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ORIGINAL ARTICLE

Higher Prevalence of Type 2 Diabetes in Men Than


in Women Is Associated With Differences in
Visceral Fat Mass

Anna Nordström*, Jenny Hadrévi, Tommy Olsson, Paul W. Franks,


and Peter Nordström
Department of Public Health and Clinical Medicine, Occupational and Environmental Medicine (A.N.),
Department of Community Medicine and Rehabilitation, Sports Medicine (J.H.), Department of Public
Health and Clinical Medicine, Medicine (T.O.), Umeå University, Umeå, Sweden; Department of Clinical
Sciences (P.W.F.), Genetic and Molecular Epidemiology Unit (P.F.W.), Lund University Diabetes Centre,
Malmö, Sweden; Department of Nutrition (P.W.F.), Harvard School of Public Health, Boston,
Massachusetts 02115; Department of Public Health and Clinical Medicine (P.W.F.); and Department of
Community Medicine and Rehabilitation, Geriatrics (P.N.), Umeå University, Umeå, Sweden

Context: We have previously found that visceral fat is a stronger predictor for cardiovascular risk
factors than body mass index (BMI).

Objective: This study sought to investigate the prevalence of diabetes in elderly men and women
in relation to objectively assessed visceral fat volume.

Design and Setting: The cohort consisted of a population-based sample of 705 men and 688
women, all age 70 y at the time of examination.

Main Outcome Measures: Associations between body fat estimates, plasma glucose level, and
diabetes prevalence were investigated using multivariable-adjusted statistical models.

Results: The prevalence of type 2 diabetes was 14.6% in men and 9.1% in women (P ⬍ .001). Mean
BMI was slightly higher in men than in women (27.3 vs 26.6 kg/m2; P ⫽ .01), with a greater difference
in mean visceral fat mass (1987 vs 1077 g; P ⬍ .001). After adjustment for physical activity and
smoking, men had about/approximately twice the odds of having type 2 diabetes compared with
women (odds ratio [OR], 1.95; 95% confidence interval [CI], 1.38 –2.76). The inclusion of BMI in this
model did not change the risk associated with male sex (OR, 1.93; 95% CI, 1.34 –2.77). However,
when visceral fat was included as a covariate, male sex was not associated with increased risk of type
2 diabetes (OR, 0.77; 95% CI, 0.51–1.18).

Conclusions: The higher prevalence of type 2 diabetes in older men than in older women was
associated with larger amount of visceral fat in men. In contrast, differences in BMI was not
associated with this difference. (J Clin Endocrinol Metab 101: 3740 –3746, 2016)

he prevalence of type 2 diabetes is growing world- population is considered to be overweight (3). The in-
T wide; approximately 382 million people (8.3% of
the global population) had the disease in 2013, and this
terplay between these two diseases, however, is not fully
understood (4).
number is estimated to exceed 592 million in less than In recent years, male sex has been regarded as a risk
25 years (1, 2). The prevalence of obesity is increasing factor for the development of type 2 diabetes (5–10). The
concomitantly, and today more than half of the world’s reason that men are more prone than women to the de-

ISSN Print 0021-972X ISSN Online 1945-7197 Abbreviations: BMI, body mass index; CI, confidence interval; HAI, Healthy Aging Initiative;
Printed in USA HDL, high-density lipoprotein; OR, odds ratio.
Copyright © 2016 by the Endocrine Society
Received April 18, 2016. Accepted July 27, 2016.
First Published Online August 4, 2016

3740 press.endocrine.org/journal/jcem J Clin Endocrinol Metab, October 2016, 101(10):3740 –3746 doi: 10.1210/jc.2016-1915

