Hybrid system with stable structure of hard/soft tissue substitutes induces re-osseointegration in a rat model of biofilm-mediated peri-implantitis.
bone substitutes
dental implant
osseointegration
peri-implantitis
regenerative treatment
Journal
Journal of biomedical materials research. Part B, Applied biomaterials
ISSN: 1552-4981
Titre abrégé: J Biomed Mater Res B Appl Biomater
Pays: United States
ID NLM: 101234238
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
19
03
2022
received:
03
12
2021
accepted:
09
05
2022
pubmed:
28
5
2022
medline:
20
9
2022
entrez:
27
5
2022
Statut:
ppublish
Résumé
Re-osseointegration of an infected/contaminated dental implant poses major clinical challenges. We tested the hypothesis that the application of an antibiotic-releasing construct, combined with hard/soft tissue replacement, increases the efficacy of reconstructive therapy. We initially fabricated semi-flexible hybrid constructs of β-TCP/PHBHHx, with tetracycline (TC) (TC amounts: 5%, 10%, and 15%). Thereafter, using in vitro assays, TC release profile, attachment to rat bone marrow-derived stem cells (rBMSCs) and their viability as well as anti-bacterial activity were determined. Thereafter, regenerative efficacies of the three hybrid constructs were assessed in a rat model of peri-implantitis induced by Aggregatibacter actinomycetemcomitans biofilm; control animals received β-TCP/Bio-Gide and TC injection. Eight weeks later, maxillae were obtained for radiological, histological, and histomorphometric analyses of peri-implant tissues. Sulcus bleeding index was chronologically recorded. Serum cytokines levels of IL-6 and IL-1β were also evaluated by enzyme-linked immunosorbent assay. Substantial amounts of tetracycline, from hybrid constructs, were released for 2 weeks. The medium containing the released tetracycline did not affect the adhesion or viability of rBMSCs; however, it inhibited the proliferation of A. actinomycetemcomitans. Osteogenesis and osseointegration were more marked for the 15% hybrid construct group than the other two groups. The height of attachment and infiltration of inflammatory cells within fibrous tissue was significantly reduced in the experimental groups than the control group. Our protocol resulted in re-osseointegration on a biofilm-contaminated implant. Thus, an antibiotic releasing inorganic/organic construct may offer a therapeutic option to suppress infection and promote guided tissue regeneration thereby serving as an integrated multi-layer substitute for both hard/soft tissues.
Substances chimiques
Anti-Bacterial Agents
0
Calcium Phosphates
0
Cytokines
0
Dental Implants
0
Interleukin-6
0
beta-tricalcium phosphate
0
Tetracycline
F8VB5M810T
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2452-2463Subventions
Organisme : Natural Science Foundation of Ningxia Province
ID : NZ17178
Organisme : National Natural Science Foundation of China
ID : 81700940
Organisme : National Natural Science Foundation of China
ID : 81800981
Organisme : National Natural Science Foundation of China
ID : 81860203
Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Lang NP, Wilson TG, Corbet EF. Biological complications with dental implants: their prevention, diagnosis and treatment. Clin Oral Implants Res. 2000;11(Suppl 1):146-155.
Schwarz F, John G, Schmucker A, Sahm N, Becker J. Combined surgical therapy of advanced peri-implantitis evaluating two methods of surface decontamination: a 7-year follow-up observation. J Clin Periodontol. 2017;44(3):337-342.
Heitz-Mayfield LJ, Needleman I, Salvi GE, Pjetursson BE. Consensus statements and clinical recommendations for prevention and management of biologic and technical implant complications. Int J Oral Maxillofac Implants. 2014;29:346-350.
Lang NP, Mombelli A, Tonetti MS, Brägger U, Hämmerle CHF. Clinical trials on therapies for peri-implant infections. Ann Periodontol. 1997;2(1):343-356.
Vervaeke S, De Bruyn H. Peri-implantitis. Rev Belg Med Dent. 1984;63(4):161-170.
Subramani K, Mathew R, Hosseinkhani H, Hosseinkhani M. Bone regeneration around dental implants as a treatment for peri-implantitis: a review of the literature. J Biomim Biomater Tissue Eng. 2011;11:21-33.
Wetzel AC, Vlassis J, Caffesse RG, Hämmerle CHF, Lang NP. Attempts to obtain re-osseointegration following experimental peri-implantitis in dogs. Clin Oral Implants Res. 1999;10(2):111-119.
Norowski PA Jr, Bumgardner JD. Biomaterial and antibiotic strategies for peri-implantitis: a review. J Biomed Mater Res B: Appl Biomater. 2009;88(2):530-543.
Machtei EE, Kim DM, Karimbux N, Zigdon-Giladi H. The use of endothelial progenitor cells combined with barrier membrane for the reconstruction of peri-implant osseous defects: an animal experimental study. J Clin Periodontol. 2016;43(3):289-297.
