Influence of keratinized mucosa on the surgical therapeutical outcomes of peri-implantitis
Andrea Ravidà
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Search for more papers by this authorIslam Saleh
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Search for more papers by this authorRafael Siqueira
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Search for more papers by this authorCarlos Garaicoa-Pazmiño
Department of Periodontology, School of Dentistry, Oregon Health & Science University, Portland, OR, USA
Search for more papers by this authorMuhammad H. A. Saleh
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Department of Periodontics, University of Louisville School of Dentistry, Louisville, KY, USA
Search for more papers by this authorAlberto Monje
Department Periodontology, Universitat Internacional de Catalunya, Barcelona, Spain
Search for more papers by this authorCorresponding Author
Hom-Lay Wang
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Correspondence
Hom-Lay Wang, Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, 1011 North University Avenue, Ann Arbor, MI, USA.
Email: [email protected]
Search for more papers by this authorAndrea Ravidà
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Search for more papers by this authorIslam Saleh
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Search for more papers by this authorRafael Siqueira
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Search for more papers by this authorCarlos Garaicoa-Pazmiño
Department of Periodontology, School of Dentistry, Oregon Health & Science University, Portland, OR, USA
Search for more papers by this authorMuhammad H. A. Saleh
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Department of Periodontics, University of Louisville School of Dentistry, Louisville, KY, USA
Search for more papers by this authorAlberto Monje
Department Periodontology, Universitat Internacional de Catalunya, Barcelona, Spain
Search for more papers by this authorCorresponding Author
Hom-Lay Wang
Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, Ann Arbor, MI, USA
Correspondence
Hom-Lay Wang, Department of Periodontics and Oral Medicine, University of Michigan School of Dentistry, 1011 North University Avenue, Ann Arbor, MI, USA.
Email: [email protected]
Search for more papers by this authorFunding information
This paper was partially supported by the University of Michigan Periodontal Graduate Student Research Fund.
Abstract
Aim
To assess the impact of keratinized mucosa (KM) width around dental implants on surgical therapeutic outcomes when treating peri-implantitis.
Material and Methods
Surgically treated peri-implantitis implants were divided into two groups (KM width < 2 mm and ≥2 mm). Retrospective data were obtained after implant placement (T0) and the day of peri-implantitis surgical treatment (T1). Patients were later recruited (≥1 year after T1) for clinical and radiographic examination (T2). Outcomes were analysed using generalized estimating equation (GEE) models.
Results
A total of 40 patients (68 implants) (average follow-up: 52.4 ± 30.5 months) were included in this study. From T0 to T1, no differences were found between KM groups in terms of peri-implant probing depths (PPD) and bleeding on probing (BOP). However, sites with <2 mm KM exhibited significantly higher suppuration (SUP) and lower marginal bone level (MBL) (p > .01). Between T1 and T2, no major differences were noted on PPD reduction, BOP and MBL changes between the two groups. GEE modelling demonstrated that MBL severity prior to surgical therapy was a better predictor for implant survival than KM width.
Conclusion
Surgical outcome in treating peri-implantitis was influenced by the severity of bone loss present at the time of treatment and not by the presence of KM at the time of treatment.
CONFLICT OF INTEREST
The authors do not have any financial interests, either directly or indirectly, in the products or information listed in the paper.
