ORIGINAL RESEARCH
Evaluation of peri-implant tissues condition after 10–15 years of loading in treated chronic periodontitis patients attending a private practice setting: A retrospective study
Renzo Guarnieri,
Dario Di Nardo,
Gianni Di Giorgio,
Gabriele Miccoli,
Luca Testarelli,
Corresponding Author
Renzo Guarnieri
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Correspondence
Renzo Guarnieri, Private Periodontal Implant Practice, Strada di Canizzano 33, 31100 Treviso, Italy.
Email: [email protected]
Search for more papers by this authorDario Di Nardo
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorGianni Di Giorgio
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorGabriele Miccoli
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorLuca Testarelli
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorRenzo Guarnieri,
Dario Di Nardo,
Gianni Di Giorgio,
Gabriele Miccoli,
Luca Testarelli,
Corresponding Author
Renzo Guarnieri
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Correspondence
Renzo Guarnieri, Private Periodontal Implant Practice, Strada di Canizzano 33, 31100 Treviso, Italy.
Email: [email protected]
Search for more papers by this authorDario Di Nardo
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorGianni Di Giorgio
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorGabriele Miccoli
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorLuca Testarelli
Department of Dental and Maxillofacial Sciences, School of Dentistry, University La Sapienza, Rome, Italy
Search for more papers by this authorAbstract
Objectives
To retrospectively evaluate the conditions of the peri-implant tissues in treated patients with chronic periodontitis (CP) and in patients without chronic periodontitis (noCP).
Materials and methods
A chart review was used to evaluate 267 implants, 134 placed in 42 CP treated patients and 133 placed in 46 noCP patients. The primary outcome was to evaluate the condition of the peri-implant tissues (health, peri-mucositis, and peri-implantitis). The secondary outcome was to evaluate the possible association of some variables, such as, Plaque Index (PI), Bleeding Index (BI), probing pocket depth (PD), bleeding on probing (BoP), bone level (BL), loading time, type of implant placement and loading protocol, type of prosthesis, type of bone, implant manufacturer, and implant diameter and length, with the implant health condition.
Results
The analysis of patient files revealed that after 10–15 years of loading (mean loading time 13.4 ± 2.07 years), six noCP patients (13%) experienced implant loss with a total of nine implants (6.7%) lost. The remaining 124 implants were classified: 54 (43.5%) as healthy, 45 (36.3%) with peri-implant mucositis, and 25 (20.2%) with peri-implantitis. Twelve CP subjects (28.5%) experienced implant loss with a total of 19 implants (14.1%) lost. The remaining 115 implants were classified: 34 (29.5%) as healthy, 40 (34.7%) with peri-implant mucositis and 41 (35.6%) with peri-implantitis. Compared with noCP subjects, only treated CP subjects with recurrent periodontal disease (RPD) showed differences statistically significant (p < .05).
Conclusions
After 10–15 years of loading, in CP patients treated in a private practice setting, most implants (70.1%) were classified with some type of peri-implant inflammation. In patients with RPD, a higher tendency for implant loss and peri-implant biologic complications was found.
CONFLICT OF INTEREST
The authors have stated explicitly that there are no conflicts of interest in connection with this article. Prof. Renzo Guarnieri, Dr. Dario DiNardo, Dr. Gianni DiGiorgio, Dr. Gabriele Miccoli, Prof. Luca Testarelli have nothing to disclose.
Supporting Information
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REFERENCES
- Adams, D. (1992). Diagnosis and treatment of refractory periodontitis. Current Opinion in Dentistry, 2, 33–38.
- Aglietta, M., Siciliano, V. I., Rasperini, G. et al (2011). A 10-year retrospective analysis of marginal bone-level changes around implants in periodontally healthy and periodontally compromised tobacco smokers. Clinical Oral Implants Research, 22, 47–53.
- Aguirre-Zorzano, L. A., Estefania-Fresco, R., Telletxea, O., & Bravo, M. (2015). Prevalence of peri-implant inflammatory disease in patients with a history of periodontal disease who receive supportive periodontal therapy. Clinical Oral Implants Research, 26, 1338–1344. https://doi.org/10.1111/clr.12462
- Anner, R., Grossmann, Y., Anner, Y., & Levin, L. (2010). 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 Dentistry, 19, 57–64. https://doi.org/10.1097/ID.0b013e3181bb8f6c
- Armitage, G. C. (1999). Development of a classification system for periodontal diseases and conditions. Annals of Periodontology, 4, 1–6.
