Research progress of antibacterial modification of orthopaedic implants surface_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHANG Chaoqun ¹ , WU Yipeng ² ,  XU Yongqing ²

1. Graduate School of Kunming Medical University, Kunming Yunnan, 650000, P. R. China;
2. Institute of All-Army Trauma Orthopaedics, No.920 Hospital of PLA Joint Service Support Force, Kunming Yunnan, 650032, P. R. China;

Corresponding author：

XU Yongqing, Email: xuyongqingkm@163.net

Keywords：

Orthopaedic implants; anti-infective therapy; surface antibacterial modification

DOI：

10.7507/1002-1892.202112109

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the related research progress of antibacterial modification of orthopaedic implants surface in recent years. Methods The domestic and foreign related literature in recent years was extensively consulted, the research progress on antibacterial modification of orthopaedic implants surface was discussed from two aspects of characteristics of infection in orthopedic implants and surface anti-infection modification. Results The orthopaedic implants infections are mainly related to aspects of bacterial adhesion, decreased host immunity, and surface biofilm formation. At present, the main antimicrobial coating methods of orthopaedic implants are antibacterial adhesion coating, antibiotic coating, inorganic antimicrobial coating, composite antimicrobial coating, nitric oxide coating, immunomodulation, three-dimensional printing, polymer antimicrobial coating, and “smart” coating. Conclusion The above-mentioned antibacterial coating methods of orthopedic implants can not only inhibit bacterial adhesion, but also solve the problems of low immunity and biofilm formation. However, its mechanism of action and modification are still controversial and require further research.

Citation： ZHANG Chaoqun, WU Yipeng, XU Yongqing. Research progress of antibacterial modification of orthopaedic implants surface. Chinese Journal of Reparative and Reconstructive Surgery, 2022, 36(4): 511-516. doi: 10.7507/1002-1892.202112109 Copy

