Namita Khandelwal Conventional SLA and chemically

Thomas W. Oates
Adriana Vargas
modified SLA implants in patients
Peggy P. Alexander with poorly controlled type 2 Diabetes
John D. Schoolfield
C. Alex McMahan
mellitus – a randomized controlled
trial

Authors’ affiliations:
Namita Khandelwal, Graduate School of
Biomedical Sciences, University of Texas Health
Science Center at San Antonio, San Antonio, TX,
USA
Thomas W. Oates, Peggy P. Alexander, John D.
Schoolfield, Department of Periodontics, University
of Texas Health Science Center at San Antonio,
San Antonio, TX, USA
Adriana Vargas, Department of Comprehensive
Dentistry, University of Texas Health Science
Center at San Antonio, San Antonio, TX, USA
C. Alex McMahan, Department of Pathology,
University of Texas Health Science Center at San
Antonio, San Antonio, TX, USA
Present Address
Department of Periodontics, University of Medicine
and Dentistry at New Jersey, Newark, NJ, USA
Corresponding author:
Dr. Thomas W. Oates
Department of Periodontics
University of Texas Health Science Center at San
Antonio
7703 Floyd Curl Drive
San Antonio, TX 78229-3900, USA
Tel.: (210) 567-3590
Fax: (210) 567-6858
e-mail: oates@uthscsa.edu
Key words: diabetes mellitus, hyperglycemia, implant stability, implant surface, resonance
frequency analysis
Abstract
Objective: The objective of this study was to evaluate the potential for a chemically modified Sand
blasted, Large grit, Acid etched (SLA) surface, compared with a conventional SLA surface, to
enhance implant healing and integration in poorly controlled diabetic patients, a group previously
demonstrated to have compromises and delays in implant stabilization during the metabolically
active healing period following implant placement.
Materials and methods: The study enrolled 24 patients with type 2 diabetes, baseline HbA1c levels
between 7.5–11.4%, and a minimum of two posterior mandibular tooth sites at least 4 months
following extraction and appropriate for implant placement. Each patient, at a randomly selected
site, received an implant with the conventional SLA surface; at the second site, the patient received
an implant with the chemically modified SLA (modSLA) surface. Thus, 48 study implants were
placed. Implant stability was assessed using Resonance Frequency Analysis (RFA). Readings were
taken from the buccal and proximal directions for each implant. Implant stability (ISQ) was assessed
at the time of surgical placement (baseline) and 2, 3, 4, 6, 8, 10, 12, and 16 weeks following
implant placement.
Results: No significant differences in implant stability were observed between conventional SLA
implants and modSLA implants, and the time courses of implant stabilization following implant
placement were similar for the two implant types. Baseline ISQ and minimum ISQ was slightly
higher in subjects with higher HbA1c levels, but were similar during 12–16 weeks following
implant placement. Forty-seven (98%) of the 48 implants were determined to be successfully
osseointegrated and continued to restoration.
Conclusion: Implant stabilization was similar for the conventional SLA and chemically modified
SLA implants in type 2 diabetic patients with relatively poor glycemic control. Furthermore, this
study demonstrated clinically successful implant placement even in poorly controlled diabetic
patients.

