YIJOM-3437; No of Pages 9

Int. J. Oral Maxillofac. Surg. 2016; xxx: xxxxxx

http://dx.doi.org/10.1016/j.ijom.2016.05.019, available online at http://www.sciencedirect.com

Systematic Review Paper

Dental Implants

The impact of diabetes on V. Moraschini, E. S. P.Barboza

Department of Periodontology, School of
Dentistry, Fluminense Federal University, Rio
de Janeiro, Brazil

dental implant failure:

a systematic review and meta-
analysis
V. Moraschini, E. S. P. Barboza: The impact of diabetes on dental implant failure:
a systematic review and meta-analysis. Int. J. Oral Maxillofac. Surg. 2016; xxx: xxx
xxx. # 2016 International Association of Oral and Maxillofacial Surgeons. Published
by Elsevier Ltd. All rights reserved.

Abstract. The aim of this study was to investigate the hypothesis that there is no
difference in implant failure rate or marginal bone loss between type 1 or 2 diabetes
subjects and non-diabetic subjects. An electronic search was conducted, without
restrictions on date or language, in the PubMed/MEDLINE, Cochrane Central
Register of Controlled Trials, Web of Science, and EMBASE databases, and in the
grey literature, through August 2015. The eligibility criteria included prospective
and retrospective cohort studies and randomized controlled trials. The initial search
resulted in 1093 titles from PubMed/MEDLINE, 164 from the Cochrane Central
Register of Controlled Trials, 134 from Web of Science, 228 from EMBASE, and
four from the grey literature. Following the search and selection process, 14 studies
published between 2000 and 2015 were included in this systematic review.
According to the risk of bias analysis, all studies were classified as high quality. The
results of this systematic review suggest that the number of implant failures does not
Key words: diabetes mellitus; hyperglycaemia;
differ between diabetic and non-diabetic subjects. Additionally, the results of the implant failure; marginal bone loss; meta-
comparison between type 1 and 2 diabetes subjects showed no difference in the analysis.
number of failures. With regard to marginal bone loss, there was a statistically
significant difference favouring non-diabetic subjects. Accepted for publication 26 May 2016

Despite dental implants showing a high
long-term success rate,1 certain risk fac-
tors can compromise the biological pro-
cess of osseointegration or negatively
impact the maintenance of peri-implant
health.1,2 Diabetes is one of these factors
and is characterized by hyperglycaemia
resulting from a deficiency in insulin se-
cretion, its mechanism of action, or both.
Diabetes is classified as type 1 (insulin-
dependent), type 2, or gestational. Studies
have demonstrated that the aetiology of
diabetes consists of a combination of ge-
netic and environmental factors (including
viral infections, an inadequate diet, and a
sedentary lifestyle).3
The epidemiological prevalence of dia-
betes is high. This disease may affect
approximately 11% of the American pop-
ulation, with 9095% of these cases diag-
nosed with type 2 diabetes, which is the
most frequent type observed in patients
older than 40 years of age.4
As a result of microvascular complica-
tions in patients with diabetes, there is a
delay in the tissue healing process; this is
due to the lower cell concentration at the

