The use of osseointegrated implants as a foundation for the prosthetic replacement
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- Ethelbert Russell
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1 The Association Between the Failure of Dental Implants and Cigarette Smoking Crawford A. Bain, BDS, DDS, MSEd/Peter K. Moy, BSc, DMD This paper reviews the outcome of 2,194 Brånemark implants placed in 540 patients by one of the authors over a 6-year period. The overall failure rate of 5.92% is consistent with other studies; however, when patients were subdivided into smokers and nonsmokers, it was found that a significantly greater percentage of failures occurred in smokers (11.28%) than in nonsmokers (4.76%) (P <.001). These differences were significant for all areas except the posterior mandible. While failure rates decreased with increasing implant length, failure rates for each implant length were consistently higher in smokers than in nonsmokers. The possible mechanisms of failure in smokers are discussed, and a protocol for cessation of smoking around the time of surgery is proposed. (INT J ORAL MAXILLOFAC IMPLANTS 1993;8: ) Key words: Brånemark implants, failure, implant length, implant location, osseointegration, smoking/adverse effects The use of osseointegrated implants as a foundation for the prosthetic replacement of missing teeth has become widespread in the last decade. By the use of a gentle surgical technique in sterile conditions, a healing period free of loading, and the development of macroretentive commercially pure titanium implants, a predictable level of success in the integration of implants with bone has been achieved. Since 1977, several retrospective studies have reviewed success rates of both individual implants and implant-supported prostheses, initially in completely edentulous and more recently in partially edentulous patients.1-12 While these studies present large sample sizes and important data on longer-term implant success, they have generally focused on the high levels of success and spent little time analyzing factors involved in the failures that occurred. Although the 5- to 9-year success rates of Adell et al2 are impressive and widely quoted, the authors offer little discussion on the much higher failure rates in the first 5 years of the study. Similarly, van Steenberghe and coworkers' multi-centered study of partially edentulous patients mentions two patients who lost all seven implants placed, but these were not included in the statistical analysis because of incomplete data.9 Several case reports identify patients who have lost an above-average number of implants9,13,14; but in general, retrospective studies have focused on success rates. A notable exception is Jaffin and Berman's paper,15 which identified a much higher failure rate in type IV bone than in all other bone types. Our own unpublished data
2 confirm this, though our failure rate in type IV bone (13.51%) was somewhat lower. Most surgical technique publications identify various local anatomic factors, as well as a few general systemic conditions, that may decrease the possibility of successful integration. Commonly, poor bone quality and quantity, as well as proximity to vital structures, are cited as negative factors. Uncontrolled diabetes, blood dyscrasias, osteoporosis, alcoholism, psychiatric conditions, high levels of head and neck radiotherapy, and general surgical contraindications are among factors that may systemically decrease the potential for implant success Few, if any, studies exist that show a lower implant success rate when patients are treated in the presence of such systemic factors. Smoking has long been identified as harmful to general health. Smokers have a much higher incidence of lung cancer and cardiovascular diseases, together with several other conditions.19 In both animal and human studies, it has repeatedly been shown that smoking compromises healing potential in the treatment of duodenal ulcers,20 plastic surgery21,22 and vascular surgery.23 In the dental field, Meeghan et al24 identified smoking as a major predisposing factor in the occurrence of painful sockets after tooth extraction. They showed that blood fill in postoperative sockets was significantly reduced in smokers, and that maxillary sockets filled more poorly than those in the mandible. Smoking has also been associated with poorer healing after mucogingival surgery25 and is associated with higher rates of refractory periodontitis.26 Cryer et al27 demonstrated an increase in serum levels of norepinephrine and epinephrine in smokers, while Mosely et al28 showed that nicotine inhibited wound healing in a rabbit ear model. Clarke et al29 showed a severe reduction in gingival circulation in rabbits exposed to intra-arterial nicotine. The direct cutaneous vasoconstrictive action of nicotine; increased platelet aggregation; increased levels of fibrinogen, hemoglobin, and blood viscosity; excess levels of carboxyhemoglobin in blood; compromised polymorphonuclear neutrophil (PMN) leukocyte function 30,31; as well as increased platelet adhesiveness have also been hypothesized as mechanisms by which smoking compromises wound healing.32,33 To date, no evaluation has been made of the outcome of dental implants placed in smokers as compared with nonsmokers. The purpose of this study was to evaluate the influence of smoking on the failure rate of Brånemark dental implants placed by one of the authors (PKM) over a period of 6 years. Materials and Methods A total of 2,194 Brånemark implants (Nobelpharma USA, Chicago) were placed in 540 patients between 1984 and These included completely and partially edentulous arches, as well as single-tooth replacements. Both fixed and removable (overdenture) prostheses were included. The patient population consisted of 311 women (57.6%) and 229 men (42.4%).
