Semin Respir Crit Care Med 2000; 21(2): 0123-0134
DOI: 10.1055/s-2000-9846
Copyright © 2000 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA. Tel.: +1(212) 584-4662

Bronchiolitis Obliterans

Luis Angel, Arturo Homma, Stephanie M. Levine
  • Division of Pulmonary Diseases/Critical Care Medicine, Department of Medicine, The University of Texas Health Science Center at San Antonio and the South Texas Veterans Health Care System, Audie L. Murphy Memorial Veterans Hospital Division, San Antonio, Texas
Further Information

Publication History

Publication Date:
03 March 2004 (online)

ABSTRACT

Bronchiolitis obliterans (BO) is a fibrotic lung disease involving the small conducting airways. BO may be classified by etiology and underlying disease or, more commonly, by histopathological pattern. The two major histopathological categories are (1) BO organizing pneumonia (BOOP) and proliferative bronchiolitis and (2) constrictive bronchiolitis. The former is often idiopathic in nature and may also be associated with connective tissue diseases and inhalation injury. Characteristic findings on chest imaging include alveolar infiltrates and ground glass opacities and pulmonary function tests (PFTs) usually reveal restrictive dysfunction. Constrictive bronchiolitis is associated with organ transplantation, infections, connective tissue diseases, inhalation injury, and drugs and may also have an idiopathic origin. The radiographic characteristic is a mosaic pattern on high-resolution computed tomography (HRCT) and PFTs most often reveal obstructive dysfunction. This article will attempt to review constrictive BO, including histopathology, clinical presentation, radiographic appearance, and physiological findings, for both idiopathic diseases, as well as specific clinical-associated entities.

