journal article·2021-03-25Open access

Surface functionalization of titanium substrates with Deoxyribonuclease I inhibit peri-implant bacterial infection

Can SHAO, Xin ZHANG, Jing YE, Ya-Chong LI, Yi-Jun BAO, Zhi-hui LI, Ying HUANG, Ying LIU

Dental Materials Journal· Volume 40· Issue 2

Abstract

This study aimed to investigate the effect of Deoxyribonuclease I (DNase I) coating on initial adhesion and biofilm formation of peri-implant bacteria. Titanium (Ti), Ti-polydopamine (Ti-PDOP), Ti-PDOP-DNase I and Ti-PDOP-inactivated DNase I samples were studied. The FE-SEM, EDS and XPS were used to confirm that DNase I was coated onto Ti. The initial adhesion and biofilm formation of Aggregatibacter actinomycetemcomitans (A.a) and Fusobacterium nucleatum (F.n) were observed by CLSM. The osteogenic induction of Ti-PDOP-DNase I on MC3T3-E1 cells was investigated by ALP activity and RT-PCR. The adhesion clearance rate of viable bacteria on the surfaces of Ti-PDOP-DNase I was 91.95% for A.a, and 96.37% for F.n, and the 24 h biofilm formation of the bacteria was significantly inhibited. In addition, on DNase I coating, the mRNA level of osteogenic marker genes (alp, opn, bsp, sp7) and the activity of ALP were both up-regulated. Therefore, DNase I coating could be an alternative approach for preventing implant-related infection.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Dental Implant Techniques and Outcomes · Orthopedic Infections and Treatments · Bone Tissue Engineering Materials

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Endodontics, School of Stomatology, Tianjin Medical University

Department of Stomatology, Peking University Third Hospital Yanqing Hospital

Department of Prosthodonictcs, School of Stomatology, Tianjin Medical University

Department of Stomatology, Tianjin Hospital

Tianjin International Travel Health Center

References (46)