0901-5027/000001+09 # 2016 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. The impact of diabetes on dental implant failure: a systematic review
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
YIJOM-3437; No of Pages 9
2 Moraschini Filho and Barboza
surgical site and subsequent lower release
of growth factors and cytokines, and re-
duced collagen synthesis.57 Furthermore,
diabetic patients may have a reduced im-
mune response, which increases the pos-
sibility of post-surgical infection.8
In studies evaluating the success or sur-
vival of dental implants in diabetic volun-
teers,911 a higher rate of early-onset
failures has been observed compared to
late-onset failures. Chronic hyperglycae-
mia can affect the synthesis of osteoblasts
and stimulate increased osteoclast func-
tion.12 In addition, the metabolism of cal-
cium and potassium may become altered.13
As a result of these phenomena, there will
be decreased bone formation during the
healing phase, which would explain a
higher rate of early failure, i.e., during
osseointegration. For these reasons, diabe-
tes is considered a relative contraindication
during dental implant treatment.14
On the other hand, diabetic patients who
maintain control of their glycaemic index
appear to have implant success and sur-
vival rates similar to those of systemically
healthy individuals.15 Thus, the aim of this
review was to investigate the hypothesis
that there is no difference in implant fail-
ure rate or marginal bone loss between
type 1 or 2 diabetes subjects and non-
diabetic subjects.
Materials and methods
The methodology of this systematic re-
view followed the recommendations of the
Cochrane Handbook for Systematic
Reviews of Interventions.16 In order to
increase the quality and transparency of
the study, the PRISMA (Preferred Report-
ing Items for Systematic Reviews and
Meta-Analyses)17 and AMSTAR (Assess-
ment of Multiple Systematic Reviews)18
checklist guidelines were followed. The
clinical questions were formulated and
organized using the PICOS process.
Focused question
Is there a difference in the failure rate and
marginal bone loss level of dental
implants between type 1 or 2 diabetes
subjects and non-diabetic subjects?
Clinical relevance
Knowing the risk factors is essential to the
success of treatment with implants. Ac-
cordingly, this systematic review will pro-
vide data to ensure that the decision-
making process and case planning for
diabetic patients is based on scientific
evidence.
Please cite this article in press as: Moraschini V, Barboza ESP. The impact of diabetes on dental implant failure: a systematic review
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
Search strategy periodontal diseases without prior treat-
ment were also excluded.
An electronic search was conducted, with-
out date or language restriction, in the
PubMed/MEDLINE, Cochrane Central Screening process
Register of Controlled Trials, Web of
The search and screening process was
Science, and EMBASE databases through
conducted by both authors/reviewers.
August 2015. In addition, a manual search
The titles and abstracts were first ana-
was conducted in the following periodic
lyzed. In the second stage, full-text articles
journals: Journal of Periodontology, Jour-
were selected for careful reading and anal-
nal of Clinical Periodontology, Journal of
ysis against the eligibility criteria (inclu-
Periodontal Research, International Jour-
sion/exclusion) for later data extraction.
nal of Periodontics and Restorative Den-
Disagreements between the reviewers
tistry, Clinical Oral Implants Research,
were settled through detailed discussions.
Clinical Implant Dentistry and Related
The concordance between the two
Research, International Journal of Oral
reviewers for the search process was eval-
and Maxillofacial Implants, International
uated using Cohens kappa (k) test. The
Journal of Oral and Maxillofacial Sur-
authors of the studies included were con-
gery, Implant Dentistry, Journal of Den-
tacted by e-mail to answer any questions,
tistry, Journal of Prosthodontics, and
if necessary.
Journal of Dental Research. A search of
the so-called grey literature in the Open-
GRAY database, the ClinicalTrials.gov Risk of bias and quality assessment
database (www.clinicaltrials.gov), and
The NewcastleOttawa scale (NOS)
the references of the included studies
(http://www.ohri.ca/programs/clinical_
(cross-referencing) was also conducted.
epidemiology/oxford.asp) was used for
The search strategy and PICOS frame-
the analysis of the quality of the non-
work can be seen in Table 1.
randomized trials (prospective and retro-
spective cohort studies) included in this
Selection criteria
review. For the selection and outcome
This review searched for prospective and categories, the studies were awarded a
retrospective cohort studies and random- star/point for each item. For the compari-
ized controlled trials (RCTs) comparing son category, two stars/points were
implant failure rates and marginal bone awarded. The highest score that can be
loss between type 1 or 2 diabetes subjects awarded to a study is nine stars/points.
and non-diabetic volunteers. This review Studies that scored 6 stars or more were
considered implant failure as absolute im- considered to be of high quality.
plant loss. The exclusion criteria were
animal studies, in vitro studies, clinical
Data extraction
series, case reports, and reviews. Studies
involving volunteers with other decom- The following data were extracted from
