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Clinical Sciences: Clinically Relevant

Association of Muscular Strength with Incidence of Metabolic Syndrome in Men

JURCA, RADIM; LAMONTE, MICHAEL J.; BARLOW, CAROLYN E.; KAMPERT, JAMES B.; CHURCH, TIMOTHY S.; BLAIR, STEVEN N.

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Medicine & Science in Sports & Exercise: November 2005 - Volume 37 - Issue 11 - p 1849-1855
doi: 10.1249/01.mss.0000175865.17614.74
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Abstract

The importance of resistance exercise in promoting health and preventing disease has become increasingly recognized (8,26). In addition to improvements in skeletal muscle strength, endurance, power, and neuromuscular function (1), resistance exercise contributes to the prevention and management of atherosclerotic coronary heart disease (19), hypertension (25), diabetes (2), and overweight and mild obesity (1). Little is known, however, whether the health benefits of resistance exercise are independent of, or additive to, those already established for large muscle dynamic aerobic activity.

The mechanism through which resistance exercise modifies chronic disease risk may be mediated by improvements in abdominal body fat (29), plasma concentrations of triglyceride (10) and high-density lipoprotein cholesterol (11), blood pressure (18), and glycemic control (20). Aerobic exercise and cardiorespiratory fitness also are strongly associated with these risk factors (16) and with chronic disease outcomes (4). Associations between muscular strength, a measure of the effects of resistance exercise, and disease risk, therefore, may be detecting the benefits of an active and fit way of living rather than an independent benefit of resistance exercise. We have shown, however, that muscular strength is inversely associated with all-cause mortality in men and women, independent of cardiorespiratory fitness levels (6). We also recently reported an inverse association between muscular strength and the prevalence of metabolic syndrome in men, independent of cardiorespiratory fitness (12).

Metabolic syndrome is a condition of coexisting risk factors that places individuals at high risk for all-cause and cardiovascular mortality (15) and for the development of diabetes (17). Evidence from prospective epidemiologic studies (5,14), including preliminary analyses in our cohort, suggests that higher levels of activity and fitness protect against developing metabolic syndrome. Based on our cross-sectional observation that the inverse association between muscular strength and metabolic syndrome prevalence is independent of cardiorespiratory fitness (12), it is possible that resistance exercise may provide protection against developing metabolic syndrome beyond what is seen for physical activity and cardiorespiratory fitness. Data testing this hypothesis are currently unavailable; therefore, we examined the prospective association between muscular strength and metabolic syndrome incidence in a cohort of men for whom measurements of cardiorespiratory fitness also were available.

METHODS

Participants.

Participants were asymptomatic men aged 20–80 yr who had a baseline preventive medical examination at the Cooper Clinic in Dallas, Texas between 1980 and 1989, and who are enrolled in the Aerobics Center Longitudinal Study (ACLS). Strength testing was voluntary and an adjunct to the standard examination protocol. Inclusion criteria for the current analysis required participants to have baseline measures of muscular strength, cardiorespiratory fitness, and a comprehensive clinical examination, and have at least one follow-up clinical examination with complete measurements for each metabolic syndrome variable (N = 3922). After excluding participants with metabolic syndrome at baseline (N = 501), those with a history or evidence of cancer (N = 14), stroke (N = 1), or coronary heart disease (N = 16), those who did not achieve at least 85% of their age-predicted maximal heart rate (N = 19) during a maximal treadmill test, and those with an abnormal exercise electrocardiography (N = 138), 3233 men remained for analysis. The participants were predominantly non-Hispanic whites (>95%), well educated, and employed in, or retired from, 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.

Outcome measures and clinical examination.

The primary study outcome was the development of metabolic syndrome, defined as meeting three or more of the following criteria (21): abdominal obesity (waist girth >102 cm [40 inches]), high triglycerides (TG) (≥1.69 mmol·L−1 [150 mg·dL−1]), low high-density lipoprotein (HDL)-C (<1.04 mmol·L−1 [40 mg·dL−1]), high blood pressure (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). All participants completed a medical history questionnaire, which included personal and family health history, smoking habit, and alcohol intake.

Details of the clinical examination and measures of muscular strength and cardiorespiratory fitness have been described elsewhere (4,12). Briefly, body mass index (BMI) was computed from measured height and weight, and waist girth was measured at the umbilicus with a plastic anthropometric tape. We measured resting BP by auscultation with a mercury sphygmomanometer following the American Heart Association protocol. Following a 12-h fast, serum TG, HDL-C, and fasting plasma glucose were assayed with automated techniques. The laboratory participates in, and meets, the quality control standards of the U.S. Centers for Disease Control and Prevention Lipid Standardization Program.

