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Not Just a Lung Disease: Peripheral Muscle Abnormalities in Cystic Fibrosis and the Role of Exercise to Address Them

Posted on: Friday, 31 March 2006, 06:00 CST

By Swisher, Anne K

ABSTRACT

Patients with cystic fibrosis (CF) typically have impaired exercise capacity, which was originally attributed to the progressive damage this disease causes to the lungs. However, there is now good evidence that reduced lung function alone does not completely explain the decrease in exercise capacity for most patients. This paper reviews the defects present in the peripheral muscle of patients with CF that might contribute to their impaired exercise capacity. The effects of a variety of exercise training protocols on muscle function are also reviewed. Emerging issues related to genotype, gender, and CF-related diabetes and the potential interactions with exercise capacity are discussed. The optimal type, intensity, duration, and frequency of exercise that optimizes outcomes for patients with CF remains to be discovered.

Key Words: cystic fibrosis, exercise, muscle

INTRODUCTION

Cystic fibrosis (CF) affects nearly 30,000 people in the United States.1 While originally described as a disease of the pancreas, it has been largely considered a lung disease, which presents with chronic, progressive, and irreversible obstructive and fibrotic components.1 However, it is clear that CF is a multisystemic disease, and that many aspects of this disease may impact exercise capacity.

Many patients with CF are limited in their ability to exercise and this has been found to impact quality of Iife23as well as life expectancy.4'5 Originally, it was assumed that the ventilatory and respiratory defects caused by this progressive lung disease were the limiting factor to exercise capacity. Although there is evidence that lung disease is the cause of premature death in patients with CF,1 muscle function may impact survival, independent of lung function. Nixon et al6 found that lung function, as measured by the 6-minute walk test, was the single strongest predictor of exercise capacity in patients with CF. However, this measure accounted for less than 50% of the variance between subjects, suggesting that additional factors contributed to this reduced exercise capacity. Other researchers demonstrated that anaerobic muscle performance was also poorly predicted by lung function.7-9

Moorecroft et al10 have demonstrated that leg fatigue, not dyspnea, is the limiting symptom to maximal cycle exercise in adults with mild to moderate lung disease. Even in subjects with severe lung disease, leg fatigue was equivalent to dyspnea as a limiting symptom.10 It has also been shown that patients who undergo lung transplantation to restore normal lung function retain deficits in exercise capacity and leg muscle strength.11 Thus, it appears that muscle mass and function are affected by CF, independent of lung function.

POTENTIAL CAUSES OF IMPAIRED EXERCISE CAPACITY RELATED TO PERIPHERAL MUSCLE

There are several reasons why the peripheral muscle function in patients with CF may be impaired. Patients with CF are known to be inactive, which may be caused by dyspnea or other problems. This inactivity certainly can affect muscle size, force output, and aerobic capacity. The pancreatic insufficiency present in most patients with CF may affect the availability of nutrients required to adequately maintain peripheral muscle. Severe caloric deprivation, which is sometimes found in patients with CF, may accelerate muscle catabolism. Inflammation associated with pulmonary exacerbations may also deleteriously affect muscle function. Complications of CF, such as CF-related diabetes, may affect muscle growth, maintenance, and function. Cystic fibrosis is a genetic disease that has multiple specific mutations and some of these mutations may adversely affect muscle. Finally, intrinsic metabolic abnormalities have been found in some patients with CF, which could affect exercise capacity. Each of these factors will be explored.

Inactivity

Although regular physical activity is recommended as part of the routine care for patients with CF, several studies have indicated that activity levels are lower for these patients than for their peers. Boas and colleagues12 discovered that parents of children with CF perceived fewer benefits of and more barriers to exercise than did parents of healthy children. Nixon et al13 found that children and adolescents with CF participated in less vigorous physical activities than their peers. This finding was confirmed in a group of adolescent males with CF by Hussey et al.14 There appears to be some variability in the activity levels of patients with CF, however. A study by Britto et al15 found no difference in activity level between adolescents with CF and their peers.

