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Nutritional status is an important predictor of diaphragm strength in young patients with cystic fibrosis^1,2,3

¹ From the Respiratory Muscle Laboratory, Royal Brompton Hospital, Fulham Road, London (NH and MIP); the Pediatric Pulmonary Department and Research Unit (NH, AC, MB, and BF) and the Pediatric Gastroenterology and Nutrition Department (PT), Armand Trousseau Hospital-AP-HP, Paris; and the Department of Clinical Physiology, Raymond Poincaré Hospital-AP-HP, Garches, France (NH and FL)

² NH was supported by a European Respiratory Society Long Term Fellowship, the Scadding-Morriston Davies Joint Respiratory Medicine Fellowship, and a grant from the Association Française Contre Les Myopathies. BF was supported by the Promotion Assistance Publique-Hôpitaux de Paris, Vaincre La Mucoviscidose, and the Societé de Pneumologie de Langue Francaise. MIP was supported by The Cystic Fibrosis Trust (United Kingdom) and the Peel Medical Research Trust.

³ Reprints not available. Address correspondence to B Fauroux, Pediatric Pulmonary Department and Research Unit INSERM E 213, Armand Trousseau Hospital-AP-HP, 28 Avenue du Docteur Arnold Netter, 75012 Paris, France. E-mail: brigitte.fauroux{at}trs.ap-hop-paris.fr.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Background: The effect of nutritional status and lung disease progression on diaphragm strength in young patients with cystic fibrosis remains unclear.

Objective: The aim of this study was to investigate the effect of nutritional status and airway obstruction on diaphragm strength.

Design: Twitch transdiaphragmatic pressure (Tw Pdi) obtained by bilateral anterior magnetic phrenic nerve stimulation, body mass index (BMI) z score, fat mass, fat-free mass (FFM), arm muscle circumference (AMC), forced expiratory volume in 1 s (FEV₁), and functional residual capacity (FRC) were measured in 20 patients aged 15.1 ± 2.8 y ( ± SD). Values were expressed as a percentage of predicted values.

Results: Mean (±SD) Tw Pdi was 24.3 ± 5.5 cm H₂O. Univariate regression analysis showed positive correlations between Tw Pdi and nutrition scores (BMI z score: r = 0.63, P = 0.003; FFM: r = 0.47, P = 0.04; AMC: r = 0.45, P = 0.04), airway obstruction (FEV₁: r = 0.68, P = 0.001), and arterial oxygen partial pressure (r = 0.68, P = 0.001). Negative correlations were observed between Tw Pdi and dynamic hyperinflation (FRC: r = –0.65, P = 0.005) and arterial carbon dioxide pressure (r = –0.50, P = 0.03). Furthermore, stepwise regression analysis showed that Tw Pdi correlated with BMI z score (r = 0.75, P = 0.0002) and FEV₁ (r = 0.69, P = 0.001).

Conclusions: Diaphragm strength is relatively well preserved in young patients with cystic fibrosis. However, the strength of the diaphragm decreases with the progression of malnutrition and airway obstruction.

Key Words: Diaphragm strength • magnetic stimulation • phrenic nerves • cystic fibrosis • respiratory muscles • body composition • nutritional status • airway obstruction • children

	INTRODUCTION

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Respiratory failure is the most common cause of death in patients with cystic fibrosis (CF), and a clear relation has been shown between nutritional status, lung function, and survival. Malnutrition in CF has several causes, including intestinal malabsorption, inadequate intake, and increased energy requirements. Although malabsorption is due to pancreatic insufficiency, impaired mucosal uptake, altered gut motility, liver disease, bile salt abnormalities, and structural bowel abnormalities, the energy imbalance is not the result of poor energy intake only but also of the increased energy requirements due to chronic infection, inflammation, and the excessive work of breathing. In a recent report, wasting was shown to be a significant predictor of survival in patients with CF, independent of lung function and gas exchange (1). Nevertheless, despite the diaphragm being the most important muscle of inspiration, the effect of nutritional status and lung disease progression on diaphragm performance still remains unclear. Although one study specifically assessed diaphragmatic function in CF, it was performed in adults and used volitional techniques to assess diaphragm strength, which are acknowledged to be of limited value because of their dependence on both the motivation and aptitude of the patient (2, 3). This limitation explains, in part, the observed inconsistency in global inspiratory muscle strength in patients with CF (4-7) and the absence of clear relations between inspiratory muscle strength, nutritional status, lung function, and gas exchange. The discrepancies between these earlier studies could be the consequence of several factors, particularly the method used to measure inspiratory muscle strength. More recently, a nonvolitional test that uses bilateral anterior magnetic phrenic nerve stimulation to measure twitch transdiaphragmatic pressure (Tw Pdi), was developed. This test allows an objective patient-independent method for evaluating diaphragm strength (8). Although this technique has been used previously to assess diaphragm strength in adults (9-12), its use in children has been limited (13, 14) and, to our knowledge, magnetic stimulation has not been used to estimate diaphragm strength in young patients with CF. The aim of this study was to investigate the effect of declining nutritional status and lung disease progression on diaphragm strength in young patients with CF.

