ORIGINAL CONTRIBUTIONS
CRITICAL SUMMARIES
Limited evidence suggests higher risk of dental implant failures in smokers than in nonsmokers A critical summary of Chrcanovic BR, Albrektsson T, Wennerberg A. Smoking and dental implants: a systematic review and meta-analysis. J Dent. 2015;43(5):487-498. Linda L. Cheng, DDS, FAGD, ABGD
Systematic review conclusion. Within the limits of the existing evidence, smokers who undergo dental implant placement may be at a statistically significant increased risk of experiencing implant failure, postoperative infection, and greater marginal bone loss than are nonsmokers. Critical summary assessment. Results from this systematic review of 107 randomized and nonrandomized studies with numerous confounding factors suggest that smokers may be more susceptible to implant loss, postoperative infections, and bone loss than are nonsmokers. Evidence quality rating. Limited.
Clinical question. In patients undergoing implant placement, are patients who smoke versus those who do not at higher risk of experiencing implant failure, postoperative infection, and greater marginal bone loss? Review methods. In September 2014, the reviewers searched, with no time or language restrictions, in 3 databases; manually searched 19 dental implant-related journals; and searched 3 online databases for ongoing clinical trials. They checked the reference lists of identified studies and relevant reviews for additional articles. They included all randomized or nonrandomized clinical human studies that provided outcome data for dental implant failure in smokers and nonsmokers with no follow-up restrictions in any group of patients of any age, race, or sex. In this systematic review, the reviewers defined smokers as patients who smoked a minimum of 1 cigarette per day and implant failure as the
complete loss of the implant. They excluded all case reports, technical reports, biomechanical studies, finite element analysis studies, animal studies, in vitro studies, and review articles. The reviewers assessed the outcomes for implant failure, postoperative infection, and marginal bone loss. All 3 reviewers independently screened titles and abstracts, resolved disagreements through discussions, and contacted authors for missing data. One reviewer performed data extraction. The reviewers assessed the quality of the studies1 and conducted the systematic review and meta-analyses according to accepted guidelines.2 Main results. A total of 107 studies were included—4 randomized clinical trials, 16 controlled clinical trials, 16 prospective studies, and 71 retrospective analyses. In 104 of the 107 studies in which the authors reported implant failure rates for smokers and nonsmokers separately, 19,836 dental implants were
placed in smokers, with 1,259 failures (6.35%), and 60,464 implants were placed in nonsmokers, with 1,923 failures (3.18%). Smokers experienced higher rates of implant failure (risk ratio [RR], 2.23; 95% confidence interval [CI], 1.96-2.53; P < .00001; heterogeneity, I2 ¼ 51%; P < .00001), more postoperative infections (RR, 2.01; 95% CI, 1.09-3.72; P ¼ .03; heterogeneity, I2 ¼ 0%; P ¼ .63), and more periimplant bone loss (mean difference, 0.32 mm; 95% CI, 0.21-0.43; heterogeneity, I2 ¼ 95%; P < .00001) than did nonsmokers. Conclusions. Within the limitations of the available evidence, patients who smoke may be at twice the risk of experiencing dental implant failure and postoperative infections than are patients who do not smoke. Smokers had more statistically significant marginal bone loss than did nonsmokers. This systematic review was supported by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico, Brasília, Brazil.