Date:
Accepted 2 October 2011
To cite this article:
Khandelwal N, Oates TW, Vargas A, Alexander PP,
Schoolfield JD, Alex McMahan C. Conventional SLA and
chemically modified SLA implants in patients with poorly
controlled type 2 Diabetes mellitus – a randomized controlled
trial.
Clin. Oral Impl. Res. 00, 2011, 1–7
doi: 10.1111/j.1600-0501.2011.02369.x
The success of dental implant therapy is crit-
ically dependent upon osseointegration. The
intimate association of the bone with the
implant surface defining osseointegration is a
direct result of bone resorption and formation
following implant placement. Based on
animal models, both bone formation and
resorption are compromised in states of
hyperglycemia, suggesting that diabetes may
lessen implant success (Takeshita et al. 1997;
Nevins et al. 1998; Fiorellini et al. 1999; Ger-
ritsen et al. 2000; McCracken et al. 2000).
Consistent with this view, poor glycemic
control is considered a contraindication for
dental implants in patients with diabetes.
The majority of studies evaluating the
effects of diabetes on implant success have
studied patients with well-controlled diabetes
(Shernoff et al. 1994; Garrett et al. 1998; Ka-
pur et al. 1998; Balshi & Wolfinger 1999; Ab-
dulwassie & Dhanrajani 2002; Farzad et al.
2002; van Steenberghe et al. 2002; Peled et al.
2003; Moy et al. 2005; Javed & Romanos
2009). In addition, several studies have inves-
tigated implant success in patients with
unknown or poor levels of glycemic control

