Effect of silver nanoparticles on <i>Staphylococcus aureus</i> biofilm formation on different orthopedic biomaterials_West China Medical Journal

Authors：

YAN Xin’an ^1,2 , Walter M Chirume ^1,2 ,  FANG Yue ^1,2

1. Department of Orthopedic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. Trauma Center, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding?author：

FANG Yue, Email: fangyue1968@163.com

Keywords：

Silver nanoparticles; Staphylococcus aureus; biofilm; implants; osteomyelitis

DOI：

10.7507/1002-0179.202110174

Video：

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Objective To observe the inhibitory characteristics of silver nanoparticles (AgNP) on bacterial biofilms and investigate their inhibitory effect on biofilm formation on three common orthopedic biomaterials. Methods The minimal inhibitory concentration (MIC) and minimal biofilm inhibitory concentration (MBIC) of AgNP were determined by microplate dilution assay. Biofilms of Staphylococcus aureus (ATCC 25923) were cultured on three orthopedic biomaterials (titanium alloy, titanium oxide, and stainless steel) and intervened with AgNP at concentrations of 32, 16, 8, 4, 2 and 0 μg/mL to determine the MBICs on the three materials. The effects of AgNP on biofilm formation were analyzed by scanning electron microscopy and measuring optical density. Results The MIC and MBIC of AgNP in the microplate assay were both 16 μg/mL. The MBICs of AgNP on biofilm formation in titanium oxide, titanium alloy, and stainless steel were 16 μg/mL, 32 μg/mL, and 32 μg/mL, respectively. Among the three materials, the lowest optical density was observed on titanium oxide, while the highest was on titanium alloy. Conclusions AgNP has strong antibacterial biofilm characteristics and can prevent the formation of Staphylococcus aureus biofilm in vitro. Biofilm formation is most pronounced on titanium alloy, least on titanium oxide, and intermediate on stainless steel.

Citation： YAN Xin’an, Walter M Chirume, FANG Yue. Effect of silver nanoparticles on Staphylococcus aureus biofilm formation on different orthopedic biomaterials. West China Medical Journal, 2023, 38(7): 1047-1052. doi: 10.7507/1002-0179.202110174 Copy