Xu L, Sun X, Bai J, et al. Reosseointegration following regenerative therapy of tissue-engineered bone in a canine model of experimental Peri-Implantitis. Clin Implant Dent Relat Res. 2016;18(2):379-391.
Park SY, Kim KH, Gwak EH, et al. Ex vivo bone morphogenetic protein 2 gene delivery using periodontal ligament stem cells for enhanced re-osseointegration in the regenerative treatment of peri-implantitis. J Biomed Mater Res A. 2015;103(1):38-47.
Caffesse RG, Echeverria JJ. Treatment trends in periodontics. Periodontol 2000. 2019;79(1):7-14.
Guerra I, Morais Branco F, Vasconcelos M, Afonso A, Figueiral H, Zita R. Evaluation of implant osseointegration with different regeneration techniques in the treatment of bone defects around implants: an experimental study in a rabbit model. Clin Oral Implants Res. 2011;22(3):314-322.
He J, Li Z, Yu T, et al. Preparation and evaluation of acellular sheep periostea for guided bone regeneration. J Biomed Mater Res A. 2020;108(1):19-29.
Wang HL, Boyapati L. "PASS" principles for predictable bone regeneration. Implant Dent. 2006;15(1):8-17.
Khoury F, Keeve PL, Ramanauskaite A, et al. Surgical treatment of peri-implantitis - consensus report of working group 4. Int Dent J. 2019;69(Suppl 2):18-22.
Chung JJ, Fujita Y, Li S, et al. Biodegradable inorganic-organic hybrids of methacrylate star polymers for bone regeneration. Acta Biomater. 2017;54:411-418.
Pang L, Shen Y, Hu H, et al. Chemically and physically cross-linked polyvinyl alcohol-borosilicate gel hybrid scaffolds for bone regeneration. Mater Sci Eng C: Mater Biol Appl. 2019;105:110076.
Zhang Y, Chen M, Tian J, et al. In situ bone regeneration enabled by a biodegradable hybrid double-network hydrogel. Biomater Sci. 2019;7(8):3266-3276.
Park JW, Kim JM, Lee HJ, Jeong SH, Suh JY, Hanawa T. Bone healing with oxytocin-loaded microporous beta-TCP bone substitute in ectopic bone formation model and critical-sized osseous defect of rat. J Clin Periodontol. 2014;41(2):181-190.
Mota C, Wang SY, Puppi D, et al. Additive manufacturing of poly[(R)-3-hydroxybutyrate-co-(R)-3-hydroxyhexanoate] scaffolds for engineered bone development. J Tissue Eng Regen Med. 2017;11(1):175-186.
Webb WR, Dale TP, Lomas AJ, et al. The application of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) scaffolds for tendon repair in the rat model. Biomaterials. 2013;34(28):6683-6694.
Li J, Yun H, Gong Y, Zhao N, Zhang X. Effects of surface modification of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate) (PHBHHx) on physicochemical properties and on interactions with MC3T3-E1 cells. J Biomed Mater Res A. 2005;75(4):985-998.
Yang S, Xu S, Zhou P, et al. Siliceous mesostructured cellular foams/poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) composite biomaterials for bone regeneration. Int J Nanomedicine. 2014;9:4795-4807.
Bian YZ, Wang Y, Aibaidoula G, Chen GQ, Wu Q. Evaluation of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) conduits for peripheral nerve regeneration. Biomaterials. 2009;30(2):217-225.
Peng Q, Zhang ZR, Gong T, Chen GQ, Sun X. A rapid-acting, long-acting insulin formulation based on a phospholipid complex loaded PHBHHx nanoparticles. Biomaterials. 2012;33(5):1583-1588.
Wang Y, Gao R, Wang PP, et al. The differential effects of aligned electrospun PHBHHx fibers on adipogenic and osteogenic potential of MSCs through the regulation of PPARgamma signaling. Biomaterials. 2012;33(2):485-493.
Wu Q, Wang X, Jiang F, Zhu Z, Wen J, Jiang X. Study of Sr-ca-Si-based scaffolds for bone regeneration in osteoporotic models. Int J Oral Sci. 2020;12(1):25.
Kim J, Ren D, Gilbert JL. Cytotoxic effect of galvanically coupled magnesium-titanium particles on Escherichia coli. J Biomed Mater Res B: Appl Biomater. 2021;109(12):2162-2173.
Merkhan IK, Hasenwinkel JM, Gilbert JL. Gentamicin release from two-solution and powder-liquid poly(methyl methacrylate)-based bone cements by using novel pH method. J Biomed Mater Res A. 2004;69(3):577-583.
Mombelli A, Feloutzis A, Brägger U, Lang NP. Treatment of peri-implantitis by local delivery of tetracycline. Clinical, microbiological and radiological results. Clin Oral Implants Res. 2001;12(4):287-294.
Park JB. Effects of doxycycline, minocycline, and tetracycline on cell proliferation, differentiation, and protein expression in osteoprecursor cells. J Craniofac Surg. 2011;22(5):1839-1842.
