Download Comparison of clinical and radiographic status around dental

Mohammad D. Al Amri
Tariq S. Abduljabbar
Abdulaziz A. Al-Kheraif
Georgios E. Romanos
Fawad Javed
Authors’ affiliations:
Mohammad D. Al Amri, Tariq S. Abduljabbar,
Department of Prosthetic Dental Sciences, College
of Dentistry, King Saud University, Riyadh, Saudi
Arabia
Abdulaziz A. Al-Kheraif, Dental Health
Department, College of Applied Medical Sciences,
King Saud University, Riyadh, Saudi Arabia
Georgios E. Romanos, Department of
Periodontology, School of Dental Medicine, Stony
Brook University, Stony Brook, NY, USA and;
Department of Oral Surgery and Implant Dentistry,
Johann Wolfgang University, Frankfurt, Germany
Fawad Javed, Department of General Dentistry,
Eastman Institute for Oral Health, University of
Rochester, Rochester, NY, USA
Corresponding author:
Dr Mohammad D. Al Amri
Department of Prosthetic Dental Sciences
College of Dentistry
King Saud University
P.O. Box 60169, Riyadh 11545, Saudi Arabia
Tel.: +966 11 467 7325
Fax: +966 11 467 8548
e-mail: [email protected]
Comparison of clinical and radiographic
status around dental implants placed in
patients with and without prediabetes:
1-year follow-up outcomes
Key words: clinical parameters, dental implant, marginal bone loss, prediabetes, success rate
Abstract
Objective: We hypothesized that peri-implant soft tissue inflammation is worse and peri-implant
marginal bone loss (MBL) is higher around dental implants placed in patients with prediabetes
compared to healthy subjects. The aim of the present 12-month follow-up study was to compare
the clinical and radiographic status around dental implants placed in patients with and without
prediabetes.
Material and methods: Twelve patients with medically diagnosed prediabetes (Group-1) and 12
controls (Group-2) were included. All patients were indicated for single tooth maxillary or
mandibular premolar replacement with the adjacent teeth intact. Success of the restored implants
was assessed by comparing clinical (peri-implant bleeding on probing [BOP], and probing pocket
depth [PPD]) and radiographic (peri-implant MBL) parameters at baseline and at 12-months followup. Statistical analysis was performed using one-way analysis of variance, and P-values <0.05 were
considered statistically significant.
Results: At 12 months of follow-up, there was no clinical evidence for the presence of plaque,
BOP and peri-implant pockets with PPD ≥ 4 mm in both groups. At 12-month follow-up, the mean
MBL among implants placed in groups 1 and 2 were 0.2 0.1 mm and 0.1 0.01 mm,
respectively. Overall, the periodontal status (PI, BOP and PPD ≥ 4 mm) at 12-month follow-up was
comparable among patients in both groups.
Conclusion: Within the limitations of this study, it is concluded that dental implants inserted in
prediabetic and healthy patients have similar success rates and remain clinically and
radiographically stable after 1-year follow-up.
Date:
Accepted 30 December 2015
To cite this article:
Al Amri MD, Abduljabbar TS, Al-Kheraif AA, Romanos GE,
Javed F. Comparison of clinical and radiographic status
around dental implants placed in patients with and without
prediabetes: 1-year follow-up outcomes.
Clin. Oral Impl. Res. 00, 2016, 1–5
doi: 10.1111/clr.12788
It is known that chronic hyperglycemia negatively influences osseointegration of dental
implants, and implant failure is a common
manifestation in such patients (Alsaadi et al.
2008; Daubert et al. 2015). Chronic hyperglycemia has also been associated with the
delayed cell proliferation and osteoblast differentiation (Colombo et al. 2011). In addition, chronic hyperglycemia has been
associated with the dysregulation of bone factors such as transforming growth factor-beta,
fibroblast growth factor, osteopontin, osteocalcin and osteoprotegerin in the peri-implant
crevicular fluid (Ghiraldini et al. 2015).
Although optimal glycemic control in
patients with diabetes has been reported to
enhance osseointegration (Javed & Romanos
2009), results from a recent clinical trial
showed that elevated hemoglobin A1c
(HbA1c) levels in patients with type 2
© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
diabetes mellitus (T2DM) were not associated with altered implant success after 1 year
of loading (Oates et al. 2014). However, alterations in early bone healing and implant stability
were
associated
with
chronic
hyperglycemia (Oates et al. 2014). Similar
results were reported in another clinical
study (Ghiraldini et al. 2015).
