Journal of Physical Activity and Health, 2015, 12, 68 -73 http://dx.doi.org/10.1123/jpah.2013-0186 © 2015 Human Kinetics, Inc.
Official Journal of ISPAH www.JPAH-Journal.com ORIGINAL RESEARCH
The Effects of Sedentary Behavior on Metabolic Syndrome Independent of Physical Activity and Cardiorespiratory Fitness Anna E. Greer, Xuemei Sui, Andréa L. Maslow, Beau Kjerulf Greer, and Steven N. Blair Background: To date, no longitudinal studies have examined the influence of sedentary behavior on metabolic syndrome development while accounting for cardiorespiratory fitness. Purpose and Methods: This prospective study examined the relationship between sedentary behavior and incident metabolic syndrome while considering the effects of physical activity and cardiorespiratory fitness on the association among 930 men enrolled in the Aerobics Center Longitudinal Study. Results: A total of 124 men developed metabolic syndrome during 8974 person-years of exposure. After adjusting for covariates, men with middle and high sedentary behavior had 65% and 76% higher risks of developing metabolic syndrome, respectively, than men with low sedentary behavior (linear trend P = .011). This association remained significant after additional adjustment for activity status and cardiorespiratory fitness. Cardiorespiratory fitness and physical activity were also inversely associated with metabolic syndrome, even after adjustment for sedentary behavior. Conclusions: The findings highlight the importance of reducing sedentary behavior, increasing physical activity, and improving cardiorespiratory fitness for preventing metabolic syndrome. Keywords: exercise, longitudinal study, risk factors Approximately 34% of adults in the US have metabolic syndrome (MetS),1 a collection of conditions that increase a person’s risk of developing cardiovascular disease (CVD)2,3 and diabetes mellitus4 and risk of dying from CVD5 and all other causes.6 Evidence from cross-sectional,7–9 longitudinal,10–12 and experimental studies13–17 suggest physical activity and cardiorespiratory fitness (CRF) independently contribute to reductions in the prevalence of MetS. This reduction is consistent with the positive influence of physical activity and CRF on cardiovascular and metabolic risk factors.18–20 Recent research suggests sedentary behavior might have a negative impact on cardiovascular and metabolic factors. This is of concern because adults are likely to spend over half of the waking day in sedentary behavior.21,22 Research examining the relationship between sedentary behavior and metabolic syndrome is limited.23 Based on a recent meta-analysis23 of 10 studies, greater time spent in sedentary behavior increased the odds of developing MetS by 73%; however, because all 10 studies were cross-sectional, no causal inferences can be made. Eight of the 10 studies adjusted for physical activity in their analyses. Sedentary behavior is recognized as a unique risk factor independent of physical activity.24 Several studies have found a relationship between sedentary behavior and MetS as well as between sedentary behavior and individual MetS risk variables25,26 independent of self-reported physical activity9,25,27–32 and accelerometer-tracked physical activity.21 Conversely, Scheers and colleagues found a significant relationship between accelerometer-tracked sitting time and MetS, but this relationship no longer existed when they controlled
for accelerometer-tracked physical-activity behavior. Longitudinal studies examining the relationship between sedentary behavior and MetS are needed23 to elucidate the causal relationship. The current study examined the association between sedentary behavior and incident MetS (ie, the development of MetS) and whether this relationship was independent of CRF and physical activity behavior. This study makes important contributions to the literature because it is the first to examine the relationship between sedentary behavior and MetS while adjusting for CRF. Furthermore, this study addresses a call for longitudinal studies examining the relationship between sedentary behavior and MetS.23
Greer ([email protected]) and Greer are with the Dept of Physical Therapy and Human Movement Science, Sacred Heart University, Bridgeport, CT. Sui and Blair are with the Dept of Exercise Science, University of South Carolina, Columbia, SC. Maslow is with the R. Stuart Dickson Institute for Health Studies, Carolinas HealthCare System, Charlotte, NC.
