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Endocrine, Metabolic & Immune Disorders - Drug Targets

Author(s): Mario Dioguardi, Stefania Cantore*, Cristian Quarta, Diego Sovereto, Nicoletta Zerman, Francesco Pettini, Lorenzo Lo Muzio, Michele Di Cosola, Luigi Santacroce and Andrea Ballini*

DOI: 10.2174/1871530323666221021100427

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Correlation between Diabetes Mellitus and Peri-implantitis: A Systematic Review

Page: [596 - 608] Pages: 13

  • * (Excluding Mailing and Handling)

Abstract

Background: Osseo-integrated implants provide effective treatment results for edentulous patients. However, despite the high success and survival rates of dental implants, several factors, such as poor oral hygiene and a history of periodontal disease, and systemic diseases, such as diabetes mellitus, could influence the outcome of the treatment. In fact, poor glycemic control can affect the healing process. Diabetes mellitus is considered a relative contraindication for dental implant therapy due to the fact that the success rates of the implants seem to be lower in diabetic patients, even if there is no total agreement among the results reported in the literature. The analysis of peri-implant inflammation indices, bone loss around the implant and glycemic index can provide us with useful information on the relationship between glycaemia in diabetic patients and the course of peri-implantitis, as well as implant success in the short term.

Objective: The purpose of this review is to establish how peri-implant inflammation parameters vary in diabetic versus non-diabetic patients.

Methods: This review was conducted on the basis of PRISMA. The search was conducted by three independent reviewers searching for keywords in three databases: PubMed, Scopus, Web Of Sciences (WOS), and the Cochrane Central Register of Controlled Trial.

Results: A total of 1159 records were identified, and 11 articles were included in the qualitative analysis.

Conclusion: The analysis of the extracted data from the included studies suggests that some periimplant inflammation indices, such as bleeding on probing and bone loss around the implant, appear to be increased in diabetic patients with glycometabolic decompensation, compared with control not affected by diabetes mellitus.

