Advances in nanostructured surfaces for enhanced mechano-bactericidal applications_Journal of Biomedical Engineering

Authors：

CHEN Shixiong ¹ ,  LIANG Ying ¹ ,  TIAN Xiaobao ¹ , WANG Kai ²

1. MOE Key Laboratory of Deep Earth Science and Engineering, College of Architecture & Environment, Sichuan University, Chengdu 610065, P. R. China;
2. School of Biological Science and Medical Engineering, Beihang University, Beijing 100191, P. R. China;

Corresponding author：

LIANG Ying, Email: liangying@scu.edu.cn

Keywords：

Nanostructure; Mechanical bactericidal; Bactericidal mechanism; Drug resistance

DOI：

10.7507/1001-5515.202407099

Video：

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Abstract Full text Figures/Tables Video References Cited by

The issue of bacterial drug resistance has remained unresolved, and in recent years, biomimetic nanostructured surfaces inspired by nature have garnered significant attention due to their bactericidal properties demonstrated through mechanical mechanisms. This article reviewed the main research progress in the field of nanostructured mechanical bactericidal surfaces, including various preparation methods for nanostructured surfaces with mechanical bactericidal properties, as well as the basic mechanisms and related physical models of the interaction between bacteria and nanostructured surfaces. In addition, the application of nanostructured surfaces in biomedicine was introduced. Finally, the article proposed the major challenges faced by mechanical bactericidal research and the future development direction.

Citation： CHEN Shixiong, LIANG Ying, TIAN Xiaobao, WANG Kai. Advances in nanostructured surfaces for enhanced mechano-bactericidal applications. Journal of Biomedical Engineering, 2024, 41(5): 1046-1052, 1061. doi: 10.7507/1001-5515.202407099 Copy

