ORIGINAL Al-Khabbaz ARTICLE
Type 2 Diabetes Mellitus and Periodontal Disease Severity Areej K. Al-Khabbaza Purpose: The aim of this cross-sectional study was to determine whether type 2 diabetes is coupled with increased severity of periodontal destruction. Materials and Methods: A total of 80 subjects with type 2 diabetes and 78 healthy control subjects underwent a fullmouth periodontal examination. The study included dentate subjects with a minimum of 7 remaining teeth in each dental arch. Plaque score, bleeding on probing and clinical attachment loss were assessed. Results: Diabetic patients showed a significantly lower percent of plaque-positive surfaces (P = 0.02) with a significant increase in the number and the percent of sites with clinical attachment loss ≥ 3 mm compared to controls. In the logistic regression analysis, age and diabetes were found to be associated with having > 15% sites with clinical attachment loss > 5 mm. There was a significant correlation between diabetes duration and the severity of periodontal attachment loss. Conclusion: Patients with type 2 diabetes were at higher risk of having severe forms of periodontal disease compared with non-diabetic subjects. The results highlight the need for frequent supportive periodontal care for patients diagnosed with type 2 diabetes mellitus. Key words: diabetes complications, periodontal disease, type 2 diabetes mellitus Oral Health Prev Dent 2014;1:77-82
Submitted for publication: 29.07.12; accepted for publication: 02.01.13
doi: 10.3290/j.ohpd.a31223
D
iabetes mellitus (DM) is a clinically and genetically diverse group of disorders affecting the metabolism. The current classification of diabetes is based on the pathophysiology of each form of the disease (American Diabetes Association, 2008). Type 2 diabetes mellitus (T2DM) results from insulin resistance, which alter the use of endogenously produced insulin at the target cells; it is the most prevalent form and occurs mainly in adults. A growing body of evidence accentuates the strong association between diabetes and periodontal disease (PD) and literature reviews support a bidirectional relationship between diabetes mellitus and periodontal disease (Mealey and Oates, 2006; Taylor and Borgnakke, 2008). Several observational studies (Tsai et al, 2002; Lu and Yang, 2004; Mattout et al, 2006; Fernandes et al, 2009) have provided consistent evidence of greater preva
Assistant Professor, Division of Periodontics, Department of Surgical Sciences, Faculty of Dentistry, Kuwait University, Safat, Kuwait.
Correspondence: Dr Areej K Al-Khabbaz, Department of Surgical Sciences, Faculty of Dentistry, Kuwait University, P.O. Box 24923, Safat, Kuwait 13110. Tel: +965-9929-9448, Fax: +965-2532-6049. Email: [email protected]
Vol 12, No 1, 2014
alence of periodontal diseases among T2DM patients compared to healthy individuals. The Middle East is an important area on the map of diabetes mellitus, with high prevalence and incidence rates. According to the International Diabetes Federation, the recorded prevalence of DM in Kuwait was 14.6% in 2010, with the expectation of a dramatic increase in the future. As severe forms of periodontal diseases may lead to tooth loss due to extensive destruction of alveolar bone (Kaur et al, 2009), evaluating the severity level of periodontal disease in diabetic patients is another essential factor in order to provide the appropriate preventive strategies, treatment and supportive periodontal care. Because many of the previously conducted studies in this field have based in their periodontal assessment on partial clinical examination of the dentition (Sandberg et al, 2000; Tsai et al, 2002; Lu and Yang, 2004; Campus et al, 2005, Mattout et al, 2006; Fernandes et al, 2009; Kaur et al, 2009), there are various reported degrees of periodontal disease among diabetic patients. The aim of this study was thus to explore diabetes-related parameters that are associated with severe periodontal destruction.
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MATERIALS AND METHODS This cross-sectional study compared a random sample of T2DM patients with medically healthy controls. The study design was approved by the Ethics Review Committee of Kuwait University, Faculty of Dentistry, and conducted during 2008 and 2009 for a period of 6 months. Study subjects were informed about the aim of the study and its voluntary nature, and informed consent was obtained prior to enrollment. Inclusion criteria for the diabetic group were: an established diagnosis of T2DM for at least one year and the willingness to undergo a dental examination. General exclusion criteria included pregnancy, the need for antibiotic prophylaxis, less than seven teeth in each dental arch, a history of recent systemic antibiotic therapy and the wearing of orthodontic appliances. Diabetic patients were recruited from the Diabetes Clinics of the Ministry of Health in Kuwait City and the controls were recruited from the Dental Clinics of Kuwait University. The medical history of diabetic patients was obtained from their physicians and included the most recent reading of glycosylated hemoglobin HbA1c values, duration of diabetes and diagnosed diabetes complications. The control subjects were considered medically healthy based on their self-reported medical history that the patient was not on any medication and had never been told by a physician that he or she has diabetes or any other medical conditions. For all subjects, data were collected on age and gender, smoking history, last dental visit, oral hygiene practice and clinical periodontal findings. All patients received a comprehensive periodontal examination for fully erupted teeth except the third molars by using a standardised manual periodontal probe. Periodontal examination was performed by a periodontist (A.K.) following intra-examiner calibration. The calibrated examiner demonstrated clinical attachment loss measurements across a range of subjects who were recruited for the purpose of calibration and training at ± 1 mm 90% of the time. The periodontal assessment included clinical attachment loss (CAL), bleeding on probing (BOP) and plaque score. Clinical attachment loss – which represents the distance from the cementoenamel junction to the bottom of the periodontal pocket – was assessed on 6 surfaces per tooth (distobuccal, mid-buccal, mesiobuccal, distolingual, mid-lingual and mesiolingual). Plaque score was calculated according to the presence of bacterial plaque on 4 surfaces per tooth
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(distal, mid-buccal, mesial, mid-lingual/palatal) and was recorded as the percent of plaque-positive surfaces. The bleeding on probing score was used to evaluate the degree of gingival inflammation and was calculated according to the presence of bleeding on probing on 6 sites per tooth. Bleeding on probing was recorded as either present or absent within 30 s after probing, and was stated as the percent of bleeding sites. At the conclusion of the comprehensive clinical examination, each patient was informed of the clinical findings, oral hygiene instructions were given and the patients were referred for periodontal treatment as needed.
