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Variation in Maximum Inspiratory and Expiratory Pressure after Application of Inspiratory Loads in Patients with COPD
Variation in Maximum Inspiratory ;and Expiratory Pressure after Application of Inspiratory Loads in Patients· with COPD* jose Fiz, M.D.; Miguel Gallego, M.D.; jose Izquierdo, M.D.; juan Ruiz, M.D.; jorge Roig, M.D.; and jose Mornra, M.D.
We studied eight men with chronic obstructive pulmonary disease (COPD) (age, 60.57 ± 7.59 years; height, 162±10.43 em; weight, 65±9.7 kg). Functional values of the sample were as follows: FEV., 46 percent; FVC, 67 percent; Po., 72.4 mm Hg; and pH, 7.41. We used a modi6cation of the Nickerson and Keens method. Patients were required to perform 65 percent of maximal inspiratory pressure (MIP). We counted the time from the start of the test to exhaustion of the patient (TLIM). We measured basal MIP and maximal expiratory pressure (MEP) (TLC) at the TLIM and 10, 20, and 30 minutes and MIP was different from the basal value (MIP basal, 85.7 em HsO; MIP 10
resistive inhalationalloads have F orbeensomeusedyearsto now, evaluate the endurance capacity of the inspiratory musculature under exertion. l-4 The capacity to sustain the muscular exertion required to inhale depends on the force and duration of the inhalational muscle contraction, which is determined by the pressure-time ratio. 1 It is known that healthy subjects and patients with COPD become fatigued with diaphragmatic pressure-time ratios over 0.15. 1•5 This technique is also used as a rehabilitative measure for the respiratory muscle function,6-ll as well as in the evaluation of the effectiveness of certain drugs such as caffeine. 6 ·s-11 In patients with COPD, it is observed that the maximum inspiratory pressures (MIPs) and the exertion capacity are diminished owing probably to pulmonary hyperinflation, to changes in the exchange of gases, and to concomitant nutritional deficiencies. 12 • 14 Nevertheless. the effects of application of resistive inhalational loads on the maximum inspiratory and expiratory pressures in such patients are not known. PURPOSE
The purpose of this study was to evaluate the possible variation of the maximum inspiratory and expiratory pressures after the application of inspiratory loads generating 65 percent of MIP in patients
minutes, 79.1 em H.O; M1P 20 minutes, 78.6 em H.O; MIP 30 minutes, 79.6 em HsO. The MEP was not different from the basal value. We concluded that in patients with COPD, MIP decreases sigoi6cantly after inspiration through umbral inspiratory weight equal to 65 percent MIP and does not return to basal value for 30 miQutes. The MEP does not change with respect to basal determination. (Cheat 1990; 97:618-20) MIP =maximal inspiratory pressure; MEP =maximal expiratory pressure; TLIM =time from the start of the test to exhaustion; Tlfl'TOI' =inspiratory' time-total time ratio
with stable COPD. MATERIAL AND METHODS
Sample
The study was conducted on eight male patients with COPD in stable phase, that is, the patients had not shown any symptoms of acute relapse in a period of at least two months prior to the study. The average age was 60.57±7.59 years, the height was 162.14± 10.43 em, and the weight was 65±9.7 kg. The patients did not have any other type of cardiorespiratory, endocrine, neuromuscular, or hepatic illness. We explained the protocol to be followed and all patients gave their consent. Various tests were conducted simultaneously within the first week of inclusion in the study. Respiratory Function Study An OHIO 827 unit (Sensor Medics) was used to determine the following factors: simple and postbronchodilator spirometry and measurement of pulmonary volumes by the technique of helium dilution and CO transfer (Dco, KCO). The American Thoracic Society rules•• were followed and the values found were compared with those gathered in the normal population.•• The MIPs and maximum expiratory pressures (MEPs) were measured from residual volume and TLC by the method of Black and Hyatt.l1 To obtain these values, a dry manometer connected to a pressure transducer with range of 0 to 300 em H10 (Sibelmed) was used. The signal was amplified and polygraphically recorded by means of a 12-channel polygraph (Sensor Medics). To obviate the learning etTect, a minimum of ten maneuvers were performed up til at least three of the determinations varied by less than 5 percent." The maneuvers were repeated immediately after finishing the load test and after 10, 20, and 30 minutes.
