Diabetes & Metabolic Syndrome: Clinical Research & Reviews 3 (2009) 192197

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Diabetes & Metabolic Syndrome: Clinical Research & Reviews

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Original paper

Oral health in Thai patients with metabolic syndrome

Umawadee Chomkhakhai a,1, Supanee Thanakun b,*, Siribang-on Piboonniyom Khovidhunkit c,2, Weerapan Khovidhunkit d,3, Sroisiri Thaweboon e,4
a

Dental practitioner, Anundamahidol Hospital, Mueng, Lopburee 15000, Thailand Department of Oral Medicine, Faculty of Dentistry, Mahidol University, 6 Yodhi, Rajthewee, Bangkok 10400, Thailand c Department of Hospital Dentistry, Faculty of Dentistry, Mahidol University, 6 Yodhi, Rajthewee, Bangkok 10400, Thailand d Department of Medicine, Faculty of Medicine Chulalongkorn University Bangkok 10330, Thailand e Department of Oral Microbiology, Faculty of Dentistry, Mahidol University, 6 Yodhi, Rajthewee, Bangkok 10400, Thailand
b

A R T I C L E I N F O

A B S T R A C T

Keywords: Oral health Metabolic syndrome Dry mouth Oral microora

Aim: To study the prevalence of oral manifestations, xerostomia, hyposalivation and level of oral microora in a group of Thai patients with metabolic syndrome (MS) and to determine if there is any association between MS and these oral health components. Methods: Data including patients histories, general health, dental and periodontal status, oral mucosal manifestations, xerostomia, hyposalivation and oral microora in 369 patients with MS were collected and statistically analyzed. Results: Ninety-four subjects (25.5%) were men and 275 (74.5%) were women, with age range from 32 to 88 years (mean = 63.9 10.4). Of these, 231 patients (62.6%) were older than 60 years old. Dental caries in at least 1 tooth and periodontitis were found in 184 (49.9%) and 192 (52.0%) patients, respectively. Oral mucosal manifestations were found in 203 patients (55.0%). The most prevalent manifestation was ssured tongue (41.5%), followed by denture stomatitis (9.2%) and depapillated tongue (3.0%). Dry mucosa was depicted in 203 patients (55.0%). Xerostomia was revealed in 157 patients (42.5%) while hyposalivation was detected in 202 patients (54.7%). Twenty four percent of patients had high Candida level. Signicant association was found between Candida level and hyposalivation and also hyposalivation, xerostomia and dry mucosa. Conclusions: Approximately half of the patients with metabolic syndrome presented with dental caries, periodontitis, dry mouth, oral mucosal changes and approximately one fourth had high Candida level. 2009 Diabetes India. Published by Elsevier Ltd. All rights reserved.

1. Introduction Metabolic syndrome (MS) is a group of interrelated components that predispose individual to increased risk for type2 diabetes mellitus (DM) and cardiovascular disease (CVD). The International Diabetes Federation (IDF) has proposed a denition of MS in order to use for clinical practice and epidemiologic studies [1]. Central obesity, determined by waist circumference, is a prerequisite criterion for the diagnosis of the MS. The minimal waist circumference varies from 90 to 102 centimeters (cm) in males and from 80 to 88 cm in females depending on ethnic group [1]. The MS can be diagnosed when central obesity plus any two of the

* Corresponding author. Tel.: +66 2 203 6500; fax: +66 2 203 6504. E-mail addresses: dtstn@mahidol.ac.th (S. Thanakun), dtspb@mahidol.ac.th (S.-o. Khovidhunkit), wkhovid@gmail.com (W. Khovidhunkit), dtstw@mahidol.ac.th (S. Thaweboon). 1 Tel.: +66 1 802 0840; fax: +66 36 427 401. 2 Tel.: +66 2 203 6530; fax: +66 2 203 6530. 3 Tel.: +66 2 256 4101; fax: +66 2 652 5347. 4 Tel.: +66 2 203 6410; fax: +66 2 203 6410.