Data Collection
68
Methods Study Sample Participants (N = 930) were men 23–82 years old who had a preventive medical examination at the Cooper Clinic (Dallas, TX) in 1982, responded to a mail-back survey in 1982, and who were enrolled in the Aerobics Center Longitudinal Study (ACLS).33,34 To be included in the study, participants had to have at least 2 clinic examinations with complete measurements for each MetS component and baseline measurements of CRF, sedentary behavior, and physical activity. Exclusion criteria included prevalent MetS at baseline, an abnormal results on resting or exercise electrocardiogram (ECG), or a history of physician-diagnosed coronary heart disease, stroke, cancer, or diabetes. Participants were mostly non-Hispanic whites (99%) who had graduated from high school (96%). The average time between first and last visits was 9.6 ± 6.9 years (range, 1–24).
All men fasted for 12 hours before a clinic examination as described elsewhere.33,34 Body mass index (BMI; kg/m2) was computed from measured height and weight, and waist girth was measured at the
Downloaded by Western University on 09/22/16, Volume 12, Article Number 1
Sedentary Behavior and Metabolic Syndrome 69
umbilicus. Resting systolic and diastolic blood pressures were recorded according to the first and fifth Korotkoff sounds using standard auscultation methods after a brief period of quiet sitting.35 Triglycerides, high-density lipoprotein cholesterol (HDL), and glucose were measured in antecubital venous blood with automated bioassays according to Centers for Disease Control and Prevention standards.33 Leisure-time physical activity (active, inactive) and family history of CVD were obtained from a standardized medical history questionnaire. CRF was quantified as the duration of a maximal treadmill exercise test using a modified Balke protocol.33 Duration of this treadmill test is highly correlated with measured maximal oxygen uptake in men (r = .92).36 As done previously with ACLS data,37–39 age-specific distributions of treadmill exercise duration were formed within the following age groups: 20 to 39, 40 to 49, 50 to 59, and ≥ 60 years. Each age-specific distribution was divided into tertiles: low CRF (≤ 19 min), middle CRF (> 19 to ≤ 22.5 min), and high CRF (> 22.5 min). Time spent engaged in sedentary behavior, current smoking status, number of alcoholic drinks per week, ethnicity, and education level were determined through mail-back survey. During the 1982 survey, men were asked to report the average time (hours per week) that they spent viewing TV and riding in a motor vehicle. As done previously,40 we computed sedentary behavior in hours per week engaged in these 2 behaviors (TV sedentary hours + car sedentary hours). The sedentary variable was then classified into tertiles: low (≤ 12 h), middle (> 12 to ≤ 19 h) and high (> 19 h). MetS was defined as the existence of 3 or more of the following criteria:41 abdominal obesity (waist girth > 40 in), triglycerides ≥ 150 mg/dL, HDL < 40 mg/dL, blood pressure ≥ 130 mm Hg systolic or ≥ 85 mm Hg diastolic, and glucose ≥ 100 mg/dL. As in other epidemiological studies of MetS incidence,37,42,43 physiciandiagnosed hypertension and diabetes were included in the definition of abnormal blood pressure and glucose, respectively. The Cooper Institute Institutional Review Board approved the study protocol, and all men provided written informed consent.
Data Analysis Follow-up time was computed as the difference between the date of the baseline examination and the date when incident MetS was identified for case subjects. For those without MetS (control subjects), follow-up time was computed as the difference between the date of the baseline and the final clinic examination. Person-years of exposure were computed as the sum of followup time among case subjects and control subjects. Incidence rates (per 1000 person-years) were computed as the number of MetS cases divided by person-years of exposure for the total sample. Descriptive statistics were used to summarize the data. Chisquare tests were used to examine associations between all subjects and current smoking (yes, no), number of baseline metabolic syndrome risk factors (0, 1, or 2), and family history of CVD (yes, no), high school education (versus less than high school education), race (white, nonwhite). Independent t tests were used to examine whether there were mean differences in age, alcoholic consumption (drinks per week), BMI, waist circumference, HDLs, triglycerides, systolic blood pressure, diastolic blood pressure, fasting blood glucose, and treadmill test duration at baseline between MetS case subjects and control subjects. Kaplan Meier curves were plotted to ensure the proportional hazards assumption for Cox regression was met. We used Cox
regression to estimate hazard ratios (HRs) and 95% confidence intervals (CIs; using Breslow method for ties) as an index of the strength of association between the various exposures of interest (sedentary behavior, physical activity status, and CRF) and MetS. Specifically, we evaluated the associations between (1) sedentary behavior and MetS, (2) physical activity status and MetS, (3) CRF and MetS, (4) sedentary behavior and MetS adjusted for physical activity status, (5) sedentary behavior and MetS adjusted for CRF, and finally (6) sedentary behavior and MetS controlled for both physical activity status and CRF. All analyses were adjusted for age, current smoking alcohol consumption, number of baseline MetS risk factors, and family history of CVD. Hereafter, these factors are referred to as covariates. Statistical significance was set at P < .05 for all statistical tests.
