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IMPLANT DENTISTRY / VOLUME 19, NUMBER 1 201057Smoking, Diabetes Mellitus, Periodontitis, andSupportive Periodontal Treatment as FactorsAssociated With Dental Implant Survival: ALong-Term Retrospective Evaluation ofPatients Followed for Up to 10 YearsRachel Anner, DMD,* Yoav Grossmann, DMD,† Yael Anner,‡ and Liran Levin, DMD§uring the past decade, the use ofosseointegrated implants as afoundation for prosthetic replacement of missing teeth has becomehighly predictable and successful.1 However, certain risk factors might predisposeindividuals to lower success rates.2Survival of oral implants has beensystematically analyzed in the 4th European Workshop on Periodontologyin 2002.1 It is evident that the survivalof oral implants is very high. However, an initial loss of 2.5% of allimplants is expected in routine implanttherapy. After functional loading, implant loss was 2% to 3%, over a 5-yearobservation period for implants supporting fixed restorations, whereas inoverdenture therapy, 5% of the implants were expected to be lost withinthat period.Furthermore, Holm-Pedersen etal3 reported that 0.5% to 1.3% im-D*Private practice, Kfar-Saba, Israel.†Senior Prosthodontist, Maxillofacial Prosthodontics Services,Oral & Maxillofacial Center, Sheba Medical Center, TelHashomer, Israel.‡Medical Student, Ben-Gurion University of the Negev, BeerSheva, Israel.§Clinical Instructor, Department of Oral Rehabilitation, TheMaurice and Gabriela Goldschleger School of Dental Medicine,Tel Aviv University, Tel Aviv, Israel; and Department ofPeriodontology, School of Graduate Dentistry, Rambam HealthCare Campus, Haifa, Israel.Reprint requests and correspondence to: Liran Levin,DMD, Department of Oral Rehabilitation, TheMaurice and Gabriela Goldschleger, School of DentalMedicine, Tel Aviv University, Tel Aviv, Israel,E-mail: [email protected] 1056-6163/10/01901-057Implant DentistryVolume 19 Number 1Copyright 2010 by Lippincott Williams & WilkinsDOI: 10.1097/ID.0b013e3181bb8f6cObjectives: To evaluate the factors associated with long-term implant survival in a large cohort ofpatients in regular follow-up untildata collection.Methods: The study populationconsisted of 475 patients who werereferred to a private clinic limited toPeriodontics and Implantology between November 1995 and July 2006.Data were collected from patient fileswith regards to smoking habits, periodontal condition, diabetes mellitus,implant survival, and time when implant failure occurred. Patients weredivided into those who participated ina supportive periodontal program inthe clinic and those who only attendedthe annual free-of-charge implantexamination.Results: A total of 1626 implantswere placed with a follow-up rangingfrom 1 to 114 months (average30.82 28.26 months). Overall, 77(4.7%) implants were lost in 58(12.2%) patients after a mean periodof 24.71 25.84 months. More thanone-half of the patients (246; 51.7%)participated in a structured supportiveperiodontal program in the clinic, and229 (48.3%) only attended to the annual free-of-charge implant examination. Smoking and attendance in aregular supportive periodontal program were statistically associatedwith implant survival. Patients with(treated) moderate-to-advanced chronicperiodontal disease demonstratedhigher implant failure rates but, thisdifference did not reach statisticalsignificance. Diabetes mellitus wasnot related to implant survival in thispatient cohort.Conclusions: Smoking and attendance in a regular supportive periodontal program were found to bestrongly related to implant survival.Special attention should be given tocontinuous periodontal supportiveprograms to implant patients.(Implant Dent 2010;19:57– 64)Key Words: tobacco, periodontitis, diabetes mellitus, supportive therapy,implant failureplants are lost per year of functionresulting in survival rates of between80% and 90% after 10 years depending on the clinical situation of the implants and prosthetic rehabilitation.In a recent systematic review ofthe literature, it was found that smok-ing adversely affects implant survivaland success and is more pronounced inareas of poor quality, trabecular bone.2Type 2 diabetes may have an adverseeffect on implant survival rates, but adefinitive conclusion could not bemade because of the limited number of