© 2011 John Wiley & Sons A/S 1

Khandelwal et al
Diabetes and implant stability
(Fiorellini et al. 2000; Dowell et al. 2007; Ta-
wil et al. 2008; Oates et al. 2009). Overall,
implant studies with diabetic patients have
documented varied levels of implant success
with failure rates ranging from 0% to 14.3%
per implant and from 0% to 31.8% per
patient, without a clear association with gly-
cemic control. One recent investigation
(Dowell et al. 2007; Oates et al. 2009) of den-
tal implant integration in patients with type
2 diabetes found that success rates for
patients with poor glycemic control were
similar to success rates in both well-con-
trolled and non-diabetic patients. However,
this study also found greater compromises in
implant stability during the metabolically
active healing period following placement in
direct relation to glycemic levels, such that
those patients with poorer control had greater
decreases in stability. Furthermore, this
study found that following the period of
decreased stability, there was a delay in the
return of stability levels to baseline levels,
again associated with glycemic levels. These
findings document specific compromises in
the implant integration process related to
glycemic levels and suggest an opportunity
for improvements in healing during the
implant integration period for patients lack-
ing good glycemic control.
Biologic alterations in implant stability
when assessed over time are a direct result of
bone turnover, the resorptive and formative
events, in proximity to the implant surface.
Although the rates of metabolic activity may
not vary over time, it is a continual process
from placement throughout the functional
life of the implant. Modifications to implant
surfaces provide the potential to alter these
biologic processes and enhance implant inte-
gration.
Implant surface modifications such as
altered surface topography, roughness, ionic
interactions, protein adsorption and cellular
activity have demonstrated the potential to
reduce healing time (Cochran et al. 2002; El-
lingsen et al. 2004; Schliephake et al. 2005;
Ferguson et al. 2006). It is thought that these
modifications influence conformational
changes in the structures and interactive nat-
ures of adsorbed proteins and cells. In vivo
studies in animals have supported the use of
alterations in surface chemistry to modify
osseointegration events. The chemically
modified Sand blasted, Large grit, Acid etched
(SLActive; Straumann®) surface demonstrated
significantly increased bone-to-implant con-
tact (49.3% more bone contact) than the con-
ventional SLA surface in 2 weeks (Buser
et al. 2004). The chemically modified SLA
2 | Clin. Oral Impl. Res. 0, 2011 / 1–7
(modSLA) implant has shown consistent
increase in level of osteocalcin, which is an
indicator of bone healing (Schwarz et al.
2007). Using the Dynamic Contact Angle
analysis, the modSLA surface has shown
increased wettability and unique hydrophilic
surface with 0° water contact angle compared
with 139.9° with conventional SLA (Rupp
et al. 2006). A 162% increase in fibronectin
absorption on the modSLA implant has been
demonstrated in comparison to the SLA
implant (Scheideler et al. 2005).
The most dynamic period for implant sta-
bility occurs 2–6 weeks following implant
placement (Barewal et al. 2003). It is during
this period that the primary stability of the
implant initially decreases, and is followed
by increasing the biologic stability. This pat-
tern of stability change is consistent with the
initiation of osseointegration (Berglundh
et al. 2003). A recent comparative evaluation
(Oates et al. 2007) of implant stabilization
with the chemically modified SLA surface
documented an earlier transition from the
resorptive phase to the formative phase con-
sistent with increases in implant stability at
earlier time points. This may be considered
as an advantage for patients with poor heal-
ing potential such as diabetics, where chemi-
cally modified SLA surface can potentially
promote faster healing around the implant.
Hence, we hypothesized that the chemically
modified SLA (modSLA) surface would
enhance implant stabilization during integra-
tion in comparison to the SLA surface in
patients with poorly controlled diabetes.
Materials and methods
This randomized, controlled trial was
designed to provide a comparative evaluation
of alterations in implant stabilization using a
chemically modified implant (modSLA) sur-
face. Participants were recruited between
June 2009 and January 2010 from among indi-
viduals seeking dental treatment within the
University of Texas Health Science Center at
San Antonio (UTHSCSA) Dental School. All
participants were provided informed consent
as approved by Institutional Review Board at
UTHSCSA.
The study population included 24 adult
patients who were missing at least two pos-
terior mandibular teeth. Implant sites were
required to have at least 4 months of healing
following tooth extraction, no previous ridge
augmentation with bone grafting, and a clini-
cal indication for implant-supported tooth
replacement. The study enrolled individuals
over 18 years of age with a diagnosis of type
2 diabetes mellitus of over 1 year duration
and baseline glycated hemoglobin A1c
(HbA1c) levels between 7.5% and 12.0%
inclusively (Quest Diagnostics Laboratory,
San Antonio, TX, USA). Physician consulta-
tions were used to confirm medical history,
diabetes status, and medications as appropri-
ate. Individuals having a history of treatment
for microvascular or macrovascular complica-
tions of diabetes, or with conditions requiring
chronic and routine use of antibiotics, were
excluded. Additional clinical findings used
for exclusion included prolonged use of ste-
roids, leukocyte dysfunction/deficiencies,
hypertension having systolic pressure at
>185 mmHg, and diastolic pressure at
>105 mmHg with or without medications,
bleeding disorders, metabolic bone disorders,
alcoholism or drug abuse, or smoking more
than 10 cigarettes per day. Local exclusion
factors included untreated oral infections or
inflammatory lesions such as untreated peri-
odontitis or erosive lichen planus, bone sur-
gery in the implant site less than 6 months
prior to implant placement, unhealed extrac-
tion sites, or presence of bone defects requir-
ing augmentation. HbA1c levels were
determined at enrollment, within 2 weeks
prior to implant placement (baseline), and at
2 and 4 months following implant placement
(Quest Diagnostics Laboratory).
For each patient, two posterior mandibular
implant sites were randomized per patient to
receive one each of either a Straumann®
Standard Plus (Institut Straumann AG, Basel,
Switzerland) SLA implant or a chemically
modified surface (modSLA) implant. Thus, 48
study implants were placed. The implant
position was determined with a permuted
block randomization plan developed using an
online pseudo-random number generator
(http://www.randomization.com). Allocation
sequence was established and maintained in
sealed envelopes concealed from study exam-
iners and therapists.
Both implants placed were of the same
dimension for each patient. All implants
used were of the same design with a 4.1 mm
diameter, 8 mm or 10 mm length, and a
1.8 mm transgingival collar. Implants were
placed as per manufacturer’s protocols, with
osteotomies completed prior to implant site
randomization, and placement requiring
unmasking of the surgeon. Implants were
covered using transgingival healing caps prior
to suturing. Patients were prescribed antibiot-
ics for 1 week post-surgically, analgesics
given as required, and chlorhexidine-
digluconate 0.12% oral rinse for 7–14 days.
© 2011 John Wiley & Sons A/S

