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843

The Relationship Between Reduction in


Periodontal Inflammation and Diabetes
Control: A Report of 9 Cases
Miller, * Mary Agnes Manwell, * Dewey Newbold, * Mary Ellen Reding, *
Lawrence S.
Allen Rasheed, * Janet Blodgett,f and Kenneth S. Komman*

The established correlation between diabetes and periodontal diseases and the in-
creasing prevalence Type of II diabetes in the general population indicate that dental
practitioners will probably treat an increasing number of diabetic patients. Despite the
fact that there is little scientific evidence to support the concept, it has been generally
accepted that treatment for periodontal disease in diabetic patients may reduce insulin
requirements and improve metabolic balance. However, to date no one has evaluated the
effects of periodontal therapy on the metabolic state of the poorly-controlled diabetic
patient. The purpose of this pilot study was to evaluate the effect of controlling gingival
inflammation on blood glucose levels as determined by glycosylation of hemoglobin and
albumin. / Periodontal 1992; 63:843-848.

Key Words: Diabetes mellitus/epidemiology; diabetes mellitus/etiology; blood glucose;


periodontitis/epidemiology; periodontitis/therapy; risk factors

Periodontists have long been aware of the apparent impact that patients with diabetes mellitus have an increased sus-
of diabetes on the treatment of periodontal disease,16 and ceptibility to infection. It is also well documented that acute
it is very likely that the periodontist will see more diabetic infections and inflammatory conditions increase glucose and
patients in the future. There are currently 12 to 14 million insulin utilization and therefore complicate the metabolic
diabetics in the United States,7 of whom approximately 80% control of diabetes. This factor is of great importance since
are classified as having Type II (non-insulin-dependent) di- it has been shown that diabetic patients who are poorly
abetes, with the remainder having Type I (insulin-depen- controlled may have an increased risk for diabetic compli-
dent). Type II diabetes is reportedly increasing at a rate of cations, such as ocular and vascular lesions.
about 6% per year suggesting that the number of people Although it has generally been taught that control of peri-
with this condition may double every 15 years.7 odontal disease is beneficial to diabetic control and may
It has been previously shown in both humans and animal reduce the insulin requirement,5-6 there is minimal evidence
models, that some of the host defects routinely observed in to support this conclusion or to suggest what magnitude of
patients with diabetes8"13 are risk factors for periodontal an effect might be expected from periodontal therapy. Wil-
disease. Although the specific pathologies associated with liams and Mahan23 found that patients required less insulin
diabetes, observations by clinicians,14'15 and a few well following stabilization of their diabetic condition and peri-
designed population studies1619 suggest an increased prev- odontal treatment. However, to date, no one has evaluated
alence and/or severity of periodontal diseases in diabetics, the effects of periodontal therapy on the metabolic state of
other studies have been unable to confirm that correla- the poorly-controlled diabetic patient.
tion.20,21 Similarly, metabolic control of blood glucose lev- The purpose of this pilot investigation was to examine
els has been reported to have varied effects on the periodontal the effects of the elimination of gingival inflammation on
condition.14'22 The prevalence of diabetes and its probable blood glucose levels, as evaluated by the glycosylation of
influence on periodontal disease suggest that diabetics will hemoglobin and albumin, in poorly-controlled diabetic pa-
very likely become an increasing part of the patient popu- tients with Periodontitis. It is hypothesized that the elimi-
lation seen by both general dentists and periodontists. nation of inflammation will lead to decreased blood sugar
A substantial body of literature supports the conclusion levels which can then be more easily controlled and/or lead
to a decrease in the amount of insulin required.
*
Department of Periodontics, The University of Texas Health Science
Center, San Antonio.
''Department of Medicine.
J Periodontol
844 REDUCTION OF PERIODONTAL INFLAMMATION IN DIABETES CONTROL October 1992