	SUBJECTS AND METHODS

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The study was approved by the local hospital ethics committee. Patients were recruited from our CF center, and the patients and their parents gave their informed consent. Patients were included in the study if they had been clinically stable for 1 mo, were not receiving oral corticosteroids, and were able to perform reproducible lung function tests.

Measurement of diaphragm strength and respiratory muscle activity
All studies were performed in the afternoon, 2 h after chest physiotherapy. Tw Pdi was measured after insertion of a catheter-mounted pressure transducer system (Gaeltec, Dunvegan, United Kingdom) with 2 pressure transducers, one placed in the stomach and one in the esophagus. Appropriate placement of the esophageal pressure transducer was achieved with methods described previously (15). Pdi was obtained online by subtracting the esophageal pressure (Pes) from the gastric pressure (Pgas). All of the signals were digitized at 128 Hz and sampled for analysis by using an analogic/numeric acquisition system (MP 100; Biopac Systems, Goletta, CA) that was run on a computer (Elonex, Gennevilliers, France) with ACKNOWLEDGE software as previously described (15, 16).

The patients performed 10–15 sniff maneuvers, from functional residual capacity (FRC); maximal sniff transdiaphragmatic pressure (Pdi_sn) was used as the volitional indicator of diaphragm strength. Indeed, Pdi_sn provides a more reproducible measure of inspiratory muscle strength than does maximal inspiratory pressure (17, 18), and this test evaluates also more specifically the diaphragm. The unpotentiated Tw Pdi elicited by phrenic nerve stimulation by the bilateral anterior magnetic phrenic nerve stimulation technique (8) with the use of two 43-mm double circular coils powered by 2 Magstim 200 magnetic stimulators (Magstim Company, Dyfed, Wales, United Kingdom), was used as the nonvolitional method of measuring diaphragm strength. The patients were instructed to breathe quietly for 20 min before phrenic nerve stimulation to avoid twitch potentiation. The subjects wore a nose clip during stimulations, which were applied at FRC determined by the end-expiratory Pes level. At least 5 phrenic nerve stimulations were obtained in each patient.

The diaphragm pressure time index (PTI_di) (19) and esophageal pressure time index (PTI_es) were calculated from the average of 10–30 breaths; PTI_di and PTI_es provided indicators of diaphragm and rib cage muscle activity, respectively. PTI_es/PTI_di was used as an index of rib cage muscle activity to diaphragmatic activity.

Clinical nutritional status
On the study day, body weight and height were determined in all of the subjects as were skinfold thickness with the use of a Holtain Skinfold Caliper (Holtain Ltd, Crymych, United Kingdom) at the biceps, triceps, subscapular, and suprailiac sites. All the skinfold-thickness measurements were done in triplicate, to the nearest millimeter, by the same investigator (PT). Fat-free mass (FFM) and fat mass (FM) were calculated from skinfold-thickness values by using the formula of Durnin and Rahaman for patients older than 13 y (20) and the formula of Brook for those aged 10–13 y (21). Arm muscle circumference (AMC) was assessed from the following formula: arm circumference – (0.314 x biceps skinfold thickness/2 + triceps skinfold thickness/2) (22). FM, FFM, and AMC were expressed as a percentage of that predicted for statural age.

Ideal body weight and height were calculated by using the reference values determined in French children by Rolland-Cachera et al (23). Body mass index (BMI) was defined as the ratio of body weight (kg) to height (cm) squared. The BMI z score was calculated by using the method and the values in French children reported by Rolland-Cachera et al (23).

