Journal of Applied Physiology Fuel your research with LabChart
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Appl Physiol 95: 1379-1384, 2003. First published June 13, 2003; doi:10.1152/japplphysiol.00506.2002
8750-7587/03 $5.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
95/4/1379    most recent
00506.2002v2
00506.2002v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (6)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Barry, S. C.
Right arrow Articles by Gallagher, C. G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Barry, S. C.
Right arrow Articles by Gallagher, C. G.

Corticosteroids and skeletal muscle function in cystic fibrosis

Sinead C. Barry and Charles G. Gallagher

Department of Respiratory Medicine and the National Referral Centre for Adult Cystic Fibrosis, St. Vincent's University Hospital, Dublin 4, Ireland

Submitted 11 June 2002 ; accepted in final form 30 May 2003


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 REFERENCES
 
Patients with cystic fibrosis (CF) have reduced peripheral muscle strength. We tested the hypothesis that steroid treatment contributes to muscle weakness in adults with CF. Twenty-three stable CF patients were studied. Measurements included knee extensor (KE), knee flexor (KF), elbow flexor (EF), handgrip (HG), expiratory (PEmax), and inspiratory (PImax) muscle strengths. Spirometry, body mass index (BMI), and days spent in hospital over the preceding 12 mo (DH) were also measured. Average daily dose of prednisolone over the preceding 12 mo (ADD) was 5.1 mg/day. Pearson's correlation analysis revealed that ADD correlated significantly with skeletal muscle strengths (KF%, r = -0.63, P < 0.01) with the exception of HG%. These findings are independent of age, BMI, pulmonary function, and DH. Multiple-regression analysis revealed that ADD was the most significant predictor of all measures of skeletal muscle function except HG%. It was independently responsible for 54% of the variance in PImax%, for 46% of the variance in PEmax%, for 45% of the variance in KE%, for 39% of the variance in KF%, and for 41% of the variance in EF%. Concomitant medications (e.g., theophylline) were shown to have no causative effect. Corticosteroids contribute to the skeletal muscle weakness seen in CF patients. The correlation of proximal muscle strength, but not HG strength, with steroid dosage further supports a cause-effect relationship.

steroids; peripheral muscle strength; respiratory muscle strength

MANY PATIENTS WITH CYSTIC FIBROSIS (CF) have weak peripheral (9, 24) and, in some cases, respiratory muscles (23, 34). There is evidence that muscle weakness in CF may have major clinical implications (9, 16). Generalized muscle weakness may occur as a result of malnutrition (2, 14), disturbance in serum electrolytes (3), hypoxia (7, 8), and disuse (4, 15). Respiratory muscle weakness is often related to hyperinflation and poor nutrition (23, 34); however, preservation of respiratory strength has also been demonstrated in some CF patients despite the presence of low body weight and significant hyperinflation. Recent work by Decramer et al. (12) in chronic obstructive pulmonary disease has demonstrated a significant relationship between steroid usage and both peripheral and respiratory muscle strength. The effect of steroid use on muscle strength in CF has not been examined to date. Despite the well-known negative side effects associated with chronic corticosteroid use, steroids still form an important part of the management of many patients with CF (5, 22, 33, 35).

We hypothesized that the muscle weakness seen in CF may be related in part to steroid use. We examined the relationship between skeletal muscle strength and steroid dosage (average daily dose in the previous year) in adults with CF who were clinically stable. We wanted to minimize the possibility that factors other than steroid usage might affect any relation between steroid dosage and muscle weakness. Therefore, we also examined the relation between skeletal muscle strength (dependent variable) and spirometry, nutritional status, and number of days spent in hospital over the previous year. Steroid myopathy preferentially affects proximal muscles and spares distal muscle groups. Therefore, we examined the relation between steroid dosage and strength of distal (e.g., handgrip) muscles as well as that between steroid dosage and strength of proximal muscles (e.g., knee flexor and extensor). We reasoned that if steroids contribute to muscle weakness in CF, proximal strength should correlate with steroid dosage but peripheral strength should not. Because acute infection or acute respiratory exacerbation may influence muscle function, patients were studied at least 1 mo after any acute exacerbation.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 DISCLOSURES
 REFERENCES
 
Twenty-three patients (13 male, 10 female) were recruited from the outpatients department at the National Referral Centre for Adult Cystic Fibrosis at St. Vincent's University Hospital, Dublin. Diagnosis of CF for each subject was based on clinical features, abnormal sweat test (sweat chloride > 60 mmol/l), and genotyping. All subjects were clinically stable for 1 mo before taking part in the study.

