Pulmonary Manifestations of Systemic Lupus Erythematosus

 

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ABSTRACT

Systemic lupus erythematosus (SLE) can affect the lung in multiple ways. All components of the respiratory system, including the pleura, pulmonary parenchyma, airways, vessels, and respiratory muscles can be involved in various degrees at some time in the disease course and contribute to its morbidity and mortality. This article reviews the clinical symptoms, imaging techniques, histopathology, prognosis, and treatment of pulmonary manifestations of SLE and the related disorder mixed connective tissue disease (MCTD), from a historical perspective and with regard to new insights into pathogenesis and therapy.

REFERENCES

• 1 Osler W. On the visceral manifestations of the erythema group of skin diseases.  Am J Med Sci. 1904;  127 1-3
  CrossrefPubMedGoogle Scholar
• 2 D'Cruz D, Khamashta M, Hughes G. Pulmonary manifestations of systemic lupus erythematosus. In: Wallace DJ, Hahn BHH Dubois' Lupus Erythematosus. Philadelphia; Lippincott, Williams and Wilkins 2002: 663-683
  Google Scholar
• 3 Estes D, Christian C L. The natural history of systemic lupus erythematosus by prospective analysis.  Medicine. 1971;  50 85-94
  PubMedGoogle Scholar
• 4 Huang C-T, Hennigar G R, Lyons H A. Pulmonary dysfunction in with systemic lupus erythematosus.  N Engl J Med. 1965;  272 288-293
  PubMedGoogle Scholar
• 5 Andonopoulos A P, Constantopoulos S H, Galanopoulou V, Drosos A A, Acritidis N C, Moutsopoulos H M. Pulmonary function of nonsmoking patients with systemic lupus erythematosus.  Chest. 1988;  94 312-315
  CrossrefPubMedGoogle Scholar
• 6 Groen H, ter Borg E J, Postma D S, Wouda A A, van der Mark T W, Kallenberg C G. Pulmonary function in systemic lupus erythematosus is related to distinct clinical, serologic, and nailfold capillary patterns.  Am J Med. 1992;  93 619-627
  CrossrefPubMedGoogle Scholar
• 7 Jonsson H, Nived O, Sturfelt G, Valind S, Jonson B. Lung function in patients with systemic lupus erythematosus and persistent chest symptoms.  Br J Rheumatol. 1989;  28 492-499
  CrossrefPubMedGoogle Scholar
• 8 Rolla G, Brussino L, Bertero M T, Bucca C, Converso M, Caligaris-Capio F. Respiratory function in systemic lupus erythematosus: relation with activity and severity.  Lupus. 1996;  5 38-43
  PubMedGoogle Scholar
• 9 Scano G, Goti P, Duranti R, Misuri G, Emmi L, Rosi E. Control of breathing in a subset of patients with systemic lupus erythematosus.  Chest. 1995;  108 759-766
  PubMedGoogle Scholar
• 10 Gibson C J, Edmonds J P, Hughes G RV. Diaphragm function and lung involvement in systemic lupus erythematosus.  Am J Med. 1977;  63 926-932
  CrossrefPubMedGoogle Scholar
• 11 Hardy K, Herry I, Attali V, Cadranel J, Similowsky T. Bilateral phrenic paralysis in a patient with systemic lupus erythematosus.  Chest. 2001;  119 1274-1277
  CrossrefPubMedGoogle Scholar
• 12 Al-Raqum H A, Uppal S S, Al-Mutairy M, Kumari R. Shrinking lung syndrome as a presenting manifestation of systemic lupus erythematosus in a female Kuwaiti.  Clin Rheumatol. 2006;  25 412-414
  CrossrefPubMedGoogle Scholar
• 13 Keane M P, Lynch III J P. Pleuropulmonary manifestations of systemic lupus erythematosus.  Thorax. 2000;  55 159-166
  CrossrefPubMedGoogle Scholar
• 14 Cervera R, Khamashta M A, Font J et al.. Systemic lupus erythematosus: clinical and immunologic patterns of disease expression in a cohort of 1000 patients. The European Working Party on Systemic Lupus Erythematosus.  Medicine (Baltimore). 1993;  72 113-124
  PubMedGoogle Scholar
• 15 Sahn S A. The pathophysiology of pleural effusions.  Annu Rev Med. 1990;  41 7-13
  CrossrefPubMedGoogle Scholar
• 16 Turner-Stokes L, Haslam P, Jones M et al.. Autoantibody and idiotype profile of lung involvement in autoimmune rheumatic disease.  Ann Rheum Dis. 1990;  49 160-162
  PubMedGoogle Scholar
