Journal of Cardiopulmonary Rehabilitation & Prevention:
Relationship Between Strength, Function, and Quality of Life in Older Adults With Chronic Lung Disease: IS THERE AN INFLUENCE OF GENDER?
Benton, Melissa J. PhD, RN; Alexander, Jeffrey L. PhD; Holland, James D. MSN
Beth-El College of Nursing & Health Sciences, University of Colorado, Colorado Springs (Dr Benton); Department of Interdisciplinary Health Sciences, A.T. Still University, Mesa, Arizona (Dr Alexander); and College of Nursing, Valdosta State University, Valdosta, Georgia (Mr Holland).
Correspondence: Melissa J. Benton, PhD, RN, FACSM, Beth-El College of Nursing & Health Sciences, University of Colorado, Colorado Springs, 1420 Austin Bluffs Parkway, Colorado Springs, CO 80918 (email@example.com).
The authors declare no conflicts of interest.
PURPOSE: Chronic lung disease results in impaired quality of life (QOL) linked to loss of muscular strength and functional ability. Inequalities in strength and function may place women at greater risk than men. This study evaluated the influence of gender on the relationship between muscular strength, functional ability, and QOL.
METHODS: Older adults (N = 40) referred to a pulmonary rehabilitation program completed assessment of upper body and lower body strength, functional ability, and QOL. To compensate for gender differences, strength was normalized for body mass.
RESULTS: Strength was greater in men than in women (P < .001). No gender differences were observed for function. Men perceived better QOL related to physical function (score: 39.3 ± 3.3 vs 27.1 ± 2.1, P < .01) and social function (score: 58.0 ± 5.8 vs 41.6 ± 4.0, P < .05). In men, strength was related directly to QOL through physical function (r = 0.53, P < .05) and social function (r = 0.52, P < .05), and functional ability had no relationship to QOL. In women, strength was related to functional ability (r = 0.57, P < .05), and functional ability was directly related to QOL through physical function (r = 0.46, P < .05), and social function (r = 0.59, P < .01).
CONCLUSIONS: Functional ability mediates the relationship between strength and QOL in women, while in men strength is directly related to QOL. These gender-specific pathways to QOL may be of importance to clinicians planning interventions for older adults with chronic lung disease.
Although cardiovascular disease is recognized as a major cause of early mortality,1 the severity of chronic lung diseases such as asthma and chronic obstructive pulmonary disease (COPD) is often underappreciated. Worldwide, COPD is 1 of the 4 leading causes of death from noncommunicable disease,2 while in the United States, mortality from chronic respiratory diseases such as asthma ranks third.3 Typically, the prevalence of pulmonary disease increases with age and is linked to poorer health outcomes as well as increased mortality.4,5 Prevalence rates for COPD are estimated to rise from 10% of adults older than 40 years to 15% of adults older than 65 years,6 while mortality rates for asthma are more than 300% greater among older adults than among younger adults.7
In addition to poor health outcomes, chronic lung disease results in impaired quality of life (QOL). Older adults with asthma and COPD report significantly lower QOL than their healthy counterparts.8–10 Although the mechanism involved in the impairment process is undoubtedly multifactorial, loss of muscular strength and functional ability accompanies the aging process and is linked to diminished QOL in older adults, including those with pulmonary disease.11–13 In fact, impairments in strength and function may be more pronounced in older adults with pulmonary diseases such as COPD due to the systemic effects of the disease.14
Participation in regular physical activity by healthy older adults can prevent or reverse loss of strength and physical function, thereby promoting QOL.15–17 Exercise training programs also lead to improvements in physical function and QOL among older individuals with chronic lung disease.18,19 There is some evidence, however, that pulmonary disease may confound the relationship between physical function and QOL, making improvements in QOL difficult to predict.20 Although the exact mechanism is not clearly understood, gender may have a differential effect on the interplay between strength, physical function, and QOL among older adults with chronic lung disease.
There are well-recognized gender-specific inequalities in strength and functional ability. Generally, women have less skeletal muscle and strength than men, and this can impair functional ability especially during older age.21 These differences in strength and muscle mass remain consistent,22 even in the presence of chronic lung disease where men have been observed to have worse pulmonary function than women.22,23 In fact, although women have less impaired lung function, they report poorer QOL than their male counterparts.24,25
Raherison et al26 identified function as an influence on QOL in women with chronic lung disease. However, previous research regarding the relationship between function and QOL has been contradictory and has not considered the influence of strength. Although both de Torres et al27 and Katsura et al28 reported that among patients with chronic lung disease, women had lower functional ability and QOL than men, their findings regarding function and QOL were less consistent. De Torres et al27 found a relationship between function and QOL only in men, while Katsura et al28 reported that function was related to QOL among both men and women. Neither researcher considered muscular strength as a factor. A greater understanding of gender differences in the relationship between strength, function, and QOL among older adults with pulmonary disease is needed. Therefore, the purpose of this study was to compare the relationship between muscular strength, functional ability, and QOL in a cohort of older men and women with chronic lung disease.
