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Evaluation of Periodontopathogenic Bacteria Levels of Peri-Implants in Patients with Type 2 Diabetes Mellitus

Year 2022, Volume: 11 Issue: 3, 295 - 304, 19.09.2022
https://doi.org/10.54617/adoklinikbilimler.1125615

Abstract

Objective: The aim of this study was to evaluate the amount of periodontal pathogens (Porphyromonas gingivalis (Pg), Aggregatibacter actinomycetemcomitans (Aa), Campylobacter rectus (Cr), Treponema denticola (Td)) in saliva, peri-implant subgingival plaque samples and from natural teeth closest to the implants in the type 2 diabetes patients
Materials and Methods: Thirteen patients with well-controlled T2DM and seven systemically healthy patients were recruited for this study. A total of 39 dental implants; 27 implants in the diabetic group and 12 implants in the control group were placed. Subgingival plaque and saliva samples were collected from the implant and natural teeth at baseline and postoperatively at 1 month, 4 months, and 7 months. Real-time polymerase chain reaction (RT-PCR) was used in the microbiological analysis.
Results: The amount of Td was found to be higher in the teeth and implants of the diabetes group than in the control group at follow-up times and the baseline value in the saliva was also higher in the diabetes group than in the control group. The Pg amounts at baseline and 7 months and the Cr amounts at baseline, 4 months, and 7 months were higher in the teeth of the control group than in the diabetes group. Pg amounts at baseline and 4 months and Cr amounts at 1 month were higher in the diabetes group than in the control group. The peri-implant amounts of Cr in the diabetes group at 1 month were higher than in the control group and its amounts were higher at 7months in the control group than in the diabetes group. The amounts of Aa around both the implant and the teeth did not differ between diabetes and control groups during the follow-up periods.
Conclusions: According to the results of the study, although some periodontal pathogenic bacteria increased in both diabetes and control groups during the follow-up periods, no infection was detected around the implant in either group.

