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Postgraduate Education Corner: CHEST IMAGING AND PATHOLOGY FOR CLINICIANS |

A Young Patient With a Minimal Smoking History Presents With Bullous Emphysema and Recurrent Pneumothorax* FREE TO VIEW

Eduardo Mireles-Cabodevila, MD; Hina Sahi, MD; Carol Farver, MD; Tan-Lucien Mohammed, MD; Daniel A. Culver, DO, FCCP
Author and Funding Information

*From the Departments of Pulmonary, Allergy and Critical Care Medicine (Drs. Mireles-Cabodevila, Sahi, and Culver), Diagnostic Radiology (Dr. Mohammed), and Anatomic Pathology (Dr. Farver), Cleveland Clinic, Cleveland, OH.

Correspondence to: Daniel A. Culver, DO, FCCP, Department of Pulmonary, Allergy and Critical Care Medicine, Cleveland Clinic, 9500 Euclid Ave, Cleveland, OH 44195; e-mail: culverd@ccf.org



Chest. 2007;132(1):338-343. doi:10.1378/chest.06-2987
Text Size: A A A
Published online

Acute-onset dyspnea and substernal chest pain radiating to the back developed in a 46-year-old African-American woman while she was watching television. There was no cough, fever, or chills. She had been admitted to the hospital 3 months earlier with a similar presentation; a spontaneous, left basal pneumothorax was found and was treated with tube thoracostomy.

Six years before that, she had been first told she had emphysema and was treated with inhaled bronchodilators; she stopped smoking (smoking history, 13 pack-years). A review of prior chest radiographs demonstrated that emphysema involving predominantly the upper lobes had been present 13 years prior (smoking history at that time, 5 pack-years). Her medical history was remarkable for two episodes of suspected pneumonia in her early thirties, hypertension, hyperlipidemia, and diffuse idiopathic skeletal hyperostosis. She worked as a data processor in a health institution; had never been exposed to fumes, dusts, asbestos, or silica; denied any drug use; and had no family history of lung disease. A careful review of systems revealed occasional arthralgias, mainly involving the hips, elbows, and the thoracic spine. There was no history of urticaria, ocular disease, or joint laxity.

Clinical Findings

Physical examination revealed a mesomorphic woman who was 166 cm tall, tachypneic (22 breaths/min), and hypoxemic (pulse oximetric saturation, 90% [while breathing room air]). The lung examination revealed decreased breath sounds bilaterally with hyperresonance at the left base. The cardiac examination findings were unremarkable. There were no skin lesions, clubbing, edema, synovitis, or joint deformities.

CBC count, comprehensive metabolic panel, α1-antitrypsin (A1AT) level (183 mg/dL), and angiotensin-converting enzyme level (30 U/L) were normal. The results of a tuberculin skin test were negative. Prior pulmonary function tests revealed an FVC of 3.60 L (99% predicted), an FEV1 of 2.80 L (92% predicted), an FEV1/FVC ratio of 77.8, and a moderate reduction in the diffusion of carbon monoxide (59% predicted). Plethysmography demonstrated normal total lung capacity (97% predicted) with mild hyperinflation (residual volume, 116% predicted).

Radiologic Findings

A chest CT scan performed 6 years prior showed extensive subpleural emphysema and no lymphadenopathy (Fig 1 ). Chest imaging performed at hospital admission demonstrated a left basal pneumothorax, bulky mediastinal and hilar lymphadenopathy, upper-lobe paraseptal emphysema, and large bullae (Fig 2 ).

Pathologic Findings

Because of recurrent pneumothorax, she was treated with bullectomy and pleurectomy. A pathologic examination demonstrated multiple nonnecrotizing granulomas in the subpleural region and in the walls of the bullae (Fig 3 ). No evidence of granulomas obstructing the airway was seen. Cultures and organismal stains were negative.