Activity level has not been found to significantly relate to the severity of lung disease,16,17 further suggesting that factors other than lung function are important in determining exercise capacity. Conversely, these findings may indicate that physical activity or exercise capacity could be improved in the absence of any changes in lung function.

Nutritional Factors

Adequate nutritional intake and absorption are a prerequisite to maintaining proper muscle function. Most patients with CF have pancreatic insufficiency that impairs their absorption of fat and fat-soluble vitamins.1 As a result, patients with CF often have low lean body mass (LBM) as well as smaller muscle mass. However, it is not clear if poor nutrition leads to specific muscle impairments.

There is ample evidence that impaired nutritional status leads to lower aerobic capacity (see work by Alan Coates, eg18,19). There is also evidence that LBM is the major determinant of anaerobic exercise capacity.7,20 Percentage of ideal body weight has also been found to correlate strongly with handgrip muscle strength.21 In addition, interventions that improve body weight and LBM for patients with CF, such as aggressive parenteral feeding or anabolic steroid injections, have been shown to improve maximal oxygen consumption22 as well as strength of peripheral23 and respiratory24 muscles. Certainly, it appears that for severely malnourished patients with CF, these interventions can improve peripheral muscle function. No studies to date, however, have added exercise training to these regimens to determine if an additive effect may occur.

Lower than normal LBM usually implies smaller muscle mass, with accompanying declines in muscle force, anaerobic, and aerobic performance. Lands and colleagues have demonstrated that lower levels of anaerobic8 and aerobic capacity9 disappear when the values are normalized to LBM. However, de Meer et al25 found that children with CF had lower work output normalize to fat-free mass, even in the absence of significant lung disease or malnourishment. These findings, although somewhat contradictory, suggest that intrinsic factors, rather than nutritional status alone, may affect muscle performance in patients with CF.

Alterations in Muscular Function and Metabolism

Several studies have indicated that although peripheral muscle mass is smaller in patients with CF than in healthy peers, the force production and metabolic function of the muscle is normal.8,9 However, recent studies have challenged these findings. Salvadurai et al26 compared muscle function in female track athletes with CF and their healthy teammates, and found that despite similar LBM, normal lung function and high levels of activity, the girls with CF had higher intramuscular pH during muscle contraction and had an impairment of the creatine phosphate energy system. These findings suggest that girls with CF were less able to use glycolytic sources of energy and that this contributed to their faster rate of muscular fatigue. A study by deMeer et al27 corroborate these findings of higher intramuscular pH during isometric finger flexion exercises, which corresponded to a 19% to 25% decreased efficiency in generating ATP from creatine phosphate. We recently reported that isometric leg muscle strength normalized to lean body mass was lower in children with CF than age-matched healthy peers, suggesting an intrinsic problem with force production.28

Findings by Braegger et al29 suggest that intramuscular stores of creatine may be limited in patients with CF. Following 12 weeks of oral supplementation of this compound, the patients in their study demonstrated improvements in maximal isometric strength of both peripheral and respiratory muscles. It is theorized that increasing phosphocreatine stores in the muscles of patients with CF could provide a reservoir of immediate energy substrates as well as providing a source of ATP to the CF transmembrane regulator (CFTR) protein, which functions suboptimally in CF.29

The ability of muscle to perform aerobic metabolism also appears to be impaired in patients with CF. Moser et al30 demonstrated that subjects with CF had lower peak oxygen consumption when normalized to muscle cross-sectional area than healthy age-matched controls. Similarly, Richards and colleagues31 demonstrated that the energy cost of physical activity was higher for adults with CF than their healthy peers. These findings suggest inefficiencies in producing muscular work utilizing aerobic pathways in patients with CF.

Other Potential Contributing Factors

The basic defect in CF is known to originate from genetic mutations. S\everal hundred specific mutations have been identified and in recent years, much effort has been put forth to associate clinical findings with specific mutations.32 One method has been to classify the mutations based on the errors in CFTR protein synthesis or function.32 One group of researchers discovered that patients who had mutations associated with more severe CFTR malfunction also had lower peak aerobic capacity.32 It is not yet clear if this is a causative factor or merely associated with poorer overall health.

