ORIGINAL ARTICLE

METABOLIC SYNDROME AND RELATED DISORDERS Volume XX, Number XX, 2015  Mary Ann Liebert, Inc. Pp. 1–10 DOI: 10.1089/met.2015.0064

Cardiorespiratory Fitness and Light-Intensity Physical Activity Are Independently Associated with Reduced Cardiovascular Disease Risk in Urban Black South African Women: A Cross-Sectional Study Kasha Dickie, MSc,1 Lisa K. Micklesfield, PhD,1,2 Sarah Chantler, MSc,1 Estelle V. Lambert, PhD,1 and Julia H. Goedecke, PhD1,3

Abstract

Background: Low levels of physical activity, poor cardiorespiratory fitness, and a sedentary lifestyle have been associated with increased risk for cardiovascular disease (CVD) and type 2 diabetes (T2D). Few studies have examined their independent associations in an urban black sub-Saharan African population. Objectives: To examine the independent associations of physical activity, cardiorespiratory fitness, and sedentary time on body composition and cardiometabolic risk factors for CVD and T2D in black South African women. Materials and Methods: A subsample (n = 76; 18–45 years) was recruited, as part of a cross-sectional study. Accelerometry, cardiorespiratory fitness, body composition, insulin sensitivity, serum lipids, and blood pressure were measured. Results: Light- but not moderate- to vigorous intensity physical activity was inversely associated with trunk fat mass (r = -0.25, P = 0.03). Sedentary time was associated with triglyceride (TG) (r = 0.36, P = 0.01) and TG/ HDL-C (r = 0.34, P = 0.04), and these relationships were independent of body fat. Cardiorespiratory fitness was inversely associated with body fat % (r = -0.34, P = 0.02), central fat mass (r = -0.31, P = 0.03), visceral adipose tissue (VAT, r = -0.47, P < 0.01), and insulin resistance (HOMA-IR; r = -0.41, P = 0.01). The association between cardiorespiratory fitness and HOMA-IR was independent of body fat and physical activity, but not VAT. Cardiorespiratory fitness was inversely associated with sedentary time (r = -0.31, P = 0.03), but not with any of the physical activity variables (P > 0.05). Conclusion: Both physical activity and cardiorespiratory fitness were associated with reduced total and central fat mass, VAT, and reduced cardiometabolic risk for CVD and T2D. Longitudinal studies are required to confirm whether the promotion of increasing light physical activity, while reducing sedentary time and increasing cardiorespiratory fitness, reduces the risk for obesity, CVD and T2D. etiology of obesity is complex, common antecedents for its development include low levels of physical activity and a sedentary lifestyle.3 Given the differences in environmental and lifestyle factors, as well as body composition and cardiometabolic risk factors between high- and low- to middle income countries such as South Africa,4 it is important to establish the relationships between these variables in different settings.

Introduction

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oncommunicable diseases (NCDs), including cardiovascular disease (CVD) and type 2 diabetes (T2D), constitute the second highest cause of mortality in South Africa.1 This may be due, in part, to the high prevalence of obesity and its rapid secular increase, particularly among urban black South African (SA) women.1,2 Although the 1

Division of Exercise Science and Sports Medicine, Department of Human Biology, University of Cape Town, Cape Town, South Africa. MRC/Wits Developmental Pathways for Health Research Unit, Department of Paediatrics, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa. 3 Non-Communicable Disease Research Unit, South African Medical Research Council, Tygerberg, South Africa. 2