Pulmonary function tests
The partial pressure of arterial oxygen (P_aO₂) and the partial pressure of arterial carbon dioxide (P_aCO₂) were measured from arterialized earlobe capillary blood gases (24). The alveolar-arterial oxygen gradient (P_AO₂ – P_aO₂; A-a gradient) was calculated according to the ideal alveolar-arterial oxygen equation (25). Forced expiratory volume in 1 s (FEV₁) and FRC were measured according to standard guidelines and were expressed as a percentage of published values (26). FRC was measured by body plethysmography (FRC_pl) (26).

Data and statistical analysis
Data are expressed as means ± SDs. Correlations between Tw Pdi and clinical nutritional status, airway obstruction, lung hyperinflation, gas exchange, and inspiratory muscle activity were assessed by using simple linear regression analysis. Stepwise regression analysis was used to evaluate the relation between Tw Pdi and BMI z score, FEV₁, A-a gradient, and PTI_es/PTI_di. A P value of < 0.05 was considered statistically significant.

	RESULTS

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Twenty patients with CF (11 females) with a mean age of 15.1 ± 2.8 y were studied. Anthropometric and nutritional characteristics for the patients are shown in Table 1, and lung function parameters and Tw Pdi are shown in Table 2. All patients tolerated the procedures well, and no problems were encountered during insertion of the pressure-monitoring catheter or during magnetic stimulation. The FEV₁ and BMI z score were lower in female patients; the FEV₁ scores were 37.1 ± 14.2% and 51.9 ± 25.3% in female and male patients, respectively, and BMI z scores were –1.34 ± 1.29 and –0.96 ± 1.29 for female and male patients, respectively. Tw Pdi values were also lower in female than in male patients with mean Tw Pdi values of 23.1 ± 3.9 and 25.5 ± 6.8 cm H₂O, respectively, but these sex differences were not statistically significant.

Figure 1

View larger version (12K): [in this window] [in a new window]   FIGURE 1.. Effect of clinical nutritional status on diaphragm strength, assessed by twitch transdiaphragmatic pressure (Tw Pdi). A positive correlation was observed between diaphragm strength and 3 indicators of clinical nutritional status: BMI (adjusted for sex and age of the patient), arm muscle circumference (AMC), and fat-free mass (FFM). n = 20.

Figure 2

Figure 3

Figure 4

View larger version (13K): [in this window] [in a new window]   FIGURE 2.. Effect of airway obstruction (n = 20) and lung hyperinflation (n = 17) on diaphragm strength, assessed by twitch transdiaphragmatic pressure (Tw Pdi). Diaphragm strength correlated positively with forced expiratory volume in 1 s (FEV1), which is a marker of airway obstruction. Diaphragm strength correlated negatively with functional residual capacity (assessed by body plethysmography; FRCpl), which is a measure of lung hyperinflation.

View larger version (11K): [in this window] [in a new window]   FIGURE 3.. Correlation between diaphragm strength, assessed by twitch transdiaphragmatic pressure (Tw Pdi), and gas exchange. PaO2, partial pressure of arterial oxygen; PaCO2, partial pressure of arterial carbon dioxide; PAO2 – PaCO2, alveolar-arterial oxygen gradient. n = 19.

View larger version (14K): [in this window] [in a new window]   FIGURE 4.. Effect of respiratory muscle activity partitioning on diaphragm strength, assessed by twitch transdiaphragmatic pressure (Tw Pdi). Diaphragm pressure time index (PTIdi) and esophageal pressure time index (PTIes) provided indicators of diaphragm and rib cage muscle activity, respectively. The esophageal pressure time index, normalized for the diaphragm pressure time index (PTIes/PTIdi), was used as an index of rib cage muscle activity to diaphragmatic activity. n = 20.

Volitional assessment of diaphragm strength
There was no correlation observed between Pdi_sn and Tw Pdi or clinical nutritional status or any marker of lung function: BMI z score (P = 0.1), AMC (P = 0.4), FFM (P = 0.3), FM (P = 0.2), FEV₁ (P = 0.4), FRC_pl (P = 0.1), PaO₂ (P = 0.3), PaCO₂ (P = 0.3), and PTI_di (P = 0.1).

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
This study, which used a nonvolitional assessment of diaphragm strength in young patients with CF, showed that diaphragmatic performance declines as nutritional status, evaluated on the basis of clinical indexes, decreases. Indeed, nutritional status confers the most important contribution to diaphragm strength, whereas airway obstruction and impairment of gas exchange play less of a role. Furthermore, in contrast with the findings in adult CF patients (2), volitional measures of diaphragm strength, such as Pdi_sn, did not correlate with any of the nutritional or pulmonary parameters measured in the younger patients with CF.

