ORIGINAL CONTRIBUTIONS
Does a higher glycemic level
lead to a higher rate of dental
implant failure?
A meta-analysis
Quan Shi, PhD(c); Juan Xu, PhD; Na Huo, PhD; Chuan Cai,
PhD; Hongchen Liu, PhD
D
iabetes mellitus, which is characterized by
relative or complete insulin deciency or
resistance leading to hyperglycemia, has
become 1 of the most challenging public
health problems worldwide.1 It has placed a heavy
burden on society and markedly increased health care
costs.2,3 In addition to medication therapy, diet plays an
important role in the treatment of diabetes and in
glycemic control. According to the latest scientic
statement from the American Heart Association and
the American Diabetes Association,4 maintaining a
careful diet and performing physical activity can affect
overall diabetes control and can safely lead to weight
loss, which can reduce the need for medication to
control cardiovascular disease risk factors without a
concomitant increase in the risk of experiencing car-
diovascular events. Unfortunately, patients with dia-
betes have an increased frequency of tooth loss,5,6
which affects their masticatory function and their
intake of nutrients, both of which can lead to challenges
in glycemic control and complications for the preven-
tion of diabetes.7,8
Clinicians generally consider dental implants to be
effective and reliable restorations to replace lost teeth
and restore masticatory function.9 Osseointegration is a
prerequisite for a successful dental implant; however,
there is evidence that diabetes has a negative inuence
on bone formation and remodeling.10 Complications,
including microvascular disease, susceptibility to
infection, and delayed wound healing caused by
hyperglycemia may affect implant osseointegration.
Therefore, clinicians have long considered diabetes to
be a relative contraindication for dental implants,
depending on the patients glycemic level.10,11 The re-
sults of animal studies also have shown decreased levels
Copyright 2016 American Dental Association. All rights reserved.
ABSTRACT
Background. Owing to limited evidence, it is unclear
whether diabetes that is not well controlled would lead to a
higher rate of dental implant failure. The authors of this
meta-analysis evaluated whether the failure rate for patients
with diabetes that was not well controlled was higher than the
failure rate for patients with well-controlled diabetes.
Types of Studies Reviewed. The authors searched
PubMed, the Cochrane Library, and ClinicalTrials.gov
without limitations for studies whose investigators
compared the dental implant failure rates between patients
with well-controlled diabetes and diabetes that was not well
controlled. The authors pooled the relative risk (RR) and
95% condence interval (CI) values to estimate the relative
effect of the glycemic level on dental implant failures. The
authors used a subgroup analysis to identify the association
between the implant failure rate and the stage at which the
failure occurred.
Results. The authors included 7 studies in this meta-
analysis, including a total of 252 patients and 587 dental
implants. The results of the pooled analysis did not indicate a
direct association between the glycemic level in patients with
diabetes and the dental implant failure rate (RR, 0.620; 95%
CI, 0.225-1.705). The pooled RR in the subgroup of patients
who experienced early implant failure was 0.817 (95% CI,
0.096-6.927), whereas in the subgroup of patients who
experienced late implant failure, the pooled RR was 0.572
(95% CI, 0.206-1.586).
Conclusions and Practical Implications. On the basis
of the evidence, the results of this meta-analysis failed to
show a difference in the failure rates for dental implants
between patients with well-controlled diabetes and patients
with diabetes that was not well controlled. However,
considering the limitations associated with this meta-
analysis, the authors determined that future studies that are
well designed and provide adequate controls for confound-
ing factors are required.
Key Words. Uncontrolled diabetes; dental implant failure;
glycemic control; meta-analysis.
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 ORIGINAL CONTRIBUTIONS
of implant osseointegration and reduced bone-to-
implant contact caused by hyperglycemia.12,13
Therefore, glycemic control is the primary consider-
ation for implant treatment. With proper treatment
planning, prophylactic remedies and adequate post-
surgical maintenance, patients with well-controlled
diabetes may be considered candidates for implant
treatment,14 whereas patients with diabetes that is not
well controlled may be ineligible for implant therapy.6
However, the results of some clinical studies have shown
that patients with diabetes that was not well controlled
had higher rates of implant success.15,16 Moreover, the
authors of a systematic review6 concluded that there
were no clinical data to support the idea that patients