1.	Ridgeway S, Wilson J, Charlet A, et al. Infection of the surgical site after arthroplasty of the hip. J Bone Joint Surg Br, 2005, 87(6): 844-850.
2.	Olsen MA, Nepple JJ, Riew KD, et al. Risk factors for surgical site infection following orthopaedic spinal operations. J Bone Joint Surg Am, 2008, 90(1): 62-69.
3.	Mahan J, Seligson D, Henry SL, et al. Factors in pin tract infections. Orthopedics, 1991, 14(3): 305-308.
4.	Lee-Smith J, Santy J, Davis P, et al. Pin site management. Towards a consensus: part 1. J Orthop Nurs, 2001, 5(1): 37-42.
5.	Zimmerli W, Moser C. Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunol Med Microbiol, 2012, 65(2): 158-168.
6.	Nohr RS, Macdonald JG. New biomaterials through surface segregation phenomenon: new quaternary ammonium compounds as antibacterial agents. J Biomater Sci Polym Ed, 1994, 5(6): 607-619.
7.	Nganga S, Travan A, Marsich E, et al. In vitro antimicrobial properties of silver-polysaccharide coatings on porous fiber-reinforced composites for bone implants. J Mater Sci Mater Med, 2013, 24(12): 2775-2785.
8.	Tyagi M, Singh H. Preparation and antibacterial evaluation of urinary balloon catheter. Biomed Sci Instrum, 1997, 33: 240-245.
9.	Akiyama T, Miyamoto H, Yonekura Y, et al. Silver oxide-containing hydroxyapatite coating has in vivo antibacterial activity in the rat tibia. J Orthop Res, 2013, 31(8): 1195-1200.
10.	An YH, Stuart GW, McDowell SJ, et al. Prevention of bacterial adherence to implant surfaces with a crosslinked albumin coating in vitro. J Orthop Res, 1996, 14(5): 846-849.
11.	Kelkawi AHA, Abbasi Kajani A, Bordbar AK. Green synthesis of silver nanoparticles using Mentha pulegium and investigation of their antibacterial, antifungal and anticancer activity. IET Nanobiotechnol, 2017, 11(4): 370-376.
12.	Li Y, Lin Z, Zhao M, et al. Silver nanoparticle based codelivery of oseltamivir to inhibit the activity of the H1N1 influenza virus through ROS-mediated signaling pathways. ACS Appl Mater Interfaces, 2016, 8(37): 24385-24393.
13.	Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, 7th ed. CLSI document M7-A7. Wayne, PA: Clinical and Laboratory Standards Institute, 2006.
14.	Brennan SA, Ní Fhoghlú C, Devitt BM, et al. Silver nanoparticles and their orthopaedic applications. Bone Joint J, 2015, 97-B(5): 582-589.
15.	Chaloupka K, Malam Y, Seifalian AM. Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol, 2010, 28(11): 580-588.
16.	Yin IX, Zhang J, Zhao IS, et al. The antibacterial mechanism of silver nanoparticles and its application in dentistry. Int J Nanomedicine, 2020, 15: 2555-2562.
17.	Xiang Y, Li J, Liu X, et al. Construction of poly(lactic-co-glycolic acid)/ZnO nanorods/Ag nanoparticles hybrid coating on Ti implants for enhanced antibacterial activity and biocompatibility. Mater Sci Eng C Mater Biol Appl, 2017, 79: 629-637.
18.	Sato M, Webster TJ. Nanobiotechnology: implications for the future of nanotechnology in orthopedic applications. Expert Rev Med Devices, 2004, 1(1): 105-114.
19.	Singh R, Lillard JW. Nanoparticle-based targeted drug delivery. Exp Mol Pathol, 2009, 86(3): 215-223.
20.	Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev, 2003, 55(3): 329-347.
21.	Rodríguez-León E, I?iguez-Palomares R, Navarro RE, et al. Synthesis of silver nanoparticles using reducing agents obtained from natural sources (Rumex hymenosepalus extracts). Nanoscale Res Lett, 2013, 8(1): 318.
22.	Shankar SS, Ahmad A, Sastry M. Geranium leaf assisted biosynthesis of silver nanoparticles. Biotechnol Prog, 2003, 19(6): 1627-1631.
23.	Mala R, Annie Aglin A, Ruby Celsia AS, et al. Foley catheters functionalised with a synergistic combination of antibiotics and silver nanoparticles resist biofilm formation. IET Nanobiotechnol, 2017, 11(5): 612-620.
24.	Ansari MA, Khan HM, Khan AA, et al. Anti-biofilm efficacy of silver nanoparticles against MRSA and MRSE isolated from wounds in a tertiary care hospital. Indian J Med Microbiol, 2015, 33(1): 101-109.
25.	Du J, Singh H, Yi TH. Antibacterial, anti-biofilm and anticancer potentials of green synthesized silver nanoparticles using benzoin gum (Styrax benzoin) extract. Bioprocess Biosyst Eng, 2016, 39(12): 1923-1931.
26.	Qin H, Cao H, Zhao Y, et al. In vitro and in vivo anti-biofilm effects of silver nanoparticles immobilized on titanium. Biomaterials, 2014, 35(33): 9114-9125.
27.	Long M, Rack HJ. Titanium alloys in total joint replacement--a materials science perspective. Biomaterials, 1998, 19(18): 1621-1639.
28.	Arens S, Schlegel U, Printzen G, et al. Influence of materials for fixation implants on local infection. An experimental study of steel versus titanium DCP in rabbits. J Bone Joint Surg Br, 1996, 78(4): 647-651.
29.	Ha KY, Chung YG, Ryoo SJ. Adherence and biofilm formation of Staphylococcus epidermidis and Mycobacterium tuberculosis on various spinal implants. Spine (Phila Pa 1976), 2005, 30(1): 38-43.
30.	Schildhauer TA, Robie B, Muhr G, et al. Bacterial adherence to tantalum versus commonly used orthopedic metallic implant materials. J Orthop Trauma, 2006, 20(7): 476-484.
31.	Malhotra R, Dhawan B, Garg B, et al. A comparison of bacterial adhesion and biofilm formation on commonly used orthopaedic metal implant materials: an in vitro study. Indian J Orthop, 2019, 53(1): 148-153.
32.	Pedeferri M. Titanium anodic oxidation: a powerful technique for tailoring surfaces properties for biomedical applications//TMS 2015 144th Annual Meeting & Exhibition. Cham: Springer International Publishing, 2016.
33.	Sharma VK, Sayes CM, Guo B, et al. Interactions between silver nanoparticles and other metal nanoparticles under environmentally relevant conditions: a review. Sci Total Environ, 2019, 653: 1042-1051.
34.	Guggenbichler JP, B?swald M, Lugauer S, et al. A new technology of microdispersed silver in polyurethane induces antimicrobial activity in central venous catheters. Infection, 1999, 27(Suppl 1): S16-S23.
35.	R?sch W, Lugauer S. Catheter-associated infections in urology: possible use of silver-impregnated catheters and the Erlanger silver catheter. Infection, 1999, 27(Suppl 1): S74-S77.
36.	Chole RA, Hubbell RN. Antimicrobial activity of silastic tympanostomy tubes impregnated with silver oxide. A double-blind randomized multicenter trial. Arch Otolaryngol Head Neck Surg, 1995, 121(5): 562-565.
37.	Paná?ek A, Smékalová M, Ve?e?ová R, et al. Silver nanoparticles strongly enhance and restore bactericidal activity of inactive antibiotics against multiresistant Enterobacteriaceae. Colloids Surf B Biointerfaces, 2016, 142: 392-399.
38.	Dos Santos CA, Seckler MM, Ingle AP, et al. Silver nanoparticles: therapeutical uses, toxicity, and safety issues. J Pharm Sci, 2014, 103(7): 1931-1944.
39.	De Jong WH, Van Der Ven LT, Sleijffers A, et al. Systemic and immunotoxicity of silver nanoparticles in an intravenous 28 days repeated dose toxicity study in rats. Biomaterials, 2013, 34(33): 8333-8343.