What is the diagnosis?
Diagnosis: Bullous sarcoidosis

Clinical and Radiologic Discussion

Our patient presented with a disease that was characterized by upper lobe-predominant paraseptal emphysema with areas of bullous disease, spontaneous pneumothorax, mediastinal adenopathy, no airflow obstruction, and protracted time to diagnosis. The differential diagnosis for bullous lung disease is limited (Table 1 ).12 Secondary causes of emphysema may be overlooked in smokers, especially since their incidence is higher in the population of people who smoke.3 The diagnosis of the underlying etiology for bullous lung disease depends on recognizing that almost all of these conditions have systemic manifestations.

A1AT deficiency is an inherited disorder that predominantly affects white persons and is responsible for 1 to 4.5% of cases of COPD.4 Clues to this disorder include unexplained or early-onset emphysema, a family history of emphysema, bronchiectasis, liver dysfunction, necrotizing panniculitis, or Wegener granulomatosis.

HIV infection confers an increased risk for emphysema when compared to control subjects (15% vs 1%, respectively), apparently due to the accelerated progression to emphysema in smoking HIV-positive individuals.5Besides tobacco, bullous lung disease has been associated with marijuana,6cocaine,7and IV drug use,89 with the latter being the strongest association.

Several autoimmune diseases have been implicated in bullous lung disease. The most common association is with hypocomplementemic urticarial vasculitis syndrome. It is an uncommon disorder of unknown etiology, which is characterized by persistent urticarial lesions, leukocytoclastic vasculitis, and decreased complement levels. Dyspnea, airflow obstruction, and emphysema are seen in half of cases, usually by the third decade of life.10Case reports of bullous lung disease have also been reported with Sjögren disease,11lupus erythematosus,12multisystem autoimmune dysfunction,13and Wegener granulomatosis disease (in the absence of A1AT deficiency).14

Marfan syndrome,15Ehler-Danlos syndrome,16and cutis laxa17can present with early-onset emphysema and spontaneous pneumothorax. These disorders are the manifestations of defects in elastin and/or collagen. Systemic features include arachnodactyly, skin and joint laxity, ectopia lentis, aortic and valvular disease, and aneurysms. Idiopathic giant bullous emphysema is a rare syndrome of unknown etiology that affects young men, usually smokers, and is characterized by paraseptal emphysema and large bullae in the upper lobes.18

Birt-Hogg-Dubé syndrome is an autosomal-dominant genodermatosis that is characterized by multiple benign cutaneous neoplasms on the head, neck, and upper trunk during the third to fourth decades of life. The lung manifestations are subpleural cystic lesions and basal-predominant bullae. Spontaneous pneumothorax develops in up to 43% of patients.19Neurofibromatosis has also been associated with bulla formation and pulmonary fibrosis in case reports. However, the largest and most recent series to date was unable to document a clear association.20

Placental transmogrification or placentoid bullous lesion of the lung is an unusual condition in which the alveoli develop a villous configuration that resembles placental villi.21The pathophysiology remains unknown.22 The characteristic presentation is a young patient with a giant bleb or cyst causing compression of a healthy lung.2122

Fabry disease is an inborn error of metabolism that results from the tissue deposition of ceramide trihexoside due to the deficiency of α-galactosidase. Airflow obstruction occurs in up to 36% of patients, and several case reports have described spontaneous pneumothorax and emphysema.23Salla disease is a very rare congenital disease that leads to the accumulation of sialic acid; reported only in Finland,24 approximately 124 patients have been identified. One case of bullous emphysema has been described in the cohort.24

Sarcoidosis affects the lungs in approximately 95% of patients,25but bullous sarcoidosis is a rare manifestation with an unknown incidence. A histopathologic review26 of lung-volume-reduction surgery specimens at one center hinted that the diagnosis may be underrecognized, since 9 of 80 subjects (11%) had noncaseating granulomas. Unfortunately, the report26did not clearly correlate this finding with clinical or radiologic information, making the diagnosis tenuous in these individuals. Bullous sarcoid should be distinguished from cavitary or fibrocystic sarcoidosis, which may also lead to spontaneous pneumothorax.2729 The paucity of fibrosis in the former contrasts with the well-established fibrosis that is typical in the latter conditions.

