Moraschini 2015

YIJOM-3245; No of Pages 11
Int. J. Oral Maxillofac. Surg. 2015; xxx: xxxxxx

http://dx.doi.org/10.1016/j.ijom.2015.08.996, available online at http://www.sciencedirect.com
Systematic Review
Dental Implants
Success of dental implants

in smokers and non-smokers:
a systematic review and metaanalysis
V. Moraschini , E. dS. PortoBarboza

Department of Periodontology, School of
Dentistry, Fluminense Federal University,
Rio de Janeiro, Brazil
V. Moraschini E. dS. Porto Barboza: Success of dental implants in smokers and nonsmokers: a systematic review and meta-analysis. Int. J. Oral Maxillofac. Surg. 2015;
xxx: xxxxxx. # 2015 International Association of Oral and Maxillofacial Surgeons.
Published by Elsevier Ltd. All rights reserved.
Abstract. The purpose of this review was to test the null hypothesis of no difference in
marginal bone loss and implant failure rates between smokers and non-smokers
with respect to the follow-up period. An extensive electronic search was performed
in PubMed, Web of Science, and the Cochrane Central Register of Controlled Trials
to identify relevant articles published up to February 2015. The eligibility criteria
included randomized and non-randomized clinical studies. After an exhaustive
selection process, 15 articles were included. The meta-analysis was expressed in
terms of the odds ratio (OR) or standardized mean difference (SMD) with a
confidence interval (CI) of 95%. There was a statistically significant difference in
marginal bone loss favouring the non-smoking group (SMD 0.49, 95% CI 0.07
0.90; P = 0.02). An independent analysis revealed an increase in marginal bone loss
in the maxilla of smokers, compared to the mandible (SMD 0.40, 95% CI 0.240.55;
P < 0.00001). A statistically significant difference in implant failure in favour of
the non-smoking group was also observed (OR 1.96, 95% CI 1.682.30;
P < 0.00001). However, the subgroup analysis for follow-up time revealed no
significant increase in implant failure proportional to the increase in follow-up time
(P = 0.26).
Dental implants have a high rate of survival

and success1; however, certain local and
systemic conditions are known to cause
dental implant failures. Factors such as
low insertion torque (e.g. poor quality bone,
poor surgical skill, inaccurate drilling), peri-implant disease, smoking, diabetes, and
bisphosphonate use have been reported
0901-5027/000001+011
previously as some of the possible causes

of dental implant failure.2,3
Some studies have shown that the nicotine absorbed by the oral mucosa in smokers can negatively affect periodontal tissue
healing and peri-implant health.46 The
risk mechanisms involving tobacco intake
are yet to be fully elucidated; however, it
Key words: dental implants; smoking; tobacco;

implant survival; marginal bone loss; metaanalysis.
Accepted for publication 27 August 2015
is believed that the negative influence of

tobacco is linked to the adverse effects on
fibroblast function, reduced collagen production, and an increase in vascular problems.7,8 Moreover, tobacco can exert a
negative effect on immune function, interfering with the chemotaxis and phagocytosis mechanisms of polymorphonuclear
# 2015 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Moraschini V, Barboza ESP. Success of dental implants in smokers and non-smokers: a systematic
review and meta-analysis, Int J Oral Maxillofac Surg (2015), http://dx.doi.org/10.1016/j.ijom.2015.08.996
Moraschini and Barboza
neutrophils, and decreasing immunoglobulin production and functioning of lymphocytes.9,10 There is still no consensus on
the number of cigarettes smoked and the
relationship with implant failure, however
heavy smokers may exhibit a higher incidence.6
Some longitudinal studies have reported
a higher rate of implant failure in smoking
patients.1115 However, these failures are
subject to many factors, such as a history
of periodontitis, hormonal or metabolic
diseases that affect bone turnover, diseases that favour infection, characteristics
of the implant used (shape and surface
treatment), and prosthetic factors, such
as the loading protocol and type of occlusion. It is rather difficult to interpret the
data and reduce the bias, as all of these
factors interact with each other.
The goal of this meta-analysis was to
compare marginal bone loss and the failure of implants during different follow-up
periods between smokers and non-smokers.
Materials and methods
The methodology of this study was

