Predictors of Peri-implant Bone Loss During Long-Term Maintenance of Patients Treated with 10-mm Implants and Single Crown Restorations

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1 Predictors of Peri-implant Bone Loss During Long-Term Maintenance of Patients Treated with 10-mm Implants and Single Crown Restorations Manuel De la Rosa, DDS, MSc 1 /Angel Rodríguez, DDS 1 /Katia Sierra, DDS 2 / Gerardo Mendoza, DDS, MSc 3 /Leandro Chambrone, DDS, MSc, PhD, Post-Doc 4 Purpose: The aim of this retrospective study was to evaluate the predictors of peri-implant bone loss in a sample of patients treated with 10-mm implants and single crowns who underwent periodontal/periimplant maintenance (PM) in a Mexican private periodontal practice. Materials and Methods: Outcomes of a group of systemically healthy, partially edentulous patients attended up to July 2012 were assessed. Patient data were considered for inclusion if they involved treatment of partially edentulous sites with 10-mm-long implants and single crown restorations, as well as at least 3 years of regular PM following implant placement. Peri-implant bone loss was evaluated from data recorded at the most recent examination. Logistic regression analysis was performed to investigate associations between peri-implant bone loss and sex, duration of PM, location and number of implants placed per patient, region of the mouth, smoking status, type of implant, and retention of restoration. Results: A sample of 104 subjects who had been treated with four different types of dental implants and maintained for at least 3 years was selected. Of the 148 implants placed and followed for an average period of continuing PM of 6 years (range, 3 to 15 years), only one implant (1.8%) was lost. The outcomes of logistic regression analysis showed that the independent variables smoking, retention of restoration (cemented vs screw-retained), and type of implant (internal- or external-hex) were found to be correlated with peri-implant bone loss, with odds ratios of 39.64, 4.85, and 0.04, respectively. Conclusions: Peri-implant bone loss was significantly associated with smoking status, the type of implant (ie, externally hexed), and type of retention (ie, cemented). Overall, all patients maintained low rates of bone loss. Int J Oral Maxillofac Implants 2013;28: doi: /jomi.3066 Key words: alveolar bone loss, dental implants, osseointegration, prognosis, smoking 1 Professor, Department of Periodontology, University of Monterrey, Monterrey, Mexico. 2 Private Practice, Yucatán, Mexico. 3 Chairman, Department of Periodontology, School of Dentistry, Cientifica del Sur University, Lima, Peru. 4 Assistant Professor, Department of Periodontology, Dental Research Division, Guarulhos University, Guarulhos, Brazil; Postdoctoral Research Fellow, Division of Periodontics, Department of Stomatology, School of Dentistry, University of São Paulo, São Paulo, Brazil. Correspondence to: Dr Leandro Chambrone, Disciplina de Periodontia Faculdade de Odontologia, Universidade de São Paulo, Av. Prof. Lineu Prestes 2227, Cidade Universitária, São Paulo SP Brazil. leandro_chambrone@ hotmail.com, chambrone@usp.br 2013 by Quintessence Publishing Co Inc. Implant-supported single crown restorations have been recommended as a gold-standard approach for the treatment of partially edentulous patients. 1 The key objectives of these restorations are successful osseointegration of the dental implants, peri-implant tissue health, and esthetic harmony between the single implant crown(s), the peri-implant soft tissue, and the adjacent teeth. 1,2 Despite the successful use of titanium dental implants for the replacement of teeth lost because of periodontitis and other nonperiodontal conditions, dental biofilm growth may lead to inflammatory lesions in the adjacent mucosa and peri-implant bone loss (ie, peri-implantitis). 3 6 On the other hand, the clinical outcome of an individual implant over time may be difficult to anticipate precisely, particularly if the implant was placed in a patient exposed to recognized risk factors influencing the host response or if the patient did not attend periodic maintenance care appointments. For instance, it is well documented that long-term periodontal maintenance can help preserve periodontal health and prevent tooth loss 7 ; however, the crown/root ratio principle has been a constant parameter for the evaluation of conventional periodontal/ prosthetic cases Volume 28, Number 3, 2013