following four factors are present. These include raised triglycerides (TG) level (!150 mg/dL, or specic treatment for this lipid abnormality), reduced high density lipoprotein cholesterol (HDLC) (<40 mg/dL in males, and <50 mg/dL in females, or specic treatment for this lipid abnormality), or raised blood pressure (BP) (systolic BP ! 130 or diastolic BP ! 85 mmHg, or treatment of previously diagnosed hypertension) and raised fasting plasma glucose (FPG) (!100 mg/dL, or previously diagnosed type2 DM) [1]. In Thailand, the prevalence of MS varies from 15 to 20% among various population groups which is comparable to those in developed countries [24]. Many drugs used in the treatment of MS can affect salivation and may induce oral complications such as glossitis, oral candidiasis, dental caries and some drugs have been reported to induce oral lichenoid reactions [58]. Moreover, high prevalence of candidiasis, denture stomatitis and periodontitis has been reported in patients with DM, a component of MS [913]. Therefore, we aimed to study the prevalence of oral manifestations, xerostomia, hyposalivation and level of oral microora in a group of Thai patients with MS and to determine if there is any association between MS and these oral health components.

1871-4021/$ see front matter 2009 Diabetes India. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.dsx.2009.08.004

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Awareness, evaluation of oral conditions and coping with these problems together with the MS treatment could benecially lead to the comprehensive treatment for patients with MS. 2. Materials and methods 2.1. Patient selection Three hundred and eighty two patients attended the Endocrine Clinic of the King Chulalongkorn Memorial Hospital were assessed for MS. In this study, the IDF criteria were used for the diagnosis of MS [1]. All participants were fully informed before completing their written consent document. These protocol and consent forms were approved by The Ethics Committee of the Faculty of Medicine, Chulalongkorn University (Reference Number: 388/2005). First, the waist circumference was measured by a measurement tape placed in a horizontal plane, midway between the inferior margin of the ribs and the superior border of the iliac crest. The inclusion criteria for the diagnosis of MS were waist circumference more than 90 cm in male and 80 cm in female. Then levels of triglyceride, HDL-C, FPG and blood pressure were evaluated from medical chart record. Finally, 369 patients were diagnosed with MS and included in this study. The age, sex, medical and personal history including smoking, drinking and denture hygiene procedure were collected. 2.2. Oral examination The number of patients presented with dental caries in at least 1 tooth was investigated. To evaluate the periodontal status, the Community Periodontal Index (CPI score) was used. The six selected teeth, one permanent molar in each quadrant, one upper central incisor and one lower central incisor, were examined for representative evaluation of all teeth in oral cavity. Healthy gingivae, gingivitis or periodontitis were then classied and recorded. Whole oral mucosa was examined. Normal variation or oral mucosal lesions were recorded. Oral mucosal dryness was evaluated and two categories were classied. Normal moist mouth was determined when most of the oral mucosa was covered with a lm of saliva. Dry mouth was diagnosed when no visible coating of saliva was presented over the entire dorsum of the tongue, buccal and labial mucosa. In addition, if a mouth mirror stuck to these tissues or no pooling of saliva in the oor of the mouth, or if only small discrete amount of frothy saliva was manifested, the patients were subjected to have clinical dry mouth. 2.3. Xerostomia and hyposalivation evaluation Questions indicating xerostomia were asked. These questions were as followed: (1) Do you sip liquids to aid in swallowing dry food? (2) Does your mouth feel dry when eating a meal? (3) Do you have difculties swallowing any food? (4) Does the amount of saliva in your mouth seem too little? And (5) does your mouth usually feel dry? Patients who answered yes in at least 1 question were considered to have xerostomia. Additionally, unstimulated salivary ow rate was measured by Modied Schirmer Test (MST) during 8.0011.00 a.m. Prior to the measurement, the patients were requested not to eat, smoke or brush their teeth for at least 2 h. The patients were asked to sit upright and swallow once to clear the secretion in the mouth. Then the edge of the Schirmer test strip was inserted to the oor of the patients mouth either to the right or the left of the lingual frenum, with the patients tongue slightly raised and gently retracted. The length of strip soaked with saliva as indicated by the level of blue dye was read at the third minute. When the reading was less than 5 mm, it was recorded as 5 mm, and when the reading was greater than

