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(Chest. 2006;130:1496-1502.)
© 2006 American College of Chest Physicians

Impact of Impaired Inspiratory Muscle Strength on Dyspnea and Walking Capacity in Sarcoidosis*

Hans-Joachim Kabitz, MD; Felix Lang; Stephan Walterspacher; Stephan Sorichter, MD; Joachim Müller-Quernheim, MD and Wolfram Windisch, MD

* From the Department of Pneumology, University Hospital, Freiburg, Germany.

Correspondence to: Wolfram Windisch, MD, Department of Pneumology, University Hospital Freiburg, Killianstrasse 5, D-79106 Freiburg, Germany; e-mail: windisch{at}med1.ukl.uni-freiburg.de

Abstract

Background: Dyspnea and fatigue are frequent but poorly understood symptoms in sarcoidosis patients. This study was aimed at assessing the clinical impact of inspiratory muscle impairment on dyspnea and exercise tolerance. This is the first study using nonvolitional tests that are independent of the patient’s cooperation and motivation in addition to volitional tests of inspiratory muscle strength in patients with sarcoidosis.

Methods: Peak maximal inspiratory mouth pressure (PImaxPEAK), maximal inspiratory pressure sustained for 1.0 s (PImax1.0), twitch mouth pressure (TwPmo), lung function test results, blood gas measurements, 6-min walking distance (6MWD), and Borg dyspnea scale (BDS) scores were assessed in 24 male sarcoidosis patients and 24 healthy male control subjects matched for age and body mass index.

Results: Mean (± SD) PImaxPEAK (95.2 ± 25.3% vs 124.6 ± 23.4% predicted, respectively; p < 0.001) and PImax1.0 (85.6 ± 31.4% vs 125.8 ± 26.8% predicted, respectively; p < 0.001) were lower in sarcoidosis patients compared to control subjects. TwPmo tended to be lower in sarcoidosis patients, and there were three patients who had TwPmo values of < 1.0 kPa, which is a strong indicator of inspiratory muscle weakness. The mean 6MWD was 582 ± 97 m in sarcoidosis patients and 638 ± 65 in control subjects (p = 0.025). The mean BDS score was higher in sarcoidosis patients (3.3 ± 1.7 vs 0.2 ± 0.5, respectively; p < 0.001). Compared to maximal inspiratory pressure, lung function parameters, and blood gas levels, TwPmo was the strongest predictor for 6MWD (r = 0.663; p = 0.003) and BDS score (r = 0.575; p = 0.012) in sarcoidosis patients following multiple linear regression analysis.

Conclusions: Impairment of inspiratory muscle strength occurs in sarcoidosis patients, and has been suggested to be an important factor causing dyspnea and reduced walking capacity, but this is only reliably detectable when using nonvolitional tests of inspiratory muscle strength.

Key Words: inspiratory muscle strength • maximal inspiratory pressure • muscle weakness • phrenic nerve stimulation • twitch mouth pressure

Dyspnea and fatigue are some of the most often reported symptoms in patients with sarcoidosis.123456 The underlying conditions causing these symptoms have yet not been completely elucidated. Previous studies678 have postulated that respiratory muscle involvement might substantially contribute to dyspnea and fatigue in sarcoidosis patients. This is supported by the observation that granulomatous skeletal muscle involvement in sarcoidosis patients is possible, as shown by biopsy.910 Furthermore, 50 to 80% of sarcoidosis patients are thought to experience subclinical skeletal muscle involvement.911 Nevertheless, symptomatic muscle involvement has been suggested to be rare,3911 and diaphragmatic involvement has been proven only in rare case reports.1213

All studies that have indicated possible inspiratory muscle weakness in the past have used volitional tests of respiratory muscle strength.67101415 However, volitional tests are highly dependent on the cooperation and motivation of the patient, and it cannot be excluded with certainty that low values for inspiratory muscle strength simply reflect insufficient effort as a consequence of various reasons.16 Therefore, it has been suggested that nonvolitional tests of inspiratory muscle strength, which are independent of the patients’ cooperation and motivation, are needed to more reliably assess inspiratory muscle involvement in sarcoidosis patients.7

Assessment of inspiratory muscle strength using nonvolitional tests has not been previously performed in sarcoidosis patients. Therefore, the aims of the present study were, first, to assess inspiratory muscle strength in sarcoidosis patients using both volitional and nonvolitional tests and, second, to verify the clinical impact of inspiratory muscle impairment on dyspnea and exercise tolerance as assessed by a 6-min walking test.

