Implant installation in the

smoking patient
Crawford A. Bain
Over the past 20 years, endosseous titanium implants,
placed under various modications of the original
Branemark protocol, have proven to be amongst
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 favor-
ably 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 replace-
ment (2, 40, 43, 64). It has been recognized for some
time that a few unfortunate patients lose a dispro-
portionately 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 consid-
erable retrospective assessment of factors, which
may have contributed to the problem. Although fac-
tors 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 smok-
ing 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.
Effects of smokingongeneral 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.
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 expec-
tancy was reduced by 7.5 years in the smoking group
regardless of amount smoked. Eighty percent of non-
smokers 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 reach-
ing pensionable age, may inuence some govern-
ments 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 signi-
cant 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. Complica-
tions 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 smok-
ers 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
185
Periodontology 2000, Vol. 33, 2003, 185193 Copyright
#
Blackwell Munksgaard 2003
Printed in Denmark. All rights reserved
PERIODONTOLOGY 2000
ISSN 0906-6713
degenerations and lumbar prolapse. Lunt et al. (47)
also show that the amount of lifetime smoking expo-
sure was associated with reduced bone mineral den-
sity. 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 postmenopau-
sal 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-smo-
kers 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 fac-
tor in post-surgical wound healing. Within period-
ontology, 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, Scab-
bia et al. (60) found that smokers exhibited a less
favorable healing response following ap debride-
ment surgery compared to non-smokers, both in
terms of probing depth reduction and clinical attach-
ment gain, and that this reached clinical and statis-
tical 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 signi-
cantly greater loss of bone height than matched non-
smokers. 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 mandibu-
lar 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 duode-
nal 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 non-
smokers. 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 retro-
spective 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 sur-
gery or the duration of preoperative smoking abate-
ment. Return-to-work was achieved in 71% of non-
smokers, 53% of non-quitters, and 75% of patients
who quit smoking for more than 6 months after sur-
gery. 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, circulationandblood
flow
Several authors have shown that smoking compro-
mises 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 com-
promised aggregation and adhesion of leukocytes to
the endothelium in venules and arterioles
Using venous occlusion plethysmography, Butler
et al. (12) assessed vascular responsiveness in smok-
ing 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.
Bain
186
In a study of ocular and orbital blood ow in cigar-
ette 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 pathol-
ogy. Enderle et al. (16) assessed endothelial function
and variables of brinolysis and coagulation in smo-
kers 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, predomi-
nantly 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 endothe-
lial-dependent vasorelaxation, platelet aggregation,
endothelial cell dysfunction and the activation of
circulating leukocytes. Through these mechanisms,
cigarette smoking elicits the aggregation and adhe-
sion of leukocytes and/or platelets to the microvas-
cular endothelium in venules and arterioles
In a study of the acute effects of nicotine on cor-
onary blood ow, Tanaka et al. (63) found that cor-
onary 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 nico-
tine or some other unknown substances inuenced
by smoking.
Smoking and implant failure
(See Table 1.) Until 1991, implant failure was gener-
ally attributed to poor surgical technique (infection,
overheating of bone and over-instrumentation), poor
prosthetic design or management (overload, non-
passive t) or patient-related factors (limited avail-
able bone, poor oral hygiene and bruxism). These
factors were largely based on clinical observation,
extrapolation from failures in tooth-supported pros-
theses 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
T
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187
Implants in smokers
patients (5 smokers and 10 nonsmokers) who under-
went 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 peri-
operative 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
consecutive Branemark system
1
implants placed
by one surgeon (P.M.) between 1984 and 1991. Fac-
tors considered included implant length and loca-
tion, 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 signi-
cant part in increased implant failure. Their results
showed an overall failure rate of 4.76% in non-smo-
kers 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 differ-
ence only in the anterior mandible. Implant failures
decreased with increased implant length, but in the
maxilla there was a signicantly higher rate in smo-
kers 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
Branemark implants in 56 patients, Wallace (66)
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 retro-
spective study of maxillary antral-nasal inlay auto-
genous bone grafts in the compromised maxilla,
found that current use of nicotine, history of sinusi-
tis, 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 pati-
ents (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 con-
sumed. 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 conven-
tional cast frameworks. While they noted no signi-
cant 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 period-
ontal 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
188
Bain
placement. Based on a prospective study of 223 con-
secutive Branemark system implants placed in 78
patients, the author found no signicant difference
in failure rates between the non-smoking controls
and the smokers who quit, whereas there was a sig-
nicant 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 achieve-
ment 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.