pensated metabolic diseases or those with the selected studies (when available):
Table 1. Systematic search strategy (PICOS strategy).
Search strategy
Population #1. (Partially edentulous[MeSH] OR edentulous[MeSH] OR
edentulous maxilla OR edentulous mandible OR diabetic[MeSH]
OR diabetes mellitus[MeSH] OR type 1 diabetes
mellitus[MeSH] OR type 2 diabetes mellitus[MeSH] OR non-
diabetic)
Intervention #2. (Dental implant[MeSH] OR dental implant surgery[MeSH]
OR single implant[MeSH] OR multiple implant[MeSH])
Comparisons #3. (Diabetic type 1 vs. diabetic type 2 vs. non-diabetic)
Outcomes #4. (Cumulative survival rate[MeSH] OR survival OR dental
implant survival OR dental implant failure OR failure OR
marginal bone loss OR implant bone resorption OR dental
implant bone loss)
Study design Prospective cohort studies, retrospective cohort studies, and
randomized controlled trials
Search combination #1 AND #2 AND #3 AND #4
Database search
Language No restriction
Electronic databases PubMed/MEDLINE, Cochrane Central Register of Controlled
Trials, Web of Science, and EMBASE
YIJOM-3437; No of Pages 9
authors, publication year, study design,
follow-up period, number of subjects,
sex, age of the subjects, diabetic condition,
number of implants placed, number of
failed implants, mean survival rates, im-
plant characteristics, healing period, num-
ber of smokers, days of antibiotic
prophylaxis, use of mouth rinse, marginal
bone loss, and the authors conclusions.
Statistical analysis
Continuous and binary variables from the
studies were subjected to meta-analysis
when at least two of the studies assessed
reported the same data type. For the binary
outcomes (e.g., implant failure), the inter-
vention effects estimated were expressed
as a percentage risk ratio (RR) with a 95%
confidence interval (CI). For the continu-
ous outcomes (e.g., marginal bone loss),
the mean and standard deviation were used
to calculate the mean difference (MD) in
millimetres with a 95% CI. The inverse-
variance method was used for the random-
effects model or the fixed-effects model.
Heterogeneity was assessed using the x2
test and any impact on the meta-analysis
was quantified via I2. Values of 25%
were classified as low heterogeneity,
values of up to 50% were classified as
medium heterogeneity, and those above
70% were classified as high heterogeneity.
When significant heterogeneity was found
(P < 0.10), the results of the random-
effects model were validated. When low
heterogeneity was verified, the fixed-
effects model was considered. The level
of statistical significance was set at
P < 0.05.
Fig. 1. Flow diagram (PRISMA format) of the screening and selection process.
Please cite this article in press as: Moraschini V, Barboza ESP. The impact of diabetes on dental implant failure: a systematic review
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
Impact of diabetes on dental implant failure
The data were analyzed using Review
Manager version 5.2.8 statistical software
(The Nordic Cochrane Centre, The
Cochrane Collaboration, Copenhagen,
Denmark, 2014).
Publication bias was explored graphi-
cally using a funnel plot. An asymmetric
funnel plot (studies falling outside the
funnel) may indicate a possible publica-
tion bias.
Results
Literature search
The initial search resulted in 1093 titles
from PubMed/MEDLINE, 164 from the
Cochrane Central Register of Controlled
Trials, 134 from Web of Science, 228 from
EMBASE, and four from the grey litera-
ture. After the first assessment, 22 full-text
articles were selected. Following careful
reading, eight studies were excluded as they
failed to conform to the eligibility criteria
of this review (Table 2).9,11,1924 Thus, 14
studies published between 2000 and 2015
were included in this systematic re-
view.3,10,2536 The article search and selec-
tion process is shown in Fig. 1.
The k value for concordance between
the two authors/reviewers for the poten-
tial articles to be included (titles and
abstracts) was 0.97 and for the selected
articles was 0.90, demonstrating excellent
concordance.16
Study characteristics
The characteristics of the selected studies
are presented in Table 3. Two prospective
3
Table 2. Excluded studies.
Reason for
rejection Authors
Case report Balshi et al. (2007)19
Duplicate study Oates et al. (2009)20
Animal study Keller et al. (1999)21
Did not state Fiorellini et al. (2000)11
the type of van Steenberghe et al.
diabetes and/or (2002)22
failures in each Moy et al. (2005)23
group Farzad et al. (2002)9
Omran et al. (2015)24
cohort studies,25,32 three retrospective co-
hort studies,26,28,31 and nine controlled
clinical trials3,10,27,29,30,3336 were includ-
ed in this systematic review. The number
of volunteers in the studies ranged from 10
to 663, and the volunteers were aged
between 15 and 89 years. Eight hundred
and two diabetic volunteers and 1532 non-
diabetic volunteers were assessed, with
the installation of 1551 and 6353 implants,
respectively. Only one study assessed sub-
jects with type 1 diabetes.28 All selected
articles included only volunteers with di-
abetes that was under control at the time of
surgery. Five articles did not report
whether participants who smoked were
included.3,10,26,30,32 The monitoring peri-
od in the studies ranged from 3 to 204
months, with an average of 45.1 months.
The mean success rate among diabetic
volunteers ranged from 31.8% to 100%
and for non-diabetic volunteers ranged
from 86.1% to 100%. The mean annual
failure was 3.92% for diabetic subjects
and 1.65% for non-diabetic subjects.
 4

