral nerve roots of the patients. The arrangement of the lumbosacral nerve roots is anatomically normal for patients exhibiting the classical clinical manifestation of lumbar disc herniation. However, atypical clinical profiles are also encountered among patients suffering from the same conditions. These clinical abnormalities can be attributed to anomalous lumbosacral nerve roots in the patients. Related studies on this topic have reported that 0.36–14% of all patients diagnosed with lumbar nerve herniation have variations of the lumbosacral nerve root. Several reports were based on operative findings, while others were based on anatomic investigations and CT, MRI, and myelography using water-soluble contrast medium. The anastomosis of the rootlets occurred in the intraspinal canal before its emergence from the spinal foramen, the anastomosis occurred at the preganglionic level. Combined variations of intradural anastomosis and extradural division were found. The aetiology of these variations is uncertain. They probably develop while the nerve roots migrate during the embryonic life. No bony defect of the spine was associated with neural variations [8]. In patients with this anatomic variation, neurologic symptoms can result from herniation of the lumbar disc, and this may lead to inaccurate diagnosis, and incorrectly interpreted variations of lumbosacral nerve roots could be misdiagnosed as disc herniation on computed tomography. Postoperative results of such patients may also be unsatisfactory. It has been suggested that pain associated with variations of nerve roots is caused by several factors. First, the variations themselves may cause somehow the symptoms; second, because variations of roots occupy most of the space in intervertebral foramen, even a slightly bulging intervertebral disc or swelling of the nerve root may cause pain [20]. And third, traction symptoms could be created in variations of roots even with normal movement of the spine. Preoperative diagnosis of variations of lumbar nerve roots through the use of the myelogram computed tomography and magnetic resonance imaging is essential to facilitate through surgical planning and prevention of unnecessary complications for the patient. Other reports have stressed the danger of potential injury to variations of nerve roots during surgery as well as possible failure to relieve symptoms if the abnormality is not adequately addressed. Confirmation of the presence of anastomoses between different levels clearly dispels any notion of the existence of “absolute innervation”. Nerve root variations may cause symptoms at more than one level as a result of pressure by, for example, herniated intervertebral disc. Pressure on

142

13  General Description

abnormally situated nerve roots may also give an incorrect indication of the level of disc herniation. Some authors have reported cases of nerve roots variations in patients with the intervertebral disc symptoms, in whom no obvious disc pathology was found at operation, the results of decompression were poor, and only a few patients being relieved of their symptoms. Observing how mobile the spinal cord was during normal flexion and extension, this suggests that traction symptoms could be created in variations of roots even with normal movements of the spine. All surgeons operating on the spine should be aware of these variations; awareness may prevent traction injuries of the roots. Sectioning some of these anomalous roots may result in irreversible motor and sensory loss. Nerve root variations should be suspected in all cases of failed disc surgery. Numerous reports on variations of the lumbosacral nerve roots, most of them concerning a single patient or a small series of patients, have appeared in the literature. Most of the variations were incidental findings during an operation for lumbar disc syndrome. Since our knowledge of variations of lumbosacral nerve roots is based only on operating findings, it is still limited, because at operation the number of nerve roots explored is usually small. Only the root variations that have a role in the cause of the clinical syndrome are discovered. In almost all of the reported cases, the fifth lumbar and first sacral nerve roots were involved. This localization has been attributed to the fact that these are the roots that most frequently are visualized during surgery for lumbar disc disease. Most lumbosacral nerve root variations are asymptomatic and are incidental findings. If there are symptoms, they usually result from a herniated disc that is compressing one or occasionally two nerve roots. At operation, the reduced mobility or the abnormal configuration of the variations of roots, or both, may make it exceedingly difficult to explore the intervertebral space without damaging the roots, especially when a small laminotomy is performed. In the presence of nerve-root variations, therefore, wide exposure allowing adequate visualization and mobilization of the involved roots is mandatory. Careful inspection of the disc space is also essential, since a small disc protrusion may easily be overloaded when anomalous roots extensively cover the intervertebral space. When one abnormal configuration or fixation of anomalous roots prevents adequate exposure of the disc space on the involved side, removal of a herniated disc through a contralateral laminectomy may have to be considered. No study has reported current occurrence between intradural and extradural communicating branches between nerve roots in the cervical, thoracic, and lumbosacral region in reference to a normal, prefixed, or postfixed type of brachial and lumbosacral plexuses. Anatomical preparations revealed a higher incidence of current occurrence of intraspinal, intradural, and extradural communicating branches mainly by the plexus formation variations and between cervical roots. Current occurrence of extradural and intradural rami communicantes between the nerve roots was observed in nine cases (20.9%). Multiple extradural rami communicantes were observed in six cases (13.95%), including the simultaneous occurrence of multiple intradural and extradural ones in

13  General Description

143

five cases (11.6%): three of them were in the cervical region and two cases in the lumbosacral region. They occurred more frequently—five cases by the plexus formation variations. Rami communicantes were mostly—in six cases—unilateral. Interneural interconnections may cloud clinical interaction [1, 21, 22]. The aetiology of these variations is unknown. One hypothesis suggests the defect of the nerve root migrations is caused during the first 4 weeks of embryonic development [22, 23]. Symptoms of radiculopathy may manifest intraspinal variations of nerve roots even in cases of the absence of pressure on nerve roots [5, 6, 9, 24]. Some papers are based on surgical findings [23]; others are based on anatomical studies [9, 12]. Their incidence ranges from 1.3% found during the operation [6] to 2–6.7% detected by imaging methods before surgery [9, 12, 16, 25] and from 8.5% to 30% during the study of cadavers [6, 24]. They can be the cause of failure in operations of discs [11]. The current occurrence of intraspinal intradural and extradural communicating branches between nerve roots is more vulnerable to mechanical stretch, including operative manoeuvres and trauma (Figs. 13.6 and 13.7). Fig. 13.6  Joined nerve roots

144

13  General Description

Fig. 13.7  Joined nerve roots

References 1. Arslan M, Cömert A, Açar Hİ, Ozdemir M, Elhan A, Tekdemir I, Tubbs RS, Uğur HÇ. Nerve root to lumbar disc relationships at the intervertebral foramen from a surgical viewpoint: an anatomical study. Clin Anat. 2012;25(2):218–23. 2. Arslan M, Cömert A, Açar Hİ, Özdemir M, Elhan A, Tekdemir İ, Tubbs RS, Attar A, Uğur HÇ. Lumbosacral intrathecal nerve roots: an anatomical study. Acta Neurochir. 2011;153(7):1435–42. 3. Bardeen CR, Elting AW. A statistical study of the variations in the formation and position of the lumbo-sacral plexus in man. Anat Anz. 1901;19:209–19. 4. Bedeschi P, Bonola A. Anomalie di origine, di decorso di lungehezza e di diametro delle radici lombari e loro importanza nella patologia dell'ernia del disco. Reumatismo. 1956;8:266–80. 5. Boden SD, Davis DO, Dina TS, Patronas NJ, Wiesel SW. Abnormal magnetic-resonance scans of the lumbar spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg Am. 1990;72(3):403–8. 6. Burke SM, Safain MG, Kryzanski J, Riesenburger RI. Nerve root anomalies: implications for transforaminal lumbar interbody fusion surgery and a review of the Neidre and Macnab classification system. Neurosurg Focus. 2013;35(2):E9. 7. Chin CH, Chew KC. Lumbosacral nerve root avulsion. Injury. 1997;28(9-10):674–8.

