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International Journal of Obesity (2006) 30, 912–917

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ORIGINAL ARTICLE
Insulin resistance, obesity, and metabolic syndrome
among non-diabetic pre- and post-menopausal
women in North Taiwan
W-Y Lin1,2,3, W-S Yang4,5,6, L-T Lee1, C-Y Chen1, C-S Liu2,3, C-C Lin2,3 and K-C Huang1
1
Department of Family Medicine, National Taiwan University Hospital, Taipei, Taiwan; 2Department of Family Medicine,
China Medical University Hospital, Taichung, Taiwan; 3Department of Family Medicine, College of Medicine, China
Medical University, Taichung, Taiwan; 4Division of Endocrinology and Metabolism, Department of Internal Medicine,
National Taiwan University Hospital, Taipei, Taiwan; 5Graduate Institute of Clinical Medicine, College of Medicine,
National Taiwan University, Taipei, Taiwan and 6Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan

Objective: To investigate the relationship between the metabolic syndrome and its related factors among non-diabetic pre- and
post-menopausal women in North Taiwan.
Design: A cross-sectional study in a medical center in North Taiwan.
Subjects: Five hundred and ninety-four, non-diabetic middle-aged women (age range ¼ 40–64 years, mean ¼ 48.975.4 years)
were recruited.
Measurements: The fasting plasma glucose, insulin, lipids levels and anthropometric indices were measured. The homeostasis
model assessment was applied to estimate the degree of insulin resistance (HOMA-IR). Metabolic syndrome was defined by
using the National Cholesterol Education Panel (NCEP) criteria and modified NCEP criteria (waist circumference 480 cm).
Results: The prevalence of metabolic syndrome was 6.2% using NCEP criteria, and 8.9% using modified NCEP criteria. Post-
menopausal women had a higher prevalence of metabolic syndrome and its individual components compared to pre-
menopausal women except hyperglycemia and low HDL-C. In multiple logistic regression analysis with adjustment for age and
menopausal status, both BMI and HOMA-IR were independently associated with the metabolic syndrome.
Conclusion: The prevalence of metabolic syndrome was higher in post-menopausal than pre-menopausal women. Both obesity
and insulin resistance may play an important role in the development of metabolic syndrome among the middle-aged women in
North Taiwan.
International Journal of Obesity (2006) 30, 912–917. doi:10.1038/sj.ijo.0803240; published online 24 January 2006

