Journal of Cardiopulmonary Rehabilitation & Prevention:
Effects of Muscular Strength on Cardiovascular Risk Factors and Prognosis
Artero, Enrique G. PhD; Lee, Duck-chul PhD; Lavie, Carl J. MD; España-Romero, Vanesa PhD; Sui, Xuemei MD, MPH; Church, Timothy S. MD, MPH, PhD; Blair, Steven N. PED
Departments of Exercise Science (Drs Artero, Lee, España-Romero, Sui, and Blair) and Epidemiology and Biostatistics (Dr Blair), Arnold School of Public Health, University of South Carolina. Columbia; Area of Physical Education and Sport, School of Education, University of Almería. Almería, Spain (Dr Artero); Department of Cardiovascular Diseases, John Ochsner Heart and Vascular Institute, Ochsner Clinical School - The University of Queensland School of Medicine. New Orleans, Louisiana (Dr Lavie); and Preventive Medicine Laboratory, Pennington Biomedical Research Center. Baton Rouge, Louisiana (Drs Lavie and Church).
Correspondence: Enrique G. Artero, PhD, Department of Exercise Science, Arnold School of Public Health, University of South Carolina, 921 Assembly St, Columbia, SC 29208 (firstname.lastname@example.org).
The authors declare no conflict of interest.
Physical fitness is one of the strongest predictors of individual future health status. Together with cardiorespiratory fitness (CRF), muscular strength has been increasingly recognized in the pathogenesis and prevention of chronic disease. We review the most recent literature on the effect of muscular strength in the development of cardiovascular disease, with special interest in elucidating its specific benefits beyond those from CRF and body composition. Muscular strength has shown an independent protective effect on all-cause and cancer mortality in healthy middle-aged men, as well as in men with hypertension and patients with heart failure. It has also been inversely associated with age-related weight and adiposity gains, risk of hypertension, and prevalence and incidence of the metabolic syndrome. In children and adolescents, higher levels of muscular fitness have been inversely associated with insulin resistance, clustered cardiometabolic risk, and inflammatory proteins. Generally, the influence of muscular fitness was weakened but remained protective after considering CRF. Also, interestingly, higher levels of muscular fitness seems to some extent counteract the adverse cardiovascular profile of overweight and obese individuals. As many of the investigations have been conducted with non-Hispanic white men, it is important to examine how race/ethnicity and gender may affect these relationships. To conclude, most important effects of resistance training are also summarized, to better understand how higher levels of muscular fitness may result in a better cardiovascular prognosis and survival.
Physical fitness is one of the strongest predictors of individual future health status.1 Health-related fitness has been characterized by the ability to perform daily activities with vigor, without undue fatigue, and by traits and capacities that are associated with a low risk for the development of chronic diseases and premature death.2,3 Together with cardiorespiratory fitness (CRF), muscular or musculoskeletal fitness is also one of its main components, and has been increasingly recognized in the pathogenesis and prevention of chronic disease.4,5 In fact, muscle-strengthening activities are currently included in most of the institutional recommendations of exercise to maintain and improve overall health.2,6–9
Muscular fitness comprises the ability of a specific muscle or muscle group to generate force or torque (muscular strength [MusS]), to resist repeated contractions over time or to maintain a contraction for a prolonged period of time (muscular endurance), and to carry out a maximal, dynamic contraction of a single muscle or muscle group in a short period of time (explosive strength, also called muscular power).3 Among the components of muscular fitness, MusS has been traditionally the most frequently studied in relation to health. Thus, this term will be preferably used in this article unless otherwise indicated.
This report reviews the most recent literature on the effect of muscular fitness, especially MusS, in the development of cardiovascular disease (CVD), with special interest in elucidating its specific benefits beyond those provided by CRF, body composition, and other related confounders.
The medical electronic databases MEDLINE, SCOPUS, and SPORTS DISCUS were used to search for studies relating muscular fitness (MusS, muscular endurance, and power) with CVD risk factors, incident CVD, and mortality. The search was preferably limited to articles from January 2000 to December 2011 and published in English, although additional studies were also identified from reference lists.
Muscular Strength and Mortality
Several prospective studies have shown that MusS is inversely associated with all-cause mortality.10–23 Furthermore, some of these studies also explored the association with cause-specific mortality, including CVD.11,17,20,21 However, all but 1 of these studies assessed MusS through a handgrip test,22 which involves relatively small muscle groups. Only 1 of them included CRF as a critical confounder,14 and most were short-term followups (4–6 years)10–12,16–19,23 or included only older adults ($65 years),10,12,16–20,22,23 which could be a problem with reverse causation in that muscle weakness could be because of poor health.