Forty (men = 20, women = 20) older adults (70 ± 1.2 years) referred to a hospital-based, outpatient pulmonary rehabilitation (PR) program for management of chronic lung disease were recruited over a 3-year period as part of 2 sequential resistance training studies.29,30 New patients were offered the opportunity to participate sequentially and enrollment continued until 20 participants were recruited for each study. Primary diagnoses included COPD (n = 29; 73%), emphysema (n = 8; 20%), asthma (n = 1; 3%), lung cancer (n = 1; 3%), and Legionnaire's disease (n = 1; 3%). All testing was conducted before beginning PR program by the same researchers, except for the 6-Minute Walk Test (6MWT) that was conducted by the PR staff. Ethical approval was obtained jointly from the university and hospital institutional review boards.
Measurement of QOL
The Medical Outcomes Survey Short Form 36 (SF-36) was used to measure QOL. The SF-36 is a self-reported questionnaire that includes a separately scored physical function subscale that tracks with both self-reported and objectively measured function.31 It has also been used previously to assess QOL in COPD patients,28 which facilitates comparison of findings. The SF-36 uses a Likert-like scale, with greater scores indicating better QOL. Participants completed the SF-36 prior to functional testing. Subscale scores for physical function, role physical, bodily pain, general health, social function, role emotional, vitality, and mental health were calculated.
Measurement of Function
The 6MWT was used to measure functional ability according to American Thoracic Society guidelines for assessment of functional capacity in a clinical setting.32 The 6MWT is a commonly reported measure of functional ability for older adults.33 In patients with chronic lung disease, it has been validated as a measure of activity tolerance and has a strong predictive value for mortality.34–36 Furthermore, among older adults, muscular strength and SF-36 scores have been found to be related to 6MWT scores.37 The testing protocol was standardized according to American Thoracic Society guidelines.32
Measurement of Strength
Upper and lower body muscular strength was measured with a 1 repetition maximum (1RM) test for incline chest press and seated leg press (Universal Gym Equipment, Versailles, OH). The 1RM is commonly used as a field test of muscle strength in patients with chronic lung disease.38 Although the 6MWT is based primarily on lower body performance and, hence, is most likely influenced by lower body strength, upper body strength was included in the study analysis to capture the potential effects of gender. Greater gender differences have been observed in upper body strength compared with lower body strength, with women of all ages having significantly less upper body strength relative to body mass than men.39 Two trials of 1RM testing were completed with at least 2 days of rest between trials. A 2-day period has been found to be sufficient to verify recovery and absence of injury from 1RM testing in older pulmonary patients.40 Because participants were naive to lifting techniques, familiarization was incorporated into the first test session. For safety and to avoid the Valsalva maneuver, participants were reminded before each attempt to exhale during exertion (arm/leg extension) and inhale during relaxation (arm/leg flexion). At the beginning of each lift, participants were positioned with elbows at 90° and aligned with the shoulder joint (chest press) or hips flexed and knees at 90° with feet flat on the footplate (leg press). Each test began with a warm-up set at a light weight that allowed completion of 10 repetitions without difficulty. After 2 minutes of rest, the load was increased and participants were asked to complete one lift through a full range of motion. Resistance was progressively increased with 2-minute rest periods between attempts until the participant could not lift a given weight through a full range of motion with good form. The greatest weight successfully lifted during the 2 trials was identified as the 1RM.
Data were analyzed using SPSS version 20 with mean and standard error reported for all measurements. Significance was set at P < .05 (2-tailed). Descriptive statistics were used to describe participant characteristics. Strength was normalized for body mass using the equation: Sn =S · m−1.41 Gender differences were evaluated using analysis of variance (ANOVA), and effect size was calculated as η2 with cut points of 0.01, 0.06, and 0.14 for small, medium, and large effects, respectively.42 Pearson correlation coefficients were used to identify relationships between strength, function, and QOL.