Bullous sarcoidosis was initially described in 1949, with a handful of subsequent case reports (Table 2 ).27,3035 The reported cases describe predominantly young patients (mean age, 36 years). Most had obstructive physiology, leading to an initial diagnosis of emphysema or asthma, and resulting in a prolonged time to diagnosis. The absence of striking spirometric abnormalities, as in our patient, has been described in patients with paraseptal emphysema.3637

Although smoking may be associated with the development of bullous sarcoidosis, only approximately half of the available case reports specify the smoking history. Interestingly, smoking is thought to protect the patient from the development of sarcoidosis in general. In A Case Control Etiologic Study of Sarcoidosis,38the odds ratio for the development of sarcoidosis among smokers was 0.62 (95% confidence interval, 0.50 to 0.77). However, a Japanese study39 compared CT scan findings in 23 sarcoidosis patients with a modest smoking history (median smoking history, 12 pack-years) and 23 nonsmoking patients. Emphysema was the only statistically different finding between both groups (11 vs 1, respectively; p < 0.002), although the type of emphysema was not specified. Mediastinal adenopathy developed in our patient 6 years after she had stopped smoking. By then, evidence of emphysema had already been present for 9 years (she had accrued 5 pack-years of smoking at that time), raising the question of whether the delayed development of typical lymph node enlargement was a manifestation of the protective nature of tobacco in sarcoidosis or simply part of the natural history of the disease.

The evaluation of bullous lung disease begins with a detailed medical history, including the age of onset of the disease, and a physical examination, including determination of the presence of extrapulmonary symptoms or signs. Given the therapeutic and genetic implications, the measurement of A1AT level and the determination of phenotype are routinely warranted.4

If chest radiograph findings suggest an atypical distribution of bullae (eg, basal predominance) or lymphadenopathy, we suggest obtaining a high-resolution chest CT scan. Features that may heighten suspicion for sarcoidosis include lymph node enlargement, micronodules in a bronchovascular or subpleural location, or infiltrates not related to bullous compression of an adjacent lung. In our case, the absence of substantial airflow obstruction was an additional feature that is atypical for the common emphysema phenotype. The diagnosis of sarcoidosis-related bullous lung disease may be difficult due to the increased risk of complications from performing a biopsy. BAL may be useful to suggest the diagnosis, and transbronchial needle aspiration can be diagnostic. When pleurodesis is attempted for pneumothorax in patients with evidence of sarcoidosis, clinicians should consider surgical biopsy as well, since the management of progressing disease would be radically altered.

Pathology Discussion

The pathologic mechanism for bullous sarcoidosis is unknown. Packe et al34have suggested that an episode of diffuse parenchymal involvement, initial “extensive shadows” on the chest imaging, precedes the development of bullous lesions. Judson and Strange35 have suggested the following three possible pathophysiologic explanations: endobronchial lesions causing obstruction; the retraction of surrounding fibrotic tissue; or inflammatory alveolitis leading to the destruction of lung tissue. As evidenced by the absence of significant spirometric or pathologic airways involvement and scant fibrosis in this case, we suspect that imbalanced protease-antiprotease manifestations of inflammation could be the culprit. Several matrix metalloproteinases have been implicated in smoking-related pulmonary emphysema,4041 and their levels are also elevated in sarcoidosis patients.42

The prognosis of bullous sarcoidosis is variable, with frequent recurrence of pneumothoraces and progression of physiologic derangements. Prolonged survival has been achieved after bullectomy, pleurodesis, or transplant.31,33,35 In our patient, 1 year after undergoing surgery, she has had no further pneumothoraces and no progression of her sarcoidosis.

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.