Materials and Methods

The study protocol was approved by the institutional review board for human studies of the Albert-Ludwig University (Freiburg, Germany) and was performed in accordance with the ethical standards laid down in the Declaration of Helsinki, 2000. Informed written consent was obtained from all subjects.

Participants
Twenty-four nonsmoking male patients with sarcoidosis diagnosed according to the criteria of the latest American Thoracic Society/European Respiratory Society/World Association of Sarcoidosis and Other Granulomatous Disorders statement on sarcoidosis3 who were seen as outpatients in our department were studied. Based on the findings of chest radiographs, 4 patients presented with type I sarcoidosis, 10 patients presented with type II, 9 patients presented with type III, and 1 patient presented with type IV. The mean duration since diagnosis was 6.7 years (SD, 7.5 years). Eight patients were receiving therapy with oral corticosteroids (dose range, 5 to 10 mg of prednisolone equivalents per day). All patients were in a stable state with no change in medication and no complaints about skeletal muscle weakness during the last 3 months and after exercise. In addition, 24 healthy, nonsmoking, age-matched, and body mass index (BMI)-matched men without lung or thoracic rib cage disease who did not take any medication were studied.

Lung Function, Blood Analysis, and Exercise Testing
Lung function parameters were measured using body plethysmography (Masterlab-Compact; Jaeger; Hochberg, Germany) according to the official statement of the European Respiratory Society.17 A 6-min walking test was performed for exercise testing with the following measurements: 6-min walking distance (6MWD); dyspnea as assessed by the Borg dyspnea scale (BDS); and blood gas levels at rest and immediately after exercise. A venous blood sample was drawn from sitting subjects to provide data on neopterin, soluble interleukin-2 receptor (s-IL2-R), and angiotensin-converting enzyme (ACE) levels, since these serum markers are used to gauge sarcoidosis activity.181920

Tests on Inspiratory Muscle Strength
Maximal inspiratory pressure (PImax) was assessed (ZAN 100; ZAN GmbH; Oberthulba, Germany). Peak PImax (PImaxPEAK) and plateau PImax sustained for 1 s (PImax1.0) were measured at residual volume, as has been described previously by our group.21 According to the latter study, predicted values have been calculated.

Nonvolitional tests for the assessment of inspiratory muscle strength were provided by measuring twitch mouth pressure (TwPmo) during bilateral anterior magnetic phrenic nerve stimulation (Magstim 2002; Magstim Inc; Dyfed, Wales, UK).2223 An inspiratory pressure trigger (ie, twitch mouth pressure during inspiratory pressure triggering [TwPmoIn]) was used at –0.5 kPa, as has been described previously.24 During all measurements of TwPmo, breathing frequency and tidal volume have been recorded as previously described.24 TwPmo was measured until five acceptable pressure tracings were achieved, according to predefined and previously published criteria.24 According to previous recommendations, a cutoff value of 1.0 kPa was used to identify patients with reduced inspiratory muscle strength.25

Statistical Analysis
Statistical analysis was performed using a statistical software package (SigmaStat, version 3.1; Systat Software, Inc; Point Richmond, CA). All data are presented as the mean ± SD after testing for normal distribution (Kolmogorov-Smirnov test). Group comparisons between sarcoidosis patients and control subjects were performed using the unpaired t test if data were normally distributed or the Mann-Whitney rank test if data were not normally distributed. Both correlation and regression analyses were performed in sarcoidosis patients. For the correlation analysis, the Pearson product moment correlation was used. Regression analysis was performed in order to calculate predictors for clinical parameters (ie, BDS score and 6MWD). For multiple linear regression analysis, BDS score was used as the dependent variable, and PImaxPEAK, PImax1.0, TwPmoIn, FVC, and PaO2 at rest were used as independent variables. In a second analysis, 6MWD was used as the dependent variable with PImaxPEAK, PImax1.0, TwPmoIn, FVC, and PaO2 at rest used as independent variables. Statistical significance was assumed with a p value of < 0.05.

