Semin Respir Crit Care Med 2011; 32(3): 310-321
DOI: 10.1055/s-0031-1279827
© Thieme Medical Publishers

Alveolar Hemorrhage in Vasculitis: Primary and Secondary

Jean-François Cordier1 , Vincent Cottin1
  • 1Department of Respiratory Medicine, National Reference Centre for Rare Pulmonary Diseases, Louis Pradel University Hospital, Lyon, France
Further Information

Publication History

Publication Date:
14 June 2011 (online)

ABSTRACT

Diffuse alveolar hemorrhage (DAH) in primary and secondary vasculitis occurs when capillaritis is present. The diagnosis of DAH is considered in patients who develop progressive dyspnea with alveolar opacities on chest imaging (with density ranging from ground glass to consolidation) that cannot be explained otherwise. Hemoptysis, a valuable sign, is often absent. A decline of blood hemoglobin level over a few days without hemolysis or any hemorrhage elsewhere should be an alert for DAH. Bronchoalveolar lavage, retrieving bright red fluid, is the best diagnostic clue. Lung biopsy is not recommended. A search for anti-neutrophil cytoplasmic autoantibodies (ANCAs) is mandatory. Once DAH is diagnosed and hemodynamic as well as infectious causes have been excluded, ANCA-associated vasculitis is taken into account (mainly microscopic polyangiitis or Wegener granulomatosis, and, exceptionally, Churg-Strauss syndrome). Drug-induced DAH, especially antithyroid drugs such as propylthiouracil may be coupled with ANCA. Isolated DAH with capillaritis with or without ANCA is rare. DAH in systemic lupus erythematosus is either associated or not with capillaritis. Treatment of DAH should target the underlying disorder. In the primary vasculitides, corticosteroids and immunosuppressants, especially cyclophosphamide, are the mainstay of therapy, but plasma exchange, particularly in severe DAH, is the rule, although evidence of its effectiveness is awaited.

REFERENCES

  • 1 Yousem S A. Immunologic lung disease: immune alveolar hemorrhage and lung allograft rejection. In: Churg A, Katzenstein A, eds. The Lung: Current Concepts. Philadelphia: Williams and Wilkins; 1993: 93-133
  • 2 Mark E J, Ramirez J F. Pulmonary capillaritis and hemorrhage in patients with systemic vasculitis.  Arch Pathol Lab Med. 1985;  109 413-418
  • 3 Travis W D, Colby T V, Lombard C, Carpenter H A. A clinicopathologic study of 34 cases of diffuse pulmonary hemorrhage with lung biopsy confirmation.  Am J Surg Pathol. 1990;  14 1112-1125
  • 4 Golde D W, Drew W L, Klein H Z, Finley T N, Cline M J. Occult pulmonary haemorrhage in leukaemia.  BMJ. 1975;  2 166-168
  • 5 Kahn F W, Jones J M, England D M. Diagnosis of pulmonary hemorrhage in the immunocompromised host.  Am Rev Respir Dis. 1987;  136 155-160
  • 6 De Lassence A, Fleury-Feith J, Escudier E, Beaune J, Bernaudin J F, Cordonnier C. Alveolar hemorrhage: diagnostic criteria and results in 194 immunocompromised hosts.  Am J Respir Crit Care Med. 1995;  151 157-163
  • 7 Letulle M. Le poumon. Paris: Maloine; 1924
  • 8 Grebski E, Hess T, Hold G, Speich R, Russi E. Diagnostic value of hemosiderin-containing macrophages in bronchoalveolar lavage.  Chest. 1992;  102 1794-1799