1.	Cui Qianqian, Liu Tianqing, Li Xiangqin, et al. Nanopillared polycarbonate surfaces having variable feature parameters as bactericidal coatings. ACS Appl Nano Mater, 2020, 3(5): 4599-4609..
2.	Ivanova E P, Linklater D P, Werner M, et al. The multi-faceted mechano-bactericidal mechanism of nanostructured surfaces. PNAS, 2020, 117(23): 12598-12605..
3.	Linklater D P, Saita S, Murata T, et al. Nanopillar polymer films as antibacterial packaging materials. ACS Appl Nano Mater, 2022, 5(2): 2578-2591..
4.	Velic A, Hasan J, Li Zhiyong, et al. Mechanics of bacterial interaction and death on nanopatterned surfaces. Biophys J, 2021, 120(2): 217-231..
5.	Lohmann S C, Tripathy A, Milionis A, et al. Effect of flexibility and size of nanofabricated topographies on the mechanobactericidal efficacy of polymeric surfaces. ACS Appl Bio Mater, 2022, 5(4): 1564-1575..
6.	Valiei A, Bryche J F, Canva M, et al. Effects of surface topography and cellular biomechanics on nanopillar-induced bactericidal activity. ACS Appl Mater Interfaces, 2024, 16(8): 9614-9625..
7.	Xie Yuan, Qu Xi, Li Jinyang, et al. Ultrafast physical bacterial inactivation and photocatalytic self-cleaning of ZnO nanoarrays for rapid and sustainable bactericidal applications. Sci Total Environt, 2020, 738: 139714..
8.	Catley T E, Corrigan R M, Parnell A J. Designing effective antimicrobial nanostructured surfaces: highlighting the lack of consensus in the literature. ACS Omega, 2023, 8(17): 14873-14883..
9.	Hayles A, Bright R, Nguyen N H, et al. Vancomycin tolerance of adherent Staphylococcus aureus is impeded by nanospike-induced physiological changes. NPJ Biofilms Microbiomes, 2023, 9(1): 1-11..
10.	Pirouz A, Papakonstantinou I, Michalska M. Antimicrobial mechanisms of nanopatterned surfaces—a developing story. Front Chem, 2024, 12: 1354755..
11.	Valiei A, Lin N, McKay G, et al. Surface wettability is a key feature in the mechano-bactericidal activity of nanopillars. ACS Appl Mater Interfaces, 2022, 14(24): 27564-27574..
12.	Li Wenlong, Thian E S, Wang Miao, et al. Surface design for antibacterial materials: from fundamentals to advanced strategies. Adv Sci, 2021, 8(19): 2100368..
13.	Patil D, Overland M, Stoller M, et al. Bioinspired nanostructured bactericidal surfaces. Curr Opin Chem Eng, 2021, 34: 100741..
14.	Ivanova E P, Hasan J, Webb H K, et al. Natural bactericidal surfaces: mechanical rupture of pseudomonas aeruginosa cells by cicada wings. Small, 2012, 8(16): 2489-2494..
15.	Hasan J, Webb H K, Truong V K, et al. Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces. Appl Microbiol Biotechnol, 2013, 97(20): 9257-9262..
16.	Silhavy T J, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol, 2010, 2(5): a000414..
17.	Mainwaring D E, Nguyen S H, Webb H, et al. The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly. Nanoscale, 2016, 8(12): 6527-6534..
18.	Ramírez-Puebla S T, Weigel B L, Jack L, et al. Spatial organization of the kelp microbiome at micron scales. Microbiome, 2022, 10(1): 52..
19.	Zhao Lidan, Liu Tianqing, Li Xiangqin, et al. Low-temperature hydrothermal synthesis of novel 3D hybrid nanostructures on titanium surface with mechano-bactericidal performance. ACS Biomater Sci Eng, 2021, 7(6): 2268-2278..
20.	Bhadra C M, Khanh T V, Pham V T. H, et al. Antibacterial titanium nano-patterned arrays inspired by dragonfly wings. Sci Rep, 2015, 5(1): 16817..
21.	Jaggessar A, Senevirathne S W M A I, Velic A, et al. Antibacterial activity of 3D versus 2D TiO₂ nanostructured surfaces to investigate curvature and orientation effects. Curr Opin Biomed Eng, 2022, 23: 100404..
22.	Roy A, Chatterjee K. Bactericidal anisotropic nanostructures on titanium fabricated by maskless dry etching. ACS Appl Nano Mater, 2022, 5(3): 4447-4461..
23.	Patil D, Golia V, Overland M, et al. Mechanobactericidal nanotopography on nitrile surfaces toward antimicrobial protective gear. ACS Macro Lett, 2023, 12(2): 227-233..
24.	Roy A, Patil D, Yarlagadda P K D V, et al. Cooperative stiffening of flexible high aspect ratio nanostructures impart mechanobactericidal activity to soft substrates. J Colloid Interface Sci, 2023, 652: 2127-2138..
25.	Linklater D P, De Volder M, Baulin V A, et al. High aspect ratio nanostructures kill bacteria via storage and release of mechanical energy. ACS Nano, 2018, 12(7): 6657-6667..
26.	Yick S, Mai-Prochnow A, Levchenko I, et al. The effects of plasma treatment on bacterial biofilm formation on vertically-aligned carbon nanotube arrays. RSC Adv, 2015, 5(7): 5142-5148..
27.	郭逦达, 张增光, 白安琪, 等. 电化学法制备 Ga 掺杂 ZnO 纳米柱阵列及其性能的研究. 太阳能, 2022(4): 87-92..
28.	Quilis N G, Hageneder S, Fossati S, et al. UV-laser interference lithography for local functionalization of plasmonic nanostructures with responsive hydrogel. J Phys Chem C, 2020, 124(5): 3297-3305..