- Astrand, P., Engquist, B., Anzén, B. et al (2004). A three-year follow-up report of a comparative study of ITI Dental Implants and Brånemark System implants in the treatment of the partially edentulous maxilla. Clinical Implant Dentistry and Related Research, 6, 130–141.
- Belibasakis, G. N. (2014). Microbiological and immuno-pathological aspects of peri-implant diseases. Archives of Oral Biology, 59(1), 66–72.
- Berglundh, T., Persson, L., & Klinge, B. (2002). A systematic review of the incidence of biological and technical complications in implant dentistry reported in prospective longitudinal studies of at least 5 years. Journal of Clinical Periodontology, 3, 197–212.
- Buser, D., Sennerby, L., & De Bruyn, H. (2017). Modern implant dentistry based on osseointegration: 50 years of progress, current trends and open questions. Periodontology 2000, 73(1), 7–21.
- Charalampakis, G., Leonhardt, Å., Rabe, P., & Dahlén, G. (2012). Clinical and microbiological characteristics of peri-implantitis cases: A retrospective multicentre study. Clinical Oral Implants Research, 23(9), 1045–1054. https://doi.org/10.1111/j.1600-0501.2011.02258.x
- 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). Periodontally compromised vs. periodontally healthy patients and dental implants: A systematic review and meta-analysis. Journal of Dentistry, 42(12), 1509–1527.
- Colombo, A. P., Haffajee, A. D., Dewhirst, F. E., Paster, B. J., Smith, C. M., Cugi, M. A., & Socransky, S. S. (1998). Clinical and microbiological features of refractory periodontitis subjects. Journal of Clinical Periodontology, 25, 169–180.
- Dabdoub, S. M., Tsigarida, A. A., & Kumar, P. S. (2013). Patient-specific analysis of periodontal and peri-implant microbiomes. Journal of Dental Research, 92(12 Suppl), 168S–175S. https://doi.org/10.1177/0022034513504950
- Daubert, D. M., Weinstein, B. F., Bordin, S., Leroux, B. G., & Flemming, T. F. (2015). Prevalence and predictive factors for peri-implant disease and implant failure: A cross-sectional analysis. Journal of Periodontology, 86(3), 337–347. https://doi.org/10.1902/jop.2014.140438
- De Boever, A. L., Quirynen, M., Coucke, W., Theuniers, G., & De Boever, J. A. (2009). Clinical and radiographic study of implant treatment outcome in periodontally susceptible and non-susceptible patients: A prospective long-term study. Clinical Oral Implants Research, 20, 1341–1350. https://doi.org/10.1111/j.1600-0501.2009.01750.x
- Derks, 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
- Doornewaard, R., Jacquet, W., Cosyn, J., & De Bruyn, H. (2018). How do peri-implant biologic parameters correspond with implant survival and peri-implantitis? A critical review. Clinical Oral Impants Research, 29(Suppl. 18), 100.
- Duarte, P. M., Serrao, C. R., Miranda, T. S. et al (2015). Could cytokine levels in the peri-implant crevicular fluid be used to distinguish between healthy implants and implants with peri-implantitis? A systematic review. Clinical Oral Implants Research, 26, 937–941.
- Dvorak, G., Arnhart, C., Heuberer, S., Huber, C. D., Watzek, G., & Gruber, R. (2011). Peri-implantitis and late implant failures in postmenopausal women: A cross-sectional study. Journal of Clinical Periodontology, 38, 950–955.
- Evian, C. I., Emling, R., Rosenberg, E. S. et al (2004). Retrospective analysis of implant survival and the influence of periodontal disease and immediate placement on long-term results. International Journal of Oral & Maxillofacial Implants, 19, 393–398.
