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Journal of Dental Research

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Association between Marginal Bone Loss around Osseointegrated Mandibular Implants and
Smoking Habits: A 10-year Follow-up Study
L.W. Lindquist, G.E. Carlsson and T. Jemt
J DENT RES 1997 76: 1667
DOI: 10.1177/00220345970760100801
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J Dent Res 76(10): 1667-1674, October, 1997

Association between Marginal Bone Loss


around Osseointegrated Mandibular Implants
and Smoking Habits: A 10-year Follow-up Study
L.W. Lindquist, G.E. Carlsson*, and T. Jemt'
Department of Prosthetic Dentistry, Faculty of Odontology, Goteborg University, Medicinaregatan 12, S-41390 Goteborg, Sweden; and 'The
BrAnemark Clinic, Public Dental Health Service, Goteborg, Sweden; *to whom correspondence and reprint requests should be addressed

Abstract. While many factors are conceivable, occlusal loading


and plaque-induced inflammation are frequently stated as the
most important ones negatively affecting the prognosis of oral
implants. Currently, little is known about the relative
importance of such factors. The aim of this study was to
analyze the influence of smoking and other possibly relevant
factors on bone loss around mandibular implants. The
participants were 45 edentulous patients, 21 smokers and 24
non-smokers, who were followed for a 10-year period after
treatment with a fixed implant-supported prosthesis in the
mandible. The peri-implant bone level was measured on intraoral radiographs, information about smoking habits was based
on a careful interview, and oral hygiene was evaluated from
clinical registration of plaque accumulation. Besides standard
statistical methods, multiple linear regression models were
constructed for estimation of the relative influence of some
factors on peri-implant bone loss. The long-term results of the
implant treatment were good, and only three implants (1%)
were lost. The mean marginal bone loss around the
mandibular implants was very small, about 1 mm for the
entire 10-year period. It was greater in smokers than in nonsmokers 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 significantly
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. The
separate models for smokers and non-smokers revealed that
oral hygiene had a greater impact on peri-implant bone loss
among smokers than among non-smokers. This study showed
that smoking was the most important factor affecting the rate
of peri-implant bone loss, and that oral hygiene also had an
influence, especially in smokers, while other factors, e.g., those
associated with occlusal loading, were of minor importance.
These results indicate that smoking habits should be included
in analyses of implant survival and peri-implant bone loss.
Key words: bite force, cigarette smoking, dental implants,
occlusal loading, oral hygiene.
Received August 26, 1996; Revised January 22, 1997;
Accepted April 8, 1997

Introduction
It has often been stated that plaque-induced inflammation
and occlusal loading are among the most important factors
influencing the prognosis for oral implant treatment
(Schnitman and Schulman, 1979; Lindhe et al., 1992;
Quirynen et al., 1992). This might be a qualified guess based
on animal experimentation, but evidence from human
clinical studies is mainly anecdotal (Carlsson, 1996). Many
other factors are certainly also of importance, including, for
example, strict adherence to the treatment protocol, which
was strongly emphasized in the early presentation of the
osseointegration concept (Branemark, 1983). Today, much
research is focused on implant material aspects, and the
design and surface structure of the implants have been
shown to be decisive for the establishment of reliable
osseointegration (Henry, 1995; Wennerberg, 1996). In the
long-term perspective, general health factors are most
probably of significance (Weyant, 1994).
The adverse effects of tobacco smoking on general health
and biological tissues are undisputed (US Department of
Health and Human Services, 1989). It is well-recognized that
cigarette smoking is associated with impaired wound healing
after surgical treatment in the oral cavity (Meechan et al.,
1988; Preber and Bergstrom, 1990), as well as in other
locations of the human body (Mosely et al., 1978). Reduced
alveolar bone height in smokers compared with non-smokers
has frequently been reported in different periodontal studies
(Arno et al., 1959; Bergstrbm and Eliasson, 1987; Bolin et al.,
1987, 1993). In an epidemiological study, it was also shown
that tobacco smoking is a major risk factor for tooth loss in
elderly subjects (Osterberg and Mellstrbm, 1986). However,
not until the last decade has it been clearly documented that
there is a direct association between smoking and periodontal
bone loss and that smoking should be considered a major risk
factor, separated from other factors, such as oral hygiene
(Haber et al., 1993; Haber, 1994).
Osseointegrated implants have been extremely
successful in the treatment of total and partial
edentulousness (Branemark, 1983; Lindquist and Carlsson,
1985; Albrektsson et al., 1986; Jemt et al., 1989; Zarb and
Schmitt, 1990; Quirynen et al., 1991). Failures sometimes
occur, however, and much interest has been directed in the
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j Dent Res 76(10) 1997

