Diabetess 6
Diabetess 6
Diabetess 6
PII: S0300-5712(15)00058-5
DOI: http://dx.doi.org/doi:10.1016/j.jdent.2015.03.001
Reference: JJOD 2435
Please cite this article as: Irani FC, Wassall RR, Preshaw PM, Impact of periodontal
status on oral health-related quality of life in patients with and without type 2 diabetes,
Journal of Dentistry (2015), http://dx.doi.org/10.1016/j.jdent.2015.03.001
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*Title Page with Author Details
Institution:
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School of Dental Sciences and Centre for Oral Health Research, Newcastle University, UK
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Institute of Cellular Medicine, Newcastle University, UK
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Corresponding Author:
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Professor Philip M. Preshaw
Framlington Place
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Newcastle University
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NE2 4BW
Email: [email protected]
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Key Words:
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Short Title: Effect of type 2 diabetes and periodontal status on quality of life
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Impact of periodontal status on oral health-related quality of life in patients
with and without type 2 diabetes
ABSTRACT
Objectives: To investigate the impact of periodontal status on oral health-related quality of life
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(OHRQoL) in patients with and without type 2 diabetes mellitus (T2DM).
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Methods: 61 patients with T2DM and 74 non-diabetic patients matched for age, gender and
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periodontal status (health, gingivitis, chronic periodontitis) were recruited. The Oral Health
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Impact Profile (OHIP)-49 was self-completed by all participants at baseline and by the patients
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Results: There were no significant differences in the overall OHIP-49 summary scores between
patients with T2DM (median; interquartile range; 37.0; 19.5-61.0) and without T2DM (30.4;
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16.8-51.0) (p>0.05). Among non-diabetic patients, there were significantly higher OHIP-49
scores (indicating poorer OHRQoL) in patients with gingivitis (41.0; 19.7-75.7) and periodontitis
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(33.0; 19.9-52.5) compared to patients who were periodontally healthy (11.1; 7.1-34.5) (p<0.05),
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though such an effect was not observed in the patients with diabetes. In the non-diabetic patients
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with periodontitis, statistically significant reductions in OHIP-49 scores were noted in the
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changes in OHIP-49 scores following periodontal treatment in the patients with diabetes.
Conclusion: T2DM does not impact on overall OHRQoL as measured by OHIP-49. Chronic
periodontitis and gingivitis were associated with poorer OHRQoL in non-diabetic patients, with
evidence of improvements following periodontal treatment, but no such effects were observed in
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Clinical Significance: Gingivitis and periodontitis are associated with reduced OHRQoL
of periodontitis. No impact of type 2 diabetes on OHRQoL was noted; this may be related to the
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burden of chronic disease (diabetes) minimising the impact of oral health issues on OHRQoL.
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INTRODUCTION
Periodontitis is a common chronic inflammatory disease that affects the supporting structures of
the teeth. Periodontal inflammation is initiated and perpetuated by the subgingival bacterial
biofilm, but the tissue damage which occurs derives mainly from the host immune-inflammatory
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response to the bacterial challenge. Certain systemic diseases are associated with increased
susceptibility to periodontitis, for example, the presence of diabetes is associated with a 2-3-fold
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increased risk, particularly if poorly controlled (1). The rise in the prevalence of diabetes in most
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populations, including in the UK, is mainly attributed to an increase in type 2 diabetes mellitus
(T2DM) (2). T2DM is associated with insulin resistance i.e. the inability of the body to respond
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normally to insulin and inability of the β-cells of the pancreas to produce sufficient insulin. The
multifactorial aetiology and chronic inflammatory nature of both diabetes and periodontitis
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highlight the complexity of the relationship between the two conditions (3).