What happens toimplantswhichare
initially successful in smokers?
Haas et al. (24), evaluating the maxilla, identied a
signicantly greater gingival bleeding index, peri-
implant probing depth, and peri-implant inamma-
tion 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 hy-
giene 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
showed that smoking was the most important factor
among those analyzed for association with peri-
implant 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 mandib-
ular overdentures, Berge & Gronningsaeter (10) using
uni- and multivariate analysis with the Cox Regres-
sion model, found an increased risk of implant fail-
ure 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 plasma-
sprayed 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 signif-
icantly post-loading failures were seen in 4% of non-
smokers 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 perfor-
mance of 219 Osseotite implants, which have a
roughened double acid etched surface of commer-
cially pure (CP) titanium. Nineteen of the 74 patients
were smokers, reporting smoking an average of 13.2
189
Implants in smokers
cigarettes per day. Using the KaplanMeier method
they reported an overall cumulative survival rate of
98.6% at 34 months and found no signicant differ-
ence 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 im-
plants (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 Osseo-
tite 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 sub-
group, 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 favor-
ably with our original maxillary data for machined
Branemark
1
implants, with 35 failures out of 196
implants 82.1 % CSR with up to 81 months'
follow-up (5).
This would appear to conrm the ndings of Grun-
der 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 sig-
nicantly higher levels of bone contact at the higher
levels of nicotine administered (P < 0.05). The per-
centage 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 his-
tologic data comparing both types of surface in smo-
kers 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 reas-
sessed our data for patients where bone classication
was available, to determine if there was any relation-
ship 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-smo-
kers, 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 ope-
rator 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 con-
rm the subjective nature of the classication.
Recent studies have used a 3-point classication:
dense/normal/soft, and this may prove more consis-
tent between operators (23, 38). The medical litera-
ture also shows that smoking is a major predictor of
reduced bone mineral density (41).
190
Bain
Conclusions
It is always challenging to draw conclusions at one
particular point in time, particularly in such a
dynamic area of research as osseointegration. How-
ever, 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 fail-
ure 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 demon-
strated 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 tech-
nique, 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
Branemark implants in smokers (5), these are at
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.
References
1. Adams CI, Keating JF, Court-Brown CM. Cigarette smoking
and open tibial fractures. Injury 2001: 32: 6165.
2. Adell R, Eriksson B, Lekholm U, Branemark P-I, Jemt T. A
long term follow up study of osseointegrated implants in
the treatment of totally edentulous jaws. Int J Oral Max-
illofac Implants 1995: 10: 347359.
3. Bain CA. The relationship between gender, age and implant
success. J Dent Res 1999: 78: 1471 (Abstract).
4. Bain CA. Long-term smoking cessation in dental implant
patients. 16th Scientific Meeting, Academy of Oseointegra-
tion, Toronto, April 2001.
5. Bain CA, Moy PK. The association between the failure of
dental implants and cigarette smoking. Int J Oral Maxillofac
Implants 1993: 8: 609615.
6. Bain CA, Moy PK. The influence of smoking on bone quality
and implant failure. Int J Oral Maxillofac Implants 1994: 9:
123.
7. Bain CA, Moy PK. The relationship between smoking and
bone quality in implant patients. Clin Oral Implant Res
1997: 8: 435 (Abstract).
8. Bain CA, Weng D, Meltzer A, Kohles SS, Stach R. A meta-
analysis of machined surfaced and Osseotite implants eval-
uating the risk for failure in patients who smoke. Compend
Contin Educ Dent 2002: 23: 695706.
9. Baron JA, Farahmand BY, Weiderpass E, Michaelsson K,
Alberts A, Persson I, Ljunghall S. Cigarette smoking, alcohol
consumption, and risk of hip fracture in women. Intern Med
2001: 161: 983988.