Statistical analysis Data were entered and analysed using SPSS software (Chicago, IL, USA), version 18. Descriptive statistics were generated for all the study variables. The chi-square test was performed to detect significant associations between categorical variables and Student’s t-test was used for continuous variables. Statistical analysis of clinical periodontal findings was performed to detect differences between diabetics and controls and to detect differences between diabetics with different duration of diabetes and complications. Since the presence of diabetic complications may reflect the level of diabetes control over a period of time, we considered the diabetic group with medical complications as diabetic patients with a history of poor metabolic control. This is more reliable than using the HbA1c reading at one time point. Binary logistic regression analysis was performed in order to examine which factors were significant in multivariate analysis after adjusting for confounding between effects. The regression model used the dependent variable ‘> 15% of sites with CAL ≥ 5 mm’. Independent variables entered in the model were age, gender, smoking and having T2DM. Statistical significance was set at P < 0.05. Association between the quantitative variables was assessed using Spearman’s correlation coefficient.
RESULTS A total of 158 patients, 80 with T2DM and 78 controls, participated in the study and were recruited according to the order of admission. The mean age and standard deviation of the participants were 49.65 and 10.58, respectively, with an age range
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of 30 to 68 years. Most of the type 2 diabetic patients were older patients. Table 1 presents the demographic characteristics, dental history and clinical findings of the study participants. No statistical difference was found between diabetic patients and controls in terms of gender distribution, with males comprising 31.0% of diabetics and 27.8% of controls (P = 0.628). A statistical difference was found between the two groups in terms of toothbrushing frequency. Both diabetic and control patients reported a very low frequency of den-
tal visits; only 45% of participants had visited a dentist during the preceding year. Although T2DM patients had a significantly lower mean plaque score than did non-diabetic patients (P = 0.03), diabetic patients had a significantly higher number and proportion of sites with CAL than did the controls (P ≤ 0.01). Table 2 represents the logistic regression analysis of factors associated with having more than 15% of sites with CAL ≥ 5 mm. Older age and T2DM were the most significant variables
Table 1 Demographic characteristics, dental history and periodontal findings Diabetics (N = 80)
Controls (N = 78)
P-value*
53.35 ± 8.60
46.28 ± 10.24
< 0.001
Gender Male Female
49 (31.0%) 31 (19.6%)
44 (27.8%) 34 (21.5%)
0.628
Smoking history Never smoked Current or past smoker
44 (27.8%) 36 (22.8%)
46 (29.1%) 32 (20.3%)
0.633
55 (34.8%) 25 (15.8%)
40 (25.3%) 38 (24.1%)
0.034
Interdental cleaning Yes No
29 (18.4%) 51 (32.3%)
17 (10.8%) 61 (38.6%)
0.055
Last dentist’s appointment During the last year Over 1 year ago
33 (20.9%) 47 (29.7%)
38 (24.1%) 40 (25.3)
0.424
Plaque score (%)
58.7 ± 34.7
69.5 ± 25.2
0.027
Bleeding on probing (%)
39.6 ± 30.6
38.6 ± 28.7
0.840
Number of sites with CAL 3–4 mm
61.2 ± 29.6
43.4 ± 23.0
< 0.01
% of sites with CAL 3–4 mm
42.6 ± 18.9
32.5 ± 15.5
< 0.01
Number of sites with CAL ≥ 5 mm
26.4 ± 27.6
13.1 ± 17.3
< 0.01
% of sites with CAL ≥ 5 mm
18.5 ± 19.8
10.7 ± 15.0
< 0.01
Variables Age
Toothbrushing per day ≥ twice per day < twice per day (once or occasionally)
Data presented as N (%) or mean ± SD (standard deviation), *chi-square (P < 0.05).
