Abdominal obesity is an established risk factor for both metabolic and cardiovascular diseases (7). Excess levels of fat located within the intra-abdominal cavity in particular, including visceral adipose tissue (VAT), intermuscular adipose tissue (IMAT), and liver fat, are associated with an increased risk of insulin resistance, dyslipidemia, glucose intolerance, hypertension, and cardiovascular disease (23,27,32,33). Subcutaneous adipose tissue (SAT) on the other hand may be relatively less important in the pathophysiology of chronic disease development (15).
General adiposity has several putative contributors, and the level of physical activity is considered a key factor. The health benefits of physical activity are well established and include a reduction in risk for many common chronic diseases, as well as reducing fat deposition, independent of body mass index (BMI) (19). Recent studies have identified associations between sedentary behaviors (e.g., sitting or lying down) and adverse health outcomes, including cardiovascular disease, diabetes, cancer, and all-cause mortality (3). Cross-sectional evidence also suggests that meeting guidelines for physical activity may not be sufficient for chronic disease prevention if accompanied by high levels of sedentary time (11). A potential pathway through which sedentary behavior may independently predict chronic disease progression is body composition, particularly amount and type of intra-abdominal fat depots.
Few studies have examined the associations between sedentary behavior and intra-abdominal fat depots, with mixed results. Some evidence suggests a positive association between sedentary time and VAT (13,26,31), whereas other studies report no association (20,22,29). To our knowledge, only one study has examined the associations between sedentary behavior and liver fat (13), or sedentary behavior and abdominal IMAT (20), two fat depots that may be independent predictors of metabolic risk (27,33). Previous studies examining sedentary behavior and intra-abdominal fat depots have been limited by small samples with little racial/ethnic diversity.
We address these important gaps in the literature by studying a large sample of Black and White men and women who completed a detailed sedentary behavior questionnaire and had computed tomography (CT) measured abdominal VAT, SAT, IMAT, and liver attenuation (a diagnostic method to assess liver fat). The aim of this study was to examine whether sedentary lifestyle habits and physical activity level are associated with abdominal fat depots (VAT, SAT, and IMAT) and liver attenuation, independent of each other and potential confounders. We hypothesized that sedentary time would be positively, and physical activity level inversely, associated with abdominal fat depots, and that sedentary time and physical activity would be independent and additive in their prediction of abdominal fat depots. Given the known race and sex differences in abdominal adipose distribution (18,30) and the potential differential effects on cardiovascular disease risk (1,9), we also examined if these associations vary by sex and race.
Coronary Artery Risk Development in Young Adults (CARDIA) is an ongoing prospective cohort study of 5115 Black and White men and women who were initially recruited in 1985–1986 from four urban centers: Birmingham, Alabama; Minneapolis, Minnesota; Chicago, Illinois; and Oakland, California. Participants completed additional measurement visits in 1987–1988 (year 2), 1990–1991 (year 5), 1992–1993 (year 7), 1995–1996 (year 10), 2000–2001 (year 15), 2005–2006 (year 20), and 2010–2011 (year 25). A total of 3173 participants who underwent abdominal CT scans in year 25 had complete data on VAT, SAT, and IMAT. Of those with complete VAT, SAT, and IMAT data, 36 participants did not complete a sedentary behavior or physical activity questionnaire, and 127 were missing data on study covariates, resulting in a final sample size of 3010 for analyses of VAT, SAT, and IMAT. After the previously mentioned exclusions, data on liver attenuation were available for 2995 participants. Heavy alcohol consumption (more than four drinks per day for men and more than three drinks per day for women), but not moderate alcohol consumption (more than two drinks per day for men and more than one drink per day for women), was associated with lower liver attenuation. We therefore excluded an additional 78 participants who reported heavy alcohol consumption, resulting in a final sample of 2917 for analyses of liver attenuation. Written informed consent was obtained from all participants at each exam, and the institutional review board at each of the clinical centers approved all study protocols.
