Periodontology 2000, Vol. 33, 2003, 185193 Printed in Denmark.

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Copyright # Blackwell Munksgaard 2003

PERIODONTOLOGY 2000
ISSN 0906-6713

Implant installation in the smoking patient

Crawford A. Bain
Over the past 20 years, endosseous titanium implants, placed under various modications of the original nemark protocol, have proven to be amongst Bra the most predictable treatments in oral health care. Success rates in excess of 95% up to 15 years and beyond, for some implant systems, compare favorably with the other methods of tooth replacement, and quality of life assessments comparing implant supported prostheses with removable partial and complete dentures show implant retained prosthesis to be a highly satisfactory method of tooth replacement (2, 40, 43, 64). It has been recognized for some time that a few unfortunate patients lose a disproportionately high number of implants (17, 40, 49). This clustering of failures has been of considerable concern to both the patients and clinicians who have experienced the phenomenon and has led to considerable retrospective assessment of factors, which may have contributed to the problem. Although factors such as implant length and location (5, 54), implant diameter (29) and bone quality (30) have been associated with excessive failure rates, smoking has become acknowledged as a leading predisposing factor in implant failure and particularly in multiple failures in the same individual (5, 15). The purpose of this paper is to review the association between smoking and implant failure; to discuss the benets of smoking cessation in the implant patient, to discuss potential mechanisms that may contribute to higher implant failure rates in smoking patients and to review recent data showing increased success in smokers with rough surfaced implants.  70% of chronic lung diseases.  80% of myocardial infarctions before the age of 50.  30% of ischaemic heart disease and strokes (19, 42, 56). Fifty percent of smokers will die from a smoking related disease and, in a 40-year longitudinal study of British doctors, Doll et al. showed that life expectancy was reduced by 7.5 years in the smoking group regardless of amount smoked. Eighty percent of nonsmokers reached the age of 70 compared with only 59% of smokers. The high tax income from cigarettes, combined with a large number of smokers not reaching pensionable age, may inuence some governments in their relative lethargy, and limited investment in anti-smoking campaigns. It is estimated that 70% of lung cancer in women and 90% in men is caused by tobacco smoking. Sixty percent of cancers of the esophagus, throat and mouth are also attributed to smoking, as is a signicant proportion of bladder and pancreatic cancer (19, 42, 56). Lung cancer alone is thought to kill around 90,000 people per year within the European Union. Smoking doubles the risk of myocardial infarction and the smoker is likely to have an infarction when 10 years younger than the non-smoker. Complications after bypass surgery and balloon dilation of the coronary arteries are much higher in smokers than non-smokers. Smoking cessation progressively reduces the risk of myocardial infarction so that after 510 years the ex-smoker is at no more risk than the non-smoker. Smoking has been implicated in 70% of Chronic Obstructive Lung Disease (bronchitis and emphysema) as well as increasing the risk of asthma in those who are genetically predisposed to the disease. Osteoporosis is commoner in long-term smokers who routinely show lower bone density than non-smoking cohorts (20, 25, 58). The potential relationship of this to intraoral bone density and implant failure will be discussed later. Smoking is also associated with higher incidences of spinal disc

Effects of smoking on general health

Smoking has been shown to be a primary etiologic factor in many serious and potentially fatal diseases. It is estimated that smoking is responsible for:  30% of all cancer diseases and deaths.  90% of all lung cancers.

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degenerations and lumbar prolapse. Lunt et al. (47) also show that the amount of lifetime smoking exposure was associated with reduced bone mineral density. This in turn increases the risk of low and moderate energy fractures. Baron et al. (9) conrmed that cigarette smoking is a signicant risk factor for hip fracture among postmenopausal women and that risk decreases after cessation. They also noted that duration of smoking, particularly postmenopausal smoking, was more important than the amount smoked. In a study of 258 healthy men, aged 4063, Medras et al. (50) found that smokers and ex-smokers had lower trabecular bone mineral content when compared to never-smokers. Low bone density has also been shown to be a strong and independent predictor of all-cause and cardiovascular mortality in older men (65).