Freire MO, Sedghizadeh PP, Schaudinn C, et al. Development of an animal model for Aggregatibacter actinomycetemcomitans biofilm-mediated oral osteolytic infection: a preliminary study. J Periodontol. 2011;82(5):778-789.
Wang X, Li Y, Feng Y, Cheng H, Li D. The role of macrophages in osseointegration of dental implants: an experimental study in vivo. J Biomed Mater Res A. 2020;108(11):2206-2216.
Zhao J, Shen G, Liu C, et al. Enhanced healing of rat calvarial defects with sulfated chitosan-coated calcium-deficient hydroxyapatite/bone morphogenetic protein 2 scaffolds. Tissue Eng Part A. 2012;18(1-2):185-197.
Vijayalashmi Ranganathan, Ravindranath Sabitha Manhalore, Jayakumar Nadathur Doraiswamy, Padmalatha, Vargheese Sheeja H, Kumaraswamy Kikkeri Laxminarayana. Kinetics of drug release from a biodegradable local drug delivery system and its effect on Porphyromonas gingivalis isolates: an in vitro study. J Indian Soc Periodontol. 2013;17(4):429-434.
Jiang X, Zhao J, Wang S, et al. Mandibular repair in rats with premineralized silk scaffolds and BMP-2-modified bMSCs. Biomaterials. 2009;30(27):4522-4532.
Sun J, Eberhard J, Glage S, et al. Development of a peri-implantitis model in the rat. Clin Oral Implants Res. 2020;31(3):203-214.
Shi Q, Song K, Zhou X, et al. Effects of non-equilibrium plasma in the treatment of ligature-induced peri-implantitis. J Clin Periodontol. 2015;42(5):478-487.
Mazza JE, Newman MG, Sims TN. Clinical and antimicrobial effect of stannous fluoride on periodontitis. J Clin Periodontol. 1981;8(3):203-212.
van Herck H, Baumans V, Brandt CJWM, et al. Blood sampling from the retro-orbital plexus, the saphenous vein and the tail vein in rats: comparative effects on selected behavioural and blood variables. Lab Anim. 2001;35(2):131-139.
Ghassib I, Chen Z, Zhu J, Wang HL. Use of IL-1 beta, IL-6, TNF-alpha, and MMP-8 biomarkers to distinguish peri-implant diseases: a systematic review and meta-analysis. Clin Implant Dent Relat Res. 2019;21(1):190-207.
Moskow BS, Tannenbaum P. Enhanced repair and regeneration of periodontal lesions in tetracycline-treated patients: case reports. J Periodontol. 1991;62(5):341-350.
Stavropoulos A, Windisch P, Gera I, Capsius B, Sculean A, Wikesjö UME. A phase IIa randomized controlled clinical and histological pilot study evaluating rhGDF-5/beta-TCP for periodontal regeneration. J Clin Periodontol. 2011;38(11):1044-1054.
Ozdemir B, Okte E. Treatment of intrabony defects with beta-tricalciumphosphate alone and in combination with platelet-rich plasma. J Biomed Mater Res B: Appl Biomater. 2012;100(4):976-983.
Bengtsson NE, Seto JT, Hall JK, Chamberlain JS, Odom GL. Progress and prospects of gene therapy clinical trials for the muscular dystrophies. Hum Mol Genet. 2016;25:R9-R17.
Varon-Shahar E, Shusterman A, Piattelli A, Iezzi G, Weiss EI, Houri-Haddad Y. Peri-implant alveolar bone resorption in an innovative peri-implantitis murine model: effect of implant surface and onset of infection. Clin Implant Dent Relat Res. 2019;21(4):723-733.
Ding L, Zhang P, Wang X, Kasugai S. A doxycycline-treated hydroxyapatite implant surface attenuates the progression of peri-implantitis: a radiographic and histological study in mice. Clin Implant Dent Relat Res. 2019;21(1):154-159.
Koutouzis T, Eastman C, Chukkapalli S, Larjava H, Kesavalu L. A novel rat model of polymicrobial peri-implantitis: a preliminary study. J Periodontol. 2017;88(2):e32-e41.
Park SY, Kim KH, Rhee SH, et al. An immediate peri-implantitis induction model to study regenerative peri-implantitis treatments. Clin Oral Implants Res. 2017;28(1):36-42.
Rok J, Buszman E, Delijewski M, Otręba M, Beberok A, Wrześniok D. Effect of tetracycline and UV radiation on melanization and antioxidant status of melanocytes. J Photochem Photobiol B. 2015;148:168-173.
Ezhilarasu H, Ramalingam R, Dhand C, et al. Biocompatible aloe vera and tetracycline hydrochloride loaded hybrid nanofibrous scaffolds for skin tissue engineering. Int J Mol Sci. 2019;20(20):5147.
Jin SH, Kweon HY, Park JB, Kim CH. The effects of tetracycline-loaded silk fibroin membrane on proliferation and osteogenic potential of mesenchymal stem cells. J Surg Res. 2014;192(2):e1-e9.