1. Ridgeway S, Wilson J, Charlet A, et al. Infection of the surgical site after arthroplasty of the hip. J Bone Joint Surg Br, 2005, 87(6): 844-850.
2. Olsen MA, Nepple JJ, Riew KD, et al. Risk factors for surgical site infection following orthopaedic spinal operations. J Bone Joint Surg Am, 2008, 90(1): 62-69.
3. Mahan J, Seligson D, Henry SL, et al. Factors in pin tract infections. Orthopedics, 1991, 14(3): 305-308.
4. Lee-Smith J, Santy J, Davis P, et al. Pin site management. Towards a consensus: part 1. J Orthop Nurs, 2001, 5(1): 37-42.
5. Zimmerli W, Moser C. Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunol Med Microbiol, 2012, 65(2): 158-168.
6. Nohr RS, Macdonald JG. New biomaterials through surface segregation phenomenon: new quaternary ammonium compounds as antibacterial agents. J Biomater Sci Polym Ed, 1994, 5(6): 607-619.
7. Nganga S, Travan A, Marsich E, et al. In vitro antimicrobial properties of silver-polysaccharide coatings on porous fiber-reinforced composites for bone implants. J Mater Sci Mater Med, 2013, 24(12): 2775-2785.
8. Tyagi M, Singh H. Preparation and antibacterial evaluation of urinary balloon catheter. Biomed Sci Instrum, 1997, 33: 240-245.
9. Akiyama T, Miyamoto H, Yonekura Y, et al. Silver oxide-containing hydroxyapatite coating has in vivo antibacterial activity in the rat tibia. J Orthop Res, 2013, 31(8): 1195-1200.
10. An YH, Stuart GW, McDowell SJ, et al. Prevention of bacterial adherence to implant surfaces with a crosslinked albumin coating in vitro. J Orthop Res, 1996, 14(5): 846-849.
11. Kelkawi AHA, Abbasi Kajani A, Bordbar AK. Green synthesis of silver nanoparticles using Mentha pulegium and investigation of their antibacterial, antifungal and anticancer activity. IET Nanobiotechnol, 2017, 11(4): 370-376.
12. Li Y, Lin Z, Zhao M, et al. Silver nanoparticle based codelivery of oseltamivir to inhibit the activity of the H1N1 influenza virus through ROS-mediated signaling pathways. ACS Appl Mater Interfaces, 2016, 8(37): 24385-24393.
13. Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, 7th ed. CLSI document M7-A7. Wayne, PA: Clinical and Laboratory Standards Institute, 2006.
14. Brennan SA, Ní Fhoghlú C, Devitt BM, et al. Silver nanoparticles and their orthopaedic applications. Bone Joint J, 2015, 97-B(5): 582-589.
15. Chaloupka K, Malam Y, Seifalian AM. Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol, 2010, 28(11): 580-588.
16. Yin IX, Zhang J, Zhao IS, et al. The antibacterial mechanism of silver nanoparticles and its application in dentistry. Int J Nanomedicine, 2020, 15: 2555-2562.
17. Xiang Y, Li J, Liu X, et al. Construction of poly(lactic-co-glycolic acid)/ZnO nanorods/Ag nanoparticles hybrid coating on Ti implants for enhanced antibacterial activity and biocompatibility. Mater Sci Eng C Mater Biol Appl, 2017, 79: 629-637.
18. Sato M, Webster TJ. Nanobiotechnology: implications for the future of nanotechnology in orthopedic applications. Expert Rev Med Devices, 2004, 1(1): 105-114.
19. Singh R, Lillard JW. Nanoparticle-based targeted drug delivery. Exp Mol Pathol, 2009, 86(3): 215-223.
20. Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev, 2003, 55(3): 329-347.
21. Rodríguez-León E, I?iguez-Palomares R, Navarro RE, et al. Synthesis of silver nanoparticles using reducing agents obtained from natural sources (Rumex hymenosepalus extracts). Nanoscale Res Lett, 2013, 8(1): 318.
22. Shankar SS, Ahmad A, Sastry M. Geranium leaf assisted biosynthesis of silver nanoparticles. Biotechnol Prog, 2003, 19(6): 1627-1631.