Subjective clinical assessments were made
prior to randomization regarding bone type
according to a four-tiered scale, based on tac-
tile assessment of mineral densities during
osteotomy: high density (type I), moderate
density (type II), low density (type III), and
very low density (type IV) (Lekholm and Zarb
1985). Implants were not restored during the
4-month evaluation period, and temporary
prostheses were adjusted as needed to mini-
mize inadvertent loading of the implants.
Implant stability was assessed by a single
masked examiner using resonance frequency
analysis (RFA) (Osstell Mentor®; Integration
Diagnostics Ltd., Oslo, Norway). Implant sta-
bility (Implant Stability Quotient, ISQ) was
determined in duplicate with a third reading
taken if there was greater than a 2 ISQ unit
difference between readings. Independent
readings were taken from the buccal and
proximal directions for each implant. RFA
was performed at the time of surgical place-
ment (baseline) and 2, 3, 4, 6, 8, 10, 12, and
16 weeks following implant placement. In
addition, each implant was evaluated at all
visits for clinic complications, including
mobility, infection, pain, or suppuration.
Statistical analysis
Resonance frequency analysis measurements,
as the primary outcome, were made in the
buccal and proximal directions and analyzed
separately as recommended by Park et al.
(2010). ISQ data were analyzed using mixed
model analysis of variance (AVOVA) (Winer
1971; Brown & Prescott 2006). The statistical
model included implant type, time following
implant placement, the interaction of
implant type, and time following implant
placement as fixed effects. Patient was con-
sidered a random effect; all observations of
ISQ were made within patient. The repeated
observations over the time following implant
placement were assumed to follow a hetero-
geneous first-order autoregressive process; in
this model, the observations closer together
in time are more correlated. Statistical analy-
ses were performed using SAS 9.1.3 (SAS
Institute, Cary, NC, USA).
Selected variables, shown previously to be
useful in the study of implant healing (Oates
et al. 2009), were used to summarize the
effects of the Implant type. These summary
variables included the baseline ISQ, the mini-
mum ISQ, the time following implant place-
ment at which the minimum ISQ was
observed, the ISQ at 16 weeks, and the time
to healing (the first time after 8 weeks at
which the ISQ was equal to or greater than
baseline ISQ).
© 2011 John Wiley & Sons A/S
In secondary analyses, we considered the
effects of HbA1c group (the median baseline
HbA1c level of 9.6% was used to classify
subjects into two HbA1c groups: HbA1c
 9.5% and HbA1c  9.6%). Again, a mixed
model analysis of variance was applied. In
addition to the effects described above, we
included the effects of HbA1c group, the two-
factor interactions of HbA1c group and
implant type and HbA1c group and time fol-
lowing implant placement, and the three-fac-
tor interaction. Patients were considered
nested within HbA1c group. The selected
summary measures were analyzed to further
assess the effects of HbA1c. The differences
in baseline ISQ values in the high HbA1c
group prevented meaningful assessments of
changes in stability relative to baseline val-
ues, as were evaluated by Oates et al. (2009).
Before the study was approved by the IRB,
it was estimated that 20 patients each receiv-
ing one SLA implant, and one modified SLA
implant was required to identify a clinically
important mean difference in implant stabil-
ity of eight ISQ units using analysis of vari-
