Determinants of Peri-implant Disease: From Biofilm Aetiology to Modifiable Risk Factors and Anatomical Predisposition
DOI:
https://doi.org/10.24191/cos.v13i1.7262Keywords:
peri-implantitis, peri-implant mucositis, biofilm, dental implants, risk factors, microbiotaAbstract
Objectives: This review critically evaluates the multifactorial determinants of peri-implant diseases, hypothesising that microbial biofilms, systemic and behavioural factors, and anatomical distinctions collectively influence disease onset and progression.
Materials and Methods: A comprehensive analysis of current literature was conducted, focusing on microbiological studies, epidemiological reports, and clinical trials related to peri-implant mucositis and peri-implantitis. Special emphasis was placed on evaluating evidence related to bacterial plaque formation, systemic conditions (diabetes mellitus), behavioural habits (smoking, oral hygiene), anatomical differences between implants and natural teeth, and prosthetic complications.
Results: Bacterial plaque is established as the primary etiological factor in peri-implant mucositis and significantly contributes to peri-implantitis. Disease severity and progression are modulated by systemic conditions such as diabetes mellitus, behavioural factors including smoking and inadequate oral hygiene, and prosthetic factors like residual cement. Individuals with previous periodontitis exhibit heightened susceptibility due to persistent periodontal pathogen colonisation. Anatomical differences such as the lack of periodontal ligament, reduced vascularity, and weaker soft tissue integration also increase vulnerability to peri-implant disease. Microbial analysis highlights a diverse microbiota associated with peri-implant diseases, including opportunistic pathogens such as Staphylococcus epidermidis.
Conclusions: Peri-implant diseases are multifactorial, requiring tailored preventive strategies focused on meticulous plaque control, systemic and behavioural risk mitigation, and routine implant maintenance. Future research should prioritise improved diagnostic biomarkers, detailed biofilm characterisation, and innovative therapies targeting the unique biological challenges of peri-implant tissues.
Keywords: peri-implantitis, peri-implant mucositis, biofilm, dental implants, risk factors
References
Albouy, J. P., Abrahamsson, I., Persson, L. G., & Berglundh, T. (2008). Spontaneous progression of peri-implantitis at different types of implants. An experimental study in dogs. I: clinical and radiographic observations. Clinical oral implants research, 19(10), 997–1002. https://doi.org/10.1111/j.1600-0501.2008.01589.x
Almehmadi A. H. (2019). Awareness of population regarding the effects of diabetes on dental implant treatment in Jeddah, Saudi Arabia. Heliyon, 5(9), e02407. https://doi.org/10.1016/j.heliyon.2019.e02407
Alzahrani, A. S., & Abed, H. H. (2016). To what extent should dental implant placement be adopted as a standard for diabetic patients?. Saudi medical journal, 37(11), 1179–1183. https://doi.org/10.15537/smj.2016.11.15512
American Diabetes Association (2021). 2. Classification and Diagnosis of Diabetes: Standards of Medical Care in Diabetes-2021. Diabetes care, 44(Suppl 1), S15–S33. https://doi.org/10.2337/dc21-S002
Apatzidou D. A. (2022). The role of cigarette smoking in periodontal disease and treatment outcomes of dental implant therapy. Periodontology 2000, 90(1), 45–61. https://doi.org/10.1111/prd.12449
