Dental implant survival in diabetic patients; Review and recommendations

Abstract

Rising population of diabetic individuals across the world has become a big concern to the society. The persistent hyperglycemia may affect each and every tissue and consequently results in morbidity and eventually mortality in diabetic patients. A direct negative response of diabetes has been observed on oral tissues with few contradictions however, little are known about effect of diabetes on dental implant treatment and the consequent results. Many studies concerned with osteointegration and prognosis of dental implant in diabetic patients have been conducted and published since 1994. These studies have been critically reviewed to understand the impact of diabetes on the success of dental implant and the factors to improve osseointegration and consequently survival of dental implant in diabetic patients. Theoretical literatures and studies in diabetic animals substantiate high failure rate of implants but most of clinical studies indicated statistically insignificant failure of dental implants even in moderately uncontrolled diabetic patients. Success of dental implant in well and fairly controlled diabetic patients with proper treatment planning, prophylactic remedies and adequate postsurgical maintenance appears as good as normal individuals.

Full text

National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 142
Review Article
IntroductIon
The recent studies in China[1] and India[2] has shown that
the number of diabetic individuals has surpassed the
estimate of IDF-2009[3] i.e., approximately 285 million
people worldwide will have diabetes in 2010 and by
2030, 438 million people of adult population is expected
to have diabetes with majority of eected population
from China, India and USA.
The comforts like natural dentition, conservative treatment
compared to teeth supported FPDs and long term success
for the edentulous patients, as well as partially edentulous
patients have made dental implants supported prosthetic
treatment as an attractive substitute to traditional
removable or xed dental prosthesis besides being costly
and lengthy procedures with surgical intervention.[4-6] The
growing economy of developing nations like china and
India has also been playing a key role in popularizing the
implant dental treatment. In light of above facts, the dental
fraternity may encounter with more number of diabetic
patients for dental implant treatments.
Diabetes mellitus is a chronic disorder of carbohydrate
metabolism characterized by hyperglycemia, reecting
distortion in physiological equilibrium in utilization
of glucose by tissue, liberation of glucose by liver and
production-liberation of pancreatic anterior pituitary and
adrenocortical hormone. The debilitating characteristic
of diabetes mellitus was known as early as in second
century AD, when Areteous named it as diabetes means
“a siphon” as he perceived that the condition was
characterized by melting down of flesh and limb into
urine.[7] Various modern research and discoveries have
Departments of Prosthodontics,
Government Dental College, Raipur,
Chhattisgarh, 1PIDS, Gorakhpur,
Uttar Pradesh, India
Address for correspondence:
Dr. Rajendra Kumar Dubey,
Department of Prosthodontics,
Government Dental College,
Raipur, Chhattisgarh, India.
E‑mail: rkdubey2005@yahoo.co.in
Access this article online
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Website:
www.njms.in
DOI:
10.4103/0975-5950.127642
Rajendra Kumar Dubey, Deepesh Kumar Gupta,
Amit Kumar Singh1
ABSTRACT
Rising population of diabetic individuals across the world has become a big concern to the
society. The persistent hyperglycemia may affect each and every tissue and consequently
results in morbidity and eventually mortality in diabetic patients. A direct negative response of
diabetes has been observed on oral tissues with few contradictions however, little are known
about effect of diabetes on dental implant treatment and the consequent results. Many studies
concerned with osteointegration and prognosis of dental implant in diabetic patients have
been conducted and published since 1994. These studies have been critically reviewed to
understand the impact of diabetes on the success of dental implant and the factors to improve
osseointegration and consequently survival of dental implant in diabetic patients. Theoretical
literatures and studies in diabetic animals substantiate high failure rate of implants but most of
clinical studies indicated statistically insignificant failure of dental implants even in moderately
uncontrolled diabetic patients. Success of dental implant in well and fairly controlled diabetic
patients with proper treatment planning, prophylactic remedies and adequate postsurgical
maintenance appears as good as normal individuals.