with diabetes that is not well controlled would have a
signicantly increased risk of experiencing implant fail-
ure, but other investigators14 noted that the authors of
that review compared only the failure rates of various
studies without conducting a statistical analysis. There-
fore, it is still controversial whether the implant failure
rate is higher in patients with diabetes who do not have
good glycemic control.
Through this meta-analysis, we evaluated the evi-
dence of the relationship between glycemic level and
dental implant failure rate in patients with diabetes, and
we analyzed whether the implant failure rate in patients
with diabetes that was not well controlled was higher
than the rate in patients with well-controlled diabetes.
The results of this meta-analysis will give clinicians a
better understanding of the risks of dental implant failure
and help patients make rational decisions.
METHODS
Search strategy and study selection. In December 2015,
we searched PubMed, the Cochrane Library, and
ClinicalTrials.gov without language or time restrictions.
We used the following key words: dental implants,
oral implants, diabetes, hyperglycemia, and dia- patients with diabetes that was not well controlled into
betes mellitus. We identied additional studies by hand-
searching the reference lists of the included studies and
related reviews. Two reviewers (Q.S., J.X.) independently
assessed these results, and they resolved any disagree-
ments by means of discussion with a third reviewer
(H.L.).
To select the studies, we rst excluded irrelevant
records after reading the titles and abstracts. Then we
scanned the full texts of articles of potential interest.
After we excluded irrelevant and duplicate records, we
included only the studies that met the inclusion criteria.
Inclusion and exclusion criteria. We included all
clinical studies whose investigators described dental
implant failure rates in patients with well-controlled
diabetes and patients with diabetes that was not well
controlled. Investigators had tested patients glycemic
levels preoperatively. We excluded animal studies and
in vitro studies, reviews, letters, case reports, comments,
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and studies whose investigators did not compare patients
with diabetes who did and who did not have good gly-
cemic control as well as studies for which we found no
available data to extract.
Data extraction and quality assessment. Two
authors (Q.S., J.X.) independently extracted the following
information from each included study: the name of the
rst author and the year of publication; the country in
which the study was conducted; the study design; the
characteristics of the study participants, including
number of patients, type of diabetes, age range, and
glycemic level; and the number of dental implants and
data related to dental implant failures.
Two authors (N.H., C.C.) completed the quality
assessment by using the Newcastle-Ottawa Scale
(NOS).17 In this assessment tool, study selection,
comparability, and outcome are used to appraise the
methodological quality of the included studies, with a
maximum of 9 points for each study.17
Data synthesis and analysis. We used the Compre-
hensive Meta-Analysis (Version 2.0; Biostat) software
to perform the meta-analysis of the extracted data.
We pooled the relative risk (RR) and 95% condence
interval (CI) values to estimate the relative effect of
glycemic level on dental implants. We tested heteroge-
neity between studies using I2 tests. I2 values of 25%, 50%,
and 75% were considered low, moderate, and high,
respectively.18 We used a xed-effects model if the
heterogeneity was low; otherwise, we used a random-
effects model.
We used the subgroup analysis to identify the asso-
ciation between implant failure rate and the stage at
which the implant failed. On the basis of the results of
previous studies,19,20 we divided the failed implants into
the following 2 groups: early failure (before or at abut-
ment connection) and late failure (after implant loading).
In some of the included studies, investigators divided
different groups, such as a group of patients with poorly
controlled diabetes and a group of patients with
moderately well-controlled diabetes. To perform a
quantitative analysis, we combined these groups.
RESULTS
Study selection. Initially, we identied 360 records by
means of our search. We reviewed 40 full-text articles
and 2 clinical trials, of which 9 studies met our inclusion
criteria.15,16,21-27 However, the investigators of 1 of the 9
studies did not provide data related to dental implant
failure rates.27 Although we sent an e-mail to the
ABBREVIATION KEY. FPG: Fasting plasma glucose.
HbA1c: Glycosylated hemoglobin. NA: Not applicable. NOS:
Newcastle-Ottawa Scale. NWCD: Not well-controlled diabetes.
T2D: Type 2 diabetes. WCD: Well-controlled diabetes.
 ORIGINAL CONTRIBUTIONS

