PAPER. Do centrally obese Chinese with normal BMI have increased risk of metabolic disorders?

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1 (2005) 29, & 2005 Nature Publishing Group All rights reserved /05 $30.00 PAPER Do centrally obese Chinese with normal have increased risk of metabolic disorders? W-T Yeh 1, H-Y Chang 2, C-J Yeh 1,3, K-S Tsai 4, H-J Chen 1 and W-H Pan 1,5 * 1 Institute of Biomedical Sciences, Academia Sinica, Nan-Kong, Taipei, Taiwan; 2 Division of Health Policy Research, National Health Research Institute, Taichung, Taiwan; 3 Department of Public Health, College of Health Care and Management, Chung Shan Medical University, Taichung, Taiwan; 4 Department of Laboratory Medicine, National Taiwan University Hospital, Taipei, Taiwan; and 5 Institute of Microbiology and Biochemistry, National Taiwan University, Taipei, Taiwan BACKGROUND: Body mass index () and waist circumference are highly correlated. One or the other predicts the metabolic syndromes better, depending on characteristic of the population studied, such as age, gender, and ethnicity. We examined the impact of isolated central obesity, isolated elevation, and the combined type of obesity on metabolic disorders, in order to shed lights on the strategy of obesity screening. METHODS: The study subjects were Chinese aged 20 or above residing in Taiwan. Their data were derived from two large-scale studies: the Nutrition and Health Survey in Taiwan (NAHSIT ) and the Cardiovascular Disease Risk Factor Twotownship Study (CVDFACTS, ). In evaluating the relations between obesity and health risks, the cut-points of (Z24 kg/m 2 for overweight) and waist circumference (Z80 cm for women and Z90 cm for men) recommended by Department of Health in Taiwan for Taiwanese people were used to define various types of obesity. RESULTS: We found that there was a small but nontrivial proportion (1.7% for men and 4.0% for women) of Taiwanese people for whom was in the normal range but their waist circumferences were above normal. These people were at a higher risk of developing metabolic syndromes than those with isolated elevation. Their risks were close to that of the combined type. CONCLUSIONS: In order to screen out high-risk obese individuals, isolated centrally obese subjects should not be overlooked. Therefore, we recommend to assess waist circumference in parallel to, not just sequential to the measurement of in Chinese. (2005) 29, doi: /sj.ijo Published online 10 May 2005 Keywords: waist circumference; metabolic syndrome; screening Introduction Issue on how to define obesity has been widely discussed and evaluated to deal with the worldwide emerging health problems associated with obesity, particularly cardiovascular related diseases and diabetes mellitus. 1 4 Body mass index () and waist circumference are two most popular indicators for assessing obesity, which are relatively inexpensive and easy to use. is strongly associated with body fat content, but has the limitation of overestimating the degree of fatness for very muscular man and underestimating those who have low muscle mass, as in the case of elderly people. In addition, there is gender, age, and ethnicity related variations in body fat for a given probably due to differences in the composition of lean and fat tissue, sitting *Correspondence: Dr W-H Pan, Institute of Biomedical Sciences, Academia Sinica, Taipei , Taiwan. pan@ibms.sinica.edu.tw Received 30 November 2004; accepted 26 February 2005; published online 10 May 2005 height, hydration status, 5 and probably genetic make-ups. On the other hand, waist circumference is highly correlated with the amount of abdominal fat, which is a predictor of metabolic syndrome independent of total body fat. 6 In many populations, waist circumference is considered as a better indicator of metabolic risk than Different age trends and gender patterns have been observed for and waist circumference in Taiwan as well as in other populations. 13,14 The association patterns between obesity and metabolic syndrome/or CVD related disorders differ with gender and with obesity indices. 15,16 It is likely that prediction power of and waist circumference vary slightly in an age- and gender-specific manner. However, a simple definition of obesity with good predictive powers is preferred in the public health study to screen people at risk. Many have evaluated whether is better than waist circumference or vice versa and whether one indicator is sufficient for screening, considering adults of all ages and both genders. Since and waist circumference are highly