Effects of smoking on wound healing

Wound healing complications in various medical and surgical disciplines
Smoking has long been noted as a complicating factor in post-surgical wound healing. Within periodontology, Preber (57) noted less reduction in probing depths in the periodontal pockets of smokers than non-smokers after scaling and root planning. Miller (52) also describes poorer healing after mucogingival surgical procedures in smokers. In a study involving 28 smokers (>10 per day) and 29 non-smokers, Scabbia et al. (60) found that smokers exhibited a less favorable healing response following ap debridement surgery compared to non-smokers, both in terms of probing depth reduction and clinical attachment gain, and that this reached clinical and statistical signicance at sites with initially deep probing depths. In a review article on the impact of tobacco use on periodontal status, Johnson & Slach (32) note that both cigar and cigarette smokers have signicantly greater loss of bone height than matched nonsmokers. Meechan et al. (51) showed signicant reductions in post-extraction socket ll with blood (P < 0.01) and more painful extraction sockets (P < 0.02) of tobacco users in a large sample of extraction patients. In oral surgery, Cheynet et al. (14) in a retrospective study of complications in 60 mandibular osteotomies identied patient-related risk factors as smoking, periodontal status, and oral hygiene. They recommend an interruption of smoking and preoperative scaling to minimize complications.

Smoking also compromises the healing of duodenal ulcers (39), and increases complications in both plastic surgery (27, 59, 68) and vascular surgery (26). In a study of healing after orthopedic surgery to the arm, Chen et al. (13) found mean union rates were 7.1 months in smokers and 4.1 months in nonsmokers. Six smokers (30%) and no non-smokers experienced delayed union or non-union in a 4-year matched study of 146 patients. Again in orthopedic surgery treating open fractures, Adams et al. (1) found a signicantly increased rate of ap failure, delayed union and non-union in the smoking group. They recommend patients should be advised to stop smoking to minimize these complications. In a retrospective review of 357 patients examining the effects of cigarette smoking and smoking cessation on spinal fusion, Glassman et al. (21) found the non-union rate was 14.2% for non-smokers and 26.5% for patients who continued to smoke after surgery (P < 0.05). Patients who quit smoking after surgery for longer than 6 months had a non-union rate of 17.1%. The non-union rate was not signicantly affected by either the quantity that a patient smoked before surgery or the duration of preoperative smoking abatement. Return-to-work was achieved in 71% of nonsmokers, 53% of non-quitters, and 75% of patients who quit smoking for more than 6 months after surgery. They state that these results validate the hypothetical assumption that postoperative smoking cessation helps to reverse the impact of cigarette smoking on outcome after spinal fusion.

Influence of smoking on the actions of polymorphonuclear leukocytes, macrophages, circulation and blood flow
Several authors have shown that smoking compromises the function of polymorphonuclear leukocytes and macrophages in several ways (37, 48, 52, 55). These include reduced compromised phagocytosis, delayed margination and diapedesis as well as compromised aggregation and adhesion of leukocytes to the endothelium in venules and arterioles Using venous occlusion plethysmography, Butler et al. (12) assessed vascular responsiveness in smoking and non-smoking men. They concluded that cigarette smoking is associated with a signicantly blunted basal and stimulated nitric oxide bioactivity. A signicant defect in the vasoconstrictor response to angiotensin I was also seen.

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Table 1. Summary of key artciles comparing implant outcomes in smokers and non-smokers