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velopment of this disease is not known. The increasing Waist circumference was measured at the umbilical level, and hip
prevalence of obesity in general may be a contributing circumference was measured at the widest part of the buttocks.
Both circumferences were measured with a tape and expressed in
factor. However, the prevalence of obesity seems to be
centimeters. The measurements were taken at the end of normal
higher in women than in men (11, 12), and men seem to expiration, while the subject was standing relaxed with his/her
be at greater risk of type 2 diabetes development than weight distributed evenly on both feet. BMI was calculated as
are women with similar BMIs (13, 14). Some of these body weight (in kilograms) divided by the square of height (in
inconsistencies may be explained by the surrogate na- meters). To measure visceral fat mass, and thus distinguish vis-
ture of body mass index (BMI) as an estimate of adi- ceral fat from sc fat in the abdominal region, dual-energy x-ray
absorptiometry was performed with a Lunar iDXA and the Co-
posity (15, 16).
reScan application (GE Healthcare). The results were derived in
A growing body of evidence suggests that central obesity, grams and cubic centimeters. In addition, total fat mass was
or visceral adiposity, is a stronger risk factor for diabetes type derived from total-body scans, and the amount of gynoid fat was
2 than BMI (17, 18). Central obesity has also been found to estimated automatically using the region of interest program.
be a stronger risk factor glucose intolerance, insulin resis- Subjects were instructed to wear light clothing with no metal
objects. Quality assurance testing of the iDXA device was per-
tance, metabolic perturbations, and hyperinsulinemia than
formed daily using standard procedures. For the different esti-
BMI (19 –21). Hypothetically, central obesity could be as- mates of fat mass, coefficients of variation (SD/mean) were
sociated with the higher risk of diabetes type 2 prevalence in 1–3%, depending on the application. Participants were also
men, given that men are more prone to android adiposity asked to complete an extensive questionnaire with items regard-
with greater abdominal adiposity, compared with women ing lifestyle, medical history, and injuries.
who are more likely to exhibit gynoid adiposity (22). After the initial clinical investigation, participants were asked
to wear a triaxial accelerometer (GT3X⫹; Actigraph) for 7 days
The aim of the present study was to assess the associ-
on their nondominant hip and to remove it only when showering,
ation of visceral and other estimates of adiposity with the swimming, or going to bed at night. For the present analysis,
prevalence of diabetes type 2 and evaluate whether the accelerometer data were converted to metabolic equivalents–
association differs in men and women. minutes (23, 24).
Participants made return visits 1 week later to receive feed-
back regarding their test results.
Blood samples were collected after at least 4 hours of fasting
Materials and Methods for the assessment of total, low-density lipoprotein, and high-
density lipoprotein (HDL) cholesterol (venous samples) and trig-
Subjects lycerides and plasma (p-)glucose (capillary samples). Trained
All participants in the present study were part of the Healthy personnel collected samples according to established sterile pro-
Aging Initiative (HAI) project, a population-based prospective tocols. Plasma and serum were separated by centrifugation 30
study with the overall aim of identifying risk factors for cardiovas- minutes after sample collection, at 3000 rpm and 20°C for 15
cular disease, diabetes, and fractures among 70-year-old men and minutes. Serum lipids were then analyzed using standard meth-
women. The study had two inclusion criteria; residence in the city ods at the Department of Clinical Chemistry, Umeå University
of Umeå, public area of Västerbotten County, northern Sweden; Hospital. p-glucose was analyzed with a HemoCue Glucose 201
and age of 70 years at the time of investigation (for more informa- RT (HemoCue AB, Ängelholm, Sweden) according to the user’s
tion, see www.healthyageinginitiative.com). Participants were se- manual; the machine was calibrated twice a week.
lected through population registers and initially received written The diagnosis of type 2 diabetes was based on questionnaire
information about the study by mail, which was followed up by responses or fasting p-glucose level of at least 7 mmol/L.
telephone contact approximately 2 weeks later. Participants who
agreed to attend were scheduled to do so on a date of their choosing.
Statistical analysis
The present study involved the first 1393 participants who com-
Data are presented as means and SDs, unless indicated oth-
pleted testing. Approximately 70% of those who received written
erwise. To test for nonlinear associations, Wald’s test was used.
information about the study agreed to participate.
Associations of different estimates of adiposity with glucose lev-
els and the prevalence of type 2 diabetes were investigated using
Ethical considerations linear and logistic regression, respectively. The outcomes of the
All participants received written and oral information about models were p-glucose and type 2 diabetes, respectively. The first
the study, and gave written consent to participate. The ethics of these models included only the different estimates of adiposity
committee of Umeå University, Umeå, Sweden, provided ethical as the exposures, and the second model additionally included
approval. data on physical activity and smoking. In the final models, we
additionally included previous myocardial infarction (MI) and
Clinical examination stroke, cholesterol, HDL, triglycerides, systolic and diastolic
Participants arrived at the test facility at 0830 1230 hours. blood pressures, given that many of these covariates likely me-
After verifying their identities and obtaining written consent, diate the association between the main exposure of adiposity and
testing was initiated. Systolic and diastolic blood pressures were the outcomes of p-glucose and type 2 diabetes. To further illus-
measured using a mercury-gauge sphygmomanometer, with the trate the relationship between visceral fat and type 2 diabetes in
patient seated in an upright position after at least 5 minutes’ rest. men and women separately, a three-knot logistic regression

