Bioinspired Antifouling Surfaces: From Marine Applications to Biomedical Protections 9782759829422
Biofouling on marine vessels and bacterial growth on biomedical surfaces bring huge economic loss to our society. Tradit
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Table of contents :
Contents
Foreword
Chapter 1 Introduction to Biofouling and Bionics
Chapter 2 Marine Biofouling and Surface Properties
Chapter 3 Bioinspired Textured Surfaces for Marine Antifouling
Chapter 4 Natural Antifoulants for Antifouling Surfaces
Chapter 5 Other Nature-Inspired Marine Antifouling Surfaces
Chapter 6 Bioinspired Medical Surfaces
Chapter 7 Bioinspired SLIPS for Medical Antifouling
Chapter 8 Superhydrophobic Surfaces for Medical Antifouling
Chapter 9 Bioinspired Mechanical Bactericidal Surfaces
Chapter 10 Bioinspired Medical Drug-Delivery Surfaces
Conclusion
Citation preview
Current Natural Sciences
Limei TIAN, Jie ZHAO, Huichao JIN, Wei BING and Rujian JIANG
Bioinspired Antifouling Surfaces From Marine Applications to Biomedical Protections
Printed in France
EDP Sciences – ISBN(print): 978-2-7598-2941-5 – ISBN(ebook): 978-2-7598-2942-2 DOI: 10.1051/978-2-7598-2941-5 All rights relative to translation, adaptation and reproduction by any means whatsoever are reserved, worldwide. In accordance with the terms of paragraphs 2 and 3 of Article 41 of the French Act dated March 11, 1957, “copies or reproductions reserved strictly for private use and not intended for collective use” and, on the other hand, analyses and short quotations for example or illustrative purposes, are allowed. Otherwise, “any representation or reproduction – whether in full or in part – without the consent of the author or of his successors or assigns, is unlawful” (Article 40, paragraph 1). Any representation or reproduction, by any means whatsoever, will therefore be deemed an infringement of copyright punishable under Articles 425 and following of the French Penal Code. The printed edition is not for sale in Chinese mainland. Ó Science Press, EDP Sciences, 2023
Contents Foreword . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . VII CHAPTER 1 Introduction to Biofouling and Bionics . . . . . . . . . . . . . . . . . . 1.1 Biofouling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Bionics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.1 Definition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2.2 Antifouling Strategies Developed by Nature . . . . 1.2.3 Materials Science and Manufacturing Techniques References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1 1 3 3 3 4 6
CHAPTER 2 Marine Biofouling and Surface Properties . . . . . . . . . . . 2.1 Marine Biofouling . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Marine Biofouling Process . . . . . . . . . . . . . . . . . . 2.3 Fouling Organisms and Their Adhesion Behavior 2.3.1 Species of Fouling Organisms . . . . . . . . . . 2.3.2 Adhesion Behavior of Fouling Organisms . 2.4 Biofouling-Related Costs . . . . . . . . . . . . . . . . . . . 2.5 History of Antifouling Coatings . . . . . . . . . . . . . . 2.6 Basics of Wettability/Surface Energy . . . . . . . . . 2.6.1 Surface Wettability . . . . . . . . . . . . . . . . . 2.6.2 Solid Surface Energy . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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CHAPTER 3 Bioinspired Textured Surfaces for Marine Antifouling 3.1 Introduction of Textured Surfaces . . . . . . . . . . 3.1.1 Lotus Leaf . . . . . . . . . . . . . . . . . . . . . . 3.1.2 Rice Leaf . . . . . . . . . . . . . . . . . . . . . . . 3.1.3 Butterfly Wings . . . . . . . . . . . . . . . . . . 3.1.4 Mosquito Eyes . . . . . . . . . . . . . . . . . . .
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3.2
Design Principles of Textured Surfaces 3.2.1 Early Attempts . . . . . . . . . . . . 3.2.2 Engineered Roughness Index . . 3.2.3 Surface Energetic Attachment . 3.2.4 Contact Mechanics Theory . . . . 3.3 Challenges and Solutions . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .
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Other Nature-Inspired Marine Antifouling Surfaces . . . . 5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2 Natural Hydrogel-Inspired Antifouling Surfaces . . 5.2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . 5.2.2 Current Hydrogels for Marine Antifouling 5.3 Slippery Liquid-Infused Porous Surfaces (SLIPS) 5.3.1 Natural SLIPS . . . . . . . . . . . . . . . . . . . . . 5.3.2 SLIPS for Antifouling . . . . . . . . . . . . . . . 5.4 Bioinspired Dynamic Surfaces . . . . . . . . . . . . . . . 5.4.1 Renewable Surfaces . . . . . . . . . . . . . . . . . 5.4.2 Unstable Surfaces . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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47 47 47 47 48 52 52 52 55 55 58 60
Bioinspired Medical Surfaces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 Bacterial Infection and Traditional Antibacterial Strategies . 6.1.1 Antibiotics and Physiological Activity . . . . . . . . . . . 6.1.2 Biofilm Infections . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 Traditional Medical Antibacterial and Antifouling Methods 6.2.1 Causes of Drug Resistance . . . . . . . . . . . . . . . . . . . . 6.2.2 Manage and Prevent Drug Resistance . . . . . . . . . . . 6.3 Bioinspired Medical Antibacterial and Antifouling Methods References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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65 65 65 66 67 68 71 72 75
CHAPTER 4 Natural Antifoulants for Antifouling Surfaces 4.1 Introduction . . . . . . . . . . . . . . . . . . . . 4.2 Antifoulants from Marine Organisms . . 4.3 Antifoulants from Terrestrial Plants . . 4.4 Synthetic Analogues . . . . . . . . . . . . . . 4.4.1 Dihydrostilbenes . . . . . . . . . . . 4.4.2 Capsaicin Analogs . . . . . . . . . . 4.4.3 Indole Derivatives . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . CHAPTER 5
CHAPTER 6
Contents
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CHAPTER 7 Bioinspired SLIPS for Medical Antifouling . . . . . . . . . . . . . . . . . . . . . . . . . 7.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 Bioinspired Prototype of Lubricant-Infused Slippery Surfaces . . . . . . 7.3 Fundamental Principle and Liquid Repellency Mechanism of SLIPS . 7.4 Fabrication Strategies of SLIPS for Antifouling Applications . . . . . . . 7.5 Conclusions and Outlook . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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CHAPTER 8 Superhydrophobic Surfaces for Medical Antifouling . . . . . . . . 8.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2 Fabrication Technologies of Superhydrophobic Textiles 8.2.1 Bottom-Up Fabrication . . . . . . . . . . . . . . . . . . 8.2.2 Top-Down Fabrication . . . . . . . . . . . . . . . . . . . 8.3 Conclusions and Outlooks . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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CHAPTER 9 Bioinspired Mechanical Bactericidal Surfaces . . . . . . . . . . . . . . . . 9.1 Naturally Occurring Nanostructured Bactericidal Surfaces . 9.2 Bactericidal Mechanism . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.3 Artificial Mechanical Bactericidal Surfaces and Fabricating Technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.4 Conclusions and Outlook . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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CHAPTER 10 Bioinspired Medical Drug-Delivery Surfaces . . . . . . . . . . . . . . . . . . 10.1 The Inspiration and Development of Drug-Delivery Surfaces 10.2 Types of Bioinspired Drug-Delivery Medical Surfaces . . . . . 10.2.1 Bioinspired Hydrogels . . . . . . . . . . . . . . . . . . . . . . . 10.2.2 Bioinspired Polymeric Carriers . . . . . . . . . . . . . . . . 10.2.3 Bioinspired Nanostructures and Surfaces . . . . . . . . . 10.2.4 Other Bioinspired Drug-Delivery Surfaces . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 153
Foreword
Biofouling is the gradual accumulation of fouling organisms (such as bacteria, diatoms, and barnacles) on wetted surfaces. Back in 1943, Zobell first discussed biofilm formation and related corrosion on solid surfaces. Since then, the negative impacts, the formation mechanism, and the solutions of biofouling have been studied by many researchers, and it became the focus of extensive research in recent years. The growth of fouling organisms on marine vessels increases drag and accelerates corrosion, which can lead to high fuel consumption and excessive maintenance costs. Marine biofouling consumes billions of dollars and causes environmental disasters every year in the global shipping industry. Excessive fuel consumption increases the emissions of greenhouse gas (e.g., CO2), harmful compounds (e.g., NOx and SOx), and atmospheric pollutants. CO2 can contribute to the global warming trend and NOx and SOx cause acid rain and soil damage. The atmospheric pollutants in the air increase the health risk of human beings. These harmful emissions cause approximately 60 000 deaths globally and €200 billion in losses every year. Historically, conventional antifouling coatings were incorporated with toxic substances, which have been banned in many countries because of their toxicity to the marine environment. Hence, the development of effective, environmentally friendly, and low-cost antifouling coatings is necessitated. The formation of biofilm on biomedical surfaces and public facilities also leads to biofouling, which can bring bacterial infection risk to patients and public health. The application of antibiotics can reduce the suffering of human beings caused by bacterial infections. However, the optimism of antibiotic application was weakened by the discovery of drug-resistant strains. Therefore, it is necessary to construct an effective and antibiotics-free anti-biofouling and antibacterial surface coating in medical settings to prevent bacterial adhesion and settlement, reducing the spread of infections.
DOI: 10.1051/978-2-7598-2941-5.c901 Ó Science Press, EDP Sciences, 2023
VIII
Foreword
In the long-term evolution process of natural organisms, they present multiple functions through the joint action of their own morphology, structure, and other factors to achieve maximum adaptation to the environment. Many natural organisms have developed antifouling strategies. Inspired by these strategies, lots of artificial surfaces have been fabricated and tested. They are highly efficient and environmental-compatibility and they have the potential to achieve enhanced antifouling capabilities and desirable properties by combining the characteristics of novel materials. This book will focus on the application of bioinspired antifouling surfaces in two major fields—the marine industry (chapters 2–5) and the biomedical field (chapters 6–10). We expect this book not only to satisfy scientific curiosity but also contribute to the design and application of bioinspired antifouling surfaces. Limei TIAN Jilin University Changchun, China
Chapter 1 Introduction to Biofouling and Bionics 1.1
Biofouling
Biofouling is a phenomenon caused by the adhesion and growth of fouling organisms (e.g., bacteria, algae, barnacles, and mussels) on wet surfaces [1]. In 1943, Zobell first discussed biofilm formation and related corrosion on solid surfaces [2]. Since then, the negative impacts, the formation mechanism, and the solutions of biofouling have been studied by many researchers, and it has become the focus of extensive research in recent years. Biofouling significantly affects humans to explore the oceans and our health. This book will focus on biofouling in two major fields—the marine industry and biomedical applications. In marine environments, biofouling contributes to the corrosion of the surfaces (figure 1.1) and increases drag resistance, leading to massive economic losses. Another impact caused by biofouling is bio-invasion. The fouling organisms can travel with the ship hulls worldwide; when they arrive in a new sea with no enemies, they may threaten the local environment. Historically, traditional antifouling coatings prevent biofouling by releasing toxic substances (e.g., arsenic, lead, copper, and mercury). In the 1950s, a superior antifouling compound, i.e., tributyltin (TBT), was discovered. TBT was then widely applied on marine vessels in the next decades. Subsequently, TBT was found toxic to various marine organisms and could be enriched in upper predators through the food chain. It was reported that TBT had to be detected in human bodies in many countries. The released toxic substances in the ocean have brought great negative impacts on the environment and our health [3]. In recent decades, many countries have passed laws to forbid the application of TBT on marine vessels. Hence, developing effective, environmentally friendly, and low-cost antifouling coatings are necessitated. The formation of biofilm on biomedical surfaces and public facilities (figure 1.2) can also lead to biofouling, which can bring bacterial infection risk to patients and public health. The application of antibiotics can reduce suffereings of human beings caused by bacterial infections. However, the optimism of antibiotic discovery was weakened by the discovery of drug-resistant strains. Nowadays, some clinical bacteria strains have evolved multiple drug resistance, which is the consequence of antibiotic abuse in the past decades. Therefore, it is necessary to construct an DOI: 10.1051/978-2-7598-2941-5.c001 © Science Press, EDP Sciences, 2023
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Bioinspired Antifouling Surfaces
FIG. 1.1 – Biofouling on a marine platform (Images were kindly provided by the Ocean Science (Hong Kong) Limited).
FIG. 1.2 – (a, b) Scanning electron microscopic images of biofilm on human breast implants
(Reproduced with permission from [4], Plast. Reconstr. Surg., 2013, 132, 1319. Copyright © 2013 Elsevier B.V.); Schematic illustration of bacterial colonization on (c) a doorknob and (d) a mouse.
effective and antibiotics-free anti-biofouling and antibacterial surface coating on medical settings to prevent bacterial adhesion and settlement, reducing the spread of infections.
Introduction to Biofouling and Bionics
1.2 1.2.1
3
Bionics Definition
The word “bionics” is a contraction of “biological electronics”, which was first introduced in 1960 by Jack Steele. Bionics is the fabrication of modern systems by imitating the systems that exist in nature [5]. Bionics is a mimetic science concerned with the ability of biological systems to the solution of engineering problems. In 1969, Otto Schmitt introduced a similar term, “biomimetics”, which was defined as the study of underlying mechanisms of natural materials or substances to produce artificial products for humans. Biomimetics involves three major categories: (i) structure and function, (ii) machinery and sensing, and (iii) biomimetics in nanoscale. Bionics and biomimetics have been widely used as synonyms. Apart from the above two terms, the words “bioinspiration” and “bioinspired” are also widely used by researchers. Both modern terms embrace everything in the study of learning from nature [6]. Bionics is a bridge that connects nature and technology, which has been a major contributor to the development of nature-based science and technology. It provides innovations and solutions to different fields, from daily life to aeronautics and astronautics. As an interscience discipline, bionics combines with multiple disciplines, and this, in turn, promotes the development of different disciplines. For example, the head of high-speed trains is inspired by hummingbirds (figure 1.3) [7] or dolphins [8], which have developed significant drag resistance.
FIG. 1.3 – Bionic head of the high-speed trains inspired by hummingbirds [7] (Reproduced under the Creative Commons Attribution License).
1.2.2
Antifouling Strategies Developed by Nature
In the long-term evolution process of natural organisms, they present multiple functions through the joint action of their own morphology, structure, and other factors to achieve maximum adaptation to the environment. Through the physicochemical properties and structural morphology of organisms, specific functions, such as drag reduction, antifouling, anticorrosion, and wear resistance, can be formed. Different materials and devices with desirable properties can be fabricated by mimicking strategies developed by nature.
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Amongst the naturally observed phenomena, non-wetting and self-cleaning properties commonly identified on lotus leaves have been investigated and used extensively in constructing biomaterial surfaces. Based on the bacteria attaching resistance mechanism, superhydrophobic surfaces aim at repelling the initial adhesion of bacteria. Taking advantage of the lotus leaf, the formation of biofilms on surfaces can be dramatically reduced and can obtain self-cleaning performance. This can be attributed to the micro/nanostructures on the surface that can trap an air layer, resulting in a significant decrease in attraction between bacteria and substrates. Many organisms have superhydrophobic surfaces, as shown in figure 1.4. A comparable study showed that humpback whales could not resist the adhesion of barnacles (figure 1.4j), while the shark skin could keep cleaning by their micro-grooves (figure 1.4k). On the other hand, Nepenthes pitcher plants inspired slippery liquid-infused porous surface (SLIPS), emerging as a functional surface, has been developed as an effective platform for antibacterial and antifouling applications. Unlike superhydrophobic surfaces, liquid-like lubricants are locked within the micro/nanotextures. With the stably molecularly smooth nature of these surfaces, the fouling organisms can be efficiently resisted. In addition to attaching resistance mechanisms, in recent years, some studies revealed that natural superhydrophobic surfaces also exhibited bactericidal performances. Thereby, the mechanism of mechanical bactericidal surfaces and a novel strategy for achieving antibacterial function were proposed. By constructing a regularly spaced micro-pillar array and nanoneedles features on the substrate, a functional-bacteria-killing surface is realized. This innovative “resist-and-kill” surface has satisfactory durability in antibacterial applications. Without any introduction of chemical bactericides, this environment-friendly approach may have a wide practical application in the medical area, as well as without causing any risks of antimicrobial resistance. These outstanding properties and remarkable biocompatibility of surfaces have already proved themselves to be a new generation of biomaterials. Hence, surfaces inspired by nature may open a new avenue to develop antifouling surfaces.
1.2.3
Materials Science and Manufacturing Techniques
Developing advanced materials science and manufacturing techniques benefits the fabrication of complex bioinspired products. Polymer materials and new metal materials with robust mechanical strength, biocompatibility, and antifouling capability are used to fabricate bioinspired bones and other artificial organs. The application of nanomaterials endows bioinspired products with many excellent properties, including enhanced mechanical strength, thermal conductivity, and self-cleaning properties. Materials science and manufacturing techniques also benefit the development of bioinspired antifouling surfaces. For example, nanocomposites are used to fabricate bioinspired superhydrophobic surfaces (figure 1.5a). The 3D printing technique is used for the rapid fabrication of complex microstructures (figure 1.5b). Soft polymer materials such as silicone elastomer are used to mimic the tentacles of corals (figure 1.5c). Long-lasting phosphor materials are used to mimic the antifouling
Introduction to Biofouling and Bionics
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FIG. 1.4 – (a, b, c) Superhydrophobic surfaces of lotus; (d, e) Superhydrophobic surfaces of rice leaves; (f, g) Microstructures on butterfly wings; (h, i) A water spider and microstructures on its leg (Adapted with permission from [3], J. Mater. Chem. B, 2020, 8, 3701. Copyright © 2020 The Royal Society of Chemistry). feature of fluorescent corals (figure 1.5d). The progress of multidisciplinary promotes unprecedented prosperity in bionics. The opportunity and the challenge coexist, difficulty and hope within. It is expected that bionics can better contribute to the development of human beings.
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Bioinspired Antifouling Surfaces
FIG. 1.5 – (a) Silicone/β–MnO2 superhydrophobic surfaces (Reproduced with permission from [9], Colloid. Surf. A, 2019, 570, 518. Copyright © 2019 Elsevier B.V.); (b) 3D printed wavy structured porous surface (Adapted with permission from [10], J. Membr. Sci., 2019, 574, 76. Copyright © 2019 Elsevier B.V.); (c) Artificial soft tentacles inspired by corals (Adapted with permission from [11], Adv. Mater. Technol., 2019, 4, 1800480. Copyright © 2019 John Wiley and Sons); (d) Fluorescent coral inspired multilayer antifouling coatings for combating marine biofouling (Adapted with permission from [12], Adv. Mater. Interfaces, 2020, 7, 1901577. Copyright © 2020 John Wiley and Sons).
References [1] Selim M.S., Shenashen M.A., El-Safty S.A., Higazy S.A., Isago H., Elmarakbi A. (2017) Recent progress in marine foul-release polymeric nanocomposite coatings, Prog. Mater. Sci. 87, 1. [2] Zobell C.E. (1943) The effect of solid surfaces upon bacterial activity, J. Bacteriol. 46, 39. [3] Selim M.S., El-Safty S.A., Shenashen M.A., Higazy S.A., Elmarakbi A. (2020) Progress in biomimetic leverages for marine antifouling using nanocomposite coatings, J. Mater. Chem. B 8, 3701. [4] Deva A.K., Adams Jr. W.P., Vickery K. (2013) The role of bacterial biofilms in device-associated infection, Plast. Reconstr. Surg. 132, 1319. [5] Helfman Cohen Y., Reich Y. (2017) Biomimetic design method for innovation and sustainability. Springer International Publishing. [6] Barthlott W., Rafiqpoor M.D., Erdelen W.R. (2016) Bionics and biodiversity – Bioinspired technical innovation for a sustainable future. Springer International Publishing.
Introduction to Biofouling and Bionics
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[7] Hu H.-X., Tang B., Zhang Y. (2018) Application of the bionic concept in reducing the complexity noise and drag of the mega high-speed train based on computer simulation technologies, Complexity 2018, 3689178. [8] Foo C.T., Omar B., Taib I. (2017) Shape optimization of high-speed rail by biomimetic, MATEC Web Conf. 135, 00019. [9] Selim M.S., Yang H., El-Safty S.A., Fatthallah N.A., Shenashen M.A., Wang F.Q., Huang Y. (2019) Superhydrophobic coating of silicone/β–MnO2 nanorod composite for marine antifouling, Colloid. Surf. A 570, 518. [10] Al-Shimmery A., Mazinani S., Ji J., Chew Y.M.J., Mattia D. (2019) 3D printed composite membranes with enhanced anti-fouling behaviour, J. Membr. Sci. 574, 76. [11] Bing W., Tian L., Wang Y., Jin H., Ren L., Dong S. (2019) Bio-inspired non-bactericidal coating used for antifouling, Adv. Mater. Technol. 4, 1800480. [12] Jin H., Bing W., Jin E., Tian L., Jiang Y. (2020) Bioinspired PDMS–phosphor–silicone rubber sandwich-structure coatings for combating biofouling, Adv. Mater. Interfaces 7, 1901577.
Chapter 2 Marine Biofouling and Surface Properties 2.1
Marine Biofouling
Marine biofouling refers to the aggregation and growth of undesirable fouling organisms (e.g., bacteria, algae, and mussels) on subsea surfaces. The growth of fouling organisms on marine vessels increases drag and accelerates corrosion, leading to excessive fuel consumption and maintenance costs. In some cases, the propellers and ship hulls can be damaged by biofouling, which threatens the safety of crews. Much subsea equipment, including submarine pipelines, oil production platforms, and aquaculture net cages, are affected by biofouling. Subsequently, the involved equipment can be damaged, and production can be decreased. When fouling organisms travel with ships and arrive at a new sea, they may threaten the local species due to the lack of natural enemies; thus, biofouling can lead to bioinvasion. Many countries (e.g., the United States, Australia, and Singapore) have taken regulatory measures to reduce the bioinvasion caused by biofouling [1]. In order to dampen the impact of bioinvasion, the International Maritime Organization (IMO) issued the 2011 Guidelines for the Control and Management of Ship’s Biofouling to Minimize the Transfer of Invasive Aquatic Species [2]. Therefore, applying antifouling coatings to marine vessels will help reduce the negative impacts of biofouling. Conventional antifouling coatings are made of toxic chemical substances, including mercury, copper, and tributyltin (TBT). These coatings release toxic chemicals to kill fouling organisms and non-target marine organisms (figure 2.1). Due to the negative environment impacts, they have been gradually banned worldwide [3]. Hence, green and effective antifouling coatings are highly required in the marine industry. In nature, many plants or animals have developed antifouling capability to adapt to environmental pressure. In the past decades, many researchers have devoted themselves to studying the antifouling strategies from nature. The natural surfaces inspire us to design and fabricate new antifouling coatings. This book focuses on insights from nature and nature-inspired antifouling coatings. The fundamentals of natural antifouling strategies, surface properties, working mechanisms, fabrication techniques, and challenges are introduced and discussed. DOI: 10.1051/978-2-7598-2941-5.c002 © Science Press, EDP Sciences, 2023
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FIG. 2.1 – The impact of TBT antifouling coatings (Reproduced with permission from [4], J. Polym. Res., 2020, 27, 85. Copyright © 2020 Springer Nature).
We expect this book not only to satisfy scientific curiosity but also to contribute to the development of bioinspired antifouling coatings.
2.2
Marine Biofouling Process
In the ocean, any immersed surface suffers from biofouling. Biofouling is generally considered a stepwise process [5], which becomes heavy over time. Biofouling begins with the formation of conditioning film, which mainly consists of organic and inorganic macromolecules (e.g., polysaccharides and proteins). Soon afterwards, bacteria and diatoms will settle on the conditioning film to form a biofilm. The biofilm formation is reversible, as the attached bacteria and diatoms can be removed. Subsequently, bacteria will release chemical signals to attract more fouling organisms (e.g., invertebrates and algal larvae) to form a compact biofilm. Hence, biofilm has a complex structure composed of different microcolonies. Biofilm is an important substrate for the survival of microcolonies since it can protect the microorganisms from natural stress, including UV irradiation, pH shift, and bactericidal attack. In further colonization, macrofouling organisms, including macroalgae, hard shells, and hydroids, settle on the biofilm to form a macrofouling community. Biofilm is a crucial stage in forming biofouling; thus, the biofilm formation metric can some extent determine the antifouling capabilities of a coating. In real marine environments, many and varied factors can affect the biofouling process, such as temperature, salinity, pH, and location of seas. Hence, biofouling is a complex process that may not follow figure 2.2.
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FIG. 2.2 – Schematic illustration of the typical biofouling stages in the marine environment (Reproduced with permission from [6], Soft Matter, 2019, 15, 1087. Copyright © 2019 Royal Society of Chemistry).
2.3 2.3.1
Fouling Organisms and Their Adhesion Behavior Species of Fouling Organisms
It is well known that oceans cover most of the earth; thus, biofouling can affect everyone’s life directly and indirectly. It is reported that more than 4000 fouling organisms have been observed worldwide [7]. Several major fouling organisms worldwide include algae, sea squirts, barnacles, bryozoans, hydroids, mussels, and serpulids. (i) Algae: they can be classed into three categories: green algae, brown algae, and red algae, depending on the colors. Algae are eukaryotes without vascular bundles and can photosynthesize to store organic matter. They have different sizes or weights, from 1 μ to 60 kg. (ii) Sea squirts, which are cystic marine invertebrates that have been found all over the world. Most live in shallow water and on animal and plant debris. (iii) Barnacles, which are arthropods of the subphylum crustacean that are close to crabs and lobsters. Barnacles are the only marine animals that like to live in shallow and tidal waters. The barnacle sticks permanently to a hard surface. More than 12 000 species of barnacles have been reported all over the world. (iv) Bryozoans, which are colonizing animals. Millions of individuals can form a colony. These colonies can vary in size from millimeters to meters, but the individuals of these bryozoans are usually less than 1 mm long. They generally prefer warm, shallow tropical waters and are widely distributed around the globe. Like barnacles, bryozoans also prefer to stick to hard surfaces. More than 8000 species of bryozoans have been reported. (v) Hydroids, which belong to the phylum stinging cell animals that contain about 90 000 species, are mainly found in the Marine environment.
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(vi) Mussels contain several kinds of shellfish, such as clams and bivalve mollusks. They have a protective shell, most of which live on intertidal coasts and are attached to hard surfaces by strong whiskers. (vii) Serpulids, one of the symmetrically bodied marine fouling organisms with calcareous tubes. Serpulids usually settle on the surface of shellfish, rocks, boats, coral, and other hard objects. The size of fouling organisms covers a range from microns to centimeters (figure 2.3) [8]. Moreover, biofouling species vary in different Spatio-temporal conditions, including seasons, lights, seas, and depths. Overall, many factors can affect the biofouling process, which requires that the antifouling coatings should perform well in different conditions.
FIG. 2.3 – Size scales of typical fouling organisms (Reproduced with permission from [9], Nat. Commun., 2011, 2, 1. Copyright © 2011 Springer Nature).
2.3.2
Adhesion Behavior of Fouling Organisms
The species of organisms have different adhesion behavior in the biofouling process. For example, the feature of bacteria (e.g., shape, size, and species) can affect the adhesion process, which also depends on the chemical and physical of solid surfaces. Some studies have revealed that the adhesion activity between bacteria and the solid surface can be mediated by nonspecific (e.g., hydrophilic or hydrophobic) interactions [8, 10]. The adhesion of bacteria is affected by many factors, such as van der Waals force, electrostatic force, gravity, and the force induced by water flow. Bacteria also produce extracellular polymeric substances (EPS) to enhance adhesion activity [11]. The carbohydrate, protein, and humic substances in EPS can provide
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energy reserves and protection against harsh environments. Once bacteria stick tightly to surfaces, they start to produce EPS and then form a biofilm. The adhesion behavior of microalgae is similar to that of bacteria, which is affected by various external forces and EPS. Since most diatom species have no flagella, their free movement is limited [8]. Hence, the adhesion of diatoms is highly dependent on various external factors, including flow force, buoyancy force, and gravity. A typical adhesion process for diatoms begins with their arrival at the target surface, and then they secrete EPS to form a favorable environment. To get a better position, diatoms can glide on the EPS [12]. Finally, the communities of bacteria and diatoms lead to the formation of biofilm, which provides a favorable substrate for further fouling. The biofilm formation is the omen of subsequent macro fouling. However, some macro-fouling organisms (e.g., bryozoan larvae) can adhere to surfaces before biofilm formation [8]. The larvae like to settle and grow on favorable surfaces. If they dislike the surface, they will leave and search for the next one. Barnacles, as a famous macro fouling organism, have strong adhesion to surfaces and spend all their lives there. When the barnacle larvae reach a new surface, they release chemical signals to attract more individuals and breed more larvae. Ultimately, the formation of macroscopic fouling communities leads to serious biofouling. Both biofilm and macroscopic fouling can lead to significant drag resistance. It was reported that biofilm could increase by 70% drag resistance [13], and the heavy calcareous fouling could slow down the cruising speed of a ship up to 86% [14]. The adhesion strength of fouling organisms on surfaces increases with the development of biofouling [15]. The adhesion of early biofouling is weak, which can be removed by a shear stress of 1 Pa. The adhesion strength of macrofouling larvae can reach up to 0.1 MPa. After metamorphosis, the adhesion of macrofouling organisms such as branches can increase to 1 MPa. Hence, the critical stress required to remove fouling organisms increases with the development of biofouling (figure 2.4). These findings can guide us the when and how to remove the established fouling organisms.
FIG. 2.4 – (a) The formation of conditioning film; (b) Microorganisms begin to adhere to the conditioning film; (c) The formation of biofilm. (d) Macrofouling larvae adhere to the surface; (e) The growth of calcareous fouling (e.g., mussels, branches) (Adapted with permission from [15], Biofouling, 2017, 33, 703. Copyright © 2017 Taylor & Francis).
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2.4
Biofouling-Related Costs
Marine biofouling consumes billions of dollars and causes environmental disasters yearly in the global shipping industry. It was reported that the US Navy spent lots of money to address biofouling issues at the cost of an annual sum of $1 billion [16]. Annually, global biofouling costs the marine industry more than $15 billion [17]. The growth of biofouling on marine vessels increases drag resistance and corrosion. In serious cases, fuel consumption can reach up to 40%, and the total cruise expenses can increase by approximately 77% [18]. Additionally, excessive fuel consumption increases the emissions of greenhouse gas (e.g., CO2), harmful compounds (e.g., NOx and SOx), and atmospheric pollutants [19]. CO2 can contribute to the global warming trend, and NOx and SOx cause acid rain and soil damage. The atmospheric pollutants in the air increase the health risk of human beings. These harmful emissions cause approximately 60 000 deaths globally and €200 billion in losses every year [20]. To minimize the negative impacts caused by biofouling, antifouling coatings with toxic antifoulants were developed by early researchers. However, these coatings also show toxicity to non-target organisms, such as fish, and shrimps, and can accumulate in the food chain.
2.5
History of Antifouling Coatings
Table 1.1 shows the history of antifouling coatings. Anciently, Humans initially developed methods for protecting marine vessels from biological fouling. Two thousand years earlier, the application of thin lead plates has achieved on boats made of wood to prevent biological fouling. About 200 BC, greases, tars, and hot pitches received the coating onto hulls made of wood [3]. In Navigation Times, since seaweed and barnacles were reported for speed reduction, brass or copper was employed for sheathing ships; this technology is represented by the Cutty Sark coated by brass [21]. The thin copper layer is conducive for the boat to resist the TAB. 1.1 – A brief introduction to the development of antifouling coatings. Timeline 200 BC 0 AD 1500–1700 AD Late 18th century 1926 AD 1950s AD 1987–1990 AD 2001 AD 2001 AD – present
Major events Hot pitch, tars, and greases Thin lead plates Copper or brass Arsenic, sulfur, and mercury Copper oxide and mercuric oxide Tributyltin (TBT) TBT coatings were banned on vessels in some countries 2003 Prohibition on manufacturing of TBT antifouling paints 2008 Prohibition on the use of TBT on ship surfaces Environmentally friendly antifouling
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adhesion of fouling organisms, and such a method may assist Britain in being a major naval force three centuries ago. Other toxic substances (e.g., mercury, sulfur, and arsenic) exhibiting a 6–12 months lifespan had received the introduction for protecting ship hulls by the late 18th century [22]. In 1926, the US Navy fabricated a rosin antifouling coating by exploiting the fillers of copper oxide and mercuric oxide, capable of resisting biological fouling for 18 months [18]. In the 1950s, antifouling coatings were undergoing a revolution. Van der Kerk et al. reported the fouling-resisting properties of tributyltin (TBT) [23]. In such a period, TBT acted as the fouling-resisting coating with the highest effectiveness, thereby leading to its global prevalence. Though the mentioned toxic coatings have highly effective fouling-resisting characteristics, they threaten organisms related to the sea. Since the 1970s, lethal influences and accumulation of heavy metal fouling resisting compounds (e.g., arsenic, lead, and copper) under aquatic conditions have been found. It is noteworthy that the use of TBT exerted significant impacts within many marine ecosystems, so it is termed a pollutant worldwide and final banning. In the 1980s, a number of oyster farmers in France identified abnormal shell growth, which included shell deformation and anomalies within larval developing process. In addition, in the 1980s, the oyster industry of Arcachon Bay, France, became impoverished. Biological accumulation research containing TBT was extensively conducted around the globe, and considerable organisms covering mammals, birds, fish, crustaceans, and even humans have been suggested to accumulate TBT [24]. TBT is capable of leading to imposex and unnatural growing processes in numerous organisms. TBT can degrade in a slow manner and accumulate in marine organisms. Subsequently, the use of TBT on marine vessels was forbidden in many countries, including UK (1987), USA (1988), Canada (1989), Australia (1989), and the EU (1989) [25]. In 2001, the International Maritime Organization (IMO) evaluated the adverse influences exerted by TBT on the marine environment and put forward a prohibition on manufacturing of TBT fouling-resisting paints from January 01, 2003, and a ban on the use of the mentioned coating on ship surfaces from January 01, 2008. Hence, the development of new environmental-friendly fouling resisting coatings is necessary. In the past decades, a wide range of environmental-friendly fouling resisting strategic procedures has been developed. These coatings include biocide-releasing coatings, protein-resisting coatings, foul-releasing coatings (FRCs), and Nature-inspired antifouling coatings. Among the mentioned strategic procedures, Nature-inspired strategies have received great attention in recent decades. Nature-inspired strategies usually have environmental-friendly and efficient advantages, and they can be further combined with other strategies to enhance antifouling capabilities. Hence, nature-inspired strategies are promising for future applications.