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Both periodontitis (4, 5) and diabetes (6, 7) have been reported to have negative impacts on
aspects of daily living and health-related quality of life. Evidence suggests that oral health
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problems can adversely affect an individual’s physical functioning, social standing and
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wellbeing, and that it can be difficult to dissociate oral health from general health with regards to
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impacts on quality of life (8-10). Oral health-related quality of life (OHRQoL) can be assessed
using the Oral Health Impact Profile-49 (OHIP-49) questionnaire (11). This contains 49 items
disability, psychological disability, social disability, handicap), with responses ranging from
score 0 indicating ‘never’ to score 4 indicating ‘very often’. Domain scores are generated by
summing the response scores to the items within the domain, and an overall summary score is
generated by summing the response scores to all 49 items. A higher score is indicative of poorer
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OHRQoL. Our group has previously identified, when using OHIP-49, that patients with chronic
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Considering that OHRQoL measures are increasingly used in assessing patient-centred outcomes
of disease and treatment, and in view of the close inter-relationship between periodontitis and
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T2DM, it is important to explore the impact of periodontal status and treatment on OHRQoL in
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patients with T2DM. The aim of this study was to use OHIP-49 to assess OHRQoL in patients
with diabetes and periodontitis, and to evaluate any impact of periodontal treatment.
in Newcastle upon Tyne, UK. Written informed consent was obtained from all participants prior
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to recruitment. The non-diabetic control group was recruited from patients attending Newcastle
Dental Hospital, UK, matched according to age, gender and periodontal status. Participants were
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assigned a diagnosis of periodontal health (no probing depths >4mm, bleeding on probing (BOP)
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≤15%, no attachment loss), gingivitis (no probing depths > 4 mm, BOP >15%, no attachment
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loss), or chronic periodontitis (≥6 sites with probing depths ≥5 mm on separate teeth, with
attachment loss and alveolar bone loss confirmed on x-ray). Exclusion criteria included
dental treatment, bleeding disorders, and any prior non-surgical treatment for periodontal disease
in the past 6 weeks. Ethical approval was granted by the UK National Research Ethics Service
(ref. 06/Q0904/8).
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The periodontal examination was performed by a single examiner using a UNC PCP15 manual
periodontal probe. Parameters recorded included plaque index (PI) (13), modified gingival index
(mGI) (14), probing depth (PD), and percent BOP. Patients with periodontitis received standard
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non-surgical periodontal therapy utilising a full mouth debridement approach with local
anaesthetic typically over 2 visits, together with oral hygiene instruction personalised to their
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clinical situation. Early periodontal maintenance follow up appointments were provided at 3 and
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6 weeks, including further prophylaxis to disrupt the biofilm and reinforcement of oral hygiene
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and 6 months healing. Patients with periodontal health or gingivitis received oral hygiene
instruction and prophylaxis at the screening appointment only, and were not followed up
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thereafter.
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OHIP-49 was used to assess OHRQoL. All participants self-completed the questionnaire at the
screening appointment prior to any treatment being provided. The patients with periodontitis
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additionally completed the questionnaire again at 3 months and 6 months following the
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periodontal therapy.
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The null hypotheses in this study were that (i) there would be no differences in OHRQoL
between diabetic and non-diabetic patients with different periodontal conditions (health,
gingivitis, chronic periodontitis), and (ii) that there would be no impact of periodontal treatment
on OHRQoL. All data were analysed using SPSS 21.0 statistical software. Patients who had not
responded to ≥ 10% of the items in OHIP-49 were eliminated from the study. For patients who
had <10% missing responses, the answers to the missing items were derived using group mean
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score imputation for each item in order to calculate the individual domain scores and the
summary scores as reported previously (12, 15). Data were tested for normality using the
Kolmogorov-Smirnov test. The medians and interquartile ranges for non-parametric variables
and means and standard deviation for parametric variables were determined. For cross-sectional
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analyses for discrete variables, the chi-squared test was used to compare between groups. The
Mann-Whitney test was used for comparisons of OHIP-49 scores between the groups with and
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without T2DM based on the periodontal status. The Kruskal-Wallis test with post-hoc Mann-
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Whitney tests was used to analyse the OHIP-49 data within the groups with and without T2DM
based on the periodontal status. The Friedman test with post-hoc Wilcoxon Signed Rank tests
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was used for longitudinal comparisons of the effects of periodontal treatment. Cronbach’s alpha
RESULTS
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63 patients with T2DM and 75 patients without diabetes were recruited to the study. However, 2
patients with T2DM and 1 non-diabetic patient failed to complete a minimum of 90% of the
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items of the OHIP-49 questionnaire, and were removed from the analysis. The final study
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population therefore comprised 61 patients with T2DM and 74 patients without diabetes.
