Evaluation of oxidative stress and total antioxidant capacity in women with general and abdominal adiposity

Obesity Research & Clinical Practice (2010) 4, e209—e216

ORIGINAL ARTICLE

Evaluation of oxidative stress and total antioxidant capacity in women with general and abdominal adiposity夽 Farshad Amirkhizi a,b,∗, Fereydoun Siassi b, Mahmoud Djalali b, Abbas Rahimi Foroushani c a

Department of Nutrition, Faculty of Health, Zabol University of Medical Sciences, Zabol, Iran Department of Nutrition and Biochemistry, Faculty of Public Health, Tehran University of Medical Sciences, Tehran, Iran c Department of Epidemiology and Biostatistics, Faculty of Public Health, Tehran University of Medical Sciences, Tehran, Iran b

Received 29 October 2009 ; received in revised form 24 January 2010; accepted 2 February 2010

KEYWORDS General adiposity; Abdominal adiposity; Oxidative stress; Antioxidant

Summary Background: Previous studies have shown that general and abdominal adiposity are closely associated with risk of diabetes and cardiovascular disease events. We sought to evaluate the oxidative stress and plasma total antioxidant capacity (TAC) levels in women with general and abdominal adiposity. Methods: In this study, 160 women 20—45 years old were randomly selected. General information data were gathered from each sample using questionnaires and face-toface interviews. Venous blood samples were drawn from subjects and plasma was separated. In this study, oxidative stress levels were assessed by measuring the concentrations of plasma malondialdehyde (MDA). We also evaluated total antioxidant capacity (TAC) of plasma in subjects. Results: Mean plasma concentration of MDA was significantly higher in overweight and obese women groups compared to healthy women group (2.62 ± 0.81 vs. 1.96 ± 0.72, p < 0.01 and 3.25 ± 0.74 vs. 1.96 ± 0.72, p < 0.001, respectively). Furthermore, plasma TAC levels were significantly lower in obese women compared to healthy women group (2.57 ± 0.58 vs. 3.45 ± 0.73, p < 0.01). No significant difference was observed between overweight and normal weight women in plasma TAC levels. In addition, women with central body fat distribution had higher MDA (3.28 ± 0.78 vs. 2.23 ± 0.52, p < 0.001) and lower TAC levels (p < 0.01) compared to

夽

This study was funded by the Research Council of School of Public Health, Tehran University of Medical Sciences. Corresponding author at: Department of Nutrition, Faculty of Health, Zabol University of Medical Sciences, Shahid Rajaie St., Zabol, Iran. Tel.: +98 542 2244800; fax: +98 542 2226025. E-mail address: [email protected] (F. Amirkhizi). ∗

1871-403X/$ — see front matter © 2010 Asian Oceanian Association for the Study of Obesity. Published by Elsevier Ltd. All rights reserved.

doi:10.1016/j.orcp.2010.02.003

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F. Amirkhizi et al. normal body fat distribution (2.41 ± 0.59 vs. 3.16 ± 0.84, p < 0.01). We also observed that aforementioned relationships remained significant even after adjusting for several confounders. Conclusions: Our results provides further evidence suggesting that obesity and, especially, abdominal adiposity associated with elevated oxidative stress and decreased levels of TAC in plasma which in turn, may contribute to obesity related diseases such as atherosclerosis, diabetes mellitus and arterial hypertension. © 2010 Asian Oceanian Association for the Study of Obesity. Published by Elsevier Ltd. All rights reserved.

Introduction Obesity has reached epidemic proportions in much of the developed countries [1—3] and is increasing in prevalence in the developing countries [4,5]. Furthermore, obesity is associated with development of metabolic syndrome and increased incidence of dyslipidemia, hypertension, type-2 diabetes and cardiovascular diseases [6]. Central fat accumulation, the so-called central adiposity, has been especially related with increased incidence of metabolic syndrome and cardiovascular events [7,8]. Unfortunately, more than 50% of adult women in Iran are abdominally obese [9]. Oxidative stress may play a critical role in the pathophysiology of cardiovascular diseases and diabetes [10]. Although the exact biochemical mechanisms responsible for the association between obesity and the above diseases have not been completely elucidated, it is known that increase production of reactive oxygen species (ROS) at high levels is associated with cellular damage including oxidation of cell membranes and proteins [11]. Furthermore, accumulating evidence from animal and human studies shows that obesity is associated with increased myocardial oxidative stress [12] and lipid peroxidation [13]. Oxidative stress can be defined as the imbalance between free radical damage (for example, the oxidation of lipids) and antioxidant protection. The determination of total antioxidant capacity (TAC) is now considered as a tool in medical diagnosis and treatment of several diseases, including cardiovascular disease and diabetes mellitus [14]. In plasma, the antioxidant molecules involved in free radical scavenging include endogenous (e.g. uric acid, albumin and circulating thiols) and exogenous (e.g. vitamins E and C) antioxidant molecules. TAC considers the sum action of all the endogenous and exogenous-derived antioxidants present in plasma and body fluids and provides an integrated parameter rather than the simple sum of measurable antioxidants. Previous studies have suggested that plasma TAC levels modified during

