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Oral Diseases (2005) 11, 293–298

 2005 Blackwell Munksgaard All rights reserved


http://www.blackwellmunksgaard.com

ORIGINAL ARTICLE

The effect of periodontal therapy on uncontrolled type 2


diabetes mellitus in older subjects
A Promsudthi1, S Pimapansri2, C Deerochanawong3, W Kanchanavasita4
1
Department of Oral Medicine, Faculty of Dentistry, Mahidol University; 2Department of Conservative Dentistry and Prosthodontics,
Faculty of dentistry, Srinakharinwirot University; 3Division of Endocrinology, Rajavithi Hospital; 4Department of Prosthodontics,
Faculty of Dentistry, Mahidol University, Bangkok, Thailand

OBJECTIVE: The purpose of this study was to examine Keywords: periodontal disease/therapy; diabetes mellitus; doxy-
the effect of periodontal therapy on glycemic control in cycline/therapeutic use; aged subjects; periodontal attachment loss
older type 2 diabetic patients.
METHODS: Fifty-two diabetic patients, age 55–80 years
(mean age = 61 years), with glycated hemoglobin
(HbA1c) 7.5–11.0% (mean ± s.d. = 8.98 ± 0.88) and Introduction
severe periodontitis were included in the present study. It is generally accepted that there is an association
The treatment group received mechanical periodontal between periodontitis and diabetes mellitus. Several
treatment combined with systemic doxycycline, studies reported poorer periodontal health in patients
100 mg day)1 for 14 days. The control group received with type 2 diabetes mellitus (Cianciola et al, 1982;
neither periodontal treatment nor systemic doxycycline. Emrich et al, 1991; Safkan-Seppala and Ainamo, 1992).
Clinical periodontal parameters, fasting plasma glucose Type 2 diabetes mellitus patients were 2.8 times more
(FPG), and HbA1c levels were measures at baseline and likely to have destructive periodontal disease (Emrich
3 months. et al, 1991) and 4.2 times more likely to have alveolar
RESULTS: Periodontal treatment significantly improved bone loss progression (Taylor et al, 1998a). The
periodontal status of the treatment group (P < 0.05), increased risk of developing periodontal disease could
however the reduction in the level of FPG and HbA1c did not be explained on the basis of age, gender or hygiene.
not reach significance. In the control group, no significant Periodontal disease has been considered to be another
changes in clinical periodontal parameters, FPG and complication of diabetes mellitus (Löe, 1993) and
HbA1c levels were observed, except for significant evidence also supports poorer glycemic control contri-
increase in attachment loss (P < 0.05). Comparing the buting to poorer periodontal health (Ainamo et al,
two groups, although the 3-month level of HbA1c of the 1990; Unal et al, 1993; Novaes et al, 1996; Taylor et al,
treatment group was lower than that of the control 1998b).
group, the difference did not reach significance. Grossi and Genco have proposed that the relation of
CONCLUSIONS: The results of the present study indi- periodontitis and diabetes is bi-directional (Grossi and
cate that the periodontal condition of older Thais with Genco, 1998). One possible biologic mechanism is that
uncontrolled diabetes is: (a) significantly improved glucose-mediated advanced glycation end products
3 months after mechanical periodontal therapy with (AGEs) accumulation impairs chemotactic and phago-
adjunctive systemic antimicrobial treatment, and cytic function of polymorphonuclear leukocytes (Wilson
(b) rapidly deteriorating without periodontal treatment. and Reeves, 1986; Marhoffer et al, 1992). Additionally,
The effect of periodontal therapy on the glycemic control when AGE-protein binds to its macrophage receptors, it
of older uncontrolled diabetics will require further stud- induces production of IL-1, and TNFa (Vlassara et al,
ies that will have to include much larger sample sizes. 1988). These proinflammatory cytokines play a role not
Oral Diseases (2005) 11, 293–298 only in the pathogenesis of diabetic complications
(Vlassara et al, 1988) but also in the pathogenesis of
periodontitis, and may explain why diabetic patients
have more severe periodontitis. Gram-negative perio-
Correspondence: Dr Ananya Promsudthi, Department of Oral Medi- dontopathic bacteria in periodontal pockets, in turn,
cine, Faculty of Dentistry, Mahidol University, Yothi Street, Bangkok serve as a chronic source of systemic challenge. The
10400, Thailand. Tel: 66(2) 644 6359, Fax: 66(2) 644 8644 ext 3419,
E-mail: dtaps@mahidol.ac.th
interaction of bacterial products with mononuclear
Received 13 November 2003; revised 10 January 2005; accepted 26 phagocytic cells and fibroblasts results in elevated
January 2005 secretion of IL-1b, PGE2, TNFa, and IL-6 (Offenbacher,
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Effect of periodontal therapy on type 2 diabetic older subjects
A Promsudthi et al