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Demographic characteristics for the groups with and without T2DM are presented in Table 1.
The groups were well matched for gender, age, ethnicity, and smoking status. As expected, the
HbA1c levels of the group with T2DM were significantly higher than the group without diabetes
(p<0.001). The patients were categorised according to diabetes and periodontal status: ND-H (no
diabetes, periodontal health), ND-G (no diabetes, gingivitis), ND-P (no diabetes, periodontitis),
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D-H (diabetes, periodontal health), D-G (diabetes, gingivitis) and D-P (diabetes, periodontitis).
Cronbach’s alpha for OHIP-49 was 0.97, indicating good internal consistency.
Periodontal data are presented in Table 2. Within the healthy and gingivitis categories at baseline
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(month 0), the T2DM patients had significantly higher PI, mGI and BOP scores compared to the
non-diabetic patients. Among the patients with periodontitis, no significant differences were
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observed between the T2DM and non-diabetic groups with regards to PI, mGI or BOP scores,
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though a slightly higher mean probing depth was observed in the non-diabetic patients.
Following treatment in the patients with periodontitis (both with and without diabetes),
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statistically significant improvements in all periodontal parameters were noted from month 0 to
month 3, and from month 0 to month 6, with the exception of a non-significant reduction in PI
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from month 0 to month 3 in the diabetes group.
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Table 3 shows the OHIP-49 domain and overall summary scores for the patients with and
without T2DM; there were no statistically significant differences between the two groups,
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indicating no differences in OHRQoL between the patients with T2DM and those without
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diabetes. However, when OHIP-49 domain and overall summary scores for patients with and
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without T2DM were categorised according to periodontal status (Table 4), we identified that,
within the non-diabetic group, patients with gingivitis and periodontitis had significantly higher
OHIP-49 scores (indicating poorer OHRQoL) in every domain as well as the overall summary
score compared to the patients who were periodontally healthy. Within the diabetic group,
however, no such differences in OHRQoL were observed between the periodontal status
categories.
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The patients with periodontitis completed OHIP-49 at 3 and 6 months following treatment. Table
5 shows OHIP-49 domain and overall summary scores at each timepoint for the non-diabetic and
diabetic groups. Within the non-diabetic patients, statistically significant reductions in OHIP-49
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scores were noted in the psychological discomfort domain at months 3 and 6, and in the
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OHRQoL. Furthermore, the overall summary score at month 6 was lower than that at month 0 or
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month 3, though this failed to achieve statistical significance. In contrast, there were no
statistically significant changes in OHIP-49 domain and summary scores at any timepoint in the
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DISCUSSION
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Assessment of the impact of diseases on daily living and quality of life is an important
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component of modern healthcare, and patient-centred outcomes are likely to be more relevant to
patients than traditional clinical measures of disease. Previously, we have identified that (non-
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diabetic) patients with chronic periodontitis have significantly poorer OHRQoL than (non-
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diabetic) patients who do not have periodontitis, with, in particular, functional, physical,
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psychological impacts on their OHRQoL as a result of their periodontitis (12). Given the known
importance of diabetes as a major risk factor for periodontitis, and the nature of the interaction
between these two disease states (3), this study aimed to investigate the impact of periodontal
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When considering the data presented in Table 3, it is clear that when considering the overall
diabetic and non-diabetic patient populations (including patients with periodontal health,
gingivitis and chronic periodontitis), that T2DM did not have an impact on OHRQoL. A similar
finding has been reported previously, in which no impact of diabetes (both type 1 and type 2) on
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OHRQoL was noted (16). Although data from epidemiological studies indicate clearly that
diabetes increases the extent and severity of periodontitis (1), the severity of periodontitis in the
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T2DM patients in our study was very similar to that seen in the non-diabetic patients, with a
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slightly lower mean probing depth at baseline being observed in the T2DM group compared to
the non-diabetic patients (Table 2). Furthermore, the level of glycaemic control in the T2DM
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population was good (mean HbA1c 6.9 ± 2.7%). Thus, in our study it is clear that the T2DM