58FACTORS ASSOCIATED WITH DENTAL IMPLANT SURVIVAL ANNERET ALTable 1. Factors Associated With Dental Implant SurvivalFactorSmokingYesNoDiabetes mellitusYesNoPeriodontal diseaseYesNoSPTYesNoNo. ofImplants (%)No. ofFailedImplants (%)0.0286226 (13.9)1400 (86.1)21 (9.3)56 (4)0.00064 (8.2)54 (12.7)0.3628177 (1.09)1449 (89.1)5 (2.8)72 (5)0.2076311 (65.5)164 (34.5)43 (13.8)15 (9.1)0.13881171 (72)455 (28)61 (5.2)16 (3.5)0.1498246 (51.8)229 (48.2)21 (8.5)37 (16.2)0.011428 (3.2)49 (6.5)0.0028No. ofPatients (%)No. of PatientsWith Failed Implants (%)63 (13.3)412 (86.7)13 (20.6)45 (10.9)49 (10.3)426 (89.7)P*873 (53.7)753 (46.3)P*P values in bold represents statistical significance. Smoking and attendance in a regular supportive periodontal program were associated with implant survival. Patients with treated moderate-to-advancedchronic periodontal disease showed higher implant failure rates but this difference did not reach statistical significance. Diabetes mellitus was not related to implant survival in this patient cohort.*z test for proportions.studies included in the review. A history of treated periodontitis does notseem to adversely affect implant survival rates but it could have a negativeinfluence on implant success rates,particularly over longer periods.2Hultin et al4 stated that there arefew available studies evaluating thelong-term effect of supportive periodontal programs for implant patients.The authors highlighted in their conclusions4 the need for such studies tobe initiated.The purpose of this study was toevaluate the influence of smoking,diabetes mellitus, periodontitis, andsupportive periodontal treatment asfactors associated with long-term (upto 10 years) implant survival in a largecohort of patients who were in regularfollow-up until data collection.MATERIALSANDMETHODSThe study population consisted of475 patients (176 men, 37%; 299women, 63%; average age 51.96 11.98) who were referred to a privateclinic limited to Periodontics and Implantology between November 1995and July 2006. A total of 1626 implantswere placed by a single surgeon (R.A.)in these patients. Implants were placedafter completion of periodontal causerelated therapy and periodontal stabilization. Follow-up ranged from 1 to 114months (average 30.82 28.26 months).All patients were offered a freeof-charge annual examination andfollow-up after implant placement.Only patients who were in routinefollow-up until data collection wereincluded in the evaluation. Demographic parameters (age, gender, etc.)were similar between this follow-upgroup and the patients who were excluded because of their lack of adherence to follow-up appointments (datanot shown).Data were collected from patientfiles with regards to smoking habits,periodontal condition, diabetes mellitus, implant survival, and time whenimplant failure occurred. Patients werealso divided into those who participated in a supportive periodontal program in the clinic and those who onlyattended the annual free-of-charge implant examination.Data were analyzed with statistical software (SPSS 12.0; SPSS, Inc.,Chicago, IL) using z test for proportions and 2 test. A 5% significancelevel was used.RESULTSSmoking was reported by 63(13.2%) patients and diabetes mellitusby 49 (10.3%). Periodontal diseasewas diagnosed in 311 (65.4%) of thepatients. Overall, 77 (4.7%) implantswere lost in 58 (12.2%) patients after amean period of 24.71 25.84 months.In the structured supportive periodontal program in the clinic, 246 patients (51.7%) participated and 229(48.3%) only attended the annualfree-of-charge implant examination.Smoking and attendance in a regularsupportive periodontal program wereassociated with implant survival(Table 1). Patients with treatedmoderate-to-advanced chronic periodontal disease showed higher