Figure Jump LinkFigure 1. Axial CT scan image obtained 6 years prior to diagnosis. The image through the subcarina shows large paraseptal bullae. No nodules or masses are identified. Slice thickness, 5 mm.Grahic Jump Location
Figure Jump LinkFigure 2. CT scan image obtained on hospital admission. This is a multiplanar coronal reconstructed image in the lung window demonstrating extensive bullous emphysema in a paraseptal distribution. The remainder of the pulmonary parenchyma is normal. The arrows indicate subcarinal and hilar adenopathy. The image was acquired with a pulmonary embolism protocol and a slice thickness of 5 mm.Grahic Jump Location
Figure Jump LinkFigure 3. Top, A: fibrous wall of bulla (B) overlying areas of multiple nonnecrotizing granulomas (arrows) in subpleural areas (hematoxylin-and eosin, original ×1.25). Bottom, B: multiple nonnecrotizing granulomas with overlying pleura (P). Giant cells (arrow) and epithelioid histiocytes are present in most granulomas. Tissue stains were negative for fungal and mycobacterial organisms (hematoxylin-eosin, original ×4).Grahic Jump Location
Table Graphic Jump Location
Table 1. Differential Diagnosis of Bullous Lung Disease*
* 

Differential diagnosis based on cases of bullous emphysema and bullous lung disease reported in the literature.

Table Graphic Jump Location
Table 2. Reports of Bullous Sarcoidosis*
* 

M = male; F = female; NS = not specified; PFT = pulmonary function test.

 

One pack per day, but no length established in years.

Teramoto, S, Fukuchi, Y (1996) Bullous emphysema.Curr Opin Pulm Med2,90-96. [PubMed] [CrossRef]
 
Lee, P, Gildea, TR, Stoller, JK Emphysema in nonsmokers: α1-antitrypsin deficiency and other causes.Cleve Clin J Med2002;69,928-929933, 936 passim. [PubMed]
 
Satoh, K, Kobayashi, T, Misao, T, et al CT assessment of subtypes of pulmonary emphysema in smokers.Chest2001;120,725-729. [PubMed]
 
American Thoracic Society, European Respiratory Society.. American Thoracic Society/European Respiratory Society statement: standards for the diagnosis and management of individuals with α1-antitrypsin deficiency.Am J Respir Crit Care Med2003;168,818-900. [PubMed]
 
Diaz, PT, King, MA, Pacht, ER, et al Increased susceptibility to pulmonary emphysema among HIV-seropositive smokers.Ann Intern Med2000;132,369-372. [PubMed]
 
Tan, C, Hatam, N, Treasure, T Bullous disease of the lung and cannabis smoking: insufficient evidence for a causative link.J R Soc Med2006;99,77-80. [PubMed]
 
van der Klooster, JM, Grootendorst, AF Severe bullous emphysema associated with cocaine smoking.Thorax2001;56,982-983. [PubMed]
 
Goldstein, DS, Karpel, JP, Appel, D, et al Bullous pulmonary damage in users of intravenous drugs.Chest1986;89,266-269. [PubMed]
 
Stern, EJ, Frank, MS, Schmutz, JF, et al Panlobular pulmonary emphysema caused by i.v. injection of methylphenidate (ritalin): findings on chest radiographs and CT scans.AJR Am J Roentgenol1994;162,555-560. [PubMed]
 
Wisnieski, JJ, Baer, AN, Christensen, J, et al Hypocomplementemic urticarial vasculitis syndrome: clinical and serologic findings in 18 patients.Medicine (Baltimore)1995;74,24-41. [PubMed]
 
Kobayashi, H, Matsuoka, R, Kitamura, S, et al Sjogren’s syndrome with multiple bullae and pulmonary nodular amyloidosis.Chest1988;94,438-440. [PubMed]
 
Masuda, A, Tsushima, T, Shizume, K, et al Recurrent pneumothoraces and mediastinal emphysema in systemic lupus erythematosus.J Rheumatol1990;17,544-548. [PubMed]
 