10. Berge TI, Gronningsaeter AG. Survival of single crystal sap-
phire implants supporting mandibular overdentures. Clin
Oral Implants Res 2000: 11: 15462.
11. Berman C. Personal communication. 1992.
12. Butler R, Morris AD, Struthers AD. Cigarette smoking in
men and vascular responsiveness. Br J Clin Pharmacol
2001: 52: 145149.
13. Chen F, Osterman AL, Mahony K. Smoking and bony union
after ulna-shortening osteotomy. Am J Orthoped 2001: 30:
486489.
14. Cheynet F, Chossegros C, Richard O, Ferrara JJ, Blanc JL.
Infectious complications of mandibular osteotomy. Rev
Stomatol Chir Maxillofac 2001: 102: 2633.
15. De Bruyn H, Collaert B. The effects of smoking on early
implant failure. Clin Oral Implants Res 1994: 5: 260264.
16. Enderle MD, Pfohl M, Kellermann N, Haering HU, Hoffme-
ister HM. Endothelial function, variables of fibrinolysis and
coagulation in smokers and healthy controls. Haemostasis
2000: 30: 149158.
17. Engquist B, Bergendal T, Kallus T, Linden U. A retrospective
multicenter evaluation of osseointegrated implants sup-
porting overdentures. Int J Oral Maxillofac Implants 1988:
3: 129134.
18. Fartash B, Tangerud T, Silness J, Arvidson K. Rehabilitation
of mandibular edentulism by single crystal sapphire im-
plants and overdentures: 312 year results in 86 patients
a dual center international study. Clin Oral Implants Res
1996: 7: 220229.
19. Fielding JA. Smoking: health effects and control. N Engl
J Med 1985: 313: 491498.
20. Forsmo S, Schei B, Langhammer A, Forsen L. How do
reproductive and lifestyle factors influence bone density
in distal and ultradistal radius of early postmenopausal
women? The Nord-Trondelag Health Survey. Osteoporos
Int 2001: 12: 222229.
21. Glassman SD, Anagnost SC, Parker A, Burke D, Johnson JR,
Dimar JR. The effect of cigarette smoking and smoking
cessation on spinal fusion. Spine 2000: 25: 26082615.
191
Implants in smokers
22. Geurs NC, Wang IC, Shulman LB, Jeffcoat MK. Retrospective
radiographic analysis of sinus graft and implant placement
procedures from the Academy of Osseointegration Consen-
sus Conference on sinus grafts. Int J Periodontics Restorative
Dent 2001: 21: 517523.
23. Grunder U, Gaberthuel T, Boitel N, Imoberdorf M,
Meyenberg K, Andreoni C, Meier T. Evaluating the clinical
performance of the Osseotite implant: defining prosthetic
predictability. Compend Contin Educ Dent 1999: 20:
628640.
24. Haas R, Haimbock W, Mailath G, Watzek G. The relationship
of smoking on peri-implant tissue: a retrospective study.
J Prosthet Dent 1996: 76: 592596.
25. Hagiwara S, Tsumura K. Smoking as a risk factor for bone
mineral density in the heel of Japanese men. J Clin Densi-
tom 1999: 2: 219222.
26. Herring M, Gardener A, Glover J. Seeding human arterial
prostheses with mechanically derived endothelium
The detrimental effect of smoking. J Vasc Surg 1984: 1:
279289.
27. Hoefflin SM, Rubin A. Smoking and cool face lifts; is there a
Buerger's type disease of the face? Plast Reconstr Surg 2001:
107: 13161318.
28. Hultin M, Fischer J, Gustafsson A, Kallus T, Klinge B. Factors
affecting late fixture loss and marginal bone loss around
teeth and dental implants. Clin Implants Dent Rel Res 2000:
2: 203208.
29. Ivanoff C-J, Grondahl K, Sennerby L, Bergstrom C. Influence
of variations in implant diameters: a 3 and 5 year retro-
spective clinical report. Int J Oral Maxillofac Implants 1999:
14: 173180.
30. Jaffin RA, Berman CL. The excessive loss of Branemark
fixtures in type IV bone. J Periodontol 1991: 62: 24.