YIJOM-3437; No of Pages 9
Table 3. Main characteristics of the studies selected.
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
Please cite this article in press as: Moraschini V, Barboza ESP. The impact of diabetes on dental implant failure: a systematic review

Study design No. of subjects Age range Diabetes type Implants Mean Implant system Implant

Moraschini Filho and Barboza

Follow-up Number per Mean age Nature of placed/implants survival size (diameter  length)
Authors (months) group Sex diabetes failed rate (%) (mm)
Morris et al. (2000)3 CCT 663 4089 Type 2 255/20 (D2) 92.2 (D2) Spectra system (NR  NR)
36 255 (D2)/408 (ND) NR Controlled 2632/180 (ND) 93.2 (ND)
NR
Olson et al. (2000)25 Prospective 89 4078 Type 2 178/16 (D2) 91.0 (D2) Paragon Implant Company,
60 89 (D2) 62.7 Controlled Nobel Biocare, Interpore
89 M Corporation
(NR  8, 10, 10.5, 11, 13, 15,
16, 18, 20)
Accursi (2000)26 Retrospective 45 1583 Type 2 59/4 (D2) 93.2 (D2) Branemark
204 15 (D2)/30 (ND) 53.9 Controlled 111/7 (ND) 93.7 (ND) (NR  NR)
16 M/29 F
Peled et al. (2003)10 CCT 41 NR Type 2 141/4 (D2) 97.2 (D2) Medical Implant System
60 41 (D2) NR Controlled (3.75  10 to 16)
26 M/15 F
Dowell et al. (2007)27 CCT 35 2981 Type 2 39/0 (D2) 100 (D2) Straumann
4 25 (D2)/10 (ND) NR Controlled 11/0 (ND) 100 (ND) (4.1  10, 12)
NR
Alsaadi et al. (2008)28 Retrospective 412 NR Types 1 and 2 33/0 (D1) 100 (D1) Nobel Biocare
24 9 (D1)/1 (D2)/402 (ND) NR Controlled 1/0 (D2) 100 (D2) (3.3, 3.75, 4, 5  10)
NR 1480/101 (ND) 93.2 (ND)
Tawil et al. (2008)29 CCT 90 2985 Type 2 255/6 (D2) 97.6 (D2) Nobel Biocare
42.4 45 (D2)/45 (ND) 62.1 Controlled 244/1 (ND) 99.6 (ND) (NR  NR)
57 M/33 F
Loo et al. (2009)30 CCT 278 3850 Type 2 255/174 (D2) 31.8 (D2) Straumann
3 138 (D2)/140 (ND) 45.5 Controlled 346/48 (ND) 86.1 (ND) (3.5  NR)
119 M/159 F
Anner et al. (2010)31 Retrospective 475 NR Type 2 177/5 (D2) 97.2 (D2) NR
114 49 (D2)/426 (ND) 51.9 Controlled 1449/72 (ND) 95.0 (ND) (NR  NR)
176 M/299 F
Turkyilmaz (2010)32 Prospective 10 4571 Type 2 23/0 (D2) 100 (D2) Astra Tech
12 10 (D2) 58 Controlled (4, 4.5  9, 11, 13, 15)
6 M/4 F
Erdogan et al. (2015)33 CCT 24 NR Type 2 22/0 (D2) 100 (D2) Straumann
12 12 (D2)/12 (ND) 51 Controlled 21/0 (ND) 100 (ND) (4.1  10, 12)
12 M/12 F
Gomez-Moreno et al. CCT 67 5964 Type 2 46/0 (D2) 100 (D2) Straumann
(2015)34 36 46 (D2)/21 (ND) 59.5 Controlled 21/0 (ND) 100 (ND) (3.3, 4.1  10 to 14)
33 M/34 F