Key words: Dental implant, hyperglycemia, osteointegration
Dental implant survival in
diabetic patients; review and
recommendations
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Dubey, et al.: Dental implant survival in diabetics
National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 143
shown that diabetes mellitus, more or less, affects
every tissues of body directly or indirectly through late
complications [Table 1].[8] Concerning the eect on oral
tissues, Loe.[9] recognized the periodontal disease as sixth
major complication of diabetes. Number of studies has
proved the adverse eect of chronic hyperglycemia on oral
mucosa and with some controversies on alveolar bone.
This review caters actual scenario to practicing dentists
regarding success and failure of dental implant treatment
in diabetic individuals observed by various studies. The
experience based suggestions and experimental studies
about increasing osteointegration and consequently
improving success rate of dental implant treatment in
diabetic patients have also been discussed.
Eect of diabetes on bone and osteointegration
The persistent hyperglycemia in diabetic individuals,
inhibit osteoblastic activity and alters the response of
parathyroid hormone that regulates metabolism of
Ca and P,[10] decreases collagen formation during callus
formation,[11] induces apoptosis in lining cells of bone[12]
and increases osteoclastic activity[13,14] due to persistent
inammatory response. It also induces deleterious eect
on bone matrix and diminishes growth and accumulation
of extracellular matrix.[15] The consequent result is
diminished bone formation during healing, which is
observed in number of experimental animal studies.[16-19]
Type -1 diabetes causes decreased bone mineral density,
as well as reduced bone formation and higher bone
resorption[20] whereas Type -2 diabetes produces normal
or greater bone mineral density in some patients.[21] It
has been observed that insulin not only reduces the
deleterious eect of hyperglycemia by controlling it but
also stimulates osteoblastic activity. Hence, bone matrix
formation in insulin treated experimental models is
similar to control ones.[22]
Most of the studies have been performed in
streptozotocin/alloxan induced diabetic experimental
models (rat/rabbit) to observe osseointegration of
implants. Histo-chemical/histomorphic/planimetric/
biomechanical torque/manometric analysis showed that
bone volume formed in diabetic animals was similar
to non-diabetic animals[23] however, bone implant
contact (BIC) in diabetic animals was lesser compared
to non-diabetics.[24] The rate of mineral apposition in
newly formed bone and bone density around implant
was signicantly less in uncontrolled diabetic animals.[25]
The bone volume and bone density around implant in
insulin controlled diabetic animals was observed similar
or greater to non-diabetic but BIC was found signicantly
less[22,26-30] (Even in insulin controlled diabetic animals).
Only few case studies for histological observation of
dental implant osseointegration in human being have
been reported. In one report,[31] an implant was placed and
intended to support an overdenture in 65-year-old diabetic
women was retrieved after 2 months due to prosthetically
unfavorable condition. In histological analysis, no
symptoms of implant failure recognized with 80% bone
implant contact ratio. A case of diabetes mellitus type-2
having implant failure within 6 months, was reported by
Park JB[32] with conclusion that osseointegration was not
aected by diabetes mellitus as there was no sign and
symptoms of failure before loading.
Success/failure of dental implants in diabetic patients
Most of the studies[43,44,46,48] observed slightly high
percentage of early failure of implants in diabetics
compared to late failure. Some reports[45,46,50] indicated
increased failure rate within rst year of placement of
implant. The published retrospective and prospective
studies data, retrieved through various sources from 1994
to 2011 [Table 2], indicated that the success rate of dental
implants in diabetic patients were in range of 85.5-100%
and were comparable to the non-diabetic patients. Most of
the studies were of opinion that success rate in well/fairly
controlled diabetics was either equal or insignicantly
lower than normal individuals. Two studies[36,39], has
taken chance to involve uncontrolled diabetic patients
for dental implantation and observed encouraging results
as early implant success was similar to non-diabetics.
However, it is noteworthy that number of patients and
implants placed (4 implants in 3 patients) in uncontrolled
diabetics was quite low and all the patients selected
were free of micro and macro-vascular complications.
Only two studies[36,41] reported signicantly high failure
of implant in diabetic patients even when glucose level
was adequately under control. One of these studies
retrospectively included early, as well as late failures of
implants over the period of 10 years but did not specify
the glycemic control over that period. While other study,
prospective in nature, observed signicantly high early
failures with probable reason that placement of multiple
adjoining implants in diabetic patients increased the
failure rates due to large wound, delayed healing and
greater force posed over implants. Inadequate time (study
period 90 days only) provided for osseointegration and
regaining stability to implant in the study seems to be the
cause of observing very high failure in diabetic patients.