Sedentary behavior was assessed with a self-reported questionnaire. Participants were asked how much time they spend sitting while engaging in six separate sedentary tasks: 1) watching television; 2) using the computer for nonwork activities or playing video games; 3) doing noncomputer office work or paperwork; 4) listening to music, reading a book or magazine, or doing arts and crafts; 5) talking on the phone or texting; and 6) sitting in a car, bus, train, or other mode of transportation. Time spent in these sedentary tasks was queried separately for the average weekday and average weekend day. Response options were none, 15 min or less, 30 min, 1 h, 2 h, 3 h, 4 h, 5 h, or 6 h or more. Average sedentary hours per day for each of the six different tasks (television, computer, paperwork, music, phone, and car) was computed by multiplying the reported time spent in each activity on a weekday by five, and time spent in each activity on a weekend day by two, summing these two values to get average hours in each sedentary activity per week. The number of hours spent per week in each sedentary task, separately, was then divided by seven to get average sedentary hours per day. Total sedentary time per day was then calculated by summing the averages across the six different tasks.
Physical activity was assessed by self-report with the validated CARDIA physical activity history (8,16,17). Participants were asked to report the frequency of participation in 13 different activities (eight vigorous, five moderate) related to recreational sports, exercise, leisure, and occupational activities. Vigorous activities included jogging or running; racket sports; bicycling faster than 10 mph; swimming; vigorous exercise classes; lifting, carrying, or digging while on the job; snow shoveling, moving heavy objects, or weight lifting; and other strenuous sports (e.g., basketball). Moderate or more leisurely activities included nonstrenuous sports (e.g., softball), walks or hikes, bowling or golf, home exercise or calisthenics, and home maintenance or gardening. Total moderate and vigorous physical activity was calculated by multiplying the number of months the activity was performed by the intensity of the activity, weighting activities performed more frequently, and then summing across all activities. Details on frequency or duration of physical activity were not directly assessed; therefore, physical activity is expressed in exercise units, with separate scores for moderate- and heavy-intensity activity and for total physical activity. Approximately 300 exercise units are roughly equivalent to meeting physical activity recommendations, or 30 min of moderate-intensity activity, 5 d·wk−1 (8). A validation study of the CARDIA Physical Activity questionnaire found that heavy physical activity was significantly associated with maximal oxygen consumption (r = 0.63), accelerometer measured activity (r = 0.31), and total 4-wk activity history (r = 0.54; all P < 0.05) (16). Inverse associations have also been reported between total physical activity, assessed by the CARDIA physical activity history, and metabolic risk factors (5).
Abdominal adipose tissue depots were measured using CT scans, which were conducted at each of the CARDIA field centers at year 25. A noncontrast CT scan of the abdomen was performed with multidetector CT scanners (GE 750HD and GE LightSpeed VCT models were used at the Birmingham and Oakland Centers, respectively; GE Healthcare, Waukesha, WI; Siemens Sensation 64 models were used at both Chicago and Minneapolis Centers; Siemens Medical Solutions, Erlangen, Germany). The images were electronically transmitted to a CT reading center for image analysis and quality control at Wake Forest University School of Medicine, Winston-Salem, NC. CT scans of the abdomen were reconstructed into 5-mm slices with a maximum 50-cm field of view to include the whole abdomen. Adipose tissue depots were measured volumetrically from two adjoining 5-mm slices located at the level of the lumbar disk between the fourth and the fifth vertebra (L3–L4 for IMAT, to avoid interference with a pelvic bone). Tissues with attenuation between −190 and −30 Hounsfield units (HU) were defined as adipose tissue. Analysts segmented the images based on anatomical boundaries into the entire abdomen, abdominal wall, and intra-abdominal compartments using the Medical Image Processing, Analysis, and Visualization application (http://mipav.cit.nih.gov/index.php). VAT, SAT, and IMAT were quantified in each compartment.
Liver attenuation, a diagnostic method to assess liver fat, was measured using noncontrast CT images of the upper abdomen while in axial scan mode. Averages of three distinct CT slices at the level of the T12–L1 intervertebral space were calculated to provide mean hepatic attenuation in HU. Analysts were trained to avoid regions that included common hepatic lesions and hepatic vasculature. Liver attenuation is inversely related to liver fat content, such that lower levels of liver attenuation indicate higher levels of liver fat (10).