Baniulyte, G., & Ali, K. (2023). How does diabetes mellitus impact on the prognosis of dental implants?. Evidence-based dentistry, 24(3), 114–115. https://doi.org/10.1038/s41432-023-00909-0
Berglundh, T., Mombelli, A., Schwarz, F., & Derks, J. (2024). Etiology, pathogenesis and treatment of peri-implantitis: A European perspective. Periodontology 2000, 10.1111/prd.12549. Advance online publication. https://doi.org/10.1111/prd.12549
Berglundh, T., Armitage, G., Araujo, M. G., Avila-Ortiz, G., Blanco, J., Camargo, P. M., Chen, S., Cochran, D., Derks, J., Figuero, E., Hämmerle, C. H. F., Heitz-Mayfield, L. J. A., Huynh-Ba, G., Iacono, V., Koo, K. T., Lambert, F., McCauley, L., Quirynen, M., Renvert, S., Salvi, G. E., … Zitzmann, N. (2018). Peri-implant diseases and conditions: Consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. Journal of clinical periodontology, 45 Suppl 20, S286–S291. https://doi.org/10.1111/jcpe.12957
Berglundh, T., Lindhe, J., Jonsson, K., & Ericsson, I. (1994). The topography of the vascular systems in the periodontal and peri-implant tissues in the dog. Journal of clinical periodontology, 21(3), 189–193. https://doi.org/10.1111/j.1600-051x.1994.tb00302.x
Berglundh, T., Lindhe, J., Ericsson, I., Marinello, C. P., Liljenberg, B., & Thomsen, P. (1991). The soft tissue barrier at implants and teeth. Clinical oral implants research, 2(2), 81–90. https://doi.org/10.1034/j.1600-0501.1991.020206.x
Borgnakke, W. S., Genco, R. J., & Eke, P. I. (2017). Oral health and diabetes. In C. C. Cowie, C. C. Menke, L. J. Eberhardt, J. B. Gregg, & M. S. Narayan (Eds.), Diabetes in America (3rd ed., NIH Publication No. 17‑1468). National Institute of Diabetes and Digestive and Kidney Diseases
Buser, D., Weber, H. P., Donath, K., Fiorellini, J. P., Paquette, D. W., & Williams, R. C. (1992). Soft tissue reactions to non-submerged unloaded titanium implants in beagle dogs. Journal of periodontology, 63(3), 225–235. https://doi.org/10.1902/jop.1992.63.3.225
Carcuac, O., Abrahamsson, I., Derks, J., Petzold, M., & Berglundh, T. (2020). Spontaneous progression of experimental peri-implantitis in augmented and pristine bone: A pre-clinical in vivo study. Clinical oral implants research, 31(2), 192–200. https://doi.org/10.1111/clr.13564
Carvalho, É. B. S., Romandini, M., Sadilina, S., Sant'Ana, A. C. P., & Sanz, M. (2023). Microbiota associated with peri-implantitis-A systematic review with meta-analyses. Clinical oral implants research, 34(11), 1176–1187. https://doi.org/10.1111/clr.14153
Cho-Yan Lee, J., Mattheos, N., Nixon, K. C., & Ivanovski, S. (2012). Residual periodontal pockets are a risk indicator for peri-implantitis in patients treated for periodontitis. Clinical oral implants research, 23(3), 325–333. https://doi.org/10.1111/j.1600-0501.2011.02264.x
Chrcanovic, B. R., Albrektsson, T., & Wennerberg, A. (2014). Diabetes and oral implant failure: a systematic review. Journal of dental research, 93(9), 859–867. https://doi.org/10.1177/0022034514538820
Coli, P., Christiaens, V., Sennerby, L., & Bruyn, H. (2017). Reliability of periodontal diagnostic tools for monitoring peri-implant health and disease. Periodontology 2000, 73(1), 203–217. https://doi.org/10.1111/prd.12162
Darby I. (2022). Risk factors for periodontitis & peri-implantitis. Periodontology 2000, 90(1), 9–12. https://doi.org/10.1111/prd.12447