Roy, TM, Fields, CL, Habenstein, KR Multisystem autoimmune dysfunction with early onset of bullous emphysema.Cleve Clin J Med1993;60,65-68. [PubMed]
 
Mouly, S, Brillet, G, Stern, M, et al Pulmonary giant bulla in Wegener’s granulomatosis.Scand J Rheumatol2000;29,333-335. [PubMed]
 
Wood, JR, Bellamy, D, Child, AH, et al Pulmonary disease in patients with Marfan syndrome.Thorax1984;39,780-784. [PubMed]
 
Safdar, Z, O’Sullivan, M, Shapiro, JM Emergent bullectomy for acute respiratory failure in Ehlers-Danlos syndrome.J Intensive Care Med2004;19,349-351. [PubMed]
 
Corbett, E, Glaisyer, H, Chan, C, et al Congenital cutis laxa with a dominant inheritance and early onset emphysema.Thorax1994;49,836-837. [PubMed]
 
Stern, EJ, Webb, WR, Weinacker, A, et al Idiopathic giant bullous emphysema (vanishing lung syndrome): imaging findings in nine patients.AJR Am J Roentgenol1994;162,279-282. [PubMed]
 
Butnor, KJ, Guinee, DG, Jr Pleuropulmonary pathology of Birt-Hogg-Dube syndrome.Am J Surg Pathol2006;30,395-399. [PubMed]
 
Ryu, JH, Parambil, JG, McGrann, PS, et al Lack of evidence for an association between neurofibromatosis and pulmonary fibrosis.Chest2005;128,2381-2386. [PubMed]
 
Cavazza, A, Lantuejoul, S, Sartori, G, et al Placental transmogrification of the lung: clinicopathologic, immunohistochemical and molecular study of two cases, with particular emphasis on the interstitial clear cells.Hum Pathol2004;35,517-521. [PubMed]
 
Fidler, ME, Koomen, M, Sebek, B, et al Placental transmogrification of the lung, a histologic variant of giant bullous emphysema: clinicopathological study of three further cases.Am J Surg Pathol1995;19,563-570. [PubMed]
 
Brown, LK, Miller, A, Bhuptani, A, et al Pulmonary involvement in Fabry disease.Am J Respir Crit Care Med1997;155,1004-1010. [PubMed]
 
Paakko, P, Ryhanen, L, Rantala, H, et al Pulmonary emphysema in a nonsmoking patient with Salla disease.Am Rev Respir Dis1987;135,979-982. [PubMed]
 
Baughman, RP, Teirstein, AS, Judson, MA, et al Clinical characteristics of patients in a case control study of sarcoidosis.Am J Respir Crit Care Med2001;164,1885-1889. [PubMed]
 
Keller, CA, Naunheim, KS, Osterloh, J, et al Histopathologic diagnosis made in lung tissue resected from patients with severe emphysema undergoing lung volume reduction surgery.Chest1997;111,941-947. [PubMed]
 
Froudarakis, ME, Bouros, D, Voloudaki, A, et al Pneumothorax as a first manifestation of sarcoidosis.Chest1997;112,278-280. [PubMed]
 
Harden, KA, Barthakur, A Cavitary lesions in sarcoidosis.Dis Chest1959;35,607-614. [PubMed]
 
Rockoff, SD, Rohatgi, PK Unusual manifestations of thoracic sarcoidosis.AJR Am J Roentgenol1985;144,513-528. [PubMed]
 
Biem, J, Hoffstein, V Aggressive cavitary pulmonary sarcoidosis.Am Rev Respir Dis1991;143,428-430. [PubMed]
 
Kumar, PD, Epstein, DL Eleven-year survival of a patient with bullous sarcoidosis after bilateral pleurodesis.Am J Med2001;111,165
 