35 mm, it was recorded as 35 mm. The patients were considered to have hyposalivation when the measurement was less than 25 mm in 3 min according to the study of Fontana et al. [14]. 2.4. Oral microora evaluation (Modied Dip-Slide technique) [15] To determine the amount of oral microora related to dental caries and oral candidiasis, the levels of Mutans streptococci, Lactobacilli, and Candida species were assessed. Stimulated whole saliva samples from all patients were collected. Briey, each patient chewed one piece of parafn for 1 min and expectorated all saliva into a sterile container. The saliva was then poured over the surface of a 3-compartment dip-slide containing selective media including Mitis-Salivarius Bacitracin agar, Rogosa SL agar and CHROMagar for the enumeration of Mutans streptococci, Lactobacilli, and Candida species, respectively. The excess saliva was removed by blotting the edge with absorbent paper and then the dip-slide was placed into a plastic tube. Each plastic tube containing dip-slide was incubated at 37 8C for 4872 h in a 5% CO2 incubator. The colonies of Mutans streptococci, Lactobacilli and Candida were counted under a stereomicroscope and checked by Gram staining. The density of the growth of each microora was graded and recorded into 4 levels by comparison with a chart provided with the test [15]. 2.5. Statistical analysis Frequency, percent, the Pearson chi-square test, the Fishers exact test, the MannWhitney U test and the Spearman rank correlation were used where appropriate to assess the association and correlation of variables. p-Value less than 0.05 was considered statistically signicant. 3. Results 3.1. Patient characteristics Of 369 patients with MS, 94 subjects (25.5%) were men and 275 (74.5%) were women. The age varied from 32 to 88 years (mean = 63.9 10.4). One hundred and thirty eight patients (37.4%) were younger than 60 years old and 231 patients (62.6%) were older than 60 years old. The majority of the patients in both genders were 6170 years old. In men, waist circumference varied from 90 to 130 cm (mean = 98.7 8.1). In women, waist circumference varied from 80 to 142 cm (mean = 96.5 9.1). General health status, each component of MS and personal history of patients with MS are presented in Table 1. Male patients were more likely to smoke and drink than female. All patients were taking one or more medications for MS. The number of prescribed medications varied from 1 to 10. Most patients were using 45 drugs. The medications often used by the patients were antilipidaemic, antihypertensive, antidiabetic drugs and acetyl salicylic acid (ASA). Elderly patients (>60 years old) had signicantly used medications daily than younger ones (p = 0.001). Along with these, almost all patients (97%) used xerogenic medications (antilipidaemic, antihypertensive drugs and ASA). 3.2. Oral manifestations One hundred and eighty four patients (49.9%) had dental caries in at least 1 tooth. The mean score of dental caries was 1.42 2.2. One hundred and ninety two patients (52.0%) had periodontitis and 203 patients (55.0%) had one or more oral mucosal manifestations. The most common nding was ssured tongue (153 patients, 41.5%). The distributions of oral mucosal manifestations are presented in Table 2. Of these patients with oral mucosal manifestations, 159

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Table 1 Number of patients according to each component of MS and personal habit. Gender Component of metabolic syndrome Raised triglyceride Male Female Total 77 232 309 (83.74%) Reduced HDL-C 77 231 308 (83.47%) Raised BP 87 238 325 (88.08%) Raised FPG 94 275 369 (100%) Personal habit Smoking 11* 5 16 (4.3%) Drinking 15* 3 18 (4.9%)

Raised triglycerides level; !150 mg/dL. Reduced high density lipoprotein cholesterol (HDL-C); <40 mg/dL in males, <50 mg/dL in females. Raised blood pressure (BP); systolic BP ! 130 mmHg or diastolic BP ! 85 mmHg. Raised fasting plasma glucose (FPG); !100 mg/dL. * p = 0.001.

patients (43.1%) had one manifestation, 38 patients (10.3%) had two and 6 patients (1.6%) had three manifestations. In addition, normal moist oral mucosa was detected in 166 patients (45.0%) whereas dry mucosa was depicted in 203 patients (55.0%). No signicant association between oral mucosal manifestations and age, gender, number of prescribed medications, general health status, complaint of mouth dryness, smoking, level of HbA1c or salivary ow rate was found. Similarly, there was no signicant association between periodontitis and smoking, salivary ow rate or level of HbA1c. In this study, there were 176 (47.7%) denture wearers. Of this group, fty-one patients (29.0%) had partial dentures whereas 125 patients (71.0%) had complete dentures. One hundred and sixty patients (90.9%) cleaned their dentures every day. One hundred and thirty seven patients (77.8%) removed their dentures at night and 127 patients (72.2%) practiced both behaviors. Denture stomatitis was the second manifestation found in 34 patients