Inspiratory Load That
*From the Servei de Pneumologia, Hospital Germans Trias i Pujol, Barcelona, Spain. Supported by grant FISS88. Manuscript received April 6; revision accepted August 31.
818
A modification of the Nickerson and Keens method• was applied. After placing the patient in the sitting position with his back resting against a rigid support, application was made of a noncollapsible mouthpiece joined to a Hans Rudolph two-way valve (2700) in Variation In Maxlnun Inspiratory and Expiratory
~18
In COPO (Fiz et el)
Table 1- Functional and Nutritional \bluea of the Sample Studied* Factor
Value, Mean±SD
FEV,,L FVC,L FEV,IFVC TLC,L RY,L RV/fLC FRC,L Po1 , mm Hg Pco1 , mmHg pH Sat Hb,% Dco,% KCO,% TLIM, minutes Weight, kg TSF, mm• Circum, em
1.46±0.78 2.59±0.74 48.8± 14.2 6.8±2.1 3.8±1.0 55.4±6.3 4.6±1.4 72.4±0.02 35.7±6.8 7.41±0.02 94.4± 1.6 74.4±45.4 73.8±29.6 3.7±1.9 65±9.7 11.2±4.0 28.3±3.4
%Predicted 46±18.3 67±12.6 117.4± 18.7 180.3±44.7 152.1±43.6
105.1±10.9
*TSF =triceps pinch measured with caliper; Circum= circumference of the upper arm; and TUM =elapsed time basal to exhaustion. which another valve was installed, and different weights were inserted through the latter. The weight was increased until the patient generated a mouth pressure equivalent to 65 percent of his MIP (threshold pressure). Once the proper load was known, the patient breathed through the device until the threshold pressure calculated during three consecutive breaths ceased to be generated (exhaustion). The time that elapsed from the start of the test to exhaustion (TUM) was counted. During the test, the pressure exerted was controlled at all times by a polygraph recording, preventing it from dropping below the threshold pressure. The inspiratory time-total time ratio ('Ii/I'ror) was kept constant and the respiratory frequency was approximately 20 breaths per minute. Nutritional Study As part of the nutritional study, the following measurements were taken: weight as a percentage of the control, body fat content measured as a percentage of total body weight (triceps pinch with caliper), and circumference of the upper arm in order to obtain muscle content. In all measurements we followed the rules of Driver and Lebruw. ••
Statistical Study
We applied the Friedman test and a Wilcoxson test of sign-range.
REsuLTS It can be seen in Table 1 that there is evidence that
the patients suffered a moderate obstruction of air and the volumes are increased. Three of the patients had a Dco of less than 80 percent due to clinical and radiologic signs of pulmonary emphysema.l9 The average TLIM of the sample was 3. 7 ± 1.96 minutes. The anthropometric measurements were normal. Table 2 shows the MIP and the MEP of the patients at the basal stage, on exhaustion, and at 10, 20, and 30 minutes following exhaustion. There was a global significant difference between the five groups (Friedman test: p
DISCUSSION
The studies that have been performed on respiratory muscle endurance are based on the capacity of the respiratory muscles to sustain and generate high levels of pressure. The most common test consists of generating a pressure against a given resistive inspiratory load. 1·2 •3·20 In our study, we used the Nickerson, Keens and Kelsen methods, 3·4 •21 that consist of breathing through a constant threshold load equivalent to 65 percent of the MIP. This pressure lies within the range of critical pressure required to induce respiratory muscle fatigue in normal subjects. 19·22 The TiffTOT ratio was kept constant at 0.5, as variations in this ratio during the test change the time of endurance under the inspiratory load owing to the fact that the endurance capacity of the inspiratory muscles depends on the ventilatory pattern and on muscular force generated. 1 It is a proven fact that the application of submaximum inspiratory loads produces low-frequency fatigue in normal subjects. 13·23 The MIP is a measure of th~ maximum force generated by all the respiratory muscles and, in turn, it measures the muscular response to the high-frequency voluntary activation of the respiratory muscles. 24 In healthy
Table 2-Baaol MtmmallRBpiratory Prenure (MIP) and Mtmmal Expiratory Preaure (MEP) at &haunion and after 10, 20, and 30 Minutea* Minutes