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However, to date, most of the research has been performed in predominantly white populations from high-income countries, with a dearth of research exploring this in urban black populations, and those from low- to middle income countries. A small number of South African studies have examined the association between physical activity, in particular moderate- to vigorous intensity physical activity and body composition variables,5–8 while only one study has examined the association with cardiometabolic risk for CVD and T2D.5 In addition, their use of anthropometric derived body composition measures5 limits the investigation of relative and absolute body fat measurements and its distribution. The use of higher precision body composition methods (dual-energy X-ray absorptiometry (DXA) and computed tomography [CT]) may strengthen the previous associations5 found, and allow exploration of associations with body fat distribution variables, namely visceral and subcutaneous adipose tissue (SAT) depots. As the majority of physical activity reported in South Africa is walking for transport, which is typically undertaken at low intensities,9 it is also important to examine the relationships between objectively measured physical activity performed at different intensities, including lower-intensity physical activity (light intensity and steps/day), which is often neglected, and body composition and cardiometabolic risk factors among urban black SA women at risk for these NCDs. Physical activity and cardiorespiratory fitness are two distinct entities with independent and different associations with body composition and cardiometabolic risk factors for CVD and T2D.10 To our knowledge, there is only one other South African study that has examined cardiorespiratory fitness level in rural black adult women, but did not examine its relation to body composition and cardiometabolic risk outcomes for CVD or T2D.5 Therefore, relationships between cardiorespiratory fitness and body composition variables, as well as cardiorespiratory fitness and cardiometabolic risk factors for CVD and T2D, independent of physical activity measured objectively need to be examined. Evidence suggests that independent of physical activity, the greater the amount of time spent in sedentary behaviors, the greater the risk of cardiometabolic disease.11–13 Other cross-sectional studies and prospective studies14–16 demonstrate positive associations between higher body mass index (BMI) and sedentary behavior. To our knowledge, there are two South African studies that have examined the association between objectively measured sedentary behavior and body composition and cardiometabolic risk outcomes for CVD and T2D among black rural women6,7 and none in relation to black urban women. Therefore, the aim of this cross-sectional study is to examine the independent associations between physical activity, cardiorespiratory fitness and sedentary time, and body composition measures and cardiometabolic risk factors for CVD and T2D, in a sample of urban black SA women.

Methods Participants The study population consisted of a subsample (n = 76) of premenopausal urban black SA women recruited as part of a follow-up study of a larger cohort (n = 240), for which the details have been published previously.17 Of the original 240 women, 108 were noncontactable, 38 women refused to

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participate in the present study, 8 women disclosed that they were HIV positive and/or taking antiretroviral medication, 1 woman was reported dead by a family member, and another woman had recently given birth and was lactating. Furthermore, 9 women were excluded due to invalid physical activity data. The original convenience sample of women, between the ages of 18 and 45 years, was recruited from advertisements in local newspapers, church groups, community centers, and universities, and excluded if they had known diseases, were taking medication that would alter metabolism, or were pregnant, lactating, or postmenopausal. Only cross-sectional data of the 76 urban black SA women are presented here. The study was conducted according to the guidelines in the Declaration of Helsinki, and all procedures were approved by the Human Research Ethics Committee of the Faculty of Health Sciences at the University of Cape Town. Written informed consent was obtained from all the participants before participation in the study.

Testing procedures Lifestyle and sociodemographic factors. All methods have been previously described.17 In brief, lifestyle factors and socioeconomic status (education, employment, and housing density) were assessed using questionnaires. Participants were categorized as smokers based on current use of tobacco products. Those who consumed ‡1 drink/week (equivalent to 10 g alcohol) were categorized as consumers of alcohol. Participants were categorized according to hormonal contraceptive use (oral or injectable vs. none). Education was categorized according to those who had completed grade 12 and those who had not. Participants were categorized as employed (including students) or unemployed. Housing density was defined as the number of persons in the household divided by the number of rooms. In addition, data on ‘‘motor vehicle ownership’’ defined as owning or having the use of a motor vehicle were also collected. Body composition and body fat distribution. Basic anthropometry (weight and height) in light-weight clothing without shoes was measured using a standard scale and stadiometer, respectively (Detecto, Model UWE BW-150; Cardinal Scale Manufacturers, Webb City, MO). BMI was calculated as weight in kilograms divided by height in meters squared. Waist circumference at the level of umbilicus, and hip circumference at the largest part of the hips were both measured. Waist to hip ratio was also calculated. Whole body composition, including fat mass and fat-free soft tissue mass, was measured by DXA (Discovery-W, software version 12.7.3.7; Hologic, Bedford, MA) according to standard procedures. In vivo precision (CV) was 0.7% and 1.67% for fat-free soft tissue mass and fat mass, respectively. Regional body fat distribution was characterized as trunk fat mass and appendicular fat mass, as previously described.18 CT (Toshiba X-press Helical Scanner, Japan) at the level of L4–L5 lumbar vertebrae was used to measure abdominal visceral adipose tissue (VAT) and SAT areas. Cardiometabolic outcomes. Cardiometabolic measurements included resting blood pressure (BP), fasting serum lipid levels, fasting plasma glucose and serum insulin concentrations, and an oral glucose tolerance test (OGTT). After an overnight fast, participants ingested 75 g of glucose diluted in 250 mL of water, following which blood samples were

