IMPLANT DENTISTRY / VOLUME 24, NUMBER 2 2015
217
Retrospective Long-Term Evaluation of Dental Implants in Totally and Partially Edentulous Patients: Part II: Periimplant Disease Anna Trullenque-Eriksson, DDS, PhD,* and Blanca Guisado Moya, MD, PhD†
ral rehabilitation with dental osseointegrated implants is nowadays a frequently chosen treatment option, which is considered safe and predictable. However, implant treatment is not without complications, which generate discomfort to the patient whose treatment is time consuming and imply an additional cost. They can be divided into early or late depending on the time of occurrence and into biological or mechanical depending on their nature.1–4 One of the biological complications that can occur once the rehabilitation is in place is periimplant disease. This is a collective term for inflammatory reactions affecting the tissues that surround an osseointegrated implant in function. It comprises 2 entities: periimplant mucositis and the so-called periimplantitis. Periimplant mucositis is a reversible inflammation of the soft tissues surrounding an implant in function without loss of supporting bone. Periimplantitis is an inflammation of the periimplant soft tissues accompanied by a progressive loss of supporting
O
*Private Practice, Bury St Edmunds, UK. †Professor of Oral Surgery, Department of Oral & Facial Medicine and Surgery, Faculty of Dentistry (UCM), Madrid, Spain.
Reprint requests and correspondence to: Blanca Guisado Moya, MD, PhD, Departamento de Medicina y Cirugía Bucofacial, Facultad de Odontología, Universidad Complutense de Madrid, Plaza Ramón y Cajal, s/n, 28013 Madrid, Spain, Phone: +34 91 394 19 68, E-mail: [email protected] ISSN 1056-6163/15/02402-217 Implant Dentistry Volume 24 Number 2 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/ID.0000000000000224
Purpose: This retrospective longitudinal study aims to assess longterm outcomes of osseointegrated dental implants placed in partially and totally edentulous patients. Material and Methods: Patients who were willing to sign the informed consent and attend a check-up were included. The prevalence of periimplant disease was calculated. Cases were further divided into mucositis or periimplantitis. Uni- and multi-variate statistical analyses were conducted to determine the influence of various factors. Results: A total of 105 patients who had received 342 implants were included. Mean follow-up was 13.19 6 3.70 years. The prevalence of periimplant disease was
14.2% of the analyzed implants and 21% of patients. An additional 4.8% of patients reported a previous presence of periimplant disease without current disease. The prevalence of mucositis and periimplantitis was 11.2% and 1.7%, respectively, of analyzed implants. Factors with possible influence on the presence of periimplant disease were gender, alcohol consumption, chemotherapy and/or head and neck radiotherapy, history of periodontal disease, and years of function. Conclusion: In our sample, periimplant disease was not infrequent, being present in 1 of 5 patients at the final check-up. (Implant Dent 2015;24:217–221) Key Words: periimplantitis, mucositis
bone, which can lead to implant loss. The evolution from one to another is gradual and sometimes slow, which can make differentiation difficult.5,6 There is large variation in the frequency of these processes in the literature, due to different criteria and follow-up times. In the long term, mucositis could be as frequent as approximately 30% of implants and more than 60% of patients, whereas the prevalence of periimplantitis could be approximately 10% of implants and 20% of patients.6,7
Although it is generally agreed that there is an infectious component in its etiology, it is argued whether the infection is primary or secondary to an initial disruption of osseointegration due to other causes. Several potential risk factors have been suggested in the literature.6 Periimplant disease is generating interest and controversy at present. Because of the large number of patients receiving dental implants and longer expected function times, the number of potential cases may be very high.
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
218
RETROSPECTIVE LONG-TERM EVALUATION
The aim of this study was to evaluate the long-term outcomes of osseointegrated dental implants placed in partially and totally edentulous patients. This part of study analyzes the presence of periimplant disease and factors that may have had an influence.