2.6
Basics of Wettability/Surface Energy
The interactions between fouling organisms and target surfaces lead to adhesion and biofouling. The inherent properties (e.g., wettability and surface energy) of a solid can determine the adhesion process. They are so important that they are considered
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one of the necessary parameters of coatings. Hence, the two parameters will be discussed in this section.
2.6.1
Surface Wettability
2.6.1.1
The Young’s Equation
Wettability refers to the capability of liquid to contact a surface of a solid, dependent on the intermolecular force between the solid surface and the liquid. Thomas Young initially presented the concepts of contact angle and wettability in 1805, since which time a wide range of wettability measuring approaches was proposed. The commonest method for determining surface wettability is the process of measuring the contact angle. For a droplet contact with a solid in the air, three phases are generated, which are gas phase, liquid phase, as well as solid phase. Static contact angle (θ, CA) has a definition of being the tangent line between the gas–liquid interface at three phases’ intersection points (figure 2.5a). Young’s equation expresses the association of the interface tension and contact angle, as expressed by cS cSL cL cosh ¼ 0
ð2:1Þ
in the equation, θ represents the contact angle; γL, γSL, and γS denote the liquid/gas, solid/liquid, and solid/gas interface tensions separately. Figure 2.5b presents four configurations exhibited by a droplet contacting with solid surfaces. Under the CA lower than 10°, the surface has a definition of being superhydrophilic. Under the CA between 10° and 90°, the surface is defined as hydrophilic. Under the CA between 90° and 150°, the surface is defined as hydrophobic. Under the CA over 150°, the surface is defined as superhydrophobic. Notably, hydrophobicity and hydrophilicity have an inflection point of 90°. Nevertheless, as revealed from the recently conducted research, the boundary between hydrophobicity and hydrophilicity is required to be 65° in terms of a flat surface [26]. Specific to a smooth surface exhibiting an over 65°CA, the CA is elevated as the surface roughness is improved, whereas, in terms of that lower than 65°, the contact angle is down-regulated as the surface roughness is improved.
2.6.1.2
The Wenzel Model
Since surface roughness was a crucial parameter to determine the surface CAs, Wenzel began to complete Young’s equation and introduced the surface roughness to revise it. Wenzel’s equation reveals the relation between Young’s CA and the roughness factor: coshw ¼ rcosh
ð2:2Þ
where r stands for the surface roughness factor, and θw stands for the apparent CA on the rough solid surface. The equation suggests that the θw increases with increasing roughness and the surface exhibits more necessary hydrophobicity (figure 2.5c). In a word, the introduction of surface roughness on a smooth surface will lead to an enhancement in non-wetting properties.
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2.6.1.3
17
The Cassie–Baxter Model
Under the Cassie–Baxter status, the chemistry heterogeneity of surfaces exerts a remarkable influence on the equilibrium contact angle. Given the influence of chemistry heterogeneity on surfaces, droplets aren’t fully in contact with the micro grooves, actually, they are on the top of textured surfaces (figure 2.5c). In such multi-state surfaces, the air–associated parts are in a non-wetting status. Hence, a droplet can easily slide off because of the low adhesion force. Cassie and Baxter expanded the Wenzel equation: cosh ¼ f1 cosh1 þ f2 cosh2 ð2:3Þ where f1 and f2 denote the apparent area fraction of matter 1 and matter 2, separately (f1 + f2 = 1). θ1 and θ2 denote the apparent contact angles of the droplet on both materials separately. θ* denotes the apparent contact angle on the surfaces. When the surface has a pore-rich architecture or other textures capable of reserving air, and matter 1 and matter 2 are solid and vapour separately, f2 denotes the apparent area fraction of the air trapped on the surface. Due to f1 + f2 = 1, and θ2 = 180°, formula (2.3) is expressed as: cosh ¼ f1 cosh1 ð1 f1 Þ
ð2:4Þ
It’s evident that the Wenzel and Cassie–Baxter modeling methods offer a method to reveal the intricate mutual effect between the 3-phase edges on the textured surfaces. The two formulas are capable of elucidating the influences of surface structures on ultra hydrophobicity.
2.6.1.4
Dynamic Contact Angles
Naturally, a range of organisms has different wettability. For instance, fish skin exhibits a hydrophilic surface as impacted by mucus. Lotus leaves, as opposed to the mentioned, display superhydrophobic surfaces. Specific to natural systems, a surface generally does not exhibit the smooth property in an absolute manner or the homogeneous property from the chemical perspective, causing droplets to be non-static under most situations. For this reason, dynamic contact angle should be investigated. Dynamic contact angles have two categories. Figure 2.5d shows one of the two categories, with a liquid drop put on a surface and with droplets introduced in a constant manner to improve the droplet volume. As the volume is up-regulated to a threshold, the liquid drop starts to advance. Meantime, the angle of contact refers to the advancing angle (θa). As opposed to the mentioned, if the liquid receives the pumping process from the droplet for decreasing the volume to a particular data, the droplet starts moving backward; meantime, the contact angle is termed as the receding angle (θr). Figure 2.5e presents the other dynamic contact angle type, in which a droplet has the settlement onto an inclined surface, rolling down, containing θr and θa as receding angle and advancing angle, separately. Nonideal surfaces (e.g., heterogeneous chemical component or topography) are capable of causing hysteresis of contact angle (θh). The slant angle α at the rolling moment is given a definition to
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be the sliding angle. The associations between receding angle (θr), advancing angle (θa), sliding angle (α) and contact angle hysteresis (θh) have the following expressions hh ¼ ha hr
ð2:5Þ
mg ðsinaÞ=x ¼ cðcoshr cosha Þ
ð2:6Þ
in the equations, m and ω denote the weight and diameter of the liquid drop, g denotes the acceleration of gravity, while γ denotes the interfacial tension of the droplet. For a surface with a small slide angle, it’s hard to keep a liquid drop;hence the sliding of the liquid drop can remove pollutants easily, creating an antifouling surface, which is called the lotus effect. Rose petals have ultra-hydrophobic surfaces as well. Nevertheless, due to the adhesion with the petal, liquid drops can’t remove pollutants, which is called the “petal effect”. In addition, the same effect was discovered in peach skins, which is called the “peach skin effect” [27]. For that reason, the angle of the slide is pivotal for an ultra-hydrophobic surface to fight against biofouling. The fouling-resisting mechanism of hydrophilic surfaces shows the inconsistency with the lotus influence since hydrogen bonding or hydration layer induced in an electrostatic manner is easy to form on a hydrophilic surface, thereby physically hindering fouling organisms, with the fouling-resisting mechanism shown in figure 2.5e. As revealed from the mechanism, hydrophilic surfaces are capable of resisting the first biofouling, inconsistent with the superhydrophobic surface and FR surface.
FIG. 2.5 – (a) Schematic illustration of static contact angle; (b) Hydrophilicity and hydrophobicity; (c) Top: a droplet penetrating the spikes (Wenzel state) and Bottom: a droplet staying on the spikes (Cassie–Baxter state); (d) Illustration of advance angle (θa) and angle of regression (θr); (e) Kinetic angle of contact on a tilting surface.
2.6.2
Solid Surface Energy
Surface energy can indicate the disruption of intermolecular bonds during the generation of a novel surface. In addition, it is termed interfacial free energy or
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surface free energy. On the whole, a droplet on a surface containing significant surface energy exhibits high wettability; as opposed to the mentioned, the droplet on a surface containing small surface energy exhibits weak wettability. Surface energy refers to a critical factor to indicate surface contamination, and it is commonly achieved with the use of a surface forces device or through a contact angle measuring process. The process of measuring contact angle achieves extensive acceptance by numerous researchers for its low-cost, efficient, and simple Properties. On the basis of the process of measuring contact angle, a wide range of methods are put forward for calculating the surface Overall energy (e.g., the Owens–Wendt–Kaelble method [28, 29], the Lifshitz–van der Waals/acid–base approach [30], and the Li–Neumann theory [31]. For commercial uses, the coatings containing small surface energy achieve an extensive application in vessels with a high speed for exerting a foul release influence, i.e., foul release coatings (FRCs). In 1973, Baier initially investigated the association of relative adhesion and surface energy and put forward the notable “Baier curve” (figure 2.6a). In accordance with various research, the surfaces containing 22–25 mNm−1 surface energy are optimally capable of combating biological adhesion in hydrodynamic scenarios [32]. Since the Baier curve refers to an empirical curve with insufficient physically-related foundation, it fails to quantify the influence exerted by surface energy on fouling-resisting capability in an accurate manner. Brady et al. first employed fracture mechanics for expressing the removal process [33]. The mechanics of fracture is concerned with the research on crack propagation in materials. In accordance with figure 2.6b, a flaw is generated within a homogeneous plate based on uniaxial tensile stress. The crack tends to have propagation within the plate, thereby causing a more significant flaw (figure 2.6c). Likewise, flaws are produced between a surface and a fouling organism in the presence of biological adhesion, which will have propagation in the interface based on slip force or outer pull. Under the sufficiently large size of the flaws, the removal takes place, which can be clarified in accordance with the mechanics of fracture [34]. Given the fracture-related Griffith theory, it yields [35] rffiffiffiffiffiffiffi Ec F¼ ð2:7Þ Ap in the equation, γ expresses the solid’s surface energy density separately; E represents the elastic modulus of the material; A and F denote half of the flaw length and the stress at fracture. In accordance with equation (2.7), F refers to the pull-off force (the force for separating the fouling organism from the surface). F denotes an Eγ function. Specific to the materials involving the identical elastic modulus, F expresses a γ function. In terms of the materials containing the identical γ, F represents an E function. The mentioned associations have the expression: pffiffiffiffiffiffi F / Ec ð2:8Þ
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In accordance with equation (2.8), F is proportionally related to the square root regarding γ, E. The mentioned equations received experimental verification [33], with the results presented in figure 2.6d. As revealed from the mentioned results, the Griffith theory of fracture is capable of predicting the surfaces’ fouling-resisting ability containing a range of elastic moduli or surface energies.
FIG. 2.6 – (a) A typical “Baier curve” (Reproduced with permission from [20], Prog. Mater. Sci., 2017, 87, 1. Copyright © 2017 Elsevier B.V.); (b) A flaw is generated in a homogeneity plate with a 2a width and 2b thickness; (c) Different stages of crack propagation; (d) Relative adhesion of fouling organisms to surfaces with various parameters (Adapted with permission from [33], Prog. Org. Coat., 2001, 43, 188. Copyright © 2001 Elsevier B.V.).
References [1] Sing L.C., Tan K.S. (2018) Challenges in managing marine bio-invasions via shipping in Singapore, ASEAN J. Sci. Technol. Dev. 35, 125. [2] IMO. 2011 Guidelines for the Control and Management of Ship’s Biofouling to Minimize the Transfer of Invasive Aquatic Species. 2011, 62. [3] Amara I., Miled W., Slama R.B., Ladhari N. (2018) Antifouling processes and toxicity effects of antifouling paints on marine environment. A review, Environ. Toxicol. Pharmacol. 57, 115.
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[4] Ali A., Jamil M.I., Jiang J., Shoaib M., Amin B.U., Luo S., Zhan X., Chen F., Zhang Q. (2020) An overview of controlled-biocide-release coating based on polymer resin for marine antifouling applications, J. Polym. Res. 27, 85. [5] Silverman H.G., Roberto F.F. (2007) Understanding marine mussel adhesion, Mar. Biotechnol. 9, 661. [6] Xie Q., Pan, J., Ma C., Zhang G. (2019) Dynamic surface antifouling: mechanism and systems, Soft Matter 15, 1087. [7] Yebra D.M., Kiil S., Dam-Johansen K. (2004) Antifouling technology—past, present and future steps towards efficient and environmentally friendly antifouling coatings, Prog. Org. Coat. 50, 75. [8] Chaudhari C. (2017) Adhesion of fouling organisms and its prevention technique, Int. J. Adv. Res. Ideas Innov. Technol. 3, 427. [9] Callow J.A., Callow M.E. (2011) Trends in the development of environmentally friendly fouling-resistant marine coatings, Nat. Commun. 2, 1. [10] Dunne W.M. (2002) Bacterial adhesion: seen any good biofilms lately? Clin. Microbiol. Rev. 2002, 15, 155. [11] Laspidou C.S., Rittmann B.E. (2002) A unified theory for extracellular polymeric substances, soluble microbial products, and active and inert biomass, Water Res. 36, 2711. [12] Wetherbee R., Lind J.L., Burke J., Quatrano R.S. (1998) Minireview—the first kiss: establishment and control of initial adhesion by raphid diatoms. J. Phycol. 34, 9. [13] Schultz M., Walker J., Steppe C., Flack K. (2015) Impact of diatomaceous biofilms on the frictional drag of fouling-release coatings, Biofouling 31, 759. [14] Schultz M.P. (2007) Effects of coating roughness and biofouling on ship resistance and powering, Biofouling 23, 331. [15] Menesses M., Belden J., Dickenson N., Bird J. (2017) Measuring a critical stress for continuous prevention of marine biofouling accumulation with aeration, Biofouling 33, 703. [16] Callow M.E., Callow J.A. (2002) Marine biofouling: a sticky problem, Biologist 49, 1. [17] Flemming H. -C. (2011) Microbial biofouling: unsolved problems, insufficient approaches, and possible solutions, In Biofilm highlights, pp. 81–109. [18] Almeida E., Diamantino T.C., de Sousa O. (2007) Marine paints: The particular case of antifouling paints, Prog. Org. Coat. 59, 2. [19] Dahlbäck B., Blanck H., Nydén M. (2010) The challenge to find new sustainable antifouling approaches for shipping, Coast. Mar. Sci. 34, 212. [20] Selim M.S., Shenashen M.A., El-Safty S.A., Higazy S.A., Isago H., Elmarakbi A. (2017) Recent progress in marine foul-release polymeric nanocomposite coatings, Prog. Mater. Sci. 87, 1. [21] Douglas L. (2012) The Cutty Sark is back, Eng. Technol. 7, 68. [22] Dafforn K.A., Lewis J.A., Johnston E.L. (2011) Antifouling strategies: History and regulation, ecological impacts and mitigation, Mar. Pollut. Bull. 62, 453. [23] Van Kerk G.D., Luijten J. (1954) Investigations on organo‐tin compounds. III. The biocidal properties of organo‐tin compounds, J. Appl. Chem. 4, 314. [24] Senthilkumar K., Tanabe S., Kannan K., Subramanian A. (1999) Butyltin residues in migratory and resident birds collected from South India, Toxicol. Environ. Chem. 68, 91. [25] Champ M.A. (2000) A review of organotin regulatory strategies, pending actions, related costs and benefits, Sci. Total. Environ. 258, 21. [26] Zhu H., Huang Y., Lou X., Xia F. (2019) Beetle-inspired wettable materials: from fabrications to applications, Mater. Today Nano 6, 100034. [27] Lu X., Cai H., Wu Y., Teng C., Jiang C., Zhu Y., Jiang L. (2015) Peach skin effect: a quasi-superhydrophobic state with high adhesive force, Sci. Bull. 60, 453. [28] Owens D.K., Wendt R. (1969) Estimation of the surface free energy of polymers, J. Appl. Polym. Sci. 13, 1741. [29] Rudawska A., Jacniacka E. (2009) Analysis for determining surface free energy uncertainty by the Owen–Wendt method, Int. J. Adhes. Adhes. 29, 451. [30] Van Oss C.J., Chaudhury M.K., Good R.J. (1988) Interfacial Lifshitz-van der Waals and polar interactions in macroscopic systems, Chem. Rev. 88, 927.
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[31] Kwok D., Neumann A.W. (2000) Contact angle interpretation in terms of solid surface tension, Colloid. Surface. A 161, 31. [32] Salta M., Wharton J.A., Stoodley P., Dennington S.P., Goodes L.R., Werwinski S., Mart U., Wood R.J. K., Stokes K.R. (2010) Designing biomimetic antifouling surfaces, Philos. T. R. Soc. A 368, 4729. [33] Brady R.F. (2001) A fracture mechanical analysis of fouling release from nontoxic antifouling coatings, Prog. Org. Coat. 43, 188. [34] Sun Y., Guo S., Walker G.C., Kavanagh C.J., Swain G.W. (2004) Surface elastic modulus of barnacle adhesive and release characteristics from silicone surfaces, Biofouling 20, 279. [35] Griffith A., Gilman J.J. (1968) The phenomena of rupture and flow in solids. Trans. ASM 61, 855.
Chapter 3 Bioinspired Textured Surfaces for Marine Antifouling 3.1
Introduction of Textured Surfaces
In ancient China, people found that the lotus could keep a clean surface. However, Nevertheless, it was impossible to reveal the self-cleaning causal link of lotuses then; for that reason, lotuses were the embodiment of nobility in ancient poems. In recent years, due to the advancement of the scanning electron microscope (SEM) technique, the lotus effect has been unveiled. Microscale pillars were discovered on lotus leave surfaces (figure 3.1a) [1]. Certain air is trapped between liquid drops and surfaces, hence avoiding the penetration of droplets into surfaces and creating the self-cleaning effect. Recent studies also revealed that nanoscale structures were present on the pillars. These micro-/nanostructures provide excellent water-repellency for the lotus leaves. Numerous organisms have been found to exhibit surfaces with textured surfaces, including sharks [2], rice leaves [3], butterflies [4], reed leaves [5], shells [6], cicadas [7], beetles [8], Ephemera pictiventris [9], ginkgo leaves [10], springtails [11], and peanut leaves [12]. Based on the inspiration from the natural world, substantial scholars are focusing on substances that can simulate the natural anti-microbe effect. Certain naturally formed surface structures can reduce adhesion and proliferative velocities of alga spores and microbes, which can be considered self-cleaning surface structures. Overall, self-cleaning surface structures (lotus leaves, rice leaves, butterfly wings, and mosquito eyes) are capable of repelling microbe adherence and cell adhesion because of the micro-ultra hydrophobic textures and architectures.
3.1.1
Lotus Leaf
The low-adhesion superhydrophobicity and antifouling attributes of lotus leaves are research hotspots. Thanks to the microscale hierarchical architectures comprising nanoscale papillae covered by waxy villi, when liquid drops fall on the leaves, they’ll slide off directly, removing biofouling and pollutants, creating the “lotus effect”. The cavities on surfaces trap air inside, preventing droplets from penetrating and minimizing wetting, which is pivotal for the anti-biofouling attributes. Based on the DOI: 10.1051/978-2-7598-2941-5.c003 © Science Press, EDP Sciences, 2023
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inspiration from nature, substantial scholars have created hierarchically-structured surfaces with ultra-hydrophobic attributes.
3.1.2
Rice Leaf
In contrast to lotus leaves exhibiting representative isotropical super wettability, rice leaves present a special anisotropical wettability. A rice leaf has waxy hierarchic nanonipples with transversal grooves and a transversal sinusoidal architecture. The arrangement of nanonipples is quasi-one-dimension order parallel to the edges of the leaf, whereas they are vertical to the edges of the leaf stochastically. Thereby, their direction-wise arrangement offers a diverse energy barrier of wetting in both orientations. As shown in figure 3.1d, water droplets move easily on rice leaf surfaces parallel to the edge, exhibiting excellent superhydrophobic and low adhesive characteristics. This behavior can be of importance in applications that require rag reduction, self-cleaning, and, thus, antifouling.
3.1.3
Butterfly Wings
Wings of butterflies have valid self-cleaning attributes because of the combination of the anisotropical flow effects discovered on shark skins and the superhydrophobic attributes of lotus leaves. Resembling leaves of lotuses, the surfaces of butterfly wings are composed of neat hierarchic scales covered by micro-grooves, about 1 2 μm in diameter. The neat scales, 30 50 μm wide and 58 146 μm long, induce the anisotropical behavior (figure 3.1g–i). Due to the high angle of contact, liquid drops can slide off axially, which primarily causes the antifouling effect and low microbe adherence attribute. Zheng et al. have discovered that the liquid drop flow is anisotropical, i.e., liquid drops slide in an inside-to-outside manner, but if droplets slide oppositely, they can easily attach to the wing surfaces.
3.1.4
Mosquito Eyes
The compound eyes with broadband antireflection comprise a microscale big eye and hexagonally close-packed nanoscale corneal nipples, where periodic hexagonal arrays of nanoscale corneal nipples cover the outer surfaces (figure 3.1j–l). Then the textures can produce a gradient in refractive index at the interface, meanwhile, the hierarchical structures give the property of good dewetting to compound eyes under the air trapped between ommatidia. Various nanotechnologies, especially nanoimprint lithography, photoetching, reactive ion etching, and self-assembly techniques, have been developed to expand the compound eyes. Gao et al. combined photolithography with soft lithography to fabricate binary arrays of silica nanoparticles on large periodic polydimethylsiloxane (PDMS) hemispheres. Superhydrophobic hierarchical structures made by combining colloidal self-assembly with annealing– induced dewetting of sputtered gold films have also been demonstrated. The mentioned textured surfaces impart prominent independent cleaning and fouling-resisting abilities to each surface. Following this strategic procedure, many
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scholars have created surface structures with attributes similar to the aforesaid biosurfaces. Methods based on chemical vapor deposition (CVD) [13], photolithography [14], molding [15], laser ablation [16], and 3D printing [17], nanocomposites [18] have been developed to produce biomimetic surfaces, and numerous investigations have demonstrated their potential in fouling resisting applications.
FIG. 3.1 – (a) Presents the superhydrophobicity of lotus leaf surfaces; (b) Spheric droplet on a lotus leaf; (c) SEM imaging of a lotus leaf; (d) Rice effect—a combination of the lotus effect and shark-skin effect. Droplets are kept on a low-free-energy hydrophobical surface; (e) A rice leaf containing transversal grooves with a transversal sinusoidal pattern (Reproduced with permission from [18], J. Mater. Chem. B, 2020, 8, 3701. Copyright © 2020 The Royal Society of Chemistry); (f) Hierarchic architectures comprising nanonipples covered by waxy nano-bumps of a rice leaf; (g) Butterfly wings; (h) and (i) SEM imaging of butterfly wings with hierarchic architectures (Adapted with permission from [14], Soft Matter, 2012, 8, 11271. Copyright © 2012 The Royal Society of Chemistry); (j) presents the villus that nucleate droplets, so as to keep the eye surface clean and dry; (k) and (l) are SEM imaging results of hcp micro hemispheres (ommatidia), and hexagonally ncp nanobumps that cover ommatidia surface, separately (Reproduced with permission from [40], Adv. Mater., 2007, 19, 2213. Copyright © 2007 John Wiley & Sons).
Bioinspired Antifouling Surfaces
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3.2 3.2.1
Design Principles of Textured Surfaces Early Attempts
Besides shark skin, a number of seashells’ surfaces have developed antifouling properties. Figure 3.2 shows the typical ridge-like micropattern from shells of the species Mytilus edulis obtained from different parts of the world [19]. The surface morphologies differ depending on location, and the “contact point theory” predicts that the different shell microstructures will exhibit different antifouling abilities. According to the mentioned theory, as impacted by insufficient contact points in terms of adherence, fouling fails to be easy to take place under the fouling organism greater than the micro-texture dimensions [20]. Bers et al. [19] researched the self-cleaning attributes of different shells against various biofouling and didn’t discover any proof to substantiate the assumption. The aforesaid discoveries challenged the contact point theory, and it was afterwards considered an experiential delineation with no physical bases, and the quantification analysis of such theory is insufficient [21]. Chen et al. [21, 22] and Xu et al. [23] investigated the antifouling ability of a wide range of textured surfaces with the aim of identifying the fouling-resisting mechanism; however, their conclusions were also based primarily on empirical evidence. For instance, in the work of Xu et al. [15], the first group samples contained circular pillars with a diameter of 3 μm (figure 3.3a), the second group samples contained grooves with a width of 3 μm (figure 3.3b), and the last group samples contain the pits with a diameter of 3 μm (figure 3.3c). All the microstructures were spaced 3 μm, 6 μm, 9 μm,
FIG. 3.2 – Scanning electron micrographs of the Mytilus edulis mussel shell obtained from different parts of the world (Adapted with permission from [19], Biofouling, 2010, 26, 367. Copyright © 2010 Taylor & Francis).
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FIG. 3.3 – Samples contain (a) circular pillars, (b) grooves, and (c) pits. Antifouling performance of the samples with (d) pillars, (e) grooves, and (f) pits (Reproduced with permission from [23], Appl. Surf. Sci., 2014, 311, 703. Copyright © 2014 Elsevier B.V.).
and 12 μm apart. In the attachment test, three algae species were used, including Ulothrix, Closterium, and Navicula. The length of the three algae was 5–8 μm, 45–55 μm, and 10–12 μm, separately, and the width of all the algae was 3–4 μm. The results revealed that the different microscale structures and distances did affect fouling-resisting performance (figure 3.3d–f). However, they still failed to obtain a universal rule to predict the antifouling performance of a new microstructure.
3.2.2
Engineered Roughness Index
The engineered roughness index (ERI), put forward by Schumacher et al. [15], is employed for predicting the fouling-resisting ability of a texturing-based surface. ERI complies with the theories by Wenzel [24] and Cassie [25]. According to their findings, the negatively correlating process was suggested between ERI and the settlement density of Ulva spores. For the second version ERIII, df receives the replacement with n, i.e., the distinct feature of the respective texture. ERII ¼ ðr df Þ=ð1 us Þ
ð3:1Þ
ERIII ¼ ðr n Þ=ð1 us Þ
ð3:2Þ
Bioinspired Antifouling Surfaces
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in the equations, df expresses the freedom degree in terms of movement; φs represents the depressed surface fraction; r denotes Wenzel’s roughness factor. Subsequently, Long et al. (equation (3.3)) [26] and Decker et al. (equation (3.4)) [27]. developed the mentioned theory. According to equation (3.3), SSM represents the attachment on a smooth surface (ERIII = 0), and S denotes the attachment on a surface containing a set of ERIII. In equation (3.4), Nt refers to the attachment density exhibited by a texturing-based surface in comparison with a smooth surface Ns, and m refers to the slope fitted in an experimental manner. S r n 2 ln ¼ 7:47 10 ð3:3Þ SSM 1 us
Nt ln Ns
¼ m
rn ¼ mERIII 1 ð1 us Þ
ð3:4Þ
The mentioned models are highly consistent with the experimentally achieved results. Next, for optimizing the ERI model, the nanoscale-force gradient model was put forward. The model consists of the equation below [28], 3EI F¼ y ð3:5Þ L3 in the equation, y refers to the end deflection distance; L indicates the height of the feature; I expresses the rectangular moment of area; E represents the elastic modulus; F denotes the applied force.
3.2.3
Surface Energetic Attachment
In addition, Decker et al. [27, 29] put forward a model that complies with surface energetic attachment for predicting the fouling-resisting ability of a texturing-based surface. The model integrates Monte-Carlo simulation statistical approaches, the point-attachment theory, and the ERI models. The model has the expression below: E P ðEot Þ t At gt e ð3:6Þ \At [ ¼ Z
Nt ln Ns
ð\At [ As Þ gt þ ln ¼ As gs
ð3:7Þ
in the equations, g refers to the number of attachment sites; A denotes the average area. The mentioned model had the verification with the attachment testing process. As revealed from the rest results, the model exhibited high performance in estimating the attachment density of fouling organisms (e.g., cypris larvae, marine bacteria, diatom, and zoospores). The model has been verified to contribute to the development of fouling-resisting coatings. However, it was not adopted over the next few years.
Bioinspired Textured Surfaces for Marine Antifouling
3.2.4
29
Contact Mechanics Theory
The distinct leaves of the mangrove tree Sonneratia apetala have recently aroused huge attention (figure 3.4a). The leaves exhibit a prominent fouling-resisting ability due to a ridge-like surface morphology (figure 3.4b). A PDMS replica (figure 3.4c) received the fabrication and the test against fouling by tubeworms, with prominent results (figure 3.4d). As per the study on the mangrove tree leaves, a contact mechanism-based modeling method was proposed by Fu et al. [30] to realize the quantification of the dependence of antifouling capability on the profiles of ridge-like morphology. Actually, the modeling method upgraded the contact point theory. The antifouling capability was hypothesized to exhibit a positive association with the adhesive force between the biofouling and the surface texture. The biofouling denotes a cylinder with 3 probable contact patterns (multiple, double and single) with a textured surface (figure 3.4e). The pull-off force (F) between 2 cylinders can be written as [31]: 2 pE W RT FpfFlat ¼ 3 1=3 ð3:8Þ 16 1=E ¼ ½ð1 vT2 Þ=ET þ ð1 vS2 Þ=ES 0
ð3:9Þ
in the equations, ET, ES, vT, and vs denote the elasticity moduli and Poisson’s ratios of the cylinder and matrix separately. RT denotes the cylinder radius, and W denotes the adhesive energy between the cylinder and matrix. The profile of the surface is hypothesized that can be delineated by a function y = −Acos(2πx/λ), where λ and A denote the wavelength and amplitude separately. Firstly, our team hypothesized A = 0.5λ for simplicity. For single-point adhesion, the pull force between a cylinder and a surface is RS S Fpf ¼ ð3:10Þ 1=3FpfFlat RS þ RT in the equation, RS denotes the radius of curvature at the contact point. The pull-off force in terms of double-point attachment has the following expression: RS ð3:11Þ FpfD ¼ 2cosh 1=3FpfFlat RS þ RT in the equation, RS expresses the radius of curvature at the contact point; θ denotes the contact angle. The pull-off force in terms of multiple-point attachment has the following expression: 2 W A k M ð3:12Þ Fpf ¼ 10=9 5=9 4=9 7=9FpfFlat p 2pERT k RT Equations (3.10)–(3.12) express the pull-off force for the 3 contact patterns. The pull-off force between biofouling and a textured surface is probably greater or
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Bioinspired Antifouling Surfaces
smaller compared with the force between biofouling and a flat sheet (figure 3.4f). The pull-off force reaches its peak when λ/RT = 10 and at minimum at λ/RT = 0.1, indicating that the optimal fouling-resisting ability can be observed under λ/RT = 0.1. In terms of various ratios, the contact force analyzing process is conducted (A/λ = 0.125, 0.5, and 2), and figure 3.4g presents the results. At higher A/λ, the pull-off force is lower than the flat surface force over a λ/RT wider range, demonstrating that higher ridges help combat biological fouling. In addition, figure 3.3g shows that inter-ridge spacing can be optimized for reducing pull-off force. In other words, (λ) is a critical parameter in terms of fouling-resisting ability. Based on the fouling attachment test on synthetic surfaces, Fu et al. verified the contact force mode [30]. This physical model theoretically underpins the design of novel texturing-based surfaces, as opposed to the contact point theory.
FIG. 3.4 – (a) Photos of S. apetala leaves; (b) SEM image of an S. apetala leaf; (c) SEM image of PDMS replica of S. apetala leaves; (d) Abundance of fouling tubeworms on the glass slide and flat PDMS, compared with that on the PDMS replica; (e) Illustration of 3 patterns of adhesion contact of biofouling with a rough surface; (f) Variation of pull-off force with λ/RT for A/λ = 0.5; (g) Effect of A/λ on pull-off force (Adapted with permission from [30], J. R. Soc. Interface, 2018, 15, 20170823. Copyright © 2018 The Royal Society).
Bioinspired Textured Surfaces for Marine Antifouling
3.3
31
Challenges and Solutions
Extended field research on the performance exhibited by synthetic texturing-based surfaces under conditions relating to the sea has been less conducted. As revealed from several results, microorganisms (e.g., bacteria or diatoms) are capable of progressively filling up the valleys, which masks the textures and kills the biofouling influence [19]. For another inherent limit, the air inside surface profiles can’t bear pressures, hence the air is eventually replaced with liquid, which decreases antifouling efficiency [32]. As revealed from recent statistics, textures exhibited not any impacts or uncertain impacts on 46% cases’ of fouling [33]. Finger press or wiping in a slight manner is likely to kill the sensitive microscale structures [34]. The textured surfaces are likely to lose their fouling-resisting ability as impacted by aging or physically-related damage [35]. The mentioned potential defects can challenge texturing-based surfaces’ utilization in fouling-resisting uses. Long-term field assessments should be further conducted to verify the applicability of this strategic procedure to marine fouling resisting. Besides, the development of the most suitable manufacturing methods to achieve mass production also issues a challenge. The manufacturing methods are partially unsuitable for mass production under a wide range of elements (e.g., high cost), creating a barrier over the relevant actual uses. For the reduction of physically-related damage to microscale structures, the superhydrophobic surfaces exhibiting significant mechanical stableness achieved the recent development. According to Zhang et al. [34], the surface received fabrication using A380 aluminum alloy with the electrodeposition approach. The surface showed microscale-nano hierarchical configurations (figure 3.5a and b). Based on a
FIG. 3.5 – (a) SEM image of the prepared surface with micro-nano hierarchical structures; (b) Morphology of the surface; (c) Abrasion test; (d) Water contact angles vary with abrasion cycles (Adapted with permission from [34], Appl. Surf. Sci., 2019, 473, 493. Copyright © 2019 Elsevier B.V.).