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taken at 30-min intervals for 2 hr for the subsequent measurement of plasma glucose and serum insulin concentrations. After at least 5 min of seated rest, BP was measured thrice at 1-min intervals using an appropriate-sized cuff and an automated BP monitor (Omron 711; Omron Health Care, Hamburg, Germany). An average of the last two readings was used for analyses. Serum total cholesterol (TC) (intra-assay % CV: 0.4%), triglyceride (TG) (intra-assay % CV: 0.6%), and high-density lipoprotein cholesterol (HDL-C) (intra-assay % CV: 0.55%) concentrations were measured on the Roche Modular Auto Analyzer (Roche/Hitachi Cobas C System from Roche Diagnostics GmbH, Mannheim, Germany) using enzymatic colorimetric assays. Low-density lipoprotein cholesterol (LDL-C) was calculated using the Friedewald equation.19 Fasting plasma glucose levels were measured using the glucose oxidase method (YSI 2300 STAT PLUS; YSI Life Sciences, Yellow Springs, OH; with intra-assay CV: 1.17% and interassay CV: 2.29%). Fasting serum insulin levels were measured by a Microparticle Enzyme Immunoassay (MEIA) (AxSym Insulin Kit, Abbot, IL) (intra-assay CV: 3.28% and interassay CV: 5.45%). The homeostasis model of insulin resistance (HOMA-IR) was calculated from the fasting insulin and glucose concentrations,20 and the Matsuda insulin sensitivity index21 was calculated from the OGTT. Physical activity. Physical activity was measured using accelerometry. The uniaxial ActiGraph MTI 7164 accelerometer (ActiGraph LLC, Pensacola, FL) was worn for 7 consecutive days by each participant. Recording of physical activity began on the first day, 2 hr after the monitor was received, and was completed when returned 8 days later. Participants were instructed to wear the accelerometer on their right hip, attached by an elastic belt, during waking hours. As the monitors were not waterproof, the women were asked to remove the belt while bathing, showering, or swimming. The time sampling interval was set at 60 sec epochs. The original ActiGraph data files (*.dat) were downloaded onto a personalized computer and processed on a Microsoft Excel spreadsheet using a custom-written program (‘‘MAHUFFE,’’ www.mrc-epid.cam.ac.uk). Data from each participant were included if they met the minimum requirement of 10 hr or more of monitor wear time on 4 or more days of the week. Wear time was determined by subtracting nonwear time from 24 hr, where non-wear time was defined as an interval of ‡60 consecutive minutes with zero activity counts allowing for intervals of 1–2 min of relatively low activity counts per minute ( 0.05) (Table 3).

Discussion Although 96.1% of the apparently healthy urban black SA women included in this study were overweight or obese, more than half of them met the Global Physical Activity Recommendations for Health27 and the recommended goal of ‡10,000 steps/day.28 We have shown that time spent in light-intensity physical activity, as well as steps/day, but not moderate- to vigorous intensity physical activity, was associated with lower body fat measures. Independent of fat mass, steps/day was associated with improved insulin sensitivity, whereas increased sedentary time was associated with an unfavorable serum lipid profile. Higher cardiorespiratory fitness was associated with reduced whole body and central fat mass, and VAT. In addition, higher cardiorespiratory fitness was associated with improved insulin sensitivity, independent of fat mass and physical activity, but not VAT. Furthermore, although there were no associations between cardiorespiratory fitness and any of the physical activity variables, cardiorespiratory fitness was inversely associated with sedentary time. To date, most research has focused only on the effects of moderate- to vigorous intensity physical activity, with little attention on light-intensity activities. Higher levels of moderate- to vigorous intensity physical activity have been associated with lower BMI and favorable patterns of body fat distribution.29 In contrast and irrespective of the majority of women meeting the recommended moderate- to vigorous intensity physical activity guidelines, results from the present study showed that greater light-intensity PA, and not moderate- to vigorous intensity physical activity, was associated with lower body fat and central accumulation of fat.