Study covariates assessed at year 25 included age, sex, race, education (years completed), study center, smoking (never, former, current), alcohol consumption (mL·d−1), fast food intake (frequency per week), sugar-sweetened beverage consumption, including regular soda and sweetened fruit drinks, sports, or energy drinks (frequency per week), and BMI (kg·m−2). For anthropometric measures, participants were dressed in light clothing without shoes. Body weight was measured to the nearest 0.2 kg using a calibrated balance beam scale. Height was measured using a vertical rule to the nearest 0.5 cm. BMI was calculated as weight in kilograms divided by height in meters squared.
All statistical analyses were conducted using SAS, version 9.4 (SAS Institute, Inc., Cary, North Carolina). Distributions of variables were examined; all dependent variables were approximately normal with low skewness and kurtosis. Total sedentary behavior and total physical activity were categorized into tertiles for descriptive purposes. A linear trend over sedentary and physical activity tertiles was tested using linear regression or chi-square test of independence, as appropriate. Differences by race and sex were tested using one-way ANOVA. Because of skewed distributions of independent variables (sedentary behaviors and physical activity), Spearman correlation coefficients were used to examine bivariate associations between abdominal adiposity measures, sedentary behaviors, and physical activity.
The first set of multivariable general linear regression models regressed means of VAT, SAT, IMAT, and liver attenuation on total sedentary time, followed separately by task-specific sedentary time (i.e., television, computer, paperwork, music, phone, and car). Model 1 adjusted for center, age, sex, race, education, smoking, alcohol, fast food intake, and sugar-sweetened beverage consumption. Model 2 additionally adjusted for total physical activity. Model 3 additionally adjusted for SAT in the models for VAT, IMAT, and liver attenuation. The betas for sedentary time in model 3 can be interpreted as the unique statistical effects of intra-abdominal fat depots, independent of any effects on total abdominal fat. The SAT models were adjusted for VAT. In model 4, we additionally adjusted for BMI (in addition to SAT or VAT) to further test for independence from effects of sedentary time on overall body size.
The second set of linear regression models regressed means of VAT, SAT, IMAT, and liver attenuation on total physical activity, followed separately by moderate and then heavy physical activity. The physical activity models followed the same pattern of adjustment as the sedentary behavior models; however, models 2–4 adjusted for total sedentary time, not total physical activity. All four models are displayed for total sedentary time. Because the addition of BMI beyond that of SAT or VAT did not appreciably alter study findings, only final models are included for task-specific sedentary time and physical activity. The beta regression coefficients for sedentary behaviors and physical activity models were standardized (e.g., 1 SD total sedentary behavior = 4.0 h·d−1, 1 SD television time = 1.5 h·d−1, 1 SD total physical activity = 275 exercise units). As activity levels and abdominal fat vary significantly by race and sex, we also examined interactions with race and sex by including cross-product terms in the models. Interactions were statistically significant for race and sex categories (P < 0.05); therefore, stratified results are reported. Given variation in the SD for sedentary behaviors and physical activity level by race/sex categories, the beta regression coefficients for the stratified models reflect the SD specific to each race/sex category.
As seen in Table 1, an inverse linear trend over sedentary tertiles was observed for age, years of education, alcohol consumption, physical activity (total, moderate, and heavy), and liver attenuation (indicating a positive association between sedentary time and liver fat). A positive trend over sedentary tertiles was found for fast food and sugar-sweetened beverage consumption, BMI, VAT, SAT, and IMAT. Current smokers reported greater levels of sedentary time as compared with those who never smoked. An inverse linear trend over physical activity tertiles was observed for BMI, VAT, SAT, and IMAT, and a positive trend was found for liver attenuation (see Table, Supplemental Digital Content 1, participant characteristics by tertiles of total physical activity, http://links.lww.com/MSS/A770).