Keywords: metabolic syndrome; insulin resistance; body mass index; menopause

Introduction 10–20%,5–7 depending on regions and criteria used to define


metabolic syndrome. Therefore, the metabolic syndrome has
The metabolic syndrome, a constellation of impaired glucose become a significant health problem worldwide and requires
metabolism, dyslipidemia, hypertension, and central obe- urgent attention.
sity, is associated with subsequent development of type 2 However recently, a joint statement from the American
diabetes mellitus and cardiovascular diseases (CVD).1 CVD Diabetes Association and European Association for the Study
and all-cause mortalities also increase with metabolic of Diabetes8 indicates that classifying someone as having the
syndrome.2 In Europe and the United States, the prevalence metabolic syndrome can arise due to various combinations
of metabolic syndrome is approximately 20% in adults.3,4 In of a variety of different clinical problems, and that this alone
Asians, the prevalence of metabolic syndrome is around is of limited value in understanding the etiology of the
abnormalities, or in the treatment of them. It also suggests
that the metabolic syndrome requires much more study
Correspondence: Dr K-C Huang, Department of Family Medicine, National before its designation as a ‘syndrome’ is truly warranted and
Taiwan University Hospital, 7 Chung-Shan South Road, Taipei 100, Taiwan.
before its clinical utility is adequately defined. In addition,
E-mail: chin3@ha.mc.ntu.edu.tw
Received 13 April 2005; revised 10 October 2005; accepted 8 December the variable contribution of risk factors to the metabolic
2005; published online 24 January 2006 syndrome between countries9 suggests that the definition of
Menopause and metabolic syndrome
W-Y Lin et al
913
metabolic syndrome in different populations should be described.21 The metabolic syndrome was defined clinically,
properly addressed, thereby to increase the comparability based on the presence of three or more of the following
in different countries. National Cholesterol Education Panel (NCEP) criteria:23 (1)
CVD is the leading cause of death in many countries.10 It central obesity (WC 490 cm in women), (2) a high
has been demonstrated that CVD risk increases after triglyceride level (X1.69 mmol/l), (3) a low-HDL cholesterol
menopause, which may be associated with the emergence level (o1.29 mmol/l in women), (4) high blood pressure
of the features of metabolic syndrome from pre- to post- (X130/85 mmHg), (5) a high fasting plasma glucose con-
menopausal status.11–14 However, hormone replacement centration (X6.1 mmol/l). Furthermore, the modified NCEP
therapy for the menopausal women does not confer criteria using a lower WC cutoff with WC 480 cm in women
cardiovascular protection according to the Women’s Health was also applied for comparison due to a different definition
Initiative trial.15 Therefore, estrogen deficiency may of central obesity in this population.6,25 Plasma insulin levels
indirectly contribute to the increased risk of CVD in post- were determined by a microparticle enzyme immunoassay
menopausal women. using AxSYM system from Abbott Diagnostics (Abbott
The prevalence of obesity is increasing in many coun- Laboratories, Dainabot Co. Ltd., Tokyo, Japan). The home-
tries.16,17 In addition to increasing mortality, obesity has ostasis model assessment is applied to estimate the degree of
been known to be associated with higher risk of hyperten- insulin resistance (HOMA-IR ¼ fasting insulin  fasting
sion, diabetes, dyslipidemia and CVD.18–21 On the other plasma glucose/22.5, where insulin in mU/mL and glucose
hand, the main features of the syndrome cluster together in mmol/l).26 Informed consent was obtained from the subjects.
more frequently than would be expected by chance alone,1
and insulin resistance has been regarded as the basic defect
leading to metabolic syndrome.22–24 Taken together, these Statistical analyses
imply that a common mechanism, such as insulin resistance The data are presented as the means and s.d. unless indicated
and/or obesity, underlies the metabolic syndrome. In this otherwise. BMI and HOMA-IR were grouped according to the
study, we investigated the prevalence of metabolic syndrome calculated data in quartiles. Log transformation was used for
and its related factors, including age, menopausal status, BMI variables with significant deviation from normal distribu-
and insulin resistance index among non-diabetic, middle- tion, assessed by Kolmogorov–Smirnov test before further
aged women. analyses. The frequency of metabolic syndrome and its
components was calculated for participants according to
menopausal status. The Wald w2 test was used to evaluate the
Methods statistical significance and odds ratios of the prevalence rates
of the metabolic syndrome. Several multivariate logistic
Subjects and characterizations regression models were performed with various combina-
Five hundred and ninety-four middle-aged women who tions of age, menopausal status, BMI, and HOMA-IR groups
attended the survey of CVD risk factors in a medical center in as independent variables, and metabolic syndrome as the
North Taiwan were recruited in 1998. The inclusion criteria outcome variable. These statistical analyses were performed
were as follows: (1) aged from 40 to 64 years old; (2) denied using the PC version of SPSS statistical software (10th
any major disease which may influence their body weight version, SPSS Inc., Chicago, IL, USA).
(ex: diabetes mellitus, thyroid diseases etc.); (3) no current
medication which may influence body weight (e.g.: hor-
mone, glucocorticoid, antiobesity medications etc.). Meno- Results
pause is defined as the absence of menstruation for 12
consecutive months, which is not due to surgical resection of The basic characteristics of the subjects are shown in Table 1
uterus or ovaries. The anthropometric measurements, in- according to menopausal status. The means of age, weight,
cluding height, weight, waist (WC) and hip circumferences BMI, WC, blood pressure, plasma TCHOL, HDL-C, LDL-C
(HC), and blood pressure measurement were performed as and triglycerides levels are higher in post-menopausal than
previously described.21 Body mass index (BMI) was calcu- in pre-menopausal women. However, statistically, the fasting
lated as weight (kg) divided by height squared (m2). This plasma glucose, LDL-C, insulin levels, and HOMA-IR are not
study has been approved by the Ethics Committee of significantly different between the two groups. Moreover,
National Taiwan University Hospital. the plasma TCHOL and LDL-C levels are not significantly
different between women with and without metabolic
syndrome either in pre-menopausal or post-menopausal
Laboratory tests women (data not shown).
A venous blood sample was taken after 12 h of fasting for The prevalence of metabolic syndrome and its individual
measuring plasma glucose, triglycerides, total cholesterol components according to the menopausal status are shown
(TCHOL), low-density lipoprotein cholesterol (LDL-C), and in Table 2. The prevalence of metabolic syndrome is 6.2%
high-density lipoprotein cholesterol (HDL-C) as previously using the NCEP-ATP III criteria, and 8.9% using the modified

