Relationship Between Respiratory

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1 Relationship Between Respiratory Muscle Strength and Lean Body Mass in Men With * Yoshihiro Nishimura, MD; Masaharu Tsutsumi, MD; Hiroyuki Nakata, MD; Tohru Tsunenari, MD; Hitoshi Maeda, MD; and Mitsuhiro Yokoyama, MD It has been suggested that low body weight may be associated with decreased respiratory muscle function in, but the precise mechanism is not known. Since body compositional change inevitably accompanies body weight change, we decided to study the possible relationship between respiratory muscle strength and body composition in patients with. We studied respiratory muscle strength, pulmonary function, and body composition in 24 Japanese male patients with. Patients were divided into two groups according to their body weight (group A, body weight lower than 80% of ideal body weight vs group B, 80% or more) and a comparison was made together with age-matched controls (group C). Maximal inspiratory mouth pressure (Plmax) and maximal expiratory mouth pressure (PEmax) were measured by a previously reported method. Body compositional analysis was performed using dual energy x-ray absorptiometry (DXA; Norland XR26). It showed significantly lower fat body mass (FAT), FAT/ body weight%, and lean body mass (LEAN) in group A than those in group B. The Plmax in group A was significantly lower than that in group B and C (44.2 ± 13.8, 76.4 ± 29.9, and 88.6 ± 18.1 cm H20, respectively). PEmax in group A was also significantly lower than that in group B and group C (61.9±20.1, 86.7±26.8, and 90.4 ± 17.6 cm H20, respectively). Both Plmax and PEmax were significantly correlated with LEAN (r=0.656, r=0.591, p<0.01, respectively) in patients with. These results show that respiratory muscle strength is closely associated with body weight and lean body mass in patients with. The present approach to compare respiratory muscle strength with lean body mass should be useful for studying the mechanism of respiratory muscle weakness in patients with. (Chest 1995; 107: ) BMC=bone mineral content; BMI=body mass index; DXA=dual-energy x-ray absorptiometry; FAT=fat body mass; FEV1=forced expiratory volume in 1 s; FVC=forced vital capacity; LEAN=Iean body mass; PEmax=maximal expiratory mouth pressure; PImax=maximal inspiratory mouth pressure; RV=residual volume; TLC=total lung capacity; VC=vital capacity Key words: body composition; body weight; ; pulmonary function; respiratory muscle strength Respiratory muscle weakness is observed in patients with, neuromuscular disease, and chronic heart disease. 15 The contributing factors for respiratory muscle weakness in these conditions are postulated to be malnutrition-related biochemical, physiologic, and anatomic changes, generalized muscle atrophy, increased residual volume, and reduced blood flow to the respiratory muscle. More studies are necessary to elucidate possible mechanisms in each specific condition. In the case of, malnutrition appears to be one of the major contributing factors for respiratory muscle weakness, because malnutrition is often found in patients with and moreover, in advanced *From the Department of Medicine, Takatsuki General Hospital, Takatsuki, (Drs. Nishimura, Tsutsumi, Nakata, and Tsunenari); and the First Department of Internal Medicine, Kobe University School of Medicine, Kobe, Japan (Drs. Maeda and Yokoyama). Manuscript received June 7, 1994; revision accepted September 21. Reprint requests: Dr. Nishimura, Takatsuku General Hospital, Kosobe-cho, Takatsuki 569 Japan 1232 cases, it is an almost inevitable manifestation of the disease.' In general, patients with malnutrition show body weight loss and presumably some kind of body compositional changes. Thus, it is reasonable to speculate that deranged respiratory muscle strength may be associated with body compositional changes, especially those changes that may be closely associated with body weight loss. Indeed, there are some reports that suggest that the loss of respiratory muscle strength was directly proportional to the degree of weight loss in nutritionally depleted patients.5 However, those indirect assessments of the weight of the diaphragm have obvious intrinsic limitations in the clinical settings. Newly developed dual-energy x-ray absorptiometry (DXA) made it possible to analyze body composition, bone mineral content (BMC), lean body mass (LEAN), and fat body mass (FAT).6 Although this method can assess only anatomic parameters by nature and may not be a good indicator of muscle strength, nevertheless its convenience and subjective-