oxidative stress conditions [15]. Therefore, plasma TAC levels might be modified in obesity. To test this hypothesis, we undertook the present study to investigate any relationship between obesity and central fat accumulation with plasma TAC levels, irrespective of nutritional habits. We also evaluated concentrations of plasma malondialdehyde (MDA), as powerful marker of oxidative stress in selected women without any clinical evidence of cardiovascular disease.

Methods Study subjects The subjects used in this study were recruited among women receiving the services of rural health centers of Kerman Province, Iran. In total, 370 women aged 20—45 years selected by a multiple cluster random sampling method. After excluding pregnant, lactating and smoker women and participants with a prior history of cancer, cardiovascular disease, diabetes, renal or liver diseases, and those taking vitamin or mineral supplements, 160 women (mean age: 31.5 years) remained for the current analysis. All participants were informed about the aims and procedure of the study and signed written consent. General data were gathered from samples using questionnaires and face-to-face interviews. Data collecting form included demographic characteristics (age, number of pregnancies and education), detailed medical history and lifestyle habits, such as smoking status and physical activity.

Anthropometric measurements Body weight was measured while the subjects were wearing light clothing without shoes to the nearest 0.1 kg. Height was measured to the nearest 0.5 cm, without shoes. Body mass index (BMI) was calculated as weight (in kilograms) divided by height (in meters squared). Based on the World Health Organi-

Evaluation of oxidative stress and total antioxidant capacity in obese women zation criteria [16], overweight was defined as BMI between 25 and 29.9 kg/m2 , while general adiposity as BMI ≥ 30 kg/m2 . Waist circumference (WC) was measured in a horizontal plane at the level of the high point of iliac crest to the nearest 0.1 cm using an unstretched tape measure, without any pressure to body surface and hip circumference was measured in a horizontal plane at the maximum extension of the buttocks. Waist-to-hip ratio (WHR) was calculated as waist circumference (cm) divided by hip circumference (cm). WC greater than 88 cm was considered an indicator of abdominal adiposity [17]. To reduce error, all measurements were taken by the same technician.

Dietary assessment We used a validated food frequency questioner (FFQ) for assessing dietary intakes [18]. The FFQ was a semiquantitative Willett format questionnaire with 168 food items listed. A trained dietitian administered all the questionnaires.

Laboratories assay Venus blood samples were obtained from median cubital vein and collected into standard tubes containing ethylene diamine tetra acetic acid (EDTA). Blood samples centrifuged at 3000 rpm for 15 min at 4 ◦ C and plasma was separated for the assay TAC and MDA concentrations. Subjects’ plasma was stored in −70 ◦ C until analysis. Plasma MDA concentration was assayed by measurement of thiobarbituric acid reactive substances (TBARS) according to Satoh method [19]. The pink chromogen produced by the reaction of thiobarbituric acid with MDA was measured at 530 nm. Plasma TAC levels were determined by colorimetric assay using 2,2 -Azino-di-[3-ethylbenzthiazoline sulphonate] (ABTS) [20]. The assay relies on the ability of antioxidants in the sample to inhibit the oxidation of ABTS to ABTS•+ by a peroxidase. The amount of ABTS•+ produced can be monitored by reading the absorbance at 600 nm. The intra- and inter-assay coefficients of variation of TAC and MDA did not exceed 4 and 7%, respectively.

Other measurements Physical activity was classified as active if subjects reported ‘‘moving’’ walking and working energetically and participating in vigorous exercise’’, otherwise, they were classified as inactive. The education level of the participants was evaluated by the number of years they had attended school.

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Systolic blood pressure (SBP) and diastolic blood pressure (DBP) were averaged by using three readings measured at 5-min intervals. Differences of <5 mmHg were allowed.