Table 2 Logistic regression analysis of factors associated with having >15% of periodontal sites with CAL ≥ 5 mm. Factor
B (Susanto et al)
Adjusted OR (95% CI)
P-value
Age
0.070 (0.021)
1.072 (1.028–1.118)
0.001
Gender
-0.060 (0.417)
0.942 (0.416–2.124)
0.886
Diabetes
0.972 (0.390)
2.643 (1.231–5.675)
0.013
Smoking
0.312 (0.409)
1.366 (0.613–3.045)
0.445
B = coefficient.
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Table 3 Descriptive statistics of clinical periodontal findings among diabetic patients Duration of diabetes
Variables
≤ 10 years N = 43 Mean ± SD
> 10 years N = 37 Mean ± SD
No. of sites with CAL 3–4 mm
56.6 ± 30.1
% of sites with CAL 3–4 mm
Diabetes complications†
P-value
No complications N = 60 Mean ± SD
≥ 1 complication N = 20 Mean ± SD
P-value
70.3 ± 28.4
0.056
56.3 ± 29.3
76.9 ± 25.1
0.004
37.1 ± 17.9
48.0 ± 17.7
0.014
39.4 ± 19.3
51.8 ± 14.5
0.004
No. of sites with CAL ≥ 5 mm
21.2 ± 29.7
35.0 ± 27.2
0.050
25.5 ± 28.7
29.0 ± 24.8
0.607
% of sites with CAL ≥ 5 mm
14.5 ± 22.7
24.0 ± 18.5
0.066
17.8 ± 20.3
20.6 ± 18.7
0.574
*(P< 0.05). †Diabetes complications: retinopathy, neuropathy and nephropathy.
associated with having more sites with severe periodontal destruction. Concerning diabetes control, the HbA1C % value was more than 9% in 28.8% of T2DM patients. Regarding diabetes duration, 37 (46.3%) of the diabetic patients had a diagnosis of type 2 diabetes for more than 10 years. In terms of diabetes complications, 20 patients had been diagnosed with at least one diabetes complication: 12 patients had neuropathy, 8 retinopathy and 5 nephropathy (5 subjects had more than one complication). Most of the diabetic patients with medical complications (70%) had a diagnosis of T2DM for more than 10 years. The mean values of variables describing the clinical periodontal condition among diabetics with different durations of diabetes and diabetes complications are presented in Table 3. Patients diagnosed with T2DM with more than 10 years duration and with diabetes complications had significantly more sites with 3–4 mm of CAL. However, a longer duration of diabetes tended to be associated with a higher number of sites with CAL ≥ 5 mm, but this was not statistically significant. The interaction between T2DM duration and the number of diagnosed medical complications with severe periodontal attachment loss is presented in Fig 1. These interactions were also confirmed by correlation testing: the duration of diabetes was significantly correlated with an increased percentage of sites with CAL ≥ 5 mm (r = 0.321; P = 0.007).
DISCUSSION The major strength of this study over previously conducted research is the comprehensive periodontal assessment including 6 sites per tooth and the independent presentation of the number and
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percent of sites with moderate and severe clinical attachment loss. Moreover, our study sample included dentate subjects with a minimum of 7 remaining teeth in each dental arch; edentulous patients were excluded in order to minimise the dilution effect of complete tooth loss on the study results. In this study, although the majority of T2DM patients reported brushing their teeth at least twice a day and they had significantly lower mean plaque scores compared to controls, diabetics had the same mean bleeding score as non-diabetic patients (Table 1). This finding indicates that patients diagnosed with T2DM may have more pronounced periodontal inflammation compared with healthy individuals given the same amount of plaque accumulation. It was suggested earlier that the inflammatory process may play a role in the development and progression of type 2 diabetes (King, 2008), especially because increases in inflammatory markers were detected in apparently healthy individuals who later developed type 2 diabetes mellitus (Pradhan et al, 2001; Thorand et al, 2003). Additionally, diabetics might harbour more aggressive bacterial species than non-diabetic subjects. Campus et al (2005) obtained subgingival plaque samples from 71 patients diagnosed with type 2 diabetes and compared them with samples from healthy individuals. P. gingivalis and T. forsythensis were significantly positively associated with diabetes. Other authors (Grossi, 2001; Dogan et al, 2003) also found these pathogens to be clearly associated with periodontal disease. Therefore, Type 2 diabetes patients may suffer from periodontal disease to the same or greater extent than control subjects, even with lower amounts of bacterial growth (plaque). The present data show that patients with type 2 diabetes had a significantly higher mean number
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Al-Khabbaz
Mean % sites with CAL ≥ 5 mm
40
30
20
10
0 no complications
one complication
2 or more complications
Fig 1 Relationship between severe attachment loss and medical complications.