Most of the studies[43,44,46,48] observed slightly high
percentage of early failure of implants in diabetics
Table 1: Late‑onset complications of diabetes
Microvascular complications Macrovascular complications
Retinopathy Cardiovascular disease
Nephropathy Peripheral vascular disease
Neuropathy-Peripheral and autonomic Cerebrovascular disease
Erectile dysfunction
Periodontal disease
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Dubey, et al.: Dental implant survival in diabetics
National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 144
Table 2: Outcome of studies showing survival/success of dental implant in diabetic patients
Investigator Year Type of
study
Type of
diabetes
Nature of
diabetes
No. of
patients
No. of
implants
Duration of
study
Surviv‑
al‑rate %
Conclusion/remark
TurkayiImaz
et al
.[33]
2010 Prospective Type-2 Controlled 10 23 1 year 100 No evidence of diminished clinical success
or signicant complication was found with
different implant supported prosthesis
like Cemented/screwed FPD or removable
overdentures placed in well or moderately
well controlled diabetes
Carr
et al
.[34]
2010 Retrospective Type-1
and 2
Controlled 412 1514 2 years Not
specied
Diabetes type-1 and 2 was not associated
with late implant failure
Oates
et al
.[35]
2009 Prospective Type-2 Controlled
and
uncontrolled
20 30 4 months 100 The study demonstrated that person with
poor glycemic control had greater decrease
in implant stability and required longer
time for healing but most of the implants
attained nearly baseline stability in long
duration even in poorly controlled diabetic
patients
ND 10 12 100
Wing Loo
et al
.[37]
2009 Prospective Type-2 Controlled 138 275 90 days 32 Early implant failure was signicantly
greater in diabetic patients when multiple
adjoining implants were placed
ND140 346 90 days 86
Twail
et al
.[38]
2008 Retrospective Type-2 Well and
fairly
controlled
45 255 1-12
months
97.2 No signicant difference in success
rate of dental implant in diabetics and
non-diabetics. No signicant effect of
duration of diabetes
ND45 244 1-12
months
98.8
Dowell
et al
.[39]
2007 Prospective Type-2 Controlled
and
Uncontrolled
35 50 4 months 100 No evidence of diminished clinical success
or signicant early healing complications
associated with implant therapy based on
the glycemic control levels of patients with
type-2 diabetes mellitus
Balshi
et al
.[39]
2007 Prospective Type -2 Controlled 1 18 30 months 100 An immediate loading protocol can be
successful and result in osseointegration in
patients with diabetes
Alsaadi
et al
.[40]
2008 Retrospective Type-1 Controlled 1 1 Not
specied
00 Local and systemic factors interfere with
the osseointegration of dental implants.
Type 1 and 2 diabetics had higher failure
than non-diabetics but insignicant
statistically
Type-2 Controlled 283 719 96
Peter Moy
et al
.[41]
2005 Retrospective Not
specied
Adequately
controlled
48 Not
specied
10 years 68.7 Failure even in adequately controlled diabetic
patients was signicantly high and failure
evenly continued from period of placement
until observational period of 10 years
Huang
et al
.[42]
2004 Prospective Type-2 Controlled 21 52 12-36
months
90.4 The clinical outcome of dental implants,
restored with FPD, in well-controlled
type 2 diabetes mellitus was satisfying
and encouraging
Pleed
et al
.[43]
2003 Prospective Type-2 Controlled 41 141 1 year 97.3 Studied failure of implant supported
overdentures and found no correlation
between failed implant and glucose level
5 years 94.4
Fazzad
et al
.[44]
2002 Retrospective Not
specied
Controlled 25 136 3-6 months 96.3 The study did not encounter a higher
failure rate in diabetic patients than
normal population, if plasma glucose level
is normal or close to normal which is
assessed by personal interview
1 year 94.1
Morris
et al.