adapted from the PRISMA statement (Preferred Reporting Items for Systematic
Reviews and Meta-analyses).16 The clinical questions were divided and categorized according to the PICO strategy
(Patient, Intervention, Comparison, and
Outcome).17
Objective
The purpose of this review was to test the

null hypothesis of no difference in marginal bone loss or implant failure rates
between smokers and non-smokers,
depending on the follow-up period.
Search strategy
Quality assessment
A comprehensive electronic search was

conducted, with no date or language
restrictions, in PubMed, Web of Science,
and the Cochrane Central Register of Controlled Trials, up to February 2015. The
search strategy and the PICO tool are
presented in Table 1. In addition, references of the studies included (crossreferencing) was also performed to obtain
further new studies.
The analysis of quality of the non-randomized studies (prospective and retrospective

cohort studies) included in this review was
performed using the NewcastleOttawa
scale (NOS). For the categories of selection and outcome, studies may obtain a
star/point for each item. For the comparability category, two stars/points may be
awarded. The highest score that could be
assigned to a study according to the NOS
was nine stars/points (highest scientific
evidence). Studies scoring six stars/points
and above were considered to be of high
quality.
Selection criteria
This review sought prospective and retrospective cohort studies, as well as randomized controlled trials (RCTs) that
compared the marginal bone loss and implant failure rates between smokers and
non-smokers. For this review, implant
failure was regarded as the absolute loss
of the implant. The exclusion criteria included animal studies, in vitro studies, and
case series, case reports, and reviews. In
addition, studies conducted on volunteers
with unbalanced metabolic diseases, or
with periodontal disease without prior
treatment, were excluded.
Screening process
The research and screening processes

were conducted by both reviewers
(V.M.F. and E.P.B.). The titles and
abstracts were first analyzed. The second
step involved the selection of full papers
for careful reading; these were analyzed
according to the eligibility criteria (inclusion/exclusion) for future data extraction.
Disagreements between the reviewers
were resolved through careful and detailed
discussions. Agreement between the two
reviewers was evaluated statistically with
Cohens kappa (k) test. The authors of the
studies were contacted via e-mail for clarification of any points, when required.
Data extraction
The following data were extracted from

the studies included (when available):
authors, publication year, follow-up period, number of subjects, gender and age of
the subjects, smoking status, number of
implants placed, implant system, implant
length and diameter, healing period, days
of antibiotic prophylaxis, use of mouth
rinse, marginal bone loss, implant survival, failed and placed implants, P-value for
implant failure rate, and the number of
drop-outs. This review regarded anyone
who consumed any quantity of tobacco at
any time during the surgery and recovery
period to be a smoker.
Statistical analysis
Binary and continuous variables from the

studies included were analyzed through
meta-analysis when the same type of data
was assessed by at least two studies. For
binary outcomes (e.g. implant failure), the
estimate of the intervention effect was
expressed in the form of an odds ratio
(OR) with a confidence interval (CI) of
95%. For continuous outcomes (e.g. marginal bone loss), the average and standard
Table 1. Systematic search strategy (PICO strategy).

