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(Chest. 2001;120:102-108.)
© 2001 American College of Chest Physicians

Respiratory Muscle Strength, Lung Function, and Dyspnea in Patients With Sarcoidosis*

Ahmet Baydur, MD, FCCP; Munif Alsalek, MD; Stan G. Louie, PharmD, PhD and Om P. Sharma, MD, FCCP

* From the School of Medicine and Los Angeles County and University of Southern California Medical Center (Drs. Baydur, Alsalek, and Sharma), Department of Medicine, Division of Pulmonary and Critical Care Medicine, and School of Pharmacy (Dr. Louie), Department of Pharmacy, University of Southern California, Los Angeles, CA.

Correspondence to: Ahmet Baydur, MD, FCCP, GNH 11–900, 2025 Zonal Ave, Los Angeles, CA 90033


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Sarcoidosis is a systemic granulomatous disorder that is estimated to involve the skeletal muscles in up to 50% of patients. There is little information on the relationship among respiratory muscle strength, lung volumes, and the degree of dyspnea in patients with sarcoidosis.

Design and patients: Lung function and maximal respiratory muscle force generation were measured in 36 patients with sarcoidosis (24 patients with pulmonary parenchymal infiltration) and 25 control subjects free of cardiorespiratory disease. Dyspnea in the sarcoidosis patients was quantitated by a score based on an activity tolerance assessment scale (ranging from rest to climbing hills or stairs).

Setting: Outpatient clinics of two teaching hospitals.

Results: Mean FVC, maximal voluntary ventilation, total lung capacity (TLC), functional residual capacity, residual volume (RV), and diffusing capacity of the lung for carbon monoxide (DLCO) were all at least 16% less than corresponding control values (in all cases, p < 0.001), while maximal inspiratory mouth pressure (PImax) and maximal expiratory mouth pressure (PEmax) were 37% and 39% less, respectively, than control values (both at p < 0.0001). PImax and PEmax declined with increasing dyspnea in a more graded, steady manner than did spirometric and DLCO values. For all measurements, however, the lowest mean values were found in patients with the most severe level of dyspnea. Strong inverse relationships were observed between PEmax and PImax with dyspnea level (p < 0.0001 and p < 0.01, respectively). Both PImax and PEmax correlated best with absolute values of FVC, while only PEmax correlated with RV (absolute and percent predicted) and percent predicted values of TLC.

Conclusions: Maximal respiratory pressures correlate more closely with dyspnea level than lung volumes and DLCO. Since dyspnea is the most common presentation in early to moderately advanced sarcoidosis, respiratory pressures may be a more reliable index of functional work capacity and reflection of activities of daily living than standard tests of lung function.

Key Words: dyspnea • lung volumes • maximal mouth pressures • respiratory muscles • sarcoidosis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Sarcoidosis is a systemic granulomatous disease of unknown origin in which asymptomatic muscle involvement is believed to occur in 50 to 80% of patients.1 Symptoms are found in 1 to 2% of patients,2 3 and occur in the form of pain, weakness, atrophy, pseudohypertrophy, or palpable nodules. While sarcoid granulomas can be demonstrated in random skeletal muscle biopsy specimens in many patients, their presence has failed to show a clear-cut relationship with the degree of respiratory muscle weakness.4 In the absence of systemic or metabolic factors that might contribute to generalized muscle weakness, decreased lung volume in patients with sarcoidosis may contribute to diminished inspiratory and expiratory muscle strength and dyspnea.

Previous authors5 have found correlations between respiratory muscle strength (RMS) and endurance time and symptoms and quality-of-life disturbances in patients with sarcoidosis. To our knowledge, however, there are no studies that specifically describe a relationship among respiratory muscle weakness, lung volume, and dyspnea in patients with sarcoidosis. Individuals with weak respiratory muscles experience intolerable exertional discomfort and dyspnea, which occur at lower power outputs than in those with strong muscles. Thus, respiratory muscle weakness in the presence of a respiratory disorder may contribute to exercise intolerance independent of pulmonary dysfunction.

