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Preventive Medicine 49 (2009) 402–406

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Preventive Medicine
j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y p m e d

Association between physical activity and insulin resistance in Iranian adults: National
Surveillance of Risk Factors of Non-Communicable Diseases (SuRFNCD-2007)
Alireza Esteghamati a,⁎, Omid Khalilzadeh a, Armin Rashidi a, Alipasha Meysamie b, Mehrdad Haghazali c,
Fereshteh Asgari c, Mehrshad Abbasi a, Shadab Rastad a, Mohammad Mehdi Gouya c
a
Endocrinology and Metabolism Research Center (EMRC), Vali-Asr Hospital, School of Medicine, Tehran University of Medical Sciences P.O. Box 13145-784, Tehran, Iran
b
Department of Community Medicine, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
c
Center for Disease Control, Ministry of Health and Medical Education, Tehran, Iran

a r t i c l e i n f o a b s t r a c t

Available online 8 September 2009 Background. Insulin resistance is an underlying mechanism of metabolic syndrome. We attempted to
determine the association between physical activity and insulin resistance in Iranian adults.
Keywords: Methods. The data of the third national Surveillance of Risk Factors of Non-Communicable Diseases
Physical activity (SuRFNCD-2007) in Iran were used. We ran the Global Physical Activity Questionnaire (GPAQ) over a
Insulin resistance
nationally representative sample of 3101 adults. Total physical activity (TPA) was calculated using metabolic
Homeostasis model assessment
Sedentary
equivalents (MET) for intensity of physical activities. Insulin resistance was measured by the homeostasis
model assessment of insulin resistance (HOMA-IR).
Results. When physical activity was classified into high, moderate, and low categories, HOMA-IR values
significantly increased from the high category to the moderate and low categories (p b 0.01). After
adjustment for age, area of residence, smoking, and body mass index (BMI), TPA (r = −0.26, p b 0.01 in males
and r = −0.21, p b 0.01 in females), duration of vigorous-intensity activity (r = −0.28, p b 0.01 in males and
r = −0.18, p = 0.01 in females), duration of moderate-intensity activity (r = −0.16, p = 0.01 in males and
r = −0.17, p b 0.01 in females), and the time spent on sedentary behaviors (r = 0.16, p = 0.01 in males and
r = −0.22, p b 0.01 in females) were significantly correlated to HOMA-IR. The prevalence of physical
inactivity increased linearly with increasing HOMA-IR quintiles.
Conclusions. Our findings indicate a significant relationship between physical inactivity and insulin
resistance. For communities in a transition phase of lifestyle, encouraging physical activity may help prevent
insulin resistance and its adverse consequences.
© 2009 Elsevier Inc. All rights reserved.

Introduction 2002). These changes in lifestyle seem to be making obesity an


increasingly common problem in the country, and may subsequently
Insulin resistance has an important role in the pathogenesis of lead to insulin resistance and its adverse metabolic consequences.
several conditions including obesity (Esteghamati et al., 2008d), Physical activity has been suggested to improve insulin sensitivity
hypertension (Esteghamati et al., 2008c), type 2 diabetes (Meigs et al., (Bradley et al., 2008; Balkau et al., 2008; Nowak et al., 2008; Kavouras
2007), dyslipidemia (Semenkovich, 2006; Chapman & Sposito, 2008), et al., 2007). However, the association between different levels of
and cardiovascular disease (Bonora et al., 2007, 2002). We and others physical activity, defined by an international standard questionnaire,
have recently shown that the prevalence of such conditions is rather and insulin resistance is yet to be explored in large scale population-
high in the Iranian population (Esteghamati et al., 2008a, 2008b; based studies. Furthermore, it is interesting to explore this association
Janghorbani et al., 2007). As a result of progressive urbanization and in different domains of physical activity (i.e., work, commuting, and
industrialization, adults tend to experience a decline in their level of leisure time) and evaluate the independent association of sedentary
physical activity and replacement of their comparatively healthier lifestyle behaviors with insulin resistance. It is particularly important
traditional diets by calorie-dense, high-fat foods (Ghassemi et al., to discover ways to improve health conditions in populations under-
going socio-cultural phase transitions. The homeostasis model
assessment of insulin resistance (HOMA-IR) is a practical method
⁎ Corresponding author. Fax: +98 21 64432466. for estimating insulin resistance in epidemiologic studies (Wallace
E-mail addresses: esteghamati@tums.ac.ir (A. Esteghamati), et al., 2004). For the first time in Iran, we investigated in this study the
khalilzadeh@razi.tums.ac.ir (O. Khalilzadeh), rasidiarmin@yahoo.com (A. Rashidi),
meysamie@tums.ac.ir (A. Meysamie), haghmehr@yahoo.com (M. Haghazali),
association between HOMA-IR and physical activity, assessed by the
asgarifcdc@yahoo.com (F. Asgari), mehrshad_abbasi@yahoo.com (M. Abbasi), Global Physical Activity Questionnaire (GPAQ) (WHO, 2008), in a
shadabrastad@yahoo.com (S. Rastad), mgoya57@yahoo.com (M.M. Gouya). large national-representative sample of Iranian adults.