Effect of malnutrition on diaphragm strength
Malnutrition in patients with CF is a major predictor of outcome. It is a consequence of poor caloric intake, malabsorption, increased resting energy expenditure, less efficient pulmonary mechanics, and a catabolic intermediary metabolism secondary to pulmonary infection and inflammation. Although severe malnutrition, as in anorexia nervosa, has been associated with a reduced diaphragm strength (27), the nutritional status of our patients was better preserved. However, other factors, such as pulmonary hyperinflation and the excessive pulmonary and systemic inflammatory response, could also be expected to contribute to the results observed in the current study. In fact, there has been no correlation observed between diaphragm strength and nutritional status in adult patients with chronic obstructive pulmonary disease (COPD), which supports the pathophysiological differences in diaphragm dysfunction between CF and COPD (28). This concept is supported by data that show the beneficial effect of refeeding on the volitional tests of respiratory muscle strength in CF patients (29). In the current study, we observed that a decrease in BMI z score, FFM, and AMC was associated with a decrease in diaphragm strength. These data emphasize that nutritional status and nonrespiratory muscle mass are good predictors of diaphragm strength. Furthermore, stepwise linear regression analysis not only confirmed that both BMI z score and FEV₁ were important predictors of Tw Pdi, but also that the BMI z score conferred a more significant benefit to the relation with Tw Pdi, which implies that nutrition has a greater effect on diaphragm strength than does the mechanical disadvantage that accompanies airway obstruction.

Effect of the progression of lung disease on diaphragm strength
Lung pathology in CF is characterized by an early, persistent, and excessive inflammatory and infectious process, which leads to a progressive destruction of the lung. One of the first clinical features of this lung injury is the development of pulmonary hyperinflation. Although previous studies have investigated the relation between inspiratory muscle strength and hyperinflation in patients with CF, this relation has been determined mainly in adults (2, 4, 30-33). The results of these studies have been varied, with significant correlations observed between inspiratory muscle strength, and hyperinflation in some studies (2, 30, 32) but not in others (4, 6, 33). The reliance on volitional techniques, such as maximal inspiratory mouth pressure (PI_max), could, in part, be an explanation for these discrepancies.

In the current study, there was a decrease in diaphragm strength with increasing airway obstruction and hyperinflation. Similar findings were observed in adults with COPD (9). As FEV₁ decreases, the subsequent rise in FRC would be expected to result in a shorter diaphragm length and impose a mechanical disadvantage on the diaphragm, which causes a reduction in the generation of the transdiaphragmatic pressure (19, 34). However, the mean value of Tw Pdi observed in the CF children in the current study was higher than that observed in adult COPD patients who had a similar degree of airway obstruction and hyperinflation (9), which suggests that diaphragm strength is relatively well preserved. Furthermore, impairment of gas exchange, as evidenced by an increase in PaCO₂ and a decrease in PaO₂, was associated with a reduction in diaphragm strength. A possible explanation is that the decrease in strength of the diaphragm contributes to the progressive development of alveolar hypoventilation and the consequent increase in PaCO₂ and decrease in PaO₂ (15).

Critique of method
A major problem of performing invasive studies in children and young patients with CF is the absence of a control group. Indeed, our ethical review committee considered that the invasive nature of the current study, specifically the insertion of a catheter-mounted pressure transducer, precluded enrolment of healthy children. Furthermore, the lowest Tw Pdi value for our group of patients of 15.8 cm H₂O, which is close to the lower limit of normal seen in adults, suggests that diaphragm strength is relatively well preserved even in young patients with very advanced CF lung disease.

In these lean patients, body fat is probably underestimated, especially in undernourished patients (35), when assessed by skinfold-thickness measurements and using formulas established from children with normal body weight (20, 21). Body composition assessed with this method may therefore artifactually overestimate FFM.

The measurement of FRC in our patients was performed by using body plethysmography (FRC_pl). Although body plethysmography can overestimate FRC in patients with very severe airway obstruction, because of delayed transmission between alveolar and mouth pressure, the helium dilution method can underestimate FRC because of air trapping. Despite this, we found no correlation between FRC measured by the helium dilution technique and Tw Pdi (P = 0.99) but found a correlation between FRC measured by body plethysmography and Tw Pdi (r = –0.65, P = 0.005), which is probably explained by the inability of the helium dilution technique to detect gas trapping.