3 After a complete medical and dental history, thorough clinical and radiographic evaluations including, as indicated, periapical, panoramic, conventional, and computerized tomographic films; diagnostic casts; and consultation with the restorative dentist were carried out. Patients were presented with treatment options and advised of the potential problems associated with dental implants, and an informed consent form was signed. Patients were not accepted for implant surgery if they were medically contraindicated for elective surgery or had unrealistic expectations. All implants were placed under sterile conditions, following the Brånemark protocol, which has been described elsewhere.34 After the appropriate healing period, the implants were exposed, abutments were connected, and patients became involved in the prosthetic stage of therapy. To be included in this study, patients completed abutment connection by March 31, 1991, and postabutment connection radiographs had to be available. These were generally panoramic radiographs or, on occasion, periapical radiographs. All patient records, histories, and radiographs were reviewed; all implant locations were recorded appropriately as posterior maxilla, anterior maxilla, posterior mandible, or anterior mandible; and all implant failures were recorded. While the criteria for failure outlined by Albrektsson et al35 were considered to be optimal, it was not feasible to assess mobility in a study based on radiographic and chart review. Accordingly, an implant was considered to be a failure when: 1. It had been removed for any reason. 2. Radiographic bone loss in excess of 50% of the fixture length was seen on nonstandardized post-treatment radiographs. These criteria may preclude identifying some failing implants according to the Albrektsson et al criteria35; however, they are considered to be realistic and practical in identifying unambiguous implant failure in a chart-review-based study. As part of their medical history, patients were asked whether they smoked. This information was assessed in relation to the success or failure of each implant, and a failure rate was established for both smoking and nonsmoking groups. No attempt was made to quantify the smoking, since this information could be considered unreliable. Data were assessed in relation to location (by sextant) and to implant length. Since bone quality was only recorded routinely after 1985, it was not evaluated in this study. A computerized chi square test was used to compare the two groups by whole mouth and by sextant. Assessment was by individual implant, rather than by patient, since implants placed in each patient were often of various lengths and placed in sites of differing bone quality.
4 Results A total of 2,194 implants in 540 patients met the inclusion criteria for the study. Of these, 1,255 implants were placed in 311 female patients and 939 implants in 229 male patients. The average age of the female patients was years (range 12 to 86) and of the male patients years (range 15 to 84). There was no significant difference between the mean ages of males and females, nor between the number of implants per patient placed in each group. No difference was found in the age, gender, number of implants per patient, or average implant length between smoking and nonsmoking groups. The time following stage 2 surgery ranged from 1 to 81 months, with a mean of months (36.59 months in smokers and months in nonsmokers). Based on the criteria for failure outlined above, 130 of the 2,194 implants were classified as failures. An additional 23 implants remained buried and were classified as "sleepers." Thus the overall failure rate was 5.92% (excluding "sleepers"), which is consistent with other studies. When patients were divided into smoking and nonsmoking groups, it was found that 390 implants (17.78%) had been placed in smokers and 1,804 implants (82.22%) in nonsmokers. Of the 390 implants placed in smokers, 44 were classified as failures (a failure rate of 11.28%), while of the 1,804 implants placed in nonsmokers, only 86 implants failed (a failure rate of 4.76%). There was a statistically significant difference between the failure rate in the smoking and nonsmoking groups (P <.001). Analysis of the different regions of the mouth revealed that overall failure rates were highest in the posterior maxilla and lowest in the anterior mandible (Table 1). Smokers had higher failure rates in all regions. Only in the posterior mandible was there no significant difference between smokers and nonsmokers (Table 2). The 23 "sleeping" implants were all radiographically healthy and were distributed between smokers (7) and nonsmokers (16). If these were included in the overall failure rate, it increased to 6.97%. Since they all appeared to be integrated from the radiographic perspective and were left unconnected for either positional, esthetic, or psychological reasons, it was felt inappropriate to include them as "failures" when assessing the individual groups. When fixture length was considered, it was found that in the maxilla, failure rates of shorter implants in smokers were extremely high and in several cases exceeded the 25% rate, which is Albrektsson et al's proposal for a maximum acceptable level of failure (Tables 3 to 6). Discussion The findings of this study for the first time identify smoking as a major factor in implant failure. This is not surprising when one considers other areas of the medical 36