Miller, A The vanishing lung syndrome associated with pulmonary sarcoidosis.Br J Dis Chest1981;75,209-214. [PubMed]
 
Pena, CM, Cosgrove, DM, Eng, P, et al Bullectomies for bullous sarcoidosis.Cleve Clin J Med1993;60,157-160. [PubMed]
 
Packe, GE, Ayres, JG, Citron, KM, et al Large lung bullae in sarcoidosis.Thorax1986;41,792-797. [PubMed]
 
Judson, MA, Strange, C Bullous sarcoidosis: a report of three cases.Chest1998;114,1474-1478. [PubMed]
 
Lesur, O, Delorme, N, Fromaget, JM, et al Computed tomography in the etiologic assessment of idiopathic spontaneous pneumothorax.Chest1990;98,341-347. [PubMed]
 
Edge, J, Simon, G, Reid, L Peri-acinar (paraseptal) emphysema: its clinical, radiological, and physiological features.Br J Dis Chest1966;60,10-18. [PubMed]
 
Newman, LS, Rose, CS, Bresnitz, EA, et al A case control etiologic study of sarcoidosis: environmental and occupational risk factors.Am J Respir Crit Care Med2004;170,1324-1330. [PubMed]
 
Terasaki, H, Fujimoto, K, Muller, NL, et al Pulmonary sarcoidosis: comparison of findings of inspiratory and expiratory high-resolution CT and pulmonary function tests between smokers and nonsmokers.AJR Am J Roentgenol2005;185,333-338. [PubMed]
 
Shapiro, SD Elastolytic metalloproteinases produced by human mononuclear phagocytes: potential roles in destructive lung disease.Am J Respir Crit Care Med1994;150,S160-S164. [PubMed]
 
Hautamaki, RD, Kobayashi, DK, Senior, RM, et al Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice.Science1997;277,2002-2004. [PubMed]
 
Henry, MT, McMahon, K, Mackarel, AJ, et al Matrix metalloproteinases and tissue inhibitor of metalloproteinase-1 in sarcoidosis and IPF.Eur Respir J2002;20,1220-1227. [PubMed]
 
Zimmerman, I, Mann, N Boeck’s sarcoid: a case of sarcoidosis complicated by pulmonary emphysema and cor pulmonale.Ann Intern Med1949;31,153-162. [PubMed]
 

Figures

Figure Jump LinkFigure 1. Axial CT scan image obtained 6 years prior to diagnosis. The image through the subcarina shows large paraseptal bullae. No nodules or masses are identified. Slice thickness, 5 mm.Grahic Jump Location
Figure Jump LinkFigure 2. CT scan image obtained on hospital admission. This is a multiplanar coronal reconstructed image in the lung window demonstrating extensive bullous emphysema in a paraseptal distribution. The remainder of the pulmonary parenchyma is normal. The arrows indicate subcarinal and hilar adenopathy. The image was acquired with a pulmonary embolism protocol and a slice thickness of 5 mm.Grahic Jump Location
Figure Jump LinkFigure 3. Top, A: fibrous wall of bulla (B) overlying areas of multiple nonnecrotizing granulomas (arrows) in subpleural areas (hematoxylin-and eosin, original ×1.25). Bottom, B: multiple nonnecrotizing granulomas with overlying pleura (P). Giant cells (arrow) and epithelioid histiocytes are present in most granulomas. Tissue stains were negative for fungal and mycobacterial organisms (hematoxylin-eosin, original ×4).Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Differential Diagnosis of Bullous Lung Disease*
* 

Differential diagnosis based on cases of bullous emphysema and bullous lung disease reported in the literature.

Table Graphic Jump Location
Table 2. Reports of Bullous Sarcoidosis*
* 

M = male; F = female; NS = not specified; PFT = pulmonary function test.

 

One pack per day, but no length established in years.