Averages for total sedentary time, task-specific sedentary time, physical activity, and abdominal fat depots, stratified by sex and race, are located in Table 2. Differences by sex and race were statistically significant (P < 0.001) across all categories. Black participants reported more hours per day engaged in sedentary behaviors than White participants. Men reported higher levels of physical activity than women, with White men reporting the highest levels of activity and Black women reporting the lowest levels. Black participants had significantly lower VAT and IMAT and greater SAT and liver attenuation than White participants. This difference by race in VAT and IMAT was driven by the large difference in abdominal fat depots among Black and White men, as the difference in VAT and IMAT among Black and White women was nonsignificant. Overall, VAT and IMAT were higher in men than women, whereas SAT and liver attenuation were higher in women.
Total sedentary time and time spent watching television or using the computer were significantly associated with VAT, SAT, IMAT, and liver attenuation in bivariate analyses (P < 0.001; see Table, Supplemental Digital Content 2, spearman correlations and p-values between abdominal fat depots, sedentary behaviors, and physical activity, http://links.lww.com/MSS/A771). Total physical activity, moderate physical activity, and heavy physical activity were also significantly associated with VAT, SAT, and IMAT (P < 0.001), but not liver attenuation. Importantly, correlations were weak between sedentary time and physical activity (ρ = −0.18–0.02), consistent with previous reports in the literature (12), indicating that these are unique independent behaviors.
Sedentary behavior and abdominal adipose depots
The associations of total sedentary time with abdominal adipose depots and liver attenuation are shown in Table 3. Total sedentary time was positively associated with VAT after adjustment for demographics and lifestyle factors (models 1 and 2); however, this association was attenuated after adjustment for SAT (model 3) and BMI (model 4). When stratified by sex and race, the association between sedentary time and VAT was significant in White men only and remained significant in all models. For a 1 SD increment in total sedentary time per day for White men (2.9 h·d−1), VAT was greater by 6.0 cm3 (P = 0.007). A similar pattern was observed for IMAT and liver attenuation, with significant associations observed in White men only (β = 5.9 cm3, P = 0.010; β = −1.3, P = 0.003, respectively). Total sedentary time was positively and significantly associated with SAT in the total sample after adjustment. After stratifying, the association remained significant in all groups except Black men.
When examining task-specific sedentary time (i.e., television, computer, paperwork, music, phone, and car), we observed strong associations between time spent watching television and abdominal adipose depots in the total sample after adjustment for all covariates (see Table 4). No other task-specific sedentary behaviors were associated with abdominal adipose depots or liver attenuation (data not shown). Television viewing was significantly and positively associated with VAT, SAT, and IMAT after adjustment. No associations were observed between television viewing and liver attenuation in the total sample. After stratifying by sex and race, VAT, IMAT, and liver attenuation were significantly associated with television viewing in White men only. For each 1 SD increment spent watching television (1.2 h·d−1), VAT increased by 4.8 cm3 (P = 0.037), IMAT increased by 5.0 cm3 (P = 0.031), and liver attenuation decreased by 1.8 HU (P < 0.001) in White men. Television viewing and SAT were significantly associated in White women only, fully adjusted (β = 6.4 cm3, P = 0.016).
Physical activity and abdominal adipose depots
A robust inverse association was observed for total physical activity and VAT, SAT, and IMAT in the total sample after adjustment for all covariates (Table 5). For each 1 SD increment in physical activity (275 exercise units), VAT, SAT, and IMAT were lower by 7.6, 6.7, and 8.1 cm3, respectively (P < 0.001 for all). This finding was consistent by race and sex, except the association between physical activity and SAT in Black women (β = −2.6, P = 0.396). Physical activity was positively associated with liver attenuation after adjustment in the total sample. After stratifying, the association was significant in White men only (β = 1.1, P = 0.013). Results were similar when examining physical activity volume by intensity category (moderate and heavy) across race and sex groups (data not shown).
Sedentary behavior, physical activity, and abdominal adipose depots
Given that the association between total sedentary behavior and abdominal adipose depots appears to be driven by time spent watching television, we depict the adjusted means of abdominal fat depots and liver attenuation by tertiles of television viewing and total physical activity (low, moderate, and high) in Figure 1. Individuals reporting the lowest levels of television viewing and the highest levels of physical activity (referent group) had significantly lower VAT (118.4 cm3), SAT (316.6 cm3), and IMAT (136.2 cm3) compared with all other groups and higher liver attenuation (56.4 HU). Those reporting the highest levels of television viewing and lowest levels of physical activity had the highest average VAT (147.5 cm3) and IMAT (167.2) and lowest liver attenuation (54.2 HU). The Figure in Supplemental Digital Content 3 (http://links.lww.com/MSS/A772) illustrates the adjusted means for VAT, SAT, IMAT, and liver attenuation by tertiles of total sedentary time and physical activity. Findings were similar across abdominal fat depots, with the referent group having the lowest average VAT, SAT, and IMAT and the highest average liver attenuation values.