294
1996; Kornman et al, 1997). TNFa is a proinflammatory value of 0.6 from previously reported study (Grossi
cytokine that has been implicated in insulin resistance. et al, 1997).
One possible mechanism is via suppression of insulin
induced tyrosine phosphorylation of insulin receptor Treatment regimen
substrate-1 (IRS-1) (Kanety et al, 1995). Conceptually, if The treatment group received periodontal treatment
TNFa is a key molecule mediating insulin resistance, including oral hygiene instruction, and removal of supra
successful periodontal treatment that reduces the TNFa and subgingival calculus. Each tooth was thoroughly
levels (Heasman et al, 1993) should improve insulin scaled and root planed with ultrasonic and hand
sensitivity and metabolic control in diabetic patients. instruments in four sessions within 2 weeks. Subjects
Periodontal therapy consisting of mechanical treatment in this group received systemic doxycycline,
combined with systemic or local antimicrobial adminis- 100 mg day)1 for 2 weeks, starting on the first session.
tration has been shown to improve diabetic status Patient compliance with 2-week course of antibiotic in
(William and Mahan, 1960; Miller et al, 1992; Grossi the treatment group was evaluated by interview. Sub-
et al, 1997, Iwamoto, 2001). While both periodontitis jects in the control group received neither oral hygiene
and diabetes mellitus have higher prevalence with instruction and periodontal treatment nor systemic
increasing age (Locker and Leake, 1988; Grossi et al, doxycycline nor placebo.
1995; Kenny et al, 1995), studies evaluating the effect of
periodontal therapy on diabetic status in older adults are Clinical assessments
scarce (Stewart et al, 2001). Therefore, it was our interest Periodontal status was assessed at baseline and
to study the relation of these two diseases in an older 3 months and included plaque assessment (Machtei
group of patients. The purpose of this study was to et al, 1992), bleeding on probing (BOP) (Ainamo et al,
investigate the effect of combined mechanical and 1990), measurement of probing depth (PD) and the
systemic antibiotic periodontal therapy on the diabetic distance from cemento-enamel junction to gingival
control in older adults. margin (CEJ-GM) on all teeth present in the mouth at
mesiobuccal, midbuccal, distobuccal, mesiolingual, mid-
lingual, and distolingual areas. Clinical attachment
Materials and methods levels were calculated from PD + (CEJ-GM) measure-
Study population ments. Probing measurements were performed with
Sixty patients, aged 55–80 years, were recruited from the standard manual periodontal probe (PCPUNC 15;
Diabetic Clinic of Rajavithi Hospital, Bangkok, Thai- Hu-Friedy, Chicago, IL, USA).
land. All patients had uncontrolled type 2 diabetes
mellitus [glycated hemoglobin (HbA1c) values between Determination of plasma glucose and glycated hemoglobin
7.5 and 11.0%]. Additionally, each patient had at least Venous blood samples were collected at baseline and
14 teeth with severe periodontitis as defined by at least at 3 months and assayed for fasting plasma glucose
eight sites with pocket depth ‡5 mm and clinical (FPG) using glucose oxidase method and HbA1c using
attachment level ‡5 mm. Patients with the following immunoassay method at Rajavithi Hospital central
conditions i.e. oral infections or periapical pathology as laboratory.
assessed by clinical and radiographic examinations,
smoking, allergy to tetracycline derivatives, severe Statistical analysis
systemic diseases, previous history of antibiotic intake Mean and standard deviation for plaque score, BOP,
and/or periodontal therapy within 3 months were not PD, clinical attachment level, plasma glucose and
included in the study. All diabetic patients were under HbA1c were calculated at baseline and at 3 months.
care of a physician. Their diabetic medications included Paired t-test and independent t-test were used to test
oral medication only, insulin only, or both. The patients changes from baseline and differences between groups.
were advised to strictly control their diet and their The treatment group was also divided into two sub-
medications. If, during the course of the study, the groups on the basis of the response for each of the four
physician opted to change a patient’s medical care (type periodontal parameters, using median values as cut off
and/or dose of medication) for improved management points, and repeated the comparisons. Subgroup analy-
of the disease, then the patient was exited from the sis of changes of HbA1c from baseline levels was
study. Patients who refused periodontal treatment were performed using Chi-square test. The data were ana-
automatically placed in the control group; others were lyzed using SPSS for windows software program (SPSS
randomly assigned to either treatment or control group Inc., Chicago, IL, USA).
by tossing a coin. The details of the study were explained
to the patients and all participants provided informed
Results
consent. The Institutional Review Board of Mahidol
University approved the study protocol and informed Eight patients did not complete the study and their
consent form. Using Altman’s nomogram (Petrie et al, baseline data were excluded from analysis; five (two in
2002), it was decided to have at least 15 subjects in each the treatment group and three in the control group) did
group in order to have a 90% chance of detecting a not comply with the 3 months evaluation appointment
difference in mean HbA1c of 1% at the 5% level of and three suffered diabetic complication. At the end of
significance, assuming the standard deviation of HbA1c the study, there were 27 and 25 patients who completed