Project Number

03/2010-13

References

  • 1. Khandelwal N, Oates TW, Vargas A, Alexander PP, Schoolfield JD, Alex McMahan C. Conventional SLA and chemically modified SLA implants in patients with poorly controlled type 2 diabetes mellitus--a randomized controlled trial. Clin Oral Implants Res. 2013;24(1):13-19.
  • 2. Wagner J, Spille JH, Wiltfang J, Naujokat H. Systematic review on diabetes mellitus and dental implants: an update. Int J Implant Dent. 2022;8(1):1.
  • 3. Chrcanovic BR, Albrektsson T, Wennerberg A. Diabetes and oral implant failure: a systematic review. J Dent Res. 2014;93(9):859-867.
  • 4. Mauri-Obradors E, Merlos A, Estrugo-Devesa A, Jane-Salas E, Lopez-Lopez J, Vinas M. Benefits of non-surgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: A randomized controlled trial. J Clin Periodontol. 2018;45(3):345-353.
  • 5. Verhulst MJL, Loos BG, Gerdes VEA, Teeuw WJ. Evaluating All Potential Oral Complications of Diabetes Mellitus. Front Endocrinol (Lausanne). 2019;10:56.
  • 6. Colombo JS, Balani D, Sloan AJ, Crean SJ, Okazaki J, Waddington RJ. Delayed osteoblast differentiation and altered inflammatory response around implants placed in incisor sockets of type 2 diabetic rats. Clin Oral Implants Res. 2011;22(6):578-586.
  • 7. Correa MG, Pimentel SP, Ribeiro FV, Cirano FR, Casati MZ. Host response and peri-implantitis. Braz Oral Res. 2019;33(suppl 1):e066.
  • 8. Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant disease. J Clin Periodontol. 2011;38 Suppl 11:203-213.
  • 9. Preethanath RS, AlNahas NW, Bin Huraib SM, et al. Microbiome of dental implants and its clinical aspect. Microb Pathog. 2017;106:20-24.
  • 10. Heuer W, Kettenring A, Stumpp SN, et al. Metagenomic analysis of the peri-implant and periodontal microflora in patients with clinical signs of gingivitis or mucositis. Clin Oral Investig. 2012;16(3):843-850.
  • 11. Chambrone L, Palma LF. Current status of dental implants survival and peri-implant bone loss in patients with uncontrolled type-2 diabetes mellitus. Curr Opin Endocrinol Diabetes Obes. 2019;26(4):219-222.
  • 12. Neilands J, Wickstrom C, Kinnby B, et al. Bacterial profiles and proteolytic activity in peri-implantitis versus healthy sites. Anaerobe. 2015;35(Pt A):28-34.
  • 13. Shi B, Lux R, Klokkevold P, et al. The subgingival microbiome associated with periodontitis in type 2 diabetes mellitus. ISME J. 2020;14(2):519-530.
  • 14. Almeida-Santos A, Martins-Mendes D, Gaya-Vidal M, Perez-Pardal L, Beja-Pereira A. Characterization of the Oral Microbiome of Medicated Type-2 Diabetes Patients. Front Microbiol. 2021;12:610370.
  • 15. Dogan SB, Kurtis MB, Tuter G, Serdar M, Watanabe K, Karakis S. Evaluation of Clinical Parameters and Levels of Proinflammatory Cytokines in the Crevicular Fluid Around Dental Implants in Patients with Type 2 Diabetes Mellitus. Int J Oral Maxillofac Implants. 2015;30(5):1119-1127.
  • 16. Tenenbaum H, Bogen O, Severac F, Elkaim R, Davideau JL, Huck O. Long-term prospective cohort study on dental implants: clinical and microbiological parameters. Clin Oral Implants Res. 2017;28(1):86-94.
  • 17. Mattout C, Bourgeois D, Bouchard P. Type 2 diabetes and periodontal indicators: epidemiology in France 2002-2003. J Periodontal Res. 2006;41(4):253-258.
  • 18. Alshahrani A, Al Deeb M, Alresayes S, et al. Comparison of peri-implant soft tissue and crestal bone status of dental implants placed in prediabetic, type 2 diabetic, and non-diabetic individuals: a retrospective cohort study. Int J Implant Dent. 2020;6(1):56.
  • 19. 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.
  • 20. Monje A, Catena A, Borgnakke WS. Association between diabetes mellitus/hyperglycaemia and peri-implant diseases: Systematic review and meta-analysis. J Clin Periodontol. 2017;44(6):636-648.
  • 21. Al-Askar M, Ajlan S, Alomar N, Al-Daghri NM. Clinical and Radiographic Peri-Implant Parameters and Whole Salivary Interleukin-1beta and Interleukin-6 Levels among Type-2 Diabetic and Nondiabetic Patients with and without Peri-Implantitis. Med Princ Pract. 2018;27(2):133-138.
  • 22. Alberti A, Morandi P, Zotti B, et al. Influence of Diabetes on Implant Failure and Peri-Implant Diseases: A Retrospective Study. Dent J (Basel). 2020;8(3).
  • 23. Sghaireen MG, Alduraywish AA, Srivastava KC, et al. Comparative Evaluation of Dental Implant Failure among Healthy and Well-Controlled Diabetic Patients-A 3-Year Retrospective Study. Int J Environ Res Public Health. 2020;17(14).
  • 24. Buser D, Broggini N, Wieland M, et al. Enhanced bone apposition to a chemically modified SLA titanium surface. J Dent Res. 2004;83(7):529-533.
  • 25. Botero JE, Gonzalez AM, Mercado RA, Olave G, Contreras A. Subgingival microbiota in peri-implant mucosa lesions and adjacent teeth in partially edentulous patients. J Periodontol. 2005;76(9):1490-1495.
  • 26. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres M. Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res. 2008;19(10):975-982.
  • 27. Kumar PS, Mason MR, Brooker MR, O'Brien K. Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol. 2012;39(5):425-433.
  • 28. Yuan K, Chang CJ, Hsu PC, Sun HS, Tseng CC, Wang JR. Detection of putative periodontal pathogens in non-insulin-dependent diabetes mellitus and non-diabetes mellitus by polymerase chain reaction. J Periodontal Res. 2001;36(1):18-24.
  • 29. Li H, Wang Y, Zhang D, Chen T, Hu A, Han X. Glycemic fluctuation exacerbates inflammation and bone loss and alters microbiota profile around implants in diabetic mice with experimental peri-implantitis. Int J Implant Dent. 2021;7(1):79.
  • 30. Tatarakis N, Kinney JS, Inglehart M, et al. Clinical, microbiological, and salivary biomarker profiles of dental implant patients with type 2 diabetes. Clin Oral Implants Res. 2014;25(7):803-812.
  • 31. Faveri M, Mayer MP, Feres M, de Figueiredo LC, Dewhirst FE, Paster BJ. Microbiological diversity of generalized aggressive periodontitis by 16S rRNA clonal analysis. Oral Microbiol Immunol. 2008;23(2):112-118.