2 correlated and depending upon the age and gender structure of the studied sample, one or the other will perform better and the magnitudes of their association with related diseases often differ just by a minute amount; we therefore set out to compare the impacts of isolated central obesity and isolated elevation on diseases in various age-gender groups, in order to shed light on the screening strategies for high-risk obese individuals. Research methods and procedures Research design The study subjects were Chinese aged 20 or above residing in Taiwan. Data were derived from two large-scale studies. The first set of data was derived from the Nutrition and Health Survey in Taiwan (NAHSIT ), a national survey with a complex sampling scheme. 17,18 A standardized and structured questionnaire was administered to collect data on detailed demographic characteristics, past medical history, and history of medication along with other nutrition related information. A response rate of 74% was obtained for the household interviews. Around 62% of those interviewed had participated the physical examinations. Following an overnight fast of 8 h or more, subjects reported to a local clinical research station in the morning for physical examinations. The target population included individuals aged 4 and above. Excluding aboriginal people and people with missing data of any of the studied variables, there were 2143 participants (1020 men and 1123 women) aged 20 and above included in this study. The second set of data set is from the Cardiovascular Disease Risk Factor Two-township Study (CVDFACTS, ), 19 which was a longitudinal study on risk factors, incidence, and subclinical disorders of the cardiovascular diseases, carried out in Chu-Dong and Pu-Tzu townships of Taiwan. Recruitment had been made from all residents of five selected villages in each township. Three invitation letters had been sent out consecutively to every household. In this study, baseline data on biomedical and blood pressure values, information on medication and anthropometric parameters were derived from 1784 men and 2168 women aged 20 and above. Data collection NAHSIT and CVDFACTS used the same protocol for measuring anthropometric parameters, and similar ones for measuring biochemical indicators and blood pressure. All participants of both studies have signed informed consent forms. Blood pressure measurement In NAHSIT, blood pressure was measured by standard sphygmomanometers at home after the participants were rested for at least 5 min. A cuff of appropriate size was used for each participant. Two blood pressure measurements were made 30 s apart with the arm at the level of the heart. If two measurements were more than 10 mmhg apart, a third measurement was taken. The two nearest blood pressure values were averaged to obtain the mean blood pressure. In CVDFACTS, the same protocol was followed except that three measurements were obtained in the clinics set up in the neighborhood of the study sites. The last two readings were averaged. Blood chemistry In NAHSIT, fasting whole-blood glucose (WBG) was measured with heparinized blood by the glucose oxidase method using a glucose analyzer (Model 23A, YSI, USA) immediately after blood drawing. In collaboration with the clinical chemistry laboratory of the affiliated hospital of National Taiwan University Medical School, a Hitachi 747 analyzer was used to measure serum uric acid, triglyceride, cholesterol, and HDL-C values of the fasting sera in both studies and to measure glucose of the NaF plasma for CVDFACTS within a month following the blood draw. Anthropometric assessment Anthropometric measurements were carried out after subjects had removed their shoes and heavy clothes. Subjects were asked to put on an examining gown if their apparel was not appropriate for taking measurements. Body weight was measured to the nearest 0.1 kg, and body height to the nearest millimeter. was calculated as weight divided by height squared (kg/m 2 ). Waist circumference was measured horizontally at the level of the natural waist, which was identified as the level at the hollow molding of the trunk when the trunk was concaved laterally. Definitions of obesity Taiwanese obesity definition was used in this study. Overweight was defined as Z24 kg/m 2 and obesity was defined as Z27 kg/m These cut-points were set lower than that of WHO, since we found that metabolic syndromes were more severe in Chinese than in Caucasians. 20 These cut-points are higher than those recommended for Asians by International Obesity Task Force ( an affiliated organization of WHO. Central obesity was defined as waist circumference Z80 cm for women and Z90 cm for men as IOTF recommended. The expected waist circumference values at ¼ 27 kg/m 2 for men and women approximate the above values by regressing waist circumference on. Definitions for selected conditions Hypertension was defined as using prescribed antihypertensive medication or having a systolic blood pressure 819