• 17 Wiedemann H P, Matthay R A. Pulmonary manifestations of the collagen vascular diseases.  Clin Chest Med. 1989;  10 677-722
  PubMedGoogle Scholar
• 18 Crestani B. The respiratory system in connective tissue disorders.  Allergy. 2005;  60 715-735
  CrossrefPubMedGoogle Scholar
• 19 Fenlon H M, Doran M, Sant S M, Breatnach E. High resolution chest CT in systemic lupus erythematosus.  AJR Am J Roentgenol. 1996;  166 301-307
  PubMedGoogle Scholar
• 20 Susanto I, Peters J I. Acute lupus pneumonitis with normal chest radiograph.  Chest. 1997;  111 1781-1783
  PubMedGoogle Scholar
• 21 Inoue T, Kanayama Y, Ohe A et al.. Immunopathologic studies of pneumonitis in systemic lupus erythematosus.  Ann Intern Med. 1979;  91 30-34
  PubMedGoogle Scholar
• 22 Boulware D W, Hedgpeth M T. Lupus pneumonitis and anti-SSA(Ro) antibodies.  J Rheumatol. 1989;  16 479-481
  PubMedGoogle Scholar
• 23 Mochizuki T, Aotsuka S, Satoh T. Clinical and laboratory features of lupus patients with complicating pulmonary disease.  Respir Med. 1999;  93 95-101
  PubMedGoogle Scholar
• 24 Raj R, Murin S, Matthay R A, Widemann H P. Systemic lupus erythematosus in the intensive care unit.  Crit Care Clin. 2002;  18 781-803
  CrossrefPubMedGoogle Scholar
• 25 Isbister J P, Ralston M, Hayes J M, Wright R. Fulminant lupus pneumonitis with acute renal failure and RBC aplasia: successful management with plasmapheresis and immunosuppression.  Arch Intern Med. 1981;  141 1081-1083
  CrossrefPubMedGoogle Scholar
• 26 Winder A, Molad Y, Osfeld I et al.. Treatment of systemic lupus erythematosus by prolonged administration of high dose of intravenous immunoglobulin: report of 2 cases.  J Rheumatol. 1993;  20 495-498
  PubMedGoogle Scholar
• 27 Eiser A R, Shanies H M. Treatment of lupus interstitial lung disease with intravenous cyclophosphamide.  Arthritis Rheum. 1994;  37 428-431
  CrossrefPubMedGoogle Scholar
• 28 Santos-Ocampo A S, Mandell B F, Fessler B J. Alveolar hemorrhage in systemic lupus erythematosus.  Chest. 2000;  118 1083-1090
  CrossrefPubMedGoogle Scholar
• 29 Haupt H M, Moore G W, Hutchins G M. The lung in systemic lupus erythematosus.  Am J Med. 1981;  71 791-798
  CrossrefPubMedGoogle Scholar
• 30 Zamora M R, Warner M L, Tuder R, Schwarz M I. Diffuse alveolar hemorrhage and systemic lupus erythematosus: clinical presentation, histology, survival, and outcome.  Medicine. 1997;  76 192-202
  CrossrefPubMedGoogle Scholar
• 31 Myers J L, Katsenstein A L. Microangiitis in lupus-induced pulmonary hemorrhage.  Am J Clin Pathol. 1986;  85 552-556
  PubMedGoogle Scholar
• 32 Onomura K, Nakata H, Tanakaya Y, Tsuda T. Pulmonary hemorrhage in patients with systemic lupus erythematosus.  J Thorac Imaging. 1991;  6 57-61
  PubMedGoogle Scholar
• 33 Orens J B, Martinez F J, Lynch J P. Pleuropulmonary manifestations of systemic lupus erythematosus.  Rheum Dis Clin North Am. 1994;  20 159-192
  PubMedGoogle Scholar
• 34 Dweik R A, Arroliga A C, Cash G M. Alveolar hemorrhage in patients with rheumatic disease.  Rheum Dis Clin North Am. 1997;  23 395-410
  CrossrefPubMedGoogle Scholar
• 35 Erickson R W, Franklin W A, Emlen W. Treatment of hemorrhagic lupus pneumonitis with plasmapheresis.  Semin Arthritis Rheum. 1994;  24 114-123
  PubMedGoogle Scholar
• 36 Sant S M, Doran M, Fenelon H M, Breatnach E S. Pleuropulmonary abnormalities in patients with systemic lupus erythematous: assessment with high resolution computed tomography, chest radiography and pulmonary function tests.  Clin Exp Rheumatol. 1997;  15 507-513
  PubMedGoogle Scholar
• 37 Bankier A A, Kiener H P, Wiesmayr M N et al.. Discrete lung involvement in systemic lupus erythematosus: CT assessment.  Radiology. 1995;  196 835-840
  PubMedGoogle Scholar
• 38 Ooi G C, Ngan H, Peh W CG et al.. Systemic lupus erythematosus patients with respiratory symptoms: the value of HRCT.  Clin Radiol. 1997;  52 775-781