Another important factor that may affect muscle in these patients is CF Related Diabetes (CFRD). Approximately 75% of patients with CF over the age of 25 will develop this condition as overall pancreatic function ceases.33 Insulin resistance is known to affect peripheral muscles in patients with diabetes mellitus, however, little is known about how CFRD affects skeletal muscle. Hardin et al33 studied a group of patients with impaired glucose tolerance, considered a precursor to CFRD. They found impaired translocation of the muscle glucose transporter (GLUT-4) to the surface of the cell. In the same subjects, they also found elevated levels of an inflammatory cytokine, TNFa, which was associated with the development of impaired glucose tolerance. As this cytokine has the potential to impair muscle growth and function, it is a potential cause of CF- related muscle dysfunction.

Many of these cytokines are released into the circulation in response to inflammation,34 which can decrease insulin-like growth factor 1 (IGF-1), a factor which influences lean body mass. Sermet- Gaudelus et al35 found that low IGF-1 levels were associated with both low LBM and impaired lung function in CF. Tirakitsoontorn and colleagues36 also found that children with CF had elevated levels of inflammatory cytokines and lower levels of IGF-1 both at rest and in response to a high-intensity exercise bout compared to healthy children. These alterations in anabolic and catabolic factors could provide a mechanism to link pulmonary exacerbation to poorer exercise capacity in patients with CF.

Skeletal muscle may also be impaired by systemic infection. One very common infection in patients with CF is pseudomonas aeruginosa.34 The toxins produced by this organism have been theorized to account for the cachexia seen in some patients who have positive sputum cultures.34 However, Divangahi et al34 demonstrated in a mouse model of CF that while colonization with pseudomonas aeruginosa led to diaphragm weakness, it did not impair peripheral muscle function.

The influence of medications used in CF on peripheral muscle cannot be excluded. Barry and Gallagher37 found that leg muscle strength was negatively correlated with average daily dose of corticosteroids taken by patients with CF, independent of BMI, nutritional status, or lung function. Other researchers have found that cyclosporin, a drug used to prevent rejection after lung transplantation, was selective in leading to leg muscle atrophy but not respiratory muscle weakness in patients with CF.11 In contrast, it has been shown that subjects taking high-dose ibuprofen had closer to normal inflammatory cytokine and growth factor responses to exercise.36 These findings are reminders that medications have multisystemic effects.

Finally, there may be other less recognized effects of CF that could influence muscle function. In an observational study by O'Riordan et al,38 62% of adults with CF tested had one or more abnormalities in peripheral nerve function. This intriguing finding may suggest that CF associated peripheral muscle weakness may result from suboptimal innervation.

EFFECTS OF EXERCISE TRAINING MODALITIES ON MUSCLE FUNCTION IN CF

Although maintaining or increasing activity levels is a universal recommendation for patients with CF,1 very few studies defining the optimal mode, intensity, frequency, and duration of exercise have been performed. Since patients with CF can be diagnosed at any age, from prenatally to mid-life, they vary widely in their motor development and potential to exercise. This variability makes designing exercise studies particularly challenging. In the following section, the findings related to exercise programs for children, adolescents, and adults with CF will be reviewed.

Aerobic Training Effects

Most studies of exercise have examined the effects of continuous, whole-body aerobic exercise. These types of exercises have been shown to blunt the decline in lung function over time. Schneiderman- Walker et al39 found that patients who participated in regular aerobic exercise over a 3-year period had a significantly smaller decline in lung function compared to those who did not exercise. Adults with CF who participated in aerobic exercise improved their peak oxygen consumption, despite declines in lung function.40 Following a 6-month home cycling program, children with CF improved their peak oxygen consumption normalized to LBM,41 which implies improvement in the efficiency of muscular oxidative metabolism. These findings suggest that exercise can improve muscle function independent of lung disease.