Prediabetes, a state of abnormal glucose
homeostasis, is characterized by the presence
of impaired fasting glucose, impaired glucose
tolerance, or both (American Diabetes Association 2015a). Prediabetes designations have
been defined by fasting glucose levels of 100–
125 milligrams per deciliter (mg/dl), hemoglobin A1c (HbA1c) levels between 5.7% and
6.4% and postglucose challenge levels of
140–199 mg/dl (Olson et al. 2010; American
Diabetes Association 2015b). Studies (Javed
et al. 2012a,b, 2013, 2014a,b, 2015; Alshehri
1
Al Amri et al Dental implants and prediabetes
& Javed 2015) have shown that scores of periodontal inflammatory parameters (such as
bleeding on probing [BOP] and probing pocket
depth [PPD]) are higher among patients with
prediabetes compared with systemically
healthy individuals (controls). Although marginal bone loss (MBL) as measured on radiograph is also higher in prediabetic patients
compared with controls (Javed et al. 2014a,b);
controversial results have also been reported
(Kowall et al. 2015).
As patients with prediabetes exhibit a
poorer periodontal (clinical and radiographic)
status compared with controls (Javed et al.
2014a,b), it is hypothesized that peri-implant
soft tissue inflammation is worse and MBL is
higher around dental implants placed in
patients with prediabetes compared to
healthy subjects. The aim of the present 1year follow-up case-control study was to
assess the clinical and radiographic status
around dental implants placed in patients
with prediabetes.
Material and methods
Ethical approvals
The study was approved by the Research
Ethics Review committee of the College of
Applied Medical Sciences, King Saud University, Riyadh, Saudi Arabia. Volunteering individuals were requested to read and sign a
consent form.
Inclusion and exclusion criteria
The inclusion criteria were (a) patients with
medically diagnosed prediabetes and (b) selfreported systemically healthy controls. The
exclusion criteria were as follows: (a) patients
with systemic disorders other than prediabetes (such as type 1 diabetes mellitus,
T2DM, renal disorders, acquired immune
deficiency syndrome and cardiovascular disorders); (b) individuals using tobacco products
(smokers and tobacco chewers); (c) pregnant
and/or lactating females; (d) patients with a
history of antibiotic and/or steroid intake
within the past 3 months of implant placement; and (e) use of bone augmentation protocols.
Participants
In total, 24 male patients (12 patients with
prediabetes [Group-1] and 12 controls [Group2]) were included. Patients in Group-1 were
requested to present their medical records to
determine the date of the most recent assessment of hemoglobin A1C, fasting plasma glucose or oral glucose tolerance test that
2 |
Clin. Oral Impl. Res. 0, 2016 / 1–5
confirmed the diagnosis of prediabetes in the
study population. These individuals were
recruited from the Department of Prosthetic
Dental Sciences, College of Dentistry, King
Saud University, Riyadh, Saudi Arabia. In
both groups, patients had implants placed for
the replacement of a single premolar tooth in
the maxilla or mandible with adjacent teeth
intact. All patients underwent full-mouth
scaling using an ultrasonic scaler (VV
DENTA, Guangxi, China) prior to implant
placement.
Measurement of hemoglobin A1c levels
In both groups, HbA1c levels were measured
at the time of surgery, after 6 months and
1 year of follow-up. Venous blood samples
were drawn in the morning, and HbA1c
levels were determined using the high-performance liquid chromatography method (BioRad Laboratories, Inc., D-10TM; Hemoglobin
Systems, Hercules, CA, USA) (Ozcelik et al.
2010). Individuals with HbA1c levels ranging
between 5.7–6.4% and 4–5.5% were categorized as prediabetic individuals and controls,
respectively (American Diabetes Association
2015a,b).