Statistical analysis Continuous variables are presented as mean values ± standard deviation (SD), while categorical variables are presented as absolute and relative frequencies. Power analysis showed that the pre-specified number of participants is adequate to evaluate two-sided standardized differences between subgroups of the study and the investigated parameters greater 0.5, achieving statistical power >0.80 at <0.05 probability level (p-value). Normality tests were applied using the Kolmogorov—Semirnov criterion. Associations between categorical variables were tested by the use of chi-squared test. The differences between groups for continuous variables were sought by using one-way analysis of variance (ANOVA) and Independent t-test. Correlations between normally distributed continuous variables were evaluated by the calculation of Pearson’s partial r coefficient, after adjusting for various potential confounders. The relationships between independent variables (BMI, WC, and WHR) and dependent variable (TAC and MDA) were then evaluated using multiple linear regression analysis, after controlling for various potential confounders. We also calculated the adjusted R2 in order to find how well each fitted model predicted the dependent variables. For all analyses, p-values of less than 0.05 were considered statistically significant. All the statistical analyses were performed by using SPSS version 12.5 (Statistical Package for Social Sciences, SPSS Inc., Chicago, IL, USA) software.

Results We observed that 15.5% and 35.0% participants were obese and overweight, respectively. Additionally, the prevalence of central adiposity was 38.5% in participants. BMI, WC and WHR were positively correlated with age (r = 0.41, p < 0.001; r = 0.32, p < 0.001 and r = 0.36, p < 0.001, respectively). Thus, all further analyses were adjusted for age. Demographic, nutrient intakes and anthropometric characteristics of the participants according to their classification of BMI (normal, overweight and obese) are shown in Table 1. Normal weight women at significantly younger age as compared

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Table 1 Plasma TAC levels, demographic, nutrient intake and anthropometric characteristics of the participants by obesity status. Variables

Normal weight (n = 79)

Overweight group (n = 56)

Obese group (n = 25)

p-Value†

Age (years) Weight (kg) Height (cm) Body mass index (kg/m2 ) Waist circumference (cm) Waist-to hip ratio Education status (years of school) Physical inactivity (%) Number of pregnancies Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Energy intake (kcal/d) Protein (% energy) Total fat (% energy) Carbohydrate (% energy) Plasma MDA levels (␮mol/L) Plasma TAC levels (␮mol/L)

27 ± 61.3 ± 157.4 ± 23.4 ± 82.2 ± 0.74 ± 8± 54 3.2 ± 121 ± 81 ± 1685 ± 13.4 ± 30.2 ± 56.6 ± 1.96 ± 3.45 ±

35 ± 71.4 ± 159.3 ± 27.2 ± 82.8 ± 0.76 ± 8± 59 3.6 ± 125 ± 83 ± 1722 ± 12.8 ± 32.7 ± 57.7 ± 2.62 ± 3.12 ±

39 ± 81.5 ± 158.6 ± 33.6 ± 83.3 ± 0.79 ± 7± 65*** 4.1 ± 131 ± 86 ± 1792 ± 13.1 ± 31.4 ± 58.5 ± 3.25 ± 2.57 ±

0.02 0.003 0.23 0.001 0.24 0.31 0.34 0.005 0.51 0.002 0.03 0.36 0.54 0.39 0.71 0.001 0.002

9 5.4 5.9 2.2 3.4 0.06 3 2.4 21 11 418 1.3 4.0 6.3 0.72 0.73

8* 6.1* 6.1 2.6* 4.5 0.05 5 2.8 29* 13* 417 1.5 4.6 5.1 0.81** 0.62

6** 7.2*** 5.3 4.7** 6.6 0.08 3 3.4 32*** 16** 543 1.7 5.2 6.2 0.74*** 0.58**

†

p-Value were calculated from the one-way ANOVA. p < 0.05 from the post hoc comparisons (Scheffe test) between overweight or obese subjects compared normal weight subjects. ** p < 0.01 from the post hoc comparisons (Scheffe test) between overweight or obese subjects compared normal weight subjects. *** p < 0.001 from the post hoc comparisons (Scheffe test) between overweight or obese subjects compared normal weight subjects. *

Table 2 Plasma TAC levels, demographic, nutrient intake and anthropometric characteristics of the participants by body fat distribution. Variables

Normal body fat distribution (n = 98)

Abdominal adiposity (n = 62)

Age (years) Weight (kg) Height (cm) Body mass index (kg/m2 ) Waist circumference (cm) Waist-to hip ratio Education status (years of school) Physical inactivity (%) Number of pregnancies Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Energy intake (kcal/d) Protein (% energy) Total fat (% energy) Carbohydrate (% energy) Plasma MDA levels(␮mol/L) Plasma TAC levels (␮mol/L)

28 ± 64.4 ± 157.2 ± 26.6 ± 81.5 ± 0.76 ± 8± 58 3.8 ± 128 ± 85 ± 1776 ± 13.2 ± 33.9 ± 59.5 ± 2.23 ± 3.16 ±