Oral Diseases
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Effect of periodontal therapy on type 2 diabetic older subjects
A Promsudthi et al

295
Table 1 Demographic information of patients at baseline significance (Table 3). Analyzing the data by subgroups
of the treatment group, on the basis of the response for
Treatment group Control group each of the four periodontal parameters using medians
(n ¼ 27) (n ¼ 25) as cut off points, again did not find the beneficial effect
Age of periodontal treatment on glycemic control (data not
Mean ± s.d. 61.11 ± 5.83 61.64 ± 5.81 shown). Six patients previously had HbA1c level ‡8%
Range 55–80 55–73 became <8% after periodontal treatment. One patient
Gender increased HbA1c level to ‡8 %.
Male (n) 11 8
Female (n) 16 17 At 3 months evaluation of the control group, more
Duration of DM (years) attachment loss was observed (P < 0.05) with no
Mean ± s.d. 8.30 ± 4.21 14.36 ± 7.57 significant changes in PD, plaque score and BOP during
Mode 10 10 3-month observation period. No significant change in
Range 2–20 4–30
the level of FPG and HbA1c was found in this group
(Table 3). Two patients in this group previously had
the study without changes in medical care in the HbA1c level ‡8% had decreased HbA1c level to <8%.
treatment and control groups, respectively. Table 1 Even though, 16 patients in the treatment and 14
shows the demographic information of the patients in patients in the control groups demonstrated decreased
both groups. The periodontal status, levels of FPG, and HbA1c level, subgroup analysis of changes in HbA1c
HbA1c of both groups at baseline are shown in Table 2. level found no association between periodontal treat-
At baseline, 24 of 27 patients in the treatment group and ment with adjunctive antimicrobial treatment and
22 of 25 patients in control group had HbA1c ‡8%. changes in HbA1c levels (v2 ¼ 0.056, P ¼ 0.812,
There were no significant differences in PD, attachment Table 4).
loss, and the level of HbA1c between groups. However, Comparing the periodontal status between the treat-
the mean plaque score and BOP of the treatment group ment and control group at 3 months, the treatment
were higher than the control, while the level of FPG was group had significant shallower PD and less attachment
lower. loss than the control group. Although the reduction of
At 3 months after treatment, the periodontal status of the level of HbA1c from baseline of the treatment group
the treatment group apparently improved. All of the was more than that of the control group, the difference
patients in this group had decreased plaque score, BOP, did not reach significance (Table 4).
and PD. Three patients of the treatment group showed
increased attachment loss. There were significant reduc- Discussion
tions in plaque score, BOP, PD and attachment loss
(P < 0.05). However, the reduction in the levels of FPG In order to better understand the relationship between
(P ¼ 0.60) and HbA1c (P ¼ 0.185) did not reach periodontal disease and diabetes mellitus, the present

Table 2 Periodontal and diabetic status of patients at baseline

PD (mm) CAL (mm) Pl (%) BOP (%) FPG (mg dl)1) HbA1c (%)

Treatment 3.22 ± 0.69 4.03 ± 1.03 91.48 ± 5.22* 61.57 ± 15.99* 151.4 ± 23.6* 8.98 ± 0.88
Control 3.27 ± 0.49 4.10 ± 0.79 86.16 ± 7.50 49.79 ± 15.32 171.6 ± 34.7 9.17 ± 1.02

Values are given as mean ± s.d.


PD, probing depth; CAL, clinical attachment level; Pl, plaque score; BOP, bleeding on probing; FPG, fasting plasma glucose; HbA1c, glycated
hemoglobin.
*Statistically significant difference compared with control group (P < 0.05).