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W-Y Lin et al
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Table 1 Demographic data, blood pressure, insulin, insulin resistance index a p<0.001
(HOMA-IR), and lipid levels categorized by menopausal status (n ¼ 594) p<0.001
25% p<0.001
Premenopause Postmenopause P-value*
(n ¼ 360) (n ¼ 234)

Age (years)a 46.073.6 53.174.4 o0.001 20%


Height (cm)a 156.675.0 155.674.8 0.014
Body weight (kg)a 56.378.1 58.078.9 0.014
BMI (kg/m2)a 22.973.0 23.973.3 o0.001
WC (cm)a 73.077.8 75.479.1 0.001

Prevalence
15%
Systolic BP (mmHg)a 116.2715.7 122.5718.6 o0.001
Diastolic BP (mmHg)a 70.0711.3 76.6711.3 o0.001
Fasting glucose (mmol/l)a 5.2370.76 5.2570.60 0.372
TCHOL (mmol/l) 5.1870.84 5.5671.02 o0.001 10%
Triglycerides (mmol/l)a 1.0370.67 1.3270.81 o0.001
HDL-C (mmol/l) 1.4670.38 1.6070.44 o0.001
LDL-C (mmol/l) 3.2570.78 3.3970.93 0.051
TCHOL/HDL-Ca 3.7471.06 3.7271.14 0.533 5%
Insulin (pmol/l)a 50.0727.8 55.1747.7 0.497
HOMA-IRa 1.6171.04 1.7871.49 0.345

BMI, body mass index; WC, waist circumference; TCHO, total cholesterol; 0%
HDL-C, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein 1 2 3 4
cholesterol; HOMA-IR, insulin resistance index by HOMA. Data are means Quartiles of HOMA-IR groups
7s.d. *Student’s t-test for unpaired data was used for the comparison of mean
values between groups. aStatistics were tested using the log-transformed p<0.001
values.
b
p<0.001
25%
p<0.001

Table 2 Prevalence (%) and crude odds ratios (OR) of metabolic syndrome 20%
and its individual components among pre- and post-menopausal women
(n ¼ 594)

Variables Pre-menopausal Post-menopausal ORa (95% CI) p<0.01


Prevalence

15%
(%) (n ¼ 360) (%) (n ¼ 234) p<0.05

Central obesity 5.8 10.7 2.09 (1.41–3.11)


Central obesity2b 16.4 29.1 1.93 (1.05–3.54) 10%
High BP 19.4 37.2 2.45 (1.69–3.56)
High fasting glucose 5.0 5.6 1.12 (0.54–2.33)
High triglycerides 9.2 20.5 2.56 (1.59–4.13)
Low HDL-C 35.6 23.9 0.57 (0.39–0.83) 5%
Metabolic syndrome 4.2 9.4 2.39 (1.21–4.70)
Metabolic 5.8 13.7 2.56 (1.44–4.56)
syndrome2b
0%
a
Reference group was pre-menopausal women. bCentral obesity was defined 1 2 3 4
by waist circumference 480 cm, 2 refers to modified definition of metabolic
syndrome. Quartiles of BMI groups
Figure 1 Relationship between the prevalence of metabolic syndrome using
modified criteria, HOMA-IR and BMI groups in quartiles (o0.93, 0.93–1.39,
1.40–2.13, 42.14 in HOMA-IR and o21.2, 21.2–22.7, 22.8–25.0, 425.1 kg/m2
NCEP-ATP III criteria. Post-menopausal women also have a in BMI) among these women. (a) The prevalence of metabolic syndrome was
significantly higher prevalence of central obesity, high blood 1.4, 2.7, 6.8 and 23.0% in the quartiles of HOMA-IR groups, respectively. The
pressure, and high triglycerides compared to pre-menopausal prevalence of metabolic syndrome was increasing with the increments of
HOMA-IR quartiles (test for trend, Po0.01). (b) The prevalence of metabolic
women.
syndrome ranged from 0.7, 2.7, 10.1 and 22.3% in the quartiles of BMI
The prevalence of metabolic syndrome using modified groups, respectively. The prevalence of metabolic syndrome was also
criteria, BMI, and HOMA-IR groups in quartiles (o0.93, increasing with the increments of BMI quartiles (test for trend, Po0.01).
0.93–1.39, 1.40–2.13, X2.14 in HOMA-IR and o21.2, 21.2–
22.7, 22.8–25.0, X25.1 kg/m2 in BMI) is shown in Figure 1.
We find that the prevalence of metabolic syndrome ranges 0.7 to 22.3% in the quartiles of BMI groups. The prevalence
from 1.4 to 23.0% in the quartiles of HOMA-IR groups. The of metabolic syndrome also increases with the increments of
prevalence of metabolic syndrome increases with the incre- BMI quartiles (test for trend, Po0.01).
ments of HOMA-IR quartiles (test for trend, Po0.01). In The odds ratios of having metabolic syndrome using
addition, the prevalence of metabolic syndrome ranges from multiple logistic regression analysis with age, menopausal