We quantified muscular strength from the results of a standardized strength assessment protocol using variable-resistance Universal weight machines (Universal Equipment, Cedar Rapids, IA). Upper body strength was assessed with a one-repetition maximum (1-RM) supine bench press, and lower body strength was assessed with a 1-RM seated leg press. Participants were instructed on proper breathing and lifting form for each movement. Initial loads were 70 and 100% of body weight for the bench and leg press, respectively. Following a brief rest period, we added increments of 2.27–4.54 kg (5–10 lbs) until maximal effort was achieved for each lift. We calculated a muscular strength score by combining the 1-RM score for the bench and leg press expressed as kilograms of weight lifted per kilogram of body weight. Distributions of the composite strength score were formed for the following age groups: 20–29, 30–39, 40–49, 50–59, and 60+ yr. We used quartiles of the age-specific composite strength score for analysis. In an earlier report, we presented a strong and direct gradient for self-reported participation in resistance exercises across quartiles of muscular strength, which suggests that our measurement of muscular strength is an adequate reflection of the resistance exercise habits among men in the ACLS (12). In a subgroup of 246 men in the ACLS who underwent two muscular strength assessments within a 1-yr period, the intraclass correlation for 1-RM bench press and leg press was R = 0.90 and R = 0.83, respectively. We believe, therefore, 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, which has been described elsewhere (4,12). Participants were given verbal encouragement to reach a maximal level of exertion, and the test was terminated when the participant was exhausted or if the physician stopped the test for medical reasons. In the current analysis, cardiorespiratory fitness was quantified as maximal exercise duration (min), which is highly correlated (r = 0.92) with measured maximal oxygen uptake (24).

Statistical analyses.

Descriptive statistics were computed for each variable. Participants were defined as a case if they met the metabolic syndrome definition at any clinical examination following baseline. The number of clinic visits among participants ranged from 2 to 27 visits (mean and SD, 4.6 ± 3.5). Among noncases, follow-up time was calculated as the time from the baseline to the last visit. Because the exact date of metabolic syndrome development is unknown, we used the midpoint between the date of the case-finding clinic examination and the date of the previous examination where participants were known to be free of metabolic syndrome. Follow-up time among cases was then calculated as the time from the baseline visit to the midpoint between the first “incident” visit and the previous visit. Man-years of exposure were computed as the sum of follow-up time among cases and noncases.

Incident rates were computed as the number of metabolic syndrome cases divided by man-years of exposure for the total population sample and within categories of muscular strength. We used Cox regression to compute hazard ratios (HR) and 95% confidence intervals (CI) for incident metabolic syndrome according to categories of the muscular strength score. Multivariable analyses were adjusted for age, baseline examination date, smoking, alcohol intake, cardiorespiratory fitness, number of baseline metabolic syndrome risk factors, and family history of diabetes, hypertension, and premature coronary disease. To determine whether the pattern of association between muscular strength and incident metabolic syndrome varied by weight status and age, we examined the association within BMI-defined categories of normal weight (BMI < 25 kg·m−2) and overweight or obese (BMI ≥ 25 kg·m−2), and within age groups of 20–39, 40–49, and 50+ yr. P values are two-sided, with P ≤ 0.05 regarded as statistically significant.

RESULTS

The mean follow-up was 6.7 ± 5.2 yr (range 0.1–22.0 yr). A total of 480 incident cases of metabolic syndrome occurred during 21,706 man-years of follow-up. Men who developed metabolic syndrome were similar in age and had comparable levels of risk factors and cardiorespiratory fitness when compared with men who remained free of metabolic syndrome during follow-up (Table 1). With the exception of elevated glucose, the baseline prevalence of each metabolic syndrome risk threshold was significantly higher (P < 0.001) in cases than in noncases. The prevalence of having two metabolic syndrome risk factors at baseline was also higher in cases than in noncases (50 vs 17%). The range of scores for the composite strength variable, treadmill time, and maximal METs were 1.0–4.9 kg lifted per kilogram of body weight, 8.2–38.2 min, and 7.1–20.2 METs, respectively.

T1-4
TABLE 1:
Baseline characteristics by metabolic syndrome status during follow-up.