5 and dental literature. Smoking has been identified by Battalia et al36 as the most important risk factor for both nonhealing (P =.04) and recurrence (P =.0025) of gastric ulcers. Mosely and Finseth37 found that when arteriosclerotic patients continued to smoke, healing of hand wounds was impaired. They further suggest that this impaired healing is also found in smokers without arteriosclerosis.28 Siana et al 38 found unsatisfactory scarring after gynecological surgery in 14 of 69 smokers and 0 of 51 nonsmokers (P <.002). In the area of microvascular surgery, Herring et al23 showed a much higher deterioration in both Dacron arterial grafts (P=.008) and vein grafts when the patients were smokers. In the plastic surgery literature, Rees et al39 reported a higher rate of skin slough after rhytidectomy in smokers, while Riefkohl et al21 identified an association between cutaneous occlusive vascular disease, cigarette smoking, and skin slough after rhytidectomy. In the dental literature, smoking has been shown to compromise healing after mucogingival surgery,40 and to be associated with greater pocket depth and loss of attachment when age-matched groups of smokers and nonsmokers were compared.41 Preber42 showed a significantly greater reduction in pocket depth after scaling and curettage in nonsmokers than in smokers. Smoking has also been associated with a higher incidence of refractory periodontitis,26 with significant reductions in postextraction sockets filling with blood (P <.01) and with a higher incidence of painful sockets (P <.02).24 As to the actual mechanism of implant failure associated with smoking, a retrospective clinical study can only offer conjecture. Cryer et al27 demonstrated a significant increase in plasma levels of both norepinephrine (P <.01) and epinephrine (P <.05) immediately after 10 minutes of smoking, which persisted for the remaining 20 minutes of the study. Sarin et al43 also showed that smoking a single cigarette reduced the velocity of blood flow to the fingers by over 40% for up to 1 hour. Although nicotine has been shown to cause increased urinary catecholamine excretion in laboratory animals,44 it should also be noted that urinary epinephrine excretion also increased after smoking of nicotine-free cigarettes,45 suggesting an additional influence of other byproducts and/or tars. It has also been shown that smokers have a compromised PMN function when compared with nonsmokers,26,30,31 which may be responsible for a compromised healing response and/or a higher risk of infection in smokers after implant placement. While the systemic vasoconstrictive effect andlor PMN dysfunction induced by smoking may well influence initial wound healing adjacent to newly placed implants, Shuler,46 and Armitage and Turner47 showed that nicotine also had a localized vasoconstrictive effect by being absorbed through the oral mucosa into the blood vessels during smoking. Thus the dental implant may be doubly at risk. If local absorption was a significant factor it could well account for lower failures in smokers in the posterior mandible, which is the area most remote and protected by the tongue from local influences of smoking. This hypothesis is currently being
6 investigated by comparison of the failure rates described in this study with failure rates in extraoral sites of osseointegrated implants in smokers and nonsmokers,25 and if validated, may give some encouragement for smokers who use a nicotine patch around the time of implant placement. If one accepts that smoking has a detrimental effect on implant prognosis, the next logical question is how long the potential implant patient who smokes will have to abstain to have an equal prognosis with the nonsmoker. To establish this with any certainty, a future prospective study will be necessary. However, it may well be feasible to first confirm that smoking is equally detrimental in an animal model system, then evaluate the effects of different periods of abstinence on implant prognosis. A method similar to Brånemark's original vital microscopic studies48 of vascular function might also be useful for evaluating the