implant failure rates, but this differencedid not reach statistical significance.Diabetes mellitus was not related toimplant survival in this patient cohort (Table 1). The odds ratio was1.89 for attendance in a regular supportive periodontal program andsmoking (P 0.05) (Table 2).DISCUSSIONAn implant-supported restorationoffers a predictable treatment for toothreplacement.7–9 Nevertheless, failuresthat mandate immediate implant removal do occur.6,10 13 The consequences of implant removal jeopardizethe clinician’s efforts to accomplishsatisfactory function and esthetics. Forthe patient, this usually involves further cost and additional procedures.14Reported predictors for implantsuccess and failure are generally divided into patient-related factors (e.g.,general patient health status, smokinghabits, quantity and quality of bone,and oral hygiene maintenance), implant characteristics (e.g., dimensions,coating, and loading), implant location, and clinician experience.15The overall first-year survivalrate for dental implants is between

IMPLANT DENTISTRY / VOLUME 19, NUMBER 1 2010Table 2. Odds Ratio Calculated for Dental Implant Failure95% ConfidenceIntervalFactorOdds RatioLowerUpperP*SmokingDiabetes mellitusPeriodontal (NS)0.11 (NS)0.012The table shows that smokers and patients not attending in a regular supportive periodontal program had an odds ratio of 1.89 forimplant failure.*Chi-square test.92% and 97%.16 An additional 1% ofall implants that are initially successful and rehabilitated are lost every year because of complications.17In this study, the survival rates fallbetween the reported survival ratesin the literature.18Hultin et al4 conducted a studythat systematically reviewed whethersupportive implant treatment during afollow-up of at least 10 years afterfunctional loading is effective in preventing biological complications andfixture loss. It was concluded that, todate, there are few available studiesthat evaluate the long-term effect ofsupportive programs for implant patients and that there is an urgent needfor such studies to be initiated. Thisreport clearly illustrates that there is animportant role for regular continuoussupportive periodontal therapy in implant patients to increase implantsurvival over time. In the treatmentstrategies for periodontitis, the needfor supervised training and reenforcement of self-performed oralhygiene is well established. Also, indental implant patients, instruction inbrushing and interproximal cleaningshould be initiated as soon as the prosthetic reconstruction is connected. Inan elderly patient, reduced capacity ofdiligence and manual dexterity is notuncommon, thus requiring frequentprofessional training visits and cleaning of abutment surfaces to removebacterial biofilms. Although there isno direct evidence in the literature tosuggest the importance of supportivetherapy for implants as for periodontally treated teeth, periodontal therapyhas been suggested to precede implanttherapy in partially dentate patients,19whereas systematic and continuousmonitoring of the periodontal andperi-implant tissue conditions issuggested to prevent recurrence ofperiodontal disease and allow earlydiagnosis and treatment of periimplant diseases.20Other environmental- and patientrelated factors contribute to implantfailures. Nitzan et al21 report a relationship between marginal implantbone loss and smoking habits. Ahigher incidence of marginal implantbone loss was found in the smokinggroup, which was more pronounced inthe maxilla. A higher degree of complications, or implant failure rates,were found in smokers with and without bone grafts.22,23 However, in an18-month study of 1183 implants, Kumar et al24 report similar survival rates(97% and 94.4%) for smokers andnonsmokers. In this study, smokersexhibited a significantly lower survival rate than nonsmokers. Smokersundergoing both implant-related surgical procedures and dental implantation should be encouraged by theirdentists, oral and maxillofacial surgeons, or treating physicians to ceasesmoking, emphasizing