A strong inverse gradient (P < 0.0001) of metabolic syndrome incidence rates was observed across categories of muscular strength (Table 2). Age-adjusted incident rates per 1000 man-years among men in the highest strength category were 46% lower than in men with low muscular strength. Hazard ratios and 95% CI were computed to quantify the strength of association between muscular strength and incident metabolic syndrome with men in the lowest strength category as the referent group (Table 2). After adjusting for age and examination date, we observed a strong inverse association (P < 0.0001) between muscular strength and the risk of incident metabolic syndrome. The association persisted (P = 0.004) after additional adjustment for smoking, alcohol intake, number of metabolic syndrome risk factors at baseline, and family history of diabetes, hypertension, and premature coronary disease. Men in the highest strength category had a 34% (95% CI, 14–50%, P = 0.002) lower risk of developing metabolic syndrome than men in the lowest strength category. Further adjustment for cardiorespiratory fitness attenuated the association between muscular strength and incident metabolic syndrome to being marginally not significant (P = 0.06). In the latter model, metabolic syndrome risk was 24% (95% CI, 1–43%, P < 0.05) lower among men with high versus low strength.

T2-4
TABLE 2:
Metabolic syndrome incident rates and hazard ratios by muscular strength categories in 3233 men in the Aerobics Center Longitudinal Study (1980-2003).

We next examined the pattern of association between muscular strength and metabolic syndrome within BMI-defined categories of normal weight (N = 1751) (BMI < 25 kg·m−2) and combined overweight (N = 1348) and obese (N = 134) (BMI ≥ 25 kg·m−2) (Fig. 1). Age-adjusted incident rates of metabolic syndrome per 1000 man-years among normal weight and overweight men were 11.5 and 37.7% (P < 0.0001), respectively. Muscular strength was inversely associated (P < 0.05) with metabolic syndrome incidence in both normal and overweight men. Age-adjusted rates of metabolic syndrome were 44 and 39% lower in men with high versus low muscular strength within the normal and overweight categories (P < 0.05), respectively.

F1-4
FIGURE 1—Age-adjusted metabolic syndrome incidence rates across muscular strength categories by BMI. Incidence rates per 1000 man-years are shown atop the bars and the number of cases within the bars. Q1 represents the lowest and Q4 the highest muscular strength category.

Figure 2 shows metabolic syndrome incident rates according to categories of muscular strength stratified by age. In all age groups, the general pattern of association was for incrementally lower rates of metabolic syndrome incidence across categories of strength. We observed significant linear trends for ages 20–39 yr (P < 0.001), 40–49 yr (P < 0.01), and 50+ yr (P < 0.05).

F2-4
FIGURE 2—Metabolic syndrome incidence rates across muscular strength categories by age groups. Incidence rates per 1000 man-years are shown atop the bars and the number of cases within the bars. Q1 represents the lowest and Q4 the highest muscular strength category.

DISCUSSION

The primary findings of this investigation were 1) muscular strength was inversely associated with incident metabolic syndrome, 2) the association between muscular strength and metabolic syndrome was significant after extensive control for potential confounders and was only marginally not significant with additional adjustment for cardiorespiratory fitness, and 3) muscular strength was protective against developing metabolic syndrome in normal and overweight men and across a broad range of ages. Although recent studies have reported protective associations between cardiorespiratory fitness exposures and incident metabolic syndrome (5,14), we believe the data reported herein are the first to demonstrate that maximal muscular strength is inversely associated with the development of metabolic syndrome.

We recently reported an inverse association between muscular strength and the prevalence of metabolic syndrome in ACLS men (12). The association between muscular strength and prevalent metabolic syndrome was independent of cardiorespiratory fitness and other confounders. Our current analysis shows that muscular strength is independently associated with lower incidence of metabolic syndrome and marginally independent of maximal cardiorespiratory fitness. In our participants, muscular strength and cardiorespiratory fitness measures were modestly correlated (age-adjusted Pearson r = 0.29). This increases the plausibility that protection against developing metabolic syndrome may be conferred by higher levels of skeletal muscle function through biological pathways that are independent of cardiorespiratory fitness. To the extent that resistance exercise determines cardiorespiratory fitness, however, their joint effects cannot be completely disentangled statistically. The specific mechanisms through which resistance exercise and muscular strength mediate the clustering of metabolic risk factors have yet to be fully elucidated.

The apparent protective effect of muscular strength against clustering high-risk metabolic phenotypes may not be a function of maximal muscular strength per se, but may reflect better metabolic homeostasis resulting from regular participation in resistance types of physical activities. We also recognize that genetic transmission contributes to the expression of muscular strength (27). However, we previously reported, a strong direct association (P < 0.001) between the frequency of self-reported resistance exercise and maximal muscular strength among men in the ACLS (12). Regular participation in resistance exercise was reported by 65% of men in the highest strength category, but by only 25% of men in the lowest strength category. This observation suggests that our measurements of muscular strength are a reflection of the resistance exercise training habits in our cohort. Other investigators have shown that resistance training increases muscle quantity and insulin action (3,9) and reduces visceral adipose tissue (22). It has been recently suggested that the improved insulin sensitivity after resistance training may occur by an attenuation of insulin-stimulated glucose uptake per unit of skeletal muscle, which supports the conclusion that the effect of resistance training cannot be ascribed solely to a mere increase in fat-free mass (3). Together, existing data on the health benefits of resistance exercise training and the prospective data reported here suggest that resistance exercise may be important to include in physical activity recommendations to prevent risk factor clustering such as seen with the metabolic syndrome (21).