The aim of this study was to assess RMS and its relationship to lung volume in patients with sarcoidosis. A secondary aim was to determine the relationship between RMS and dyspnea.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Thirty-six outpatients with sarcoidosis who attended the clinics of the University of Southern California University Hospital, and Los Angeles County and University of Southern California Medical Center were studied. The diagnosis of sarcoidosis was based on clinical features together with biopsy specimen-proven noncaseating epithelioid cell granulomas. The conditions of the patients were staged according to the criteria described by Scadding.6 Five patients had no radiographic evidence of thoracic involvement (stage 0), 7 patients demonstrated only nodal involvement (stage 1), 15 patients showed parenchymal involvement alone (stage III), 8 patients demonstrated both parenchymal and nodal involvement (stage II), and 1 patient had extensive pulmonary fibrosis (stage IV). None of the patients presented with symptoms of peripheral muscle involvement. Only one patient demonstrated a significant anemia (hemoglobin level of 6.9 g/dL); otherwise, none of the participating subjects had any medical history that might have influenced quality of life. Patients with significant comorbidity (eg, cardiac and other respiratory disorders) were excluded. Four patients were receiving prednisone at the time of the study: three patients with stage III disease and one patient with stage II disease. The highest dosage of prednisone any patient received was 20 mg/d. Patients were compared to a control group of 25 nonsmoking subjects free of cardiorespiratory illness. Their clinical characteristics and respiratory function data are shown in Table 1 . All subjects read and signed written consents approved by the investigational review board of the medical center.


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  		Table 1. Physical Characteristics, Respiratory Function, and Muscle Strength Data in 36 Patients With Sarcoidosis and 25 Control Subjects*

 
Each patient underwent a physical examination, a CBC count, an automated serum chemistry panel, and posteroanterior and lateral upright chest radiographs. Pulmonary function studies were performed with the subjects in the seated position. At least three FVC maneuvers were obtained using a 10-L water displacement spirometer (GS Module; Warren E. Collins, Inc.; Braintree, MA). The spirographic curve yielding the greatest FEV1, provided the FVC was within 10% of the best FVC, was used for the calculation of FVC and FEV1. Their predicted values were from Schoenberg et al.7 Reference values for maximal voluntary ventilation (MVV) were from Grimby and Soderholm.8 Lung volumes were measured by the helium dilution technique (Warren E. Collins, Inc.), and their reference values were from Crapo et al.9 The diffusing capacity of the lung for carbon monoxide (DLCO) was measured by the single-breath method; reference values were from Cotes.10 RMS was defined as follows: (PImax [% predicted]) + PEmax [% predicted])/2, where PEmax = maximal expiratory mouth pressure, and PImax = maximal inspiratory mouth pressure.

Measurements of RMS were obtained using the method of Black and Hyatt.11 PImax was measured at least five times at residual volume (RV), while PEmax was similarly recorded at total lung capacity (TLC). The best effort of each set was recorded. A small needle was inserted through the side of the mouthpiece to prevent collapse of the upper airway during inspiratory efforts.

Dyspnea Evaluation
A simple scale for the quantification of the perception of dyspnea modified from that of the British Medical Research Council (MRC)12 and based on exertion level was used in patients with sarcoidosis. Subjects were asked if and when they got short of breath. Scores were assigned from 0 to 4, with the higher values indicating increasing dyspnea: level 0 = does not feel dyspnea at all; level 1 = dyspnea while climbing hills or stairs; level 2 = dyspnea while walking at a rapid pace on level ground; level 3 = dyspnea while walking at own pace on level ground; level 4 = dyspnea at rest.

Statistical Analysis
For all variables, descriptive statistics (mean, SD, and SE) were generated separately for the sarcoidosis patients and the control group. Due to the skewed nature of many of the score distributions, nonparametric statistical procedures were used to conduct hypothesis tests.13 With respect to each of the study parameters shown in Table 1 , Wilcoxon rank-sum tests were used to assess the significance of differences in central tendency between patients with sarcoidosis and control subjects. Analysis of variance was performed to assess relationships between maximal respiratory pressures and lung volumes and dyspnea scores. Multiple comparisons seeking significant differences among group means between dyspnea scores and respiratory functions were performed using Tukey’s method.13 All significance tests were two tailed and were conducted at the 0.05 {alpha} level.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Table 1 lists the means ± SDs of the physical characteristics and physiologic data for the sarcoidosis patients and control subjects. As can be seen, patients with sarcoidosis had functional values that were overall significantly less than corresponding values for the control subjects. In particular, FVC, MVV (as percent predicted), TLC, functional residual capacity (FRC), and DLCO (as percent predicted) were 38% (p < 0.0001), 21% (p < 0.0001), 30% (p < 0.0001), 13% (p < 0.001), and 16% (p < 0.006) less, respectively, than corresponding control values. PEmax and PImax were 39% (p < 0.0001) and 37% (p < 0.0001) less, respectively, than the corresponding control values.

