Professional Documents
Culture Documents
1667 Full
1667 Full
http://jdr.sagepub.com/
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
The online version of this article can be found at:
http://jdr.sagepub.com/content/76/10/1667
Published by:
http://www.sagepublications.com
On behalf of:
International and American Associations for Dental Research
Additional services and information for Journal of Dental Research can be found at:
Email Alerts: http://jdr.sagepub.com/cgi/alerts
Subscriptions: http://jdr.sagepub.com/subscriptions
Reprints: http://www.sagepub.com/journalsReprints.nav
Permissions: http://www.sagepub.com/journalsPermissions.nav
Citations: http://jdr.sagepub.com/content/76/10/1667.refs.html
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010
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
1667
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010
1668
Lindquist et al.
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.
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010
1669
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
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.
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010
1670
Lindquist et al.
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).
Discussion
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010
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.
...
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010
1672
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
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.
References
Adell R, Lekholm U, Branemark P-I (1985). Surgical procedures.
In: Tissue-integrated prostheses. Osseointegration in dinical
dentistry. Branemark P-I, Zarb GA, Albrektsson T, editors.
Chicago: Quintessence, pp. 211-232.
Adell R, Lekholm U, Rockler B, Branemark P-I, Lindhe J,
Eriksson B, et al. (1986). Marginal tissue reactions at
osseointegrated titanium fixtures. A 3-year longitudinal
prospective study. Int J Oral Maxillofac Surg 15:39-52.
Albrektsson T, Zarb GA, Worthington P, Ericsson AR (1986).
The long-term efficacy of currently used dental implants:
A review and proposed criteria for success. Int J Oral
Maxillofac Implants 1:11-25.
Arno A, Schei 0, Lovdal A, Waerhaug J (1959). Alveolar
bone loss as a function of tobacco consumption. Acta
Odontol Scand 17:3-10.
Bain CA, Moy PK (1993). The association between the failure
of dental implants and cigarette smoking. Int J Oral
Maxillofac Implants 8:609-615.
Bergstrom J, Eliasson S (1987). Cigarette smoking and
alveolar bone height in subjects with a high standard of
oral hygiene. J Clin Periodontol 14:466-469.
Bolin A, Lavstedt S, Frithiof L, Henriksson CO (1987).
Proximal alveolar bone loss in a longitudinal
radiographic investigation: IV. Smoking and some other
factors influencing the progress in individuals with at
least 20 remaining teeth. Gerodontics 3:43-46.
Bolin A, Eklund G, Frithiof L, Lavstedt S (1993). The effect of
changed smoking habits on marginal bone loss. Swed
Dent J 17:211-216.
1673
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010
1674
Lindquist et al.
Downloaded from jdr.sagepub.com at International Association for Dental Research on July 20, 2010