(9.2%) and signicantly associated with Candida level (p = 0.006) but not with cleansing of denture or denture removal at night (Table 3). Additionally, there was no signicant association between denture stomatitis and the level of HbA1c (p = 0.49). In this examination, eleven patients (3.0%) presented with glossitis and 8 patients (2.2%) presented with oral lichenoid reaction. Nevertheless, signicant association between these two oral mucosal conditions and possible induced medications were not detected. 3.3. Xerostomia and hyposalivation One hundred and fty seven patients (42.5%) complained that they had dry mouth. There was signicant association between female and complaints of xerostomia (p = 0.004). However, no statistically signicant association was detected between xerostomia and number of xerogenic medications (p = 0.71) or level of HbA1c (p = 0.23). The salivary ow rate in the patients with MS varied from 5 to 35 mm/3 min (mean = 22.68 10.27 mm/3 min). Two hundred and two patients (54.7%) had hyposalivation. Signicant association between xerostomia and hyposalivation was found (p = 0.006). In addition, there was signicant association between the questions Does the amount of saliva in your mouth seem too little? or Does your mouth usually feel dry? with hyposalivation (p = 0.001). Interestingly, the statistically signicant association between dryness of oral mucosa and complaints of xerostomia or hyposalivation was found (p = 0.001) (Table 4). Nevertheless, no signicant association between hyposalivation and age, gender, number of xerogenic medications or level of HbA1c was found in this study. 3.4. Oral microora By Modied Dip-Slide technique, saliva could be collected from 354 patients. The numbers of patients according to level of oral microora are presented in Fig. 1. There was statistically signicant
Table 3 Association between denture stomatitis and related factors. Related factors Denture stomatitis Yes n % 17.0 2.3 No n 130 12 % 73.9 6.8 0.516 p-Value

Table 2 Number of patients with oral manifestations and xerostomia. Oral health status Dental caries 1 tooth 2 teeth More than 3 teeth Periodontal status Healthy gingivae Gingivitis Periodontitis Oral mucosal manifestations Fissured tongue Denture stomatitis (from total subjects) Denture stomatitis (from denture wearers) Depapillated tongue Oral lichenoid reaction or oral lichen planus Traumatic ulcer Varicosity Smokers melanosis Frictional keratosis Other melanin pigmentation Pseudomembranous candidiasis Angular cheilitis Geographic tongue Fibroma Median rhomboid glossitis Oral mucosal dryness Normal moist mucosa Dry mucosa Xerostomia Q1 yes Q2 yes Q3 yes Q4 yes Q5 yes Salivary ow rate Normal (!25 mm/3 min) Hyposalivation (<25 mm/3 min) Number 184 68 46 70 % 49.9 18.4 12.5 19.0

11 166 192 203 153 34 34 11 8 8 8 7 5 5 5 2 2 2 1

3.0 45.0 52.0 55.0 41.5 9.2 19.3 3.0 2.2 2.2 2.2 1.9 1.4 1.4 1.4 0.5 0.5 0.5 0.3

166 203 157 91 91 88 101 119

45.0 55.0 42.5 24.7 24.7 23.9 27.4 32.2

Cleansing denture Yes No

30 4

Denture removal at night Yes 23 No 11 Candida level 1 (low) 2 (medium) 3 (high) 4 (very high)

13.0 6.3

114 28

64.8 15.9

0.111

167 202

45.3 54.7

8 5 11 8

4.9 3.0 6.6 4.8

57 34 21 22

43.3 20.5 12.7 13.3

0.006

U. Chomkhakhai et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews 3 (2009) 192197 Table 4 Association between dryness of oral mucosa, complaints of xerostomia and hyposalivation. Oral mucosal dryness Xerostomia Yes n Moist Dry 54 103 % 14.6 27.9 No n 112 100 % 30.4 27.1 0.001 p-Value Hyposalivation Yes n 17 185 % 4.6 50.1 No n 149 18 % 40.4 4.9 0.001