1.	Rodríguez-Merchán EC, Davidson DJ, Liddle AD. Recent strategies to combat infections from biofilm-forming bacteria on orthopaedic implants. Int J Mol Sci, 2021, 22(19): 10243. doi: 10.3390/ijms221910243.
2.	Hetrick EM, Schoenfisch MH. Reducing implant-related infections: active release strategies. Chem Soc Rev, 2006, 35(9): 780-789.
3.	Kaasch AJ, Kern WV, Joost I, et al. Effect of clinically uninfected orthopedic implants and pacemakers/AICDs in low-risk Staphylococcus aureus bloodstream infection on crude mortality rate: A post hoc analysis of a large cohort study. Open Forum Infect Dis, 2019, 6(5): ofz170. doi: 10.1093/ofid/ofz170.
4.	Martínez-Pérez M, Conde A, Arenas MA, et al. The “race for the surface” experimentally studied: In vitro assessment of Staphylococcus spp. adhesion and preosteoblastic cells integration to doped Ti-6Al-4V alloys. Colloids Surf B Biointerfaces, 2019, 173: 876-883.
5.	王加兴, 秦晖, 张先龙. 骨科内植物纳米涂层抗菌性能研究进展. 国际骨科学杂志, 2014, 35(2): 83-85.
6.	刘洋, 周君琳. 浅谈骨科植入物的抗感染修饰. 中华临床医师杂志 (电子版), 2012, 6(8): 1982-1985.
7.	Schierholz JM, Beuth J. Implant infections: a haven for opportunistic bacteria. J Hosp Infect, 2001, 49(2): 87-93.
8.	López-Abarrategui C, Figueroa-Espí V, Reyes-Acosta O, et al. Magnetic nanoparticles: new players in antimicrobial peptide therapeutics. Curr Protein Pept Sci, 2013, 14(7): 595-606.
9.	von Eiff C, Kohnen W, Becker K, et al. Modern strategies in the prevention of implant-associated infections. Int J Artif Organs, 2005, 28(11): 1146-1156.
10.	Hofstee MI, Muthukrishnan G, Atkins GJ, et al. Current concepts of osteomyelitis: From pathologic mechanisms to advanced research methods. Am J Pathol, 2020, 190(6): 1151-1163.
11.	Liu S, Chen L, Tan L, et al. A high efficiency approach for a titanium surface antifouling modification: PEG-o-quinone linked with titanium via electron transfer process. J Mater Chem B, 2014, 2(39): 6758-6766.
12.	Liu P, Hao Y, Zhao Y, et al. Surface modification of titanium substrates for enhanced osteogenetic and antibacterial properties. Colloids Surf B Biointerfaces, 2017, 160: 110-116.
13.	张志清, 孙艳华. 氧化锆基台与钛基台细菌黏附的比较. 黑龙江医药科学, 2011, 34(5): 31-32.
14.	Garvin KL, Miyano JA, Robinson D, et al. Polylactide/polyglycolide antibiotic implants in the treatment of osteomyelitis. A canine model. J Bone Joint Surg (Am), 1994, 76(10): 1500-1506.
15.	Turner TM, Urban RM, Gitelis S, et al. Radiographic and histologic assessment of calcium sulfate in experimental animal models and clinical use as a resorbable bone-graft substitute, a bone-graft expander, and a method for local antibiotic delivery. One institution’s experience. J Bone Joint Surg (Am), 2001, Suppl 2(Pt 1): 8-18.
16.	Ding H, Chen S, Song WQ, et al. Dimethyloxaloylglycine improves angiogenic activity of bone marrow stromal cells in the tissue-engineered bone. Int J Biol Sci, 2014, 10(7): 746-756.
17.	Berberich CE, Josse J, Laurent F, et al. Dual antibiotic loaded bone cement in patients at high infection risks in arthroplasty: Rationale of use for prophylaxis and scientific evidence. World J Orthop, 2021, 12(3): 119-128.