More recent epidemiologic studies extend the association between MusS and mortality to younger populations. In the Aerobics Center Longitudinal Study (ACLS) cohort, we observed that a higher level of MusS, measured as 1 repetition maximum (1 RM) for bench and leg presses, was inversely and independently associated with deaths from all causes and cancer in 8762 men (mean age, 42.3 years) followed up on average 19 years.24 The association was independent of central and total adiposity,24,25 whereas the association with death from CVD was attenuated after adjustment for CRF (maximal treadmill time).24 The attenuation in CVD mortality when including CRF may suggest a higher protection from this physical fitness component in the development of CVD, although we must also consider the difficulty of disentangling the combined effects of CRF and MusS in an observational study.24 Future prospective studies should investigate whether MusS protects against CVD mortality beyond the benefits provided by CRF, especially among women, where studies are particularly scarce.
Hypertension (HTN) is clearly associated with an increased risk of CVD mortality.26 Using the ACLS cohort, we explored the association between MusS (1 RM for bench and leg presses) and all-cause deaths among 1506 men with HTN (mean age, 50.2 years) after 18 years of followup.27 After comprehensive adjustment, including CRF, men with HTN and a high level of MusS had a lower risk of all-cause mortality. The lowest mortality risk was observed among participants with high levels of both MusS and CRF. However, the relatively small number of deaths, even during a nearly 20-year followup, did not allow examining disease-specific mortality risk.27
A study by Hulsmann et al28 in patients with congestive heart failure provided insight into the association of MusS with CVD mortality. All participants (n = 93; mean age, 56 ± 9 years) had a left ventricular (LV) ejection fraction <35%, and were followed up for mortality on average 24 months. In this heart failure cohort, knee flexor muscles isokinetic strength significantly predicted mortality when expressed per kilogram of body weight, independent of CRF (peak VO2 during upright maximal bicycle test), neurohormones, and b-blocker therapy.28
Muscular Strength and Incident CVD
To the best of our knowledge, we did not find in the literature any study investigating the association between MusS and the incidence of CVD while taking into account the confounding effects of CRF. However, the study by Silventoinen et al29 must be highlighted given the sample size (1 145 467 men), participant age at baseline (18.2 years), the long followup (24.4 years), and the inclusion of different CVD endpoints (fatal and nonfatal coronary heart disease and 3 types of stroke). Elbow flexion, handgrip, and knee extension were used as indicators of MusS, and the analyses were adjusted for height, body mass index (BMI), systolic and diastolic blood pressure (BP), and social position. All MusS indicators were inversely associated with disease risk. For coronary heart disease and intracerebral infarction, handgrip strength was the best predictor, whereas for intracerebral and subarachoid hemorrhage, knee extension strength was the best predictor.29 Whether this protective effect was because of MusS per se or rather was expressing the role of general physical fitness status cannot be elucidated from this study.
Muscular Strength and CVD Risk Factors: Primary Prevention
Two studies have hypothesized that MusS could have a role in preventing a positive energy balance and unhealthful weight gain. Mason et al30 observed that a low level of muscular fitness was associated with higher odds of gaining at least 10 kg in 291 men and 315 women followed up for 20 years. The assessment of muscular fitness included handgrip strength, push-ups, sit-ups, and sit-and-reach tests, and the association was independent of BMI, CRF (submaximal step test) and physical activity.30 Using a considerably larger sample size (3258 men) although with shorter followup (8.3 years), we observed that MusS measured as 1 RM for bench and leg presses, was inversely associated with prevalence and incidence of excessive total and abdominal fat, defined as $25% and $102 cm, respectively.31 The association remained after controlling for body weight, CRF, and other confounders.31 These findings suggest that age-related weight and adiposity gains may be more pronounced among individuals with low levels of muscular fitness.