0091-7435/$ – see front matter © 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.ypmed.2009.09.005
A. Esteghamati et al. / Preventive Medicine 49 (2009) 402–406 403

Materials and methods Physical examination and biochemical measurements

Participants Weight and height of participants were determined in light clothing and
without shoes. Portable calibrated electronic weighing scale and portable
This study was based on the data of the third SuRFNCD in Iran carried measuring inflexible bars were used. Waist circumference was measured using
out in 2007. Details of the survey are reported elsewhere (CDC of Iran, constant tension tape at the end of a normal expiration, with arms relaxed at the
2008). In brief, a cluster sampling scheme was applied to randomly select a sides, at the midpoint between the lower part of the lowest rib and the highest
representative sample of Iranian adults aged 25–64 years. Addresses were point of the hip on the mid-axillary line. Blood pressure was measured with a
randomly selected from the postal codes across the country. Two males calibrated Omron M7 sphygmomanometer (HEM-780-E). The average of three
and two females were assigned to each age category (15–24, 25–34, measurements, made at intervals of 5 min, was used for analysis. The body mass
35–44, 45–54, and 55–64 years). The sample taken from each province was index (BMI; kg/m2) was calculated according to the Quetelet formula.
proportional in size to the total population of the province. For instance, 51 Venous blood (10 ml) was taken in sitting position, collected in four tubes,
(1020 participants) and 2 (40 participants) clusters were taken from centrifuged immediately, and transferred under cold chain condition to the
Tehran and Ilam, the largest and smallest provinces in Iran, respectively. Central Reference Laboratory of Ministry of Health of Iran (Tehran, Iran).
Trained healthcare professionals conducted household interviews and Fasting plasma glucose (FPG) was measured by the enzymatic colorimetric
physical examinations. Interviewers were instructed on details of the method using glucose oxidize test (intra- and inter-assay coefficients of
survey and how to conduct the interviews in a 1-day workshop in Tehran variation of 2.1% and 2.6%, respectively). One tube was treated with 2 μg
prior to the commencement of the survey. All interviews were in Persian. sodium fluoride for glucose preservation to enhance the accuracy of glucose
The data were recorded in standardized questionnaires and were measurement. The two remaining tubes were transferred to the endocrine
rechecked based on a predetermined schedule. Blood sampling was done laboratory of Vali-Asr Hospital (Tehran University of Medical Sciences,
within a few days of the interview. The survey received ethics approval Tehran, Iran) for fasting plasma insulin (FPI) measurement. Plasma insulin
from the Center for Disease Control (CDC) of Iran and all participants gave was measured by the radioimmunoassay method (Immunotech, Prague,
informed consent. Czech Republic). Sensitivity was 0.5 mU/ml, and the upper limits of intra- and
inter-assay coefficients of variation were 4.3 and 3.4, respectively.
Physical activity assessment
Statistical analysis
The second version of the GPAQ was employed in the survey (WHO,
HOMA-IR was calculated as FPG (mmol/l) × FPI (mU/l)/22.5 (Matthews
2008). This questionnaire, which has been developed by WHO, is composed
et al., 1985). Complex sample survey analysis was performed using SPSS 16
of 16 questions about physical activity in a typical week and assesses physical
for Windows (Chicago, IL). Data were weighted for sex, age, and residential
activity in three domains, namely, work, transportation, and recreational
area (urban/rural) strata, according to the population of Iran (national
activities. The evaluation of physical activity in three domains is one of the
census, 2006). The method of general linear modeling was used to adjust the
factors that make GPAQ distinct from other questionnaires including the less
variables of interest for factors such as age, sex, area of residence, BMI, and
sophisticated, short version of the international physical activity question-
smoking, and to compare the adjusted variables across quintiles of HOMA-IR
naire IPAQ (available at: http://www.ipaq.ki.se). It also determines the
(1.237, 1.556, 1.947, and 2.822) and categories of physical activity.
intensity of activity (i.e., vigorous or moderate) in each domain as well as the
Multivariate regression analysis was used to find independent correlates of
time spent on sedentary behaviors such as watching TV. Sedentary behavior
HOMA-IR. p b 0.05 was considered statistically significant.
was defined as activities such as sitting at a desk, traveling in car/bus/train,
reading, working with computer, and watching television.
Results
In order to measure energy expenditure, the concept of metabolic equi-
valents (MET) was used. MET is the ratio of a person's working metabolic rate
relative to the resting metabolic rate. One MET is defined as the energy cost of After excluding participants with missing data in questionnaires
sitting quietly, and is equivalent to a caloric consumption of 1 kcal/kg/h. It is (n = 113), analyses were performed in the remaining 3101 individuals.
estimated that a person's caloric consumption is four times as high when
being moderately active, and eight times as high when being vigorously Table 1
active. Therefore, when calculating a person's overall energy expenditure Characteristics of study participants in groups with low, moderate, and high levels of
using the GPAQ data, four METs are assigned to the time spent on moderate physical activity (SuRFNCD-2007, Iran).
activities, and eight METs to the time spent on vigorous activities. The total
Low Moderate High P
physical activity score (TPA) was calculated as the sum of all MET × minutes
for moderate- or vigorous-intensity physical activity performed in work, n (total = 3101) 1239 (40.0%) 765 (24.7%) 1097 (35.4%) —
commuting, and recreation. Burden (n)a 12.5 7.7 11.1 —
b
Age (year) 44.5 (0.3) 44.3 (0.4) 43.4 (0.3) 0.05
Participants were classified into the following three categories, as defined
Males (%) 468 (37.8) 350 (45.7) 680 (62.0) b0.01
by the GPAQ analysis framework:
Area of residence b0.01
Urban (%) 862 (69.6) 542 (70.6) 668 (60.9)
1) High: a person reaching any of the following criteria is classified in this Rural (%) 377 (30.4) 223 (29.4) 429 (39.1)
category: BMI (kg/m2)b 27.2 (0.2) 26.6 (0.2) 25.9 (0.2) b0.01
Waist circumference (cm)b 90.3 (0.4) 89.1 (0.4) 87.4 (0.4) b0.01
• Vigorous-intensity activity on at least 3 days a week achieving a
Systolic blood pressure 123.9 (0.7) 122.9 (0.8) 121.4 (0.6) 0.02
minimum of at least 1500 MET-minutes per week, or (mmHg) b