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3742 Nordström et al Visceral Fat and Diabetes J Clin Endocrinol Metab, October 2016, 101(10):3740 –3746

Table 1. Baseline Characteristics of the Study Cohort Presented as Mean and SD


Men (n ⴝ 705) Women (n ⴝ 688) P
Age, y 70 70 1.00
Weight, kg 84.4 ⫾ 12.7 71.2 ⫾ 13.2 ⬍.001
Height, cm 176 ⫾ 8 164 ⫾ 6 ⬍.001
Current smoking 4.4% 7.2% .02
Physical activity, METS 1.20 ⫾ 0.15 1.15 ⫾ 0.10 ⬍.001
Fasting plasma glucose, mmol/L 5.8 ⫾ 1.1 5.5 ⫾ 1.2 ⬍.001
Cholesterol, mmol/L 5.0 ⫾ 1.1 5.8 ⫾ 1.1 ⬍.001
HDL cholesterol, mmol/L 1.30 ⫾ 0.37 1.59 ⫾ 0.42 ⬍.001
Triglycerides, mmol/L 1.42 ⫾ 0.81 1.35 ⫾ 0.62 .07
Systolic blood pressure, mm/Hg 138 ⫾ 16 143 ⫾ 17 ⬍.001
Diastolic blood pressure, mm/Hg 80 ⫾ 9 80 ⫾ 9 .57
Diagnoses at baseline, n (%)
Diabetes 104 (14.6%) 63 (9.1%) .001
MI 81 (11.4%) 19 (2.7%) ⬍.001
Stroke 40 (5.6%) 15 (2.2%) .001
Variables associated with obesity
BMI, kg/m2 27.3 ⫾ 5.4 26.6 ⫾ 4.8 .01
Waist circumference, cm 100 ⫾ 12 90 ⫾ 13 ⬍.001
Hip circumference, cm 103 ⫾ 7 103 ⫾ 9 .12
Total fat mass, kg 26.4 ⫾ 8.4 28.8 ⫾ 9.2 ⬍.001
Gynoid fat mass, g 3414 ⫾ 1098 4570 ⫾ 1389 ⬍.001
Gynoid fat mass/body weight 39.5 ⫾ 7.6 63.2 ⫾ 10.3 ⬍.001
Visceral fat mass, g 1987 ⫾ 1043 1077 ⫾ 682 ⬍.001
Visceral fat mass/body weight 22.5 ⫾ 9.6 14.4 ⫾ 7.5 ⬍.001
METS, metabolic equivalents.