Supporting Information
| Filename | Description |
|---|---|
| jcpe13250-sup-0001-FigS1.tiffTIFF image, 6.4 MB | |
| jcpe13250-sup-0002-TableS1.docxWord document, 16.2 KB | |
| jcpe13250-sup-0003-TableS2.docxWord document, 21.4 KB |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Aljateeli, M., Fu, J. H., & Wang, H. L. (2012). Managing peri-implant bone loss: Current understanding. Clinical Implant Dentistry and Related Research, 14(Suppl 1), e109–e118. https://doi.org/10.1111/j.1708-8208.2011.00387.x
- Bengazi, F., Wennstrom, J. L., & Lekholm, U. (1996). Recession of the soft tissue margin at oral implants. A 2-year longitudinal prospective study. Clinical Oral Implants Research, 7, 303–310. https://doi.org/10.1034/j.1600-0501.1996.070401.x
- Berglundh, T., Armitage, G., Araujo, M. G., Avila-Ortiz, G., Blanco, J., Camargo, P. M., … 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., Wennstrom, J. L., & Lindhe, J. (2018). Long-term outcome of surgical treatment of peri-implantitis. A 2–11-year retrospective study. Clinical Oral Implants Research, 29, 404–410. https://doi.org/10.1111/clr.13138
- Bouri, A. Jr, Bissada, N., Al-Zahrani, M. S., Faddoul, F., & Nouneh, I. (2008). Width of keratinized gingiva and the health status of the supporting tissues around dental implants. International Journal of Oral and Maxillofacial Implants, 23, 323–326.
- Cha, J. K., Lee, J. S., & Kim, C. S. (2019). Surgical therapy of peri-implantitis with local minocycline: A 6-month randomized controlled clinical trial. Journal of Dental Research, 98, 288–295. https://doi.org/10.1177/0022034518818479
- Charalampakis, G., Rabe, P., Leonhardt, A., & Dahlen, G. (2011). A follow-up study of peri-implantitis cases after treatment. Journal of Clinical Periodontology, 38, 864–871. https://doi.org/10.1111/j.1600-051X.2011.01759.x
- Chung, D. M., Oh, T. J., Shotwell, J. L., Misch, C. E., & Wang, H. L. (2006). Significance of keratinized mucosa in maintenance of dental implants with different surfaces. Journal of Periodontology, 77, 1410–1420. https://doi.org/10.1902/jop.2006.050393
- Cionca, N., Hashim, D., Cancela, J., Giannopoulou, C., & Mombelli, A. (2016). Pro-inflammatory cytokines at zirconia implants and teeth. A cross-sectional assessment. Clinical Oral Investigations, 20, 2285–2291. https://doi.org/10.1007/s00784-016-1729-z
- Crespi, R., Cappare, P., & Gherlone, E. (2010). A 4-year evaluation of the peri-implant parameters of immediately loaded implants placed in fresh extraction sockets. Journal of Periodontology, 81, 1629–1634. https://doi.org/10.1902/jop.2010.100115
- de Tapia, B., Valles, C., Ribeiro-Amaral, T., Mor, C., Herrera, D., Sanz, M., & Nart, J. (2019). The adjunctive effect of a titanium brush in implant surface decontamination at peri-implantitis surgical regenerative interventions: A randomized controlled clinical trial. Journal of Clinical Periodontology, 46, 586–596. https://doi.org/10.1111/jcpe.13095
- Derks, J., Schaller, D., Hakansson, J., Wennstrom, J. L., Tomasi, C., & Berglundh, T. (2016). Peri-implantitis - Onset and pattern of progression. Journal of Clinical Periodontology, 43, 383–388. https://doi.org/10.1111/jcpe.12535
- 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.12334
- Esposito, M., Grusovin, M. G., & Worthington, H. V. (2012). Interventions for replacing missing teeth: Treatment of peri-implantitis. Cochrane Database Systematic Review, 1, CD004970. https://doi.org/10.1002/14651858.CD004970.pub5
- Faggion, C. M. Jr, Listl, S., Fruhauf, N., Chang, H. J., & Tu, Y. K. (2014). A systematic review and Bayesian network meta-analysis of randomized clinical trials on non-surgical treatments for peri-implantitis. Journal of Clinical Periodontology, 41, 1015–1025. https://doi.org/10.1111/jcpe.12292
- French, D., Cochran, D. L., & Ofec, R. (2016). Retrospective Cohort Study of 4,591 Straumann implants placed in 2,060 patients in private practice with up to 10-year follow-up: The relationship between crestal bone level and soft tissue condition. International Journal of Oral and Maxillofacial Implants, 31, e168–e178. https://doi.org/10.11607/jomi.4932
- Frisch, E., Ziebolz, D., Vach, K., & Ratka-Kruger, P. (2015). The effect of keratinized mucosa width on peri-implant outcome under supportive postimplant therapy. Clinical Implant Dentistry and Related Research, 17(Suppl 1), e236–244. https://doi.org/10.1111/cid.12187
- Froum, S. J., & Rosen, P. S. (2012). A proposed classification for peri-implantitis. International Journal of Periodontics & Restorative Dentistry, 32, 533–540.