Derks, J., & Tomasi, C. (2015). Peri-implant health and disease. A systematic review of current epidemiology. Journal of clinical periodontology, 42 Suppl 16, S158–S171. https://doi.org/10.1111/jcpe.12334Derks, J., Schaller, D., Håkansson, J., Wennström, J. L., Tomasi, C., & Berglundh, T. (2016). Effectiveness of Implant Therapy Analyzed in a Swedish Population: Prevalence of Peri-implantitis. Journal of dental research, 95(1), 43–49. https://doi.org/10.1177/0022034515608832
, J., Schaller, D., Håkansson, J., Wennström, J. L., Tomasi, C., & Berglundh, T. (2016). Effectiveness of Implant Therapy Analyzed in a Swedish Population: Prevalence of Peri-implantitis. Journal of dental research, 95(1), 43–49. https://doi.org/10.1177/0022034515608832
Dowell, S., Oates, T. W., & Robinson, M. (2007). Implant success in people with type 2 diabetes mellitus with varying glycemic control: a pilot study. Journal of the American Dental Association (1939), 138(3), 355–398. https://doi.org/10.14219/jada.archive.2007.0168
Enteghad, S., Shirban, F., Nikbakht, M. H., Bagherniya, M., & Sahebkar, A. (2024). Relationship Between Diabetes Mellitus and Periodontal/Peri-Implant Disease: A Contemporaneous Review. International dental journal, 74(3), 426–445. https://doi.org/10.1016/j.identj.2024.03.010 Enteghad, S., Shirban, F., Nikbakht, M. H., Bagherniya, M., & Sahebkar, A. (2024). Relationship Between Diabetes Mellitus and Periodontal/Peri-Implant Disease: A Contemporaneous Review. International dental journal, 74(3), 426–445. https://doi.org/10.1016/j.identj.2024.03.010
Gruber, R., & Bosshardt, D. D. (2015). Dental implantology and implants—tissue interface. In A. Vishwakarma, P. Sharpe, S. Shi, & M. Ramalingam (Eds.), Stem cell biology and tissue engineering in dental sciences (pp. 735–747). Academic Press. https://doi.org/10.1016/B978-0-12-397157-9.00078-3
Hardt, C. R., Gröndahl, K., Lekholm, U., & Wennström, J. L. (2002). Outcome of implant therapy in relation to experienced loss of periodontal bone support: a retrospective 5- year study. Clinical oral implants research, 13(5), 488–494. https://doi.org/10.1034/j.1600-0501.2002.130507.x
Heitz-Mayfield, L. J. A., & Salvi, G. E. (2018). Peri-implant mucositis. Journal of clinical periodontology, 45 Suppl 20, S237–S245. https://doi.org/10.1111/jcpe.12953
Hill A. B. (1965). THE ENVIRONMENT AND DISEASE: ASSOCIATION OR CAUSATION?. Proceedings of the Royal Society of Medicine, 58(5), 295–300. https://doi.org/10.1177/003591576505800503
Karoussis, I. K., Müller, S., Salvi, G. E., Heitz-Mayfield, L. J., Brägger, U., & Lang, N. P. (2004). Association between periodontal and peri-implant conditions: a 10-year prospective study. Clinical oral implants research, 15(1), 1–7. https://doi.org/10.1111/j.1600-0501.2004.00982.x
Koldsland, O. C., Scheie, A. A., & Aass, A. M. (2010). Prevalence of peri-implantitis related to severity of the disease with different degrees of bone loss. Journal of periodontology, 81(2), 231–238. https://doi.org/10.1902/jop.2009.090269
Koldsland, O. C., Scheie, A. A., & Aass, A. M. (2011). The association between selected risk indicators and severity of peri-implantitis using mixed model analyses. Journal of clinical periodontology, 38(3), 285–292. https://doi.org/10.1111/j.1600-051X.2010.01659.x
Kröger, A., Hülsmann, C., Fickl, S., Spinell, T., Hüttig, F., Kaufmann, F., Heimbach, A., Hoffmann, P., Enkling, N., Renvert, S., Schwarz, F., Demmer, R. T., Papapanou, P. N., Jepsen, S., & Kebschull, M. (2018). The severity of human peri-implantitis lesions correlates with the level of submucosal microbial dysbiosis. Journal of clinical periodontology, 45(12), 1498–1509. https://doi.org/10.1111/jcpe.13023