that smokingcan increase complications and reducethe success rate of these procedures.Successful osseointegration hasbeen shown in patients with differenttypes of periodontitis.25,26 However,these reports do not offer comparative data between periodontallycompromised patients who havebeen treated and periodontallyhealthy patients. Nevertheless, a systematic review by Van der Weijdenet al27 conclude that the outcome ofimplant therapy in periodontitis patients may be different comparedwith individuals without such a his-59tory in terms of loss of supportingbone and implant loss.In a systematic review of implantoutcomes in treated periodontitis subjects, Ong et al20 conclude that there issome evidence that patients treated forperiodontitis may experience more implant loss and complications aroundimplants including higher bone lossand peri-implantitis than nonperiodontitis patients. Evidence was strongerfor implant survival than implant success. In this report, periodontal diseasepatients demonstrated higher implantfailure rates but this difference did notreach statistical significance, whichcould be attributed to the fact that thepatients were treated in a periodontalclinic and their periodontal conditionwas “controlled.” Consequently, appropriate consent should be obtainedbefore implant therapy is provided toperiodontal patients.Diabetes mellitus is one of themost commonly encountered contraindications to dental implant therapy.Glycemic control is viewed as a critical variable in identifying whether patients with diabetes are eligible forimplant therapy.28 –30 This view on theimportance of glycemic control in implant success has been reinforced.31–33Several clinical reports suggest that inpatients with “well-controlled” type 2diabetes mellitus, dental implant success rates (92%–100%) may not besignificantly compromised.32–34 In addition, a large multicenter study ofdental implant success report an implant failure rate of only 7.8% for 255implants placed in “selected” patientswith type 2 diabetes mellitus.31The hypothesis that patients withdiabetes are appropriate candidatesfor implants and that compromises inglycemic control may not excludeimplant success has been explored.35This study found no evidence ofdiminished clinical success or significant early healing complications associated with implant therapy inpatients with controlled type 2 diabetes mellitus, which agrees with theformer study.CONCLUSIONSSmoking and attendance in a regular supportive periodontal program

60FACTORS ASSOCIATED WITH DENTAL IMPLANT SURVIVAL ANNERwere found to be strongly related toimplant survival. It is highly recommended to maintain implant patientsunder a strict supportive periodontaltreatment protocol that might contribute to implant survival.ACKNOWLEDGMENTSThe authors thank Ms. Rita Lazar, Scientific Editor, The Maurice and Gabriela Goldschleger School of DentalMedicine, Tel Aviv University, TelAviv, Israel, for scientific editorialassistance.DisclosureThe authors claim to have no financial interest in any company or any ofthe products mentioned in this article.REFERENCES1. Berglundh T, Persson L, Klinge B. Asystematic review of the incidence ofbiological and technical complications inimplant dentistry reported in prospectivelongitudinal studies of at least 5 years.J Clin Periodontol. 2002;29:197-212.2. Klokkevold PR, Han TJ. How dosmoking, diabetes, and periodontitis affectoutcomes of implant treatment? Int J OralMaxillofac Implants. 2007;22:173-202.3. Holm-Pedersen P, Lang NP, Müller F.What are the longevities of teeth and oralimplants? Clin Oral Implants Res. 2007;18:15-19.4. Hultin M, Komiyama A, Klinge B. Supportive therapy and the longevity of dentalimplants: A systematic review of the literature. Clin Oral Implants Res. 2007;8:50-62.5. Pjetursson BE, Tan K, Lang NP, etal. A systematic review of the survival andcomplication rates of fixed partial dentures(FPDs) after an observation period of atleast 5 years. Clin Oral Implants Res. 2004;15:625-642.6. Esposito M, Grusovin MG,Coulthard P, et al. A 5-year follow-up comparative analysis of the efficacy of variousosseointegrated dental implant systems: Asystematic review of randomized controlled clinical trials. Int J Oral MaxillofacImplants. 