In a study of ocular and orbital blood ow in cigarette smokers Steigerwalt et al. (62) conclude that the decrease in the ow velocity of these vessels may be due to an increase in the vascular resistance of the vessels of the retina and optic nerve head in smokers. This may contribute to the ocular or orbital pathology. Enderle et al. (16) assessed endothelial function and variables of brinolysis and coagulation in smokers compared to healthy controls. They found that peripheral endothelial dysfunction is common in smokers even without major alterations in molecular markers of the coagulation and brinolysis system In a comprehensive review article, Lehr (44) discusses the deleterious effects of cigarette smoking on the microcirculation. These are divided into morphologic aspects, particularly vessel wall injury and capillary loss and functional aspects, predominantly changes in tissue perfusion and its regulatory mechanisms, notably reactive hyperemia, and sequestration of blood cells in the microcirculation. The mechanisms of action of cigarette smoking on the microcirculation include compromised endothelial-dependent vasorelaxation, platelet aggregation, endothelial cell dysfunction and the activation of circulating leukocytes. Through these mechanisms, cigarette smoking elicits the aggregation and adhesion of leukocytes and/or platelets to the microvascular endothelium in venules and arterioles In a study of the acute effects of nicotine on coronary blood ow, Tanaka et al. (63) found that coronary ow reserve decreased after smoking high nicotine cigarettes, but not low nicotine cigarettes or in the non-smoking control group. They conclude that this reduction may have been mediated by nicotine or some other unknown substances inuenced by smoking.

In sinus grafts includes post loading

Includes post loading

Pre-loading failures; maxilla only

nemark machined Bra

3i Osseotite acid etched 1.4 1.2 219 Grunder et al. (23) Prospective; 4 centers

Type of implant

Not specified

Includes post loading

Smokers

16.6

11.3

Non-smokers

% Failures

17.3

4.8

6.9

34.7

# Implants

244

187

2,194

228

(See Table 1.) Until 1991, implant failure was generally attributed to poor surgical technique (infection, overheating of bone and over-instrumentation), poor prosthetic design or management (overload, nonpassive t) or patient-related factors (limited available bone, poor oral hygiene and bruxism). These factors were largely based on clinical observation, extrapolation from failures in tooth-supported prostheses and dogma. In an article on smoking and wound healing in patients undergoing intraoral bone grafting and simultaneous implant placement Jones & Triplett (34) implicated smoking as a potentially signicant risk factor. Fifteen consecutive adult

Type of study

Smoking and implant failure

De Bruyn & Collaert (15)

Bain & Moy (5)

Kan et al. (35)

Bain et al. (8)

Wallace (6)

Author

Prospective: 25 centers

Retrospective; 1 center

2,288

1.6

1.3

Includes post loading

Comments

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patients (5 smokers and 10 nonsmokers) who underwent intraoral bone grafting with simultaneous implant placement were retrospectively reviewed. Five of 15 patients experienced impaired wound healing dened as loss of bone and/or implants. Four of these ve (80%) admitted to smoking in the perioperative period. In an effort to evaluate the possible risk factors which contributed to implant failure, Bain & Moy (5) carried out a retrospective evaluation of 2,194 nemark system1 implants placed consecutive Bra by one surgeon (P.M.) between 1984 and 1991. Factors considered included implant length and location, diabetes, steroid medication, age and gender, time placed along ``the learning curve'' and smoking (3, 7, 54). It soon became apparent that, of all of the factors considered, smoking played the most signicant part in increased implant failure. Their results showed an overall failure rate of 4.76% in non-smokers as against 11.3% in smokers (P < 0.01). More interestingly, when the maxilla alone was considered there were 17.9% failure in smokers and only 7.3% failure in non-smokers (P < 0.001). The difference in the mandible was less, with 4.64% failure in smokers and 2.4% in non-smokers, with a signicant difference only in the anterior mandible. Implant failures decreased with increased implant length, but in the maxilla there was a signicantly higher rate in smokers at implant lengths up to 15 mm. Bone quality was not considered in this study, since the data base went back to 1984, while Lekholm & Zarb's bone quality classication (45) was only used routinely from late 1986. De Bruyn & Collaert (15) conrmed these results. Limiting their assessment to the point of implant exposure to avoid loading, oral hygiene and other compounding factors, they identied 9% failure in the maxilla of smokers as against 1% in non-smokers. From the clinical perspective it is important to note that they had at least one failed implant in one in three smokers, while only one in 25 non-smokers had one or more failures. Using a chi-square test to assess 187 machined nemark implants in 56 patients, Wallace (66) Bra found failure rates of 16.6% in smokers compared to 6.9% in non-smokers (P < 0.01), with shorter implants (10 mm or less) being more susceptible to failure in smokers. In a study of 43 patients with severely resorbed maxillae, Widmark et al. (69) found that the failure rate was higher in smokers than in non-smokers. Keller et al. (36), in a 12-year retrospective study of maxillary antral-nasal inlay autogenous bone grafts in the compromised maxilla,