Kröger, A., Hülsmann, C., Fickl, S., Spinell, T., Hüttig, F., Kaufmann, F., Heimbach, A., Hoffmann, P., Enkling, N., Renvert, S., Schwarz, F., Demmer, R. T., Papapanou, P. N., Jepsen, S., & Kebschull, M. (2018). The severity of human peri-implantitis lesions correlates with the level of submucosal microbial dysbiosis. Journal of clinical periodontology, 45(12), 1498–1509. https://doi.org/10.1111/jcpe.13023
Lang, N. P., Berglundh, T., & Working Group 4 of Seventh European Workshop on Periodontology (2011). Periimplant diseases: where are we now?--Consensus of the Seventh European Workshop on Periodontology. Journal of clinical periodontology, 38 Suppl 11, 178–181. https://doi.org/10.1111/j.1600-051X.2010.01674.x
Lee, C. T., Huang, Y. W., Zhu, L., & Weltman, R. (2017). Prevalences of peri-implantitis and peri-implant mucositis: systematic review and meta-analysis. Journal of dentistry, 62, 1–12. https://doi.org/10.1016/j.jdent.2017.04.011Linkevicius, T., Puisys, A., Vindasiute, E., Linkeviciene, L., & Apse, P. (2013). Does residual cement around implant-supported restorations cause peri-implant disease? A retrospective case analysis. Clinical oral implants research, 24(11), 1179–1184. https://doi.org/10.1111/j.1600-0501.2012.02570.x
Listgarten M. A. (1965). Electron Microscopic Observations on The Bacterial Flora of Acute Necrotizing Ulcerative Gingivitis. The Journal of periodontology, 36, 328–339. https://doi.org/10.1902/jop.1965.36.4.328
Loe, H., Theilade, E., & Jensen, S. B. (1965). EXPERIMENTAL GINGIVITIS IN MAN. The Journal of periodontology, 36, 177–187. https://doi.org/10.1902/jop.1965.36.3.177
Löe H. (1993). Periodontal disease. The sixth complication of diabetes mellitus. Diabetes care, 16(1), 329–334.
Martinez-Amargant, J., de Tapia, B., Pascual, A., Takamoli, J., Esquinas, C., Nart, J., & Valles, C. (2023). Association between smoking and peri-implant diseases: A retrospective study. Clinical oral implants research, 34(10), 1127–1140. https://doi.org/10.1111/clr.14147
Meyer, S., Giannopoulou, C., Courvoisier, D., Schimmel, M., Müller, F., & Mombelli, A. (2017). Experimental mucositis and experimental gingivitis in persons aged 70 or over. Clinical and biological responses. Clinical oral implants research, 28(8), 1005–1012. https://doi.org/10.1111/clr.12912
Mombelli, A., & Décaillet, F. (2011). The characteristics of biofilms in peri-implant disease. Journal of clinical periodontology, 38 Suppl 11, 203–213. https://doi.org/10.1111/j.1600-051X.2010.01666.x
Mombelli, A., Casagni, F., & Madianos, P. N. (2002). Can presence or absence of periodontal pathogens distinguish between subjects with chronic and aggressive periodontitis? A systematic review. Journal of clinical periodontology, 29 Suppl 3, 10–38. https://doi.org/10.1034/j.1600-051x.29.s3.1.x
Mombelli, A., van Oosten, M. A., Schurch, E., Jr, & Land, N. P. (1987). The microbiota associated with successful or failing osseointegrated titanium implants. Oral microbiology and immunology, 2(4), 145–151. https://doi.org/10.1111/j.1399-302x.1987.tb00298.x
Oates, T. W., Jr, Galloway, P., Alexander, P., Vargas Green, A., Huynh-Ba, G., Feine, J., & McMahan, C. A. (2014). The effects of elevated hemoglobin A(1c) in patients with type 2 diabetes mellitus on dental implants: Survival and stability at one year. Journal of the American Dental Association (1939), 145(12), 1218–1226. https://doi.org/10.14219/jada.2014.93