model was constructed using the mkspline command in Stata tics, lifestyle factors, and different estimates of body adi-
software (version 12.1; StataCorp LP). For all analyses, P ⬍ .05 posity are presented in Table 1. Less men than women
was considered to be significant. Stata and SPSS (version 21;
smoked, and men had higher p-glucose levels and more
IBM) software was used to fit the statistical models and graph-
ically illustrate the results. previous MIs, strokes, and type 2 diabetes compared with
women. Men also had slightly higher BMI (P ⫽ .01),
whereas the differences in amounts of visceral fat and vis-
Results ceral fat per kilogram body weight were greater than in
women (both P ⬍ .001). In contrast, women were found
The study population comprised 1393 participants (705 to have higher total fat mass, gynoid fat mass, and gynoid
men and 688 women, all age 70 y). Physical characteris- fat mass per kilogram body weight
(all P ⬍ .001). Of 167 cases of type 2
diabetes in the study cohort, 41 were
detected for the first time during the
HAI investigation. These 41 patients
did not differ from those with known
type 2 diabetes at baseline (n ⫽ 126) in
BMI (30.1 vs 30.2 kg/m2), total fat
mass (31.9 vs 33.1 kg), gynoid fat
mass (4156 vs 4528 g), or amount of
visceral fat (2551 vs 2322 g; all
P ⬎ .05).
Figure 1 illustrates the associa-
tions between p-glucose and visceral
fat per kilogram body weight. Before
and after adjustment for physical ac-
tivity and smoking, visceral fat was
the strongest predictor of p-glucose
Figure 1. Associations between visceral fat per kilogram body weight and plasma glucose in in men (adjusted B ⫽ 0.42 per SD
men and women, showing the absence of a sex difference. increase; P ⬍ .001) and women (ad-

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Table 2. Associations Between Different Estimates of Obesity and Plasma-glucose and Diabetes Presented as OR
Unadjusted Analyses

Men (n ⴝ 705) Women (n ⴝ 688)


B 95% CI B 95% CI P Interaction
a
Exposure Outcome: plasma glucose level
BMI 0.33 0.24 – 0.42 0.17 0.09 – 0.25 .007
Waist circumference 0.37 0.28 – 0.47 0.22 0.14 – 0.31 .02
Hip circumference 0.23 0.13–32 0.15 0.07– 0.23 .21
Total fat mass 0.3 0.22– 0.38 0.19 0.10 – 0.27 .06
Gynoid fat mass 0.25 0.16 – 0.34 0.14 0.04 – 0.24 .11
Gynoid fat mass/body weight 0.12 0.04 – 0.21 0.03 0.05 .12
Visceral fat mass 0.41 0.32– 0.50 0.24 0.14 – 0.34 .02
Visceral fat mass/body weight 0.38 0.29 – 0.47 0.21 0.11– 0.41 .01