Results

Demographic data and lung function parameters are given in Table 1 . Ten patients had an FVC of < 80% predicted, and 5 patients had an FEV1/FVC ratio of < 70% predicted. Blood gas values and parameters of the 6-min walk test are shown in Table 2 . PaO2 and arterial oxygen saturation (SaO2) both at rest and after exercise were significantly lower compared to those values in control subjects (Table 2). In addition, sarcoidosis patients presented with a significantly higher degree of dyspnea and a significantly lower 6MWD. Skeletal muscle exhaustion or weakness of the legs was not reported in any patient.


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  		Table 1.. Demographic Data and Lung Function Parameters in Sarcoidosis Patients and Control Subjects*

 

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  		Table 2.. Blood Gas and 6-min Walk Test Values*

 
Volitional Tests of Inspiratory Muscle Strength
Volitional tests of inspiratory muscle strength indicated significantly lower values for both PImaxPEAK and PImax1.0 (in absolute values and as percent predicted), as is indicated in Table 3 and Figure 1 . However, both absolute values and predicted values for PImaxPEAK and PImax1.0 tended to be higher in control subjects compared to age-related and gender-related normal values, which have been achieved by the same methods.21 In patients with sarcoidosis, PImaxPEAK and PImax1.0 were significantly correlated to FVC (PImaxPEAK: r = 0.61; p = 0.002; PImax1.0: r = 0.50; p = 0.007) and total lung capacity (PImaxPEAK: r = 0.61; p = 0.002; PImax1.0: r = 0.48; p = 0.017). However, apart from a correlation between PImax1.0 and 6MWD (r = 0.48; p = 0.022), there was no further statistically significant correlation between any PImax and BDS score or blood gas values and SaO2. Interestingly, neopterin level was inversely correlated to PImaxPEAK (r = –0.46; p = 0.031) and PImax1.0 (r = –0.56; p = 0.007). No correlations were found with s-IL2-R and ACE levels. s-IL2-R level was inversely correlated with 6MWD (r = –0.47; p = 0.022). However, serum marker levels were not correlated to any other parameter.


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  		Table 3.. Different Tests of Inspiratory Muscle Strength in Sarcoidosis Patients and Control Subjects*

 

Figure 1
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  		Figure 1.. Box plots for PImaxPEAK and PImax1.0 in sarcoidosis patients and control subjects. Controls = control subjects; Sarcoidosis = sarcoidosis patients.

 
Nonvolitional Tests of Inspiratory Muscle Strength
Nonvolitional tests of inspiratory muscle strength assessed by the measurement of TwPmoIn were sufficiently assessed in 18 sarcoidosis patients and in 18 control subjects. From the remaining subjects, five patients and four control subjects denied the use of magnetic stimulation. In one patient and two control subjects, not enough acceptable pressure-time curves could be generated according to clearly predefined criteria, as previously published.24 Here, TwPmoIn tended to be lower in sarcoidosis patients compared to control subjects, although this did not reach significance (Table 3). The median breathing frequency (16.7 vs 15.2 breaths/min, respectively; p = 0.31), tidal volume (0.85 vs 0.74 L, respectively; p = 0.84), and calculated minute ventilation (12.0 vs 10.9 L/min, respectively; p = 0.44) showed a nonsignificant trend to higher values in sarcoidosis patients compared to control subjects.

Three patients were identified as having reduced inspiratory muscle strength according to predefined criteria, while 15 patients had normal values for TwPmoIn (Table 4 ).25 In these patients with inspiratory muscle weakness, PImaxPEAK, PImax1.0, 6MWD, and FVC were lower, and neopterin, s-IL2-R, and ACE levels, prednisolone dosage, and BDS score were higher compared to the remaining 15 patients without inspiratory muscle impairment. However, these findings were purely descriptive, since further statistical analysis was not performed due to the low number of cases.