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915
Table 3 Odds ratios (95% confidence interval) of having metabolic syndrome using the modified NCEP criteria derived from a multiple logistic regression analysis
using age, menopause, BMI groups, and HOMA-IR groups as independent variables

Model 1 Model 2 Model 3 Model 4 Model 5

a w
Menopause 2.56 (1.44–4.56) 1.30 (0.61–2.81) 1.33 (0.62–2.86) 2.18 (066–7.24) 2.04 (0.61–6.83)
Age (years) F 1.10 (1.03–1.18)w 1.06 (0.99–1.14) 1.09 (0.98–1.22) 1.10 (0.98–1.22)
BMI (1) F F 1.00 (Reference) F 1.00 (Reference)
BMI (2) F F 3.88 (0.43–35.1) F 1.34 (0.12–14.6)
BMI (3) F F 13.3 (1.73–102.9)* F 2.13 (0.23–20.0)
BMI (4) F F 34.1 (4.58–254.3)w F 3.80 (0.42–34.2)
HOMA-IR (1) F F F 1.00 (Reference) 1.00 (Reference)
HOMA-IR (2) F F F 1.85 (0.16–21.2) 1.34 (0.11–16.1)
HOMA-IR (3) F F F 5.31 (0.60–47.2) 3.81 (0.41–35.8)
HOMA-IR (4) F F F 20.7 (2.64–162.2)w 12.1 (1.42–103.1)*

*Po0.05, wPo0.01, zPo0.001. aReference was pre-menopausal women. BMI and HOMA-IR were grouped in quartiles (o21.2, 21.2–22.7, 22.8–25.0, X25.1 kg/m2
in BMI, and o0.92, 0.93–1.39, 1.40–2.13, X2.14 in HOMA-IR). Group 1 is the lowest (reference), and Group 4 is the highest group.

status, BMI, and HOMA-IR quartiles as independent variables atherogenic lipid profile, and high blood pressure.12,28–30
are shown in Table 3. With age, menopausal status, and BMI The emergence of these CVD risk factors may be a direct
quartiles as the independent variables, the odds ratios of result of ovarian failure, or an indirect result of the metabolic
having metabolic syndrome increase with the increments of consequences of body fat centralization with estrogen
BMI groups in model 3. With age, menopausal status, and deficiency. Previous studies have also demonstrated that
HOMA-IR quartiles as the independent variables, the odds menopause is associated with a modest increase in total
ratios of having metabolic syndrome increase with the fatness and an accelerated accumulation of central body fat
increments of HOMA-IR groups in model 4. However, only that exceeds changes normally attributed to the aging
the highest HOMA quartile is significantly associated with process.28 Similarly in our studies, post-menopausal women,
the odds ratio of metabolic syndrome when putting age, when compared to pre-menopausal women, had a higher
menopausal status, BMI and HOMA-IR groups into the WC, plasma triglycerides level and blood pressure (Table 1).
independent variables in model 5. Although menopausal In addition, most studies have shown that plasma HDL-C
status is significantly associated with the metabolic syn- levels either fall slightly12,13,31 or remain stable11 with
drome in model 1 (Po0.01), no statistical significance of menopause. However, plasma HDL-C levels have been found
menopausal status versus the metabolic syndrome was found to increase with menopause in Koreans and Iranians.29,32 In
in other models. our study, plasma HDL-C level increased with menopause
and the prevalence of low HDL-C decreased with menopause
(Tables 1 and 2).
The literature to date is not clear as to whether menopause
Discussion itself is directly associated with increased insulin resistance.
Lindheim et al.,33 for example, have found reduced insulin
Post-menopausal women have been found to be at higher sensitivity (i.e. higher insulin resistance) in post-menopausal
risk for metabolic syndrome than pre-menopausal women in women, compared with BMI-matched pre-menopausal
Americans.27 Similarly in our study, we also demonstrated women. However, others have shown no significant differ-
that the prevalence of metabolic syndrome was higher in ence in insulin sensitivity among post-menopausal women
post-menopausal than pre-menopausal women (9.4 versus compared to pre-menopausal women.34,35 In our study, there
4.2% using the NCEP criteria, and 13.7 versus 5.8% using the was no significant difference in fasting plasma glucose,
modified NCEP criteria). Furthermore, we found that both insulin levels, HOMA-IR, and prevalence of hyperglycemia
BMI and insulin resistance index were independently between pre-menopausal and post-menopausal women
associated with the prevalence of metabolic syndrome in (Tables 1 and 2).
non-diabetic, aged 40–64 years women. However, with It has been recognized that the underlying pathophysiol-
adjustment for age, BMI, insulin resistance, there was an ogy of metabolic syndrome is related to hyperinsulinemia
increased odds ratio of having metabolic syndrome without and insulin resistance.1,22–24,36 However, other studies have
statistically significant difference in post-menopausal wo- shown that obesity is the central feature of metabolic
men. It could be due to the small sample size or multi- syndrome.37,38 In our study, both BMI and insulin resistance
colinearity in these variables in our study. index were independently associated with the prevalence of
The transition from pre- to post-menopause may be metabolic syndrome in non-diabetic middle-aged women,
associated with features of the metabolic syndrome, includ- adjusted for age and menopausal status (Table 3). Therefore,
ing an increased central body fat, a shift toward a more our results implicated that insulin resistance and obesity

