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Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2016) xxx–xxx

Contents lists available at ScienceDirect

Diabetes & Metabolic Syndrome: Clinical Research &

Reviews
journal homepage: www.elsevier.com/locate/dsx

Original article

Association of obesity with hypertension and dyslipidemia in type 2

diabetes mellitus subjects
Razieh Anaria , Reza Amanib,* , Seyed Mahmoud Latific , Masoud Veissid ,
Hajieh Shahbazianc
a
Department of Nutrition, Faculty of Arvand International Division, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
b
Health Research Institute, Diabetes Research Center, Department of Nutrition, School of Paramedicine, Ahvaz Jundishapur University of Medical Sciences,
Ahvaz, Iran
c
Health Research Institute, Diabetes Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran
d
Health Research Institute, Nutrition and Metabolic Disease Research Center, Department of Nutrition, School of Paramedicine, Ahvaz Jundishapur University
of Medical Sciences, Ahvaz, Iran

A R T I C L E I N F O A B S T R A C T

Article history: Aim: Obesity and diabetes are contributed to cardiovascular disease risk. The current study was
Available online xxx performed to evaluate the association of central and general obesity and cardio-metabolic risk factors,
including dyslipidemia and hypertension in T2DM patients.
Methods: This was a cross-sectional study in T2DM adults. Body mass index (BMI) was used to identify
Keywords: general obesity and waist circumference (WC) was measured to define abdominal obesity (based on ATP
Central obesity
III). Biochemical analyses, and anthropometric and blood pressure measurements were done for all
Dyslipidemia
participants.
General obesity
Hypertension
Results: Participants with central obesity showed significantly higher systolic (132.5 mmHg vs.
T2DM 125.4 mmHg, p = 0.024) and diastolic blood pressures (84.9 mmHg vs. 80 mmHg, p = 0.007) than
participants without obesity. Dyslipidemia was more prevalent in all participants either by BMI (98.3% vs.
97%, 95% CI: 0.18–17.53) or by WC (97.2% vs. 98%, 95% CI: 0.07–7.19). Abdominal adiposity in diabetic
subjects showed significant reverse association with high level of physical activity (OR = 0.22, 95% CI:
0.06–0.85). Hypertriglyceridemia rate was increased with both central (OR = 2.11; p = 0.040) and general
obesity (OR = 2.68; p = 0.021). After adjustment for energy intake and age, females had higher risk of
general (OR = 4.57, 95% CI = 1.88–11.11) and central obesity (OR = 7.93, 95% CI = 3.48–18.08).
Conclusions: Females were more susceptible to obesity. Hypertension was associated with both obesity
measures. Dyslipidemia, except for hypertriglyceridemia, was correlated to neither abdominal nor
general obesity.
ã 2016 Diabetes India. Published by Elsevier Ltd. All rights reserved.

1. Introduction On the other hand, there is a mutual association between

obesity and diabetes. Type 2 diabetes mellitus (T2DM), the most
Obesity is correlated to some major metabolic abnormalities prevalent form of diabetes, accompanies with obesity [6]. Obesity
like hypertension [1]. It is supposed that obesity have some could also result in some degrees of insulin resistance which
contributions in hypertension, dyslipidemia and hyperglycemia, worsen the diabetes outcomes [6]. Patients with diabetes who
and is independently associated with higher cardiovascular (CVD) have obesity are at increased risk for long-term vascular outcomes
risk [2–4]. Abdominal obesity is the second risk factor for [7,8]. In 1999–2002, the prevalence of obesity (BMI 30 kg/m2)
myocardial infarction [5]. was 54.8% in the US T2DM patients [9]. There is a great discrepancy
in the rate of obesity in diabetic population around the world.
Various investigations have reported the general obesity preva-
* Corresponding author at: Health Research Institute, Diabetes Research Center, lence from 7.14% [10] to 85.5% [11]. A systematic review on
Department of Nutrition, School of Paramedicine, Ahvaz Jundishapur University of observational studies demonstrated that more than 70% of Asian
Medical Sciences, Ahvaz, Iran.
and more than 80% of European T2DM adults with obesity had
E-mail addresses: [email protected] (R. Anari), [email protected]
(R. Amani), [email protected] (S.M. Latifi), [email protected] (M. Veissi), hypertension [12].
[email protected] (H. Shahbazian).