effects of smoking on the microvascular system adjacent to an integrating implant in an animal model. This could establish whether vasoconstriction and/or platelet aggregation in the proximity of the implant were influenced by smoking. In the absence of any directly related dental literature, one is left to extrapolate guidelines for smoking abstinence from medicine. Webster et al22 suggest that patients cease smoking for several weeks before and at least 2 weeks after plastic surgery, while in the same discipline Kaye49 advises abstinence 2 weeks before and 1 week after surgery. Riefkohl et al21 suggest that cessation from the day before until 5 days after plastic surgery will allow nicotine clearance and an elimination of increased vasoconstriction, as well as a resolution of any carboxyhemoglobin-induced hypoxia. They feel that 5 days postoperatively will be sufficient to allow flap revascularization. All of these recommendations relate to soft tissue healing and are essentially untested in any prospective study. It seems likely that the longer time frame associated with osseous healing and the osseointegration process would require a longer period of abstinence. In the absence of any research-based data, we would suggest that the patient cease smoking at least 1 week prior to surgery to allow reversal of higher levels of platelet adhesion and blood viscosity, as well as the shorter-term effects associated with nicotine. The patient should continue to avoid tobacco for at least 2 months after implant placement, by which time bony healing will have progressed to the osteoblastic phase, and early osseointegration should be established. It is realized that this period will be perceived by some as unrealistic as far as compliance is concerned; however, it has a biologic rationale. When informed consent is obtained, careful clarification of the harmful effects of smoking, together with an establishment of the patient's responsibilities in achieving the best prognosis, will ensure the best obtainable level of compliance as well as cover the clinician in the event of implant failure in a noncompliant patient. These recommendations, while based on a sound biologic rationale, are as yet not substantiated by clinical research data. While this study establishes smoking as a significant factor in the failure of
7 dental implants, it would be naive to assume that it is either the only or the most significant factor. Further research is necessary to identify other possible factors that contribute to failure, as well as the possible relationship of the coexistence of several factors in the same individual. Once these factors have been identified, it may then be feasible to use multiple regression analysis to develop a formula whereby a more meaningful, customized prognosis is established for each patient. It is hoped that second-generation clinical research in implant dentistry will focus more on identifying causes for failure than on presenting high success rates, manipulated by creative statistical analysis to present the various systems in the best possible light. It is a well-worn truism that more is learned from failures than successes, and it appears likely that the selection of one implant system over another has less potential to increase success rates than does careful and comprehensive patient selection based on a clear understanding of factors that have been shown to contribute to implant failure. This, combined with an honest presentation of the individual patient's prognosis based on evaluation of the pertinent factors, can only enhance overall success and patient satisfaction. Conclusions This study identifies smoking as a significant factor in increasing the potential failure rate of dental implants. The overall failure rate of 5.92% is consistent with other reported studies. This study further identifies that implant success is poorest in the posterior maxilla and best in the anterior mandible. In all areas except the posterior mandible, the failure rate in smokers was significantly higher than in nonsmokers. When implant length was considered, smokers had consistently higher failure rates than nonsmokers. The maxillary failure rates for shorter implants in smokers exceeded previously proposed acceptable levels. To date, no clear evidence exists as to the mechanism whereby smoking contributes to the failure of dental implants. This paper identifies potential areas of future research to investigate this mechanism and recommends a cessation protocol that, though based on a sound biologic rationale, requires experimental verification in a prospective study. More research is also necessary into other factors that contribute to implant failure, and to potential interrelationships where more than one factor is present in any given patient.