MATERIALS AND METHODS pies were used to determine the expected change in glucose
metabolism without any periodontal intervention. Two post-
Patients treatment blood samples were drawn during the study. One
Approximately 200 patients were screened at The Univer- sample was taken approximately 4 weeks post-initial ther-
sity of Texas Health Science Center at San Antonio Dental apy and the other sample was taken 8 weeks post-initial
School. Ten patients met the following inclusionary crite- therapy.
ria: 1) participants must have been diagnosed with insulin-
dependent diabetes more than 1 year prior; 2) a glycated Procedure
hemoglobin ("Glycated hemoglobin" is used synony-
mously with "glycosylated hemoglobin" in the literature,
Each patient was seen 6 times during the study. The treat-
but has recently become the preferred terminology.) and/or ment protocol was specifically designed to reduce the mi-
crobial challenge as rapidly as possible and to gain control
a glycated albumin level which fell above the normal con-
of the periodontal disease within a time frame that allowed
trol range and thereby considered to be uncontrolled; 3) the
for few confounding events that might interfere with the
presence of at least 15 natural teeth; 4) moderate to severe diabetic status of each patient. Blood was drawn on the first
Periodontitis as defined by at least 6 sites with a loss of visit to evaluate the glycated hemoglobin and glycated al-
attachment of 4 mm or greater (using a force controlled
bumin levels and clinical and radiographie assessments were
probe), radiographie evidence of greater than 25% bone loss
in multiple sites, and generalized inflammation; 5) the dem- performed to evaluate the patients' periodontal status. If the
onstrated ability to perform self-blood glucose monitoring; patients had moderate to severe Periodontitis and blood glu-
cose values above the normal range they returned for the
6) the demonstrated ability to keep a diary of blood glucose second visit. On this visit, blood was again drawn to es-
levels, illness, and activity levels; and 7) the physical and tablish a second baseline value. The second baseline sample
mental ability to control their plaque to a clinically accept-
was taken at least 6 weeks after the first sample. The sub-
able level.
The exclusionary criteria were as follows: 1) severe di- jects were also given oral hygiene instructions and in-
abetic complications (greater than stage 1 background di- structed in the use of the blood glucose monitor§ for home
abetic retinopathy, loss of limb, or autonomie neuropathy); monitoring. Clinical indices were then evaluated using a
standardized probe. On the third visit, scaling and root planing
2) presence of any contributing dermal infections or indo- with local anesthetic was performed in one visit. If scaling
lent bladder infections; 3) any recent change in diabetic
status or change in insulin requirements; 4) any severe den-
and root planing could not be completed in one visit, the
tal infections requiring drainage, antibiotics, extractions, or subjects returned within 2 days in order to complete the
treatment. All patients were then instructed to begin home
endodontic therapy; and 5) history of allergic reactions to
tetracycline. monitoring and were placed on doxycycline 100 mg (b.i.d.
for the first day and then 1 tab per day thereafter) for 14
Clinical Evaluation
days, and a Chlorhexidine rinse11 twice daily for 30 seconds.
Two weeks after completion of scaling and root planing,
The clinical examination included an assessment of the
patients returned for evaluation of home care and to receive
radiographie findings and the recording of clinical indices. a prophylaxis. Approximately 4 and 8 weeks following
The subjects' periodontal conditions were evaluated using
treatment, patients returned for re-evaluation of the clinical
a force controlled probe* set to consistently deliver a force
indices and to have blood drawn to evaluate glycated hemo-
of 20 grams. Pocket depth and attachment levels were re-
corded at 6 sites per tooth. Additionally, each site was
globin and albumin levels. Patients were advised to con-
tinue their normal daily insulin regimen and dietary
evaluated for bleeding upon probing and suppuration. Vis-
ual signs of color, contour, and texture were also recorded.
requirements as instructed by their physician. Patients were
asked to record any changes in insulin requirements or med-
ications taken during the study.
Blood Glucose Levels Self-monitoring of blood glucose values was originally
Control of blood glucose levels were evaluated by means intended to assist the patients with tracking insulin need.
of the glycated hemoglobin and glycated albumin levels. This procedure was intended to serve as a precaution to
Fifty milliliters of blood were sent to one of three labora- guide insulin dosing if a dramatic change in blood glucose
tories: 1) The University of Texas Health Science Center resulted from the therapy. As is characteristic of the poorly
at San Antonio; 2) Smithkline Beecham Laboratory (St. controlled diabetic, most subjects did not use the monitor
Louis, Missouri); or 3) Medlab (San Antonio, Texas). All or did so inconsistently; therefore, no data were collected.
assays for each patient were performed by the same labo- None of the patients maintained written diaries of insulin
ratory throughout the study. Two blood samples were drawn dosage or blood glucose values.
6 to 14 weeks apart and prior to any oral hygiene instruc- Following completion of the study, patients were referred
tions or periodontal treatment. The two pretreatment sam-
§Glucoscan 3000, Lifescan, Inc., Mountain View, CA.
*Florida Probe Corp, Gainesville FL. "Peridex, Procter & Gamble Co., Cincinnati, OH.
Volume 63
Number 10 MILLER, MANWELL, NEWBOLD, REDING, RASHEED, BLODGETT, KORNMAN 845