ance with significance level 0.05 level and
power 0.80 (computed using PASS 6.0 soft-
ware [NCSS, Kaysville, UT, USA]). The esti-
mate of within-subject variance was obtained
from Oates et al. (2009).
Results
Patient characteristics
Characteristics of the 24 type 2 diabetic
patients in this study are given in Table 1.
Fifteen (62.5%) of the patients were women
and the majority (66.7%) of the patients were
Hispanic. The average age was 57.3 years,
and the average BMI was 36.7 kg/m2.
Throughout this study, patients had HbA1c
levels between 7% and 12.5% (Table 1). The
average HbA1c did not differ significantly
among the measurements made at baseline,
Table 1. Patient characteristics
Variable Number (%)
Female sex 15 (62.5)
Ethnicity
Hispanic white 16 (66.7)
Non-Hispanic white 6 (25.0)
African American 2 (8.3)
Insulin 15 (62.5)
Mean ± SD (Min–Max)
Age (years) 57.3 ± 9.5 (38–76)
BMI (kg/m2) 36.7 ± 7.0 (24.4–54.6)
HbA1c (%)
Baseline 9.5 ± 1.0 (7.5–11.4)
Week 8 9.4 ± 1.6 (7–12.5)
Week 16 9.1 ± 1.6 (7–12.4)
Khandelwal et al
Diabetes and implant stability
8 weeks, and 16 weeks. Baseline HbA1c lev-
els for the 24 patients ranged from 7.5% to
11.4%. Of these patients, 11 were found to
have HbA1c levels between 7.5% and 9.1%,
with the remaining 13 patients having
HbA1c levels between 9.6% and 11.4%.
Table 2 shows the classifications of patients
into the two HbA1c groups at 8 and
16 weeks compared with the classification at
baseline. Ten of the patients were classified
in the lower HbA1c level at baseline, com-
pared with 13 after 8 weeks and 14 after
16 weeks. One patient with HbA1c  9.5%
at baseline had HbA1c  9.6% at 8 weeks.
Three patients with HbA1c  9.6% at base-
line had HbA1c  9.5% at 8 weeks, and four
patients with HbA1c  9.6% at baseline had
HbA1c  9.5% at 16 weeks.
The majority of the implants were placed
in types II and III bone. In 15 of the 24
patients, the two implant designs were placed
in the same bone type, and in all cases, the
bone type categories were within one unit of
change between implants.
Clinical observations
Clinically, 47 of 48 implants were determined
to be successfully osseointegrated and contin-
ued to restoration. One SLA implant failed
between week 4 and 6 following implant
placement, and was associated with the
patient’s report of an episode of acute pain at
the site during mastication on a hard food
item. One SLA implant showed rotational
movement and tenderness at weeks 2 and 3
following placement and was then excluded
from additional RFA during the remainder of
the 16-week study. This implant was fol-
lowed with RFA at 20, 24, and 28 weeks, and
successfully restored 9 months after implant
placement. Three implants showed gingival
inflammation, post-operatively through week
2. Other implant healing was uneventful. In
all patients, there were no adverse clinical
complications or infections associated with
soft tissue healing around the transgingival
implants. Few adverse events were encoun-
tered during the course of the study. The
most common adverse events were rotational
movement of the implant (three implants),
tenderness or pain at the implants site (two
implants), and pain on rotation of transgingi-
val healing cap (three implants) during the 4-
month assessment period. The frequency of
implants with complications was 9 of 24
(38%) for SLA implants, and 8 of 24 (33%) for
modSLA implants; the proportions of
implants with complications were not signifi-
cantly different. Two patients reported histo-
ries of cancer remote from the head and neck
3 | Clin. Oral Impl. Res. 0, 2011 / 1–7
Khandelwal et al
Diabetes and implant stability