found that current use of nicotine, history of sinusitis, shorter implant lengths and posterior sites had the most inuence on implant failure. In a retrospective radiographic analysis of implants placed in sinus grafts, Geurs et al. (22) found that smoking resulted a signicant decrease in implant survival (P < 0.05). Similarly, in a study of the effects of smoking on implant success in grafted maxillary sinuses, Kan et al. (35) assessed outcomes in 60 patients (16 smokers and 44 non-smokers) who had 228 titanium implants, of unspecied type, placed in 84 grafted maxillary sinuses. Seventy implants were placed in 26 maxillary sinuses in smokers, and 158 implants were placed in 58 sinuses in non-smokers. The number of implant failures and the amount of cigarette consumption was recorded. With a mean follow-up period of 41.6 months (260 months), there was a signicantly higher cumulative implant success rate in non-smokers (82.7%) than in smokers (65.3%) (P 0.03). There was no correlation between implant failures and the amount of cigarettes consumed. Several other studies conrm the association between smoking and implant failure (46, 53). Our own research (7) indicates a dose relationship between amount smoked and failure rates. Patients smoking 10 or fewer cigarettes per day had no higher failure rate than non-smokers (see below). Jemt et al. (31) compared the edentulous maxillas of 28 patients who received laser-welded titanium frameworks and 30 patients who received conventional cast frameworks. While they noted no signicant differences between the groups, they noted two patients (one in each group) with total prosthesis failure. The only obvious factor that could possibly be related to the two complete failures was a smoking habit.

What happens if the potential implant patient stops smoking?

As with the association between smoking and periodontal diseases, there is much more evidence of the detrimental effect of smoking on implant outcomes than there is on the potential benet of stopping smoking. In one study, Bain (4) examined a cessation protocol in which potential implant patients who smoked were encouraged to stop for 1 week before and 8 weeks after implant placement. This protocol was based on the medical literature, which, by and large, indicated improvements in circulation within 1 week of cessation, and histologic evidence of early osseointegration occurring within 8 weeks of implant

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placement. Based on a prospective study of 223 con nemark system implants placed in 78 secutive Bra patients, the author found no signicant difference in failure rates between the non-smoking controls and the smokers who quit, whereas there was a signicant difference between the continuing smokers and smokers who followed the cessation protocol (P < 0.05). Although, within this protocol, patients were only asked to stop for a period of 9 weeks, Bain (4) has shown that implant patients who stop smoking for the time around implant placement often keep off of cigarettes in the longer term. Of 57 smokers who underwent implant surgery, 51 (89.5%) started on the cessation protocol and 48 (84.2%) completed the 9 weeks without smoking. At 3 months, 40 patients (70.2%), were still smoke free, at 6 months 25 (43.9%) had not resumed smoking and at 12 months 23 patients (40.4%) had still stopped. This compares favorably with cessation levels achieved using the various nicotine replacement aids and Zyban (bupropion SR), which is currently the most effective non-nicotine based cessation drug. The most common reasons given for compliance were the potential high costs of implant failure, the nite time frame, and the fact that this was ``a good reason for stopping''. The duration of the protocol is long enough for most quitters to appreciate their achievement and may well lead to the high level of continued cessation. Clearly, dentists, periodontists and oral surgeons as health care professionals have an obligation to encourage and assist their patients in smoking cessation.

showed that smoking was the most important factor among those analyzed for association with periimplant bone loss. In a study of late implant failure (post-loading) Hultin et al. (28) assessed 143 consecutively treated patients who had received an implant-anchored xed prosthesis and completed a 5-year follow-up. They found that seven of the nine patients who lost xtures after loading were smokers. Patients who lost implants also lost more bone around the remaining implants. There was no correlation between bone loss around implants and that around remaining natural teeth.