3 820 Z140 mmhg or above or a diastolic blood pressure Z90 mmhg. Diabetes mellitus was defined as using insulin or hypoglycemic agents or having an abnormal fasting plasma glucose level. The abnormal level was defined if plasma level was Z126 mg/dl in CVDFACTS or WBG level was Z110 mg/dl in NAHSIT. 21 Hypercholesterolemia was defined as using lipid-lowering medication or having a serum cholesterol level Z240 mg/dl. Hypertriglyceridemia was defined as using lipid-lowering medication or having a serum triglyceride level Z200 mg/dl. Low HDL-C was defined as serum HDL-C r35 mg/dl. Hyperuricemia was defined as a serum uric acid level Z6.6 mg/dl for women and Z7.7 mg/dl for men. Age-adjusted relative risk (RR) was estimated by Poisson regression to study the effect of obesity types on DM and CVD related conditions in each age and gender group. These RR estimates were compared using CONTRAST statement under Poisson regression in SAS. In evaluating the need to screen isolated central obese individuals in Taiwan, the cut-points of (Z24 kg/m 2 for overweight) and waist circumference (Z80 cm for women and Z90 cm for men) recommended by Department of Health in Taiwan for Taiwanese people were used to define various types of obesity. Statistical package SAS, version 8.0 was used for the above analyses. Statistical analysis In order to examine the age-specific phenomenon, the subjects were grouped into young (20 44), middle-aged (45 64), and old (Z65) age groups. In estimating prevalence rate ratio of various types of obesity, the 75th percentile value of both waist circumference and in each age and gender group was used as cutpoint to define nonobese group and three obesity types to ensure adequate sample size in each subgroups. The nonobese group consisted of those with both waist circumference and below their 75th percentiles. The isolated central obesity group was those with waist circumference above 75th percentile but below 75th percentile. The isolated elevation group was that with above 75th percentile but waist circumference below 75th percentile. The combined type was that with both waist circumference and above their 75th percentile values. Waist circumference,, and age were expressed as mean7standard deviation (s.d.) and age was compared among nonobese group and those obesity types by Duncan analysis. The prevalence of several obesity-related diseases was also compared among these groups. Results Table 1 showed the quartile values of waist circumference and, and prevalence of obesity by age and gender. The quartile values of waist circumference and the prevalence of central obesity increased with age in both genders, and subsequent to middle age it increased to a greater extent in women than in men. On the other hand, values and the prevalence of general obesity increased with age and declined after middle age and this decrease was more so in men than in women. There were more centrally obese women than men in every age group. There were more obese men than women in young age, but vice versa in middle and old age groups. Table 2 showed the estimates of waist circumference, values, and disease prevalence rates by sex, age, and obesity types. Varying with age and gender groups, nearly 66 69% of the people were grouped into the nonobese group. Around 6 9% people were categorized into the isolated central obesity group, 5.5 8% into the isolated elevation group, and % into the combined type group. The mean age was usually younger in the nonobese group than in the three Table 1 Quartile values of waist circumference and and prevalence of obesity by age and gender groups Men Women Gender group Age group N Prevalence of central obesity a 14.8% 29.5% 33.2% 15.3% 41.9% 60.1% Waist circumference (cm) 25th th th Prevalence of general obesity b (kg/m 2 ) 14.1% 16.8% 13.1% 9.9% 25.0% 22.6% 25th th th a Central obesity was defined as waist circumference Z90 cm for men and Z80 cm for women. b General obesity was defined as Z27 kg/m 2 for both men and women. (According to the obesity definition recommended by DOH in Taiwan for Taiwanese people).