Conte et al. (2015)35 CCT 54 3770 Type 2 35/0 (D2) 100 (D2) S.I.N.
12 35 (D2)/19 (ND) 55.3 Controlled 19/0 (ND) 100 (ND) (NR  NR)
25 M/29 F
Ghiraldini et al. (2015)36 CCT 51 3770 Type 2 32/0 (D2) 100 (D2) S.I.N.
12 32 (D2)/19 (ND) 54.2 Controlled 19/0 (ND) 100 (ND) (3.75  8.5 to 11.5)
28 M/23 F
 YIJOM-3437; No of Pages 9
Healing No. of Antibiotics/mouth Marginal bone
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
Please cite this article in press as: Moraschini V, Barboza ESP. The impact of diabetes on dental implant failure: a systematic review

Authors period smokers rinse (days) loss (mean  SD) (mm) Author conclusions
Morris et al. (2000)3 NR NR NR NR The use of endosseous dental implants in type 2 diabetic
patients involves a marginal risk to long-term implant
survival
Olson et al. (2000)25 4 months 34 NR/NR NR This study supports the use of dental implants in type 2
diabetic patients
Accursi (2000)26 NR NR NR/NR 0.25  0.07 (D2) The diabetic patients were no more likely to experience
0.06  0.03 (ND) implant failure than the non-diabetic patients
Peled et al. (2003)10 3 months NR 5/NR NR The clinical outcome of dental implant placement in a
selected group of patients with well-controlled type 2
diabetes mellitus is encouraging
Dowell et al. (2007)27 4 months 0 10 to D2 and 3 for ND/NR NR We found no evidence of diminished clinical success or
significant early healing complications associated with
implant therapy based on the glycaemic control levels of
patients with type 2 diabetes mellitus
Alsaadi et al. (2008)28 NR 61 NR NR Systemic health factors do not seem to be prominent
players in the aetiology of late implant loss
Tawil et al. (2008)29 NR 40 7/14 0.5  0.71 (D2) No statistically significant difference was found for patients
0.21  0.3 (ND) or for implants for the advanced surgery cases or the
conventional approach in diabetic patients compared to
non-diabetic patients
Loo et al. (2009)30 3 months NR NR/14 NR Implant failure in diabetics was significantly greater than
that in non-diabetics when multiple adjoining implants
were placed
Anner et al. (2010)31 NR 63 NR NR This study found no evidence of diminished clinical
success or significant early healing complications
associated with implant therapy in patients with controlled
type 2 diabetes mellitus
Turkyilmaz (2010)32 3 months NR 5/14 0.3  0.2 (D2) This clinical report supports the use of dental implants in
patients with well- or moderately well-controlled type 2