Search strategy
Population
#1
(edentulous partially[MeSH] OR edentulous[MeSH] OR edentulous jaw[MeSH] OR edentulous
maxilla*[all fields] OR edentulous mandible*[all fields] OR smoke*[all fields] OR smokers*[all
fields] OR nonsmokers*[all fields])
Intervention
#2
(implant*[all fields] OR dental implant[MeSH] OR single implant*[all fields] OR multiple
implant*[all fields] OR immediate loading*[all fields] OR conventional loading*[all fields])
Comparisons
#3
(smokers*[all fields] OR nonsmokers*[all fields])
Outcomes
#4
(survival*[all fields] OR implant survival*[all fields] OR dental implant survival*[all fields] OR
bone loss[MeSH] marginal bone loss*[all fields] OR implant bone resorption*[all fields] OR
dental implant bone loss*[all fields])
Search combination
#1 AND #2 AND #3 AND #4
Database search
Language
Electronic databases
No restriction
MEDLINE/PubMed, Web of Science, and Cochrane Central Register of Controlled Trials
Medline/PubMed
Records identified through
database searching
(n = 965)
Cochrane (CENTRAL)
database searching
(n = 85)
Included
Web of Science
database searching
(n = 240)
Records excluded
(n = 1261)
Full-text articles assessed for
eligibility (n = 29)
Eligibility
Screening
Identification
Success of implants in smokers and non-smokers
Full-text articles excluded

(n = 14)
Studies included in the present

meta-analysis
(n = 15)
14 full-text articles excluded:

3 animal studies
4 did not compare smokers vs. non-smokers
2 evaluated groups with decompensated diseases
5 did not report the number of implants/group
Fig. 1. Flow diagram (PRISMA format) of the screening and selection process.
deviation (SD) were used to calculate the

standardized mean difference (SMD) with
a 95% CI. The results were pooled using
the fixed-effects model (MantelHaenszelPeto test) or random-effects model
(DerSimonianLaird test). The I2 statistical test was used to express the percentage
of heterogeneity in the studies. Values up
to 25% were classified as indicating low
heterogeneity, values of 50% as indicating
medium heterogeneity, and values of
70% as indicating high heterogeneity.
The results of the random-effects model
were validated when significant heterogeneity was observed (P < 0.10). The fixedeffects model was considered when low
heterogeneity was observed. The level of
statistical significance was set at P < 0.05.
Publication bias was explored graphically through a funnel plot. Asymmetry in
the funnel plot may indicate possible publication bias.
All data were analysed using the statistical software Review Manager version
5.2.8 (The Nordic Cochrane Centre, The
Cochrane Collaboration, Copenhagen,
Denmark; 2014).
Results
Literature search
The initial search yielded 965 titles from

Medline/PubMed, 85 titles from the
Cochrane Central Register of Controlled
Trials, and 240 titles from the Web of
Science. After the initial evaluation, 29
full papers were selected. Fourteen studies

were excluded after careful reading, as
they did not conform to the eligibility
criteria of this review. Therefore, 15 studies published between 1993 and 2013 were
included in this meta-analysis.6,11,12,14,18
28
The selection process and the grounds
for exclusion of studies are presented in
Fig. 1.
The k value for agreement between the
reviewers for the inclusion of potential
studies (titles and abstracts) was 0.79
and for selected articles was 0.85, demonstrating a substantial agreement between
the reviewers for inclusion of potential
articles and an almost perfect concordance for studies selected, according to the
criteria proposed by Landis and Koch.29
used implant system.6,14,21,23,28 In one

study, all patients received implants in
areas of bone regeneration18; another
study included patients susceptible to periodontal disease (which was clinically controlled).28
Ten studies reported a statistically significant difference in the average number
of implant failures between smokers and
non-smokers6,12,14,18,20,22,2528; the difference was not statistically significant in
only one study.24 With regards to postsurgical care, two studies reported the use
of antibiotic prophylaxis,12,25 while only
one provided information related to the
prescription of chlorhexidine mouthwash.25
Quality assessment
Study characteristics
The characteristics of the studies included

are presented in Table 2. Five prospective
studies11,12,1921 and 10 retrospective cohort studies6,14,18,2228 were included. The
number of participants in the studies ranged from 60 to 1727, and the average age
was 52.5 years. The follow-up period ranged from 8 to 240 months. The number of
implants installed in smokers was 5840
and in non-smokers was 14,683. The number of implants installed in the groups was
not clearly reported in one article.23
Implants were installed without surface
treatment in four studies.6,14,21,23 The Branemark system (Nobel Biocare AB, Goteborg, Sweden) was the most commonly
Only two studies obtained a score of less