  • 9 Myers J L, Katzenstein A L. Wegener's granulomatosis presenting with massive pulmonary hemorrhage and capillaritis.  Am J Surg Pathol. 1987;  11 895-898
  • 10 Cordier J F. A lung biopsy is unnecessary in the management of ANCA-positive patients with chest-roentgenographic abnormalities.  Sarcoidosis Vasc Diffuse Lung Dis. 1996;  13 235-237
  • 11 Myers J L, Katzenstein A L. Microangiitis in lupus-induced pulmonary hemorrhage.  Am J Clin Pathol. 1986;  85(5) 552-556
  • 12 Hughson M D, He Z, Henegar J, McMurray R. Alveolar hemorrhage and renal microangiopathy in systemic lupus erythematosus.  Arch Pathol Lab Med. 2001;  125 475-483
  • 13 Imoto E M, Lombard C M, Sacks D PL. Pulmonary capillaritis and hemorrhage: a clue to the diagnosis of systemic necrotizing vasculitis.  Chest. 1989;  96 927-928
  • 14 Castaner E, Alguersuari A, Gallardo X et al.. When to suspect pulmonary vasculitis: radiologic and clinical clues.  Radiographics. 2010;  30 33-53
  • 15 Primack S L, Miller R R, Muller N L. Diffuse pulmonary hemorrhage: clinical, pathologic, and imaging features.  AJR Am J Roentgenol. 1995;  164 295-300
  • 16 Ando Y, Okada F, Matsumoto S, Mori H. Thoracic manifestation of myeloperoxidase-antineutrophil cytoplasmic antibody (MPO-ANCA)-related disease. CT findings in 51 patients.  J Comput Assist Tomogr. 2004;  28 710-716
  • 17 Holguin F, Ramadan B, Gal A A, Roman J. Prognostic factors for hospital mortality and ICU admission in patients with ANCA-related pulmonary vasculitis.  Am J Med Sci. 2008;  336 321-326
  • 18 Niles J L, Böttinger E P, Saurina G R et al.. The syndrome of lung hemorrhage and nephritis is usually an ANCA- associated condition.  Arch Intern Med. 1996;  156 440-445
  • 19 Schwarz M I, Zamora M R, Hodges T N, Chan E D, Bowler R P, Tuder R M. Isolated pulmonary capillaritis and diffuse alveolar hemorrhage in rheumatoid arthritis and mixed connective tissue disease.  Chest. 1998;  113 1609-1615
  • 20 de Prost P N, Parrot A, Picard C et al.. Diffuse alveolar haemorrhage: factors associated with in-hospital and long-term mortality.  Eur Respir J. 2010;  35 1303-1311
  • 21 Picard C, Cadranel J, Porcher R et al.. Alveolar haemorrhage in the immunocompetent host: a scale for early diagnosis of an immune cause.  Respiration. 2010;  80 313-320
  • 22 Rabe C, Appenrodt B, Hoff C et al.. Severe respiratory failure due to diffuse alveolar hemorrhage: clinical characteristics and outcome of intensive care.  J Crit Care. 2010;  25 230-235
  • 23 Choi H K, Merkel P A, Walker A M, Niles J L. Drug-associated antineutrophil cytoplasmic antibody-positive vasculitis.  Arthritis Rheum. 2000;  43 405-413
  • 24 Kudoh Y, Kuroda S, Shimamoto K, Iimura O. Propylthiouracil-induced rapidly progressive glomerulonephritis associated with antineutrophil cytoplasmic autoantibodies.  Clin Nephrol. 1997;  48 41-43
  • 25 Short A K, Lockwood C M. Antigen specificity in hydralazine associated ANCA positive systemic vasculitis.  Q J Med. 1995;  88 775-783
  • 26 Yazisiz V, Ongüt G, Terzioğlu E, Karayalçin U. Clinical importance of antineutrophil cytoplasmic antibody positivity during propylthiouracil treatment.  Int J Clin Pract. 2010;  64 (1) 19-24