Impact of diabetes on dental implant failure

Erdogan et al. (2015)33
Gomez-Moreno et al. (2015)34
Conte et al. (2015)35
Ghiraldini et al. (2015)36
CCT, controlled clinical trial; D1, type 1 diabetes; D2, type 2 diabetes; ND, non-diabetes; NR, not reported; M, male; F, female; SD, standard deviation.
diabetes mellitus as a dental treatment modality
4 months 0 NR/NR 2.96  0.59 (D2) The results of the present study suggest that type 2 diabetic
2.86  0.64 (ND) patients may undergo staged guided bone regeneration
procedures securely
4 months 0 7/14 0.5  0.14 (D2) Implant therapies for diabetic patients can be predictable,
0.41  0.18 (ND) providing these patients fall within controlled ranges of
glycaemia over time
4 months 0 Single dose 1 h before/7 NR The patients glycaemic status appears to modulate bone-
related genes in a different manner
4 months 0 Single dose 1 h before/7 NR Poor glycaemic control negatively modulated the bone
factors during healing

5
YIJOM-3437; No of Pages 9

6 Moraschini Filho and Barboza

Total 9/9
The healing period from implant instal-

6/9
7/9
7/9
6/9
6/9
6/9
6/9
7/9
7/9
6/9
8/9
7/9
7/9
7/9
lation to prosthetic loading ranged from 3
to 4 months. All implants used in the
studies were surface-treated. Implants
were installed in bone regeneration areas

Adequacy of

of cohorts
follow-up
in two studies.29,33 A marginal bone loss

$
assessment was conducted in five studies

0
0
0
0
0
0

0
0
0
using peri-apical and/or panoramic radio-

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.
graphs, in which the implant platform in
relation to the alveolar bone crest was used
as the reference.26,29,3234 Antibiotic med-

enough for
Outcome
Follow-up

to occurb
was long

outcome
ication was administered in seven studies,

$
$
$
$
$
$
$

$
$
$
$
$
$
0
either before35,36 or after10,27,29,32,34 sur-
gery. Six studies reported prescribing
chlorhexidine mouthwash postoperative-
ly.29,30,32,3436

Assessment
of outcome
$
$
$
$
$
$
$
$
$
$
$
$
$
$
Risk of bias and quality assessment
The quality analysis results for the studies
included in the review are presented in

basis of the design

Comparability of
Table 4. No study scored fewer than 6

cohorts on the
Comparability

or analysisa
points.

$$

$$
$$
$$
$0
$0
$0
$0
$0
$0
$0

$0
$0
$0
Meta-analysis
For this study, the random-effects model
was used to assess implant failure in type 2
diabetic subjects, due to the high hetero-
present at start
Outcome of
interest not

geneity found (P < 0.00001, I2 = 90%).

There was no statistically significant dif-
$
$
$
$
$
$
$
$
$
$
$
$
$
$
ference (P = 0.47) between type 2 diabetes
subjects and non-diabetic subjects for im-
plant failure, with a RR of 1.43 (95% CI
0.543.82). The analysis of type 1 diabetes

One year of follow-up was chosen to be enough for the outcome survival to occur.
Ascertainment
of exposure

subjects also failed to show a statistically

significant difference when compared to
$
$
$
$
$
$
$
$
$
$
$
$
$
$
non-diabetic subjects (P = 0.29), with a
RR of 3.65 (95% CI 0.3340.52). The
Selection

random-effects model was used to analyze

the type 1 and type 2 diabetes subgroups,
Table 4. Risk of bias and quality assessment of the studies included.