35 ± 76.4 ± 158.3 ± 27.4 ± 96.3 ± 1.02 ± 7± 67** 4.7 ± 136 ± 88 ± 1832 ± 14.5 ± 35.8 ± 62.4 ± 3.28 ± 2.41 ±

6 6.3 6.1 3.4 5.2* 0.03 6 3.4 31* 11* 521 2.4 5.5 7.3 0.52 0.84

8** 5.1** 7.2 4.7 6.0** 0.04** 5 4.6** 43** 16* 632 2.7 6.4 7.8 0.78*** 0.59**

* p < 0.05 from the independent t-test between subjects with normal body fat distribution compared to subjects with abdominal adiposity. ** p < 0.01 from the independent t-test between subjects with normal body fat distribution compared to subjects with abdominal adiposity. *** p < 0.001 from the independent t-test between subjects with normal body fat distribution compared to subjects with abdominal adiposity.

Evaluation of oxidative stress and total antioxidant capacity in obese women

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Table 3 Partial correlation coefficients between MDA and TAC levels with anthropometric indices in all the subjects (n = 160).a . Anthropometric indices

Plasma MDA (␮mol/L) Correlation coefficients (r)

p-Value

Correlation coefficients (r)

p-Value

Weight (kg) BMI(kg/m2 ) Waist circumference (cm) Waist-to-hip ratio

0.185 0.464 0.582 0.474

<0.01 <0.0001 <0.0001 <0.0001

−0.23 −0.27 −0.37 −0.30

<0.001 <0.001 <0.0001 <0.001

a

Plasma TAC (␮mol/L)

Adjusted for age, number of pregnancies, systolic and diastolic blood pressure and nutrient intakes.

to overweight and obese women (p = 0.02). As we can see from the descriptive results presented in Table 1, obese women had higher MDA (p < 0.001) and lower TAC levels (p < 0.01) compared to normal weight women. Although significant difference was observed between overweight and normal weight women in MDA levels (p < 0.01), no significant difference was observed between these groups in plasma TAC levels (Table 1). In Table 2, demographic, nutrient intakes and anthropometric characteristics of the participants by body fat distribution are shown. As shown in this table, women with central body fat distribution had higher MDA (p < 0.001) and lower TAC levels (p < 0.01) compared to normal body fat distribution. Moreover, all anthropometric indices studied (i.e. weight, BMI, WC and WHR) were positively correlated with plasma MDA levels and inversely correlate with plasma TAC levels (Table 3). As expected, an inverse relationship was observed between plasma MDA and TAC levels (r = −0.26, p < 0.001). However, the previous findings may be confounded by several clinical, lifestyle and demographic characteristics of the participants. Therefore, we adjusted our analyses for several confounders like age, physical activity, number of pregnancies, systolic and diastolic blood pressures and nutrient intakes. Table 4 shows the results from the multiple linear regression models. We observed that MDA and TAC levels were independently associated with anthropometric indices studied (i.e. WC, WHR and BMI). Moreover, presence of MDA and TAC levels as independent variables seems to have higher explanatory ability in the models that evaluated BMI (i.e. higher R2 ) than the model-evaluated WC or WHR.

Discussion In this study, we revealed that obese and overweight women had higher plasma MDA (as oxidative stress marker) compared to normal weight women.

Furthermore, we found that abdominal adiposity as determined by high waist circumference significantly associated with increased plasma levels of MDA. The notion that obesity is associated with a state of increased oxidative stress is not without precedent and evidence that obesity is related to an increase in oxidative stress can be found in the literature [21—23]. Despite much evidence which indicates obesity is a state of oxidative stress, the mechanisms contribution to increased reactive oxygen species (ROS) production in obesity remains still elusive. During past years, several mechanisms have been reported by previous studies that obesity can increases production of ROS. For example, Vincent et al. [12] in their study reported increased the mechanical and metabolic load on the myocardium, thus increasing myocardial oxygen consumption. A negative consequence of such increased myocardial oxygen consumption is the production of ROS such as superoxide and hydrogen peroxides from increased mitochondrial respiration [24]. Furthermore, oxidative stress elevated due to decreased antioxidant enzymes such as copper zinc-superoxide dismutase (CuZn-SOD) and glutathione peroxidase (GPX) have shown in published studies [13,23]. It is well-established that abdominal adiposity is more closely associated with the risk of cardiovascular disease and diabetes than general adiposity [25,26], but this relationship has not been fully illustrated. Human abdominal visceral adipose tissue has been reported to release more inflammatory factors (i.e. interleukin-6) compared to subcutaneous adipose tissue [27]. There may be differences in oxidative stress and inflammation between subjects with and without increased abdominal adiposity. Therefore, we assessed MDA levels, as marker of oxidative stress in abdominal obese women. In our results, women who were abdominal obese showed higher levels of MDA compared to women with normal body fat distribution. This finding comes in accordance with findings of other studies that found increased oxidative stress

