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ABSTRACT
JURCA, R., M. J. LAMONTE, C. E. BARLOW, J. B. KAMPERT, T. S. CHURCH, and S. N. BLAIR. Association of Muscular
Strength with Incidence of Metabolic Syndrome in Men. Med. Sci. Sports Exerc., Vol. 37, No. 11, pp. 1849 –1855, 2005. Purpose:
To examine the association between muscular strength and incidence of metabolic syndrome. Methods: Participants were 3233 men
(20 – 80 yr) initially free of metabolic syndrome who had two or more clinical examinations between 1980 and 2003, including baseline
muscular strength and cardiorespiratory fitness assessment. Metabolic syndrome was defined according to NCEP-ATP III criteria.
Muscular strength was quantified by combining body weight-adjusted one-repetition maximal measures for leg and bench presses.
Cardiorespiratory fitness was assessed by maximal treadmill test. Results: A total of 480 men developed metabolic syndrome during
a mean follow-up period of 6.7 ⫾ 5.2 yr. In a Cox regression analysis adjusted for age, the hazard ratios (95% confidence intervals)
of metabolic syndrome associated with the incremental categories of muscular strength were 1.00 (referent), 0.88 (0.69 –1.12), 0.77
(0.60 – 0.98), and 0.54 (0.42– 0.71), respectively (linear trend P ⬍ 0.0001). The inverse trend persisted after adjustment for smoking,
alcohol intake, number of baseline metabolic syndrome risk factors, family history of diabetes, hypertension, and premature coronary
disease (P ⫽ 0.004), but was attenuated (P ⫽ 0.06) when further adjusted for cardiorespiratory fitness. Compared with the lowest
strength category, the highest strength category was associated with 44 and 39% lower risk (P ⬍ 0.05 each) of incident metabolic
syndrome among normal weight body mass index (BMI ⬍ 25) and overweight or obese (BMI ⱖ 25) men, respectively. An inverse
association of incident rates was also seen within stratum of age (20 –39 yr, P ⬍ 0.001; 40 – 49 yr, P ⬍ 0.01; and 50⫹ yr, P ⬍ 0.05).
Conclusions: Muscular strength was inversely associated with metabolic syndrome incidence, independent of age and body size.
Potential benefits of greater muscular strength presumably through resistance exercise training should be considered in primary
prevention of metabolic syndrome. Key Words: RESISTANCE EXERCISE, CARDIORESPIRATORY FITNESS, BODY MASS
INDEX, PREVENTION, AGE
T
he importance of resistance exercise in promoting in abdominal body fat (29), plasma concentrations of tri-
health and preventing disease has become increas- glyceride (10) and high-density lipoprotein cholesterol (11),
ingly recognized (8,26). In addition to improvements blood pressure (18), and glycemic control (20). Aerobic
in skeletal muscle strength, endurance, power, and neuro- exercise and cardiorespiratory fitness also are strongly as-
muscular function (1), resistance exercise contributes to the sociated with these risk factors (16) and with chronic disease
prevention and management of atherosclerotic coronary outcomes (4). Associations between muscular strength, a
heart disease (19), hypertension (25), diabetes (2), and over- measure of the effects of resistance exercise, and disease
weight and mild obesity (1). Little is known, however, risk, therefore, may be detecting the benefits of an active
whether the health benefits of resistance exercise are inde- and fit way of living rather than an independent benefit of
pendent of, or additive to, those already established for large resistance exercise. We have shown, however, that muscular
muscle dynamic aerobic activity. strength is inversely associated with all-cause mortality in
The mechanism through which resistance exercise mod- men and women, independent of cardiorespiratory fitness
ifies chronic disease risk may be mediated by improvements levels (6). We also recently reported an inverse association
between muscular strength and the prevalence of metabolic
Address for correspondence: Radim Jurca, Ph.D., The Cooper Institute,
syndrome in men, independent of cardiorespiratory fitness
12330 Preston Road, Dallas, TX 75230; E-mail: djurca@cooperinst.org. (12).
Submitted for publication February 2005. Metabolic syndrome is a condition of coexisting risk factors
Accepted for publication June 2005. that places individuals at high risk for all-cause and cardiovas-
0195-9131/05/3711-1849/0 cular mortality (15) and for the development of diabetes (17).
MEDICINE & SCIENCE IN SPORTS & EXERCISE® Evidence from prospective epidemiologic studies (5,14), in-
Copyright © 2005 by the American College of Sports Medicine cluding preliminary analyses in our cohort, suggests that higher
DOI: 10.1249/01.mss.0000175865.17614.74 levels of activity and fitness protect against developing meta-
1849
bolic syndrome. Based on our cross-sectional observation that anthropometric tape. We measured resting BP by ausculta-
the inverse association between muscular strength and meta- tion with a mercury sphygmomanometer following the
bolic syndrome prevalence is independent of cardiorespiratory American Heart Association protocol. Following a 12-h
fitness (12), it is possible that resistance exercise may provide fast, serum TG, HDL-C, and fasting plasma glucose were
protection against developing metabolic syndrome beyond assayed with automated techniques. The laboratory partici-
what is seen for physical activity and cardiorespiratory fitness. pates in, and meets, the quality control standards of the U.S.