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Bioinspired Antifouling Surfaces
finger-wipe process, the droplet was capable of maintaining a ball shape (figure 3.5c). According to the abrasion testing process, a 40 g pressure was employed onto sandpaper, following the surface reciprocation, and the surface was capable of maintaining hydrophobicity after 19 cycles (figure 3.5d). Likewise, Roy et al. [36] developed one surface displaying dual-scale wrinkles, exhibiting prominent robustness against mechanically-related damage, even when 50 cycles of abrasion testing were performed. Besides the mentioned methods, boiling water treating process in the short term, HF/HCl, and HNO3/HCl approaches were exploited for fabricating the superhydrophobic surfaces exhibiting significant mechanically-related characteristics [37]. The stableness enables the superhydrophobic surfaces to be exploited under actual conditions. The self-repair approach is another valid way to uplift the physical performance of surfaces. Pan et al. [38] discovered a restorable micro-scale architecture and self-healing surface to reinforce the mechanical intensity of the micro-scale architectures. Figure 3.6 presents the related preparation process. The micropillar array was decorated with pH-responsive capsules involving fluoroalkylsilane. The surface could repair the impaired micro-scale architectures through heating. It could be
FIG. 3.6 – Schematic illustration of shape memory antifouling surfaces (Reproduced with
permission from [38], ACS Appl. Mater. Interfaces, 2020, 12, 5157. Copyright © 2020 American Chemical Society).
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restored in an independent way posterior to the stimulation of acidic stimuli. In addition, Wang et al. [39] proposed a similar superhydrophobic surface with perpendicularly aligned ZnO@STA nano-cones, which could form the intersection and stacked structure via pressures or frictions (figure 3.7). Such architecture exhibited independent repairability and defended the STA against abrasion. Although the experimental outcomes are thrilling, the impairment-resisting property and durableness in the real world are still elusive. As the impairment-resisting property is pivotal for the application of the micro-scale architecture, more research is needed. Future studies should focus on the effect of the impairment-resisting property in the independent repair approach.
FIG. 3.7 – Schematic illustration of ZnO@stearic acid nanocone arrays (Reproduced with permission from [39], J. Alloys. Compd., 2019, 807, 151663. Copyright © 2019 Elsevier B.V.).
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[8] Parker A.R., Lawrence C.R. (2001) Water capture by a desert beetle, Nature 414, 33. [9] Han Z., Guan H., Cao Y., Niu S., Ren L. (2014) Antifogging properties and mechanism of micron structure in Ephemera pictiventris McLachlan compound eyes, Chin. Sci. Bull. 59, 2039. [10] Pan S., Guo R., Xu W. (2014) Investigating and biomimicking the surface wetting behaviors of ginkgo leaf, Soft Matter 10, 8800. [11] Hensel R., Helbig R., Aland S., Voigt A., Neinhuis C., Werner C. (2013) Tunable nano-replication to explore the omniphobic characteristics of springtail skin, NPG Asia Mater. 5, e37. [12] Gou X., Guo Z. (2018) Superhydrophobic plant leaves with micro-line structures: An optimal biomimetic objective in bionic engineering, J. Bionic Eng. 15, 851. [13] Cao X., Pettitt M.E., Wode F., Sancet M.P.A., Fu J., Jian J., Callow M.E., Callow J.A., Rosenhahn A., Grunze M. (2010) Interaction of zoospores of the green alga Ulva with bioinspired micro- and nanostructured surfaces prepared by polyelectrolyte layer-by-layer self-assembly, Adv. Funct. Mater. 20, 1984. [14] Bixler G.D., Bhushan B. (2012) Bioinspired rice leaf and butterfly wing surface structures combining shark skin and lotus effects, Soft Matter 8, 11271. [15] Schumacher J.F., Carman M.L., Estes T.G., Feinberg A.W., Wilson L.H., Callow M.E., Callow J.A., Finlay J.A., Brennan A.B. (2007) Engineered antifouling microtopographies– effect of feature size, geometry, and roughness on settlement of zoospores of the green alga Ulva, Biofouling 23, 55. [16] O’Neill P., Barrett A., Sullivan T., Regan F., Brabazon D. (2016) Rapid prototyped biomimetic antifouling surfaces for marine applications, Mater. Today Proceed. 3, 527. [17] Yan C., Jiang P., Jia X., Wang X. (2020) 3D printing of bioinspired textured surfaces with superamphiphobicity, Nanoscale 12, 2924. [18] Selim M.S., El-Safty S.A., Shenashen M.A., Higazy S.A., Elmarakbi A. (2020) Progress in biomimetic leverages for marine antifouling using nanocomposite coatings, J. Mater. Chem. B 8, 3701. [19] Bers A.V., Díaz E.R., Da G.B., Vieira-Silva F., Dobretsov S., Valdivia N., Thiel M., Scardino A.J., Mcquaid C.D., Sudgen H.E. (2010) Relevance of mytilid shell microtopographies for fouling defence–a global comparison, Biofouling 26, 367. [20] Scardino A.J., Guenther J., De N.R. (2008) Attachment point theory revisited: the fouling response to a microtextured matrix, Biofouling 24, 45. [21] Chen Z., Zhao W., Mo M., Zhou C., Liu G., Zeng Z., Wu X., Xue Q. (2015) Architecture of modified silica resin coatings with various micro/nano patterns for fouling resistance: Microstructure and antifouling performance, RSC Adv. 5, 97862. [22] Chen Z., Zhao W., Xu J., Mo M., Peng S., Zeng Z., Wu X., Xue Q. (2015) Designing environmentally benign modified silica resin coatings with biomimetic textures for antibiofouling, RSC Adv. 5, 36874. [23] Xu J., Zhao W., Peng S., Zeng Z., Zhang X., Wu X., Xue Q. (2014) Investigation of the biofouling properties of several algae on different textured chemical modified silicone surfaces, Appl. Surf. Sci. 311, 703. [24] Wenzel R.N. (1936) Resistance of solid surfaces to wetting by water, Ind. Eng. Chem. 28, 988. [25] Cassie A.B.D., Baxter S. (1944) Wettability of porous surfaces, Trans. Faraday Soc. 40, 546. [26] Long C.J., Schumacher J.F., Robinson P.A., Finlay J.A., Callow M.E., Callow J.A., Brennan A.B. (2010) A model that predicts the attachment behavior of Ulva linza zoospores on surface topography, Biofouling 26, 411. [27] Decker J.T., Kirschner C.M., Long C.J., Finlay J.A., Callow M.E., Callow J.A., Brennan A.B. (2013) Engineered antifouling microtopographies: An energetic model that predicts cell attachment, Langmuir 29, 13023. [28] Schumacher J.F., Long C.J., Callow M.E., Finlay J.A., Callow J.A., Brennan A.B. (2008) Engineered nanoforce gradients for inhibition of settlement (attachment) of swimming algal spores, Langmuir 24, 4931. [29] Decker J.T., Sheats J.T., Brennan A.B. (2014) Engineered antifouling microtopographies: Surface pattern effects on cell distribution, Langmuir 30, 15212.
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[30] Fu J., Hua Z., Guo Z., Feng D.-Q., Thiyagarajan V., Yao H. (2018) Combat biofouling with microscopic ridge-like surface morphology: A bioinspired study, J. R. Soc. Interface 15, 20170823. [31] Chaudhury M.K., Weaver T., Hui C.Y., Kramer E.J. (1996) Adhesive contact of cylindrical lens and a flat sheet, J. Appl. Phys. 80, 30. [32] Nhung Nguyen T.P., Brunet P., Coffinier Y., Boukherroub R. (2010) Quantitative testing of robustness on superomniphobic surfaces by drop impact, Langmuir 26, 18369. [33] Carve M., Scardino A., Shimeta J. (2019) Effects of surface texture and interrelated properties on marine biofouling: A systematic review, Biofouling 35, 597. [34] Zhang D., Li L., Wu Y., Zhu B., Song H. (2019) One-step method for fabrication of bioinspired hierarchical superhydrophobic surface with robust stability, Appl. Surf. Sci. 473, 493. [35] Bocquet L., Lauga E. (2011) A smooth future? Nat. Mater. 10, 334. [36] Roy P.K., Ujjain S.K., Dattatreya S., Kumar S., Pant R., Khare K. (2019) Mechanically tunable single-component soft polydimethylsiloxane (PDMS)-based robust and sticky superhydrophobic surfaces, Appl. Phys. A 125, 535. [37] Calabrese L., Khaskhoussi A., Patane S., Proverbio E. (2019) Assessment of super-hydrophobic textured coatings on AA6082 Aluminum alloy, Coatings 9, 352. [38] Pan S., Chen M., Wu L. (2020) Smart superhydrophobic surface with restorable microstructure and self-healable surface chemistry, ACS Appl. Mater. Interfaces 12, 5157. [39] Wang J., Zhang J., Yin Y., Jin H., Liu S., Li Y., Wang C. (2019) The stable superhydrophobic ZnO@stearic acid nanocone array and its remarkable all-sided protective abilities in various extreme environments, J. Alloys. Compd. 807, 151663. [40] Gao X., Yan X., Yao X., Xu L., Zhang K., Zhang J., Yang B., Jiang L. (2007) The dry-style antifogging properties of mosquito compound eyes and artificial analogues prepared by soft lithography, Adv. Mater. 19, 2213.
Chapter 4 Natural Antifoulants for Antifouling Surfaces 4.1
Introduction
Naturally formed sea products are an underlying source to extract antifouling agents. As per the U.S. Navy Program, the composite with EC50 < 25 μg/ml can be a prospective antifouling agent (EC50 expresses the concentration for half of the maximum effect). Over the past few decades, masses of naturally formed compounds have been discovered [1] and tested, and the quantity of new naturally-formed antifouling agents increases annually. The chemistry constituents and architectures of the aforesaid naturally-formed antifouling agents can offer illumination for developing new oceanic anti-biofouling and medical anti-biofouling coatings. Nevertheless, the massive collection of natural species might damage the ecosystem, and the abstraction procedures are intricate and expensive, which impedes their business prospects. Synthetical analogs are remarkably promising when dealing with the aforesaid challenges. Although many natural antifoulants have been isolated and tested, the molecular antifouling mechanisms of these antifoulants are insufficient at present [2]. The study of molecular antifouling mechanisms is not a top priority for the marine coating industry because it takes a lot of money and time. The top priorities for the ship coating industry are cost-effectiveness and quick returns; hence, finding novel high-efficiency antifouling agents tops the agenda.
4.2
Antifoulants from Marine Organisms
Naturally formed products or isolates with anti-biofouling properties have been discovered from oceanic invertebrates (like sponges, corals, ascidians, mussels, and bryozoans), marine plants (e.g., seaweeds, seagrasses, and mangroves), and marine microorganisms (bacteria and diatoms). These natural compounds include fatty acids, lactones, terpenes, steroids, benzenoids, phenyl ethers, polyketides, alkaloids, nucleosides, peptides, and enzymes [3]. Several of these compounds have shown DOI: 10.1051/978-2-7598-2941-5.c004 © Science Press, EDP Sciences, 2023
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antifouling activities against bacteria, diatoms, barnacles, bryozoans, and tube worms. However, many studies reported that the antifouling activity of a single compound is limited. Zhang et al. researched 12 membrane diterpenes from the soft coral Sarcophyton glaucum [4]. The architectures of the substances were presented in figure 4.1. The microbe-resisting attribute of the aforesaid substances was evaluated against gram-negative and gram-positive bacteria, and negative outcomes were acquired. Nevertheless, substances 2 and 5 presented antilarval attachment properties, and substances 10–12 presented potent antifouling capability against barnacle Balanus Amphitrite. The aforesaid outcomes revealed that not one substance displayed a broad-spectrum antifouling capability. A similar discovery was made by other scholars [5, 6]. Wang et al. [5] evaluated the antifouling capability of substances 1–7 against the bryozoan Bugula neritina and the barnacle Balanus albicostatus. Among these substances, merely substances 1, 3, 4, and 6 realized EC50 lower than 50 μg/ml against barnacle attachment, and not one substance exhibited antifouling capability against both biofouling organisms. Apart from corals, organic isolates from sponges exhibited antifouling capability [7]. The outcomes coincided with the results of the coral; namely, not one extract was bioactive in every assay, and many were valid against 1 biofouling species, whereas they displayed few or no activities against other species.
FIG. 4.1 – Structures of compounds from soft coral Sarcophyton glaucum (Reproduced with
permission from [4], Org. Chem. Front., 2019, 6, 2004. Copyright © 2019 The Royal Society of Chemistry).
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In 1994, Nys et al. explored the antifouling activity of several secondary metabolites of the red alga Delisea pulchra (Greville) Montagne. The secondary metabolites showed antifouling ability against marine bacteria (strain SW 8), the macroalga Ulva lactuca Linnaeus, as well as barnacle Balanus Amphitrite amphitirite Darwin. Nevertheless, consistent with extracts from sponges and corals, no single compound was reported to be most active for overall testing processes. Besides red algae, the compounds from brown algae [8] and green algae [9] did not show broad-spectrum antifouling performance, thereby challenging the relevant uses. Among the natural antifoulants from marine organisms, products produced by microorganisms has a promising future. Marine microorganisms are abundant in the ocean and can breed fast; these advantages can provide sufficient samples for researchers to study their antifouling behaviors. Natural products produced by marine bacteria and diatoms are capable of suppressing biofilm from being formed [10], so they are likely to act as marine antifoulants. Song et al. have recently explored the activities of components from coral symbiotical microbe extract against the forming of biological films [11]. The substance (V. alginolyticus 12) exhibits a remarkable decrease effect of biological films at 10 μg/ml. Viju et al. explored the antifouling capability of isolates from a symbiotical oceanic microbe Bacillus subtilis MUT: M15 related to the cuttlefish Sepia sp. [12]. The exocellular extract realized 42.48% inhibition of biological films, whereas the endocellular extract realized 35.62% inhibition of biological films. In oceanic in-situ experiments, coatings fabricated from the isolates were immersed in the sea for 100 days. The aforesaid coatings were valid against barnacles, tube worms, gastropods, and bivalves. Fungi have been discovered to generate antifouling constituents [13]. Bovia et al. assessed the antifouling capability of 7 substances from the sponge-originated fungus Eurotium chevalieri MUT 2316 (figure 4.2a) [14]. The antifouling capability of the substances was evaluated against oceanic microbes and microalgae. The outcomes presented by figure 4.2b revealed that these 7 substances had various selectivity for biofouling organisms. The study reveals that the substance cyclo-L-Trp-L-Ala (7)
FIG. 4.2 – (a) Compounds from sponge-derived fungus Eurotium chevalieri MUT 2316; (b) The anti-biofouling capability of the substances were evaluated against oceanic microbes and algae (Reproduced with permission from [14], Mar. Biotechnol., 2019, 1. Copyright © 2019 Springer Nature).
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was a most promising antifouling agent against algae. The Low observable effect concentration (LOEC) of cyclo-L-Trp-L-Ala is 0.001 μg/ml, displaying that it exhibits a remarkable suppressive effect. Zhang et al. explored 176 substances from fungi in mangrove sediments in a largescale assay to determine biology-based antifouling constituents from microbes [15]. The antifouling capability was assessed against oceanic microbes (Loktanella hongkongensis, Micrococcus luteus, and Pseudoalteromonas piscida) and macro-foulers (bryozoan Bugula neritina and barnacle Balanus amphitrite). About 40% of substances displayed remarkable anti-biofouling capability, and 17 fungal extracts displayed potent and broad-spectrum antifouling capability, which revealed that the aforesaid substances had underlying application significance.
4.3
Antifoulants from Terrestrial Plants
Several terrestrial organisms release allelochemicals in their surroundings to inhibit the growth of other species. These allelochemicals include alkaloids, flavonoids, lignans, terpenoids, phenolic acids, and stilbenes. Feng et al. [16] investigated the antifouling activities of 18 alkaloids derived from terrestrial plants. The results showed that 4 of 18 alkaloids could prevent the settlement of B. neritina (EC50 = 6.18 43.11 μm), and 15 of 18 alkaloids could inhibit the settlement of B. albicostatus (EC50 = 1.18 67.58 μm). Among these compounds, the alkaloid capsaicin ((8-methyl-N-vanillyl-6-nonenamide)) has attracted great interest in recent years. Capsaicin exhibits prominent fouling-resisting activities, excellent degradability, and relatively low toxicity to the environment [17]. Since the discovery of anti-biofouling coatings involving capsaicin in 1995 [18], it’s been considered one of the most prospective anti-biofouling antifouling agents. Organic coatings are at present a hot spot for research on antifouling capability; capsaicin has been utilized to reinforce anti-biofouling capability, e.g., a microbe-resisting acrylate polymeric compound modified via capsaicin displayed remarkable microbe-resisting capability [19]. Likewise, an investigation was conducted on the process of incorporating capsaicin inside silicone coatings [20]. Nevertheless, as impacted by the rapid capsaicin leaching, fouling-resisting activity showed the only temporary property. Hence, recent technological breakthrough focuses on nonleaking techniques, including “polystyrene-block-poly-capsaicin-CoFe2O4” [21] and “in-situ polymerization-blending” [22]. The former complied with polystyrene-block-poly (PSDV) under the mixing with capsaicin bonded to CoFe2O4/ gelatin magnetic nanoscale particles (MNPs) (figure 4.3). The capsaicin leakage received the blocking based on the chemical bonds by using CoFe2O4/gelatin nanoscale spheres. In the tests against Navicula subminuscula, a comparison was drawn for the performance exhibited by five distinct surfaces, i.e., PSDV/FeCap (Capsaicin bonded to CoFe2O4/gelatin MNPs), PSDV/MNPs, PSDV, Polystyrene-block-poly-block-polystyrene (SEBS); glass. Figure 4.4 presents various surfaces’ optical images when the attachment testing processes. PSDV/FeCap showed the optimal fouling-resisting ability against Navicula subminuscula. The “in-situ polymerization-blending” was used to prepare capsaicin-containing
Natural Antifoulants for Antifouling Surfaces
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FIG. 4.3 – Preparation of antifouling coating with non-leaching capsaicin (Reproduced with permission from [21], ACS Appl. Mater. Interfaces, 2018, 10, 9718. Copyright © 2018 American Chemical Society). polysulfone membranes [22], in which the capsaicin derivative containing two carbon– carbon double bonds (N-(2-hydroxyl-3-methyl acrylamide-4,6-dimethyl benzyl) acrylamide, (HMDA)). The carbon–carbon double bonds promote the self-polymerization of HMDA, leading the capsaicin to be stably anchored on the coatings. Nevertheless, long-term and marine field tests are still required to confirm the potential of the mentioned novel fouling-resisting coatings.
4.4
Synthetic Analogues
Collecting antifouling agents from naturally formed substances might exert an unfavorable influence on the survival of source species. Hence, obtaining the aforesaid substances by fostering microorganisms and planted plants is an environmentally friendly approach. In addition, the antifouling capability of naturally formed antifouling substances might not be as satisfactory as anticipated. For that reason, chemistry synthesis is an underlying practical approach for commercialisation. Substantial composites have been synthesised and examined at present, like dihydrostilbenes [23], indole derivates [24], sulfated composites [25], oligo (ethylene glycol) catecholates [26], and capsaicin analogs [27]. The aforesaid synthesised composites are green, low-cost, and efficient, the commercialisation of which is prospective.
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FIG. 4.4 – Evaluation of antifouling activity of different coatings (Reproduced with per-
mission from [21], ACS Appl. Mater. Interfaces, 2018, 10, 9718. Copyright © 2018 American Chemical Society).
4.4.1
Dihydrostilbenes
Dihydrostilbenes are substances abstracted from land plants [28], sponges [29], and macroalgae [30]. The aforesaid substances, called allelopathic plant chemicals, can spread into the environment to suppress their overgrowth and the excessive growth of other organisms; hence, such competitive activity promotes their survival. Defensive behavior offers probabilities to fight against biological fouling through nontoxic and invertible causal links. Batatasin-III is one of the dihydrostilbenes abstracted from the evergreen dwarf shrub Empetrum nigrum (crowberry) (figure 4.5a and b). On the foundation of such substance, Moodie et al. [23] synthesised 22 dihydrostilbenes with various substitution patterns and explored the antifouling capability against microbes, balanide, and ascidian. The outcomes revealed that certainly synthesised dihydrostilbenes displayed remarkable
Natural Antifoulants for Antifouling Surfaces
43
antifouling capability. Especially, 3,5-dimethoxybibenzyl, 3,4-dimethoxybibenzyl, and 3-hydroxy-3’,4,5’-trimethoxybibenzyl displayed superior antifouling capability in contrast to commercially available antifouling agent Sea-nineTM. Substantial naturally formed antifouling substances have been discovered to have oxime functionality (C = NOH), like the antifouling constituents from the Arctic sponge Stryphnus fortis (figure 4.5c). The combination of Batatasin-III with oxime is another approach to synthesising compound antifouling substances (figure 4.5d). In diatom adhesion, massive substances displayed remarkable anti-biofouling capability [31].
FIG. 4.5 – (a) Photo of the crowberry; (b) Chemical structure of Batatasin-III (Reproduced with permission from [23], J. Nat. Prod., 2017, 80, 2001. Copyright © 2017 The American Chemical Society and American Society of Pharmacognosy); (c) Photo of the Arctic sponge Stryphnus fortis; (d) An example of Batatasin-III and oxime hybrids (Reproduced with permission from [31], Mar. Biotechnol., 2018, 20, 257. Copyright © 2018 Springer Nature).
4.4.2
Capsaicin Analogs
Capsaicin analogs have aroused remarkable academic interest recently because of their excellent anti-biofouling capability against biofouling species in the oceanic in-situ experiment [32]. Capsaicin is capable of killing microbes via surface contact [27]; hence it’s capable of fighting against biological fouling directly. Scholars discovered that the antifouling capability of capsaicin analogs was associated with pungency levels, which were identified via their chemistry architectures [27]. Peng et al. [33] examined the anti-biofouling capability of capsaicin analogs via shallow sea buoyant raft hung-plate assay. Posterior to the 9-month assay, the outcomes revealed that merely 0.1% capsaicin analog displayed satisfactory antifouling capability. Yan et al. [34] synthesised 3 capsaicin derivates (HMOBA, BMA, and HMMBA). They assessed the antifouling capability in the Qingdao Sea for 186 d; these 3 capsaicin derivates exhibited remarkable anti-biofouling capability. Nevertheless, their research displayed that the anti-biofouling capability attenuated during the long-term assay in the sea [35]. These outcomes reveal that it’s difficult to maintain the validity of capsaicin’s antifouling capability.
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4.4.3
Indole Derivatives
Recently, an extensive investigation was conducted for the antifouling performance exhibited by indole derivatives originating from organisms relating to the sea [36]. Meantime, their analogs received the synthesis and the test. The analogs under the modification were partially reported to exhibit more significant antifouling activity as compared with the natural compounds [37]. Furthermore, some indole derivatives were capable of inhibiting >90% of diatoms and bacteria [38]. The mentioned prominent bacteria-destroying and algal-resisting activities exhibit promising uses under real conditions. On the whole, the inhibiting influence exerted by indole derivatives on the algal is assumed to be attributed to Ca2+ efflux [39]. To be specific, the Ca2+ balance in algal cells was subject to disruption by indole derivatives, and subsequently, the algae growing process and adhesion were suppressed [24]. For the mentioned reason, the bacteria-destroying mechanism has an association with the functionally-related groups of indole derivatives. Furthermore, indole derivatives were reported to exhibit various fouling-resisting activities against a range of bacteria cells for the distinctions within cell walls [40].
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[32] Wang J., Gao X., Wang Q., Sun H., Wang X., Gao C. (2015) Enhanced biofouling resistance of polyethersulfone membrane surface modified with capsaicin derivative and itaconic acid, Appl. Surf. Sci. 356, 467. [33] Peng B.X., Peng Z.H., Zhou S.Z., Wang F.Q., Ji Y.L., Ye Z.J., Zhou X.F., Tong L. (2012) Studies on the synthesis, pungency and anti-biofouling performance of capsaicin analogues, Sci. China. Chem. 55, 435. [34] YAN X.-F., YU L.-M., JIANG X.-H. (2013) Synthesis of acrylamides containing capsaicin derivative and their bacteriostatic activity and antifouling capability, Period. Ocean. Univ. China 43, 64. [35] Wu G., Jiang X., Yu L., Xia S., Yu X. (2015) Synthesis and quantum chemical calculation of benzamide derivatives containing capsaicin and their bacteriostatic and antifouling properties, J. Chin. Chem. Soc-Taip 62, 861. [36] Wang X., Huang Y., Sheng Y., Su P., Qiu Y., Ke C., Feng D. (2017) Antifouling activity towards mussel by small-molecule compounds from a strain of Vibrio alginolyticus bacterium associated with sea anemone Haliplanella sp, J. Microbiol. Biotechnol. 27, 460. [37] Majik M.S., Rodrigues C., Mascarenhas S., D’Souza L. (2014) Design and synthesis of marine natural product-based 1H-indole-2,3-dione scaffold as a new antifouling/antibacterial agent against fouling bacteria, Bioorg. Chem. 54, 89. [38] Feng K., Ni C., Yu L., Zhou W., Li X. (2019) Synthesis and evaluation of acrylate resins suspending indole derivative structure in the side chain for marine antifouling, Colloid Surface B 184, 110518. [39] Yang C., Yu Y., Sun W., Xia C. (2014) Indole derivatives inhibited the formation of bacterial biofilm and modulated Ca2+ efflux in diatom, Mar. Pollut. Bull. 88, 62. [40] Yusof N.A.A., Zain N.M., Pauzi N. (2019) Synthesis of ZnO nanoparticles with chitosan as stabilizing agent and their antibacterial properties against Gram-positive and Gram-negative bacteria, Int. J. Biol. Macromol. 124, 1132.
Chapter 5 Other Nature-Inspired Marine Antifouling Surfaces 5.1
Introduction
Besides textured surfaces and natural antifoulants, a number of organisms have evolved special antifouling strategies. The mentioned consist of hydrogel surfaces under the exemplification of fish epidermal mucus, slippery surfaces under the exemplification of Nepenthes pitcher plants, the elastic surface under the exemplification of dolphins, soft polyps under the exemplification of soft corals, and desquamation surfaces under the exemplification by corals and dolphins. The mentioned antifouling strategies exhibit high efficiency, non-toxicity, and environmental-friendly property, demonstrating their promising marine uses. Nevertheless, research on some of the antifouling strategies has been rarely conducted. Besides this, novel methods and materials are considered to be designed more progressively for mimicking the mentioned antifouling strategies. In the present section, the mentioned special bioinspired antifouling strategies and a number of recent researches by the group of the authors are presented.
5.2 5.2.1
Natural Hydrogel-Inspired Antifouling Surfaces Introduction
Fish skin mucus is critical to resist fouling organisms. The mucus exhibits hydrophilic and soft characteristics while forming gel properties in the water, complying with hydrogel. Hydrogel contains 3D polymer networks that are cross-linked, and capable of absorbing considerable water. The mentioned hydration layer promotes a physical barrier to be formed to fouling organisms. Thus, broad research on the roles of hydrogel coatings in marine fouling-resisting uses was conducted. DOI: 10.1051/978-2-7598-2941-5.c005 © Science Press, EDP Sciences, 2023
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For instance, Rasmussen et al. [1] determined the roles of a wide range of gels to destroy the adhesion of bacteria and diatom relating to the sea. According to the mentioned results, all gels suppressed barnacle settlement in comparison with the polystyrene controls. Ekblad et al. [2] created a thin protein-resistant poly (ethylene glycol) (PEG)-based hydrogel coating to combat biological fouling. The coating was fabricated by free-radical polymerization on the silanized glass. The coatings exhibited prominent stableness when immersed in artificial seawater for six months, as well as showing significant fouling-resisting activities against marine bacteria, diatoms, algal zoospores, and barnacle larvae. Furthermore, the broad-spectrum influence exerted by the coating was suggested from the results. Nevertheless, the fabricating method is sophisticated, increasing its unsuitability for complicated geometries or wide areas.
5.2.2
Current Hydrogels for Marine Antifouling
5.2.2.1
Tough Hydrogels
The weak mechanically-related characteristics exhibited by hydrogel restrict its uses relating to the sea. A wide range of strategic procedures was recently designed for enhancing hydrogel’s mechanically-related strength and the relevant fouling-resisting performance. These strategies include interpenetrating and double networks, slide ring polymer hydrogels, topological hydrogels, ionically cross-linked copolymers, nanocomposite polymer hydrogels, and self-assembled micro composite hydrogels. For example, Jiang et al. [3] found a wide range of mixed-charge hydrogels by complying with the double-network (DN) rule (figure 5.1a). The hydrogels received the preparation according to a range of rates of [2-(meth-acryloyloxy) ethyl] trimethylammonium (TMA) and 3-sulfopropyl methacrylate (SA). The hydrogel containing equivalent SA and TMA amounts showed optimal protein resistance. Moreover, as revealed from the results, hydrogels (DN-0-10, DN-3-7, and DN-5-5) charged in a negative manner exhibited more significant fouling-resisting activity against algae in comparison with hydrogels charged in a positive manner (DN-10-0 and DN-7-3) (figure 5.1b). Furthermore, the hydrogels displayed improved mechanically-related strength, which shows its promising uses relating to the sea. Likewise, Wu et al. [4] conducted the preparation of a hydrogel coating with improved mechanically-related strength and thermally-related stableness, and this hydrogel showed independently peeling and independently generating characteristics as well. As revealed from the marine testing process in seawater, the coatings exhibited prominent fouling-resisting performance.
5.2.2.2
Hydrogel Brushes
The hydrogel under the modification with poly brushes is another effective fouling-resisting strategic procedure. The fouling organisms cannot adhere tightly to the brushes, thereby enhancing the fouling-resisting performance exhibited by the
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FIG. 5.1 – (a) Schematic illustration of preparing DN hydrogels; (b) Anti-algae test results with Chlorella and Phaeodactylum tricornutum as fouling organisms (Adapted with permission from [3], RSC Adv., 2016, 6, 47349. Copyright © 2016 The Royal Society of Chemistry).
hydrogel. Nevertheless, the previous studies primarily placed stress on medical fouling-resisting uses. To date, their marine antifouling applications are still rarely reported. Several recent reports confirmed their potential for marine antifouling applications. For example, Wang et al. [5] and Zhang et al. [6] found the hydrogels containing brushes to indicate their fouling-resisting activities relating to the sea. According to Wang et al., hydrogel brushes received the grafting process from the surface of stainless steel (SS) (green substrate in figure 5.2a). The brushes received the preparation with the use of the atom transfer radical polymerization (SI-ATRP) initiated from surfaces, belonging to 2-methacryloyloxyethyl phosphorylcholine (MPC) and poly (ethylene glycol) methyl ether methacrylate (PEGMA), separately, under a range of crosslinker fractions in the feed. According to the bacteria-destroying tests, the SS surface exhibiting the coating by using hydrogel brushes showed prominent fouling-resisting performance in comparison with pristine SS (figure 5.2b). In addition, the hydrogel coatings showed significant inhibition to the settlement of barnacle cyprids. The prominent properties of the mentioned hydrogel coatings suggested their promising applications.
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FIG. 5.2 – (a) Preparation of polymer brushes on stainless steel (SS) surfaces; (b) Antibacterial test results (Adapted with permission from [5], Appl. Surf. Sci., 2016, 382, 202. Copyright © 2016 Elsevier B.V.).
5.2.2.3
Hydrogel Composites
Recently, Guo et al. [7] have proposed a novel synthetic orthosilicic acid analog (SOSA) incorporated aquagel (figure 5.3a). The SOSA complied with orthosilicic acid, which is important for diatoms to establish their SiO2 cell walls. As diatoms can’t tell the difference between SOSA and orthosilicic aid, the relevant activity will be inhibited if they ingest SOSA. The SOSA aquagel displayed remarkable anti-diatom adherence against Navicula (figure 5.3b) and Nitzschia closteriums (figure 5.3c). Moreover, the outcomes revealed that the diatom-resisting effect merely occurred when diatoms tried to attach to surfaces. Such a new strategy offers illumination for designing oceanic antifouling coatings. Nano-materials have aroused remarkable academic interest in recent years because of their splendid performances. For that reason, scholars have designed diverse aquagels with various nanofillers, like nano copper oxide [8], silver nanoparticles [9, 10], spheric cuprous oxide–tannic acid submicron particles [11], and nano silicon dioxide [12], and so on. The aforesaid nanofillers can remarkably uplift the mechanical intensity and antifouling capability of aquagels. Tian et al. [9] designed a mixed silicone-based antifouling coating combining several antifouling features of aquagel, nanoparticles, and silicone (figure 5.4a). The coating displayed remarkable antifouling capability against microbes and algae. Amongst the fabricated compound coatings, the SH-0.25-1.5 specimen eliminated nearly 100% E. coli. Besides Ag nanofillers, Cu2O nanoparticles are also widely used in fouling-resisting materials. Lin et al. [11] prepared a hydrogel with Cu2O nanofillers to improve its mechanical properties and fouling-resisting performance. The nanofillers received the incorporated within PVA hydrogels through a freeze–thaw process (figure 5.4b), a low-cost and simple method. The low copper release rates are capable of exhibiting a durable activity against fouling organisms, as well as minimizing environmental influence.