2 With respect to dental implants, recent implant research has suggested that bone-implant contact seems to be more important than the crown/root relationship (ie, implant length) Furthermore, implant success also seems to be related to the manner in which ankylosed structures distribute masticatory forces at the crest of the bone (stress around implant neck). 12 It has been shown that both direct and indirect factors may influence the long-term success of dental implants. Implant surface characteristics, occlusion, 16 bone-implant contact, 1,4,16 surgical procedures (eg, immediate extraction), and the type of restoration 4,17,18 are considered the main direct factors. Similarly, smoking and patient compliance 7 have been reported as important indirect factors affecting implant outcomes. Given the importance of regular long-term maintenance care and the potential effect of different factors on the amount of peri-implant bone loss, the purpose of this study was to assess the predictors of peri-implant bone loss among patients treated with 10-mm-long implants and single crown restorations who underwent long-term periodontal/peri-implant maintenance (PM). MATERIALS AND METHODS This retrospective survey evaluated the records of systemically healthy subjects attended at a private periodontal practice up to July Patients were considered for inclusion if they met the following criteria: (1) age > 18 years at implant placement; (2) no antibiotic treatment in the 6 months prior to implant placement; (3) treatment of partially edentulous sites with 10-mm-long implants and single crowns; and (4) attendance for a minimum of 3 years of maintenance therapy (every 3 to 4 months) performed by the same experienced periodontist (MR) following implant placement. Heavy smokers (ie, subjects who smoked 10 or more cigarettes per day) were considered ineligible for participation. Assessment of Peri-implant Bone Loss Peri-implant bone loss was assessed from data recorded at the time of crown placement and the most recent examination of each patient based on clinical and radiographic measurements performed by the same experienced examiner (MR). Clinical data included probing depth (PD), measured at six sites around the implant, and presence/absence of bleeding on probing (BoP), measured with a PCP-UNC15 manual probe. Radiographic measurements provided information about the level of the alveolar bone (extent of periimplant bone loss). Periapical radiographs were taken before and after implant placement, after crown placement, and every 2 years during PM and compared to assess bone levels. Soft polyether impression material (Impregum, 3M ESPE) guides were fabricated for each implant area and attached to a Flow Right Angle Positioning Device to allow standardization of radiographs (ie, same angulation) taken at different times. Statistical Analysis All analyses were performed using a software package (Number Cruncher Statistical System 2007, NCSS). Descriptive statistics were used to synthesize collected data (mean final PD and BoP). Logistic regression analysis was performed to investigate associations between peri-implant bone loss and sex (male or female), duration of PM (< 5 years or 5 years), location (maxilla or mandible), number of implants placed per patient (one or more), region of the mouth (anterior or posterior), smoking status (yes or no), type of implant (internalhex or external-hex), and retention of restoration (cemented or screw-retained). The dependent variable was the presence of peri-implant bone loss, ie, subjects who had lost peri-implant bone around at least one dental implant, to assess factors that might identify individuals who were more likely to experience peri-implant bone loss. Odds ratios (ORs) with 95% confidence intervals (CIs) were calculated. Differences at P <.05 were considered statistically significant. RESULTS A sample of 104 Hispanic patients of high or average economic status (50 men and 54 women), 20 to 68 years of age (mean age, 44 years), who had been treated with 148 implants (10 mm in length) and who underwent regular PM was selected from subjects attending a private periodontal practice in Monterrey, Mexico. In general, all patients followed a similar treatment protocol: (1) oral hygiene instructions, (2) scaling and root planning where indicated, (3) tooth polishing, and (4) implant placement. Prior to the surgical phase of treatment, all cases were reviewed by a dental specialist team, and a comprehensive treatment plan was elaborated for each patient. The patient approved the treatment plan and completed surgical consent forms. Implant placement was conducted as a flapless procedure or as an open flap procedure. The majority of the cases were treated using flapless procedures, and all implants were placed at the bone level. None of the implants were placed in grafted sinuses or where guided bone regeneration had been performed. Four different implants were used: (1) mm external-hex Osseotite implants (Biomet 3i); (2) mm internalhex MTX microtextured titanium implants (Zimmer The International Journal of Oral & Maxillofacial Implants 799