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  		Table 4.. Subgroup Analysis of Sarcoidosis Patients With and Without Inspiratory Muscle Impairment*

 
In patients with sarcoidosis, TwPmoIn was significantly correlated to SaO2 at rest (r = 0.51; p = 0.030) and to SaO2 after exercise (r = 0.49; p = 0.036). Further, TwPmoIn was correlated to PaO2 at rest (r = 0.49; p = 0.041) and to PaO2 after exercise (r = 0.53; p = 0.023). TwPmoIn was not correlated to levels of neopterin, s-IL2-R, and ACE.

Following multiple linear regression analysis, TwPmoIn was shown to be the strongest predictor for BDS score and 6MWD findings (Fig 2, 3 ). In addition, PaO2 at rest was predictive of BDS score (r = 0.52; p = 0.012) and 6MWD (r = 0.49; p = 0.019). FVC was predictive of 6MWD only (r = 0.52; p = 0.011) but not for BDS score. In addition, PImaxPEAK and PImax1.0 were not significant predictors for BDS score or 6MWD. Subgroup analysis did not reveal any difference in inspiratory muscle strength or level of serum markers for sarcoidosis when patients receiving therapy with corticosteroids were compared with those who were not receiving such therapy.


Figure 2
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  		Figure 2.. Relationship between BDS score and TwPmoIn following linear regression analysis.

 

Figure 3
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  		Figure 3.. Relationship between 6MWD and TwPmoIn following linear regression analysis.

 
Discussion

This is the first study in which nonvolitional tests of respiratory muscle strength have been used to quantify inspiratory muscle strength in sarcoidosis patients. The assessment of TwPmoIn showed no clear difference in sarcoidosis patients compared to age-matched and BMI-matched control subjects. This indicates that inspiratory muscle strength is, on average, not substantially reduced in sarcoidosis patients. However, there were three patients in whom inspiratory muscle weakness was diagnosed according to predefined criteria.25 Consequently, a minority of patients with sarcoidosis experiences impaired inspiratory muscle strength, but the majority of patients does not.

The present study demonstrates that inspiratory muscle strength is more strongly predictive for both dyspnea and 6MWD compared to lung function parameters and oxygenation. In particular, the three patients with substantially reduced TwPmoIn and PImax values had the lowest 6MWD and the highest degree of dyspnea. Therefore, the results of this study would suggest that the impairment of inspiratory muscle strength occurs in some patients with sarcoidosis, substantially increases dyspnea on exertion, and reduces 6MWD. Accordingly, these frequently observed symptoms in sarcoidosis patients can be explained in part by reduced inspiratory muscle strength. Nonetheless, there are several other variables, such as an increase in central drive, as previously shown,10 that might also have a substantial impact on dyspnea and 6MWD in sarcoidosis patients. With this in mind, breathing frequency, tidal volume, and minute ventilation tended to be higher in sarcoidosis patients compared to control subjects, although these differences did not reach significance, and are therefore not suggested to explain increased dyspnea and reduced 6MWD in sarcoidosis patients. However, further studies assessing additional parameters such as ergospirometric investigations, lactate levels, lung compliance, and peripheral skeletal muscle strength should be measured in future studies to objectify the present findings.

Steroids are known to cause skeletal myopathy, which could also affect respiratory muscles, but the dosages of steroids were small in the present study, and subgroup analysis did not reveal any effect of steroids on inspiratory muscle strength or levels of sarcoidosis serum markers. Therefore, the influence of steroids on the findings of the present study is thought to be negligible.

The following three different types of symptomatic skeletal muscle involvement have been indicated: acute myositis; palpable muscle nodules; and chronic myopathy.11 Furthermore, respiratory muscle impairment has been reported previously by three case reports and one small series10262728 in patients with biopsy-proven (quadriceps muscle) skeletal muscle involvement. In contrast, patients in the present study had no clinical signs of skeletal muscle involvement. Therefore, respiratory muscle impairment in sarcoidosis patients is possible even in patients who have no clinical evidence of skeletal muscle involvement. However, a muscle biopsy was not performed in the present study and in previous studies, hence it is impossible to define for certain which type of muscle involvement causes these symptoms.671415 Therefore, the relationship between symptomatic skeletal muscle and respiratory muscle involvement remains unclear and requires further investigation.