References

145

8. Chotigavanich C, Sawangnatra S.  Anomalies of the lumosacral nerve roots. An anatomic investigation. Clin Orhop Relat Res. 1992;278:46–50. 9. Ethelberg S, Riishede J. Malformation of lumbar spinal roots and sheaths in the causation of low backache and sciatica. J Bone Joint Surg (Br). 1952;34(3):442–6. 10. Goffin J, Plets C. Association of conjoined and anastomosed nerve roots in the lumbar region. A case report. Clin Neurol Neurosurg. 1987;89(2):117–20. 11. Haijiao W, Koti M, Smith FW, Wardlaw D. Diagnosis of lumbosacral nerve roots anomalies by magnetic resonance imaging. J Spinal Disord. 2001;14(2):143–9. 12. Hasue M. Pain and the nerve root. An interdisciplinary approach. Spine. 1993;18(14):2053–8. 13. Kadish LJ, Simmons EH. Anomalies of the lumbosacral nerve roots. An anatomical investigation and myelographic study. J Bone Joint Surg (Br). 1984;66(3):411–6. 14. Keegan JJ. Relations of nerve roots to abnormalities of lumbar and cervical portions of the spine. Arch Surg. 1947;55(3):246–70. 15. Keon-Cohen B. Abnormal arrangement of the lower lumbar and first sacral nerves within the spinal canal. J Bone Joint Surg (Br). 1968;50(2):261–5. 16. Kikuchi S, Hasue M, Nishiyama K, Ito T. Anatomic and clinical studies of radicular symptoms. Spine. 1984;9(1):23–30. 17. Kitab SA, Miele VJ, Lavelle WF, Benzel EC. Pathoanatomic basis for stretch-induced lumbar nerve root injury with a review of the literature. Neurosurgery. 2009;65(1):161–7; discussion 167–168. 18. Cannon BW, Hunter SE, Picaza JA. Nerve-root anomalies in lumbar disc surgery. J Neurosurg. 1962;19:208–14. 19. Maiuri F, Gambardella A.  Anomalies of the lumbosacral nerve roots. Neurol Res. 1989;11(3):130–5. 20. Transfeld EE, Simmons EH. Functional and pathological biomechanics of the spinal cord: an in vivo study, Toronto: Presented at the International Society for the study of the lumbar spine meeting. 1982. 21. Kyoshima K, Nishiura I, Koyama T. Kyoshima K, Nishiura I, Koyama T. [Conjoined lumbosacral nerve roots—diagnosis by metrizamide myelography and metrizamide CT] [Article in Japanese]. No Shinkei Geka. 1986;14(7):865–71. 22. Marieb EN, Mallat J.  Základy embryologie, kapitola 3. In: Marieb EN, Mallat J, editors. Anatomie lidského těla. Brno: Computer Press a.s; 2005. p. 62–7. 23. O’rahilly R, Müller F, Meyer DB. The human vertebral column at the end of the embryonic period proper. 4. The sacrococcygeal region. J Anat. 1990;168:95–111. 24. Neidre A, Macnab I. Anomalies of the lumbosacral nerve roots. Review of 16 cases and classification. Spine. 1983;8(3):294–9. 25. Petraco DM, Spivak JM, Cappadona JG, Kummer FJ, Neuwirth MG.  An anatomic evaluation of L5 nerve stretch in spondylolisthesis reduction. Spine. 1996;21(10):1133–8; discussion 1139

Extradural Connections of the Lumbosacral Nerve Roots

14

Anomalies of lumbosacral segments in the population range between 5% and 10%. These observations point to a possible etiological relationship between spinal anomalies and nerve root variations. Although the current prevalence of spondylolysis and intervertebral disc herniation is common, variations of the nerve roots accompanying these lesions are very rare. A summary of previous studies revealed some problems with the diagnosis. Most of the work of lumbosacral nerve root variations involved one patient or a small series of patients. In almost all cases, those were incidental observations discovered during surgery. In these cases, the significance of the above-mentioned observations is limited, since during operation the examination of nerve roots is restricted. MRI may not detect anomalies and anastomosis between nerve roots. Therefore, a neurosurgeon should consider such a possibility to avoid inadvertent damage to the nerve [1]. Further studies were based on myelography, at which the contrast medium gets into the root sleeves and visualizes the roots and their variations. In all these reports, only the patients with LIS and lesions of L5 and S1 nerve roots were involved. The location may be influenced by the fact that the roots mentioned earlier are most often befallen by degenerated intervertebral discs in the lumbosacral region. In a series of 2123 patients examined by myelography, 48 (2.1%) of nerve root anomalies were found. The anomalies were generally unilateral and most frequently observed at the fifth lumbar and first sacral nerve root. Some authors (e.g. Burke et al. [2]; Kilocucni et al. [3]) indicated conflicting investigations accompanying other diagnostic methods because the lumbosacral variations may be asymptomatic and they are often discovered incidentally during surgery or PMG examination. In other cases, radiculopathy was observed at a different level or on a contralateral side to the graphic finding. In the case of an ipsilateral finding, symptoms are significant also in the cases of a small protrusion. This is probably caused by the fact that the anomalous roots are less mobile than normal and are, therefore, more susceptible to the external compression. In such cases, a wide surgical approach is necessary during operation to allow adequate visualization and mobilization of the altered roots. © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_14

147

148

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The occurrence of nerve variations was 14%, most often at the level of L5/S1 [4]. The arrangement of lumbosacral nerve roots is regular in the majority of patients presenting with typical neurological symptomatology of intervertebral disc herniation [5]. However, atypical neurological symptomatology may also appear in these patients [6]. The motor, sensitive deficits as well as hyporeflexia may or may not be present. If only one root is afflicted, symptoms and signs may be convincing. The diagnosis of radiculopathy is difficult in many cases. Symptoms and signs do not always correlate with the expected pattern of dermatomes and myotomes. Variations of the nerve roots were observed in patients with symptoms of intervertebral disc hernia, in whom a similar finding [7] was found during the operation. The result of the surgery was unsatisfactory; only a few patients were improved or asymptomatic. Two reasons have been anticipated: (1) variations can cause pain, and (2) variations of the roots occupy more space in the spinal canal, so even small bulging of an intervertebral disc may elicit clinical symptoms. Confirmation of the presence of communicating branches between the different levels points to the absence of “absolute innervations”. Spinal surgeons should take into account possible variations and prevent traction injuries of the roots. Interruption of some “anomalous” roots can lead to an irreversible motor and sensory deficit. Variations in the distance of nerve roots in relation to the dura mater may also be the cause of some problems. Based on different studies, extradural and intradural variations of nerve roots were divided into four groups depending on different morphologic features of anomalies. We have summarized three classifications (Postacchini et al. [8], Kadish and Simmons [4], Neidre and McNab [9]), into one. As for type 1A, we distinguish three types of distance between nerve roots [2]. In Fig. 13.5, two nerves run from one dural sleeve. The cranial nerve root component is separated from the common nerve at an acute angle and passes under the corresponding pedicle. The lower component of the nerve root continues downward in the spinal canal and lies below the corresponding pedicle. For type 1B (Fig. 14.1), the cranial nerve component lies at 90° angle from the common nerve root, similar to the cervical nerve roots. For type 2A (Fig. 14.2), two separated nerve roots exit through one intervertebral neuroforamen. One neuroforamen is empty, or (in rare cases) some of the nerve roots can separate from one trunk and leave above the pedicle, so that the nerve roots leave through all foramina—type 2B (Fig. 14.3). Type 2 (Figs. 14.2, 14.3, and 14.4) represents “variations” when two nerve roots leave through one common foramen. In these “cases”, the root canal may be free as in Fig. 14.2, or the nerve roots may be found in all foramina, but one neuroforamen contains two separate roots as in Fig. 14.4. In type 3 (Figs. 12.19 and 12.20), the adjacent nerve roots are joined by a vertical anastomosis.

14  Extradural Connections of the Lumbosacral Nerve Roots

149

Fig. 14.1  Joined nerve roots

Type 4 presents extradural nerve root branching. Variations of joined nerve roots may additionally reduce the space for the lumbosacral nerve roots in the lateral recess of the spinal canal. Therefore, minor bulging of the intervertebral discs can manifest itself by more prominent radicular symptomatology. When joined nerve roots are identified preoperatively, the extruded material of the herniated discs can be hidden in the axilla of the connected neural structures. Furthermore, joined nerve roots are less mobile, and thus, it is much more difficult to move them during surgery than normal nerve roots compromised by the disc [5]. The most common variation is the common nerve roots, in which the two of them share the same dural sleeve. The preoperative diagnosis of variations of joined nerve roots is difficult. Lack of preoperative vigilance can lead to an iatrogenic injury of the nerve roots, especially in minimally invasive surgical procedures with limited visualization. In patients with anatomic variations and concomitant intervertebral disc herniation, unusual neurological symptoms may occur. Abnormal adherence of the two nerve roots is commonly observed [4, 10]. The incidence of this disorder ranges from 1.2% to 17%, and MRI shows 6%, but postmortem studies report 30% [8, 9, 11–14]. The most commonly affected level is L5–S1 [4, 8, 9, 13, 15, 16].