Do different materials and surfaces make a difference?

In a study of sapphire implants supporting mandibular overdentures, Berge & Gronningsaeter (10) using uni- and multivariate analysis with the Cox Regression model, found an increased risk of implant failure in patients over 60 years old at time of operation, and in patients who smoke. The overall cumulative survival rate for the sapphire implants was 68.7%. Similarly Fartash et al. (18) identied heavy smoking as a risk factor for failure in a prospective study of mandibular edentulism, treated with overdentures supported by Bioceram sapphire implants (Kyocera Corporation, Kyoto, Japan). In a 5-year comparison of hydroxyapatite-coated titanium plasma-sprayed and titanium plasmasprayed cylindrical Implamed implants, Jones et al. (33) found no difference in cumulative failure rates between the surfaces, but that a smoking history was a signicant factor in failure (chi-square test P 0.002). They identied preloading failures in 9% in non-smokers vs. 26% in smokers. More significantly post-loading failures were seen in 4% of nonsmokers vs. 37% of smokers. However, in a study of overdentures supported by hydroxyapatite-coated endosseous dental implants with Watson et al. (67) found that, in 139 Calcitek implants placed in 43 patients to support 14 maxillary and 30 mandibular overdentures, the cumulative success rate by year 6 had fallen to 39%. Failure rates were higher in the maxillary arch, in poor quality bone, in smokers, and where implants were opposed by a natural dentition. Grunder et al. (23) evaluated the clinical performance of 219 Osseotite implants, which have a roughened double acid etched surface of commercially pure (CP) titanium. Nineteen of the 74 patients were smokers, reporting smoking an average of 13.2

What happens to implants which are initially successful in smokers?

Haas et al. (24), evaluating the maxilla, identied a signicantly greater gingival bleeding index, periimplant probing depth, and peri-implant inammation as well as signicantly greater mesial and distal marginal bone loss in smokers than in non-smokers. Lindquist et al. (43) in a 10-year follow-up study of mandibular implant supported prostheses found that marginal bone loss was greater in smokers than in non-smokers and correlated to the amount of cigarette consumption. Smokers with poor oral hygiene showed greater marginal bone loss around the mandibular implants than those with good oral hygiene. Oral hygiene did not signicantly affect bone loss in non-smokers. Multivariate analyses

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cigarettes per day. Using the KaplanMeier method they reported an overall cumulative survival rate of 98.6% at 34 months and found no signicant difference in failures between smokers and non-smokers. Bain et al. (8) examined the inuence of smoking on the integration success and longevity of machined and acid etched titanium implants. This study combined three prospective multicenter studies on machined implants (n 2,614), and six prospective multicenter studies on Osseotite acid etched implants (n 2,288), all with standardized protocols. Cumulative success rates were calculated using the KaplanMeier estimator. In all, 492 (18.9%) machined and 397 Osseotite implants (17.5%, not signicant) were placed in smokers. Mean smoking consumption was 12.1 cigarettes per day in machined implants and 12.7 cigarettes per day in Osseotite implants (not signicant). There was no signicant differences between groups in age or gender. Signicantly more Osseotite implants were placed in the posterior parts of the mouth in relation to the anterior (ant : post ratio machined 3.14 : 1; ant : post ratio Osseotite 2.1 : 1). The overall cumulative success rates were 92.8% for the machined implants and 98.4% for the Osseotite implants. Within the smoking subgroup, cumulative success rates were 93.5% for the machined implants and 98.7% for the Osseotite implants. There was no signicant difference between smokers and non-smokers with either type of surface, but there was a signicant difference between machined surfaces and acid etched surfaces in both smokers and non-smokers. The results for the etched Osseotite implants in the maxilla, with ve failures out of 200 implants 97.3 % CSR with up to 70 months' follow-up, compare very favorably with our original maxillary data for machined nemark1 implants, with 35 failures out of 196 Bra implants 82.1 % CSR with up to 81 months' follow-up (5). This would appear to conrm the ndings of Grunder et al. (23) that acid etched roughened surfaces may negate the inuence of smoking and at present offer the highest documented success rates in the smoking patient. A recent histometric study in rabbits (61) assessed the inuence of various systemic nicotine levels on bone to implant contact using both machined and rough surfaced titanium implants. They found signicantly higher levels of bone contact at the higher levels of nicotine administered (P < 0.05). The percentage contact on rough surface implants in the highest level of nicotine used was comparable with surface contact in machined implants in the control