No gender differences in age, body mass index, or pulmonary function were observed (Table 1). Functional ability, measured as the 6MWT distance, was 20% greater for men than for women, although this did not achieve a level of significance. Absolute strength was significantly (P < .001) greater in men for 1RM chest press (75% greater than women) and 1RM leg press (60% greater than women), while normalized upper and lower body strength remained 45% (UBSn) and 27% (LBSn) greater in men than in women (P < .001). Effect sizes were large (η2= 0.3–0.56) for all strength differences.
Gender differences in QOL were observed for only 2 SF-36 subscales, physical function and social function (Table 2). Men reported significantly greater scores for physical function (45% greater than women; P < .01) and social function (39% greater than women; P < .05), indicating better QOL. Effect sizes were medium to large (η2= 0.13–0.21) for differences in QOL.
Correlation analysis demonstrated direct relationships between functional ability (6MWT) and upper body strength (chest press: r = 0.41, P < .05) and lower body strength (leg press: r = 0.45, P < .01). These direct relationships with functional ability remained after strength was normalized for body mass (UBSn: r = 0.36, P < .05; LBSn: r = 0.53, P < .01). Strength and functional ability were directly related to QOL through the physical function subscale (chest press: r = 0.40, P < .05; leg press: r = 0.53, P < .01; 6MWT: r = 0.46, P < 0.01), although only strength was directly related to the social function subscale (chest press: r = 0.38, P < .05; leg press: r = 0.53, P < .01). However, social function was directly and strongly related to physical function (r = 0.54; P < .001). After normalization, only lower body strength was directly related to QOL through both the physical function (LBSn: r = 0.52, P < .01) and social function (LBSn: r = 0.52, P < .01) subscales (Figure 1).
Gender analysis revealed differences between men and women in the relationship between strength, function, and QOL. In men, functional ability had no relationship to strength or QOL (Figure 2). Lower body strength was directly related to QOL through the physical function subscale (leg press: r = 0.53, P < .05) and the social function subscale (LBSn: r = 0.52, P < .05). Although upper body strength was strongly related to lower body strength (chest press-leg press: r = 0.56, P < .05; UBSn-LBSn: r = 0.54, P < .05), there was no direct relationship to QOL.
In women, functional ability was directly related to QOL through both the physical (r = 0.46, P < .05) and social (r = 0.59 P < .01) function subscales (Figure 3). Lower body strength was directly related to QOL only through the social function subscale (r = 0.54, P < .05) that had no direct relationship to the physical function subscale. Instead, lower body strength was related to the physical function component of QOL only through its relationship to functional ability. Furthermore, upper body strength was related to QOL only through its relationship with lower body strength (chest press-leg press: r = 0.51, P < .05).
To our knowledge, this is the first study that has attempted to elucidate the pathway between muscular strength, functional ability, and QOL in older men and women with chronic lung disease. Our principal finding was that gender-specific pathways exist. Among all participants combined, both strength and function were directly related to QOL. However, in men alone, functional ability had no relationship with QOL. Instead, strength was directly related to QOL. By comparison, among women, functional ability mediated the relationship between strength and QOL. Although lower body strength was directly related to the social function subscale of QOL, there was no direct relationship between the social and physical function subscales, and hence functional ability, which was related to both the social and physical components of QOL, remained the intervening relationship.
Surprisingly, normalization of upper body strength for body mass did not significantly influence the pathway in women. Upper body strength was not observed to have a direct relationship to QOL in either men or women, which may explain the lack of effect of normalization. Normalization for body mass merely allows for a more direct comparison of strength between individuals with different body mass, such as men and women. Since no direct influence on QOL was observed after equalizing gender differences in upper body strength, it would appear that QOL in men and women with chronic lung disease is not directly influenced by upper body strength.
Our current findings partially agree with prior research by Katsura et al,28 who found that older Japanese men with chronic lung disease reported significantly better scores than women on the physical function subscale of the SF-36. However, contrary to our findings, they found that functional ability, measured as 6MWT, was directly related to QOL in men as well as women. This inconsistency may be due to the fact that the relationship they reported with function was based on the St. George's Respiratory Questionnaire (SGRQ) rather than the SF-36. The SGRQ was developed specifically to measure the impact of respiratory disease with airflow limitation on QOL, and the validation process included agreement with 6MWT.43 It is, therefore, not entirely surprising that Katsura et al28 observed a direct relationship between QOL and function without regard for gender. It is possible that gender differences in the relationship between QOL and function would have been apparent had they included the SF-36 in their correlation analysis.