Analyses adjusted for physical activity and smoking
BMI 0.34 0.25– 0.43 0.17 0.09 – 0.25 .005
Waist circumference 0.37 0.27– 0.47 0.22 0.14 – 0.31 .02
Hip circumference 0.23 0.13– 0.33 0.16 0.09 – 0.24 .28
Total fat mass 0.31 0.22– 0.39 0.2 0.11– 0.29 .07
Gynoid fat mass 0.25 0.16 – 0.34 0.17 0.07– 0.27 .25
Gynoid fat mass/body weight 0.12 0.03– 0.21 0.05 0.1 .28
Visceral fat mass 0.42 0.33– 0.51 0.23 0.13– 0.34 .009
Visceral fat mass/body weight 0.39 0.30 – 0.48 0.19 0.09 – 0.29 .004
Fully adjusted analysesb
BMI 0.32 0.21– 0.44 0.08 0.16 ⬍.001
Waist circumference 0.35 0.22– 0.47 0.12 0.02– 0.23 .001
Hip circumference 0.18 0.07– 0.30 0.09 0.00 – 0.18 .04
Total fat mass 0.27 0.16 – 0.38 0.1 0.00 – 0.21 .06
Gynoid fat mass 0.2 0.08 – 0.31 0.05 0.09 .03
Gynoid fat mass/body weight 0.07 0.15 0.01 ⫺0.03 .16
Visceral fat mass 0.42 0.30 – 0.54 0.15 0.02– 0.27 ⬍.001
Visceral fat mass/body weight 0.4 0.29 – 0.52 0.13 0.01– 0.25 ⬍.001
Outcome: diabetes
BMI 2.62 1.99 –3.44 1.89 1.46 –2.45 .09
Waist circumference 3.1 2.31– 4.16 2.05 1.59 –2.65 .04
Hip circumference 1.98 1.52–2.58 1.51 1.19 –1.92 .13
Total fat mass 2.38 1.86 –3.05 1.7 1.30 –2.23 .07
Gynoid fat mass 2.02 1.59 –2.57 1.54 1.14 –2.08 .17
Gynoid fat mass/body weight 1.48 1.19 –1.84 1.08 0.83–1.42 .08
Visceral fat mass 3.4 2.54 – 4.54 2.04 1.47–2.84 .02
Visceral fat mass/body weight 3 2.28 –3.94 1.82 1.31–2.53 .02
Analyses adjusted for physical activity and smoking
BMI 2.52 1.91–3.33 1.79 1.37–2.34 .08
Waist circumference 2.92 2.17–3.94 1.98 1.52–2.60 .06
Hip circumference 1.91 1.46 –2.49 1.49 1.17–1.91 .2
Total fat mass 2.26 1.76 –2.91 1.63 1.22–2.16 .1
Gynoid fat mass 1.91 1.49 –2.45 1.53 1.11–2.09 .32
Gynoid fat mass/body weight 1.4 1.12–1.75 1.08 0.82–1.43 .19
Visceral fat mass 3.24 2.41– 4.36 1.86 1.32–2.62 .02
Visceral fat mass/body weight 2.88 2.17–3.82 1.64 1.17–2.29 .01
Fully adjusted analysesb
BMI 2.26 1.61–3.17 1.42 1.00 –2.03 .04
Waist circumference 2.85 1.93– 4.19 1.44 1.01–2.05 .02
Hip circumference 1.78 1.27–2.50 1.15 0.84 –1.56 .08
Total fat mass 2.07 1.50 –2.87 1.14 0.78 –1.65 .03
Gynoid fat mass 1.64 1.20 –2.25 1.07 0.71–1.60 .13
Gynoid fat mass/body weight 1.23 0.93–1.62 0.93 0.64 –1.37 .19
Visceral fat mass 3.45 2.31–5.15 1.22 0.77–1.95 .001
Visceral fat mass/body weight 3.64 2.53–5.25 1.41 0.93–2.13 .001
a
Per SD increase.
b
Adjusted for smoking, physical activity, blood pressure, cholesterol, HDL, triglycerides, previous MI, and stroke.