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were related to the development of metabolic syndrome. cardiovascular disease mortality in middle-aged men. JAMA 2002;
However, when putting BMI and HOMA-IR together into 288: 2709–2716.
3 Ford ES, Giles WH, Dietz WH. Prevalence of the metabolic
model 5 in Table 3, we found that only HOMA-IR was
syndrome among US adults: findings from the third National
associated with the prevalence of metabolic syndrome with Health and Nutrition Examination Survey. JAMA 2002; 287:
statistically significant difference although the prevalence of 356–359.
metabolic syndrome increased with an increment of BMI 4 Panagiotakos DB, Pitsavos C, Chrysohoou C, Skoumas J, Tousou-
lis D, Toutouza M et al. Impact of lifestyle habits on the
without statistical significance. It could be due to the small prevalence of the metabolic syndrome among Greek adults from
sample size or multicolinearity between BMI and HOMA-IR the ATTICA study. Am Heart J 2004; 147: 106–112.
in our study. 5 Gu D, Reynolds K, Wu X, Chen J, Duan X, Reynolds RF et al.
Although CVD risk increases with metabolic syndrome in Prevalence of the metabolic syndrome and overweight among
adults in China. Lancet 2005; 365: 1398–1405.
western countries,1,2 it remains unclear whether metabolic 6 Tan CE, Ma S, Wai D, Chew SK, Tai ES. Can we apply the National
syndrome can predict CVD independently in Asians from Cholesterol Education Program Adult Treatment Panel definition
the limited evidences of prospective studies. In a 7-year study of the metabolic syndrome to Asians? Diabet Care 2004; 27:
among the middle-aged Japanese, for examples, clustered 1182–1186.
7 Park HS, Oh SW, Cho SI, Choi WH, Kim YS. The metabolic
features of the metabolic syndrome are closely associated syndrome and associated lifestyle factors among South Korean
with development of CVD.39 In contrast, metabolic syn- adults. Int J Epidemiol 2004; 33: 328–336.
drome does not predict CVD independently of other 8 Kahn R, Buse J, Ferrannini E, Stern M. The metabolic syndrome:
time for a critical appraisal: joint statement from the American
established CVD risk factors in the non-diabetic American
Diabetes Association and the European Association for the Study
Indians.40 Recently, the NCEP-defined metabolic syndrome of Diabetes. Diabet Care 2005; 28: 2289–2304.
predicts the 8-year CVD risk in Japanese men with type 2 9 Patel A, Huang KC, Janus ED, Gill T, Neal B, Suriyawongpaisal P
diabetes, but not in women with type 2 diabetes.41 It is et al. Is a single definition of the metabolic syndrome appro-
priate? A comparative study of the USA and Asia. Atherosclerosis
possible that the (modified) NCEP definition identifies a
2006; 184: 225–232.
heterogeneous group of individuals with the metabolic 10 Thom TJ. International mortality from heart disease: rates and
syndrome in different populations.9 Therefore, ethnic- trends. Int J Epidemiol 1989; 18: S20–8.
specific definitions of metabolic syndrome are warranted in 11 Kannel WB, Hjortland MC, McNamara PM, Gordon T. Meno-
pause and risk of cardiovascular disease: the Framingham study.
an attempt to adapt for global use. Ann Intern Med 1976; 85: 447–452.
In conclusion, we have demonstrated that the prevalence 12 Matthews KA, Meilahn E, Kuller LH, Kelsey SF, Caggiula AW,