150 Fig. 14.2  Two roots exit through one neuroforamen. One neuroforamen is free, unoccupied

Fig. 14.3  Two nerve roots can be separated from one nerve root and exit above the pedicle, so that nerve roots exit through all neuroforamens

14  Extradural Connections of the Lumbosacral Nerve Roots

14  Extradural Connections of the Lumbosacral Nerve Roots

151

Fig. 14.4  Two roots exit through a common neuroforamen. The nerve roots are in all foramens, but one neuroforamen contains two separate roots

Radicular symptoms of these diseases are the results of stretching—tension of adhering root or roots. Variations of roots can cause radiculopathy even in the absence of mechanical compression, even in disc hernia or spinal stenosis at a remote site. They are the main cause of failed back surgery syndrome (FBSS), as the anomalous nerve roots are particularly sensitive to the retraction. So, a discectomy is technically more complicated. Nerve roots cannot be safely mobilized, and a possibility of their damage increases. In variations of nerve roots, e.g. in the common root of L4–L5, the patient may have symptomatology from the nerve root overtension. The root L5 can be found stretched above the pedicle S1. Therefore, foraminotomy is needed within the operation. In all cases of FBSS, variations of nerve roots should be suspected. Symptomatology of the herniated disc is the most common cause of variation detection. For a wide area of incidence of possible nerve root variations and the effect of stretching from contributing branches, in patients with these variations, a greater suspicion of a possible radicular syndrome arises, and the patients require extensive decompression in order to increase the chances for a favourable clinical outcome [12, 17]. The preoperative diagnosis of nerve root variations through MRI or CT myelography is possible in indicated cases to facilitate surgical planning and avoid unwanted complications.

152

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Three independent neuroradiologists who had no knowledge of the clinic of examined patients evaluated the results of MRI and CT graphic documentation, in those who have never had back pain, lumbar-ischiatic syndrome, or neurogenic claudication. About one-third of patients presented with serious abnormalities. In patients younger than 60 years, hernias were found in 20%, and in one of them, spinal stenosis was diagnosed. In a group of patients older than 60 years, 57% of scans showed abnormal findings—36% had disc hernias and 21% spinal stenosis. Degeneration or disc bulging, at least at the level of one lumbar vertebra, was diagnosed in 35% of 20–39-year-old patients and all but one between 60–90 years of age. Based on the above-mentioned observations, surgeons have concluded that abnormalities on MRI have to be correlated with age, clinical signs, and symptoms before indicating any surgical procedure [4]. Anatomical studies on sections have revealed extradural variations of the lumbosacral roots in 8.5% [18, 19], 14% [8], and 30% [11]. We have verified extradural variations of the lumbosacral nerve roots in nine cases (20.9%), variations of the cranial origin in two cases, and the caudal origin in two cases.

References 1. Haiijiao W, Koti M, Smith FW, Wardlaw D. Diagnosis of lumbosacral nerve roots anomalies by magnetic resonance imaging. J Spinal Disord. 2001;14(2):143–9. 2. Burke SM, Safain MG, Kryzanski J, Riesenburger RI. Nerve root anomalies: implications for transforaminal lumbar interbody fusion surgery and a review of the Neidre and Macnab classification system. Neurosurg Focus. 2013;35(2):E9. 3. Kilocucni S, Masne M, Nishiyama K, Ito T. Anatomic and clinical studies of radicular symptoms. Spine. 1984;9:23. 4. Kadish LJ, Simmons EH. Anomalies of the lumbosacral nerve roots. An anatomical investigation and myelographic study. J Bone Joint Surg (Br). 1984;66(3):411–6. 5. Chotigavanich C, Sawangnatra S.  Anomalies of the lumbosacral nerve roots. An anatomic investigation. Clin Orhop Relat Res. 1992;278:46–50. 6. Boden SD, Davis DO, Dina TS, Patronas NJ, Wiesel SW. Abnormal magnetic-resonance scans of the lumbar spine in asymptomatic subjects. A prospective investigation. J Bone Joint Surg Am. 1990;72(3):403–8. 7. Rask MR. Anomalous lumbosacral nerve roots associated with spondylolisthesis. Surg Neurol. 1977;8(2):139–40. 8. Postacchini F, Urso S, Ferro L.  Lumbosacral nerve-root anomalies. J Bone Joint Surg Am. 1982;64(5):721–9. 9. Neidre A, Macnab I. Anomalies of the lumbosacral nerve roots. Review of 16 cases and classification. Spine. 1983;8(3):294–9. 10. Zagnosi C. Reperto di un tipo non conosciuto di anastomosi nervosa delle radici spinali. Atti Soc Med Chir (Padova). 1949;27:48–52. 11. Bedeschi P, Bonola A. Anomalie di origine, di decorso di lungehezza e di diametro delle radici lombari e loro importanza nella patologia dell’ernia del disco. Reumatismo. 1956;8(5):266–80. 12. Ethelberg S, Riishede J. Malformation of lumbar spinal roots and sheaths in the causation of low backache and sciatica. J Bone Joint Surg (Br). 1952;34-B(3):442–6. 13. Goffin J, Plets C. Association of conjoined and anastomosed nerve roots in the lumbar region. A case report. Clin Neurol Neurosurg. 1987;89(2):117–20.

References

153

14. Scarf FF, Dalman DE, Toleikis JR, Bunch WM. Dermatomal evoked potentials in the diagnosis of lumbar root entrapment. Sur Forum. 1981;32:489–91. 15. Shane M, Burke BS, Nina G, Safain MD, James Kryzanski MD, Ron I, Riesenburger MD. Nerve roots anomalies: implications for transforaminal lumbar interbody fusion surgery and a review of the Neidre and Macnab classification system. Neurosurg Focus. 2013;35(2):E9, p. 1–6. 16. Yilmaz T, Turan Y, Gulsen I, Dalbayrak S.  Co-occurrence of lumbar spondylolysis and lumbar disc herniation with lumbosacral nerve root anomaly. J Cardiovertebral Jun Spine. 2014;5:99–101. 17. Pfeifer J. Neurologie v rehabilitaci. 1.vyd. Praha: Grada Publishing; 2007, 352 p. 18. Bardeen CR, Elting AW. A statistical study of the variations in the formation and position of the lumbo-sacral plexus in man. Anat Anz. 1901;19:209–19. 19. Keon-Cohen B. Abnormal arrangement of the lower lumbar and first sacral nerves within the spinal canal. J Bone Joint Surg (Br). 1968;50(2):261–5.

Part VI Anastomoses in the Region of Plexuses

Axonal Pathways to Innervation Regions of the Upper Limbs

15

The communicating branch between peripheral nerves, reduction or enlargement of innervation regions of nerves and sometimes even a complete replacement of one nerve by another, is an expression of the complexity of limb formation. A large number of segments (neurotomes, myotomes, dermatomes), from which the upper limb develops, the complexity and instability of their formation, are reflected in the complexity of pathways of axons and anatomical differences of the peripheral nerves. In the cases when two or three nerves with a common source of origin (in the sense of belonging to the uniform or adjacent segments) participate in innervations of any region of a limb, the axons may pass through the area in arrangement of one or more nerves. As an example, we can show possible pathways of axons to innervations of the dorsum of the hand, in which branches of ulnar, radial, and sometimes musculocutaneous nerves (n. ulnaris, n. radialis, n. musculocutaneus) participate. The ulnar nerve (n. ulnaris) contains axons of the C7, C8, and T1 segments. The radial nerve (n. radialis) contains axons from all segments involved in the formation of brachial plexus. Therefore, C7 and C8 are the segments, which are common for ulnar and radial nerves. The axons of the cells originating from these segments can pass to the innervation regions (skin segment of the dorsum of the hand) as in the arrangement of ulnar nerve as well as in the arrangement of the radial nerve. In the radial type of innervations, the radial nerve is innervating the whole region (Fig. 15.1); in the ulnar type, it is the ulnar nerve. Figure 15.2 shows possible pathways of the axons from the centre to the periphery. A common segmentary origin of the nerves explains frequent observations of connections between the nerves and overlapping lines in the regions that peripherally correspond to the above-mentioned segments. Some connections and the size of overlapping zones are unstable. Variability is an expression of instability of the peripheral nervous system. The nerve anatomy of the upper extremity is continuously studied through surgical findings, electrodiagnostic studies, and cadaver dissections. Although it is recognized that the anatomy is not changing rapidly, knowledge of the anatomic © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_15