3 Table 1 Distribution of Patients According to Potential Predictors of Peri-implant Bone Loss N Sex Male 50 Female 54 Implant location Maxilla 75 Mandible 29 Implant region Anterior 39 Posterior 65 Implants per patient = 1 > 1 Period of PM < 5 years 5 years Smoking habits Nonsmokers Smokers Type of implant Internal-hex External-hex Type of retention Cemented Screwed Patients with at least one implant with peri-implant bone loss 30 (60.0%) 30 (55.5%) 43 (57.3%) 17 (58.6%) 20 (51.3%) 40 (61.5%) 43 (58.9%) 17 (54.8%) 28 (57.1%) 32 (58.2%) 28 (41.2%) 32 (88.9%) 28 (43.7%) 32 (80.0%) 27 (56.2%) 33 (58.9%) Dental); (3) mm internal-hex Laser-Lok implants (Biohorizons IPH); and (4) mm external-hex etched-titanium Steri-Oss System implants (Nobel Biocare). Patients were seen at 10 days postsurgery, and digital periapical radiographs were taken. All patients were seen again at 6 and 12 weeks. At 12 weeks, all implants were restored with single crowns. Posterior crowns were cemented or screw-retained, whereas all anterior crowns were cemented for esthetic reasons. PM care appointments included an update of medical and dental histories, dental and implant(s) examination, review of plaque removal efficacy, periodontal probing, removal of dental plaque and calculus from supragingival and subgingival sites, sulcular irrigation with 0.12% chlorhexidine (at implant sites only), and tooth polishing. The average duration of PM was 6 years (range, 3 to 15 years). The mean recall frequency of the 104 patients was 3.5 months. Of the 148 implants placed, only one (0.7%) was lost. During PM, 87 implants (58.8%) in 60 patients (57.0%) showed clinical and radiographic signs of peri-implant bone loss (the measurements taken immediately after crown placement were compared to the most recent outcomes). Among these implants, bone loss did not involve more than 30% of the implant length. The majority of the implants presenting with problematic bone loss (60.9%) were external-hex implants. Also, all external-hex implants with bone loss (n = 53) experienced 30% of bone loss around the implant body neck, whereas only 3% of the internal-hex implants showing bone loss experienced the same scenario. The mean final PD was 3.3 ± 0.5 mm (range, 2.5 to 4.5 mm), and only eight (7.7%) of the 104 implants showed positive BoP. Exposure of implant threads or mobility was not found among implants with bone loss. Thus, they remained in situ and functioned normally. Overall, maxillary posterior implants lost peri-implant bone most frequently, while mandibular anterior implants lost bone least frequently. Smokers (88.9%), men (60.0%), external-hex implants (80.0%), posterior implants (61.5%), mandibular implants (58.2%), screw-retained restorations (58.9%), and patients who attended periodic PM for at least 5 years (58.2%) experienced the highest percentages of peri-implant bone loss (Table 1). However, the degree of association between the dependent variables and the suspected predictors factors was investigated by statistical analysis in an attempt to avoid confounding effects. The results of the logistic regression analysis are shown in Table 2. The independent variables smoking (P =.00000), type of implant (external-hex, P =.00001), and retention of restoration (cemented, P =.03215) were found to be correlated with peri-implant bone loss, with ORs of (95% CI: 8.62 to ), 0.04 (95% CI: 0.01 to 0.17), and 4.85 (95% CI: 1.14 to 20.59), respectively. Conversely, no significant differences were found between the dependent variable and the other predictor factors, ie, sex (P =.84), number of implants placed per patient (P =.69), arch (P =.97), region (anterior/posterior; P =.76), and duration of PM (P =.31). DISCUSSION Although 10-mm implants are not considered short from a clinical point of view, clinicians may prefer to avoid restoring them as single-unit crowns. Therefore, the present study evaluated only patients treated with this protocol to determine the long-term stability of this technique. In the present retrospective, practicebased study, although some degree of bone loss was diagnosed in more than half of the patients, it did not progress beyond one-third of the implant surface. Also, patient smoking status, type of implant (externalhex), and restoration (cemented) were associated with peri-implant bone loss (P <.05). More than half of the patients showing bone loss were smokers (80.0%) or were treated with external-hex implants (53.3%). 800 Volume 28, Number 3, 2013