  • 27 Ye H, Zhao M H, Gao Y, Guo X H, Wang H Y. Anti-myeloperoxidase antibodies in sera from patients with propylthiouracil-induced vasculitis might recognize restricted epitopes on myeloperoxidase molecule.  Clin Exp Immunol. 2004;  138 (1) 179-182
  • 28 Tsai M H, Chang Y L, Wu V C, Chang C C, Huang T S. Methimazole-induced pulmonary hemorrhage associated with antimyeloperoxidase-antineutrophil cytoplasmic antibody: a case report.  J Formos Med Assoc. 2001;  100 (11) 772-775
  • 29 Dobre M, Wish J, Negrea L. Hydralazine-induced ANCA-positive pauci-immune glomerulonephritis: a case report and literature review.  Ren Fail. 2009;  31 (8) 745-748
  • 30 Marie I, Levesque H, Dominique S et al.. Atteintes pulmonaires au cours de la sclérodermie systémique, Partie I: Pneumopathie interstitielle chronique fibrosante.  Rev Med Interne. 1999;  20 1004-1016
  • 31 Dhillon S S, Singh D, Doe N, Qadri A M, Ricciardi S, Schwarz M I. Diffuse alveolar hemorrhage and pulmonary capillaritis due to propylthiouracil.  Chest. 1999;  116 (5) 1485-1488
  • 32 Leelarathna L, Karalliede J, Kosky C, D'cruz D, Carroll P V. Pulmonary haemorrhage and vasculitis in Grave's disease.  Breathe. 2009;  6 169-174
  • 33 Katayama K, Hata C, Kagawa K et al.. Diffuse alveolar hemorrhage associated with myeloperoxidase-antineutrophil cytoplasmic antibody induced by propylthiouracil therapy.  Respiration. 2002;  69 (5) 473
  • 34 Romas E, Henderson D R, Kirkham B W. Propylthiouracil therapy: an unusual cause of antineutrophil cytoplasmic antibody associated alveolar hemorrhage.  J Rheumatol. 1995;  22 (4) 803
  • 35 Ohtsuka M, Yamashita Y, Doi M, Hasegawa S. Propylthiouracil-induced alveolar haemorrhage associated with antineutrophil cytoplasmic antibody.  Eur Respir J. 1997;  10 (6) 1405-1407
  • 36 Stankus S J, Johnson N T. Propylthiouracil-induced hypersensitivity vasculitis presenting as respiratory failure.  Chest. 1992;  102 (5) 1595-1596
  • 37 D'Cruz D, Chesser A M, Lightowler C et al.. Antineutrophil cytoplasmic antibody-positive crescentic glomerulonephritis associated with anti-thyroid drug treatment.  Br J Rheumatol. 1995;  34 (11) 1090-1091
  • 38 Calañas-Continente A, Espinosa M, Manzano-García G, Santamaría R, Lopez-Rubio F, Aljama P. Necrotizing glomerulonephritis and pulmonary hemorrhage associated with carbimazole therapy.  Thyroid. 2005;  15 (3) 286-288
  • 39 Thong H Y, Chu C Y, Chiu H C. Methimazole-induced antineutrophil cytoplasmic antibody (ANCA)-associated vasculitis and lupus-like syndrome with a cutaneous feature of vesiculo-bullous systemic lupus erythematosus.  Acta Derm Venereol. 2002;  82 (3) 206-208
  • 40 Jennette J C, Falk R J. Pathogenesis of the vascular and glomerular damage in ANCA-positive vasculitis.  Nephrol Dial Transplant. 1998;  13 (suppl 1) 16-20
  • 41 Nicolls M R, Terada L S, Tuder R M, Prindiville S A, Schwarz M I. Diffuse alveolar hemorrhage with underlying pulmonary capillaritis in the retinoic acid syndrome.  Am J Respir Crit Care Med. 1998;  158 (4) 1302-1305
  • 42 Savage C O, Winearls C G, Evans D J, Rees A J, Lockwood C M. Microscopic polyarteritis: presentation, pathology and prognosis.  Q J Med. 1985;  56 (220) 467-483
  • 43 Guillevin L, Durand-Gasselin B, Cevallos R et al.. Microscopic polyangiitis: clinical and laboratory findings in eighty-five patients.  Arthritis Rheum. 1999;  42 (3) 421-430