In this population-based cohort study, we found that sedentary time and physical activity were differentially associated with abdominal fat depots and liver attenuation. Although significant associations between television viewing, physical activity, and fat depots were observed in the entire cohort, the relationship between total sedentary time and VAT, IMAT, and liver attenuation was significant in White men only after controlling for physical activity and other potential confounders. Our findings add to the existing literature by demonstrating independent associations between sedentary behavior, physical activity, and various measures of abdominal adiposity, in a large population of Black and White adult men and women. These findings indicate potential differences in the magnitude of the association between sedentary behaviors and abdominal fat deposition by sex and race.
Our findings are consistent with other smaller studies that have also reported sex differences when examining the association between sedentary behaviors and abdominal fat deposition (13,26,31). For example, Henson et al. (13) reported positive associations between accelerometer measured sedentary time and magnetic resonance imaging measured VAT and liver fat in a sample of 66 White men and women at risk for type 2 diabetes. In their study, sedentary time had a stronger association with VAT in men than that in women, similar to our findings among Whites. In a cross-sectional sample of Chinese adults (N = 398), significant associations were observed for men, but not women, in self-reported hours per day of television viewing and CT-measured VAT and SAT (26). One other study to date has examined both sex and race differences in the associations of sedentary behaviors, physical activity, and abdominal fat depots. A multiethnic analysis of 539 older adults found stronger associations between physical activity, but not sedentary behavior, and VAT and IMAT in White men as compared with White, African American, and Filipino women (20).
The stronger associations observed in White men in our study and others may be partly explained by the greater absolute amount and variation of VAT and IMAT in this subpopulation as compared with Black men or women of either race. Alternately, it is possible that White men have different behavioral patterns than other groups, which may explain the stronger association. There may also be differences in how sedentary behaviors are recalled or reported by race and sex. Although it is unclear why we observed differences by race and sex, there is a clear need to further explore this heterogeneity to avoid inappropriately generalization of findings.
Interestingly, when examining associations between different sedentary behaviors and fat deposition, significant findings were observed for television viewing only, and not for time spent engaging in other sedentary tasks. To our knowledge, this is the first study to examine the associations of various types of sedentary behavior with CT-measured abdominal fat depots. Hu et al. (14) also reported stronger associations between television viewing and BMI as compared with time spent sitting at work, at home, or while driving in a sample of women from the Nurses' Health Study. Television viewing may have a unique effect on fat deposition and health risks as a result of increased snacking behaviors (4). Other potential mechanisms explaining the association between television viewing and abdominal fat deposition may include reduced resting metabolic rate or the influence of food and beverage advertisements on food consumption (6). It is also possible that recall of television viewing may be more accurate than other sedentary behaviors because time can be more easily quantified within the context of 30 or 60 min television programming.
We observed a robust association between physical activity and VAT, SAT, and IMAT. A weaker but statistically significant association was observed for physical activity and liver attenuation. The relationships observed between physical activity and abdominal fat depots are consistent with many (20,21,24,28) but not all studies in the literature (20,22,26). The associations between physical activity and fat depots did not differ when examining moderate- and heavy-intensity physical activity separately, indicating a potentially protective effect of physical activity on fat deposition at either intensity level. Furthermore, the association between physical activity and VAT was independent of both SAT and BMI, indicating that the relationship between physical activity and VAT cannot be fully explained by total adiposity.