Previous studies have already reported reduced inspiratory muscle strength in sarcoidosis patients (Table 5 ). Here, only volitional tests have been used to measure inspiratory muscle strength (Table 5 ). In all studies, PImax tended to be lower or was significantly reduced in sarcoidosis patients. From these data, it was concluded that respiratory muscle involvement occurs frequently in sarcoidosis patients and substantially affects symptoms such as dyspnea. The results of the present study regarding volitional tests are in line with the previous findings, as PImax was significantly reduced in sarcoidosis patients.


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  		Table 5.. PImax1.0 in Sarcoidosis Patients: Literature Review*

 
However, the results when using PImax to quantify respiratory muscle involvement must be viewed with caution for the following reasons. First, the assessment occurs volitionally, and it is, therefore, difficult to ensure that subjects are making a truly maximal effort.1629 This is particularly important in patients presenting with unspecific fatigue, as those with sarcoidosis often do.12345 Second, the interpretations of studies that included different numbers of women and men for patients and control subjects671415 might be misleading, because the substantially lower values in women than in men significantly affect absolute PImax.21303132 This was avoided in the present study by including men only, but further studies are required to provide data on women. Third, study comparisons were also hindered by the fact that different regression equations have been used to calculate predicted values, which is suggested to significantly influence predicted values.21 Fourth, in all studies, including the present one comparing PImax in sarcoidosis patients and control subjects (Table 5), control subjects achieved higher PImax values than the predicted norms, and sarcoidosis patients had only mildly reduced values. The occurrence of higher PImax values in control subjects might be explained by the inclusion of highly motivated participants in the control group, as in the present and previous studies.715

Therefore, the number of patients who were found to exhibit inspiratory muscle impairment may be overestimated if only PImax is assessed. Low values of PImax might simply reflect the unachieved maximal effort for different reasons. Accordingly, PImax was inconsistently related to clinical parameters. In contrast, respiratory muscle impairment has been shown to significantly predict dyspnea on exertion and reduced walking capacity in the present study when using nonvolitional tests for the assessment of inspiratory muscle strength. Therefore, it is suggested that these nonvolitional tests assess respiratory muscle strength more sufficiently in sarcoidosis patients. However, there was only a trend toward lower values for TwPmo in sarcoidosis patients, which is a finding that is in contrast to its predictive impact. This might be explained by the fact that even mildly reduced TwPmo leads to a substantial increase of dyspnea. On the other hand, inspiratory muscle impairment must be severe in order to be significantly lower compared to healthy subjects,33 thus explaining our observation that only a trend toward lower values of TwPmo was observed in sarcoidosis patients. Further studies including a higher number of patients are needed to verify this discrepancy. Interestingly, lung function parameters were not predictive for dyspnea in sarcoidosis patients but have been shown to be correlated to dyspnea in COPD patients,34 indicating that the feasibility of predicting dyspnea from lung function is variable in patients with different chronic respiratory diseases.

In conclusion, the impairment of inspiratory muscle strength occurs in sarcoidosis patients, but this is reliably detectable only when using tests of inspiratory muscle strength that are independent from the cooperation and motivation of the patient being tested. Impairment of inspiratory muscle strength, if present, is suggested to be an important factor causing dyspnea on exertion and reduced walking capacity. Further studies are needed in order to substantiate the impact of impaired inspiratory muscle strength on symptoms in sarcoidosis patients.

Footnotes

Abbreviations: ACE = angiotensin-converting enzyme; BDS = Borg dyspnea scale; BMI = body mass index; 6MWD = 6-min walking distance; PImax = maximal inspiratory pressure; PImax1.0 = plateau maximal inspiratory pressure sustained for 1 s; PImaxPEAK = peak maximal inspiratory pressure; SaO2 = arterial oxygen saturation; s-IL2-R = soluble interleukin-2 receptor; TwPmo = twitch mouth pressure; TwPmoIn = twitch mouth pressure during inspiratory pressure triggering

The authors have reported to the ACCP that no significant conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Received for publication February 14, 2006. Accepted for publication April 24, 2006.

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