than six stars.20,24 The scores for each
study are summarized in Table 3.
Marginal bone loss
Seven studies reported on the analysis of

marginal bone loss.11,14,21,22,2628 All studies performed this analysis via radiographic
measurements of the implant platform in
relation to the alveolar bone crest. The
marginal bone loss in the group of smokers
ranged from 0.07 to 2.7 mm; in the nonsmoking group, the marginal bone loss
ranged from 0.04 to 3.13 mm. The analysis
of marginal bone loss among the groups
was performed using the random-effects
No. of
subjects
No. per
group
Bain and Moy (1993)6
Retrospective
72
540
NR
Haas et al. (1996)14
Retrospective
Up to 108
Kan et al. (1999)18
Age range
Mean age
Gender
Implant brand
Surface
Implant
size (mm)
(diameter
length)
Smoking definition
No. of implants
1385
55.1
229 M/311 F
Smoker and non-smoker
2194
Branemark
Machined
NR 7,
10, 13,
15, 18, 20
421
107 (G1)/
314 (G2)
1688
53.1
171 M/250 F
1366
Branemark, Friatec
Machined, rough
NR NR
Retrospective
41.6
60
16 (G1)/
44 (G2)
4184
64.6
27 M/33 F
Low consumption (<15

cigarettes/day); high
consumption (15
cigarettes/day)
228
NR
NR
NR NR
Lambert et al. (2000)19
Prospective
36
>800
NR
3089
NR
NR
Smoker and never smoker
2887
NR
NR
NR NR
Kumar et al. (2002)20
Prospective
18
461
72 (G1)/
389 (G2)
NR
NR
NR
Smoker consisted of
patients who smoked half
a pack or more cigarettes a
day
1183
Straumann
Rough
NR NR
Schwartz-Arad et al.
(2002)12
Prospective
36
261
89 (G1)/
172 (G2)
1867
48
NR
Non-smokers; mild
smokers (up to 10
cigarettes/day); heavy
smokers (>10 cigarettes/
day)
959
NR
NR
NR NR
Nitzan et al. (2005)11
Prospective
9.486.6
(mean 45.5)
161
59 (G1)/
102 (G2)
2389
57
NR
Non-smokers; mild
smokers (up to 10
cigarettes/day); heavy
smokers (>10 cigarettes/
day)
646
NR
NR
NR NR
DeLuca and Zarb

(2006)21
Prospective
Up to 240
200
54 (G1)/
146 (G2)
1577
52.1
NR
1539
Branemark
Machined
NR NR
Sanchez-Perez et al.
(2007)22
Retrospective
60
66
40 (G1)/
26 (G2)
1571
43.4
NR
Non-smokers; light
smokers (<10 cigarettes/
day); moderate smokers
(1020 cigarettes/day);
heavy smokers (>20
cigarettes/day)
165
Biotech
Rough
NR NR
Authors (year)
Study design
Follow-up
time in
months
(mean or
range)
Table 2. Main characteristics of the studies selected.
Authors (year)
Study design
Follow-up
time in
months
(mean or
range)
No. of
subjects
No. per
group
Age range
Mean age
Gender
Smoking definition
No. of implants
Implant
size (mm)
(diameter
length)
Implant brand
Surface
Balshe et al. (2008)23
Retrospective
130
1498
199 (G1)/
1299 (G2)
1492
49.7
637 M/861 F
4607
Branemark, Nobel
Biocare
Machined, rough
3.3, 3.75, 4,
5 7, 8.5, 10,
11.5, 13, 15,
18, 20
Sverzut et al. (2008)24
Retrospective
8
650
76 (G1)/
574 (G2)
1384
42.7
NR
1628
NR
NR
Cavalcanti et al. (2011)25
Retrospective
60
1727
549 (G1)/
1178 (G2)
1785
49.2
702 M/1025 F
5843
Biomet 3i, Astra Tech,

