Daisuke Hinode
Shin-ichi Tanabe
Masaaki Yokoyama
Kenji Fujisawa
Eiji Yamauchi
Youji Miyamoto
Authors affiliations:
Daisuke Hinode, Shin-ichi Tanabe, Masaaki
Yokoyama, Department of Preventive Dentistry,
Institute of Health Bioscience, The University of
Tokushima Graduate School, Tokushima City,
Japan
Kenji Fujisawa, Department of Oral and
Maxillofacial Surgery, Tokushima University
Hospital, Tokushima City, Japan
Eiji Yamauchi, Department of Oral Care and
Clinical Education, Tokushima University
Hospital, Tokushima City, Japan
Youji Miyamoto, Division of Dentistry and Oral
Surgery, School of Medicine, Akita University,
Akita City, Japan
Correspondence to:
D. Hinode
Department of Preventive Dentistry
Subdivision of Stomatology
Division of Biosystem and Nutritional Science
Institute of Health Bioscience
The University of Tokushima Graduate School
Tokushima 770-8504
Japan
Tel.: 81 88 633 7337
Fax: 81 88 633 7338
e-mail: hinode@dent.tokushima-u.ac.jp
Date:
Accepted 5 October 2005
To cite this article:
Hinode D, Tanabe S-i, Yokoyama M, Fujisawa K,
Yamauchi E, Miyamoto Y. The influence of smoking on
osseointegrated implant failure: a meta-analysis.
Clin. Oral Impl. Res. 17, 2006; 473478
doi: 10.1111/j.1600-0501.2005.01244.x
Copyright r Blackwell Munksgaard 2006
Influence of smoking on osseointegrated
implant failure: a meta-analysis
Key words: implant failure, meta-analysis, smoking
Abstract: The aim of this study was to examine the influence of smoking on osseointegrated
implant failure by performing a meta-analysis. A computerized literature search using
PubMed database (in English) and Japana Centra Revuo Medicina (in Japanese) was carried
out to identify all relevant studies. Among 175 studies identified and chosen for detailed
review, 19 were appropriate for inclusion in our meta-analysis. When smokers were
compared with non-smokers, odds ratio (OR) for osseointegrated implant failure was
significantly elevated (OR 2.17, 95% confidence intervals (CI), 1.672.83). Seven studies
were appropriate to examine the influence of intra-oral location (maxillary arch vs.
mandibular arch) of implant failure on smoking. The OR for implant failure occurring in the
maxillary arch was significantly elevated (OR 2.06, 95% CI, 1.612.65), whereas the OR in the
mandibular arch did not demonstrate a significant increased risk associated with smoking
(OR 1.32, 95% CI, 0.722.4). Our meta-analysis revealed a significant relationship between
smoking and the risk of osseointegrated implant failure, more particularly those implants
located in the maxillary arch.
The success of osseointegration between an accounting for the majority of the differ-
endosseous titanium implant and bone can ence.
be expected. Failure to achieve osseointe- On the contrary, Bain et al. (2002) re-
gration and loss of acquired osseointegra- cently reported that no difference in im-
tion has been related to several factors such plant failure between smoking and non-
as the length, diameter and surface rough- smoking groups was detected. Kumar et
ness of the fixture, overloading and infec- al. (2002) also showed that the success rate
tion (Esposito et al. 1998a, 1998b). A was not significantly different between
literature review revealed that information smokers and non-smokers when the suc-
related to the effect of smoking on endoss- cess was defined as no clinical signs or
eous dental implants is poorly described. symptoms of peri-implant pathosis, no
Wallace (2000) has demonstrated the dele- clinically visible mobility and no evidence
terious effect of tobacco use on implant of bone loss.
treatment, and proposed that smoking To clarify the relationships between smok-
should be considered a relative contraindi- ing habit and osseointegrated implant failure,
cation to implant placement when plan- we conducted a meta-analysis of published
ning treatment. Johnson & Hill (2004) epidemiological reports. In addition, we ex-
reported that implant failure in smokers amined the influence of intra-oral location
is twice as much as those in non-smokers, (maxillary arch vs. mandibular arch) of os-
with a higher failure rate in maxillary arch seointegrated implant failure in smokers.
473
Hinode et al . Smoking and implant failure