To assess the effects of corticosteroids on skeletal muscle function we measured inspiratory (PImax), expiratory (PEmax), knee extensor (KE), knee flexor (KF), elbow flexor (EF), and handgrip (HG) strengths. Pulmonary function tests were performed, and total steroid dose over the previous 12 mo was calculated in milligrams per day. All tests were performed during a single visit to the research laboratory. Because of both ethical and logistical difficulties, it was not possible to include a control group.

The local Ethics Committee approved the study. All patients gave informed consent to the procedures.

Corticosteroid treatment. The average daily dose (ADD) of corticosteroids taken during the previous 12 mo was calculated. No subject in the study had taken fluorinated steroids at any time in their past. Corticosteroids included oral prednisolone and intravenous hydrocortisone. Calculation of the ADD involved examination of patient files, patient interviews, and examination of each patient's local pharmacy notes over the preceding 12 mo. The Irish Health Care system provides free medication to all patients with CF, which is paid retrospectively by the government to each pharmacy. As a result, accurate records are available from the local pharmacy on all medications received by each patient. All doses were converted into prednisolone equivalent and expressed in milligrams per day. We also examined the effects of concomitant therapies (theophylline, antibiotics, etc.) on skeletal muscle function.

Concurrent medication. All patients involved in the study continued on their maintenance medication at the time of testing. The following is an account of all medications used by the study population before and during the study: 20 subjects used colomycin nebulized, 1 subject used nebulized tobramycin, 2 subjects used nebulized gentamicin, 18 used pancreatin with meals, 8 used flucloxacillin orally, 4 used cefaclor orally, 1 subject used cefuroxime orally, 1 subject took co-amoxiclav orally, 7 used omeprazole, 13 subjects used oral theophylline, 7 used dornase alpha nebulized, 4 subjects took ursodeoxycholic acid, all subjects used vitamin supplements, 15 subjects used salbutamol nebulized, 1 subject used budesonide nebulized, 21 subjects used a salbutamol inhaler, 4 subjects used ipratropium bromide and salbutamol in a combination inhaler, 11 subjects used a beclomethasone diproprionate inhaler, 1 subject used an ipratropium bromide inhaler, and 6 subjects used a fluticasone propionate inhaler.

Pulmonary function testing. Forced vital capacity and forced expiratory volume in 1 s (FEV1) were measured by use of a spirometer (Vitalograph Compact 11, Fannin Ireland) according to the recommendations of the American Thoracic Society (32), and predicted normal values (31) were used to calculate the percentage predicted values.

Respiratory muscle strength. Mouth pressures during PImax and PEmax at functional residual capacity were measured as indexes of inspiratory and expiratory muscle strength, respectively (25, 36). Pressure was measured with a transducer (P.K. Morgan Pmax), which was calibrated with a manometer before each test. Identical methods to those used by McParland et al. (26) were employed.

Peripheral muscle strength. Static contractions were measured by using the Compufet system (Biometrics, Kabelstraat, The Netherlands), which was attached to the rigid arm of the quadriceps bench. Each subject was instructed to push as hard as possible against the rigid arm of the quadriceps bench and to sustain the contraction for 8 s as required by the Compufet software. Visual feedback was given representing contraction time during each voluntary effort. The maximum voluntary contractions were recorded as the best of three contractions for each leg and compared with predicted values (29a). Two practice efforts were performed, and this was followed by sufficient tests until three were achieved within 10% of each other. Bilateral limbs were assessed, and the strength of the stronger limb was used for analysis.

To assess isometric KE, KF, and EF, identical positions to those previously described were employed (29a). An adjustable strap was used to secure the pelvis for both KE and KF and to secure the trunk for EF testing. HG strength was assessed by using the same equipment and methods as previously described (26).

Data analysis. Percentage predicted values for isometric peripheral muscle strengths were calculated (29a). Predictive equations for analysis of respiratory muscle strengths are those used by Hamilton et al. (18).