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ORIGINAL CONTRIBUTIONS
COMMENTARY Importance and context. Smokers have a higher prevalence of moderate to severe periodontitis and a higher number of missing teeth than do nonsmokers.3 One theory about how smoking may delay or inhibit bone healing after surgery is that the nicotine in tobacco may affect the function of immune cells and constrict the blood vessels and blood flow that carry oxygen and nutrients needed for bone formation and remodeling around dental implants.4-11 The authors of this systematic review investigated the effects of smoking on implant failure rates and postoperative complications. Strengths and weaknesses of the systematic review. The authors of the systematic review had an extensive search strategy. They contacted authors for missing information but did not search for gray literature or contact content experts. The systematic review authors used fixed and random effects models according to the homogeneity or consistency of the evidence available. Although results from the sensitivity analyses suggest that smoking was associated with more failures regardless of the type of implant surface and that smoking may affect implant survival significantly in the maxilla, the reviewers were careful to point out that the results may be biased heavily because these studies may not have been designed to show these effects. The reviewers acknowledged that the unit of analysis was at the implant level instead of the patient level, which technically does not adjust for clustered, correlated observations.12 Only 1 reviewer performed the data extraction, which may be a source of bias. Strengths and weaknesses of the evidence. Most of the studies were retrospective analyses that relied on the accuracy of the original examination and may have been incomplete regarding certain information. Eightyfive studies were of high quality, and 22 were of moderate quality.1 For implant failures, funnel plots suggested no publication bias was present. Most studies had small sample sizes, short follow-ups, and low specificity for smoking’s effects on dental implants. Follow-ups varied from 3 months to 22 years. The findings of 15 studies on postoperative infections were consistent (P ¼ .63; heterogeneity, I2 ¼ 0%). The findings for implant failures among smokers and nonsmokers had moderate heterogeneity (P < .00001; heterogeneity, I2 ¼ 51%). The meta-analysis of 18 studies on marginal bone loss had significant heterogeneity (P < .00001; heterogeneity, I2 ¼ 95%). The amount of bone loss in smokers as compared with that in nonsmokers was statistically greater but not necessarily clinically significant (MD, 0.32 mm; 95% CI,
2 JADA
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0.21-0.43; P < .00001). Except for postoperative infections, no patient-oriented outcomes were assessed. Not all the study investigators reported the number of implants that were placed and that survived or were lost in different conditions, the criteria of classifying patients as smokers or nonsmokers, the quantity of cigarettes smoked per day, or the number of years the patients smoked. Some confounding variables included the use of grafting, different brands and surface treatments, immediate implant placement, implants placed in different sites, different healing periods, various prosthetic restorations, types of opposing dentition, different implant angulations, splinting of implants, use of antimicrobial agents, and the presence of bruxism or diabetes. Implications for dental practice. As part of informed consent, practitioners should make patients aware that the risk of experiencing implant failure and postoperative infections for smokers may be twice that for nonsmokers. This review, with its substantial limitations, suggests that smokers have higher implant failure rates, greater marginal bone loss, and higher incidences of postoperative infections than do nonsmokers. More well-conducted research is needed to account for the numerous confounding factors identified in this review and to assess the dose-related effect and size of the effect of smoking.13 In the future, smoking control and cessation may become an increasing part of risk management in implant therapy. n http://dx.doi.org/10.1016/j.adaj.2016.01.003 Copyright ª 2016 American Dental Association. All rights reserved.
Dr. Cheng is a clinical assistant professor, Department of General Dentistry, Texas A&M University Baylor College of Dentistry, 3302 Gaston Ave., Dallas, TX 75246, e-mail [email protected]. Address correspondence to Dr. Cheng. Disclosure. Dr. Cheng did not report any disclosures. These summaries, published under the auspices of the American Dental Association Center for Evidence-Based Dentistry, are prepared by practitioners trained in critical appraisal of published systematic reviews who work under the mentorship of experts. The summaries are not intended to, and do not, express, imply, or summarize standards of care, but rather provide a concise reference for dentists to aid in understanding and applying evidence from the referenced systematic review in making clinically sound decisions as guided by their clinical judgment and by patient needs. For more information on the evidence quality rating provided above and additional critical summaries, please visit http://ebd.ada.org. 1. Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical_ epidemiology/oxford.asp. Accessed July 31, 2015.