• Seven or more days of any combination of walking and moderate- or Diastolic blood pressure 81.0 (0.5) 80.3 (0.5) 80.2 (0.5) 0.35
vigorous-intensity activities achieving a minimum of at least 3000 MET- (mmHg)b
minutes per week. Smoking statusc b0.01
2) Moderate: a person not meeting the criteria for the “high” category, but Never smoker 83.8 (1.7) 83.3 (1.7) 76.2 (1.7)
meeting any of the following criteria is classified in this category: Ex-smoker 3.9 (0.5) 4.6 (0.7) 6.2 (0.8)
Current smoker 12.3 (1.5) 12.1 (1.4) 17.6 (1.5)
• Three or more days of vigorous-intensity activity of at least 20 min per
Fasting plasma glucose 5.30 (0.08) 5.12 (0.06) 5.03 (0.05) b0.01
day, or (mmol/l)b
• Five or more days of moderate-intensity activity or walking of at least Fasting plasma insulin (mU/l)b 9.78 (0.24) 9.74 (0.27) 9.24 (0.21) 0.13
30 min per day, or HOMA-IRb 2.71 (0.08) 2.32 (0.07) 1.99 (0.06) b0.01
• Five or more days of any combination of walking and moderate- or
Variables (except age, sex, and area of residence) are standardized for age, sex, and
vigorous-intensity activities achieving a minimum of at least 600 MET-
residential area of the 2006 population of Iran.
minutes per week. a
National estimate rounded to the nearest million.
3) Low: a person not meeting any of the above mentioned criteria falls in this b
Mean (SE).
c
category. % (SE).
404 A. Esteghamati et al. / Preventive Medicine 49 (2009) 402–406