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FIG. 5.3 – (a) Schematic illustration of preparing SOSA hydrogel and the anti-diatom mechanism; (b) Diatom adhesion test against Navicula; (c) Diatom adhesion test against Nitzschia Closterium (Reproduced with permission from [7], J. Mater. Chem. A, 2018, 6, 19125. Copyright © 2018 The Royal Society of Chemistry.
FIG. 5.4 – (a) Schematic illustration of the formation of hybrid coatings (Reproduced with permission from [9], Chem. Eng. J., 2019, 370, 1. Copyright © 2019 Elsevier B.V.); (b) Schematic illustration of preparing Cu2O-TAPVA composite hydrogels by a freeze–thaw process (Reproduced with permission from [11], J. Colloid Interface Sci., 2019, 535, 491. Copyright © 2019 Elsevier B.V.).
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5.3 5.3.1
Slippery Liquid-Infused Porous Surfaces (SLIPS) Natural SLIPS
Pitcher plants refer to one type of carnivorous plant capable of capturing prey by complying with a slippery liquid film on their peristomes. ‘Slippery surface’ shows the conceptual and physical difference with the lotus influence, comprising a lubricating fluid surface under an infusion, maintaining a significantly low contact angle hysteretic phenomenon. The mentioned characteristics lead to the prevention of water and oil droplets from adhering to the surface, so slippery surfaces have an obviously independent cleaning ability. The mentioned characteristic is reported in humans’ microscale-configuration gastrointestinal tract. The gastrointestinal tract receives the covering by using a liquid mucus layer, thereby protecting the tissue from being adhered to by bacteria. Likewise, earthworms can pass via soil with no resistance or dirt pickup through the lubrication of their skin. The texturing-based skin’s mucus layer of the earthworm leads to the formation of a slippery surface which endows the surface with a prominent fouling-resisting ability. On the whole, a slippery surface comprises microscale structures and lubricating liquid, capable of being identified in the pitcher peristome (figure 5.5a). Figure 5.5b shows the fabrication of a typical SLIPS surface; the lubricating liquid was locked within a micro/nano-porous substrate, forming a liquid layer. This SLIPS has extreme liquid repellency as signified by a very low sliding angle (figure 5.5c). Moreover, the increased interfacial slippage induced by the lubricants leads to a reduction of the adhesion strength of marine organisms. The mentioned properties provide the SLIPS with a prominent fouling-resisting ability.
5.3.2
SLIPS for Antifouling
Epsteina et al. researched SLIPS on the foundation of PTFE membranes [15] and assessed the antifouling capability. A mean 99.6% decrease in biological films on SLIPS was recorded in contrast to the PTFE. Similarly, the SLIPS membranes displayed remarkable antifouling capability against Staphylococcus aureus (S. aureus) and E. coli. The elimination of S. aureus and E. coli in contrast to PTFE was 97.2% and 96%, separately. Such a remarkable antifouling capability of SLIPS makes its commercialization perspective. For the sake of validating the antifouling capability of SLIPS in the sea, Amini et al. [16] contrasted 3 substances: (i) PDMS polymeric net with silicone oil infusion (i-PDMS), (ii) a commercially available antifouling coating Intersleek900 (IS900), and (iii) pristine PDMS. The aforesaid coatings were submerged in Scituate Harbor, America, and the surface was analyzed 8 days and 16 days later. i-PDMS displayed superior antifouling capability in contrast to the commercially available IS900, hence, the application of SLIPS is prospective.
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FIG. 5.5 – (a) Images of the pitcher of N. alata and microstructures on its peristome surface
(Reproduced with permission from [13], Nature, 2016, 532, 85. Copyright © 2016 Springer Nature); (b) Preparation of SLIPS; (c) Optical micrographs of hexane sliding on a SLIPS at a low angle (α = 3°) (Reproduced with permission from [14], Nature, 2011, 477, 443. Copyright © 2011 Springer Nature).
In terms of uses relating to the sea, it is necessary to have SLIPS with long-term stableness. Nonetheless, the outcomes from Keller et al. [17] were discouraging, and the lubricants were practically lost posterior to 7 days due to the shear stress of water flow. A slippery surface that is stable is currently necessary to achieve actual uses. Wong et al. [14] and Preston et al. [18] put forward several basic rules for constructing stable slippery surfaces. However, the mentioned rules within production are hard to satisfy [19]. Zhao et al. [20, 21] have discovered an earthworm inspired self-replenishment lubricant polymeric coating capable of dealing with the aforesaid challenge. This coating had a textured surface, and lubricants were preserved in droplets in a polymeric substrate (figure 5.6a). When the original oil tier was removed, more oil was directly released to cover surfaces under ambient pressure. The coating displayed remarkable antifouling capability in a sticky soil milieu.
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FIG. 5.6 – (a) Illustration of the synthesis method, and causal link of self-replenishment lubricant (Reproduced with permission from [20], Adv. Mater., 2018, 30, 1802141. Copyright © 2018 John Wiley and Sons); (b) Self-repair and anti-biofouling causal link of SABFPs (Reproduced with permission from [22], Colloid Surface A, 2019, 582, 123865. Copyright © 2019 Elsevier B.V.)
From a theoretical perspective, such a coating should exhibit antifouling capability in the sea as well. For the sake of exploring the antifouling capability of lubricant surfaces, Li et al. [22] fabricated a self-repair acrylate-boron-fluorinated polymeric coating. The self-repair surface (figure 5.6b) had an alike causal link as the earth worm-mimicking coating. A 60-day sea test in the Bohai Sea unveiled that the lubricant surface displayed remarkable antifouling capability in contrast to the controls. Such an excellent coating method may arouse mounting academic interest in the future. Apart from the aforesaid approaches, the nano wall-enclosed structure with lubricant infusion could remarkably sustain stability. The partition architecture that is independent improves the anchoring influence on the oil phase, thereby enhancing the stableness [23]. However, the stableness exhibited by the mentioned surfaces in long-term environments relating to the sea requires in-depth research. To sum up, the stableness exhibited by SLIPS remains challenging, and more effort should be given.
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Bioinspired Dynamic Surfaces
5.4.1
Renewable Surfaces
5.4.1.1
Natural Renewable Surfaces
In nature, several creatures have developed the ability to slough off their fouled outer layers to maintain a clean surface. Such antifouling strategies have been found in many creatures, including algae [24–28], dolphins [29], pilot whales [30], and corals [31]. For example, corals can release mucous sheets and slough off them to clear their surfaces. Figure 5.7a and b provide evidence that a colony of coral repeats mucous sheet formation and sloughing process. For this reason, the skin of the mentioned marine organisms has a renewable surface, whereas such a surface helps combat biological fouling. The mechanism of sacrificial coatings, self-polishing, and degradable copolymers show a consistency with the epithelium shedding influence, in other words, the coating surface achieves continuous independent renewal, which can remove fouling organisms accordingly.
5.4.1.2
Variable Viscosity Materials
The viscosity of several types of materials can increase when they exposure to seawater. The changes in viscosity lead to continuous self-shedding and chemical dissolution, which help surfaces to resist biofouling. This idea was confirmed by researchers by using viscoelastic surfactant (VES) and acid gelling agent (AGA) as antifouling coatings [30]. By adjusting the ratio of the two mentioned materials, composites consisting of 3% AGA and 97% VES showed a rapid increase in viscosity and an appropriate life span in aqueous environments. As indicated from the fouling-resisting tests (figure 5.7c and d), the diffusing element under the protection by the coating exhibited noticeably enhanced fouling-resisting performance in comparison with the metal surface without any protection.
5.4.1.3
Degradable Acrylic Copolymers
Acrylic copolymers that involve hydrolysable pendant groups (e.g., zinc or copper acrylate polymer and silyl acrylate [32]), receive the development and application in uses relating to the sea. For instance, an indole derivative (N-(1H-2-phenyl-indole-3-ylmethyl) acrylamide, NPI) has received the synthesis and the introduction to acrylate resins as side chains [33]. As impacted by the indole moiety’s inherent fouling-resisting activity and acrylate resins’ independently polishing properties, the copolymers showed obvious foulingresisting characteristics. The mentioned were confirmed by marine testing for three months. The side chains of co-polymers are quite vital for antifouling capability. Searching new side chain substances can reveal new valid antifouling coatings. Recently, Li et al. [34] have synthesized a self-replenishing acrylate boron polymer
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FIG. 5.7 – (a) Red alga Dilsea carnosa displays a quite clean surface in contrast to the environment; (b) Proof for cuticle peeling by the red alga (Reproduced with permission from [45], Mar. Ecol. Prog. Ser., 2005, 299, 111. Copyright © 2005 Inter-Research Science Publisher); (c) Diffuser protected with sacrificial skin; (d) Unprotected diffuser (Reproduced with permission from [30], Smart Mater. Struct., 2009, 18, 104027. Copyright © 2009 IOP Publishing).
via pyridine-diphenylborane as side chains (figure 5.8a). The hydrolytic action of pendant groups induces satisfactory antifouling capability against diatoms in the lab and marine environment. Nonetheless, independent polishing of the aforesaid acrylic co-polymers is restricted because they display a non-reactive major chain [35]. To tackle the aforesaid issue, Ma et al. [36, 37] fabricated the co-polymer of acrylate which involved antifouling constituent side groups. The polymer covered a degradable backbone and hydrolysable pendant groups (figure 5.8b). As presented by the outcomes, the degradable and antifouling capability could be modulated by polymeric constituents of the pendant groups and main chains.
5.4.1.4
Degradable Polyurethane Copolymers
Cross-linkable degradable polyurethane (PU) coatings have prominent low-temperature flexibility, toughness, and abrasion resistance, so they receive an extensive application to be a fouling-resisting backbone that is degradable [38, 39]. Researchers have conducted the preparation of various degradable polyurethane
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FIG. 5.8 – (a) Self-renew acrylate boron polymers with pyridine-diphenylborane side chains, and their anti-biofouling procedure (Reproduced with permission from [34], New J. Chem., 2018, 42, 19908. Copyright © 2018 The Royal Society of Chemistry and the Centre National de la Recherche Scientifique); (b) Anti-biofouling causal link of co-polymer of acrylate with antifouling agent side groups (Reproduced with permission from [36], Ind. Eng. Chem. Res., 2015, 54, 9559. Copyright © 2015 American Chemical Society).
coatings and studied their potential in fouling-resisting uses relating to the sea. The results of the marine field test meet the relevant requirements and are considered to be promising. Similar to acrylic copolymers, the degradation rate of PU is hard to control. Hence, recent studies focus on the pendant groups of PU to obtain an optimal degradation rate and antifouling capability. These pendant groups include ε-caprolactone (CL)/glycolide (GA) [40], poly (ε-caprolactone) (PCL) [41], poly (propylene carbonate) (PPC) [42]. Apart from the above methods, star-shaped polyester polyols [43] and PU with nanofillers (e.g., graphene) [44] were confirmed to improve the antifouling capability and duration of PU.
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5.4.2
Unstable Surfaces
5.4.2.1
Actively Deformed Surfaces
Several marine creatures (e.g., soft corals and dolphins) exhibit antifouling fouling resisting ability due to their soft skin [46, 47], which generates an unsteady surface under flow [48]. It’s hard for biofouling species to attach to an unsteady surface. Following such a strategic procedure, a wide range of dynamic surfaces was developed. For example, the electro-active dynamic surface was confirmed to exhibit antifouling capability [49] (figure 5.9a). The electrical field could cause distortion, which facilitated microbial detachment from surfaces. Pneumatic actuation silicon rubbers with unsteady surface display anti-biofouling properties as well (figure 5.9b)
FIG. 5.9 – Illustrations of (a) electro-active dynamic surface (Reproduced with permission from [49], Adv. Mater., 2013, 25, 1430. Copyright © 2013 John Wiley and Sons) and (b) gas-driven silicone elastomers (Reproduced with permission from [50], Biofouling, 2015, 31, 265. Copyright © 2015 Taylor & Francis).
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[50], in which the distortion of the silicon rubbers was modulated through pneumatical actuation. Through regulated surface distortion, over 90% of biological films were detached in the assays. Nonetheless, the aforesaid antifouling coatings need additional power, which might affect the cost-effectiveness.
5.4.2.2
Passively Deformed Surfaces
Actually, as indicated by soft skin, the skin realizes a low elasticity modulus which has been evidenced to facilitate the fight against biofouling [51], hence the soft skin assists in resisting biofouling. Due to the inspiration from dolphin skins, Kramer [52] and Babenko [53] designed compliant coatings fabricated from naturally formed soft rubber and explored the anti-drug property. Similarly, they fabricated soft coatings using silicon rubber (figure 5.10a), and a series of graphene constituents were utilized to uplift the performances [54]. The coatings display diverse Young’s modulus. The studies of Kulik revealed that micro-distortion was identified on flexible surfaces under turbulence. On the foundation of Kulik’s formulas, the distortion of the 4 coatings under turbulence was identified, unveiling that there was micro-distortion. Afterwards, our team determined the distortion on the surfaces, and examined the coatings’ antifouling capabilities; the outcomes were presented in figure 5.10a. The aforesaid outcomes revealed that low modulus induced greater distortion, which fabricated the removal of biofouling species under the successive micro motions on the surface. Collectively, low-modulus coatings exhibit superior antifouling capability. The causal link of such effect was presented in figure 5.10a. In addition, our team investigated the impact of elasticity modulus on antifouling capability via DEM–CFD coupled simulation, and an identical result was acquired [55]. According to the recently performed study by the authors, a novel dynamic surface category was put forward, complying with the inspiration of the soft coral Sarcophyton trocheliophorum [56]. Artificial tentacles received the preparation by using soft silicone rubber with the filler of graphene (figure 5.10b). The surface exhibits a hydrophobic property and exerts an FR influence. Soft coral surfaces receive the covering with numerous soft tentacles, capable of swaying in the water flow. For the mentioned reason, the fouling organism fails to adhere tightly to the soft coral surface due to the surface is not stable. The fouling-resisting performance is prominent. Figure 5.10b also illustrates the fouling-resisting mechanism of this coating, and the fouling-resisting ability of this strategic procedure complies with physical properties and exhibits environmental-friendly and low-cost properties.
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FIG. 5.10 – (a) Antifouling mechanism of elastic surface (Reproduced with permission from
[54], J. Mater. Chem. B, 2019, 7, 488. Copyright © 2019 The Royal Society of Chemistry); (b) i-ii. The soft coral Sarcophyton trocheliophorum and its tentacles; iii. Artificial tentacles based on soft silicone rubber; iv. Antifouling mechanism of soft tentacles (Reproduced with permission from [56], Adv. Mater. Technol., 2019, 4, 1800480. Copyright © 2019 John Wiley and Sons).
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[3] Jiang D., Liu Z., He X., Han J., Wu X. (2016) Polyacrylamide strengthened mixed-charge hydrogels and their applications in resistance to protein adsorption and algae attachment, RSC Adv. 6, 47349. [4] Wu G., Li C.-C., Jiang X.-H., Yu L.-M. (2016) Highly efficient antifouling property based on self-generating hydrogel layer of polyacrylamide coatings, J. Appl. Polym. Sci. 133, 44111. [5] Wang J., Wei J. (2016) Hydrogel brushes grafted from stainless steel via surface-initiated atom transfer radical polymerization for marine antifouling, Appl. Surf. Sci. 382, 202. [6] Zhang R., Zhang L., Tian N., Ma S., Liu Y., Yu B., Pei X., Zhou F. (2017) The Tethered Fibrillar Hydrogels Brushes for Underwater Antifouling, Adv. Mater. Interfaces 4, 1601039. [7] Chen W., Hao D., Guo X., Hao W., Jiang L. (2018) Preventing diatom adhesion using a hydrogel with an orthosilicic acid analog as a deceptive food, J. Mater. Chem. A 6, 19125. [8] Ashraf P.M., Edwin L. (2016) Nano copper oxide incorporated polyethylene glycol hydrogel: An efficient antifouling coating for cage fishing net, Int. Biodeterior. Biodegrad. 115, 39. [9] Tian S., Jiang D., Pu J., Sun X., Li Z., Wu B., Zheng W., Liu W., Liu Z. (2019) A new hybrid silicone-based antifouling coating with nanocomposite hydrogel for durable antifouling properties, Chem. Eng. J. 370, 1. [10] Jiang D., Xue Q., Liu Z., Han J., Wu X. (2017) Novel anti-algal nanocomposite hydrogels based on thiol/acetyl thioester groups chelating with silver nanoparticles, New. J. Chem. 41, 271. [11] Lin X., Huang X., Zeng C., Wang W., Ding C., Xu J., He Q., Guo B. (2019) Poly (vinyl alcohol) hydrogels integrated with cuprous oxide–tannic acid submicroparticles for enhanced mechanical properties and synergetic antibiofouling, J. Colloid Interface Sci. 535, 491. [12] Mohan A., Ashraf P.M. (2019) Biofouling control using nano silicon dioxide reinforced mixed-charged zwitterionic hydrogel in aquaculture cage nets, Langmuir 35, 4328. [13] Chen H., Zhang P., Zhang L., Liu H., Jiang Y., Zhang D., Han Z., Jiang L. (2016) Continuous directional water transport on the peristome surface of Nepenthes alata, Nature 532, 85. [14] Tak-Sing W., Sung Hoon K., Tang S.K.Y., Smythe E.J., Hatton B.D., Alison G., Joanna A. (2011) Bioinspired self-repairing slippery surfaces with pressure-stable omniphobicity, Nature 477, 443. [15] Epstein A.K., Wong T.-S., Belisle R.A., Boggs E.M., Aizenberg J. (2012) Liquid-infused structured surfaces with exceptional anti-biofouling performance, Proc. Natl. Acad. Sci. USA 109, 13182. [16] Amini S., Kolle S., Petrone L., Ahanotu O., Sunny S., Sutanto C.N., Hoon S., Cohen L., Weaver J.C., Aizenberg J. (2017) Preventing mussel adhesion using lubricant-infused materials, Science 357, 668. [17] Keller N., Bruchmann J., Sollich T., Richter C., Thelen R., Kotz F., Schwartz T., Helmer D., Rapp B.E. (2019) Study of biofilm growth on slippery liquid-infused porous surfaces made from fluoropor, ACS Appl. Mater. Interfaces 11, 4480. [18] Preston D.J., Song Y., Lu Z., Antao D.S., Wang E.N. (2017) Design of lubricant infused surfaces, ACS Appl. Mater. Interfaces 9, 42383. [19] Li Z., Guo Z. (2019) Bioinspired surfaces with wettability for antifouling application, Nanoscale 11, 22636. [20] Zhao H., Sun Q., Deng X., Cui J. (2018) Earthworm-inspired rough polymer coatings with self-replenishing lubrication for adaptive friction-reduction and antifouling surfaces, Adv. Mater. 30, 1802141. [21] Cui J., Daniel D., Grinthal A., Lin K., Aizenberg J. (2015) Dynamic polymer systems with self-regulated secretion for the control of surface properties and material healing, Nat. Mater. 14, 790. [22] Li Y., Chen R., Zhang L., Liu Q., Yu J., Liu J., Liu P., Wang J. (2019) Fabrication and antifouling behavior research of self-healing lubricant impregnated films with dynamic surfaces, Colloid Surface A 582, 123865. [23] Ouyang Y., Zhao J., Qiu R., Hu S., Niu H., Zhang Y., Chen M. (2020) Nanowall enclosed architecture infused by lubricant: A bio-inspired strategy for inhibiting bio-adhesion and bio-corrosion on stainless steel, Surf. Coat. Technol. 381, 125143.
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[24] Masaki T., Fujita D., Hagen N. The surface ultrastructure and epithallium shedding of crustose coralline algae in an ‘Isoyake’area of southwestern Hokkaido, Japan. In Proceedings of Eleventh International Seaweed Symposium, pp. 218–223. [25] Fujita D., Masaki T. (1986) The antifouling by shedding of epithallium in articulated coralline algae, Mar. Fouling 6, 1. [26] Gonzalez M.A., Goff L.J. (1989) The red algal epiphytes Microcladia coulteri and M. californica (Rhodophyceae, Ceramiaceae) II. Basiphyte specificity, J. Phycol. 25, 558. [27] Yamamoto K., Endo H., Yoshikawa S., Ohki K., Kamiya M. (2013) Various defense ability of four sargassacean algae against the red algal epiphyte Neosiphonia harveyi in Wakasa Bay, Japan, Aquat. Bot. 105, 11. [28] Borowitzka M.A., Larkum A.W. (1977) Calcification in the green alga Halimeda. I. An ultrastructure study of thallus development, J. Phycol. 13, 6. [29] Nagamine H., Yamahata K., Hagiwara Y., Matsubara R. (2004) Turbulence modification by compliant skin and strata-corneas desquamation of a swimming dolphin, J. Turbul. 5, 1. [30] Ganguli R., Mehrotra V., Dunn B. (2009) Bioinspired living skins for fouling mitigation, Smart Mater. Struct. 18, 104027. [31] Bessell-Browne P., Fisher R., Duckworth A., Jones R. (2017) Mucous sheet production in Porites: an effective bioindicator of sediment related pressures, Ecol. Indic. 77, 276. [32] Kim S.-M., Kim A.Y., Lee I., Park H., Hwang D.-H. (2016) Synthesis and Characterization of Self-Polishing Copolymers Containing a New Zinc Acrylate Monomer, J. Nanosci. Nanotechno. 16, 10903. [33] Feng K., Ni C., Yu L., Zhou W., Li X. (2019) Synthesis and evaluation of acrylate resins suspending indole derivative structure in the side chain for marine antifouling, Colloid Surface B 184, 110518. [34] Li Y., Chen R., Feng Y., Liu L., Sun X., Tang L., Takahashi K., Wang J. (2018) Antifouling behavior of self-renewal acrylate boron polymers with pyridine-diphenylborane side chains, New J. Chem. 42, 19908. [35] Xu W., Ma C., Ma J., Gan T., Zhang G. (2014) Marine biofouling resistance of polyurethane with biodegradation and hydrolyzation, ACS Appl. Mater. Interfaces 6, 4017. [36] Xi Z., Xie Q., Ma C., Chen Z., Zhang G. (2015) Inhibition of Marine Biofouling by Use of Degradable and Hydrolyzable Silyl Acrylate Copolymer, Ind. Eng. Chem. Res. 54, 9559. [37] Dai G., Xie Q., Ma C., Zhang G. (2019) Biodegradable poly (ester-co-acrylate) with antifoulant pendant groups for marine anti-biofouling, ACS Appl. Mater. Interfaces 11, 11947. [38] Chen M., Ou B., Guo Y., Yan G., Kang Y., Liu H., Yan J., Li T. (2018) Preparation of an environmentally friendly antifouling degradable polyurethane coating material based on medium-length fluorinated diols, J. Macromol. Sci. Part A 55, 1. [39] Xu Y., Wang G., Xie Z., Wang A. (2019) Preparation and evaluation of degradable polyurethane with low surface energy for marine antifouling coating, J. Coat. Technol. Res. 16, 1055. [40] Ma C., Xu L., Xu W., Zhang G. (2013) Degradable polyurethane for marine anti-biofouling, J. Mater. Chem. B 1, 3099. [41] Jielin M., Chunfeng M., Guangzhao Z. (2015) Degradable Polymer with Protein Resistance in a Marine Environment, Langmuir 31, 6471. [42] Chen Y., Liu Z., Sheng H., Jin H., Jiang D. (2016) Poly(propylene carbonate) polyurethane self-polishing coating for marine antifouling application, J. Appl. Polym. Sci. 133, 43667. [43] Jie Y., Huang C., Zhuang H., Hui G., Zhang C., Ren R., Ma Y. (2015) Degradable polyurethane based on star-shaped polyester polyols (trimethylolpropane and ɛ-caprolactone) for marine antifouling, Prog. Org. Coat. 87, 161. [44] Ou B., Chen M., Guo Y., Kang Y., Yan G., Zhang S., Yan J., Liu Q., Li D. (2018) Preparation of novel marine antifouling polyurethane coating materials, Polym. Bull. 75, 1. [45] Nylund G., Pavia, H. (2005) Chemical versus mechanical inhibition of fouling in the red alga Dilsea carnosa, Mar. Ecol. Prog. Ser. 299, 111. [46] Kramer M.O. (1960) Boundary layer stabilization by distributed damping, J. Am. Soc. Nav. Eng. 72, 25.
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[47] Stromberg M. (1989) Dermal‐Epidermal Relationships in the Skin of the Bottlenose Dolphin (Tursiops truncates) 1, Anat, Histol, Embryol 18, 1. [48] Tian L., Jin E., Mei H., Ke Q., Li Z., Kui H. (2017) Bio-inspired graphene-enhanced thermally conductive elastic silicone rubber as drag reduction material, J. Bionic Eng. 14, 130. [49] Phanindhar S., Qiming W., Beatriz O., Daniel R., López G.P., Xuanhe Z. (2013) Bioinspired surfaces with dynamic topography for active control of biofouling, Adv. Mater. 25, 1430. [50] Shivapooja P., Wang Q., Szott L.M., Orihuela B., Rittschof D., Zhao X., López G.P. (2015) Dynamic surface deformation of silicone elastomers for management of marine biofouling: laboratory and field studies using pneumatic actuation, Biofouling 31, 265. [51] Jin H., Bing W., Tian, L., Wang, P.; Zhao, J. (2019) Combined Effects of Color and Elastic Modulus on Antifouling Performance: A Study of Graphene Oxide/Silicone Rubber Composite Membranes, Materials 12, 2608. [52] Kramer M.O. (1965) Hydrodynamics of the Dolphin, Adv. Hydrosci. 2, 111. [53] Babenko V.V., Chun H.-H., Lee I. (2012) Boundary layer flow over elastic surfaces: compliant surfaces and combined methods for marine vessel drag reduction; Butterworth-Heinemann. [54] Jin H., Zhang T., Bing W., Dong S., Tian L. (2019) Antifouling performance and mechanism of elastic graphene–silicone rubber composite membranes, J. Mater. Chem. B 7, 488. [55] Tian L., Jin E., Wang J., Wang X., Bing W., Jin H., Zhao J., Ren L. (2019) Exploring the antifouling effect of elastic deformation by DEM–CFD coupling simulation. RSC Adv. 2019, 9, 40855. [56] Bing W., Tian L., Wang Y., Jin H., Ren L., Dong S. (2019) Bio‐inspired non‐bactericidal coating used for antibiofouling, Adv. Mater. Technol. 4, 1800480.
Chapter 6 Bioinspired Medical Surfaces 6.1
6.1.1
Bacterial Infection and Traditional Antibacterial Strategies Antibiotics and Physiological Activity
The discovery of the antibiotic penicillin by Alexander Fleming in 1928 brought a revolutionary change in the field of medicine and made great contributions to the treatment of bacterial infections [1]. Antibiotics refer to a class of secondary metabolites produced by microorganisms or other higher animals or plants. Antibiotics can resist pathogens and interfere with the development of other living cells. However, the continued use of penicillin and similar antibiotics has led to an increase in drug-resistant strains, which has also prompted the demand for alternative therapy. Based on data reported by the Center for Disease Control (CDC), at least 2 million people are infected with antibiotic-resistant bacteria every year [2]. Most notably, there are high threat-resistant strains among several species. Among them, methicillin-resistant Staphylococcus aureus (MRSA) causes about 80 000 infections each year, and drug-resistant Streptococcus pneumoniae causes about 1.2 million infections each year [2]. For patients with high-risk factors of bacterial infection, such as chronic injury, burn, or immune system damage, these drug-resistant bacteria can significantly worsen the prognosis. Bacterial infections are related to human immunity, and the immune system will automatically make a response to remove invading bacteria. Monocytes, macrophages, and neutrophils are the key to resisting bacterial pathogens since these three kinds of cells participate in phagocytosis and eventually eliminate pathogens in the body [3]. In addition, platelets can enhance immune cell response, and it changes the expression of signal molecules, which guide the behavior of neutrophils and monocytes and form an aggregate of platelets, neutrophils, and monocytes. Platelets can bind with bacteria and release antibacterial substances as well [4].
DOI: 10.1051/978-2-7598-2941-5.c006 © Science Press, EDP Sciences, 2023
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Since these mechanisms have been fully used in vivo, it is possible to reproduce this behavior by bionic methods as a new strategy for designing new strategies against antibiotic-resistant bacteria. Therefore, researchers have explored the combination of these antibacterial mechanisms in a variety of applications against antibiotic-resistant bacteria.
6.1.2
Biofilm Infections
Biofilm is the matrix-enclosed microbial accretions that adhere to a solid surface, which is an important growth mode of bacteria. Biofilm adheres to the substrate to form localized clusters making it more resistant to antibiotic therapy, and this phenomenon is similar in both the natural environment and animal hosts. The basic cognition of biofilm formation obtained from environmental research is helpful to study stubborn biofilms attached to medical instrument surfaces and provides insights into biofilm infection [5]. A significant feature of colonization and infection of biofilm and other microorganisms is the presence of microbial communities attached to the surface. The biofilm formation may have a profound impact on the host because the pathogenic microorganisms growing in extracellular polymeric substances (EPS) are more resistant to antibiotics and host defense. Biofilm fundamentally challenges the uniform distribution of infectious agents, which may bring great medical challenges, for example, antibiotic resistance, inflammation, persistence, metastasis, or spread of infectious embolism. Device-associated infection is the first clinical infection identified as having biofilm etiology. Host inflammatory molecules promote the adhesion of microorganisms on the surface of equipment, thus promoting the formation of biofilm. Figure 6.1 shows how bacterial colonization on the surface of artificial implants enters the body. Biomedical devices, such as venous catheters, artificial heart valves, cardiac pacemakers, joint prostheses, and endotracheal intubation, have saved millions of lives, but they all carry an inherent risk of biofilm-related infections. Biofilms associated with medical instrument infection first appeared in the early 1980s, when electron microscopy showed that bacteria deposited on the surface of inherent devices such as venous catheters and cardiac pacemakers [6, 7]. The most common microorganisms associated with medical devices are Staphylococcus (especially Staphylococcus epidermidis and Staphylococcus aureus), followed by Pseudomonas aeruginosa and a large number of other environmental bacteria. These bacteria may infect the host damaged by invasive medical intervention, chemotherapy, or pre-existing disease status. The formation of biofilms on medical implants has even led to a new feature of the infectious disease called chronic polymer-associated infection [8, 9]. Therefore, biofilm formation can be considered as a self-protection strategy of bacteria, which helps to enhance its ability to cause infection.
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FIG. 6.1 – The schematic diagram shows three possible sites for infectious biofilm to enter the body: catheter, hip replacement, and periodontal disease. The arrows show how biofilms (green) are spread around the body through individual cells or protected emboli, such as infective endocarditis of natural or artificial heart valves (Reproduced with permission from [5], Nat. Rev. Microbiol., 2004, 2, 95. Copyright © 2004 Springer Nature).
6.2
Traditional Medical Antibacterial and Antifouling Methods
The discovery of antibiotics is the most important event in the history of modern drugs. It has played a very important role in combating bacterial infection and improving human life. However, the optimism of antibiotic discovery was weakened by the discovery of drug-resistant strains. Nowadays, the common clinical bacteria not only have the characteristics of single drug resistance but also have multiple drug resistance, which is the consequence of antibiotic abuse in the past decades. Drug resistance to microbial pathogens and antimicrobial agents is a growing global
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public health threat [10, 11]. Diseases were once to be controlled by antibiotics, but they are re-emerging as new coalitions of resistance to these therapies. Drug-resistant strains first appeared in hospitals, where the frequency of antibiotic use was high. For example, sulfonamide-resistant Streptoccoccus pyogenes and penicillin-resistant Staphylococcus aureus were first found in hospitals [11, 12]. Driven by the increased use of antibiotics, the frequency of drug resistance in a large number of bacteria has increased. This situation is more evident in developing countries, where antibiotics are available without a prescription. Poor health conditions contribute to transmission and reduced medical budgets, preventing access to new effective but more expensive antibiotics. Since the 1980s, tuberculosis has reappeared, which is usually caused by multidrug resistance (MDR). Due to the severity and refractory nature of multidrug-resistant strains, sometimes six to seven different drugs are required [13].
