Advances in surface modification of orthopedic titanium implants for anti-infection_West China Medical Journal

Authors：

CHEN Li ¹ , XING Fei ¹ , XIANG Zhou ¹ ,  DUAN Xin ^1,2,3

1. Department of Orthopedic Surgery, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;
2. Department of Orthopedics, Gerontological Hospital of Sichuan Province, the Fifth People’s Hospital of Sichuan Province, Chengdu, Sichuan 610041, P. R. China;
3. Department of Orthopedics, Ganzi Tibetan Autonomous Prefecture People’s Hospital, Ganzi, Sichuan 626000, P. R. China;

Corresponding author：

DUAN Xin, Email: dxbaal@hotmail.com

Keywords：

Surface modification; anti-infection; osteogenesis; bone integration; immune regulation

DOI：

10.7507/1002-0179.202207144

Video：

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Abstract Full text Figures/Tables Video References Cited by

Titanium and its alloys have become one of the most widely used implant materials in orthopedics because of their excellent mechanical properties and biocompatibility. Implant-associated infection is the main reason of failure of orthopedic implant surgery. The anti-infection modification of implant surface has received more attention in the field of infection prevention and developed rapidly. This article focuses on the current research status of simple anti-infection surface modifications that make titanium implants possess anti-adhesion, bactericidal activity or antibacterial membrane activity, as well as the research progress of composite functional surface modifications that promote bone integration, osteogenesis or immunomodulatory effects on the basis of anti-infection, so as to provide references for the construction of orthopedic implants with composite functions.

Citation： CHEN Li, XING Fei, XIANG Zhou, DUAN Xin. Advances in surface modification of orthopedic titanium implants for anti-infection. West China Medical Journal, 2023, 38(10): 1578-1584. doi: 10.7507/1002-0179.202207144 Copy