Clinical implications
In the current study, in which using nonvolitional tests were used to assess diaphragm function, we considered that both chronic pulmonary hyperinflation and nutritional factors are important in predicting diaphragm strength. However, the patient's nutritional state has a significantly greater role in predicting diaphragm strength. From these data, we suggest that those patients with CF and advanced disease could benefit from refeeding and additional nutritional supplementation combined with pharmacologic and physiotherapy-assisted reductions in airway obstruction. This would potentially improve diaphragm performance and limit the progression of respiratory failure.

In conclusion, in young patients with CF, the strength of the diaphragm decreases with the progression of malnutrition and airway obstruction, which in turn precipitates alveolar hypoventilation. The measurement of twitch transdiaphragmatic pressure appears to be a valuable nonvolitional test for evaluating the effect of nutritional and respiratory interventions on diaphragm strength in young patients with CF.

	ACKNOWLEDGMENTS

 
We thank all the patients and their parents for their enthusiastic participation.

NH and BF designed the study, recruited the patients, performed the respiratory muscle study, and wrote the manuscript. PT performed the nutritional study, discussed the results, and helped write the manuscript. MB performed the lung function tests and helped write the manuscript. AC, MIP, and FL helped design the study, discussed the results, and helped write the manuscript. None of the authors declared a conflict of interest.