Table 2. Number of patients with HbA1c  9.5% and number of patients with HbA1c  9.6%, by (a)
time of observation 85
Week 8* Week 16*

Implant stability quotient

80
Baseline n HbA1c  9.5% HbA1c  9.6% HbA1c  9.5% HbA1c  9.6%
HbA1c  9.5% 11 10 1 10 0 75
HbA1c  9.6% 13 3 9 4 9
Total 24 13 10 14 9 70

*
One observation missing. 65

60
0 2 4 6 8 10 12 14 16
(a) between the patterns of implant integration Time following implant placement (weeks)
85
for the two implant types, that is, there were (b)
85
Implant stability quotient

80 neither significant main effects of implant

type (P > 0.6565) nor were there any signifi- 80

Implant stability quotient

75 cant interactions of implant type with time
75
following implant placement (P > 0.3140).
70
There were significant changes with time fol- 70
65 lowing implant placement in both the buccal HbA1c ≤ 9.5% SLA
65
(P  0.0001) and proximal directions HbA1c ≤ 9.5% ModSLA
HbA1c ≥ 9.6% SLA
60 (P  0.0001). ISQ levels declined after 60
0 2 4 6 8 10 12 14 16 HbA1c ≥ 9.6% ModSLA
Time following implant placement (weeks) implant placement, and by week 8, the aver- 55
age ISQ levels were approximately equal to or 0 2 4 6 8 10 12 14 16
(b) Time following implant placement (weeks)
85 higher than the baseline measurements. Fol-
lowing the week 8 measurements, the RFA Fig. 2. Mean implant stability quotient by time follow-
Implant stability quotient

80 ing implant placement, HbA1c group, and implant type.

75
70
65
60
0 2 4 6
Time following implant placement (weeks)
Fig. 1. Mean implant stability quotient by implant type
and time following implant placement. Panel (a) repre-
sents measurements made in the buccal direction, and
Panel (b) represents measurements made in the proxi-
mal direction. Error bars represent standard errors.
area followed by radiotherapy and chemother-
apy more than 5 years before implant place-
ment. There were no adverse events or
healing complications for either of these
patients.
Implant stability
Figure 1 shows the mean ISQ for each implant
type by time, following implant placement.
No significant differences were identified
showed increases in ISQ levels through weeks
10–12 and then changed minimally from week
12 to 16. The ISQ levels showed similar pat-
terns in both buccal and proximal directions.
SLA
ModSLA The means of the selected summary mea-
sures by implant type and direction are
shown in Table 3. There were no significant
8 10 12 14 16 differences in any of the selected summary
measures between implant types.
The mean ISQ by HbA1c group, implant
type, and time following implant placement
are shown in Fig. 2. Overall, no significant
differences were identified between the pat-
terns of implant integration for the two
implant types, that is, there were neither sig-
nificant main effects of implant type
(P > 0.6434) nor were there any significant
interactions of implant type with HbA1c
group (P > 0.2423) or of implant type with
time following implant placement
(P > 0.2869). There were main effects of
HbA1c group in both the buccal (P = 0.0181)
and proximal directions (P = 0.0075); in both
directions, the HbA1c  9.5% group had
Panel (a) represents measurements made in the buccal
direction, and Panel (b) represents measurements made
in the proximal direction.
higher average ISQ levels. Also, there was an
interaction of HbA1c group and time follow-
ing implant placement in measurements
made in the buccal direction (P = 0.0011).
There were no significant three-factor inter-
actions (P > 0.3654).
To further investigate the foregoing differ-
ences associated with HbA1c level, we show
the means of the selected summary measures
by HbA1c group and direction in Table 4. In
both directions, the baseline ISQ level was
slightly higher for the HbA1c  9.6% than for
the HbA1c  9.5%. Similarly, the minimum
ISQ was higher for the HbA1c  9.6% than
for the HbA1c  9.5%. We believe that the
differences in minimum ISQ in the two
HbA1c groups is explained by the differences
in ISQ levels at baseline. Importantly, the ISQ
levels were similar in the two HbA1c groups
by 16 weeks following implant placement.

Table 3. Effects of implant type on implant stabilization, by direction

Time to minimum Time to healing
Baseline ISQ Minimum ISQ (weeks) ISQ at 16 weeks (weeks)
Direction Implant type Mean ± SE Mean ± SE Mean ± SE Mean ± SE Mean ± SE
Buccal SLA 70.1 ± 2.2 64.8 ± 2.7 3.5 ± 0.3 78.8 ± 0.8 6.7 ± 0.9
Mod SLA 74.4 ± 1.4 66.2 ± 2.0 4.2 ± 0.4 79.0 ± 0.9 8.4 ± 0.9
Difference *
(95% CI) 4.2 ± 2.1 ( 0.2, 8.7) 1.4 ± 2.9 ( 4.5, 7.3) 0.6 ± 0.3 ( 0.1, 1.3) 0.6 ± 1.0 ( 1.4, 2.6) 1.7 ± 1.0 ( 0.4, 3.8)
Proximal SLA 72.6 ± 2.1 67.1 ± 2.8 3.9 ± 0.3 79.3 ± 1.1 7.8 ± 1.0
Mod SLA 75.4 ± 1.4 64.9 ± 2.7 4.1 ± 0.2 79.1 ± 0.9 9.0 ± 1.0
Difference *
(95% CI) 2.7 ± 2.0 ( 1.4, 6.8) 2.3 ± 3.0 ( 8.4, 3.9) 0.2 ± 0.3 ( 0.5, 0.9) 0.3 ± 1.1 ( 2.0, 2.7) 1.3 ± 1.2 ( 1.2, 3.7)
*
Difference of SLA and Modified SLA.