http://dx.doi.org/10.1016/j.dsx.2016.07.004
1871-4021/ã 2016 Diabetes India. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: R. Anari, et al., Association of obesity with hypertension and dyslipidemia in type 2 diabetes mellitus subjects,
Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.07.004
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2 R. Anari et al. / Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2016) xxx–xxx

Both general adiposity and abdominal obesity are important levels. Standardized enzymatic colorimetric methods were per-
situations that influence the health. Up to now, several criteria formed to determine lipid profile (Pars Azmun kits, Pars Azmun
have been established to measure the obesity status. Some indices Co., Karaj, Iran). LDL-C levels were derived using Friedewald
are frequently utilized for obesity determination, however, there is equation [18].
no consensus on their application. Body mass index (BMI), the
highly used index for obesity estimation, could not properly reflect 2.4. Anthropometric data
body fat distribution, whereas the visceral deposition of fat is a
major contributor to development of hypertension, insulin Anthropometric measures were evaluated by a trained dieti-
resistance, DM and dyslipidemia [13,14]. Other anthropometric tian. Weight was measured using a digital scale to the nearest 100 g
indices such as waist circumference (WC) have been applied as (Omron 212, Omron Corp., range 0.1–150 kg, Germany). Partic-
alternatives for BMI. Waist circumference could indicate obesity ipants' height was assessed using a standard tape measure without
and some major metabolic risks [15,16]. shoes and recorded to the nearest millimeter. To calculate BMI,
With regards to a recent high prediction of CVD in Ahvaz T2DM weight in kilogram was divided by squared height in meter (kg/
patients [17], this study was carried out to examine any possible m2). WC was measured using a flexible tape measure at the
link between the two obesity indices and two major metabolic midpoint of belly between the lowest ribs and the iliac crest over
abnormalities, i.e. hypertension and dyslipidemia, in these light clothes without any pressure and was recorded to the nearest
patients. 0.1 centimeter. After 10 min resting in sitting position, systolic and
diastolic blood pressure levels were measured using a digital blood
1.1. Subjects pressure monitor (OMRON, model M3, Kyoto, Japan).

This cross-sectional study was carried out on T2DM adults 28– 2.5. Categories definition
75 years old (mean age: 54.5 years, N = 222). Study population was
collected from outpatients attending Diabetes Clinic of Golestan BMI equal to or more than 30 kg/m2 was identified as general
Hospital, Ahvaz, Khuzestan province, Iran (from January to April obesity [19]. Having WC  102 cm in men and  88 cm in women
2015). has been recognized as abdominal obesity according to ATP III
criterion [20]. Systolic blood pressure (SBP)  130 mmHg or
2. Materials and methods diastolic blood pressure (DBP)  85 mmHg or treatment with
antihypertensive medications were considered as hypertension
2.1. Ethics [21]. Serum HDL-C concentrations below 50 mg/dL in women and
below 40 mg/dL in men were considered as low HDL-C levels.
All participants were informed about the study procedure Serum TG 150 mg/dL was defined as hypertriglyceridemia
through a written consent form before participation. The study was [20,21]. Serum cholesterol levels  200 mg/ld. and LDL-C levels
complied with the Declaration of Helsinki and the research  100 mg/dL were considered as abnormal levels [22]. Dyslipide-
protocol was approved by the Ahvaz Jundishapur University of mia was described as high serum cholesterol, LDL-C, or TG levels, or
Medical Sciences Research Ethics Committee. low HDL-C or using lipid lowering medications [20,21].