and percent of sites with clinical attachment loss ≥ 3 mm compared to non-diabetic patients, and the differences between the two groups almost doubled for sites with clinical attachment loss ≥ 5 mm (Table 1). Furthermore, the prevalence of sites with moderate to severe CAL increases with longer duration of diabetes, with a significant correlation between the duration of diabetes and percent of sites with ≥ 5 mm of CAL (Table 3). The comparison between type 2 diabetes mellitus and non-diabetic patients demonstrated that the periodontal disease severity level was significantly higher in the type 2 diabetes mellitus group, confirming the data of Sunsanto et al (2011), which were based on full-mouth periodontal assessment. Other studies have also reported significantly poorer periodontal health in adult subjects with type 2 diabetes compared to non-diabetic individuals in other parts of the world (Taylor et al, 1998; Sandberg et al, 2000; Lu and Yang, 2004; Campus et al, 2005; Mattout et al, 2006; Kaur et al, 2009; Susanto et al, 2011). Severe periodontal disease has been associated with tooth loss and reported as more prevalent among people with diabetes than among those without diabetes (Al-Shammari et al, 2005; Kapp et al, 2007). A study by Jansson et al (2006) reported that patients with type 2 diabetes and periodontal disease had a significantly lower mean number of teeth than did type 2 diabetes patients but without periodontal disease. The consequences of periodontal disease and subsequent tooth loss
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are not only important considerations for the quality of life of patients with diabetes, but they may significantly affect overall health by compromising a patient’s ability to maintain a healthy diet and a proper glycemic control. Although the relationship between type 2 diabetes and tooth loss due to periodontal disease is complicated by the fact that T2DM onset generally occurs in middle to late age, coinciding with the point when periodontal disease also becomes more prevalent, it is still very important to control the effect of diabetes on periodontal health. In this study, having at least one diabetic complication was also significantly associated with having more sites with 3–4 mm of CAL. One possible explanation is that severe forms of periodontal destruction may increase in diabetic individuals with more advanced systemic complication due to their uncontrolled diabetic condition (Löe, 1993, Moore et al, 2000). Although the data of our study are cross sectional and a causal association between medical complications and periodontal disease cannot be concluded, the results indicate that severe periodontal disease could be used as a predictor for early recognition of diabetic complications or the presence of an uncontrolled diabetic condition. Additional longitudinal clinical studies are essential to confirm such a relationship. A recent report from the longitudinal study of diabetes and its complications in the Gila River Indian Community in Arizona have shown that individuals with severe periodontal disease had 3.2 times greater risk for cardiorenal mortality (Saremi et al, 2005). Moreover, periodontitis and edentulism were significantly associated with overt neuropathy and end-stage renal disease (Shultis et al, 2007).
CONCLUSION The present study demonstrated an association between type 2 diabetes and an increased severity of periodontal disease compared with non-diabetic subjects. Patients diagnosed with type 2 diabetes might be susceptible to advanced forms of periodontal disease. Based on the current observations, periodontal disease is an important complication of diabetes mellitus and periodontal supportive periodontal treatment should be an integral part of the medical management of diabetes mellitus patients.
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REFERENCES 1. American Diabetes Association Position Statement. Diagnosis and classification of diabetes mellitus. Diabetes Care 2008;31(suppl 1):S55–60. 2. Al-Shammari KF, Al-Khabbaz AK, Al-Ansari JM, Neiva R, Wang HL. Risk indicators for tooth loss due to periodontal disease. J Periodontol 2005;76:1910–1918. 3. Campus G, Salem A, Uzzau S, Baldoni E, Tonolo G. Diabetes and periodontal disease: a case-control study. J Periodontol 2005;76:418–425. 4. Dogan B, Antiheimo J, Cetiner D, Bodur A, Emingil G, Buduneli E, Uygur C, Firatli E, Lakio L, Asikainen S. Subgingival microflora in Turkish patients with periodontitis. J Periodontol 2003;74:803–814. 5. Fernandes JK, Wiegand RE, Salinas CF, Grossi SG, Sander JJ, Lopes-Virella MF, Slate EH. Periodontal disease status in gullah African Americans with type 2 diabetes living in South Carolina. J Periodontol 2009;80:1062–1068. 6. Grossi SG. Treatment of periodontal disease and control of diabetes: an assessment of the evidence and need for future research. Ann Periodontol 2001;6:138–145. 7. Jansson H, Lindholme E, Lindh C, Groop L, Bratthall G. Type 2 diabetes and risk for periodontal disease: a role for dental health awareness. J Clin Periodontol 2006;33:408–414. 8. Kapp JM, Boren SA, Yun S, Lemaster J. Diabetes and tooth loss in a national sample of dentate adults reporting annual dental visits. Prev Chronic Dis 2007;4:A59. 9. Kaur G, Holtfreter B, Rathmann W, Schwahn C, Wallaschofski H, Schipf S, Nauck M, Kocher T. Association between type 1 and type 2 diabetes with periodontal disease and tooth loss. J Clin Periodontol 2009;36:765–774. 10. King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol 2008;79:1527–1534. 11. Löe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329–334. 12. Lu HK, Yang PC. Cross-sectional analysis of different variables of patients with non-insulin dependent diabetes and their periodontal status. Int J Periodontics Restorative Dent 2004;24:71–79.