MIP, cmH1 0 MEP, cmH1 0
Basal
Exhaustion
10
20
30
85.7±18.1
82.6±18.1 (ns) 141.3±51.9 (ns)
79.1±17.2 p
78.6± 16.3 p
79.6±19.1 p
139±43.9
•ns =not significant with respect to the basal determination. The significance was for p<0.05 (Wilcoxon test of sign range). CHEST I 97 I 3 I MARCH, 1990
819
individuals, the MIP decreases significantly five minutes after breathing has begun through the test with inspiratory load 21 and this reduction reflects the reduction in the mechanical capacity of the respiratory muscles to generate pressure. We have shown that in patients with COPD the MIP is decreased at the end of the test with respect to its basal value, but not significantly (85.7 to 82.6 em H 20). The decrease in MIP becomes significant (79.1 em H 20) ten minutes after exhaustion (Table 2) with respect to its basal value. The drop in MIP reaches a plateau after ten minutes and is maintained throughout the 30-minute recovery phase, so there is no recovery of maximum inspiratory muscle force. The decrease in MIP is probably related to the fatigue of rapid muscle fiber contraction (type II). For the most part, the fibers are responsible for respiratory muscle force25 and these muscle fibers are activated with a high frequency, but the inspiratory load test measures endurance of respiratory muscle. 14 •22 We cannot discard the possibility that the decrease in MIP is caused by a motivational effort; however, if this is indeed the case, we think that the MIP would decrease significantly at exhaustion and not ten minutes after. Also, it is curious that MEP did not decrease as well. We may conclude that in patients with COPD, the decrease in MIP lasts 30 minutes after the application of inspiratory loads and consequently, the high-frequency fatigue extends even beyond 30 minutes after exhaustion of the patient. The MEP did not vary after application of loads, although insignificant increases were obtained in it, probably the result of the learning effort. Musculature showed no fatigue, or at least no high-frequency fatigue, which seems to be related to the normality of the MEPs of the sample (MEP= 139.4 ±43.9). Therefore, the application of resistive inspiratory loads does not produce fatigue of the expiratory muscles as is the case in normal subjects. 26 CoNCLUSIONS
On the basis of foregoing results, it may be said that the MIP decreases in the patients with COPD after the application of inspiratory loads equivalent to 65 percent ofMIP. The drop in MIP begins to take place at the end of the test and becomes significant ten minutes after exhaustion, without returning to its basal value even beyond 30 minutes after the end of the test. The MEP does not vary with respect to the value obtained at rest. REFERENCES
1 Bellemare F, Gmssino A. Effect of pressure and timing on contraction on human diaphmgm fatigue. J Appl Physiol1982;
620
53:1190 2 McCool FD, McCannor LD. Pressure-flow effects on endurance of inspiratory muscles. J Appl Physiol1986; 60:299 3 Roussos CS, Macklem Pr. Diaphragmatic fatigue in man. J Appl Physiol1977; 43:189 4 Nickerson T, Kens G. Measuring ventilatory muscle endurance in humans as sustainable inspimtory pressure. J Appl Physiol 1982; 52:768-72 5 Bellemare F, Grassino A. Fbrce reserve of the diaphmgm in patients with chronic obstructive pulmonary disease. J Appl Physiol 1983; 55:8 6 Bjerre-Jepsen K, Seeber NH. Inspiratory resistance training in severe chronic obstructive pulmonary disease. Eur J Respir Dis 1981; 62:405-11 7 Pardy R, Rivington L. The effects of inspimtory muscle training on exercise performance in chronic airflow limitation. Am Rev Respir Dis 1981; 123:426-33 8 Pardy R, Macklem P. Inspiratory muscle training compared with physiotherapy in patients with chronic airflow limitation. Am Rev Respir Dis 1981; 123:421-25 9 Estrup C, Lyager S, Olsen C. Effect of respiratory muscle training in patients with neuromuscular diseases and in normals. Respiration 1986; 50:36-43 10 Supinski GS, LevinS, Kelsen SG. Caffeine effect on respiratory muscle endurance and sense of effort during loaded breathing. J Appl Physiol1988; 9:225-36 11 Jones DT, Thompson RJ. Physical exercise and resistive