Statistical analysis. Data are reported as means ± SD. Correlation among variables was assessed by using Pearson's correlation coefficient. Stepwise multiple-regression analysis was performed for muscle strengths; variables used in the model included age, gender, body mass index (BMI), FEV1%, and days spent in hospital over the preceding 12 mo. Only variables significantly contributing to the model were retained in the final analysis, and the limits of significance were set at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 DISCLOSURES
 REFERENCES
 
Patient characteristics. Patient characteristics are summarized in Table 1. The population was quite diverse with regard to disease state. Nutritional status ranged from significantly malnourished (BMI = 16.4) to normal (BMI = 25.5), whereas airflow obstruction ranged from normal (FEV1 = 108% predicted) to severely obstructed (FEV1 = 25% predicted). Inspiratory muscle strength ranged from 40 to 175% predicted. Expiratory muscle strength also demonstrated a similar spread, with values ranging from 31 to 166% predicted (Table 2). Limb muscle strength also demonstrated a wide variation from significantly weak to normal levels (EF% = 24-105%), but mean strength was reduced for all limb muscles tested.


View this table:
[in this window]
[in a new window]
  		Table 1. Patient characteristics

 

View this table:
[in this window]
[in a new window]
  		Table 2. Peripheral muscle strengths expressed as percentage predicted

 

Prednisolone ADD was 5.1 mg/day. No subject was treated with corticosteroids for allergic bronchopulmonary aspergillosis.

Relationship between limb muscle and respiratory muscle strengths. Respiratory muscle strength and limb muscle strength correlated significantly with each other (P < 0.05); PImax% correlated with KE% (r = 0.76), KF% (r = 0.64), EK% (r = 0.87), HG% (r = 0.47), and PEmax% (r = 0.84). PEmax% was also significantly correlated with limb muscle strength, KE% (r = 0.73), KF% (r = 0.62), EK% (r = 0.83), and HG% (r = 0.51).

Relationship between muscle strength and steroid treatment. Using Pearson's correlation analysis (Table 3; Fig. 1), we assessed the relationship between limb muscle and respiratory muscle strength and steroid dose and found a significant relationship between ADD and KE%, KF%, EF%, PImax%, and PEmax%.


View this table:
[in this window]
[in a new window]
  		Table 3. Correlation analysis between muscle forces and BMI, FEV1%, age, and DH

 


View larger version (11K):
[in this window]
[in a new window]
  		Fig. 1. Correlation of percentage predicted knee extensor strength with average daily dose of corticosteroid over the previous 12 mo.

 

Relationship between muscle strength and BMI, FEV1%, age, and DH. The relationships between muscle forces and BMI, FEV1%, age, and days spent in hospital (DH) were tested by using Pearson's correlation analysis (Table 3; Fig. 2). BMI was chosen as a marker of nutritional status in CF. No significant correlations were identified between age and any of the variables of muscle function nor between DH and any of the variables of muscle function. Significant positive correlations were identified between BMI and both PImax% and PEmax%. Significant positive correlations were also found between FEV1% and KE%, PImax%, and PEmax%. Significant negative correlations were identified between ADD and all measures of muscle strength except HG%. The correlations found between ADD and KE% and ADD and respiratory muscle strength (PImax% and PEmax%) were more significant than those seen between FEV1% and KE% and FEV1% and respiratory muscle strength.



View larger version (10K):
[in this window]
[in a new window]
  		Fig. 2. Correlation of percentage predicted knee extensor strength with days spent in hospital over the previous 12 mo.

 

Determinants of muscle forces using stepwise multiple-regression analysis. Average daily dose predicted 45% of the variance in KE% with gender being responsible for 24%. (Table 4) Thirty-nine percent of the variance in KF% was due to ADD. Forty-one percent of the variance in EF% was related to ADD, with gender being responsible for a further 36%. HG% had no significant predictors. ADD predicted 54% of the variance in PImax%, with 9% being due to BMI and 13% being due to gender. ADD also explained 46% of the variance in PEmax%, with 22% being related to gender. For all muscle groups tested except HG%, ADD of corticosteroids explained the largest proportion of muscle weakness seen (Table 4). None of the concurrent medications contributed significantly to the regression model. Figure 3 illustrates the lack of correlation between theophylline dose expressed in milligrams per day and KE%.