MATERIALS
AND
METHODS
This is a retrospective longitudinal study based on data collected through the patients’ medical and dental records, clinical and radiological examinations, and satisfaction questionnaires. A detailed description of the Material and Methods can be found in part I of this study. Briefly, patients who had been rehabilitated through dental implants placed before or during 2002 in the Master in Oral Surgery and Implantology, Faculty of Dentistry, Complutense University of Madrid were contacted. As long as no important information regarding the implants was lacking, patients who agreed to sign the informed consent and attend an examination of their remaining implants were included in the study. Data were collected from their medical and dental records, and a clinical and radiological examination was performed. The prevalence of periimplant disease was calculated. The presence of a probing depth equal or greater than 5 mm accompanied by bleeding on probing and/or suppuration was considered periimplant disease. When a valid baseline radiograph was available, further differentiation was made as follows: in the absence of bone loss greater than 3 mm, the implant was recorded as suffering periimplant mucositis; when present, it was considered as periimplantitis. Periimplant disease prevalence was also evaluated with the patient as
OF
DENTAL IMPLANTS
TRULLENQUE-ERIKSSON
statistical unit (the presence of at least 1 implant with periimplant disease). Regarding the factors that could have influenced these variables, univariate and multivariate (logistic regression) statistical analyses were carried out for age at implant placement, gender, smoking, alcohol consumption, diabetes, hypertension, osteopenia or osteoporosis, bisphosphonate intake, thyroid dysfunction, hypercholesterolemia, chemotherapy and/or head and/or neck radiotherapy, anticoagulant intake, check-up frequency, history of periodontal disease, implant shape, surface, diameter, length, and position, 1- or 2stage surgery, need for regeneration techniques, prosthesis type, and followup time. Because of the high proportion of machined surface cylindrical Brånemark system implants, this group was also analyzed separately.
RESULTS As described in part I of this study, 105 patients were finally included in the study. Of note, 35.2% of the included patients were men and 64.8% women. The average age at implant placement was 47.84 6 14.42 years. These patients had received 342 osseointegrated dental implants. The mean follow-up of those implants was 13.19 6 3.70 years (further details can be consulted in part I of this study). Periimplant Disease
Probing depths and the presence of bleeding on probing and/or suppuration are summarized in Table 1. Of the 296 implants present at the examination in which probing was possible, 14.2% had periimplant disease. Twenty-one percent of patients had periimplant disease in 1 or more
Probing Depth (mm) #3 4 5 $6 Total
Absence of Bleeding on Probing and/or Suppuration
Presence of Bleeding on Probing and/or Suppuration
Total
119 16 6 3 144
66 44 26 16 152
185 60 32 19 296
Cases considered as periimplant disease are formatted bold.
GUISADO MOYA
Table 2. Marginal Bone Level
Distance to Reference Point (mm) #1 1.01–2 2.01–3 3.01–4 4.01–5 5.01–6 6.01–7 7.01–8 Total
Probing Depth $5 mm With Bleeding on No. of Probing and/or Implants Suppuration 87 95 65 33 7 5 2 2 296
11 10 6 7 3 3 0 2 42
implants. The percentage is calculated on 100 patients rather than 105 because 3 had lost all of the implants and probing was not possible in 2 patients (1 patient did not give his permission for probing and another had recently received chemotherapy, and only visual inspection and radiological examination were allowed by the oncologist). An additional 4.8% of patients reported a history of periimplant disease but did not suffer from it at present. Bone levels and bone loss in combination with a probing depth equal to or greater than 5 mm accompanied by bleeding on probing and/or suppuration are summarized in Tables 2 and 3. Of the 242 probed implants with a valid baseline radiograph, 11.2% had periimplant mucositis; these implants were placed in 14 patients: 1 patient had mucositis in 4 implants, 2 in 3 implants,
Table 3. Marginal Bone Loss
Modification of Marginal Bone (mm)
Table 1. Clinical Condition of Implants
AND
#1 or “gain” 1.01–2 2.01–3 3.01–4 4.01–5 5.01–6 Total
Probing Depth $5 mm With Bleeding on Probing and/or No. of Implants Suppuration 157 56 24 3 0 2 242
22 4 1 3 0 1 31
Only probed implants with valid baseline radiograph are shown. Cases considered as periimplantitis are formatted bold.
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
IMPLANT DENTISTRY / VOLUME 24, NUMBER 2 2015
Table 4. Logistic Regression: Periimplant Disease (Unit ¼ Implant) Independent Variables
Effect
B
Significance
Exp(B)
95% CI for Exp(B)
History of periodontal disease Chemotherapy/ radiotherapy
No/Yes
2.288
0.002
9.854
2.308–42.083
No/Yes
1.328
0.010
3.775
1.382–10.312
CI indicates confidence interval.