breathing training in severe chronic airways obstruction: are they effective? Eur J Respir Dis 1985; 67:159-66 12 Grassino A, Bellemare F. Force reserve of the diaphragm in COPD patients. Rev Tx Mal Respir 1980; 23-9 13 Martin J, Engel JA. The role of respiratory muscles in the hyperinflation of bronchial asthma. Am Rev Respir Dis 1980; 121:441-48 14 Narinder S, Arora MD, Rochester. COPD and human diaphragm muscle dimensions. Chest 1987; 91:5 15 Standardization of spirometry 1987-update. Am Rev Respir Dis 1987; 136:1285-98 16 Roca J, Segarra F, Rodriguez R. Static lung volumes and singlebreath diffusing capacity reference values from a Latin population. Am Rev Respir Dis 1985; 131:4(pt 2) A352 17 Black LF, Hyatt RE. Masimal inspiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis 1969; 99:696-702 18 Driver AG, Lebruw M. Nutritional assessment of patients with chronic obstructive pulmonary disease and acute respiratory failure. Chest 1982; 82:568-71 19 Gibson GJ. Clinical tests of respiratory function. London: Macmillan Press. 1984; 150-52 20 Esau SA, Bellemare F, Grassino A. Changes in relaxation rate with diaphragmatic fatigue in humans. J Appl Physiol 1983; 54:1353 21 Supinski GS, Clary SJ, Kelsen SG. Effect of inspiratory muscle fatigue on perception of effort during loaded breathing. J Appl Physiol1987; 62:3()().07 22 Roussos C, Fixley M, Cross D, Macklem PT. Fatigue of inspiratory muscles and their synergic behavior. J Appl Physiol 1979; 46:897-904 23 Moxham J, McGreen. Contractile properties and fatigue of the diaphragm in man. Thorax 1981; 86:164-68 24 Thomas K, Aldrch MD. Respiratory muscle fatigue. Clin Chest Med 1988; 9:225-36 25 Gary C, Sieck PD. Diaphragm muscle: structural and functional organization. Clin Chest Med 1988; 9:195-210 26 Martin J, Engel JA. The behaviour of the abdominal muscles during inspiratory mechanical loading. Respir Physiol 1982; 50:63-73 Variation In Maximum Inspiratory and Expiratory Pnlssura In COPD (Fiz et a/)
We studied eight men with chronic obstructive pulmonary disease (COPD) (age, 60.57 ± 7.59 years; height, 162±10.43 em; weight, 65±9.7 kg). Functional values of the sample were as follows: FEV., 46 percent; FVC, 67 percent; Po., 72.4 mm Hg; and pH, 7.41. We used a modi6cation of the Nickerson and Keens method. Patients were required to perform 65 percent of maximal inspiratory pressure (MIP). We counted the time from the start of the test to exhaustion of the patient (TLIM). We measured basal MIP and maximal expiratory pressure (MEP) (TLC) at the TLIM and 10, 20, and 30 minutes and MIP was different from the basal value (MIP basal, 85.7 em HsO; MIP 10
resistive inhalationalloads have F orbeensomeusedyearsto now, evaluate the endurance capacity of the inspiratory musculature under exertion. l-4 The capacity to sustain the muscular exertion required to inhale depends on the force and duration of the inhalational muscle contraction, which is determined by the pressure-time ratio. 1 It is known that healthy subjects and patients with COPD become fatigued with diaphragmatic pressure-time ratios over 0.15. 1•5 This technique is also used as a rehabilitative measure for the respiratory muscle function,6-ll as well as in the evaluation of the effectiveness of certain drugs such as caffeine. 6 ·s-11 In patients with COPD, it is observed that the maximum inspiratory pressures (MIPs) and the exertion capacity are diminished owing probably to pulmonary hyperinflation, to changes in the exchange of gases, and to concomitant nutritional deficiencies. 12 • 14 Nevertheless. the effects of application of resistive inhalational loads on the maximum inspiratory and expiratory pressures in such patients are not known. PURPOSE
The purpose of this study was to evaluate the possible variation of the maximum inspiratory and expiratory pressures after the application of inspiratory loads generating 65 percent of MIP in patients
minutes, 79.1 em H.O; M1P 20 minutes, 78.6 em H.O; MIP 30 minutes, 79.6 em HsO. The MEP was not different from the basal value. We concluded that in patients with COPD, MIP decreases sigoi6cantly after inspiration through umbral inspiratory weight equal to 65 percent MIP and does not return to basal value for 30 miQutes. The MEP does not change with respect to basal determination. (Cheat 1990; 97:618-20) MIP =maximal inspiratory pressure; MEP =maximal expiratory pressure; TLIM =time from the start of the test to exhaustion; Tlfl'TOI' =inspiratory' time-total time ratio