Lindquist et al.

last few years to analyzing the causes of implant failure and


other complications of implant treatment (Friberg et al.,
1991; Jemt, 1994). Smoking has been found to be one
important factor related to the loss of and soft tissue changes
around implants, according to some studies (Bain and Moy,
1993; De Bruyn and Collaert, 1994; Gorman et al., 1994;
Weyant, 1994). Bone loss around implants in relation to
smoking does not seem to have been studied systematically.
Because the titanium implant is attached directly to the
alveolar bone, and no intermediate layer of connective tissue
exists between the bone and the implant, as it does between
the bone and a natural tooth, direct measurement of alveolar
bone loss is possible in longitudinal studies of oral implants.
Since the outer surface of the implant is scored by threads of
an identical dimension, they serve as a measuring stick
when a sensitive radiographic technique is used (Hollender
and Rockler, 1980; Strid, 1985). Thus, conditions for
evaluating, with a high degree of precision, the alveolar
bone level surrounding the implant at different times after
its insertion are optimal (Lindquist et al., 1988, 1996).
The aim of this study was to measure and compare
marginal bone loss in smoking and non-smoking implant
patients and to analyze further the role of poor oral hygiene
and other factors of possible relevance for marginal bone
loss in these two groups.

Materials and methods


This longitudinal study was comprised of 45 edentulous
patients, 13 men and 32 women, under 65 yrs of age (range, 33 to
64) at the time of implant placement. All patients could be
followed for the entire 10-year period except for one woman
who died after 6 yrs. The composition of the study population
with respect to age, gender, smoking habits, and other
descriptive statistics is given in Table 1. All the patients had
worn complete dentures in both jaws for at least 1 yr before
consulting or being referred to the Dental School, Goteborg
University, for possible treatment with fixed prostheses on
osseointegrated implants (OIFPs) because of severe difficulties
with the removable dentures. The selection, treatment principles,
and examination procedures have previously been described in
detail (Lindquist and Carlsson, 1985; Lindquist, 1987; Lindquist
et al., 1987); only a brief description is given here.
After initial examinations and recordings, all the patients
were fitted with optimized complete dentures, mainly so that
we could judge whether they could adapt to the improved
removable prostheses, before installation of the mandibular
implants was begun.
Implant installation was carried out by three experienced
surgeons during the period 1978 to 1982, according to principles
described elsewhere (Adell et al., 1985). A total of 266 standard
Branemark implants (Nobel Biocare AB, Goteborg, Sweden) was
inserted. All implants had a length of 10 mm, the longest available
at that time. Two of the implants were lost before abutment
connection, and 5 were left unconnected ("sleeping"). All but eight
patients received 6 implants in the lower jaw. Of the remaining
patients, five had 5 and three had 4 implants connected. In each
patient, two of the implants were placed bilaterally in the premolar
region anterior to the mental foramina, the others in the incisor
area. Standard abutment cylinders were connected to the implant