Table 2 and HOMA-IR (p b 0.01) significantly increased across categories of


Association between several features of physical activity with HOMA-IR after decreasing physical activity.
adjustment for potential confounders (SuRFNCD-2007, Iran).
In both genders (and after adjustment for age, area of residence,
Males Females BMI, and smoking), HOMA-IR was significantly associated with TPA,
Standardized P Standardized P the duration of vigorous- and moderate-intensity activity, and
beta beta sedentary behaviors. The association between HOMA-IR and TPA
Total physical activity (TPA) was independent of the duration of sedentary behaviors. Similarly, the
Adjustment for association between HOMA-IR and both vigorous and moderate types
Age and area of residence −0.28 b 0.01 −0.23 b0.01 of activity was independent of the duration of sedentary behaviors
Age, area of residence, BMI, −0.26 b 0.01 −0.21 b0.01 (Table 2).
and smoking
Age, area of residence, BMI, −0.24 b 0.01 −0.20 b0.01
TPA and MET-minutes of activity at work and at commuting were
smoking, and duration of significantly lower at higher HOMA-IR quintiles after adjustment for
sedentary behaviors age, sex, area of residence, BMI, and smoking (p b 0.01). The same
pattern was seen for the duration of vigorous- or moderate-intensity
Duration of vigorous activity
physical activity (p b 0.01), whereas the duration of sedentary
Adjustment for
Age and area of residence −0.30 b 0.01 −0.19 0.01 behaviors was significantly (p b 0.01) higher at higher HOMA-IR
Age, area of residence, BMI, −0.28 b 0.01 −0.18 0.01 values (Fig. 1). As shown in Fig. 2, the percentage of individuals with
and smoking vigorous-intensity activity was significantly lower while that of
Age, area of residence, BMI, −0.25 b 0.01 −0.15 0.02 inactive individuals was significantly higher at higher HOMA-IR
smoking, duration of
moderate activity,
quintiles (p b 0.01). The percentage of individuals in high (low)
and sedentary behaviors category activity was negatively (positively) correlated with HOMA-
IR quintiles (p b 0.01).
Duration of moderate activity In order to evaluate the situation in postmenopausal women, we
Adjustment for
restricted the analysis to this subset of participants (n = 545). HOMA-
Age and area of residence −0.15 0.01 −0.18 0.01
Age, area of residence, BMI, −0.16 0.01 −0.17 0.01 IR was significantly associated with TPA (r = −0.17, p b 0.01), duration
and smoking of vigorous-intensity activity (r = −0.15, p = 0.02), duration of
Age, area of residence, BMI, −0.13 0.03 −0.14 0.02 moderate-intensity activity (r = −0.13, p = 0.01), and duration of
smoking, duration of sedentary behaviors (r = 0.27, p b 0.01). The associations remained
vigorous activity, and
significant after additional adjustment for BMI and smoking.
sedentary behaviors

Duration of sedentary behaviors Discussion


Adjustment for
Age and area of residence 0.17 0.01 0.25 b0.01
Our study population represents the adult population of Iran. The
Age, area of residence, BMI, 0.16 0.01 0.22 b0.01
and smoking duration and intensity (vigorous vs. moderate) of physical activity in
Age, area of residence, BMI, 0.12 0.03 0.17 b0.01 three domains of work, commuting, and recreation were assessed
smoking, and TPA using the GPAQ questionnaire. Considering that most physical
activities in developing countries take place while working and
commuting, separating these domains from recreational activities is a
Anthropometric characteristics of participants are presented in Table 1. logical approach recommended by WHO in GPAQ, in order to yield a
The body mass index (BMI; p b 0.01), waist circumference (p b 0.01), more comprehensive estimate of overall physical activity. In addition,
systolic blood pressure (p = 0.02), fasting plasma glucose (p b 0.01), through controlling the potential confounding effects of work and

Fig. 1. The association between HOMA-IR and TPA, activity at work, activity at commuting, and activity at recreation after adjustment for age, sex, residential area, BMI, and smoking
(A). The association between HOMA-IR and the duration of sedentary behaviors, moderate activity, and vigorous activity after adjustment for age, sex, residential area, BMI, and
smoking (B) (SuRFNCD-2007, Iran). ⁎p b 0.05, ⁎⁎p b 0.01, ⁎⁎⁎p b 0.001. Handles represent SE.
A. Esteghamati et al. / Preventive Medicine 49 (2009) 402–406 405

Fig. 2. The percentage of individuals with vigorous, non-vigorous, and without activity across quintiles of HOMA-IR (A). The percentage of individuals in different categories of
activity across quintiles of HOMA-IR (B). Sufficient activity is defined as high or moderate categories of physical activity (B). The number in each box refers to the percentage of
individuals that correspond to the given activity category/intensity. Variables are adjusted for age, sex, and area of residence (SuRFNCD-2007, Iran).