4 Table 2 Mean age, waist circumference, and and disease prevalence by sex, age, and obesity types Gender Age group Obesity group N N% Age a,b (y) Waist a (cm) a (kg/m 2 ) ZOne conditions Hypertension Hypertriglyceridemia Hypercholesterolemia DM Low HDL Hyperuricemia Men Control b Iso. central ob a Iso. elevated b Combined a Control b Iso. central ob a Iso. elevated b Combined a,b Control a Iso. central ob a Iso. elevated b Combined a,b Women Control b Iso. central ob a Iso. elevated a Combined a Control c Iso. central ob a Iso. elevated d Combined b Control b Iso. central Ob a Iso. elevated b Combined b Control: Both waist circumference and values are below their 75th percentiles; isolated central obesity: waist circumference value is above 75th percentile but value is below 75th percentile; isolated elevation: value is above 75th percentile but waist circumference value is below 75th percentile; combined type: both waist circumference and values are above their 75th percentiles. a Mean7s.d. b Means with the same letter superscript are not significantly different, P ¼ 0.05 (Duncan s multiple-range test). 821

5 822 obesity types in each age and gender strata. In general, the disease prevalence rates were low in most nonobese groups and high in most of the combined type groups. For the nearly 6 9% of the population with isolated central obesity, their prevalence of many of the studied conditions were almost as high as that of the combined type. However, the isolated centrally obese group was usually older than the group with isolated elevation. The age effect is adjusted in the following analysis. Age-adjusted RRs of obesity-associated conditions in three types of obesity were shown in Table 3. In terms of the risk of having one or more of the studied conditions, we found that isolated central obesity had higher RR than isolated elevation in most age and gender groups, except in old age men, in whom no significant difference in RR estimates was found between these two types of isolated obesity. For men in all age groups and women in young and middle age groups, the combined type showed the highest RR compared to the other obesity groups. However in old age women, isolated central obesity had the highest RR. For every obesity type, the RRs for having one or more of the condition decreased with age in men. In women, only the RR of the combined type of obesity has a clear decreasing trend with age. In terms of individual disorders, RR was higher for isolated central obesity than for isolated elevation in middle age women for most of the studied conditions. However, this phenomenon holds for about half of the studied conditions in other gender and age group. The RRs of hypertension and diabetes were higher for isolated elevation group than isolated centrally obese group in men and young women, but vice versa in middle and old age women. Isolated central obese men in all age groups had higher RR of hyperuricemia than men with isolated elevation, whereas vice versa in women after 45 y old. However, in comparing RRs between isolated centrally obese groups and isolated elevation groups, there were no consistent patterns of RRs for hypertriglycemia and hypercholesterolemia in all age and sex groups. For the condition of low HDL-C, isolated central obesity showed higher RR than isolated elevation in all age and gender groups, and it was especially high in the young age group. In women, the RR of low HDL-C for isolated central obesity was apparent in its decrease with age. The prevalence of obesity defined by Taiwan definition and associated disorders by and waist circumference categories are shown in Table 4. According to the definition for Taiwanese people, near 50% of both men and women Table 3 group) Age-adjusted relative risk on obesity-associated conditions for three types of obesity by each gender and by age group (all were compared to the nonobese Men Women Types of obesity* Iso. central ob Iso. elevated Combined Iso. central ob Iso. elevated Combined Age ¼ N ¼ 62 N ¼ 59 N ¼ 193 N ¼ 87 N ¼ 75 N ¼ 262 ZOne conditions 1.68b 1.53c 1.85a 1.32b 1.18c 2.51a Hypertension 1.69b 1.67b 2.79a 1.76c 3.59b 5.43a DM (1.21)b 3.62a 3.80a b 8.65a Hypertriglyceridemia 1.13c 1.84b 4.11a 1.84b 1.42c 6.52a