View this table:
[in this window]
[in a new window]
  		Table 4. Stepwise multiple-regression analysis

 


View larger version (11K):
[in this window]
[in a new window]
  		Fig. 3. Correlation of percentage predicted knee extensor strength with theophylline dose over the previous 12 mo.

 


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
DISCLOSURES
 REFERENCES
 
The major new findings of this work are that 1) corticosteroid treatment independently correlates with limb and respiratory muscle strength in patients with CF; 2) the effects of corticosteroid treatment on skeletal muscle function are independent of airflow obstruction, nutrition, and DH; and 3) this correlation is seen for proximal muscles but not for the distal HG muscles. These results are in support of the hypothesis that treatments with corticosteroids have a negative effect on skeletal muscle strength in CF patients.

Possible limitations of this study are the following: 1) We used an indirect measurement of nutritional status, and no direct measure of lean body mass was performed. However, BMI has been shown to be a valuable measure of nutritional status in CF and to relate to exercise capacity (28), bone mineral density (17), and prognosis (20). 2) Our measures of limb muscle strength and respiratory muscle strength are effort dependent; however, each subject was tested repeatedly by the same investigator, making it difficult to perform repeated submaximal efforts. 3) We did not measure total body muscle mass, and as a result it is difficult to say conclusively whether we are seeing true myopathy, in which strength would be reduced at a disproportionate rate to muscle mass. 4) DH provides a useful marker of periods of extreme disuse; however, activity of daily living may contribute to disuse atrophy and has not been accounted for here.

A number of authors have looked at the presence of limb muscle weakness in CF patients. Lands et al. (24) demonstrated that leg strength was reduced in CF patients compared with controls and that strength was strongly related to body mass (r = 0.816, P < 0.01). Mier et al. (27) found that quadriceps strength was on average 68% predicted in their CF group. More recently, de Meer et al. (9) demonstrated that limb muscle force was reduced in CF children even in the absence of reduced pulmonary or nutritional status, whereas Elkin et al. (16) have demonstrated that both limb muscle strength and mass were reduced in their CF group compared with controls. The causes of muscle weakness in CF remain unclear; some authors suggest impairment in the quality of the muscle (9-11, 29), whereas others suggest that the differences in strength seen between CF patients and controls are related to body mass (16, 19, 24). No conclusive data are available at this time.

Studies of respiratory muscle function in CF are difficult to compare because of differences in the age of subjects studied, the methods used, and the indexes of muscle function. The tendency throughout the literature has been for inspiratory strength to be preserved in CF (20, 23, 24, 27, 30), and this is in agreement with our findings. Significant negative correlations were found between PImax%, PEmax%, and ADD (Table 3). Our results demonstrate a wide range of values for PImax% (39.9-175%) with an equally wide range seen for PEmax% (30.6-166.1%). We have shown that some patients have preserved respiratory muscle strength, whereas others have markedly reduced strength and still others have supernormal levels of respiratory muscle strength. The mechanisms responsible for these variations in strength are not clear. Factors such as reduced nutritional status, hypoxia, acidosis, electrolyte disturbances, and disuse may contribute to reduced strength, whereas chronic cough and increased work of breathing have been implicated in both preserved and increased respiratory muscle strength. It is likely that a number of factors simultaneously cause respiratory muscle variation. We have demonstrated a relationship between the widely varying respiratory strength seen in adults with CF and ADD, which have not been described previously.

There are many possible factors that can affect skeletal muscle function in CF. Weight loss, protein calorie insufficiency, abnormal ion transport, inflammation, sepsis, electrolyte disturbances, hypoxia, and corticosteroid usage all have myopathic potential. The purpose of this study was to assess the independent effects of corticosteroid therapy on limb muscle strength and respiratory muscle strength in a group of stable CF patients. It is known that myopathy may occur with virtually all steroids in common use (1, 13, 37). There are no previous data, to our knowledge, on the effects of treatment with corticosteroids on muscle strength in CF patients.