157

158 Fig. 15.1  Pathways of axons to the end territories in the nerves of the upper limb

15  Axonal Pathways to Innervation Regions of the Upper Limbs T1

C8

n. ulnaris

C7

C6

n. radialis

relationships and their significance is increasing. The purpose of the current study is to provide a comprehensive analysis of the nerve anatomy of the upper extremity to include innervation patterns, critical landmarks, and clinical applications. The surgeon’s ability to diagnose and treat patients is dependent on a fund of knowledge about anatomy. Although the anatomy of the upper extremity is fairly constant, knowledge of anatomy is increasing rapidly. The axillary nerve begins at the ventral rami of C5 and C6 spinal nerves and continues at the smaller branch of the posterior cord of the brachial plexus. It innervates the deltoid and teres minor muscles via the anterior and posterior branches, respectively. Innervation of the deltoid muscles allows for the abduction of the arm after the action from the supraspinatus has already reached 15°. Teres minor is responsible for lateral rotation and also participates in maintaining the stability of

15  Axonal Pathways to Innervation Regions of the Upper Limbs Fig. 15.2  Pathways of axons to the end territories in the nerves of the upper limb

T1

159 C8

n. ulnaris

C7

C6

n. radialis

the glenohumeral joint. The posterior branch of the axillary nerve also gives rise to the upper lateral cutaneous nerve providing sensation to the inferior lateral deltoid region, at an area called the regimental badge area. After exiting the quadrangular space posteriorly, the anterior branch of the axillary nerve wraps around the surgical neck of the humerus to then innervate the deltoid muscle. The posterior branch continues from the quadrangular space to innervate the posterior portion of the deltoid, the teres minor, and the skin of the lateral upper to mid-arm. Injury to the axillary nerve presents as the result of an overstretched angle between the neck and the shoulder secondary to trauma or excessive force. Stretching of the axillary nerve at spinal roots C5 and C6 interrupts the innervation to the deltoid and teres minor. The prolonged injury will lead to atrophy of the deltoid muscle, resulting in the flattening of the shoulder curvature. The limb also hangs to the side in an adducted

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position due to the failure of the deltoid muscle to counter the actions of the adductor muscles in the arm and chest. Avulsion or rupture of the superior trunk affects not only the axillary nerve but also the biceps brachial and brachialis, which accentuates the clinical manifestations of axillary nerve injury, as well as leads to a persistent extension at the elbow. Axillary nerve injury can result from an inferior dislocation of the humerus, as well as a fracture at the surgical neck of the humerus, where the anterior branch of the axillary nerve wraps around, exposing the nerve to potential harm. Any irritation of the axillary nerve can also result in paraesthesia, numbness, tingling, or overall loss in sensation at the regimental badge area because the cutaneous branch coming from posterior axillary nerve is the only source of cutaneous innervation at this area. An abrupt onset of pain, followed by an extended period of progressive muscle weakness, atrophy, and sensory deficit, is another condition that can affect the axillary nerve. The radial nerve, including the radial nerve proper and the posterior interosseous nerve, innervates the muscles of the extensor surfaces of the brachium and forearm. The radial nerve arises from the posterior cord of the brachial plexus and receives a contribution from the fifth through eight cervical roots. Anterior to the subscapularis, the posterior cord divides into the axillary and the radial nerves. The axillary nerve enters quadrangular space, which is bounded by the shoulder capsule and subscapularis tendon superiorly, by the teres major inferiorly, by the long head of the triceps medially, and by the neck of the humerus laterally [1]. The radial nerve commences its descent into the arm by passing anterior to the latissimus insertion and dives into the triceps to lie on the posterior surface of the humerus distal to the acromion. It has been observed that the radial nerve lies on the surface of the medial head of the triceps, rather than the bony surface of the humerus, and does not do so until it crosses to the lateral aspect of the humerus along the spiral groove. The lower portion of the radial nerve crosses the midline and pierces the lateral intermuscular septum. The radial nerve is relatively safe during a posterior approach to the humerus (splitting the triceps). Above the elbow, the radial nerve innervates the long, lateral, and medial heads of the triceps and the brachioradialis [2]. Distal to the lateral epicondyle and deep to the brachioradialis, the radial nerve splits into the superficial radial nerve and the posterior interosseous nerve. The superficial radial nerve continues down to the forearm along the lateral border of the brachioradialis and becomes subcutaneous at its middle 1/3, innervating the skin on the radial aspect of the forearm and the dorsal aspects of the radial three and one-half digits. The posterior interosseous nerve continues down to the forearm dividing into the supinator and then emerging to split into several branches that supply the extensors of the wrist and hand. The innervation pattern is important in determining levels of entrapment of the posterior interosseous nerve. The nerve to the extensor carpi radialis brevis originated from the posterior interosseous nerve in 45%, at the bifurcation in 30%, and from the superficial branch of the radial nerve in 25%. The nerves to the extensor carpi radialis longus were branches from

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the posterior interosseous nerve. Innervation of the common extensor origin at the level of the bifurcation of the posterior interosseous nerve is highly variable. The order of innervation of the musculature (proximal to distal) is important in assessing entrapment syndromes of the radial nerve. The terminal branch of the posterior interosseous nerve is a sensory branch to the dorsal wrist capsule. Distal to its origin, the posterior interosseous nerve is prone to entrapment at several levels by various structures. Classically posterior interosseous nerve entrapment is known as radial tunnel syndrome. The radial tunnel begins shortly after the bifurcation of the radial nerve. The posterior interosseous nerve passes deep to fibrous bands that are confluent with the brachialis, brachioradialis, extensor carpi radialis brevis, and superficial head of the supinator, which forms the most proximal roof of the radial tunnel. These fibrous bands are the first structures that may compress the posterior interosseous nerve. Proximally, the floor of the tunnel consists of the capsule of the radiocapitellar joint. As the nerve travels distally, the floor is made up of the deep head of the supinator muscle until the posterior interosseous nerve dives into the substance of this muscle. As the posterior interosseous nerve continues through the tunnel and reaches the level of the radial neck, the roof is made up of recurrent vessels of the radial artery (Leash of Henry). The Leash of Henry is the second structure that may entrap the nerve. The posterior interosseous nerve then encounters the extensor carpi radialis brevis and gives off a branch to it (if the innervation comes from the posterior interosseous nerve). The extensor carpi radialis brevis may compress the nerve at this location. The posterior interosseous nerve passes beneath the sharp proximal edge of the supinator (Arcade of Frohse), which is the final location where it may be compressed. Although radial tunnel syndrome and posterior interosseous nerve entrapment often are used interchangeably, they should be considered two separate entities. The symptoms of radial tunnel syndrome are mostly pain and often are confused with lateral epicondylitis. The pain associated with the radial tunnel syndrome can be differentiated from that of the lateral epicondylitis by its location: because the pain associated with the lateral epicondylitis is located at the epicondyle versus 6–7 cm distal over the belly of the brachioradialis muscle in the radial tunnel syndrome. Also, pain associated with radial tunnel syndrome often is provoked by resisted supination and repetitive forearm pronation or wrist flexion. However, because the posterior interosseous nerve is primarily a motor nerve, weakness is the hallmark of its entrapment. The posterior interosseous nerve gives off branches to the extensor digitorum communis, extensor indicis, extensor pollicis longus, and extensor pollicis brevis muscles, distal to where the supinator exists. Therefore, the presence of motor weakness with the extension of the fingers or thumbs with pain at the lateral aspect of the elbow should raise suspicion of posterior nerve entrapment. The superficial branch is producing pain when injured. The superficial branch of the radial nerve is highly susceptible to injury from the placement of pins, wires, or external fixation pins.