[45]
2000 Retrospective Type-2 Controlled 255 36 months 92.2 Success rate of implants, supporting
mixed variety prosthesis was marginally
signicant less in diabetics than
non-diabetics. The experience of surgeon
does not produce clinically signicant
improvement in implant survival, while
use of 2% chlorhexidine, preoperative
antibiotics, and hydroxy-appetite implants
improves the survival rate in diabetics by
4.5%, 10.55, and 13.2% respectively
ND 2,
637
36 month 93.2
Fiorllini
et al
.[46]
2000 Retrospective Not
specied
Controlled 40 215 1 year 88.8 Out of 31 failures, 24 failures occurred
within rst year of functional loading.
Interestingly, implant failure was not
signicantly different from non-diabetic
patients
6.5 years 88.8
Contd
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Dubey, et al.: Dental implant survival in diabetics
National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 145
compared to late failure. Some reports[45,46,50] indicated
increased failure rate within first year of loading
suggesting the risk of implant failure is associated with
uncovering of implants and early phase of implant
loading. T W Oates observation[35] also supports high
early failure in diabetic patients as such patients
experienced low implant stability quotient (ISQ) in
period of 2-12 weeks and lower the level of glycemic
control, higher the amount of ISQ reduction and
longer the duration of recovery in ISQ at base level was
required. However, most of implants aained base level
of stability within 4 months even in uncontrolled diabetic
patients, if the patients were refrained with micro- and
macro-vascular complications.
Duration of diabetes signicantly aected the success of
dental implant, observed in one study[48] while another
did not demonstrate signicantly higher late implant
failures in diabetic patients even with longer duration.
Overall lower success of implant in patients with diabetes
of longer duration may be due to higher chance of
micro-vascular complications which consequently lead
to delayed healing around implants and hence higher
early failure.
Few studies,[40] demonstrated signicantly higher failure
of implant in type-1 diabetic patients than patients with
type-2 diabetes (in one study, only one implant placed
in a person with diabetes type-1 and it failed i.e., failure
rate=100%, an extremely unlikely true estimate of risk).
While one study[34] did not nd any signicant dierence
in late failure of dental implant in type-1 and type-2
diabetic patients. Higher failure rate in diabetic type-1
Table 2: Contd...
Investigator Year Type of study Type of
diabetes
Nature of
diabetes
No. of
patients
No. of
implants
Duration of
study
Survival‑
rate %
Conclusion/remark
Accursi[47]
(Thesis)
2000 Retrospective Mixed Controlled 15 59 1-17 years 93 The diabetic patients were no more likely
to experience implant failure than the
non-diabetic patients
ND 111 1-17 years 94
Oslen and
Shernoff
et al.
[48]
2000 Prospective Type-2 Controlled 89 178 5 years 88.0 Success rate of implants supporting
overdentures was found satisfactory level in
type-2 diabetic patients. In regression analysis,
duration of diabetes (
P
<0.025) and implant
length (
P
<0.001) was found to be statistically
signicant predictors of implant failure
Balshi
et al.
[49]
1999 Retrospective Type-2 Controlled 34 227 At time
of second
surgery
94.4 Early implant failure greater than late implant
failure. The success rate in diabetic patients
were comparable to non- diabetics (when
compared with results of other studies as
control group was not provided in this study).
Glycemic control, antibiotic protection and
smoking avoidance protocol recommended
177 After
restoration
(after
loading
99.9
Shernoff
and Oslen
et al
.[50]
1994 Prospective Type-2 Controlled 89 178 12 months 92.7 Survival rate of implants for supporting
removable over dentures was 97.8% at
uncovering (4 implants failed), while success
rate decreases up to level of 92.7% as 9
additional implants had failed during 1 year
period
*ND‑ denotes non‑diabetic controls undertaken in study
may be due to depletion of insulin in tissues whereas
presence of insulin in tissues of type-2 diabetic individuals
may reduce deleterious eect of hyperglycemia. There
is no study exclusively reported the survival/success of
implant in type-1 diabetes however, very few retrospective
studies had subject with type-1 and type-2 diabetes but
lile number of type-1 diabetic subjects.
Immediate loading did not signicantly aect the survival
of dental implant in diabetic patients provided their
plasma glucose level were under normal range.[37,39,44,45]
Balshi SF[39] reported 100% survival of 18 implants after
2.5 years after placement followed by immediate loading
with screwed retained xed prosthesis in a 71-year-old
diabetic patient. The study suggests that controlled
mechanical stimuli over implant can be benecial for
osseointegration and implant survival.