31. Jemt T, Bergendal B, Arvidsson K, Bergendal T Karlsson U,
Linden B, Palmqvist S, Rundcrantz T, Bergstrom C. Laser-
welded titanium frameworks supported by implants in the
edentulous maxilla: a 2-year prospective multicenter study.
Int. J. Prosthodont 1998: 11: 551557.
32. Johnson GK, Slach NA. Impact of tobacco use on period-
ontal status. J Dent Educ 2001: 65: 313321.
33. Jones JD, Lupori J, Van Sickels JE, Gardner W. A 5-year
comparison of hydroxyapatite-coated titanium plasma-
sprayed and titanium plasma-sprayed cylinder dental
implants. Oral Surg Oral Med Oral Pathol 1999: 87:
649652.
34. Jones JK, Triplett RG. The relationship of cigarette smoking
to impaired intraoral wound healing: a review of evidence
and implications for patient care. J Oral Maxillofac Surg
1992: 50: 237239.
35. Kan JYK, Rungcharassaeng K, Lozada JL, Goodacre CJ. Ef-
fects of smoking on implant success in grafted maxillary
sinuses. J Prosthet Dent 1999: 82: 307311.
36. Keller EE, Tolman DE, Eckert SE. Maxillary antral-nasal
inlay autogenous bone graft reconstruction of compro-
mised maxilla: a 12-year retrospective study. Int J Oral
Maxillofac Implants 1999: 14: 707721.
37. Kenney EB, Kraal JH, Saxe SR, Jones J. The effect of cigarette
smoke on human PMN leukocytes. J Periodontal Res 1977:
12: 22734.
38. Khang W, Feldman S, Hawley CE, Gunsolley J. A multi-
center study comparing dual acid-etched and machined-
surfaced implants in various bone qualities. J Periodontol
2001: 72: 13841390.
39. Kirkendahl JW, Evaul J, Johnson LF. The effects of cigarette
smoking on GI physiology and non-neoplastic digestive
disease. J Clin Gastroenterol 1984: 6: 6578.
40. Kirsch A, Ackerman KL. The IMZ osseointegrated implant
system. Dent Clin North Am 1989: 33: 733791.
41. Larcos G. Predicting clinical discordance of bone mineral
density. Mayo Clin Proc 1998: 73: 824828.
42. La Vecchia C, Boyle P, Franceschi S. Smoking and cancer
with emphesis on Europe. Eur J Cancer 1991: 27: 94104.
43. Lindquist LW, Carlsson GE, Jemt T. Association between
marginal bone loss around osseointegrated mandibular im-
plants and smoking habits: a 10-year follow-up study.
J Dent Res 1997: 76: 16671674.
44. Lehr HA. Microcirculatory dysfunction induced by cigarette
smoking. Microcirculation 2000: 7: 367384.
45. Lekholm U, Zarb GA. Patient selection and preparation. In:
Branemark PI, Zarb GA, Albrecktssen T, eds. Tissue inte-
grated prostheses. Chicago: Quintessence, 1987: 199209.
46. Lemons JE, Laskin DM, Roberts WE, Tarnow DP. Changes in
patient screening for a clinical study of dental implants
after increased awareness of tobacco use as a risk factor.
J Oral Maxillofac Surg 1997: 55 (Suppl 5): 7275.
47. Lunt M, Masaryk P, Scheidt-Nave C, Nijs J, Poor G, Pols H,
Falch JA, Hammermeister G, Reid DM, Benevolenskaya L,
Weber K, Cannata J, O'Neill TW, Felsenberg D, Silman AJ,
Reeve J. The effects of lifestyle, dietary dairy intake and
diabetes on bone density and vertebral deformity preva-
lence: the EVOS study. Osteoporos Int 2001: 12: 688698.
48. MacFarlane GD, Hetzberg MC, Wolff L, Hardie NA. Refrac-
tory periodontitis associated with abnormal PMN leucocyte
phagocytosis and cigarette smoking. J Periodontol 1992: 63:
908913.
49. Malmstrom HS, Fritz ME, Timmins DP, Van Dyke TE. Os-
seointegrated implant treatment of a patient with rapidly
progressive periodontitis. J Periodontol 1990: 61: 300304.