- Faot, F., Nascimento, G. G., Bielemann, A. M., Campao, T. D., Leite, F. R., & Quirynen, M. (2015). Can peri-implant crevicular fluid assist in the diagnosis of peri-implantitis? A systematic review and meta-analysis. Journal of Periodontology, 86, 631–645. https://doi.org/10.1902/jop.2015.140603
- Fardal, Ø., & Linden, G. J. (2008). Tooth loss and implant outcomes in patients refractory to treatment in a periodontal practice. Journal of Clinical Periodontology, 35(8), 733–738. https://doi.org/10.1111/j.1600-051X.2008.01247.x
- Ferreira, S. D., Martins, C. C., Amaral, S. A., Vieira, T. R., Albuquerque, B. N., Cota, L. O. M., Esteves Lima, R. P., & Costa, F. O. (2018). Periodontitis as a risk factor for peri-implantitis: Systematic review and meta-analysis of observational studies. Journal of Dentistry, 79, 1–10.
- Ferreira, S. D., Silva, G. L., Cortelli, J. R., Costa, J. E., & Costa, F. O. (2006). Prevalence and risk variables for peri-implant disease in Brazilian subjects. Journal of Clinical Periodontology, 33(12), 929–935.
- García-Bellosta, S., Bravo, M., Subirá, C., & Echeverría, J. J. (2010). Retrospective study of the long-term survival of 980 implants placed in a periodontal practice. International Journal of Oral Maxillofacial Implants, 25, 613–619.
- Ghassib, I., Chen, Z., Zhu, J., & Wang, H.-L. (2018). Use of IL-1 β, IL-6, TNF-α, and MMP-8 biomarkers to distinguish peri-implant diseases: A systematic review and metaanalysis. Clinical Implant Dentistry and Related Research, 1–18.
- Graetz, C., El-Sayed, K. F., Geiken, A. et al (2018). Effect of periodontitis history on implant success: A long-term evaluation during supportive periodontal therapy in a university setting. Clinical Oral Investigations, 22(1), 235–244.
- Haffajee, A. D., Socransky, S. S., Dzink, J. L. et al (1988). Clinical, microbiological and immunological features of subjects with refractory periodontal diseases. Journal of Clinical Periodontology, 15, 390–398.
- Hirschfeld, L., & Wasserman, B. (1978). A long-term survey of tooth loss in 600 treated periodontal patients. Journal of Periodontology, 49, 225–237.
- Hultin, M., Gustafsson, A., Hallstrom, H., Johansson, L. A., Ekfeldt, A., & Klinge, B. (2002). Microbiological findings and host response in patients with peri-implantitis. Clinical Oral Implant Research, 13, 349–358.
- Karoussis, I. K., Kotsovilis, S., & Fourmousis, I. (2007). A comprehensive and critical review of dental implant prognosis in periodontally compromised partially edentulous patients. Clinical Oral Implants Research, 18, 669–679.
- Karoussis, I. K., Salvi, G. E., Heitz-Mayfeld, L. J. et al (2003). Long-term implant prognosis in patients with and without a history of chronic periodontitis: A 10-year prospective cohort study of the ITI Dental Implant System. Clinical Oral Implants Research, 14, 329–339.
- Klokkevold, P. R., & Han, T. J. (2007). How do smoking, diabetes, and periodontitis affect outcomes of implant treatment? International Journal of Oral & Maxillofacial Implants, 22(Suppl), 173–202.
- 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.
- Laine, M. L., Crielaard, W., & Loos, B. G. (2012). Genetic susceptibility to periodontitis. Periodontology 2000, 58, 37–68.
- Lang, N. P., & Berglundh, T. (2011). Periimplant diseases: Where are we now? Consensus of the Seventh European Workshop on Periodontology. Journal of Clinical Periodontology, 38(Suppl. 11), 178–181.
- Lasserre, J. F., Brecx, M. C., & Toma, S. (2018). Oral microbes, Biofilms and their role in periodontal and peri-implant diseases. Materials (Basel), 11(10), 1802.
- Leonhardt, A., Renvert, S., & Dahlen, G. (1999). Microbial findings at failing implants. Clinical Oral Implants Research, 10, 339–345. https://doi.org/10.1034/j.1600-0501.1999.100501.x
- Levin, L., Ofec, R., Grossmann, Y., & Anner, R. (2011). Periodontal disease as a risk for dental implant failure over time: A long-term historical cohort study. Journal of Clinical Periodontology, 38, 732–737. https://doi.org/10.1111/j.1600-051X.2011.01745.x
- Lindhe, J., & Meyle, J. (2008). Peri-implant diseases: Consensus Report of the Sixth European Workshop on Periodontology. Journal of Clinical Periodontology, 35(Suppl. 8), 282–285. https://doi.org/10.1111/j.1600-051X.2008.01283.x
- Marrone, A., Lasserre, J., Bercy, P., & Brecx, M. C. (2013). Prevalence and risk factors for peri-implant disease in Belgian adults. Clinical Oral Implants Research, 24(8), 934–940.