Camlog, FriadentDentsply, Nobel Biocare,
Straumann, Sweden and
Martina, Zimmer Dental
Rough
NR NR
Vandeweghe and De
Bruyn (2011)26
Retrospective
60
329
41 (G1)/
288 (G2)
1884
54
141 M/188 F
712
Southern Implants
Rough
3.5, 3.75, 4, 4.3,

5, 6 8.5, 10, 10.5,
11.5, 12, 13, 13.5,
15, 16.5, 18
Vervaeke et al. (2012)27
Retrospective
24
300
65 (G1)/
235 (G2)
1782
56
114 M/186 F
1093
NR
NR
3.5, 4, 4.5, 5 8,
9, 11, 13, 15, 17
Sayardoust et al. (2013)28
Retrospective
60
80
40 (G1)/
40 (G2)
NR
57.6
38 M/42 F
80
Branemark; Nobel
Biocare
Rough
NR
Healing period
for loading
(months)
Antibiotics/mouth
rinse (days)
Marginal bone loss

(mm) (mean SD)
Implant survival
rate (%)
Failed/placed
implants
P-value (for implant

failure rate)
Drop-outs
6 (maxilla)
3 (mandible)
NR
NR
88.7 (G1)
95.2 (G2)
44/390 (G1)
86/1804 (G2)
<0.001
NR
3 to 7
NR
2.7 1.87 (G1)

1.58 1.42 (G2)
NR
NR/366 (G1)
NR/1000 (G2)
NR
NR
Kan et al. (1999)18
NR
NR
NR
65.3 (G1)
82.7 (G2)
12/70 (G1)
11/158 (G2)
0.027
NR
NR
NR
91.1 (G1)
94 (G2)
85/959 (G1)
115/1928 (G2)
NR
NR
1 to 3
NR
NR
97 (G1)
98.3 (G2)
8/269 (G1)
15/914 (G2)
<0.05
NR
Table 2 (Continued )
Antibiotics/mouth
rinse (days)
Marginal bone loss

(mm) (mean SD)
Implant survival
rate (%)
Failed/placed
implants
P-value (for implant

failure rate)
Drop-outs
Schwartz-Arad et al. (2002)
NR
7/NR
NR
96 (G1)
98 (G2)
15/380 (G1)
12/579 (G2)
<0.05
NR
NR
NR
0.15 0.09 (G1)

0.04 0.04 (G2)
NR
NR
NR/271 (G1)
NR/375 (G2)
NR
NR
DeLuca and Zarb (2006)21
6 (maxilla)
3 (mandible)
NR
0.07 0.26 (G1)

0.04 0.12 (G2)
NR
NR
NR/494 (G1)
NR/1045 (G2)
NR
NR
Sanchez-Perez et al. (2007)22
NR
NR
2.41 1.46 (G1)

3.13 1.59 (G2)
84.2 (G1)
98.6 (G2)
15/95 (G1)
1/70 (G2)
<0.001
NR
NR
NR
NR
91.2 (G1)
95.2 (G2)
NR
NR
23
NR
NR
NR
96.6 (G1)
97.1 (G2)
7/197 (G1)
43/1431 (G2)
0.5994
NR
0 to 9
5/14
NR
94.5 (G1)
97.1 (G2)
107/1961 (G1)
112/3882 (G2)
0.003
250
Vandeweghe and De Bruyn

(2011)26
NR
NR
1.56 0.53 (G1)

1.32 0.38 (G2)
95.2 (G1)
98.8 (G2)
5/104 (G1)
7/608 (G2)
0.007
NR
NR
NR
0.53 0.92 (G1)

0.29 0.54 (G2)
96.7 (G1)
98.7 (G2)
8/244 (G1)
11/849 (G2)
0.025
3 to 4
NR
1.39 1.57 (G1)

