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(Chest. 2005;128:1483-1489.)
© 2005 American College of Chest Physicians

Distinctive Clinical, Radiographic, and Functional Characteristics of Patients With Sarcoidosis-Related Pulmonary Hypertension*

Roxana Sulica, MD; Alvin S. Teirstein, MD; Shudhir Kakarla, MD; Nimish Nemani, MD; Anousheh Behnegar, MD and Maria L. Padilla, MD

* From the Pulmonary, Critical Care, and Sleep Division, Mount Sinai School of Medicine, New York, NY.

Correspondence to: Maria L. Padilla, MD, Pulmonary, Critical Care, and Sleep Division, Mount Sinai Medical Center, One Gustave L. Levy Place, Box 1232, New York, NY 10029; e-mail: maria.padilla{at}mssm.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objective: To differentiate the clinical, radiographic, and physiologic profile in patients with sarcoidosis with and without pulmonary hypertension.

Design: Retrospective survey.

Setting: Tertiary care center.

Patients: One hundred six patients with sarcoidosis were classified by two-dimensional echocardiography into two groups: group 1, 54 patients with pulmonary hypertension; group 2, 52 patients without pulmonary hypertension.

Interventions: Patients underwent two-dimensional and Doppler echocardiography, chest radiography (CXR), pulmonary function testing, and arterial oxygen saturation determination, and the test results were compared between the two groups. Statistical analysis was performed using independent-sample t test and {chi}2 test, as appropriate; p < 0.05 was considered to be significant.

Results: Predicted spirometric values and lung diffusing capacity were significantly lower in patients in group 1 compared to patients in group 2: FVC, 54% vs 64% (p = 0.0065), FEV1, 47% vs 61% (p = 0.0005), forced expiratory flow, midexpiratory phase, 35% vs 52% (p = 0.0363), and single-breath diffusing capacity of the lung for carbon monoxide (DLCOsb), 39% vs 54% (p = 0.0001). Sixty percent of patients in group 1 had radiographic Scadding stage 4 sarcoidosis, while no radiographic stage predominated in group 2. Arterial oxygen saturation, need for oxygen supplementation, and degree of desaturation after exercise did not differ between groups.

Conclusions: The presence of pulmonary hypertension in patients with sarcoidosis is associated with higher prevalence of stage 4 sarcoidosis by CXR and lower predicted spirometric and DLCOsb measurements.

Key Words: chest radiography • echocardiography • oxygen saturation • pulmonary function • pulmonary hypertension • sarcoidosis


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Pulmonary hypertension (PH) is a well-recognized complication of chronic lung disease. In patients with sarcoidosis, the prevalence of PH and right-heart dysfunction has been reported to range from 4 to 28%.12345 In most cases, sarcoidosis-related PH is mild to moderate or is manifest only with exercise.2356 Severe PH and right heart failure have been described in sarcoidosis, usually in association with severe fibrotic parenchymal disease.12789 Right ventricular failure has been reported in up to 30% of sarcoidosis-related deaths49 and is an important predictor of mortality in patients with sarcoidosis awaiting lung transplantation.10

Although both the prevalence and severity of PH in sarcoidosis increase in patients with lung parenchymal fibrocystic abnormalities,2356 severe PH may occur in the absence of obvious radiographic advanced lung disease. Granulomatous vasculitis of the pulmonary vessels or plexiform pulmonary arteriopathy have been proposed as the cause of PH in this subset of patients.111213 Prior studies36814 have yielded inconsistent results regarding the presence and strength of the association of pulmonary hemodynamics and right ventricular function with radiographic, functional, and gas exchange abnormalities.

This study aims to delineate clinical, radiographic, pulmonary functional, and gas exchange characteristics in a large cohort of patients with sarcoidosis-related PH and to compare them with findings in subjects without PH. A better characterization of the clinicopathologic profile of patients with sarcoidosis-related PH may aid in diagnosis and serve as a guide to therapy.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
PH was defined according to World Health Organization Doppler echocardiographic criteria as estimated right ventricular systolic pressure (RVSP) of at least 40 mm Hg, which corresponds to a peak tricuspid regurgitant velocity of 3.0 to 3.5 m/s.15 Echocardiographic findings of right ventricular dilatation, hypertrophy, or dysfunction were considered corroborative evidence of PH. Only patients with normal left ventricular function were included in the analysis. Echocardiography was performed with commercially available equipment (Acuson Sequoia; Siemens; Mountain View, CA; or HDI-5000; ATL-Phillips; Bothell, WA) with 3.5-mHz transducers. Transthoracic Doppler and two-dimensional images in standard views were obtained. Tricuspid regurgitant flow was identified by color Doppler techniques, and the maximum jet velocity was measured by continuous-wave Doppler echocardiography. RVSP was estimated based on the modified Bernoulli equation: RVSP = transtricuspid gradient + right atrial pressure.16 Transtricuspid gradient is 4v2 (v = peak velocity of tricuspid regurgitation), and right atrial pressures were estimated to be 5, 10, and 15 mm Hg based on the respiratory variation of the inferior vena cava.17