29.	Shimizu Y. Laser interference lithography for fabrication of planar scale gratings for optical metrology. Nanomanufacturing Metrol, 2021, 4(1): 3-27..
30.	Liu Ri, Cao Liang, Liu Dongdong, et al. Laser interference lithography—a method for the fabrication of controlled periodic structures. Nanomaterials, 2023, 13(12): 1818..
31.	Lee W, Jin M K, Yoo W C, et al. Nanostructuring of a polymeric substrate with well-defined nanometer-scale topography and tailored surface wettability. Langmuir, 2004, 20(18): 7665-7669..
32.	Zhang Xin, Zhang Jiteng, Han Xiaoli, et al. A photothermal therapy enhanced mechano-bactericidal hybrid nanostructured surface. J Colloid Interface Sci, 2023, 645: 380-390..
33.	Zhao Xingyu, Xu Zhihao, Wei Zhouxia, et al. Nature-inspired mechano-bactericidal nanostructured surfaces with photothermally enhanced antibacterial performances. Prog Org Coat, 2023, 182: 107599..
34.	Liu Ziting, Yi Yaozhen, Wang Shujin, et al. Bio-inspired self-adaptive nanocomposite array: from non-antibiotic antibacterial actions to cell proliferation. ACS Nano, 2022, 16(10): 16549-16562..
35.	Śliwa A, Mikuła J, Gołombek K, et al. Prediction of the properties of PVD/CVD coatings with the use of FEM analysis. Appl Surf Sci, 2016, 388: 281-287..
36.	蒋如剑. 仿生微纳结构表面设计制备及抗菌性能研究. 长春: 吉林大学, 2021..
37.	Bandara C D, Singh S, Afara I O, et al. Bactericidal effects of natural nanotopography of dragonfly wing on escherichia coli. ACS Appl Mater Interfaces, 2017, 9(8): 6746-6760..
38.	Köller M, Ziegler N, Sengstock C, et al. Bacterial cell division is involved in the damage of gram-negative bacteria on a nano-pillar titanium surface. Biomedical Phys Eng Express, 2018, 4(5): 055002..
39.	Zhao Shuo, Li Zheyu, Linklater D P, et al. Programmed death of injured pseudomonas aeruginosa on mechano-bactericidal surfaces. Nano Lett, 2022, 22(3): 1129-1137..
40.	Le P H, Linklater D P, Aburto-Medina A, et al. Apoptosis of multi-drug resistant candida species on microstructured titanium surfaces. Adv Mater Interfaces, 2023, 10(34): 2300314..
41.	Jenkins J, Mantell J, Neal C, et al. Antibacterial effects of nanopillar surfaces are mediated by cell impedance, penetration and induction of oxidative stress. Nat Commun, 2020, 11(1): 1626..
42.	Pogodin S, Hasan J, Baulin V A, et al. Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys J, 2013, 104(4): 835-840..
43.	Xue Fudong, Liu Junjie, Guo Longfang, et al. Theoretical study on the bactericidal nature of nanopatterned surfaces. J Theor Biol, 2015, 385: 1-7..
44.	Li Xinlei. Bactericidal mechanism of nanopatterned surfaces. Phys Chem Chem Phys, 2015, 18(2): 1311-1316..
45.	Senevirathne S W M A I, Hasan J, Mathew A, et al. Bactericidal efficiency of micro- and nanostructured surfaces: a critical perspective. RSC Adv, 2021, 11(3): 1883-1900..
46.	Valiei A, Lin N, Bryche J F, et al. Hydrophilic mechano-bactericidal nanopillars require external forces to rapidly kill bacteria. Nano Lett, 2020, 20(8): 5720-5727..
47.	刘丽, 魏强. 细菌活性检测方法研究进展及其应用探讨. 疾病监测, 2023, 38(12): 1519-1525..
48.	Wang Ziyue, Sheng Lina, Yang Xingxing, et al. Natural biomass-derived carbon dots as potent antimicrobial agents against multidrug-resistant bacteria and their biofilms. Sustain Mater Technol, 2023, 36: e00584..
49.	Zhao Zihao, Matsushita Y, Ogawa N, et al. Bactericidal performance of nanostructures resin surfaces: nanopillars versus nanocones. ACS Appl Nano Mater, 2024, 7(12): 14040-14049..
50.	Viela F, Ortega I V, Hernández J J, et al. Real-time imaging of the mechanobactericidal action of colloidal nanomaterials and nanostructured topographies. Small Sci, 2023, 3(5): 2300002..
51.	Wada M, Nomura T. Direct measurement of adhesion force between a yeast cell and a lactic acid bacterium cell with atomic force microscopy. J Biosci Bioeng, 2022, 133(2): 155-160..
52.	de Sousa K M, Linklater D P, Baulin V A, et al. Understanding the influence of serum proteins adsorption on the mechano-bactericidal efficacy and immunomodulation of nanostructured titanium. Adv Mater Interfaces, 2024, 11(17): 2301021..
53.	de Sousa K M, Linklater D P, Murdoch B J, et al. Modulation of MG-63 osteogenic response on mechano-bactericidal micronanostructured titanium surfaces. ACS Appl Bio Mater, 2023, 6(3): 1054-1070..
54.	Yi Yaozhen, Jiang Rujian, Liu Ziting, et al. Bioinspired nanopillar surface for switchable mechano-bactericidal and releasing actions. J Hazard Mater, 2022, 432: 128685..
55.	Liu Ziting, Yi Yaozhen, Song Lingjie, et al. Biocompatible mechano-bactericidal nanopatterned surfaces with salt-responsive bacterial release. Acta Biomater, 2022, 141: 198-208..