Material and methods 1. Test of heterogeneity (Q statistic test)

Literature search
Studies with potential relevance for our Random effects model Fixed effects model
meta-analysis were identified by using (DerSimonian-Laird method) (general variance-based method)
both exploded MeSH heading and text
words in search of MEDLINE (online 2. Sensitivity analysis
PubMed 1993 to August 2004) and Japana 1) study design (cohort versus case-control study)
Centra Revuo Medicina (19932003) data- 2) year of publication (before 2000 versus after 2000)
bases. The main search terms were smok- 3) case number (less than 200 versus 200 or more)
ing, smoke and tobacco in combination 4) success rate (less than 90% versus 90% or more)
with implant. Additional articles of po-
3. Analysis of the potential for publication bias
tential relevance were identified in current
1) formal tests by Beggs method
journals (Dentistry in Japan, 19932004,
2) Fail-Safe N statistical measure
Japan Printing Co., Ltd, Tokyo, Japan and
Clinical Research in Dentistry, 2004,
Quintessence Publishing, Tokyo, Japan).
Synthesized odds ratio Adjust synthesized odds ratio

Inclusion criteria Fig. 1. Key steps of statistical analysis.

Data extraction was performed by two of
the authors and the selected data were
entered into a standard evidence table.
Selected studies were limited to casecon-
trol and cohort studies that included data in
which smoking was examined as a risk
factor for the failure of osseointegrated
implant and variance for that estimate
were provided. Failures of implant can be
divided into biological failure, mechanical
failure, iatrogenic failure, and inadequate
patient adaptation as described by Esposito
et al. (1998a, 1998b). Several kinds of
definition of implant failure have been
reported by researchers. We chose the defi-
nitions of implant failure according to the
criteria of Bain & Moy (1993) with slight
modification. In brief, an implant was
considered to be a failure when it had
been removed for any reason, and showed
progressive bone loss assessed by radio-
graph. Furthermore, the data extracted
were entered into each table of the max-
illary arch or the mandibular arch when
this information was available. Studies
were excluded if they were case reports,
case series or reviews. When studies over-
lapped, only the largest data set, or the data
set with the most relevant data, was in-
cluded.
Statistical analysis
Figure 1 enumerates the key steps of the
statistical analysis of this study. The
strength of the relationship between smok-
ing and osseointegrated implant failure was
assessed by odds ratio (OR). All calcula-
tions for the meta-analysis were performed
using Microsoft Excel 2000 (Microsoft
Corporation, Redmond, WA, USA) or the
SPSS 11 for Windows statistical software
package (SPSS Inc., Chicago, IL, USA). We
used both random-effects and fixed-effects
models to derive the pooled OR from com-
binations of studies. Heterogeneity among
the studies was assessed using the Q-sta-
tistic test and by comparing random-effects
and fixed-effects estimates. A random-ef-
fects model (DerSimonianLaird method)
of meta-analysis was used if the P-value
was less than 0.05. When there was no
significant difference, we used a fixed-ef-
fects model (general variance-based
method). Statistical significance was
judged by using the OR and 95% confi-
dence interval (CI), and there was statisti-
cal significance if the 95% CI did not
include one.
A sensitivity analysis was conducted to
assess the friability of our findings with
respect to different assumptions as shown
in Fig. 1. It was performed on pooled out-
comes in terms of study design (cohort vs.
casecontrol study), year of publication
(before 2000 vs. after 2000), case number
(less than 200 vs. 200 or more) and the
ratio of implant failure (less than 10% vs.
10% or more). Estimates of OR and the
95% CI were calculated. To explore the
potential for publication bias, data were
examined by means of the formal tests
proposed by Beggs method (Begg & Ma-
zumdar 1994) in addition to the Fail-Safe n
statistical measure (Rosenthal 1979). The
Fail-Safe n is the number of unpublished
studies finding no association that would
be required to change a significant meta-
analysis result (based on the published
studies) to a non-significant result. If n is
more than 5 times the number of studies
plus 10, then in general publication bias is
not considered to be a problem.
Results
Of the 175 studies identified by our litera-
ture search in MEDLINE and Japana Cen-
tra Revuo Medicina databases, 19 were
chosen for detailed review. The number
of cases and selected study design charac-
teristics are shown in Table 1. Among
these, 12 casecontrol and seven cohort
studies were appropriate for inclusion in
our analysis. A significant heterogeneity
was demonstrated by the Q-statistic test
(Po0.05); therefore, a random-effects
model was used. The synthesized OR for
overall studies was 2.17 (95% CI: 1.67
2.83) with a range of 0.64 to 23.1 (Fig. 2).
No publication bias was confirmed by the
analysis of Beggs method (P40.1) and the
Fail-Safe n statistical measure (n 6954
5
19 10). Therefore, the result of the
synthesized OR for overall studies was not
adjusted.
By investigating dependence of OR on
study characteristics, we have already im-
plicitly examined sensitivity of results to
these characteristics (study design, year of
publication, case number and rate of im-
plant failure) as shown in Table 2. The