group, which had no nicotine exposure. While this goes some way to explaining the human clinical data for rough surface implants in smokers, human histologic data comparing both types of surface in smokers is needed to fully explain the mechanism leading to higher success rates of rough surface implants in smoking patients.

Bone density, smoking and implant success

Jafn & Berman (30) identied a disproportionate number of failures in patients with type 4 bone. Their study showed 65% success in type 4 bone as against 97% in types 1, 2 and 3 combined. Since the Lekholm & Zarb bone density classication was not published until 1987 it was not used in our initial smoking study. At Berman's suggestion (11) we have reassessed our data for patients where bone classication was available, to determine if there was any relationship between bone quality and smoking (6). Our patients were additionally divided into light (<10 cigarettes per day), moderate (1120 per day) and heavy smokers (>20 per day). A total of 1,379 implants in 412 patients were assessed. Within the non-smoking and light smoking group, 17.6% of implant sites were classied as having type 4 bone, whereas within the moderate and heavy smokers, 37.9% of sites had type 4 bone (P < 0.01). With regard to failures, a signicant difference (P < 0.05) was seen between light smokers, who had a failure rate no different from non-smokers (4.9% vs. 4.4%; not signicant), and moderate and heavy smokers, who had failure rates of 15.1% and 12.87%, respectively. It was concluded that smoking predisposes to both type 4 bone and implant failure, that this effect relates to the amount smoked, with light smokers having no more failures than non-smokers, and that the previously independently observed failures in smokers and patients with type 4 bone are in fact related (6). One should bear in mind that the Lekholm & Zarb bone density classication has a subjective component to it and may be open to operator variability. Jafn & Berman's group included only 13% of patients with type 4 bone, while our own group exceeded 24%. This is more likely to conrm the subjective nature of the classication. Recent studies have used a 3-point classication: dense/normal/soft, and this may prove more consistent between operators (23, 38). The medical literature also shows that smoking is a major predictor of reduced bone mineral density (41).

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Implants in smokers

Conclusions
It is always challenging to draw conclusions at one particular point in time, particularly in such a dynamic area of research as osseointegration. However, based on a review of the currently available information is seems clear that, at the time of writing:  Smoking and particularly heavy smoking increases the failure rates for machined titanium implants, likely due to a compromise of the blood supply in bone during early healing.  This increased failure rate clusters largely in the maxilla, with much smaller differences of success rates, often statistically insignicant, between smokers and non-smokers for implants placed in the mandible.  Smoking is associated with a particularly high failure rate for implants placed into grafted maxillary sinuses. Some operators may consider this to be too great a risk to take, if the patient is unable of unwilling to stop smoking.  There would appear to be a relationship between heavy smoking and reduced bone density. This is seen in various areas of medicine, as well as in implant surgery and goes some way to explaining high failure rates in Type 4 bone.  Smoking cessation, as well as being of general benet to all of our patients, has been demonstrated to improve success rates in machined implant patients. Implant placement may well be an effective motivator in assisting a smoker with cessation.  There is early evidence that rough surface implants, prepared with a double acid etched technique, have a high success rate in smokers. With success rates around 10% better overall (98.7% vs. 88.7%) and 15% better in the maxilla (97.3% vs. 82.1%) than our original results with machined nemark implants in smokers (5), these are at Bra present considered to be the implant of choice in smokers who cannot or will not stop smoking for implant placement.  Future research should examine the success of other rough surface implants in the maxilla of heavy smokers.
3. 4.

5.

6.

7.

8.

9.

10.

11. 12.

13.

14.

15. 16.

17.

18.

19. 20.

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