after a healing time of 4 mos. Within 3 wks after abutment


connection, a full-arch 12-unit fixed mandibular prosthesis was
fabricated in Type III gold alloy with resin teeth and with posterior
bilateral cantilever sections of an average length of 15 mm
(Lindquist et al., 1987). For all patients, the clinical prosthetic work
was performed by one experienced prosthodontist and the
technical laboratory work by one senior dental technician.
After the patients had received their mandibular OIFPs, a
follow-up program with annual clinical check-ups for the
following 10 yrs was begun. During the follow-up period, 13
patients were also treated with fixed implant-supported
prostheses in the maxilla (Carlsson and Lindquist, 1994). The
remaining 32 patients had removable maxillary complete
dentures throughout the observation period.
The design of the study was approved by the Ethical Research
Committee of the Faculties of Medicine and Odontology,
Goteborg University. The patients were informed of the aims and
methods of the study, and all consented to participate.

Registrations
Bone loss. The marginal bone level around the implants was
documented with apical intra-oral radiographs according to a
previously described technique (Hollender and Rockler, 1980;
Strid, 1985). The radiographic examinations for this
investigation were performed at the time of insertion of the
fixed prosthesis and then 1, 3, 5 to 6, and 10 yrs thereafter. The
radiographs were examined with respect to osseointegration
and bone loss around the implants. The marginal bone level
(i.e., the height of the bone anchorage zone) of each implant was
measured on the radiographs to the nearest 0.3 mm in relation
to the reference point on the mesial and distal sides of the
implant (Lindquist et al., 1988). Based on these measurements, a
mean bone level was calculated for each implant as well as for
the individual patient.

Oral hygiene. Plaque accumulation on the titanium abutments


was recorded at the annual follow-ups during the observation
period. The level of oral hygiene was evaluated on a three-point
scale: 0 = no plaque; 1 = local plaque accumulation (< 25% of the
visible abutment area); and 2 = general plaque accumulation (>
25%). We calculated an oral hygiene index retrospectively for
each patient by scrutinizing the records and then adding the
scores for the annual visits and dividing by the number of visits.
The values for the index thus ranged from 0 (good) to 2 (poor).

Smoking habits. Information about smoking habits for the entire


observation period was based on the patients' answers to an
interview at the 10-year follow-up and notes in the patient
records. Non-smokers were subjects who, at the start of the 10year follow-up, had never smoked. Patients were also
considered non-smokers if they had ceased smoking 1 yr or
more before implant treatment. Current smokers were those
who had been smoking cigarettes 1 yr or more before implant
treatment and during the entire observation period of 10 yrs.
Smoking exposure was expressed in cigarettes per day, and
the median value of cigarette consumption for the subjects
during the 10-year observation period in the smoking group
was 20 cigarettes per day (range, 8 to 30) during the time of the
investigation. None of the subjects used snuff tobacco.

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J Dent Res 76(10) 1997

Smoking and Bone Loss around Implants

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Table 1. Descriptive statistics of the patients with respect to gender and smoking habits
Bone
Implants
Maxilla
n
Aged Height
6
5
CD
FP
OH
Non-smokers

Bone Loss
Mean
SD

male

58

3a

1.3

0.6

0.1

female
Smokers
male
female

19

55

16a b

12

0.5

0.7

0.3

a
b

46

1.3

1.4

0.7

13c

53

13

0.5

1.2

0.4

One implant failed before abutment connection.


One implant failed after connection of the prosthesis.
One patient died 6 yrs after the start of implant treatment.
Age: Median age at insertion of implants, in yrs. Bone height: median value of the height of the mandibular
residual ridge at time of implant placement according to a scale of 1 to 3. Implants: distribution of the patients
according to number of implants connected. Maxilla: prosthetic situation in the maxilla at the 10-year follow-up.
CD = complete denture; FP = fixed implant-supported prosthesis; OH = median value of oral hygiene index
according to a scale 0-2. Bone loss: mean and standard deviation (SD) of peri-implant bone loss after 10 yrs, in mm.