474 | Clin. Oral Impl. Res. 17, 2006 / 473478

 Hinode et al . Smoking and implant failure

Table 1. Characteristics of studies selected in meta-analysis aimed to examine the influence of smoking on osseointegrated implant failure
Author, the year of publish No. cases/ OR 95% CI Rate of Study Cigarette Diagnosis
no. controls (confidence implant design smoking of implant
interval) failure (%) failure
Bain & Moy (1993) 390/1804 2.54 1.743.72 5.93 Casecontrol nr r, bn
De Bruyn & Collaert (1994) 114/338 5.46 1.5719.02 2.43 Casecontrol nr r
Gorman et al. (1994) 646/1420 2.03 1.333.11 4.31 Cohort nr r
Minsk et al. (1996) 157/570 1.21 0.682.16 9.49 Casecontrol nr r
Wang et al. (1996) 13/70 0.98 0.195.02 15.66 Casecontrol nr r
Yamada et al. (1997) 389/347 2.08 1.044.18 5.3 Casecontrol nr r, bnn
Keller et al. (1999) 32/216 2.05 0.805.2 13.31 Casecontrol Current vs. never or former r
De Bruyn et al. (1999) 30/32 0.64 0.22.08 24.19 Cohort nr r
Jones et al. (1999) 126/217 4.06 1.3811.96 4.66 Casecontrol nr r
Wallace (2000) 72/115 2.68 1.046.91 10.70 Casecontrol nr r
Lambert et al. (2000) 959/1928 1.53 1.152.05 6.93 Cohort Current vs. never or former r
Kuroyama et al. (2001) 1522/2994 1.22 0.931.59 5.43 Casecontrol nr r
Geurs et al. (2001) 62/279 2.6 0.996.83 5.87 Casecontrol Current vs. never or former r
Widmark et al. (2001) 67/131 5.3 2.5311.12 20.2 Cohort nr r
Schwartz-Arad et al. (2002) 380/579 1.86 0.794.34 2.29 Cohort nr r
Kan et al. (2002) 70/158 2.76 1.166.62 10.09 Casecontrol Current vs. never or former r
Karoussis et al. (2003) 28/84 2.08 0.3313.12 4.46 Cohort nr r
Leonhardt et al. (2003) 31/13 3.5 0.3931.81 18.18 Cohort nr r
Shiratori & Isokawa (2003) 303/592 23.1 5.3998.9 2.68 Casecontrol nr r

vs., versus; nr, not reported; current, current smoker; quit, subject who quit smoking; never, subjects who had never smoked; r, removal; b, progressive bone
loss assessed by the radiograph; bn, bone loss in excess of 50% of the fixture length; bnn, progressive bone loss with mobility or pain.