During a mean followup of 19 years, Maslow et al32 analyzed the influence of MusS on incident HTN among 4147 men (mean age, 43 years) in the ACLS cohort. In only prehypertensive men (systolic BP of 120–139 mm Hg or diastolic BP of 80–89 mm Hg), middle and high levels of MusS (ie, 1 RM) were associated with a reduced risk of HTN. Although it remained protective, the relationship was no longer significant after controlling for CRF. In normotensive men, such an association was not apparent.32
Skeletal muscle is the primary tissue for glucose and triglyceride (TG) metabolism, thereby providing rationale for its role in the metabolic syndrome (MetS).5 Wijndaele et al33 investigated the cross-sectional association of MusS and CRF with a continuous MetS risk score in male and female Flemish adults aged 18 to 75 years. Muscular strength was evaluated by measuring isometric knee extension and flexion peak torque, whereas CRF (peak VO2) was determined during a maximal cycle ergometer exercise test. The MetS risk score was based on waist circumference (WC), TGs, BP, fasting plasma glucose, and high-density lipoprotein (HDL) cholesterol. After adjusting for dietary intake, CRF, and other confounders, MetS risk was inversely associated with MusS in women. In men, however, adjustment for CRF attenuated this association. Independently of MusS, however, CRF was inversely and more strongly associated with MetS risk in both men and women. The significant associations of MusS and CRF with the individual MetS risk factors were only partially mediated by central and total adiposity (WC and BMI, respectively).33
In the ACLS cohort, Jurca et al34 reported an inverse association between MusS (ie, 1 RM) and prevalence of MetS in 8570 men aged 20 to 75 years. The association was notably attenuated when adjusted for CRF, whereas the effect of CRF was stronger and remained unchanged after adjusting for MusS.34 Furthermore, MusS was inversely associated with MetS in low and moderate CRF groups, but did not provide any additional benefit in participants with high CRF. The joint protective effect of MusS and CRF on the prevalence of MetS was observed among overweight and obese men.34
The same authors analyzed the prospective association of MusS with MetS incidence in 3233 men after 7 years of followup.35 After adjusting for potential confounders, such as number of risk factors at baseline, and family history of diabetes, HTN, and premature coronary heart disease, the authors observed an inverse association between 1 RM MusS and the risk of incident MetS. Further adjustment for CRF attenuated the association to being marginally not significant, although the risk of developing MetS was still significantly lower among men with high compared with low MusS.35
A cross-sectional analysis in the ACLS cohort found no beneficial effects of greater MusS on total cholesterol, TGs, and low-density lipoprotein (LDL) and HDL cholesterol.36 The study included 5460 men and 1193 women aged 20 to 69 years (mean age, ∼40 years), and took into account the possible confounding effect of CRF and body composition (sum of 7 skinfolds, BMI, or weight).36
Inflammatory proteins have been negatively associated with MusS in the elderly.37–39 The causal pathway leading from inflammation to loss of MusS has not been fully explained, but it has been suggested that low-grade inflammation may cause a decline of physical functioning through its catabolic effects on skeletal muscle.40 No studies have been found relating MusS (as exposure) and inflammatory proteins (outcome) in middle-aged adults.
Muscular Strength and Cardiometabolic Health in Youth: Primordial Prevention
It is recognized that CVD is partly a pediatric problem because the onset of atherosclerosis seems to occur in early childhood.41 Thus, timing is critical and interventions should not only focus on the modification of risk factors once they are established (primary prevention), but most importantly should prevent risk factor development in the first place (primordial prevention). Extensive evidence supports current physical activity recommendations for youth42 for the inclusion of muscle-strengthening activities in addition to aerobic exercise to maintain cardiometabolic health at early ages and later in life.