Data testing this hypothesis are currently unavailable; there- Centers for Disease Control and Prevention Lipid Standard-
fore, we examined the prospective association between mus- ization Program.
cular strength and metabolic syndrome incidence in a cohort of We quantified muscular strength from the results of a
men for whom measurements of cardiorespiratory fitness also standardized strength assessment protocol using variable-
were available. resistance Universal weight machines (Universal Equip-
ment, 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
METHODS leg press. Participants were instructed on proper breathing
and lifting form for each movement. Initial loads were 70
Participants. Participants were asymptomatic men
and 100% of body weight for the bench and leg press,
aged 20 – 80 yr who had a baseline preventive medical
respectively. Following a brief rest period, we added incre-
examination at the Cooper Clinic in Dallas, Texas between
ments of 2.27– 4.54 kg (5–10 lbs) until maximal effort was
1980 and 1989, and who are enrolled in the Aerobics Center
achieved for each lift. We calculated a muscular strength
Longitudinal Study (ACLS). Strength testing was voluntary
score by combining the 1-RM score for the bench and leg
and an adjunct to the standard examination protocol. Inclu-
press expressed as kilograms of weight lifted per kilogram
sion criteria for the current analysis required participants to
of body weight. Distributions of the composite strength
have baseline measures of muscular strength, cardiorespi-
score were formed for the following age groups: 20 –29,
ratory fitness, and a comprehensive clinical examination,
30 –39, 40 – 49, 50 –59, and 60⫹ yr. We used quartiles of the
and have at least one follow-up clinical examination with
complete measurements for each metabolic syndrome vari- age-specific composite strength score for analysis. In an
able (N ⫽ 3922). After excluding participants with meta- earlier report, we presented a strong and direct gradient for
bolic syndrome at baseline (N ⫽ 501), those with a history self-reported participation in resistance exercises across
or evidence of cancer (N ⫽ 14), stroke (N ⫽ 1), or coronary quartiles of muscular strength, which suggests that our mea-
heart disease (N ⫽ 16), those who did not achieve at least surement of muscular strength is an adequate reflection of
85% of their age-predicted maximal heart rate (N ⫽ 19) the resistance exercise habits among men in the ACLS (12).
during a maximal treadmill test, and those with an abnormal In a subgroup of 246 men in the ACLS who underwent two
exercise electrocardiography (N ⫽ 138), 3233 men re- muscular strength assessments within a 1-yr period, the
mained for analysis. The participants were predominantly intraclass correlation for 1-RM bench press and leg press
non-Hispanic whites (⬎95%), well educated, and employed was R ⫽ 0.90 and R ⫽ 0.83, respectively. We believe,
in, or retired from, professional or executive positions. The therefore, that the muscular strength variable used in the
Cooper Institute institutional review board approved the present study has acceptable reliability.
study protocol annually, and all participants provided writ- Cardiorespiratory fitness was assessed by a maximal
ten informed consent before data collection. treadmill test using a modified Balke protocol, which has
Outcome measures and clinical examination. been described elsewhere (4,12). Participants were given
The primary study outcome was the development of meta- verbal encouragement to reach a maximal level of exertion,
bolic syndrome, defined as meeting three or more of the and the test was terminated when the participant was ex-
following criteria (21): abdominal obesity (waist girth ⬎102 hausted or if the physician stopped the test for medical
cm [40 inches]), high triglycerides (TG) (ⱖ1.69 mmol·L⫺1 reasons. In the current analysis, cardiorespiratory fitness
[150 mg·dL⫺1]), low high-density lipoprotein (HDL)-C was quantified as maximal exercise duration (min), which is
(⬍1.04 mmol·L⫺1 [40 mg·dL⫺1]), high blood pressure (BP) highly correlated (r ⫽ 0.92) with measured maximal oxygen
(ⱖ130 mm Hg systolic or ⱖ85 mm Hg diastolic or self- uptake (24).
reported hypertension), and high fasting glucose (ⱖ6.1 Statistical analyses. Descriptive statistics were com-
mmol·L⫺1 [110 mg·dL⫺1] or self-reported diabetes). All puted for each variable. Participants were defined as a case
participants completed a medical history questionnaire, if they met the metabolic syndrome definition at any clinical
which included personal and family health history, smoking examination following baseline. The number of clinic visits
habit, and alcohol intake. among participants ranged from 2 to 27 visits (mean and
Details of the clinical examination and measures of mus- SD, 4.6 ⫾ 3.5). Among noncases, follow-up time was cal-
cular strength and cardiorespiratory fitness have been de- culated as the time from the baseline to the last visit.