Our results are also inconsistent with those of de Torres et al,27 who evaluated the relationship between functional ability (6MWT) and QOL in older Spanish men and women with pulmonary disease. Although de Torres et al27 reported that men had better overall QOL than women, which agrees with our findings, they also observed that function was directly related to QOL in men but not in women, which is directly in contrast to our findings. In fact, they reported that among women, only dyspnea had a strong relationship to QOL. However, as in the Katsura et al28 study, QOL was measured with the SGRQ, which is likely more sensitive to dyspnea than functional ability. Furthermore, female participants in the de Torres et al27 study were notably younger (56 ± 11 vs 68.5 ± 1.7 years) and able to achieve a 6MWT score that was 65% greater than the women in our study. This appreciably greater level of fitness may have moderated the relationship between function (6MWT) and QOL (SGRQ) that would be anticipated in women based not only on our findings, but also on those of Katsura et al.28
The principal question raised by this study is the mechanism that determines the gender-specific pathways between strength, function, and QOL. Muscle fiber types may provide some insight into this question. Functional ability, when measured as the 6MWT, involves primarily muscular endurance, which is strongly dependent on type I muscle fibers, while muscular strength, measured as 1RM, relies heavily on type II muscle fibers.44 Among older adults, men and women have relatively equal type I muscle cross-sectional area, while men have significantly greater type II cross-sectional area than women.45 Furthermore, older men can exert significantly greater force with type II fibers compared with type I fibers, while women's ability to generate force does not appear to vary between fiber types.46 Finally, in the presence of chronic lung disease, a shift in fiber composition from type I to type II has been observed47 that may disproportionately affect men because of their initially greater preponderance of type II fibers, resulting in a decreased reliance on endurance and an increased reliance on strength. By comparison, this shift may have a blunted effect on women who generate relatively equivalent force with both type I and type II fibers. Hence, in men, muscular strength may directly influence the physical component of QOL, while among women, functional ability or the “work capacity” of muscles becomes the mediating influence between strength and QOL.
We recognize that there are limitations to this study that include our sample size, which was smaller than that of either de Torres et al27 or Katsura et al.28 However, although our findings differ regarding the association between functional ability and QOL, this is most likely due to the QOL tool itself. The physical function subscale of the SF-36 was developed to measure multidimensional limitations in physical activities and self-care due to general health problems48 rather than specifically dyspnea, which was the basis for the SGRQ. As such, we believe that the SF-36 is more appropriate for evaluation of the relationship between function and QOL than the SGRQ. In addition to the differences in measurement tools, an effect of culture cannot be completely ruled out. The older men and women in this study may have had cultural characteristics unique to the United States that were not mutually shared by older Japanese and Spanish men and women. Further research on cultural influences on the determinants of QOL is certainly merited.
One of the strengths of this study is the inclusion of upper and lower body muscular strength in our analysis. In addition, to compensate for gender differences, we normalized strength relative to body mass. Although this is a well-recognized technique for comparison of intraindividual strength differences, we have not observed its frequent use in research studies.
In conclusion, our findings demonstrate that functional ability mediates the relationship between muscular strength and QOL in women, while in men strength is directly related to QOL with no intervening influence of function. These gender-specific pathways to QOL may be of importance to clinicians planning interventions for community-dwelling older adults with chronic lung disease.
1. Pagidipati NJ, Gaziano TA. Estimating deaths from cardiovascular disease: a review of global methodologies of mortality measurement. Circulation. 2013;127:749–756.
2. Lozano R, Naghavi M, Foreman K, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380(9859):2095–2128.
3. Minino AM, Murphy SL, Xu J, Kochanek KD. Deaths: final data for 2008. Natl Vital Stat Rep. 2011;59:1–126.
4. Akgun KM, Crothers K, Pisani M. Epidemiology and management of common pulmonary diseases in older persons. J Gerontol A Biol Sci Med Sci. 2012;67:276–291.
5. Lindberg A, Jonsson AC, Ronmark E, Lundgren R, Larsson LG, Lundback B. Ten-year cumulative incidence of COPD and risk factors for incident disease in a symptomatic cohort. Chest. 2005;127:1544–1552.
6. Halbert RJ, Natoli JL, Gano A, Badamgarav E, Buist AS, Mannino DM. Global burden of COPD: systematic review and meta-analysis. Eur Respir J. 2006;28:523–532.