18.	Jiang N, Dusane DH, Brooks JR, et al. Antibiotic loaded β-tricalcium phosphate/calcium sulfate for antimicrobial potency, prevention and killing efficacy of Pseudomonas aeruginosa and Staphylococcus aureus biofilms. Sci Rep, 2021, 11(1): 1446. doi: 10.1038/s41598-020-80764-6.
19.	Tunney MM, Patrick S, Gorman SP, et al. Improved detection of infection in hip replacements. A currently underestimated problem. J Bone Joint Surg (Br), 1998, 80(4): 568-572.
20.	Chang Y, Goldberg VM, Caplan AI. Toxic effects of gentamicin on marrow-derived human mesenchymal stem cells. Clin Orthop Relat Res, 2006, 452: 242-249.
21.	Wahlig H, Dingeldein E. Antibiotics and bone cements. Experimental and clinical long-term observations. Acta Orthop Scand, 1980, 51(1): 49-56.
22.	Berger TJ, Spadaro JA, Chapin SE, et al. Electrically generated silver ions: quantitative effects on bacterial and mammalian cells. Antimicrob Agents Chemother, 1976, 9(2): 357-358.
23.	Li JX, Wang J, Shen LR, et al. The influence of polyethylene terephthalate surfaces modified by silver ion implantation on bacterial adhesion behavior. Surface & Coatings Technology, 2006, 201(19-20): 8155-8159.
24.	Zhao L, Chu PK, Zhang Y, et al. Antibacterial coatings on titanium implants. J Biomed Mater Res B Appl Biomater, 2009, 91(1): 470-480.
25.	Percival SL, Bowler PG, Russell D. Bacterial resistance to silver in wound care. J Hosp Infect, 2005, 60(1): 1-7.
26.	Bosetti M, Massè A, Tobin E, et al. Silver coated materials for external fixation devices: in vitro biocompatibility and genotoxicity. Biomaterials, 2002, 23(3): 887-892.
27.	Yan Y, Zhang X, Huang Y, et al. Antibacterial and bioactivity of silver substituted hydroxyapatite/TiO₂ nanotube composite coatings on titanium. Applied Surface Science, 2014, 314: 348-357.
28.	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.
29.	Nazir KZ, Tayyaba I, Saira R, et al. Antibacterial, magnetic and dielectric properties of nano-structured V doped TiO₂ thin films deposited by dip coating technique. Materials Chemistry and Physics, 2021: 267. doi: 10.1016/j.matchemphys.2021.124659.
30.	Kazemzadeh-Narbat M, Lai BF, Ding C, et al. Multilayered coating on titanium for controlled release of antimicrobial peptides for the prevention of implant-associated infections. Biomaterials, 2013, 34(24): 5969-5977.
31.	Chua PH, Neoh KG, Kang ET, et al. Surface functionalization of titanium with hyaluronic acid/chitosan polyelectrolyte multilayers and RGD for promoting osteoblast functions and inhibiting bacterial adhesion. Biomaterials, 2008, 29(10): 1412-1421.
32.	Deupree SM, Schoenfisch MH. Morphological analysis of the antimicrobial action of nitric oxide on gram-negative pathogens using atomic force microscopy. Acta Biomater, 2009, 5(5): 1405-1415.
33.	Li M, Aveyard J, Fleming G, et al. Nitric oxide releasing titanium surfaces for antimicrobial bone-integrating orthopedic implants. ACS Appl Mater Interfaces, 2020, 12(20): 22433-22443.
34.	Nablo BJ, Schoenfisch MH. Antibacterial properties of nitric oxide-releasing sol-gels. J Biomed Mater Res A, 2003, 67(4): 1276-1283.