1. Cui Qianqian, Liu Tianqing, Li Xiangqin, et al. Nanopillared polycarbonate surfaces having variable feature parameters as bactericidal coatings. ACS Appl Nano Mater, 2020, 3(5): 4599-4609..
2. Ivanova E P, Linklater D P, Werner M, et al. The multi-faceted mechano-bactericidal mechanism of nanostructured surfaces. PNAS, 2020, 117(23): 12598-12605..
3. Linklater D P, Saita S, Murata T, et al. Nanopillar polymer films as antibacterial packaging materials. ACS Appl Nano Mater, 2022, 5(2): 2578-2591..
4. Velic A, Hasan J, Li Zhiyong, et al. Mechanics of bacterial interaction and death on nanopatterned surfaces. Biophys J, 2021, 120(2): 217-231..
5. Lohmann S C, Tripathy A, Milionis A, et al. Effect of flexibility and size of nanofabricated topographies on the mechanobactericidal efficacy of polymeric surfaces. ACS Appl Bio Mater, 2022, 5(4): 1564-1575..
6. Valiei A, Bryche J F, Canva M, et al. Effects of surface topography and cellular biomechanics on nanopillar-induced bactericidal activity. ACS Appl Mater Interfaces, 2024, 16(8): 9614-9625..
7. Xie Yuan, Qu Xi, Li Jinyang, et al. Ultrafast physical bacterial inactivation and photocatalytic self-cleaning of ZnO nanoarrays for rapid and sustainable bactericidal applications. Sci Total Environt, 2020, 738: 139714..
8. Catley T E, Corrigan R M, Parnell A J. Designing effective antimicrobial nanostructured surfaces: highlighting the lack of consensus in the literature. ACS Omega, 2023, 8(17): 14873-14883..
9. Hayles A, Bright R, Nguyen N H, et al. Vancomycin tolerance of adherent Staphylococcus aureus is impeded by nanospike-induced physiological changes. NPJ Biofilms Microbiomes, 2023, 9(1): 1-11..
10. Pirouz A, Papakonstantinou I, Michalska M. Antimicrobial mechanisms of nanopatterned surfaces—a developing story. Front Chem, 2024, 12: 1354755..
11. Valiei A, Lin N, McKay G, et al. Surface wettability is a key feature in the mechano-bactericidal activity of nanopillars. ACS Appl Mater Interfaces, 2022, 14(24): 27564-27574..
12. Li Wenlong, Thian E S, Wang Miao, et al. Surface design for antibacterial materials: from fundamentals to advanced strategies. Adv Sci, 2021, 8(19): 2100368..
13. Patil D, Overland M, Stoller M, et al. Bioinspired nanostructured bactericidal surfaces. Curr Opin Chem Eng, 2021, 34: 100741..
14. Ivanova E P, Hasan J, Webb H K, et al. Natural bactericidal surfaces: mechanical rupture of pseudomonas aeruginosa cells by cicada wings. Small, 2012, 8(16): 2489-2494..
15. Hasan J, Webb H K, Truong V K, et al. Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces. Appl Microbiol Biotechnol, 2013, 97(20): 9257-9262..
16. Silhavy T J, Kahne D, Walker S. The bacterial cell envelope. Cold Spring Harb Perspect Biol, 2010, 2(5): a000414..
17. Mainwaring D E, Nguyen S H, Webb H, et al. The nature of inherent bactericidal activity: insights from the nanotopology of three species of dragonfly. Nanoscale, 2016, 8(12): 6527-6534..
18. Ramírez-Puebla S T, Weigel B L, Jack L, et al. Spatial organization of the kelp microbiome at micron scales. Microbiome, 2022, 10(1): 52..
19. Zhao Lidan, Liu Tianqing, Li Xiangqin, et al. Low-temperature hydrothermal synthesis of novel 3D hybrid nanostructures on titanium surface with mechano-bactericidal performance. ACS Biomater Sci Eng, 2021, 7(6): 2268-2278..