  CrossrefPubMedGoogle Scholar
• 39 Jacobsen S, Petersen J, Ullman S et al.. A multicenter study of 513 Danish patients with systemic lupus erythematosus, I: Disease manifestations and analysis of clinical subsets.  Clin Rheumatol. 1998;  17 468-477
  CrossrefPubMedGoogle Scholar
• 40 Weinrib L, Sharma O P, Quismorio Jr F P. A long-term study of interstitial lung disease in systemic lupus erythematosus.  Semin Arthritis Rheum. 1990;  20 48-56
  CrossrefPubMedGoogle Scholar
• 41 Colby T V. Pulmonary pathology in patients with systemic autoimmune diseases.  Clin Chest Med. 1998;  19 587-612
  CrossrefPubMedGoogle Scholar
• 42 Swigris J J, Olson A L, Fischer A et al.. Mycophenolate mofetil is safe, well tolerated, and preserves lung function in patients with connective tissue-related interstitial lung disease.  Chest. 2006;  130 30-36
  CrossrefPubMedGoogle Scholar
• 43 Langford C A, Waes C. Upper airway obstruction in the rheumatic diseases: life-threatening complications of autoimmune disease.  Rheum Dis Clin North Am. 1997;  23 345-363
  CrossrefPubMedGoogle Scholar
• 44 Smith G A, Ward P H, Berci G. Laryngeal lupus erythematosus.  J Laryngol Otol. 1978;  92 67-73
  PubMedGoogle Scholar
• 45 Teitel A D, MacKenzie C R, Stern R et al.. laryngeal involvement in systemic lupus erythematosus.  Semin Arthritis Rheum. 1992;  22 203-214
  CrossrefPubMedGoogle Scholar
• 46 Curley J W, Byron M A, Bates G J. Cryco-arytenoid joint involvement in acute systemic lupus erythematosus.  J Otol  1986;  100 727-732
  PubMedGoogle Scholar
• 47 Nossent J, Berend K. Cricoarytenoiditis in systemic lupus erythematosus.  Scand J Rheumatol. 1998;  27 237-238
  CrossrefPubMedGoogle Scholar
• 48 Karim A, Shahid A, Siddiqui R et al.. Severe upper airway obstruction from crycoarytenoiditis as the sole presenting manifestation of a systemic lupus erythematosus flare.  Chest. 2002;  121 990-993
  CrossrefPubMedGoogle Scholar
• 49 Godeau B, Cormier C, Menkes C J. Bronchiolitis obliterans in systemic lupus erythematosus: beneficial effect of intravenous cyclophosphamide.  Ann Rheum Dis. 1991;  50 956-958
  CrossrefPubMedGoogle Scholar
• 50 Hinderliter A L, Willis P W, Barst R J et al.. Effects of long-term infusion of prostacyclin (epoprostenol) on echocardiographic measures of right ventricular structure and function in primary pulmonary hypertension: Primary Pulmonary Hypertension Study Group.  Circulation. 1997;  95 1479-1486
  PubMedGoogle Scholar
• 51 Winslow T M, Ossipov M A, Fazio G P et al.. The left ventricle in systemic lupus erythematosus: initial observations and a five-year follow-up in a university medical center population.  Am Heart J. 1993;  125 1117-1122
  CrossrefPubMedGoogle Scholar
• 52 Hosoda Y, Suzuki Y, Takano M et al.. Mixed connective tissue disease with pulmonary hypertension: a clinical and pathological study.  J Rheumatol. 1987;  14 826-830
  PubMedGoogle Scholar
• 53 Sullivan W D, Hurst D J, Harmon C E et al.. A prospective evaluation emphasizing pulmonary involvement in patients with mixed connective tissue disease.  Medicine. 1984;  63 92-107
  CrossrefPubMedGoogle Scholar
• 54 Chung S M, Lee C K, Lee E Y, Yoo B, Lee S D, Moon H B. Clinical aspects of pulmonary hypertension in patients with idiopathic pulmonary arterial hypertension.  Clin Rheumatol. 2006;  25 866-872
  CrossrefPubMedGoogle Scholar
• 55 Burdt M A, Hoffman R W, Deutscher S L et al.. Long-term outcome in mixed connective tissue disease: longitudinal clinical and serologic findings.  Arthritis Rheum. 1999;  42 899-909
  CrossrefPubMedGoogle Scholar
• 56 Quismorio Jr F P, Shjarma O, Koss M et al.. Immunopathologic and clinical studies in clinical studies in pulmonary hypertension associated with systemic lupus erythematosus.  Semin Arthritis Rheum. 1984;  13 349-359
  CrossrefPubMedGoogle Scholar