Table 5. Logistic Regression: Periimplant Disease (Unit ¼ Patient) 95% CI for Exp(B) Independent Variables
Effect
B
Sig
Exp(B)
Min
Max
History of periodontal disease
No/Yes
2.328
0.003
10.262
2.170
48.517
CI indicates confidence interval.
6 in 2 implants, and 5 in 1 implant. Of note, 1.7% presented periimplantitis; these cases occurred in 3 patients. Factors
According to the univariate analyses, periimplant disease was significantly more frequent for implants placed in male patients (when analyzing the subgroup “machined surface cylindrical Brånemark implants,” P ¼ 0.024), frequent drinkers (when analyzing the subgroup “machined surface cylindrical Brånemark implants,” P ¼ 0.020), patients who had received chemotherapy and/or radiotherapy (P ¼ 0.001), patients with a history of periodontal disease (P , 0.001), and those with more than 20 years of function (P ¼ 0.023). At patient level, those with a history of periodontal disease presented periimplant disease more frequently (P ¼ 0.002). The significant results from the multivariate analyses are summarized in Tables 4 and 5.
DISCUSSION In this retrospective longitudinal study, the long-term results of implants were evaluated based on survival, changes in marginal bone levels (described in part I), and the presence of periimplant disease. Different follow-up times and lack of consensus regarding criteria makes it difficult to compare our results with those of other authors. In the 2000 study by Koldsland et al,8 these differences were highlighted with the prevalence
of periimplantitis varying between 36.6% of implants and 47.1% of patients and 5.4% of implants and 11.3% of patients depending on the applied criteria. The probing depth limit for periimplant disease was established at 5 mm. Around implants, a probing depth of up to 4 mm is considered normal, and initial probing could be even higher in esthetic areas where the implant shoulder has been placed deeper or in areas with thicker soft tissues.3,6,9 Regarding bleeding on probing, in 1993, Ericsson and Lindhe demonstrated in a study in dogs that periimplant probing produced a connective tissue damage that could lead to bleeding not necessarily related to inflammation.10 According to this, a 4-mm probing may not imply pathology, not even in the presence of bleeding, which may be due to trauma from probing. Therefore, a more conservative limit was chosen with the intention of not overestimating the prevalence of periimplant disease. Regarding bone loss, a limit of 3 mm was set. Some authors have not included bone loss limits within their criteria or these limits were lower, which would lead to higher incidence/prevalence. Other authors have chosen marginal bone level at a certain distance from a reference point as criteria. However, when there is no information on the initial state, it is difficult to establish a differential diagnosis from previous problems, such as improper implant placement.6 In the literature, prevalence figures for periimplant mucositis of between
219
10% and 80% of implants and between 40% and 77% of patients can be found.7,8,11–18 In the 2006 study by Roos-Jansåker et al,14,15 with our criteria, mucositis would have been present in 19% of implants and 40.8% of patients. For periimplantitis, prevalence figures of between 0.3% and 37% of implants and between 5% and 65% of patients can be found.2,6–8,10,13–25 With the same criteria as in this study, Cho-Yan Lee et al23 gave a periimplantitis prevalence of 6% of implants and 11.7% of patients. Significant differences were found in the frequency of periimplant disease according to gender, being higher for implants placed in men than in women. Ferreira et al13 and Koldsland et al26 also found an increased presence of mucositis and/or periimplantitis in men. However, other authors found no statistically significant differences.12,15,16 In the Sixth European Workshop of Periodontology in 2008,27,28 it was concluded that, among other factors, there was evidence of an association of periimplant disease with cigarette smoking and a history of periodontitis, and limited evidence of association with alcohol consumption. Although in our study the proportion of implants with periimplant disease was higher in frequent drinkers, the difference between smokers and nonsmokers was not statistically significant. A higher prevalence of periimplant disease was observed in patients with a history of periodontal disease. As in this study, other authors have reported a higher prevalence/incidence of periimplantitis in patients suffering or had suffered from periodontal disease.13,15,19,21,24,26 Some studies have found differences depending on the severity of the periodontal disease.29–32 Other studies did not detect significant differences in the long-term results in patients with a history of chronic periodontal disease and those without.16,29,33,34 Study Limitations
As commented in part I of this study, the design of this study entails a number of limitations.35 This study can only give prevalence figures. To determine the incidence of
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
220
RETROSPECTIVE LONG-TERM EVALUATION
periimplant disease, long-term prospective studies with adequate sampling and an appropriate sample size would be required. Also, our results can only suggest a possible influence; long-term randomized clinical trials are necessary to establish cause-effect relationships.