A diagnosis of sarcoidosis was confirmed in all patients by organ biopsy specimen and/or positive Kveim-Siltzbach skin test result. A histologic diagnosis of sarcoidosis was made if biopsy findings showed noncaseating epithelioid cell granulomas, with exclusion of known causes of granulomas.18 With correctly validated suspensions in our institution, the Kveim-Siltzbach skin test has a sensitivity > 80% and a specificity of 99.5% in the diagnosis of sarcoidosis.1920

We reviewed the records of all patients with proven sarcoidosis treated at the Mount Sinai Sarcoidosis Service, in New York, from January 1, 1997, to December 31, 2001. Of 354 reviewed records, two-dimensional echocardiograms were performed in 106 patients with sarcoidosis. Indications for echocardiography were represented by chest pain or palpitations, shortness of breath judged out of proportion to radiographic and pulmonary function findings, clinical or ECG findings suggestive of PH or arrhythmias, and signs or symptoms of heart failure. Fifty-four patients had a diagnosis of PH as defined above (group 1). Group 2 consisted of the remaining 52 patients with sarcoidosis without echocardiographic evidence of PH.

Patients underwent routine chest radiography (CXR) [posteroanterior and lateral views] and spirometry with single-breath diffusing capacity of the lung for carbon monoxide (DLCOsb). The time interval between echocardiography and pulmonary function tests did not exceed 4 weeks. CXR was performed within 3 months of the echocardiograms.

CXR findings were staged according to Scadding: stage 0, normal CXR findings; stage 1, bilateral hilar lymph node enlargement and normal pulmonary parenchyma; stage 2, bilateral hilar lymph node enlargement plus pulmonary densities; stage 3, pulmonary densities and no hilar lymph node enlargement; and stage 4, pulmonary fibrosis (as evidenced by honeycombing, hilar retraction, bullae, cysts, and emphysema).18 The same pulmonary physician determined the radiographic stage in all patients without knowledge of the echocardiographic determination of PH. Arterial oxygen saturations at rest and after exercise (at the end of a 6-min walk test) were recorded in 57 patients (31 patients with PH and 26 patients without PH).

The Mount Sinai Institutional Review Board approved the study. All data are presented as mean ± SEM. Statistical analysis was performed using independent-sample t test or {chi}2 tests, as appropriate; p < 0.05 was considered significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Demographic Characterization
Demographic characteristics of both patient groups are shown in Table 1 . There was no difference in the age distribution (p = 0.93), with mean age in the both groups of approximately 50 years. Female patients outnumbered male patients in both groups by a ratio of 2–3:1 (p = 0.6). There was no significant difference in race between groups (p = 0.85), with a predominance of African-American patients in both groups.


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  		Table 1.. Patient Demographics*

 
Clinical Characterization
For 39 patients in group 1 and 48 patients in group 2, clinical presentation data were available. The most common symptom in both groups was dyspnea on exertion, but we found no statistically significant difference in the distribution of the presenting complaint between groups (Table 2 ). Signs and symptoms of right heart failure (ie, elevated jugular venous pressure, S3 or S4 right heart sound, hepatojugular reflux, lower extremity edema, and/or right ventricular heave) were encountered in 8 of 39 patients (21%) with PH and none of the 48 patients without PH. In addition, four patients presented with syncope, two patients in each group, and three patients had hemoptysis, one patient in group 1 and two patients in group 2. Body mass index values were available for 34 patients in group 1 and 41 patients in group 2. Body mass index for patients in group 1 was 27.7 ± 1.0 and for patients in group 2 was 29.1 ± 1.0, with no statistically significant difference between means (p = 0.37).


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  		Table 2.. Presenting Symptoms*

 
Information regarding treatment administration was available for 40 patients in group 1 and 35 patients in group 2 (Table 3 ). Although more patients with PH received specific therapy for sarcoidosis compared to patients without PH, there was no significant difference between groups in the type of drug used or the average dose of prednisone. From the entire cohort of 106 patients with sarcoidosis, 54 patients (51%) were referred for lung transplant evaluation, 26 of 54 patients (48%) in group 1 and 16 of 52 patients (31%) in group 2 (p = 0.02).