2005;20:557-568.7. Levin L, Laviv A, Schwartz-Arad D.Long-term success of implants replacing aET ALsingle molar. J Periodontol. 2006;77:1528-1532.8. Levin L, Sadet P, Grossmann Y. Aretrospective evaluation of 1387 singletooth implants: A six-year follow up. J Periodontol. 2006;77:2080-2083.9. Levin L, Pathael S, Dolev E, et al.Aesthetic versus surgical success of singledental implants: 1- to 9-year follow-up.Pract Proced Aesthet Dent. 2005;17:533538.10. Duyck J, Naert I. Failure of oralimplants: Aetiology, symptoms and influencing factors. Clin Oral Investig. 1998;2:102-114.11. Grossmann Y, Levin L. Successand survival of single dental implantsplaced in sites of previously failed implants.J Periodontol. 2007;78:1670-1674.12. Jung RE, Pjetursson BE, GlauserR, et al. A systematic review of the 5-yearsurvival and complication rates of implantsupported single crowns. Clin Oral Implants Res. 2008;19:119-130.13. Schwartz-Arad D, Laviv A, Levin L.Failure causes, timing, and clusterbehavior: An 8-year study of dental implants. Implant Dent. 2008;17:200-207.14. Levin L. Dealing with dental implantfailures. J Appl Oral Sci. 2008;16:171-175.15. Porter JA, von Fraunhofer JA. Success or failure of dental implants? A literature review with treatment considerations.Gen Dent. 2005;53:423-432.16. Rosenberg ES, Cho SC, Elian N, etal. A comparison of characteristics of implant failure and survival in periodontallycompromised and periodontally healthypatients: A clinical report. Int J Oral Maxillofac Implants. 2004;19:873-879.17. Perry J, Lenchewski E. Clinicalperformance and 5-year retrospectiveevaluation of Frialit-2 implants. Int J OralMaxillofac Implants. 2004;19:887-891.18. Lang NP, Berglundh T, HeitzMayfield LJ, et al. Consensus statementsand recommended clinical procedures regarding implant survival and complications. Int J Oral Maxillofac Implants.2004;19 (suppl):150-154.19. Van Steenberghe D. Fostering andmaintaining a sound periodontal environment with root-form implants. Dent Implantol Update. 1993;4:85-88.20. Ong CT, Ivanovski S, NeedlemanIG, et al. Systematic review of implant outcomes in treated periodontitis subjects.J Clin Periodontol. 2008;35:438-462.21. Nitzan D, Mamlider A, Levin L, et al.Impact of smoking on marginal bone loss.Int J Oral Maxillofac Implants. 2005;20:605-609.22. Levin L, Hertzberg R, Har-Nes S, etal. Long-term marginal bone loss aroundsingle dental implants affected by currentand past smoking habits. Implant Dent.2008;17:422-429.23. Levin L, Schwartz-Arad D. The effect of cigarette smoking on dental implants and related surgery. Implant Dent.2005;14:357-361.24. Kumar A, Jaffin RA, Berman C. Theeffect of smoking on achieving osseointegration of surface modified implants: Aclinical report. Int J Oral Maxillofac Implants. 2002;17:816-819.25. Ellegaard B, Baelum V, Karring T.Implant therapy in periodontally compromised patients. Clin Oral Implants Res.1997;8:180-188.26. Nevins M, Langer B. The successful use of osseointegrated implants for thetreatment of the recalcitrant periodontalpatient. J Periodontol. 1995;66:150-157.27. Van der Weijden GA, van BemmelKM, Renvert S. Implant therapy in partiallyedentulous, periodontally compromisedpatients: A review. J Clin Periodontol.2005;32:506-511.28. Proceedings of the 1996 WorldWorkshop in Periodontics. Lansdowne,Virginia, July 13–17, 1996. Ann Periodontol. 1996;1:816-820.29. Blanchaert RH. Implants in themedically challenged patient. Dent ClinNorth Am. 1998;42:35-45.30. Beikler T, Flemmig TF. Impla

supportive programs for implant pa-tients and that there is an urgent need for such studies to be initiated. This report clearly illustrates that there is an important role for regular continuous supportive periodontal therapy in im-plant patients to increase implant survival over time. In the treatment strategies for periodontitis, the need