2.2. Inclusion & exclusion criteria 2.6. Statistical analyses

Diabetic adults with no insulin treatment were entered the SPSS software version 21.0 was used to perform statistical
study. Diabetes had previously been diagnosed by a general analyses (SPSS Inc., Chicago, IL, USA). Quantitative variables were
practitioner [6]. Patients who had cancer or any serious disease, or presented as mean  standard deviation (SD), and categorical
being pregnant were excluded from the study. variables were declared as percentage. Categorical variables (e.g.
BMI and obesity indices) were compared using chi-squared test
2.3. Biochemical assays with 95% confidence interval. Two-tailed independent sample t-
test was used to compare serum lipids, blood pressures and
Fasting blood samples were drawn to measure serum choles- anthropometric values in two obesity categories. Two-tailed p-
terol (Chop), high density lipoprotein cholesterol (HDL-C), low values were applied to distinguish significant values and figures
density lipoprotein cholesterol (LDL-C) and triglycerides (TG) less than 0.05 were considered reliable.

Table 1
comparison of blood pressures and serum lipids in patients with and without obesity by BMI and waist circumference.

BMI WC
a c
Non-Obesity Obesity (n = 58) OR (95% CI) Non-Obesity (n = 49) Obesity b (n = 108) ORc (95% CI)
(n = 99)
SBP (mmHg) 129.35  18.76 131.93  19.32 1.01 (0.99–1.03) 125.39  15.32 132.54  20.05 1.03 (1.00–1.05)*
DBP (mmHg) 82.28  10.55 85.26  10.57 1.02 (0.99–1.06) 80.04  7.99 84.90  11.33 1.06 (1.02–1.11)*
TG (mg/dL) 152.94  98.36 161.21  62.91 1.00 (1.00–1.01) 141.90  98.61 162.39  80.61 1.00 (1.00–1.01)
HDL-C (mg/dL) 42.69  9.35 46.53  10.04 1.03 (0.99–1.07) 42.98  10.26 44.62  9.53 0.49 (0.95–1.03)
LDL-C (mg/dL) 97.99  31.66 98.05  29.57 1.00 (0.99–1.01) 99.27  31.74 97.45  30.51 1.00 (0.98–1.01)
Chol (mg/dL) 169.75  40.01 176.71  36.63 1.00 (0.99–1.01) 169.96  41.86 173.39  37.52 1.00 (0.99–1.01)

Values are mean  SD. *P < 0.05.

Chol Cholesterol; DBP diastolic blood pressure; HDL-C high density lipoprotein cholesterol; LDL-C low density lipoprotein cholesterol; SBP systolic blood pressure; TG
triglycerides.
a
BMI 30 kg/m2.
b
WC  102 cm in men and  88 cm in women [24].
c
After adjustment for energy intake, age and sex.