4 | Clin. Oral Impl. Res. 0, 2011 / 1–7 © 2011 John Wiley & Sons A/S

Table 4. Effects of HbA1c on implant stabilization, by direction
Baseline ISQ
Direction HbA1c group Mean ± SE
Buccal HbA1c  9.5% 70.1 ± 2.2
HbA1c  9.6% 74.1 ± 2.0
*
Difference (95% CI) 3.9 ± 2.9 ( 2.1, 10.0)
Proximal HbA1c  9.5% 71.7 ± 2.1
HbA1c  9.6% 76.0 ± 1.9
*
Difference 4.3 ± 2.8 ( 1.6, 10.2)
*
Difference between HbA1c groups.
There was no difference in time to minimum
ISQ or in time to healing between the two
HbA1c groups.
Discussion
The purpose of our study was to evaluate the
potential for a chemically modified SLA sur-
face (modSLA) compared with a conventional
SLA surface, to enhance implant healing and
integration in diabetic patients with demon-
strated compromises and delays in implant
stabilization during the metabolically active
healing period following implant placement.
The results of this study did not identify a sig-
nificant difference in the patterns of implant
stabilization between the two implant sur-
faces for patients with type 2 diabetes having
poor glycemic control. Importantly, this study
did document high levels of clinical success
for both implant types in patients demonstrat-
ing systemic conditions traditionally consid-
ered as contraindications to implant therapy
(World Workshop in Periodontics 1996;
Blanchaert 1998; Wilson & Higgenbottom
1998; Beikler & Flemmig 2003).
Patients with diabetes have increased
chances of developing periodontitis and may
be more susceptible to tooth loss than non-
diabetics. Implant therapy offers the potential
to benefit patients with diabetes by improv-
ing masticatory function and dietary intake
critical to their disease management. Diabe-
tes patients have alterations in immunologic
responses thought to increase chances of
developing micro and macro vascular compli-
cations, compromising wound healing, and
increasing risk of infection (Pearl & Kanat
1988; Gallacher et al. 1995; McMahon &
Bristrian 1995; Delamaire et al. 1997; Shurtz-
Swirski et al. 2001). These concerns for dia-
betes patients have provided the rationale for
limiting the use of dental implants with gly-
cemic control as a relative contraindication.
However, recent reports have documented
successful implant placement in patients
with elevations in glycemic levels (Dowell
© 2011 John Wiley & Sons A/S
Time to minimum
Minimum ISQ (weeks)
Mean ± SE Mean ± SE
61.6 ± 2.6 4.0 ± 0.3
68.8 ± 2.4 3.7 ± 0.3
7.2 ± 3.6 (0.2, 14.7) 0.3 ± 0.4 ( 1.2, 0.6)
61.4 ± 3.2 3.9 ± 0.3
69.9 ± 3.0 4.1 ± 0.3
8.5 ± 4.4 (0.7, 17.6) 0.2 ± 0.4 ( 0.6, 1.0)
et al. 2007; Tawil et al. 2008; Oates et al.
2009; Turkyilmaz 2010). These findings are
reinforced in the current study by the clinical
success of 47 of 48 study implants in diabetes
patients with HbA1c levels ranging from
7.0% to 12.5% over the course of the study.
It is noteworthy that the study protocol for
this investigation did provide all patients
with antibiotic coverage for 7 days following
surgical placement along with 14 days of
antimicrobial rinse. While the study contin-
ues with longer-term evaluation, this report
is limited in that it examines the integration
period during the first 4 months following
implant placement.
Surface characteristics of implants are con-
sidered to be a critical factor influencing the
integration of dental implants. A comparative
study between SLA and modSLA implants in
dogs showed increased osteocalcin and
increased bone-to-implant contact in 14 days
for the modSLA implant surface (Schwarz