20. Bhadra C M, Khanh T V, Pham V T. H, et al. Antibacterial titanium nano-patterned arrays inspired by dragonfly wings. Sci Rep, 2015, 5(1): 16817..
21. Jaggessar A, Senevirathne S W M A I, Velic A, et al. Antibacterial activity of 3D versus 2D TiO₂ nanostructured surfaces to investigate curvature and orientation effects. Curr Opin Biomed Eng, 2022, 23: 100404..
22. Roy A, Chatterjee K. Bactericidal anisotropic nanostructures on titanium fabricated by maskless dry etching. ACS Appl Nano Mater, 2022, 5(3): 4447-4461..
23. Patil D, Golia V, Overland M, et al. Mechanobactericidal nanotopography on nitrile surfaces toward antimicrobial protective gear. ACS Macro Lett, 2023, 12(2): 227-233..
24. Roy A, Patil D, Yarlagadda P K D V, et al. Cooperative stiffening of flexible high aspect ratio nanostructures impart mechanobactericidal activity to soft substrates. J Colloid Interface Sci, 2023, 652: 2127-2138..
25. Linklater D P, De Volder M, Baulin V A, et al. High aspect ratio nanostructures kill bacteria via storage and release of mechanical energy. ACS Nano, 2018, 12(7): 6657-6667..
26. Yick S, Mai-Prochnow A, Levchenko I, et al. The effects of plasma treatment on bacterial biofilm formation on vertically-aligned carbon nanotube arrays. RSC Adv, 2015, 5(7): 5142-5148..
27. 郭逦达, 张增光, 白安琪, 等. 电化学法制备 Ga 掺杂 ZnO 纳米柱阵列及其性能的研究. 太阳能, 2022(4): 87-92..
28. Quilis N G, Hageneder S, Fossati S, et al. UV-laser interference lithography for local functionalization of plasmonic nanostructures with responsive hydrogel. J Phys Chem C, 2020, 124(5): 3297-3305..
29. Shimizu Y. Laser interference lithography for fabrication of planar scale gratings for optical metrology. Nanomanufacturing Metrol, 2021, 4(1): 3-27..
30. Liu Ri, Cao Liang, Liu Dongdong, et al. Laser interference lithography—a method for the fabrication of controlled periodic structures. Nanomaterials, 2023, 13(12): 1818..
31. Lee W, Jin M K, Yoo W C, et al. Nanostructuring of a polymeric substrate with well-defined nanometer-scale topography and tailored surface wettability. Langmuir, 2004, 20(18): 7665-7669..
32. Zhang Xin, Zhang Jiteng, Han Xiaoli, et al. A photothermal therapy enhanced mechano-bactericidal hybrid nanostructured surface. J Colloid Interface Sci, 2023, 645: 380-390..
33. Zhao Xingyu, Xu Zhihao, Wei Zhouxia, et al. Nature-inspired mechano-bactericidal nanostructured surfaces with photothermally enhanced antibacterial performances. Prog Org Coat, 2023, 182: 107599..
34. Liu Ziting, Yi Yaozhen, Wang Shujin, et al. Bio-inspired self-adaptive nanocomposite array: from non-antibiotic antibacterial actions to cell proliferation. ACS Nano, 2022, 16(10): 16549-16562..
35. Śliwa A, Mikuła J, Gołombek K, et al. Prediction of the properties of PVD/CVD coatings with the use of FEM analysis. Appl Surf Sci, 2016, 388: 281-287..
36. 蒋如剑. 仿生微纳结构表面设计制备及抗菌性能研究. 长春: 吉林大学, 2021..
37. Bandara C D, Singh S, Afara I O, et al. Bactericidal effects of natural nanotopography of dragonfly wing on escherichia coli. ACS Appl Mater Interfaces, 2017, 9(8): 6746-6760..