Surgical protocol
A 7-day course of wide-spectrum antibiotic
(Amoxicillin 500 mg 8 h) was started 3 days
before the participants were scheduled for
implant surgery. Clindamycin (150 mg 6 h
for 7 days) was prescribed as an alternate
antibiotic for individuals with a self-reported
history of penicillin allergy. Following local
anesthesia, a crestal incision was made
using a #15 blade and full-thickness
mucoperiosteal flaps were raised to expose
the bone. A total of 24 bone level implants
(12 implants in Group-1 and 12 in Group-2)
were placed in the center of the healed alveolar ridge (day 0) using an insertion torque
of 30–35 Ncm. The implants used had a
diameter of 3.5 mm and ranging in length
from 10 to 16 mm (Straumannâ Dental
Implant System, Institut Straumann, AG
Peter Merian-Weg 12 CH-4002 Basel,
Switzerland). Healing abutments were connected to the implants using hand torque
(day 0). The flaps were sutured around the
healing abutment using resorbable sutures
(4/0 Vicryl), and digital intraoral postoperative radiographs were taken. After a mean
duration of 3.5 months, final impressions
were made for the fabrication of a definitive
porcelain-fused-to-metal (PFM) implant-supported prosthesis (day 112). All implants
were loaded with screw-retained PFM
crowns.
Postoperative management
Participants were advised to complete the 7day antibiotic course, which had started
3 days before surgery. Analgesics (Ibuprofen
600 mg 6 h for 5 days) were also prescribed
for pain control. Acetaminophen (325 mg 6 h
for 5 days) was prescribed as an alternate
analgesic for individuals who reported to be
allergic to ibuprofen. Participants in both
groups were instructed to rinse with a 0.12%
chlorhexidine gluconate solution (Corsodyl,
Boots, Nottingham, UK) twice daily for
2 weeks. Oral hygiene instructions were
given to all patients, and they were also
enrolled in a 6-month follow-up dental prophylaxis program (ultrasonic cleaning) for
1 year. Patients were advised to maintain
their serum glycemic levels and were also
suggested to contact their primary care physicians in this regard.
Clinical and radiographic parameters
Peri-implant and full-mouth plaque index
(PI), BOP and PPD ≥ 4 mm were assessed
among individuals in both groups. These
parameters were assessed at six sites per
tooth/implant (mesiobuccal, midbuccal, distobuccal, mesiolingual, midlingual and distolingual). For the assessment of PPD, a
metal periodontal probe with a tip diameter
of 0.42 mm (Zeffiro, Lascod spa, Sesto Fiorentino, Italy) was inserted into the peri-implant
sulcus and the most apically probable distance was recorded in millimeters (Abreu
et al. 2007; Zitzmann & Berglundh 2008). In
both groups, evidence of any radiolucency
and mesial and/or distal marginal bone loss
(MBL) around the implants was determined
at 6 and 12 months of follow-up. Digital
intraoral radiographs were taken and visualized on a computer screen. Radiographs were
analyzed at 209 magnification using a software (CorelDraw 11.0, Corel Corp and Coral
Ltd, Ottawa, Canada). MBL was defined as
the distance from the widest supracrestal part
of the implant to the crestal bone level
(Mumcu et al. 2011).
Criteria for implant success
The criteria for implant success were (a)
stable implants and superstructures, (b) no
symptoms of pain, (c) no signs of BOP and/or
purulent discharge, (d) MBL of ≤1 mm around
the implant in the first year, and (e) absence
of radiolucency around implants.
Statistical analysis
Statistical analysis was performed using a
software program (SPSS Version 18, Chicago,
IL, USA). BOP, PPD and MBL among patients
© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Al Amri et al Dental implants and prediabetes
at 6 months and 12 months of follow-up in
both groups were compared using the nonparametric Mann–Whitney U-test. P-values
less than 0.05 were considered statistically
significant.
Results
Marginal bone loss among individuals in
groups 1 and 2 after 6 and 12 months of
follow-up
There was no radiographic evidence of MBL
around implants placed in groups 1 and 2 at
6-month follow-up. At 12-month follow-up,
the mean MBL among implants placed in
groups 1 and 2 were 0.2 0.1 mm and
0.1 0.01 mm, respectively (P = 0.12).
General characteristics of the study population
The mean age of participants in groups 1 and
2
were
44.5 years
(41–49 years)
and
43.3 years (39–47 years), respectively. At
baseline, the mean HbA1c levels were significantly higher among patients in Group-1
compared to patients in Group-2 (P = 0.002).
There was no statistically significant difference in mean HbA1c levels among patients
in groups 1 and 2 at 6 and 12 months of follow-up (Table 1). In both groups, all implants
were clinically stable with no signs of mobility and/or inflammation. None of the participants were allergic to amoxicillin or
ibuprofen.