Table 1. Patient characteristics A. Patients with Consistent Decrease B. Patients with No or Inconsistent
in BOP Decrease in BOP
Positive
Natural % Sites % Sites Treatment
Gender Ethnicity Teeth 4-6 mm > 6 mm Response
M Hispanic 17 28.4 3.9 Yes
M Hispanic 24 8.3 0.0 Yes
M Hispanic 27 6.2 11.1 No
M Anglo 24 16.6 2.1 Yes
M Hispanic 29 39.0 5.7 Yes
F Hispanic 28 14.3 0.0 Yes
F Hispanic 18 21.3 0.0 No
M Anglo 18 16.6 0.0 No
F Hispanic 28 25.0 9.0 No

Pre-Tx

for continued periodontal treatment if they so desired. The Figure 1. The change in bleeding on probing as measured by a constant-
patients were able, at any time, to exit the study if neces- pressure periodontal probe is shown for each of the post-treatment (Post-
sary. At no time during the study did the periodontal con- Tx) monitoring periods for each patient. Bleeding scores for patients who
dition of any patient worsen sufficiently to require intervening had a consistent decrease at both 4 and 8 weeks following therapy are
shown in 1A, with the remaining patients presented in IB.
therapy beyond that specified in the experimental protocol.
This clinical study was approved by the Institutional Re-
view Board at The University of Texas Health Science Cen- Therapy produced a reduction in inflammation in 7 of 9
ter at San Antonio. patients, as measured by bleeding on probing. Two patients
exhibited an increase in bleeding on probing.
Statistical Analysis For the 7 patients who showed an improvement, the mean
Data on each patient are presented in a descriptive format pretreatment bleeding on probing was 29.3% ± 20.9 of
due to the small number of cases. In some instances the the sites with a mean post-treatment bleeding on probing
means of duplicate pre- and post-therapy glycated hemo- of 11.0% ± 4.7. Since the primary objective was to assess
globin and albumin value were determined and compared the change in metabolic control of patients in whom peri-
by means of a paired r-test. Although more appropriate odontal inflammation had been controlled, the patients were
statistical methodologies exist for analysis of repeated mea- divided as shown in Figure 1 based on the consistency of
sures data, these methodologies are impractical and essen- bleeding reduction. The 5 patients in Figure 1A had a sub-
tially meaningless for such a small number of patients. stantial and consistent improvement in bleeding on probing
through the 8 weeks following therapy. The other four pa-
RESULTS tients (Figure IB) either had an increase in bleeding or an
inconsistent response to therapy such that they could not
Patients qualify as having consistent improvement in periodontal
Nine of the 10 patients completed the study. The presenting inflammation.
characteristics of each patient are shown in Table 1. No
significant medical or dental complications occurred during Metabolic Parameters
the monitoring period and all the patients tolerated the treat- The pretreatment glycated hemoglobin (Fig. 2) values were
ment procedures well. However, one patient experienced unchanged and remarkably stable between the 2 sampling
an allergic reaction approximately 4 days after the initiation time points. The glycated albumin values, which are more
of the Chlorhexidine rinse which manifested as a generalized affected by short-term glucose fluctuations, varied substan-
mucositis. This condition resolved after the Chlorhexidine tially between the 2 pretreatment samples.
was discontinued and the patient completed the study, rins- The mean glycated hemoglobin for the 9 patients pre-
ing with warm saline instead of Chlorhexidine. treatment was 9.44 ± 1.69 and decreased (P 0.11) to=