corresponding author,
we did not receive a reply. Total articles (n = 360)
Moreover, we noted that PubMed (n = 310)
2 articles15,24 were 2 parts The Cochrane Library (n = 30)
of 1 clinical research trial ClinicalTrials.gov (n = 17)
that had the same results; Hand search (n = 3)
therefore, we included
only the article15 whose Duplicates removed (n = 11)
authors had focused on
the implant failure rate Titles and abstracts screened
and had provided (n = 349)
comprehensive data.
Ultimately, we included 7 Articles excluded as
studies15,16,21-23,25,26 in our obviously irrelevant (n = 307)
meta-analysis. Figure 1
shows the ow diagram Assessed for eligibility (n = 42)
of the study selection Full-text articles (n = 40)
process. Clinical trials (n = 2) Articles excluded (n = 35)
Not grouped according to glycemic level (n = 19)
Summary of the
No group of patients with diabetes that was not
included studies. Re- well controlled (n = 12)
garding design type of Clinical trials at the recruiting stage (n = 2)
the included studies, No available data (n = 1)*
5 were prospective Articles included in the
Duplicate study (n = 1)
15,16,21,22,25 meta-analysis (n = 7)
studies and
2 were retrospective
studies.23,26 These studies
included a total of 252 Figure 1. Flowchart of retrieved studies. * The authors e-mailed the corresponding author but did not receive a
reply. The data of 1 study were the same as 1 included study because they were 2 parts of the same clinical
patients, including 136 research trial.
patients with well-
controlled diabetes and
116 patients with diabetes that was not well controlled; all A total of 587 dental implants had been implanted in
patients had type 2 diabetes. The investigators of 6 patients in the included studies, and 25 of those implants
studies15,16,21-23,25 provided information about the glyce- had failed. Nine failed dental implants were in patients
mic level of the patients by stating an estimation of with well-controlled diabetes, and 16 were in patients
glycosylated hemoglobin (HbA1c). For the group of pa- with diabetes that was not well controlled. Therefore, the
tients with well-controlled diabetes, the HbA1c level was total implant failure rates were 3.15% (patients with well-
less than 8%, whereas for the group of patients with controlled diabetes) and 5.32% (patients with diabetes
diabetes that was not well controlled, the HbA1c level that was not well controlled). Table 215,16,21-23,25,26 shows
26
ranged from 7% to 13.8%. In 1 study, the investigators information related to the dental implants.
had determined patients glycemic levels mainly by the Meta-analysis. The results of a pooled analysis did
fasting plasma glucose (FPG) level. For the group with not indicate a direct association between the glycemic
well-controlled diabetes, the FPG level was less than 6.1 level in patients with diabetes and the dental implant
millimoles per liter, and for the group of patients with failure rate (Figure 216,22,25,26). The pooled RR for patients
diabetes that was not well controlled, the FPG level ranged with well-controlled diabetes versus patients with dia-
from 6.2 mmol/L to 8.3 mmol/L. Table 115-17,21-23,25,26 shows betes that was not well controlled was 0.620 (95% CI,
the characteristics of the patients. 0.225-1.705), and there was no signicant difference
We used the NOS17 to assess the included studies (P .354). The I2 value was 0 (P .437); therefore, we
methodological quality; Table 115-17,21-23,25,26 shows the considered the heterogeneity between studies to be low,
results. Five studies15,16,21,22,25 scored more than 6 points, and we selected a xed-effects model for the meta-
so we considered those studies to be of high quality. Two analysis.
studies23,26 scored 6 points, so we considered those We evaluated the time at which the implant failure
studies to be of moderate quality. For the item of selec- occurred (that is, early and late) in patients with diabetes
tion, because of small sample sizes, we determined that by means of a subgroup analysis. There was no signi-
the representativeness of the patients with diabetes in the cant difference in either early or late failures between the
studies by Turkyilmaz23 and Huang and colleagues26 may 2 groups (Figure 216,22,25,26). The pooled RR in the early
have been inadequate. failure subgroup was 0.817 (95% CI, 0.096-6.927; P .853,