Graphical Abstract

[1]
Schwartz-Arad, D.; Kidron, N.; Dolev, E. A long-term study of implants supporting overdentures as a model for implant success. J. Periodontol., 2005, 76(9), 1431-1435.
[http://dx.doi.org/10.1902/jop.2005.76.9.1431] [PMID: 16171428]
[2]
Ballini, A. Comparison of manual nylon bristled versus thermoplastic elastomer toothbrushes in terms of cleaning efficacy and biological potential role on gingival health. Appl. Sci., 2021, 11, 7180.
[http://dx.doi.org/10.3390/app11167180]
[3]
Di Cosola, M.; Ballini, A.; Zhurakivska, K.; Ceccarello, A.; Nocini, R.; Malcangi, A.; Mori, G.; Lo Muzio, L.; Cantore, S.; Olivo, A. Retrospective analysis of clinical and radiologic data regarding zygomatic implant rehabilitation with a long-term follow-up. Int. J. Environ. Res. Public Health, 2021, 18(24), 12963.
[http://dx.doi.org/10.3390/ijerph182412963] [PMID: 34948572]
[4]
Cosyn, J.; Vandenbulcke, E.; Browaeys, H.; Van Maele, G.; De Bruyn, H. Factors associated with failure of surface-modified implants up to four years of function. Clin. Implant Dent. Relat. Res., 2012, 14(3), 347-358.
[http://dx.doi.org/10.1111/j.1708-8208.2010.00282.x] [PMID: 20491819]
[5]
Borsani, E.; Salgarello, S.; Mensi, M.; Boninsegna, R.; Stacchiotti, A.; Rezzani, R.; Sapelli, P.; Bianchi, R.; Rodella, L.F. Histochemical and immunohistochemical evaluation of gingival collagen and metalloproteinases in peri-implantitis. Acta Histochem., 2005, 107(3), 231-240.
[http://dx.doi.org/10.1016/j.acthis.2005.06.002] [PMID: 16054676]
[6]
Veiseh, O.; Langer, R. A smart insulin patch. Nature, 2015, 524(7563), 39-40.
[http://dx.doi.org/10.1038/524039a] [PMID: 26245577]
[7]
Kearney, K.; Tomlinson, D.; Smith, K.; Ajjan, R. Hypofibrinolysis in diabetes: A therapeutic target for the reduction of cardiovascular risk. Cardiovasc. Diabetol., 2017, 16(1), 34.
[http://dx.doi.org/10.1186/s12933-017-0515-9] [PMID: 28279217]
[8]
Blanchaert, R.H. Implants in the medically challenged patient. Dent. Clin. North Am., 1998, 42(1), 35-45.
[http://dx.doi.org/10.1016/S0011-8532(22)00603-6] [PMID: 9421668]
[9]
Jiao, H.; Xiao, E.; Graves, D.T. Diabetes and its effect on bone and fracture healing. Curr. Osteoporos. Rep., 2015, 13(5), 327-335.
[http://dx.doi.org/10.1007/s11914-015-0286-8] [PMID: 26254939]
[10]
Nevins, M.L.; Karimbux, N.Y.; Weber, H.P.; Giannobile, W.V.; Fiorellini, J.P. Wound healing around endosseous implants in experimental diabetes. Int. J. Oral Maxillofac. Implants, 1998, 13(5), 620-629.
[PMID: 9796145]
[11]
Gerritsen, M.; Lutterman, J.A.; Jansen, J.A. Wound healing around bone-anchored percutaneous devices in experimental diabetes mellitus. J. Biomed. Mater. Res., 2000, 53(6), 702-709.
[http://dx.doi.org/10.1002/1097-4636(2000)53:6<702::AID-JBM13>3.0.CO;2-V] [PMID: 11074430]
[12]
Javed, F.; Näsström, K.; Benchimol, D.; Altamash, M.; Klinge, B.; Engström, P.E. Comparison of periodontal and socioeconomic status between subjects with type 2 diabetes mellitus and non-diabetic controls. J. Periodontol., 2007, 78(11), 2112-2119.
[http://dx.doi.org/10.1902/jop.2007.070186] [PMID: 17970677]
[13]
Aguilar, S.A.; Calvo, G.J.L.; González, J.M.; Moreu, G.; Delgado, R.R.A.; Gómez, M.G. Peri-implant evaluation of immediately loaded implants placed in esthetic zone in patients with diabetes mellitus type 2: A two-year study. Clin. Oral Implants Res., 2016, 27(2), 156-161.
[http://dx.doi.org/10.1111/clr.12552] [PMID: 25623884]
[14]
Gómez, M.G.; Aguilar, S.A.; Rubio, R.J.; Guardia, J.; Gargallo, J.; Calvo, G.J.L. Peri-implant evaluation in type 2 diabetes mellitus patients: A 3-year study. Clin. Oral Implants Res., 2015, 26(9), 1031-1035.
[http://dx.doi.org/10.1111/clr.12391] [PMID: 24684438]
[15]
Abduljabbar, T.; Al-sahaly, F.; Al-kathami, M.; Afzal, S.; Vohra, F. Comparison of periodontal and peri-implant inflammatory parameters among patients with prediabetes, type 2 diabetes mellitus and non-diabetic controls. Acta Odontol. Scand., 2017, 75(5), 319-324.
