Metabolic syndrome is characterized by abdominal obesity and disorders of lipid and carbohydrate metabolism (29). Approximately 23.7% of U.S. adults meet the criteria for metabolic syndrome (9). Individuals with metabolic syndrome are at elevated risk for Type 2 diabetes (24) and cardiovascular disease (21). Metabolic syndrome has been described as insulin resistance syndrome, and it is clear that insulin resistance is a key component of the pathophysiology of metabolic syndrome. Maintaining muscular mass has been found to be protective against the development of insulin resistance and Type 2 diabetes (27,32). Thus, there is a sound physiological mechanism whereby higher levels of muscular strength may be associated with lower prevalence of metabolic syndrome.
Lifestyle modification, including increased physical activity, is the cornerstone of national recommendations for treating metabolic syndrome (29). Several studies have reported lower metabolic syndrome prevalence among individuals with higher levels of aerobic physical activity and cardiorespiratory fitness (6,16,22,37). Preliminary evidence for the efficacy of physical activity as a treatment of metabolic syndrome was recently shown by Katzmarzyk et al. (17), who reported significant reductions in metabolic syndrome prevalence among a relatively small sample of adults following 20 wk of supervised aerobic exercise training. Available data tend to support an inverse association for aerobic activity and cardiorespiratory fitness with metabolic syndrome prevalence; however, little is known about the relationship between skeletal muscle strength and the metabolic syndrome.
Therefore, the purpose of our study was to examine the independent and joint associations of muscular strength and cardio-respiratory fitness to the prevalence of ATP-III defined metabolic syndrome in a large group of healthy middle-aged men.
The current study includes 8570 men aged 20–75 yr who are enrolled in the Aerobics Center Longitudinal Study (ACLS). Participants had a preventive medical examination between 1981 and 1989 at the Cooper Clinic, Dallas, TX, during which they submitted to voluntary strength testing as an adjunct to the regular examination protocol. The men were predominantly non-Hispanic whites (97.5%), well educated, and employed in professional or executive positions. The Cooper Institute institutional review board approved the study protocol annually, and all participants provided written informed consent before data collection.
After an overnight fast of at least 12 h, participants undertook the following examination components: personal and family health histories, anthropometry, blood chemistry analyses, resting blood pressure, resting and exercise electrocardiography, and a maximal treadmill exercise test for the assessment of cardiorespiratory fitness. Waist girth was measured at the level of the umbilicus with a plastic anthropometric tape. Resting blood pressure (BP) was obtained with a mercury sphygmomanometer. Serum triglycerides (TG), high-density lipoprotein cholesterol (HDL-C), and fasting plasma glucose were assayed with automated techniques in accord with quality control standards of the U.S. Centers for Disease Control and Prevention Lipid Standardization Program. All measurement procedures are standardized to a manual of operations and have been previously described in greater detail (6,19).
Muscular strength was quantified from the results of a standardized strength assessment using variable-resistance Universal (Universal Equipment, Cedar Rapids, IA) weight machines (4,8,10,19). Upper-body strength was assessed with a one-repetition maximum (1-RM) supine bench press. Participants were aligned on the machine with the bar at nipple level and their feet flat on the floor. Keeping the back flat on the bench, and following an appropriate breathing pattern, arms were extended upward and slowly returned to the starting position. The initial load was 70% of body weight. After a brief rest period, increments of 2.27–4.54 kg were added until maximal effort was achieved. Lower-body strength was assessed with a 1-RM seated leg press. Participants were aligned with the ball of their foot on the footplate of the machine so that their knee angle approximated 70° of flexion. Keeping their back flat against the chair and with an appropriate breathing pattern, participants extended their legs outward, stopping before full knee extension (approximately 5–10° flexion) and then slowly returned to the starting position. Initial load was set at 100% body weight and increased 2.27–4.54 kg until maximum effort was achieved. A muscular strength index was computed by combining the 1-RM score for the bench press and the leg press expressed as weight lifted per kilogram body weight. We placed the composite strength score into distributions for each of five age groups (20–29, 30–39, 40–49, 50–59, and 60 + yr) and then divided each age group into quartiles based on the combined score.