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 ORIGINAL CONTRIBUTIONS

TABLE 1
Summary of the included studies.
STUDY STUDY FOLLOW-UP DIABETES PATIENTS, AGE, Y METHOD OF GLYCEMIC GLYCEMIC NOS
DESIGN TIME TYPE NO. GLYCEMIC LEVEL OF LEVEL OF SCORE
(WCD*/ LEVEL PATIENTS PATIENTS
NWCD) ASSESSMENT WITH WCD WITH NWCD
Huang and Retrospective 12-37 mo T2D 21 (5/16) 45-67 FPG# < 6.1 mmol/L** 6.1-8.3 mmol/L 6
Colleagues,26
2004
Dowell and Prospective 4 mo T2D 25 (10/15) 51-81 HbA1c 6.1%-8.0% 8.0%-13.8% 7
Colleagues,15
2007
Tawil and Prospective 0-12 y T2D 45 (22/23) 43-84 HbA1c # 7% > 7% 7
Colleagues,25
2008
Turkyilmaz,23 Retrospective 12 mo T2D 10 (6/4) 45-71 HbA1c 5.0%-8.0% 9.0%-10.0% 6
2010
Oates and Prospective 12 mo T2D 67 (47/20) 38-83 HbA1c 6.0%-8.0% > 8% 7
Colleagues,16
2014
Ghiraldini and Prospective 12 mo T2D 32 (16/16) 37-70 HbA1c 7.22% (0.56) 10.04% (1.15) 8
Colleagues,21
2015
Aguilar- Prospective 2y T2D 52 (30/22) 57 (3.8)/ HbA1c 6.1%-8% 8.1%-10% 8
Salvatierra and 61 (1.9)
Colleagues,22
2016
* WCD: Well-controlled diabetes.
NWCD: Not well-controlled diabetes.
Values given as a range or mean (standard deviation).
NOS: Newcastle-Ottawa Scale.
T2D: Type 2 diabetes.
# FPG: Fasting plasma glucose.
** mmol/L: Millimoles per liter.
HbA1c: Glycosylated hemoglobin.

xed-effects model), whereas in the late failure subgroup,
it was 0.572 (95% CI, 0.206-1.586; P .283, xed-effects
model).
DISCUSSION
Diabetes can have many negative effects on health.28
Complications in the vascular system may delay wound
healing, increase postoperative infection, and affect bone
metabolism in patients with diabetes.29-31 A careful diet
could effectively control the level of blood glucose and
the development and course of the illness.4,32 Unfortu-
nately, patients with diabetes lose more teeth than people
who do not have diabetes, and this certainly affects their
mastication function and diet.5,6
Owing to the many advantages of dental implant
restorations, increasingly, people, including patients with
diabetes, have accepted them as treatment. As mentioned
previously, osseointegration is a prerequisite for a suc-
cessful dental implant, and complications related to
hyperglycemia may affect this process and increase the
failure rate of dental implants, especially in patients with
diabetes that is not well controlled.10,11 Therefore, clini-
cians view glycemic control as being a critical variable in
identifying whether patients with diabetes are eligible for
implant therapy.15 On the basis of previous evidence, the
success rate for dental implants in patients with well-
controlled diabetes appears to be as good as the success
rate for dental implants in the general population.5,9,33
However, with limited evidence, the inuence of poor
diabetes control on implant success is unclear.
In our meta-analysis, we aimed to compare the
implant failure rates between patients with well-
controlled diabetes and patients with diabetes that was
not well controlled. After screening, we determined that
7 studies15,16,21-23,25,26 met our inclusion criteria, and we
noted that the investigators of all 7 of those studies had
provided information about patients glycemic control.
The investigators of 6 of the studies had reported the
HbA1c values of the patients with diabetes,15,16,21-23,25 and
the investigators of 1 study had reported the patients
FPG level.26 According to the results of 3 of the
studies,15,22,23 there were no dental implant failures in
patients with diabetes that was well-controlled or not
well-controlled. Some patients with diabetes in the
included studies received more than 1 dental implant.
However, according to the reports, patients with diabetes
in 6 of the studies did not have multiple implant failures.
In 1 study,16 3 patients (2 of whom had well-controlled