4 Table 2 Logistic Regression Analysis of Predictors of Peri-implant Bone Loss OR SE z P > z 95% CI Duration of PM (> 5 y) Gender (male) Location (maxilla) No. of implants (one) Region (posterior) Smoker (yes) Type of implant (internal hex) Retention of restoration (cemented) SE = standard error. Even with a strict PM regimen, it is not easy to predict an individual implant s clinical response over time, especially if the patient is exposed to one or more risk factors known to influence host response. Most of the existing evidence identifying tobacco use as a risk factor in the progression of periodontal disease and tooth loss relates to cigarette smoking. 7,22 It has been reported that smoking at least 10 cigarettes per day is strongly associated with an increased risk of bleeding pockets, 22 periodontitis, 22 and tooth loss. 7 Moreover, outcomes from several publications following the landmark paper by Bain and Moy 19 have been unanimous in establishing the detrimental impact of tobacco smoking on the likelihood of implant failure. 20,21 In the present study, heavy smokers were excluded, but subjects classified as light smokers were nevertheless 28.6 times more likely to lose peri-implant bone than nonsmoking patients (Table 2). It should be considered that maintenance of implants may represent a challenge for the clinician, because an implant does not have the same characteristics of a tooth. For instance, a normal tooth has a living periodontal ligament to support it and to indicate when a traumatic occlusion or an occlusal interference is present. 16 In this study, the high rate of implants that remained in function (99%) is probably related to the strict maintenance therapy protocol applied. Female patients were more consistent with PM therapy visits, while male patients were less so, but such an outcome did not significantly influence outcomes (P =.84). Regarding the type of implant used for treatment, the logistic regression analysis indicated that internal-hex implants acted as a protective factor for peri-implant bone loss (OR = 0.04). This is in line with previous data. 23 One of the main complaints with external-hex implants is frequent prosthetic screw loosening. This screw loosening commonly leads to maintenance problems and sometimes even necessitates a new crown. 23 Moreover, the implant-prosthetic connection of external-hex implants is closer to the bone surface than with internalhex implants, and as a result, an internal-hex implant may prevent peri-implant bone loss. 23 With respect to other important factors of this survey, it is important to emphasize that all implants were placed in nongrafted sites. Sixty-eight percent (68%) of the implants were placed in posterior areas, but all of them were placed 4 months after tooth extraction. For implants placed in anterior sites, simultaneous tooth extraction and implant placement were performed (ie, flapless approach), and implants were selected on the basis of the measurements of the roots to be extracted. Moreover, none of the implants in the present study were immediately loaded. All of the implants were placed and left to heal for approximately 10 weeks. During this time frame, posterior implants remained without any provisional restoration, while anterior implants received a Maryland provisional. In addition, this practice-based study has some inherent limitations, such as the lack of a standardized parallel control group, its nonprospective nature, and the evaluation of several implant brands. Furthermore, clinical and radiographic examinations were performed by the same experienced examiner in his private practice, but no specific calculations were performed to calibrate his exams or the accuracy of the measurements. The absence of an appropriate control group, especially in a private periodontal practice, is the chief concern. It could be seen that the majority of patients without a clinical or visible diagnosis of peri-implantitis may not return periodically for maintenance care appointments with the periodontist. Also, individual variations in susceptibility to peri-implantitis in a private practice, even in a group of patients treated by the same clinician and who received similar surgical approaches and continuing PM, may represent a limitation in estimating peri-implant bone loss. These issues need to be considered when interpreting the present findings. The International Journal of Oral & Maxillofacial Implants 801