Benson et al43 investigated in 126 children (mean age, 12.1 ± 1.2 years) the cross-sectional association of CRF and MusS with estimated insulin resistance (Homeostasis Assessment Model 2; HOMA2-IR). Muscular strength was measured as 1 RM for bench press and leg press, whereas CRF was determined as peak VO2 in a maximal treadmill walk protocol. Greater insulin resistance was associated with greater WC, lower CRF, and lower MusS. Upper body MusS and WC were the only independent predictors of insulin resistance, accounting for 39% of the variance. Children in the highest and middle tertiles of upper body MusS were 98% less likely to have high insulin resistance than those with the lowest MusS, adjusted for maturation, WC, and BMI. When further adjusted for CRF, upper body MusS was slightly attenuated but still significant for the high MusS group and attenuated and of borderline significance for the moderate MusS group. Similar trends were present for high versus low CRF, and this association was only slightly attenuated when adjusted for upper body MusS.43
In 460 boys and girls aged 13 to 18.5 years, we investigated the independent association of muscular fitness and CRF with a continuous cardiometabolic risk score, based on TGs, LDL and HDL cholesterol, and glucose.44 The 20-m shuttle run test was used to assess CRF, and a muscular fitness index was created on the basis of handgrip, standing long jump, and bent arm hang tests. After adjusting for age, maturation, and CRF, muscular fitness presented an inverse association with cardiometabolic risk score in both genders, although statistically significant only among girls.44 Similarly, those adolescents with higher CRF had a healthier cardiometabolic score after adjusting for age, maturation, and muscular fitness, with the association reaching statistical signification only in boys. Self-reported physical activity was not associated with the cardiometabolic cluster.44 With 709 European adolescents (mean age, 14.9 ± 1.3 years) from 9 different countries, we observed that muscular fitness was negatively associated with clustered metabolic risk in both boys and girls, independent of CRF.45 Handgrip strength and standing long jump were included in the muscular fitness score, whereas 20-m shuttle run test was used to determine CRF. The continuous metabolic risk score included WC, systolic BP, TGs, total cholesterol/HDL cholesterol ratio, and insulin resistance (HOMA). Interestingly, the inverse association between muscular fitness and cardiometabolic risk persisted among nonoverweight and overweight/obese adolescents.45
In this latter work with European adolescents,45 muscular fitness presented a slightly stronger association with clustered cardiometabolic risk compared with CRF, which can be related to the use of 20-m shuttle run test. In contrast, in a similar study by Steene-Johannessen et al,46 the positive influence of CRF (peak VO2 in a cycle ergometry test) on clustered cardiometabolic risk was stronger than that provided by muscular fitness. Nevertheless, muscular fitness was inversely and independently associated with cardiometabolic risk after adjusting for CRF. The study comprised 1592 Norwegian youths aged 9 and 15 years, and muscular fitness included handgrip strength, standing long jump, sit-up, and modified Biering-Sørensen test (endurance of trunk extensor muscles). Risk factors contained in the clustered cardiometabolic risk were systolic BP, TGs, HDL cholesterol, insulin resistance (HOMA), and WC.46 Similar to our results,45 the protective role of muscular fitness in Norwegian youths46 was observed across both normal and overweight participants, the association being stronger in the overweight group.
A stronger association of CRF compared with MusS was also reported by Janz et al47 in relation to several CVD risk factors, among 125 boys and girls aged 10.5 years at baseline. Authors investigated whether changes over 4 years in fat-free mass (bioelectric impedance), peak VO2 (cycle ergometry), and handgrip strength could predict levels of CVD risk factors in year 5. After considering age, gender, and fat-free mass, CRF explained 11% of the variability in total cholesterol/HDL cholesterol, 5% in LDL cholesterol, and 7% in both sum of 6 skinfolds and WC. Muscular strength explained 4% of variability in systolic BP and 8% of variability in both skinfolds and WC.47
Apart from CVD traditional risk factors, muscular fitness has also shown to be inversely and independently associated with other emerging cardiometabolic biomarkers in youths. Ruiz et al48 investigated in 416 boys and girls (mean age, 15.4 ± 1.4 years) the association between muscular fitness (handgrip strength and standing long jump) and C-reactive protein, complement factors C3 and C4, ceruloplasmin, and prealbumin levels. After controlling for gender, age, maturation, weight, height, socioeconomic status, and CRF (20-m shuttle run test), muscular fitness was inversely associated with C-reactive protein, C3, and ceruloplasmin. Moreover, C-reactive protein, which appears to be a predictor of CVD and is associated with CRF and especially with being overweight or obese,49,50 was inversely associated with muscular fitness in overweight adolescents after controlling for body fat and fat-free mass.
Summarizing and Interpreting the Evidence
The observational studies reviewed suggest in middle-aged adults an independent protective effect of MusS on all-cause and cancer mortality,24,25 as well as all-cause mortality in men with HTN27 and in patients with heart failure.28 It has also been inversely and independently associated with age-related weight30 and adiposity31 gains, risk of HTN in prehypertensive men,32 and prevalence and incidence of the MetS.33–35 In children and adolescents, higher levels of muscular fitness have been inversely and independently associated with insulin resistance,43 clustered cardiometabolic risk,44–47 and inflammatory proteins48 (Table 1). In only a few studies, the protective influence of MusS became nonsignificant after considering CRF.24,32,35,44 Also, interestingly, higher levels of MusS seems to some extent counteract the adverse cardiovascular profile of overweight and obese individuals.34,35,45,46,48
Many studies (not discussed in this review) have focused on elderly people,10,12,16–20,22,23 in whom frailty and sarcopenia make it difficult to explore the true connection between MusS and cardiovascular health. More prospective and intervention studies are needed in middle-aged adults in relation with incident CVD, CRF and body composition being crucial elements in this debate.