38. Köller M, Ziegler N, Sengstock C, et al. Bacterial cell division is involved in the damage of gram-negative bacteria on a nano-pillar titanium surface. Biomedical Phys Eng Express, 2018, 4(5): 055002..
39. Zhao Shuo, Li Zheyu, Linklater D P, et al. Programmed death of injured pseudomonas aeruginosa on mechano-bactericidal surfaces. Nano Lett, 2022, 22(3): 1129-1137..
40. Le P H, Linklater D P, Aburto-Medina A, et al. Apoptosis of multi-drug resistant candida species on microstructured titanium surfaces. Adv Mater Interfaces, 2023, 10(34): 2300314..
41. Jenkins J, Mantell J, Neal C, et al. Antibacterial effects of nanopillar surfaces are mediated by cell impedance, penetration and induction of oxidative stress. Nat Commun, 2020, 11(1): 1626..
42. Pogodin S, Hasan J, Baulin V A, et al. Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys J, 2013, 104(4): 835-840..
43. Xue Fudong, Liu Junjie, Guo Longfang, et al. Theoretical study on the bactericidal nature of nanopatterned surfaces. J Theor Biol, 2015, 385: 1-7..
44. Li Xinlei. Bactericidal mechanism of nanopatterned surfaces. Phys Chem Chem Phys, 2015, 18(2): 1311-1316..
45. Senevirathne S W M A I, Hasan J, Mathew A, et al. Bactericidal efficiency of micro- and nanostructured surfaces: a critical perspective. RSC Adv, 2021, 11(3): 1883-1900..
46. Valiei A, Lin N, Bryche J F, et al. Hydrophilic mechano-bactericidal nanopillars require external forces to rapidly kill bacteria. Nano Lett, 2020, 20(8): 5720-5727..
47. 刘丽, 魏强. 细菌活性检测方法研究进展及其应用探讨. 疾病监测, 2023, 38(12): 1519-1525..
48. Wang Ziyue, Sheng Lina, Yang Xingxing, et al. Natural biomass-derived carbon dots as potent antimicrobial agents against multidrug-resistant bacteria and their biofilms. Sustain Mater Technol, 2023, 36: e00584..
49. Zhao Zihao, Matsushita Y, Ogawa N, et al. Bactericidal performance of nanostructures resin surfaces: nanopillars versus nanocones. ACS Appl Nano Mater, 2024, 7(12): 14040-14049..
50. Viela F, Ortega I V, Hernández J J, et al. Real-time imaging of the mechanobactericidal action of colloidal nanomaterials and nanostructured topographies. Small Sci, 2023, 3(5): 2300002..
51. Wada M, Nomura T. Direct measurement of adhesion force between a yeast cell and a lactic acid bacterium cell with atomic force microscopy. J Biosci Bioeng, 2022, 133(2): 155-160..
52. de Sousa K M, Linklater D P, Baulin V A, et al. Understanding the influence of serum proteins adsorption on the mechano-bactericidal efficacy and immunomodulation of nanostructured titanium. Adv Mater Interfaces, 2024, 11(17): 2301021..
53. de Sousa K M, Linklater D P, Murdoch B J, et al. Modulation of MG-63 osteogenic response on mechano-bactericidal micronanostructured titanium surfaces. ACS Appl Bio Mater, 2023, 6(3): 1054-1070..
54. Yi Yaozhen, Jiang Rujian, Liu Ziting, et al. Bioinspired nanopillar surface for switchable mechano-bactericidal and releasing actions. J Hazard Mater, 2022, 432: 128685..
55. Liu Ziting, Yi Yaozhen, Song Lingjie, et al. Biocompatible mechano-bactericidal nanopatterned surfaces with salt-responsive bacterial release. Acta Biomater, 2022, 141: 198-208..

Journal of Biomedical Engineering

Advances in nanostructured surfaces for enhanced mechano-bactericidal applications

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