1.01 1.09 (G2)
89.6 (G1)
96.9 (G2)
4/40 (G1)
1/40 (2)
<0.05
12
M, male; F, female; NR, not reported; SD, standard deviation; G1, smokers; G2, non-smokers.
Healing period
for loading
(months)
Table 2 (Continued )
A study can be awarded a maximum of one star for each item within the selection and outcome categories. A maximum of two stars can be given for comparability.
Two years of follow-up was chosen to be sufficient for the outcome survival to occur.
7/9
7/9
0
0
*
*
0
0
*
*
*
*
**
**
*
*
*
*
Total 9/9
0
0
*
0
0
0
0
0
0
*
0
*
0
*
*
*
*
0
*
*
*
*
*
0
*
*
*0
*0
*0
*0
*0
*0
*0
*0
**
*0
*0
*0
**
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*

Kan et al. (1999)18
Schwartz-Arad et al. (2002)12
DeLuca and Zarb (2006)21
Sanchez-Perez et al. (2007)22
Vandeweghe and
De Bruyn (2011)26
0
0
0
*
0
0
0
0
*
0
0
*
0
Ascertainment
of exposure
Representativeness
of the exposed
cohort
Selection of
external
control
Outcome of
interest not
present at start
*
*
*
*
*
*
*
*
*
*
*
*
*
Adequacy of
follow-up
of cohorts
Was follow-up
long enough
for outcomes
to occur?b
Assessment
of outcome
Outcome
Comparability
Comparability
of cohorts on
the basis of the
design or analysisa
Selection
Authors (year)
Table 3. Quality assessment of the studies using the NewcastleOttawa scale.
6/9
6/9
7/9
7/9
5/9
6/9
6/9
6/9
8/9
7/9
5/9
8/9
7/9
model because of the considerable amount

of heterogeneity observed (I2 = 98%;
P < 0.00001). An SMD of 0.49 (95% CI
0.070.90) was observed, showing a statistically significant difference in favour of
non-smokers (P = 0.02; Fig. 2). Four studies analyzed the marginal bone loss between the maxilla and mandible in
smokers.11,14,26,27 The fixed-effects model
was used for this analysis, as there was no
evidence of heterogeneity (I2 = 0%;
P = 0.47). An SMD of 0.40 (95% CI
0.240.55) was observed, showing a statistically significant difference in favour of
the mandible (P < 0.00001; Fig. 3).
Implant failure rate
The number of implant failures in relation

to each measured group was not clearly
reported in four studies.6,11,21,23 The average survival of implants varied from
65.3% to 97% in the group of smokers,
and from 82.7% to 98.8% in the group of
non-smokers. The results of the analysis of
implant failure were classified into subgroups according to the follow-up time:
1.1.1 for 1 year, 1.1.2 for t < 2 years,
1.1.3 for t < 3 years, 1.1.4 for t < 4 years,
and 1.1.5 for t 5 years. The fixed-effects
model was used for this analysis because
of the lack of evidence of heterogeneity
(I2 = 20%; P = 0.26). The total OR for the
subgroups examined was 1.96 (95% CI
1.682.30), demonstrating a statistically
significant difference in favour of the
non-smoking group (P < 0.00001). However, these results did not demonstrate a
significant increase in implant failure with
the increase in follow-up time (P = 0.26).
The OR for each subgroup examined is
given in Fig. 4.
Publication bias
An analysis of implant failure revealed

symmetry of the funnel plot, therefore
rejecting the possibility of publication bias
(Fig. 5).
Discussion
This review attempted to identify studies

comparing the marginal bone loss and rate
of implant failure between smokers and
non-smokers. The search yielded only
prospective and retrospective cohort studies. It was therefore not possible to include
an RCT. The absence of RCTs in a metaanalysis can increase the risk of bias.30
However, the inclusion of a large number
of longitudinal observational studies in a
meta-analysis can increase the amount of
Fig. 2. Forest plot for the event marginal bone loss.
Fig. 3. Forest plot for the event marginal bone loss between the maxilla and mandible in smokers.
Fig. 4. Forest plot for the event implant failure rate.
Fig. 5. Funnel plot for the studies reporting the outcome event implant failure rate.
information and consolidate the results