8 1. Brånemark P-I, Hansson BO, Adell R, Breine U, Lindstrom J, Hallen O, Ohman A. Osseointegrated implants in the treatment of the edentulous jaw. Scand J Plast Reconstr Surg 1977;11(suppl 16). 2. Adell R, Lekholm U, Rockler B, Brånemark P-I. A 15-year study of osseointegrated implants in the treatment of the edentuous jaw. Int J Oral Surg 1981;l0: Adell R, Eriksson B, Lekholm U, Brånemark P-I, Jemt T. A long-term follow-up study of osseointegrated implants in the treatment of totally edentuous jaws. Int J Oral Maxillofac Implants 1990;5: Albrektsson T, Dahl E, Enbom L, Engevall S, Engquist B, Eriksson AR, et al. A Swedish multi-centered study of 8139 consecutively inserted Nobelpharma implants. J Periodontol 1988;59: Albrektsson T. A multi-centered report on osseointegrated oral implants. J Prosthet Dent 1988;60: Zarb G, Schmitt A. The longitudinal clinical effectiveness of osseointegrated dental implants: The Toronto study, Part 1. Surgical results. J Prosthet Dent 1990;63: Zarb G, Schmitt A. The longitudinal clinical effectiveness of osseointegrated dental implants: The Toronto study, Part 2. The prosthetic results. J Prosthet Dent 1990;64: Buser DA, Schroeder A, Sutter F, Lang NP. The new concept of ITI hollow-cylinder screw implants: Part 2. Clinical aspects, indications and early clinical results. Int J Oral Maxillofac Implants 1988;3: Kirsch A, Ackerman KL. The IMZ osseointegrated implant system. Dent Clin North Am 1989;33: Patrick D, Zosky J, Lubar R, Buchs A. The longitudinal clinical effectiveness of Core-Vent dental implants. A 5 year report. J Oral Implantol 1989;15: Kent JN, Block MS, Finger IM, Guerra L, Larsen H, Misiek DJ. Biointegrated hydroxyapatite-coated dental implants: 5 year clinical observations. J Am Dent Assoc 1990;121: van Steenberghe D. A retrospective multicenter evaluation of survival rate of osseointegrated implant fixtures supporting fixed partial prostheses in the treatment of partial edentulism. J Prosthet Dent 1989;61: Engquist B, Bergendal T, Kallus T, Linden U. A retrospective multicenter evaluation of osseointegrated implants supporting overdentures. Int J Oral Maxillofac Implants 1988;3:
9 14. Malmstrom HS, Fritz ME, Timmis DP, VanDyke TE. Osseo-integrated implant treatment of a patient with rapidly progressive periodontitis. J Periodontol 1990;61: Jaffin RA, Bemlan CL. The excessive loss of Brånemark fixtures in type IV bone. J Periodontol 1991;62: Laney WR. Selecting edentulous patients for tissue-integrated prostheses. Int J Oral Maxillofac Implants 1986;1: Lekholm U, Zarb GA. Patient selection and preparation. In: Brånemark P-I, Zarb GA, Albrektsson T (eds). Tissue-lntegrated Prostheses: Osseointegration in Clinical Dentistry. Chicago: Quintessence, 1987: Beumer J III, Lewis SG. Patient selection and treatment planning. In: Beumer J III, Lewis SG (eds). The Brånemark Implant System: Clinical and Laboratory Procedures. St Louis: Ishiyaku EuroAmerica, 1989: Ball K, Turner R. Smoking and the heart; the basis for action. Lancet 1974;2: Kikendahl JW, Evaul J, Johnson LF. Effects of cigarette smoking on gastrointestinal physiology and non-neoplastic digestive disease. J Clin Gastroenterol 1984;6: Riefkohl R, Wolfe JA, Cox EB, McCarthy KS Jr. Association between cutaneous occlusive vascular disease, cigarette smoking and skin sloughing after rhytidectomy. Plast Reconstr Surg 1986;77: Webster RC, Kazda G, Hamdan US, Fuleihan NS, Smith RC. Cigarette smoking and facelift: Conservative vs. wide undenmining. Plast Reconstr Surg 1986;77: Herring M, Gardener A, Glover J Seeding human arterial prostheses with mechanically derived endothelium The detrimental effect of smoking. J Vasc Surg 1984;1: Meechan JG, MacGregor DM, Rogers SM, Hobson RS, Bates JPC, Dennison M. The effect of smoking on immediate post-extraction socket filling with blood and on the incidence of painful sockets. Br J Oral Maxillofac Surg 1988;26: Moy PK, Bain CA, Sagai T, Beumer J III. Effects of smoking on osseointegrated implants in oral and extra-oral sites. In preparation. 