1.	Akshaya S, Rowlo PK, Dukle A, et al. Antibacterial coatings for titanium implants: recent trends and future perspectives. Antibiotics (Basel), 2022, 11(12): 1719.
2.	Ren Y, Qin X, Barbeck M, et al. Mussel-inspired carboxymethyl chitosan hydrogel coating of titanium alloy with antibacterial and bioactive properties. Materials (Basel), 2021, 14(22): 6901.
3.	Yu S, Jiang B, Jia C, et al. Investigation of biofilm production and its association with genetic and phenotypic characteristics of OM (osteomyelitis) and non-OM orthopedic Staphylococcus aureus. Ann Clin Microbiol Antimicrob, 2020, 19(1): 10.
4.	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.
5.	Goodman SB, Yao Z, Keeney M, et al. The future of biologic coatings for orthopaedic implants. Biomaterials, 2013, 34(13): 3174-3183.
6.	Manivasagam VK, Perumal G, Arora HS, et al. Enhanced antibacterial properties on superhydrophobic micro-nano structured titanium surface. J Biomed Mater Res A, 2022, 110(7): 1314-1328.
7.	Benčina M, Resnik M, Starič P, et al. Use of plasma technologies for antibacterial surface properties of metals. Molecules, 2021, 26(5): 1418.
8.	Zhang E, Zhao X, Hu J, et al. Antibacterial metals and alloys for potential biomedical implants. Bioact Mater, 2021, 6(8): 2569-2612.
9.	Jimenez E, Hamdan-Partida A, Padilla-Godinez FJ, et al. Spectroscopic analysis and microbicidal effect of Ag/TiO₂-SiO₂ bionanocatalysts. IEEE Trans Nanobioscience, 2022, 21(2): 246-255.
10.	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.
11.	Poon TKC, Iyengar KP, Jain VK. Silver nanoparticle (AgNP) technology applications in trauma and orthopaedics. J Clin Orthop Trauma, 2021, 21: 101536.
12.	Zhao L, Wang H, Huo K, et al. Antibacterial nano-structured titania coating incorporated with silver nanoparticles. Biomaterials, 2011, 32(24): 5706-5716.
13.	Cazzola M, Barberi J, Ferraris S, et al. Bioactive titanium surfaces enriched with silver nanoparticles through an in situ reduction: looking for a balance between cytocompatibility and antibacterial activity. Adv Eng Mater, 2022, 25: 2200883.
14.	Gao C, Cheng H, Xu N, et al. Poly(dopamine) and Ag nanoparticle-loaded TiO2 nanotubes with optimized antibacterial and ROS-scavenging bioactivities. Nanomedicine (Lond), 2019, 14(7): 803-818.
15.	Chouirfa H, Bouloussa H, Migonney V, et al. Review of titanium surface modification techniques and coatings for antibacterial applications. Acta Biomater, 2019, 83: 37-54.
16.	Aguilera-Correa JJ, Garcia-Casas A, Mediero A, et al. A new antibiotic-loaded sol-gel can prevent bacterial prosthetic joint infection: from in vitro studies to an in vivo model. Front Microbiol, 2020, 10: 2935.
17.	Rams TE, Degener JE, van Winkelhoff AJ. Antibiotic resistance in human peri-implantitis microbiota. Clin Oral Implants Res, 2014, 25(1): 82-90.
18.	Ghosh S, Rajesh K, Roy PP, et al. Multilayered porous hydroxyapatite coating on Ti6Al4V implant with enhanced drug delivery and antimicrobial properties. J Drug Deliv Sci Technol, 2022, 70: 103155.
19.	Lv H, Chen Z, Yang X, et al. Layer-by-layer self-assembly of minocycline-loaded chitosan/alginate multilayer on titanium substrates to inhibit biofilm formation. J Dent, 2014, 42(11): 1464-1472.
20.	Zoghi N, Fouani MH, Bagheri H, et al. Characterization of minocycline loaded chitosan/polyethylene glycol/glycerol blend films as antibacterial wound dressings. J Appl Polym Sci, 2021, 138: e50781.
21.	Campoccia D, Montanaro L, Arciola CR. A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials, 2013, 34(34): 8533-8554.