CONCLUSIONS 1. Of note, 14.2% of the analyzed implants in 21% of patients presented periimplant disease. Of the analyzed implants, which had a valid baseline radiograph, 11.2% had periimplant mucositis and 1.7% had periimplantitis. 2. It seems that certain factors may have an influence on the presence of periimplant disease, such as gender, alcohol consumption, chemotherapy and/or head and neck radiotherapy, and history of periodontal disease. In summary, in our sample, periimplant disease was not infrequent, being present in 1 of 5 patients at the final check-up.
REFERENCES 1. Esposito M, Hirsch JM, Lekholm U, et al. Biological factors contributing to failures of osseointegrated oral implants. (I). Success criteria and epidemiology. Eur J Oral Sci. 1998;106:527–551. 2. Berglundh T, Persson L, Klinge B. A systematic review of the incidence of biological and technical complications in implant dentistry reported in prospective longitudinal studies of at least 5 years. J Clin Periodontol. 2002;29(suppl 3): 197–212. 3. Lang NP, Berglundh T, HeitzMayfield LJ, et al. Consensus statements and recommended clinical procedures regarding implant survival and complications. Int J Oral Maxillofac Implants. 2004; 19(suppl):150–154. 4. Jung RE, Pjetursson BE, Glauser R, et al. A systematic review of the 5-year survival and complication rates of implant-supported single crowns. Clin Oral Implants Res. 2008;19:119–130. 5. Albrektsson T, Isidor F. Consensus report session IV. In: Lang NP, Karring T, eds. Proceedings of the 1st European Workshop on Periodontology. London,
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United Kingdom: Quintessence; 1994: 365–369. 6. Mombelli A, Müller N, Cionca N. The epidemiology of peri-implantitis. Clin Oral Implants Res. 2012;23(suppl 6):67–76. 7. Atieh MA, Alsabeeha NH, Faggion CM Jr, et al. The frequency of peri-implant diseases: A systematic review and Metaanalysis. J Periodontol. 2012;13:1586– 1598. 8. Koldsland OC, Scheie AA, Aass AM. Prevalence of peri-implantitis related to severity of the disease with different degrees of bone loss. J Periodontol. 2010; 81:231–238. 9. Lang NP, Wilson TG, Corbet EF. Biological complications with dental implants: Their prevention, diagnosis and treatment. Clin Oral Implants Res. 2000; 11(suppl 1):146–155. 10. Åstrand P, Ahlqvist J, Gunne J, et al. Implant treatment of patients with edentulous jaws: A 20-year follow-up. Clin Implant Dent Relat Res. 2008;10:207–217. 11. Adell R, Lekholm U, Rockler B, et al. Marginal tissue reactions at osseointegrated titanium fixtures (I). A 3-year longitudinal prospective study. Int J Oral Maxillofac Surg. 1986;15:39–52. 12. Lekholm U, Adell R, Lindhe J, et al. Marginal tissue reactions at osseointegrated titanium fixtures. (II) A cross-sectional retrospective study. Int J Oral Maxillofac Surg. 1986;15:53–61. 13. Ferreira SD, Silva GL, Cortelli JR, et al. Prevalence and risk variables for peri-implant disease in Brazilian subjects. J Clin Periodontol. 2006;33:929–935. 14. Roos-Jansåker AM, Lindahl C, Renvert H, et al. Nine- to fourteen-year follow-up of implant treatment. Part II: Presence of peri-implant lesions. J Clin Periodontol. 2006;33:290–295. 15. Roos-Jansåker AM, Renvert H, Lindahl C, et al. Nine- to fourteen-year follow-up of implant treatment. Part III: Factors associated with peri-implant lesions. J Clin Periodontol. 2006;33:296–301. 16. Rinke S, Ohl S, Ziebolz D, et al. Prevalence of periimplant disease in partially edentulous patients: A practicebased cross-sectional study. Clin Oral Implants Res. 2011;22:826–833. 17. Charyeva O, Altynbekov K, Zhartybaev R, et al. Long-term dental implant success and survival–a clinical study after an observation period up to 6 years. Swed Dent J. 2012;36:1–6. 18. Degidi M, Nardi D, Piattelli A. 10-year follow-up of immediately loaded implants with TiUnite porous anodized surface. Clin Implant Dent Relat Res. 2012;14:828–838. 19. Karoussis IK, Salvi GE, Heitz-Mayfield LJ, et al. Long-term implant prognosis in patients with and without a history of chronic periodontitis: A 10-year prospective cohort