Table 3 Changes in periodontal and diabetic status of the treatment and control groups between baseline and 3 months

PD (mm) CAL (mm) Pl (%) BOP (%) FPG (mg dl)1) HbA1c (%)

Treatment
3 months 2.28 ± 0.35a 3.58 ± 1.21a 68.25 ± 13.37a 24.35 ± 8.77a 147.81 ± 28.88 8.78 ± 1.24
Changes 0.94 ± 0.41 0.45 ± 0.50 23.23 ± 13.54 37.22 ± 14.69 3.63 ± 35.55 0.19 ± 0.74
Control
3 months 3.28 ± 0.54c 4.34 ± 0.86b, c
87.74 ± 7.67 49.78 ± 16.28 171.80 ± 46.67 9.28 ± 1.50
Changes )0.01 ± 0.24 )0.24 ± 0.45 )1.58 ± 7.32 0.01 ± 9.85 )0.2 ± 54.22 )0.12 ± 1.05

Values are given as mean ± s.d.


PD, probing depth; CAL, clinical attachment level; Pl, plaque score; BOP, bleeding on probing; FPG, fasting plasma glucose; HbA1c, glycated
hemoglobin.
a
Statistically significant decrease compared with baseline (P < 0.05).
b
Statistically significant increase compared with baseline (P < 0.05).
c
Statistically significant difference compared with the treatment group (P < 0.05).

Oral Diseases
16010825, 2005, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1601-0825.2005.01119.x by COMSATS Inst of Info Techn - I, Wiley Online Library on [22/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Effect of periodontal therapy on type 2 diabetic older subjects
A Promsudthi et al

296
Table 4 Distribution of patients at 3 months stratified by changes in compared with diabetics with good control and no
glycated hemoglobin (HbA1c) from baseline levels complication, 1 year after therapy (Tervonen and Karj-
alainen, 1997).
Treatment group Control group In contrast to the periodontal health improvements
(n ¼ 27) (n ¼ 25)
observed in the uncontrolled diabetic older patients
Decrease in HbA1c levels 16 14 receiving periodontal therapy, the clinical attachment
No change or increase in HbA1c 11 11 level of the patients who did not receive periodontal
levels therapy significantly increased within 3 months. One
interesting finding was the magnitude of the deterior-
Chi-square test, v2 ¼ 0.056, P ¼ 0.812.
ation of periodontal health. The non-treated diabetics
lost 0.24 ± 0.45 mm of periodontal attachment in
study aimed to investigate the effect of periodontal 3 months. The rate of attachment loss, 0.96 mm year)1,
therapy in older patients with both chronic periodontitis in diabetic older patients was almost the same as the
and diabetes mellitus, in the absence of any changes in annual loss of attachment rate, 1 mm year)1, in the
medical therapy during the study period. We chose to rapidly progressing disease group of Sri Lankan tea
focus on older patients because aging is associated with workers who had never been exposed to dental treat-
increased prevalence of periodontal disease (Locker and ment and tooth brushing (Löe et al, 1986). The results of
Leake, 1988) and increased insulin resistance (Paolisso the present study suggest that, without periodontal
et al, 1998, 1999). Additionally, the incidence and treatment, uncontrolled older diabetics are at risk of
severity of diabetes increase with advancing age (Bar- rapidly losing their periodontally-affected teeth.
bagallo et al, 1997; Perry, 1999). Our results clearly At baseline, the treatment group had higher mean
demonstrate that mechanical periodontal treatment plaque score and BOP than the control group. After
combined with systemic doxycycline, 100 mg day)1 for periodontal therapy, mean plaque score and BOP of the
14 days, improved periodontal status of uncontrolled treatment group decreased by 25 and 60%, respectively,
type 2 diabetic patients. PD reduction and clinical while those of the control group remained unchanged.
attachment gain of the treatment group were 29.19 and Despite this significant 25% reduction in plaque score in
11.17% respectively. Similar to previous studies (Grossi the treatment group, the improvement in plaque control
et al, 1997; Iwamoto et al, 2001; Stewart et al, 2001), we in these older diabetic patients was far less than the
found that levels of HbA1c in the treatment group plaque control level expected of treated periodontal
decreased, yet, contrary to these other studies, the patients (DeVore et al, 1990). We found that the older
decrease did not reach statistical significance. Conven- patients had diminished manual dexterity as well as
tional mechanical therapy has been shown to effectively lesser ability to learn new oral hygiene technique, such
treat chronic periodontitis (Drisko, 1996), while the as brushing and use of interdental device, to prevent
adjunctive use of systemic doxycycline provided a disease than younger adults as previously reported
modest improvement beyond that obtained by scaling (Banting, 1986). It has also been previously reported
and root planning (Ng and Bissada, 1998). Although that diabetic patient compliance with dental recommen-
inconclusive, adjunctive antimicrobial periodontal treat- dations is related to HbA1c levels, with better compli-
ment has been reported to significantly reduce circula- ance among those with better glycemic control (Syrjälä
ting TNF a and HbA1c levels (Grossi et al, 1997; et al, 1999). Therefore, for reasons that include age and
Iwamoto et al, 2001). Because of these earlier findings, systemic health control (the latter probably being an
we chose the adjunctive use of systemic doxycycline. indicator of overall health behavior), the population of
The magnitude of pocket depth reduction and clinical the present study, i.e. older and poorly controlled
attachment gain found in our study (0.94 and 0.45 mm, diabetics, appear to represent a particular challenging
respectively) is similar to the response to non-surgical group of periodontal patients in term of the therapist’s
periodontal therapy in non-diabetics, whether treated by ability to motivate them and alter their oral health
mechanical therapy alone (Badersten et al, 1981; Lindhe behavior.
et al, 1982; Proye et al, 1982) or with adjunctive There are many factors influencing the short-term
systemic doxycycline treatment (Ng and Bissada, glucose level of a diabetic patient, and one of these is
1998). The improvements in periodontal parameters medical care. To determine the relative contribution of
reported here are higher than those reported in doxy- periodontal therapy in glycemic control of poorly
cycline-treated uncontrolled diabetic middle-aged controlled older diabetics, the present study was
patients with comparable baseline pocket depth and designed to include such patients that did not receive
clinical attachment level (Grossi et al, 1997). It is any change in their diabetic control regimen during the
interesting that the short-term (3 months) response to 3-month study period. Even though long-term study
non-surgical periodontal therapy in uncontrolled dia- would have been preferable, the ethical dilemma of
betics was similar to that reported in non-diabetics. withholding any change in medical treatment for a
However, long-term response to non-surgical periodon- period significantly longer than 3 months in patients
tal therapy in poorly controlled diabetics should be with poorly controlled diabetes made such a longer-term
further investigated as Tervonen reported higher recur- study impossible. The results suggest that periodontal
rence of sites with PD ‡4 mm in Type 1 diabetic patients therapy, consisting of non-surgical mechanical therapy
with poor metabolic control or multiple complications with adjunctive systemic antibiotics in older Thai