7. Tsai CL, Lee WY, Hanania NA, Camargo CA Jr. Age-related differences in clinical outcomes for acute asthma in the United States, 2006–2008. J Allergy Clin Immunol. 2012;129:1252.e1–1258.e1.
8. Arne M, Janson C, Janson S, et al. Physical activity and quality of life in subjects with chronic disease: chronic obstructive pulmonary disease compared with rheumatoid arthritis and diabetes mellitus. Scand J Prim Health Care. 2009;27:141–147.
9. Farkas J, Kosnik M, Zaletel-Kragelj L, Flezar M, Suskovic S, Lainscak M. Distribution of self-rated health and association with clinical parameters in patients with chronic obstructive pulmonary disease. Wien Klin Wochenschr. 2009;121:297–302.
10. Kauppi P, Kupiainen H, Lindqvist A, et al. Overlap syndrome of asthma and COPD predicts low quality of life. J Asthma. 2011;48:279–285.
11. Groessl EJ, Kaplan RM, Rejeski WJ, et al. Health-related quality of life in older adults at risk for disability. Am J Prev Med. 2007;33:214–218.
12. Reardon JZ, Lareau SC, ZuWallack R. Functional status and quality of life in chronic obstructive pulmonary disease. Am J Med. 2006;119(10) (suppl 1):32–37.
13. Kapella MC, Larson JL, Covey MK, Alex CG. Functional performance in chronic obstructive pulmonary disease declines with time. Med Sci Sports Exerc. 2011;43:218–224.
14. Eisner MD, Blanc PD, Yelin EH, et al. COPD as a systemic disease: impact on physical functional limitations. Am J Med. 2008;121:789–796.
15. Stewart KJ, Turner KL, Bacher AC, et al. Are fitness, activity, and fatness associated with health-related quality of life and mood in older persons? J Cardiopulm Rehabil. 2003;23:115–121.
16. Katula JA, Rejeski WJ, Marsh AP. Enhancing quality of life in older adults: a comparison of muscular strength and power training. Health Qual Life Outcomes. 2008;6:45.
17. Elavsky S, McAuley E, Motl RW, et al. Physical activity enhances long-term quality of life in older adults: efficacy, esteem, and affective influences. Ann Behav Med. 2005;30:138–145.
18. Turner S, Eastwood P, Cook A, Jenkins S. Improvements in symptoms and quality of life following exercise training in older adults with moderate/severe persistent asthma. Respiration. 2011;81:302–310.
19. Corhay JL, Nguyen D, Duysinx B, et al. Should we exclude elderly patients with chronic obstructive pulmonary disease from a long-time ambulatory pulmonary rehabilitation programme? J Rehabil Med. 2012;44:466–472.
20. Troosters T, Gosselink R, Decramer M. Exercise training in COPD: how to distinguish responders from nonresponders. J Cardiopulm Rehabil. 2001;21:10–17.
21. Fragala MS, Clark MH, Walsh SJ, et al. Gender differences in anthropometric predictors of physical performance in older adults. Gend Med. 2012;9:445–456.
22. Verhage TL, Heijdra Y, Molema J, Vercoulen J, Dekhuijzen R. Associations of muscle depletion with health status. Another gender difference in COPD? Clin Nutr. 2011;30:332–338.
23. Carrasco-Garrido P, de Miguel-Diez J, Rejas-Gutierrez J, et al. Characteristics of chronic obstructive pulmonary disease in Spain from a gender perspective. BMC Pulm Med. 2009;9:2.
24. Naberan K, Azpeitia A, Cantoni J, Miravitlles M. Impairment of quality of life in women with chronic obstructive pulmonary disease. Respir Med. 2012;106:367–373.
25. Rodriguez-Pecci MS, de la Fuente-Aguado J, Montero-Tinnirello J, Sanjurjo-Rivo AB, Sanchez-Conde P, Fernandez-Fernandez FJ. [Chronic obstructive pulmonary disease: differences between men and women]. Medicina (B Aires). 2012;72:207–215.
26. Raherison C, Biron E, Nocent-Ejnaini C, Taille C, Tillie-Leblond I, Prudhomme A. [Are there specific characteristics of COPD in women?]. Rev Mal Respir. 2010;27:611–624.
27. de Torres JP, Casanova C, Hernandez C, et al. Gender associated differences in determinants of quality of life in patients with COPD: a case series study. Health Qual Life Outcomes. 2006;4:72.
28. Katsura H, Yamada K, Wakabayashi R, Kida K. Gender-associated differences in dyspnoea and health-related quality of life in patients with chronic obstructive pulmonary disease. Respirology. 2007;12:427–432.