  • 44 Haworth S J, Savage C O, Carr D, Hughes J M, Rees A J. Pulmonary haemorrhage complicating Wegener's granulomatosis and microscopic polyarteritis.  Br Med J (Clin Res Ed). 1985;  290 (6484) 1775-1778
  • 45 Takahashi K, Hayashi S, Ushiyama O, Sueoka N, Fukuoka M, Nagasawa K. Development of microscopic polyangiitis in patients with chronic airway disease.  Lung. 2005;  183 (4) 273-281
  • 46 Adu D, Howie A J, Scott D GI, Bacon P A, McGonigle R JS, Micheal J. Polyarteritis and the kidney.  Q J Med. 1987;  62 (239) 221-237
  • 47 Nachman P H, Hogan S L, Jennette J C, Falk R J. Treatment response and relapse in antineutrophil cytoplasmic autoantibody-associated microscopic polyangiitis and glomerulonephritis.  J Am Soc Nephrol. 1996;  7 (1) 33-39
  • 48 Hogan S L, Nachman P H, Wilkman A S, Jennette J C, Falk R J. Prognostic markers in patients with antineutrophil cytoplasmic autoantibody-associated microscopic polyangiitis and glomerulonephritis.  J Am Soc Nephrol. 1996;  7 (1) 23-32
  • 49 Casian A L, Berden A, Jayne D RW. Alveolar haemorrhage in ANCA associated vasculitis: a retrospective analysis from the European Vasculitis Study Group.  NDT Plus. 2010;  3 (suppl 3) 278
  • 50 Villiger P M, Guillevin L. Microscopic polyangiitis: clinical presentation.  Autoimmun Rev. 2010;  9(12) 812-819
  • 51 Chen M, Zhao M H. Severe pulmonary hemorrhage in patients with end-stage renal disease in antineutrophil cytoplasmic autoantibody-associated vasculitis.  Am J Med Sci. 2009;  337 (6) 411-414
  • 52 Lauque D, Cadranel J, Lazor R et al.. Microscopic polyangiitis with alveolar hemorrhage: a study of 29 cases and review of the literature. Groupe d'Etudes et de Recherche sur les Maladies “Orphelines” Pulmonaires (GERM”O”P).  Medicine (Baltimore). 2000;  79 (4) 222-233
  • 53 Doebbeling B N, Bonsib S M, Walker W P. Pulmonary-renal syndrome with “triad” involvement due to small vessel vasculitis.  J Rheumatol. 1990;  17 (8) 1087-1090
  • 54 Schwarz M I, Mortenson R L, Colby T V et al.. Pulmonary capillaritis: the association with progressive irreversible airflow limitation and hyperinflation.  Am Rev Respir Dis. 1993;  148 (2) 507-511
  • 55 Brugiere O, Raffy O, Sleiman C et al.. Progressive obstructive lung disease associated with microscopic polyangiitis.  Am J Respir Crit Care Med. 1997;  155 (2) 739-742
  • 56 Hoffman G S, Kerr G S, Leavitt R Y et al.. Wegener granulomatosis: an analysis of 158 patients.  Ann Intern Med. 1992;  116 (6) 488-498
  • 57 Cordier J F, Valeyre D, Guillevin L, Loire R, Brechot J M. Pulmonary Wegener's granulomatosis: a clinical and imaging study of 77 cases.  Chest. 1990;  97 (4) 906-912
  • 58 Reinhold-Keller E, Beuge N, Latza U et al.. An interdisciplinary approach to the care of patients with Wegener's granulomatosis: long-term outcome in 155 patients.  Arthritis Rheum. 2000;  43 (5) 1021-1032
  • 59 Lenclud C, De Vuyst P, Dupont E, Depierreux M, Ketelbant P, Goldman M. Wegener's granulomatosis presenting as acute respiratory failure with anti-neutrophil-cytoplasm antibodies.  Chest. 1989;  96 (2) 345-347
  • 60 Sanchez-Masiques J, Ettensohn D B. Alveolar hemorrhage in Wegener's granulomatosis.  Am J Med Sci. 1989;  297 (6) 390-393