Other recordings. At each follow-up, clinical examination was also


performed of variables other than oral hygiene, such as mucosal
conditions around the implants, prosthodontic complications
and stability, occlusion, occlusal wear, and changes in function
and esthetics of the prostheses (Lindquist, 1987; Lindquist et al.,
1987). These observations were entered into the patients'
records. We performed function tests to measure bite force using
an apparatus with strain gauges mounted in a bite fork and
chewing efficiency using a sieving method. A visual analog scale
was used to record the patients' own evaluation of their chewing
ability. The length of the posterior cantilever units from the
distal side of the most posterior implant was measured in
millimeters. The degree of bone resorption in the mandible prior
to implant surgery was estimated according to a three-point
scale by means of measurements on profile radiographs: 1 =
little, 2 = moderate, and 3 = advanced resorption. Details of the
recording methods have been presented previously (Lindquist
and Carlsson, 1985; Lindquist, 1987).

Statistical methods
We first analyzed the influence of various factors on marginal
bone loss by dividing the material into subgroups. Since no
significant difference was found between men and women with
respect to marginal bone loss, the subjects were pooled in all
succeeding analyses. The significance of differences between
two groups was tested by Student's t test for paired and
unpaired observations, when applicable, and covariance
analysis when differences among three groups were tested. We
analyzed bivariate linear correlations by calculating Pearson's
coefficient of correlation in smokers and non-smokers
separately. The influence of some factors on bone loss around
the implants was studied in multiple linear regression models.
Separate models were constructed for bone loss after 1 and 10
yrs after the start of implant treatment in smokers, nonsmokers, and the entire group. The following independent
variables were tested: age (yrs), period of edentulousness before
implant treatment (yrs), height of the mandibular ridge before
implant treatment (low, medium, high), length of the cantilever
sections (mm, mean of left and right sides), maximal bite force
(N, measured at the one-year examination), occlusal wear (from

0 to 3), oral hygiene (from 0 to 2), and smoking (yes, no, and
number of cigarettes per day).

Results
The mean marginal bone loss around the mandibular
implants was very small, about 1 mm for the entire 10-year
period. It was significantly greater (P < 0.001), however, in
smokers than in non-smokers. The mean values were already
about twice as large for the smokers 1 yr after the implant
treatment, and the ratio remained the same throughout the
observation period. The difference between smokers and nonsmokers had reached a mean of about 0.6 mm after 10 yrs.
The bone loss was smaller around the more posterior
implants than around those in the mesial incisor region. In
smokers, the difference in bone loss between implants in the
incisor and premolar regions was already strongly significant
(P < 0.001) after 1 yr and remained so throughout the period.
In non-smokers, this difference was smaller and did not
become statistically significant until after 5 to 6 yrs (Table 2).
When both smoking and non-smoking groups were
analyzed together, patients with poor oral hygiene were
found to have greater marginal bone loss around the
mandibular implants than those with good oral hygiene.
The difference was evident after 1 yr but did not become
significant (P < 0.05) until after 3 yrs. When the smoking and
non-smoking groups were analyzed separately, no
significant differences in bone loss between those with good
and poor oral hygiene could be seen among the nonsmokers. Among the smokers, those with poor oral hygiene
had a significantly greater bone loss (P < 0.001) than those
with good oral hygiene at all examinations (Table 3, Fig.).
When we analyzed the bone loss in relation to cigarette
exposure by dividing the patients into three groups (nonsmokers, smokers smoking < 14 cigarettes a day, and
smokers smoking > 14 cigarettes a day), we found
significant differences among the means of all three
groups. The non-smokers had less bone resorption than
either of the smoking groups, and the smokers with low
cigarette consumption had less bone loss than those with
high consumption.