6.2.1
Causes of Drug Resistance
Drug-resistance genes and their hosts are spread and propagated under continuous antimicrobial selection, thus extending the problem to other hosts and geographical locations. The target of many antibiotics is related to the basic physiological or metabolic function of bacterial cells. Millions of kilograms of antimicrobial agents are used for the human, animal, and agricultural every year [14–16]. Drug resistance is promoted by killing susceptible strains and selecting resistant strains. Drug resistance among bacteria can be transferred, and drug-resistance genes can be transferred between bacteria of different classifications and ecological groups through genetic elements, including phages, naked DNA, plasmids, or transposons, as shown in figure 6.2 [14, 17]. Plasmids and transposons carrying integrons increase the transmission of antibiotic resistance genes between bacteria. Integron can integrate multiple drug resistance genes through site-specific gene recombination, which plays an important role in the formation of bacterial multiple drug resistance. [18]. Integrons were first found in Gram-negative bacteria and have been in Gram-positive symbionts since then. This is a newly discovered repository of these unique genetic elements [19]. A model of drug-resistant gene transmission is the tet (M) tetracycline-resistant gene, which is usually located on transposon Tn916 [20]. It exists in almost all bacteria and has a great risk of transmission. A model of drug-resistant gene transmission is the tet (M) tetracycline-resistant gene, which is usually located on transposon Tn916 [20]. Chromosomal genes can also be transferred, and they are acquired by one bacterium by absorbing naked DNA from another bacteria. This transfer process resulted in penicillin-resistant Streptococcus pneumoniae by obtaining genes from naturally occurring penicillin-resistant symbiotic Streptococcus viridans and forming a penicillin-binding protein [21, 22]. It has been proved from pneumococci that the chromosomal location of the determinants of drug resistance does not prevent its transmission. Bacteria themselves are mobile and can easily spread between people and countries. Drug-resistant pneumococci from Iceland and the United States are from strains that first appeared in Spain [23]. As a result,
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FIG. 6.2 – The genetics and spread of drug resistance. Drug-resistant genes can be transmitted from one bacterium to another by plasmid, phage, naked DNA, or transposon (Reproduced with permission from [10], Nat. Med., 2005, 10, S122. Copyright © 2005 Springer Nature). countries, and citizens around the world have become part of the global microbial ecology, sharing and disseminating the consequences of drug resistance. Resistance genes are usually targeted at a single family or type of antibiotics, although multiple genes, each with a single resistance characteristic, can be accumulated in the same organism. As revealed in figure 6.3, the mechanisms of drug resistance are diverse. Some of them are targeted at antibiotics, such as beta-lactamases that destroy penicillin and cephalosporins. Modifying enzymes inactivate chloramphenicol and aminoglycosides, such as streptomycin and gentamicin. Targeted transport of other drugs, such as active efflux of drugs, mediates resistance to tetracycline, chloramphenicol, and fluoroquinolones [24, 25]. It can also change the targets of drugs in cells, such as ribosomes, metabolic enzymes, or proteins involved in DNA replication or cell wall synthesis so that drugs cannot inhibit important functions in microbial cells. In the absence of plasmids and transposons, which usually mediate a high level of resistance, bacteria develop resistance from a low level to a high level through sequence mutation of chromosomes [26, 27]. This process is responsible for the initial emergence of penicillin and tetracycline resistance in Neisseria gonorrhoeae. The organism later acquired transposon genes that are highly resistant to these drugs.
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FIG. 6.3 – The biological mechanisms of bacterial resistance, including enzymes against antibiotics, drug efflux mediates drug resistance, and changes the targets of drugs (Reproduced with permission from [10], Nat. Med., 2005, 10, S122. Copyright © 2005 Springer Nature). Escherichia coli and other Enterobacteriaceae strains have evolved to become increasingly resistant to fluoroquinolones, due to mutations in the target enzyme (topoisomerase) and increased expression of membrane proteins that pump drugs out of cells [26, 27]. Chromosomal mutations in Staphylococcus aureus with intermediate resistance to vancomycin first appeared in the response to vancomycin [28], followed by mutants with high levels of resistant transposons from enterococci [29, 30]. A small increase in the minimum inhibitory concentration (MIC) of an antimicrobial agent should alert clinical microbiologists in hospitals and communities to an initial problem of drug resistance. Strains that are less sensitive to drugs may eventually lead to higher levels of resistance, and efforts should be encouraged to change the use of this antimicrobial agent in the environment. Long-term use of an antibiotic will not only make the bacteria resistant to the antibiotic, but also to other kinds of antibiotics [14]. This phenomenon is found in the long-term use of tetracycline in the treatment of urinary tract infections [31] and acne [32]. In animals, the use of tetracycline in feed resulted in multidrug resistance (MDR) [33]. After a few days, tetracycline-resistant E. coli began to appear in chickens; two weeks later, the
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excreted E. coli developed resistance to several antibiotics. This phenomenon reflects the linkage of different resistance genes on the same transposon or plasmid. However, it is not clear why multidrug-resistant plasmids appear after long-term use of single antimicrobial agents. Bacteria that are already resistant to one antibiotic seem to be more likely to obtain additional resistance characteristics from other bacteria sharing the environment. Antibiotic-resistant bacteria may rapidly appear in the host or environment after the use of antibiotics, but they are difficult to disappear even if antibiotics are not selected. This phenomenon reflects the lowest survival cost of new drug-resistant strains. In addition, resistance genes are usually associated with genes on the same plasmid that are resistant to other antimicrobial agents or toxic substances [34]. The existence of MDR plasmids ensures the maintenance of the plasmids, as long as any one of the MDR plasmids provides a survival advantage for the host bacteria. This principle also applies to the determinants of insecticide resistance, such as quaternary ammonium compounds, because bactericide efflux genes can be found on plasmids containing antibiotic resistance genes in S. aureus [35]. Some studies have tracked a decline in resistance rates when antibiotics are removed [36]. The nationwide campaign to reduce the use of macrolides in Finland has led to a significant reversal of macrolide resistance in Streptococcus pyogenes. The substitution of susceptible bacteria is the main reason for the decrease in resistant strains.
6.2.2
Manage and Prevent Drug Resistance
In the face of a shortage of new antimicrobial agents, we must use our existing drugs more carefully. Reducing and improving the use of existing antibiotics can reduce drug resistance and eventually make drugs become an effective treatment again [36]. Proper use of antibiotics not only helps to reverse the high rate of drug resistance but also inhibits the emergence of resistance to newer drugs [36]. The reduction of antibiotic use in intensive care units and other hospitals has proved that the susceptible indigenous strains will regain their niche in the absence of drug selection pressure. However, the process of dealing with multidrug-resistant strains is slow and more difficult. Therefore, it is necessary to change the overuse of antibiotics to affect the existence of multidrug-resistant strains. The continued use of the same drugs in drug-resistant areas should be stopped, and short courses of treatment with highly active antibiotics will also reduce the pressure on multidrug resistance. It is very important to develop new antibiotics, whether to block or evade the mechanism of drug resistance or to attack new targets. These antibiotics will avoid the current resistance mechanism, which may hinder the success of new structurally similar drugs. Another method is to inhibit the key gene products in the process of infection, deeply study the role of gene products in regulating the formation and maintenance of persistent infection, and find the key host molecules or regulatory elements in the formation and maintenance of persistent infection. Since inhibition of these targets will not affect bacterial growth, antagonistic selection can be greatly reduced. The production line for new drugs is small because major pharmaceutical companies have largely abandoned antibiotic research and development [37]. Small
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or start-up companies are addressing this problem, and they can be fully focused on this goal, but will eventually need the support of investors or the large pharmaceutical industry.
6.3
Bioinspired Medical Antibacterial and Antifouling Methods
Bacteria, fungi, and other pathogenic microorganisms often cause pathological changes in body tissues, which seriously threaten the physical and mental health of human beings. Medical antibacterial materials can effectively reduce the risk of disease by blocking or killing pathogenic microorganisms. Infection is one of the main causes of implant failure, especially in orthopedic surgery [38]. Once contaminated by microorganisms, the risk of reinfection around the implant will be doubled, requiring repeated operations and even amputation [39]. At present, antibiotics are still widely used in implant-related infections [40]. However, for many deep tissue regions, limited antibiotic concentrations make it difficult to inhibit invasive pathogens. On the other hand, abuse and overuse of antibiotics will also lead to the drug resistance of bacteria [41]. Compared with anti-bacterial biotics, implant surface modification is a potentially healthier way to reduce infection. Bacterial adhesion to the surface of implants often leads to infection, which leads to surgical failure [42]. Therefore, it is better to modify its surface to improve its antibacterial properties. In the long-term evolution process of natural organisms, they present multiple functions through the joint action of their morphology, structure, and other factors to achieve maximum adaptation to the environment. Through the physicochemical properties and structural morphology of organisms, specific functions, such as drag reduction [43], noise reduction, antifouling [44] and wear resistance, can be formed. The existing bionic functionalization strategies include the use of biomimetic materials to enhance the existing antibacterial strategies. Especially, these strategies attempt to modify existing methods to reduce cytotoxicity and improve drug delivery ability and antimicrobial efficacy. These bionic approaches provide a variety of solutions for antibiotic-resistant bacteria infection. Most commonly used in biomimetic materials are insect wings (especially cicadas and dragonflies), shark skins, etc. The surface of the cicada wing can kill some bacteria by simple physical interaction, and have impressive long-term inhibition ability. When the bacteria contact the nanopillars of the cicada wing, the attached bacteria will deform and the cell membrane is destroyed, eventually leading to bacterial death [44]. However, the antimicrobial properties of this topographical feature are still lacking, usually less than 60% (especially Gram-positive bacteria). Therefore, further modification is needed to improve its properties. In theory, zinc oxide (ZnO) is expected to be a candidate material to repair the inherent defects of cicada bionic antibacterial structure. ZnO-based nanomaterials have a good antibacterial effect, especially against Gram-positive bacteria [45]. In addition, ZnO has FDA-approved nanomaterials for in vivo applications [46]. However, zinc oxide is a material with poor
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chemical stability and rapid degradation in vivo, which is difficult to provide long-term antibacterial activity for implant interface. Based on the characteristics of the above two antibacterial strategies, Ye et al. put forward the technical idea of “insect and catkin” dual bionic antibacterial structure to modify the surface of poly (ether-ether-ketone) (PEEK) for the first time, as shown in figure 6.4 [38]. The bottom layer is the PEEK substrate, the middle is the cicada wing bionic pattern surface, and the top layer is catkin-like ZnO nanosheets (figure 6.4c). In the initial stage, the release of ZnO nanosheets effectively killed pathogenic bacteria around the implant (figure 6.4d). After that, the inner surface of the nanopillar structure was gradually exposed and began to exert its structure-related long-term antibacterial properties (figure 6.4e and f).
FIG. 6.4 – Schematic illustrated the inspiration and the mechanism of double bionic antibacterial structure. (a, b) The bionic prototype of cicada and catkin; (c) Three-dimensional schematic diagram of double bionic antibacterial structure; (d) Early release of the ZnO nanosheets; (e, f) At the second stage, the long-term inhibition effect of biomimetic nanopillars on bacteria (Reproduced with permission from [38], Biomater. Sci., 2019, 7, 2826. Copyright © 2019 Royal Society of Chemistry). Wound healing is a dynamic and interactive process, involving extracellular matrix (ECM), cytokines, blood cells, parenchyma cells, etc. [47]. In the process of wound healing, there are five overlapping stages: hemostasis, inflammation, proliferation, contraction, and remodeling [48]. In this process, the prevention of wound infection is a major challenge that needs to be addressed urgently, because microbial
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colonization in the wound site delays wound healing and may lead to life-threatening conditions [3]. Wound care dressings have been extensively studied in order to maintain favorable conditions for the healing process and to protect the wound from environmental threats and bacterial penetration. Various materials, such as animal fat, cotton, honey, and vegetable fiber, have been used in wound dressings [49, 50]. However, these traditional treatments may have many disadvantages, such as strong adhesion to the wound, frequent replacement, and the presence of microorganisms or chemicals that may be detrimental to the normal healing of the wound. Therefore, the electrospun polymer has great potential as wound dressing material due to its similar structure to ECM (which can promote tissue growth), high porosity, and gas permeability. With a large surface volume ratio, it provides an open structure for discharging intensified exudates and enhancing the hemostatic effect [51]. Tonda-Turo et al. used gelatin (GL) nanofibrous matrices loaded with the antibacterial drug gentamicin sulphate (GS) or silver nanoparticles (AgNPs) to fabricate a potent antibacterial material. In the process of tissue healing, the high surface area volume ratio of nanofiber makes it have an antibacterial effect on both Gram-negative bacteria and Gram-positive bacteria and ensures the controllable release of antibiotics in time and space. In addition, the bioabsorbable nanofiber matrix only targeted the infected site, which can reduce the risk of excessive toxicity and systemic toxicity [52]. Infection during or after human stent transplantation remains challenging because they reduce the effect of bone healing [53]. After transplantation, the infection may also spread from other inflammatory sources to the stent through blood flow [54]. In bone tissue engineering, biomimetic scaffolds composed of calcium phosphate bioceramics and hydroxyapatite can guide the formation of new bone tissue. At this time, it is also very important to prevent biological colonization and the formation of biofilm. The growth of antibiotic-resistant strains encourages researchers to develop new antimicrobial strategies [55]. Thus, platforms containing antibacterial compounds, such as quaternary ammonium salts [56], copper [57], ZnO [58], and AgNPs [59], have been used to overcome bacterial infection. Some of these systems have been used in bone tissue engineering and have been found to promote bone formation [60]. Among these compounds, AgNPs show a strong ability to inhibit or reduce infection and are also used for bone regeneration [61]. Considering the properties of β‐tricalcium phosphate (β-TCP) and hyaluronic acid (HA), Makvandi et al. fabricate thermosensitive hydrogels for bone tissue repair which possess antimicrobial functions to prevent infection (figure 6.5) [62]. The biosynthesis of AgNPs was carried out in the aqueous medium of corn silk extract and did not use any toxic chemicals. The green synthesis of AgNPs uses renewable materials, avoiding harmful compounds and non-environmentally friendly solvents, making them more suitable for clinical and biomedical applications. The new type of thermosensitive HA-based nanocomposite hydrogel has good mechanical properties. In addition, from the biological point, nanocomposites show appropriate biocompatibility and can promote cell differentiation, which is expected to become an ideal scaffold material for bone tissue regeneration.
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FIG. 6.5 – Schematic illustration of injection of the thermosensitive hydrogels for bone tissue repair accompanied with antimicrobial functions (Reproduced with permission from [62], Mater. Sci. Eng. C, 2020, 107, 110195. Copyright © 2020 Elsevier B.V.).
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[38] Ye J., Deng J., Chen Y., Yang T., Zhu Y., Wu C., Wu T., Jia J., Cheng X., Wang X. (2019) Cicada and catkin inspired dual biomimetic antibacterial structure for the surface modification of implant material, Biomater. Sci. 7, 2826. [39] Montanaro L., Speziale P., Campoccia D., Ravaioli S., Cangini I., Pietrocola G., Giannini S., Arciola C.R. (2011) Scenery of staphylococcus implant infections in orthopedics, Future Microbiol. 6, 1329. [40] Hickok N.J., Shapiro I.M. (2012) Immobilized antibiotics to prevent orthopaedic implant infections, Adv. Drug Deliv. Rev. 64, 1165. [41] Ma M., Liu X., Tan L., Cui Z., Yang X., Liang Y., Li Z., Zheng Y., Yeung K.W.K., Wu S. (2019) Enhancing the antibacterial efficacy of low-dose gentamicin with 5 minute assistance of photothermy at 50 °C, Biomater. Sci. 7, 1437. [42] Khonsari R.H., Berthier P., Rouillon T., Perrin J.-P., Corre P. (2014) Severe infectious complications after peek-derived implant placement: Report of three cases, J. Oral Maxillofac. Surg. Med. Pathol. 26, 477. [43] Kurtz S.M., Devine J.N. (2007) Peek biomaterials in trauma, orthopedic, and spinal implants, Biomaterials 28, 4845. [44] Elbourne A., Crawford R.J., Ivanova E.P. (2017) Nano-structured antimicrobial surfaces: From nature to synthetic analogs, J. Colloid Interface Sci. 508, 603. [45] Brayner R., Ferrari-Iliou R., Brivois N., Djediat S., Benedetti M.F., Fiévet F. (2006) Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium, Nano Lett. 6, 866. [46] Augustine R., Malik H.N., Singhal D.K., Mukherjee A., Malakar D., Kalarikkal N., Thomas S. (2014) Electrospun polycaprolactone/ZnO nanocomposite membranes as biomaterials with antibacterial and cell adhesion properties, J. Poly. Res. 21, 347. [47] Tonda-Turo C., Ruini F., Ceresa C., Gentile P., Varela P., Ferreira A.M., Fracchia L., Ciardelli G. (2018) Nanostructured scaffold with biomimetic and antibacterial properties for wound healing produced by ‘green electrospinning’, Colloids Surf. B 172, 233. [48] Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. (2008) Wound repair and regeneration, Nature 453, 314. [49] Inngjerdingen K., Nergård C.S., Diallo D., Mounkoro P.P., Paulsen B.S. (2004) An ethnopharmacological survey of plants used for wound healing in Dogonland, Mali, West Africa, J Ethnopharmacol. 92, 233. [50] Mensah A.Y., Houghton P.J., Dickson R.A., Fleischer T.C., Heinrich M., Bremner P. (2006) In vitro evaluation of effects of two ghanaian plants relevant to wound healing, Phytother. Res. 20, 941. [51] Zahedi P., Rezaeian I., Ranaei-Siadat S.-O., Jafari S.-H., Supaphol P. (2010) A review on wound dressings with an emphasis on electrospun nanofibrous polymeric bandages, Polym. Advan. Technol. 21, 77. [52] Griffis C.D., Metcalfe S., Bowling F.L., Boulton A.J.M., Armstrong D.G. (2009) The use of gentamicin-impregnated foam in the management of diabetic foot infections: A promising delivery system? Expert Opin. Drug Deliv. 6, 639. [53] Nair M.B., Kretlow J.D., Mikos A.G., Kasper F.K. (2011) Infection and tissue engineering in segmental bone defects—A mini review, Curr. Opin. Biotechnol. 22, 721. [54] Mankin H.J., Hornicek F.J., Raskin K.A. (2005) Infection in massive bone allografts, Clin. Orthop. Relat. Res. 432, 210. [55] Ribeiro M., Ferraz M.P., Monteiro F.J., Fernandes M.H., Beppu M.M., Mantione D., Sardon H. (2017) Antibacterial silk fibroin/nanohydroxyapatite hydrogels with silver and gold nanoparticles for bone regeneration, Nanomedicine 13, 231. [56] Makvandi P., Jamaledin R., Jabbari M., Nikfarjam N., Borzacchiello A. (2018) Antibacterial quaternary ammonium compounds in dental materials: A systematic review, Dent. Mater. 34, 851. [57] Lu Y., Li L., Zhu Y., Wang X., Li M., Lin Z., Hu X., Zhang Y., Yin Q., Xia H., et al. (2018) Multifunctional copper-containing carboxymethyl chitosan/alginate scaffolds for eradicating clinical bacterial infection and promoting bone formation, ACS Appl. Mater. Interfaces 10, 127.
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[58] Siddiqi K.S., ur Rahman A., Tajuddin, Husen A. (2018) Properties of zinc oxide nanoparticles and their activity against microbes, Nanoscale Res. Lett. 13, 141. [59] Zhang R., Lee P., Lui V.C.H., Chen Y., Liu X., Lok C.N., To M., Yeung K.W.K., Wong K.K.Y. (2015) Silver nanoparticles promote osteogenesis of mesenchymal stem cells and improve bone fracture healing in osteogenesis mechanism mouse model, Nanomedicine 11, 1949. [60] Cao H., Zhang W., Meng F., Guo J., Wang D., Qian S., Jiang X., Liu X., Chu P.K. (2017) Osteogenesis catalyzed by titanium-supported silver nanoparticles, ACS Appl. Mater. Interfaces 9, 5149. [61] Lalani R., Liu L. (2012) Electrospun zwitterionic poly(sulfobetaine methacrylate) for nonadherent, superabsorbent, and antimicrobial wound dressing applications, Biomacromolecules 13, 1853. [62] Makvandi P., Ali G.W., Sala F.D., Abdelfattah W.I., Borzacchiello A. (2020) Hyaluronic acid/corn silk extract based injectable nanocomposite: A biomimetic antibacterial scaffold for bone tissue regeneration, Mater. Sci. Eng. C 107, 110195.
Chapter 7 Bioinspired SLIPS for Medical Antifouling 7.1
Introduction
The attachment, adhesion, and colonisation of pathogenic bacteria on medical devices are still one of the global common and intractable issues [1–3]. Nosocomial infections caused by pathogenic bacteria and biofilms, which lead to increasing uses of antibiotics and substantial costs to the healthcare system, have been a major health threat, [4–6]. In particular, at least 80% of all human infectious diseases are related to biofilm [7–10]. A “biofilm” is the accumulation of microbial cells, in which bacterial aggregates tightly adhere to both biotic and abiotic surfaces and are encased in the self-produced matrix of EPS (extracellular polymeric substances) [11–13]. Once established, this three-dimensional matrix can constitute a major treatment obstacle that leads to the inefficiency of host immune defense and conventional antimicrobial therapy, as a result, chronic inflammation arises [14]. Biofilm formation is considered to start from the two stages consisting of unspecific reversible and specific irreversible attachment of planktonic bacteria onto a surface [15]. Therefore, it is necessary to construct an antifouling and antibacterial surface coating in medical settings to prevent the bacterial adhesion of harmful pathogens, reducing the spread of infections [16].
7.2
Bioinspired Prototype of Lubricant-Infused Slippery Surfaces
Bioinspired surfaces with special wettability have received increasing attention for their applications in medical material due to their unique biological structures and good biocompatibility. Pitcher plants of the genus Nepenthes are famous for their conspicuous leaves that can capture and digest arthropods. As early as 1893, J.M. Macfarlane discovered that pitcher plants consisted of morphologically distinct DOI: 10.1051/978-2-7598-2941-5.c007 © Science Press, EDP Sciences, 2023
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zones with different functions the waxy zone can make insects slip into the pitcher [17]. Surfaces with low–friction to insects have aroused great interest in constructing smooth and slippery surfaces, opening a versatile horizon to contrive materials coating with the excellent antifouling property. Pitchers on the Nepenthes are regarded as the “trap”, filling with digestive fluid. At the upper rim is an arch- inner to the outer side (figure 7.1a). The surface of the well–developed peristome with a regular microstructure that consists of first and second-order radial ridges. Typically, different species have a diversity of first-order ridges (figure 7.1b), differing in height, spacing, and shape. The second-order ridges are composed of straight rows of overlapping epidermal cells which form a series of steps towards the pitcher inside. The dimension of these second-order ridges is related to the function of the peristome [18].
FIG. 7.1 – (a) Optical image of N. alata with prey–trapping peristome and pitcher (left), together with a cross-sectional image of the peristome (right) (Reproduced with permission from [17], Nature, 2016, 532, 85. Copyright © 2016 Springer Nature); (b) Peristome surface (p) of N. alata, structured by first (r1) and second order radial ridges. The pores of large extrafloral nectaries (n) can be seen. The wax-covered inner wall surface (w) lies under the peristome; (c) Straight rows of overlapping epidermal cells formed the second-order ridges (r2) (Reproduced with permission from [18], Plant. Signal. Behav., 2009, 4, 1019. Copyright © 2009 Landes Bioscience). With a unique microstructure caused by surface hydrophilicity and secretion of hygroscopic nectar, the peristome of the pitcher plant plays an important role in initial prey capture. [19, 20]. As for the majority of Nepenthes species, the slippery zone, which is located underneath the peristome, was recognized as an important structure for prey trapping and retention, on account of its particular downward– directed lunate cells and thick crystalline wax coverage. Gorb et al. [21] observed that the lunate cells scattered between tabular epidermal cells and microscopic epicuticular wax crystals on top of both cell types (figure 7.2a and d). Each lunate cell is equipped with a single, enlarged and overlapping guard cell, demonstrating a crescent shape with ends pointing toward the pitcher bottom [22]. When the wax crystals were entirely removed by chloroform and replicated by polymer, both samples displayed a similar surface structure with a clear pattern of lunate cells
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FIG. 7.2 – SEM images of (a, d) intact Nepenthes alata pitchers and (b, e) de-waxed pitcher samples, and (c, f) the polymer replicas. LC: lunate cells; WC: wax crystals. White arrows indicate the direction to botto of the pitcher. (Scale bars: 50 μm (a–c), 2 μm (d), 10 μm (e, f)) (Reproduced with permission from [21], Beilstein. J. Nanotechnol., 2011, 2, 302. Copyright © 2011 Gorb and Gorb).
(figure 7.2b and c). The surface of lunate cells and the areas between them became smooth as well (figure 7.2e and f). It was found that the slippery pitcher zone, with its particular shape of the lunate cells, had anisotropic frictional properties in terms of insect attachment. Compared to chemically de–waxed pitchers and their polymer replicas, insects can slide more easily in the intact pitchers because of the failure of the claw interlocking on upright pitchers. Considering that the epicuticular wax can be found in aquatic and wetland plants which is responsible for non-wetting (antifouling) and self-cleaning capabilities, the waxy zone of Nepenthes enhances its hydrophobic property by increasing the microscale roughness [23]. The waxy crystals are easy to detach so that once the insect is attracted by the nectar at the top of the pitcher, it can fall into the trap. Since the trapped insects are almost impossible to flee, they would then get digested by enzymes of the pitcher fluid and the Nepenthes infauna [24]. Federle et al. reported that the specific surface properties of peristomes and insects “aquaplaning” played an important role in capturing insects. Perisomes with regular microstructure can be wetted by nectar or rainwater and thus a liquid film is formed.
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In other words, the unique structure with a water film on the surface is the key to reflecting the slippery effect for insects. Inspired by the insect capture mechanism of the Nepenthes pitcher plant, Aizenberg et al. designed “slippery liquid-infused porous surface(s)” (SLIPS). (figure 7.3a). The SLIPS was synthesized based on three criteria. At first, the lubricating liquid, which is wicked into the substrate, should remain stable. Generally, rough substrates with micro/nanostructures were used for locking the lubricating liquid due to their large surface contacting area and the chemical affinity between lubricant and substrate [25, 26]. Secondly, substrates must be preferentially wetted by the lubricant instead of the liquid that wanted to be repelled. Thirdly, the
FIG. 7.3 – (a) Scheme illustration of the fabrication process for constructing SLIPS; (b) Time-sequence images comparing mobility of pentane droplets on a SLIPS and a superhydrophobic surface. Pentane (surface tension:) can be repelled on SLIPS, but the traditional superhydrophobic surfaces will be wetted and contaminated; (c) Liquid repellency ability of the SLIPS surfaces can be maintained even after physical damage, compared to a typical Teflon AF treated hydrophobic flat surface (Reproduced with permission from [27], Nature, 2011, 477, 443. Copyright © 2011 Springer Nature].
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lubricant must be immiscible with the extraneous liquid. The SLIPS exhibited omnipotent liquid-repellent capacity toward either polar or non-polar liquids like water, acids, bases, alkanes, and alcohol (figure 7.3b). More notably, SLIPS can maintain restoration of liquid repellency upon physical damage as compared to a typical hydrophobic flat surface (figure 7.3c). The SLIPS, prepared by infiltrating lubricating liquids into porous solids with relatively low surface energy, stimulates the exploration of effective and versatile surfaces with liquid repellency and fouling resistance capacity.
7.3
Fundamental Principle and Liquid Repellency Mechanism of SLIPS
To fabricate SLIPS, the choice of components, including the substrate, lubricant, and repellent liquids is very important to ensure surfaces keep their slippery property. Crucially, the chemical and physical properties of three indispensable components need to be determined. The test liquid one wants to repel was abbreviated as Liquid A and the lubricant infused into micro/nanostructured porous substrates was abbreviated as Liquid B. The total interfacial energies of individual wetting configurations were compared to identify whether a textured solid will be wetted preferentially by the lubricating liquid or the test liquid (figure 7.4). When the roughened solid was completely wetted by Liquid A, this specific state referred to Configuration A. Configuration 1 and Configuration 2 represented the state where the substrate was completely wetted by Liquid B with and without a fully wetted Liquid A, respectively. In light of the configuration with lower total energy being easy to be wetted, it can be confirmed whether the selected solid/liquid combination can remain in the slippery state by comparing the energy states of Configurations 1 and 2 with that of Configuration A. In other words, satisfying both ΔE1 = EA – E1 > 0 and ΔE2 = EA – E2 > 0, it will ensure a stable lubricating film formation. The equations can be reduced to measurable quantities with the use of the Young equation and expressed as [27, 28]: DE1 ¼ RðcB coshB cA coshA Þ cAB [ 0
ð7:1Þ
DE2 ¼ RðcB coshB cA coshA Þ þ cA cB [ 0
ð7:2Þ
where E1, E2, and EA refer to the total interfacial energies per unit area of Configurations 1, 2, and A, respectively. In addition, γA and γB are the surface tensions for the liquid to be repelled and the lubricant, γAB is the interfacial tension at the liquid–liquid interface, θA, and θB are the equilibrium contact angles of the immiscible test liquid, and the lubricating fluid on a flat solid surface, and R is the roughness factor [25, 27]. Considering that the contact line morphology governs droplet pinning and its mobility on the SLIPS, it is important to examine how the interactions among them
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FIG. 7.4 – Illustration of the maintenance of a stable lubricating film under different working
conditions (Reproduced with permission from [27], Nature, 2011, 477, 443. Copyright © 2011 Springer Nature).
determine the morphology of the contact line. Smith and coworkers described the fundamental principles governing droplet mobility on lubricant-impregnated surfaces and provided guidelines for their design [29]. All the possible thermodynamic configurations for a solid/lubricant/air and solid/lubricant/water system were investigated, as shown in figure 7.5a. There are up to three different contact lines, two of which can get pinned on the textured solid. The value of the rolling angle relies on the degree of pinning. If the droplet completely displaced the lubricant, it would be unable to roll off (A3–W1 and A2–W1). When the droplet with emergent post tops, it has reduced mobility (A3–W2, A2–W2, and A2–W3), whereas those in states with encapsulated posts outside and beneath the droplet are expected to exhibit no pinning and consequently infinitesimally small roll-off angles (the A3–W3). With regard to various lubricants and textured substrates, it is necessary to predict whether the chosen fluids and solids will form a stable slippery surface. Preston et al. [30] presented a model to determine the ability to repel given fluid by the SLIPS surfaces constructed through the arbitrary combination. The spreading parameter Sxy for each interface was used as the criteria for designing the slippery surface. Five criteria were summarized for failures of constructing slippery surfaces, as shown in figure 7.5b. Specifically, if the criterion Sld \ 0
ð7:3Þ
is met, the lubricant does not wrap external droplets and undesirable loss of lubricant is avoided in the process of droplets departure. If criterion Sdl \ 0
ð7:4Þ
is met, the impinging fluid does not spread on the lubricant. If criterion Sls þ c1 R [ 0
ð7:5Þ
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FIG. 7.5 – (a) Possible thermodynamic states of a water droplet placed on a lubricant-impregnated surface (Reproduced with permission from [29], Soft Matter, 2013, 9, 1772. Copyright © 2013 The Royal Society of Chemistry); (b) Failure modes predicted from surface-energy-based criteria for liquid infused surface design (Reproduced with permission from [30], ACS Appl. Mater. Interfaces, 2017, 9, 42383. Copyright © 2017 American Chemical Society).
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and criterion Slsðd Þ þ cdl R [ 0
ð7:6Þ
are met, it means that the lubricant can spread over the structured substrate surface. Particularly, if criterion (7.5) is met, the lubricating fluid will infiltrate onto the rough substrate (factor R reflects the roughness) in the presence of the surrounding vapor, and when the criterion (7.6) is met, the lubricant can infuse into the textured with the impinging droplet in existence. Notably, when the spreading coefficients Sls and Sls(d) in the criteria (7.5) and (7.6) exceed zero, the lubricating oil completely covers the underlying substrate, resulting in a remarkable reduction in contact angle hysteresis. If criterion cdl [ 0
ð7:7Þ
is met, the lubricant is miscible with the impinging droplet. In the above inequalities, subscripts l, d, and s refer to lubricants, droplets, and solid substrates. The spreading parameter Sxy represents x spreading over y. R = (r − 1)/ (r − φ) is the roughness factor that is calculated using roughness, r, and a solid fraction, φ. In addition, the group of Sett [31] tried to test the miscibility and cloaking behavior of fluids having various surface tensions (12–73 mN/m) with different viscosities and the chemical nature of lubricants (figure 7.6a). They proposed a criterion based on the miscibility of the lubricant–working fluid to ensure the applications of SLIPS requiring long-term stability, as outlined in figure 7.6b. The SLIPS is acknowledged as an omniphobic surface that has a range of attractive characteristics. Based on the fundamental criteria of constructing the SLIPS and the ingenious choice of a rough substrate and lubricant for a given impinging fluid based on energetic considerations, spreading parameter, or miscibility and cloaking, this surface can play an important role while applying to antifouling surface modification.