- Gobbato, L., Avila-Ortiz, G., Sohrabi, K., Wang, C. W., & Karimbux, N. (2013). The effect of keratinized mucosa width on peri-implant health: A systematic review. International Journal of Oral and Maxillofacial Implants, 28, 1536–1545. https://doi.org/10.11607/jomi.3244
- Hammerle, C. H. F., & Tarnow, D. (2018). The etiology of hard- and soft-tissue deficiencies at dental implants: A narrative review. Journal of Clinical Periodontology, 45(Suppl 20), S267–S277. https://doi.org/10.1111/jcpe.12955
- Hashim, D., Cionca, N., Combescure, C., & Mombelli, A. (2018). The diagnosis of peri-implantitis: A systematic review on the predictive value of bleeding on probing. Clinical Oral Implants Research, 29(Suppl 16), 276–293. https://doi.org/10.1111/clr.13127
- Heitz-Mayfield, L. J., & Mombelli, A. (2014). The therapy of peri-implantitis: A systematic review. International Journal of Oral and Maxillofacial Implants, 29(Suppl), 325–345. https://doi.org/10.11607/jomi.2014suppl.g5.3
- Heitz-Mayfield, L. J. A., Salvi, G. E., Mombelli, A., Loup, P. J., Heitz, F., Kruger, E., & Lang, N. P. (2018). Supportive peri-implant therapy following anti-infective surgical peri-implantitis treatment: 5-year survival and success. Clinical Oral Implants Research, 29, 1–6. https://doi.org/10.1111/clr.12910
- Howe, M. S., Keys, W., & Richards, D. (2019). Long-term (10-year) dental implant survival: A systematic review and sensitivity meta-analysis. Journal of Dentistry, 84, 9–21. https://doi.org/10.1016/j.jdent.2019.03.008
- Isler, S. C., Soysal, F., Ceyhanli, T., Bakirarar, B., & Unsal, B. (2018). Regenerative surgical treatment of peri-implantitis using either a collagen membrane or concentrated growth factor: A 12-month randomized clinical trial. Clinical Implant Dentistry and Related Research, 20, 703–712. https://doi.org/10.1111/cid.12661
- Karlsson, K., Derks, J., Hakansson, J., Wennstrom, J. L., Petzold, M., & Berglundh, T. (2019). Interventions for peri-implantitis and their effects on further bone loss: A retrospective analysis of a registry-based cohort. Journal of Clinical Periodontology, 46(8), 872–879. https://doi.org/10.1111/jcpe.13129
- Kim, B. S., Kim, Y. K., Yun, P. Y., Yi, Y. J., Lee, H. J., Kim, S. G., & Son, J. S. (2009). Evaluation of peri-implant tissue response according to the presence of keratinized mucosa. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology and Endodontics, 107, e24–28. https://doi.org/10.1016/j.tripleo.2008.12.010
- Koldsland, O. C., Wohlfahrt, J. C., & Aass, A. M. (2018). Surgical treatment of peri-implantitis: Prognostic indicators of short-term results. Journal of Clinical Periodontology, 45, 100–113. https://doi.org/10.1111/jcpe.12816
- Lim, H. C., Wiedemeier, D. B., Hammerle, C. H. F., & Thoma, D. S. (2019). The amount of keratinized mucosa may not influence peri-implant health in compliant patients: A retrospective 5-year analysis. Journal of Clinical Periodontology, 46, 354–362. https://doi.org/10.1111/jcpe.13078
- Lin, G. H., Chan, H. L., & Wang, H. L. (2013). The significance of keratinized mucosa on implant health: A systematic review. Journal of Periodontology, 84, 1755–1767. https://doi.org/10.1902/jop.2013.120688
- Lindhe, J., Meyle, J. & Group, D. o. E. W. o. P (2008). Peri-implant diseases: Consensus Report of the Sixth European Workshop on Periodontology. Journal of Clinical Periodontology, 35, 282–285. https://doi.org/10.1111/j.1600-051X.2008.01283.x