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13. Mattout C, Bourgeois D, Bouchard P. Type 2 diabetes and periodontal indicators: epidemiology in France 2002– 2003. J Periodontal Res 2006;41:253–258. 14. Mealey BL, Oates TW. Diabetes mellitus and periodontal diseases. J Periodontol 2006;77:1289–1303. 15. Moore PA, Orchard T, Guggenheimer J, Weyant RJ. Diabetes and oral health promotion: a survey of disease prevention behaviors. J Am Dent Assoc 2000131:1333–1341. 16. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. Creactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001;286:327–334. 17. Sandberg GE, Sunderberg HE, Fjellstrom CA, Wikblad KF. Type 2 diabetes and oral health: a comparison between diabetic and non-diabetic subjects. Diabetes Res Clin Pract2000;50:27–34. 18. Saremi A, Nelson RG, Tulloch-Reid M, Hanson RL, Sievers ML, Taylor GW, Shlossman M, Bennett PH, Genco R, Knowler WC. Periodontal disease and mortality in type 2 diabetes. Diabetes Care 2005;28:27–32. 19. Shultis WA, Weil EJ, Looker HC, Curtis JM, Shlossman M, Genco RJ, Knowler WC, Nelson RG. Effect of periodontitis on overt nephropathy and end-stage renal disease in type 2 diabetes. Diabetes Care 2007;30:306–11. 20. Susanto H, Nesse W, Dijkstra PU, Agustina D, Vissink A, Abbas F. Periodontitis prevalence and severity in Indonesians with type 2 diabetes. J Periodontol 2011;82:550–557. 21. Taylor GW, Borgnakke WS. Periodontal disease: associations with diabetes, glycemic control and complications. Oral Dis 2008;14:191–203. 22. Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, Pettitt DJ. Non-insulin dependent diabetes mellitus and alveolar bone loss progression over 2 years. J Periodontol 1998;69:76–83. 23. Thorand B, Lowel H, Schneider A, Kolb H, Meisinger C, Fröhlich M, König W. 2003. C-reactive protein as a predictor for incident diabetes mellitus among middle-aged men: results from the MONICA Augsburg cohort study, 1984– 1998. Arch Intern Med 2003;163:93–99. 24. Tsai C, Hayes C, Taylor GW. Glycemic control of type 2 diabetes and severe periodontal disease in the US adult population. Community Dent Oral Epidemiol 2002;30:182–192.
Oral Health & Preventive Dentistry
Type 2 Diabetes Mellitus and Periodontal Disease Severity Areej K. Al-Khabbaza Purpose: The aim of this cross-sectional study was to determine whether type 2 diabetes is coupled with increased severity of periodontal destruction. Materials and Methods: A total of 80 subjects with type 2 diabetes and 78 healthy control subjects underwent a fullmouth periodontal examination. The study included dentate subjects with a minimum of 7 remaining teeth in each dental arch. Plaque score, bleeding on probing and clinical attachment loss were assessed. Results: Diabetic patients showed a significantly lower percent of plaque-positive surfaces (P = 0.02) with a significant increase in the number and the percent of sites with clinical attachment loss ≥ 3 mm compared to controls. In the logistic regression analysis, age and diabetes were found to be associated with having > 15% sites with clinical attachment loss > 5 mm. There was a significant correlation between diabetes duration and the severity of periodontal attachment loss. Conclusion: Patients with type 2 diabetes were at higher risk of having severe forms of periodontal disease compared with non-diabetic subjects. The results highlight the need for frequent supportive periodontal care for patients diagnosed with type 2 diabetes mellitus. Key words: diabetes complications, periodontal disease, type 2 diabetes mellitus Oral Health Prev Dent 2014;1:77-82
Submitted for publication: 29.07.12; accepted for publication: 02.01.13
doi: 10.3290/j.ohpd.a31223
D
iabetes mellitus (DM) is a clinically and genetically diverse group of disorders affecting the metabolism. The current classification of diabetes is based on the pathophysiology of each form of the disease (American Diabetes Association, 2008). Type 2 diabetes mellitus (T2DM) results from insulin resistance, which alter the use of endogenously produced insulin at the target cells; it is the most prevalent form and occurs mainly in adults. A growing body of evidence accentuates the strong association between diabetes and periodontal disease (PD) and literature reviews support a bidirectional relationship between diabetes mellitus and periodontal disease (Mealey and Oates, 2006; Taylor and Borgnakke, 2008). Several observational studies (Tsai et al, 2002; Lu and Yang, 2004; Mattout et al, 2006; Fernandes et al, 2009) have provided consistent evidence of greater preva
Assistant Professor, Division of Periodontics, Department of Surgical Sciences, Faculty of Dentistry, Kuwait University, Safat, Kuwait.