Valid and reliable MusS tests such as 1 RM,24,25,27,31,32,34–36,43 handgrip,30,44–48 or isokinetic tests28,33 do not require propulsion or lifting of the body mass. When using these tests, it is critical to somehow consider body size to express strength values. Different approaches have been used, such as normalizing strength per kilogram of body weight,24,25,27,28,32,34,35,43,45,46 the use of allometric exponents,33,47 the adjustment for body weight,31,36,48 BMI,24,25,27,30,36 total and/or central adiposity,25,36,43,48 or fat-free mass,47,48 and also stratified analyses by BMI categories.34,35,45,46,48 By doing this, we can more accurately compare individuals with different body sizes and focus on muscle quality rather than muscle quantity. The literature reviewed suggests that increasing or maintaining appropriate levels of MusS has many health-related implications other than those ascribed to morphologic factors.
Potential Mechanisms: Insights from Resistance Training Interventions
In different population studies, muscular fitness and CRF have shown to be moderately correlated.24,30 Maintaining adequate MusS, muscular endurance, and flexibility will facilitate ability to carry out activities of daily living and to participate in physical activity, and this will likely help to maintain CRF. However, the reported level of that association is only moderate (r ∼ 0.3–0.4),24,25,27,30 indicating that muscular fitness may prevent CVD at least partially through biological pathways different than those associated with CRF.
Individual MusS level is influenced by several factors, such as age, gender, genotype, nutritional factors, or subclinical disease. Nevertheless, it is clear that muscle-strengthening activities are major determinants of MusS.7,51 We have previously reported a strong and positive association between the frequency of self-reported resistance training (RT) and maximal MusS in men enrolled in the ACLS,34 which indicates that objective standardized MusS measurements can provide an adequate representation of RT exercise habits at the population level. It is likely that the protective role of MusS is a function of participation in regular muscle-strengthening activities, rather than a mere consequence of other factors affecting both MusS and cardiovascular health.
Several reviews have summarized the health-related benefits of RT.7,52–57 Among those closely related with CVD, we must highlight the positive effects on muscle mass, muscle quality (increased strength for same muscle mass), and adipose tissue; maintenance of or an increase in resting metabolic rate; prevention of age-associated fat gains; reduction of visceral adipose tissue; improvements in blood glucose levels, basal insulin levels, insulin response, and insulin sensitivity; improvements in resting BP, and decreases in HbA1c in diabetic man and women7,52–58 (Table 2). There is still little evidence that RT may improve lipoprotein-lipid profiles.52 Other less explored mechanisms include improved endothelial function,59 antioxidant defense,60,61 and immune function,62 and decreased central arterial stiffness.63
Intensive RT characteristically increases LV wall thickness and mass, with little or no change in LV diameter,7 a process that is termed concentric LV hypertrophy.64,65 Concentric LV hypertrophy associated with RT appears to be a response to the pressure load (in contrast to the volume load of aerobic exercise) and serves to reduce the systolic burden per myofiber, thereby preserving normal LV wall stress. The increase in skeletal muscle strength induced by RT results in a lower hemodynamic stress (heart rate and systolic BP) for a given skeletal muscle force after RT.7 Also, although RT does not impose a large aerobic burden, some studies have demonstrated a modest increase in peak VO2 and decreases in submaximal heart rate and systolic BP during aerobic exercise after a program of RT.7
Among the many studies of RT in healthy adults, there have been no reported cardiovascular complications. The American College of Sports Medicine66 and the American Heart Association7 indicate that the contraindications to RT are similar to those for aerobic exercise. Thus, the same screening criteria used for healthy adults before participation in aerobic exercise would apply.52
CONCLUSIONS AND FUTURE DIRECTIONS
Considerable evidence supports the important and independent role of MusS in the prevention of CVD. However, as most efforts have focused on mortality and CVD risk factors, more prospective and intervention studies are needed in relation with incident CVD. Whenever possible, CRF, body composition, and other related factors should be considered. Also, the majority of investigations have been conducted with non-Hispanic white men,24,25,27,31,32,34,35 so it is important to examine how race/ethnicity and gender may affect these relationships.67 Special attention should be paid to growth and development stages,68 when CRF, MusS, and body composition are mostly determined.