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Lindquist et al.

j Dent Res 76(10) 1997

Table 2. Marginal bone loss (mean and standard deviation, in mm) around i,mplants
inserted into different regions of the mandible in 21c smokers and 24 non-smokers 1, 3,
5/6, and 10 yrs after implant treatment
Obs. Time
Smokers
Non-smokers
Region
Mean SD
(yrs)
Mean SD
pd
***b
Mesial incisors
0-1
0.86
0.62
0.40
0.30
Anterior
0-1
0.78
0.55
0.33
0.30
pap

*NSa

Premolar

0-1

0.49

0.34

0.29

0.27

Mesial incisors
Anterior

0-3
0-3

1.28
1.07

0.84
0.73

0.34
0.34

Premolar

0-3

0.59

0.40

0.59
0.48
NS
0.38

Mesial incisors
Anterior

0-5/6
0-5/6

1.45
1.24

0.77
0.69

0.76
0.64

0.39
0.39

Premolar

0-5/6

0.71

0.42

0.43

0.32

Mesial incisors
Anterior

0-10
0-10

1.71
1.51

0.94
0.83

0.90
0.78

0.46
0.45

Premolar

0-10

0.89

0.50

0.47

0.35

pap

pap

pap

a
b

0.30

NS = not significant.
*** P < 0.001.
C
At the 10-year follow-up, the number of smokers was 20.
d P denotes difference between smokers and non-smokers (righ t
column) and
between implants in the anterior and premolar regions (PaP).

Of the 266 inserted implants, 3 (1%) were lost during the


observation period. Two of the failures occurred before
abutment connection and one 6 yrs after connection of the
fixed prosthesis. The losses occurred in two patients,
neither of whom was a smoker. In spite of the implant
failures, both these patients, as well as all other patients,
had stable fixed mandibular implant-supported prostheses
at the last follow-up examination.
Bivariate correlations
The correlation analyses gave different results for the
smokers and non-smokers. Oral hygiene showed a moderate
(r = 0.5-0.6) and significant association with bone loss at all
examinations in the smokers, while it was not significant in
the non-smokers (Table 4).
In the smokers, correlation coefficients of similar
strength (r = 0.5-0.6) were also found between the number
of cigarettes per day and bone loss. The correlation between
number of cigarettes smoked per day and oral hygiene was
0.56 (P < 0.01), indicating that high consumers had poorer
oral hygiene than low consumers. One more variable,
duration of edentulousness before implant treatment,
showed significant, negative correlation to bone loss during
the first part of the follow-up period.
In the non-smokers, no significant correlations between bone
loss and the other variables were found. In the entire group,
smoking and oral hygiene but no other factors were
significantly correlated to the average bone loss. The correlation
between the bone loss up to 1 yr and from 1 to 10 yrs was r =
0.52 (P < 0.001) in the entire group, but differed between
smokers (r = 0.43) and non-smokers (r = 0.15).

Multiple linear regression models


In the models for the group as a whole,
smoking was the most important factor
associated with bone loss. In the one-year
model, smoking was the only significant
factor, and the model had an explanatory
value of 42% (R2 = 0.42). In the 10-year
model, not only smoking but also oral
hygiene was significant (Table 5). The
separate models for smokers and nonsmokers revealed that oral hygiene had a
greater influence on peri-implant bone loss
among smokers than among non-smokers.
Bite force was the second most important
factor among the smokers, while length of
cantilevers and pre-treatment ridge height
were significant factors among the nonsmokers. The predictive (R2) values were
higher in the smoking than in the nonsmoking group, and the models were not
significant for the non-smokers (Table 5).