Correspondence: Dr Areej K Al-Khabbaz, Department of Surgical Sciences, Faculty of Dentistry, Kuwait University, P.O. Box 24923, Safat, Kuwait 13110. Tel: +965-9929-9448, Fax: +965-2532-6049. Email: [email protected]
Vol 12, No 1, 2014
alence of periodontal diseases among T2DM patients compared to healthy individuals. The Middle East is an important area on the map of diabetes mellitus, with high prevalence and incidence rates. According to the International Diabetes Federation, the recorded prevalence of DM in Kuwait was 14.6% in 2010, with the expectation of a dramatic increase in the future. As severe forms of periodontal diseases may lead to tooth loss due to extensive destruction of alveolar bone (Kaur et al, 2009), evaluating the severity level of periodontal disease in diabetic patients is another essential factor in order to provide the appropriate preventive strategies, treatment and supportive periodontal care. Because many of the previously conducted studies in this field have based in their periodontal assessment on partial clinical examination of the dentition (Sandberg et al, 2000; Tsai et al, 2002; Lu and Yang, 2004; Campus et al, 2005, Mattout et al, 2006; Fernandes et al, 2009; Kaur et al, 2009), there are various reported degrees of periodontal disease among diabetic patients. The aim of this study was thus to explore diabetes-related parameters that are associated with severe periodontal destruction.
77
Al-Khabbaz
MATERIALS AND METHODS This cross-sectional study compared a random sample of T2DM patients with medically healthy controls. The study design was approved by the Ethics Review Committee of Kuwait University, Faculty of Dentistry, and conducted during 2008 and 2009 for a period of 6 months. Study subjects were informed about the aim of the study and its voluntary nature, and informed consent was obtained prior to enrollment. Inclusion criteria for the diabetic group were: an established diagnosis of T2DM for at least one year and the willingness to undergo a dental examination. General exclusion criteria included pregnancy, the need for antibiotic prophylaxis, less than seven teeth in each dental arch, a history of recent systemic antibiotic therapy and the wearing of orthodontic appliances. Diabetic patients were recruited from the Diabetes Clinics of the Ministry of Health in Kuwait City and the controls were recruited from the Dental Clinics of Kuwait University. The medical history of diabetic patients was obtained from their physicians and included the most recent reading of glycosylated hemoglobin HbA1c values, duration of diabetes and diagnosed diabetes complications. The control subjects were considered medically healthy based on their self-reported medical history that the patient was not on any medication and had never been told by a physician that he or she has diabetes or any other medical conditions. For all subjects, data were collected on age and gender, smoking history, last dental visit, oral hygiene practice and clinical periodontal findings. All patients received a comprehensive periodontal examination for fully erupted teeth except the third molars by using a standardised manual periodontal probe. Periodontal examination was performed by a periodontist (A.K.) following intra-examiner calibration. The calibrated examiner demonstrated clinical attachment loss measurements across a range of subjects who were recruited for the purpose of calibration and training at ± 1 mm 90% of the time. The periodontal assessment included clinical attachment loss (CAL), bleeding on probing (BOP) and plaque score. Clinical attachment loss – which represents the distance from the cementoenamel junction to the bottom of the periodontal pocket – was assessed on 6 surfaces per tooth (distobuccal, mid-buccal, mesiobuccal, distolingual, mid-lingual and mesiolingual). Plaque score was calculated according to the presence of bacterial plaque on 4 surfaces per tooth
78
(distal, mid-buccal, mesial, mid-lingual/palatal) and was recorded as the percent of plaque-positive surfaces. The bleeding on probing score was used to evaluate the degree of gingival inflammation and was calculated according to the presence of bleeding on probing on 6 sites per tooth. Bleeding on probing was recorded as either present or absent within 30 s after probing, and was stated as the percent of bleeding sites. At the conclusion of the comprehensive clinical examination, each patient was informed of the clinical findings, oral hygiene instructions were given and the patients were referred for periodontal treatment as needed.
Statistical analysis Data were entered and analysed using SPSS software (Chicago, IL, USA), version 18. Descriptive statistics were generated for all the study variables. The chi-square test was performed to detect significant associations between categorical variables and Student’s t-test was used for continuous variables. Statistical analysis of clinical periodontal findings was performed to detect differences between diabetics and controls and to detect differences between diabetics with different duration of diabetes and complications. Since the presence of diabetic complications may reflect the level of diabetes control over a period of time, we considered the diabetic group with medical complications as diabetic patients with a history of poor metabolic control. This is more reliable than using the HbA1c reading at one time point. Binary logistic regression analysis was performed in order to examine which factors were significant in multivariate analysis after adjusting for confounding between effects. The regression model used the dependent variable ‘> 15% of sites with CAL ≥ 5 mm’. Independent variables entered in the model were age, gender, smoking and having T2DM. Statistical significance was set at P < 0.05. Association between the quantitative variables was assessed using Spearman’s correlation coefficient.