Tip 2 Diabetli Bireylerde İmplant Çevresi Periodontopatojenik Bakteri Seviyelerinin Değerlendirilmesi

Year 2022, Volume: 11 Issue: 3, 295 - 304, 19.09.2022
https://doi.org/10.54617/adoklinikbilimler.1125615

Abstract

Amaç: Bu çalışmanın amacı tip 2 diabetli bireylere uygulanmış olan dental implantlardan ve implantlara en yakın doğal dişlerden toplanmış olan subgingival plak örneklerinde ve tükürükteki Porphyromonas gingivalis (Pg), Aggregatibacter actinomycetemcomitans(Aa), Camploybacter rectus (Cr), Treponema denticola (Td) gibi periodontal patojen miktarlarını değerlendirmektir.
Gereç ve Yöntem: Çalışmaya 13 tip 2 diabet ve 7 sistemik sağlıklı birey olmak üzere toplamda 20 kişi dahil edildi. Toplam 39 diş implantı, 27 implant diabet grubuna, 12 implant kontrol grubundaki bireylere olmak üzere uygulandı. İmplant ve doğal dişlerden başlangıçta, operasyon sonrası 1. ay, 4. ay ve 7. ayda subginval plak ve tükürük örnekleri toplandı. Mikrobiyolojik analiz için real-time polimeraz zincir reaksiyonu kullanıldı (RT-PZR).
Bulgular: Td miktarı diabet grubunda hem doğal dişlerde hemde implant çevrelerinde tüm takip dönemlerinde ve tükürükteki başlangıç değeride kontrol grubuna göre yüksek bulundu. Pg miktarı ise başlangıç ve 7. ayda, Cr miktarı ise baslangıç, 4. ay ve 7. ayda kontrol grubundaki doğal dişlerde diabet grubuna göre istatistiksel olarak yüksek bulunurken, yine Pg miktarı 1. ay ve 4. ayda ve Cr miktarı ise 1. ayda diabet grubunda kontrol grubuna göre yüksek bulundu. Diabet grubunda implant çevresindeki Cr miktarı ise 1. ayda kontrol grubuna göre, 7. ayda ise kontrol grubunda diabetli gruba göre anlamlı derecede yüksek bulundu. Hem implant hemde doğal diş çevresindeki Aa miktarı ise takip dönemlerinde diabet ve kontrol grupları arasında farklılık göstermedi.
Sonuç: Çalışmanın sonuçlarına göre bazı periodontal patojen bakteriler takip dönemlerinde hem diabet hemde kontrol grubunda artış göstermiş olmakla birlikte, implant çevresinde her iki grupta da herhangi bir enfeksiyon tespit edilmedi

Supporting Institution

Gazi Üniversitesi Bilisel Araştırmalar Proje Birimi

Project Number

03/2010-13

Thanks

Bu çalışma Gazi Üniversitesi Bilimsel Araştırma Projeleri Birimi tarafından 03/2010-13 nolu proje kodu ile desteklenmiştir.