5 CONCLUSION Within the limits of this study, this practice-based, descriptive, retrospective analysis showed that the types of implants and retention, as well as patients smoking status, can act as potential predictors of peri-implant bone loss during long-term peri-implant/periodontal maintenance. Overall, 10-mm-long implants were maintained in function with low rates of peri-implant bone loss when periodic peri-implant/periodontal maintenance was provided. Acknowledgment The authors report no conflicts of interest related to this study. REFERENCES 1. Lang NP, Zitzmann NU, on behalf of Working Group 3 of the VIII European Workshop on Periodontology. Clinical research in implant dentistry: Evaluation of implant-supported restorations, aesthetic and patient-reported outcomes. J Clin Periodontol 2012;39(suppl 12): Phillips K, Kois JC. Aesthetic peri-implant site development. The restorative connection. Dent Clin North Am 1998;42: Pjetursson BE, Bragger U, Lang NP, Zwahlen M. Comparison of survival and complication rates of tooth-supported fixed dental prostheses (FPDs) and implant-supported FPDs and single crowns (SCs). Clin Oral Implants Res 2007;18(suppl 3): Amarante ES, Chambrone L, Lotufo RF, Lima LA. Early dental plaque formation on toothbrushed titanium implants surfaces. Am J Dent 2008;21: Faggion CM Jr, Chambrone L, Gondim V, Schmitter M, Tu Y-K. Comparison of the effects of treatment of periimplant infection in animal and human studies: Systematic review and meta-analysis. Clin Oral Implants Res 2010;21: Faggion CM Jr, Chambrone L, Listl S, Tu YK. Network meta-analysis for evaluating interventions in implant dentistry: The case of periimplantitis treatment. Clin Implant Dent Relat Res 2011 Aug 11. [epub ahead of print] 7. Chambrone L, Chambrone D, Lima LA, Chambrone LA. Predictors of tooth loss during long-term periodontal maintenance: A systematic review of observational studies. J Clin Periodontol 2010;37: Lulic M, Brägger U, Lang NP, Zwahlen M, Salvi GE. Ante s (1926) law revisited: A systematic review on survival rates and complications of fixed dental prostheses (FDPs) on severely reduced periodontal tissue support. Clin Oral Implants Res 2007;18(suppl 3): Renouard F, Nisand D. Impact of implant length and diameter on survival rates. Clin Oral Implants Res 2006;17(suppl 2): Brocard D, Barthet P, Baysse E, et al. A multicenter report on 1,022 consecutively placed ITI implants: A 7-year longitudinal study. Int J Oral Maxillofac Implants 2000;15: Rokni S, Todescan R, Watson P, Pharoah M, Adegbembo AO, Deporter D. An assessment of crown-to-root ratios with short sintered porous-surfaced implants supporting prostheses in partially edentulous patients. Int J Oral Maxillofac Implants 2005;20: Himmlová L, Dostálová T, Kácovský A, Konvicková S. Influence of implant length and diameter on stress distribution: A finite element analysis. J Prosthet Dent 2004;91: Kotsovilis S, Fourmousis I, Karoussis IK, Bamia C. A systematic review and meta-analysis on the effect of implant length on the survival of rough-surface dental implants. J Periodontol 2009;80: Fugazzotto PA. Shorter implants in clinical practice: Rationale and treatment results. Int J Oral Maxillofac Implants 2008;23: Deporter D, Al-Sayyed A, Pilliar RM, Valiquette N. Biologic width and crestal bone remodeling with sintered porous-surfaced dental implants: A study in dogs. Int J Oral Maxillofac Implants 2008;23: Chambrone L, Chambrone LA, Lima LA. Effects of occlusal overload on peri-implant tissue health: A systematic review of animal-model studies. J Periodontol 2010;81: Pjetursson BE, Tan WC, Zwahlen M, Lang NP. A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation: Part I: Lateral approach. J Clin Periodontol 2008;35(suppl 8): Pjetursson BE, Tan K, Lang NP, Brägger U, Egger M, Zwahlen M. A systematic review of the survival and complication rates of fixed partial dentures (FPDs) after an observation period of at least 5 years. I. Implant-supported FPDs. Clin Oral Implants Res 2004;15: Bain CA, Moy PK. The association between the failure of dental implants and cigarette smoking. Int J Oral Maxillofac Implants 1993; 8: Hinode D, Tanabe S-I, Yokoyama M, Fujisawa K, Yamauchi E, Miyamoto Y. The influence of smoking on osseointegrated implant failure: A meta-analysis. Clin Oral Implants Res 2006;17: Strietzel FP, Reichart PA, Kale A, Kulkarni M, Wegner B, Küchler I. Smoking interferes with the prognosis of dental implant treatment: A systematic review and meta-analysis. J Clin Periodontol 2007;34: Tonetti MS, Claffey N, on behalf of the European Workshop in Periodontology Group C. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. J Clin Periodontol 2005;32(suppl 6): Cochran DL, Hermann JS, Schenk RK, Higginbottom FL, Buser D. Biologic width around titanium implants. A histometric analysis of the implanto-gingival junction around unloaded and loaded nonsubmerged implants in the canine mandible. J Periodontol 1997; 68: Volume 28, Number 3, 2013

Mechanical and technical risks in implant therapy.

Mechanical and technical risks in implant therapy. Salvi GE, Brägger U. Int J Oral Maxillofac Implants. 2009;24 Suppl:69-85. Department of Periodontology, School of Dental Medicine, University of Bern,