195

p-Value

Fig. 1. Number of patients at each level of microora. Mutans streptococci: level 1 = <103 CFU/mL, level 2 = !103 to <105 CFU/mL, level 3 = !105 to <106 CFU/mL, level 4 = !106 CFU/mL. Lactobacilli: level 1 = <103 CFU/mL, level 2 = !103 to <104 CFU/mL, level 3 = !104 to <105 CFU/mL, level 4 = !105 CFU/mL. Candida: level 1 = <102 CFU/mL, level 2 = !102 to <103 CFU/mL, level 3 = !103 to <104 CFU/ mL, level 4 = !104 CFU/mL.

association between Candida level and hyposalivation (p = 0.035). While there was no correlation between dental caries with Mutans streptococci level (r = 0.088) and Lactobacilli level (r = 0.105). 4. Discussion Through our review, there has been no study of oral conditions in patients with metabolic syndrome. According to the IDF criteria for the diagnosis of MS, proper waist circumference upon ethnicity is an important factor [1]. For Thai people, no specic cut-off point of waist circumference has been reported during the investigation period. Therefore, in this study, the cut-off point dened for South Asian and Chinese population (more than 90 cm in male and 80 cm in female) has been used for waist circumference evaluation since these ethnic groups have the most similar nature compared to other ethnic groups. Of this studied group, two third were elderly who were older than 60 years old. Unfortunately, all patients in this study were taking one or more medication due to their abnormality in each component of MS. The signicant association between the number of medications and the increasing age has been found. This result is comparable to the study conducted in

elderly Thai people in that the presence of medical conditions was high in the elderly and the incidence of medication use increased with advancing age [16]. Dental caries had been presented in 49.9% of our patients, however, there were no correlations between dental caries and Mutans streptococci level, Lactobacilli level, hyposalivation or glycaemic control. These results are contrast to the previous studies that reported the correlation of dental caries with salivary Mutans streptococci and Lactobacilli [17]. Syrjala et al. presented an association of high level of Mutans streptococci and Lactobacilli with dental caries, especially when glycemic control was poor [18]. Almstahl et al. showed that the increase of Mutans streptococci and Lactobacilli levels was associated with hyposalivation. This can be explained in part by the fact that different diet type and good oral hygiene maintenance in most patients may affect low levels of microora and dental caries in this study. The presence of periodontitis was found in approximately one half of the subjects. In contrast to the previous studies [19,20], periodontitis was not signicantly associated with poor glycaemic control in the present study even though 253 patients (68.6%) were uncontrolled type2 DM (HbA1c more than 6.5%). Since this study is a cross sectional, there may be a limitation in the collection of the longitudinal data. Further cohort study should be conducted to evaluate the progression of periodontitis and the glycemic levels in these patients. The prevalence of oral mucosal manifestations in this study (55.0%) was in the range reported by other studies conducted in the elderly (12.083.6%) [2128]. The commonly found oral mucosal manifestations which were ssured tongue, denture stomatitis, depapillated tongue, lichen planus, traumatic ulcer and varicosity are similar to oral lesions found in elderly Thai population though the prevalence in the study of Jainkittivong et al. was higher [21]. This may be due to the fact that the subjects in the latter study were patients seeking for treatment from a dental school and most of these patients had chief complaints of having oral mucosal lesions but the subjects in this present study were general patients attending the endocrine clinic and had no complaint of oral mucosal disorders. The most common condition found in this study was ssured tongue. Previous studies showed that the prevalence of ssured tongue was in the range of 19.927.3% [23,2831]. This lesion was the most prevalent condition in the study of Santos et al. [29]. In addition, there was a strong correlation between tongue lesions and increasing age [28]. In the study of Guggenheimer et al., ssured tongue was signicantly related to the older subjects who had a longer duration of DM [31]. A manifestation of aging, changing in the salivary ow rate or DM might be the explanation of the pathogenesis of this tongue condition. Prevalence of denture stomatitis in this study (9.2%) was higher than those of generalized elderly population in other studies (1 6%) [22,24,25]. This is not surprising since there were reports about the association between denture stomatitis and type2 DM [10] and almost two third of our patients (68.6%) had uncontrolled type2 DM. A positive relationship between Candida level and the presence of denture stomatitis was also found. This nding is in consistent with another study in that the density of oral Candida in

