Namita KhandelwalThomas W. OatesAdriana VargasPeggy P. AlexanderJohn D. SchoolfieldC. Alex McMahan

Conventional SLA and chemicallymodified SLA implants in patientswith poorly controlled type 2 Diabetesmellitus – a randomized controlledtrial

Authors’ affiliations:Namita Khandelwal, Graduate School ofBiomedical Sciences, University of Texas HealthScience Center at San Antonio, San Antonio, TX,USAThomas W. Oates, Peggy P. Alexander, John D.Schoolfield, Department of Periodontics, Universityof Texas Health Science Center at San Antonio,San Antonio, TX, USAAdriana Vargas, Department of ComprehensiveDentistry, University of Texas Health ScienceCenter at San Antonio, San Antonio, TX, USAC. Alex McMahan, Department of Pathology,University of Texas Health Science Center at SanAntonio, San Antonio, TX, USAPresent AddressDepartment of Periodontics, University of Medicineand Dentistry at New Jersey, Newark, NJ, USA

Corresponding author:Dr. Thomas W. OatesDepartment of PeriodonticsUniversity of Texas Health Science Center at SanAntonio7703 Floyd Curl DriveSan Antonio, TX 78229-3900, USATel.: (210) 567-3590Fax: (210) 567-6858e-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.

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

Date:Accepted 2 October 2011

To cite this article:Khandelwal N, Oates TW, Vargas A, Alexander PP,Schoolfield JD, Alex McMahan C. Conventional SLA andchemically modified SLA implants in patients with poorlycontrolled type 2 Diabetes mellitus – a randomized controlledtrial.Clin. Oral Impl. Res. 00, 2011, 1–7doi: 10.1111/j.1600-0501.2011.02369.x

© 2011 John Wiley & Sons A/S 1

(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

(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.

2 | Clin. Oral Impl. Res. 0, 2011 / 1–7 © 2011 John Wiley & Sons A/S

Khandelwal et al �Diabetes and implant stability

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).

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,

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

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)

© 2011 John Wiley & Sons A/S 3 | Clin. Oral Impl. Res. 0, 2011 / 1–7

Khandelwal et al �Diabetes and implant stability

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

between the patterns of implant integration

for the two implant types, that is, there were

neither significant main effects of implant

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

cant interactions of implant type with time

following implant placement (P > 0.3140).

There were significant changes with time fol-

lowing implant placement in both the buccal

(P � 0.0001) and proximal directions

(P � 0.0001). ISQ levels declined after

implant placement, and by week 8, the aver-

age ISQ levels were approximately equal to or

higher than the baseline measurements. Fol-

lowing the week 8 measurements, the RFA

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.

The means of the selected summary mea-

sures by implant type and direction are

shown in Table 3. There were no significant

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

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 2. Number of patients with HbA1c �9.5% and number of patients with HbA1c � 9.6%, bytime of observation

Baseline n

Week 8* Week 16*

HbA1c �9.5% HbA1c � 9.6% HbA1c �9.5% HbA1c � 9.6%

HbA1c �9.5% 11 10 1 10 0HbA1c �9.6% 13 3 9 4 9Total 24 13 10 14 9

*One observation missing.

Time following implant placement (weeks)

Impl

ant s

tabi

lity

quot

ient

600 2 4 6 8 10 12 14 16

0 2 4 6 8 10 12 14 16

65

70

75

80

85

Time following implant placement (weeks)

Impl

ant s

tabi

lity

quot

ient

60

65

70

75

80

85

SLAModSLA

(a)

(b)

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.

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

Direction Implant typeBaseline ISQ Minimum ISQ

Time to minimum(weeks) ISQ at 16 weeks

Time to healing(weeks)

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 ± 0.9Mod SLA 74.4 ± 1.4 66.2 ± 2.0 4.2 ± 0.4 79.0 ± 0.9 8.4 ± 0.9Difference * (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 ± 1.0Mod SLA 75.4 ± 1.4 64.9 ± 2.7 4.1 ± 0.2 79.1 ± 0.9 9.0 ± 1.0Difference * (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.

Time following implant placement (weeks)

Impl

ant s

tabi

lity

quot

ient

60

65

70

75

80

85

0 2 4 6 8 10 12 14 16

Time following implant placement (weeks)

Impl

ant s

tabi

lity

quot

ient

55

60

65

70

75

80

85

HbA1c ≤ 9.5% SLAHbA1c ≤ 9.5% ModSLAHbA1c ≥ 9.6% SLAHbA1c ≥ 9.6% ModSLA

0 2 4 6 8 10 12 14 16

(a)

(b)

Fig. 2. Mean implant stability quotient by time follow-

ing implant placement, HbA1c group, and implant type.

Panel (a) represents measurements made in the buccal

direction, and Panel (b) represents measurements made

in the proximal direction.

4 | Clin. Oral Impl. Res. 0, 2011 / 1–7 © 2011 John Wiley & Sons A/S

Khandelwal et al �Diabetes and implant stability

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

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

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).

Table 4. Effects of HbA1c on implant stabilization, by direction

Direction HbA1c groupBaseline ISQ Minimum ISQ

Time to minimum(weeks) ISQ at 16 weeks

Time to healing(weeks)

Mean ± SE Mean ± SE Mean ± SE Mean ± SE Mean ± SE

Buccal HbA1c �9.5% 70.1 ± 2.2 61.6 ± 2.6 4.0 ± 0.3 78.8 ± 1.0 6.4 ± 1.1HbA1c �9.6% 74.1 ± 2.0 68.8 ± 2.4 3.7 ± 0.3 78.8 ± 1.0 8.5 ± 1.0Difference

*

(95% CI) 3.9 ± 2.9 (�2.1, 10.0) 7.2 ± 3.6 (0.2, 14.7) �0.3 ± 0.4 (�1.2, 0.6) 0.0 ± 1.4 (�3.0, 3.0) 2.2 ± 1.5 (�0.9, 5.3)Proximal HbA1c �9.5% 71.7 ± 2.1 61.4 ± 3.2 3.9 ± 0.3 78.4 ± 1.1 7.4 ± 1.2

HbA1c �9.6% 76.0 ± 1.9 69.9 ± 3.0 4.1 ± 0.3 79.8 ± 1.1 9.3 ± 1.1Difference

*

4.3 ± 2.8 (�1.6, 10.2) 8.5 ± 4.4 (0.7, 17.6) 0.2 ± 0.4 (�0.6, 1.0) 1.4 ± 1.5 (�1.8, 4.6) 1.9 ± 1.6 (�1.4, 5.3)

*Difference between HbA1c groups.

© 2011 John Wiley & Sons A/S 5 | Clin. Oral Impl. Res. 0, 2011 / 1–7

Khandelwal et al �Diabetes and implant stability

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