ORIGINAL CONTRIBUTIONS
2. Moher D, Liberati A, Tetzlaff J, Altman DG; the PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264-269. 3. Albandar JM, Streckfus CF, Adesanya MR, Winn DM. Cigar, pipe, and cigarette smoking as risk factors for periodontal disease and tooth loss. J Periodontol. 2000;71(12):1874-1881. 4. MacFarlane GD, Hetzberg MC, Wolff L, Hardie NA. Refractory periodontitis associated with abnormal PMN leukocyte phagocytosis and cigarette smoking. J Periodontol. 1992;63(11):908-913. 5. Kwiatkowski TC, Hanley EN Jr, Ramp WK. Cigarette smoking and its orthopedic consequences. Am J Orthop. 1996;25(9):590-597. 6. Scolaro JA, Schenker ML, Yannascoli S, Baldwin K, Mehta S, Ahn J. Cigarette smoking increases complications following fracture: a systemic review. J Bone Joint Surg Am. 2014;96(8):674-681. 7. Palmer RM, Wilson RF, Hasan AS, Scott DA. Mechanisms of action of environmental factors: tobacco smoking. J Clin Periodontol. 2005; 32(suppl 6):180-195.
8. Patel RA, Wilson RF, Palmer RM. The effect of smoking on periodontal bone regeneration: a systematic review and meta-analysis. J Periodontol. 2012;83(2):143-155. 9. Ma L, Zheng LW, Sham MH, Cheung LK. Uncoupled angiogenesis and osteogenesis in nicotine-compromised bone healing. J Bone Miner Res. 2010;25(6):1305-1313. 10. Wang Y, Wan C, Deng L, et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest. 2007;117(6):1616-1626. 11. Fleming JT, Barati MT, Beck DJ, et al. Bone blood flow and vascular reactivity. Cells Tissues Organs. 2001;169(3):279-284. 12. Fleming PS, Koletsi D, Polychronopoulou A, Eliades T, Pandis N. Are clustering effects accounted for in statistical analysis in leading dental specialty journals? J Dent. 2013;41(3):265-270. 13. Moraschini V, Barboza ED. Success of dental implants in smokers and non-smokers: a systematic review and meta-analysis. Int J Oral Maxillofac Surg. 2016;45(2):205-215.
JADA
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http://jada.ada.org
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2016 3
CRITICAL SUMMARIES
Limited evidence suggests higher risk of dental implant failures in smokers than in nonsmokers A critical summary of Chrcanovic BR, Albrektsson T, Wennerberg A. Smoking and dental implants: a systematic review and meta-analysis. J Dent. 2015;43(5):487-498. Linda L. Cheng, DDS, FAGD, ABGD
Systematic review conclusion. Within the limits of the existing evidence, smokers who undergo dental implant placement may be at a statistically significant increased risk of experiencing implant failure, postoperative infection, and greater marginal bone loss than are nonsmokers. Critical summary assessment. Results from this systematic review of 107 randomized and nonrandomized studies with numerous confounding factors suggest that smokers may be more susceptible to implant loss, postoperative infections, and bone loss than are nonsmokers. Evidence quality rating. Limited.