RESULTS A total of 158 patients, 80 with T2DM and 78 controls, participated in the study and were recruited according to the order of admission. The mean age and standard deviation of the participants were 49.65 and 10.58, respectively, with an age range
Oral Health & Preventive Dentistry
Al-Khabbaz
of 30 to 68 years. Most of the type 2 diabetic patients were older patients. Table 1 presents the demographic characteristics, dental history and clinical findings of the study participants. No statistical difference was found between diabetic patients and controls in terms of gender distribution, with males comprising 31.0% of diabetics and 27.8% of controls (P = 0.628). A statistical difference was found between the two groups in terms of toothbrushing frequency. Both diabetic and control patients reported a very low frequency of den-
tal visits; only 45% of participants had visited a dentist during the preceding year. Although T2DM patients had a significantly lower mean plaque score than did non-diabetic patients (P = 0.03), diabetic patients had a significantly higher number and proportion of sites with CAL than did the controls (P ≤ 0.01). Table 2 represents the logistic regression analysis of factors associated with having more than 15% of sites with CAL ≥ 5 mm. Older age and T2DM were the most significant variables
Table 1 Demographic characteristics, dental history and periodontal findings Diabetics (N = 80)
Controls (N = 78)
P-value*
53.35 ± 8.60
46.28 ± 10.24
< 0.001
Gender Male Female
49 (31.0%) 31 (19.6%)
44 (27.8%) 34 (21.5%)
0.628
Smoking history Never smoked Current or past smoker
44 (27.8%) 36 (22.8%)
46 (29.1%) 32 (20.3%)
0.633
55 (34.8%) 25 (15.8%)
40 (25.3%) 38 (24.1%)
0.034
Interdental cleaning Yes No
29 (18.4%) 51 (32.3%)
17 (10.8%) 61 (38.6%)
0.055
Last dentist’s appointment During the last year Over 1 year ago
33 (20.9%) 47 (29.7%)
38 (24.1%) 40 (25.3)
0.424
Plaque score (%)
58.7 ± 34.7
69.5 ± 25.2
0.027
Bleeding on probing (%)
39.6 ± 30.6
38.6 ± 28.7
0.840
Number of sites with CAL 3–4 mm
61.2 ± 29.6
43.4 ± 23.0
< 0.01
% of sites with CAL 3–4 mm
42.6 ± 18.9
32.5 ± 15.5
< 0.01
Number of sites with CAL ≥ 5 mm
26.4 ± 27.6
13.1 ± 17.3
< 0.01
% of sites with CAL ≥ 5 mm
18.5 ± 19.8
10.7 ± 15.0
< 0.01
Variables Age
Toothbrushing per day ≥ twice per day < twice per day (once or occasionally)
Data presented as N (%) or mean ± SD (standard deviation), *chi-square (P < 0.05).
Table 2 Logistic regression analysis of factors associated with having >15% of periodontal sites with CAL ≥ 5 mm. Factor
B (Susanto et al)
Adjusted OR (95% CI)
P-value
Age
0.070 (0.021)
1.072 (1.028–1.118)
0.001
Gender
-0.060 (0.417)
0.942 (0.416–2.124)
0.886
Diabetes
0.972 (0.390)
2.643 (1.231–5.675)
0.013
Smoking
0.312 (0.409)
1.366 (0.613–3.045)
0.445
B = coefficient.
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Table 3 Descriptive statistics of clinical periodontal findings among diabetic patients Duration of diabetes
Variables
≤ 10 years N = 43 Mean ± SD
> 10 years N = 37 Mean ± SD
No. of sites with CAL 3–4 mm
56.6 ± 30.1
% of sites with CAL 3–4 mm
Diabetes complications†
P-value
No complications N = 60 Mean ± SD
≥ 1 complication N = 20 Mean ± SD
P-value
70.3 ± 28.4
0.056
56.3 ± 29.3
76.9 ± 25.1
0.004
37.1 ± 17.9
48.0 ± 17.7
0.014
39.4 ± 19.3
51.8 ± 14.5
0.004
No. of sites with CAL ≥ 5 mm
21.2 ± 29.7
35.0 ± 27.2
0.050
25.5 ± 28.7
29.0 ± 24.8
0.607
% of sites with CAL ≥ 5 mm
14.5 ± 22.7
24.0 ± 18.5
0.066
17.8 ± 20.3
20.6 ± 18.7
0.574
*(P< 0.05). †Diabetes complications: retinopathy, neuropathy and nephropathy.
associated with having more sites with severe periodontal destruction. Concerning diabetes control, the HbA1C % value was more than 9% in 28.8% of T2DM patients. Regarding diabetes duration, 37 (46.3%) of the diabetic patients had a diagnosis of type 2 diabetes for more than 10 years. In terms of diabetes complications, 20 patients had been diagnosed with at least one diabetes complication: 12 patients had neuropathy, 8 retinopathy and 5 nephropathy (5 subjects had more than one complication). Most of the diabetic patients with medical complications (70%) had a diagnosis of T2DM for more than 10 years. The mean values of variables describing the clinical periodontal condition among diabetics with different durations of diabetes and diabetes complications are presented in Table 3. Patients diagnosed with T2DM with more than 10 years duration and with diabetes complications had significantly more sites with 3–4 mm of CAL. However, a longer duration of diabetes tended to be associated with a higher number of sites with CAL ≥ 5 mm, but this was not statistically significant. The interaction between T2DM duration and the number of diagnosed medical complications with severe periodontal attachment loss is presented in Fig 1. These interactions were also confirmed by correlation testing: the duration of diabetes was significantly correlated with an increased percentage of sites with CAL ≥ 5 mm (r = 0.321; P = 0.007).