22.	Zhu X, Tang W, Cheng X, et al. Roles of self-assembly and secondary structures in antimicrobial peptide coatings. Coatings, 2022, 12(10): 1456.
23.	Moreno D, Buxadera-Palomero J, Ginebra MP, et al. Comparison of the antibacterial effect of silver nanoparticles and a multifunctional antimicrobial peptide on titanium surface. Int J Mol Sci, 2023, 24(11): 9739.
24.	Kazemzadeh-Narbat M, Noordin S, Masri BA, et al. Drug release and bone growth studies of antimicrobial peptide-loaded calcium phosphate coating on titanium. J Biomed Mater Res B Appl Biomater, 2012, 100(5): 1344-1352.
25.	Zhou W, Bai T, Wang L, et al. Biomimetic AgNPs^@ antimicrobial peptide/silk fibroin coating for infection-trigger antibacterial capability and enhanced osseointegration. Bioact Mater, 2022, 20: 64-80.
26.	Masimen MAA, Harun NA, Maulidiani M, et al. Overcoming methicillin-resistance Staphylococcus aureus (MRSA) using antimicrobial peptides-silver nanoparticles. Antibiotics (Basel), 2022, 11(7): 951.
27.	Zhu M, Liu X, Tan L, et al. Photo-responsive chitosan/Ag/MoS2 for rapid bacteria-killing. J Hazard Mater, 2020, 383: 121122.
28.	Tian Y, Qi Y, Fang Y, et al. Near-infrared light-responsive multifunctional photothermal/photodynamic titanium diboride nanocomposites for the treatment of antibiotic-resistant bacterial infections. ACS Appl Bio Mater, 2023, 6(7): 2837-2848.
29.	Yang M, Qiu S, Coy E, et al. NIR-responsive TiO2 biometasurfaces: toward in situ photodynamic antibacterial therapy for biomedical implants. Adv Mater, 2022, 34(6): e2106314.
30.	Hlabangwane K, Matshitse R, Managa M, et al. The application of Sn(Ⅳ)Cl2 and In(Ⅲ)Cl porphyrin-dyed TiO2 nanofibers in photodynamic antimicrobial chemotherapy for bacterial inactivation in water. Photodiagnosis Photodyn Ther, 2023, 44: 103795.
31.	Vestby LK, Grønseth T, Simm R, et al. Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics (Basel), 2020, 9(2): 59.
32.	Bjarnsholt T, Buhlin K, Dufrêne YF, et al. Biofilm formation - what we can learn from recent developments. J Intern Med, 2018, 284(4): 332-345.
33.	Guo G, Zhang H, Shen H, et al. Space-selective chemodynamic therapy of CuFe₅O₈ nanocubes for implant-related infections. ACS Nano, 2020, 14(10): 13391-13405.
34.	Jiao Y, Tay FR, Niu LN, et al. Advancing antimicrobial strategies for managing oral biofilm infections. Int J Oral Sci, 2019, 11(3): 28.
35.	Schilcher K, Horswill AR. Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol Mol Biol Rev, 2020, 84(3): e00026-19.
36.	Koo H, Allan RN, Howlin RP, et al. Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol, 2017, 15(12): 740-755.
37.	Kucharíková S, Gerits E, De Brucker K, et al. Covalent immobilization of antimicrobial agents on titanium prevents Staphylococcus aureus and Candida albicans colonization and biofilm formation. J Antimicrob Chemother, 2016, 71(4): 936-945.
38.	Peeters E, Hooyberghs G, Robijns S, et al. An antibiofilm coating of 5-aryl-2-aminoimidazole covalently attached to a titanium surface. J Biomed Mater Res B Appl Biomater, 2019, 107(6): 1908-1919.
39.	Coppola GA, Onsea J, Moriarty TF, et al. An improved 2-aminoimidazole based anti-biofilm coating for orthopedic implants: activity, stability, and in vivo biocompatibility. Front Microbiol, 2021, 12: 658521.
40.	Beck S, Sehl C, Voortmann S, et al. Sphingosine is able to prevent and eliminate Staphylococcus epidermidis biofilm formation on different orthopedic implant materials in vitro. J Mol Med (Berl), 2020, 98(2): 209-219.