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The majority of physical activity time was spent in light intensity (*5.3 hr/day). We used the Freedson cut points,22 which have been used in other studies.30 However, using the Troiano cut points [31], which were used in the National Health And Nutrition Examination Surveys,31 the proportion of time spent in light-intensity PA and moderate- to vigorous intensity physical activity was remarkably similar to those in our study (median: 320 vs. 318 min/day and 27 vs. 31 min/ day for Troiano and Freedson, respectively). Rather, differences in our findings to others may be due to the relatively low proportion of moderate- to vigorous intensity physical activity performed by the women in the present study compared to higher levels performed by women in larger prospective studies from low- to middle income countries.32,33 Similar to our findings, Cook et al.6 reported a dose-dependent relationship between the number of steps/day and reduction in obesity risk in a rural sample of SA women. After adjusting for age, motor vehicle access, education, tobacco use, and comorbidities, BMI was shown to be 1.4 kg/m2 lower per 5,000 steps/day. These findings may suggest that the WHO PA cut points, largely based on self-report epidemiology and not objective measures, be revised. In addition, the independent effects of light-intensity physical activity on body composition should be examined in further longitudinal studies to verify whether light-intensity physical activity is associated with improvements in health in other populations. We have also shown that increased physical activity was weakly but significantly associated with improved insulin sensitivity. Specifically, the total number of steps/day was inversely associated with fasting serum insulin concentrations and HOMA-IR, while moderate- to vigorous intensity physical activity was inversely associated with 2-hr plasma glucose levels. However, all of these associations were not independent of total body fat. This contrasts to other studies that have shown an association between total physical activity and reduced cardiometabolic risk for T2D, independent of differences and changes in adiposity.12,30 The low intensity of the activity performed by the participants in this study could possibly explain this difference. High-intensity physical activity is associated with cardiometabolic changes that, for example, including an increase GLUT4, increase target tissue sensitivity (liver, skeletal muscle, and adipose tissue) and lead to an overall improvement in plasma glucose regulation, which is independent of the effects on body fatness.34 The results from the present study showed that greater cardiorespiratory fitness was associated with lower total adiposity, as well as less centralization of body fat, in particular, lower VAT. Comparably, Cook et al.5 used a similar measure to predict cardiorespiratory fitness among a group of rural black SA women (*36.3 years) and showed that those with the highest cardiorespiratory fitness had significantly less body fat. In a sample of African American and European American women, Hunter et al.34 showed that women in the highest cardiorespiratory fitness tertile had lower abdominal VAT compared to women in the other two tertiles. Together, the results suggest that cardiorespiratory fitness may have positive health benefits by maintaining favorable adiposity levels and reducing VAT. In contrast to physical activity, the associations between cardiorespiratory fitness and improved serum lipid concentrations and measures of insulin sensitivity were independent of fat mass (kg). Notably, these associations were also independent of physical activity. These results support those