9.01 ± 2.01 post-treatment. No change was observed in


Clinical Parameters the glycated albumin value following periodontal therapy
The patients presented prior to therapy with bleeding on when all patients were included in the analysis.
probing at a mean of 26.4% of the sites examined. A mean As seen in Figure 3A, the 5 subjects with a consistent
of 23.1% of the sites per patient had probing depths 3=4 improvement in bleeding all showed a decrease in glycated
mm and 3.5% of the sites probed >6 mm. hemoglobin levels post-treatment (mean pretreatment
Therapy produced a reduction in bleeding on probing AiC 8.7%, mean post-treatment 7.8%; <0.01 paired
= =

from 26.4% ± 19.0 (standard deviation) of sites to 16.6% r-test). Patients with no consistent improvement in bleeding
± 13.1 (P 0.25, paired r-test). A 1.0 mm decrease in
=
also showed no change or an increase in glycated hemo-
the mean probing depth per patient (range: 0.3 mm to 2.0 globin values following therapy (Figure 3B). Mean glycated
mm) was observed following treatment. albumin levels also decreased in the 5 patients with a con-
J Periodontol
846 REDUCTION OF PERIODONTAL INFLAMMATION IN DIABETES CONTROL October 1992

%A1C DISCUSSION
13
Periodontitis is a complex multifactorial disease. Similarly
12 diabetes mellitus is a complex metabolic syndrome. It is
11 the complexities of both of these disease processes which
10 may contribute to the controversy found in the literature.
Many investigators have studied oral manifestations of di-
abetic patients,8,14'24 periodontal disease severity,15-19'25"28
immunological responses of diabetic patients,9,10'11 and the
effects of controlling diabetes on the periodontium.6'11'14'20
Diabetes has long been identified by periodontists as a
Pre-Tx
complicating factor in periodontal therapy. Both epidemi-
Sample #1
Pre-Tx
Sample #2
ologie studies16-19 and case reports14,15 have shown diabetes
to be a major risk factor for Periodontitis. The most exten-
Figure 2. Glycated hemoglobin values are shown for each patient at each sive analysis of the relationship between diabetes and Peri-
of the two pretreatment (Pre-Tx) sample times, which were 6 to 14 weeks
apart. odontitis was recently accomplished in a well controlled
comparison between Type II diabetic and non-diabetic Pirna
Indians.19 The presence of diabetes increased the risk of
A. Patients with Consistent Decrease B. Patients with No Decrease
in Bleeding on Probing in Bleeding on Probing developing Periodontitis threefold. Diabetes was found to
A1C A1C increase the prevalence and severity of Periodontitis inde-
Chg
2.5
Chg
2.5 pendent of the effects of age or oral hygiene. Although this
relationship appears to be strong, the compounding varia-
bles inherent in studying two chronic diseases may result
in less clear associations in selected populations.
The impact of diabetes on periodontal diseases is also
evident during therapy. Conventional periodontal therapy
that is directed to reducing the bacterial challenge is less
predictable in poorly-controlled diabetics,15 and the optimal
clinical outcome in a Periodontitis patient with diabetes must
Post-Tx Post-Tx Pre-Tx Post-Tx Post-Tx include control of both the diabetes and the bacterial
4 wks 8 wks 4 wks 8 wks