7.4
Fabrication Strategies of SLIPS for Antifouling Applications
In the past couple of decades, numerous strategies have been developed for fabricating SLIPS. In early studies, researchers utilized surface wettability to achieve bacterial fouling resistance. Inspired by Nepenthes pitcher, Alexander et al. [32] provided a method of building artificial SLIPS to achieve the anti-biofilm property by infusing lubricants onto superhydrophobic micro arrays modified silicon wafer (figure 7.7a). Various perfluorinated fluids were chosen as lubricating fluids and soaked into porous surfaces. After removing the redundant lubricant that is unable to stand steady on the surface, the obtained SLIPS had a meniscus morphology when the droplet was dropped onto the surface, achieving a strong antifouling ability and it can maintain stability in many hostile environments (figure 7.7b–e). They chose three types of bacteria to examine the antifouling property under both
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FIG. 7.6 – (a) Combined miscibility and cloaking results; (b) Conditions while effectively selecting lubricant in designing stable slippery surfaces (Reproduced with permission from [31], ACS Appl. Mater. Interfaces, 2017, 9, 36400. Copyright © 2017 American Chemical Society).
static and dynamic conditions, and all have achieved over 96% bacterial resistance. In addition, there was a meniscus character on the side of the droplet when a bacteria culture droplet was dropped on the resulting SLIPS. After the evaporation in time, as shown in figure 7.7f, this droplet had no coffee ring formation on the slippery surface, which demonstrated the SLIPS presenting any pinning points on the surface. Li et al. [33] also combined hydrophobicity into consistent slippery surfaces. BMA-EDMA polymer was adopted as the porous substrate to lock the hydrophobic lubricant liquid to form an overlying slippery liquid layer. They used various bacteria strains of P. aeruginosa to examine the anti-biofilm ability of this BMA–EDMA surface, which turned out that this surface had a 7-day-long resistance to different P. aeruginosa. Erica et al. [34] first proposed that SLIPS can also resist the adhesion of eukaryotic cells. To vividly demonstrate the antiadhesion property, they build a grid structure containing both superhydrophobic and superhydrophilic areas. After sequentially immersing with water and hydrophobic liquid, this resulted in grid patterned surface presenting bio-selective ability. They used human cervical tumor
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FIG. 7.7 – (a) Formation of slippery liquid-infused porous surface (SLIPS) can effectively resist bacterial attachment; Formations of Fluorescent stained P. aeruginosa biofilms on (b) SLIPS and (c) superhydrophobic PTFE (Scale bar = 30 μm); Evaporation residues of P. aeruginosa culture droplets on (d) SLIPS and (e) superhydrophobic PTFE (Scale bar = 2 cm); (f) Dynamic evaporation behavior process of P. aeruginosa culture droplets on SLIPS and PTFE porous surface. Different from normal PTFE surfaces, SLIPS present a meniscus morphology and do not have the formation of coffee ring (Reproduced with permission from [32], P. Natl. Acad. Sci., USA, 2012, 109, 13182. Copyright © 2012 National Academy of Science).
cells to contaminate the obtained surface, and after 7 days the substrate can still maintain cells in the field of hydrophilic, and keep hydrophobic barriers unattached. Similar to the work of Erica, Julia et al. [35] built uniform arrays consisting of SLIPS and hydrophilic areas. Different strains of bacteria microclusters can be obtained
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through this unique pattern, which provides a new way to investigate the interaction factors of biofilm formation. Apart from substrates of SLIPS built from reaction etching, Layer-by-Layer (LbL) deposition is another very common way of constructing functional coatings. The group of Steffi fabricated a transparent slippery coating surface with the ability of repellent biological liquid through the LbL deposition method after 4 7 cycles (figure 7.8) [36]. In this method, charged nanoscale particles and polyelectrolytes deposited on the substrate provided a nanoporous structure to immobilize the lubricant liquid firmly. Combined with appropriate biocompatible lubricants, the LbL SLIPS strategy had universality on different substrates which can acquire SLIPS suitable for various materials and occasions.
FIG. 7.8 – Schematic depicting the presence of using layer-by-layer (LbL) process to construct SLIPS and SEM images of the substrate after different times of deposition cycles. (Scale bars = 500 nm) The flat substrate is charged with negative (i) and positive (ii) to form a polyelectrolyte layer. Then silica nanoparticles with negative charge are introduced onto the first layer (iii) to produce a thin film (iv), and after calcining, a porous structure is obtained (v). After functionalizing by fluorinated silanes (vi) and infusing lubricant liquid (vii), the surface can slide fouling away (viii) (Reproduced with permission from [36], Adv. Funct. Mater., 2014, 24, 6658. Copyright © 2014 John Wiley and Sons). The SLIPS have shown significant improvement in anti-biofouling properties, yet this performance may fail due to poor mechanical durability and the limited quantity of lubricants. In 2011, Wang et al. [37] firstly reported a method of self-healing repellent surfaces by coating hydrolysate on fabrics. Based on this strategy of infusing lubricant liquids into the pores, and inspired by the curves in the leaves, Caitlin et al. [38] created a system that achieved self-healing when the lubricant layer was injured. In this method, the silicone oil will fill up the vascular networks which were immobilized on the PDMS substrate, and the extra oil will
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spread upon the surface to form a smooth and slippery layer. The PDMS itself could release fouling, and the oil stored in networks was able to be released and fix the gap when the slippery layer was destroyed. By examining the amount of biofilm that formed on vascularized SLIPS and normal liquid-infused PMDS surface, the self-replenishing property was verified (figure 7.9a and b).
FIG. 7.9 – (a) Quantification comparison and representative images of formation biofilm on vascularized infused PDMS and control PDMS under evaporation for 48 h. (P < 0.05, purple color is from crystal violet staining); (b) The antifouling property comparison between vascularized infused PDMS and the control sample. The immersed glass is half–original and half–coated with lubricant–infused PDMS. (Reproduced with permission from [38], ACS Appl. Mater. Interfaces, 2014, 6, 13299. Copyright © 2014 American Chemical Society).
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Through photocuring, the fluorinated compound and cross linker on the substrate, Yao et al. [39] built a polymer network and infused fluorinated lubricant into the elastomers. Benefiting from the polymer chain which can swing freely the wet surroundings, the slippery performance was improved significantly (figure 7.10a). This obtained slippery surface had great resistance to blood and other biofouling with a maintaining of biocompatibility (figure 7.10b). Based on a similar strategy, Wei et al. [40] utilized the polycondensation reaction between the polymer and coupling reagents to promote the bonding of the nanostructure substrate and coating layer (figure 7.11a). These slippery hybrid coatings (SHCs) showed excellent long-term slippery stability even under extreme operating conditions like high shear rate, elevated evaporation, or flowing aqueous immersion (figure 7.11b). In 2014, the slippery liquid-infused surface was first introduced into medical-grade device applications. Daniel et al. [41] tethered the molecular layer of fibrous perfluorocarbon steadily onto the substrate, and then the perfluorodecalin (medical level) was surface coated to fabricate a smooth layer. The obtained tethered-liquid perfluorocarbon (TLP) coating was capable of repelling both
FIG. 7.10 – (a) Schematic of dispersing lubricant into the polymer network and forming a smooth layer on the surface, and achieving slipperiness through free polymer chain ends; (b) Adhesion mouse embryonic fibroblasts quantification comparison and its corresponding fluorescent images on different substrates. And blood repellence comparison between bare and infused substrate (Reproduced with permission from [39], Angew. Chem. Int. Ed., 2014, 53, 4418. Copyright © 2014 John Wiley and Sons).
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FIG. 7.11 – (a) Schematics of fabricating cross-linked networks and slippery hybrid coatings (SHC); (b) Schematics of the long-term biofouling property and stability of SHC (Reproduced with permission from [40], ACS Appl. Mater. Interfaces, 2016, 8, 34810. Copyright © 2016 American Chemical Society).
blood and bacteria which can also suppress the formation of thrombosis (figures 7.12 and 7.13). The medical tube modified with TLP surface was implanted into pigs to examine the anti-thrombosis property in vivo, and the in vitro test was taken underflow, which both resulted in a very significant resistance to thrombus. This TLP slippery modified surface avoided the risk of using heparin. Based on a textured surface formed by the photo–grafting polymerization with osmotically driven wrinkling, Yuan et al. [42] built a slippery surface by infusing fluorocarbon liquid onto the underlying substrate that the lubricant can stick robustly inside the surface and spread as a smooth layer (figure 7.14a). This fluorocarbon liquid-infused wrinkling surface (FLIWS) presented excellent properties of resistance bio-attachments such as proteins, blood, and bacteria, but had no
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FIG. 7.12 – (a) Schematic of TLP-coated surface and its blood repellency; (b) Resistance to blood adhesion showed by dropping a blood droplet on the control surface and TLP-coated surface both with a 30° lean (Scale bars = 1 cm) (Reproduced with permission from [41], Nat. Biotechnol., 2014, 32, 1134. Copyright © 2014 Springer Nature). toxoid to L929 cells (figure 7.14b). Uttam et al. [43] proposed a SLIPS building method that infused hydrophobic liquid oil as the lubricant into nanoporous polymer multilayer substrates (figure 7.15a). This SLIPS had a stable resistance to the adhesion and formation of both bacteria and fungus. Innovative of this method, a bactericidal agent can be successfully stored and released, which gave the slippery surface the ability to eliminate pathogens that dissociated in the surroundings. A novel strategy that constructed slippery antifouling surfaces was provided by Hizal and his coworkers [44]. First, the aluminum substrate was anodized to accomplish a 2D nanoporous layer structure, then the nanoholes were widened through chemical etching. Along with the broader of the nanoholes, the wall between them became thinner and at last, the 3D alumina nanopillar structure was obtained. To form a conical shape of the nanocluster, the 3D nanostructure was then dried by evaporation which can be explained by capillary force at the principle level. With the spinning coating of Teflon on the ordered nanocluster, the hydrophobicity was successfully acquired (figure 7.15b). As shown in figure 7.15c, the FE–SEM images were taken to illustrate the antifouling behaviors of the formed surface. Underflow liquid conditions, the bacteria that are stuck within the nanostructures can be unbundled and blown away completely. Ban et al. [45] used a similar strategy
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FIG. 7.13 – (a) Photographs of polyurethane cannulae with and without TLP–coated in inner surfaces (Scale bars = 5 mm); (b) Images of adhered P. aeruginosa on control surfaces and TLP-coated surfaces after 16 h culture (Purple color is stained by Crystal violet, Scale bars = 5 mm. InsetSEM images. Scale bars = 2 µm). (Reproduced with permission from [41], Nat. Biotechnol., 2014, 32, 1134. Copyright © 2014 Springer Nature).
to form nanopillar on AAO substrate, and infused oil lubricant subsequently to build a SLIPS that can both resist bacterial adhesion and biofilm formation. To avoid the potential risk of chemicals towards biocompatibility, the principle proposed by Katharina et al. [46] was using a physical approach to create nanostructures on a titanium substrate. The lubricant liquid was immobilized into the nanoporous which was constructed through ultrashort pulsed laser ablation. The obtained SLIPS could prevent the attachment of bacteria while keeping the original biological properties (figure 7.16a). Chen et al. [47] adopted the clinical use material ePTFE as the substrate and perfluorocarbon liquids as the lubricant to produce a SLIPS coating that can be put in vivo. In vivo, experimental results demonstrated that the surface resisted the adhesion of S. aureus and inflammation while maintaining the functions of macrophages (figure 7.16b). SLIPS had also been used in the food-safe aspect. Tarek et al. [48] infused food-grade oil into the caves of the stainless steel (SS) surface and the extra oil dispersed on the fulfilled SS to form a smooth surface that can slip residues and bacteria away. With the storage oil in the breaches, this slippery surface can restore its lubricant layer subsequently when the layer was destroyed (figure 7.17a). And even the residual oil can have enough to spread as a whole layer after wearing,
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FIG. 7.14 – (a) Schematic of fabricating Fluorocarbon Liquid-Infused Wrinkling Surface (FLIWS); (b) FESEM images of SIBS, FTWS, and FLIWS substrates after contacting bacteria for 24 h (Scale bar = 20 μm) (Reproduced with permission from [42], ACS Appl. Mater. Interfaces, 2015, 7, 19466. Copyright © 2015 American Chemical Society).
the remaining could still be a barrier to protect the substrate for a while. Featuring exceptional antifouling performance, the SLIPS can be employed in the field of dairy product storage. Zouaghi et al. [49] presented and discussed the antifouling and antibacterial behavior of three biomimetic surfaces (figure 7.17b). Fouling behaviors and bacterial adhesion test results showed that the nano-rough plasma coated surface (PL) and SLIPS exhibited significant fouling resistance performance compared to the lotus-like surfaces (LL). Almost no biofouling was found on SLIPS surfaces. The surface morphology and wetting transition state resulted in the different properties of antifouling. Specifically, during the process of pasteurization, fouling substances tended to penetrate the LL surface due to the open morphology and deep relief. In addition, to prevent bacterial adhesion on surfaces, alive planktonic bacteria in the surrounding medium still have the risk of contaminating nearby unprotected surfaces, resulting in the formation of biofilms. Taking advantage of small–molecule inhibitors of quorum sensing (QSIs), Kratochvil et al. [50] developed a novel slippery and antifouling surface that can be applied as robust platforms for the controlled release or delivery of QSIs and biofilm inhibitors (figure 7.18). When the QSIs dimethyl–2–aminobenzamidazole (DMABI) was integrated into the SLIPS, P. aeruginosa biofilms were avoided both in the SLIPS and the regions of surrounding non–SLIPS coated surfaces.
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FIG. 7.15 – (a) Fluorescence micrographs of control substrates and SLIPS substrates after culturing in four bacteria for 24 h (i–iii, v– vii) and 72 h (iv, viii). (Colors are from SYTO-9 green fluorescent nucleic acid and calcein-AM staining. Scale bars = 100 µm) (Reproduced with permission from [43], Adv. Funct. Mater., 2016, 26, 3599. [44] Copyright © 2016 John Wiley and Sons); (b) Schematic of the fabrication process to build nanopillar structures on anodic aluminum oxide (AAO) surfaces; (c) Schematic illustration of antifouling process of FLIWS under wet and flow conditions (Reproduced with permission from, ACS Appl. Mater. Interfaces, 2017, 9, 12118. Copyright © 2017 American Chemical Society). In order to combat oral cavity implant-associated infections, Doll et al. [51] developed a liquid-infused titanium surface integrating the superhydrophobic microand nanopattern with a perfluoropolyether lubricant. Four inoculated biofilms were used as typical oral multispecies models to investigate the antifouling capacity of the titanium SLIPS (figure 7.19). As shown in figure 7.20a and b, compared to the
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FIG. 7.16 – (a) Schematic illustration showing the antibacterial property of SLIPS Titanium substrates and initial Titanium substrates (Reproduced with permission from [46], ACS Appl. Mater. Interfaces, 2017, 9, 9359. Copyright © 2017 American Chemical Society); (b) SEM images of retrieved implants and staining images of implant-tissue interface (Blue arrow: leukocytes; Yellow arrow: matrix; Red arrow: bacteria highlighted in green; Pink arrow: red blood cell; Scale bar = 10 mm; S. aureus dark purple, red arrow: bacteria, *implant pocket, Scale bar = 100 mm) (Reproduced with permission from [47], Biomaterials, 2017, 113, 80. Copyright © 2017 Elsevier B.V.).
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FIG. 7.17 – (a) Schematic of inhibiting attachment of organic residue and bacteria on untreated stainless surfaces (SS) and oil-coated SS surfaces (Reproduced with permission from [48], ACS Appl. Mater. Interfaces, 2018, 10, 22902. Copyright © 2018 American Chemical Society); (b) Schematic of the three biomimetic surfaces: laser ablated Lotus-like surface (LL), slippery liquid-infused surface (SLIS) and nano-rough plasma coated surface (PL) (Reproduced with permission from [49], Food Bioprod. Process., 2019, 113, 32. Copyright © 2019 Elsevier B.V.). control surfaces, the biofilm volume on the SLIPS was significantly reduced, demonstrating the obvious repellency of biofilms. In addition, the resulting SLIPS can maintain stability over 13 days under continuous flow in an oral flow chamber system, expanding the future application of liquid-infused titanium in oral implantology. Shi et al. [52] designed a multipotential wound dressing iPDMS/AgNPs mainly applied in burn injuries treatments for patients. As for the iPDMS/AgNPs, the 3D-printed PDMS was infused with lubricating oil with Ag nanoparticles (figure 7.20c and d). The slippery surface can prevent the adhesion of two standard bacteria that possess drug resistance, S. aureus, and E. coli, and show
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FIG. 7.18 – Schematic depicting the fabrication of the QSI-loaded SLIPS and the behavior of antifouling and killing nearby planktonic bacteria (Reproduced with permission from [50], ACS Infect. Dis., 2016, 2, 509. Copyright © 2016 American Chemical Society).
FIG. 7.19 – (a) Staining Microscopic images of FISH-stained oral multispecies biofilm formed on titanium substrates. (Blue: S. oralis, green: A. naeslundii; yellow: V. dispar; red: P. gingivalis. (The left images are four different individual bacteria and the right image is an overlay of four bacteria; Scale bars = 30 μm) (Reproduced with permission from [51], ACS Appl. Mater. Interfaces, 2019, 11, 23026. Copyright © 2019 American Chemical Society). antibacterial performance due to the presence of AgNPs. Specifically, the iPDMS/AgNPs exhibited good biocompatibility and were able to accelerate wound healing by promoting neo–epithelial and granulation tissue formation effectively, providing a new choice in the application of wound dressings.
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FIG. 7.20 – (a) Tukey box plots of multispecies biofilm volume per image and (b) mean ± standard deviation of multispecies biofilm live/dead distribution on SLIPS and titanium control surfaces after 24 h growth in the flow chamber system and pulsed washing. (All graphs N = 9. (*) indicates statistical significance at p ≤ 0.05.) (Reproduced with permission from [51], ACS Appl. Mater. Interfaces, 2019, 11, 23026. Copyright © 2019 American Chemical Society). 3D-printed mesh and nanosilver dotting micrographs of iPDMS membrane with flexibility and (c) folded iPDMS/AgNPs, and (d) stretched iPDMS/AgNPs (Reproduced with permission from [52], Mater. Sci. Eng. C, 2019, 100, 915. Copyright © 2019 Elsevier B.V.); (e) Schematic of 7 days long antifouling property of SLIPS based on depositing silver nanoparticles on the PVC surfaces (Reproduced with permission from [53], ACS Omega, 2020, 5, 7771. Copyright © 2020 American Chemical Society).
Recently, Wylie et al. [53] used phosphonium ionic liquid (PIL) as a lubricating liquid to construct the SLIPS, aiming at improving the stability and introducing antibacterial properties. By depositing silver nanoparticles on the PVC surface, a rough substrate can thus be created and an underlying bactericidal surface can play a role when the lubricant infusion fails. In addition, the PIL–infused SLIPS exhibited fouling resistance for at least 7 days upon repeated bacterial challenge by S. aureus and P. aeruginosa (figure 7.20e).
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Conclusions and Outlook
We summarized the up-to-date progress and advancement of SLIPS for antifouling and antibacterial applications. The field of SLIPS bears a huge potential for both fundamental research and real-life applications. Lubricant–infused surfaces offer an unprecedented opportunity to cater to the requirement of the wetting system at complex interfaces due to their lubricity and excellent repellency against various liquids. The bioinspired prototype of lubricant-infused slippery surfaces, Nepenthes, was described based on its unique physiological structures, which were relevant to the slippery property directly. The first example of SLIPS was introduced and three criteria for constructing such surface were proposed, which provided new insight into exploited diverse slippery surfaces. Additionally, it is critical to choose the components, including the substrate, lubricant, and repellent liquids, to ensure surfaces keep their slippery property. Furthermore, the spreading parameter can be used to predict whether the chosen fluids and solids will form a stable slippery surface. The contact line morphology can determine droplet pinning and its mobility on the SLIPS and the miscibility and cloaking behavior of fluids also play a role in the applications of antifouling. To obtain the functionalized SLIPS, there are various methods to fabricate the underlying substrate for infusing lubricating liquids subsequently. A series of technology was chosen, such as 3D printing, impregnation, LbL deposition, photographing polymerization, hydrophilic–hydrophobic micropattern, and anodizing with the post-etching method. Integrating with applicable lubricants, the SLIPS demonstrated outstanding antifouling and antibacterial performance on medical–associated surfaces. To date, with the increasing need for such antifouling surfaces, it is essential to develop the SLIPS to face the complex operating environment over time and with use. The durability of the slippery surface needs to be improved, thus preparing long-term stable SLIPS is vitally important. Therefore, the understanding of the mechanisms and pathways to guide the construction of the SLIPS is still a topical subject. As the indispensable components of SLIPS, it is a feasible approach to adopt novel solid substrates and lubricants, endowing the SLIPS with unanticipated properties. On a final note, multifunctional SLIPS should be explored to meet the requirement of multidisciplinary applications, expanding its practical applications in the future.
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Chapter 8 Superhydrophobic Surfaces for Medical Antifouling 8.1
Introduction
Biofouling infections of biomedical materials caused by undesired biomolecules, bacteria, cells, and organisms, are one of the most critical risks that threaten global public health [1, 2]. To reduce the morbidities and mortalities caused by bacterial infections, the antibacterial materials/surfaces that are easy and economical to combat the spread of infection are increasingly urgent. Bacteria cells tend to adhere to material surfaces and form robust colonisation, known as biofilms, as a strategy to protect themselves from pharmacological therapies and to establish infections [3]. The formation of biofilms may be composed of several sequential processes. Step I is the initial interaction as well as the rapid and reversible course between the bacterial cell and the material surfaces. Comparatively, step II is slowly reversible, therefore often termed as irreversible, which involves interactions between bacterial surface proteins and binding molecules on the material surfaces [4]. Once bacteria adhered to the material surface, cells may undergo the following processes such as cell differentiation, proliferation, colony, and finally formulating stubborn biofilm, which leads to medical infections and public health risks [5]. Therefore preventing initial bacterial adhesion is a critical step to hinder bacterial infections. Recently, increasing attention has been concentrated on the inspiration from nature to resolve many technological and scientific challenges. Since the first reported “lotus effect” by Barthlott and Neinhuis in 1997, the bio-inspired superhydrophobic surfaces, with high static water contact angle (>150°) and low sliding angle (99.95% oil purity after filtration and an extremely high flux, much larger than commercial filtration membranes. Wang et al. [28] fabricated a synergistic hybrid membrane with remarkable super-repellent ability and photodynamic bactericidal activity via a facile non-solvent induced phase separation process (figure 8.5b). This synergistic membrane exhibited highly effective antibacterial performances, as demonstrated by a totally “bacteria-free” surface.
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FIG. 8.4 – (a) Schematic illustration for preparing Fe3O4@SiO2/HMDS particles (Reproduced with permission from [24], ACS Appl. Mater. Interfaces, 2020, 12, 17004. Copyright © 2016 American Chemical Society); (b) SEM images of LDPE matrix with GBs and LDPE with GBs matrix coated with SNFs; The insert shows the magnified image of functionalized SNFs with TiO2 NPs (Adapted with permission from [25], Small, 2019, 15, e1901822. Copyright © 2019 John Wiley and Sons).
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FIG. 8.5 – (a) SEM images of titanium phosphate thin films with various morphologies (Reproduced with permission from [26], ACS Appl. Mater. Interfaces, 2014, 6, 7695. Copyright © 2014 American Chemical Society); (b) Structural evolution of the formation of superhydrophobic Rf-PVDF@SiO2@Ce6 membrane and synergistic bactericidal performances (Reproduced with permission from [28], J. Membr. Sci., 2020, 614, 118482. Copyright © 2020 Elsevier B.V.).
8.2.2
Top-Down Fabrication
8.2.2.1
Photolithography
Photolithography technology, through which patterned surfaces and other sizes or shape-controlled surfaces with special topography, is a commonly used method for micro-/nanostructure fabrication. Such a method is widely applied in the fabrication of micro-/nanostructures for numerous applications since its templates are easily fabricated and reusable. Jiang et al. [29] reported a micro-/nanostructures graphene film with anisotropic wettability via a process combining photolithography and laser holography technologies. Grooved structures with a period of 200 μm were
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fabricated via photolithography on a smooth Si wafer using a conventional photopolymer, SU-8. After coating the grooved substrates with a layer of GO, a two-beam laser interference treatment was performed to induce hierarchical micro-/ nanostructures (10–100 nm interlayer spacings), significantly increasing the surface roughness. Zhao et al. [30] created various structures (*3 μm diameter pillars, height of *7 μm) on silicon wafer via a simple photolithography technology (figure 8.6a–d). Then, the superoleophobicity surface was synthesized by the molecular vapor deposition with (tridecafluoro-1,1,2,2-tetrahydrooctyl)trichlorosilane. Furthermore, Zhao and coworkers concluded that surface modification and pillary topography contribute to surface superoleophobicity.
FIG. 8.6 – SEM images of *3 μm-diameter pillar array FOTS surfaces with (a) 4.5 μm, (b) 6 μm, (c) 9 μm, and (d) 12 μm center-to-center spacing. (Insets: sessile drops of water and hexadecane on the pillar array surfaces) (Reproduced with permission from [30], Langmuir, 2012, 28, 14925. Copyright © 2012 American Chemical Society).
8.2.2.2
Etching
As a facile, low-cost, easy-operation method, etching can be used to fabricate micro-/nanostructure on surfaces. According to whether using solutions or not, etching can be categorized as dry or wet etching. As a typical wet etching process, chemical etching is usually accomplished in an acidic or alkaline bath. Through etching and coating, Wang et al. [31] prepared four aluminum surfaces varied from superhydrophilic to superhydrophobic. The superhydrophilic surfaces were converted to superhydrophobic surfaces by coating a PTES layer using a simple dip-coating process. Besides, other engineering metals also can be roughed by chemical etching. For instance, Yu et al. [32] made the hierarchical micro-/nanostructure on the copper alloys through etching, heat treatment, and then stearic acid modification to achieve super wetting reversibility under temperature control (figure 8.7). The superhydrophobic surfaces exhibited excellent water repellence with a static contact angle of 159.7 ± 1.2°, and a sliding angle of 3.1 ± 0.6°. Although the method of wet etching is suitable for wettability modifications on simple equipment,
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FIG. 8.7 – SEM images of the copper alloys surface topography treated by different steps: (a1) Bare, (b1) E5, (c1) E10, (d1) E15, (e1) E20. (a2)–(e2) corresponding high magnification. “E” means an etching processing in 1 M FeCl3 solution and the number behind represents the etching time (min) (Reproduced with permission from [32], Appl. Surf. Sci., 2020, 517, 146145. Copyright © 2020 Elsevier B.V.).
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it is rather hard accurately control the surface topography, especially morphology fabrication on tiny objects. Compared with wet chemical etching, the dry etching procedure can be well controlled without residues from the solution. Ellinas et al. [33] first fabricated hierarchical structure on polymeric surfaces of polymethyl methacrylate (PMMA), polyether ether ketone (PEEK), and polydimethylsiloxane (PDMS) by combining plasma etching and perfluorinated monolayer grafting together (figure 8.7e). As for cellulose-based substrates such as paper, Li et al. [34] presented a similar method to fabricate super amphiphobic paper by combining the control of fibre size and structure with plasma etching and fluoropolymer deposition. In addition to the aforementioned etching methods, other etching techniques such as electrochemical etching, ion etching, and so on, can also be employed on basis of the different chemical properties of the substrates.
8.3
Conclusions and Outlooks
Even though superhydrophobicity and micro/nano-structures are recently developed concepts, they play essential roles in case of overcoming many intractable problems. In this part, typical inspiring creatures, fundamental theories, and fabrication methodologies are summarized. Furthermore, the synthesis of a range of different superhydrophobic micro/nano-structure surfaces using various materials is presented. With regard to superhydrophobic structure manufacturing, classical bottom-up and top-down fabrication methods have been reported, including physical deposition by spray- and dip-coating, electrospinning, sol–gel, hydrothermal method, phase inversion, photolithography, and etching. Inspired by natural antifouling surfaces with superhydrophobicity like a lotus leaf, rice leaf, butterfly wings, and mosquito eyes have been successfully developed as antifouling surfaces against the adhesion of bacteria, cells, and marine organisms. Benefiting from the trapped air cushions between the bacteria cells and the micro-/nanostructure surface, these surfaces can reduce the close contact and adhesion between fouling organisms and material surfaces, enabling the superhydrophobic surface to be a new strategy in the antibacterial design. Moreover, the low interaction has helped researchers fabricate antibacterial surfaces to kill or remove bacteria without using any antibiotics. For example, Lin et al. fabricated durable antibacterial and bacterial adhesion-resistant cotton fabrics. Although amounts of studies have been done in such a field in the past few years, challenges from several aspects are still waiting to be addressed. Bacteria will attach, adhere, and colonize on superhydrophobic surfaces after the entrapped air layer is diminished or vanished. The long-term durability of the superhydrophobic surface against mechanical abrasion or chemical etching may be a crucial problem for its applications in harsh bacteria environments. Thus most of the fabrication techniques are confined to scientific research in the laboratory for the moment and are hard to be achieved and applied for large-scale production. The gap between laboratory studies and practical products is a challenging but rewarding problem to be addressed. Probably 3D printing is a promising candidate, which is advantageous in the controllability, repeatability, and reduction of cost.
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References [1] Wei T., Zhan W., Cao L., Hu C., Qu Y., Yu Q., Chen H. (2016) Multifunctional and regenerable antibacterial surfaces fabricated by a universal strategy, ACS Appl. Mater. Interfaces 8, 30048. [2] Pavithra D., Doble M. (2008) Biofilm formation, bacterial adhesion and host response on polymeric implants—Issues and prevention, Biomed. Mater. 3, 034003. [3] Arciola C.R., Campoccia D., Speziale P., Montanaro L., Costerton J.W. (2012) Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials, Biomaterials 33, 5967. [4] Lichter J.A., Van Vliet K.J., Rubner M.F. (2009) Design of antibacterial surfaces and interfaces: Polyelectrolyte multilayers as a multifunctional platform, Macromolecules 42, 8573. [5] Zhang X., Wang L., Levänen E. (2013) Superhydrophobic surfaces for the reduction of bacterial adhesion, RSC Adv. 3, c3ra40497h. [6] Latthe S.S., Terashima C., Nakata K., Sakai M., Fujishima A. (2014) Development of sol–gel processed semi-transparent and self-cleaning superhydrophobic coatings, J. Mater. Chem. A 2, 5548. [7] England M.W., Urata C., Dunderdale G.J., Hozumi A. (2016) Anti-fogging/self-healing properties of clay-containing transparent nanocomposite thin films, ACS Appl. Mater. Interfaces 8, 4318. [8] Howarter J.A., Youngblood J.P. (2007) Self-cleaning and anti-fog surfaces via stimuli-responsive polymer brushes, Adv. Mater. 19, 3838. [9] Li J.J., Zhou Y.N., Luo Z.H. (2015) Smart fiber membrane for pH-induced oil/water separation, ACS Appl. Mater. Interfaces 7, 19643. [10] Lin J., Chen X., Chen C., Hu J., Zhou C., Cai X., Wang W., Zheng C., Zhang P., Cheng J., et al. (2018) Durably antibacterial and bacterially antiadhesive cotton fabrics coated by cationic fluorinated polymers, ACS Appl. Mater. Interfaces 10, 6124. [11] Bormashenko E. (2015) Progress in understanding wetting transitions on rough surfaces, Adv. Colloid Interface Sci. 222, 92. [12] Zuo Y., Zheng L., Zhao C., Liu H. (2020) Micro-/nanostructured interface for liquid manipulation and its applications, Small 16, 201903849. [13] Sun Y., Guo Z. (2019) Recent advances of bioinspired functional materials with specific wettability: From nature and beyond nature, Nanoscale Horiz. 4, 52. [14] Zhang H., Hou C., Song L., Ma Y., Ali Z., Gu J., Zhang B., Zhang H., Zhang Q. (2018) A stable 3D sol–gel network with dangling fluoroalkyl chains and rapid self-healing ability as a long-lived superhydrophobic fabric coating, Chem. Eng. J. 334, 598. [15] Deka B.J., Lee E.J., Guo J., Kharraz J., An A.K. (2019) Electrospun nanofiber membranes incorporating PDMS-aerogel superhydrophobic coating with enhanced flux and improved antiwettability in membrane distillation, Environ. Sci. Technol. 53, 4948. [16] Li D.-W., Wang H.-Y., Liu Y., Wei D.-S., Zhao Z.-X. (2019) Large-scale fabrication of durable and robust super-hydrophobic spray coatings with excellent repairable and anti-corrosion performance, Chem. Eng. J. 367, 169. [17] Wang S., Li D., Zhou Y., Jiang L. (2020) Hierarchical Ti3C2Tx MXene/Ni chain/ZnO array hybrid nanostructures on cotton fabric for durable self-cleaning and enhanced microwave absorption, ACS Nano 14, 8634. [18] Celik N., Torun I., Ruzi M., Esidir A., Onses M.S. (2020) Fabrication of robust superhydrophobic surfaces by one-step spray coating: Evaporation driven self-assembly of wax and nanoparticles into hierarchical structures, Chem. Eng. J. 396, 125230. [19] Li Y., Li B., Zhao X., Tian N., Zhang J. (2018) Totally waterborne, nonfluorinated, mechanically robust, and self-healing superhydrophobic coatings for actual anti-icing, ACS Appl. Mater. Interfaces 10, 39391. [20] Wu M., Ma B., Pan T., Chen S., Sun J. (2016) Silver-nanoparticle-colored cotton fabrics with tunable colors and durable antibacterial and self-healing superhydrophobic properties, Adv. Funct. Mater. 26, 569.