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study of the ITI dental implant system. Clin Oral Implants Res. 2003;14:329–339. 20. Fransson C. Prevalence, Extent and Severity of Periimplantitis. (PhD Thesis). Gothemburg, Sweden: Department of Periodontology, University of Gothemburg; 2009. 21. Simonis P, Dufour T, Tenenbaum H. Long-term implant survival and success: A 10-16-year follow-up of non-submerged dental implants. Clin Oral Implants Res. 2010;21:772–777. 22. Buser D, Janner SF, Wittneben JG, et al. 10-Year survival and success rates of 511 titanium implants with a sandblasted and acid-etched surface: A retrospective study in 303 partially edentulous patients. Clin Implant Dent Relat Res. 2012;14:839– 851. 23. Cho-Yan Lee J, Mattheos N, Nixon KC, et al. Residual periodontal pockets are a risk indicator for peri-implantitis in patients treated for periodontitis. Clin Oral Implants Res. 2012;23:325–333. 24. Renvert S, Lindahl C, Rutger Persson G. The incidence of peri-implantitis for two different implant systems over a period of thirteen years. J Clin Periodontol. 2012;39:1191–1197. 25. Stoker G, van Waas R, Wismeijer D. Long-term outcomes of three types of implant-supported mandibular overdentures in smokers. Clin Oral Implants Res. 2012;23:925–929. 26. Koldsland OC, Scheie AA, Aass AM. The association between selected risk indicators and severity of peri-implantitis using mixed model analyses. J Clin Periodontol. 2011;38:285–292. 27. Heitz-Mayfield LJ. Peri-implant diseases: Diagnosis and risk indicators. J Clin Periodontol. 2008;35(8 suppl):292–304. 28. Lindhe J, Meyle J. Group D of european workshop on periodontology. Peri-implant diseases: Consensus report of the sixth european workshop on periodontology. J Clin Periodontol. 2008;35(8 suppl):282–285. 29. Mengel R, Flores-de-Jacoby L. Implants in patients treated for generalized aggressive and chronic periodontitis: A 3-year prospective longitudinal study. J Periodontol. 2005;76:534–543. 30. De Boever AL, Quirynen M, Coucke W, et al. Clinical and radiographic study of implant treatment outcome in periodontally susceptible and non-susceptible patients: A prospective long-term study. Clin Oral Implants Res. 2009;20: 1341–1350. 31. Roccuzzo M, De Angelis N, Bonino L, et al. Ten-year results of a threearm prospective cohort study on implants in periodontally compromised patients. Part 1: Implant loss and radiographic bone loss. Clin Oral Implants Res. 2010;21:490–496.
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
IMPLANT DENTISTRY / VOLUME 24, NUMBER 2 2015 32. Roccuzzo M, Bonino F, Aglietta M, et al. Ten-year results of a three arms prospective cohort study on implants in periodontally compromised patients. Part 2: Clinical results. Clin Oral Implants Res. 2012;23:389–395. 33. García-Bellosta S, Bravo M, Subirá C, et al. Retrospective study of the long-term
survival of 980 implants placed in a periodontal practice. Int J Oral Maxillofac Implants. 2010;25:613–619. 34. Vercruyssen M, Quirynen M. Long-term, retrospective evaluation (implant and patient-centered outcome) of the two-implant-supported overdenture in the mandible. Part 2: Marginal
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bone loss. Clin Oral Implants Res. 2010; 21:466–472. 35. Trullenque-Eriksson A, GuisadoMoya B. Restrospective long-term evaluation of dental implants in totally and partially edentulous patients. Part 1: Survival and marginal bone loss. Implant Dent. 2014;23:732–737.