50. Medras M, Jankowska EA, Rogucka E. The effect of smoking
tobacco and drinking of alcohol and coffee on bone mineral
density of healthy men 40 years of age. Polsk Archiw Med
Wewnetrznej 2000: 103: 187193.
51. Meechan JG, MacGregor DM, Rogers SM, Hobson RS. The
effect of smoking on immediate post-extraction socket fill-
ing with blood and on the incidence of painful sockets. Br J
Oral Maxillofac Surg 1988: 26: 402409.
52. Miller PD. Regenerative and reconstructive periodontal
plastic surgery. Dent Clin North Am 1988: 32: 287312.
53. Minsk L, Polson AM. Dental implant outcomes in postme-
nopausal women undergoing hormone replacement. Com-
pend Contin Educ Dent 1998: 19: 859864.
54. Moy PK, Bain CA. Relationship of fixture length and implant
failure. J Dent Res 1992: 71: 637 (Abstract).
55. Noble RC, Penny BB. Comparison of leucocyte count and
function in smoking and non-smoking young men. Infect
Immun 1975: 12: 550555.
56. Peto R, Lopez AD, Boreham J, Thun M, Health C, Jr, Doll R.
Mortality from smoking worldwide. Br Med Bull 1996: 52:
1221.
57. Preber H. Clinical and theraputic aspects. In: Preber H, ed.
Smoking and periodontal disease. Stockholm: Karolinska
Institute, 1985: pp. 85101.
58. Rapuri PB, Gallagher JC, BalhornKE, RyschonKL. Smokingand
bone metabolisminelderly women. Bone 2000: 27: 429436.
59. Riefkohl R, Wolfe JA, Cox EB, McCarthy KS, Jr. Association
between cutaneous occlusive vascular disease, cigarette
192
Bain
smoking and skin sloughing after rhytidectomy. Plast Re-
constr Surg 1986: 77: 592595.
60. Scabbia A, Cho KS, SigurdssonTJ, KimCK, Trombelli L. Cigar-
ette smoking negatively affects healing response following
flap debridement surgery. J Periodontol 2001: 72: 4349.
61. Stefani AM, Filho GRN, SallumEA, De Toledo S. Influence of
nicotine administration on different implant surfaces: a his-
tometric study in rabbits. J Periodontol 2002: 73: 206212.
62. Steigerwalt RD, Jr, Laurora G, Incandela L, Cesarone MR,
Belcaro GV, De Sanctis MT. Ocular and orbital blood flow in
cigarette smokers. Retina 2000: 20: 394397.
63. Tanaka T, Oka Y, Tawara I, Sada T, Kira Y. Acute effects
of nicotine content in cigarettes on coronary flow velocity
and coronary flow reserve in men. Am J Cardiol 1998: 82:
12751278.
64. Testori T, WisemanL, Woolfe S, Porter S. Aprospective multi-
center clinical study of the Osseotite implant: four year inter-
imreport. Int J Oral Maxillofac Implants 2001: 16: 193200.
65. Trivedi DP, Khaw KT. Bone mineral density at the hip
predicts mortality in elderly men. Osteoporos Int 2001: 12:
259265.
66. Wallace RH. The relationship between cigarette smoking
and dental implant failure. Eur J Prosthet Restorative Dent
2000: 8: 103106.
67. Watson CJ, Ogden AR, Tinsley D, Russell JL, Davison EM. A
3- to 6-year study of overdentures supported by hydroxya-
patite-coated endosseous dental implants. Int J Prostho-
dont 1998: 11: 610619.
68. Webster RC, Kazda G, Hamdan US, Fuleihan NS. Cigarette
smoking and facelift: conservative vs. wide undermining.
Plast Reconstr Surg. 1986: 77: 596602.
69. Widmark G, Andersson B, Carlsson GE, Lindvall AM, Ivanoff
CJ. Rehabilitation of patients with severely resorbed max-
illae by means of implants with or without bone grafts: a 3-
to 5-year follow-up clinical report. Int J Oral Maxillofac
Implants 2001: 16: 7379.
193
Implants in smokers