Based on the dyspnea evaluation questionnaires, 7 patients with sarcoidosis reported no dyspnea at all (level 0), while 3 patients reported level 1, 14 patients reported level 2, 7 patients reported level 3, and 5 patients reported level 4 dyspnea. Table 2 shows the distribution of values for FVC, FEV1, MVV, TLC, RV, DLCO, PEmax, and PImax in control subjects and patients with sarcoidosis according to dyspnea score. Patients who were dyspneic while walking on level ground at their own pace (level 3) had values of FVC, FEV1, TLC, RV, MVV, and DLCO that were 49% (p < 0.01), 50% (p < 0.01), 41% (p < 0.01), 32% (p < 0.01), 45% (p < 0.05), and 36% (p < 0.01) less, respectively, than the corresponding control values (Table 2) . PEmax and PImax in patients with grade 3 dyspnea were also 36% and 39% less than corresponding control values, respectively (p < 0.01). While in most cases, lung volumes and DLCO trended downward as the dyspnea score increased, the changes were not statistically significant (Table 2) . By contrast, there were statistically significant declines in PEmax and PImax as the dyspnea score increased (Fig 1 and Table 2 ). In Figure 1 , PEmax and PImax are assessed as continuous variables, as percent predicted values, and correlate strongly with dyspnea score. There was also an increase in the predictability of breathlessness when RMS (PImax [% predicted] + PEmax [% predicted])/2, was used (Fig 2 ). Again, no such relationship was found between dyspnea score and lung functions. TLC values (as percent predicted) in patients with radiographic stage II and III disease were 12% and 17% less, respectively, than in patients with stage I disease (both p < 0.05), while their DLCO was 26% and 15% less (both p < 0.05), respectively, than in patients with stage I disease (Table 3 ).


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  		Table 2. Relationship Between Dyspnea Score and Respiratory Function Tests*

 


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  		Figure 1. Relationships between (top, a) PEmax and (bottom, b) PImax, and dyspnea score using Pearson’s correlation coefficient.

 


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  		Figure 2. Relationship between RMS (top, a) (PImax [% predicted] + PEmax [% predicted])/2 (bottom, b) (PImax + PEmax)/2(cm H2O) and dyspnea score, using Pearson’s correlation coefficient.

 

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  		Table 3. Key Pulmonary Functions by Disease Stage in 36 Patients With Sarcoidosis*

 
Table 4 lists Pearson’s correlation coefficients with maximal respiratory pressures and variables of lung volume in patients with sarcoidosis. There were statistically significant linear correlations between PEmax and FVC (in liters; p < 0.05), PImax and FVC (p < 0.01), and PImax and FRC (p < 0.05).


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  		Table 4. Correlations Between Maximal Respiratory Pressures and Thoracic Volumes in 36 Patients With Sarcoidosis*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The key findings in our study of patients with sarcoidosis are (1) a progressive, statistically significant decline in maximal respiratory (mouth) pressures with increasing severity of dyspnea; (2) certain strong direct correlations between maximal respiratory pressures and lung volumes; and (3) absence of relationships between dyspnea ratings and lung functions.

We found that dyspnea ratings (based on a scoring system modified from that of the MRC) correlated best with maximal respiratory muscle force generation but not with results of pulmonary function. These findings were not unexpected, since dyspnea is a subjective symptom and has not corresponded with spirometric measurements in many previous studies in patients with COPD.14 15 16 Using factor analysis, some authors17 18 have found that dyspnea ratings, maximal respiratory pressures, and lung function are separate factors that independently characterize the condition of patients with COPD. Furthermore, others who have studied patients with interstitial lung disease describe either no relationship,19 or at best limited correlation,20 between lung volumes and breathlessness. Dyspnea results from dissociation or a mismatch between central drive and afferent information from receptors in the airways, lungs, and chest wall structures.21 This mismatch contributes to the dyspnea experienced by patients with sarcoidosis and skeletal muscle weakness5 22 23 in whom central drive has been shown to be increased.23

In the present study, the patients with the lowest overall TLC and DLCO values (as percent predicted) were those with radiographic stages II through IV disease (Table 3) . This trend was also observed with PImax and PEmax, however, although differences among disease stages were not statistically significant. In our study, however, we found that respiratory muscle pressures demonstrated a more consistent, graded decline with increasing dyspnea level than did DLCO or, for that matter, lung volumes (Table 2) . These findings are similar to those described by Wirnsberger et al,5 and suggest that maximal mouth pressures may be more sensitive than the DLCO or vital capacity (VC) in predicting functional impairment in sarcoidosis. Recently, Hamilton et al24 found that muscle strength was a significant contributor to symptom intensity and work capacity in 4,617 subjects (of whom 3,698 [80%] had cardiorespiratory disorders). Dyspnea and RMS in all groups were closely related.