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denture wearers with denture stomatitis was statistically signicantly higher than non-denture wearers and denture wearers without denture stomatitis [32]. Regarding the third most common oral mucosal manifestation, it was depapillated tongue and 3% of all subjects had this lesion. This result is comparable with several previous studies in elderly (14.4%) [22,23,25,26,28] but less than that of the elderly Thai population (8.2%) investigated in a Thai dental school [21]. The prevalence of oral lichenoid reaction among the elderly was 0.43% in the previous studies [2124,27]. The prevalence of this lesion in our study was in this range (2.2%). Surprisingly, no signicant association between medications and depapillated tongue or oral lichenoid reaction was found in this study although the side effects of medications used have been reported to induce oral lichenoid reaction or depapillated tongue [5]. Indeed, these two lesions have not necessarily occurred in all patients who take these medications. Furthermore, in depapillated tongue, several other causes can induce this lesion including chronic trauma, nutritional deciency, hematological abnormalities, peripheral vascular disease and chronic candidiasis [33]. To evaluate the complaint of dry mouth, questions for determining xerostomia in this study was selected from questionnaires reported to be used effectively in the evaluation of salivary gland hyposalivation [34,35]. The prevalence of xerostomia (42.5%) was higher than those of elderly populations in the previous studies (1239%) [3540]. This might be explained by the fact that almost all subjects in this study (97%) were taking xerogenic medications that can induce the reduction of salivary ow rate [41]. However, the association between the number of xerogenic medications, age and xerostomia has not been found. In addition, there was no association between xerostomia and glycemic control status though all subjects in this study were type2 DM. This result is similar to the study by Chavez et al. which revealed that xerostomia was not associated with poorly controlled diabetes [42]. To determine decreased salivary ow rate from side effects of drugs which were used for treatment of MS, Modied Schirmer test was selected. It is a simple method for unstimulated whole saliva ow rate measurement. Cut-off point value for the diagnosis hyposalivation is varied [43]. Fontana et al. found that saliva secretion between 1 and 25 mm/3 min was a good indication of hyposalivation [14]. Comparable to Zunt et al., they suggested that a cut-off point of 25 mm/3 min may be used to identify patients with hyposalivation and a value of 10 mm/3 min or less might be able to identify patients with severe hyposalivation [44]. The mean unstimulated salivary ow rate of the subjects in this study (22.68 mm/3 min) is closest to that of patients who have certain pathologies (SLE, scleroderma, rheumatoid arthritis or pharmacologically related xerostomia), lower than healthy subjects but higher than patients with Sjogrens syndrome in the study of LopezJornet et al. [45]. It may be assumed that the patients with treatment of MS have decreased salivary ow rate comparable to patients who have some autoimmune diseases or taking medication. There was no association between hyposalivation and number of xerogenic medications in this study. Navazesh et al. reported the effect of duration of prescribed medication to hyposalivation [46]. Consequently, duration of taking medication might inuence this result. Association between xerostomia and hyposalivation has been analyzed in order to select the questions that can be used in clinical evaluation. The present study used four questions of Fox and one question of Narhi [34,35]. These questions have been reported to be associated with hyposalivation, both unstimulated and stimulated whole saliva [34,35,47,48]. Similarly, statistically signicant association between xerostomia and hyposalivation has been found in this study. When each question was analyzed

separately, there was statistically signicant association between the question Does the amount of saliva in your mouth seem too little? or the question Does your mouth usually feel dry? and hyposalivation. This result suggested that both questions may be used clinically to screen for any patients with hyposalivation. The patients who have positive answer should be aware and considered to have decreased salivary ow rate. Besides the use of questions to evaluate hyposalivation, clinical assessment could predict salivary gland function by inspection of oral dryness. Oral mucosal dryness has signicant association with hyposalivation in this study. Similarly, Longman et al. reported that the clinicians subjective assessment of oral dryness was indicative of reduction of unstimulated salivary ow rate [49]. Future study would be performed from the patients with untreated MS in general population. This future information may lead to the best understanding and treatment planning for the people who have MS. Acknowledgements This study was supported by Chulalongkorn University Research Grant 2005. References
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