Full-mouth plaque index, bleeding on probing
and probing depth among individuals in
groups 1 and 2
At baseline, there was no statistically significant difference of plaque, BOP and
PPD ≥ 4 mm among patients in groups 1
and 2. In both groups, there was a statistically significant difference in PI, BOP and
PPD ≥ 4 mm at 6 months (P = 0.00) and
12 months (P = 0.00) of follow-up. There
was no significant difference in PI, BOP
and PPD ≥ 4 mm at 6- and 12-month follow-ups among patients in groups 1 and 2
(Table 2).
Peri-implant plaque index, bleeding on probing
and probing depth among individuals in
groups 1 and 2 after 6 and 12 months of
follow-up
In both groups, there was no clinical evidence
of
peri-implant
pockets
with
PPD ≥ 4 mm at 6 and 12 months of followup. At 6 and 12 months of follow-up, there
was no clinical evidence for the presence of
plaque, BOP and peri-implant pockets with
PPD ≥ 4 mm in both groups.
Discussion
To our knowledge from indexed literature,
this is the first study, which assessed the
clinical and radiographic parameters status
of implants placed in patients with and
without prediabetes. We reviewed the
patients’ records to determine the date of
the most recent assessment of HbA1C, fasting plasma glucose or oral glucose tolerance
test which was performed. This was used
mainly to confirm the prediabetic state of
the participants. However, for the present
study, we elected to measure HbA1c levels
to have the most updated glycemic levels in
the present study. In this study, it was
hypothesized that the peri-implant soft tissue inflammation is worse and MBL is
higher around dental implants placed in
patients with prediabetes compared to controls. This hypothesis was based on the fact
that chronic hyperglycemia is associated
with an increased formation and accumulation of advanced glycation endproducts in
periodontal tissues, which augment inflammation, and if hyperglycemia is left uncontrolled, it may lead to MBL around teeth
(Lalla et al. 2000; Chang et al. 2013, 2014).
Interestingly, the present results showed
that all implants remained clinically stable
up to 12 months of follow-up with no signs
of soft tissue inflammation. An explanation
in this regard could be derived from the fact
that all participants were given strict oral
hygiene maintenance instructions and were
also enrolled in a 6-month dental prophylaxis program. In the dental prophylaxis program, ultrasonic scalers were used to
eradicate any stagnated plaque from teeth
Table 1. Mean HbA1c levels among patients in groups 1 and 2 at baseline and after 6 and
12 months of follow-up
Hemoglobin A1c (%)
Study groups (n)
Baseline
(mean SD)
6 months follow-up
(mean SD)
12 months follow-up
(mean SD)
Group-1 (n = 12)
Group-2 (n = 12)
6.1 0.4*
4.4 0.2
5.8 0.2
4.4 0.1
5.5 0.2
4.2 0.1
*Compared to Group-2 at baseline (P = 0.002).
SD, standard deviation.
© 2016 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
and implant surfaces, and at every visit, it
was clinically ensured that the patients are
maintaining good oral hygiene status. It is
interesting to note that the overall periodontal status of individuals with and without
prediabetes was comparable at 6 and
12 months of follow-up (Table 2). In a 10year follow-up clinical study, Degidi et al.
(2012) found that the long-term bone levels
around dental implants can be maintained
when levels of oral hygiene are kept adequate. Likewise, clinical results by Lin et al.
(2011) demonstrated that a 100% success
rate of implants can be achieved provided
that oral hygiene maintenance and periimplant gingival health are ensured. Authors
of the present study support the studies by
Degidi et al. (2012) and Lin et al. (2011).
However, from the present results, it is evident that optimal oral hygiene maintenance
not only prevents MBL around implants in
systemically healthy individuals, but also in
hyperglycemic patients, such as those with
prediabetes. It is therefore imperative for
clinicians to educate patients about the
importance of regular oral hygiene maintenance and its beneficial influences on teeth
and implants.
Studies have shown that non-surgical periodontal therapy (NSPT) plays a role in reducing periodontal inflammation and serum
glycemic levels among patients with chronic
hyperglycemia (Stewart et al. 2001; Simpson
et al. 2010; Corbella et al. 2013; Javed et al.