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 ORIGINAL CONTRIBUTIONS

diabetes and 1 of TABLE 2

whom had dia- Dental implant failure rates in included studies.
betes that was not
well controlled) STUDY DENTAL IMPLANTS IN THE DENTAL IMPLANTS IN THE
GROUP WITH WCD* GROUP WITH NWCD
had multiple
Total Early Late Failure Total Early Late Failure
implant failures Failure Failure Rate, % Failure Failure Rate, %
each of these pa-
Huang and Colleagues,26 2004 10 0 0 0 42 3 2 11.90
tients had 2 failed
Dowell and Colleagues,15 2007 18 0 NA 0 21 0 NA 0
implants. Further-
Tawil and Colleagues,25 2008 103 NA 1 0.97 152 NA 6 3.95
more, the authors
16 Turkyilmaz,23 2010 15 0 0 0 8 0 0 0
of this study
Oates and Colleagues,16 2014 94 1 6 7.45 40 0 2 5.00
considered these 3
Ghiraldini and Colleagues,21 2015 16 0 0 0 16 0 0 0
patients implants
Aguilar-Salvatierra and Colleagues,22 2016# 30 NA 1 3.33 22 NA 3 13.64
to be failures
* WCD: Well-controlled diabetes.
because the pa- NWCD: Not well-controlled diabetes.
tients had been The authors only studied early failure rate.
lost to follow-up. NA: Not applicable.
The investigators did not report the early failure rate.
The total rate of # In this study, the investigators immediately loaded the implants.
implant failure
among the patients
with diabetes that was not well controlled was 5.32%; this types of failure are different.19,20,34 Early failures happen
rate was higher than the rate among patients with well- before abutment connection, which means that the
controlled diabetes (3.15%). However, the results of our implant fails to establish osseointegration with the alve-
pooled analysis indicated that patients with diabetes that olar bone. Late failures happen after abutment connec-
was not well controlled were not likely to have a higher tion and implant loading and are associated mainly with
rate of dental implant failure than were patients with peri-implantitis and overloading. For patients with dia-
well-controlled diabetes (RR 0.620; 95% CI, 0.225-1.705; betes that is not well-controlled, hyperglycemia may
P .354). affect the turnover of the alveolar bone, which can lead to
Investigators categorize dental implant failures as failed or delayed osseointegration16; hyperglycemia also
early and late failures, and the etiologies of these may increase the risk of experiencing peri-implantitis.35

Statistics for
Each Study Relative
Risk
Study Subgroup Ratio 95% CI z Value P Value Risk Ratio and 95% CI Weight, %

Huang and Colleagues,26 2004 Both 0.782 0.040-15.137 0.163 .871 11.66
Tawil and Colleagues,25 2008 Both 0.246 0.030-2.013 1.308 .191 23.18
Oates and Colleagues,16 2014 Both 1.489 0.323-6.860 0.511 .609 43.91
Aguilar-Salvatierra and Colleagues,22 2016 Both 0.244 0.027-2.196 1.258 .208 21.25
Total 0.620 0.225-1.705 0.926 .354
Huang and Colleagues,26 2004 Early failure 0.558 0.031-10.031 0.395 .693 54.79
Oates and Colleagues,16 2014 Early failure 1.295 0.054-31.121 0.159 .873 45.21
Subtotal 0.817 0.096-6.927 0.186 .853
Huang and Colleagues,26 2004 Late failure 0.782 0.040-15.137 0.163 .871 11.86
Tawil and Colleagues,25 2008 Late failure 0.246 0.030-2.013 1.308 .191 23.57
Oates and Colleagues,16 2014 Late failure 1.277 0.269-6.057 0.307 .759 42.96
Aguilar-Salvatierra and Colleagues,22 2016 Late failure 0.244 0.027-2.196 1.258 .208 21.61
Subtotal 0.572 0.206-1.586 1.074 .283

0.01 0.1 1 10 100

Favors WCD Favors NWCD

Figure 2. Forest plot of the comparison between patients with well-controlled diabetes and patients with diabetes that was not well-controlled.
CI: Condence interval. NWCD: Not well-controlled diabetes. WCD: Well-controlled diabetes.