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15.1 Ulnar Nerve After the medial cord of the brachial plexus gives off its contribution to the median nerve, the terminal branch continues into the axilla as the ulnar nerve with contributions from the eight cervical and first thoracic roots, with occasional contributions from C7. As the ulnar nerve passes through the axilla into the brachium, it lies superficial to the subscapularis, the teres major, and the latissimus dorsiʾs tendinous attachment to the proximal humerus. The ulnar nerve moves into a position that is posterior to the medial humerus condyle, wrapping around the medial epicondyle at the level of the elbow. As the nerve passes posteriorly to the epicondyle, it is encased within a fibrous sheath (Osborne’s ligament) laterally and the head of the flexor carpi ulnaris posteromedially. Together, these two structures form the cubital tunnel. The first branch of the ulnar nerve provides sensory innervation to the elbow capsule [1]. As the ulnar nerve exits the cubital tunnel, it courses between the two heads of the flexor carpi ulnaris and enters the anterior compartment of the forearm. Shortly after exiting the cubital tunnel, the ulnar nerve gives off more branches to the flexor carpi ulnaris. At approximately 5 cm distal to the medial epicondyle, the ulnar nerve gives off branches to the ulnar aspect of the flexor digitorum profundus providing innervation to the long flexors of the ring and little fingers. In the middle of the forearm, the ulnar nerve becomes superficial before the flexor carpi ulnaris becomes tendinous, and the ulnar nerve divides. The more superficial of the two branches courses dorsally toward the distal ulna and dorsum of the hand and becomes the dorsal sensory branch of the ulnar nerve. That supplies the dorsal ulnar side of the hand. An inconsistent palmar contribution of the ulnar nerve to the palm, the palmar cutaneous branch of the ulnar nerve arises proximally and carries innervation to the hypothenar skin and sympathetic fibres to the ulnar artery. Near the wrist, the ulnar nerve rises superficial to the flexor retinaculum and lies under the tendon of the flexor carpi ulnaris before its attachment to the piriformis. The ulnar nerve then turns radial – to the pisiform to lie in a fibrous tunnel known as Guyon’s canal. Within the canal, the ulnar nerve divides into motor and sensory branches. The superficial branch first gives off motor fibres to palmaris brevis and divides to innervate the ulnar side of the palm and ring finger and the entire small finger. The deep branch provides innervation to the adductor pollicis, opponens digiti minimi, abductor digiti minimi, flexor digiti minimi brevis, flexor pollicis brevis (deep head), interossei, and lumbricals. The two well-described connections between the median and ulnar nerves should be mentioned, the Martin-Gruber or proximal anastomosis [3] and the Riche-Cannieu anastomosis which occurs distally as a communication between the palmar cutaneous branches of the median and ulnar nerves. The Martin-Gruber anastomosis is an anastomotic connection between the median and ulnar nerve in the forearm.

15.2 Median Nerve The medial and lateral cords of the brachial plexus emerge from beneath the pectoralis minor’s attachment to the coracoid process of the scapula and split. The more lateral branch of the lateral cord is the musculocutaneous nerve, which has contributions from C5–C7. The musculocutaneous nerve dives into the coracobrachialis

15.2  Median Nerve

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distal to the coracoid and travels between the biceps and brachialis, innervating the coracobrachialis, long and short heads of the biceps, and half of the brachialis. The musculocutaneous nerve terminates at the lateral antebrachial cutaneous nerve of the forearm providing sensation of the lateral volar surface of the forearm. The median nerve has contributions from essentially the entire brachial plexus (C5–T1) and is formed by the portions of the lateral and medial cord [4]. The median nerve does not provide motor or sensory innervation until it reaches the elbow. Motor branches most commonly are found at the level of the elbow flexion crease; however, branches have been seen as far as 4 cm proximal to the elbow. The median nerve courses down the arm within the lateral intermuscular septum to the short head of the biceps and lateral to the brachial artery. In the antecubital fossa, the median nerve lies deep to the bicipital aponeurosis, medial to the antecubital vein, and medial to the brachial artery, making it the most medial structure encountered with the exception of the common origin of the flexor and pronator tendons. Although the median nerve is anterior to the trochlea and superficial to the brachialis, it occasionally can be found medial to the trochlea, such that it lies anterior to the medial epicondyle. This is of clinical importance in elbow dislocations. In theory, the nerve would be at higher risk of entrapment within the joint and in surgical fixation of medial epicondyle fractures. Distal to the elbow, the median nerve courses down to the forearm deep to the flexor digitorum superficialis and superficial to the flexor digitorum profundus. In the distal 1/3 of the forearm, the median nerve emerges from beneath the flexor digitorum superficialis to lie medial to the flexor carpi radialis and lateral to the palmaris longus, before entering the carpal tunnel. The most consistent order of branches of the median nerve is the pronator teres, flexor carpi radialis, flexor digitorum superficialis, palmaris longus, anterior interosseous nerve, and terminal or recurrent branches to flexor digitorum superficialis and palmaris longus. The innervation to the pronator teres is proximal to the elbow, whereas the remaining muscles are innervated distal to the elbow [5]. The median nerve gives a palmar cutaneous branch that provides sensation to the thenar skin of the palm, and its most common branches are 4–5 cm proximal to the wrist, lying on the ulnar side of the flexor carpi radialis. The palmar cutaneous branch divides into a radial branch that supplies the skin at the base of the thenar eminence and the ulnar branch that supplies part of the palm [6]. The ulnar branch of the palmar cutaneous branch often is found to penetrate the transverse carpal ligament before innervating the skin of the palm. Therefore, radial placement of the incision for a carpal tunnel release places this nerve at risk. The pronator teres has two heads of origin, a humeral head which is part of the common origin of the flexor and pronator tendons of the medial epicondyle and an ulnar head that originates distal to the coronoid process of the ulna. At the level of the junction of the two heads of the pronator teres, the median nerve gives off the anterior interosseous nerve. The anterior interosseous nerve quickly dives deep to the flexor and pronator mass and travels with the anterior interosseous artery to travel on the volar surface of the interosseous membrane. Along with its course, the anterior interosseous nerve innervates the flexor pollicis longus, pronator quadratus, and the flexor digitorum profundus to the index and middle finger before terminating as the sensory fibres to the volar capsule of the carpus. Within the carpal tunnel, the median nerve divides into three terminal branches.

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Compression of the anterior interosseous nerve may present with pain at the volar elbow and forearm. However, the differentiating feature is the lack of sensory symptoms in the fingers. Although there may be weakness of the flexor pollicis longus and flexor digitorum profundus to the index finger with anterior interosseous nerve compression, the thenar muscle should be spared, and electrodiagnostic studies may be helpful in differentiating these syndromes [7]. The lateral-most division gives off the terminal motor innervation of the median nerve, the recurrent motor branch that innervates the abductor pollicis brevis, flexor pollicis brevis, opponens pollicis, and the lateral two lumbricals before dividing into its terminal sensory branches [8, 9]. The branches of the median nerve must be visualized during a carpal tunnel release. The median nerve may become entrapped proximally or distally. There are two proximal entrapment syndromes, the pronator syndrome and the anterior interosseous syndrome, which have similar symptoms making them difficult to differentiate. The pronator syndrome occurs when the median nerve proper is compressed at the level of the elbow and may be compressed by four different structures: the proximal ligamentous attachment of the humeral head of the pronator teres (ligament of Struthers), lacertus fibrosus, muscle belly of the pronator, and the proximal edge of the flexor digitorum superficialis. The nerves of the arm and hand perform a substantial twofold role: commanding the intricate movements of the arms all the way down to the dexterous fingers while also receiving the vast sensory information supplied by the sensory nerves of the hands and the fingers. The movements of the arms must be fast and strong to complete the diverse activities the body engages in throughout the day. Even the tiny hand muscles, which perform very delicate and precise movements, are driven by about 250,000 neurons. Rapid conduction of sensory nerve signals from the hands provides critical information to the brain and feedback during precise activities. Five major nerves extend from the brachial plexus into the arm. Each of these nerves carries information in the form of nerve impulses to and from a particular region of the arm and hand. Some of these impulses are sent from various parts of the brain and spinal cord, some come from sense organs located in the joints, ligaments, and tendons, and some come from nervous tissue in the muscles themselves. As major sensory components of the body, the hands are a destination for a majority of the nerves in the upper limb, the radial, ulnar, and median nerve, having already supplied connections to the arm and forearm, and continue into the hand where they form a branching network of nerve fibres. These myriad nerve fibres work together to control many delicate, precise muscles of the hand and receive signals from millions of sensory receptors that detect the touch, pressure, temperature, and pain. The median nerve supplies the muscles and sensory receptors of the skin in the lateral (thumb side) palm; first, second, and third digits (thumb, index, and middle fingers); and lateral half of the fourth digit (ring fingers). Along the dorsum (back) of the hand, the radial nerve supplies the muscles and sensory receptors in the lateral dorsum and the first, second, and third digits. On the medial side of the hand, the ulnar nerve supplies the sensory receptors and muscles in the medial palm, medial dorsum, and medial half of the fourth digit (pinkie finger). The sum of these nerves and sensory receptors allows the peripheral nerves in the arms and hands to collect

References

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information about the external conditions in relation to the body’s internal state, to analyse this information, and to initiate appropriate responses to satisfy the body’s needs. The speed at which we can, for instance, remove our hand from surprisingly hot surface exemplifies the power of the central and peripheral nervous system in coordination within the upper extremities.