Clinical question. In patients undergoing implant placement, are patients who smoke versus those who do not at higher risk of experiencing implant failure, postoperative infection, and greater marginal bone loss? Review methods. In September 2014, the reviewers searched, with no time or language restrictions, in 3 databases; manually searched 19 dental implant-related journals; and searched 3 online databases for ongoing clinical trials. They checked the reference lists of identified studies and relevant reviews for additional articles. They included all randomized or nonrandomized clinical human studies that provided outcome data for dental implant failure in smokers and nonsmokers with no follow-up restrictions in any group of patients of any age, race, or sex. In this systematic review, the reviewers defined smokers as patients who smoked a minimum of 1 cigarette per day and implant failure as the
complete loss of the implant. They excluded all case reports, technical reports, biomechanical studies, finite element analysis studies, animal studies, in vitro studies, and review articles. The reviewers assessed the outcomes for implant failure, postoperative infection, and marginal bone loss. All 3 reviewers independently screened titles and abstracts, resolved disagreements through discussions, and contacted authors for missing data. One reviewer performed data extraction. The reviewers assessed the quality of the studies1 and conducted the systematic review and meta-analyses according to accepted guidelines.2 Main results. A total of 107 studies were included—4 randomized clinical trials, 16 controlled clinical trials, 16 prospective studies, and 71 retrospective analyses. In 104 of the 107 studies in which the authors reported implant failure rates for smokers and nonsmokers separately, 19,836 dental implants were
placed in smokers, with 1,259 failures (6.35%), and 60,464 implants were placed in nonsmokers, with 1,923 failures (3.18%). Smokers experienced higher rates of implant failure (risk ratio [RR], 2.23; 95% confidence interval [CI], 1.96-2.53; P < .00001; heterogeneity, I2 ¼ 51%; P < .00001), more postoperative infections (RR, 2.01; 95% CI, 1.09-3.72; P ¼ .03; heterogeneity, I2 ¼ 0%; P ¼ .63), and more periimplant bone loss (mean difference, 0.32 mm; 95% CI, 0.21-0.43; heterogeneity, I2 ¼ 95%; P < .00001) than did nonsmokers. Conclusions. Within the limitations of the available evidence, patients who smoke may be at twice the risk of experiencing dental implant failure and postoperative infections than are patients who do not smoke. Smokers had more statistically significant marginal bone loss than did nonsmokers. This systematic review was supported by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico, Brasília, Brazil.
JADA
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http://jada.ada.org
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2016 1
ORIGINAL CONTRIBUTIONS
COMMENTARY Importance and context. Smokers have a higher prevalence of moderate to severe periodontitis and a higher number of missing teeth than do nonsmokers.3 One theory about how smoking may delay or inhibit bone healing after surgery is that the nicotine in tobacco may affect the function of immune cells and constrict the blood vessels and blood flow that carry oxygen and nutrients needed for bone formation and remodeling around dental implants.4-11 The authors of this systematic review investigated the effects of smoking on implant failure rates and postoperative complications. Strengths and weaknesses of the systematic review. The authors of the systematic review had an extensive search strategy. They contacted authors for missing information but did not search for gray literature or contact content experts. The systematic review authors used fixed and random effects models according to the homogeneity or consistency of the evidence available. Although results from the sensitivity analyses suggest that smoking was associated with more failures regardless of the type of implant surface and that smoking may affect implant survival significantly in the maxilla, the reviewers were careful to point out that the results may be biased heavily because these studies may not have been designed to show these effects. The reviewers acknowledged that the unit of analysis was at the implant level instead of the patient level, which technically does not adjust for clustered, correlated observations.12 Only 1 reviewer performed the data extraction, which may be a source of bias. Strengths and weaknesses of the evidence. Most of the studies were retrospective analyses that relied on the accuracy of the original examination and may have been incomplete regarding certain information. Eightyfive studies were of high quality, and 22 were of moderate quality.1 For implant failures, funnel plots suggested no publication bias was present. Most studies had small sample sizes, short follow-ups, and low specificity for smoking’s effects on dental implants. Follow-ups varied from 3 months to 22 years. The findings of 15 studies on postoperative infections were consistent (P ¼ .63; heterogeneity, I2 ¼ 0%). The findings for implant failures among smokers and nonsmokers had moderate heterogeneity (P < .00001; heterogeneity, I2 ¼ 51%). The meta-analysis of 18 studies on marginal bone loss had significant heterogeneity (P < .00001; heterogeneity, I2 ¼ 95%). The amount of bone loss in smokers as compared with that in nonsmokers was statistically greater but not necessarily clinically significant (MD, 0.32 mm; 95% CI,
2 JADA
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http://jada.ada.org
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2016
0.21-0.43; P < .00001). Except for postoperative infections, no patient-oriented outcomes were assessed. Not all the study investigators reported the number of implants that were placed and that survived or were lost in different conditions, the criteria of classifying patients as smokers or nonsmokers, the quantity of cigarettes smoked per day, or the number of years the patients smoked. Some confounding variables included the use of grafting, different brands and surface treatments, immediate implant placement, implants placed in different sites, different healing periods, various prosthetic restorations, types of opposing dentition, different implant angulations, splinting of implants, use of antimicrobial agents, and the presence of bruxism or diabetes. Implications for dental practice. As part of informed consent, practitioners should make patients aware that the risk of experiencing implant failure and postoperative infections for smokers may be twice that for nonsmokers. This review, with its substantial limitations, suggests that smokers have higher implant failure rates, greater marginal bone loss, and higher incidences of postoperative infections than do nonsmokers. More well-conducted research is needed to account for the numerous confounding factors identified in this review and to assess the dose-related effect and size of the effect of smoking.13 In the future, smoking control and cessation may become an increasing part of risk management in implant therapy. n http://dx.doi.org/10.1016/j.adaj.2016.01.003 Copyright ª 2016 American Dental Association. All rights reserved.