Results A total of 124 men developed MetS during 8974 person-years of exposure. The crude incidence rate of MetS was 3.8 cases per 1000 person-years. As shown in Table 1, MetS case subjects had higher baseline values for mean BMI, waist circumference, and triglycerides, and lower baseline values for HDL and treadmill test duration. A greater proportion of MetS case subjects also had at least one MetS risk factor and low or middle CRF compared with control subjects. Hazard ratios of MetS according to sedentary behavior groups are shown in Table 2. After adjusting for covariates, men with middle and high sedentary behavior had 65% and 76% higher risks of MetS, respectively, than those with low sedentary behavior (linear trend P = .011). Inactive men had double the risk of MetS of active men after adjusting for covariates. As shown in Table 2, CRF was inversely associated with MetS (linear trend P < .0001). As shown in Table 3, the positive association between sedentary behavior and MetS remained significant after additional adjustment for physical activity status (linear trend P = .023). The positive association between sedentary behavior and MetS also remained significant after adjustment for CRF (linear trend P =.025). Finally, the association between sedentary behavior and MetS remained significant after adjusting for both physical activity status and CRF (see Table 3); however, the P value for the linear trend (.074) was no longer significant. The high group, which spent the most time in sedentary behavior, had a significantly increased risk of MetS compared with the low group, which spent the least time in sedentary behavior, but the middle-sedentary-behavior group did not have a significantly higher risk of MetS than the low-sedentarybehavior group.
Discussion Efforts to prevent MetS are needed because approximately one third of adults experience this condition,1 which is associated with increased risk of morbidity2–4 and mortality.4–6 This longitudinal study makes an important contribution to the literature because it examined whether sedentary behavior is a risk factor for MetS among men after adjusting for both physical activity status and CRF. Findings from the current study suggest that sedentary behavior is a risk factor for MetS independent of physical activity status; this finding is similar to those from cross-sectional studies.9,21,25,27–32 However, the longitudinal nature of this study provides evidence of temporal precedence,44 which had not previously been established.23
70 Greer et al
Table 1 Participant Demographic and Clinical Characteristics at Baseline in the Total Sample and by Subjects With and Without the Metabolic Syndrome at Follow-Up, N = 930
Downloaded by Western University on 09/22/16, Volume 12, Article Number 1
Characteristics Current smoker, no White, yes High school education, yes CVD family history, no Number of MetS risk factors 0 1 2 Physically active, yes Cardiorespiratory fitness Low Middle High Sedentary time Low Middle High Age, y Alcoholic drinks/wk Waist circumference, in Lipids, mg/dL High-density lipoproteins Triglycerides Blood pressure, mm Hg Systolic Diastolic Fasting blood glucose, mg/dL Treadmill test duration, min
Total (N = 930)
MetS (N = 124)
No MetS (N = 806)
n (%)
n (%)
n (%)
c2
df
P
887 (95.38) 926 (99.57) 898 (96.56) 591 (63.55)
118 (95.16) 124 (100.00) 119 (95.97) 75 (60.48)
769 (95.41) 802 (99.50) 779 (96.65) 516 (64.02)
0.015 0.618 0.151 0.580 21.068
1 1 1 1 3
.903 .564 .698 .446 .001
280 (30.11) 373 (40.11) 277 (29.79) 852 (91.61)
20 (16.13) 48 (38.71) 56 (45.16) 110 (88.71)
260 (32.26) 325 (40.32) 221 (27.42) 742 (92.06)
1.570 26.062
1 2
.210
Official Journal of ISPAH www.JPAH-Journal.com ORIGINAL RESEARCH