References 1. Basmajian JV, Slonecker CE. In: Kist K, editor. Grant’s method of anatomy: a clinical problemsolving approach. 11th ed. Baltimore: Williams & Wilkins; 1989. 2. Guse TR, Ostrum RF.  The surgical anatomy of the radial nerve around the humerus. Clin Orthop Relat Res. 1995;320:149–53. 3. Brandsma JW, Birke JA, Sims DS Jr. The Martin-Gruber innervated hand. J Hand Surg [Am]. 1986;11A(4):536–9. 4. Hoppenfeld S, de Boer P.  Surgical exposures in orthopaedics. Philadelphia: JB Lippincott; 1994. p. 1–214. 5. Zvěřina E, Stejskal L. Poranění periferních nervů. Praha, Avicenum, vol. 303; 1979. 6. Moore KL.  Clinically oriented anatomy. 2nd ed. Baltimore: Williams & Wilkins; 1985. p. 626–793. 7. Eversmann WW. Proximal median nerve compression. Hand Clin. 1992;8(2):307–15. 8. Kozin SH, Porter S, Clark P, Thoder JJ. The contribution of the intrinsic muscles to grip and pinch strength. J Hand Surg [Am]. 1999;24(1):64–72. 9. Papathanassiou BT. A variant of the motor branch of the median nerve in the hand. J Bone Joint Surg. 1968;50B(1):156–7.

Axonal Pathways to the Innervation Regions of the Lower Limbs

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The complexity of the formation of the lower limbs, which involves a large number of segments, and the assimilation of lumbar and sacral segments have resulted in observations of couplings between nerves and differences in vastness and territories of the nerve. All lumbar and sacral segments are a source of nerves of the lower limb. For example, axons of L1–L4 constitute basic nerves on the front extensor side of the lower extremities. The axons of the last lumbar and sacral segments S1–S4 are basically involved in the formation of common fibular and tibial nerves (n. peroneus communis and n. tibialis)—branches from sciatic nerve (n. ischiadicus) (Fig. 9.33). Genetic relatedness of segments of nerve sources enables the course of axons to the end innervation territories in several nerves that have a common source of the origin in the sense of belonging to their homonymous or adjacent segments. This is particularly important in regions where two or three nerves innervate any region, for example, the pathways of axons to the instep. In some cases, saphenous, superficial, and deep peroneal and sural nerves (n. saphenus, n. peroneus profundus, n. peroneus superficialis, and n. suralis) participate in innervations. The mentioned nerves have in their arrangement also the axons from L4, L5, and S1 roots. As the axons of L4 have the course of nerve arrangement of the lumbar and sacral plexus, so on the periphery, in this case the instep, we can observe in the borders of L4, L5, and S1 the nerve branches of the lumbar plexus (n. saphenus) and sacral plexus (nn. peronei superficiales and profundi, n. suralis, communicating branches between them and the overlapping zones). In the cases (Fig. 16.1) when the axons pass from the L4 and L5 to the end territory, in particular in the arrangement of the superficial and deep peroneal nerves (nn. peronei superficialis and profundus), only the branches of the mentioned nerves participate in the innervation of the instep within the borders of L4–L5. This example shows that the principal issue is seen only after clarification of the complex of the nerves involved in the innervations of any region (because the differences of the formation level of limbs or plexuses are reflected in the projections of segments on the periphery). © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_16

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Fig. 16.1  Pathways of axons to the end territories of innervation in the nerves of the lower limb

S1

n. suralis

L5

n. peroneus superficialis

L4

n. peroneus profundus

n. saphenus

Various ways of passage of axons to the end territories are possible, especially in the location of overlapping zones and replacing the territories of extending branches of a single nerve with the branches of another one. Figure 16.2 and Fig. 9.33 show a possible way of axons from the centre to the periphery of the nerves of a lower extremity. It is seen that the common origin of the lateral cutaneous femoral nerve (n. cutaneus femoris lateralis) and the femoral nerve (n. femoralis) (L1–L2) explains the location of connectors on the periphery of the borders L2. In addition, the presence of numerous connections between the obturator nerve (n. obturatorius) and femoral nerve (n. femoralis) finds its clarifications here. The figures show that the axons of L2, L3, and L4 segments can pass to their end territories in the arrangement of femoral nerve (n. femoralis) or the obturator nerve (n. obturatorius), and depending on it, the nature of branching, in the sense of the presence or absence of specific nerve branches of the mentioned nerves as well as overlapping zones, will be differentiated. The axons of segments L4 pass in the arrangement of the peroneal nerves (nn. peronei) and the saphenous nerve (n. saphenous). This explains the fact that in some

16  Axonal Pathways to the Innervation Regions of the Lower Limbs Fig. 16.2  Pathways of axons to the end territories of innervation in the nerves of the lower limb

S1

n. peroneus profundus

169 L5

L4

n. peroneus superficialis

cases, the peroneal nerve (n. peroneus) participates in innervations of the instep, and in others, its terminal branches are depleted at a much higher level. In the region of L4 on the periphery, there is the overlapping region due to the connections between both mentioned nerves. A common segmentary origin of the sciatic nerve (n. ischiadicus) explains the frequent occurrence of connections and overlapping zones observed on the posterior part of the femur and the dorsum pedis. Connections on the periphery do not occur randomly and cannot be attributed to anomalies. Their presence brings a certain regularity. In their location, there is certain dependence reflecting the complex genesis and explanation in a segmental body structure. Knowledge of the pathway and the relationship of the peripheral nerves increases the effectiveness of treatment. The following includes the nerves of the lower extremity, their pathways, and relationships. Fascicules, the building blocks of nerves, are composed of axons, Schwann cells, collagen, and endoneurial fluid surrounded by perineurium.

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Individual fascicles are separated by collagen and are bundled together by epineurium to form nerves. These features give nerves a characteristic “honeycomb” appearance in short axis. Nerves of lower limb arise from lumbar and sacral plexus. The main nerves of the lumbar plexus are femoral nerve, obturator nerve, and lateral cutaneous nerve of the thigh. The main nerves of the sacral plexus are superior gluteal nerve, inferior gluteal nerve, pudendal nerve, and sciatic nerve which terminates in the popliteal fossa into (1) the tibial nerve and (2) the common peroneal nerve. The femoral nerve arises from the posterior divisions of the anterior rami of the L2–L4 nerves. The location of the roots of the femoral nerve is within the matrix of the psoas major muscle. It travels deep to the inguinal ligament as it crosses from the trunk into the lower extremity, just lateral to the femoral artery in the femoral triangle. In the triangle, the nerve divides into several branches. It has muscular branches to the muscles of the anterior thigh, and a terminal cutaneous branch, the saphenous nerve. The patient may present with weakness of hip flexion and may complain of difficulty when walking or buckling of the knee. The saphenous nerve is composed of fibres from L3 and L4 nerve roots. As the femoral nerve passes deep to the inguinal ligament, it begins to give off its branches. The saphenous nerve is one of these branches. Distally the saphenous nerve is in a subcutaneous position as it descends the medial aspect of the leg with the great saphenous vein. It ends along the medial arch of the foot, supplying cutaneous innervation. This nerve is a pure sensory nerve, so no muscular weakness should be observed with it. If weakness is present, suspect femoral nerve involvement occurs, as it is the source of saphenous nerve.

16.1 Obturator Nerve The fibres from the anterior portions of the anterior rami of L2–L4 fuse to form the obturator nerve. As the nerve descends from the pelvis into the lower extremity, it gives anterior and posterior branches that travel around the obturator internus. The obturator nerve supplies motor innervation to the adductor muscles of the thigh and a patch of cutaneous sensation to the medial and distal aspect of the thigh and knee. Symptoms of entrapment of the obturator nerve usually involve difficulty with walking or a feeling of instability in the thigh. The pain is typically in the location of the pubic bone and increases with activity and may radiate down the medial aspect of the thigh and knee [1, 2]. Lateral femoral cutaneous nerve arises from the anterior rami of L2–L4. Common presentation is burning, pain, or tingling in the region of the anterolateral thigh that is worse when standing, walking, or lying prone (hip extension).