The studies[37,45] observed lower survival of implant in
diabetic patients of very old age group but dierence was
not statically signicant. Although, none of the studies
had compared success of implant in diabetic females and
males but number of studies reported survival as good
as in females compared to males in general population.
The experience of surgeons and advance surgical process
did not signicantly aect success of dental implant in
diabetics as observed in studies.[38,46]
Measures for improving success of dental implant in
diabetics
Good glycemic control, preoperative and post-operative,
is required to achieve improved osseointegration in
diabetics.[51] Prophylactic antibiotics [Table 3] have
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Dubey, et al.: Dental implant survival in diabetics
National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 146
shown to be eective for success of dental implants
in diabetic patients and use of 0. 12% chlorhexidine
further improves the success rate.[45,48-52] Certain factors
like implant surface characteristics (implant coated
with bioactive material) and higher implant length
and width has been shown to improve success rate of
implant in diabetic patients. Some researcher has found
positive results in experimental studies to improve
osseointegration and results are yet to be veried in
human being. In few studies,[53,54] it was observed that
systemic administration of aminoguanidine reduced
the deleterious eect of diabetes on osseointregration.
Satana et al.[55] used rhFGF2 (recombinant human
fibroblast growth factor-2) encapsulated with poly
glycosylated poly lactide (PGLA) membrane in
calvarial defect of diabetic rat and formation of normal
bone level was observed in histomorphic analysis.
Wang et al.,[56] in a study based on similar concept,
used rrIGF-1(Recombinant rat insulin like growth
factor) encapsulated with PGLA around Ti implant
inserted in calvaria of diabetic rat. It was found in
histomorphic analysis that diabetic rat with rrIGF-1
had higher BIC around the implant compare to rat
without rrIGF-1 after 4-8 weeks of surgical placement.
A recent hypothesis was made by Bai et al.[57] that
adiponectin, an insulin sensitive adipokine may
improve osseointregration in diabetic patients by
infusing it systemically or using locally as it has shown
potent anti-inflammatory properties and increased
bone density by enhancing osteoblast and inhibiting
osteoclast formation.
dIscussIon
Most of the experimental studies have been indicated
that the bone matrix formation and bone mineralization
was almost equal in controlled diabetic and non-diabetic
animals but BIC was lower even in controlled diabetic
subjects. Number of studies has proposed and explained
mechanism of deleterious eect of diabetes over wound
healing and true association (osseointegration) of
bone to implant surface [Figures 1 and 2]. However
studies,[31,32] performed in humans specifically with
diabetes type-2, observed insignicant eect over BIC
and consequently good osseointegration of dental
implant in controlled diabetic patients. As most of the
experimental studies conducted in rats and rabbits,
the architectural and compositional dierence in bone,
higher metabolic rate, very permissive bone healing,
faster skeletal changes and bone turnover[58,59] may be
the reason for the dierence in results of experimental
animals and humans. The difference in developing
diabetes (alloxan or streptozotocin destruct beta
cells of Langerhans consequently induces diabetes)
in experimental animals and human being (type-2
diabetes develop due to glucose resistance at cellular
level and higher level of glucose in tissue consequently
suppress the function of beta cells of Langerhans in
long duration) maybe one reason for the difference
in BIC. The result of an experimental study in obese
diabetic rat strengthens the above explanation, as no
difference in BIC was observed in obese diabetic rat
than normal one.[60]
Most of clinical studies reported success of dental
implant in diabetic individual as good as normal
peoples. The reason may appear to be the inclusion
of controlled diabetics in the almost all studies.
The persistent hyperglycemia is responsible for
development of micro-vascular complication and
consequently the early or late implant failure. Hence
the uncontrolled level of diabetes, reected through
measurement of glycated hemoglobin HbAc1 (indicate
average glucose level over preceding 2-3 months
period,[61] level 6 to 8 shows well controlled, 8.1 to 10
moderately controlled and more than 10 shows poorly
controlled diabetes), persistent for longer duration
with sign of micro-vascular complication may aect
the success of dental implant signicantly. However,
none of the study included such uncontrolled patients
or in other word it can be concluded that none of the
surgeon had taken risk to insert dental implant in such
human beings.