Like others, we have demonstrated the presence of limb muscle weakness in adults with CF (9, 16, 24, 27) and the preservation, on average, of respiratory muscle strength (21, 24, 30). We have shown that ADD of corticosteroids is significantly correlated with all measures of skeletal muscle function except HG%. We were unable to identify significant predictors of HG strength. HG was on average reduced at 67.9% predicted. Possible mechanisms of reduced HG strength are similar to those already described for generalized skeletal myopathy, with the exception of corticosteroid usage. These results are in agreement with our biological knowledge of steroid myopathy and its preference for proximal muscle atrophy, hence the lack of correlation with HG%.

Stepwise multiple-regression analysis revealed that ADD was responsible for the largest proportion of the muscle weakness seen in our CF patients, to a greater extent than nutritional status, pulmonary function, and DH. Single-regression analysis revealed a lack of correlation between peripheral muscle forces and FEV1%, BMI, age, and DH. The only significant correlation found was between KE% and FEV1%; however, this correlation was less than that seen for KE% and ADD. These findings suggest that treatment with corticosteroids contributes to muscle weakness in CF patients.

Nutritional status, disuse, and severity of disease all potentially affect muscle strengths in CF. To control for these potential cofactors, we assessed the effects of FEV1%, BMI, age, gender, and DH on strength of peripheral and respiratory muscles using both single- and multiple-regression analysis. Single-regression analysis revealed a significant relationship between KE% and FEV1%, which was less significant than between KE% and ADD. Stepwise multiple-regression analysis revealed that ADD was the most significant predictor of KE%, KF%, EF%, PImax%, and PEmax% with no significant effect on HG%. These results are in agreement with our hypothesis, i.e., that corticosteroids contribute to skeletal muscle weakness in CF.

In conclusion, this study demonstrates a significant association between corticosteroid dosage and skeletal muscle weakness in adults with CF. This correlation occurs at doses used in clinical practice. The correlation with steroid dosage is much greater than that attributable to age, sex, lung function, or overall nutritional status. These results have significant clinical implications.


   DISCLOSURES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
REFERENCES
 
We thank the Cystic Fibrosis Research Trust, the Cystic Fibrosis Association of Ireland, the Health Research Board of Ireland, and the National Rehabilitation Board of Ireland for their support. We also thank the Cystic Fibrosis patients at St. Vincent's University Hospital for their continued support.


   FOOTNOTES
 

Address for reprint requests and other correspondence: C. G. Gallagher, Dept. of Respiratory Medicine, St. Vincent's Univ. Hospital, Dublin 4, Ireland (E-mail: v.hearn{at}st-vincents.ie).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 REFERENCES
 