23. Mala R, Annie Aglin A, Ruby Celsia AS, et al. Foley catheters functionalised with a synergistic combination of antibiotics and silver nanoparticles resist biofilm formation. IET Nanobiotechnol, 2017, 11(5): 612-620.
24. Ansari MA, Khan HM, Khan AA, et al. Anti-biofilm efficacy of silver nanoparticles against MRSA and MRSE isolated from wounds in a tertiary care hospital. Indian J Med Microbiol, 2015, 33(1): 101-109.
25. Du J, Singh H, Yi TH. Antibacterial, anti-biofilm and anticancer potentials of green synthesized silver nanoparticles using benzoin gum (Styrax benzoin) extract. Bioprocess Biosyst Eng, 2016, 39(12): 1923-1931.
26. Qin H, Cao H, Zhao Y, et al. In vitro and in vivo anti-biofilm effects of silver nanoparticles immobilized on titanium. Biomaterials, 2014, 35(33): 9114-9125.
27. Long M, Rack HJ. Titanium alloys in total joint replacement--a materials science perspective. Biomaterials, 1998, 19(18): 1621-1639.
28. Arens S, Schlegel U, Printzen G, et al. Influence of materials for fixation implants on local infection. An experimental study of steel versus titanium DCP in rabbits. J Bone Joint Surg Br, 1996, 78(4): 647-651.
29. Ha KY, Chung YG, Ryoo SJ. Adherence and biofilm formation of Staphylococcus epidermidis and Mycobacterium tuberculosis on various spinal implants. Spine (Phila Pa 1976), 2005, 30(1): 38-43.
30. Schildhauer TA, Robie B, Muhr G, et al. Bacterial adherence to tantalum versus commonly used orthopedic metallic implant materials. J Orthop Trauma, 2006, 20(7): 476-484.
31. Malhotra R, Dhawan B, Garg B, et al. A comparison of bacterial adhesion and biofilm formation on commonly used orthopaedic metal implant materials: an in vitro study. Indian J Orthop, 2019, 53(1): 148-153.
32. Pedeferri M. Titanium anodic oxidation: a powerful technique for tailoring surfaces properties for biomedical applications//TMS 2015 144th Annual Meeting & Exhibition. Cham: Springer International Publishing, 2016.
33. Sharma VK, Sayes CM, Guo B, et al. Interactions between silver nanoparticles and other metal nanoparticles under environmentally relevant conditions: a review. Sci Total Environ, 2019, 653: 1042-1051.
34. Guggenbichler JP, B?swald M, Lugauer S, et al. A new technology of microdispersed silver in polyurethane induces antimicrobial activity in central venous catheters. Infection, 1999, 27(Suppl 1): S16-S23.
35. R?sch W, Lugauer S. Catheter-associated infections in urology: possible use of silver-impregnated catheters and the Erlanger silver catheter. Infection, 1999, 27(Suppl 1): S74-S77.
36. Chole RA, Hubbell RN. Antimicrobial activity of silastic tympanostomy tubes impregnated with silver oxide. A double-blind randomized multicenter trial. Arch Otolaryngol Head Neck Surg, 1995, 121(5): 562-565.
37. Paná?ek A, Smékalová M, Ve?e?ová R, et al. Silver nanoparticles strongly enhance and restore bactericidal activity of inactive antibiotics against multiresistant Enterobacteriaceae. Colloids Surf B Biointerfaces, 2016, 142: 392-399.
38. Dos Santos CA, Seckler MM, Ingle AP, et al. Silver nanoparticles: therapeutical uses, toxicity, and safety issues. J Pharm Sci, 2014, 103(7): 1931-1944.
39. De Jong WH, Van Der Ven LT, Sleijffers A, et al. Systemic and immunotoxicity of silver nanoparticles in an intravenous 28 days repeated dose toxicity study in rats. Biomaterials, 2013, 34(33): 8333-8343.

West China Medical Journal

Effect of silver nanoparticles on Staphylococcus aureus biofilm formation on different orthopedic biomaterials

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