To determine the degree to which the maximal strength values correlated with the resistance exercise habits of study participants, we examined a subsample of 1071 men who completed detailed records of usual physical activity habits and underwent maximal strength testing. We observed a strong and direct gradient for self-reported participation in resistance exercises across quartiles of muscular strength. The number of men in each strength quartile (Q) and the percentage indicating regular participation in resistance exercise were Q1:N = 70/271 (25%); Q2:N = 88/230 (38%); Q3:N = 91/240 (38%); and Q4:N = 215/330 (65%); (P trend < 0.0001). This observation suggests that our measurements of muscular strength are an adequate reflection of the resistance exercise habits among our cohort.
Because the ACLS is an observational study of individuals undergoing a comprehensive preventive medical exam, from which the current strength data were voluntarily obtained, participants were not asked to complete a second maximal strength test shortly after the first, so test-retest reliability could not be assessed. However, we evaluated the reproducibility 1-RM for upper- and lower-body strength measurements in a subgroup of 246 men who underwent two assessments within a 1-yr period. Intraclass correlations for 1-RM bench press and leg press were 0.90 and 0.83, respectively. Therefore, we think that the muscular strength variable used in the present study has acceptable reliability.
Cardiorespiratory fitness was assessed by a maximal treadmill test using a modified Balke protocol. Patients began walking at 88 m·min−1 (3.3 mph) with no elevation. The incline was increased to 2% after the first minute and was increased 1% each minute thereafter until the 25th minute. For the small amount of participants still able to continue the test beyond 25 min, the elevation was maintained at 25%, and the speed was increased by 5.4 m·min−1 (0.2 mph) each min to the end of the test. The test was terminated when the participants were exhausted or if the physician stopped the test for medical reasons. We assigned men to age-specific fitness categories based on their treadmill exercise time in min and the following age groups: 20–39, 40–49, 50–59, and 60+ yr. We then created three fitness categories based on the age-specific treadmill time distributions as follows: the least fit 20% as low fit, the next 40% of the fitness distribution as moderately fit, and the most fit 40% as high fit. Maximal METs were estimated from age-specific treadmill time using the following formula (31): (1.44 × (time, min) + 14.99)/3.5. Time on the treadmill test with this protocol is highly correlated (r = 0.92) with measured maximal oxygen uptake (31).
The metabolic syndrome was defined as meeting three or more of the following criteria (29): abdominal obesity (waist girth > 102 cm [40 inches]); high TG (≥1.69 mmol·L−1 [150 mg·dL−1]); low HDL-C (<1.04 mmol·L−1 [40 mg·dL−1]); high BP (≥130 mm Hg systolic or ≥85 mm Hg diastolic, or self-reported hypertension); and high fasting glucose (≥6.1 mmol·L−1 [110 mg·dL−1], or self-reported diabetes). In addition, all participants were classified as never, past, or current smokers based on self-report.