Table 2. Distribution of odds ratio between

smoking and non-smoking
Group Studies OR (95% CI)
(n)
All study 19 2.17 (1.672.83)
Study design
Cohort 7 1.98 (1.313)
Casecontrol 12 2.36 (1.633.42)
Year of publication
Before 2000 9 2.05 (1.652.55)
2000 or more 10 2.50 (1.643.82)
Case numbers
Less than 200 6 2.57 (1.614.12)
200 After 13 2.12 (1.612.8)
Implant failure rate
Less than 10% 12 2.10 (1.562.82)
10% or more 7 2.53 (1.723.73)

synthesized OR of the subgroup by cohort

study and by casecontrol study was 1.98
(95% CI: 1.313) and 2.36 (95% CI:
1.633.42), respectively. Furthermore, the
synthesized OR of the subgroup (case num-
ber 4200, n 13) and the subgroup (im-
plant failure rate o10%, n 12) was 2.12
(95% CI: 1.612.8) and 2.1 (95% CI: 1.56
2.82), respectively. In subgroup based on
the year of publication, the synthesized OR
before 2000 (n 9) and after 2000 (n 10)
was 2.05 (95% CI: 1.652.55) and 2.5
Fig. 2. Random effects of the odds ratios of osseointegrated implant failure on smoking for individual studies
(95% CI: 1.643.82), respectively, and
and overall. The diamond symbol shows the odds ratio and the horizontal line represents the 95% confidence both of them revealed a significant differ-
intervals. ence between smokers and non-smokers.

475 | Clin. Oral Impl. Res. 17, 2006 / 473478

Hinode et al . Smoking and implant failure

Table 3. Studies selected in meta-analysis aimed to examine the influence of intra-oral location on osseointegrated implant failure
Author, the year In the maxillary arch In the mandible arch
of publication
No. cases/ OR 95% CI No. cases/ OR 95% CI
no. controls no. controls
Bain & Moy (1993) 196/883 2.78 1.784.34 194/921 1.99 0.904.39
Minsk et al. (1996) 84/285 1.41 0.732.72 73/285 0.55 0.122.45
Yamada et al. (1997) 175/131 2.36 0.846.68 214/216 1.77 0.684.6
De Bruyn et al. (1999) 30/32 0.64 0.22.08
Wallace (2000) 42/84 4.31 1.3413.83 30/31 1.04 0.195.59
Lambert et al. (2000) 478/793 1.78 1.192.66 481/1135 1.23 0.801.9
Shiratori & Isokawa (2003) 117/302 16.27 1.94136.66 186/290 27.20 3.58206.93