Discussion

The outcome of this prospective study has


clearly shown the extremely favorable
results of treatment with osseointegrated
implants supporting fixed prostheses in the
mandible. However, the significant influence of smoking on
mandibular peri-implant bone loss was also evident. This is
not surprising, considering the negative effects of smoking in
other areas of the human body as well as in the oral cavity
(US Department of Health and Human Services, 1989). The
effect of cigarette smoking on tissues in the oral cavity has
also been well-established by many studies. Most of them
have focused on the periodontal tissues, and, in general,
smokers seem to have more marginal bone loss than nonsmokers. In the light of current knowledge of the effects of
smoking, the finding in this study that high consumers had
more bone loss than low consumers who had more than nonsmokers was a logical one. The underlying mechanisms,
however, are not yet completely understood (Thomson et al.,
1993). Many factors are involved in marginal bone loss in the
natural dentition. Long-term longitudinal studies on
marginal bone loss in humans are quite rare (Bolin et al.,
1987). Such studies are said to require an observation period
of at least 10 yrs for the results to be reliable, due to the
relatively slow progression of the alveolar bone loss. In the
present implant study, however, the effect of smoking on the
rate of bone loss was already evident at the one-year followup. This indicates that smoking may have an influence on
wound healing, as reported previously (Moseley et al., 1978;
Preber and Bergstrom, 1990), and perhaps on the initial
phase of osseointegration. Our long-term observations found
an ongoing increase in the difference in bone loss between
smokers and non-smokers. It should be noted, however, that
the bone loss, although markedly greater in smokers, did not
lead to any implant loss over the 10-year period in this group
of patients. On the average, the bone loss was extremely
small considering the long follow-up period. The only

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j Dent Res 76(10) 1997

Smoking and Bone Loss around Implants

1671

implant failure that occurred after Table 3. Marginal bone loss (mean and standard deviation, SD, in mm) around implants
prosthesis connection was probably with respect to smoking habits and oral hygiene
caused by trauma.
Oral
Obs. Time
Smokersa
Non-smokers
Information about smoking habits Hygiene
pb
(yrs)
Mean SD
n
Mean SD
n
was recorded at a careful interview
0-1
0.50
0.21
10
0.37 0.16
14
NSd
performed by the first author at the 10- Good
**
Poor
0-1
0.85
0.35
11
0.25 0.23
10
year examination. Notes on smoking
phc
*
NS
habits had previously been entered into
Good
0-3
0.67
0.23
10
0.47 0.20
14
*f
patients' records, but not always Poor
0-3
1.09
0.36
11
0.41 0.26
10
*
systematically. This was the reason
ph
NS
smoking was not included in the earlier
0-5/6
0.85
0.26
10
0.59 0.25
14
*
reports of this material (Lindquist, 1987; Good
Poor
0-5/6
1.26
0.39
11
0.54 0.23
10
*
Lindquist et al., 1988). The available
ph
***
NS
notes, however, were now used to check
Good
0-10
0.99
0.35
10
0.69 0.31
14
*
the answers to the interviews. All Poor
0-10
1.61
0.45
10
0.65 0.27
10
*
patients included in the study showed
ph
***
NS
consistent smoking habits during the
observation period. Cigarette smoking a Smokers and non-smokers are divided into two groups: those above (poor) and those
was the dominant mode of tobacco use. b P below (good) the median value of the oral hygiene index, ranging from 0 to 2.
the difference between smokers and non-smokers (right column).
Only minor fluctuations over time in the c phdenotes
denotes the difference between those with good and those with poor oral hygiene.
number of cigarettes smoked per day d NS = not significant.
were reported. Two subjects occasionally e ***p < 0.001.
smoked cigarillos during the observation f * 0.01 < P< 0.05.
period but only to a minor extent. This
oral hygiene, according to the multivariate analysis. Patients
was not considered a problem in the analyses.
with the combination of smoking and poor oral hygiene had
The importance of oral hygiene factors and the effect of
about three times greater bone loss after 10 yrs than nonmicrobiota on peri-implant tissues have been intensively
smokers. This suggests that when the importance of oral
studied during the last few years, but the results have not been
hygiene on peri-implant tissues is studied, smoking should be
consistent (Adell et al., 1986; Lekholm et al., 1986; Lindquist et
included as a factor in the analysis.
al., 1988; Lindhe et al., 1992; Quirynen, 1993; Leonhardt, 1996).
Although convincing documentation of the negative effects of
Bone
poor oral hygiene on implant
Go- Smokers poor oral hygiene
loss
success is scarce, most authors
Smokers good oral hygiene
-a-mm
and textbooks stress the
- Nonsmokers good oral hygiene
importance of good oral hygiene
- -0- - Nonsmokers poor oral hygiene
in implant patients. In a study
covering 6 yrs after implant
treatment, poor oral hygiene was
found to be associated with 1.5
increased peri-implant bone loss
(Lindquist et al., 1988). When
smoking habits were included in
the analysis of the same patient
material, now followed for 10 yrs,
1
the influence of poor oral hygiene
was less marked, and in nonsmokers the effect of poor oral
: : : : :6
hygiene was insignificant (Fig.).
4E)
Another observation indicating 0.5
-0- "
that poor oral hygiene might be
of less importance is the fact that
oral hygiene was much better
among the women than the men,
1 Years
but there was no significant
I
I
I
I
I
I
I
difference in bone loss between
3
5
10
the genders (Table 1). On the
other hand, the most important Figure. Mean marginal bonLe loss (mm) around implants with respect to smoking habits and oral
factor for increased peri-implant hygiene. Smokers and non-si,mokers are divided into two groups: those above (poor) and those below
bone loss in smokers was poor (good) the median value of t]:he oral hygiene index, ranging from 0 to 2.
...