Descriptive statistics were computed for each variable. Triglyceride values were skewed, therefore, natural log transformed values are used in analyses and geometric means ± SE are used for reporting. Analysis of variance was used to examine univariate and multivariate associations for muscular strength and cardiorespiratory fitness with each component of the metabolic syndrome as a continuous variable. Multivariate models were adjusted for potential confounding effects of age and smoking. Chi-square analysis was used to examine associations for muscular strength and cardiorespiratory fitness with the prevalence of abnormal values for each metabolic syndrome component. To examine this association adjusted for potential confounding factors, the continuous metabolic syndrome variables were adjusted with linear regression (38) for the effects of age and smoking, and then categorical variables were defined according to ATP-III cutpoints. Logistic regression was used to estimate odds ratios (OR) and 95% confidence intervals (CI) to examine the association for muscular strength and cardiorespiratory fitness with prevalent metabolic syndrome. Two separate models were used to assess strength and fitness exposures. The first model was adjusted for age and smoking, and the second model was further adjusted for the other exposure. We also examined the effects of muscular strength and cardiorespiratory fitness on prevalent metabolic syndrome within BMI-defined categories of normal weight (BMI <25 kg·m−2, N = 3877), overweight (BMI 25–30 kg·m−2, N = 3863), and obese (BMI ≥30 kg·m−2, N = 830) men. For this analysis, dichotomies were created for fitness and strength. Men who were in the lowest fitness category were considered unfit, whereas their moderately and highly fit peers were considered fit. Men in the lowest two strength quartiles were classified as “low strength,” whereas men in strength quartiles three and four were classified as “high strength.” We then compared the effect of each combination of strength and fitness status (low strength-unfit; high strength-unfit; low strength-fit, high strength-fit) with the referent group (low strength and unfit) within each BMI category. All analyses were conducted with SAS version 8.2 (SAS Institute, Cary, NC). P values are two-sided, with P ≤ 0.05 regarded as significant.
On average, study participants were middle-aged with favorable risk factor profiles (Table 1). The range of scores for strength, treadmill time, and maximal METs were 1.1–5.3 kg lifted per kilogram body weight, 3.0–38.3 min, and 5.5–20.1 METs, respectively. The age-adjusted Pearson correlation between maximal treadmill exercise time and the muscular strength score was r = 0.36 (P < 0.0001). Significant inverse associations for muscular strength and cardiorespiratory fitness (P < 0.0001) were observed with each metabolic syndrome component as continuous (Table 2) and categorical (Table 3) variables, except for HDL-C, which was directly associated with both exposures. The prevalence of the metabolic syndrome among all study participants was 15.4% (N = 1322). Table 3 shows a strong inverse gradient for metabolic syndrome prevalence across higher levels of muscular strength (P < 0.0001) and cardiorespiratory fitness (P < 0.0001), which persisted (P < 0.0001 for both exposures) after adjusting for age and smoking habits.
Separate logistic regression models were used to examine the magnitude of association for muscular strength and cardiorespiratory fitness with metabolic syndrome prevalence, initially adjusting for age and smoking, and then adjusting for the other exposure variable (e.g., strength or fitness). We first examined the muscular strength and cardiorespiratory fitness exposures as continuous measures. After adjusting for age and smoking, a strong inverse association was observed between the muscular strength score and metabolic syndrome prevalence (β = −1.3, 95% CI = −1.9 to −0.75, P < 0.0001). Further adjustment for treadmill exercise time attenuated but did not eliminate the association between strength and metabolic syndrome (β = −0.33, 95% CI = −0.92 to −0.25, P = 0.0007). Similarly, after adjustment for age and smoking, an inverse association was seen between cardiorespiratory fitness and metabolic syndrome prevalence (β = −0.24, 95% CI = −0.42 to −0.06, P < 0.0001). Further adjustment for muscular strength did not change this association (β = −0.23, 95% CI = −0.40 to −0.05, P < 0.0001).
Table 4 shows the association for categorical models of muscular strength and cardiorespiratory fitness with metabolic syndrome. After adjustment for age and smoking, a steep graded inverse association (β = −0.37, P < 0.0001) was seen between metabolic syndrome prevalence and level of muscular strength. Further adjustment for maximal treadmill time attenuated but did not eliminate the inverse association (β = −0.08, P < 0.01) between strength and metabolic syndrome prevalence. After adjusting for age and smoking, a sharp and graded inverse association (β = −1.2, P < 0.0001) was observed between categories of cardiorespiratory fitness and metabolic syndrome prevalence, and this association was essentially unchanged (β = −1.2, P < 0.0001) after additional adjustment for muscular strength.