References

  • 1. Khandelwal N, Oates TW, Vargas A, Alexander PP, Schoolfield JD, Alex McMahan C. Conventional SLA and chemically modified SLA implants in patients with poorly controlled type 2 diabetes mellitus--a randomized controlled trial. Clin Oral Implants Res. 2013;24(1):13-19.
  • 2. Wagner J, Spille JH, Wiltfang J, Naujokat H. Systematic review on diabetes mellitus and dental implants: an update. Int J Implant Dent. 2022;8(1):1.
  • 3. Chrcanovic BR, Albrektsson T, Wennerberg A. Diabetes and oral implant failure: a systematic review. J Dent Res. 2014;93(9):859-867.
  • 4. Mauri-Obradors E, Merlos A, Estrugo-Devesa A, Jane-Salas E, Lopez-Lopez J, Vinas M. Benefits of non-surgical periodontal treatment in patients with type 2 diabetes mellitus and chronic periodontitis: A randomized controlled trial. J Clin Periodontol. 2018;45(3):345-353.
  • 5. Verhulst MJL, Loos BG, Gerdes VEA, Teeuw WJ. Evaluating All Potential Oral Complications of Diabetes Mellitus. Front Endocrinol (Lausanne). 2019;10:56.
  • 6. Colombo JS, Balani D, Sloan AJ, Crean SJ, Okazaki J, Waddington RJ. Delayed osteoblast differentiation and altered inflammatory response around implants placed in incisor sockets of type 2 diabetic rats. Clin Oral Implants Res. 2011;22(6):578-586.
  • 7. Correa MG, Pimentel SP, Ribeiro FV, Cirano FR, Casati MZ. Host response and peri-implantitis. Braz Oral Res. 2019;33(suppl 1):e066.
  • 8. Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant disease. J Clin Periodontol. 2011;38 Suppl 11:203-213.
  • 9. Preethanath RS, AlNahas NW, Bin Huraib SM, et al. Microbiome of dental implants and its clinical aspect. Microb Pathog. 2017;106:20-24.
  • 10. Heuer W, Kettenring A, Stumpp SN, et al. Metagenomic analysis of the peri-implant and periodontal microflora in patients with clinical signs of gingivitis or mucositis. Clin Oral Investig. 2012;16(3):843-850.
  • 11. Chambrone L, Palma LF. Current status of dental implants survival and peri-implant bone loss in patients with uncontrolled type-2 diabetes mellitus. Curr Opin Endocrinol Diabetes Obes. 2019;26(4):219-222.
  • 12. Neilands J, Wickstrom C, Kinnby B, et al. Bacterial profiles and proteolytic activity in peri-implantitis versus healthy sites. Anaerobe. 2015;35(Pt A):28-34.
  • 13. Shi B, Lux R, Klokkevold P, et al. The subgingival microbiome associated with periodontitis in type 2 diabetes mellitus. ISME J. 2020;14(2):519-530.
  • 14. Almeida-Santos A, Martins-Mendes D, Gaya-Vidal M, Perez-Pardal L, Beja-Pereira A. Characterization of the Oral Microbiome of Medicated Type-2 Diabetes Patients. Front Microbiol. 2021;12:610370.
  • 15. Dogan SB, Kurtis MB, Tuter G, Serdar M, Watanabe K, Karakis S. Evaluation of Clinical Parameters and Levels of Proinflammatory Cytokines in the Crevicular Fluid Around Dental Implants in Patients with Type 2 Diabetes Mellitus. Int J Oral Maxillofac Implants. 2015;30(5):1119-1127.
  • 16. Tenenbaum H, Bogen O, Severac F, Elkaim R, Davideau JL, Huck O. Long-term prospective cohort study on dental implants: clinical and microbiological parameters. Clin Oral Implants Res. 2017;28(1):86-94.
  • 17. Mattout C, Bourgeois D, Bouchard P. Type 2 diabetes and periodontal indicators: epidemiology in France 2002-2003. J Periodontal Res. 2006;41(4):253-258.