DISCUSSION The major strength of this study over previously conducted research is the comprehensive periodontal assessment including 6 sites per tooth and the independent presentation of the number and
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percent of sites with moderate and severe clinical attachment loss. Moreover, our study sample included dentate subjects with a minimum of 7 remaining teeth in each dental arch; edentulous patients were excluded in order to minimise the dilution effect of complete tooth loss on the study results. In this study, although the majority of T2DM patients reported brushing their teeth at least twice a day and they had significantly lower mean plaque scores compared to controls, diabetics had the same mean bleeding score as non-diabetic patients (Table 1). This finding indicates that patients diagnosed with T2DM may have more pronounced periodontal inflammation compared with healthy individuals given the same amount of plaque accumulation. It was suggested earlier that the inflammatory process may play a role in the development and progression of type 2 diabetes (King, 2008), especially because increases in inflammatory markers were detected in apparently healthy individuals who later developed type 2 diabetes mellitus (Pradhan et al, 2001; Thorand et al, 2003). Additionally, diabetics might harbour more aggressive bacterial species than non-diabetic subjects. Campus et al (2005) obtained subgingival plaque samples from 71 patients diagnosed with type 2 diabetes and compared them with samples from healthy individuals. P. gingivalis and T. forsythensis were significantly positively associated with diabetes. Other authors (Grossi, 2001; Dogan et al, 2003) also found these pathogens to be clearly associated with periodontal disease. Therefore, Type 2 diabetes patients may suffer from periodontal disease to the same or greater extent than control subjects, even with lower amounts of bacterial growth (plaque). The present data show that patients with type 2 diabetes had a significantly higher mean number
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Mean % sites with CAL ≥ 5 mm
40
30
20
10
0 no complications
one complication
2 or more complications
Fig 1 Relationship between severe attachment loss and medical complications.
and percent of sites with clinical attachment loss ≥ 3 mm compared to non-diabetic patients, and the differences between the two groups almost doubled for sites with clinical attachment loss ≥ 5 mm (Table 1). Furthermore, the prevalence of sites with moderate to severe CAL increases with longer duration of diabetes, with a significant correlation between the duration of diabetes and percent of sites with ≥ 5 mm of CAL (Table 3). The comparison between type 2 diabetes mellitus and non-diabetic patients demonstrated that the periodontal disease severity level was significantly higher in the type 2 diabetes mellitus group, confirming the data of Sunsanto et al (2011), which were based on full-mouth periodontal assessment. Other studies have also reported significantly poorer periodontal health in adult subjects with type 2 diabetes compared to non-diabetic individuals in other parts of the world (Taylor et al, 1998; Sandberg et al, 2000; Lu and Yang, 2004; Campus et al, 2005; Mattout et al, 2006; Kaur et al, 2009; Susanto et al, 2011). Severe periodontal disease has been associated with tooth loss and reported as more prevalent among people with diabetes than among those without diabetes (Al-Shammari et al, 2005; Kapp et al, 2007). A study by Jansson et al (2006) reported that patients with type 2 diabetes and periodontal disease had a significantly lower mean number of teeth than did type 2 diabetes patients but without periodontal disease. The consequences of periodontal disease and subsequent tooth loss
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are not only important considerations for the quality of life of patients with diabetes, but they may significantly affect overall health by compromising a patient’s ability to maintain a healthy diet and a proper glycemic control. Although the relationship between type 2 diabetes and tooth loss due to periodontal disease is complicated by the fact that T2DM onset generally occurs in middle to late age, coinciding with the point when periodontal disease also becomes more prevalent, it is still very important to control the effect of diabetes on periodontal health. In this study, having at least one diabetic complication was also significantly associated with having more sites with 3–4 mm of CAL. One possible explanation is that severe forms of periodontal destruction may increase in diabetic individuals with more advanced systemic complication due to their uncontrolled diabetic condition (Löe, 1993, Moore et al, 2000). Although the data of our study are cross sectional and a causal association between medical complications and periodontal disease cannot be concluded, the results indicate that severe periodontal disease could be used as a predictor for early recognition of diabetic complications or the presence of an uncontrolled diabetic condition. Additional longitudinal clinical studies are essential to confirm such a relationship. A recent report from the longitudinal study of diabetes and its complications in the Gila River Indian Community in Arizona have shown that individuals with severe periodontal disease had 3.2 times greater risk for cardiorenal mortality (Saremi et al, 2005). Moreover, periodontitis and edentulism were significantly associated with overt neuropathy and end-stage renal disease (Shultis et al, 2007).
CONCLUSION The present study demonstrated an association between type 2 diabetes and an increased severity of periodontal disease compared with non-diabetic subjects. Patients diagnosed with type 2 diabetes might be susceptible to advanced forms of periodontal disease. Based on the current observations, periodontal disease is an important complication of diabetes mellitus and periodontal supportive periodontal treatment should be an integral part of the medical management of diabetes mellitus patients.
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