Our findings make a novel contribution by examining the associations of sedentary behaviors and physical activity with IMAT and liver attenuation, two understudied abdominal fat depots that may be independent risk factors for cardiometabolic disease. A study by Yim et al. (33) found stronger associations between IMAT and glucose, protein-bound glucose, and total cholesterol than observed for VAT. Adverse associations have also been reported between liver fat and fasting glucose and triglycerides, independent of other fat depots (31). In our study, we found that among White men, total sedentary time and television viewing were adversely associated with IMAT and liver attenuation, whereas the opposite associations were observed for physical activity and these fat depots in the entire cohort. Only one other study to date has examined the associations of physical activity with abdominal IMAT (20). The authors also reported an inverse association between physical activity and IMAT; however, this was attenuated after adjustment for BMI. Our findings suggest that reducing sedentary time and increasing physical activity may result in lower levels of IMAT and liver fat, independent of total body adiposity, thus reducing cardiometabolic risk.
When we examined the combined association of television viewing and physical activity, we found that those reporting high levels of television viewing and low levels of physical activity had the highest levels of VAT, a strong risk factor for cardiometabolic diseases (2). Although television viewing and physical activity were independently associated with abdominal fat deposition, it appears that their relationship may be additive. Those who reported high levels of television viewing and low levels of physical activity had a 29 cm3 greater average VAT volume compared with those reporting low levels of television viewing and high levels of physical activity. This amount of VAT is equivalent to 39% of the population SD of VAT. Of note, we found that television viewing and physical activity were jointly associated with VAT, independent of SAT and BMI. It therefore appears that the associations of inactivity and activity with VAT may act through an independent mechanism beyond total body adiposity. Thus, when making recommendations related to adipose deposition, it appears important to emphasize both reducing sedentary time, particularly television viewing, and increasing physical activity.
A major strength of this study is the large sample size that allows for comparisons by sex and race. In addition, although sedentary behavior was self-reported, the questionnaire used in this study was more detailed than previous studies, allowing us to examine the associations of various types of sedentary behavior (e.g., television, computer) with intra-abdominal fat depots. Furthermore, we examined the associations of sedentary behavior and physical activity with multiple measures of adipose tissue, including IMAT and liver attenuation, which are understudied fat depots, and may play an independent role in cardiometabolic risk.
Although this study contributes novel findings to the existing literature, multiple limitations must be noted. This study was limited to Black and White adults; therefore, study findings cannot be generalizable to individuals from other racial/ethnic backgrounds. The cross-sectional study design limits inference on causality between sedentary behavior, physical activity, and abdominal adipose depots. Future studies are needed that follow individuals over time to assess the longitudinal effects of sedentary behavior and physical activity on adipose depots. It is also possible that unmeasured variables may have confounded the observed associations. For example, we were not able to fully control for diet quality or snacking behaviors. However, we did assess fast food frequency and sugar-sweetened beverage consumption, which are associated with unhealthy dietary patterns (25). Both sedentary behavior and physical activity were assessed through self-report, and sedentary time at work was not queried. It is therefore possible that subjects may have underreported their sedentary behavior and overreported their physical activity. Finally, we estimated liver fat using CT-measured liver attenuation, which is a less direct measurement method than biopsy or magnetic resonance techniques.
In conclusion, this study provides evidence that sedentary behavior, particularly television viewing, and physical activity have distinct, independent associations with abdominal adipose tissue deposition patterns. Importantly, the associations of television viewing in the entire sample and total sedentary time in White men remained after controlling for physical activity, SAT, and BMI. These findings suggest that sedentary behavior, particularly television viewing, may have a unique, independent influence on intra-abdominal fat depots that is not explained by total adiposity or total physical activity level.
The CARDIA is supported by contracts HHSN268201300025C, HHSN268201300026C, HHSN268201300027C, HHSN268201300028C, HHSN268201300029C, and HHSN268200900041C from the National Heart, Lung, and Blood Institute (NHLBI), the Intramural Research Program of the National Institute on Aging (NIA), and an intra-agency agreement between NIA and NHLBI (AG0005). This work was supported by grant R21 HL121627-01A1 from the National Heart, Lung and Blood Institute. KMW was supported in part by research training grant T32 HL007779. The authors thank the investigators, the staff, and the participants of the CARDIA study for their valuable contributions.
The authors report no conflicts of interest. The results of the present study do not constitute endorsement by the American College of Sports Medicine. The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation.
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