Please cite this article in press as: R. Anari, et al., Association of obesity with hypertension and dyslipidemia in type 2 diabetes mellitus subjects,
Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.07.004
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3. Results Body fat percent was 24% and 90% higher in participants with
central and general obesity, respectively (p < 0.001 for both,
Totally, 222 type 2 diabetic patients were enrolled the study Table 3). No association was found between physical activity
between January to April 2015. From all enrolled patients, 64 levels and general adiposity (p > 0.05, Table 3); however, it was
participants did not complete the study and one patient was near significant for central obesity (p = 0.085, Table 3). Also, after
excluded for overestimating the energy intake. Finally, 157 patients adjustment for confounding factors, patients with high level of
were included in the study. About two-third of the participants physical activity had 78% lower risk of abdominal obesity
were female (N = 104). The rate of obesity using BMI and WC were (OR = 0.22, 95% CI: 0.06–0.85; p = 0.029, Table 3).
36.9% and 68.8%, respectively. Most participants used oral A significant correlation was found between BMI and diastolic
hypoglycemic agents (OHA) (91.7%) and about half used anti- blood pressure (r = 0.23; p = 0.004). There was no correlation
hypertensive medications (51.0%) and lipid lowering medications between BMI and serum lipids. WC was correlated to TG (r = 0.17;
(54.1%). Subjects with BMI  30 kg/m2 had higher risk of central p = 0.035), but not to blood pressures or other lipids.
obesity than patients with BMI < 30 kg/m2 (93.1% vs. 54.5%,
OR = 8.71, 95% CI: 2.71–27.99, p < 0.001 after adjustment for age,
4. Discussion
gender and energy intake).
Blood pressure levels were similar in subjects with and without
The relative risk of CVD for diabetic subjects is double more
general obesity (Table 1). Participants with central obesity had
than others [23]. General and central obesity are also contributed
significantly higher systolic (OR = 1.03, p = 0.024) and diastolic
to increased risk of cardiovascular disease [24]. Our study revealed
blood pressures than participants without obesity (OR = 1.06,
that 36.9% of diabetic patients had general obesity, which was
p = 0.007, Table 1). After adjustment for energy intake, age and sex
lower than another study performed in Iranian diabetic subjects by
subjects with abdominal obesity had 5.5 times higher chance for
85.5% [11]. Also, 68.8% of patients had central obesity, which was
having elevated DBP (48.1% vs. 20.4%; OR = 5.49, p < 0.001, Table 2).
higher than regional report of one-third of total population [25]
Subjects with obesity either by BMI (86.2% vs. 69.7%, OR = 3.77;
and lower than previous findings among diabetic subjects in Iran
p = 0.006) or by WC (81.5% vs. 63.3%, OR = 4.10; p = 0.003) had
(81.5%) [11] and European countries like UK(96.9%), Spain(77.3%),
higher prevalence of hypertension than patients without obesity
Germany (92%), but higher than other Asian regions, such as India
after adjusting energy intake, age and sex (Table 3).
(67%), Pakistan (61.5%), China(54.8%), and Korea(37.2%) [12].
No difference in serum lipids was observed among patients
Obesity was strongly associated with gender. As mentioned
with and without obesity using BMI except for HDL-C that also
before, women had 4.6 times higher general obesity and about 8
disappeared after adjustment for confounding factors (Table 1).
times higher central adiposity rates than men (Table 3). That could
This could be attributed to more female subjects in obesity group.
augment the diabetes outcome in women.
The association between elevated TG levels and obesity was
About half of participants had hypertension. This was in line
significant in patients with both general (53.4% in obesity vs. 37.4%
with a previous finding in Isfahan province in Iran, with the
in non-obesity groups; OR = 2.11, 95% CI: 1.03–4.31; p = 0.04,
prevalence of 49.9% among T2DM patients [26]. Obesity, either in
Table 2) and abdominal adiposity groups (49.1% in obesity vs.
central or in general form, was associated with hypertension.
30.6% in non-obesity groups; OR = 2.68, 95% CI: 1.16–6.19; p = 0.021,
Abdominal adiposity demonstrated stronger association with DBP,
Table 2).
hypertension and serum TG concentrations. Hypertension was
High prevalence of dyslipidemia was observed in participants
about four times more prevalent in subjects in both central and
regardless the obesity status (Table 3).
general obesity groups (Table 2). Also, participants with central
Females had higher rate of general obesity than males (86.2% vs.
obesity had 3% and 6% higher risk of systolic diastolic blood
13.8%; OR = 4.57, 95% CI = 1.88-11.11, p < 0.001 after adjustment for
pressures elevation than subjects with normal waist circumference
energy intake and age, Table 3). Also, central obesity was about 8
(Table 1). High prevalence of hypertension (75.8%) observed in this
times more prevalent in diabetic females than their male
study was in accordance with another finding in obese T2DM
counterparts (80.6% vs. 19.4%; OR = 7.93, 95% CI = 3.48-18.08,
patients in Asia (76.5% and 72.4%) [27,28] and lower than European
p < 0.001, after adjustment for energy intake and age, Table 3).
reports (80% in UK and 82.5% in Sweden) [8,29]. In our study, 86.2%
Obesity prevalence whether in central or in general form had no
of patients with general obesity had hypertension; while, it was
association with age, diabetes duration, or family history of
87.5% in Swedish patients [29].
diabetes (p > 0.05, Table 3).

Table 2
Prevalence of hypertension and dyslipidemia among patients with and without obesity by BMI and waist circumference.