Sensitivity analysis for all studies did not
show much difference between study de-
sign, case number and the rate of implant
failure. Our meta-analysis of 19 studies
revealed a statistically significant associa-
tion between smoking and osseointegrated
implant failure by the results of the synthe-
sized OR.
The studies selected to investigate the
influence of intra-oral location (placed in
the maxillary or mandibular arch) are listed
in Table 3. The data of De Bruyn et al.
(1999) were entered into the table of the
maxillary arch, because the number of im-
plant failures in smokers and non-smokers
was only available in the maxillary arch.
Tests of homogeneity of implant failure in
seven papers selected were examined, and
no significant difference was found in the
maxillary arch. Then, the fixed-effects
model was used to calculate OR. The
synthesized OR of the maxillary arch was
2.06 (95% CI: 1.612.65). Beggs method
was carried out to explore the potential
publication bias, and the results of the
maxillary arch showed no significant dif-
ference. The Fail-Safe n calculation for the
maxillary analysis was 100 (45
7 10)
and publication bias was not considered to
be a large factor; therefore, the synthesized
OR of the maxillary arch was not adjusted.
On the other hand, tests of homogeneity of
implant failure in the mandibular arch
found a significant difference (Po0.05),
and the random-effects model was used.
The synthesized OR was 1.66 (95% CI:
0.893.09). No significant difference was
found by Beggs method whereas the Fail-
Safe n calculation for the maxillary analysis
was 28 (o5
6 10); therefore publica-
tion bias was considered to be a factor and
the synthesized OR of the mandibular arch
was adjusted (1.32 (95% CI: 0.722.4)).
Finally, analysis of implant failure on
smoking by the influence of intra-oral loca-
tion indicated an increased OR in the max-
illary arch but not in the mandibular arch.
Discussion
Sweet (1992) and Bain & Moy (1993)were
the first authors to report that smoking is a
risk factor for osseointegrated implant fail-
ure, and some prospective studies sup-
ported this relationship. However, several
recent studies have indicated no effect of
smoking on the survival of dental im-
plants (Esposito et al. 1998a, 1998b; Berge
& Gronningsaeter 2000; Carlsson et al.
2000; Lambert et al 2000; Quirynen et al.
2001). Although a meta-analysis study was
previously reported (Bain et al. 2002), no
evaluation using the synthesized OR esti-
mates has been published. Therefore, we
constructed and performed this study. Our
meta-analysis of the 19 studies examining
this relationship revealed a significant in-
creased risk for the implant failure among
smokers compared with that among non-
smokers (OR 2.17). Several casecontrol
studies and cross-sectional studies with
different case numbers and ratio of implant
failure have found similar associations.
Therefore, it confirmed a significant rela-
tionship between smoking and the risk of
osseointegrated implant failure.
In this report, we also attempted to
evaluate the location of the implant failure
on smoking by using a meta-analysis, and
found only seven studies that met the
inclusion criteria. There has been consider-
able discussion regarding implant location
and failure. In our analysis, the maxillary
arch showed a statistically significant in-
crease in the implant failure in smokers
compared with non-smokers; however, the
mandibular arch did not show any differ-
ence. Factors contributing to higher im-
plant failure in maxillary arch than in
mandibular arch are not yet understood.
The high implant failure rate observed in
the maxilla suggests that bone density may
have some bearing upon early implant fail-
ure (Friberg et al. 1991). In addition, smok-
ing has been reported to be the strongest
risk factor for periodontal bone loss (Pau-
lander et al. 2004). On the other hand, it
has been reported that the short-term prog-
nosis is greatly affected by peri-implant
infection related to smoking (Mau 1993;
De Bruyn & Collaert 1994; Gorman et al.
1994). Reibel (2003) suggested that the
increase of implant failures in smokers is
due to exposure of peri-implant tissue to
tobacco smoke, possibly linking the smok-
ing effects on implant survival to the smok-
ing effects on peri-implantitis. Haffajee &
Socransky (2001) showed that a greater
difference in prevalence of orange and red
bacterial complexes (both complexes in-
clude periodontopathogens) exists at sites
with periodontal pocket in the maxilla in
comparison with the mandibular in both
smokers and non-smokers. Smoking might
thus modulate the implant failure by
influencing bacterial infections in the max-
illary and the mandibular arches differ-
ently.
Using meta-analysis, it has been demon-
strated in this study that smoking has
significant negative effects on the survival
rate of dental implants. Dentists have an
important role to play in preventing the
effects of smoking in osseointegrated im-
plant failure and tobacco-related oral dis-
eases. Reibel (2003) suggested in his review
that practitioners should pursue more for-
mal training in smoking cessation counsel-
ing, which should be as much a part of
their job as plaque control and dietary
advice. The evidence presented in this

476 | Clin. Oral Impl. Res. 17, 2006 / 473478


study may contribute to develop tobacco
intervention habits by dental practitioners.
Several investigators have reported that
the surface roughness of implants (fixture)
also represents a factor of implant failure
(Kumar et al. 2002; Feldman et al. 2004).
Feldman et al. (2004) reported that there
was a 9% difference in 5-year cumulative
survival rates in the maxilla between ma-
chined-surfaced short-length (86.8%) and
dual acid-etched short-length implants
(95.8%). It has recently been reported that
no significant difference of the effect of
smoking on achieving initial osseointegra-
tion exists when surface-modified dental
implants were used (Kumar et al. 2002). In
the systematic review of Bain et al. (2002),
93.5% of success rate in smokers for the
implant group with smooth surface and
98.7% for the implant group with rough
surface was observed, a clinically relevant
difference between these two groups. Be-
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