Hypercholesterolemia 1.42b 1.51b 1.71a (0.98)a (0.91)a 1.48a Low HDL 2.40b 1.25c 2.72a 3.08a 0.48c 2.90b Hyperuricemia 2.10a 1.79c 2.07b 0.92b (0.95)b 2.60a Age ¼ N ¼ 76 N ¼ 65 N ¼ 223 N ¼ 117 N ¼ 101 N ¼ 247 ZOne conditions 1.30b 1.19c 1.34a 1.34b 1.20c 1.49a Hypertension 1.54b 1.78a 1.48c 1.54b 1.10c 1.81a DM 1.18c 1.84b 2.04a 2.76b 1.64c 3.36a Hypertriglyceridemia 2.49a 1.25c 2.36b 2.75a 1.65c 2.48b Hypercholesterolemia 1.22c 1.55a 1.32b 1.32a 1.20b (1.02)c Low HDL 1.91a 1.16c 1.79b 1.97a 0.81c 1.76b Hyperuricemia 1.51b 1.40c 1.82a 1.55c 1.67b 2.17a Age ¼ 65+ N ¼ 58 N ¼ 38 N ¼ 124 N ¼ 44 N ¼ 43 N ¼ 95 ZOne conditions 1.15b 1.15b 1.29a 1.21a 1.11c 1.17b Hypertension 1.09c 1.24b 1.51a 1.26b 1.13c 1.28a DM 1.69c 2.61a 2.49b 2.41a 1.31c 1.71b Hypertriglyceridemia 2.42b 2.58b 3.30a 1.68b 1.85a 1.38c Hypercholesterolemia (1.07)a (0.94)b 1.31ab (1.05)a (0.99)a 1.29a Low HDL 2.03a (1.07)b 2.26a 1.09a 0.81c (0.99)b Hyperuricemia 1.43b 0.70c 1.77a 1.25c 1.55a 1.51b *Isolated central obesity: Waist is above 75th percentile but is below 75th percentile. Isolated elevation: is above 75th percentile but waist is below 75th percentile. Combined: Waist is above 75th percentile and is below 75th percentile. a,b,c Different symbols represent significantly different (Po0.05) from each other in the descending order, tested using CONTRAST statement under Poisson regression in SAS. (): not significantly different from control group.

6 Table 4 The prevalence of obesity and associated disorders by and waist circumference categories recommended by Department of Health 823 Age group Obesity type a N N% ZOne conditions Hypertension DM Hypertriglyceridemia Hypercholesterolemiaemia Low HDL Hyperuricemia Men 20+ Normal Iso. central ob Iso. elevated Combined Normal Iso. central ob Iso. elevated Combined Normal Iso. central ob Iso. elevated Combined Normal Iso. central ob Iso. elevated Combined Women 20+ Normal Iso. central ob Iso. elevated Combined Normal Iso. central ob Iso. elevated Combined Normal Iso. central ob Iso. elevated Combined Normal Iso. central Ob Iso. elevated Combined a Cut-points for waist circumference: 90 cm for men and 80 cm for women; Cut points for : 24 kg/m 2. Normal: Both waist circumference and are below their cut-ponts. Isolated central obesity: Waist circumference is above its cut-point but is below its cut-point. Isolated elevation: is above its cut-point but waist circumference is below its cut-point. Combined type: both waist circumference and are above their cut-points. were classified in the normal and normal waist circumference group, 21% of men and 15% of women were overweight (Z24 kg/m 2 ) but normal in their waist circumference (isolated elevation). There were small but nontrivial proportions of men (1.7%) and women (4%) classified in normal but centrally obese group (isolated central obesity). Another 23% of men and 28% of women fell within the category of both high and waist circumference (the combined type). The proportions of those classified in the isolated central obesity group increased with age, and were greater in women than in men. In both adult men and women, the prevalence of having one or more of the studied conditions was much higher in the large waist circumference group than in the normal waist circumference group at both normal (isolated centrally obese group vs normal) and elevated groups (combined group vs isolated elevation). For those isolated centrally obese people, their prevalence of having one or more of the studied conditions was around 70% in both genders, which was almost equivalent to that for men with isolated elevation, but much higher than that for women with isolated elevation. In terms of individual disorders, for women, the pattern was similar to that of having one or more conditions as described above. In men, prevalence of most conditions did not differ much between the isolated central obesity group