of metabolic syndrome was higher in post-menopausal than Wing RR. Menopause and risk factors for coronary heart disease.
pre-menopausal women, using either the NCEP or modified New Engl J Med 1989; 321: 641–646.
13 Torng PL, Su TC, Sung FC, Chien KL, Huang SC, Chow SN et al.
NCEP criteria. BMI and insulin resistance were positively
Effects of menopause and obesity on lipid profiles in middle-aged
associated with the odds ratios of having metabolic syn- Taiwanese women: the Chin-Shan Community Cardiovascular
drome in the non-diabetic, middle-aged Taiwanese women. Cohort Study. Atherosclerosis 2000; 153: 413–421.
However, our study was limited by the cross-sectional design 14 Carr MC. The emergence of the metabolic syndrome with
menopause. J Clin Endocrinol Metab 2003; 88: 2404–2411.
and potentially biased from the subjects. Further research
15 Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg
may be required as to whether the transition to menopause C, Stefanick ML et al. Risks and benefits of estrogen plus progestin
increases CVD risk in all women or only those who develop in healthy postmenopausal women: principal results From the
features of the metabolic syndrome. Furthermore, a better Women’s Health Initiative randomized controlled trial. JAMA
2002; 288: 321–333.
understanding of these metabolic changes with menopause
16 James PT, Leach R, Kalamara E, Shayeghi M. The worldwide
may aid in the recognition and treatment of women at risk obesity epidemic. Obes Res 2001; 9: 228s–233s.
for CVD. 17 Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and
trends in obesity among US adults, 1999–2000. JAMA 2002; 288:
1723–1727.
18 Calle EE, Thun MJ, Petrelli JM, Rodriguez C, Heath Jr CW. Body-
Acknowledgements mass index and mortality in a prospective cohort of U.S. adults.
N Engl J Med 1999; 341: 1097–1105.
This study was funded by the National Science Council of 19 Lin WY, Lee LT, Chen CY, Lo H, Hsia HH, Liu IL et al. Optimal cut-
Taiwan (NSC 89-2314-B-002-094). We thank Dr Patty Li for off values for obesity: using simple anthropometric indices to
predict cardiovascular risk factors in Taiwan. Int J Obes Relat Metab
kindly reviewing this manuscript. We also thank Miss Hsu, Disord 2002; 26: 1232–1238.
Mei-Yu and Mr. Chan Inn-Jei for technical assistance. 20 Bray GA. Medical consequences of obesity. J Clin Endocrinol Metab
2004; 89: 2583–2589.
21 Huang KC, Lin WY, Lee LT, Chen CY, Lo H, Hsia HH et al. Four
anthropometric indices and cardiovascular risk factors in Taiwan.
References Int J Obes Relat Metab Disord 2002; 26: 1060–1068.
22 Alberti KG, Zimmet PZ. Definition, diagnosis and classification of
1 Haffner SM, Valdez RA, Hazuda HP, Mitchell BD, Morales PA, diabetes mellitus and its complications. Part 1: diagnosis and
Stern MP. Prospective analysis of the insulin-resistance syndrome classification of diabetes mellitus provisional report of a WHO
(syndrome X). Diabetes 1992; 41: 715–722. consultation. Diabet Med 1998; 15: 539–553.
2 Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, 23 National Cholesterol Education Program. Executive summary
Tuomilehto J et al. The metabolic syndrome and total and of the third report of the National Cholesterol Education