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
217
Retrospective Long-Term Evaluation of Dental Implants in Totally and Partially Edentulous Patients: Part II: Periimplant Disease Anna Trullenque-Eriksson, DDS, PhD,* and Blanca Guisado Moya, MD, PhD†
ral rehabilitation with dental osseointegrated implants is nowadays a frequently chosen treatment option, which is considered safe and predictable. However, implant treatment is not without complications, which generate discomfort to the patient whose treatment is time consuming and imply an additional cost. They can be divided into early or late depending on the time of occurrence and into biological or mechanical depending on their nature.1–4 One of the biological complications that can occur once the rehabilitation is in place is periimplant disease. This is a collective term for inflammatory reactions affecting the tissues that surround an osseointegrated implant in function. It comprises 2 entities: periimplant mucositis and the so-called periimplantitis. Periimplant mucositis is a reversible inflammation of the soft tissues surrounding an implant in function without loss of supporting bone. Periimplantitis is an inflammation of the periimplant soft tissues accompanied by a progressive loss of supporting
O
*Private Practice, Bury St Edmunds, UK. †Professor of Oral Surgery, Department of Oral & Facial Medicine and Surgery, Faculty of Dentistry (UCM), Madrid, Spain.
Reprint requests and correspondence to: Blanca Guisado Moya, MD, PhD, Departamento de Medicina y Cirugía Bucofacial, Facultad de Odontología, Universidad Complutense de Madrid, Plaza Ramón y Cajal, s/n, 28013 Madrid, Spain, Phone: +34 91 394 19 68, E-mail: [email protected] ISSN 1056-6163/15/02402-217 Implant Dentistry Volume 24 Number 2 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/ID.0000000000000224
Purpose: This retrospective longitudinal study aims to assess longterm outcomes of osseointegrated dental implants placed in partially and totally edentulous patients. Material and Methods: Patients who were willing to sign the informed consent and attend a check-up were included. The prevalence of periimplant disease was calculated. Cases were further divided into mucositis or periimplantitis. Uni- and multi-variate statistical analyses were conducted to determine the influence of various factors. Results: A total of 105 patients who had received 342 implants were included. Mean follow-up was 13.19 6 3.70 years. The prevalence of periimplant disease was
14.2% of the analyzed implants and 21% of patients. An additional 4.8% of patients reported a previous presence of periimplant disease without current disease. The prevalence of mucositis and periimplantitis was 11.2% and 1.7%, respectively, of analyzed implants. Factors with possible influence on the presence of periimplant disease were gender, alcohol consumption, chemotherapy and/or head and neck radiotherapy, history of periodontal disease, and years of function. Conclusion: In our sample, periimplant disease was not infrequent, being present in 1 of 5 patients at the final check-up. (Implant Dent 2015;24:217–221) Key Words: periimplantitis, mucositis
bone, which can lead to implant loss. The evolution from one to another is gradual and sometimes slow, which can make differentiation difficult.5,6 There is large variation in the frequency of these processes in the literature, due to different criteria and follow-up times. In the long term, mucositis could be as frequent as approximately 30% of implants and more than 60% of patients, whereas the prevalence of periimplantitis could be approximately 10% of implants and 20% of patients.6,7
Although it is generally agreed that there is an infectious component in its etiology, it is argued whether the infection is primary or secondary to an initial disruption of osseointegration due to other causes. Several potential risk factors have been suggested in the literature.6 Periimplant disease is generating interest and controversy at present. Because of the large number of patients receiving dental implants and longer expected function times, the number of potential cases may be very high.
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
218
RETROSPECTIVE LONG-TERM EVALUATION
The aim of this study was to evaluate the long-term outcomes of osseointegrated dental implants placed in partially and totally edentulous patients. This part of study analyzes the presence of periimplant disease and factors that may have had an influence.
MATERIALS
AND
METHODS
This is a retrospective longitudinal study based on data collected through the patients’ medical and dental records, clinical and radiological examinations, and satisfaction questionnaires. A detailed description of the Material and Methods can be found in part I of this study. Briefly, patients who had been rehabilitated through dental implants placed before or during 2002 in the Master in Oral Surgery and Implantology, Faculty of Dentistry, Complutense University of Madrid were contacted. As long as no important information regarding the implants was lacking, patients who agreed to sign the informed consent and attend an examination of their remaining implants were included in the study. Data were collected from their medical and dental records, and a clinical and radiological examination was performed. The prevalence of periimplant disease was calculated. The presence of a probing depth equal or greater than 5 mm accompanied by bleeding on probing and/or suppuration was considered periimplant disease. When a valid baseline radiograph was available, further differentiation was made as follows: in the absence of bone loss greater than 3 mm, the implant was recorded as suffering periimplant mucositis; when present, it was considered as periimplantitis. Periimplant disease prevalence was also evaluated with the patient as
OF
DENTAL IMPLANTS
TRULLENQUE-ERIKSSON
statistical unit (the presence of at least 1 implant with periimplant disease). Regarding the factors that could have influenced these variables, univariate and multivariate (logistic regression) statistical analyses were carried out for age at implant placement, gender, smoking, alcohol consumption, diabetes, hypertension, osteopenia or osteoporosis, bisphosphonate intake, thyroid dysfunction, hypercholesterolemia, chemotherapy and/or head and/or neck radiotherapy, anticoagulant intake, check-up frequency, history of periodontal disease, implant shape, surface, diameter, length, and position, 1- or 2stage surgery, need for regeneration techniques, prosthesis type, and followup time. Because of the high proportion of machined surface cylindrical Brånemark system implants, this group was also analyzed separately.