Anaerobic Training Effects

Since many patients with CF are children, there is a need to match exercise mode with the child's developmental abilities. Children have been observed to perform activity in short, intense bursts rather than moderate intensity long bouts.42 Klinj et al42 used this finding to design an anaerobic exercise program for children aged 9 to 17 with CF. Children with mild lung disease were randomized to a training or control group, who performed their normal daily activities. The training consisted of activities lasting 20 to 30 seconds each for 45 minutes twice weekly for 12 weeks. Following the training, improvements were seen in anaerobic peak and mean power, peak oxygen consumption, peak cycle workload, and quality of life. Peak oxygen consumption declined in the control group over the course of the study. Similarly, a home exercise program of trampoline jumping, lasting 2 to 6 minutes performed 3 times per day, was found to improve maximal oxygen consumption in 10- to 13-year-old children with CF.43 Holzer and colleagues44 prescribed a daily regimen of calisthenics for children aged 8 to 14 with CF to be performed at home for 3 months. This program also led to modest improvements in maximal oxygen consumption. These findings support the use of age-appropriate exercise training for children with CF.

Recently, Gruber et al45 have found that children with CF have lower scores on standardized motor performance tasks, such as ball bouncing and standing vertical jumping than their healthy peers. They have also demonstrated improvements in these skills following a 6-week intensive sports and exercise program.46 From these findings it is unclear if children with CF might have neuromotor problems or if a lack of regular physical activity/sports participation accounts for their poor motor performance.

Resistance Training Effects

One of the rationales for resistance training in CF is to provide a muscle stimulus that is not limited by ventilatory capacity. A pioneering study in this area was performed in 1987 by Strauss et al.47 Subjects with CF over the age of 16 performed resistance training using a circuit of machines 3 times per week for 6 months. Although there was no control group for comparison, the training led to increases in body weight and strength, as well as decreases in residual volume on pulmonary function testing. This study paved the way for more recent examinations of resistance training in CF.

Selvaduarai et al48 compared the effects of resistance training to those of aerobic training during a 3-week hospitalization for pulmonary exacerbations. Subjects were randomly assigned to either a resistance or aerobic exercise group and exercised 30 minutes per day, 5 times per week at 70% of peak heart rate (aerobic group) or 70% of 1-RM (resistance group). Aerobic training led to improvements in peak oxygen consumption, voluntary activity levels, and quality of life, while resistance training improved muscle strength, fat- free mass, and lung function. Since all of these effects could improve health in CF, the authors recommended using both exercise modalities.

Recently, a large, controlled trial of resistance training in children aged 8 to 18 years with CF was performed by Orenstein et al.49 Subjects were randomized to perform exercise on either a stepper or an upper body resistance device 3 times weekly for 1 year. The study was designed to minimize crossover effects from exercise modality; however, the authors found improvements in peak work capacity and strength in both groups. These findings suggest that exercise training may have broad effects on muscle function in CF.

EMERGING ISSUES/UNANSWERED QUESTIONS

From this review of the literature, it is evident that the influence of CF on peripheral muscle cannot be ignored. There are multiple effects and influences on peripheral muscle size, strength, and aerobic capacity that have yet to be fully explored. Other issues are emerging that may make studying peripheral muscle function in CF even more complicated. For example, it appears that females may differ in their intrinsic muscle response to CF from their male counterparts.50-52 It is well recognized that life expectancy is lower for women than men with CF, and that LBM is a predictor of survival.53 Therefore, delineating any mechanisms within peripheral muscle that may affect LBM and survival in women with CF is particularly important.

Physical activity level has been found to be lower in adolescent girls than boys with CF.51 In addition, these researchers found that those females with the lowest levels of activity had the greatest declines in lung function. No such relationship between habitual activity and lung function was observed in adolescent boys.54 Females have also been found to have higher \resting energy expenditure than their peers without CF,53 potentially further exacerbating low LBM.

Sahlberg et al50 found different patterns of weakness between men and women with CF, when compared to their gender-matched peers. The women demonstrated weakness in handgrip and knee bending, while the men were weaker in sit-ups and knee extension. Females with CF- Related Diabetes had worse lung function than male subjects with the same condition, suggesting a gender-specific interaction of glucose handling and lung function.52 In addition, lung function values have been found to vary in relation to the menstrual cycle in women with CF,55 suggesting an interaction of female hormones with lung obstruction.