7 824 and the isolated elevation group, except for the prevalence of diabetes, which was particularly high in isolated centrally obese group. Considering age and genderspecific patterns, higher prevalence rates for those with isolated central obesity than those with isolated elevation were seen for about half of the studied conditions in young and middle aged men, and for low HDL-C in old age men. This phenomenon was also observed for hypertriglyceridemia in young age women, for all of the studied conditions in middle age women and or about half of the studied conditions in old age women. Discussion From this study we found that there was a small but nontrivial proportion of Taiwanese people for whom was in the normal range, but their waist circumferences were above normal (Table 4). These people were at a high risk of developing metabolic syndromes than their counterpart with only elevation. The phenomenon could only partially be explained by their older age. It is well known that for a given, older persons often have more fat than younger persons, and women may have more body fat than men. 5 Our age and gender-specific obesity prevalence data not only support this view, but also depict an even more apparent age and gender associated pattern of abdominal fat accumulation. This phenomenon is consistent with our previous study 13 and others. 22,23 In both men and women, the prevalence of central obesity increased with age to a greater degree than that of general obesity. The prevalence of central obesity differed between women and men also to a greater extent than that of general obesity. Thus, the predictability of anthropometric measurements on metabolic disorders may be a function of gender and agerelated differences in body fat distribution. Findings of many studies 7,15,24 are consistent with the above hypothesis in that waist circumference is a better predictor of obesity-related diseases in older than in younger individuals, and in women than in men. Irrespective of the obesity types, the RRs of obesity for having one or more of the metabolic disorders tend to decrease with age, consistent with other studies. 25,26 This demonstrates that the relative impact of obesity on disease risk was stronger in young age. Aging and its related factors (such as accumulative effect of environmental exposures) took a more important role on the development of disease in the elderly than in their younger counterpart. The largest RR observed for the middle aged women among all age groups in women suggested that the high prevalence of obesity, especially the sudden rise of the central obesity in them, had a strong effect on the development of metabolic disorders for middle age women in Taiwan. Among all the studied disorders, RRs of having low HDL-C were consistently higher for isolated central obesity groups than isolated elevation group in all age and gender groups, suggests an intimate relationship between central obesity and lowered HDL-C. A possible mechanism, as suggested by Vajo, 27 is that intra-abdominal fat may lower HDL-C levels through the increase of the fractional catabolic rate of Lp A-I (apolipoprotein A-II). The degrees of predictivity of waist circumference and often varied for each studied disease in an age- and genderspecific manner. We also found that in women of young age, hypertension was related more to perhaps because body fluid and peripheral resistance expansion is the primary mechanism, 28 while in the middle aged, hypertension may largely emerge from metabolic disorder and thus related more to waist circumference. This age- and gender-specific phenomenon may explain why, in the literature, or waist circumference takes turns to be the more significant predictor of obesity-related metabolic disorders, 29 depending on the age and gender structure of the population studied. In order to screen out high-risk obese individuals including isolated centrally obese subjects, we recommend to measure waist circumference in parallel to, not just sequential to the measurement of in Chinese. Although it is more challenging to measure waist circumference reliably than, designing an easy-to-use reliable measuring tape should be able to circumvent the situation. Acknowledgements The survey was supported by grants (DOH-83-FS-41, DOH- 84-FS-11, DOH-85-FS-11, DOH-86-FS-11, and DOH-83-TD- 015, DOH-84-TD-006) from Department of Health, Taiwan, Republic of China, and grant (NHRI-EX PP) from National Health Research Institute, Taipei, Taiwan. References 1 Ford ES, Williamson DF, Liu S. 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