26. MacFarlane GD, Herzberg MC, Wolff LF, Hardie NA. Refractory periodontitis associated with abnormal PMN leukocyte phagocytosis and cigarette smoking. J Periodontol 1992;63: Cryer PE, Haymond MW, Santiago JV, Shah SD. Norepinephrine and epinephrine
10 release and androgenic mediation of smoking associated hemodynamic and metabolic events. New Engl J Med 1976;295: Mosely LH, Finseth F, Goody M. Nicotine and its effects on wound healing. Plast Reconstr Surg 1978;61: Clarke NG, Shephard BC, Hirsch RS. The effects of intra-arterial epinephrine and nicotine on gingival circulation. Oral Surg 1981;52: Noble RC, Penny BB. Comparison of leukocyte count and function in smoking and non-smoking young men. Infect Immun 1975;12: Kenney EB, Kraal JH, Saxe SR, Jones J. The effect of cigarette smoke on human polymorphonuclear leukocytes. J Periodont Res 1977;12: Nadler JL, Velasco JS, Horton R. Cigarette smoking inhibits prostacycline formation. Lancet 1983;1: Lawrence WT, Murphy RC, Robson MC, Heggers JP. The detrimental effect of cigarette smoking on flap survival: An experimental study in the rat. Br J Plast Surg 1984;37: Adell R, Lekholm U, Brånemark P-I. Surgical procedures. In: Brånemark P-I, Zarb GA, Albrektsson T (eds). Tissue-lntegrated Prostheses: Osseointegration in Clinical Dentistry. Chicago: Quintessence, 1985: Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-term efficacy of currently used dental implants: A review and proposed criteria for success. Int J Oral Maxillofac Implants 1986;1: Battaglia G, Di Marco F, Piccoli A, Vianello F, Farinati F, Naccarato R. Clinical markers of slow healing and relapsing gastric ulcer. Gut 1987;28: Mosely LH, Finseth F. Cigarette smoking: Impairment of digital blood flow and wound healing in the hand. Hand Clin 1977;9: Siana JE, Rex S, Gottrup F. The effects of cigarette smoking on wound healing. Scand J Plast Reconstr Surg 1989;23: Rees TD, Liverett DM, Guy CL. The effect of cigarette smoking on skin flap survival in the face lift patient. Plast Reconstr Surg 1984;73: Millar PD. Regenerative and reconstrictive periodontal plastic surgery. Dent Clin North Am 1988;32: Bridges RB, Saxe SR, McKean HE. Cigarette smoking and diabetes effects on loss of attachment [abstract 2601]. J Dent Res 1991;70: Preber H. Clinical and therapeutic aspects. In: Preber H (ed). Smoking and Periodontal Disease. Stockholm: Karolinska Institute, 1986:
11 43. Sarin CL, Austin JC, Nickel WO. Effects of smoking on digital blood flow velocity. JAMA 1974;229: Westfall TC, Brase DA. Studies on the mechanism of tolerance of nicotine-induced elevations of urinary catecholamines. Biochem Pharmacol 1971;20: Ague C. Urinary catecholamines, flow rate and tobacco smoking. Biol Physiol 1974;1: Shuler RL. Effects of cigarette smoking on the circulation of the oral mucosa. J Dent Res 1968;47: Armitage AK, Turner DM. Absorption of nicotine in cigarette and cigar smoking through the oral mucosa. Nature 1970;226: Brånemark P-I. Bone marrosv microvascular structure and function. Adv Microcirc 1968;1: Kaye BL. Discussion. Plast Reconstr Surg 1986;77:
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