- Matarasso, S., Rasperini, G., Iorio Siciliano, V. et al. (2010). A 10-year retrospective analysis of radiographic bone-level changes of implants supporting single-unit crowns in periodontally compromised vs. periodontally healthy patients. Clinical Oral Implants Research, 21(9), 898–903. https://doi.org/10.1111/j.1600-0501.2010.01945.x
- Máximo, M. B., de Mendonça, A. C., Alves, J. F., Cortelli, S. C., Peruzzo, D. C., & Duarte, P. M. (2008). Peri-implant diseases may be associated with increased time loading and generalized periodontal bone loss: Preliminary results. Journal of Oral Implantology, 34(5), 268–273.
- Mir-Mari, J., Mir-Orfila, P., Figueiredo, R., Valmaseda-Castellón, E., & Gay-Escoda, C. (2012). Prevalence of peri-implant diseases. A cross-sectional study based on a private practice environment. Journal of Clinical Periodontology, 39, 490–494. https://doi.org/10.1111/j.1600-051X.2012.01872.x
- Mombelli, A., Marxer, M., Gaberthuel, T., Grunder, U., & Lang, N. P. (1995). The microbiota of osseointegrated implants in patients with a history of periodontal disease. Journal of Clinical Periodontology, 22, 124–130. https://doi.org/10.1111/j.1600-051X.1995.tb00123.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 & Immunology, 2(4), 145–151. https://doi.org/10.1111/j.1399-302X.1987.tb00298.x
- Mouhyi, J., Dohan Ehrenfest, D. M., & Albrektsson, T. (2012). The peri-implantitis: Implant surfaces, microstructure, and physicochemical aspects. Clinical Implant Dentistry and Related Research, 14, 170–183.
- Nowzari, H., Botero, J. E., DeGiacomo, M., Villacres, M. C., & Rich, S. K. (2008). Microbiology and cytokine levels around healthy dental implants and teeth. Clinical Implant Dentistry & Related Research, 10, 166–173. https://doi.org/10.1111/j.1708-8208.2007.00076.x
- Ong, C. T. 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, 438–462. https://doi.org/10.1111/j.1600-051X.2008.01207.x
- Ormianer, Z., & Patel, A. (2012). The use of tapered implants in the maxillae of periodontally susceptible patients: 10-year outcomes. International Journal of Oral & Maxillofacial Implants, 27(2), 442–448.
- Papaioannou, W., Quirynen, M., & Van Steenberghe, D. (1996). The influence of periodontitis on the subgingival flora around implants in partially edentulous patients. Clinical Oral Implants Research, 7(4), 405–409. https://doi.org/10.1034/j.1600-0501.1996.070415.x
- Papapanou, P. N., Sanz, M., Buduneli, N., Dietrich, T., Feres, M., Fine, D. H., Flemmig, T. F., Garcia, R., Giannobile, W. V., Graziani, F., Greenwell, H., Herrera, D., Kao, R. T., Kebschull, M., Kinane, D. F., Kirkwood, K. L., Kocher, T., Kornman, K. S., Kumar, P. S., … Tonetti, M. S. (2018). Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the classification of periodontal and peri-implant diseases and conditions. Journal of Periodontology, 89(Suppl 1), S173–S182. https://doi.org/10.1002/JPER.17-0721
- Persson, G. R., & Renvert, S. (2014). Cluster of bacteria associated with peri-implantitis. Clinical Implant Dentistry and Related Research, 16(6), 783–793. https://doi.org/10.1111/cid.12052
- Pjetursson, B. E., Tan, K., Lang, N. P., Brägger, U., Egger, M., & Zwahlen, M. (2004). A systematic review of the survival and complication rates of fixed partial dentures (FPDs) after an observation period of at least 5 years. Clinical Oral Implants Research, 15(6), 667–676.