Show source-provided references
1. 1) Parnia F, Yazdani J, Javaherzadeh V, Maleki Dizaj S. Overview of nanoparticle coating of dental implants for enhanced osseointegration and antimicrobial purposes. J Pharm Pharm Sci 2017; 20: 148-160.10.18433/J3GP6G ↗
2. 2) Jemat A, Ghazali MJ, Razali M, Otsuka Y. Surface modifications and their effects on titanium dental implants. Biomed Res Int 2015; 2015: 791725.10.1155/2015/791725 ↗
3. 3) Liu HC. [Influence of implant restoration on traditional restoration idea]. Zhonghua Kou Qiang Yi Xue Za Zhi 2016; 51: 3-6.
4. 4) Kashbour WA, Rousseau NS, Ellis JS, Thomason JM. Patients’experiences of dental implant treatment: A literature review of key qualitative studies. J Dent 2015; 43: 789-797.10.1016/j.jdent.2015.04.008 ↗
5. 5) Liu X, Chen S, Tsoi JKH. Binary titanium alloys as dental implant materials-a review. Regen Biomater 2017; 4: 315-323.10.1093/rb/rbx027 ↗
6. 6) Subbiahdoss G, Kuijer R, Grijpma DW, van der Mei HC, Busscher HJ. Microbial biofilm growth vs. tissue integration: “the race for the surface” experimentally studied. Acta Biomater 2009; 5: 1399-1404.10.1016/j.actbio.2008.12.011 ↗
7. 7) Busscher HJ, van der Mei HC, Subbiahdoss G, Jutte PC, van den Dungen JJ, Zaat SA, et al. Biomaterial-associated infection: locating the finish line in the race for the surface. Sci Transl Med 2012; 4: 153rv10.10.1126/scitranslmed.3004528 ↗
8. 8) Atieh MA, Alsabeeha NH, Faggion CM Jr, Duncan WJ. The frequency of peri-implant diseases: a systematic review and meta-analysis. J Periodontol 2013; 84: 1586-1598.10.1902/jop.2012.120592 ↗
9. 9) Zitzmann NU, Berglundh T. Definition and prevalence of peri-implant diseases. J Clin Periodontol 2008; 35: 286-291.10.1111/j.1600-051X.2008.01274.x ↗
10. 10) Hall Snyder AD, Vidaillac C, Rose W, McRoberts JP, Rybak MJ. Evaluation of high-dose daptomycin versus vancomycin alone or combined with clarithromycin or rifampin against Staphylococcus aureus and s. epidermidis in a novel in vitro PK/PD model of bacterial biofilm. Infect Dis Ther 2015; 4: 51-65.10.1007/s40121-014-0055-5 ↗
11. 11) Lv H, Chen Z, Yang X, Cen L, Zhang X, Gao P. Layer-by-layer self-assembly of minocycline-loaded chitosan/alginate multilayer on titanium substrates to inhibit biofilm formation. J Dent 2014; 42: 1464-1472.10.1016/j.jdent.2014.06.003 ↗
12. 12) He S, Zhou P, Wang L, Xiong X, Zhang Y, Deng Y, et al. Antibiotic- decorated titanium with enhanced antibacterial activity through adhesive polydopamine for dental/bone implant. J R Soc Interface 2014; 11: 20140169.10.1098/rsif.2014.0169 ↗
13. 13) Unosson E, Rodriguez D, Welch K, Engqvist H. Reactive combinatorial synthesis and characterization of a gradient Ag-Ti oxide thin film with antibacterial properties. Acta Biomater 2015; 11: 503-510.10.1016/j.actbio.2014.09.048 ↗
14. 14) Zhou L, Lai Y, Huang W, Huang S, Xu Z, Chen J, et al. Biofunctionalization of microgroove titanium surfaces with an antimicrobial peptide to enhance their bactericidal activity and cytocompatibility. Colloids Surf B Biointerfaces 2015; 128: 552-560.10.1016/j.colsurfb.2015.03.008 ↗
15. 15) Zhang Y, Xu Z, Suo H, Feng W. [Research progress of drug-loaded antibacterial coating of orthopedic metal implants]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2017; 31: 1396-1401.
16. 16) Cordeiro AL, Hippius C, Werner C. Immobilized enzymes affect biofilm formation. Biotechnol Lett 2011; 33: 1897-1904.10.1007/s10529-011-0643-3 ↗
17. 17) Fulaz S, Vitale S, Quinn L, Casey E. Nanoparticle-biofilm interactions: The role of the EPS matrix. Trends Microbiol 2019; 27: 915-626.10.1016/j.tim.2019.07.004 ↗
18. 18) Alves D, Olivia Pereira M. Mini-review: Antimicrobial peptides and enzymes as promising candidates to functionalize biomaterial surfaces. Biofouling 2014; 30: 483-499.10.1080/08927014.2014.889120 ↗
19. 19) Okshevsky M, Meyer RL. The role of extracellular DNA in the establishment, maintenance and perpetuation of bacterial biofilms. Crit Rev Microbiol 2015; 41: 341-352.10.3109/1040841X.2013.841639 ↗
20. 20) Kang J, Tada S, Kitajima T, Son TI, Aigaki T, Ito Y. Immobilization of bone morphogenetic protein on DOPA-or dopamine-treated titanium surfaces to enhance osseointegration. Biomed Res Int 2013; 2013: 265980.10.1155/2013/265980 ↗
21. 21) Cai Y, Wang X, Poh CK, Tan HC, Soe MT, Zhang S, et al. Accelerated bone growth in vitro by the conjugation of BMP2 peptide with hydroxyapatite on titanium alloy. Colloids Surf B Biointerfaces 2014; 116: 681-686.10.1016/j.colsurfb.2013.11.004 ↗
22. 22) Ye J, Shao C, Zhang X, Guo X, Gao P, Cen Y, et al. Effects of DNase I coating of titanium on bacteria adhesion and biofilm formation. Mater Sci Eng C Mater Biol Appl 2017; 78: 738-747.10.1016/j.msec.2017.04.078 ↗
23. 23) Cortelli SC, Cortelli JR, Romeiro RL, Costa FO, Aquino DR, Orzechowski PR, et al. Frequency of periodontal pathogens in equivalent peri-implant and periodontal clinical statuses. Arch Oral Biol 2013; 58: 67-74.10.1016/j.archoralbio.2012.09.004 ↗