Figure 3. The glycated hemoglobin is shown for each of the


change in
challenge.15,22,29
post-treatment (Post-Tx) monitoring periods for each patient. Patients are study was initiated as one of multiple pilot projects
This
grouped according to the bleeding response patterns of Figure 1. to explore the relative influence of different variables in the
relationship between diabetes and Periodontitis. This pilot
A. Patients with Consistent Decrease B. Patients with No Decrease
study therefore asked a very simple directed question: If
in Bleeding on Probing in Bleeding on Probing periodontal inflammation in poorly-controlled diabetics can
be controlled is there a reduction in blood glucose values?
Although a small number of patients were involved, this
study appears to demonstrate some association between im-
provement in the periodontal bleeding response and im-
proved metabolic control of blood glucose levels.
The only previous attempt to directly address the value
of periodontal therapy in the metabolic control of diabetes23
used the best technology at the time which included re-
cording of insulin usage. One other report17 noted reduced
diabetic complications and insulin requirement in diabetics
Pre-Tx who were treated for Periodontitis. The present study em-
Figure 4. The change in glycated albumin is shown for each of the post-
ployed the assessment of plasma levels of glycated hemo-
treatment (Post-Tx) monitoring periodsfor each patient. Patients are grouped globin and albumin, to which glucose is attached.30 Since
according to the bleeding response patterns of Figure 1. these levels are a reflection of the chronic exposure of
hemoglobin and albumin to blood glucose as well as the
half-life of these compounds, the assays do not depend upon
sistent improvement in bleeding on probing, but there was patient cooperation and are not greatly affected by blood
more variability in this parameter (Fig. 4). glucose fluctuations on the day of the assay. The glycated
No changes in lifestyle or medications that may contrib- albumin is considered an indicator of blood glucose levels
ute to these findings were recorded for any patients. within the previous 1 to 2 weeks and glycated hemoglobin
Volume 63
Number 10 MILLER, MANWELL, NEWBOLD, REDING, RASHEED, BLODGETT, KORNMAN 847

is considered an indicator of blood glucose levels within accomplished in one to two visits within a 2-day period.
the previous 4 to 8 weeks. Although this may not be the optimal way to deliver care
Some tetracycline derivatives have produced transient to diabetic periodontal patients, this approach was consid-
hypoglycémie effects in diabetics but not in normal sub- ered necessary to achieve similar time lines for monitoring
jects. This was most likely not a factor in the results ob- the patients. Future studies should evaluate the ability of
served in the current study since the post-treatment glycated different therapeutic approaches to resolve the inflammation
hemoglobin measurements were taken 4 and 8 weeks fol- in diabetic patients who appear less responsive to peri-
lowing therapy, and the decrease in blood glucose appeared odontal therapy.
to be related to inflammation control. In general this study uses current techniques for moni-
It is reasonable to conclude from this pilot study that the toring blood glucose values that appear to confirm the value
metabolic control of diabetics can be altered by controlling of periodontal therapy as one significant factor in the met-
the periodontal inflammation. Three considerations appear abolic control of diabetes.
to be important in the appropriate interpretation of this con-
clusion. First, caution must be used in interpreting results
from such a small number of patients. Patients with con-
Acknowledgments
The authors very much appreciate the encouragement and
sistent improvement in bleeding scores had a decrease in assistance of Ms. Debra Moore, formerly of the Procter &
glycated hemoglobin that was not seen in repeated pretreat- Gamble Company, in initiating this project; the assistance
ment samples or in patients with no improvement in bleed- of Drs. Sam Miller and Michelle Saunders in the acquisition
ing. Although this pattern appeared to be consistent, the of patients; and the research assistance of Ms. Gail Gilbert.
actual magnitude of change in glucose metabolism appeared The Glucoscan units were provided by Lifescan, Inc. This
to be small. This view is supported by the inconsistent
study was supported in part by a grant from Procter &
response of glycated albumin, which is an indicator of short Gamble Oral Care Product Development, Health and Per-
term glucose control. It therefore seems reasonable to con-
sonal Care Division, Cincinnati, OH.
clude that control of periodontal inflammation has the po-
tential to influence glucose metabolism in diabetics but the
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