RESULTS As described in part I of this study, 105 patients were finally included in the study. Of note, 35.2% of the included patients were men and 64.8% women. The average age at implant placement was 47.84 6 14.42 years. These patients had received 342 osseointegrated dental implants. The mean follow-up of those implants was 13.19 6 3.70 years (further details can be consulted in part I of this study). Periimplant Disease
Probing depths and the presence of bleeding on probing and/or suppuration are summarized in Table 1. Of the 296 implants present at the examination in which probing was possible, 14.2% had periimplant disease. Twenty-one percent of patients had periimplant disease in 1 or more
Probing Depth (mm) #3 4 5 $6 Total
Absence of Bleeding on Probing and/or Suppuration
Presence of Bleeding on Probing and/or Suppuration
Total
119 16 6 3 144
66 44 26 16 152
185 60 32 19 296
Cases considered as periimplant disease are formatted bold.
GUISADO MOYA
Table 2. Marginal Bone Level
Distance to Reference Point (mm) #1 1.01–2 2.01–3 3.01–4 4.01–5 5.01–6 6.01–7 7.01–8 Total
Probing Depth $5 mm With Bleeding on No. of Probing and/or Implants Suppuration 87 95 65 33 7 5 2 2 296
11 10 6 7 3 3 0 2 42
implants. The percentage is calculated on 100 patients rather than 105 because 3 had lost all of the implants and probing was not possible in 2 patients (1 patient did not give his permission for probing and another had recently received chemotherapy, and only visual inspection and radiological examination were allowed by the oncologist). An additional 4.8% of patients reported a history of periimplant disease but did not suffer from it at present. Bone levels and bone loss in combination with a probing depth equal to or greater than 5 mm accompanied by bleeding on probing and/or suppuration are summarized in Tables 2 and 3. Of the 242 probed implants with a valid baseline radiograph, 11.2% had periimplant mucositis; these implants were placed in 14 patients: 1 patient had mucositis in 4 implants, 2 in 3 implants,
Table 3. Marginal Bone Loss
Modification of Marginal Bone (mm)
Table 1. Clinical Condition of Implants
AND
#1 or “gain” 1.01–2 2.01–3 3.01–4 4.01–5 5.01–6 Total
Probing Depth $5 mm With Bleeding on Probing and/or No. of Implants Suppuration 157 56 24 3 0 2 242
22 4 1 3 0 1 31
Only probed implants with valid baseline radiograph are shown. Cases considered as periimplantitis are formatted bold.
Copyright © 2015 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
IMPLANT DENTISTRY / VOLUME 24, NUMBER 2 2015
Table 4. Logistic Regression: Periimplant Disease (Unit ¼ Implant) Independent Variables
Effect
B
Significance
Exp(B)
95% CI for Exp(B)
History of periodontal disease Chemotherapy/ radiotherapy
No/Yes
2.288
0.002
9.854
2.308–42.083
No/Yes
1.328
0.010
3.775
1.382–10.312
CI indicates confidence interval.
Table 5. Logistic Regression: Periimplant Disease (Unit ¼ Patient) 95% CI for Exp(B) Independent Variables
Effect
B
Sig
Exp(B)
Min
Max
History of periodontal disease
No/Yes
2.328
0.003
10.262
2.170
48.517
CI indicates confidence interval.
6 in 2 implants, and 5 in 1 implant. Of note, 1.7% presented periimplantitis; these cases occurred in 3 patients. Factors
According to the univariate analyses, periimplant disease was significantly more frequent for implants placed in male patients (when analyzing the subgroup “machined surface cylindrical Brånemark implants,” P ¼ 0.024), frequent drinkers (when analyzing the subgroup “machined surface cylindrical Brånemark implants,” P ¼ 0.020), patients who had received chemotherapy and/or radiotherapy (P ¼ 0.001), patients with a history of periodontal disease (P , 0.001), and those with more than 20 years of function (P ¼ 0.023). At patient level, those with a history of periodontal disease presented periimplant disease more frequently (P ¼ 0.002). The significant results from the multivariate analyses are summarized in Tables 4 and 5.