- Listgarten, M. A., Lang, N. P., Schroeder, H. E., & Schroeder, A. (1991). Periodontal tissues and their counterparts around endosseous implants. Clinical Oral Implants Research, 2(3), 1–19. https://doi.org/10.1034/j.1600-0501.1991.020309.x
- Mombelli, A., Muller, N., & Cionca, N. (2012). The epidemiology of peri-implantitis. Clinical Oral Implants Research, 23(Suppl 6), 67–76. https://doi.org/10.1111/j.1600-0501.2012.02541.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, 145–151. https://doi.org/10.1111/j.1399-302X.1987.tb00298.x
- Monje, A., & Blasi, G. (2019). Significance of keratinized mucosa/gingiva on peri-implant and adjacent periodontal conditions in erratic maintenance compliers. Journal of Periodontology, 90, 445–453. https://doi.org/10.1002/JPER.18-0471
- Monje, A., Caballe-Serrano, J., Nart, J., Penarrocha, D., Wang, H. L., & Rakic, M. (2018a). Diagnostic accuracy of clinical parameters to monitor peri-implant conditions: A matched case-control study. Journal of Periodontology, 89, 407–417. https://doi.org/10.1002/JPER.17-0454
- Monje, A., Insua, A., Rakic, M., Nart, J., Moyano-Cuevas, J. L., & Wang, H. L. (2018b). Estimation of the diagnostic accuracy of clinical parameters for monitoring peri-implantitis progression: An experimental canine study. Journal of Periodontology, 89, 1442–1451. https://doi.org/10.1002/JPER.18-0081
- Monje, A., Wang, H. L., & Nart, J. (2017). Association of preventive maintenance therapy compliance and peri-implant diseases: A cross-sectional study. Journal of Periodontology, 88, 1030–1041. https://doi.org/10.1902/jop.2017.170135
- Perussolo, J., Souza, A. B., Matarazzo, F., Oliveira, R. P., & Araujo, M. G. (2018). Influence of the keratinized mucosa on the stability of peri-implant tissues and brushing discomfort: A 4-year follow-up study. Clinical Oral Implants Research, 29, 1177–1185. https://doi.org/10.1111/clr.13381
- Pjetursson, B. E., Thoma, D., Jung, R., Zwahlen, M., & Zembic, A. (2012). A systematic review of the survival and complication rates of implant-supported fixed dental prostheses (FDPs) after a mean observation period of at least 5 years. Clinical Oral Implants Research, 23(Suppl 6), 22–38. https://doi.org/10.1111/j.1600-0501.2012.02546.x
- Renvert, S., Persson, G. R., Pirih, F. Q., & Camargo, P. M. (2018). Peri-implant health, peri-implant mucositis, and peri-implantitis: Case definitions and diagnostic considerations. Journal of Clinical Periodontology, 45(Suppl 20), S278–S285. https://doi.org/10.1111/jcpe.12956
- Renvert, S., Roos-Jansaker, A. M., & Persson, G. R. (2018). Surgical treatment of peri-implantitis lesions with or without the use of a bone substitute-a randomized clinical trial. Journal of Clinical Periodontology, 45, 1266–1274. https://doi.org/10.1111/jcpe.12986
- Romanos, G., Grizas, E., & Nentwig, G. H. (2015). Association of keratinized mucosa and periimplant soft tissue stability around implants with platform switching. Implant Dentistry, 24, 422–426. https://doi.org/10.1097/ID.0000000000000274
- Roos-Jansaker, A. M., Lindahl, C., Renvert, H., & Renvert, S. (2006). Nine- to fourteen-year follow-up of implant treatment. Part II: Presence of peri-implant lesions. Journal of Clinical Periodontology, 33, 290–295. https://doi.org/10.1111/j.1600-051X.2006.00906.x