  • 18. Alshahrani A, Al Deeb M, Alresayes S, et al. Comparison of peri-implant soft tissue and crestal bone status of dental implants placed in prediabetic, type 2 diabetic, and non-diabetic individuals: a retrospective cohort study. Int J Implant Dent. 2020;6(1):56.
  • 19. 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.
  • 20. Monje A, Catena A, Borgnakke WS. Association between diabetes mellitus/hyperglycaemia and peri-implant diseases: Systematic review and meta-analysis. J Clin Periodontol. 2017;44(6):636-648.
  • 21. Al-Askar M, Ajlan S, Alomar N, Al-Daghri NM. Clinical and Radiographic Peri-Implant Parameters and Whole Salivary Interleukin-1beta and Interleukin-6 Levels among Type-2 Diabetic and Nondiabetic Patients with and without Peri-Implantitis. Med Princ Pract. 2018;27(2):133-138.
  • 22. Alberti A, Morandi P, Zotti B, et al. Influence of Diabetes on Implant Failure and Peri-Implant Diseases: A Retrospective Study. Dent J (Basel). 2020;8(3).
  • 23. Sghaireen MG, Alduraywish AA, Srivastava KC, et al. Comparative Evaluation of Dental Implant Failure among Healthy and Well-Controlled Diabetic Patients-A 3-Year Retrospective Study. Int J Environ Res Public Health. 2020;17(14).
  • 24. Buser D, Broggini N, Wieland M, et al. Enhanced bone apposition to a chemically modified SLA titanium surface. J Dent Res. 2004;83(7):529-533.
  • 25. Botero JE, Gonzalez AM, Mercado RA, Olave G, Contreras A. Subgingival microbiota in peri-implant mucosa lesions and adjacent teeth in partially edentulous patients. J Periodontol. 2005;76(9):1490-1495.
  • 26. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres M. Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res. 2008;19(10):975-982.
  • 27. Kumar PS, Mason MR, Brooker MR, O'Brien K. Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol. 2012;39(5):425-433.
  • 28. Yuan K, Chang CJ, Hsu PC, Sun HS, Tseng CC, Wang JR. Detection of putative periodontal pathogens in non-insulin-dependent diabetes mellitus and non-diabetes mellitus by polymerase chain reaction. J Periodontal Res. 2001;36(1):18-24.
  • 29. Li H, Wang Y, Zhang D, Chen T, Hu A, Han X. Glycemic fluctuation exacerbates inflammation and bone loss and alters microbiota profile around implants in diabetic mice with experimental peri-implantitis. Int J Implant Dent. 2021;7(1):79.
  • 30. Tatarakis N, Kinney JS, Inglehart M, et al. Clinical, microbiological, and salivary biomarker profiles of dental implant patients with type 2 diabetes. Clin Oral Implants Res. 2014;25(7):803-812.
  • 31. Faveri M, Mayer MP, Feres M, de Figueiredo LC, Dewhirst FE, Paster BJ. Microbiological diversity of generalized aggressive periodontitis by 16S rRNA clonal analysis. Oral Microbiol Immunol. 2008;23(2):112-118.
There are 31 citations in total.

Details

Primary Language Turkish
Subjects Dentistry
Journal Section Araştırma Makalesi
Authors

Şeyma Bozkurt Doğan 0000-0001-5670-6430

Mazlum Bülent Kurtiş 0000-0002-1124-3097

Gülçin Akca 0000-0002-8877-4144

Gülay Tüter 0000-0002-4264-0829

Project Number 03/2010-13
Publication Date September 19, 2022
Submission Date June 3, 2022
Published in Issue Year 2022 Volume: 11 Issue: 3

Cite

Vancouver Bozkurt Doğan Ş, Kurtiş MB, Akca G, Tüter G. Tip 2 Diabetli Bireylerde İmplant Çevresi Periodontopatojenik Bakteri Seviyelerinin Değerlendirilmesi. ADO Klinik Bilimler Dergisi. 2022;11(3):295-304.