We next examined the combined association of muscular strength and cardiorespiratory fitness on metabolic syndrome prevalence. Figure 1 shows the age and smoking adjusted prevalence of metabolic syndrome across categories of muscular strength and categories of cardiorespiratory fitness. For each category of strength, a significant graded inverse association (P < 0.0001) in metabolic syndrome prevalence was observed with progressively higher levels of cardiorespiratory fitness. Conversely, significant inverse associations between muscular strength and metabolic syndrome were observed only among men in the low (P = 0.0002) and moderate (P < 0.0001) cardiorespiratory fitness categories.
Finally, we examined the combined association of muscular strength and cardiorespiratory fitness to prevalent metabolic syndrome among men within BMI-defined categories of normal weight, overweight, and obese (Table 5). Metabolic syndrome prevalence among normal weight, overweight, and obese men was 4.2%, 17.5%, and 58.2%, respectively (P trend < 0.0001). Among normal weight, overweight, and obese men, respectively, being strong and fit was associated with substantially lower odds (73%, 69%, and 62%, respectively, P < 0.0001) of having prevalent metabolic syndrome for any of the exposure combinations compared with men who were less strong and unfit.
The primary findings of this investigation were: 1) muscular strength and cardiorespiratory fitness are both independently and inversely associated with metabolic syndrome prevalence; 2) muscular strength may exert additive protection against prevalent metabolic syndrome beyond that associated with cardiorespiratory fitness; however, the additive effect may not extend throughout the entire range of cardiorespiratory fitness levels; and 3) the joint, and apparently protective effect, of muscular strength and cardiorespiratory fitness against prevalent metabolic syndrome was observed among overweight and obese men. Strengths of our findings include objective and standardized measures of muscular strength and cardiorespiratory fitness in a large cohort of men. We believe our findings are noteworthy given the overall healthy profile of the study cohort. To our knowledge, this is the first epidemiological study to show an inverse association between muscular strength and metabolic syndrome prevalence and to examine the joint associations of strength and cardiorespiratory fitness related to metabolic syndrome prevalence.
Several investigators have reported lower metabolic syndrome prevalence among individuals with higher levels of self-reported physical activity or measured cardiorespiratory fitness (5,6,22,37). Most of these studies have, however, included relatively small sample sizes, have been inconsistent in defining the metabolic syndrome, and none of these previous investigations have considered the association between muscular strength and metabolic syndrome prevalence. Our analyses showed that muscular strength and cardiorespiratory fitness were both inverse independent correlates of prevalent metabolic syndrome. Men in the highest category of strength had 67% lower odds (OR = 0.33, 95% CI 0.28–0.40) of having the metabolic syndrome compared with men in the lowest strength quartile. Similarly, men with high cardiorespiratory fitness had 92% lower odds (OR = 0.08, 95% CI = 0.06–0.10) of having the metabolic syndrome, when compared with low fit men. The pattern and strength of association between cardiorespiratory fitness and metabolic syndrome observed among ACLS men is comparable to associations reported among other populations of men (22) and women (16).
Because the association with metabolic risk factors is more established for cardiorespiratory fitness (1,3,23) than muscular strength (14), it is reasonable to question whether the association between strength and metabolic syndrome is merely a surrogate index of the protective effect exerted by cardiorespiratory fitness. The two exposures were only modestly associated (r = 0.36) with each other in our sample population. Nonetheless, the association between muscular strength and metabolic syndrome was clearly attenuated when adjusted for fitness, whereas the effect of fitness reminded unchanged after adjusting for strength. The strong influence of cardiorespiratory fitness on the association between muscular strength and metabolic syndrome is not surprising given the strong and established effect fitness has on metabolic risk factors (1,3,6,16,22,23).
However, as shown in Figure 1, muscular strength appears to add to the protective effect of fitness against prevalent metabolic syndrome among low and moderately fit men. The lack of added protection by strength among highly fit men may be partly attributed to the small number of cases (N = 153) or low statistical power among high fit men. Furthermore, the joint protective association of muscular strength and cardiorespiratory fitness against prevalent metabolic syndrome was consistently observed across strata of BMI-defined weight status. The health benefit of cardiorespiratory fitness among overweight and obese individuals is well established (2), and findings of the current investigation suggest that additional benefits may be conferred with the development of muscular strength. Although cross-sectional in nature, our data suggest that the development of muscular strength should be included in physical activity recommendations for the prevention of risk factor clustering such as seen with the metabolic syndrome (29). Prospective studies in diverse populations of men and women are needed to better understand the joint and independent roles that cardiorespiratory fitness and muscular strength have in preventing the development of metabolic syndrome and related outcomes like diabetes and cardiovascular disease.