BMI WC

Non-Obesity Obesitya ORc (95% CI)c Non-Obesity Obesityb ORc (95% CI)c
N (%) N (%) N (%) N (%)
SBP 130 mmHg 43(43.4) 29(50.0) 1.43 (0.71–2.87) 18(36.7) 54(50.0) 1.94 (0.87–4.25)
DBP  85 mmHg 34(34.3) 28(48.3) 1.94 (0.95–3.95) 10(20.4) 52(48.1) 5.49 (2.15–14.03)**
TG  150 mg/dL 37(37.4) 31(53.4) 2.11 (1.03–4.31)* 15(30.6) 53(49.1) 2.68 (1.16–6.19)*
HDL-C 64(64.6) 35(60.3) 0.61 (0.29–1.27) 29(59.2) 70(64.8) 1.02 (0.46–2.28)
M < 40 mg/dL,
F < 50 mg/dL
LDL-C 100 mg/dL 46(46.5) 26(44.8) 0.86 (0.45–1.74) 26(53.1) 46(42.6) 0.54 (0.25–1.18)
Chol 200 mg/dL 23(23.2) 12(20.7) 1.00 (0.42–2.39) 12(24.5) 23(21.3) 1.12 (0.44–2.85)

Values are number (%). *p-value < 0.05, **p-value< 0.001.

Chol Cholesterol; DBP diastolic blood pressure; HDL-C high density lipoprotein cholesterol; LDL-C low density lipoprotein cholesterol; SBP systolic blood pressure; TG
triglycerides.
a
BMI  30 kg/m2.
b
WC  102 cm in men and  88 cm in women [24].
c
After adjustment for energy intake, age and sex.

Please cite this article in press as: R. Anari, et al., Association of obesity with hypertension and dyslipidemia in type 2 diabetes mellitus subjects,
Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.07.004
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Table 3
Characteristics of participants with and without general and central obesity.

BMI WC
a c c b
Non-Obesity Obesity OR 95% CI Non-Obesity Obesity ORc 95%CIc
N (%) N (%) N (%) N (%)
Sexd 1.88–11.11** 3.48–18.08**
Male 45(45.5) 8(13.8) Ref. 32(65.3) 21(19.4) Ref.
Female 54(54.5) 50(86.2) 4.57 17(34.7) 87(80.6) 7.93
Age (year) 0.93–1.00 0.95–1.02
50 31(31.3) 19(32.8) Ref. – 14(28.6) 36(33.3) Ref. –
51–60 31(31.3) 25(43.1) 1.20 0.56–2.92 18(36.7) 38(35.2) 0.72 0.31–1.96
>60 37(37.4) 14(24.1) 0.51 0.18–1.01 17(34.7) 34(31.5) 0.61 0.21–1.20
Diabetes duration (year) 0.91–1.01 0.96–1.08
<5 47(47.5) 31(53.4) Ref. 27(55.1) 51(47.2) Ref.
5 52(52.5) 27(46.6) 0.74 22(44.9) 57(52.8) 1.28
Body fate,f (%) 31.4(8.5) 44.8(6.6) 1.90 1.54–2.35** 27.5(8.8) 40.4(8.1) 1.24 1.13–1.36**
Hypertensione 69(69.7) 50(86.2) 3.77 1.47–9.64* 31(63.3) 88(81.5) 4.10 1.64–10.27*
Dyslipidemiae 96(97.0) 57(98.3) 1.49 0.46–4.84 48(98.0) 105(97.2) 1.32 0.40–4.41
Lipid lowering drugse (%) 26(53.1) 59(54.6) 1.79 0.91–3.50 48(48.5) 37(63.8) 0.98 0.49–1.96
Anti-hypertensive drugse (%) 48(48.5) 32(55.2) 1.18 0.60–2.30 20(40.8) 60(55.6) 1.61 0.80–3.25
Oral hypoglycemic agentse (%) 91(91.9) 53(91.4) 1.79 0.91–3.50 43(87.8) 101(93.5) 0.84 0.26–2.75
Physical activity levele 0.99–1.00 0.99–1.00
Low 44(44.4) 32(55.2) Ref. – 17(34.7) 59(54.6) Ref. –
Moderate 48(48.5) 21(36.2) 0.775 0.37–1.63 27(55.1) 42(38.9) 0.650 0.28–1.50
High 7(7.1) 5(8.6) 0.762 0.21–2.72 5(10.2) 7(6.5) 0.217 0.06–0.85*
Family history of diabetes (%) 61(62.2) 42(72.4) 1.66 0.48–2.08 32(66.7) 71(65.7) 1.04 0.81–3.39
a
BMI 30 kg/m2.
b
WC 102 cm in men and  88 cm in women [24].
c
After adjustment for energy intake.
d
After adjustment for energy intake and age.
e
After adjustment for energy intake, age and sex.
f
Presented as mean (SD) and analyzed by t-test. P-values less than 0.05 were considered significant. *p < 0.05, **p < 0.001.