with stable COPD. MATERIAL AND METHODS
Sample
The study was conducted on eight male patients with COPD in stable phase, that is, the patients had not shown any symptoms of acute relapse in a period of at least two months prior to the study. The average age was 60.57±7.59 years, the height was 162.14± 10.43 em, and the weight was 65±9.7 kg. The patients did not have any other type of cardiorespiratory, endocrine, neuromuscular, or hepatic illness. We explained the protocol to be followed and all patients gave their consent. Various tests were conducted simultaneously within the first week of inclusion in the study. Respiratory Function Study An OHIO 827 unit (Sensor Medics) was used to determine the following factors: simple and postbronchodilator spirometry and measurement of pulmonary volumes by the technique of helium dilution and CO transfer (Dco, KCO). The American Thoracic Society rules•• were followed and the values found were compared with those gathered in the normal population.•• The MIPs and maximum expiratory pressures (MEPs) were measured from residual volume and TLC by the method of Black and Hyatt.l1 To obtain these values, a dry manometer connected to a pressure transducer with range of 0 to 300 em H10 (Sibelmed) was used. The signal was amplified and polygraphically recorded by means of a 12-channel polygraph (Sensor Medics). To obviate the learning etTect, a minimum of ten maneuvers were performed up til at least three of the determinations varied by less than 5 percent." The maneuvers were repeated immediately after finishing the load test and after 10, 20, and 30 minutes.
Inspiratory Load That
*From the Servei de Pneumologia, Hospital Germans Trias i Pujol, Barcelona, Spain. Supported by grant FISS88. Manuscript received April 6; revision accepted August 31.
818
A modification of the Nickerson and Keens method• was applied. After placing the patient in the sitting position with his back resting against a rigid support, application was made of a noncollapsible mouthpiece joined to a Hans Rudolph two-way valve (2700) in Variation In Maxlnun Inspiratory and Expiratory
~18
In COPO (Fiz et el)
Table 1- Functional and Nutritional \bluea of the Sample Studied* Factor
Value, Mean±SD
FEV,,L FVC,L FEV,IFVC TLC,L RY,L RV/fLC FRC,L Po1 , mm Hg Pco1 , mmHg pH Sat Hb,% Dco,% KCO,% TLIM, minutes Weight, kg TSF, mm• Circum, em
1.46±0.78 2.59±0.74 48.8± 14.2 6.8±2.1 3.8±1.0 55.4±6.3 4.6±1.4 72.4±0.02 35.7±6.8 7.41±0.02 94.4± 1.6 74.4±45.4 73.8±29.6 3.7±1.9 65±9.7 11.2±4.0 28.3±3.4
%Predicted 46±18.3 67±12.6 117.4± 18.7 180.3±44.7 152.1±43.6
105.1±10.9
*TSF =triceps pinch measured with caliper; Circum= circumference of the upper arm; and TUM =elapsed time basal to exhaustion. which another valve was installed, and different weights were inserted through the latter. The weight was increased until the patient generated a mouth pressure equivalent to 65 percent of his MIP (threshold pressure). Once the proper load was known, the patient breathed through the device until the threshold pressure calculated during three consecutive breaths ceased to be generated (exhaustion). The time that elapsed from the start of the test to exhaustion (TUM) was counted. During the test, the pressure exerted was controlled at all times by a polygraph recording, preventing it from dropping below the threshold pressure. The inspiratory time-total time ratio ('Ii/I'ror) was kept constant and the respiratory frequency was approximately 20 breaths per minute. Nutritional Study As part of the nutritional study, the following measurements were taken: weight as a percentage of the control, body fat content measured as a percentage of total body weight (triceps pinch with caliper), and circumference of the upper arm in order to obtain muscle content. In all measurements we followed the rules of Driver and Lebruw. ••
Statistical Study
We applied the Friedman test and a Wilcoxson test of sign-range.