	REFERENCES

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1. Sharma R, Florea VG, Bolger AP, et al. Wasting as an independent predictor of mortality in patients with cystic fibrosis. Thorax 2001;56:746-50.[Abstract/Free Full Text]
2. Pradal U, Polese G, Braggion C, et al. Determinants of maximal transdiaphragmatic pressure in adults with cystic fibrosis. Am J Respir Crit Care Med 1994;150:167-73.[Abstract]
3. Society AT, Society ER. ATS/ERS statement on respiratory muscle testing. Am J Respir Crit Care Med 2002;166:518-624.[Free Full Text]
4. O'Neill S, Leahy F, Pasterkamp H, Tal A. The effects of chronic hyperinflation, nutritional status, and posture on respiratory muscle strength in cystic fibrosis. Am Rev Respir Dis 1983;128:1051-4.[Medline]
5. Asher MI, Pardy RL, Coates AL, Thomas E, Macklem P. The effects of inspiratory muscle training in patients with cystic fibrosis. Am Rev Respir Dis 1982;126:855-9.[Medline]
6. Marks J, Pasterkamp H, Tal A, Leahy F. Relationship between respiratory muscle strength, nutritional status, and lung volume in cystic fibrosis and asthma. Am Rev Respir Dis 1986;133:414-7.[Medline]
7. Hanning RM, Blimkie CJR, Bar-Or O, et al. Relationship among nutritional status and skeletal and respiratory muscle function in cystic fibrosis: does early dietary supplementation make a difference? Am J Clin Nutr 1993;57:580-7.[Abstract/Free Full Text]
8. Mills GH, Kyroussis D, Hamnegard CH, et al. Bilateral magnetic stimulation of the phrenic nerves from an anterolateral approach. Am J Respir Crit Care Med 1996;154:1099-105.[Abstract]
9. Polkey MI, Kyroussis D, Hamnegard CH, et al. Diaphragm strength in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1996;154:1310-7.[Abstract]
10. Mills GH, Kyroussis D, Hamnegard CH, et al. Cervical magnetic stimulation of the phrenic nerves in bilateral diaphragm paralysis. Am J Respir Crit Care Med 1997;155:1565-9.[Abstract]
11. Hughes PD, Polkey MI, Harris ML, et al. Diaphragm strength in chronic heart failure. Am J Respir Crit Care Med 1999;160:529-34.[Abstract/Free Full Text]
12. Hughes PD, Polkey MI, Moxham J, Green M. Long-term recovery of diaphragm strength in neuralgic amyotrophy. Eur Respir J 1999;13:379-84.[Abstract]
13. Rafferty GF, Greenough A, Dimitriou G, et al. Assessment of neonatal diaphragm function using magnetic stimulation of the phrenic nerves. Am J Respir Crit Care Med 2000;162:2337-40.[Abstract/Free Full Text]
14. Rafferty GF, Greenough A, Manczur T, et al. Magnetic phrenic nerve stimulation to assess diaphragm function in children following liver transplantation. Pediatr Crit Care Med 2001;2:122-6.[Medline]
15. Hart N, Polkey MI, Clement A, et al. Changes in pulmonary mechanics in children and young adults with cystic fibrosis. Am J Respir Crit Care Med 2002;166:61-6.[Abstract/Free Full Text]
16. Fauroux B, Pigeot J, Polkey MI, et al. In vivo physiological comparison of two ventilators used for domiciliary ventilation in children with cystic fibrosis. Crit Care Med 2001;29:2097-105.[Medline]
17. Laroche CM, Mier AK, Moxham J, Green M. The value of sniff esophageal pressures in the assessment of global inspiratory muscle strength. Am Rev Respir Dis 1988;138:598-603.[Medline]
18. Stefanutti D, Fitting J-W. Sniff nasal inspiratory pressure. Reference values in children. Am J Respir Crit Care Med 1999;159:107-11.[Abstract/Free Full Text]
19. Bellemare F, Grassino A. Effect of pressure and timing of contraction on human diaphragm fatigue. J Appl Physiol 1982;53:1190-5.[Abstract/Free Full Text]
20. Durnin JV, Rahaman MM. The assessment of the amount of fat in the human body from measurements of skin fold thickness. Br J Nutr 1967;2:681-9.
21. Brook CGD. Determination of body composition of children from skinfold measurements. Arch Dis Child 1971;46:182-4.
22. Borowitz D, Baker RD, Stallings V. Consensus report on nutrition for pediatric patients with cystic fibrosis. J Pediatr Gastroenterol Nutr 2002;35:246-59.[Medline]
23. Rolland-Cachera MF, Cole TJ, Sempé M, et al. Body mass index variations: centiles from birth to 87 years. Am J Clin Nutr 1991;45:13-21.
24. Gaultier C, Boulé M, Allaire Y, et al. Determination of capillary oxygen tension in infants and children: assessment of methodology and normal values during growth. Bull Eur Physiopathol Respir 1978;14:287-94.
25. Kufel TJ, Grant BJB. Arterial blood-gas monitoring: respiratory assessment. In: Tobin MJ, ed. Principles and practices of intensive care monitoring. New York: McGraw-Hill, 1998:197-215.
26. Quanjer PH. Standardized lung function testing. Eur Respir J 1993;6(suppl 16):5-30s.[Medline]
27. Murciano D, Rigaud D, Pingleton S, et al. Diaphragmatic function in severely malnourished patients with anorexia nervosa. Am J Respir Crit Care Med 1994;150:1569-74.[Abstract]
28. Hamnegard CH, Bake B, Mowham J, Polkey MI. Does undernutrition contribute to diaphragm weakness in patients with COPD? Clin Nutr 2002;21:239-43.[Medline]
29. Mansell AL, Anderson JC, Muttart CR, et al. Short-term pulmonary effects of total parenteral nutrition in children with cystic fibrosis. J Pediatr 1984;104:700-5.[Medline]
30. Szeinberg A, England S, Mindorff C, Fraser I, Levison H. Maximal inspiratory and expiratory pressures are reduced in hyperinflated, malnourished young adult patients with cystic fibrosis. Am Rev Respir Dis 1985;132:766-9.[Medline]
31. Mier AK, Redington A, Brophy C, Hodson ME, Green M. Respiratory muscle function in cystic fibrosis. Thorax 1990;45:750-2.[Abstract/Free Full Text]
32. Ionescu AA, Chatham K, Davies CA, et al. Inspiratory muscle function and body composition in cystic fibrosis. Am J Respir Crit Care Med 1998;158:1271-6.[Abstract/Free Full Text]
33. Lands LC, Heigenhauser GJF, Jones NL. Respiratory and peripheral muscle function in cystic fibrosis. Am Rev Respir Dis 1993;147:865-9.[Medline]
34. Gibson GJ, Clark E, Pride NB. Static transdiaphragmatic pressures in normal subjects and in patients with chronic hyperinflation. Am Rev Respir Dis 1981;124:685-9.[Medline]
35. Melchior JC, Rigaud D, Rozen R, Malon D, Apfelbaum M. Energy expenditure economy induced by decrease in lean body mass in anorexia nervosa. Eur J Clin Nutr 1989;43:793-9.[Medline]

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