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  		Table 3.. Sarcoidosis-Specific Therapy*

 
CXR Staging
CXR was performed within 3 months of the echocardiograms, and radiographic staging was available for 38 patients in group 1 and 44 patients in group 2. Radiographic stage distribution differed significantly between the two groups (p = 0.01) [Table 4 ]. In group 1, 23 patients (60%) showed evidence of fibrosis on CXR (stage 4 sarcoidosis). In this group of patients, 10% had no evidence of parenchymal lung disease on CXR. No radiographic stage predominated in group 2. Twenty-three percent of patients without PH exhibited stage 4 sarcoidosis by CXR.


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  		Table 4.. Radiographic Stage Distribution in the Two Groups (Scadding System)*

 
Spirometric Characteristics
All spirometric parameters and DLCOsb were decreased in both groups. There was a statistically significant difference in FVC, FEV1, forced expiratory flow, midexpiratory phase (FEF25–75), and DLCOsb between the groups when expressed both in absolute value and as a percentage of predicted (Table 5 ). The ratio of percentage of predicted FVC (FVC%) to percentage of predicted DLCOsb (DLCOsb%) was significantly higher in group 1 compared to group 2. The FEV1/FVC ratio did not differ significantly between the groups: 72 ± 2.0% and 76 ± 1.1%, respectively (p = 0.12).


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  		Table 5.. Spirometry and DLCOsb: Comparison Between Patients With and Without PH*

 
Separate analyses were performed in patients with radiographic stage 4 and stages 0 to 3 sarcoidosis (Table 6 ). In patients with radiographic evidence of fibrosis (stage 4), there were no differences in FVC and FVC% between patients with and without PH. However, FEV1 and DLCOsb% showed significant differences in patients with stage 4 radiographic evidence, with and without PH (Table 4). The mean FEV1 of 1.1 L in the group with PH was lower than the mean of 1.4 L in patients without PH (p < 0.05). Mean percentage of predicted FEF25–75 was 26% in the patients with PH and fibrosis, compared to 40% in patients with fibrosis and no PH, and showed a trend for statistical significance (p = 0.07). Mean DLCOsb% was 33% in patients with radiographic stage 4 sarcoidosis and PH, which was significantly lower than in patients with stage 4 sarcoidosis but no PH, in whom mean DLCOsb% was 43% (p < 0.05). The FVC%/DLCOsb% ratio was higher in patients with PH and radiographic stage 4 sarcoidosis, with a trend for statistical significance (p = 0.07) [Table 6].


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  		Table 6.. Spirometry and DLCOsb: Comparison Between Patients With and Without PH, in Radiographic Stages 4 and 0–3*

 
In patients without pulmonary fibrosis (radiographic stages 0 to 3), there was no difference in spirometric parameters between the groups of patients with and without PH. DLCOsb% was lower in patients with PH (42%) compared to the DLCOsb% of patients without PH (55%) and showed a trend for statistical significance (p = 0.07). In the group of patients with radiographic stages 0 to 3, the FVC%/DLCOsb% ratio was significantly higher (p < 0.05) in patients with PH compared to patients without PH (Table 6).

Oxygen Saturation and Supplementation
Oxygen saturation and oxygen supplementation data were available in 31 patients in group 1 and 26 patients in group 2. Eleven patients with PH received oxygen supplementation by nasal cannula (1 to 6 L/min), and 4 patients without PH received nasal oxygen at 2 to 5 L/min. There was no difference in the arterial oxygen saturation between patients in group 1 and 2, either at rest or after exercise, with or without oxygen supplementation (Table 7 ). Both groups demonstrated a significant decrease in the arterial oxygen saturation following exercise (8% in group 1 and 7.5% in group 2, p = 0.69) [Table 8 ].