[http://dx.doi.org/10.1080/00016357.2017.1303848] [PMID: 28325134]
[16]
Beikler, T.; Flemmig, T.F. Implants in the medically compromised patient. Crit. Rev. Oral Biol. Med., 2003, 14(4), 305-316.
[http://dx.doi.org/10.1177/154411130301400407]
[17]
Moy, P.K.; Medina, D.; Shetty, V.; Aghaloo, T.L. Dental implant failure rates and associated risk factors. Int. J. Oral Maxillofac. Implants, 2005, 20(4), 569-577.
[PMID: 16161741]
[18]
Bornstein, M.M.; Cionca, N.; Mombelli, A. Systemic conditions and treatments as risks for implant therapy. Int. J. Oral Maxillofac. Implants, 2009, 24(Suppl.), 12-27.
[PMID: 19885432]
[19]
Anner, R.; Grossmann, Y.; Anner, Y.; Levin, L. Smoking, diabetes mellitus, periodontitis, and supportive periodontal treatment as factors associated with dental implant survival: A long-term retrospective evaluation of patients followed for up to 10 years. Implant Dent., 2010, 19(1), 57-64.
[http://dx.doi.org/10.1097/ID.0b013e3181bb8f6c] [PMID: 20147817]
[20]
Sanz, M.; Chapple, I.L. Clinical research on peri-implant diseases: Consensus report of Working Group 4. J. Clin. Periodontol., 2012, 39(Suppl. 12), 202-206.
[http://dx.doi.org/10.1111/j.1600-051X.2011.01837.x] [PMID: 22533957]
[21]
Shang, R.; Gao, L. Impact of hyperglycemia on the rate of implant failure and peri-implant parameters in patients with type 2 diabetes mellitus. J. Am. Dent. Assoc., 2021, 152(3), 189-201.e1.
[http://dx.doi.org/10.1016/j.adaj.2020.11.015] [PMID: 33632408]
[22]
Jiang, X.; Zhu, Y.; Liu, Z.; Tian, Z.; Zhu, S. Association between diabetes and dental implant complications: A systematic review and meta-analysis. Acta Odontol. Scand., 2021, 79(1), 9-18.
[http://dx.doi.org/10.1080/00016357.2020.1761031] [PMID: 32401121]
[23]
Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gøtzsche, P.C.; Ioannidis, J.P.A.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. BMJ, 2009, 339(jul21 1), b2700.
[http://dx.doi.org/10.1136/bmj.b2700] [PMID: 19622552]
[24]
Al-Shibani, N.; Al-Aali, K.A.; Al-Hamdan, R.S.; Alrabiah, M.; Basunbul, G.; Abduljabbar, T. Comparison of clinical peri-implant indices and crestal bone levels around narrow and regular diameter implants placed in diabetic and non-diabetic patients: A 3-year follow-up study. Clin. Implant Dent. Relat. Res., 2019, 21(2), 247-252.
[http://dx.doi.org/10.1111/cid.12712] [PMID: 30624014]
[25]
Mokeem, S.; Alfadda, S.A.; Al-Shibani, N.; Alrabiah, M.; Al-Hamdan, R.S.; Vohra, F.; Abduljabbar, T. Clinical and radiographic peri-implant variables around short dental implants in type 2 diabetic, prediabetic, and non-diabetic patients. Clin. Implant Dent. Relat. Res., 2019, 21(1), 60-65.
[http://dx.doi.org/10.1111/cid.12691] [PMID: 30411841]
[26]
Alasqah, M.N.; Alrabiah, M.; Al-Aali, K.A.; Mokeem, S.A.; Binmahfooz, A.M. ArRejaie, A.S.; Abduljabbar, T. Peri-implant soft tissue status and crestal bone levels around adjacent implants placed in patients with and without type-2 diabetes mellitus: 6 years follow-up results. Clin. Implant Dent. Relat. Res., 2018, 20(4), 562-568.
[http://dx.doi.org/10.1111/cid.12617] [PMID: 29787632]
[27]
Al Amri, M.D.; Abduljabbar, T.S.; Al-Johany, S.S.; Al Rifaiy, M.Q.; Alfarraj Aldosari, A.M.; Al-Kheraif, A.A. Comparison of clinical and radiographic parameters around short (6 to 8 mm in length) and long (11 mm in length) dental implants placed in patients with and without type 2 diabetes mellitus: 3-year follow-up results. Clin. Oral Implants Res., 2017, 28(10), 1182-1187.
[http://dx.doi.org/10.1111/clr.12938] [PMID: 27469294]
[28]
Bignozzi, I.; Ciobanu, G.; Quaranta, A.; Pompa, G. Dental implant sites in healthy versus diabetic subjects: A two-year clinical and bacteriological assessment. Eur. J. Inflamm., 2013, 11(3), 813-823.
[http://dx.doi.org/10.1177/1721727X1301100324]