  • 61 Travis W D, Carpenter H A, Lie J T. Diffuse pulmonary hemorrhage: an uncommon manifestation of Wegener's granulomatosis.  Am J Surg Pathol. 1987;  11 (9) 702-708
  • 62 Stokes T C, McCann B G, Rees R T, Sims E H, Harrison B DW. Acute fulminating intrapulmonary haemorrhage in Wegener's granulomatosis.  Thorax. 1982;  37 (4) 315-316
  • 63 Kjellstrand C M, Simmons R L, Uranga V M, Buselmeier T J, Najarian J S. Acute fulminant Wegener granulomatosis: therapy with immunosuppression, hemodialysis, and renal transplantation.  Arch Intern Med. 1974;  134 (1) 40-43
  • 64 Esposito S, Corona F, Defilippi A et al.. Wegener's granulomatosis presenting with life-threatening lung hemorrhage in a 7-year-old child.  Rheumatol Int. 2010;  30 (12) 1665-1668
  • 65 Lorini R, Alibrandi A, Ravelli A, d'Annunzio G, Castelnuovo P, Martini A. Wegener's granulomatosis presenting with life-threatening pulmonary hemorrhage in a boy with type 1 diabetes.  Diabetes Care. 1999;  22 (9) 1591-1592
  • 66 Bosch X, López-Soto A, Mirapeix E, Font J, Ingelmo M, Urbano-Márquez A. Antineutrophil cytoplasmic autoantibody-associated alveolar capillaritis in patients presenting with pulmonary hemorrhage.  Arch Pathol Lab Med. 1994;  118 (5) 517-522
  • 67 Hensley M J, Feldman N T, Lazarus J M, Galvanek E G. Diffuse pulmonary hemorrhage and rapidly progressive renal failure: an uncommon presentation of Wegener's granulomatosis.  Am J Med. 1979;  66 (5) 894-898
  • 68 Bosch X. Microscopic polyangiitis (microscopic polyarteritis) with late emergence of generalised Wegener's granulomatosis.  Ann Rheum Dis. 1999;  58 (10) 644-647
  • 69 Lara A R, Schwarz M I. Diffuse alveolar hemorrhage.  Chest. 2010;  137 (5) 1164-1171
  • 70 Jennings C A, King Jr T E, Tuder R, Cherniack R M, Schwarz M I. Diffuse alveolar hemorrhage with underlying isolated, pauciimmune pulmonary capillaritis.  Am J Respir Crit Care Med. 1997;  155 (3) 1101-1109
  • 71 Seo P. Cases from the medical grand rounds of the Osler Medical Service at Johns Hopkins University.  Am J Med. 2002;  112 (9) 730-732
  • 72 Bosch X, Font J, Mirapeix E, Revert L, Ingelmo M, Urbano-Márquez A. Antimyeloperoxidase autoantibody-associated necrotizing alveolar capillaritis.  Am Rev Respir Dis. 1992;  146 (5 Pt 1) 1326-1329
  • 73 Barker R A, Knowles G K, Sheppard M N. Breathlessness and profuse haemoptysis.  Lancet. 1998;  351 (9096) 108
  • 74 Benson A, Schwarz M. A 26-year-old woman with recurrent hemoptysis and a sleep disturbance.  Chest. 2008;  134 (6) 1325-1331
  • 75 Pagnoux C, Guillevin L. Churg-Strauss syndrome: evidence for disease subtypes?.  Curr Opin Rheumatol. 2010;  22 (1) 21-28
  • 76 Katzenstein A L. Diagnostic features and differential diagnosis of Churg-Strauss syndrome in the lung: a review.  Am J Clin Pathol. 2000;  114 (5) 767-772
  • 77 Churg A. Recent advances in the diagnosis of Churg-Strauss syndrome.  Mod Pathol. 2001;  14 (12) 1284-1293
  • 78 Sinico R A, Di Toma L, Maggiore U et al.. Prevalence and clinical significance of antineutrophil cytoplasmic antibodies in Churg-Strauss syndrome.  Arthritis Rheum. 2005;  52 (9) 2926-2935
  • 79 Sinico R A, Di Toma L, Maggiore U et al.. Renal involvement in Churg-Strauss syndrome.  Am J Kidney Dis. 2006;  47 (5) 770-779