The Effects of Sedentary Behavior on Metabolic Syndrome Independent of Physical Activity and Cardiorespiratory Fitness Anna E. Greer, Xuemei Sui, Andréa L. Maslow, Beau Kjerulf Greer, and Steven N. Blair Background: To date, no longitudinal studies have examined the influence of sedentary behavior on metabolic syndrome development while accounting for cardiorespiratory fitness. Purpose and Methods: This prospective study examined the relationship between sedentary behavior and incident metabolic syndrome while considering the effects of physical activity and cardiorespiratory fitness on the association among 930 men enrolled in the Aerobics Center Longitudinal Study. Results: A total of 124 men developed metabolic syndrome during 8974 person-years of exposure. After adjusting for covariates, men with middle and high sedentary behavior had 65% and 76% higher risks of developing metabolic syndrome, respectively, than men with low sedentary behavior (linear trend P = .011). This association remained significant after additional adjustment for activity status and cardiorespiratory fitness. Cardiorespiratory fitness and physical activity were also inversely associated with metabolic syndrome, even after adjustment for sedentary behavior. Conclusions: The findings highlight the importance of reducing sedentary behavior, increasing physical activity, and improving cardiorespiratory fitness for preventing metabolic syndrome. Keywords: exercise, longitudinal study, risk factors Approximately 34% of adults in the US have metabolic syndrome (MetS),1 a collection of conditions that increase a person’s risk of developing cardiovascular disease (CVD)2,3 and diabetes mellitus4 and risk of dying from CVD5 and all other causes.6 Evidence from cross-sectional,7–9 longitudinal,10–12 and experimental studies13–17 suggest physical activity and cardiorespiratory fitness (CRF) independently contribute to reductions in the prevalence of MetS. This reduction is consistent with the positive influence of physical activity and CRF on cardiovascular and metabolic risk factors.18–20 Recent research suggests sedentary behavior might have a negative impact on cardiovascular and metabolic factors. This is of concern because adults are likely to spend over half of the waking day in sedentary behavior.21,22 Research examining the relationship between sedentary behavior and metabolic syndrome is limited.23 Based on a recent meta-analysis23 of 10 studies, greater time spent in sedentary behavior increased the odds of developing MetS by 73%; however, because all 10 studies were cross-sectional, no causal inferences can be made. Eight of the 10 studies adjusted for physical activity in their analyses. Sedentary behavior is recognized as a unique risk factor independent of physical activity.24 Several studies have found a relationship between sedentary behavior and MetS as well as between sedentary behavior and individual MetS risk variables25,26 independent of self-reported physical activity9,25,27–32 and accelerometer-tracked physical activity.21 Conversely, Scheers and colleagues found a significant relationship between accelerometer-tracked sitting time and MetS, but this relationship no longer existed when they controlled
for accelerometer-tracked physical-activity behavior. Longitudinal studies examining the relationship between sedentary behavior and MetS are needed23 to elucidate the causal relationship. The current study examined the association between sedentary behavior and incident MetS (ie, the development of MetS) and whether this relationship was independent of CRF and physical activity behavior. This study makes important contributions to the literature because it is the first to examine the relationship between sedentary behavior and MetS while adjusting for CRF. Furthermore, this study addresses a call for longitudinal studies examining the relationship between sedentary behavior and MetS.23
Greer ([email protected]) and Greer are with the Dept of Physical Therapy and Human Movement Science, Sacred Heart University, Bridgeport, CT. Sui and Blair are with the Dept of Exercise Science, University of South Carolina, Columbia, SC. Maslow is with the R. Stuart Dickson Institute for Health Studies, Carolinas HealthCare System, Charlotte, NC.