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  		Table 7.. Oxygen Saturation at Rest and After Exercise, With and Without Supplementation*

 

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  		Table 8.. Degree of Oxygen Desaturation After Exercise*

 
Echocardiographic Data
In group 1, mean RVSP by echocardiography was 59 mm Hg (SEM, 3.4) and median RVSP was 52 mm Hg. In contrast, mean RVSP was 31 mm Hg in group 2 (SEM, 1.8), and median RVSP was 32 mm Hg. Of the 54 patients in group 1, 29 patients (54%) had estimated RVSP between 40 and 50 mm Hg. There were nine patients (17%) with RVSP > 75 mm Hg. Right heart abnormalities, manifested as right ventricular enlargement, hypertrophy, or dysfunction, were detectable by echocardiography in 35 patients (65%) in group 1 and in 3 patients (5%) in group 2. These abnormalities were of mild-to-moderate degree in 25 of 35 patients (71%) with PH. Pericardial effusions were present in 8 of the 54 patients (15%) with PH. In five patients, right heart catheterization was performed on the same day as echocardiography. Comparative data for patients who had simultaneous echocardiography and right heart catheterization are depicted in Table 9 .


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  		Table 9.. Comparative Echocardiographic and Right Heart Catheterization Data for Patients Who Underwent Both Tests the Same Day

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
To our knowledge, this study represents the largest published cohort of patients with sarcoidosis in whom clinical picture, pulmonary function tests, CXR, and oximetry findings were compared in patients with and without PH detected by echocardiography.

Patients with sarcoidosis-related PH are more likely to present with stage 4 sarcoidosis by CXR compared to patients without PH. Also, they are also more likely to have significantly lower values for spirometric parameters and DLCOsb%. Decreases of DLCOsb% below 50% in the absence of pulmonary fibrosis on CXR and decreases below 30% in patients with stage 4 sarcoidosis by CXR were associated with PH. There was no difference in oxygen saturation at rest or after exercise in patients with and without PH, and the degree of desaturation with exercise was similar in the two groups. Clinical and echocardiographic findings of right heart dysfunction were almost exclusively encountered in patients with PH. In addition, patients with PH were more likely to be treated with sarcoidosis-specific therapy and to be referred for lung transplant evaluation.

In our series, 60% of patients with PH had evidence of pulmonary fibrosis on CXR (radiographic stage 4), 10% had normal radiographic appearance of the lung parenchyma, and approximately 30% had parenchymal densities but no evidence of fibrosis. In the group of patients without PH, no radiographic stage predominated (Table 4). Advanced lung disease, with destruction and distortion of the pulmonary vascular bed secondary to fibrosis and granulomatous inflammation, has been reported in the majority of patients with PH and sarcoidosis.12789 In those patients without radiographic evidence of pulmonary fibrosis, other mechanisms, such as granulomatous vasculitis, plexogenic pulmonary arteriopathy, thrombotic occlusion of the small and medium pulmonary vessels, and hypoxic pulmonary vasoconstriction, may play a role in the development of PH.11121314212223 Prior studies23624 have shown that in patients with sarcoidosis without evidence of radiographic fibrosis, the prevalence of PH diagnosed by right heart catheterization is relatively low. In patients with sarcoidosis and pulmonary fibrosis, the reported prevalence of catheterization-diagnosed PH is higher, often with a significant increase in the pulmonary pressures with exercise.23624 The prevalence of only 60% of stage 4 sarcoidosis by CXR in our patients with PH demonstrates that extensive fibrosis may be less commonly the predominant mechanism of PH in sarcoidosis as reported in prior studies.127 This underscores the importance of a high index of suspicion for PH in sarcoidosis patients with suggestive clinical and pulmonary functional abnormalities.

In patients with sarcoidosis, pulmonary function abnormalities generally correlate with the radiographic staging, although a degree of discordance is not uncommon.232526 In our study, FVC, FEV1, FEF25–75, and DLCOsb were decreased in both groups of patients, but were significantly lower in patients with PH. (Table 5). These findings are in concert with prior studies,814 which have shown that the degree of right ventricular dysfunction and pulmonary hemodynamics correlate with the severity of the restrictive dysfunction as expressed by percentage of predicted total lung capacity and with measures of flow.

Our data show that in patients with sarcoidosis and radiographic stage 4 sarcoidosis, percentage of predicted FEF25–75 (FEF25–75%) tends to be lower in patients with PH, compared to patients without PH (Table 6). Decreased FEF25–75% in the presence of fibrosis has been reported to correlate with mean pulmonary artery pressure measured during exercise.8 Decreased FEF25–75% and the development of PH are probably explained by the presence of granulomatous inflammation and fibrosis at the level of the bronchovascular bundle, in which both medium- and small-sized vessels and small-caliber airways are located.32122 Decreased DLCOsb% may occur in all radiographic stages of sarcoidosis, and there is no close relationship between the radiographic pattern and DLCOsb.232223 However, some studies3814 have shown a degree of correlation of DLCOsb with the presence and severity of PH and with the severity of restrictive ventilatory dysfunction. DLCOsb% was moderately decreased in our patients without associated PH or fibrosis. The DLCOsb% decrease was relatively more pronounced compared to the FVC% decrease, as shown by increased FVC%/DLCOsb% ratio. The presence of either PH or fibrosis was associated with a decrease in DLCOsb% below 50%, and below 30% when both were present. In a prior study8 of patients with sarcoidosis and pulmonary fibrosis, DLCOsb% was severely decreased (approximately 33% of predicted) and correlated well with hemodynamic parameters, such as cardiac output, mean pulmonary artery pressure, total pulmonary resistance, and pulmonary vascular resistance.