To conclude, RT must be considered in addition to aerobic exercise in the prevention and treatment of CVD, since both MusS and CRF may provide unique benefits. In fact, RT might be a more attractive type of exercise for overweight and obese individuals, who are at a higher risk of developing CVD and who may be averse to aerobic exercise. Clinicians and fitness professionals are directed to several guidelines and statements that have been developed for the prescription of RT in different populations: apparently healthy middle-aged and older adults,53 children and adolescents,69,70 and patients with CVD.7
This work was supported by National Institutes of Health grants (AG06945, HL62508, R21DK088195), and in part by an unrestricted research grant from The Coca-Cola Company; Spanish Ministry of Education (EX-2009-0899; EX-2010-1008).
1. Kodama S, Saito K, Tanaka S, et al. Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis. JAMA. 2009;301:2024–2035.
3. Ruiz JR, Castro-Pinero J, Artero EG, et al. Predictive validity of health-related fitness in youth: a systematic review. Br J Sports Med. 2009;43:909–923.
4. Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84:475–482.
5. Stump CS, Henriksen EJ, Wei Y, Sowers JR. The metabolic syndrome: role of skeletal muscle metabolism. Ann Med. 2006;38: 389–402.
6. Kraemer WJ, Adams K, Cafarelli E, et al. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2002;34: 364–380.
7. Williams MA, Haskell WL, Ades PA, et al. Resistance exercise in individuals with and without cardiovascular disease: 2007 update: a scientific statement from the American Heart Association. Circulation. 2007;116:572–584.
10. Phillips P. Grip strength, mental performance and nutritional status as indicators of mortality risk among female geriatric patients. Age Ageing. 1986;15:53–56.
11. Fujita Y, Nakamura Y, Hiraoka J, et al. Physical-strength tests and mortality among visitors to health-promotion centers in Japan. J Clin Epidemiol. 1995;48:1349–1359.
12. Laukkanen P, Heikkinen E, Kauppinen M. Muscle strength and mobility as predictors of survival in 75-84-year-old people. Age Ageing. 1995;24:468–473.
13. Rantanen T, Harris T, Leveille SG, et al. Muscle strength and body mass index as long-term predictors of mortality in initially healthy men. J Gerontol A Biol Sci Med Sci. 2000;55:M168–173.
14. Katzmarzyk PT, Craig CL. Musculoskeletal fitness and risk of mortality. Med Sci Sports Exerc. 2002;34:740–744.
15. Metter EJ, Talbot LA, Schrager M, Conwit R. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol A Biol Sci Med Sci. 2002;57:B359–365.
16. Al Snih S, Markides KS, Ray L, Ostir GV, Goodwin JS. Handgrip strength and mortality in older Mexican Americans. J Am Geriatr Soc. 2002;50:1250–1256.
17. Rantanen T, Volpato S, Ferrucci L, Heikkinen E, Fried LP, Guralnik JM. Handgrip strength and cause-specific and total mortality in older disabled women: exploring the mechanism. J Am Geriatr Soc. 2003;51:636–641.
18. Newman AB, Kupelian V, Visser M, et al. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci. 2006;61:72–77.
19. Rolland Y, Lauwers-Cances V, Cesari M, Vellas B, Pahor M, Grandjean H. Physical performance measures as predictors of mortality in a cohort of community-dwelling older French women. Eur J Epidemiol. 2006;21:113–122.
20. Gale CR, Martyn CN, Cooper C, Sayer AA. Grip strength, body composition, and mortality. Int J Epidemiol. 2007;36:228–235.
21. Sasaki H, Kasagi F, Yamada M, Fujita S. Grip strength predicts cause-specific mortality in middle-aged and elderly persons. Am J Med. 2007;120:337–342.
22. Swallow EB, Reyes D, Hopkinson NS, et al. Quadriceps strength predicts mortality in patients with moderate to severe chronic obstructive pulmonary disease. Thorax. 2007;62:115–120.
23. Buchman AS, Boyle PA, Wilson RS, Gu L, Bienias JL, Bennett DA. Pulmonary function, muscle strength and mortality in old age. Mech Ageing Dev. 2008;129:625–631.
24. Ruiz JR, Sui X, Lobelo F, et al. Association between muscular strength and mortality in men: prospective cohort study. BMJ. 2008;337:a439.
25. Ruiz JR, Sui X, Lobelo F, et al. Muscular strength and adiposity as predictors of adulthood cancer mortality in men. Cancer Epidemiol Biomarkers Prev. 2009;18:1468–1476.