  • 80 Vaglio A, Martorana D, Maggiore U Secondary and Primary Vasculitis Study Group et al. HLA-DRB4 as a genetic risk factor for Churg-Strauss syndrome.  Arthritis Rheum. 2007;  56 (9) 3159-3166
  • 81 Sablé-Fourtassou R, Cohen P, Mahr A French Vasculitis Study Group et al. Antineutrophil cytoplasmic antibodies and the Churg-Strauss syndrome.  Ann Intern Med. 2005;  143 (9) 632-638
  • 82 Keogh K A, Specks U. Churg-Strauss syndrome: clinical presentation, antineutrophil cytoplasmic antibodies, and leukotriene receptor antagonists.  Am J Med. 2003;  115 (4) 284-290
  • 83 Solans R, Bosch J A, Pérez-Bocanegra C et al.. Churg-Strauss syndrome: outcome and long-term follow-up of 32 patients.  Rheumatology (Oxford). 2001;  40 (7) 763-771
  • 84 Della Rossa A, Baldini C, Tavoni A et al.. Churg-Strauss syndrome: clinical and serological features of 19 patients from a single Italian centre.  Rheumatology (Oxford). 2002;  41 (11) 1286-1294
  • 85 Clutterbuck E J, Pusey C D. Severe alveolar haemorrhage in Churg-Strauss syndrome.  Eur J Respir Dis. 1987;  71 (3) 158-163
  • 86 Ciledağ A, Deniz H, Eledağ S et al.. An aggressive and lethal course of Churg-Strauss syndrome with alveolar hemorrhage, intestinal perforation, cardiac failure and peripheral neuropathy.  Rheumatol Int. 2009;  Dec 19. [Epub ahead of print]
  • 87 Sugino K, Kikuchi N, Muramatsu Y et al.. Churg-Strauss syndrome presenting with diffuse alveolar hemorrhage and rapidly progressive glomerulonephritis.  Intern Med. 2009;  48 (20) 1807-1811
  • 88 Takigawa N, Kawata N, Shibayama T et al.. Successful treatment of a patient with severe Churg-Strauss syndrome by a combination of pulse corticosteroids, pulse cyclophosphamide, and high-dose intravenous immunoglobulin.  J Asthma. 2005;  42 (8) 639-641
  • 89 Olson J C, Kelly K J, Pan C G, Wortmann D W. Pulmonary disease with hemorrhage in Henoch-Schöenlein purpura.  Pediatrics. 1992;  89 (6 Pt 2) 1177-1181
  • 90 Vats K R, Vats A, Kim Y, Dassenko D, Sinaiko A R. Henoch-Schönlein purpura and pulmonary hemorrhage: a report and literature review.  Pediatr Nephrol. 1999;  13 (6) 530-534
  • 91 Markus H S, Clark J V. Pulmonary haemorrhage in Henoch-Schönlein purpura.  Thorax. 1989;  44 (6) 525-526
  • 92 Shichiri M, Tsutsumi K, Yamamoto I, Ida T, Iwamoto H. Diffuse intrapulmonary hemorrhage and renal failure in adult Henoch-Schönlein purpura.  Am J Nephrol. 1987;  7 (2) 140-142
  • 93 Kathuria S, Cheifec G. Fatal pulmonary Henöch-Schonlein syndrome.  Chest. 1982;  82 (5) 654-656
  • 94 Yokose T, Aida J, Ito Y, Ogura M, Nakagawa S, Nagai T. A case of pulmonary hemorrhage in Henoch-Schönlein purpura accompanied by polyarteritis nodosa in an elderly man.  Respiration. 1993;  60 (5) 307-310
  • 95 Barile L A, Jara L J, Medina-Rodriguez F, García-Figueroa J L, Miranda-Limón J M. Pulmonary hemorrhage in systemic lupus erythematosus.  Lupus. 1997;  6 (5) 445-448
  • 96 Schwab E P, Schumacher Jr H R, Freundlich B, Callegari P E. Pulmonary alveolar hemorrhage in systemic lupus erythematosus.  Semin Arthritis Rheum. 1993;  23 (1) 8-15
  • 97 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 (Baltimore). 1997;  76 (3) 192-202