More patients with PH in our study were receiving oxygen supplementation than those without PH. Although all patients demonstrated significant desaturation with exercise, there was no difference in the degree of desaturation between patients with and without PH. In both groups, arterial oxygen saturation with exercise dropped below 90%. There is prior evidence that in some patients with sarcoidosis, hypoxic pulmonary vasoconstriction plays a role in exacerbation of the PH.31727

The presenting symptoms were not different between the two groups of patients, and the most commonly encountered symptom in both groups was dyspnea on exertion. Clinical evidence of right heart failure was present in 21% of patients with PH, echocardiographic right heart abnormalities were detectable in 65%, and pericardial effusion was present in 15%. In prior studies4579 of patients with sarcoidosis, cor pulmonale was present at autopsy in approximately 4%, and clinical and ECG signs of right ventricular dysfunction were found in 28% of patients. Our data show that more than one half of our patients with sarcoidosis-related PH had elevation in RVSP in the 40 to 50 mm Hg range and mild-to-moderate right ventricular enlargement and dysfunction by echocardiography. Fewer than 20% of the patients with PH had RVSP elevated > 75 mm Hg and, in < 30% of the patients, echocardiographically determined right ventricular enlargement and dysfunction were graded as severe. Although neither the treatment type nor the dose of corticosteroids differed between groups, more patients with PH were receiving therapy and were referred for lung transplant evaluation.

There are several limitations to our study. Data were obtained from review of records, the diagnosis of PH was made echocardiographically, and the presence of pulmonary fibrosis was based on the findings of Scadding stage 4 sarcoidosis by CXR. Other known causes of PH, such as sleep-disordered breathing and nocturnal hypoxemia, congenital heart defects, HIV infection, connective tissue disease, liver disease, left heart abnormalities, or chronic thromboembolic disease, were not consistently excluded.

In a large study28 of 374 patients with advanced lung disease who underwent echocardiography and right heart catheterization within 72 h of each other, echocardiography had a sensitivity of 85% in diagnosing PH. Specificity was lower, and a large percentage of patients are misclassified as having PH, especially when the estimated RVSP is close to the cut-off point of 40 mm Hg.28 We limited this investigation to studies included in the routine clinical care of patients with sarcoidosis at our institution. Thus, CT of the chest and right heart catheterization were not performed routinely. Smoking status was not recorded in all patients.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
These results suggest that certain clinical, radiographic, and pulmonary functional abnormalities are suggestive of the presence of PH in patients with sarcoidosis. Most patients with sarcoidosis and PH have evidence of pulmonary fibrosis on CXR, but PH developed in 40% of our patients in the absence of radiographic stage 4 disease. Patients with PH had decreased vital capacity, flow rates, and DLCOsb compared to patients without PH. A decreased DLCOsb in the 40% range in patients with sarcoidosis may be related to presence of either fibrosis or of PH, but when fibrosis and pulmonary vascular disease coexist, the DLCOsb% approaches 30 to 35%, FEF25–75% decreases to ≤ 30%, and FEV1 decreases to < 1.2 L.

Findings from our study may guide future prospective investigations aimed at identifying predictive markers of PH in sarcoidosis. An earlier diagnosis of this severe complication of sarcoidosis may prompt the search for new therapeutic strategies directed at sarcoidosis-related PH and earlier referral for transplantation.


   Footnotes
 
Abbreviations: CXR = chest radiography; DLCOsb = single-breath diffusing capacity of the lung for carbon monoxide; DLCOsb% = percentage of predicted single-breath diffusing capacity of the lung for carbon monoxide; FEF25–75 = forced expiratory flow, midexpiratory phase; FEF25–75% = percentage of predicted forced expiratory flow, midexpiratory phase; FVC% = percentage of predicted FVC; PH = pulmonary hypertension; RVSP = right ventricular systolic pressure

Received for publication September 21, 2004. Accepted for publication February 1, 2005.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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