26. Chobanian AV, Bakris GL, Black HR, et al. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA. 2003;289:2560–2572.
27. Artero EG, Lee DC, Ruiz JR, et al. A prospective study of muscular strength and all-cause mortality in men with hypertension. J Am Coll Cardiol. 2011;57:1831–1837.
28. Hulsmann M, Quittan M, Berger R, et al. Muscle strength as a predictor of long-term survival in severe congestive heart failure. Eur J Heart Fail. 2004;6:101–107.
29. Silventoinen K, Magnusson PK, Tynelius P, Batty GD, Rasmussen F. Association of body size and muscle strength with incidence of coronary heart disease and cerebrovascular diseases: a population-based cohort study of one million Swedish men. Int J Epidemiol. 2009;38:110–118.
30. Mason C, Brien SE, Craig CL, Gauvin L, Katzmarzyk PT. Musculoskeletal fitness and weight gain in Canada. Med Sci Sports Exerc. 2007;39:38–43.
31. Jackson AW, Lee DC, Sui X, et al. Muscular strength is inversely related to prevalence and incidence of obesity in adult men. Obesity (Silver Spring). 2010;18:1988–1995.
32. Maslow AL, Sui X, Colabianchi N, Hussey J, Blair SN. Muscular strength and incident hypertension in normotensive and prehypertensive men. Med Sci Sports Exerc. 2010;42:288–295.
33. Wijndaele K, Duvigneaud N, Matton L, et al. Muscular strength, aerobic fitness, and metabolic syndrome risk in Flemish adults. Med Sci Sports Exerc. 2007;39:233–240.
34. Jurca R, Lamonte MJ, Church TS, et al. Associations of muscle strength and fitness with metabolic syndrome in men. Med Sci Sports Exerc. 2004;36:1301–1307.
35. Jurca R, Lamonte MJ, Barlow CE, Kampert JB, Church TS, Blair SN. Association of muscular strength with incidence of metabolic syndrome in men. Med Sci Sports Exerc. 2005;37:1849–1855.
36. Kohl HW 3rd, Gordon NF, Scott CB, Vaandrager H, Blair SN. Musculoskeletal strength and serum lipid levels in men and women. Med Sci Sports Exerc. 1992;24:1080–1087.
37. Visser M, Pahor M, Taaffe DR, et al. Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci. 2002;57:M326–332.
38. Schaap LA, Pluijm SM, Deeg DJ, Visser M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med. 2006;119:526 e529–517.
39. Taaffe DR, Harris TB, Ferrucci L, Rowe J, Seeman TE. Cross-sectional and prospective relationships of interleukin-6 and C-reactive protein with physical performance in elderly persons: MacArthur studies of successful aging. J Gerontol A Biol Sci Med Sci. 2000;55:M709–715.
40. Ferrucci L, Penninx BW, Volpato S, et al. Change in muscle strength explains accelerated decline of physical function in older women with high interleukin-6 serum levels. J Am Geriatr Soc. 2002;50:1947–1954.
41. Kavey RE, Daniels SR, Lauer RM, Atkins DL, Hayman LL, Taubert K. American Heart Association guidelines for primary prevention of atherosclerotic cardiovascular disease beginning in childhood. Circulation. 2003;107:1562–1566.
42. U.S. Department of Health and Human Servics. Physical Activity and Health: A Report of the Surgeon General. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Centre for Chronic Disease Prevention and Health Promotion. http://www.cdc.gov/nccdphp/sgr/sgr.htm
. Accessed March 11, 2008.
43. Benson AC, Torode ME, Singh MA. Muscular strength and cardiorespiratory fitness is associated with higher insulin sensitivity in children and adolescents. Int J Pediatr Obes. 2006;1:222–231.
44. Garcia-Artero E, Ortega FB, Ruiz JR, et al. [Lipid and metabolic profiles in adolescents are affected more by physical fitness than physical activity (AVENA study)]. Rev Esp Cardiol. 2007;60: 581–588.
45. Artero EG, Ruiz JR, Ortega FB, et al. Muscular and cardiorespiratory fitness are independently associated with metabolic risk in adolescents: the HELENA study. Pediatr Diabetes. 2011;12:704–712.
46. Steene-Johannessen J, Anderssen SA, Kolle E, Andersen LB. Low muscle fitness is associated with metabolic risk in youth. Med Sci Sports Exerc. 2009;41:1361–1367.