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Lindquist et al.

Table 4. Significant (P < 0.05) correlation coefficients between mean ma:rginal bone loss
around implants after various periods and 7 other factors in smokers arad non-smokers
(there were no significant correlations among the non-smokers)
Follow-up periods in years
0-1
1-10
0-3
0-5/6
0-1t0
Smokers
0.54a
Oral hygiene
0.53a
0.57b
0.55b
0.64b
Number of cigarettes
0.49a
0.52a
0.56b
0.45a
0.5i6b
Length of edentulism -0.46a
-0.46a
Length of cantilevers
0.49a

Occlusal loading is another factor often


stated to be of importance for implant
survival. Theoretically, it is easy to show
the unfavorable biomechanical effects of,
for example, heavy loading, unstable
occlusion, and long cantilevers (Skalak,
1983; Rangert et al., 1989; Brunski and
Skalak, 1992). These statements are
primarily supported by anecdotal observations, and systematic long-term clinical
studies showing the consequences of such
Non-smokers
no significant correlations
factors are scarce, perhaps partly due to the
a 0.01 <P < 0.05.
fact that it is difficult for overload to be
b 0.001 < P < 0.01.
determined in the clinical setting (Quirynen
et al., 1992; Carlsson, 1996). In a three- to sixLittle has been published about the association between
year report of the data from this study, there
smoking and implant failure and between smoking and was some evidence that factors indicating heavy or
bone loss around dental implants. In fact, a search of the
unfavorable occlusal loading (reported tooth clenching,
Medline system revealed only four studies concerning
increased dental wear, long cantilever extensions) were
dental implants and smoking between 1992 and May, 1996,
associated with increased peri-implant bone loss (Lindquist
and no publications before 1992. Two retrospective studies
et al., 1988). The dominating role of smoking found in this 10(Bain and Moy, 1993; De Bruyn and Collaert, 1994) showed a
year follow-up may have masked the effects of other factors,
connection between cigarette smoking and failures of dental
e.g., biomechanics and loading. The recording of increased
implants, while another investigation (Weyant, 1994), which dental wear at the first examinations was certainly associated
used a statistical logistic regression model on a large
with great occlusal forces, but the recording at the last
multicenter patient population, reported that patients' use of examination might not truly reflect long-term occlusal
tobacco negatively affected peri-implant soft tissue health
loading, since several of the prostheses including the
but not implant failure. Implant survival was associated
artificial teeth had been adjusted or replaced during the
with the medical status of the patient, the surface coating
observation period. Para-functional habits are known to
material of the implant, and surgical and healing
fluctuate over time and had obviously done so among our
complications after implant installation. Another
patients. In smokers, however, not only oral hygiene but also
multicenter study, including more than 2000 implants, bite force was a significant factor. In non-smokers, the
analyzed implant survival at stage 2 surgery. It was
lengths of the cantilever sections were of some importance
concluded that smoking is detrimental to implant success
according to the multivariate analyses. Nevertheless, the
(Gorman et al., 1994).