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from a prospective study, in which individuals who increased their cardiorespiratory fitness over a period of 1 year had reduced levels of fasting plasma glucose and fasting serum insulin and increased concentrations of HDL-C at follow-up (ProActive trial).35 Furthermore, a low cardiorespiratory fitness level has been shown to be a strong and independent predictor of incident cardiometabolic syndrome, independent of BMI.36 Unique to our study was our ability to measure body fat distribution using DXA- and CT-scanning techniques. The inverse association between cardiorespiratory fitness and VAT is of significance, as results from the Framingham Heart Study showed that VAT was more closely associated with insulin resistance than SAT.37 In this study of urban black SA women, we showed that the association between cardiorespiratory fitness and insulin sensitivity was mediated through VAT. This was a surprising result given that research from our laboratory38 and others39 has shown that urban black women have less VAT than BMI-matched white women and that insulin resistance is more closely associated with SAT than VAT in urban black SA women. In contrast to other studies,40,41 we did not find an association between sedentary time and body composition measurements. However, we did show an inverse association between sedentary time and cardiorespiratory fitness. This finding is supported by cross-sectional studies in young adolescent girls,42,43 as well as in an intervention study, which showed a reduction in sedentary time with the increasing cardiorespiratory fitness level.44 Despite no associations with body composition, we showed an association between sedentary time and serum lipid concentrations (TG and TG/HDL-C ratio). This finding is supported by other studies that have shown an association between sedentary behavior and increased risk for CVD and cardiometabolic-related diseases.11,13 It has been proposed that these effects may be mediated by a reduction in the lipoprotein lipase (LPL) activity when exposed to acute and chronic periods of sedentary behavior.45 The strengths of the present study include the use of robust and high-precision measurements. Although the total sample size and the number of women who completed the submaximal step test were low, the study still showed independent associations between body composition measures, cardiometabolic risk factors for CVD and T2D, and fitness level. Although we cannot exclude the possibility of a biased selection, the majority of the women that were not included in the study were noncontactable, which is typical of a population in transition, and only 16% of the women refused to participate in the study. However, these results should be viewed as hypothesis generating and should be repeated in a larger more representative sample. Physical activity and cardiorespiratory fitness accounted for only 25% of the variance in VAT and insulin resistance; further studies are required to determine the contribution of other lifestyle factors, including dietary intake, to the remaining variance in cardiometabolic risk. Indeed, a recent meta-analysis comparing objectively measured physical activity energy expenditure among adult women between high- and lowto middle-income countries has questioned the impact of physical activity energy expenditure on body composition.46 Despite group differences in body size reported by Dugas et al.,46 total physical activity energy expenditure was the same for both groups (high- and low- to middle income countries). Thus, the disparity in the prevalence of obesity that exists between highand low- to middle income countries may be the result of other lifestyle factors. This should be addressed in future studies.

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Conclusions In conclusion, the present study showed that higher cardiorespiratory fitness and light-intensity physical activity were associated with reduced adiposity and lower VAT among a sample of apparently healthy urban black SA women. In addition, higher cardiorespiratory fitness level was also associated with lower cardiometabolic risk for CVD and T2D. Although, the majority of women met the WHO Global physical activity recommendations, it was light-intensity physical activity and cardiorespiratory fitness, rather than moderate- to vigorous intensity physical activity, which were more closely associated with reduced total and central fat mass and improved insulin sensitivity. These findings should be confirmed in larger independent cohorts, that include men, and future studies should also consider the contribution of other lifestyle factors, including dietary intake, to cardiometabolic risk.

Acknowledgments The authors thank the research volunteers for their participation in this study, Nandipha Sinyanya for her fieldwork, Hendriena Victor for her technical assistance, and Linda Bewerunge for performing DXA scans. This study was funded by the Sugar Association of South Africa, the Medical Research Council of South Africa, the International Atomic Energy Agency, and the National Research Foundation of South Africa.

Authors’ Contributions K.D. was involved in the conception and design of the research study, data cleaning, and analysis, as well as in the drafting and writing of the article and general management of the research team. S.C. assisted with data collection, the cleaning and analysis of some of the data, and in the writing and editing of the article. J.H.G. and L.K.M. were both involved in the conception and design of the research study and assisted and guided the statistical analysis and the writing and editing of the article. E.V.L. assisted with editing the article. All authors read and approved the final article.

Author Disclosure Statement No conflicting financial interests exist.

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Address correspondence to: Julia H. Goedecke, PhD Non-Communicable Disease Research Unit South African Medical Research Council PO Box 19070 Tygerberg 7505 South Africa E-mail: [email protected]

Cardiorespiratory Fitness and Light-Intensity Physical Activity Are Independently Associated with Reduced Cardiovascular Disease Risk in Urban Black South African Women: A Cross-Sectional Study.

Low levels of physical activity, poor cardiorespiratory fitness, and a sedentary lifestyle have been associated with increased risk for cardiovascular...
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