Dr. Cheng is a clinical assistant professor, Department of General Dentistry, Texas A&M University Baylor College of Dentistry, 3302 Gaston Ave., Dallas, TX 75246, e-mail [email protected]. Address correspondence to Dr. Cheng. Disclosure. Dr. Cheng did not report any disclosures. These summaries, published under the auspices of the American Dental Association Center for Evidence-Based Dentistry, are prepared by practitioners trained in critical appraisal of published systematic reviews who work under the mentorship of experts. The summaries are not intended to, and do not, express, imply, or summarize standards of care, but rather provide a concise reference for dentists to aid in understanding and applying evidence from the referenced systematic review in making clinically sound decisions as guided by their clinical judgment and by patient needs. For more information on the evidence quality rating provided above and additional critical summaries, please visit http://ebd.ada.org. 1. Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical_ epidemiology/oxford.asp. Accessed July 31, 2015.
ORIGINAL CONTRIBUTIONS
2. Moher D, Liberati A, Tetzlaff J, Altman DG; the PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264-269. 3. Albandar JM, Streckfus CF, Adesanya MR, Winn DM. Cigar, pipe, and cigarette smoking as risk factors for periodontal disease and tooth loss. J Periodontol. 2000;71(12):1874-1881. 4. MacFarlane GD, Hetzberg MC, Wolff L, Hardie NA. Refractory periodontitis associated with abnormal PMN leukocyte phagocytosis and cigarette smoking. J Periodontol. 1992;63(11):908-913. 5. Kwiatkowski TC, Hanley EN Jr, Ramp WK. Cigarette smoking and its orthopedic consequences. Am J Orthop. 1996;25(9):590-597. 6. Scolaro JA, Schenker ML, Yannascoli S, Baldwin K, Mehta S, Ahn J. Cigarette smoking increases complications following fracture: a systemic review. J Bone Joint Surg Am. 2014;96(8):674-681. 7. Palmer RM, Wilson RF, Hasan AS, Scott DA. Mechanisms of action of environmental factors: tobacco smoking. J Clin Periodontol. 2005; 32(suppl 6):180-195.
8. Patel RA, Wilson RF, Palmer RM. The effect of smoking on periodontal bone regeneration: a systematic review and meta-analysis. J Periodontol. 2012;83(2):143-155. 9. Ma L, Zheng LW, Sham MH, Cheung LK. Uncoupled angiogenesis and osteogenesis in nicotine-compromised bone healing. J Bone Miner Res. 2010;25(6):1305-1313. 10. Wang Y, Wan C, Deng L, et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest. 2007;117(6):1616-1626. 11. Fleming JT, Barati MT, Beck DJ, et al. Bone blood flow and vascular reactivity. Cells Tissues Organs. 2001;169(3):279-284. 12. Fleming PS, Koletsi D, Polychronopoulou A, Eliades T, Pandis N. Are clustering effects accounted for in statistical analysis in leading dental specialty journals? J Dent. 2013;41(3):265-270. 13. Moraschini V, Barboza ED. Success of dental implants in smokers and non-smokers: a systematic review and meta-analysis. Int J Oral Maxillofac Surg. 2016;45(2):205-215.
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