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[21] Yin X., Mu P., Wang Q., Li J. (2020) Superhydrophobic ZIF-8-based dual-layer coating for enhanced corrosion protection of Mg alloy, ACS Appl. Mater. Interfaces 12, 35453. [22] Jiang G.S., Luo L.Q., Tan L., Wang J.L., Zhang S.X., Zhang F., Jin J. (2018) Microsphere-fiber interpenetrated superhydrophobic PVDF microporous membranes with improved waterproof and breathable performance, ACS Appl. Mater. Interfaces 10, 28210. [23] Li X., Yu X.F., Cheng C., Deng L., Wang M., Wang X.F. (2015) Electrospun superhydrophobic organic/inorganic composite nanofibrous membranes for membrane distillation, ACS Appl. Mater. Interfaces 7, 21919. [24] Zhu R., Liu M., Hou Y., Zhang L., Li M., Wang D., Fu S. (2020) One-pot preparation of fluorine-free magnetic superhydrophobic particles for controllable liquid marbles and robust multifunctional coatings, ACS Appl. Mater. Interfaces 12, 17004. [25] Zhang X., Liu S., Salim A., Seeger S. (2019) Hierarchical structured multifunctional self-cleaning material with durable superhydrophobicity and photocatalytic functionalities, Small 15, e1901822. [26] Yada M., Inoue Y., Sakamoto A., Torikai T., Watari T. (2014) Synthesis and controllable wettability of micro- and nanostructured titanium phosphate thin films formed on titanium plates, ACS Appl. Mater. Interfaces 6, 7695. [27] Zhang W., Shi Z., Zhang F., Liu X., Jin J., Jiang L. (2013) Superhydrophobic and superoleophilic PVDF membranes for effective separation of water-in-oil emulsions with high flux, Adv. Mater. 25, 2071. [28] Wang H., Song L., Jiang R., Fan Y., Zhao J., Ren L. (2020) Super-repellent photodynamic bactericidal hybrid membrane, J. Membr. Sci. 614, 118482. [29] Jiang H.B., Liu Y.Q., Zhang Y.L., Liu Y., Fu X.Y., Han D.D., Song Y.Y., Ren L., Sun H.B. (2018) Reed leaf-inspired graphene films with anisotropic superhydrophobicity, ACS Appl. Mater. Interfaces 10, 18416. [30] Zhao H., Park K.C., Law K.Y. (2012) Effect of surface texturing on superoleophobicity, contact angle hysteresis, and “robustness”, Langmuir 28, 14925. [31] Wang Y., Xue J., Wang Q., Chen Q., Ding J. (2013) Verification of icephobic/anti-icing properties of a superhydrophobic surface, ACS Appl. Mater. Interfaces 5, 3370. [32] Yu Z., Ji Z., Tao D., Zhang Q., Liu R. (2020) Research on a reversible superwetting behavior and its corrosion resistance, Appl. Surf. Sci. 517. [33] Ellinas K., Pujari S.P., Dragatogiannis D.A., Charitidis C.A., Tserepi A., Zuilhof H., Gogolides E. (2014) Plasma micro-nanotextured, scratch, water and hexadecane resistant, superhydrophobic, and superamphiphobic polymeric surfaces with perfluorinated monolayers, ACS Appl. Mater. Interfaces 6, 6510. [34] Li L., Breedveld V., Hess D.W. (2013) Design and fabrication of superamphiphobic paper surfaces, ACS Appl. Mater. Interfaces 5, 5381.
Chapter 9 Bioinspired Mechanical Bactericidal Surfaces Recently, a novel approach to combat bacterial contamination has emerged: biomaterial surfaces with topographical features with high aspect ratios have potent bactericidal activity against bacteria. The antibacterial activity of such surfaces has been attributed to the physical interactions between the nanopatterned substrate and the attached bacterial cells, meaning that such activity is independent of biochemical surface functionality [1]. Consequently, such a physical bactericidal method has become an attractive approach for tackling multi-antibiotic-resistant bacteria [2]. This section will summarize the latest research on natural and bioinspired nanostructured bactericidal surfaces, while the understanding of the lethal mechanisms, nanostructures fabrications, and particularly regarding the artificial analog applications will be emphatically presented.
9.1
Naturally Occurring Nanostructured Bactericidal Surfaces
Natural surfaces have developed their protective mechanisms over the past hundreds of million years. For example, surfaces with micro- and nano-structural features can afford a broad spectrum of favorable properties, often including antireflection, superhydrophobicity, and antifouling properties. More recently, several studies have revealed that natural superhydrophobic surfaces also demonstrate bactericidal performances. The first and one of most famous examples of the naturally occurring mechano-bactericidal surface, cicada wings, was reported in 2012 by Ivanova et al. (figure 9.1a–e) [3]. The spherically capped nanopillars presented on the wings could immediately penetrate the Pseudomonas aeruginosa (P. aeruginosa) cells upon cell attachment, killing most of them within 5 min. The bactericidal effect of the wing surface coated with gold film ( 10 nm) was still preserved even after changing the surface chemistry and hydrophobicity, demonstrating that the lethal mechanism of the wing for P. aeruginosa cells is purely based on the surface structure instead of DOI: 10.1051/978-2-7598-2941-5.c009 © Science Press, EDP Sciences, 2023
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the surface chemical features. This expands a completely new area of research to the production of mechanical bactericidal surfaces. To further reveal the correlation of the surface topography with the bactericidal property of cicada wings, S. M. Kelleher et al. studied the wing surface bactericidal capacity of three different species of cicada (Megapomponia intermedia, Ayuthia spectabile, and Cryptotympana aguila) against P. aeruginosa. Bacterial cell testing showed that compared with wings of Ayuthia spectabile, Megapomponia intermedia, the Cryptotympana aguila with tighter packing and more sharpness nanopillars presented a greater bactericidal activity which was primarily attributed to a greater amount of nanopillars contacting the bacterial cell [4]. On the other hand, Hasan et al. provided further insights into the interaction between one cicada (P. claripennis) wing surface and a wide spectrum of bacteria with different morphologies (rod-shaped vs. coccus) and cell wall types (Gram-positive vs. Gram-negative bacteria). The result demonstrated that the nanostructure of the wings surface can effectively rupture Gram-negative cells, regardless of the morphology, while Gram-positive bacteria were found to remain resistant [5]. The disconformity of the bactericidal behaviors was supposedly attributed to the dissimilar constitution of the cell walls between Gram-negative and Gram-positive bacteria. It is well-known that the peptidoglycan cell wall of Gram-positive bacteria was 4–5 times thicker than that of Gram-negative species, which requires greater deformational stress to disrupt the cell wall and cause cell death [6].
FIG. 9.1 – (a) Image of Psaltoda claripennis; (b) Structural physiology of the cicada forewing; (c) SEM image of the upper surface of the forewing; (d) P. aeruginosa cells on the surface of a cicada wing; (e) SEM image of a P. aeruginosa cell sinking between the nanopillars on the cicada wing surface at an angle of 53° [3] (Adapted with permission from [3], Small, 2012, 8, 2489. Copyright © 2012 John Wiley and Sons).
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Based on the underlying physical bactericidal principle of cicada wings patterned with spherically capped, conical, nano-scale pillars, it can be supposed that other surfaces possessing nanopatterned characteristics may exhibit similar bactericidal action. Following the report of mechano-bactericidal properties of cicada wings, Ivanova et al. revealed that dragonfly (Diplacodes bipunctata) wings patterned with nanostructures distributed at random (in terms of shape, size, and distribution) presented surpassing bactericidal performance compared with cicada wings (figure 9.2a–c). More importantly, the formation of adjacent nanoprotrusions in a high density on the surface of D. bipunctata wings formed hierarchical structures, which were proven to efficiently kill both Gram-negative (P. aeruginosa) and even Gram-positive bacteria (S. aureus and B. subtilis) [6]. The improved bactericidal performance of dragonfly wings was attributed to the sigmoidal clusters composed of
FIG. 9.2 – (a) SEM image of the upper surface of dragonfly forewings; (b, c) SEM images of P. aeruginosa and S. aureus (Reproduced with permission from [6], Nat. Commun., 2013, 4, 2838. Copyright © 2013 Springer Nature).
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secondary structures on the surface which could impose a greater capillarity to the contacted cells, as a result, inducing the increase of the cell deformation and cell wall stress. Through investigating three dragonfly species (D. bipunctata, H. papuensis, and A. multipunctat) that inhabit similar environments and differ in their physical morphology, a more detailed interaction between dragonfly wings and bacteria was revealed. Compared with its counterparts, the topology of D. bipunctata wing had a significantly higher gradient of curvature and presented a more efficient bactericidal behavior. Modeling the interaction between bacterial cells and the wing surface lipids of 3 species of dragonflies suggested that the D. bipunctata wing surface provides both a distinctly greater achievable force into the nanocolumn topography and also a higher force gradient with penetration. It is suggested that an obviously greater achievable force into the nanostructure as well as a higher force gradient with penetration can be furnished by the D. bipunctata wing surface through simulating bacterial cells contacting the wing surface lipids of 3 species of dragonflies. Those together promoted the excellent bactericidal property of D. bipunctata wing [7]. Over thousands of years of evolution, microorganisms have optimized mature strategies for desired colonization on abiotic surfaces. In contrast, many surfaces in nature are found to be immune to pathogenic contamination. Apart from the cicada and dragonfly, the wings of damselfly (Calopteryx haemorrhoidalis) and planthopper (Desudaba danae) were also reported to be lethal against the contracted bacteria. The observation of bacterial behaviors on damselfly wings demonstrated that the nanostructured wing surface could vary the susceptibility of the rigidity of the bacterial cell walls of both S. aureus and P. aeruginosa, leading to the mechanical rupture of bacterial cells [8]. On the other hand, planthopper insect wings have similar morphology compared to the lotus leaf surface structure. They exhibit remarkable nonwetting properties and low adhering forces with contaminants in conjunction with the capacity of mechanical bactericidal even subjected to incessant attacks of bacterial colonization over 7 days (figure 9.3a–d). Moreover, the hierarchical planthopper surface demonstrated compatibility for mammalian cells (e.g., among human stem cells and dermal fibroblasts) which could support eukaryote cell attachment, division, and growth [9]. It seems reasonable that insect wings have a bactericidal function which is able to prevent the accumulation of microbial. Therefore, the lightweight of the insect wing can be maintained during flight [10]. Intriguingly, the skin of gecko lizards is bactericidal in the same mechanism as their nano-tipped hairs termed spinules [11, 12]. The gecko skin surface with fewer spinule/nanopillars packing density (2–4 spinules per μm2) and larger spacing (*500 nm) compared with the cicada wing surface presented superior bactericidal properties which could induce bacterial cells impairment and lethal to both Gram-negative and Gram-positive species. W. Green et al. proposed that although the spinules have similar tip apex dimensions compared to cicada pillars, they significantly broaden towards the base which may increase the contact area with bacteria in a non-linear fashion and thus play a significant factor in the bactericidal activity. Besides, an alternate hypothesized mechanism maybe account for the phenomena. Bacteria cells with a larger width
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FIG. 9.3 – SEM images of (a) natural gecko skin and (b) artificial replicas; (c) SEM image of P. gingivalis that are penetrated by replica spinules; (d) live and dead characterization of P. gingivalis cells on gecko replica at 3 days taken at a furrow region (Reproduced with permission from [12], Nanoscale, 2016, 8, 18860. Copyright © 2016 The Royal Society of Chemistry). than spinule spacing could sit directly on top of the spinule nanotips and undergo gradual penetration from interacting with the outer cell layer or extracellular substances. In contrast, bacterial cells with smaller dimensions will undergo complex interactions, including stretching, compressing, tearing, or disrupting the bacterial cell wall. Additionally, the spinules and rib arrays topography features on the gecko skin surface may conduce to the increase of bacterial impairment and death through compression and stretching, together with activating synergistic responses and stress on the bacterial cells (figure 9.2f–i) [12]. More and more comprehensive structure-based bactericidal surfaces have been discovered and reported with further studies. More recently, the widely-known superhydrophobic lotus leaf surface was proved to be capable of both bacterial repelling and mechano-bactericidal (figure 9.4a–d) [13]. It is well known that the excellent antifouling performance of the lotus leaf surface was ascribed to the surface construction consisting of micro-sized papillae and nano-sized wax tubes, from which a stable air layer can be entrapped at the solid–liquid interface. For many years, people have only been concerned about the contribution of nanostructures on the lotus leaf surface to the roughness increase and its improvement of superhydrophobic performance. However, it must also be noted that living in a humid environment where microorganisms are easy to propagate and continuous exposure
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FIG. 9.4 – (a) Digital photograph of superhydrophobic lotus leaves and the water droplet on the lotus leaf; (b) SEM image of a lotus leaf at 45° tilting angle; (c) SEM images demonstrate the deformation of E. coli cells at fresh lotus leaf; (d) CLSM images of E. coli cells attached on lotus leaves (Reproduced with permission from [13], Chem. Eng. J., 2020, 398, 125609. Copyright © 2020 Elsevier B.V.). of the surface to these environmental contaminants, lotus leaves can hardly keep their large leaves standing on the water for a long time without being invaded by microorganisms just depending on the passive-defense of air cushion. Inspired by the mechano-bactericidal principles, Zhao and coworkers envisaged that this superhydrophobic surface might also hold similar bactericidal activities that take advantage of the mechanical killing mechanism, just like the mechano-bactericidal surfaces of insect wings. Gram-negative bacteria E. coli was chosen as the representative microorganism to verify this theory to explore bacterial repellency and bactericidal properties. The results revealed that the lotus leaf surface demonstrated excellent anti-adhesion activity against a high concentration of bacterial medium (108 cells mL−1) in the initial 3 h incubation. A time-related increase in bacterial adhesion on the superhydrophobic leaf surface is observed with prolonged incubation. The morphology of adhered bacteria is highly deformed and the cellular components are engulfed by the spaces between nanotubes which are very similar to those on dragonfly or cicada wings. To identify the bactericidal mechanism, a non-toxic gold layer ( 10 nm) was sputter-coated onto the lotus leaf surface to change the surface chemistry. In contrast, the surface bactericidal activity was unaffected by this surface modification. Moreover, the inhibition zone was nonexistent which means that the leaked chemical components are not responsible for the bacteria death. Those together demonstrated that the bactericidal property was a purely physical action. Furthermore, the conclusions could trigger deeper thought of the structure with
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bactericidal ability since the random-arranged nanotubes are rather different from cicada wing bactericidal structures with vertical arrangement [13]. Similarly, one of the famous slippery surfaces, nepenthes, was found to be an effective mechanical bactericidal platform. Different from traditional mechano-bactericidal surfaces relying mainly on nanopillars/columns to exert adverse influences on the contacted bacteria, nepenthes surfaces performed the bactericidal action through the particular nano-dagger arrays (figure 9.5a–c) [14].
FIG. 9.5 – (a) SEM images of pristine Nepenthes; CLSM images and bactericidal performance statistical results of (b) E. coli and (c) S. aureus on NSZ surface (Reproduced with permission from [14], RSC Adv., 2019, 9, 27904. Copyright © 2019 The Royal Society of Chemistry).
9.2
Bactericidal Mechanism
According to physical models and related experimental studies, it has been revealed that the mechanism responsible for cell death at nanostructured surfaces is mechanical rather than chemical compound interaction. However, the exact killing mechanism and the role of various factors in regulating the bactericidal behavior of nanopatterns remains to be not conclusively determined, as the result of the interactions between the nanostructured surface and bacteria cells are multi-faceted. In this section, we summarized the recent progress being made towards delineating the basis of these mechanical antimicrobial mechanisms. By coating the surface with a 10 nm thick gold film, P. Ivanova et al. firstly demonstrated that the bactericidal capacity of the cicada wing is physical in their initial report about the mechanical bactericidal study. They concluded that the physical structure of cicada wing surfaces is responsible for bacterial lethality instead of any surface chemical factors [3]. Pogodin et al. [15] built a biophysical simulative model to illustrate the interaction between bacterial cells and the nanostructure of cicada wing surfaces (figure 9.6). By changing the rigidity of surface-resistant strains by microwave irradiation of the cells, they demonstrated that mechanical properties, particularly cell rigidity, are critical factors in determining bacterial resistance/sensitivity to the bactericidal nature of the wing surface. In other words, if a degree of stretching to the bacterial cells adsorbed on the nanopillar is sufficient, cell rupture and death can be realized. This study confirmed that the bactericidal mechanism of the cicada wing was certainly biophysical and no specific biological interaction was implied directly, which was consistent with the bactericidal result of surfaces coated by the gold film.
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FIG. 9.6 – (a) SEM of the surface of a cicada wing as viewed from above; (b–e) The physical interaction between a bacteria cell and the nanostructure on cicada wing surface [15] (Reproduced with permission from [15], Biophys. J., 2013, 104, 835. Copyright © 2013 Biophysical Society). Li et al. [16] conducted amounts of investigation on the total free energy change of bacterial cells on different morphological substrates and then built a thermodynamic model to explore the bactericidal mechanism of nanopatterned surfaces. Their results demonstrated that cicada wing-like nanopatterned surfaces could significantly increase the contact adhesion area than flat surfaces, which was responsible for the more effective bactericidal properties of the structured surface. Based on this conclusion, they proposed that the bactericidal efficiency could be enhanced by appropriately increasing the surface roughness, i.e., increasing the surface distribution density, radius, and height of nanopillars. Dickson et al. [17] drew a similar conclusion through the experimental results. They found that the percentage of dead cells could increase by 97% on nanopillar surfaces with a spacing of 130 nm and a 114% increase could be measured on surfaces with a spacing of 100 nm while enlarging the space of nanopillars to 380 nm led to only 16% increase of the dead bacteria compared with that on the flat substrates. Linklater et al. [18] developed a series of nanopillars patterned surfaces with linearly increasing heights of approximately 280, 430, and 610 nm, respectively to study the influence of nanoscale topology on bactericidal efficiency. The results showed that the highest number of adhered cells was seen on the tallest pillars (approximately 23 000 cells mm−2). In contrast, the smaller pillars are more effective in inhibiting the adhesion for both Gram-negative and Gram-positive bacteria. Moreover, nanopillars with a height below 300 nm, approximately 60 nm tip diameter, and approximately 60 nm spacing could perform more effective bactericidal properties than larger features. Cui et al. [19] demonstrated that the bactericidal surfaces require a critical height of nanostructure, *200 nm, meanwhile, an optimal range of interpillar spacing ( 170 nm) and a smaller cap diameter (less than 60 nm) will result in the high bactericidal activity (figure 9.7). More recently, P. Ivanova et al. [20] revealed that the mechanical lysis of bacterial cells could be induced by releasing elasticity force stored in the deflected and deformed nanopillars. Increasing the pillar height from 220 to 360 and 420 nm could lead to the mechanical energy stored in the pillars increasing by one order of magnitude, which could produce excellent bactericidal activity that leads to 95 ± 5% and 83 ± 12% cell death for Gram-negative Pseudomonas aeruginosa and Gram-positive S. aureus, respectively.
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FIG. 9.7 – (a) Illustration of the fabrication procedure for PC nanopillar surfaces by AAO template-assisted hot embossing and wet etching; (b) SEM images showing the nanotopography of PC surfaces; (c, d) SEM image and representative fluorescence of E. coli bacterial cells on nanostructured PC surfaces: 300 nm of interpillar spacing (Reproduced with permission from [19] ACS Appl. Nano Mater., 2020, 3, 4599. Copyright © 2020 American Chemical Society).
Although many reports emphasized that the bacterial death on the nanostructured surfaces resulted from direct physical interactions, some studies described a different story. D. Bandara et al. [21] utilized advanced microscopy techniques to investigate the nanotopography and mechanical properties of the dragonfly wing nanopillars. The events occurring at the interface between a bacterial cell and the nanostructure were successively observed. They revealed that the adhesion of bacteria to the nanopillars was mediated by the secreted extracellular polymeric substance (EPS), rather than the direct contact between the bacterial cell membrane and nanopillars as the EPS is filled between the nanopillars and the cells membrane. A separation of the inner-cell membrane from the outer-cell membrane would thus be induced as the movement of bacteria occurred, owing to the strong adhesion of the bacteria onto a surface through the EPS. Ultimately, the membrane damage and cell cytoplasm leak could be observed. Accordingly, they illustrated the dragonfly wing nanostructure bactericidal activity with two mechanisms. The first is the strong adhesive force between bacteria and the nanostructure while the other is the shear force when immobilized bacteria attempts to move on the nanostructured surfaces. However, an opposing opinion about this result was declared by the group of P. Ivanova [22]. They developed two types of silicon surfaces with different
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wettability (superhydrophilic and superhydrophobic) and observed that approximately 84% and 98% killing efficiency against P. aeruginosa could be realized on hydrophilic and hydrophobic silicon surfaces respectively Additionally, similar killing efficiencies were observed for S. aureus (figure 9.6e–i). This result demonstrated that the adhesion affinity or force between bacteria cells and the surface nanostructure was not the key motivation to induce the mechanical bactericidal capacity. In addition, they observed that the bacterial rupturing upon contact with cicada wing surfaces takes between 3 and 5 min, during which the EPS had not been secreted. Thereby, this work believed that cellular affinity for a surface or motility of bacterial cells did not determine the bactericidal efficacy and EPS was not necessary for the mechano-bactericidal action of nanostructured surfaces. A significant finding about the mechano-bactericidal phenomena was reported recently by Valiei et al., through real-time and end-point analysis techniques. They found that bacteria on multiple hydrophilic nanostructured surfaces could remain viable unless exposed to a moving air–liquid interface, which caused considerable cell death. They proved external forces that may be applied either by design or inadvertently to be vital in driving rapid cell death on nanopillar surfaces (figure 9.8) [23]. Besides this external force, Jenkins et al. demonstrated that oxidative stress within bacterial cells upon contact with the mimetic titanium nanopillars could mediate the antibacterial activities. The rupture or lysis of bacterial cells was not required for bacteria death on nanopillars’ structured surfaces [24]. These findings provide a better understanding of mechano-mechanism bactericidal properties and could afford us invaluable references to improve the antibacterial performance of nanotextured materials.
FIG. 9.8 – (a, b) SEM images of P. aeruginosa morphology on NanoSi and flat Si at the wet and after water evaporation; (c) Bacterial viability as a function of time on NanoSi and flat Si subject to evaporation (Adapted with permission from [23], Nano Lett., 2020, 20, 5720. Copyright © 2020 American Chemical Society).
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Artificial Mechanical Bactericidal Surfaces and Fabricating Technologies
Naturally occurring bactericidal surfaces have provided that surfaces bearing a continuous array of high aspect-ratio nano-architectures can prevent bacteria colonization or biofilm formation in a mechanical way. Inspired by this, benefiting from the development of the nanostructure fabrication techniques, researchers have constructed a number of two-dimensional or even three-dimensional bioinspired antimicrobial substrates, such as black silicon, titania nanowire arrays, Ti alloy nanospike, Au nanostructured surface, nanopatterned polymer, and a lotus leaf-like artificial surfaces. Several most commonly used nanofabrication methods and some recent advances made in the fabrication of bio-inspired bactericidal surfaces will be described in detail next. Taking advantage of the reactive ion etching technology, Ivanova et al. developed the first biomimetic example of black silicon nano-patterned surface to mimic dragonfly wings (figure 9.9) [6]. Different from the cicada wing topography showing a regular array of pillars 50–70 nm in diameter, spaced 200 nm apart, the nanoprotrusions presented on the dragonfly wing surfaces and the artificial analog, black silicon surfaces, showed a random size with a bimodal distribution spanning 20–80 nm. The spatial distributions of both black silicon and dragonfly wing clusters ranged from 200 to 1800 nm in diameter, which arises from the randomness in their perimeters, demonstrating the presence of a more significant number of more complex, more acceptable clusters. The antibacterial results demonstrated that the
FIG. 9.9 – (a) SEM images of the upper surface of bSi; (b) Optical profilometry shows the nanoprotrusions of bSi; (c, d) SEM images of P. aeruginosa, S. aureus appear to be significantly disrupted through interaction with the bSi (Reproduced with permission from [6], Nat. Commun., 2013, 4, 2838. Copyright © 2013 Springer Nature).
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synthetic antibacterial nanomaterials, nanostructured black silicon surface, exhibited comparably effective bactericidal performance to the naturally occurring dragonfly wing which was highly bactericidal against all tested Gram-negative bacteria, Gram-positive bacteria, and endospores. Such findings provide opportunities for developing new approaches to fabricating or designing a range of synthetic, mechano-responsive bio-inspired antimicrobial surface analogs [1]. M. Bhadra et al. [25] designed amounts of black silicon surfaces with a variety of pillar heights (ranging from 652.7 to 1063.2 nm) and density (ranging from 8 to 11 tips per μm2) using deep reactive ion etching to explore the relationship between the nanopattern parameters of the black silicon surface and the bactericidal efficiency. Although the fabricated three types of black silicon surfaces have a nano-architecture with visual similarity, including undistinguishable topology from the top view analysis, the bactericidal performance could substantially alter due to minor variations in the nano-architecture of substrata. Interestingly, the surface with the tallest pillars reaching 1000 nm presented less bactericidal efficiency than that of the surface that possessed shorter pillars. They demonstrated that the highest bactericidal efficiency correlated with the combination of different parameters rather than the effect imparted by a single nano-topographic parameter. Apart from investigating the interaction of bacteria with bare nanostructured black silicon surfaces, some studies have constructed synergistic antibacterial surfaces in combination with mediated bactericidal properties and chemical antibacterial effects. Tripathy et al. observed the different bacterial cell morphologies between a bare nanostructured black silicon surface and an ultrathin metal-coated surface to study the bacterial lethality of the synergistic nanostructured surface [26]. They first used the deep reactive ion etching method to fabricate tall (8–9 μm high) nanostructures with sharp tips (35–110 nm) on silicon surfaces. Subsequently, a thin copper layer (*20 nm) was sputtered through an E-beam evaporator process. After being co-cultured with the as-prepared surfaces, the bacteria on the coated and uncoated nanostructured silicon surface exhibited distinct morphologies, which seems the extent of bacterial cells stretching increased from the Cu layer modified nanostructured surface to bare nanostructured surface. It is interestingly found that the Cu-coated surfaces displayed improved killing efficiency when compared to the uncoated counterpart. Such phenomena could be attributed to Cu ions that anchored on the nanostructured surface imposed an adverse effect on the cell wall, which is easily ruptured due to the physical interaction with the nanostructures. Similarly, Tripathy et al. combined the deep reactive ion etching technique with a layer-by-layer dip-coating process fabricating chitosan-modified organic–inorganic hybrid nanostructured silicon surface. This hybrid surface exhibited superior antibacterial properties against Gram-negative and Gram-positive bacteria compared with regular flat silicon coated with chitosan and bare nanostructures [27]. Those studies provide examples that weak biocidal agents’ antibacterial and antibiofilm efficiency can be augmented by combining them with a sharp nanomorphology. The reactive ion etching technique is a common and suitable method for fabricating nanostructures on the silicon surface, however, it will be powerless for other substrates, such as metal or polymer materials. Alternatively, as an environmentally friendly method, the alkaline hydrothermal etching technique is usually applied
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under controlled temperature and pressure to construct nanostructures on metal substrates. Among those, due to the excellent inherent property (including biocompatibility, mechanical stability, and osseointegration) titanium and its alloys have emerged as the most popular choice of implant materials applied to medical equipment including orthopedic and dental implants. However, the two main issues are bacterial infection and lack of tissue cell adhesion while using titanium and titanium alloy based orthopedic implants [28]. Hence, surfaces equipped with the capability to exhibit differential responses to bacterial and eukaryotic cells represent excellent prospects for biomedical applications. To this end, Diu et al. developed two types of engineered titania arrays, persistent nanowire coverage (brush type) and isolated nanowire pockets (niche type), on titanium surfaces taking advantage of the alkaline hydrothermal etching technique. Homogenously dense coverage of spike-like titania nanowires with an averaged diameter of ca. 100 nm and heights of ca. 3 mm were generated through a three-hour hydrothermal treatment (240 °C). Prolonging the hydrothermal treatment to eight hours produced the niche surface, which contained longer structures with intertwined tips and formed dispersed niches or pockets. These niches were ca. 10–15 μm in diameter and peaked at ca. 3 μm. They found that the persistent nanowire (brush type) patterned surface is sufficiently dense for mammalian cells to proliferate and much smaller bacterial cells that can be trapped and even inactivated by the nanowire arrays. The isolated pockets in the niche type are easily colonized by bacteria but are not sufficiently large to confine mammalian cells and arrest their spreading. Additionally, the bactericidal capacity of surface nanostructure against motilebacteria (P. aeruginosa, E. coli, and B. subtilis) was more remarkable than that against nonmotile species (S. aureus, E. faecalis, and K. pneumonia) (figure 9.10) [29].
FIG. 9.10 – (a) SEM image of niche type patterns; (b, c) SEM images of nanowire-pierced bacterial cells after coculture for one hour; (d) Fluorescence micrographs of bacterial cells incubated on brush type surface for one hour (Reproduced with permission from [29], Sci. Rep., 2014, 4, 7122. Copyright © 2014 Springer Nature).
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Further, M. Bhadra et al. [30] provided more details about the surface properties such as surface topography features and wettability that play roles in the bacteria cell attachment process. They revealed that the nano-wire arrays patterned titanium surface exhibited a contrary tendency of cell attachment. Bacteria prefer to attach on the flat titanium surface, while a much larger number of fibroblast cells could be reached on the nano-wire arrays patterned surface. Interestingly, after 10 days of incubation, although there was no difference in the overall cell coverage area on the flat and patterned surfaces, it was observed that a significant quantitatively increase of fibroblast cells attaching to the patterned surface was observed. To achieve superior antibacterial efficacy of the nanostructured titanium surface, V. Wandiyanto et al. [31] systematically tuned the morphology of the nanostructures by controlling hydrothermal etching time ranging from 0.5 to 60 h. They demonstrated that the surface treated by 6 h of alkaline hydrothermal etching could achieve the utmost antibacterial efficiency of 99 ± 3% against Gram-negative P. aeruginosa and 90 ± 9% against Gram-positive S. aureus. Until their report, the nanotopographies fabricated in the work represented the most efficient mechano-bactericidal capacity of nanostructured titanium topography against both bacteria strains. It has been mostly stressed that the antibacterial activity on nanostructured surfaces can be interpreted as the interaction between the cell and nanopillars with a relatively high-aspect ratio through a mechano-bactericidal mechanism, which possesses no lethal selectivity. Such surfaces could thus have considerable potential to fight against bacterial multidrug resistance. However, until now few available literature have demonstrated that nanostructures could effectively inactivate multidrug-resistant bacteria. V. Wandiyanto et al. [32] carried out precursory work in that they investigated the interactions between hydrothermal etched nanostructured titanium surfaces and bacteria strains with susceptiblility or resistance to antibiotics. The nanostructured titanium surfaces proved to be equally effective and highly bactericidal against both the susceptible and resistant S. aureus strains, with killing efficiencies of 80.7% ± 12.0 and 86.8% ± 11.6, respectively. This result confirmed that the mechano-bactericidal activity of these nanostructured titanium surfaces could show enormous potential to cope with multidrug-resistant bacteria that put medical industries at great risk. The mentioned nanofabrication techniques, reactive ion etching, deep reactive ion etching, and alkaline hydrothermal etching have paved the way for developing novel opportunities to fabricate nanostructures restricted only to inorganic nonmetal and metal substrates. In contrast, flexible polymer substrates cannot be realized. In certain situations, the nanostructures on solid surfaces are challenging to apply to existing inanimate surfaces and equipment. In this regard, polymeric nanostructured films are promising alternatives because they can be readily attached to any surface as protection films for a window. To mimic cicada wings, Dickson et al. [17] used a scalable process, the nanoimprint lithography technique, showing the first example of constructing biomimetic bactericidal polymer nanopillars with varying periodicity on the surfaces of poly (methyl methacrylate) (PMMA) films. Their findings demonstrated optimal nanopillars space ranging between 130 and 380 nm against E. coli proliferation, whereas periodicity of 600 nm caused noticeably less cell death. Kim et al. [33] reported multifunctional nanopillars
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patterned PMMA surfaces with a period of 300 nm and an aspect ratio of 3.0 through thermal nanoimprint lithography. The obtained nanoimprinted hydrophobic polymer film exhibited desired optical characteristics with less than 0.5% reflectance. It displayed lower bacteria and mammalian cell adhesion and higher bactericidal properties than the corresponding flat surface (figure 9.11).
FIG. 9.11 – (a) Schematic illustration for the design of multifunctional nanostructures; (b) SEM images of the nanostructured surface; (c, d) Fluorescence microscopic images of the bacterial cells and the mammalian cells on the nanostructured surfaces (Adapted with permission from [33], ACS Appl. Mater. Interfaces, 2015, 7, 326. Copyright © 2015 American Chemical Society).
The template method is another widely used simple fabrication strategy to develop bactericidal nanostructured polymer surfaces. The technique uses substrates in different textures (e.g., bio-species bodies, nanopatterned silicon substrate, and anodic aluminum oxide templates) to act as replica surfaces for imprinting surface structures into a polymeric nano-emboss [1]. Tsui et al. [34] prepared flexible polystyrene antibacterial films with precisely controlled three-dimensional (3D) nanopyramid arrays on the surface by tuning the structures of the inverted nanopyramid templates. The fabricated nanopyramids patterned hydrophobic films with a water contact angle of 120° exhibited an outstanding antibacterial performance that more than a 90% decrease of the bacterial contamination could be realized even incubated in a relatively high concentration of bacterial suspension (1 × 109 cells per mL) for 168 h. This study provides a facile example to manufacture large-scale, flexible nanostructured films with controllable
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topological features. Cui et al. [19] fabricated a series of highly controllable nanometer-scale characteristic polycarbonate (PC) surfaces by anodic aluminum oxide template-assisted hot embossing and wet etching. Through systematically and independently investigating the height, diameter, and interspacing of the nanopatterned surface, they concluded that *200 nm is the critical height of nanostructures that was able to kill bacteria. Additionally, the highest bactericidal rates (98.4% for E. coli) were found in the nanostructures with 170 nm of interpillars spacing less than 60 nm of cap diameter, and above 200 nm of height. This study indicated that nanostructures with larger and smaller interpillar spacing cannot exhibit excellent performance as bactericidal surfaces. An optimal range of interpillar spacing may be conducive to an excellent performance of the bactericidal activity. Despite the advances in micro/nanofabrication techniques as mentioned above, it is quite challenging to accomplish the fabrication of nanopatterns on a surface that is not restricted by substrate materials. Yi et al. [35] developed a simple and scalable strategy to create bactericidal nanopillars on various substrates, including zinc foil, galvanized steel, titanium, silicon, glass, ceramics, and PMMA. They found that the nanopillars fabricated on the zinc foil and galvanized steel surfaces exhibited superior bacteria-killing properties compared with that on the other substrates (figure 9.12). Unexpectedly, conventional nanostructures-based bactericidal surfaces are deadly only to adhered bacteria via rupturing mechanism, while ZnO nanopillars on zinc exhibited super bactericidal properties for both adhered and non-adhered bacteria. The mechanistic study showed that a high level of •O2− derived from the ZnO/Zn system is responsible for the super and remote antibacterial property of ZnO nanopillars on Zn.