Recently, urinary incontinence has been recognized as a significant problem for women with CF, with 41% of patients surveyed reporting this condition.56 Although hypothesized to result from excessive coughing, this condition has been shown to be partially remediable with pelvic floor muscle exercises.57

CONCLUSIONS

Therefore, it is clear that physical therapists need to consider peripheral muscle function in relation to the unique manifestations of CF. Knowledge of genetics, development, biomechanics, and exercise training are all important to provide the optimal assessment and intervention to improve function and quality of life in these patients. Much more research is needed to elucidate the mechanisms and potential means to remediate assaults on the muscle in patients with CF, from cellular and animal models to clinical applications.

REFERENCES

1. Orenstein D, Rosenstein B, Stern R. Cystic Fibrosis: Medical Care. Philadelphia, Pa: Lippincott Williams & Wilkins; 2000.

2. Orenstein D, Nixon P, Ross E, Kaplan R. The quality of well- being in cystic fibrosis. Chest. 1989;95:344-347.

3. de Jong W, Kaptein A, van der Schans C, et al. Quality of life in patients with cystic fibrosis. Pediatr Pulmonol. 1997;23:95-100.

4. Nixon P, Orenstein D, Kelsey S, Doershuk C. The prognostic value of exercise testing in patients with cystic fibrosis. N Engl J Med. 1992;327:1785-1788.

5. Moorcroft A, Dodd M, Webb A. Exercise testing and prognosis in adult cystic fibrosis. Thorax. 1997;52:291-293.

6. Nixon P, Joswiak M, Fricker F. A six-minute walk test for assessing exercise tolerance in severely ill children. J Pediatrics. 1996;129:362-366.

7. Boas S, Joswiak M, Nixon P, Fulton J, Orenstein D. Factors limiting anaerobic performance in adolescent males with cystic fibrosis. Med Sci Sports Exerc. 1996;28:291-298.

8. Lands L, Heigenhauser G, Jones N. Respiratory and peripheral muscle function in cystic fibrosis. Am Rev Respir Dis. 1993;147:865- 869.

9. Lands L, Heigenhauser G, Jones N. Analysis of factors limiting maximal exercise performance in cystic fibrosis. CHn Sci. 1992;83:391-397.

10. Moorcroft A, Dodd M, Morris J, Webb A. Symptoms, lactate and exercise limitation at peak cycle ergometry in adults with cystic fibrosis. Eur Respir J. 2005;25:1050-1056.

11. Pinet C, Scillia P, Cassart M, et al. Preferential reduction of quadriceps over respiratory muscle strength and bulk after lung transplantation for cystic fibrosis. Thorax. 2004;59:783-789.

12. Boas S, Danduran M, McColley S. Parental attitudes about exercise regarding their children with cystic fibrosis. Int J Sports Med. 1999;20:334-338.

13. Nixon P, Orenstein D, Kelsey S. Habitual physical activity in children and adolescents with cystic fibrosis. Med Sci Sports Exerc. 2001;33:30-35.

14. Hussey J, Gormley J, Leen G, Greally P. Peripheral muscle strength in young males with cystic fibrosis. J Cyst Fibros. 2002;1:116-121.

15. Britto M, Garret J, Konrad T, Majure J, Leigh M. Comparison of physical activity in adolescents with cystic fibrosis versus age- matched controls. Ped Pulmonol. 2000;30:86-91.

16. Boucher G, Lands L, Hay J, Hornby L. Activity levels and the relationship to lung function and nutritional status in children with cystic fibrosis. Am J Phys Med Rehabil. 1997;76:311-315.

17. Loutzenhiser J, Clark R. Physical activity and exercise in children with cystic fibrosis. J Pediatr Nurs. 1993;8:112-119.

18. Coates A, Boyce P, Muller D, Mearns M, Godfrey S. The role of nutritional status, airway obstruction, hypoxia, and abnormalities in serum lipid composition in limiting exercise tolerance in children with cystic fibrosis. Acta Paediatr Scand. 1980;69:353- 358.

19. Marcotte J, Canny G, Grisdale R, et al. Effects of nutritional status on exercise performance in advanced cystic fibrosis. Chest. 1986;90:375-379.