WC, waist circumference, WHR, waist-to-hip ratio, BMI, body mass index, MDA, malondialdehyde, TAC, total antioxidant capacity. a p-Value derived from linear regression models that evaluated the association of anthropometric indices (independent) on MDA and TAC (dependent), after adjusting for age, physical activity, number of pregnancies, systolic and diastolic blood pressures and nutrient intakes.

0.001 0.002 9.4 8.5 4.275 −3.451 0.539 −0.342 0.04 ‘0.03 6.4 7.6 2.879 −2.188 0.247 −0.176 0.002 0.03 8.3 7.2 3.470 −2.156 0.349 −0.194

Beta Beta

t

pa Variables

MDA (␮mol/L) TAC (␮mol/L)

R2 (%) t Beta R2 (%) R2 (%)

t

WHR standardized coefficient WC standardized coefficient

pa

BMI Standardized coefficient

pa

F. Amirkhizi et al. Table 4 Results from multiple linear regression analysis that evaluated the association between dependent (MDA and TAC) and independent (WC, WHR and BMI) variables.

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in central fat distribution [21,28]. One of the studies by Furukawa et al. [21] illustrated that plasma adiponectin levels negatively related with oxidative stress levels and that probably increased oxidative stress in accumulated fat leads to decreased production of adipocytokines. After we confirmed a positive association between general and abdominal adiposity with plasma MDA levels, we attempted to identify factors associated with increased MDA levels. Two possible factors may lead to increased oxidative stress: the increasing production of free radicals and the declining body antioxidant system activities. Therefore, we assessed plasma total antioxidant capacity (TAC) levels in participants. Plasma levels of each antioxidant can be measured separately in the laboratory, but measurements are time-consuming, labor-intensive and costly. Since the effects of the antioxidant components in plasma are additive, measurement of TAC can accurately reflect the redox status of the plasma [29]. Thus, instead of measuring individual antioxidant components of plasma in multiple tests, one TAC measurement may be more useful and practical to evaluate the plasma antioxidant status of participants. However, the results of our study indicate that the antioxidant defense system is compromised in general and abdominal adiposity, as evidence by increased MDA levels and decreased levels of TAC in plasma. This finding was in line to previous reports, which found decreased plasma TAC levels in general, and central adiposity [28,30]. Furthermore, Suzuki et al. [31] have found decreased serum levels of carotenoids (as antioxidant components in serum) in women with abdominal adiposity. Decreased plasma TAC levels in obesity and fat accumulation may indirectly indicate whole free radical activity. Interestingly, plasma TAC levels decreased in both overweight and obese groups but this was only significant in obese group, probably because the free radical activity were more marked in this group. These states of oxidative stress and TAC levels in general and abdominal adiposity might be closely linked to the occurrence of cardiovascular events. Although the cross-sectional design of this study precludes inferences of causality, it is not likely that the observed associations were confounded by all factors of which were controlled for in the analysis. Furthermore, unlike previous studies, we used a case-control design, which is particularly efficient in controlling for the confounding effect of BMI, allowing us to compare people with different fat distribution but the same BMI. One limitation of this study is that we could not assess metabolic

Evaluation of oxidative stress and total antioxidant capacity in obese women syndrome status, lipid profile, C-reactive protein, plasma glucose levels and nutrient intakes (including antioxidant nutrients) of participants. Other limitations of our study were the limited number of subjects, and the fact that only women were included in the analysis. In conclusion, the present study provides further evidence suggesting that obesity and, especially, abdominal adiposity leads to oxidative stress, which in turn, may contribute to obesity related diseases such as atherosclerosis, diabetes mellitus and arterial hypertension. Furthermore, the study shows that in healthy women, plasma oxidative stress and TAC levels associated with abdominal adiposity independent of BMI, thus supporting current recommendations that in women with high BMI (obese women), waist circumference should be measured to identify women at high cardiovascular and metabolic risk.

Conflict of interest The authors declare that they have no conflict of interests.

Acknowledgements The authors are very grateful to Mrs. Sara Minaie who helped greatly in conducting the study and the interviews, and also to Mrs. Maryam Chamari who helped to data collection. We also extend our sincerest thanks to all subjects who served as samples of this study.

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