29. Alexander JL, Phillips WT, Wagner CL. The effect of strength training on functional fitness in older patients with chronic lung disease enrolled in pulmonary rehabilitation. Rehabil Nurs. 2008;33:91–97.
30. Phillips WT, Benton MJ, Wagner CL, Riley C. The effect of single set resistance training on strength and functional fitness in pulmonary rehabilitation patients. J Cardiopulm Rehabil. 2006;26:330–337.
31. Reuben DB, Valle LA, Hays RD, Siu AL. Measuring physical function in community-dwelling older persons: a comparison of self-administered, interviewer-administered, and performance-based measures. J Am Geriatr Soc. 1995;43:17–23.
32. ATS statement: guidelines for the Six-Minute Walk Test. Am J Respir Crit Care Med. 2002;166:111–117.
33. Perera S, Mody SH, Woodman RC, Studenski SA. Meaningful change and responsiveness in common physical performance measures in older adults. J Am Geriatr Soc. 2006;54:743–749.
34. Enfield K, Gammon S, Floyd J, et al. Six-Minute Walk Distance in patients with severe end-stage COPD: association with survival after inpatient pulmonary rehabilitation. J Cardiopulm Rehabil Prev. 2010;30:195–202.
35. Gerald LB, Sanderson B, Redden D, Bailey WC. Chronic obstructive pulmonary disease stage and 6-minute walk outcome. J Cardiopulm Rehabil. 2001;21:296–299.
36. Pinto-Plata VM, Cote C, Cabral H, Taylor J, Celli BR. The 6-min walk distance: change over time and value as a predictor of survival in severe COPD. Eur Respir J. 2004;23:28–33.
37. Lord SR, Menz HB. Physiologic, psychologic, and health predictors of 6-minute walk performance in older people. Arch Phys Med Rehabil. 2002;83:907–911.
38. Robles PG, Mathur S, Janaudis-Fereira T, Dolmage TE, Goldstein RS, Brooks D. Measurement of peripheral muscle strength in individuals with chronic obstructive pulmonary disease: a systematic review. J Cardiopulm Rehabil Prev. 2011;31:11–24.
39. Montoye HJ, Lamphiear DE. Grip and arm strength in males and females, age 10 to 69. Res Q. 1977;48:109–120.
40. Kaelin ME, Swank AM, Adams KJ, Barnard KL, Berning JM, Green A. Cardiopulmonary responses, muscle soreness, and injury during the one repetition maximum assessment in pulmonary rehabilitation patients. J Cardiopulm Rehabil. 1999;19:366–372.
41. Jaric S. Muscle strength testing: use of normalisation for body size. Sports Med. 2002;32:615–631.
42. Fritz CO, Morris PE, Richler JJ. Effect size estimates: current use, calculations, and interpretation. J Exp Psychol Gen. 2012;141:2–18.
43. Jones PW, Quirk FH, Baveystock CM, Littlejohns P. A self-complete measure of health status for chronic airflow limitation. The St. George's Respiratory Questionnaire. Am Rev Respir Dis. 1992;145:1321–1327.
44. Kirkendall DT, Garrett WE Jr. The effects of aging and training on skeletal muscle. Am J Sports Med. 1998;26:598–602.
45. Hakkinen K, Kraemer WJ, Newton RU, Alen M. Changes in electromyographic activity, muscle fibre and force production characteristics during heavy resistance/power strength training in middle-aged and older men and women. Acta Physiol Scand. 2001;171:51–62.
46. Frontera WR, Suh D, Krivickas LS, Hughes VA, Goldstein R, Roubenoff R. Skeletal muscle fiber quality in older men and women. Am J Physiol Cell Physiol. 2000;279:C611–C618.
47. Gosker HR, Kubat B, Schaart G, van der Vusse GJ, Wouters EF, Schols AM. Myopathological features in skeletal muscle of patients with chronic obstructive pulmonary disease. Eur Respir J. 2003;22:280–285.
48. McHorney CA, Ware JE Jr, Lu JF, Sherbourne CD. The MOS 36-item Short-Form Health Survey (SF-36): III. Tests of data quality, scaling assumptions, and reliability across diverse patient groups. Med Care. 1994;32:40–66.
pulmonary disease; 6-Minute Walk Test; Short Form 36; strength; strength normalization
© 2014 Wolters Kluwer Health | Lippincott Williams & Wilkins
Highlight selected keywords in the article text.