  1. Afifi AK, Bergman RA, and Harvey JC. Steroid myopathy. Clinical, histologic and cytologic observations. Johns Hopkins Med J 123: 158-173, 1968.[ISI][Medline]
  2. Arora NS and Rochester DF. Respiratory muscle strength and maximal voluntary ventilation in undernourished patients. Am Rev Respir Dis 126: 5-8, 1982.[ISI][Medline]
  3. Aubier M, Murciano D, Lecocguic Y, Viires N, Jacquens Y, Squara P, and Pariente R. Effect of hypophosphatemia on diaphragmatic contractility in patients with acute respiratory failure. N Engl J Med 313: 420-424, 1985.[Abstract]
  4. Booth FW and Gollnick PD. Effects of disuse on the structure and function of skeletal muscle. Med Sci Sports Exerc 15: 415-420, 1983.[ISI][Medline]
  5. Cheng K, Ashby D, and Smyth R. Oral steroids for cystic fibrosis. Cochrane Database Syst Rev 2: 2000.
  6. Coates AL, Boyce P, Muller D, Mearns M, and 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. Bull Eur Physiopath Respir 15: 341-342, 1979.[ISI][Medline]
  7. Connett RJ, Honig CR, Gayeski TE, and Brooks GA. Defining hypoxia: a systems view of O2, glycolysis, energetics, and intracellular PO2. J Appl Physiol 68: 833-842, 1990.[Abstract/Free Full Text]
  8. De Meer K, Gulmans VA, and van Der Laag J. Peripheral muscle weakness and exercise capacity in children with cystic fibrosis. Am J Respir Crit Care Med 159: 748-754, 1999.[Abstract/Free Full Text]
  9. De Meer K, Jeneson JA, Gulmans VA, van der Laag J, and Berger R. Efficiency of oxidative work performance of skeletal muscle in patients with cystic fibrosis. Thorax 50: 980-983, 1995.[Abstract]
  10. Dechecchi MC, Girella E, Cabrini G, and Berton G. The Km of NADH dehydrogenase is decreased in mitochondria of cystic fibrosis cells. Enzyme 40: 45-50, 1988.[ISI][Medline]
  11. Decramer M, Lacquet LM, Fagard R, and Rogiers P. Corticosteroids contribute to muscle weakness in chronic airflow obstruction. Am J Respir Crit Care Med 150: 11-16, 1994.[Abstract]
  12. Dekhuijzen PN and Balkom RH. Steroid-induced change in the respiratory muscles: its relevance in patients with obstructive airways disease. Respir Med 88: 335-341, 1994.[ISI][Medline]
  13. Donahoe M, Rogers RM, Wilson DO, and Pennock BE. Oxygen consumption of the respiratory muscles in normal and malnourished patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 94: 1260-1263, 1989.
  14. Dudois D. Disuse atrophy of skeletal muscle is associated with an increase in number of glucocorticoid receptors. Endocrinology 107: 1649-1651, 1980.[Abstract]
  15. Elkin SL, Williams L, Moore M, Hodson ME, and Rutherford OM. Relationship of skeletal muscle mass, muscle strength and bone mineral density in adults with cystic fibrosis. Clin Sci (Colch) 99: 309-314, 2000.[Medline]
  16. Grey AB, Ames RW, Matthews RD, and Reid IR. Bone mineral density and body composition in adult patients with cystic fibrosis. Thorax 48: 589-593, 1993.[Abstract]
  17. Hamilton AL, Killian KJ, Summers E, and Jones NL. Muscle strength, symptom intensity, and exercise capacity in patients with cardiorespiratory disorders. Am J Respir Crit Care Med 152: 2021-2031, 1995.[Abstract]
  18. Hanning RM, Blimkie CJ, Bar-Or O, Lands LC, Moss LA, and Wilson WM. Relationships among nutritional status and skeletal and respiratory muscle function in cystic fibrosis: does early dietary supplementation make a difference? Am J Clin Nutr 57: 580-587, 1993.[Abstract/Free Full Text]
  19. Ionescu AA, Chatham K, Davies CA, Nixon LS, Enright S, and Shale DJ. Inspiratory muscle function and body composition in cystic fibrosis. Am J Respir Crit Care Med 158: 1271-1276, 1998.[Abstract/Free Full Text]
  20. Keens TG, Krastins IR, Wannamaker EM, Levison H, Crozier DN, and Bryan AC. Ventilatory muscle endurance training in normal subjects and patients with cystic fibrosis. Am Rev Respir Dis 116: 853-960, 1977.[ISI][Medline]
  21. Kennedy MJ. Inflammation and cystic fibrosis pulmonary disease. Pharmacotherapy 21: 593-603, 2001.[ISI][Medline]
  22. Lands L, Desmond K, Demizio D, Pavilanis A, and Coates A. The effects of nutritional status and hyperinflation on respiratory muscle strength in children and young adults. Am Rev Respir Dis 141: 1506-1509, 1990.[ISI][Medline]
  23. Lands LC, Heigenhauser GJ, and Jones NL. Respiratory and peripheral muscle function in cystic fibrosis. Am Rev Respir Dis 147: 865-869, 1993.[ISI][Medline]
  24. McParland C, Krishnan B, Wang Y, and Gallagher CG. Inspiratory muscle weakness and dyspnea in chronic heart failure. Am Rev Respir Dis 146: 467-472, 1992.[ISI][Medline]
  25. McParland C, Resch EF, Krishnan B, Wang Y, Cujec B, and Gallagher CG. Inspiratory muscle weakness in chronic heart failure: role of nutrition and electrolyte status and systemic myopathy. Am J Respir Crit Care Med 151: 1101-1107, 1995.[Abstract]
  26. Mier A, Redington A, Brophy C, Hodson M, and Green M. Respiratory muscle function in cystic fibrosis. Thorax 45: 750-752, 1990.[Abstract]
  27. Moorcroft AJ, Dodd ME, and Webb AK. Long-term change in exercise capacity, body mass, and pulmonary function in adults with cystic fibrosis. Chest 111: 338-343, 1997.[Abstract/Free Full Text]
  28. Moser C, Tirakitsoontorn P, Nussbaum E, Newcomb R, and Cooper DM. Muscle size and cardiorespiratory response to exercise in cystic fibrosis. Am J Respir Crit Care Med 162: 1823-1827, 2000.[Abstract/Free Full Text]
  29. Muscular weakness assessment: use of normal isometric strength data. The National Isometric Muscle Strength (NIMS) Database Consortium. Arch Phys Med Rehabil 77: 1251-1255, 1996.[ISI][Medline]
  30. O'Neill S, Leahy F, Pasterkamp H, and Tal A. The effects of chronic hyperinflation, nutritional status, and posture on respiratory muscle strength in cystic fibrosis. Am Rev Respir Dis 128: 1051-1054, 1983.[ISI][Medline]
  31. Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, and Yernault JC. Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal Official Statement of the European Respiratory Society [see comments]. Eur Respir J Suppl 16: 5-40, 1993.[Medline]
  32. Standardization of spirometry, 1994 update. American Thoracic Society. Am J Respir Crit Care Med 152: 1107-1136, 1994.[ISI]
  33. Stutman HR and Marks MI. Pulmonary infections in children with cystic fibrosis. Semin Respir Infect 2: 166-176, 1987.[Medline]
  34. Szeinberg A, England S, Mindorff C, Fraser IM, and Levison H. Maximal inspiratory and expiratory pressures are reduced in hyperinflated, malnourished, young adult male patients with cystic fibrosis. Am Rev Respir Dis 132: 766-769, 1985.[ISI][Medline]
  35. Van Haren EH, Lammers JW, Festen J, Heijerman HG, Groot CA, and van Herwaarden CL. The effects of the inhaled corticosteroid budesonide on lung function and bronchial hyperresponsiveness in adult patients with cystic fibrosis. Respir Med 89: 209-214, 1995.[ISI][Medline]
  36. Wang YM, Zintel T, Vasquez A, and Gallagher CG. Corticosteroid therapy and respiratory muscle function in humans. Am Rev Respir Dis 144: 108-112, 1991.[ISI][Medline]
  37. Wilcox PG, Hards JM, Bockhold K, Bressler B, and Pardy RL. Pathologic changes and contractile properties of the diaphragm in corticosteroid myopathy in hamsters: comparison to peripheral muscle. Am J Respir Cell Mol Biol 1: 191-199, 1989.