41.	Maia I, Carvalho O, Henriques, et al. Electrical potential approaches to inhibit biofilm adhesion on titanium implants. Mater Lett, 2019, 255: 126577.
42.	Mao C, Zhu W, Xiang Y, et al. Enhanced near-infrared photocatalytic eradication of mrsa biofilms and osseointegration using oxide perovskite-based P-N heterojunction. Adv Sci (Weinh), 2021, 8(15): e2002211.
43.	Han Q, Jiang Y, Brandt BW, et al. Regrowth of microcosm biofilms on titanium surfaces after various antimicrobial treatments. Front Microbiol, 2019, 10: 2693.
44.	He X, Yamada M, Watanabe J, et al. Titanium nanotopography induces osteocyte lacunar-canalicular networks to strengthen osseointegration. Acta Biomater, 2022, 151: 613-627.
45.	Wang S, Zhao X, Hsu Y, et al. Surface modification of titanium implants with Mg-containing coatings to promote osseointegration. Acta Biomater, 2023, 169: 19-44.
46.	Sun Y, Zhao YQ, Zeng Q, et al. DDual-functional implants with antibacterial and osteointegration-promoting performances. ACS Appl Mater Interfaces, 2019, 11(40): 36449-36457.
47.	Yang Z, Xi Y, Bai J, et al. Covalent grafting of hyperbranched poly-L-lysine on Ti-based implants achieves dual functions of antibacteria and promoted osteointegration in vivo. Biomaterials, 2021, 269: 120534.
48.	Meng F, Yin Z, Ren X, et al. Construction of local drug delivery system on titanium-based implants to improve osseointegration. Pharmaceutics, 2022, 14(5): 1069.
49.	Watson GS, Green DW, Schwarzkopf L, et al. A gecko skin micro/nano structure - a low adhesion, superhydrophobic, anti-wetting, self-cleaning, biocompatible, antibacterial surface. Acta Biomater, 2015, 21: 109-122.
50.	Jiang R, Hao L, Song L, et al. Lotus-leaf-inspired non-fouling, mechanical bactericidal surfaces. Chem Eng J, 2020, 398: 125609.
51.	Yuan Z, Tao B, He Y, et al. Biocompatible MoS2/PDA-RGD coating on titanium implant with antibacterial property via intrinsic ROS-independent oxidative stress and NIR irradiation. Biomaterials, 2019, 217: 119290.
52.	Liu Y, Wu J, Zhang H, et al. Covalent immobilization of the phytic acid-magnesium layer on titanium improves the osteogenic and antibacterial properties. Colloids Surf B Biointerfaces, 2021, 203: 111768.
53.	Wang L, Dai F, Yang Y, et al. Zeolitic imidazolate framework-8 with encapsulated naringin synergistically improves antibacterial and osteogenic properties of Ti implants for osseointegration. ACS Biomater Sci Eng, 2022, 8(9): 3797-3809.
54.	Wang Z, Wang X, Wang Y, et al. NanoZnO-modified titanium implants for enhanced anti-bacterial activity, osteogenesis and corrosion resistance. J Nanobiotechnology, 2021, 19(1): 353.
55.	Chen D, Yu C, Ying Y, et al. Study of the osteoimmunomodulatory properties of curcumin-modified copper-bearing titanium. Molecules, 2022, 27(10): 3205.
56.	Corrêa MG, Pimentel SP, Ribeiro FV, et al. Host response and peri-implantitis. Braz Oral Res, 2019, 33(suppl 1): e066.
57.	Chae K, Jang WY, Park K, et al. Antibacterial infection and immune-evasive coating for orthopedic implants. Sci Adv, 2020, 6(44): eabb0025.
58.	Villegas M, Zhang Y, Badv M, et al. Enhancing osseointegration and mitigating bacterial biofilms on medical-grade titanium with chitosan-conjugated liquid-infused coatings. Sci Rep, 2022, 12(1): 5380.
59.	Horwood NJ. Macrophage polarization and bone formation: a review. Clin Rev Allergy Immunol, 2016, 51(1): 79-86.
60.	Xue, Y, Zhang, L, Liu, F, et al. Immunomodulation and osteointegration of infected implants by ion-riched and hierarchical porous TiO2 matrix. Nano Res, 2022, 16: 2905-2914.