from the clinical surveys.31
Tobacco smoking is an accepted potential risk factor for oral health. Several
clinical studies have shown that the survival of implants can be affected by tobacco usage. However, the quantity and
frequency of cigarettes consumed (or
packs per year) can be a key factor in
determining the predictability of the
implants. Only five studies included in
this review defined or classified smokers11,12,18,20,22; this is a critical factor for
data interpretation. Currently, there is no
standardization in the classification of
patients regarding the number of cigarettes
smoked per day. Five different types of
classification in relation to smoking were
used by the studies, i.e. smoker and nonsmoker6,14,21,2328; smoker and never
smoker19; low consumption and high consumption18; non-smokers, mild smokers,
and heavy smokers11,12,22; and one study
considered smokers who smoked half a
pack or more of cigarettes a day.20 In addition, other risk factors (confounding factors) are known to influence the results by
generating publication bias.1,2 There is still
no consensus in the literature regarding the
procedures that can minimize the risk of
smoking on the health of implants. Choosing to leave the implant submerged during
the healing period would decrease the physical contact with the smoke and prevent the
accumulation of bacterial biofilms on the
upper surface, which would facilitate healing of the implant, as it is already known
that smoking patients tend to display greater
bacterial biofilm adhesion.13 In addition,

effecting improvements in the gingival phenotype (increasing the area of keratinized
gingiva) in the areas adjacent to the implant
would be a prudent measure, as demonstrated in previous studies.32,33
As tobacco can affect immune function,9,10 patients susceptible to periodontal
disease may present a greater risk of biological complications, such as mucositis
and peri-implantitis, and a higher rate of
marginal bone loss, as demonstrated by a
study included in this review.28 However, a
recent meta-analysis that evaluated the interaction between smoke and peri-implantitis concluded that there is low evidence
implicating smoking as a risk factor for the
development of peri-implant disease.34
The study by Kan et al.18 assessed the
effect of smoking on 228 implants installed
in areas of bone regeneration. After the
follow-up period (average 41 months),
the authors reported a significantly higher
implant success rate among non-smokers
(82.7%) compared to smokers (65.3%). The
negative impact of tobacco on implants
installed in graft areas was also reported
in a systematic review conducted by Chambrone et al.35 There is growing evidence in
the medical literature indicating that smoke
ingredients, such as the nicotine, may delay
or inhibit bone healing after surgery.36,37
The most accepted theory for the influence
of smoking on healing in grafted areas is the
decrease in local blood flow resulting from
vasoconstriction, which in turn causes
changes in the cell numbers and the inflammatory process (repair).8,38
The marginal bone loss was significantly

higher in smokers compared to non-smokers (P = 0.02). A comparison of the dental
arches revealed the highest level of resorption in the maxillary arch (P < 0.00001).
No other systematic review has compared
marginal bone loss between smokers and
non-smokers, which complicates the comparison of data. However, other studies
have shown that the maxilla is more susceptible to the harmful effects of tobacco
compared to the mandible.6,14,19,39 As the
maxilla features a larger medullary area,
and consequently has greater vascularity, it
is believed to be more permeable to the
harmful agents of smoke.11
The bacterial biofilm tends to adhere at
a faster rate in the epithelial cells of smokers.13 This may cause an increase in the
incidence of biological complications,
such as mucositis and peri-implantitis;
consequently, this could lead to an increase in the rate of peri-implant bone
loss. Very few clinical studies have compared bone loss around implants between
smokers and non-smokers. Bain and Moy6
proposed that tobacco use, associated with
poor bone quality, could hinder healing
and lead to an increase in bone loss,
primarily in the maxilla.14,15
The implant failure rate was found to be
significantly higher in the group of smokers (P < 0.00001). However, the metaanalysis showed that the rate of implant
failure does not increase in line with the
increase in follow-up time (P = 0.26). This
suggests that the implant failure in smokers may occur early (<4 months) or at an
10
intermediate date (4 to 24 months) postsurgery, as per the classification proposed