Ong, C. T., Ivanovski, S., Needleman, I. G., Retzepi, M., Moles, D. R., Tonetti, M. S., & Donos, N. (2008). Systematic review of implant outcomes in treated periodontitis subjects. Journal of clinical periodontology, 35(5), 438–462. https://doi.org/10.1111/j.1600-051X.2008.01207.x
Petersmann, A., Müller-Wieland, D., Müller, U. A., Landgraf, R., Nauck, M., Freckmann, G., Heinemann, L., & Schleicher, E. (2019). Definition, classification and diagnosis of diabetes mellitus [Clinical practice guidelines]. Experimental and Clinical Endocrinology & Diabetes, 127(Suppl. 1), S1–S7. https://doi.org/10.1055/a-1018-9078
Pjetursson, B. E., Helbling, C., Weber, H. P., Matuliene, G., Salvi, G. E., Brägger, U., Schmidlin, K., Zwahlen, M., & Lang, N. P. (2012). Peri-implantitis susceptibility as it relates to periodontal therapy and supportive care. Clinical oral implants research, 23(7), 888–894. https://doi.org/10.1111/j.1600-0501.2012.02474.x
Pontoriero, R., Tonelli, M. P., Carnevale, G., Mombelli, A., Nyman, S. R., & Lang, N. P. (1994). Experimentally induced peri-implant mucositis. A clinical study in humans. Clinical oral implants research, 5(4), 254–259. https://doi.org/10.1034/j.1600-0501.1994.050409.x
Quirynen, M., & Van Assche, N. (2011). Microbial changes after full-mouth tooth extraction, followed by 2-stage implant placement. Journal of clinical periodontology, 38(6), 581–589. https://doi.org/10.1111/j.1600-051X.2011.01728.x
Roccuzzo, M., De Angelis, N., Bonino, L., & Aglietta, M. (2010). Ten-year results of a three-arm prospective cohort study on implants in periodontally compromised patients. Part 1: implant loss and radiographic bone loss. Clinical oral implants research, 21(5), 490–496. https://doi.org/10.1111/j.1600-0501.2009.01886.x
Roccuzzo, M., Pittoni, D., Roccuzzo, A., Charrier, L., & Dalmasso, P. (2017). Surgical treatment of peri-implantitis intrabony lesions by means of deproteinized bovine bone mineral with 10% collagen: 7-year-results. Clinical oral implants research, 28(12), 1577–1583. https://doi.org/10.1111/clr.13028
Ronin, D., Boyer, J., Alban, N., Natoli, R. M., Johnson, A., & Kjellerup, B. V. (2022). Current and novel diagnostics for orthopedic implant biofilm infections: a review. APMIS : acta pathologica, microbiologica, et immunologica Scandinavica, 130(2), 59–81. https://doi.org/10.1111/apm.13197
Roos-Jansåker, A. M., Lindahl, C., Renvert, H., & Renvert, S. (2006). Nine- to fourteen-year follow-up of implant treatment. Part I: implant loss and associations to various factors. Journal of clinical periodontology, 33(4), 283–289. https://doi.org/10.1111/j.1600-051X.2006.00907.x
Rothman, K. J., & Greenland, S. (2005). Causation and causal inference in epidemiology. American journal of public health, 95 Suppl 1, S144–S150. https://doi.org/10.2105/AJPH.2004.059204
Salvi, G. E., Aglietta, M., Eick, S., Sculean, A., Lang, N. P., & Ramseier, C. A. (2012). Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clinical oral implants research, 23(2), 182–190. https://doi.org/10.1111/j.1600-0501.2011.02220.x
Schnitman, P. A., & Han, R. K. (2015). Completely Digital Two-Visit Immediately Loaded Implants: Proof of Concept. The Journal of oral implantology, 41(4), 429–436. https://doi.org/10.1563/aaid-joi-D-15-00060Schwarz, F., Becker, K., & Renvert, S. (2015). Efficacy of air polishing for the non-surgical treatment of peri-implant diseases: a systematic review. Journal of clinical periodontology, 42(10), 951–959. https://doi.org/10.1111/jcpe.12454