DISCUSSION In this retrospective longitudinal study, the long-term results of implants were evaluated based on survival, changes in marginal bone levels (described in part I), and the presence of periimplant disease. Different follow-up times and lack of consensus regarding criteria makes it difficult to compare our results with those of other authors. In the 2000 study by Koldsland et al,8 these differences were highlighted with the prevalence
of periimplantitis varying between 36.6% of implants and 47.1% of patients and 5.4% of implants and 11.3% of patients depending on the applied criteria. The probing depth limit for periimplant disease was established at 5 mm. Around implants, a probing depth of up to 4 mm is considered normal, and initial probing could be even higher in esthetic areas where the implant shoulder has been placed deeper or in areas with thicker soft tissues.3,6,9 Regarding bleeding on probing, in 1993, Ericsson and Lindhe demonstrated in a study in dogs that periimplant probing produced a connective tissue damage that could lead to bleeding not necessarily related to inflammation.10 According to this, a 4-mm probing may not imply pathology, not even in the presence of bleeding, which may be due to trauma from probing. Therefore, a more conservative limit was chosen with the intention of not overestimating the prevalence of periimplant disease. Regarding bone loss, a limit of 3 mm was set. Some authors have not included bone loss limits within their criteria or these limits were lower, which would lead to higher incidence/prevalence. Other authors have chosen marginal bone level at a certain distance from a reference point as criteria. However, when there is no information on the initial state, it is difficult to establish a differential diagnosis from previous problems, such as improper implant placement.6 In the literature, prevalence figures for periimplant mucositis of between
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10% and 80% of implants and between 40% and 77% of patients can be found.7,8,11–18 In the 2006 study by Roos-Jansåker et al,14,15 with our criteria, mucositis would have been present in 19% of implants and 40.8% of patients. For periimplantitis, prevalence figures of between 0.3% and 37% of implants and between 5% and 65% of patients can be found.2,6–8,10,13–25 With the same criteria as in this study, Cho-Yan Lee et al23 gave a periimplantitis prevalence of 6% of implants and 11.7% of patients. Significant differences were found in the frequency of periimplant disease according to gender, being higher for implants placed in men than in women. Ferreira et al13 and Koldsland et al26 also found an increased presence of mucositis and/or periimplantitis in men. However, other authors found no statistically significant differences.12,15,16 In the Sixth European Workshop of Periodontology in 2008,27,28 it was concluded that, among other factors, there was evidence of an association of periimplant disease with cigarette smoking and a history of periodontitis, and limited evidence of association with alcohol consumption. Although in our study the proportion of implants with periimplant disease was higher in frequent drinkers, the difference between smokers and nonsmokers was not statistically significant. A higher prevalence of periimplant disease was observed in patients with a history of periodontal disease. As in this study, other authors have reported a higher prevalence/incidence of periimplantitis in patients suffering or had suffered from periodontal disease.13,15,19,21,24,26 Some studies have found differences depending on the severity of the periodontal disease.29–32 Other studies did not detect significant differences in the long-term results in patients with a history of chronic periodontal disease and those without.16,29,33,34 Study Limitations
As commented in part I of this study, the design of this study entails a number of limitations.35 This study can only give prevalence figures. To determine the incidence of
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RETROSPECTIVE LONG-TERM EVALUATION
periimplant disease, long-term prospective studies with adequate sampling and an appropriate sample size would be required. Also, our results can only suggest a possible influence; long-term randomized clinical trials are necessary to establish cause-effect relationships.
CONCLUSIONS 1. Of note, 14.2% of the analyzed implants in 21% of patients presented periimplant disease. Of the analyzed implants, which had a valid baseline radiograph, 11.2% had periimplant mucositis and 1.7% had periimplantitis. 2. It seems that certain factors may have an influence on the presence of periimplant disease, such as gender, alcohol consumption, chemotherapy and/or head and neck radiotherapy, and history of periodontal disease. In summary, in our sample, periimplant disease was not infrequent, being present in 1 of 5 patients at the final check-up.
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