[29]
Tatarakis, N.; Kinney, J.S.; Inglehart, M.; Braun, T.M.; Shelburne, C.; Lang, N.P.; Giannobile, W.V.; Oh, T.J. Clinical, microbiological, and salivary biomarker profiles of dental implant patients with type 2 diabetes. Clin. Oral Implants Res., 2014, 25(7), 803-812.
[http://dx.doi.org/10.1111/clr.12139] [PMID: 23445216]
[30]
Erdogan, Ö.; Uçar, Y. Tatlı, U.; Sert, M.; Benlidayı, M.E.; Evlice, B. A clinical prospective study on alveolar bone augmentation and dental implant success in patients with type 2 diabetes. Clin. Oral Implants Res., 2015, 26(11), 1267-1275.
[http://dx.doi.org/10.1111/clr.12450] [PMID: 25041273]
[31]
Cabrera, D.J.J.; Castellanos, C.L.; Torres, L.D.; Pérez, F.M.; Machuca, P.G. Clinical performance of titanium-zirconium implants with a hydrophilic surface in patients with controlled type 2 diabetes mellitus: 2-year results from a prospective case-control clinical study. Clin. Oral Investig., 2020, 24(7), 2477-2486.
[http://dx.doi.org/10.1007/s00784-019-03110-9] [PMID: 31701247]
[32]
Dioguardi, M.; Cantore, S.; Scacco, S.; Quarta, C.; Sovereto, D.; Spirito, F.; Alovisi, M.; Troiano, G.; Aiuto, R.; Garcovich, D.; Crincoli, V.; Laino, L.; Covelli, M.; Malcangi, A.; Lo Muzio, L.; Ballini, A.; Di Cosola, M. From bench to bedside in precision medicine: diabetes mellitus and peri-implantitis clinical indices with a short-term follow-up: A systematic review and meta-analysis. J. Pers. Med., 2022, 12(2), 235.
[http://dx.doi.org/10.3390/jpm12020235] [PMID: 35207724]
[33]
Eskow, C.C.; Oates, T.W. Dental implant survival and complication rate over 2 years for individuals with poorly controlled type 2 diabetes mellitus. Clin. Implant Dent. Relat. Res., 2017, 19(3), 423-431.
[http://dx.doi.org/10.1111/cid.12465] [PMID: 27990756]
[34]
Chiu, H.C.; Fu, M.M.J.; Yang, T.S.; Fu, E.; Chiang, C.Y.; Tu, H.P.; Chin, Y.T.; Lin, F.G.; Shih, K.C. Effect of high glucose, Porphyromonas gingivalis lipopolysaccharide and advanced glycation end-products on production of interleukin-6/-8 by gingival fibroblasts. J. Periodontal Res., 2017, 52(2), 268-276.
[http://dx.doi.org/10.1111/jre.12391] [PMID: 27397896]
[35]
Chang, P.C.; Chien, L.Y.; Yeo, J.F.; Wang, Y.P.; Chung, M.C.; Chong, L.Y.; Kuo, M.Y.P.; Chen, C.H.; Chiang, H.C.; Ng, B.N.; Lee, Q.Q.; Phay, Y.K.; Ng, J.R.; Erk, K.Y. Progression of periodontal destruction and the roles of advanced glycation end products in experimental diabetes. J. Periodontol., 2013, 84(3), 379-388.
[http://dx.doi.org/10.1902/jop.2012.120076] [PMID: 22554295]
[36]
Chang, P.C.; Chong, L.Y.; Tsai, S.C.; Lim, L.P. Aminoguanidine inhibits the AGE-RAGE axis to modulate the induction of periodontitis but has limited effects on the progression and recovery of experimental periodontitis: A preliminary study. J. Periodontol., 2014, 85(5), 729-739.
[http://dx.doi.org/10.1902/jop.2013.130238] [PMID: 23855839]
[37]
Quintero, D.G.; Winger, J.N.; Khashaba, R.; Borke, J.L. Advanced glycation endproducts and rat dental implant osseointegration. J. Oral Implantol., 2010, 36(2), 97-103.
[http://dx.doi.org/10.1563/AAID-JOI-D-09-00032] [PMID: 20426586]
[38]
Pan, C.; Liu, J.; Wang, H.; Song, J.; Tan, L.; Zhao, H. Porphyromonas gingivalis can invade periodontal ligament stem cells. BMC Microbiol., 2017, 17(1), 38.
[http://dx.doi.org/10.1186/s12866-017-0950-5] [PMID: 28212613]
[39]
De Waal, Y.C.; Eijsbouts, H.V.; Winkel, E.G.; van Winkelhoff, A.J. Microbial characteristics of peri-implantitis: A case-control study. J. Periodontol., 2017, 88(2), 209-217.
[http://dx.doi.org/10.1902/jop.2016.160231] [PMID: 27666672]
[40]
Alsahhaf, A.; Al-Aali, K.A.; Alshagroud, R.S.; Alshiddi, I.F.; Alrahlah, A.; Abduljabbar, T.; Javed, F.; Vohra, F. Comparison of yeast species in the subgingival oral biofilm of individuals with type 2 diabetes and peri-implantitis and individuals with peri-implantitis without diabetes. J. Periodontol., 2019, 90(12), 1383-1389.