While the degree of physiologic impairment in sarcoidosis has been shown to correlate with the radiographic stage of disease,25 the overlap between stages is large enough to make it difficult to predict a given patient’s lung function from the radiograph. In the present study, 4 patients (33%) with radiographic stage 0 or stage I had a mean TLC of 72% predicted, while conversely, 13 patients (54%) with stage II through IV had a mean TLC of 90%. The finding of a normal TLC or VC despite a decrease in maximal respiratory pressures in some patients may be related to two factors: (1) preservation of diaphragmatic function, reflecting sparing from involvement by sarcoidosis; or (2) because it has considerable reserve as a pressure generator.26 Thus, the diaphragm must be markedly weakened before its function as a volume generator is impaired. Conversely, granulomatous involvement of the diaphragm and other respiratory muscles might alter force generation and account for the reduced lung volumes and greater sensation of dyspnea. Isolated or small groups of cases of histologic evidence for granulomatous involvement of respiratory muscle have been reported in sarcoidosis.27 28

DeTroyer et al29 found that by plotting maximal mouth pressure values of patients with chronic neuromuscular disorders against their VC, there were reductions in VC disproportionate to the degree of muscle weakness, consistent with the change in pulmonary elastic characteristics which in many multisystem diseases may be the underlying mechanism of dyspnea. In addition, our finding of a linear, not exponential, relationship between maximal pressure and volume suggests the following: (1) as in neuromuscular and interstitial lung diseases,29 progressive decrease in lung volume may be a more useful test than RMS for following the course of disease; and (2) mechanisms other than respiratory muscle weakness are implicated in loss of lung volumes. Other factors such as poor nutrition and drug therapy did not significantly impact our results. None of our patients were undernourished or had clinically significant cardiac disease, which could have contributed to the muscle weakness. Factors such as the use of corticosteroids were insignificant since only four patients (11%) were receiving prednisone, and at relatively low doses. Only one patient had significant anemia (hemoglobin level of 6.9 g/dL).

We used a modified MRC dyspnea scale that focuses on the patient’s report of dyspnea while either walking distances or climbing stairs.12 This form of dyspnea quantification is useful as a guide at a single point in time. We realize that with this scale it may be difficult to establish a change in dyspnea while monitoring therapy, but this was not an issue in this cross-sectional study. Another shortcoming of this scale is the absence of clear limits between grades,30 and that it relates to the magnitude of the tasks that provokes dyspnea, but not the associated effort.15 In addition, because the intensity of exercise-related dyspnea depends on the rate of work performance, patients may decrease work performance, minimizing the intensity of symptoms.14 Since people may overestimate or underestimate their capacity to exercise, the established measures (on which our scale is based) correct for some of these limitations, but do not deal directly with the possibility that patients may evaluate their work performance optimistically. Finally, the MRC scale has been validated primarily in patients with chronic obstructive lung disease, and not in those with interstitial lung disease. For these reasons, we considered it most appropriate to relate our modified MRC dyspnea score to RMS by applying Pearson’s correlation.

Generally, the maximum static mouth pressure during an inspiratory or expiratory effort is a simple means of assessing the combined strength of the inspiratory or expiratory muscles, respectively. Measurement of maximal mouth pressures, however, has its own limitations. When interpreting PImax and PEmax, submaximal efforts cannot be distinguished from central fatigue; this represents a major limitation, particularly in dyspneic patients.31

In conclusion, RMS is decreased in patients with sarcoidosis. Decreased RMS was found to be related to a dyspnea/activity scale, with patients exhibiting steadily decreasing RMS in a graded fashion as their level of dyspnea increased. This was in contrast to lung volumes and DLCO, which were found to decrease less consistently with increase in the dyspnea score. Since fatigue and general weakness are difficult to assess objectively, measuring respiratory muscle function seems to quantify functional impairment and reflect symptoms more consistently than lung volumes and gas transfer.


   Acknowledgements
 
The authors thank members of the pulmonary function laboratories in obtaining these data, and Irene Hernandez and Carolina De La Cruz in preparation of this article.


   Footnotes
 
Abbreviations: DLCO = diffusion capacity of the lung for carbon monoxide; FRC = functional residual capacity; MRC = Medical Research Council; MVV = maximal voluntary ventilation; PEmax = maximal expiratory mouth pressure; PImax = maximal inspiratory mouth pressure; RMS = respiratory muscle strength; RV = residual volume; TLC = total lung capacity; VC = vital capacity

Received for publication August 19, 1999. Accepted for publication February 14, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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