• 57 Grunig E, Janssen B, Mereles D et al.. Abnormal pulmonary artery pressure response in asymptomatic carriers of primary pulmonary hypertension gene.  Circulation. 2000;  102 1145-1150
  CrossrefPubMedGoogle Scholar
• 58 McGoon M, Gutterman D, Steen V et al.. Screening, early detection, and diagnosis of pulmonary artery hypertension.  Chest. 2004;  126 14S-34S
  CrossrefPubMedGoogle Scholar
• 59 Miyamoto S, Nagaya N, Satoh T et al.. Clinical correlates and prognostic significance of six-minute walk test in patients with primary pulmonary hypertension: comparison with cardiopulmonary exercise testing.  Am J Respir Crit Care Med. 2000;  161 487-492
  CrossrefPubMedGoogle Scholar
• 60 Humbert M, Sitbon O, Simonneau G. Treatment of pulmonary artery hypertension.  N Engl J Med. 2004;  351 1425-1436
  CrossrefPubMedGoogle Scholar
• 61 Simonson J S, Schiller N B, Petri M et al.. Pulmonary hypertension in systemic lupus erythematosus.  J Rheumatol. 1989;  16 918-925
  PubMedGoogle Scholar
• 62 Asherson R A, Higenbottom T W, Dihn Xuan A T et al.. Pulmonary hypertension in a lupus clinic: experience with twenty four patients.  J Rheumatol. 1990;  17 1292-1298
  PubMedGoogle Scholar
• 63 Christman B W, McPherson C D, Newman J H et al.. An imbalance between the excretion of thromboxane and prostacyclin metabolites in pulmonary hypertension.  1992;  327 70-75
  CrossrefPubMedGoogle Scholar
• 64 Giaid A, Yanagisawa M, Langleben D et al.. Expression of endothelin-1 in the lungs of patients with pulmonary hypertension.  1993;  328 1732-1739
  CrossrefPubMedGoogle Scholar
• 65 Cella G, Belloto F, Tona F et al.. Plasma markers of endothelial dysfunction in pulmonary hypertension.  Chest. 2001;  120 1226-1230
  CrossrefPubMedGoogle Scholar
• 66 McLaughlin V V, Presberg K W, Doyle R L et al.. Prognosis of pulmonary arterial hypertension: ACCP evidence-based clinical practice guidelines.  Chest. 2004;  126 78S-92S
  CrossrefPubMedGoogle Scholar
• 67 Galiè N, Ghofrani H A, Torbicki A et al.. Sildenafil citrate therapy for pulmonary arterial hypertension.  N Engl J Med. 2005;  353 2148-2157
  CrossrefPubMedGoogle Scholar
• 68 Fuster V, Steele P M, Edwards W D, Gersh B J, McGoon M D, Frye R L. Primary pulmonary hypertension: natural history and the importance of thrombosis.  Circulation. 1984;  70 580-587
  CrossrefPubMedGoogle Scholar
• 69 Abu-Shakra M, Gladman D D, Urowits M B et al.. Anticardiolipin antibodies in systemic lupus erythematosus: clinical and laboratory correlations.  Am J Med. 1995;  99 624-628
  CrossrefPubMedGoogle Scholar
• 70 Asherson R A, Cervera R, Piette J C et al.. Catastrophic antiphospholipid syndrome: clinical and laboratory features of 50 patients.  Medicine. 1998;  77 195-207
  CrossrefPubMedGoogle Scholar
• 71 Hoffbrand B I, Beck E R. Unexplained dyspnea and shrinking lungs in systemic lupus erythematosus.  BMJ. 1965;  1 1273-1277
  PubMedGoogle Scholar
• 72 Rubin L A, Urowitz M B. Shrinking lung syndrome in SLE: a clinical pathologic study.  J Rheumatol. 1983;  10 973-976
  PubMedGoogle Scholar
• 73 Laroche C M, Mulvey D A, Hawkins P N et al.. Diaphragm strength in the shrinking lung syndrome of with systemic lupus erythematosus.  Q J Med. 1989;  71 429-439
  PubMedGoogle Scholar
• 74 Warrington K J, Moder K G, Brutinel W M. The shrinking lungs syndrome in systemic lupus erythematosus.  Mayo Clin Proc. 2000;  75 467-472
  PubMedGoogle Scholar
• 75 Abramson S B, Dobro J, Eberle M A et al.. Acute reversible hypoxemia in systemic lupus erythematosus.  Ann Intern Med. 1991;  114 941-947
  PubMedGoogle Scholar
• 76 Kim W U, Kim S I, Yoo W H et al.. Adult respiratory distress syndrome in systemic lupus erythematosus: causes and prognostic factors: a single center, retrospective study.  Lupus. 1999;  8 552-557
  CrossrefPubMedGoogle Scholar

Ellen M GinzlerM.D. 

State University of New York-Downstate Medical Center

450 Clarkson Ave., Box 42, Brooklyn, NY 11203

Email: ellen.ginzler@downstate.edu