16.2 Sciatic Nerve The sciatic nerve arises from the anterior rami of L4 through S2 nerves. In the pelvis, these roots from the lumbosacral plexus lay on the anterior surface of the piriformis as they exit the pelvis through the greater sciatic notch. As the nerve

References

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approaches the superior aspect of the posterior thigh, it travels deep to the common origin of the hamstring muscles where it travels just superficial to the adductor magnus. As the sciatic nerve reaches the superior aspect of the popliteal fossa (split of biceps femoris and semimembranosus), it splits into tibial and common fibular branches. The symptoms usually consist of pain along the pathway of the nerve as it descends down the posterior thigh and into the posterior leg and foot. Symptoms may be alleviated somewhat if the patient externally rotates their hip, which will decrease the tightness of the muscle and stress on the nerve.

16.3 Tibial Nerve Tibial division of sciatic is composed of L4–S3 spinal nerves. As the tibial nerve descends toward the medial malleolus, it lies posterior to it and deep to the flexor retinaculum and abductor hallucis muscle. At this point, the nerve splits to its terminal branches, the medial and lateral plantar nerves. The calcaneal nerve emerges from either the tibial nerve or the medial plantar nerve and supplies sensation to the medial and posterior heel. Patients may exhibit symptoms of burning, numbness, or tingling on the plantar aspect of the foot. Symptoms are typically worse with standing or walking for extended periods of time that will improve with rest.

16.4 Fibular Nerve The common fibular nerve arises from the split of sciatic into its branches at the superior margin of the popliteal fossa. The nerve innervates the short head of biceps femoris along its pathway. The nerve then courses around the head of the fibula and through a fibrous tunnel of the fibularis longus muscle, referred to as the fibular tunnel. Distal to this tunnel, the common fibular nerve divides into two branches, the superficial and deep fibular nerves. Patients typically present with vague pain over the dorsal aspect of the foot. They may also present with pain the lateral leg or numbness and tingling over the distribution of the nerve. The deep fibular nerve emerges from the common fibular nerve after the fibular tunnel. Symptoms include vague pain, cramping, or burning on the dorsal aspect of the foot and between the first two digits. Tenderness is usually present over the entrapped segment at or below the ankle joint. Proximal entrapment of the deep fibular nerve may present with foot drop or weakness in dorsiflexion of the foot, or difficulty walking on heels.

References 1. Čihák R. Anatomie 3. 2nd ed. Praha: Grada Publishing; 2004. 673 p. isbn:80-247-1132-X. 2. Mráz P. Anatómia ľudského tela 2. 1st ed. Bratislava: Slovak Akademic Press; 2005. 286 p.

Anastomoses Between the Individual Nerves and Inside Nerves

17

17.1 C  haracteristics of the Macroscopic Structure of the Peripheral Nerves When we remove the epineurium (basically consisting of loose connective tissue), we can see fascicles—bundles of nerve fibres bordering by the perineurium (Figs. 17.1, 17.2, 17.3, and 17.4). The overall character of nerve structure resembles a plexus. Single fascicles have different thickness and form the mutual enlacement (Figs.  17.1 and 17.2). Such plexiform structure is found in all spinal nerves. There is no significant difference in macroscopic structure of sensitive and motor nerves. The plexiform structure appears to be the result of the presence of fascicular rami communicantes, in which groups of axons pass. They are divided by the septum of loose tissue of the Fig. 17.1 Intratruncal construction of peripheral nerves—scheme of peripheral nerves

© Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_17

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17  Anastomoses Between the Individual Nerves and Inside Nerves

Fig. 17.2 Intratruncal construction of peripheral nerves—scheme of peripheral nerves

Fig. 17.3  Intratruncal construction of peripheral nerves—scheme of peripheral nerves

17.2  Anastomoses Inside the Nerves

175

Fig. 17.4  Intratruncal construction of peripheral nerves—scheme of peripheral nerves

endoneurium (Figs. 17.3 and 17.4). The axons in the neural trunk pass from one perineural sleeve to the other in a different way in each particular case. Therefore, in the longitudinal resection of the nerve, we can see that the number of fascicles of the central stub is not identical with the number of fascicles of the peripheral stub. We can hardly expect the same clinical picture in partial damage to the uniform nerves at the same level, as plexiformity can be expressed in different grades and, in this context, the pathway of axons will have different orientations. The peripheral nervous system is (concerning its structure) extremely variable. The variety of structures is sometimes associated with a different function. Undefined or unrecognized variability can be the cause of symptoms of a vague disorder [1, 2].

17.2 Anastomoses Inside the Nerves This group includes anastomoses occurring even within the borders of one root (Fig. 17.5).

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17  Anastomoses Between the Individual Nerves and Inside Nerves

Fig. 17.5 Anastomoses between fascicles of the sensitive nerve visible after removing the epineurium— cells forming spinocerebellar ganglion (1) are scattered in the course of the individual fascicles (2) extending to the periphery

17.3 The Musculocutaneous Nerve It can emerge from the top of the median nerve bifurcation, from the top of bifurcation of the median and ulnar nerve, or from the median nerve. –– Terminal branches from the nerve can originate before entering the coracobrachialis muscle or enter another muscle. –– Anastomoses—with the median nerve, but also with the cutaneous antebrachii medialis, ulnar or radial nerve. The median nerve: –– Origin—the fusion of two roots, more or less lower, sometimes in the lower third of the arm, which indicates two median nerves, an additional branch forming the third median nerve.

17.4  Lumbosacral Plexus

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–– Course—various relations to the axillary and brachialis artery. –– Anastomoses—with the musculocutaneous nerve. The ulnar nerve: –– Origin—it can receive the lateral root of the median and musculocutaneous nerve under the bifurcation of the median nerve. –– Anastomoses—with the musculocutaneous, median, radial, and the cutaneous antebrachial nerve. The axillary nerve: –– It can emerge from the posterior fascicle, from the radial nerve or rarely laterally. We found anatomical variations of the axillary nerve as a continuation of the posterior division of superior trunks. –– Course—its course throughout the suprascapular muscle, generally it goes in front of it. The radial nerve—described variations were related to its origin: from two roots formed variably from the posterior division of trunks. The n. cutaneous brachii medialis: –– Origin—from the radial, axillary, and T1 nerve. The n. cutaneous antebrachii medialis: –– Origin—from the posterior fascicle, from the inferior trunk or the common root with the pectoral nerve or with the cutaneous brachii medialis nerve. –– Anastomoses—with the cutaneous brachii medialis, musculocutaneous, ulnar, median, axillary, and radial nerve.

17.4 Lumbosacral Plexus We followed the extraforaminal variations up to the terminal branches and the presence of the T12 and L4, or L5. Shorter motor branches terminate in the psoas major muscle directly, and longer ones leave the muscle and pass obliquely downwards to the pelvis, leaving it under the inguinal ligament. The obturator nerve leaves the pelvis through the obturator foramen. The following lumbar nerves—iliohypogastric, ilioinguinal, genitofemoral, lateral femoral cutaneous, obturator, femoral nerve, and sacral nerves—sciatic, superior gluteal, inferior gluteal, posterior cutaneous femoral, and pudendal nerve were identified bilaterally. The L4 participated in the lumbosacral trunk in all cases. The L5 did not contribute to the lumbar plexus in any case. We found a connection of the L3 to the L4–L5-S1  in the lumbar plexus; a duplicate and a plexiform root origin was observed. The L1 was the thinnest and the L4 the thickest. Among the nerves, the longest was the iliohypogastric nerve, the

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17  Anastomoses Between the Individual Nerves and Inside Nerves

thinnest was the ilioinguinal nerve, and the thickest was the femoral nerve. The majority of variations were found in the femoral nerve. Contributions from the L2 and L3 dominated, and the contribution from the L4 was small. The formation of the common femoral nerve may be more distal or not formed. The L4 participated in the sacral plexus in all cases. A missing connection between the two plexuses was not observed in any case. In the postfixed type, the lumbosacral trunk was thin and the S1 and S2 thicker. Changes of the sacral plexus at root level were present. We observed a plexiform origin of the L5 and a duplicated origin of S1, S2, and S3. In two cases the ischiatic nerve was divided into the pelvis minor. The posterior femoral cutaneous nerve leaves the S1 and receives a contribution from the S2 and S3. The pudendal nerve is formed from the S2 and S3 depending on the type of plexus. The main pudendal root is leaving the S3, and it receives a contribution from the S2 root. The lumbosacral plexus is the brachial plexus analogue. Variations are manifested on the periphery as variable contributions of some nerves, including variable tissue innervation. In addition to atypical clinical and electromyographic findings, many variations of the lumbosacral plexus are the source of diagnostic problems. It is important to understand which nerve functions are transmitted in the individual parts of the plexus. Simultaneously, it should be considered that due to various connections between the plexus roots, the muscle innervation can change independently to the root number entering the plexus. In the prefixed type, the nerve roots receive more fibres from the high spinal roots. The injuries of the high nerve roots or nerves are associated with larger lesions on the periphery than the same injuries affecting the postfixed type. In the postfixed type, the S3 can have many fibres usually carried in the S2, and the contribution of S4 can be more prominent.