Mechanisms through which enhanced fitness reduces the likelihood of metabolic syndrome have been described (1,3,6,16,22,23). The mechanisms for muscular strength are similar and include improvements in abdominal body fat (35), plasma concentrations of triglyceride (12) and high-density lipoprotein cholesterol (14), blood pressure (25), and glycemic control (28). Excessive accumulation of intramuscular triglyceride and disruption of the glucose-fatty acid cycle have been identified as possible shared pathways for central obesity and insulin resistance to promote the development of dyslipidemia, hypertension, and Type 2 diabetes (18). Aerobic and resistance exercise improve elements of the glucose-fatty acid cycle (13,33) and may affect muscle triglyceride flux (15,36). Modifications in skeletal muscle fiber composition and increased capillary density may also underlie associations for cardiorespiratory fitness and muscular strength with lower metabolic syndrome prevalence (11,26). Controlled experimental studies are required to elucidate the specific mechanisms through which enhanced cardiorespiratory fitness and muscular strength improve metabolic control and lowers disease risk.
The type and amount of aerobic physical activity recommended for disease prevention (30) is likely a sufficient dose to result in or maintain cardiorespiratory fitness levels comparable to those seen among moderately fit ACLS men (e.g., ∼8–12 maximal METs) (7). Recommendations for health-related levels of muscular strength are currently rudimentary (20,30) and lacking on a disease-specific basis. Because our data are cross-sectional, it is difficult to identify a specific level of muscular strength to recommend for public health. Likewise, it is impossible to discern whether health benefits are derived from maximal muscular strength, per se, or from regular participation in resistance exercises that result in the observed strength phenotype. It may be that a threshold level of muscular strength is required to engage in physical activities that maintain cardiorespiratory fitness and lower disease risk. Previous work among ACLS participants also showed higher muscular strength to be associated with better physical function (4) and lower all-cause mortality (8) independent of cardiorespiratory fitness. Although it appears that enhanced skeletal muscle fitness, as indexed by muscular strength, confers health benefits through mechanisms that are independent of cardiorespiratory fitness, we believe the appropriate public health application of these findings is to promote regular participation in both strength and aerobic activities as a means of lower metabolic risk factors associated with chronic disease.
The current study has limitations that require caution when interpreting and generalizing the findings reported herein. These include the cross-sectional design, predominately white and affluent study population, lack of data in women, and lack of information on nutrient intake and medication usage. We also recognize that genetic transmission contributes to the expression of muscular strength (34). However, we observed a strong and direct gradient for self-report of participation in resistance exercises across levels of muscular strength. This observation increases our confidence that a major contribution to the strength phenotypes observed in the current study is likely due in part to regular participation in resistance exercises.
In summary, the present study showed that cardiorespiratory fitness and muscular strength were independently associated with metabolic syndrome prevalence in healthy middle-aged men. Muscular strength appears to add to the protective effects of cardiorespiratory fitness against prevalent metabolic syndrome even among overweight and obese men. Our findings among a healthy group of men may be even stronger among diseased individuals. Prospective studies among diverse populations are needed to examine the independent and joint effects of cardiorespiratory fitness and muscular strength in preventing the development of metabolic syndrome and related disease outcomes.
We thank Kenneth H. Cooper, M.D., for establishing the Aerobics Center Longitudinal Study; the physicians and technicians of the Cooper Clinic for collecting the baseline data; Margo Simmons and her staff for data entry, and Melba Morrow for editorial assistance.
This research was partially supported by the NIH grant from the National Institute on Aging (AG06945).
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