- Roos-Jansaker, A. M., Persson, G. R., Lindahl, C., & Renvert, S. (2014). Surgical treatment of peri-implantitis using a bone substitute with or without a resorbable membrane: A 5-year follow-up. Journal of Clinical Periodontology, 41, 1108–1114. https://doi.org/10.1111/jcpe.12308
- Sahrmann, P., Attin, T., & Schmidlin, P. R. (2011). Regenerative treatment of peri-implantitis using bone substitutes and membrane: A systematic review. Clinical Implant Dentistry and Related Research, 13, 46–57. https://doi.org/10.1111/j.1708-8208.2009.00183.x
- Schwarz, F., Becker, J., Civale, S., Sahin, D., Iglhaut, T., & Iglhaut, G. (2018a). Influence of the width of keratinized tissue on the development and resolution of experimental peri-implant mucositis lesions in humans. Clinical Oral Implants Research, 29, 576–582. https://doi.org/10.1111/clr.13155
- Schwarz, F., Becker, J., Civale, S., Sahin, D., Iglhaut, T., & Iglhaut, G. (2018b). Influence of the width of keratinized tissue on the development and resolution of experimental peri-implant mucositis lesions in humans. Clinical Oral Implants Research, 29(6), 576–582. https://doi.org/10.1111/clr.13155
- 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
- Schwarz, F., Sahm, N., Schwarz, K., & Becker, J. (2010). Impact of defect configuration on the clinical outcome following surgical regenerative therapy of peri-implantitis. Journal of Clinical Periodontology, 37, 449–455. https://doi.org/10.1111/j.1600-051X.2010.01540.x
- Serino, G., Turri, A., & Lang, N. P. (2015). Maintenance therapy in patients following the surgical treatment of peri-implantitis: A 5-year follow-up study. Clinical Oral Implants Research, 26, 950–956. https://doi.org/10.1111/clr.12418
- Silness, J., & Loe, H. (1964). Periodontal disease in Pregnancy II. Correlation between oral hygiene and periodontal condtion. Acta Odontologica Scandinavica, 22, 121–135.
- Sinjab, K., Garaicoa-Pazmino, C., & Wang, H. L. (2018). Decision making for management of periimplant diseases. Implant Dentistry, 27, 276–281. https://doi.org/10.1097/ID.0000000000000775
- Tonetti, M. S., Greenwell, H., & Kornman, K. S. (2018). Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. Journal of Periodontology, 89(Suppl 1), S159–S172. https://doi.org/10.1002/JPER.18-0006
- Ueno, D., Nagano, T., Watanabe, T., Shirakawa, S., Yashima, A., & Gomi, K. (2016). Effect of the keratinized mucosa width on the health status of periimplant and contralateral periodontal tissues: A cross-sectional study. Implant Dentistry, 25, 796–801. https://doi.org/10.1097/ID.0000000000000483
- Wennstrom, J. L., Bengazi, F., & Lekholm, U. (1994). The influence of the masticatory mucosa on the peri-implant soft tissue condition. Clinical Oral Implants Research, 5, 1–8. https://doi.org/10.1034/j.1600-0501.1994.050101.x
- Wennstrom, J. L., & Derks, J. (2012). Is there a need for keratinized mucosa around implants to maintain health and tissue stability? Clinical Oral Implants Research, 23(Suppl 6), 136–146. https://doi.org/10.1111/j.1600-0501.2012.02540.x
- Zigdon, H., & Machtei, E. E. (2008). The dimensions of keratinized mucosa around implants affect clinical and immunological parameters. Clinical Oral Implants Research, 19, 387–392. https://doi.org/10.1111/j.1600-0501.2007.01492.x
Citing Literature