References 1. Matejčík V. Anatomical variations of lumbosacral plexus. Surg Radiol Anat. 2010;32(4):409–14. 2. Šulla JI, Pilátová M, Balik V, Kollová A, Szilasiová J, Šulla I, Foltánová T. Selected topics from neurosurgery—textbook for physicians and students of general medicine. Košice: Pavol Jozef Šafárik University Press; 2011. 310 p.

Conclusion

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Some variability in certain dimensions, form, structure, and position is natural for the human body and internal organs. Simply said, it is tolerated and part of natural variability. Any deviation exceeding the expected variability is commonly called anomaly [1]. It is caused by any different developing process during the formation of individual structures. It may be caused by genetic, chromosomal, or environmental factors [1, 2]. Minor and major anomalies are classified according to functional and cosmetic differences [3, 4]. While major anomalies are common causes of diseases, disability, and death, minor anomalies usually do not have medical consequences [2–4]. Therefore, minor anomalies sometimes need to be clearly distinguished from variations. The frequency ranges from 7% to 41% while that of major anomalies from 2% to 3% [4]. A term minor anomaly is used to describe a morphological defect that can be observed from the outside (flat occiput, hypotelorism, cleft uvula, microglossia, pigmented spots, shawl scrotum, cubitus valgus, prominent heel, etc.) [3, 4]. The presence of several minor anomalies can draw attention to the existence of other more severe defects [2, 3]. Minor anomalies differ from variations, as they can be associated with major anomalies [2]. A term anomaly or malformation is used when structural changes have a negative impact on the function of the organism, in contrast to variations. Under certain conditions, however, even small and harmless variations may have a negative effect [5]. The history of anatomic variations and anomalies is closely linked to the history of anatomy itself, with the history of search and provision of a picture of normal structures and composition of the human body. Ancient anatomists Galen (AD 129–200) and Vesalius drew attention to individual variations. Therefore, in their work, expressions such as always, often, sometimes, rarely, and very rarely can be found. Claudius Galenus (Galen) first described Galen’s “anastomosis”-ramus communicans nervi laryngei cum nervo laryngeo inferiore and venae cerebri internae and vena cerebri magna. Andreas Vesalius (1514–1564) in his work Humani Corporis Fabrica (1542) described the © Springer Nature Switzerland AG 2019 V. Matejčík et al., Intraspinal Variations of Nerve Roots, https://doi.org/10.1007/978-3-030-01686-9_18

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anatomical variations of bones, muscles, and blood vessels. To understand the structure of the human body, he used dissection as the main instrument. Centuries were needed to establish normality, abnormality, and variations of the human body. These findings are based on the work of many anatomists, biologists, and clinicians. Their efforts continue to the present in publishing books and articles focused on anatomical variations that do not usually affect the function of the body. Medicine needs more accurate knowledge of the variability of the human body construction to improve the diagnosis and treatment. About 10% of misdiagnoses are based on ignorance of the anatomical variability [6, 7]. Newer imaging methods—echography, endoscopy, CT, and MRI—have opened the space for further research of anatomical variations and anomalies. In this work, we have focused on intraspinal variations of nerve roots. The results of anatomical studies are needed for more accurate interpretation of the perioperative as well as clinical findings. Knowledge about the structure of the peripheral nervous system is a mean to achieve the aim, which is perfect management of peripheral nerve injuries and treatment of partial or total disorders of sensitive and motor functions. Peripheral nerve lesions differ from all other injuries by their clinical course and results, which are largely determined by the complexity of the process of degeneration and regeneration. Neurons are the only cells, in which after section or constriction of the part of the body (axon) some changes may be induced leading to the regeneration of an amputated part of the axon and then to the adjustment of the functional oneness. The introduction of an operating microscope in the late 1960s and detailed knowledge of the structure of neurons have significantly improved results of operations. Excellent visibility of the surgical field, the optical magnification of corresponding structures, their perfect illumination, and fine microinstruments enable a delicate and precise preparation. Nerve fibres entering the brachial plexus and the lumbosacral plexus (plexus brachialis and plexus lumbosacralis) can exit from nerve cells of the spinal cord segments higher or lower, as published in textbooks, i.e. as is usually the highest incidence. These fibres find their tangle (plexus) of nerves and peripheral nerves to manage activities of relevant parts of the extremities. This common phenomenon is not called anomaly but variation. The aim of the work is to show the anatomical intraspinal variabilities and their participation in radiculopathy. Our observations (that we present in this book) are the results of the several years of systematic work on cadavers of previously healthy people who died by a violent death (most often in car accidents). The work on the intraspinal anomalies of the peripheral nervous system has enabled us to define exceptional and hitherto undescribed anatomical variations. We found that extradural shifts in the brachial and lumbosacral plexuses are associated with shifts of intradural intercommunications between adjacent ventral and dorsal roots. Because physical examinations often reveal unusual results, the presence of such intercommunications should be appreciated by the clinician involved with the diagnosis and treatment of patients with cervical and lumbosacral pathological entities. Clinical examinations that reveal unexpected results such as

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altered deep tendon reflexes or sensory dermatomes are different from the expected. Segmental innervation patterns may be the results that other vertebral levels contributed to intradural changes. To sum up, it may be said that intraspinal intradural and extradural neuroanatomical variations of nerve roots and their interrelationships through the spinal canal have a potential impact on the clinical picture. Anatomical dissections revealed a higher incidence of intraspinal intradural variations mainly between sacral roots. Reliance of their incidence of the type of plexus was observed. We believe that the data obtained will be helpful for spinal surgeons in improving a success rate of spinal operations. This work is dealing with the issue of intraspinal variations of the peripheral nervous system. Deviations, anomalies, variations, and everything that is subject to differences are actually a driving force for medicine. We cannot forget William Osler’s quote (1988) [8]: “Variability is the law of life”. The main contribution of this project is to provide a coherent picture of variations of the peripheral nervous system. The work is one of a few comprehensive documents evaluating the topic of intraspinal variations of the peripheral nervous system. We believe that this work will contribute to the better understanding of the complex problems of the topic. Acknowledgments  The authors would like to express their gratitude to Anna Francová for her help with the illustrations and preparation of this book. Ethical Standards Conflict of Interest  Figures of intraspinal variations of nerve roots were obtained by careful dissection and within the forensic expertise with the approval of the Ethics Committee ASHC, Grösslingova 5, 812 62 Bratislava, Slovak Republic. All studies related to intraspinal variations of nerve roots were made with the written consent of the competent bodies and in accordance with all applicable standards, rules, regulations, and laws and supervised by the responsible officials.

References 1. Arey LB. Developmental anatomy. Philadelphia/London: W.B. Saunders Company; 1940. 2. Holmes LB. Congenital malformations. N Engl J Med. 1976;12:204–7. 3. Marden PM, Smith DW, Mcdonald MJ. Congenital anomalies in the newborn infant, including minor variations. J Pediatr. 1964;64:357–71. 4. Stevenson RE, Hall JG.  Terminology. In: Stevenson RE, Hall JG, Goodman RM, editors. Human malformations and related anomalies, vol. I. London: Oxford University Press; 1993. p. 21–30. 5. Lippert H, Pabst R.  Arterial variations in man: classification and frequency. J.F.  BergmanVerlag: Műnchen; 1985. 6. Cahill DR, Leonardo RJ. Missteps and masquerade in medical academe: clinical anatomists call for action. Clin Anat. 1999;12:220–2. 7. Šulla JI, Lukáč I, Šulla I.  Syndroma caudae equinae discogenes. Košice: Univerzita Pavla Jozefa Šafárika v Košiciach; 2009. 231 p. isbn:978-80-7097-769-9. 8. Osler W. Profiles in Cardiology. Clin Cardiol. 1988;11:356–8.