commuting activities, this approach assesses the association between clamp technique and accelerometer to measure insulin resistance and
physical inactivity and metabolic abnormalities more precisely than physical activity, respectively, Balkau et al. (2008) showed in 801
traditional questionnaires which focus mainly on evaluating recrea- adults that the duration of physical activity and total physical activity is
tional activities. significantly related to insulin sensitivity in both genders. After
To estimate physical activity energy expenditure, MET-minutes of adjusting for total activity, however, the relationship between the
activities in different domains were calculated and summed up to yield duration of activity and insulin sensitivity lost its significance. In
TPA. After adjustments for age, gender, residential area, smoking, and another study on 1262 adults aged 20 years or older in south India,
BMI, we demonstrated a significant association between TPA and physical activity was measured in three domains: job-related activity,
HOMA-IR. Furthermore, both moderate- and vigorous-intensity leisure-time activity, and exercise. Subjects were then categorized into
activities were independently correlated with lower HOMA-IR values. three groups: light-, moderate-, and heavy-grade activity. HOMA-IR
The time spent on sedentary behaviors was also associated with was significantly higher in subjects with light-grade activity compared
HOMA-IR independent of physical activity at other domains. We to those with heavy-grade activity (Mohan et al., 2005).
demonstrated a significant linear association between HOMA-IR Different mechanisms have been proposed to explain the effect of
quintiles and various aspects of physical activity. As shown in Fig. 1A, physical activity on insulin sensitivity. One theory points out that
work-time physical activity had a higher (compared to commuting and physical activity enhances glucose transport into the muscle cells,
recreation) contribution to the association between TPA and HOMA-IR. possibly by up-regulating the expression of glucose transporter 4
The advantages of this study include a large sample size (Goodyear & Kahn, 1998; Perseghin et al., 1996; O'Gorman et al.,
representative of the nation, using a standardized international 2006; Holloszy, 2005). Moreover, regular physical activity decreases
questionnaire (WHO, 2008) and the concept of metabolic equivalents, the fat mass and replaces it with lean mass, such that the amount of
exploring the association in different domains of physical activity (i.e., muscle available for glucose absorption increases (Perseghin et al.,
work, commuting, and recreation) and evaluation of the association 1996). Obesity stimulates the production of inflammatory cytokines
between some of the less studied aspects of physical activity and which result in insulin resistance (Bradley et al., 2008). Indeed,
insulin resistance. For example, the association between sedentary lowering the body weight may be a mechanism through which
behavior and insulin resistance has not been evaluated in previous physical activity increases insulin sensitivity (Balkau et al., 2008).
works. The association between insulin resistance and physical activity Enhanced blood perfusion of muscles during physical activity is
or exercise has been the topic of many recent studies (Balkau et al., another mechanism (Baron et al., 1995).
2008; Nowak et al., 2008; Bradley et al., 2008; Kavouras et al., 2007; Our study is the first attempt of its kind in Iran and one of the
Franks et al., 2007; Foy et al., 2006; Mohan et al., 2005; Brage et al., largest studies on the subject. A recent study on 3600 adults (age:
2004; Kriska et al., 2001; Mayer-Davis et al., 1998). The results of the 20–70 years) living in urban areas of northern Iran showed that job-
available reports, however, have sometimes been inconsistent, mainly related activity was low in 64.3% of individuals, and leisure-time
due to differences in the study design, sampling protocol, age range of activity was very low or low in 81.3% of subjects. Furthermore, 79.2%
participants, method for assessing physical activity (e.g., different of subjects had less than 2 h of exercise per week (Hajian-Tilaki &
questionnaires), and insulin resistance estimation methods. Mayer- Heidari, 2007). A study in Tehran indicated that 45% of women aged
Davis et al. (1998) showed in a study on 1467 individuals aged 40–69 40–60 years have low levels of physical activity, as assessed by the
years that physical activity (total, vigorous-intensity, and moderate- IPAQ questionnaire (Azadbakht & Esmaillzadeh, 2008). Together with
intensity) has a direct relationship with insulin sensitivity measured our results, one can conclude that the level of physical activity among
by the frequently sampled intravenous glucose test (FSIGT). Using the Iranian adults is low in several dimensions.
406 A. Esteghamati et al. / Preventive Medicine 49 (2009) 402–406

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Conflict of interest statement Janghorbani, M., Amini, M., Willett, W.C., et al., 2007. First nationwide survey of
The authors declare that there are no conflicts of interest. prevalence of overweight, underweight, and abdominal obesity in Iranian adults.
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