20. Shah A, Gozal D, Keens T. Determinates of aerobic and anaerobic exercise performance in cystic fibrosis. Am J Respir Crit Care Med. 1998;157:1145-1150.

21. Ionescu A, Chatham k, Davies C, Nixon L, Enright S, Shale D. lnspiratory muscle function and body composition in cystic fibrosis. Am J Respir Crit Care Med. 1998;158:1271-1276.

22. Hutler M, Schnabel D, Staab D, et al. Effect of growth hormone on exercise tolerance in children with cystic fibrosis. Med Sd Sports Exerc. 2002;34:567-572.

23. Hardin D, Stratton R, Kramer J, de Ia Rocha R, Govaerts K, Wilson D. Growth hormone improves weight velocity and height velocity in prepubertal children with cystic fibrosis. Norm Metab Res. 1998;30:636-641.

24. Hardin D, Ellis K, Dyson M, Rice J, McConnell R, Seilheimer D. Growth hormone improves clinical status in prepubertal children with cystic fibrosis: results of a randomized controlled trial. J Pediatr. 2001;139:636-642.

25. de Meer K, Gulmans V, van der Laag J. Peripheral muscle weakness and exercise capacity in children with cystic fibrosis. Am J Respir Crit Care Med. 1999;159:748-754.

26. Selvadurai H, Allen J, Sachinwalla T, Macauley J, Blimkie C, Van Asperen P. Muscle function and resting energy expenditure in female athletes with cystic fibrosis. Am J Respir Crit Care Med. 2003;168:1476-1480.

27. deMeer K, Jeneson J, Gulmans V, van der Laag J, Berger R. Efficiency of oxidative work performance of skeletal muscle in patients with cystic fibrosis. Thorax. 1995;50:980-983.

28. Swisher A, Moffett K, Baer L, Yeater R. Effect of body fat, leg muscle strength and lung function on 6-minute walk in children with cystic fibrosis. Cardiopulm Phys Ther. 2000;11:155.

29. Braegger C, Schlattner U, Wallimann T, et al. Effects of creatine supplementation in cystic fibrosis: results of a pilot study. J Cyst Fibros. 2003;2:177-182.

30. Moser C, Tirakitsoontorn P, Nussbaum E, Newcomb R, Cooper D. Muscle size and cardiorespiratory response to exercise in cystic fibrosis. Am J Respir Crit Care Med. 2000;162:1823-1827.

31. Richards M, Davies P, Bell S. Energy cost of physical activity in cystic fibrosis. European Am J Clin Nutr. 2001;55:690- 697.

32. Selvadurai H, McKay K, Blimkie C, Cooper P, Mellis C. The relationship between genotype and exercise tolerance in children with cystic fibrosis. Am J Respir Crit Care Med. 2002;165:762-765.

33. Hardin D, LeBlanc A, Marshall G, Seilheimer D. Mechanisms of insulin resistance in cystic fibrosis. Am J Physiol Endocrinol Metab. 2001 ;281:E1022-E1028.

34. Divangahi M, Matecki S, Dudley R, et al. Preferential diaphragmatic weakness during sustained pseudomonas aeruginosa lung infection. Am J Respir Crit Care Med. 2004;169:679-686.

35. Sermet-Gaudelus I, Souberbielle J, Azhar I, et al. Insulin- like growth factor I correlates with lean body mass in cystic fibrosis patients. Arch Dis Child. 2003;88:956-961.

36. Tirakitsoontorn P, Nussbaum E, Moser C, Hill M, Cooper D. Fitness, acute exercise, and anabolic and catabolic mediators in cystic fibrosis. Am J Respir Crit Care Med. 2001 ;164:1432-1437.

37. Barry S, Gallagher C. Corticosteriods and skeletal muscle function in cystic fibrosis. J Appl Physiol. 2003;95:1379-1384.

38. O'Riordan J, Hayes J, Fitzgerald M, Redmond J. Peripheral nerve dysfunction in adults patients with cystic fibrosis. Ir J Med Sci. 1995;164:207-208.