- Quirynen, M., Vogels, R., Peeters, W., van Steenberghe, D., Naert, I., & Haffajee, A. (2006). Dynamics of initial subgingival colonization of ‘pristine’ peri-implant pockets. Clinical Oral Implant Research, 17, 25–37. https://doi.org/10.1111/j.1600-0501.2005.01194.x
- Rehman, A., Hu, J., Ott, S. J. et al (2012). Microbial community composition on modified dental implant surfaces: An in vivo study. International Journal of Oral and Maxillofacial Implants, 27, 811–819.
- Renvert, S., & Persson, G. R. (2009). Periodontitis as a potential risk factor for peri-implantitis. Journal of Clinical Periodontololgy, 36(suppl 10), 9–14. https://doi.org/10.1111/j.1600-051X.2009.01416.x
- Roccuzzo, M., Bonino, L., Dalmasso, P., & Aglietta, M. (2014). Long-term results of a three arms prospective cohort study on implants in periodontally compromised patients: 10-year data around sandblasted and acid-etched (SLA) surface. Clinical Oral Implants Research, 25(10), 1105–1112.
- 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 I: Implant loss and radiographic bone loss. Clinical Oral Implants Research, 21, 490–496.
- Rokn, A., Aslroosta, H., Akbari, S., Najafi, H., Zayeri, F., & Hashemi, K. (2017). Prevalence of peri-implantitis in patients not participating in well-designed supportive periodontal treatments: A cross-sectional study. Clinical Oral Implants Research, 28, 314–319. https://doi.org/10.1111/clr.12800
- Roos-Jansåker, 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(4), 290–295.
- Roos-Jansaker, A. M., Renvert, H., Lindahl, C., & Renvert, S. (2006). b) Nine-to fourteen-year follow-up of implant treatment. Part III: Factors associated with peri-implant lesions. Journal of Clinical Periodontology, 33, 296–301. https://doi.org/10.1111/j.1600-051X.2006.00908.x
- Safi, S. H., Palmer, R. M., & Wilson, R. F. (2010). Risk of implant failure and marginal bone loss in subjects with a history of periodontitis: A systematic review and meta-analysis. Clinical Implant Dentistry and Related Research, 12(3), 165–174.
- Sánchez-Siles, M., Muñoz-Cámara, D., Salazar-Sánchez, N., Ballester-Ferrandis, J. F., & Camacho-Alonso, F. (2015). Incidence of peri-implantitis and oral quality of life in patients rehabilitated with implants with different neck designs: A 10-year retrospective study. Journal of Craniomaxillofacial Surgery, 43(10), 2168–2174.
- Sanz, M., & Chapple, I. L. (2012). Clinical research on peri-implant diseases: Consensus report of Working Group 4. Journal of Clinical Periodontology, 39(Suppl 12), 202–206. https://doi.org/10.1111/j.1600-051X.2011.01837.x
- Schou, S., Holmstrup, P., Worthington, H. V., & Esposito, M. (2006). Outcome of implant therapy in patients with previous tooth loss due to periodontitis. Clinical Oral Implants Research, 17(suppl 2), 104–123.
- Schwarz, F., Becker, K., Sahm, N., Horstkemper, T., Rousi, K., & Becker, J. (2017). The prevalence of peri-implant diseases for two-piece implants with an internal tube-in-tube connection: A cross-sectional analysis of 512 implants. Clinical Oral Implants Research, 28, 24–28.
- Schwarz, F., Derks, J., Monje, A., & Wang, H.-L. (2018). Peri-implantitis. Journal of Periodontology, 89(Suppl 1), S267–S290.
- 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
- Slots, J. (1996). Systemic antibiotics in periodontitis. Journal of Periodontology, 67, 831–838.
- Souza, V., Mardas, N., Farias, B., Petrie, A., Needleman, I., Spratt, D., & Donos, N. (2016). A systematic review of implant outcomes in treated periodontitis patients. Clinical Oral Implants Research, 27, 787–844. https://doi.org/10.1111/clr.12684
- 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.
- Turri, A., Rossetti, P. H., Canullo, L., Grusovin, M. G., & Dahlin, C. (2016). Prevalence of peri-implantitis in medically compromised patients and smokers: A systematic review. International Journal of Oral & Maxillofacial Implants, 31(1), 111–118. https://doi.org/10.11607/jomi.4149
- Van der Weijden, G. A., van Bemmel, K. M., & Renvert, S. (2005). Implant therapy in partially edentulous periodontally compromised patients: A review. Journal of Clinical Periodontology, 32, 506–511.
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