This article has been cited by other articles:


Home page
 J EndocrinolHome page
O Schakman, H Gilson, and J P Thissen
Mechanisms of glucocorticoid-induced myopathy
J. Endocrinol., April 1, 2008; 197(1): 1 - 10.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
M. E. Sahlberg, U. Svantesson, E. M. L. M. Thomas, and B. Strandvik
Muscular Strength and Function in Patients With Cystic Fibrosis
Chest, May 1, 2005; 127(5): 1587 - 1592.
[Abstract] [Full Text] [PDF]

Home page
 ThoraxHome page
M A Spruit, M J Thomeer, R Gosselink, T Troosters, A Kasran, A J T Debrock, M G Demedts, and M Decramer
Skeletal muscle weakness in patients with sarcoidosis and its relationship with exercise intolerance and reduced health status
Thorax, January 1, 2005; 60(1): 32 - 38.
[Abstract] [Full Text] [PDF]

Home page
 ThoraxHome page
C Pinet, P Scillia, M Cassart, M Lamotte, C Knoop, C Melot, and M Estenne
Preferential reduction of quadriceps over respiratory muscle strength and bulk after lung transplantation for cystic fibrosis
Thorax, September 1, 2004; 59(9): 783 - 789.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
95/4/1379    most recent
00506.2002v2
00506.2002v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (6)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Barry, S. C.
Right arrow Articles by Gallagher, C. G.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Barry, S. C.
Right arrow Articles by Gallagher, C. G.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Visit Other APS Journals Online
Copyright © 2003 by the American Physiological Society.