References

Teramoto, S, Fukuchi, Y (1996) Bullous emphysema.Curr Opin Pulm Med2,90-96. [PubMed] [CrossRef]
 
Lee, P, Gildea, TR, Stoller, JK Emphysema in nonsmokers: α1-antitrypsin deficiency and other causes.Cleve Clin J Med2002;69,928-929933, 936 passim. [PubMed]
 
Satoh, K, Kobayashi, T, Misao, T, et al CT assessment of subtypes of pulmonary emphysema in smokers.Chest2001;120,725-729. [PubMed]
 
American Thoracic Society, European Respiratory Society.. American Thoracic Society/European Respiratory Society statement: standards for the diagnosis and management of individuals with α1-antitrypsin deficiency.Am J Respir Crit Care Med2003;168,818-900. [PubMed]
 
Diaz, PT, King, MA, Pacht, ER, et al Increased susceptibility to pulmonary emphysema among HIV-seropositive smokers.Ann Intern Med2000;132,369-372. [PubMed]
 
Tan, C, Hatam, N, Treasure, T Bullous disease of the lung and cannabis smoking: insufficient evidence for a causative link.J R Soc Med2006;99,77-80. [PubMed]
 
van der Klooster, JM, Grootendorst, AF Severe bullous emphysema associated with cocaine smoking.Thorax2001;56,982-983. [PubMed]
 
Goldstein, DS, Karpel, JP, Appel, D, et al Bullous pulmonary damage in users of intravenous drugs.Chest1986;89,266-269. [PubMed]
 
Stern, EJ, Frank, MS, Schmutz, JF, et al Panlobular pulmonary emphysema caused by i.v. injection of methylphenidate (ritalin): findings on chest radiographs and CT scans.AJR Am J Roentgenol1994;162,555-560. [PubMed]
 
Wisnieski, JJ, Baer, AN, Christensen, J, et al Hypocomplementemic urticarial vasculitis syndrome: clinical and serologic findings in 18 patients.Medicine (Baltimore)1995;74,24-41. [PubMed]
 
Kobayashi, H, Matsuoka, R, Kitamura, S, et al Sjogren’s syndrome with multiple bullae and pulmonary nodular amyloidosis.Chest1988;94,438-440. [PubMed]
 
Masuda, A, Tsushima, T, Shizume, K, et al Recurrent pneumothoraces and mediastinal emphysema in systemic lupus erythematosus.J Rheumatol1990;17,544-548. [PubMed]
 
Roy, TM, Fields, CL, Habenstein, KR Multisystem autoimmune dysfunction with early onset of bullous emphysema.Cleve Clin J Med1993;60,65-68. [PubMed]
 
Mouly, S, Brillet, G, Stern, M, et al Pulmonary giant bulla in Wegener’s granulomatosis.Scand J Rheumatol2000;29,333-335. [PubMed]
 
Wood, JR, Bellamy, D, Child, AH, et al Pulmonary disease in patients with Marfan syndrome.Thorax1984;39,780-784. [PubMed]
 
Safdar, Z, O’Sullivan, M, Shapiro, JM Emergent bullectomy for acute respiratory failure in Ehlers-Danlos syndrome.J Intensive Care Med2004;19,349-351. [PubMed]
 
Corbett, E, Glaisyer, H, Chan, C, et al Congenital cutis laxa with a dominant inheritance and early onset emphysema.Thorax1994;49,836-837. [PubMed]
 
Stern, EJ, Webb, WR, Weinacker, A, et al Idiopathic giant bullous emphysema (vanishing lung syndrome): imaging findings in nine patients.AJR Am J Roentgenol1994;162,279-282. [PubMed]
 
Butnor, KJ, Guinee, DG, Jr Pleuropulmonary pathology of Birt-Hogg-Dube syndrome.Am J Surg Pathol2006;30,395-399. [PubMed]
 
Ryu, JH, Parambil, JG, McGrann, PS, et al Lack of evidence for an association between neurofibromatosis and pulmonary fibrosis.Chest2005;128,2381-2386. [PubMed]
 