2 ness attracted us to initiate this study. First we studied which body component is affected most in patients with with low body weight and then studied whether this component has an association with respiratory muscle weakness. We found that lean body mass appears to be affected in patients with with low body weight and the parameters of respiratory muscle function seem to be closely related to this particular component of the body. Therefore, we propose that lean body mass loss that manifests itself as body weight loss may be an important contributing factor for respiratory muscle weakness in patients with. METHODS Subjects We studied in 24 male patients with. Diagnostic criteria for was forced expiratory volume in 1 s/forced vital capacity (FEV,:FVC) ratio less than 50% and response to bronchodilators less than 15%. The patients were in clinically stable conditions and had no congestive heart failure, recent respiratory infection within 4 weeks, malabsorption, or diabetes mellitus. All patients with were treated with long-acting theophylline derivatives (200 to 600 mg/d), but corticosteroids were used in only one of the patients with who received 5 mg of prednisolone per day for 2 years. We divided the patients into two groups on the basis of body weight per ideal body weight ratio.7 Group A consisted of 11 patients with low body weight (less than 80% of standard body weight). Group B consisted of 13 patients with 80% of standard body weight or more. Group C consisted of 13 age-matched controls to compare the respiratory muscle strength. Informed consent was obtained from each subject for this protocol. Respiratory Muscle Strength Maximal static inspiratory and expiratory mouth pressure was measured in all patients according to the technique of Black and Hyatt8 (using Vitalopower KH11, Chest MI Co Ltd, Tokyo, Japan). The time-pressure curve is displayed on a display. Maximal inspiratory mouth pressure (Plmax) was measured at level of residual volume (RV) and maximal expiratory mouth pressure (PEmax) was obtained at level of total lung capacity (TLC). Patients performed maximal inspiratory and expiratory efforts at least three times at two lung volume levels and we adopted the maximal values for analysis. The predicted values for age and sex correction were obtained from previously reported formulas, and percentages of Plmax and PEmax for predicted values were calculated (%Plmax and %PEmax, respectively). The formulas established for Japanese follow.9 Men: PImax= XAGE (r= , p<0.01) PEmax= XAGE (r= , p<0.05) Women: PImax= XAGE (r= , p<0.01) PEmax=93-.33XAGE (r= , p<0.05) Pulmonary Function Test Slow vital capacity (VC), FVC, FEV1, RV, and TLC were measured using the spirometer of computer processing (Chestac 25, Chest MI Co Ltd; Tokyo, Japan), and the ratio of FEV, for forced vital capacity (FEV,:FVC) was calculated. Two milliliters of arterial blood were sampled anaerobically from the brachial artery while the patient breathed room air, and the blood was quickly analyzed to obtain arterial oxygen tension (PaO2), arterial carbon dioxide tension (PaCO2), and ph with a ph blood gas analyzer (model 213, Instrumentation Laboratories; Lexington, Mass.). Body Compositional Measurement Body composition was measured by DXA (XR-26, Norland) using whole-body absorptiometry software version Principles involved in DXA analysis of body composition were recently reviewed.'0 Briefly, unattenuated photon flux is recorded for each energy in air prior to the measurement and stored in the computer memory; then the patient is scanned and attenuated photon flux is recorded on a pixel-by-pixel basis for both energies as the photon beam scans the patients in a rectilinear fashion. Bone mineral content and soft-tissue mass that is partitioned into fat mass (FAT) and nonfat, lean mass (LEAN) was calculated separately based on its difference in mass attenuation coefficients." The patient disrobed completely and put on a cotton gown so that no artificial density was added during body composition analysis. The patient then lay down on the patient pad in a supine position and his/her whole body was scanned by the scanner. It usually takes about 15 min to complete the whole analysis. Each value of the body composition was expressed as kilograms. The percentage of BMC, LEAN, and FAT was calculated by dividing each absolute value of body composition by total body mass, and expressed as %BMC, %LEAN, and %FAT, respectively. Body mass index (BMI) was calculated by dividing body weight (kg) by squared body height (m2). Statistical Analyses All values are given as mean + SD. Statistical differences for variables of respiratory muscle strength and pulmonary function were analyzed by analysis of variance. Correlation analysis was performed between parameters of respiratory muscle strength and body composition. Values of p<0.05 were considered to be statistically significant. RESULTS Age, Body Height, Body Weight, and BMI As shown in Table 1, there was no significant difference in age and body height among three groups. In group A, body weight, percent of ideal body weight, and BMI were significantly lower than those in group B and C. Body weight of group B was not significantly different as compared with that of group C. Pulmonary Function In pulmonary function tests (Table 2), VC, %VC, and FEV1 of group A were significantly lower than Table 1-Anthropometric Data Controls, Group A Group B Group C Age, yr 71.5 ± ± ± 9.0 Body height, cm ± ± ± 4.4 Body weight, kg 43.8 ± 6.21t 55.3 ± ± 4.1 %IBW* 73.2 ± 7.31f 95.2 ± ± 7.2 BMI 16.2 ± 1.7 f ± ±1.5 %IBW=percent of ideal body weight. fp<0.05 compared with group B. $p<o.o5 compared with group C. CHEST / 107/5/ MAY,