et al. 2007). Similarly, modSLA implants
have shown the potential to enhance the rate
of implant integration in comparison to SLA
implants. Woven bone formation was evident
as early as 2 weeks in miniature pigs, with
reduced time to osseointegration and 60%
increased bone-to-implant contact (Buser
et al. 2004). A pilot study in medically
healthy patients suggested that the modSLA
has potential for enhanced healing, reduced
risks, and more predictability in early/imme-
diate loading procedures (Oates et al. 2007).
In this study, the modSLA implants showed
signs of transition from one of decreasing sta-
bility to increasing stability after 2 weeks, in
comparison to 4 weeks for implants with the
standard SLA surface.
In the current study, for both implant
types, the minimum in implant stability
occurred at 3–4 weeks following placement.
The minimum stability point is thought to
mark the transition from primarily bone
resorption to bone formation initiating the
osseointegration phase. This may be a critical
phase during implant healing. In our study,
the sole implant failure was encountered in
Khandelwal et al
Diabetes and implant stability
Time to healing
ISQ at 16 weeks (weeks)
Mean ± SE Mean ± SE
78.8 ± 1.0 6.4 ± 1.1
78.8 ± 1.0 8.5 ± 1.0
0.0 ± 1.4 ( 3.0, 3.0) 2.2 ± 1.5 ( 0.9, 5.3)
78.4 ± 1.1 7.4 ± 1.2
79.8 ± 1.1 9.3 ± 1.1
1.4 ± 1.5 ( 1.8, 4.6) 1.9 ± 1.6 ( 1.4, 5.3)
this “critical” period between 4 and 6 weeks
following placement. However, the present
investigation failed to identify a significant
difference in stability patterns between the
two implant surfaces during the 4-month
integration period following implant place-
ment for diabetic patients with the potential
for compromised healing.
Bone undergoes constant remodeling. In
diabetic patients, altered insulin levels and
increased AGE’s and pro-inflammatory cyto-
kines can affect this remodeling, resulting in
bone loss. Numerous studies have demon-
strated altered bone physiology in hyperglyce-
mic murine models (Funk et al. 2000; Amir
et al. 2002; Lu et al. 2003). However, in a
recent non-human primate study, diabetes
had no effect on implant osseointegration
and trabecular bone volume at 4 weeks
(Casap et al. 2008). This discrepancy may be
explained by the hyper-insulinemic and nor-
mo-insulinemic status of the primates. Insu-
lin has been shown to have a metabolic role
in bone formation (Follak et al. 2004a,b). In
some animal studies, low levels of insulin
were associated with decreased osteoid sur-
face and decreased rate of mineral apposition
(Lu et al. 2003). Although the current study
did not assess serum insulin levels, patients
receiving insulin therapy did not show any
significant alterations in stability patterns.
In conclusion, our study identified similar
levels of implant stabilization for both stan-
dard SLA and chemically modified SLA
implants for type 2 diabetes patients with rel-
atively poor glycemic control. Importantly,
this study also demonstrates predictable clin-
ically successful implant integration in
patients with poorly controlled diabetes, and
offers additional support for the application
of dental implant therapy for patients having
a broader range of glycemic control than has
traditionally been proposed.
Acknowledgement: This study was
supported by Institut Straumann AG (Basel,
Switzerland).
5 | Clin. Oral Impl. Res. 0, 2011 / 1–7
Khandelwal et al
Diabetes and implant stability
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