of external
Selection

due to the high heterogeneity found

control

(P < 0.00001, I2 = 88%). There was no

$
$
$
$
$
$
$
$
$
$
$
$
$
$

significant difference (P = 0.34) between

the two types of diabetic subjects with
regard to implant failure, with a RR of
Representativeness

1.56 (95% CI 0.623.91) (Fig. 2).

of the exposed

The fixed-effects model was used to

cohort

assess marginal bone loss, due to the

$

$
0
0

0
0
0
0

0
0

0
0
0

medium heterogeneity found between

the studies reviewed (P = 0.15, I2 = 44%).
A statistically significant difference
(P < 0.00001) was observed in favour of
the non-diabetic group, with a MD of 0.18
Gomez-Moreno et al. (2015)34

(95% CI 0.140.21) (Fig. 3).

Ghiraldini et al. (2015)36
Erdogan et al. (2015)33
Alsaadi et al. (2008)28
Dowell et al. (2007)27

Publication bias
Anner et al. (2010)31

Conte et al. (2015)35

Olson et al. (2000)25
Morris et al. (2000)3

Tawil et al. (2008)29

Turkyilmaz (2010)32
Peled et al. (2003)10

Loo et al. (2009)30

The funnel plot was asymmetric when

Accursi (2000)26

implant failure was analyzed between

the subgroups, which indicated potential
publication bias. Three studies contributed
Authors

to the asymmetry as they fell outside the

b
a

95% CI funnel (Fig. 4).3,30,31

Please cite this article in press as: Moraschini V, Barboza ESP. The impact of diabetes on dental implant failure: a systematic review
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
YIJOM-3437; No of Pages 9

Impact of diabetes on dental implant failure 7

Fig. 2. Forest plot for the event implant failure rate. No statistically significant difference was detected between the groups.

Fig. 3. Forest plot for the event marginal bone loss. A statistically significant difference was observed in favour of the non-diabetic group
(P < 0.00001).

Discussion

The aim of this review was to investigate

the hypothesis that there is no difference in
implant failure rate or marginal bone loss
between type 1 or 2 diabetes subjects and
non-diabetic subjects.
A broad search for studies was con-
ducted, including electronic, manual,
and grey literature searches. To avoid
publication bias, no restriction was im-
posed on the date or language of the
publications. The authors of one of the
studies had to be contacted to answer some
questions.36 Despite RCTs being the study
type with the lowest potential bias,37 none
were included in this systematic review.
Fig. 4. Funnel plot for the studies reporting the outcome event implant failure rate. The absence of RCTs in the literature