24. 24) Zhuang LF, Watt RM, Mattheos N. Periodontal and peri-implant microbiota in patients with healthy and inflamed periodontal and peri-implant tissues. Clin Oral Implants Res 2016; 27: 13-21.10.1111/clr.12508 ↗
25. 25) Wang HL, Garaicoa-Pazmino C, Collins A, Ong HS, Chudri R, Giannobile WV. Protein biomarkers and microbial profiles in peri-implantitis. Clin Oral Implants Res 2016; 27: 1129-1136.10.1111/clr.12708 ↗
26. 26) Lafaurie GI, Sabogal MA, Castillo DM, Rincon MV, Gomez LA, Lesmes YA, et al. Microbiome and microbial biofilm profiles of peri-implantitis: A systematic review. J Periodontol 2017; 88: 1066-1089.10.1902/jop.2017.170123 ↗
27. 27) Kadkhoda Z, Amarlu Z, Eshraghi S, Samiei N. Antimicrobial effect of chlorhexidine on Aggregatibacter actinomycetemcomitans biofilms associated with peri-implantitis. J Dent Res Dent Clin Dent Prospects 2016; 10: 176-180.10.15171/joddd.2016.028 ↗
28. 28) Albertini M, Lopez-Cerero L, O’Sullivan MG, Chereguini CF, Ballesta S, Rios V, et al. Assessment of periodontal and opportunistic flora in patients with peri-implantitis. Clin Oral Implants Res 2015; 26: 937-941.10.1111/clr.12387 ↗
29. 29) Perez-Chaparro PJ, Duarte PM, Shibli JA, Montenegro S, Lacerda Heluy S, Figueiredo LC, et al. The current weight of evidence of the microbiologic profile associated with peri-implantitis: A systematic review. J Periodontol 2016; 87: 1295-1304.10.1902/jop.2016.160184 ↗
30. 30) Rakic M, Grusovin MG, Canullo L. The microbiologic profile associated with peri-implantitis in humans: A systematic review. Int J Oral Maxillofac Implants 2016; 31: 359-368.10.11607/jomi.4150 ↗
31. 31) Hultin M, Gustafsson A, Hallstrom H, Johansson LA, Ekfeldt A, Klinge B. Microbiological findings and host response in patients with peri-implantitis. Clin Oral Implants Res 2002; 13: 349-358.10.1034/j.1600-0501.2002.130402.x ↗
32. 32) da Silva ES, Feres M, Figueiredo LC, Shibli JA, Ramiro FS, Faveri M. Microbiological diversity of peri-implantitis biofilm by Sanger sequencing. Clin Oral Implants Res 2014; 25: 1192-1199.10.1111/clr.12231 ↗
33. 33) Su EP, Justin DF, Pratt CR, Sarin VK, Nguyen VS, Oh S, et al. Effects of titanium nanotubes on the osseointegration, cell differentiation, mineralisation and antibacterial properties of orthopaedic implant surfaces. Bone Joint J 2018; 100-b: 9-16.10.1302/0301-620X.100B1.BJJ-2017-0551.R1 ↗
34. 34) Persson GR, Renvert S. Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res 2014; 16: 783-793.10.1111/cid.12052 ↗
35. 35) Coli P, Christiaens V, Sennerby L, Bruyn H. Reliability of periodontal diagnostic tools for monitoring peri-implant health and disease. Periodontol 2000 2017; 73: 203-217.10.1111/prd.12162 ↗
36. 36) Feller L, Jadwat Y, Chandran R, Lager I, Altini M, Lemmer J. Radiolucent inflammatory implant periapical lesions: a review of the literature. Implant Dent 2014; 23: 745-752.10.1097/ID.0000000000000140 ↗
37. 37) Veerachamy S, Yarlagadda T, Manivasagam G, Yarlagadda PK. Bacterial adherence and biofilm formation on medical implants: a review. Proc Inst Mech Eng H 2014; 228: 1083-1099.10.1177/0954411914556137 ↗
38. 38) de la Fuente-Nunez C, Reffuveille F, Fernandez L, Hancock RE. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 2013; 16: 580-589.10.1016/j.mib.2013.06.013 ↗
39. 39) Ferraris S, Spriano S. Antibacterial titanium surfaces for medical implants. Mater Sci Eng C Mater Biol Appl 2016; 61: 965-978.10.1016/j.msec.2015.12.062 ↗
40. 40) Yang SY, Kim ES, Jeon G, Choi KY, Kim JK. Enhanced adhesion of osteoblastic cells on polystyrene films by independent control of surface topography and wettability. Mater Sci Eng C Mater Biol Appl 2013; 33: 1689-1695.10.1016/j.msec.2012.12.081 ↗
41. 41) Jia L, Han F, Wang H, Zhu C, Guo Q, Li J, et al. Polydopamine-assisted surface modification for orthopaedic implants. J Orthop Translat 2019; 17: 82-95.10.1016/j.jot.2019.04.001 ↗
42. 42) Gittens RA, Olivares-Navarrete R, McLachlan T, Cai Y, Hyzy SL, Schneider JM, et al. Differential responses of osteoblast lineage cells to nanotopographically-modified, microroughened titanium-aluminum-vanadium alloy surfaces. Biomaterials 2012; 33: 8986-8994.10.1016/j.biomaterials.2012.08.059 ↗
43. 43) Ridwan RD, Sidarningsih, Kusumaningsih T, Salim S. Effect of lipopolysaccharide derived from surabaya isolates of Actinobacillus actinomycetemcomitans on alveolar bone destruction. Vet World 2018; 11: 161-166.10.14202/vetworld.2018.161-166 ↗
44. 44) Hendrickson EL, Wang T, Beck DA, Dickinson BC, Wright CJ, R JL, et al. Proteomics of Fusobacterium nucleatum within a model developing oral microbial community. Microbiologyopen 2014; 3: 729-751.10.1002/mbo3.204 ↗
45. 45) Chien CY, Tsai WB. Poly(dopamine)-assisted immobilization of Arg-Gly-Asp peptides, hydroxyapatite, and bone morphogenic protein-2 on titanium to improve the osteogenesis of bone marrow stem cells. ACS Appl Mater Interfaces 2013; 5: 6975-6983.10.1021/am401071f ↗
46. 46) Lee BH, Do Kim Y, Shin JH, Hwan Lee K. Surface modification by alkali and heat treatments in titanium alloys. J Biomed Mater Res 2002; 61: 466-473.10.1002/jbm.10190 ↗