35.	Babensee JE, Stein MM, Moore L. Interconnections between inflammatory and immune responses in tissue engineering. Ann N Y Acad Sci, 2002, 961: 360-363.
36.	Scott MG, Dullaghan E, Mookherjee N, et al. An anti-infective peptide that selectively modulates the innate immune response. Nat Biotechnol, 2007, 25(4): 465-472.
37.	Bowdish DM, Davidson DJ, Lau YE, et al. Impact of LL-37 on anti-infective immunity. J Leukoc Biol, 2005, 77(4): 451-459.
38.	Zhao DW, Zuo KQ, Wang K, et al. Interleukin-4 assisted calcium-strontium-zinc-phosphate coating induces controllable macrophage polarization and promotes osseointegration on titanium implant. Mater Sci Eng C Mater Biol Appl, 2021, 118: 111512. doi: 10.1016/j.msec.2020.111512.
39.	Lim HJ, Shin HS. Antimicrobial and immunomodulatory effects of bifidobacterium strains: A review. J Microbiol Biotechnol, 2020, 30(12): 1793-1800.
40.	韩倞, 杨轶, 张弛, 等. 骨科植入物表面抗感染修饰及其骨整合性的研究进展. 中国临床医学, 2017, 24(1): 134-140.
41.	Xue C, Song X, Liu M, et al. A highly efficient, low-toxic, wide-spectrum antibacterial coating designed for 3D printed implants with tailorable release properties. J Mater Chem B, 2017, 5(22): 4128-4136.
42.	Liu J, Yao X, Ye J, et al. A printing-spray-transfer process for attaching biocompatible and antibacterial coatings to the surfaces of patient-specific silicone stents. Biomed Mater, 2020, 15(5): 055036. doi: 10.1088/1748-605X/ab99d6.
43.	Wang BB, Quan YH, Xu ZM, et al. Preparation of highly effective antibacterial coating with polydopamine/chitosan/silver nanoparticles via simple immersion. Progress in Organic Coatings, 2020: 149. doi: 10.1016/j.porgcoat.2020.105967.
44.	Gouveia Z, Perinpanayagam H, Zhu J. Development of robust chitosan—silica class Ⅱ hybrid coatings with antimicrobial properties for titanium implants. Coatings, 2020, 10(6). doi: 10.3390/coatings10060534.
45.	Sasmita M, Ankita A, Abhijit M. Surface immobilization of a short antimicrobial peptide (AMP) as an antibacterial coating. Materialia, 2019: 6. doi: 10.1016/j.mtla.2019.100350.
46.	de Breij A, Riool M, Kwakman PH, et al. Prevention of Staphylococcus aureus biomaterial-associated infections using a polymer-lipid coating containing the antimicrobial peptide OP-145. J Control Release, 2016, 222: 1-8.
47.	李健, 王颖, 高新蕾. 智能涂层——类生物表面活性智能涂层. 材料保护, 2006, 39(1): 36-39.
48.	Sang S, Guo G, Yu J, et al. Antibacterial application of gentamicin-silk protein coating with smart release function on titanium, polyethylene, and Al₂O₃ materials. Mater Sci Eng C Mater Biol Appl, 2021, 124: 112069. doi: 10.1016/j.msec.2021.112069.
49.	Zhang Y, Hu K, Xing X, et al. Smart titanium coating composed of antibiotic conjugated peptides as an infection-responsive antibacterial agent. Macromol Biosci, 2021, 21(1): e2000194. doi: 10.1002/mabi.202000194.
50.	Pornpattananangkul D, Zhang L, Olson S, et al. Bacterial toxin-triggered drug release from gold nanoparticle-stabilized liposomes for the treatment of bacterial infection. J Am Chem Soc, 2011, 133(11): 4132-4139.