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 ORIGINAL CONTRIBUTIONS
Therefore, we performed a subgroup analysis to identify
the association between the rate of dental implant failure
and the stage at which the failure occurred. In our meta-
analysis, the investigators of 5 studies15,16,21,23,26 described
the early failure of dental implants, and the results of our
pooled analysis indicated that there was no signicant
difference in the 2 groups of patients (RR, 0.817; 95% CI,
0.096-6.927; P .853). Hence, our results may indicate
that patients with diabetes that is not well controlled
could achieve adequate osseointegration. This conclusion
is similar to that of Oates and colleagues,16 who suggested
that patients with diabetes that is not well controlled
need a delayed healing period. The investigators of 3
studies15,21,23 found no early failures among patients in
the 2 groups. The investigators of 6 studies16,21-23,25,26
described the rate of late failure, and the investigators of
2 of those studies21,23 reported that there were no failed
implants in patients with diabetes that was either well
controlled or not well controlled. After conducting the
pooled analysis, we found no signicant difference
(RR 0.572; 95% CI, 0.206-1.586; P .283). These results
indicate that, under certain conditions, dental implants
placed in patients with diabetes that is not well
controlled could have similar failure rates as implants
placed in patients with well-controlled diabetes.
To our knowledge, we believe that our study is the
rst to compare the dental implant failure rates of pa-
tients with well-controlled diabetes and patients with
diabetes that was not well controlled using a compre-
hensive quantitative analysis. Not only did we research
electronic databases to identify potential interests, but
also we manually examined reference lists from relevant
studies. In the meta-analysis and subgroup analyses, we
noted that the included studies had low heterogeneity,
which signicantly increased the statistical power of our
analysis. On the basis of the evidence, the failure rate in
patients with diabetes that was not well controlled was
not higher than in patients with well-controlled diabetes.
However, we identied 3 limitations in our meta-
analysis. First, the glycemic levels of the patients with
diabetes overlapped. The HbA1c levels were less than 8%
in patients with well-controlled diabetes, and the levels
ranged from 7% to 13.8% in patients with diabetes that
was not well controlled. Besides, the methods of evalu-
ating glycemic levels were inconsistent: the investigators
of 6 studies used HbA1c, and the investigators of 1 study
used FGP. Second, because of the limited number of
included clinical studies, we did not perform an analysis
of publication bias of the included studies. Third, because
of insufcient data, we did not analyze the effect of
multiple implant failures to determine the statistical
power of this meta-analysis.
CONCLUSIONS
On the basis of the evidence, the results of our meta-
analysis failed to show a difference in the failure rates for
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dental implants between patients with well-controlled
diabetes and patients with diabetes that was not well
controlled; however, this result does not mean that the
failure rates were the same for these 2 groups. Patients with
diabetes that is not well controlled may need a longer
healing period after surgery. Considering the limitations of
the results of this meta-analysis, we believe that future
well-designed studies whose investigators allow for
adequate control for confounding factors are required. n
Dr. Shi is a doctoral candidate, Institute of Stomatology, Chinese Peoples
Liberation Army General Hospital, Beijing, China.
Dr. Xu is the chief physician, Institute of Stomatology, Chinese Peoples
Liberation Army General Hospital, Beijing, China.
Dr. Huo is an attending physician, Institute of Stomatology, Chinese
Peoples Liberation Army General Hospital, Beijing, China.
Dr. Cai is an attending physician, Institute of Stomatology, Chinese
Peoples Liberation Army General Hospital, Beijing, China.
Dr. Liu is a professor and chief physician, Institute of Stomatology,
Chinese Peoples Liberation Army General Hospital, Fuxing Road, #28,
100853 Beijing, China, e-mail liuhc301@hotmail.com. Address correspon-
dence to Dr. Liu.
Disclosure. None of the authors reported any disclosures.
This study was supported in part by grants from the National High
Technology Research and Development Program (863 Program) of China
(2015AA033502) and the National Natural Science Foundation of China
(81541111).
Drs. Shi and Xu contributed to this article equally and should be regarded
as co-rst authors.
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