[http://dx.doi.org/10.1002/JPER.19-0091] [PMID: 31318043]
[41]
Rocha, M.; Nava, L.E.; De La Torre, C.V.; Sánchez, M.F.; Garay, S.M.E.; Malacara, J.M. Clinical and radiological improvement of periodontal disease in patients with type 2 diabetes mellitus treated with alendronate: A randomized, placebo-controlled trial. J. Periodontol., 2001, 72(2), 204-209.
[http://dx.doi.org/10.1902/jop.2001.72.2.204] [PMID: 11288794]
[42]
Javed, F.; Romanos, G.E. Impact of diabetes mellitus and glycemic control on the osseointegration of dental implants: A systematic literature review. J. Periodontol., 2009, 80(11), 1719-1730.
[http://dx.doi.org/10.1902/jop.2009.090283] [PMID: 19905942]
[43]
Al Amri, M.D.; Kellesarian, S.V.; Al-Kheraif, A.A.; Malmstrom, H.; Javed, F.; Romanos, G.E. Effect of oral hygiene maintenance on HbA1c levels and peri-implant parameters around immediately-loaded dental implants placed in type-2 diabetic patients: 2 years follow-up. Clin. Oral Implants Res., 2016, 27(11), 1439-1443.
[http://dx.doi.org/10.1111/clr.12758] [PMID: 26756309]
[44]
Corbella, S.; Francetti, L.; Taschieri, S.; De Siena, F.; Fabbro, M.D. Effect of periodontal treatment on glycemic control of patients with diabetes: A systematic review and meta-analysis. J. Diabetes Investig., 2013, 4(5), 502-509.
[http://dx.doi.org/10.1111/jdi.12088] [PMID: 24843701]
[45]
Yadav, R.; Agrawal, K.K.; Rao, J.; Anwar, M.; Alvi, H.A.; Singh, K.; Himanshu, D. Crestal bone loss under delayed loading of full thickness versus flapless surgically placed dental implants in controlled type 2 diabetic patients: A parallel group randomized clinical trial. J. Prosthodont., 2018, 27, 611-617.
[http://dx.doi.org/10.1111/jopr.12549]
[46]
Al Amri, M.D.; Alfarraj Aldosari, A.M.; Al-Johany, S.S.; Al Baker, A.M.; Al Rifaiy, M.Q.; Al-Kheraif, A.A. Comparison of clinical and radiographic status around immediately loaded versus conventional loaded implants placed in patients with type 2 diabetes: 12 and 24-month follow-up results. J. Oral Rehabil., 2017, 44(3), 220-228.
[http://dx.doi.org/10.1111/joor.12466] [PMID: 27981620]
[47]
Becker, W.; Goldstein, M.; Becker, B.E.; Sennerby, L.; Kois, D.; Hujoel, P. Minimally invasive flapless implant placement: Follow-up results from a multicenter study. J. Periodontol., 2009, 80(2), 347-352.
[http://dx.doi.org/10.1902/jop.2009.080286] [PMID: 19186977]
[48]
Wadhwa, B.; Jain, V.; Bhutia, O.; Bhalla, A.S.; Pruthi, G. Flapless versus open flap techniques of implant placement: A 15-month follow-up study. Indian J. Dent. Res., 2015, 26, 372-377.
[http://dx.doi.org/10.4103/0970-9290.167629]
[49]
Agrawal, K.K.; Rao, J.; Anwar, M.; Singh, K.; Himanshu, D. Flapless vs flapped implant insertion in patients with controlled type 2 diabetes subjected to delayed loading: 1-year follow-up results from a randomised controlled trial. Eur. J. Oral Implantology, 2017, 10(4), 403-413.
[PMID: 29234747]
[50]
Singh, K.; Rao, J.; Afsheen, T.; Tiwari, B. Survival rate of dental implant placement by conventional or flapless surgery in controlled type 2 diabetes mellitus patients: A systematic review. Indian J. Dent. Res., 2019, 30, 600-611.
[http://dx.doi.org/10.4103/ijdr.IJDR_606_17]
[51]
Esposito, M.; Dojcinovic, I.; Germon, L.; Lévy, N.; Curno, R.; Buchini, S.; Péchy, P.; Aronsson, B.O. Safety and efficacy of a biomimetic monolayer of permanently bound multi-phosphonic acid molecules on dental implants: 1 year post-loading results from a pilot quadruple-blinded randomised controlled trial. Eur. J. Oral Implantology, 2013, 6(3), 227-236.
[PMID: 24179977]
[52]
Jokstad, A.; Alkumru, H. Immediate function on the day of surgery compared with a delayed implant loading process in the mandible: A randomized clinical trial over 5 years. Clin. Oral Implants Res., 2014, 25(12), 1325-1335.
[http://dx.doi.org/10.1111/clr.12279] [PMID: 24148020]