47. Janz KF, Dawson JD, Mahoney LT. Increases in physical fitness during childhood improve cardiovascular health during adolescence: the Muscatine Study. Int J Sports Med. 2002;23(suppl 1):S15–S21.
48. Ruiz JR, Ortega FB, Warnberg J, et al. Inflammatory proteins and muscle strength in adolescents: the Avena study. Arch Pediatr Adolesc Med. 2008;162:462–468.
49. Lavie CJ, Church TS, Milani RV, Earnest CP. Impact of physical activity, cardiorespiratory fitness, and exercise training on markers of inflammation. J Cardiopulm Rehabil Prev. 2011;31: 137–145.
50. Lavie CJ, Milani RV, Ventura HO. Obesity and cardiovascular disease: risk factor, paradox, and impact of weight loss. J Am Coll Cardiol. 2009;53:1925–1932.
51. Thomis MA, Beunen GP, Maes HH, et al. Strength training: importance of genetic factors. Med Sci Sports Exerc. 1998;30:724–731.
52. Braith RW, Stewart KJ. Resistance exercise training: its role in the prevention of cardiovascular disease. Circulation. 2006;113: 2642–2650.
53. American College of Sports Medicine. Position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2009;41:687–708.
54. American College of Sports Medicine. Position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43:1334–1359.
55. Kelley GA, Kelley KS. Progressive resistance exercise and resting blood pressure: a meta-analysis of randomized controlled trials. Hypertension. 2000;35:838–843.
56. Cornelissen VA, Fagard RH. Effect of resistance training on resting blood pressure: a meta-analysis of randomized controlled trials. J Hypertens. 2005;23:251–259.
57. Kell RT, Bell G, Quinney A. Musculoskeletal fitness, health outcomes and quality of life. Sports Med. 2001;31:863–873.
58. Church TS, Blair SN, Cocreham S, et al. Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes: a randomized controlled trial. JAMA. 2010;304: 2253–2262.
59. Maeda S, Miyauchi T, Iemitsu M, Sugawara J, Nagata Y, Goto K. Resistance exercise training reduces plasma endothelin-1 concentration in healthy young humans. J Cardiovasc Pharmacol. 2004;44(suppl 1):S443–S446.
60. Garcia-Lopez D, Hakkinen K, Cuevas MJ, et al. Effects of strength and endurance training on antioxidant enzyme gene expression and activity in middle-aged men. Scand J Med Sci Sports. 2007;17:595–604.
61. Parise G, Phillips SM, Kaczor JJ, Tarnopolsky MA. Antioxidant enzyme activity is up-regulated after unilateral resistance exercise training in older adults. Free Radic Biol Med. 2005;39:289–295.
62. Simonson SR, Jackson CG. Leukocytosis occurs in response to resistance exercise in men. J Strength Cond Res. 2004;18:266–271.
63. Fahs CA, Heffernan KS, Ranadive S, Jae SY, Fernhall B. Muscular strength is inversely associated with aortic stiffness in young men. Med Sci Sports Exerc. 2010;42:1619–1624.
64. Patel DA, Lavie CJ, Milani RV, Ventura HO. Left atrial volume index predictive of mortality independent of left ventricular geometry in a large clinical cohort with preserved ejection fraction. Mayo Clin Proc. 2011;86:730–737.
65. Artham SM, Lavie CJ, Milani RV, Patel DA, Verma A, Ventura HO. Clinical impact of left ventricular hypertrophy and implications for regression. Prog Cardiovasc Dis. 2009;52:153–167.
66. American College of Sports Medicine. ACSM's Guidelines For Exercise Testing And Prescription. 8th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2009.
67. Rattarasarn C, Leelawattana R, Soonthornpun S. Contribution of skeletal muscle mass on sex differences in 2-hour plasma glucose levels after oral glucose load in Thai subjects with normal glucose tolerance. Metabolism. 2010;59:172–176.
68. Jimenez-Pavon D, Ortega FB, Valtuena J, et al. Muscular strength and markers of insulin resistance in European adolescents: the HELENA Study. Eur J Appl Physiol. 2012;112:2455–2465.
69. McCambridge TM, Stricker PR. Strength training by children and adolescents. Pediatrics. 2008;121:835–840.
70. Faigenbaum AD, Kraemer WJ, Blimkie CJ, et al. Youth resistance training: updated position statement paper from the national strength and conditioning association. J Strength Cond Res. 2009;23(5)(suppl):S60–S79.
cardiorespiratory fitness; cardiovascular disease; muscular strength; resistance training
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