Data Collection
68
Methods Study Sample Participants (N = 930) were men 23–82 years old who had a preventive medical examination at the Cooper Clinic (Dallas, TX) in 1982, responded to a mail-back survey in 1982, and who were enrolled in the Aerobics Center Longitudinal Study (ACLS).33,34 To be included in the study, participants had to have at least 2 clinic examinations with complete measurements for each MetS component and baseline measurements of CRF, sedentary behavior, and physical activity. Exclusion criteria included prevalent MetS at baseline, an abnormal results on resting or exercise electrocardiogram (ECG), or a history of physician-diagnosed coronary heart disease, stroke, cancer, or diabetes. Participants were mostly non-Hispanic whites (99%) who had graduated from high school (96%). The average time between first and last visits was 9.6 ± 6.9 years (range, 1–24).
All men fasted for 12 hours before a clinic examination as described elsewhere.33,34 Body mass index (BMI; kg/m2) was computed from measured height and weight, and waist girth was measured at the
Downloaded by Western University on 09/22/16, Volume 12, Article Number 1
Sedentary Behavior and Metabolic Syndrome 69
umbilicus. Resting systolic and diastolic blood pressures were recorded according to the first and fifth Korotkoff sounds using standard auscultation methods after a brief period of quiet sitting.35 Triglycerides, high-density lipoprotein cholesterol (HDL), and glucose were measured in antecubital venous blood with automated bioassays according to Centers for Disease Control and Prevention standards.33 Leisure-time physical activity (active, inactive) and family history of CVD were obtained from a standardized medical history questionnaire. CRF was quantified as the duration of a maximal treadmill exercise test using a modified Balke protocol.33 Duration of this treadmill test is highly correlated with measured maximal oxygen uptake in men (r = .92).36 As done previously with ACLS data,37–39 age-specific distributions of treadmill exercise duration were formed within the following age groups: 20 to 39, 40 to 49, 50 to 59, and ≥ 60 years. Each age-specific distribution was divided into tertiles: low CRF (≤ 19 min), middle CRF (> 19 to ≤ 22.5 min), and high CRF (> 22.5 min). Time spent engaged in sedentary behavior, current smoking status, number of alcoholic drinks per week, ethnicity, and education level were determined through mail-back survey. During the 1982 survey, men were asked to report the average time (hours per week) that they spent viewing TV and riding in a motor vehicle. As done previously,40 we computed sedentary behavior in hours per week engaged in these 2 behaviors (TV sedentary hours + car sedentary hours). The sedentary variable was then classified into tertiles: low (≤ 12 h), middle (> 12 to ≤ 19 h) and high (> 19 h). MetS was defined as the existence of 3 or more of the following criteria:41 abdominal obesity (waist girth > 40 in), triglycerides ≥ 150 mg/dL, HDL < 40 mg/dL, blood pressure ≥ 130 mm Hg systolic or ≥ 85 mm Hg diastolic, and glucose ≥ 100 mg/dL. As in other epidemiological studies of MetS incidence,37,42,43 physiciandiagnosed hypertension and diabetes were included in the definition of abnormal blood pressure and glucose, respectively. The Cooper Institute Institutional Review Board approved the study protocol, and all men provided written informed consent.
Data Analysis Follow-up time was computed as the difference between the date of the baseline examination and the date when incident MetS was identified for case subjects. For those without MetS (control subjects), follow-up time was computed as the difference between the date of the baseline and the final clinic examination. Person-years of exposure were computed as the sum of followup time among case subjects and control subjects. Incidence rates (per 1000 person-years) were computed as the number of MetS cases divided by person-years of exposure for the total sample. Descriptive statistics were used to summarize the data. Chisquare tests were used to examine associations between all subjects and current smoking (yes, no), number of baseline metabolic syndrome risk factors (0, 1, or 2), and family history of CVD (yes, no), high school education (versus less than high school education), race (white, nonwhite). Independent t tests were used to examine whether there were mean differences in age, alcoholic consumption (drinks per week), BMI, waist circumference, HDLs, triglycerides, systolic blood pressure, diastolic blood pressure, fasting blood glucose, and treadmill test duration at baseline between MetS case subjects and control subjects. Kaplan Meier curves were plotted to ensure the proportional hazards assumption for Cox regression was met. We used Cox
regression to estimate hazard ratios (HRs) and 95% confidence intervals (CIs; using Breslow method for ties) as an index of the strength of association between the various exposures of interest (sedentary behavior, physical activity status, and CRF) and MetS. Specifically, we evaluated the associations between (1) sedentary behavior and MetS, (2) physical activity status and MetS, (3) CRF and MetS, (4) sedentary behavior and MetS adjusted for physical activity status, (5) sedentary behavior and MetS adjusted for CRF, and finally (6) sedentary behavior and MetS controlled for both physical activity status and CRF. All analyses were adjusted for age, current smoking alcohol consumption, number of baseline MetS risk factors, and family history of CVD. Hereafter, these factors are referred to as covariates. Statistical significance was set at P < .05 for all statistical tests.