  • 98 Santos-Ocampo A S, Mandell B F, Fessler B J. Alveolar hemorrhage in systemic lupus erythematosus: presentation and management.  Chest. 2000;  118 (4) 1083-1090
  • 99 Miller L R, Greenberg S D, McLarty J W. Lupus lung.  Chest. 1985;  88 (2) 265-269
  • 100 Eagen J W, Memoli V A, Roberts J L, Matthew G R, Schwartz M M, Lewis E J. Pulmonary hemorrhage in systemic lupus erythematosus.  Medicine (Baltimore). 1978;  57 (6) 545-560
  • 101 Verzegnassi F, Marchetti F, Zennaro F, Saccari A, Ventura A, Lepore L. Prompt efficacy of plasmapheresis in a patient with systemic lupus erythematosus and diffuse alveolar haemorrhage.  Clin Exp Rheumatol. 2010;  28 (3) 445-446
  • 102 Gertner E. Diffuse alveolar hemorrhage in the antiphospholipid syndrome: spectrum of disease and treatment.  J Rheumatol. 1999;  26 (4) 805-807
  • 103 Gertner E, Lie J T. Pulmonary capillaritis, alveolar hemorrhage, and recurrent microvascular thrombosis in primary antiphospholipid syndrome.  J Rheumatol. 1993;  20 (7) 1224-1228
  • 104 Naniwa T, Banno S, Sugiura Y et al.. Pulmonary-renal syndrome in systemic sclerosis: a report of three cases and review of the literature.  Mod Rheumatol. 2007;  17 (1) 37-44
  • 105 Griffin M T, Robb J D, Martin J R. Diffuse alveolar haemorrhage associated with progressive systemic sclerosis.  Thorax. 1990;  45 (11) 903-904
  • 106 Bar J, Ehrenfeld M, Rozenman J, Perelman M, Sidi Y, Gur H. Pulmonary-renal syndrome in systemic sclerosis.  Semin Arthritis Rheum. 2001;  30 (6) 403-410
  • 107 Vázquez-Del Mercado M, Mendoza-Topete A, Best-Aguilera C R, Garcia-De La Torre I. Diffuse alveolar hemorrhage in limited cutaneous systemic sclerosis with positive perinuclear antineutrophil cytoplasmic antibodies.  J Rheumatol. 1996;  23 (10) 1821-1823
  • 108 Endo H, Hosono T, Kondo H. Antineutrophil cytoplasmic autoantibodies in 6 patients with renal failure and systemic sclerosis.  J Rheumatol. 1994;  21 (5) 864-870
  • 109 Casari S, Haeney M, Farrand S, Herrick A. Antineutrophil cytoplasmic antibodies a “red flag” in patients with systemic sclerosis.  J Rheumatol. 2002;  29 (12) 2666-2667
  • 110 Wutzl A L, Foley R N, O'Driscoll B R, Reeve R S, Chisholm R, Herrick A L. Microscopic polyangiitis presenting as pulmonary-renal syndrome in a patient with long-standing diffuse cutaneous systemic sclerosis and antibodies to myeloperoxidase.  Arthritis Rheum. 2001;  45 (6) 533-536
  • 111 Schwarz M I, Sutarik J M, Nick J A, Leff J A, Emlen J W, Tuder R M. Pulmonary capillaritis and diffuse alveolar hemorrhage: a primary manifestation of polymyositis.  Am J Respir Crit Care Med. 1995;  151 (6) 2037-2040
  • 112 Genta M S, Genta R M, Gabay C. Systemic rheumatoid vasculitis: a review.  Semin Arthritis Rheum. 2006;  36 (2) 88-98
  • 113 Verburgh C A, Bruijn J A, Daha M R, van Es L A. Sequential development of anti-GBM nephritis and ANCA-associated Pauci-immune glomerulonephritis.  Am J Kidney Dis. 1999;  34 (2) 344-348
  • 114 Beechler C R, Enquist R W, Hunt K K, Ward G W, Knieser M R. Immunofluorescence of transbronchial biopsies in Goodpasture's syndrome.  Am Rev Respir Dis. 1980;  121 (5) 869-872
  • 115 Case records of the Massachusetts General Hospital: case 52–1993: a 17-year-old girl with massive hemoptysis and acute oliguric renal failure.  N Engl J Med. 1993;  329 2019-2026