results showed convincingly that smoking had a greater
influence than factors indicating occlusal
loading on peri-implant bone loss.
Table 5. Significant associations with bone loss around implants ac cording to
The length of the pre-treatment period of
multiple regression models using 7 independent variables
edentulousness and the height of the edentulous
ridge were negatively correlated to the periGroup. Period
Pb
Sign. Factor
R2c
Model pd implant bone loss (Tables 4 and 5). This means
that subjects who had extensive ridge resorption
Whole Samplea
0-1 yr
Smoking
0.004
0.42
0.01
after long periods of denture-wearing at the time
0-10 yrs
Smoking
0.001
0.57
0.001
of implant treatment lost less bone around the
Oral hygiene
0.03
implants than those with better-preserved
ridges. Patient age was not significantly
Smokers
0-1 yr
Oral hygiene
0.004
0.74
0.03
correlated to peri-implant bone loss.
Bite force
0.03
A large patient population and multivariate
0-10 yrs
Oral hygiene
0.002
0.78
0.02
statistical methods are probably necessary for
Bite force
0.06
analysis of the relative importance of the
Non-smokers
numerous
factors that influence the long-term
0-1 yr
Length of cantilever
0.01
0.50
0.08
prognosis of osseointegrated implants. This
Oral hygiene
0.03
study has shown that smoking, which
0-10 yrs
Pre-treatment ridge
height
0.04
0.38
0.28
previously was seldom included in systematic
Length of cantilever
0.09
analyses of implant survival, was the most
factor of those correlated with
important
a cSenaratp
(-1
nv%A
ranctr.+mtr+ for
hnan
Ineer
A1l-rinczr
aaLtC mntilfNl
LlUUtlb wPrP
Wl-C LU>LlfULt:U
n-1n
lUF VUUtI JUSS alLg U-1 aCi U-1U
yrs
for
the
increased
peri-implant
bone loss. A clinical
whole sample and for smokers and non-smokers separately.
b P value for bivariate correlation.
implication
would
be
that
smoking habits
C
R2 exploratory value for the multiple linear regression model.
should be recorded and evaluated in the
d P value for the multiple linear
regression model.
examination of candidates for implant
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010

j Dent Res 76(10) 1997

Smoking and Bone Loss around Implants

treatment. Since good oral hygiene seemed to be able to


reduce the negative influence of smoking, the
recommendation that good oral hygiene be maintained in
implant patients is corroborated.
In conclusion, this study on edentulous patients provided
with osseointegrated mandibular implants has shown
extremely successful long-term results, with a loss of only
1% of the implants and a small mean peri-implant bone loss
of about 1 mm over a 10-year period. The marginal periimplant bone loss was greater in smokers than in nonsmokers and correlated to the amount of cigarette
consumption. In smokers, it was also greater in those with
poor than in those with good oral hygiene. Multivariate
analyses showed that smoking was the most important
factor for peri-implant bone loss. Poor oral hygiene also had
an influence, especially in smokers, while other factors
analyzed, e.g., those related to occlusal loading, were of
minor importance. These results indicate that smoking
habits should be included in analyses of implant survival
and peri-implant bone loss.

Acknowledgments
This study was supported by a grant (no. 9531) from Swedish
Match-Svenska Tobaks AB. We are indebted to Dr. Tommy
Johnsson, biostatistician, for help with the statistical analyses.

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