2014a,b). However, it has also been reported
that NSPT reduces periodontal inflammation
but does not significantly affect metabolic
control in hyperglycemic patients (Serrano
et al. 2012; Alshehri & Javed 2015). In the
present study, a trend toward decrease in
HbA1c level was observed among patients
with prediabetes (Group-1); however, compared to baseline glycemic levels, HbA1c
levels measured at 12-months of follow-up
failed to show any statistically significant
difference. The present 1-year follow-up
results support the study by Oates et al.
(2014), which showed that elevated HbA1c
levels in patients with type 2 diabetes were
not associated with altered implant success
1 year after loading. Moreover, clinical evidence from several investigations has suggested that although glycemic control is an
important consideration that may require
modifications in the treatment protocols,
hyperglycemia may not be as a contraindication to implant therapy in diabetic patients
(Oates & Huynh-Ba 2012; Oates et al. 2013,
2014).
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Clin. Oral Impl. Res. 0, 2016 / 1–5
Al Amri et al Dental implants and prediabetes
Table 2. Median standard deviation full-mouth plaque index, bleeding on probing and probing depth among individuals in groups 1 and 2 after 6
and 12 months of follow-up
Group-1 (n = 12)
Group-2 (n = 12)
Parameters
Baseline
6-month follow-up
12-month follow-up
Baseline
6-month follow-up
12-month follow-up
Plaque index (%)
Bleeding on probing (%)
Probing depth ≥4 mm (%)
27.3 7.7*†
20.1 2.5*†‡
5.1 1.4*
6.5 2.6
5.7 0.4
1.9 0.6
5.6 0.8
2.5 1.4
0
23.2 2.5‡§
11.2 0.4‡§
2.7 0.5
6.7 0.7
3.6 0.3
0
4.8 0.2
1.7 0.1
0
*Compared to 6-month follow-up in Group-1 (P = 0.000).
†Compared to 12-month follow-up in Group-1 (P = 0.00).
‡Compared to 6-month follow-up in Group-2 (P = 0.00).
§Compared to 12-month follow-up in Group-2 (P = 0.00).
It is well-known that a history of periodontal disease is a significant risk factor for periimplant diseases (peri-implant mucositis and
peri-implantitis) (Serino & Str€
om 2009;
Renvert & Quirynen 2015). From the baseline
assessment of periodontal inflammatory
parameters (PI, BOP and PPD), it is noteworthy that all participants had a relatively good
oral hygiene status, with plaque accumulation
and periodontal pockets of ≥4 mm in less than
30% and 5% sites, respectively (Table 2). This
suggests that participants in both groups had
an acceptable oral hygiene status and were
most likely maintaining good oral hygiene.
However, it is speculated that a history of periodontal disease would have most likely influenced the success of dental implants placed in
both groups. Further long-term prospective
studies are needed in this regard.
There are a few limitations of the present
study. As the present results were based on
1-year follow-up results, it is hypothesized
that optimal long-term oral hygiene maintenance among patients with prediabetes
would positively influence the success of
implants in these patients. Moreover, it is
well-established that the outcomes of oral
surgical interventions and marginal bone
levels are compromised in smokers as compared to non-smokers (Javed et al. 2007,
2012a,b; Kotsakis et al. 2015). It is speculated
that regardless of daily oral hygiene maintenance, habitual tobacco smoking jeopardizes
the outcomes of implant treatment among
patients with and without prediabetes by
increasing MBL around implants. In the present study, strict eligibility criteria (such as
absence of other systemic diseases, no use of
antibiotics/steroids within the past 3 months
and absence of tobacco habits) were established for the inclusion of prediabetic
patients. It is therefore possible that such factors may have influenced the outcomes of
the present study. Furthermore, in the present study, implants were placed in both
arches. As the bone density varies between
the maxilla and mandible (Fuster-Torres
et al. 2011), it is hypothesized that in the
long term, jaw location may influence MBL
around implants. Further long-term clinical
trials are needed to test the aforementioned
hypothesis.
Conclusion
Within the limitations of this study, it is
concluded that dental implants inserted in
prediabetic and healthy patients have similar success rates and remain clinically and
radiographically stable after 1-year follow-up. Regular oral hygiene maintenance
plays a potentially vital role for implant
therapy in patients with and without
prediabetes.
Acknowledgements: The project was
financially supported by Vice Deanship of
Research Chairs, King Saud University,
Riyadh, Saudi Arabia.
Conflict of interest and financial
disclosure
The authors declare no conflict of interest.
There was no external source of funding for
this study.
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