1. Rodríguez-Merchán EC, Davidson DJ, Liddle AD. Recent strategies to combat infections from biofilm-forming bacteria on orthopaedic implants. Int J Mol Sci, 2021, 22(19): 10243. doi: 10.3390/ijms221910243.
2. Hetrick EM, Schoenfisch MH. Reducing implant-related infections: active release strategies. Chem Soc Rev, 2006, 35(9): 780-789.
3. Kaasch AJ, Kern WV, Joost I, et al. Effect of clinically uninfected orthopedic implants and pacemakers/AICDs in low-risk Staphylococcus aureus bloodstream infection on crude mortality rate: A post hoc analysis of a large cohort study. Open Forum Infect Dis, 2019, 6(5): ofz170. doi: 10.1093/ofid/ofz170.
4. Martínez-Pérez M, Conde A, Arenas MA, et al. The “race for the surface” experimentally studied: In vitro assessment of Staphylococcus spp. adhesion and preosteoblastic cells integration to doped Ti-6Al-4V alloys. Colloids Surf B Biointerfaces, 2019, 173: 876-883.
5. 王加兴, 秦晖, 张先龙. 骨科内植物纳米涂层抗菌性能研究进展. 国际骨科学杂志, 2014, 35(2): 83-85.
6. 刘洋, 周君琳. 浅谈骨科植入物的抗感染修饰. 中华临床医师杂志 (电子版), 2012, 6(8): 1982-1985.
7. Schierholz JM, Beuth J. Implant infections: a haven for opportunistic bacteria. J Hosp Infect, 2001, 49(2): 87-93.
8. López-Abarrategui C, Figueroa-Espí V, Reyes-Acosta O, et al. Magnetic nanoparticles: new players in antimicrobial peptide therapeutics. Curr Protein Pept Sci, 2013, 14(7): 595-606.
9. von Eiff C, Kohnen W, Becker K, et al. Modern strategies in the prevention of implant-associated infections. Int J Artif Organs, 2005, 28(11): 1146-1156.
10. Hofstee MI, Muthukrishnan G, Atkins GJ, et al. Current concepts of osteomyelitis: From pathologic mechanisms to advanced research methods. Am J Pathol, 2020, 190(6): 1151-1163.
11. Liu S, Chen L, Tan L, et al. A high efficiency approach for a titanium surface antifouling modification: PEG-o-quinone linked with titanium via electron transfer process. J Mater Chem B, 2014, 2(39): 6758-6766.
12. Liu P, Hao Y, Zhao Y, et al. Surface modification of titanium substrates for enhanced osteogenetic and antibacterial properties. Colloids Surf B Biointerfaces, 2017, 160: 110-116.
13. 张志清, 孙艳华. 氧化锆基台与钛基台细菌黏附的比较. 黑龙江医药科学, 2011, 34(5): 31-32.
14. Garvin KL, Miyano JA, Robinson D, et al. Polylactide/polyglycolide antibiotic implants in the treatment of osteomyelitis. A canine model. J Bone Joint Surg (Am), 1994, 76(10): 1500-1506.
15. Turner TM, Urban RM, Gitelis S, et al. Radiographic and histologic assessment of calcium sulfate in experimental animal models and clinical use as a resorbable bone-graft substitute, a bone-graft expander, and a method for local antibiotic delivery. One institution’s experience. J Bone Joint Surg (Am), 2001, Suppl 2(Pt 1): 8-18.
16. Ding H, Chen S, Song WQ, et al. Dimethyloxaloylglycine improves angiogenic activity of bone marrow stromal cells in the tissue-engineered bone. Int J Biol Sci, 2014, 10(7): 746-756.
17. Berberich CE, Josse J, Laurent F, et al. Dual antibiotic loaded bone cement in patients at high infection risks in arthroplasty: Rationale of use for prophylaxis and scientific evidence. World J Orthop, 2021, 12(3): 119-128.
18. Jiang N, Dusane DH, Brooks JR, et al. Antibiotic loaded β-tricalcium phosphate/calcium sulfate for antimicrobial potency, prevention and killing efficacy of Pseudomonas aeruginosa and Staphylococcus aureus biofilms. Sci Rep, 2021, 11(1): 1446. doi: 10.1038/s41598-020-80764-6.
19. Tunney MM, Patrick S, Gorman SP, et al. Improved detection of infection in hip replacements. A currently underestimated problem. J Bone Joint Surg (Br), 1998, 80(4): 568-572.
20. Chang Y, Goldberg VM, Caplan AI. Toxic effects of gentamicin on marrow-derived human mesenchymal stem cells. Clin Orthop Relat Res, 2006, 452: 242-249.
21. Wahlig H, Dingeldein E. Antibiotics and bone cements. Experimental and clinical long-term observations. Acta Orthop Scand, 1980, 51(1): 49-56.
22. Berger TJ, Spadaro JA, Chapin SE, et al. Electrically generated silver ions: quantitative effects on bacterial and mammalian cells. Antimicrob Agents Chemother, 1976, 9(2): 357-358.
23. Li JX, Wang J, Shen LR, et al. The influence of polyethylene terephthalate surfaces modified by silver ion implantation on bacterial adhesion behavior. Surface & Coatings Technology, 2006, 201(19-20): 8155-8159.
24. Zhao L, Chu PK, Zhang Y, et al. Antibacterial coatings on titanium implants. J Biomed Mater Res B Appl Biomater, 2009, 91(1): 470-480.
25. Percival SL, Bowler PG, Russell D. Bacterial resistance to silver in wound care. J Hosp Infect, 2005, 60(1): 1-7.
26. Bosetti M, Massè A, Tobin E, et al. Silver coated materials for external fixation devices: in vitro biocompatibility and genotoxicity. Biomaterials, 2002, 23(3): 887-892.