patients were not suffering from more advanced periodontitis than the non-diabetic control
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group, and therefore, it is perhaps unsurprising that OHRQoL scores did not differ between the
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When the patients were categorised according to periodontal status, we found that, similar to
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previous research (4, 12) OHRQoL was significantly poorer in the non-diabetic patients with
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gingivitis or periodontitis compared to those with periodontal health, in every domain of OHIP-
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49 as well as the overall summary scores (Table 4). However, by contrast, among the T2DM
patients, no significant differences were observed in OHRQoL between those with health,
gingivitis or periodontitis. This may be a function of the relatively small numbers of patients in
the various subgroups, but may potentially also indicate that patients with diabetes are less
concerned about the impact of their periodontal condition than they are about other health issues
that they must manage as part of their diabetes. Potentially, non-diabetic, systemically healthy
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individuals may be more concerned about the signs and symptoms of periodontitis than diabetic
individuals who are used to managing other comorbidities (and this may be reflected in the
finding of higher plaque, gingivitis and bleeding scores in the T2DM patients with periodontal
health and gingivitis compared to the corresponding non-diabetes groups). It has been identified
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that as chronic disease states have an increasing impact on individuals, then there is a tendency
for oral health to be prioritised less, particularly if the benefits of attaining oral health are
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perceived to be minimal (17). The need to balance a number of pressing health issues may lead
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to better coping with impacts of periodontitis, or indeed lower expectations of oral health. This
could be a reason for the finding that OHRQoL of patients with T2DM was not worse in people
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with periodontitis or gingivitis compared to those with healthy periodontal tissues. Further
A systematic review of the impact of periodontal therapy on OHRQoL has identified that non-
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surgical periodontal therapy can moderately improve OHRQoL (18). In our study, among the
OHIP-49 at months 3 and 6, and improvement in the psychological disability domain of OHIP-
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49 at month 6, compared to baseline, but no change in the overall OHIP-49 summary score as a
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result of treatment. This could be a result of many factors such as relatively small number of
patients, moderate periodontal disease at baseline (as opposed to very advanced disease),
relatively short follow-up period, poor sensitivity of the measurement tool to change, or
potentially because of the negative impacts that the requirement for ongoing maintenance and
management of chronic diseases can have on quality of life (19). Patients with chronic conditions
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into their daily life (20). The burden of measures they must take to improve their health
condition may prevent them from experiencing the benefits of the treatment they receive. This
may be a reason, at least in part, for the finding that in patients with T2DM, neither periodontal
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OHIP-49 has been used for many years to measure the impact of oral health status on quality of
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life. It has been assessed particularly in the context of prosthetic dentistry, but its utility in
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periodontal diseases and its sensitivity to detect meaningful change following treatment are yet
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may have yielded different results. Further research is warranted to identify whether there are
other tools (potentially yet to be developed) which may have better utility for investigating the
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impact of periodontal diseases on OHRQoL.
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CONCLUSION
T2DM does not impact on overall OHRQoL as measured by OHIP-49. Chronic periodontitis and
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gingivitis were associated with poorer OHRQoL in non-diabetic patients, with evidence of
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improvements following periodontal treatment, but no such effects were observed in patients
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with diabetes.
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Table
No Diabetes T2DM p
n=74 n=61
Gender: male n (%) 43 (58.1%) 40 (65.6%) NS
Age (years) (mean ± SD) 47.7 ±7.4 48.2 ± 6.9 NS
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Ethnicity n (%)
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Caucasian 74 (100 %) 59 (96.7 %)
Black 0 1 (1.6 %) NS
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Asian 0 1 (1.6 %)
HbA1c (%) (mean ± SD) 5.5 ± 0.5 6.9 ± 2.7 < 0.001
Smoking Status n (%)
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Current 8 (10.8 %) 6 (9.8 %)
Ex 22 (29.7 %) 17 (27.9 %) NS
Never 44 (59.5 %) 38 (62.3 %)
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Pack years of smoking 15 (5.0 - 23.7) 15 (4.5 - 40.0) NS
T2DM; type 2 diabetes, NS; not significant.
Data are presented as either means ± SD, or as medians (interquartile range).