1. Akshaya S, Rowlo PK, Dukle A, et al. Antibacterial coatings for titanium implants: recent trends and future perspectives. Antibiotics (Basel), 2022, 11(12): 1719.
2. Ren Y, Qin X, Barbeck M, et al. Mussel-inspired carboxymethyl chitosan hydrogel coating of titanium alloy with antibacterial and bioactive properties. Materials (Basel), 2021, 14(22): 6901.
3. Yu S, Jiang B, Jia C, et al. Investigation of biofilm production and its association with genetic and phenotypic characteristics of OM (osteomyelitis) and non-OM orthopedic Staphylococcus aureus. Ann Clin Microbiol Antimicrob, 2020, 19(1): 10.
4. 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.
5. Goodman SB, Yao Z, Keeney M, et al. The future of biologic coatings for orthopaedic implants. Biomaterials, 2013, 34(13): 3174-3183.
6. Manivasagam VK, Perumal G, Arora HS, et al. Enhanced antibacterial properties on superhydrophobic micro-nano structured titanium surface. J Biomed Mater Res A, 2022, 110(7): 1314-1328.
7. Benčina M, Resnik M, Starič P, et al. Use of plasma technologies for antibacterial surface properties of metals. Molecules, 2021, 26(5): 1418.
8. Zhang E, Zhao X, Hu J, et al. Antibacterial metals and alloys for potential biomedical implants. Bioact Mater, 2021, 6(8): 2569-2612.
9. Jimenez E, Hamdan-Partida A, Padilla-Godinez FJ, et al. Spectroscopic analysis and microbicidal effect of Ag/TiO₂-SiO₂ bionanocatalysts. IEEE Trans Nanobioscience, 2022, 21(2): 246-255.
10. 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.
11. Poon TKC, Iyengar KP, Jain VK. Silver nanoparticle (AgNP) technology applications in trauma and orthopaedics. J Clin Orthop Trauma, 2021, 21: 101536.
12. Zhao L, Wang H, Huo K, et al. Antibacterial nano-structured titania coating incorporated with silver nanoparticles. Biomaterials, 2011, 32(24): 5706-5716.
13. Cazzola M, Barberi J, Ferraris S, et al. Bioactive titanium surfaces enriched with silver nanoparticles through an in situ reduction: looking for a balance between cytocompatibility and antibacterial activity. Adv Eng Mater, 2022, 25: 2200883.
14. Gao C, Cheng H, Xu N, et al. Poly(dopamine) and Ag nanoparticle-loaded TiO2 nanotubes with optimized antibacterial and ROS-scavenging bioactivities. Nanomedicine (Lond), 2019, 14(7): 803-818.
15. Chouirfa H, Bouloussa H, Migonney V, et al. Review of titanium surface modification techniques and coatings for antibacterial applications. Acta Biomater, 2019, 83: 37-54.
16. Aguilera-Correa JJ, Garcia-Casas A, Mediero A, et al. A new antibiotic-loaded sol-gel can prevent bacterial prosthetic joint infection: from in vitro studies to an in vivo model. Front Microbiol, 2020, 10: 2935.
17. Rams TE, Degener JE, van Winkelhoff AJ. Antibiotic resistance in human peri-implantitis microbiota. Clin Oral Implants Res, 2014, 25(1): 82-90.
18. Ghosh S, Rajesh K, Roy PP, et al. Multilayered porous hydroxyapatite coating on Ti6Al4V implant with enhanced drug delivery and antimicrobial properties. J Drug Deliv Sci Technol, 2022, 70: 103155.
19. Lv H, Chen Z, Yang X, et al. Layer-by-layer self-assembly of minocycline-loaded chitosan/alginate multilayer on titanium substrates to inhibit biofilm formation. J Dent, 2014, 42(11): 1464-1472.
20. Zoghi N, Fouani MH, Bagheri H, et al. Characterization of minocycline loaded chitosan/polyethylene glycol/glycerol blend films as antibacterial wound dressings. J Appl Polym Sci, 2021, 138: e50781.
21. Campoccia D, Montanaro L, Arciola CR. A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials, 2013, 34(34): 8533-8554.
22. Zhu X, Tang W, Cheng X, et al. Roles of self-assembly and secondary structures in antimicrobial peptide coatings. Coatings, 2022, 12(10): 1456.
23. Moreno D, Buxadera-Palomero J, Ginebra MP, et al. Comparison of the antibacterial effect of silver nanoparticles and a multifunctional antimicrobial peptide on titanium surface. Int J Mol Sci, 2023, 24(11): 9739.
24. Kazemzadeh-Narbat M, Noordin S, Masri BA, et al. Drug release and bone growth studies of antimicrobial peptide-loaded calcium phosphate coating on titanium. J Biomed Mater Res B Appl Biomater, 2012, 100(5): 1344-1352.
25. Zhou W, Bai T, Wang L, et al. Biomimetic AgNPs^@ antimicrobial peptide/silk fibroin coating for infection-trigger antibacterial capability and enhanced osseointegration. Bioact Mater, 2022, 20: 64-80.
26. Masimen MAA, Harun NA, Maulidiani M, et al. Overcoming methicillin-resistance Staphylococcus aureus (MRSA) using antimicrobial peptides-silver nanoparticles. Antibiotics (Basel), 2022, 11(7): 951.
27. Zhu M, Liu X, Tan L, et al. Photo-responsive chitosan/Ag/MoS2 for rapid bacteria-killing. J Hazard Mater, 2020, 383: 121122.
28. Tian Y, Qi Y, Fang Y, et al. Near-infrared light-responsive multifunctional photothermal/photodynamic titanium diboride nanocomposites for the treatment of antibiotic-resistant bacterial infections. ACS Appl Bio Mater, 2023, 6(7): 2837-2848.
29. Yang M, Qiu S, Coy E, et al. NIR-responsive TiO2 biometasurfaces: toward in situ photodynamic antibacterial therapy for biomedical implants. Adv Mater, 2022, 34(6): e2106314.
30. Hlabangwane K, Matshitse R, Managa M, et al. The application of Sn(Ⅳ)Cl2 and In(Ⅲ)Cl porphyrin-dyed TiO2 nanofibers in photodynamic antimicrobial chemotherapy for bacterial inactivation in water. Photodiagnosis Photodyn Ther, 2023, 44: 103795.