Please cite this article in press as: Moraschini V, Barboza ESP. The impact of diabetes on dental implant failure: a systematic review
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
YIJOM-3437; No of Pages 9
8 Moraschini Filho and Barboza
assessing diabetic subjects vs. non-diabet-
ic subjects in relation to implant success
was one of the observations of this study.
Despite diabetes being considered a
relative contraindication to treatment with
implants,38 diabetic subjects with con-
trolled glucose may have success rates
that are similar to those of non-diabetic
subjects.15,39 However, no study included
in this review monitored the glycaemic
control of the volunteers throughout the
observation period of the work, and this
factor may possibly lead to confusion.
In the short term, hyperglycaemia in
pregnant women (gestational diabetes) or
in subjects on temporary corticotherapy
may not present as many detrimental
effects to peri-implant health as does hyper-
glycaemia in chronic decompensated dia-
betic patients, since insulin not only has an
effect on hyperglycaemia, but may also
control and even stimulate osteoblastic
activity.12,40,41 In addition, chronic hyper-
glycaemia can lead to microvascular com-
plications. This can pose a problem for
patients with type 1 diabetes, which is
the subtype that affects patients during
the early stages and which, as a conse-
quence, can lead to long-term diseases.
This systematic review sought to ana-
lyze the differences in failure rate and
marginal bone loss between type 1 and
type 2 diabetes subjects. However, only
one article investigating type 1 diabetes
subjects and implants was identified.28
After reviewing the subgroups of the
two types of diabetes, there was no sta-
tistically significant difference in implant
failure (P = 0.34). The low number of
published studies in relation to type 1
diabetes when compared to type 2 diabetes
could be the result of the greater preva-
lence of the latter (>90% of cases). Con-
sequently, differences in bone metabolism
between the two types of diabetes have yet
to be clarified in the literature.15
The implant failure rate in diabetic vs.
non-diabetic subjects showed no statisti-
cally significant difference for type 1
(P = 0.29) or type 2 (P = 0.47) diabetic
subjects. Only two studies included in this
systematic review showed a statistically
significant difference in implant failure
between diabetic and non-diabetic sub-
jects.3,30 However, one of these studies
presented a follow-up period of less than
12 months, which may be insufficient to
obtain reliable results.30 Two studies con-
ducted a biomolecular analysis of peri-
implant bone healing comparing type 2
diabetes subjects and non-diabetic sub-
jects.35,36 Both articles noted that diabetes
negatively affected the gene expression of
factors related to bone tissue.
Please cite this article in press as: Moraschini V, Barboza ESP. The impact of diabetes on dental implant failure: a systematic review
and meta-analysis, Int J Oral Maxillofac Surg (2016), http://dx.doi.org/10.1016/j.ijom.2016.05.019
Four studies conducted an analysis of
marginal bone loss comparing diabetic to
non-diabetic subjects. The meta-analysis
showed a statistically significant differ-
ence (P < 0.00001) in favour of the
non-diabetic group, which showed lower
marginal bone loss. The study by Erdogan
et al. presented an average bone loss that
was significantly higher than that in the
other studies.33 A characteristic of this
study was that the implants were installed
in areas of bone regeneration, and this may
have contributed to greater bone remodel-
ling. Nonetheless, this article presented a
100% implant survival rate for both dia-
betic and non-diabetic subjects. As the
survival rate is a quantitative analysis,1
this parameter may mask problems such as
the marginal bone loss and, therefore,
should be analyzed with caution.
Possible confounding factors can influ-
ence and interact with the effects of diabe-
tes, thus jeopardizing the reliability of the
study results, such as the inclusion of volun-
teers with implants installed in bone regen-
eration areas29,33 and those with a smoking
habit.25,28,29,31 None of the studies ana-
lyzed these factors separately and this
may have compromised the evaluation of
the effect (i.e., meta-regression) of these
variables on the survival of the implants.
Studies (preferably RCTs) examining
the influence of types 1 and 2 diabetes on
the survival of implants should be con-
ducted in the future. Possible modulating
factors (confounding factors) should be
analyzed separately, thus providing data
on any negative interaction with diabetes.
It is essential to monitor the glycaemic
index of volunteers at predetermined time
points during the study follow-up period.
In conclusion, the results of this system-
atic review suggest that the rate of implant
failure is not higher for diabetic subjects
than for non-diabetic subjects. Additional-
ly, the comparison between type 1 and type
2 diabetes subjects showed no evidence of a
higher failure rate for either group. With
regard to marginal bone loss, there was a
statistically significant difference favour-
ing non-diabetic subjects. A greater number
of studies are required in the future so that
these conclusions can be confirmed.
Funding
The authors declare that no funding was
provided for the elaboration of this study.
Competing interests
The authors declare that there was no
conflict of interest during the elaboration
of this study.
Ethical approval
Not required.
Patient consent
Not required.
Acknowledgements. The authors would
like to thank Dr Fernanda Vieira Ribeiro
for providing us with some missing study
information.
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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
Tel: +55 2130268190
E-mail: vittoriomf@terra.com.br