Oral Diseases
16010825, 2005, 5, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1601-0825.2005.01119.x by COMSATS Inst of Info Techn - I, Wiley Online Library on [22/05/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Effect of periodontal therapy on type 2 diabetic older subjects
A Promsudthi et al

297
subjects, does not result in significant improvement of larger sample size is needed for any future study in older
glycemic control, as determined by HbA1c levels. The poorly controlled diabetics. Taking all together, the
present findings are in contrast to the results obtained by aforementioned factors may explain the lack of statisti-
Stewart et al (2001). They conducted a study in type 2 cally significant effect of periodontal therapy on glycemic
diabetic older patients and found that level of HbA1c control of type 2 diabetic older patients in this study.
decreased after non-surgical periodontal treatment. In conclusion, the results of the present study indicate
However, unlike in the present study, the method of that, in the absence of any medical intervention, the
diabetes control was changed during the study period of periodontal condition of older Thais with poorly con-
Stewart et al (2001). Therefore, the relative contribution trolled diabetes is: (a) significantly improved 3 months
of periodontal therapy in improving the glycemic after mechanical periodontal therapy with adjunctive
control of type 2 older diabetics remains unclear. systemic antimicrobial treatment, and (b) rapidly deteri-
Significant reduction of HbA1c value has been orating without periodontal treatment. Furthermore, the
reported 1 month after the completion of antimicrobial results suggest that documenting an independent effect of
periodontal therapy (Iwamoto et al, 2001). In longer periodontal therapy on the glycemic control of older
observation, significant reduction of HbA1c value was poorly controlled diabetics will require further studies
reported at 3 months; however, this significance could that will have to include much larger sample sizes.
not be observed at 6 months (Grossi et al, 1997). There
are several differences that could account for the
Acknowledgements
discrepancy between the findings of the present study
and those by Grossi et al (1997) and Iwamoto et al The authors are very grateful to Professor Dimitris N. Tatakis,
(2001). The study of Grossi and coworkers included a Section of Periodontology, Ohio State University, for his
wide age range (25–65 years) of Native Americans with advice on preparing the manuscript. This study was supported
significant predisposition for type 2 diabetes (Grossi by grant from Royal Thai Government.
et al, 1997), while the present study was conducted on
significantly older (age range: 55–80 years) Thai References
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