39. Schneiderman-Walker J, Pollock S, Corey M, et al. A randomized controlled trial of a 3-year home exercise program in cystic fibrosis. J Pediatr. 2000;136:304-310.

40. Moorcroft A, Dodd M, Webb A. Long-term change in exercise capacity, body mass, and pulmonary function in adults with cystic fibrosis. Chest. 1997;111:338-343.

41. Gulmans V, de Meer K, Brackel H, Faber J, Berger R, Helders P. Outpatient exercise training in children with cystic fibrosis: Physiological effects, perceived competence, and acceptability. Pediatr Pulmonol. 1999;28:39-46.

42. Klijn E, Oudshoorn A, van der Ent C, van der Net J, Kimpen J, Helders P. Effects of anaerobic training in children with cystic fibrosis: A randomized controlled study. Chest. 2004;125:1299-1305.

43. Stanghelle J, Hjeltnes N, Bangstad H, Michalsen H. Effect of daily short bouts of trampoline exercise during 8 weeks on the pulmonary function and the maixmal oxygen uptake of children with cystic fibrosis. Int J Sports Med. 1988;9:32-6 Supplement.

44. Holzer F, Schnall R, Landau L. The effect of a home exercise programme in children with cystic fibrosis and asthma. Aust Paedriatr J. 1984;20:297-302.

45. Gruber W, Braumann M, Paul K, Huels G. Is motor performance reduced in CF-patients? Ped Pulmonol. 2005;[Suppl 28]:320.

46. Gruber W, Braumann M, Paul K, Huels G. Effects of an exercise program on motor performance in CFpatients. Ped Pulmonol. 2005;[Suppl 28]:320-321.

47. Strauss G, Osher A, Chun-l W, et al. Variable weight training in Cystic Fibrosis. Chest. 1987;92:273-276.

48. Selvadurai H, Blimkie C, Meyers N, Mellis C, Cooper P, Van Asperen P. Randomized controlled study of inhospital exercise training programs in children with cystic fibrosis. Pediatr Pulmonol. 2002;33:194-200.

49. Orenstein D, Hovell M, Mulvihill M, et al. Strength vs aerobic training in children with cystic fibrosis. Chest. 2004;126:1204-1214.

50. Sahlberg M, Svantesson U, Magnusson TE, Strandvik B. Muscular strength and function in patients with cystic fibrosis. Chest. 2005;127:1587-1592.

51. Selvadurai H, Blimkie C, Co\oper P, Mellis C, Van Asperen P. Gender differences in habitual activity in children with cystic fibrosis. Arch Dis Child. 2004;89:928-933.

52. Sims E, Green M, Mehta A. Decreased lung function in female but not male subjects wtih established cystic fibrosis-related diabetes. Diabetes Care. 2005;28:1581-1587.

53. Stallings V, Tomezsko J, Schall J, et al. Adolescent development and energy expenditure in females with cystic fibrosis. Clin Nutr. 2005;24:737-745.

54. Schneiderman-Walker J, Wilkes D, Strug L, et al. Sex differences in habitual physical activity and lung function decline in children with cystic fibrosis. J Pediatr. 2005;147:321-326.

55. Johannesson M, Ludviksdottir D, Janson C. Lung function changes in relation to menstrual cycle in females with cystic fibrosis. Respir Med. 2000;94:1043-1046.

56. Cornacchia M, Zenorini A, Perobelli S, Zanolla L, Mastella G, Braggion C. Prevalence of urinary incontinence in women with cystic fibrosis. BJU International 2001;88:44-8.

57. McVean R, Orr A, Webb A, et al. Treatment of urinary incontinence in cystic fibrosis. J Cyst Fibros. 2003;2:171-176.

Anne K. Swisher PT, PhD, CCS

Division of Physical Therapy, West Virginia University, Morgantown, WV

Address correspondence to: Anne K. Swisher, PT, PhD, CCS, Division of Physical Therapy, West Virginia University, Morgantown, WV 26506-9226 (aswisher@hsc.wvu.edu).

Copyright Cardiopulmonary Physical Therapy Journal Mar 2006

Source: Cardiopulmonary Physical Therapy Journal

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