International Journal of Obesity


Menopause and metabolic syndrome
W-Y Lin et al
917
Program(NCEP) Expert panel on detection, evaluation, and 33 Lindheim SR, Buchanan TA, Duffy DM, Vijod MA, Kojima T,
treatment of high blood cholesterol in adults(Adult Treatment Stanczyk FZ et al. Comparison of estimates of insulin sensitivity
Panel III). JAMA 2001; 285: 2486–2497. in pre- and postmenopausal women using the insulin tolerance
24 Cheal KL, Abbasi F, Lamendola C, McLaughlin T, Reaven GM, test and the frequently sampled intravenous glucose tolerance
Ford ES. Relationship to insulin resistance of the adult treatment test. J Soc Gynecol Investig 1994; 1: 150–154.
panel III diagnostic criteria for identification of the metabolic 34 Walton C, Godsland IF, Proudler AJ, Wynn V, Stevenson JC. The
syndrome. Diabetes 2004; 53: 1195–1200. effects of the menopause on insulin sensitivity, secretion and
25 WHO Expert Panel. Appropriate body-mass index for Asian elimination in non-obese, healthy women. Eur J Clin Invest 1993;
populations and its implications for policy and intervention 23: 466–473.
strategies. Lancet 2004; 363: 157–163. 35 Toth MJ, Sites CK, Eltabbakh GH, Poehlman ET. Effect of
26 Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, menopausal status on insulin-stimulated glucose disposal:
Turner RC. Homeostasis model assessment: insulin resistance and comparison of middle-aged premenopausal and early postmeno-
beta-cell function from fasting plasma glucose and insulin pausal women. Diabet Care 2000; 23: 801–806.
concentrations in man. Diabetologia 1985; 28: 412–419. 36 Ferrannini E, Haffner SM, Mitchell BD, Stern MP. Hyperinsuli-
27 Park YW, Zhu S, Palaniappan L, Heshka S, Carnethon MR, naemia: the key feature of a cardiovascular and metabolic
Heymsfield SB. The metabolic syndrome: prevalence and asso- syndrome. Diabetologia 1991; 34: 416–422.
ciated risk factor findings in the US population from the Third 37 Bjorntorp P. Abdominal obesity and the metabolic syndrome.
National Health and Nutrition Examination Survey, 1988–1994. Ann Med 1992; 24: 465–468.
Arch Intern Med 2003; 163: 427–436. 38 Maison P, Byrne CD, Hales CN, Day NE, Wareham NJ. Do
28 Toth MJ, Tchernof A, Sites CK, Poehlman ET. Effect of meno- different dimensions of the metabolic syndrome change together
pausal status on body composition and abdominal fat over time? Evidence supporting obesity as the central feature.
distribution. Int J Obes Relat Metab Disord 2000; 24: 226–231. Diabet Care 2001; 24: 1758–1763.
29 Azizi F, Ainy E. Coronary heart disease risk factors and 39 Nakanishi N, Takatorige T, Fukuda H, Shirai K, Li W, Okamoto M
menopause: a study in 1980 Tehranian women, the Tehran Lipid et al. Components of the metabolic syndrome as predictors of
and Glucose Study. Climacteric 2003; 6: 330–336. cardiovascular disease and type 2 diabetes in middle-aged
30 Reckelhoff JF, Fortepiani LA. Novel mechanisms responsible Japanese men. Diabetes Res Clin Pract 2004; 64: 59–70.
for postmenopausal hypertension. Hypertension 2004; 43: 40 Resnick HE, Jones K, Ruotolo G, Jain AK, Henderson J, Lu W et al.
918–923. Insulin resistance, the metabolic syndrome, and risk of incident
31 Torng PL, Su TC, Sung FC, Chien KL, Huang SC, Chow SN et al. cardiovascular disease in nondiabetic american indians: the
Effects of menopause on intraindividual changes in serum lipids, Strong Heart Study. Diabet Care 2003; 26: 861–867.
blood pressure, and body weight–the Chin-Shan Community 41 Sone H, Mizuno S, Fujii H, Yoshimura Y, Yamasaki Y, Ishibashi S
Cardiovascular Cohort study. Atherosclerosis 2002; 161: 409–415. et al. Is the diagnosis of metabolic syndrome useful for predicting
32 Kim CJ, Kim TH, Ryu WS, Ryoo UH. Influence of menopause on cardiovascular disease in asian diabetic patients? Analysis from
high density lipoprotein-cholesterol and lipids. J Korean Med Sci the Japan Diabetes Complications Study. Diabet Care 2005; 28:
2000; 15: 380–386. 1463–1471.

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