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3744 Nordström et al Visceral Fat and Diabetes J Clin Endocrinol Metab, October 2016, 101(10):3740 –3746

95% CI, 1.34 –1.77). In contrast, no


significant association between male
sex and type 2 diabetes prevalence
was observed in analyses including
visceral fat (OR, 0.77; 95% CI,
0.51–1.18) and visceral fat per kilo-
gram body weight (OR, 0.93; 95%
CI, 0.62–1.40).

Discussion
In the present population-based co-
hort of 70-year-olds, p-glucose levels
and type 2 diabetes prevalence were
higher in men than in women. Fur-
thermore, visceral fat was generally
Figure 2. Associations between visceral fat per kilogram body weight and diabetes prevalence,
the strongest predictor of p-glucose
showing the absence of a sex difference. level and type 2 diabetes compared
with other estimates of obesity, such
justed B ⫽ 0.23 per SD increase; P ⬍ .001; Table 2). Anal- as BMI, and the associations were stronger in men than in
yses of interaction suggested that most associations be- women. Importantly, after adjusting for the larger amount
tween p-glucose and the different estimates of obesity were of visceral fat in men, the risk of type 2 diabetes was similar
stronger in men than in women. In unadjusted analyses, in men and women.
the amount of visceral fat was the strongest predictor of Recent studies have found a higher prevalence of type
type 2 diabetes prevalence in men (odds ratio [OR], 3.00; 2 diabetes in men than in women (6, 25, 26), but the reason
95% confidence interval [CI], 2.28 –3.94) whereas vis- for this difference has been unclear. In the present cohort
ceral fat (OR, 2.04; 95% CI, 1.47–2.84) and waist cir- of elderly individuals, the mean amounts of visceral fat
cumference were the best predictors of this outcome in were approximately 2 kg in men and 1 kg in women. In
women (OR, 2.05; 95% CI, 1.59 –2.65; Table 2). The contrast, women had more total fat and gynoid fat. After
associations between visceral fat per kilogram, total body controlling for the influence of visceral fat on the sex-
weight and type 2 diabetes prevalence are presented in specific prevalence, men and women were found to have
Figure 2; the association was significantly stronger in men similar risks of type 2 diabetes. Our data are supported by
than in women (P ⫽ .02). Although the figure suggests a a recent study reporting a prevalence of type 2 diabetes in
nonlinear relationship in women, this was not significant 4% of women and 8% of men, in a sample of individuals
(Wald’s test, P ⫽ .11). After adjusting for physical activity with a large age variation (19 – 81 y) (27). This difference
and smoking, the amount of visceral fat remained the best
predictor of type 2 diabetes prevalence in men (OR, 3.24;
95% CI, 2.41– 4.36), and waist circumference was the best Table 3. Associations Between Sex and Diabetes
predictor of this outcome in women (OR, 1.98; 95% CI, Prevalence, Adjusted for Confounders Presented as OR
1.52–2.60). In analyses including all covariates, other pre-
Outcome: Diabetes
dictors of type 2 diabetes prevalence included serum cho-
lesterol and triglyceride levels (both P ⬍ .05), and the Main exposure OR 95% CI
objective amount of physical activity, which was lower in Male sex 1.72 1.23–2.39
women with than in those without type 2 diabetes (P ⫽ Adjusted for:
.01). Physical activity and smoking 1.95 1.38 –2.76
And:
At baseline, type 2 diabetes was more prevalent in men BMI 1.93 1.34 –2.77
than in women (14.6 vs 9.1%; OR, 1.72; 95% CI, 1.23– Waist circumference 1.13 0.77–1.64
2.39; Table 3). Adjustment for smoking and physical ac- Hip circumference 2.21 1.54 –3.17
Total fat mass 2.39 1.66 –3.44
tivity increased the risk associated with male sex slightly Gynoid fat mass 3.12 2.10 – 4.63
(OR, 1.95; 95% CI, 1.38 –2.76). The additional inclusion Gynoid fat mass/body weight 3.56 1.98 – 6.41
of BMI in the analysis did not change the association be- Visceral fat mass 0.77 0.51–1.18
Visceral fat mass/body weight 0.93 0.62–1.40
tween male sex and type 2 diabetes prevalence (OR, 1.93;
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in diabetes prevalence was associated with a mean of 1.6 the present study also suggest that the higher type 2 dia-
kg visceral fat in men compared with 0.8 kg in women. betes prevalence in older men vs women is associated with
Notably, this sex difference in visceral fat mass was found differences in visceral fat accumulation, although it cannot
early in life, which may contribute to an increased risk of be concluded from the present study that the association
later type 2 diabetes development in men. With respect to is causal.
the observed sex differences in type 2 diabetes, recent find-
ings suggesting that the prevalence of obesity is increasing
more in men than in women are of interest (28, 29). Acknowledgments
The potential mechanisms linking obesity in general
and visceral obesity in particular to p-glucose levels and Address all correspondence and requests for reprints to: Anna
Nordström, PhD, Department of Public Health and Clinical
type 2 diabetes are not clear. The association between
Medicine, Occupational and Environmental Medicine, Umeå
visceral fat with insulin resistance in particular has been University, 901 87 Umeå, Sweden. E-mail: Anna.h.nordstrom@
linked to increased low-grade inflammation (30), exces- umu.se.
sive release of TNF-␣ (31, 32), and increased expression of This work was supported by the Swedish research council.
suppressor of cytokine signaling-3 (33). In addition, Fon- Disclosure Summary: The authors have nothing to disclose.
tana et al (34) showed that the concentration of IL-6 was
50% higher in the portal vein, which is in close conjunc-
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