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Table 2 Periodontal data according to diabetes and periodontal status
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ND-H D-H p ND-G D-G p ND-P D-P p
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n=17 n=15 n=17 n=20 n=40 n=26
Month 0 PI 0.25 (0.00-0.48) 0.45 (0.41-0.79) <0.01 0.62 (0.47-0.75) 0.83 (0.66-0.90) <0.01 0.64 (0.41-0.80) 0.71 (0.58-0.89) NS
Month 3 PI 0.40 ± 0.37* 0.65 ± 0.31 <0.05
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Month 6 PI 0.35 (0.12-0.62)* 0.58 (0.41-0.72)* <0.05
Month 0 mGI 0.50 (0.25-0.95) 1.33 (0.58-1.83) <0.05 1.33 (0.87-1.64) 2.27 (1.79-2.76) <0.01 2.43 (2.12-2.70) 2.29 (1.68-2.79) NS
Month 3 mGI 1.55 ± 0.73* 1.68 ± 0.71* NS
Month 6 mGI 1.35 ± 0.71* 1.60 ± 0.57* NS
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Month 0 PD (mm) 1.59 ± 0.12 1.72 ± 0.21 NS 1.99 ± 0.29 2.09 ± 0.14 NS 2.97 ± 0.63 2.64 ± 0.56 <0.05
Month 3 PD (mm) 2.53 ±0.51* 2.32 ± 0.42* NS
Month 6 PD (mm) 2.50 ± 0.63* 2.23 ± 0.44* NS
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Month 0 BOP (%) 0.7 (0.0-2.6) 12.2 (0.9-14.0) <0.01 25 (17.7-36.9) 37.1 (25.9-48.6) <0.05 41.0 (28.5-51.4) 33.3 (17.7-51.8) NS
Month 3 BOP (%) 13.5 (9.5-24.9)* 14.2 (6.2-36.0)* NS
Month 6 BOP (%) 10.5 (7.0-23.6)* 8.6 (6.6-20.8)* NS
ND-H; no diabetes, periodontal health, ND-G; no diabetes, gingivitis, ND-P; no diabetes, periodontitis, D-H; diabetes, periodontal health, D-G;
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diabetes, gingivitis, D-P; diabetes, periodontitis, PI; plaque index, mGI; modified gingival index, PD; probing depth, BOP; bleeding on probing,
NS; not significant. Data are presented as either means ± SD, or as medians (interquartile range). P values show cross-sectional comparisons
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between no diabetes and diabetes groups within periodontal status categories. * p<0.05 when comparing scores at Month 3 and Month 6 to those at
Month 0 in the ND-P and D-P groups.
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Table 3 OHIP-49 scores in patients with and without diabetes at baseline (month 0)
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Physical disability 3.0 (0.2-6.2) 3.4 (1.8-12.3) NS
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Psychological disability 3.0 (0.8-7.0) 4.0 (1.0-7.5) NS
Social disability 0.0 (0.0-3.3) 0.0 (0.0-2.0) NS
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Handicap 0.0 (0.0-3.0) 1.0 (0.0-4.0) NS
Summary score 30.4 (16.8-51.0) 37.0 (19.5-61.0) NS
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T2DM; type 2 diabetes, NS; not significant.
Data are presented as medians (interquartile range).
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Table 4 OHIP-49 scores in patients with and without diabetes at baseline (month 0)
categorised by periodontal status
Functional limitation 4.0 (2.0 - 8.0) 10.0 (6.5 - 14.5)* 9.4 (6.0 - 12.8)**
Physical pain 6.0 (3.1 - 11.5) 10.0 (7.0 - 16.0)* 8.7 (6.3 - 14.8)*
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Psychological discomfort 2.0 (0.0 - 6.5) 7.0 (2.0 - 11.5)* 5.5 (3.0 - 10.0)*