FIG. 9.12 – (a) SEM image of ZnO nanopillars on glass slides; (b) SEM image of E. coli on ZnO nanopillar/zinc foil; (c) SEM images of P. aeruginosa on ZnO nanopillar/glass; (d, e) E. coli attached on ZnO nanopillars and Fluorescence live/dead assay of it (Reproduced with permission from [35], Small, 2018, 14, e1703159. Copyright © 2018 John Wiley and Sons).
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Recently, plasma etching, as a common technique used in the semiconductor industry, has demonstrated great potential in fabricating nanostructured bactericidal surfaces due to its high anisotropic nature, fine controllability, and excellent versatility to various materials [36]. Hazell et al. [37] constructed poly (ethylene terephthalate) nanocone array patterned films through a polystyrene nanosphere-mask colloidal lithographic process subsequently oxygen plasma etching (figure 9.13). The result showed that surfaces in the highest density of populated nanocone arrays (center-to-center spacing of 200 nm), high aspect ratios of more than 3, and tip widths less than 20 nm kill the highest percentage of bacteria (>30%). Mehrjou et al. [38] fabricated a homogeneous nanocones patterned surface on natural, biocompatible Bombyx mori silk films by means of oxygen plasma etching technology. After plasma treatment, this silk-based material was coated with close-packed hexagonal arrays of nanocones and become more hydrophilic, which led to a more than 90% reduction of bacterial attachment. More importantly, even the nanopatterned silk samples preinjected with bacteria suspension and then in conjunction with MC3T3 cells, this surface could still facilitate the proliferation of MC3T3 cells. This study provided a significant method to fabricate biocompatible materials with an intrinsic bactericidal property without extraneous chemical agents.
FIG. 9.13 – (a) Illustration of fabrication procedure of surfaces with polymer nanocone arrays; (b) SEM image of PET nanocone structures obtained for 200 nm PS colloidal mask through 10-min etching; (c) SEM image showing E. coli on PET nanocone surfaces; (d) CLSM images of plane PET film after co-incubation with E. coli for an hour (Reproduced with permission from [37], J. Colloid Interface Sci., 2018, 528, 389. Copyright © 2018 Elsevier B.V.).
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Inspired by the mechano-bactericidal activity of superhydrophobic lotus leaf, Jiang et al. [13] fabricated a hierarchical synergistic antibacterial surface with hierarchical microcylinders and nanoneedles via plasma etching and hydrothermal reaction. Such micro/nano-structured surfaces displayed a high water contact angle (>174°) and extremely low rolling angle (99%) that contact the surface will be repelled instead of adhering to the substrate (figure 9.14). During the contact between the bacteria cell and the surface with unique topography, those tenacious bacteria managed to be killed completely. This work not only demonstrated an example of constructing a physical bactericidal surface with three dimensions but importantly, exhibited a synergistic antimicrobial activity that could base entirely on the physical mechanisms, without causing any risks of antimicrobial resistance.
FIG. 9.14 – (a) Schematic illustration of procedure for fabricating the lotus-leaf inspired hierarchical antibacterial structured surface; (b) SEM image of microscale structure patterned silicon surface; (c, d) Representative SEM images showing the deformation of E. coli cells after co-incubation for 24 h (Reproduced with permission from [13], Chem. Eng. J., 2020, 398, 125609. Copyright © 2020 Elsevier B.V.).
9.4
Conclusions and Outlook
The effort to develop conventional antimicrobial agents has been currently overwhelmed by the rapid spread of antimicrobial resistance. Recently, naturally occurring surfaces like insect wings and plant leaves, which possess sharp nanostructures on their surfaces, are capable of killing bacteria by physically rupturing/stretching the cell wall via contact killing mechanism, representing an excellent prospect and template for developing novel antibacterial surfaces without triggering any antimicrobial resistance. Inspired by this, a series of artificial nanostructured surfaces such as nanostructured silicon, nanostructured titania, and
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nanostructured polymer surfaces are fabricated through advanced, simple, scalable, and versatile techniques. Give insight into bactericidal mechanisms of nanostructured surfaces, past works have confirmed that mechanical forces are responsible for damaging bacteria on nanopillars. However, the exact killing mechanism remains controversial, and the factors controlling the bactericidal efficiency are not ascertained completely. Thus, the correlation between bacteria cells and nanostructured surfaces needs further research to examine and could thus promote the optimization of surface parameters to improve the antibacterial performances. Additionally, and more importantly, before applying such mechano-bactericidal surfaces to practical biomedical implants surface modification, two inherent barriers should be overcome as follows. Firstly, after the bactericidal activity, the surfaces will then be contaminated with substances like dead bacteria cells and it would then fail to function as a bactericidal surface. Secondly, how to realize the selectivity of the nanostructured surfaces, i.e., benign or even functionally active towards mammalian cells but hostile towards bacteria.
References [1] Elbourne A., Crawford R.J., Ivanova E.P. (2017) Nano-structured antimicrobial surfaces: From nature to synthetic analogs, J. Colloid Interface Sci. 508, 603. [2] Tripathy A., Sen P., Su B., Briscoe W.H. (2017) Natural and bioinspired nanostructured bactericidal surfaces, Adv. Colloid Interface Sci. 248, 85. [3] Ivanova E.P., Hasan J., Webb H.K., Truong V.K., Watson G.S., Watson J.A., Baulin V.A., Pogodin S., Wang J.Y., Tobin M.J., et al. (2012) Natural bactericidal surfaces: Mechanical rupture of Pseudomonas aeruginosa cells by cicada wings, Small 8, 2489. [4] Kelleher S.M., Habimana O., Lawler J., O’reilly B., Daniels S., Casey E., Cowley A. (2016) Cicada wing surface topography: An investigation into the bactericidal properties of nanostructural features, ACS App. Mater. Interfaces 8, 14966. [5] Hasan J., Webb H.K., Truong V.K., Pogodin S., Baulin V.A., Watson G.S., Watson J.A., Crawford R.J., Ivanova E.P. (2013) Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces, Appl. Microbiol. Biotechnol. 97, 9257. [6] Ivanova E.P., Hasan J., Webb H.K., Gervinskas G., Juodkazis S., Truong V.K., Wu A.H., Lamb R.N., Baulin V.A., Watson G.S., et al. (2013) Bactericidal activity of black silicon, Nat. Commun. 4, 2838. [7] The nature of inherent bactericidal activity: Insights from the nanotopology of three species of dragonfly (2016), Nanoscale 8, 6527. [8] Truong V.K., Geeganagamage N.M., Baulin V.A., Vongsvivut J., Tobin M.J., Luque P., Crawford R.J., Ivanova E.P. (2017) The susceptibility of Staphylococcus aureus CIP 65.8 and Pseudomonas aeruginosa ATCC 9721 cells to the bactericidal action of nanostructured Calopteryx haemorrhoidalis damselfly wing surfaces, Appl. Microbiol. Biotechnol. 101, 4683. [9] Watson G.S., Green D.W., Cribb B.W., Brown C.L., Meritt C.R., Tobin M.J., Vongsvivut J., Sun M., Liang A.P., Watson J.A. (2017) Insect analogue to the lotus leaf: A planthopper wing membrane incorporating a low-adhesion, nonwetting, superhydrophobic, bactericidal, and biocompatible surface, ACS Appl. Mater. Interfaces 9, 24381. [10] Lin N., Berton P., Moraes C., Rogers R.D., Tufenkji N. (2018) Nanodarts, nanoblades, and nanospikes: Mechano-bactericidal nanostructures and where to find them, Adv. Colloid Interface Sci. 252, 55.
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[11] Watson G.S., Green D.W., Schwarzkopf L., Li X., Cribb B.W., Myhra S., Watson J.A. (2015) A gecko skin micro/nano structure – A low adhesion, superhydrophobic, anti-wetting, self-cleaning, biocompatible, antibacterial surface, Acta Biomater. 21, 109. [12] Li X., Cheung G.S., Watson G.S., Watson J.A., Lin S., Schwarzkopf L., Green D.W. (2016) The nanotipped hairs of gecko skin and biotemplated replicas impair and/or kill pathogenic bacteria with high efficiency, Nanoscale 8, 18860. [13] Jiang R., Hao L., Song L., Tian L., Fan Y., Zhao J., Liu C., Ming W., Ren L. (2020) Lotus-leaf-inspired hierarchical structured surface with non-fouling and mechanical bactericidal performances, Chem. Eng. J. 398, 125609. [14] Xie Y., Li J., Bu D., Xie X., He X., Wang L., Zhou Z. (2019) Nepenthes-inspired multifunctional nanoblades with mechanical bactericidal, self-cleaning and insect anti-adhesive characteristics, RSC Adv. 9, 27904. [15] Pogodin S., Hasan J., Baulin V.A., Webb H.K., Truong V.K., Phong Nguyen T.H., Boshkovikj V., Fluke C.J., Watson G.S., Watson J.A., et al. (2013) Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces, Biophys. J. 104, 835. [16] Li X. (2016) Bactericidal mechanism of nanopatterned surfaces, Phys. Chem. Chem. Phys. 18, 1311. [17] Dickson M.N., Liang E.I., Rodriguez L.A., Vollereaux N., Yee A.F. (2015) Nanopatterned polymer surfaces with bactericidal properties, Biointerphases 10, 021010. [18] Linklater D.P., Nguyen H.K.D., Bhadra C.M., Juodkazis S., Ivanova E.P. (2017) Influence of nanoscale topology on bactericidal efficiency of black silicon surfaces, Nanotechnology 28, 245301. [19] Cui Q., Liu T., Li X., Song K., Ge D. (2020) Nanopillared polycarbonate surfaces having variable feature parameters as bactericidal coatings, ACS Appl. Nano Mater. 3, 4599. [20] Ivanova E.P., Linklater D.P., Werner M., et al. (2020) The multi-faceted mechano-bactericidal mechanism of nanostructured surfaces, Proc. Natl. Acad. Sci. USA 117, 12598. [21] Bandara C.D., Singh S., Afara I.O., Wolff A., Tesfamichael T., Ostrikov K., Oloyede A. (2017) Bactericidal effects of natural nanotopography of dragonfly wing on Escherichia coli, ACS Appl. Mater. Interfaces 9, 6746. [22] Linklater D.P., Juodkazis S., Rubanov S., Ivanova E.P. (2017) Comment on “Bactericidal effects of natural nanotopography of dragonfly wing on Escherichia coli ”, ACS Appl. Mater. Interfaces 9, 29387. [23] Valiei A., Lin N., Bryche J.F., McKay G., Canva M., Charette P.G., Nguyen D., Moraes C., Tufenkji N. (2020) Hydrophilic mechano-bactericidal nanopillars require external forces to rapidly kill bacteria, Nano Lett. 20, 5720. [24] Jenkins J., Mantell J., Neal C., Gholinia A., Verkade P., Nobbs A.H., Su B. (2020) Antibacterial effects of nanopillar surfaces are mediated by cell impedance, penetration and induction of oxidative stress, Nat. Commun. 11, 1626. [25] Bhadra C.M., Werner M., Baulin V.A., Truong V.K., Kobaisi M.A., Nguyen S.H., Balcytis A., Juodkazis S., Wang J.Y., Mainwaring D.E., et al. (2018) Subtle variations in surface properties of black silicon surfaces influence the degree of bactericidal efficiency, Nanomicro. Lett. 10, 36. [26] Tripathy A., Sreedharan S., Bhaskarla C., Majumdar S., Peneti S.K., Nandi D., Sen P. (2017) Enhancing the bactericidal efficacy of nanostructured multifunctional surface using an ultrathin metal coating, Langmuir 33, 12569. [27] Tripathy A., Pahal S., Mudakavi R.J., Raichur A.M., Varma M.M., Sen P. (2018) Impact of bioinspired nanotopography on the antibacterial and antibiofilm efficacy of chitosan, Biomacromolecules 19, 1340. [28] Li J., Tan L., Liu X., Cui Z., Yang X., Yeung K.W.K., Chu P.K., Wu S. (2017) Balancing bacteria–osteoblast competition through selective physical puncture and biofunctionalization of ZnO/polydopamine/arginine–glycine–aspartic acid–cysteine nanorods, ACS Nano 11, 11250. [29] Diu T., Faruqui N., Sjostrom T., Lamarre B., Jenkinson H.F., Su B., Ryadnov M.G. (2014) Cicada-inspired cell-instructive nanopatterned arrays, Sci. Rep. 4, 7122.
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[30] Bhadra C.M., Truong V.K., Pham V.T., Al Kobaisi M., Seniutinas G., Wang J.Y., Juodkazis S., Crawford R.J., Ivanova E.P. (2015) Antibacterial titanium nano-patterned arrays inspired by dragonfly wings, Sci. Rep. 5, 16817. [31] Wandiyanto J.V., Tamanna T., Linklater D.P., Truong V.K., Al Kobaisi M., Baulin V.A., Joudkazis S., Thissen H., Crawford R.J., Ivanova E.P. (2020) Tunable morphological changes of asymmetric titanium nanosheets with bactericidal properties, J. Colloid Interface Sci. 560, 572. [32] Wandiyanto J.V., Cheeseman S., Truong V.K., Kobaisi M.A., Bizet C., Juodkazis S., Thissen H., Crawford R.J., Ivanova E.P. (2019) Outsmarting superbugs: Bactericidal activity of nanostructured titanium surfaces against methicillin- and gentamicin-resistant Staphylococcus aureus ATCC 33592, J. Mater. Chem. B 7, 4424. [33] Kim S., Jung U.T., Kim S.K., Lee J.H., Choi H.S., Kim C.S., Jeong M.Y. (2015) Nanostructured multifunctional surface with antireflective and antimicrobial characteristics, ACS Appl. Mater. Interfaces 7, 326. [34] Tsui K.H., Li X., Tsoi J.K.H., Leung S.F., Lei T., Chak W.Y., Zhang C., Chen J., Cheung G.S. P., Fan Z. (2018) Low-cost, flexible, disinfectant-free and regular-array three-dimensional nanopyramid antibacterial films for clinical applications, Nanoscale 10, 10436. [35] Yi G., Yuan Y., Li X., Zhang Y. (2018) ZnO nanopillar coated surfaces with substrate-dependent superbactericidal property, Small 14, e1703159. [36] Xiao L., Li J., Mieszkin S., Di Fino A., Clare A.S., Callow M.E., Callow J.A., Grunze M., Rosenhahn A., Levkin P.A. (2013) Slippery liquid-infused porous surfaces showing marine antifouling properties, ACS Appl. Mater. Interfaces 5, 10074. [37] Hazell G., Fisher L.E., Murray W.A., Nobbs A.H., Su B. (2018) Bioinspired bactericidal surfaces with polymer nanocone arrays, J. Colloid Interface Sci. 528, 389. [38] Mehrjou B., Mo S., Dehghan-Baniani D., Wang G., Qasim A.M., Chu P.K. (2019) Antibacterial and cytocompatible nanoengineered silk-based materials for orthopedic implants and tissue engineering, ACS Appl. Mater. Interfaces 11, 31605.
Chapter 10 Bioinspired Medical Drug-Delivery Surfaces 10.1
The Inspiration and Development of Drug-Delivery Surfaces
The discovery and development of drugs is a long, arduous and expensive process, and in many cases, the best treatment effect cannot be provided in clinical trials because of side effects. In order to improve the therapeutic properties, the drug molecule needs to reach the target site at the correct time. Therefore, the drug-delivery system is used to control the non-specific toxicity, immunogenicity, pharmacokinetics, and biological recognition of drugs. In recent years, the application of bionic technology in the development of materials and medicine has achieved rapid development, and bioinspired materials have attracted great attention as potential drug-delivery vehicles. Currently, targeted drug delivery system has become a research direction in the field of advanced drug delivery. New drug delivery strategies involve the improvement of drug-carrying capacity, cell uptake of drug carriers, and sustained drug release within target cells. Among them, bioinspired drug carriers can significantly improve the efficiency of drug delivery in the targeted system. The application of bionics to prove the essential problems in medicine and pharmaceutics is a promising method to treat bacterial infections. The targeted drug delivery system can transfer drugs to specific sites without harmful effects on healthy tissues or organs. Before that, using nanotechnology to encapsulate drugs into nano-carriers, solved the problems of insoluble drugs, biodegradable therapeutic agents, and high toxicity to biological systems. In addition, the small size of nanoparticles enables them to diffuse between cells [1]. The utilization of nano-carriers for the delivery of drugs can function in a highly efficient and directed manner, and understanding the interactions of nanomaterials with biological systems can improve the drug delivery of nano-carriers. Bionics in advanced drug delivery systems can create the inherent ability of bionic drug carriers by surface modification with amino acids, sugars, and lipids [2]. For this reason, special attention to the basic core materials, size, and shape of drug DOI: 10.1051/978-2-7598-2941-5.c010 © Science Press, EDP Sciences, 2023
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carriers are critical in order to be able to mimic natural cells. In addition, local drug delivery within target cells can be achieved by combining these nanocarriers with specific biological ligands for biomimetic surface functionalization [3, 4]. Bioinspired preparation methods are being successfully implemented to create a wide range of polymers and hybrid structures. Simulating the surface, shape, and movement of natural organisms or components can help to overcome phagocytosis and achieve effective targeting of drug carriers. The application of bionics principles can not only make drug carriers have bionic structure or function, but also provide new methods to prepare the drug-delivery carriers (figure 10.1).
FIG. 10.1 – Mimicking natural processes, structures, and functions provides a useful tool for drug delivery technology (Reproduced with permission from [2], Curr. Opin. Biotechnol., 2013, 24, 1167. Copyright © 2013 Elsevier B.V.). In recent years, in vivo cellular pathways with the ability to simulate cell microenvironments have been studied by means of the biomimetic process and bioinspired signal pathway. Scientists are trying to increase the circulation half-life of drug carriers and suppress immune stimulation. In addition, the sustained drugs release through endocytosis in target cells and the reduction of toxic effects on other healthy living cell functions can be regarded as another goal [5–7]. Synthetic carriers, such as polymers and lipid particles, often difficult to meet clinical expectations. Therefore, natural particles from pathogens to mammalian cells deserve further study because their special functions in vivo are highly optimized and have the characteristics often required in drug delivery carriers. Natural drug carriers provide the basis and inspiration for new drug delivery systems. Inspired by the organisms in nature, natural drug carriers provide the basis and inspiration for new drug-delivery systems, the bioinspired drug delivery carriers have provided the basis and inspiration for new drug-delivery systems.
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10.2
10.2.1
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Types of Bioinspired Drug-Delivery Medical Surfaces Bioinspired Hydrogels
A hydrogel is a group of natural or synthetic hydrophilic polymer materials, which can absorb huge amounts of water or biological fluids to produce huge expansion. The hydrogel is insoluble in the water environment due to chemical or physical crosslinking of individual polymer chains [8]. The hydrogel has good biocompatibility and the conditions for gel formation are relatively mild, so they are very similar to natural living cells and tissues [9]. By modifying the hydrogel matrix, it can produce a fast and reversible response under various chemical and physical stimuli, such as pH, temperature, and ionic strength. This property of hydrogel makes them useful in delivering biomolecules, such as protein and peptide therapy, and it is suitable for the long-term sustained and active release of drugs [8]. Figure 10.2 shows the drug release of hydrogel under the swollen and shrunken state.
FIG. 10.2 – Schematic of hydrogels at the swollen or shrunken states for drug release carries
(Reproduced with permission from [8], Adv. Drug Deliv. Rev., 2006, 58, 1379. Copyright © 2006 Elsevier B.V.).
Bioinspired hydrogels emerged as biomarking sites increased to cover cell activity and synchronize responses to environmental stimuli. In addition, the inert polymer chains of hydrogels should be adjusted according to the selected biological parts to make them suitable for targeting drug delivery systems in vivo [8]. In addition, the cell microenvironment can be simulated by integrating biological molecules, such as peptides, growth factors, and proteins into the hydrogel matrix, and a new controlled drug delivery system is developed to regenerate tissue [9]. Figure 10.2 shows the combination of growth factors in the biomimetic hydrogel matrix for controlling drug delivery. In situ forming hydrogels offer an effective method to solve the wound defect with unique advantages, for example, good biocompatibility, minimally invasive
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technique, and drug-delivery properties [10–13]. In addition, the hydrogel is a soft and humid material that can be compared with the extracellular matrix of natural tissue. These hydrogels can fill irregular shape defects and promote wound healing [10]. Despite the latest progress in-situ hydrogel research, the abundant body fluids and water in hydrogels have seriously hindered the adhesion of polymer and surface by forming a hydrate layer, resulting in obvious adhesive failure [14–16]. Hydrogel inspired by Mussel is a kind of biomimetic material with good wet adhesion ability and it has been widely used in biomedicine [17, 18]. As shown in figure 10.3a, mussels exhibit strong adhesion energy under humid conditions, mainly due to a large amount of adherent mussel foot proteins (mfps) secreted by its byssus, especially mfp-3 and mfp-5, which are rich in 3,4-dihydroxyphenylalanine (DOPA) (figure 10.3b) [14, 19]. DOPA is considered to be the key factor for rapid and strong wet adhesion due to its various interfacial interactions with the tissue surface, such as hydrogen bonding, metal chelation, π − π, and/or cation −π interactions [17, 19]. However, a key restriction for their application for hydrogels is the strong adherence leading them are easy to absorb microorganisms, thereby triggering wound infection [20, 21]. Wang et al. have designed a hydrogel inspired by mfp5, which has a strong affinity for waterborne tissue and anti-infection ability (figure 10.3c). The hydrogels are prepared by modifying ε-poly-l-lysine (EPL) employing dopamine (DA). EPL is a major candidate polymer for antibacterial materials, which have inherent antibacterial properties without the need for exogenous antibiotics [22]. In their study, polyethylene glycol (PEG), which is widely used in biomedical applications, was incorporated into the polymer system to improve adhesion strength and biocompatibility [23–25]. As exhibited in figure 10.3d, the EPL-PEG-DA hydrogels
FIG. 10.3 – Schematic of an engineered PPD hydrogel inspired by mussel. (a) Mfp-5 in mussel plaque is the major component of mussel adhesion protein; (b) Primary structure of mfp-5, mainly includes dopa and lysine; (c) Dopamine was coupled with EPL to form Mfp-5-mimetic polymer; (d) PPD hydrogels are prepared by HRP cross-linking reaction; (e) Application of PPD hydrogels in wound dressings (Reproduced with permission from [26], Adv. Funct. Mater., 2017, 27, 1604894. Copyright © 2017 John Wiley and Sons).
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(PPD hydrogels) were prepared in situ by horseradish peroxidase (HRP) cross-linking method, and that allows the hydrogel to be injectable, easy manipulation, and mechanical stiffness characteristics. Importantly, PPD hydrogels combine well with tissue, promote wound healing, and effectively prevent wound infection (figure 10.3e). All these properties make PPD hydrogel a promising biomimetic material for wound repair and other biomedical applications.
10.2.2
Bioinspired Polymeric Carriers
Bioinspired polymers can be defined as artificial polymers that mimic the useful properties of biological systems [27]. Inspired by the cell membrane, Ringsdorf et al. designed the first artificial polymeric liposome [28]. Synthetic biomimetic polymers with biodegradability have become attractive alternatives for drug delivery for the following reasons because the structure and properties are easy to control and further modifications. Moreover, biomimetic polymer utilizes the interactions of natural materials and the biological system, and it usually shows good biocompatibility and high drug delivery efficiency. Bioinspired polymer is a new kind of biomaterial carrier, which can simulate the interaction mechanism between cells and the environment, such as cell adhesion, cytokine signal transduction, and endocytosis. In addition, the biological activity of these polymers makes it possible to transfer drugs through the cell barrier within the target lesion cells. Similarly, appropriate biomimetic polymer-carriers can reduce the nonspecific interactions on the surface cells and extract the desired cellular reactions [29]. Figure 10.4 illustrates the importance of biomimetic polymer surface coating
FIG. 10.4 – Special ligands on the surface of biomimetic polymeric drug carriers can promote endocytosis and intercellular drug release (Reproduced with permission from [30], Colloids Surf. B, 2014, 124, 80. Copyright © 2014 Elsevier B.V.).
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and modification in controlling specific cell interactions through endocytosis [30]. Ekkelenkamp et al. prepared two kinds of poly (amido amine)s (PAAs) nanogels by zwitterionic PAAs [31], and one of them was selected as a biomimetic biocompatible polymer carrier. PAA nanogel with low dispersion and negative surface charge had the least toxicity to living cells, and it is more suitable as a drug-delivery carrier than that with a positive surface charge. In summary, surface modification of polymer drug-delivery carriers can promote drug release in target cells without adverse effects on the function of healthy cells. Further understanding of intercellular transport pathways and physiological characteristics of modified ligands can promote the preparation of biomimetic polymer drug carriers. Meanwhile, optimizing the chemical properties of synthetic polymers is of great significance for reducing the cell-mediated immune response.
10.2.3
Bioinspired Nanostructures and Surfaces
Therapeutic nanoparticles as drug carriers commonly refer to particles with a size range between 10 and 1000 nm, including nanotubes, nanofibers, nanoparticles, etc. [32]. As revealed in figure 10.5a, hollow cylindrical nanotubes are produced by rolling up the inorganic materials (such as carbon nanotubes) or by self-assembling biological material (such as a peptide) [33, 34]. Nanofibers with fiber shapes were produced from natural or synthetic polymers by self-assembly, electrospinning, and phase separation. Besides, these nanoparticles have the advantages of biodegradability, biocompatibility, efficient cellular internalization, and large drug-loading capacity, and are considered to be a beneficial supplement for complex cell therapy and drug therapy in medical fields. [35]. In addition, the inorganic nanoparticles based on fullerene, gold, silica, and graphene are suitable drug-delivery carriers as well [36]. As illustrated in figure 10.5b, instead of passing through the membrane by wrapping, the carbon nanotube (CNTs) can pass through the membrane directly [37]. CNTs have unique thermal, electronic, mechanical, and biological properties, and it was widely used in targeted drug-delivery systems. Hevia et al. used biomimetic multi-walled CNTs (MWCNTs), which have inherent anti-proliferation effects on cells [38]. Chen et al. used novel biomimetic Rosette nanotubes (RNTs) as drug-delivery carriers which were self-assembled in the physiological environment [39]. The basic components of RNT super-molecular structures include cytosine (C) and guanine (G) DNA base pairs, which were arranged by hydrogen bonding. Then, medicine could be easily encapsulated into the RNT nanotubes through hydrophobic or stacking interactions.
10.2.4
Other Bioinspired Drug-Delivery Surfaces
Inspired by the flexible and soft leg/foot structures in many living organisms, Wang et al. report a soft millirobot with multi-tapered soft feet [40]. Under the trigger of the external magnetic field, their robots can realize intermittent and continuous movement, and show many superior functions in wet and dry conditions, such as excellent mobility and deformation ability, heavy load capacity, and obstacle-crossing ability.
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FIG. 10.5 – (a) Organic functionalization of CNTs (Reproduced with permission from [33], Curr. Opin. Chem. Biol., 2005, 9, 674. Copyright © 2005 Elsevier B.V.); (b) Pristine CNTs can be treated with acids to purify them and form carboxyl groups at the ends (i), or react with amino acid derivatives and aldehydes, adding solubilizing parts around the outer surface (ii) (Reproduced with permission from [37], Acta Mech. Sin., 2008, 24, 161. Copyright © 2008 Springer Nature). Time sequence of six snapshots of single-walled CNTs penetrating membrane driven by van der Waal forces. The operation of millirobots was performed in several harsh environments, including slippery surfaces, heavy loading, and highly sloppy obstacles. As revealed in figure 10.6a, the millirobots can move 10 mm at an average speed of 0.5 mm/s on the wet surface under the drive frequency of 1 Hz. The transport capacity of millirobots is comparable to ants in nature and it is stronger than most animals. A robot of 39.4 mg can carry a capsule weighing up to 3980.6 mg (figure 10.6b), and it can move 8 mm in 45 s under the driving frequency of 1 Hz. In addition, the
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FIG. 10.6 – Demonstration of millirobot movement under harsh environment. (a) Locomotion on wet surface of liquid film; (b) Millirobot moves with a loading 100 times its own weight; (c) Cross a steep obstacle that 10 times higher than its leg; (d) Comparison of the normalized speed between the soft robot and other animals; (e) Demonstration of drug-delivery in a stomach model under wet environment (Reproduced with permission from [40], Nat. Commun., 2018, 9, 3944. Copyright © 2018 Springer Nature).
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flexible feet enhanced the stability and climbing ability of the barrier, and can cross the obstacle with a height of 6.5 mm and a slope of 60° in 113 s (figure 10.6c) [40]. In order to quantify the locomotion efficiency of millirobot and other natural lives, the researchers define a dimensionless number Vl, which is a distance of one-second movement relative to the length of the lower limb (legs or feet). As shown in figure 10.6d, the maximum speeds of humans and cheetahs are 10.4 m/s and 33.3 m/s, corresponding to Vl 7.4 and 33.3, respectively. In contrast, the millirobot can reach Vl 44 at a swing frequency of 16 Hz, which is 30% faster than the cheetah (figure 10.6d). To further demonstrate the drug-delivery ability in vivo environment, the locomotion of millirobot on a human stomach-like structure was verified (figure 10.6e) [40]. The results show that the millirobot can still move 32 mm in 50 s in the complex stomach-simulated environment with 1.5–6.8 mm in depth and 2.4–6.2 mm in width. To sum up, the design and synthesis of drug carriers inspired by natural organisms and molecules are a proper method to prepare high-performance materials with the least resources, and also an appropriate model for the design of advanced drug delivery systems. With the rapid development of biomedical materials and the progress of modern medicine, the great prospect of an advanced drug-delivery system is becoming increasingly clear. The advanced drug-delivery system is not only a revolutionary change from traditional drug delivery, but also promotes the development of currently infeasible bacterial infection treatment. With the continuous development of new technologies, the production of drug-delivery materials and the drug-controlled-release system has become an important part of the whole pharmaceutical industry, which has an important prospect in the delivery of antibacterial drugs.
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Conclusion
Green and effective antifouling coatings are highly required in the marine industry. Bioinspired antifouling strategies have attracted great concerns in recent years due to their high efficiency and environmental compatibility. Advanced materials and techniques have brought great help to the development of bioinspired antifouling coatings. The potential drawbacks of current bioinspired antifouling coatings are being solved. In a real marine environment, a single bioinspired antifouling strategy may lack broad-spectrum antifouling performance, and a single strategy may lose efficacy due to the complex marine environment or physical damage. Therefore, it is still a challenge to apply a single bioinspired antifouling strategy in a harsh marine environment; however, the synergistic antifouling coatings may provide a solution for this. We believe bioinspired antifouling coatings have a promising future. In numerous surgeries, bacterial infections and biofoulings have become the most dreadful recovery problems. However, using antibiotics to realize anti-bacteria can arise serious drug resistance with the increasing of time. To evade this circumstance, various environmentally friendly and biocompatible bioinspired surfaces have been proposed. These materials have a huge potential to be used in the medical area, and some of the bioinspired materials have already been used in reality. In the above chapters, we exhibited four main bionic materials, including slippery-liquid-infused surfaces, superhydrophobic surfaces, mechanical bactericidal surfaces, and drug-delivery materials, which can be utilized to achieve antifouling and antibacterial properties without the worry of being invalid caused by the resistance of bacteria. These bioinspired antifouling/bacterial materials all have solid fundamental theories and have already been studied and developed over decades, while most of these materials are still staying in laboratory studies. Therefore, durability and reusability have always been the main issues that limit these materials for more widespread applications in real life: (i) For durability, a series of methods for constructing slippery–liquid-infused– surfaces porous substrates were proposed, including layer–by–layer deposition, impregnation, 3D printing, photographing polymerization, hydrophilic–
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hydrophobic micropattern, and anodizing with post etching method. However, it is urgent to improve the durability for adapting to a more complex real surgery environment. And the dose limitation of lubricant liquid which is stored in porous substrates significantly influences the service time of SLIPS. As for superhydrophobic surfaces, the micro-/nanostructure which can be obtained through various technologies has difficulty sustaining mechanical wear and chemical etching, which may affect the industry quantity production of the surface. (ii) Reusability strongly limits practical applications of mechanical bactericidal surfaces. The bacteria-killing nanostructures can be rapidly piled up or buried by dead cells, which leads to the invalid antibacterial property. For superhydrophobic surfaces, after surfaces become fully wettable, bacteria cells will colonize the surface and crowd the trapped air out of the nanostructure. The drug-delivery system has a similar reusability problem, for which the drug carrier becomes useless after the stowage is totally released. Therefore, expanding the choice of porous substrates and lubricant liquids with great biocompatibility and realizing novel properties, finding new approaches that can achieve structure controllability, repeatability, reduction of cost, and digging a deeper understanding of mechanism may lead to a more practical application for these materials in future life.