31. Vestby LK, Grønseth T, Simm R, et al. Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics (Basel), 2020, 9(2): 59.
32. Bjarnsholt T, Buhlin K, Dufrêne YF, et al. Biofilm formation - what we can learn from recent developments. J Intern Med, 2018, 284(4): 332-345.
33. Guo G, Zhang H, Shen H, et al. Space-selective chemodynamic therapy of CuFe₅O₈ nanocubes for implant-related infections. ACS Nano, 2020, 14(10): 13391-13405.
34. Jiao Y, Tay FR, Niu LN, et al. Advancing antimicrobial strategies for managing oral biofilm infections. Int J Oral Sci, 2019, 11(3): 28.
35. Schilcher K, Horswill AR. Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol Mol Biol Rev, 2020, 84(3): e00026-19.
36. Koo H, Allan RN, Howlin RP, et al. Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol, 2017, 15(12): 740-755.
37. Kucharíková S, Gerits E, De Brucker K, et al. Covalent immobilization of antimicrobial agents on titanium prevents Staphylococcus aureus and Candida albicans colonization and biofilm formation. J Antimicrob Chemother, 2016, 71(4): 936-945.
38. Peeters E, Hooyberghs G, Robijns S, et al. An antibiofilm coating of 5-aryl-2-aminoimidazole covalently attached to a titanium surface. J Biomed Mater Res B Appl Biomater, 2019, 107(6): 1908-1919.
39. Coppola GA, Onsea J, Moriarty TF, et al. An improved 2-aminoimidazole based anti-biofilm coating for orthopedic implants: activity, stability, and in vivo biocompatibility. Front Microbiol, 2021, 12: 658521.
40. Beck S, Sehl C, Voortmann S, et al. Sphingosine is able to prevent and eliminate Staphylococcus epidermidis biofilm formation on different orthopedic implant materials in vitro. J Mol Med (Berl), 2020, 98(2): 209-219.
41. Maia I, Carvalho O, Henriques, et al. Electrical potential approaches to inhibit biofilm adhesion on titanium implants. Mater Lett, 2019, 255: 126577.
42. Mao C, Zhu W, Xiang Y, et al. Enhanced near-infrared photocatalytic eradication of mrsa biofilms and osseointegration using oxide perovskite-based P-N heterojunction. Adv Sci (Weinh), 2021, 8(15): e2002211.
43. Han Q, Jiang Y, Brandt BW, et al. Regrowth of microcosm biofilms on titanium surfaces after various antimicrobial treatments. Front Microbiol, 2019, 10: 2693.
44. He X, Yamada M, Watanabe J, et al. Titanium nanotopography induces osteocyte lacunar-canalicular networks to strengthen osseointegration. Acta Biomater, 2022, 151: 613-627.
45. Wang S, Zhao X, Hsu Y, et al. Surface modification of titanium implants with Mg-containing coatings to promote osseointegration. Acta Biomater, 2023, 169: 19-44.
46. Sun Y, Zhao YQ, Zeng Q, et al. DDual-functional implants with antibacterial and osteointegration-promoting performances. ACS Appl Mater Interfaces, 2019, 11(40): 36449-36457.
47. Yang Z, Xi Y, Bai J, et al. Covalent grafting of hyperbranched poly-L-lysine on Ti-based implants achieves dual functions of antibacteria and promoted osteointegration in vivo. Biomaterials, 2021, 269: 120534.
48. Meng F, Yin Z, Ren X, et al. Construction of local drug delivery system on titanium-based implants to improve osseointegration. Pharmaceutics, 2022, 14(5): 1069.
49. Watson GS, Green DW, Schwarzkopf L, et al. A gecko skin micro/nano structure - a low adhesion, superhydrophobic, anti-wetting, self-cleaning, biocompatible, antibacterial surface. Acta Biomater, 2015, 21: 109-122.
50. Jiang R, Hao L, Song L, et al. Lotus-leaf-inspired non-fouling, mechanical bactericidal surfaces. Chem Eng J, 2020, 398: 125609.
51. Yuan Z, Tao B, He Y, et al. Biocompatible MoS2/PDA-RGD coating on titanium implant with antibacterial property via intrinsic ROS-independent oxidative stress and NIR irradiation. Biomaterials, 2019, 217: 119290.
52. Liu Y, Wu J, Zhang H, et al. Covalent immobilization of the phytic acid-magnesium layer on titanium improves the osteogenic and antibacterial properties. Colloids Surf B Biointerfaces, 2021, 203: 111768.
53. Wang L, Dai F, Yang Y, et al. Zeolitic imidazolate framework-8 with encapsulated naringin synergistically improves antibacterial and osteogenic properties of Ti implants for osseointegration. ACS Biomater Sci Eng, 2022, 8(9): 3797-3809.
54. Wang Z, Wang X, Wang Y, et al. NanoZnO-modified titanium implants for enhanced anti-bacterial activity, osteogenesis and corrosion resistance. J Nanobiotechnology, 2021, 19(1): 353.
55. Chen D, Yu C, Ying Y, et al. Study of the osteoimmunomodulatory properties of curcumin-modified copper-bearing titanium. Molecules, 2022, 27(10): 3205.
56. Corrêa MG, Pimentel SP, Ribeiro FV, et al. Host response and peri-implantitis. Braz Oral Res, 2019, 33(suppl 1): e066.
57. Chae K, Jang WY, Park K, et al. Antibacterial infection and immune-evasive coating for orthopedic implants. Sci Adv, 2020, 6(44): eabb0025.
58. Villegas M, Zhang Y, Badv M, et al. Enhancing osseointegration and mitigating bacterial biofilms on medical-grade titanium with chitosan-conjugated liquid-infused coatings. Sci Rep, 2022, 12(1): 5380.
59. Horwood NJ. Macrophage polarization and bone formation: a review. Clin Rev Allergy Immunol, 2016, 51(1): 79-86.
60. Xue, Y, Zhang, L, Liu, F, et al. Immunomodulation and osteointegration of infected implants by ion-riched and hierarchical porous TiO2 matrix. Nano Res, 2022, 16: 2905-2914.

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