Results A total of 124 men developed MetS during 8974 person-years of exposure. The crude incidence rate of MetS was 3.8 cases per 1000 person-years. As shown in Table 1, MetS case subjects had higher baseline values for mean BMI, waist circumference, and triglycerides, and lower baseline values for HDL and treadmill test duration. A greater proportion of MetS case subjects also had at least one MetS risk factor and low or middle CRF compared with control subjects. Hazard ratios of MetS according to sedentary behavior groups are shown in Table 2. After adjusting for covariates, men with middle and high sedentary behavior had 65% and 76% higher risks of MetS, respectively, than those with low sedentary behavior (linear trend P = .011). Inactive men had double the risk of MetS of active men after adjusting for covariates. As shown in Table 2, CRF was inversely associated with MetS (linear trend P < .0001). As shown in Table 3, the positive association between sedentary behavior and MetS remained significant after additional adjustment for physical activity status (linear trend P = .023). The positive association between sedentary behavior and MetS also remained significant after adjustment for CRF (linear trend P =.025). Finally, the association between sedentary behavior and MetS remained significant after adjusting for both physical activity status and CRF (see Table 3); however, the P value for the linear trend (.074) was no longer significant. The high group, which spent the most time in sedentary behavior, had a significantly increased risk of MetS compared with the low group, which spent the least time in sedentary behavior, but the middle-sedentary-behavior group did not have a significantly higher risk of MetS than the low-sedentarybehavior group.
Discussion Efforts to prevent MetS are needed because approximately one third of adults experience this condition,1 which is associated with increased risk of morbidity2–4 and mortality.4–6 This longitudinal study makes an important contribution to the literature because it examined whether sedentary behavior is a risk factor for MetS among men after adjusting for both physical activity status and CRF. Findings from the current study suggest that sedentary behavior is a risk factor for MetS independent of physical activity status; this finding is similar to those from cross-sectional studies.9,21,25,27–32 However, the longitudinal nature of this study provides evidence of temporal precedence,44 which had not previously been established.23
70 Greer et al
Table 1 Participant Demographic and Clinical Characteristics at Baseline in the Total Sample and by Subjects With and Without the Metabolic Syndrome at Follow-Up, N = 930
Downloaded by Western University on 09/22/16, Volume 12, Article Number 1
Characteristics Current smoker, no White, yes High school education, yes CVD family history, no Number of MetS risk factors 0 1 2 Physically active, yes Cardiorespiratory fitness Low Middle High Sedentary time Low Middle High Age, y Alcoholic drinks/wk Waist circumference, in Lipids, mg/dL High-density lipoproteins Triglycerides Blood pressure, mm Hg Systolic Diastolic Fasting blood glucose, mg/dL Treadmill test duration, min
Total (N = 930)
MetS (N = 124)
No MetS (N = 806)
n (%)
n (%)
n (%)
c2
df
P
887 (95.38) 926 (99.57) 898 (96.56) 591 (63.55)
118 (95.16) 124 (100.00) 119 (95.97) 75 (60.48)
769 (95.41) 802 (99.50) 779 (96.65) 516 (64.02)
0.015 0.618 0.151 0.580 21.068
1 1 1 1 3
.903 .564 .698 .446 .001
280 (30.11) 373 (40.11) 277 (29.79) 852 (91.61)
20 (16.13) 48 (38.71) 56 (45.16) 110 (88.71)
260 (32.26) 325 (40.32) 221 (27.42) 742 (92.06)
1.570 26.062
1 2
.210