by ten Bruggenkate et al.40
In conclusion, a statistically significant
difference in marginal bone loss was
found between the smoking group and
the non-smoking group, in favour of the
non-smoking group (SMD 0.49, 95% CI
0.070.90; P = 0.02). When analyzed independently, the marginal bone loss in
smokers was increased in the maxilla
compared to the mandible (SMD 0.40,
95% CI 0.240.55; P < 0.00001). A statistically significant difference in implant
failure in favour of the non-smoking group
was also observed (OR 1.96, 95% CI 1.68
2.30; P < 0.00001). However, the subgroup analysis for follow-up time did
not reveal any significant increase in implant failure proportionate to the increase
in monitoring time (P = 0.26). The data in
this review should be interpreted with
caution because of the selective inclusion
of prospective and retrospective cohort
studies. A greater number of RCTs based
on the CONSORT statement41 is critical to
better understand the correlation between
smoking and the success of implants.
Funding
The authors declare that no funding was

provided for the performance of this study.
Competing interests
The authors declare that there was no

conflict of interest during the performance
of this study.
Ethical approval
The study did not involve human subjects.

Patient consent
The study did not involve human subjects.

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Address:
Vittorio Moraschini Filho
Department of Periodontology
School of Dentistry
Fluminense Federal University
Rua Mario dos Santos Braga
30
Centro
Niteroi
Rio de Janeiro
Cep. 24020-140
Brazil
E-mail: vittoriomf@terra.com.br

Moraschini 2015

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YIJOM-3245; No of Pages 11

Int. J. Oral Maxillofac. Surg. 2015; xxx: xxxxxx

Success of dental implants

V. Moraschini , E. dS. PortoBarboza

Dental implants have a high rate of survival

previously as some of the possible causes

Key words: dental implants; smoking; tobacco;

is believed that the negative influence of

Moraschini and Barboza

Materials and methods

The methodology of this study was

The purpose of this review was to test the

A comprehensive electronic search was

The analysis of quality of the non-randomized studies (prospective and retrospective

The research and screening processes

The following data were extracted from

Binary and continuous variables from the

Table 1. Systematic search strategy (PICO strategy).

Success of implants in smokers and non-smokers

Full-text articles excluded

Studies included in the present

14 full-text articles excluded:

deviation (SD) were used to calculate the

The initial search yielded 965 titles from

full papers were selected. Fourteen studies

used implant system.6,14,21,23,28 In one

The characteristics of the studies included

Only two studies obtained a score of less

Seven studies reported on the analysis of

Bain and Moy (1993)6

Haas et al. (1996)14

Kan et al. (1999)18

Smoker and non-smoker

Smoker and non-smoker

Low consumption (<15

Lambert et al. (2000)19

Smoker and never smoker

Kumar et al. (2002)20

Nitzan et al. (2005)11

DeLuca and Zarb

Smoker and non-smoker

Moraschini and Barboza

Table 2. Main characteristics of the studies selected.

Balshe et al. (2008)23

Smoker and non-smoker

Sverzut et al. (2008)24

Smoker and non-smoker

Cavalcanti et al. (2011)25

Smoker and non-smoker

Biomet 3i, Astra Tech,

Smoker and non-smoker

3.5, 3.75, 4, 4.3,

Vervaeke et al. (2012)27

Smoker and non-smoker

Sayardoust et al. (2013)28

Smoker and non-smoker

Marginal bone loss

P-value (for implant

Bain and Moy (1993)6

Haas et al. (1996)14

2.7  1.87 (G1)

Kan et al. (1999)18

Lambert et al. (2000)19

2.7 1.87 (G1)

0.15 0.09 (G1)

0.07 0.26 (G1)

2.41 1.46 (G1)

1.56 0.53 (G1)

0.53 0.92 (G1)

1.39 1.57 (G1)