  • 116 García-Rostan y Pérez G M, García Bragado F, Puras Gil A M. Pulmonary hemorrhage and antiglomerular basement membrane antibody-mediated glomerulonephritis after exposure to smoked cocaine (crack): a case report and review of the literature.  Pathol Int. 1997;  47 (10) 692-697
  • 117 Lazor R, Bigay-Gamé L, Cottin V Groupe d'Etudes et de Recherche sur les Maladies Orphelines Pulmonaires (GERMOP) et al. Alveolar hemorrhage in anti-basement membrane antibody disease: a series of 28 cases.  Medicine (Baltimore). 2007;  86 (3) 181-193
  • 118 Lombard C M, Colby T V, Elliott C G. Surgical pathology of the lung in anti-basement membrane antibody-associated Goodpasture's syndrome.  Hum Pathol. 1989;  20 (5) 445-451
  • 119 Lai F M, Li E K, Suen M W, Lui S F, Li P K, Lai K N. Pulmonary hemorrhage: a fatal manifestation in IgA nephropathy.  Arch Pathol Lab Med. 1994;  118 (5) 542-546
  • 120 Badesch D B, Zamora M, Fullerton D et al.. Pulmonary capillaritis: a possible histologic form of acute pulmonary allograft rejection.  J Heart Lung Transplant. 1998;  17 (4) 415-422
  • 121 Magro C M, Klinger D M, Adams P W et al.. Evidence that humoral allograft rejection in lung transplant patients is not histocompatibility antigen-related.  Am J Transplant. 2003;  3 (10) 1264-1272
  • 122 Magro C M, Deng A, Pope-Harman A et al.. Humorally mediated posttransplantation septal capillary injury syndrome as a common form of pulmonary allograft rejection: a hypothesis.  Transplantation. 2002;  74 (9) 1273-1280
  • 123 Gómez-Tello V, Oñoro-Cañaveral J J, de la Casa Monje R M et al.. Diffuse recidivant alveolar hemorrhage in a patient with hepatitis C virus-related mixed cryoglobulinemia.  Intensive Care Med. 1999;  25 (3) 319-322
  • 124 Kramer J, Hennig H, Lensing C et al.. Multi-organ affecting CMV-associated cryoglobulinemic vasculitis.  Clin Nephrol. 2006;  66 (4) 284-290
  • 125 Khan S A, Subla M R, Behl D, Specks U, Afessa B. Outcome of patients with small-vessel vasculitis admitted to a medical ICU.  Chest. 2007;  131 (4) 972-976
  • 126 Seror R, Pagnoux C, Ruivard M French Vasculitis Study Group et al. Treatment strategies and outcome of induction-refractory Wegener's granulomatosis or microscopic polyangiitis: analysis of 32 patients with first-line induction-refractory disease in the WEGENT trial.  Ann Rheum Dis. 2010;  69 (12) 2125-2130
  • 127 Casian A, Jayne D. Plasma exchange in the treatment of Wegener's granulomatosis, microscopic polyangiitis, Churg-Strauss syndrome and renal limited vasculitis.  Curr Opin Rheumatol. 2011;  23 (1) 12-17
  • 128 Gómez-Puerta J A, Hernández-Rodríguez J, López-Soto A, Bosch X. Antineutrophil cytoplasmic antibody-associated vasculitides and respiratory disease.  Chest. 2009;  136 (4) 1101-1111
  • 129 Betensley A D, Yankaskas J R. Factor VIIA for alveolar hemorrhage in microscopic polyangiitis.  Am J Respir Crit Care Med. 2002;  166 (9) 1291-1292

Jean-François CordierM.D. 

Department of Respiratory Medicine, National Reference Centre for Rare Pulmonary Diseases, Louis Pradel University Hospital

69677 Lyon (Bron), France

Email: jean-francois.cordier@chu-lyon.fr

    >