scribed elsewhere (4,12). Briefly, body mass index (BMI) Because the exact date of metabolic syndrome development
was computed from measured height and weight, and is unknown, we used the midpoint between the date of the
waist girth was measured at the umbilicus with a plastic case-finding clinic examination and the date of the previous
1850 Official Journal of the American College of Sports Medicine http://www.acsm-msse.org
examination where participants were known to be free of TABLE 1. Baseline characteristics by metabolic syndrome status during follow-up.
metabolic syndrome. Follow-up time among cases was then Metabolic Syndrome during Follow-Up
calculated as the time from the baseline visit to the midpoint Present (N ⴝ 480) Absent (N ⴝ 2753)
between the first “incident” visit and the previous visit. Age (yr) 43.7 (8.7) 42.8 (9.3)
Man-years of exposure were computed as the sum of fol- BMI (kg䡠m⫺2) 26.5 (2.9) 24.7 (2.5)
Waist (cm) 95.2 (8.7) 89.8 (7.8)
low-up time among cases and noncases. Systolic blood pressure (mm Hg) 119.7 (11.6) 117.0 (12.2)
Incident rates were computed as the number of metabolic Diastolic blood pressure (mm Hg) 79.8 (8.2) 77.7 (8.4)
Triglyceride (mmol䡠dL⫺1) 1.68 (1.07) 1.13 (0.68)
syndrome cases divided by man-years of exposure for the HDL-cholesterol (mmol䡠dL⫺1) 1.09 (0.26) 1.27 (0.29)
total population sample and within categories of muscular Glucose (mmol䡠dL⫺1) 5.52 (0.50) 5.42 (0.65)
Upper body strength
strength. We used Cox regression to compute hazard ratios Kilograms 70.6 (15.5) 70.8 (17.3)
(HR) and 95% confidence intervals (CI) for incident meta- Kilograms per kilogram of body weight 0.83 (0.17) 0.89 (0.21)
bolic syndrome according to categories of the muscular Lower body strength
Kilograms 140.3 (26.6) 133.0 (24.8)
strength score. Multivariable analyses were adjusted for age, Kilograms per kilogram of body weight 1.64 (0.24) 1.67 (0.27)
baseline examination date, smoking, alcohol intake, cardio- Maximal METs 12.3 (1.8) 12.9 (1.9)
Current smoker (N) (%) 68 (14) 320 (12)
respiratory fitness, number of baseline metabolic syndrome ⱖ5 alcoholic drinks per week (N) (%) 243 (51) 1414 (51)
risk factors, and family history of diabetes, hypertension, Abdominal obesity (N) (%) 85 (18) 135 (5)
High blood pressure (N) (%) 167 (35) 742 (27)
and premature coronary disease. To determine whether the High triglyceride (N) (%) 150 (31) 304 (11)
pattern of association between muscular strength and inci- Low HDL-cholesterol (N) (%) 197 (41) 538 (19)
dent metabolic syndrome varied by weight status and age, High glucose (N) (%) 47 (10) 211 (8)
Number of metabolic syndrome risk factors
we examined the association within BMI-defined categories (N) (%)
of normal weight (BMI ⬍ 25 kg䡠m⫺2) and overweight or 0 75 (16) 1278 (46)
obese (BMI ⱖ 25 kg䡠 m⫺2), and within age groups of 1
2
164 (34)
241 (50)
1020 (37)
455 (17)
20 –39, 40 – 49, and 50⫹ yr. P values are two-sided, with P BMI, body mass index; HDL, high-density lipoprotein; MET, metabolic equivalent
ⱕ 0.05 regarded as statistically significant. estimated from final maximal treadmill speed and grade (3).
Data are mean (SD) unless otherwise indicated.
observation suggests that our measurements of muscular with high compared with low muscular strength had signif-
strength are a reflection of the resistance exercise training icantly lower metabolic syndrome incidence rates even
habits in our cohort. Other investigators have shown that re- when grouped into BMI categories of normal weight (8.7 vs
sistance training increases muscle quantity and insulin action 15.7, P ⬍ 0.05) and overweight (25.9 vs 42.7, P ⬍ 0.01).