REsuLTS It can be seen in Table 1 that there is evidence that
the patients suffered a moderate obstruction of air and the volumes are increased. Three of the patients had a Dco of less than 80 percent due to clinical and radiologic signs of pulmonary emphysema.l9 The average TLIM of the sample was 3. 7 ± 1.96 minutes. The anthropometric measurements were normal. Table 2 shows the MIP and the MEP of the patients at the basal stage, on exhaustion, and at 10, 20, and 30 minutes following exhaustion. There was a global significant difference between the five groups (Friedman test: p
DISCUSSION
The studies that have been performed on respiratory muscle endurance are based on the capacity of the respiratory muscles to sustain and generate high levels of pressure. The most common test consists of generating a pressure against a given resistive inspiratory load. 1·2 •3·20 In our study, we used the Nickerson, Keens and Kelsen methods, 3·4 •21 that consist of breathing through a constant threshold load equivalent to 65 percent of the MIP. This pressure lies within the range of critical pressure required to induce respiratory muscle fatigue in normal subjects. 19·22 The TiffTOT ratio was kept constant at 0.5, as variations in this ratio during the test change the time of endurance under the inspiratory load owing to the fact that the endurance capacity of the inspiratory muscles depends on the ventilatory pattern and on muscular force generated. 1 It is a proven fact that the application of submaximum inspiratory loads produces low-frequency fatigue in normal subjects. 13·23 The MIP is a measure of th~ maximum force generated by all the respiratory muscles and, in turn, it measures the muscular response to the high-frequency voluntary activation of the respiratory muscles. 24 In healthy
Table 2-Baaol MtmmallRBpiratory Prenure (MIP) and Mtmmal Expiratory Preaure (MEP) at &haunion and after 10, 20, and 30 Minutea* Minutes
MIP, cmH1 0 MEP, cmH1 0
Basal
Exhaustion
10
20
30
85.7±18.1
82.6±18.1 (ns) 141.3±51.9 (ns)
79.1±17.2 p
78.6± 16.3 p
79.6±19.1 p
139±43.9
•ns =not significant with respect to the basal determination. The significance was for p<0.05 (Wilcoxon test of sign range). CHEST I 97 I 3 I MARCH, 1990
819
individuals, the MIP decreases significantly five minutes after breathing has begun through the test with inspiratory load 21 and this reduction reflects the reduction in the mechanical capacity of the respiratory muscles to generate pressure. We have shown that in patients with COPD the MIP is decreased at the end of the test with respect to its basal value, but not significantly (85.7 to 82.6 em H 20). The decrease in MIP becomes significant (79.1 em H 20) ten minutes after exhaustion (Table 2) with respect to its basal value. The drop in MIP reaches a plateau after ten minutes and is maintained throughout the 30-minute recovery phase, so there is no recovery of maximum inspiratory muscle force. The decrease in MIP is probably related to the fatigue of rapid muscle fiber contraction (type II). For the most part, the fibers are responsible for respiratory muscle force25 and these muscle fibers are activated with a high frequency, but the inspiratory load test measures endurance of respiratory muscle. 14 •22 We cannot discard the possibility that the decrease in MIP is caused by a motivational effort; however, if this is indeed the case, we think that the MIP would decrease significantly at exhaustion and not ten minutes after. Also, it is curious that MEP did not decrease as well. We may conclude that in patients with COPD, the decrease in MIP lasts 30 minutes after the application of inspiratory loads and consequently, the high-frequency fatigue extends even beyond 30 minutes after exhaustion of the patient. The MEP did not vary after application of loads, although insignificant increases were obtained in it, probably the result of the learning effort. Musculature showed no fatigue, or at least no high-frequency fatigue, which seems to be related to the normality of the MEPs of the sample (MEP= 139.4 ±43.9). Therefore, the application of resistive inspiratory loads does not produce fatigue of the expiratory muscles as is the case in normal subjects. 26 CoNCLUSIONS