In our analysis, 50% of men who developed the metabolic syndrome had two metabolic syndrome risk factors at baseline compared with only 17% of men who did not become a case. A ninefold (95% CI, 7.3–12.3, P < 0.0001) increase in the age-adjusted risk of metabolic syndrome was observed in men with two metabolic syndrome risk factors at baseline compared with men who had none (data not shown). Clearly, individuals with two of three metabolic syndrome risk factors have underlying homeostatic metabolic dysregulation and are more susceptible for case development during follow-up, analogous to the increased risk for diabetes and hypertension that is seen in individuals who are prediabetic and prehypertensive, respectively. Even after controlling for the number of baseline metabolic syndrome factors, men with high strength had 34% lower risk (95% CI, 14–50%, P < 0.01) of developing metabolic syndrome as compared with men with low strength. It appears that higher levels of muscular strength may provide protection against metabolic syndrome development even in men at high-risk susceptibility for this condition.

The risk of developing abnormal glucose metabolism, dyslipidemia, and hypertension is higher among obese versus normal weight individuals (23). We observed that men with high compared with low muscular strength had significantly lower metabolic syndrome incidence rates even when grouped into BMI categories of normal weight (8.7 vs 15.7, P < 0.05) and overweight (25.9 vs 42.7, P < 0.01). These results are consistent with our cross-sectional study showing an inverse association between muscular strength and metabolic syndrome prevalence in normal weight, overweight, and obese men (12). Obesity is a heterogeneous disorder for which both healthy and adverse metabolic phenotypes have been described (13). It is possible that measures of maximal muscular strength are sensitive enough to discriminate individuals for whom skeletal muscle metabolism is efficient and favors maintaining healthy metabolic risk profiles through mechanisms mediated by activity-related energy expenditure that are independent of cardiorespiratory fitness and body composition (28).

National data indicate the prevalence of metabolic syndrome increases across decades of age (7). Cross-sectional data from our cohort of men showed lower prevalence of metabolic syndrome with higher levels of muscular strength (12), independent of age. Our current prospective analysis shows that risk of metabolic syndrome was lower in those with high muscular strength across the age groups. Our findings support extant data on the importance of physical activity, including resistance exercise, in promoting health and reducing disease risk among younger and older individuals (8).

Limitations exist to the findings of our study that should be considered when interpreting and generalizing the data reported herein. All of the participants underwent a comprehensive medical examination, which was used to limit the muscular strength assessment to individuals without cardiovascular disease and severe obesity. Generalization of our data applies only to apparently healthy white men with higher socioeconomic affluence. We do not have detailed information on resistance exercise habits and medication usage in this group of ACLS men. It is possible that some men were prescribed medication and, indeed, adhered sufficiently enough to the medication regimen during the follow-up period such to bias the association between strength and incident metabolic syndrome away from unity. Because the baseline strength exposure was obtained during the 1980s, which is before the widespread clinical use of medications that have recently been shown to affect the complex phenotype of metabolic syndrome (e.g., statins, ace-inhibitors, PPAR-gamma inhibitors), we believe the potential influence of medications on the associations reported here would be only marginal. Finally, it is important to recognize that metabolic syndrome defined by different criteria might result in diverse findings. Strengths of our findings include objective and standardized measures of muscular strength in a large cohort of men with extensive follow-up for incident metabolic syndrome cases. To our knowledge, this is the first prospective epidemiologic study to examine the association between muscular strength and metabolic syndrome incidence.

In summary, the present study showed that muscular strength was independently associated with metabolic syndrome incidence in healthy men. Muscular strength may protect against developing the metabolic syndrome among men who are normal weight or overweight, younger or older, and after adjustment for a number of baseline metabolic syndrome variables and maximal cardiorespiratory fitness. Randomized controlled trials among diverse populations are needed to examine the possible role of resistance exercise training in preventing the development of metabolic syndrome and related disease outcomes. Until such trials are completed, clinicians may wish to consider counseling their patients on the importance of aerobic physical activity and resistance exercise training for the primary prevention of metabolic disorders.

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Keywords:

RESISTANCE EXERCISE; CARDIORESPIRATORY FITNESS; BODY MASS INDEX; PREVENTION; AGE

©2005The American College of Sports Medicine