(3,9) and reduces visceral adipose tissue (22). It has been These results are consistent with our cross-sectional study
recently suggested that the improved insulin sensitivity after showing an inverse association between muscular strength
resistance training may occur by an attenuation of insulin- and metabolic syndrome prevalence in normal weight, over-
stimulated glucose uptake per unit of skeletal muscle, which weight, and obese men (12). Obesity is a heterogeneous
supports the conclusion that the effect of resistance training disorder for which both healthy and adverse metabolic phe-
cannot be ascribed solely to a mere increase in fat-free mass notypes have been described (13). It is possible that mea-
(3). Together, existing data on the health benefits of resistance sures of maximal muscular strength are sensitive enough to
exercise training and the prospective data reported here suggest discriminate individuals for whom skeletal muscle metabo-
that resistance exercise may be important to include in physical lism is efficient and favors maintaining healthy metabolic
activity recommendations to prevent risk factor clustering such risk profiles through mechanisms mediated by activity-
as seen with the metabolic syndrome (21). related energy expenditure that are independent of cardio-
In our analysis, 50% of men who developed the metabolic respiratory fitness and body composition (28).
syndrome had two metabolic syndrome risk factors at base- National data indicate the prevalence of metabolic syn-
line compared with only 17% of men who did not become drome increases across decades of age (7). Cross-sectional
a case. A ninefold (95% CI, 7.3–12.3, P ⬍ 0.0001) increase data from our cohort of men showed lower prevalence of
in the age-adjusted risk of metabolic syndrome was ob- metabolic syndrome with higher levels of muscular strength
served in men with two metabolic syndrome risk factors at (12), independent of age. Our current prospective analysis
baseline compared with men who had none (data not shows that risk of metabolic syndrome was lower in those
shown). Clearly, individuals with two of three metabolic with high muscular strength across the age groups. Our
syndrome risk factors have underlying homeostatic meta- findings support extant data on the importance of physical
bolic dysregulation and are more susceptible for case de- activity, including resistance exercise, in promoting health
velopment during follow-up, analogous to the increased risk and reducing disease risk among younger and older indi-
for diabetes and hypertension that is seen in individuals who viduals (8).
are prediabetic and prehypertensive, respectively. Even after Limitations exist to the findings of our study that should be
controlling for the number of baseline metabolic syndrome considered when interpreting and generalizing the data re-
factors, men with high strength had 34% lower risk (95% ported herein. All of the participants underwent a comprehen-
CI, 14 –50%, P ⬍ 0.01) of developing metabolic syndrome sive medical examination, which was used to limit the mus-
as compared with men with low strength. It appears that cular strength assessment to individuals without cardiovascular
higher levels of muscular strength may provide protection disease and severe obesity. Generalization of our data applies
against metabolic syndrome development even in men at only to apparently healthy white men with higher socioeco-
high-risk susceptibility for this condition. nomic affluence. We do not have detailed information on
The risk of developing abnormal glucose metabolism, resistance exercise habits and medication usage in this group of
dyslipidemia, and hypertension is higher among obese ver- ACLS men. It is possible that some men were prescribed
sus normal weight individuals (23). We observed that men medication and, indeed, adhered sufficiently enough to the
STRENGTH AND METABOLIC SYNDROME INCIDENCE Medicine & Science in Sports & Exercise姞 1853
medication regimen during the follow-up period such to bias men who are normal weight or overweight, younger or
the association between strength and incident metabolic syn- older, and after adjustment for a number of baseline meta-
drome away from unity. Because the baseline strength expo- bolic syndrome variables and maximal cardiorespiratory
sure was obtained during the 1980s, which is before the wide- fitness. Randomized controlled trials among diverse popu-
spread clinical use of medications that have recently been lations are needed to examine the possible role of resistance
shown to affect the complex phenotype of metabolic syndrome exercise training in preventing the development of meta-
(e.g., statins, ace-inhibitors, PPAR-gamma inhibitors), we be- bolic syndrome and related disease outcomes. Until such
lieve the potential influence of medications on the associations trials are completed, clinicians may wish to consider coun-
reported here would be only marginal. Finally, it is important seling their patients on the importance of aerobic physical
to recognize that metabolic syndrome defined by different activity and resistance exercise training for the primary
criteria might result in diverse findings. Strengths of our find- prevention of metabolic disorders.
ings 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 We thank Kenneth H. Cooper, M.D, for establishing the Aerobics
the first prospective epidemiologic study to examine the asso- Center Longitudinal Study, the physicians and technicians of the
Cooper Clinic for collecting the data, William L. Haskell, Ph.D., for
ciation between muscular strength and metabolic syndrome comments on an earlier draft, Margo Simmons and her staff for data
incidence. entry, and Melba Morrow for editorial assistance.
In summary, the present study showed that muscular This research was supported by NIH grants AG06945 and
strength was independently associated with metabolic syn- HL62508. Additional support has been provided by the Communi-
ties Foundation of Texas on recommendation of Nancy Ann and Ray
drome incidence in healthy men. Muscular strength may L. Hunt.
protect against developing the metabolic syndrome among There is no conflict of interest for any of the authors.
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STRENGTH AND METABOLIC SYNDROME INCIDENCE Medicine & Science in Sports & Exercise姞 1855