27. Yan Y, Zhang X, Huang Y, et al. Antibacterial and bioactivity of silver substituted hydroxyapatite/TiO₂ nanotube composite coatings on titanium. Applied Surface Science, 2014, 314: 348-357.
28. 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.
29. Nazir KZ, Tayyaba I, Saira R, et al. Antibacterial, magnetic and dielectric properties of nano-structured V doped TiO₂ thin films deposited by dip coating technique. Materials Chemistry and Physics, 2021: 267. doi: 10.1016/j.matchemphys.2021.124659.
30. Kazemzadeh-Narbat M, Lai BF, Ding C, et al. Multilayered coating on titanium for controlled release of antimicrobial peptides for the prevention of implant-associated infections. Biomaterials, 2013, 34(24): 5969-5977.
31. Chua PH, Neoh KG, Kang ET, et al. Surface functionalization of titanium with hyaluronic acid/chitosan polyelectrolyte multilayers and RGD for promoting osteoblast functions and inhibiting bacterial adhesion. Biomaterials, 2008, 29(10): 1412-1421.
32. Deupree SM, Schoenfisch MH. Morphological analysis of the antimicrobial action of nitric oxide on gram-negative pathogens using atomic force microscopy. Acta Biomater, 2009, 5(5): 1405-1415.
33. Li M, Aveyard J, Fleming G, et al. Nitric oxide releasing titanium surfaces for antimicrobial bone-integrating orthopedic implants. ACS Appl Mater Interfaces, 2020, 12(20): 22433-22443.
34. Nablo BJ, Schoenfisch MH. Antibacterial properties of nitric oxide-releasing sol-gels. J Biomed Mater Res A, 2003, 67(4): 1276-1283.
35. Babensee JE, Stein MM, Moore L. Interconnections between inflammatory and immune responses in tissue engineering. Ann N Y Acad Sci, 2002, 961: 360-363.
36. Scott MG, Dullaghan E, Mookherjee N, et al. An anti-infective peptide that selectively modulates the innate immune response. Nat Biotechnol, 2007, 25(4): 465-472.
37. Bowdish DM, Davidson DJ, Lau YE, et al. Impact of LL-37 on anti-infective immunity. J Leukoc Biol, 2005, 77(4): 451-459.
38. Zhao DW, Zuo KQ, Wang K, et al. Interleukin-4 assisted calcium-strontium-zinc-phosphate coating induces controllable macrophage polarization and promotes osseointegration on titanium implant. Mater Sci Eng C Mater Biol Appl, 2021, 118: 111512. doi: 10.1016/j.msec.2020.111512.
39. Lim HJ, Shin HS. Antimicrobial and immunomodulatory effects of bifidobacterium strains: A review. J Microbiol Biotechnol, 2020, 30(12): 1793-1800.
40. 韩倞, 杨轶, 张弛, 等. 骨科植入物表面抗感染修饰及其骨整合性的研究进展. 中国临床医学, 2017, 24(1): 134-140.
41. Xue C, Song X, Liu M, et al. A highly efficient, low-toxic, wide-spectrum antibacterial coating designed for 3D printed implants with tailorable release properties. J Mater Chem B, 2017, 5(22): 4128-4136.
42. Liu J, Yao X, Ye J, et al. A printing-spray-transfer process for attaching biocompatible and antibacterial coatings to the surfaces of patient-specific silicone stents. Biomed Mater, 2020, 15(5): 055036. doi: 10.1088/1748-605X/ab99d6.
43. Wang BB, Quan YH, Xu ZM, et al. Preparation of highly effective antibacterial coating with polydopamine/chitosan/silver nanoparticles via simple immersion. Progress in Organic Coatings, 2020: 149. doi: 10.1016/j.porgcoat.2020.105967.
44. Gouveia Z, Perinpanayagam H, Zhu J. Development of robust chitosan—silica class Ⅱ hybrid coatings with antimicrobial properties for titanium implants. Coatings, 2020, 10(6). doi: 10.3390/coatings10060534.
45. Sasmita M, Ankita A, Abhijit M. Surface immobilization of a short antimicrobial peptide (AMP) as an antibacterial coating. Materialia, 2019: 6. doi: 10.1016/j.mtla.2019.100350.
46. de Breij A, Riool M, Kwakman PH, et al. Prevention of Staphylococcus aureus biomaterial-associated infections using a polymer-lipid coating containing the antimicrobial peptide OP-145. J Control Release, 2016, 222: 1-8.
47. 李健, 王颖, 高新蕾. 智能涂层——类生物表面活性智能涂层. 材料保护, 2006, 39(1): 36-39.
48. Sang S, Guo G, Yu J, et al. Antibacterial application of gentamicin-silk protein coating with smart release function on titanium, polyethylene, and Al₂O₃ materials. Mater Sci Eng C Mater Biol Appl, 2021, 124: 112069. doi: 10.1016/j.msec.2021.112069.
49. Zhang Y, Hu K, Xing X, et al. Smart titanium coating composed of antibiotic conjugated peptides as an infection-responsive antibacterial agent. Macromol Biosci, 2021, 21(1): e2000194. doi: 10.1002/mabi.202000194.
50. Pornpattananangkul D, Zhang L, Olson S, et al. Bacterial toxin-triggered drug release from gold nanoparticle-stabilized liposomes for the treatment of bacterial infection. J Am Chem Soc, 2011, 133(11): 4132-4139.

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