Cavazza, A, Lantuejoul, S, Sartori, G, et al Placental transmogrification of the lung: clinicopathologic, immunohistochemical and molecular study of two cases, with particular emphasis on the interstitial clear cells.Hum Pathol2004;35,517-521. [PubMed]
 
Fidler, ME, Koomen, M, Sebek, B, et al Placental transmogrification of the lung, a histologic variant of giant bullous emphysema: clinicopathological study of three further cases.Am J Surg Pathol1995;19,563-570. [PubMed]
 
Brown, LK, Miller, A, Bhuptani, A, et al Pulmonary involvement in Fabry disease.Am J Respir Crit Care Med1997;155,1004-1010. [PubMed]
 
Paakko, P, Ryhanen, L, Rantala, H, et al Pulmonary emphysema in a nonsmoking patient with Salla disease.Am Rev Respir Dis1987;135,979-982. [PubMed]
 
Baughman, RP, Teirstein, AS, Judson, MA, et al Clinical characteristics of patients in a case control study of sarcoidosis.Am J Respir Crit Care Med2001;164,1885-1889. [PubMed]
 
Keller, CA, Naunheim, KS, Osterloh, J, et al Histopathologic diagnosis made in lung tissue resected from patients with severe emphysema undergoing lung volume reduction surgery.Chest1997;111,941-947. [PubMed]
 
Froudarakis, ME, Bouros, D, Voloudaki, A, et al Pneumothorax as a first manifestation of sarcoidosis.Chest1997;112,278-280. [PubMed]
 
Harden, KA, Barthakur, A Cavitary lesions in sarcoidosis.Dis Chest1959;35,607-614. [PubMed]
 
Rockoff, SD, Rohatgi, PK Unusual manifestations of thoracic sarcoidosis.AJR Am J Roentgenol1985;144,513-528. [PubMed]
 
Biem, J, Hoffstein, V Aggressive cavitary pulmonary sarcoidosis.Am Rev Respir Dis1991;143,428-430. [PubMed]
 
Kumar, PD, Epstein, DL Eleven-year survival of a patient with bullous sarcoidosis after bilateral pleurodesis.Am J Med2001;111,165
 
Miller, A The vanishing lung syndrome associated with pulmonary sarcoidosis.Br J Dis Chest1981;75,209-214. [PubMed]
 
Pena, CM, Cosgrove, DM, Eng, P, et al Bullectomies for bullous sarcoidosis.Cleve Clin J Med1993;60,157-160. [PubMed]
 
Packe, GE, Ayres, JG, Citron, KM, et al Large lung bullae in sarcoidosis.Thorax1986;41,792-797. [PubMed]
 
Judson, MA, Strange, C Bullous sarcoidosis: a report of three cases.Chest1998;114,1474-1478. [PubMed]
 
Lesur, O, Delorme, N, Fromaget, JM, et al Computed tomography in the etiologic assessment of idiopathic spontaneous pneumothorax.Chest1990;98,341-347. [PubMed]
 
Edge, J, Simon, G, Reid, L Peri-acinar (paraseptal) emphysema: its clinical, radiological, and physiological features.Br J Dis Chest1966;60,10-18. [PubMed]
 
Newman, LS, Rose, CS, Bresnitz, EA, et al A case control etiologic study of sarcoidosis: environmental and occupational risk factors.Am J Respir Crit Care Med2004;170,1324-1330. [PubMed]
 
Terasaki, H, Fujimoto, K, Muller, NL, et al Pulmonary sarcoidosis: comparison of findings of inspiratory and expiratory high-resolution CT and pulmonary function tests between smokers and nonsmokers.AJR Am J Roentgenol2005;185,333-338. [PubMed]
 
Shapiro, SD Elastolytic metalloproteinases produced by human mononuclear phagocytes: potential roles in destructive lung disease.Am J Respir Crit Care Med1994;150,S160-S164. [PubMed]
 
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