On the basis of foregoing results, it may be said that the MIP decreases in the patients with COPD after the application of inspiratory loads equivalent to 65 percent ofMIP. The drop in MIP begins to take place at the end of the test and becomes significant ten minutes after exhaustion, without returning to its basal value even beyond 30 minutes after the end of the test. The MEP does not vary with respect to the value obtained at rest. REFERENCES
1 Bellemare F, Gmssino A. Effect of pressure and timing on contraction on human diaphmgm fatigue. J Appl Physiol1982;
620
53:1190 2 McCool FD, McCannor LD. Pressure-flow effects on endurance of inspiratory muscles. J Appl Physiol1986; 60:299 3 Roussos CS, Macklem Pr. Diaphragmatic fatigue in man. J Appl Physiol1977; 43:189 4 Nickerson T, Kens G. Measuring ventilatory muscle endurance in humans as sustainable inspimtory pressure. J Appl Physiol 1982; 52:768-72 5 Bellemare F, Grassino A. Fbrce reserve of the diaphmgm in patients with chronic obstructive pulmonary disease. J Appl Physiol 1983; 55:8 6 Bjerre-Jepsen K, Seeber NH. Inspiratory resistance training in severe chronic obstructive pulmonary disease. Eur J Respir Dis 1981; 62:405-11 7 Pardy R, Rivington L. The effects of inspimtory muscle training on exercise performance in chronic airflow limitation. Am Rev Respir Dis 1981; 123:426-33 8 Pardy R, Macklem P. Inspiratory muscle training compared with physiotherapy in patients with chronic airflow limitation. Am Rev Respir Dis 1981; 123:421-25 9 Estrup C, Lyager S, Olsen C. Effect of respiratory muscle training in patients with neuromuscular diseases and in normals. Respiration 1986; 50:36-43 10 Supinski GS, LevinS, Kelsen SG. Caffeine effect on respiratory muscle endurance and sense of effort during loaded breathing. J Appl Physiol1988; 9:225-36 11 Jones DT, Thompson RJ. Physical exercise and resistive breathing training in severe chronic airways obstruction: are they effective? Eur J Respir Dis 1985; 67:159-66 12 Grassino A, Bellemare F. Force reserve of the diaphragm in COPD patients. Rev Tx Mal Respir 1980; 23-9 13 Martin J, Engel JA. The role of respiratory muscles in the hyperinflation of bronchial asthma. Am Rev Respir Dis 1980; 121:441-48 14 Narinder S, Arora MD, Rochester. COPD and human diaphragm muscle dimensions. Chest 1987; 91:5 15 Standardization of spirometry 1987-update. Am Rev Respir Dis 1987; 136:1285-98 16 Roca J, Segarra F, Rodriguez R. Static lung volumes and singlebreath diffusing capacity reference values from a Latin population. Am Rev Respir Dis 1985; 131:4(pt 2) A352 17 Black LF, Hyatt RE. Masimal inspiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis 1969; 99:696-702 18 Driver AG, Lebruw M. Nutritional assessment of patients with chronic obstructive pulmonary disease and acute respiratory failure. Chest 1982; 82:568-71 19 Gibson GJ. Clinical tests of respiratory function. London: Macmillan Press. 1984; 150-52 20 Esau SA, Bellemare F, Grassino A. Changes in relaxation rate with diaphragmatic fatigue in humans. J Appl Physiol 1983; 54:1353 21 Supinski GS, Clary SJ, Kelsen SG. Effect of inspiratory muscle fatigue on perception of effort during loaded breathing. J Appl Physiol1987; 62:3()().07 22 Roussos C, Fixley M, Cross D, Macklem PT. Fatigue of inspiratory muscles and their synergic behavior. J Appl Physiol 1979; 46:897-904 23 Moxham J, McGreen. Contractile properties and fatigue of the diaphragm in man. Thorax 1981; 86:164-68 24 Thomas K, Aldrch MD. Respiratory muscle fatigue. Clin Chest Med 1988; 9:225-36 25 Gary C, Sieck PD. Diaphragm muscle: structural and functional organization. Clin Chest Med 1988; 9:195-210 26 Martin J, Engel JA. The behaviour of the abdominal muscles during inspiratory mechanical loading. Respir Physiol 1982; 50:63-73 Variation In Maximum Inspiratory and Expiratory Pnlssura In COPD (Fiz et a/)