Dyslipidemia was prevalent in most subjects regardless the management could improve the insulin resistance and dyslipide-
obesity status, with a total prevalence of 97.5% which was higher mia, commonly found in these patients, it should be considered
than the study conducted in India on T2DM patients (83%) [30] and as the first line implementation in diabetes health care process
the regional prevalence in adults by 81% [31]. General and central [40]. Health care providers should consider weigh loss manage-
obesity groups had the same rates of dyslipidemia (p < 0.05, ment, especially in females who had higher adiposity rates, to
Table 3). This results was higher than a Swedish study conducted decrease obesity prevalence and its consequent outcomes, in
on T2DM patients with obesity indicating 80.6% had hyperlipid- particular CVD.
emia (P < 0.001) [29]. However, hypertriglyceridemia demonstrat- To the best of the authors' knowledge, this was the first study
ed a significant association with both central (OR = 2.11; p = 0.040) that evaluates dyslipidemia and hypertension prevalence in
and general obesity (OR = 2.68; p = 0.021). This would be due to Iranian T2DM subjects in the area. According to the findings of
excess visceral fat in abdomen which elevate TG and Apo this research, TG and hypertension might be controlled by losing
lipoprotein B and reduce high density lipoprotein cholesterol weight and waist circumference. It is also suggested to confirm
production by liver [20]. Serum TG is a risk factor for CVD and also these findings through prospective studies with regards to long-
elevates insulin resistance which worsen the glycemic control term vascular outcomes and to investigate the wider range of
[32,33]. The exact mechanism of dyslipidemia occurrence in T2DM underlying factors for hypertension and dyslipidemia in T2DM.
subjects is still unclear.
In our study, abdominal adiposity showed significant negative Conflicts of interest
association with high physical activity, suggesting possible
protective role of exercise for controlling such obesity type. None.
Individuals who meet the recommended daily physical activity
may overcome the effect of FTO genotype on obesity-related Funding
diseases such as diabetes, hypertension, and the metabolic
syndrome [34]. This work was supported by Vice-Chancellor for Research at
Central (abdominal) obesity is independently associated with Ahvaz Jundishapur University of Medical Sciences (Grant number
each of the other metabolic syndrome components including B-94011).
insulin resistance [35]. Abdominal obesity has also been suggested
to have a strong association with metabolic risk factors, Acknowledgements
cardiovascular events, and death [36,10]. Previous studies have
suggested that an increase in WC is associated with 4.25 time We kindly appreciate the contribution of all participants and
higher risk of stroke and ischemic attacks [37]. Also, greater central the personnel of Golestan Diabetes Clinic.
obesity is correlated to elevated systemic inflammation which The authors contribute to the research as the following: R.
could directly result in CVD [38]. A survey in the UK revealed T2DM Anari did the data collection and wrote the first draft; R. Amani
patients with BMI  30 kg/m2 had higher blood pressure and and M. Veissi supervised the research, S.M. Latifi, and H.B.
triglyceride levels than patients with normal weight [39]. Shahbazian did the statistical and clinical assistance. R. Anari and
It is highly recommended diabetic patients lose their extra S.M. Latifi analyzed data or performed statistical analysis; R.
weight for achieving the adequate glycemic control [6]. As weight Amani did the final revision of the manuscript. None of the authors

Please cite this article in press as: R. Anari, et al., Association of obesity with hypertension and dyslipidemia in type 2 diabetes mellitus subjects,
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approved the final content of the article. Cholesterol in Adults: Executive Summary of the third national cholesterol
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Please cite this article in press as: R. Anari, et al., Association of obesity with hypertension and dyslipidemia in type 2 diabetes mellitus subjects,
Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.07.004