3 Table 3-Respiratory Muscle Strength and Body Composition in Study Subjects* Controls Group A Group B Group C Respiratory muscle strength Plmax, cm H f ± 18.1 %PImax f ± PEmax, cm H f1 86.7± ±17.6 %PEmax f ± 16.3 Body composition BMC, kg %BMC ± 0.5 LEAN, kg 38.1±3.81f 42.4± ±4.7 %LEAN f ±6.8 FAT, kg f ±4.2 %FAT 9.0 ± 8.3f *%Plmax=percent of maximal inspiratory mouth pressure for predicted value; %PEmax=percent of maximal inspiratory mouth pressure for predicted value; %BMC=percent of bone mineral content per body weight; %LEAN=percent of lean body mass per body weight; %FAT=percent of fat mass per body weight. Values shown are means + SD. fp<0.05 compared with group B. Jp<0.05 compared with group C. Table 2-Pulmonary Function in Patients With Group A Group B VC, L * %VC * FEV1, L/s * FEV1/FVC, % ±8.7 TLC, L 5.72± %TLC RV, L ±0.50 RV/TLC, % PaO2, mm Hg 69.8 ± ± 13.0 PaCO2, mm Hg *p<0.05 compared with group B. those of group B. The TLC, RV, RV/TLC, and variables of arterial blood gas analysis showed no significant difference between the two groups with. Respiratory Muscle Strength Respiratory muscle strength of patients is also shown in Table 3. Plmax of group A was 44.2 ± 13.8 cm H20, which was significantly smaller than those in group B and group C (76.4 ± 29.9, cm H20, p<0.05, respectively). %PImax in group A was also significantly smaller than those in the other two groups. PEmax of group A was 61.9 ±20.1 cm H20, which was significantly smaller than those of group B and group C (86.7 ± 26.8, 90.4 ± 17.6 cm H20, p<0.05, respectively). %PEmax of group A was also significantly lower than those of group B and group C Body Composition Variables of body composition are shown in Table 3. The BMC of group A was significantly lower as compared with group C. The BMC of group A, however, did not significantly differ from that of group B. No significant difference of %BMC was found among three groups. LEAN was significantly lower in group A than in group B and group C. FAT was significantly lower in group A than in group B and group C. The %FAT in group A was also lower than in group B and group C. Relationship Between Respiratory Muscle Strength and Pulmonary Functions In the coefficient of correlation between respiratory muscle strength and variables of pulmonary function obtained from linear regression analysis, there were significant positive correlations among Plmax and VC, %VC, and FEV1 in patients with (r=0.426, r=0.426, r=0.432, p<0.05, respectively). Furthermore, these relationships were observed in PEmax in patients with (r=0.492, r=0.501, r=0.782, p<0.05, respectively). Respiratory muscle strength, however, had no significant correlation with TLC, RV, RV/TLC, PaO2, and PaCO2 in patients with. Relationship Between Respiratory Muscle Strength and Body Composition In the coefficient of correlation between respiratory muscle strength and body composition variables, there were significant positive correlations between Plmax and LEAN in both patients with and

4 Pimax (cmh20) 200 PEmax (cmh2o) ** o -, ~ 0 0-~ 0, 100 %b 0.~~~ LEAN (kg) FIGURE 1. Relationship between maximal inspiratory mouth pressure (Plmax) and lean body mass (LEAN) in patients with (closed circles) and in control subjects (open circles). The continuous line shows the regression line in patients with. The broken line shows the regression line in control subjects LEAN (kg) FIGURE 2. Relationship between maximal expiratory mouth pressure (PEmax) and lean body mass (LEAN) in patients with (closed circles) and in control subjects (open circles). The continuous line shows the regression line in patients with. controls (r=0.656, p<0.001, r=0.575, p<0.05, respectively) (Fig 1). Furthermore, PEmax significantly correlated with LEAN in patients with (r=0.591, p<0.01) (Fig 2). DISCUSSION Our results show that lean body mass change may be closely associated with decreased respiratory strength in patients with. It is not known from the present study whether a similar relation exists in normal subjects or other conditions that result in decreased respiratory function. However, it appears to be the case at least in normal male subjects, because we found age-dependent decrease after age 40 years in respiratory muscle strength.9 This pattern appears to be very similar to that described in LEAN differences in Japanese young, middle-, and old-age male control subjects."1 Moreover, Plmax had a significant correlation with LEAN in normal control subjects. It is therefore conceivable that LEAN may well be a good indicator of respiratory muscle strength at least in patients with and normal male subjects. In patients with, diaphragm muscle mass and thickness vary with body weight in a fashion similar to that in patients without. In normalweight patients with, diaphragm muscle mass, thickness, and area were within normal limits.1 Thurlbeck12 showed a similar linear relation between diaphragm and body weights in patients with emphysema. However, the functioning of the diaphragms of patients with stable, whose body weight is not reduced, is as good as in normal subjects at the same lung volume.13 In the present study, we also showed reduction in respiratory muscle strength in the patients with with body weight loss but not in the