Table 3: Prophylactic antibiotics and their doses
Name of antibiotic Preoperative (1 hour prior to surgery) Post‑operative (after surgery)
Adult dose Pediatric dose Adult dose Pediatric dose
Amoxicillin 2 gm VO 50 mg/kg of
body weight VO
500 mg orally every 8 h 25-50 mg/kg/day in divided dose 8 hourly
Amoxicillin+Clavulanate 2 g+125 mg VO 25-50 mg+2.5
mg/kg VO
500 mg+125 mg orally
every 12 h
25-45 mg/kg/day in doses divided every 12 h
Clindamycin 600 mg VO 20 mg/Kg VO 150-450 mg every 6 h 8-20 mg/kg/day in 3-4 divided doses as hydrochloride
Cephalexin or cefadroxil 2 g VO 50 mg/Kg VO 250-1000 mg every 6 h 25-100 mg/kg/day in divided doses every 6-8 h
Clarithromycin and
Azithromycin
500 mg VO 15 mg/kg VO 250-500 mg once a day 5-20 mg/kg once a day
Note: *The total dose in children should not surpass the adult dose, *Cephalosporins should not be used in patients with type‑1 penicillin hypersensitivity reaction, *Post‑oper‑
ative regimen should be prescribed minimum for 5‑7 days in diabetic patients, *Placement of dental implant in diabetic children is very rare, *Gentamycin, Metronidazole and
Vancomycin are also used as prophylactic antibiotics in I.V form but unusually nowadays
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Dubey, et al.: Dental implant survival in diabetics
National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 147
Figure 1: Mechanism of development of diabetic complication
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Even the fairly or moderately controlled diabetes
persisting for very longer duration (more than 10 years)
may produce complications and diminish the health of
tissues. The compromised condition along with some
unfavorable restorative factors may bargain the success of
dental implants. Therefore, numerous factors associated
with rehabilitation and diabetes itself, more or less, aect
the survival of dental implant in diabetic subjects[62]
[Table 4]. Cautious consideration of the mentioned factors
during rehabilitation improves the success and hence the
survival of dental implants in diabetic individuals.
conclusIon
The survival of dental implant in well/fairly
controlled diabetic patients appears as good as in
general population. Use of prophylactic antibiotic,
longer duration of post surgical antibiotic course,
chlorhexidine mouth rinse, bioactive material coated
implants and implant with higher width and length
seems to further improve the survival of implant in
diabetic individuals. Systemic administration of some
insulin sensitive adipokine and use of local growth
factors have been found to improve osseointegration
in diabetic experimental animals but yet to be veried
in human beings. However, it is advisable to delay the
placement of implant in poorly controlled diabetics till
the control of diabetes. Longer duration prospective
clinical studies with greater number of diabetic
individuals and non-diabetic controls are still required
to develop beer understanding of impact of diabetes
over dental implant success.
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Dubey, et al.: Dental implant survival in diabetics
National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 148
Figure 2: Possible effects of diabetes over mechanism of osteointegration
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Table 4: Probable factors affecting survival of dental implants
Factors associated with diabetes Rehabilitative factors
Type of diabetes Type of restoration
Diabetes duration Fixed/removable
Long span/short span
Diabetic condition i.e., level of
diabetes control reected through
HbAc1 level
Implant location
Maxillary/mandibular
Status of diabetic complication
i.e., micro- and/or
macro-angiopathy-absent/mild/
moderate/severe
Anterior/posterior
Implant length
Bone type and quality
Method of controlling hyperglycemia-
through dietary control/oral
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Surgical protocols
Surgical complexity
Duration for
osteointegration before
second surgery and
functional loading
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National Journal of Maxillofacial Surgery | Vol 4 | Issue 2 | Jul-Dec 2013 | 149
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How to cite this article: Dubey RK, Gupta DK, Singh AK. Dental
implant survival in diabetic patients; review and recommendations. Natl J
Maxillofac Surg 2013;4:142-50.
Source of Support: Nil. Conict of Interest: None declared.
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