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Physical disability 1.0 (0.0 - 4.0) 4.0 (1.2 - 12.7)* 3.2 (1.0 - 6.2)*
Psychological disability 1.0 (0.0 - 4.0) 4.0 (0.5 - 9.0)* 3.0 (1.0 - 7.0)*
Social disability 0.0 (0.0 - 0.0) 0.2 (0.0 - 4.5)* 1.0 (0.0 - 3.8)*
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Handicap 0.0 (0.0 - 0.0) 2.0 (0.0 - 5.5)* 0.5 (0.0 - 3.0)*
Summary score 11.1 (7.1 - 34.5) 41.0 (19.7 - 75.7)* 33.0 (19.9 - 52.5)**
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D-H D-G D-P
Functional limitation 6.0 (4.0 - 17.7) 8.7 (6.7 - 12.9) 12.5 (6.8 - 18.0)
Physical pain 10.0 (6.7 - 19.7) 9.2 (5.3 – 13.0) 12.0 (6.8 - 15.3)
Psychological discomfort 5.0 (0.0 - 15.0) 6.0 (3.0 - 8.5) 7.0 (2.0 - 10.3)
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Physical disability 2.0 (1.0 -12.6) 5.0 (2.0 - 10.0) 3.7 (2.1 - 14.0)
Psychological disability 4.0 (0.0 - 12.0) 4.2 (1.0 - 6.8) 3.5 (1.8 - 7.3)
Social disability 0.0 (0.0 - 5.0) 0.0 (0.0 - 1.0) 0.0 (0.0 - 2.0)
Handicap 1.0 (0.0 - 6.0) 1.0 (0.0 - 2.8) 1.5 (0.0 - 5.0)
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Summary score 28.0 (13.9 - 93.9) 37.1 (23.8 - 50.7) 44.9 (23.9 - 64.5)
ND-H; no diabetes, periodontal health, ND-G; no diabetes, gingivitis, ND-P; no diabetes, periodontitis,
D-H; diabetes, periodontal health, D-G; diabetes, gingivitis, D-P; diabetes, periodontitis. Data are
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Table 5 OHIP-49 scores in patients with periodontitis, and with and without diabetes at at
month 0, moth 3 and month 6
Functional limitation 8.4 (5.0 - 12.9) 9.4 (6.0 - 14.4) 6.4 (4.0 - 11.4)
Physical pain 8.3 (5.8 - 13.3) 9.4 (7.0 - 15.4) 9.1 (5.0 - 11.8)
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Psychological discomfort 6.0 (3.0 - 9.5) 4.0 (2.0 - 8.0)* 3.0 (1.0 - 7.0)*
ip
Physical disability 3.2 (0.6 - 6.2) 3.2 (1.0 - 8.6) 2.0 (0.4 - 5.1)
Psychological disability 3.0 (1.0 - 7.0) 2.0 (0.0 - 6.5) 1.0 (0.0 - 4.8)*
Social disability 0.0 (0.0 - 3.5) 1.0 (0.0 - 3.5) 0.0 (0.0 - 1.8)
cr
Handicap 0.0 (0.0 - 2.5) 1.0 (0.0 - 2.5) 0.0 (0.0 - 0.0)
Summary score 32.9 (19.9 - 50.9) 34.0 (16.5 - 53.5) 19.9 (12.2 - 38.9)
us
D-P0 D-P3 D-P6
Functional limitation 15.0 (8.0 - 18.0) 12.0 (8.0 - 19.0) 15.0 (5.5 – 16.0)
Physical pain 12.0 (10.0 - 16.0) 13.0 (11.0 - 17.0) 11.0 (7.0 – 13.0)
Psychological discomfort 8.0 (5.0 - 11.0) 7.0 (2.6 - 10.0) 6.0 (1.0 – 7.0)
an
Physical disability 4.0 (3.0 - 14.0) 5.0 (2.0 - 11.0) 5.0 (0.4 - 11.0)
Psychological disability 4.0 (3.0 - 8.0) 4.0 (2.0 - 9.0) 3.0 (0.0 - 9.0)
Social disability 0.0 (0.0 - 2.0) 2.0 (0.0 - 4.0) 0.0 (0.0 - 2.0)
Handicap 1.0 (0.0 - 5.0) 2.0 (0.0 - 6.0) 0.0 (0.0 - 2.0)
M
Summary score 55.0 (30.0 - 60.0) 52.4 (26.0 - 69.0) 40.0 (16.0 - 66.0)
ND-P0; no diabetes, periodontitis month 0, ND-P3; no diabetes, periodontitis month 3, ND-P6; no
diabetes, periodontitis month 6, D-P0; D-P0; diabetes, periodontitis month 0, D-P3; diabetes, periodontitis
d
month 3, D-P6; diabetes, periodontitis month 6. Data are presented as medians (interquartile range).
* p<0.05 for paired comparisons of month 3 and month 6 timepoints to baseline (month 0).
p te
ce
Ac
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