patients without weight loss or in control subjects. These results suggested that the patients with without body weight loss might still maintain their respiratory muscle mass and strength. FAT was significantly lower in group A as compared with groups B and C. It was slightly lower in group B as compared with group C, but did not reach statistical significance. These results suggest that FAT loss may precede a decrease in body weight below 80% of ideal body weight over the time course of. However, the role of fat metabolism in the relatively early stage of before body weight loss becomes obvious was not shown in this study. It appears to be a universal phenomenon in any kind of malnutrition caused by a body's fuel economy or it could be a compensatory mechanism to minimize LEAN loss that eventually leads to a better preservation of respiratory muscle function in patients with. The latter notion may be supported by our data that LEAN in group B did not significantly differ from that in group C. Further study is necessary to elucidate whether a -specific pattern of lipid metabolism may exist. Pulmonary function influences respiratory muscle strength. Rochester and Braun14 pointed out the importance of muscle length in determining muscle strength in. We found a significant correlation between respiratory muscle strength and both VC and FEV1. This could be explained by hyperinflation CHEST / 107 / 5 / MAY,

5 of the lungs, resulting in a decrease in tension produced by inspiratory muscle shortening. However, we could find no correlation between Plmax and RV. Moreover, there were no significant differences in both TLC and RV between the two groups with. Therefore, decrease in respiratory muscle strength may be affected by factors other than air trapping. The fact that acute hypercapnea can cause some interference with the development of maximal respiratory pressures has been shown in normal subjects.15 In the present study, there were no significant differences in variables of blood gas analysis between the two groups with. The variables of blood gas analysis were not significantly correlated with respiratory muscle strength. The limitation of the present study needs to be mentioned. This is not a longitudinal study but a cross-sectional study; therefore, we do not know how much body weight was "lost" during the long time course of in our patients. Further prospective study is necessary to quantitatively assess the degree of body weight loss, LEAN loss, and the decreasing rate of respiratory muscle strength. Such a study is now underway in our hospital. The clinical significance of the present study would be that if respiratory muscle weakness is closely related with a change in LEAN in patients with, it may be possible that any efforts to preserve LEAN in these patients would retard the deterioration in respiratory muscle function in some way. Indeed, there are some reports that special nutritional intervention may benefit patients with by improving pulmonary function.16 Much needs to be done before this approach proves useful, but our study provides a new approach to assessing body composition in clinical settings. Lastly, this study provides a new aspect for the study of respiratory muscle function. Since the first measurement of respiratory muscle function was reported more than 20 years ago, extensive study has been reported. Recently, we reported Japanese normative data for Plmax and PEmax,9 Plmax in patients with heart failure,4 and Plmax in patients with neuromuscular disease.3 The present study continues our effort to elucidate what factors should influence respiratory muscle strength in various states. Respiratory muscle strength was significantly correlated with age, pulmonary function, cardiac output, and generalized muscle atrophy. Since various factors are responsible for respiratory muscle strength, a change in LEAN may exist in these conditions and may affect respiratory muscle function at least in part. The assessment of the changes in body composition, especially in LEAN, should be important to elucidate the mechanism of respiratory muscle weakness in various conditions. These results show that respiratory muscle strength is closely associated with body weight and LEAN in patients with. The present approach to compare respiratory muscle strength with LEAN should be useful for studying the mechanism of respiratory muscle weakness in patients with. REFERENCES 1 Rochester DF. Malnutrition and the respiratory muscles. Clin Chest Med 1986; 7: Rochester DF, Arora NS, Braun NMT, et al. The respiratory muscles in chronic obstructive pulmonary disease (). Bull Eur Physiopathol Respir 1079; 15: Nishimura Y, Hida W, Taguchi 0, et al. Respiratory muscle strength and gas exchange in neuromuscular disease: comparison with chronic pulmonary emphysema and idiopathic pulmonary fibrosis. Tohoku J Exp Med 1989; 159: Nishimura Y, Maeda H, Tanaka K, et al. Respiratory muscle strength and hemodynamics in chronic heart failure. Chest 1994; 105: Openbrier D, Irwin M, Rogers RM, et al. Nutritional status and lung function in patients with emphysema and chronic bronchitis. 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