Schwarz, F., Derks, J., Monje, A., & Wang, H. L. (2018). Peri-implantitis. Journal of clinical periodontology, 45 Suppl 20, S246–S266. https://doi.org/10.1111/jcpe.12954
Serino, G., & Ström, C. (2009). Peri-implantitis in partially edentulous patients: association with inadequate plaque control. Clinical oral implants research, 20(2), 169–174. https://doi.org/10.1111/j.1600-0501.2008.01627.x
Sgolastra, F., Petrucci, A., Severino, M., Gatto, R., & Monaco, A. (2015). Periodontitis, implant loss and peri-implantitis. A meta-analysis. Clinical oral implants research, 26(4), e8–e16. https://doi.org/10.1111/clr.12319
Taylor G. W. (2001). Bidirectional interrelationships between diabetes and periodontal diseases: an epidemiologic perspective. Annals of periodontology, 6(1), 99–112. https://doi.org/10.1902/annals.2001.6.1.99
Turkyilmaz I. (2010). One-year clinical outcome of dental implants placed in patients with type 2 diabetes mellitus: a case series. Implant dentistry, 19(4), 323–329. https://doi.org/10.1097/ID.0b013e3181e40366
Vámos, O., Komora, P., Gede, N., Hegyi, P., Kelemen, K., Varga, G., Mikulás, K., Kerémi, B., & Kispélyi, B. (2024). The effect of nicotine-containing products on peri-implant tissues: A systematic review and network meta-analysis. Nicotine & Tobacco Research, 26(10), 1276–1285. https://doi.org/10.1093/ntr/ntae085
Valente NA, Andreana S. Peri-implant disease: what we know and what we need to know. J Periodontal Implant Sci. 2016 Jun;46(3):136-51. doi: 10.5051/jpis.2016.46.3.136. Epub 2016 Jun 29. PMID: 27382503; PMCID: PMC4928203.
Verhulst, M. J. L., Loos, B. G., Gerdes, V. E. A., & Teeuw, W. J. (2019). Evaluating All Potential Oral Complications of Diabetes Mellitus. Frontiers in endocrinology, 10, 56. https://doi.org/10.3389/fendo.2019.00056
Wang, H. L., Garaicoa-Pazmino, C., Collins, A., Ong, H. S., Chudri, R., & Giannobile, W. V. (2016). Protein biomarkers and microbial profiles in peri-implantitis. Clinical oral implants research, 27(9), 1129–1136. https://doi.org/10.1111/clr.12708 Zitzmann, N. U., Berglundh, T., Ericsson, I., & Lindhe, J. (2004). Spontaneous progression of experimentally induced periimplantitis. Journal of clinical periodontology, 31(10), 845–849. https://doi.org/10.1111/j.1600-051X.2004.00567.x
Zitzmann, N. U., Berglundh, T., Ericsson, I., & Lindhe, J. (2004). Spontaneous progression of experimentally induced periimplantitis. Journal of clinical periodontology, 31(10), 845–849. https://doi.org/10.1111/j.1600-051X.2004.00567.x
Downloads
Published
Issue
Section
License
Copyright (c) 2026 Compendium of Oral Science
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Materials contained in the journal may be reproduced for educational purposes provided that both the author(s) and the journal are appropriately recognised; otherwise duplication is not permitted. No articles, reports, or portions there of may be translated into other languages, published in books, journals, magazines, or any other print form without written permission from the authors and from the journal.
Disclaimer: The statements, opinions and data expressed in the articles and reports herein are those of the author(s) and not of the publisher and the editor(s). The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any schemes, methods, instructions or ideas referred to in the content.