REFERENCES

  • 1 Lange W. Ueber eine eigenthumliche Erkrankung der kleinen Bronchien und Bronchiolen (Bronchitis and Bronchiolitis obliterans).  Dtsch Arch Klin Med . 1901;  342-364
  • 2 King T E. Bronchiolitis. In: Schwarz MI, King TE, Jr (eds). Interstitial Lung Diseases. 3rd ed. Hamilton, Canada: BC Decker 1998: 645-684
  • 3 Guerry-Force M, Muller N L, Wright J L. A comparison of bronchiolitis obliterans with organizing pneumonia, usual interstitial pneumonia and small airways disease.  Am Rev Respir Dis . 1987;  135 705-712
  • 4 King T E. Overview of bronchiolitis.  Clin Chest Med . 1993;  14 607-610
  • 5 Wright J, Cagle P, Churg A, Colby T V, Myers J. Diseases of the small airways.  Am Rev Respir Dis . 1992;  146 240-262
  • 6 Colby T V. Bronchiolar pathology. In: Epler GR, ed. Diseases of the Bronchioles New York: Raven Press, 1994: 77-100
  • 7 Muller N L, Staples C A, Miller R R. Bronchiolitis obliterans organizing pneumonia. CT features in 14 patients.  AJR Am J Roentgenol . 1990;  154 983-987
  • 8 Colby T V. Bronchiolitis: Pathologic considerations.  Am J Clin Pathol . 1998;  109 101-109
  • 9 Colby T V, Myers J L. The clinical and histologic spectrum of bronchiolitis obliterans including bronchiolitis obliterans organizing pneumonia (BOOP).  Semin Respir Med . 1992;  13 119
  • 10 Lynch D A. Imaging of small airways disease.  Clin Chest Med . 1993;  14 623-634
  • 11 Worthy S A, Muller N L. Small airways diseases.  Radiol Clin North Am . 1998;  36 163-173
  • 12 Muller N L, Miller R R. Diseases of the bronchioles: CT and histopathologic findings. State of the art review.  Radiology . 1995;  196 3-12
  • 13 Hwang J, Rim T S, Lee K S. Bronchiolitis in adults: Pathology and Imaging.  J Comput Assist Tomogr . 1997;  21 913-919
  • 14 Lentz D, Bergin C J, Berry G J, Stoehr C, Theodore J. Diagnosis of bronchiolitis obliterans in heart-lung transplantation patients. Importance of bronchial dilatation on CT.  Am J Radiol . 1992;  59 463-467
  • 15 Turton C W, William G, Green M. Cryptogenic obliterative bronchiolitis in adults.  Thorax . 1981;  36 805-810
  • 16 Dorinsky P M, Davis W B, Lucas J G, Weiland J E, Gadek J E. Adult bronchiolitis. Evaluation by bronchoalveolar lavage and response to prednisone therapy.  Chest . 1985;  88 58-63
  • 17 Kindt G C, Weiland J E, Davis W B, Gadek J E, Dorinsky P M. Bronchiolitis in adults. A reversible cause of airway obstruction associated with airway neutrophils and neutrophil products.  Am Rev Respir Dis . 1989;  140 483-492
  • 18 St. John C R, Dorinsky P M. Cryptogenic bronchiolitis.  Clin Chest Med . 1993;  14 667-675
  • 19 Kraft M, Mortenson R L, Colby T V, Newman L, Waldron Jr A J, King Jr E T. Cryptogenic constrictive bronchiolitis.  Am Rev Respir Dis . 1993;  148 1093-1011
  • 20 Fitzgerald J E, King Jr E T, Lynch D A, Tuder R M, Schwarz M I. Diffuse panbronchiolitis in the United States.  Am J Respir Crit Care Med . 1996;  154 497-503
  • 21 Tsang K WT, Ooi C GC, Ip M SM. Clinical profiles of Chinese patients with diffuse panbronchiolitis.  Thorax . 1998;  53 274-280
  • 22 Park M H, Kim Y W, Yoon H I. Association of HLA class I antigens with diffuse panbronchiolitis in Korean patients.  Am J Respir Crit Care Med . 1999;  159 526-529
  • 23 Sugiyama Y, Kudoh S, Maeda H, Suzaki H, Takaku F. Analysis of HLA antigens in patients with diffuse panbronchiolitis.  Am Rev Respir Dis . 1990;  141 1459-1462
  • 24 Homma H, Yamanaka A, Tanimoto S. Diffuse panbronchiolitis. A disease of the transitional zone of the lung.  Chest . 1983;  83 63-69
  • 25 Sugiyama Y. Diffuse panbronchiolitis.  Clin Chest Med . 1993;  14 765-772
  • 26 Homma S, Kawabata M, Kishi K. Diffuse panbronchiolitis in rheumatoid arthritis.  Eur Respir J . 1998;  12 444-452
  • 27 Kudoh S, Azuma A, Yamamoti M, Izumi T, Ando M. Improvement of survival in patients with diffuse panbronchiolitis treated with low-dose erythromycin.  Am J Respir Crit Care Med . 1998;  157 1829-1832
  • 28 Ichikawa Y, Hotta M, Sumita S, Fujimoto K, Oizumi K. Reversible airway lesions in diffuse panbronchiolitis: Detection by high-resolution computed tomography.  Chest . 1995;  107 120-125
  • 29 Koyama H, Geddes DM: Erythromycin and diffuse panbronchiolitis. Thorax .  1997;  52 915-918
  • 30 Kadota J-I, Sakito O, Kohno S. A mechanism of erythromycin treatment in patients with diffuse panbronchiolitis.  Am Rev Respir Dis . 1993;  147 153-159
  • 31 Commins B T, Raveney F J, Jesson M W. Toxic gases in tower silos.  Ann Occup Hyg . 1971;  14 275
  • 32 Horvath E P, do Pico A G, Barbee R A, Dickie H A. Nitrogen dioxide-induced pulmonary disease.  J Occup Med . 1978;  20 103-110
  • 33 Fleming G M, Chester E H, Montenegro H D. Dysfunction of small airways following pulmonary injury due to nitrogen dioxide.  Chest . 1979;  75 720-721
  • 34 Zwemer F L, Pratt D S, May J J. Silo filler's disease in New York State.  Am Rev Respir Dis . 1992;  146 650-653
  • 35 Douglas W W, Colby T V. Fume-related bronchiolitis obliterans. In: Epler GR, ed. Diseases of the Bronchioles New York: Raven Press, 1994: 187-213
  • 36 Milne J EH. Nitrogen dioxide inhalation and bronchiolitis obliterans.  J Occup Med . 1969;  11 538-547
  • 37 Moskowitz R L, Lyons H A, Cottle H R. Silo-filler's disease: Clinical, physiologic and pathologic study of patient.  Am J Med . 1964;  36 457-462
  • 38 Becklake M R, Goldman H I, Bosman A R. The long-term effects of exposure to nitrous fumes.  Am Rev Tuberc . 1957;  76 398-409
  • 39 Ramirez R J, Dowell A R. Silo-filler's disease: Nitrogen dioxide-induced lung injury: long-term follow-up and review of the literature.  Ann Intern Med . 1971;  74 569-576
  • 40 Jones G R, Proudfoot A T, Hall J I. Pulmonary effects of acute exposure to nitrous fumes.  Thorax . 1973;  28 61-65
  • 41 Douglas W W, Norman G, Hepper G, Colby T V. Silo-filler's disease.  Mayo Clin Proc . 1989;  64 291-304
  • 42 Wells A U, du Bois M R. Bronchiolitis in association with connective tissue disorders.  Clin Chest Med . 1993;  14 655-666
  • 43 Epler G, Colby T, McLoud T, Carrington C B, Gaensler E A. Bronchiolitis obliterans organizing pneumonia.  N Engl J Med . 1985;  312 152-158
  • 44 Katzenstein A-L, Myers J, Prophet W, Corley III S L, Shin M S. Bronchiolitis obliterans an usual interstitial pneumonia. A comparative clinicopathologic study.  Am J Surg Pathol . 1986;  10 373-38
  • 45 Rees J H, Woodhead M A, Sheppard M M, du Bois M R. Rheumatoid arthritis and cryptogenic organizing pneumonia.  Respir Med . 1991;  29 1582-1590
  • 46 Yousem S A, Colby T V, Carrington C B. Lung biopsy in rheumatoid arthritis.  Am Rev Respir Dis . 1985;  131 770-777
  • 47 Epler G R, Snider G L, Gaensler E A, Cathcart E S, FitzGerald M X, Carrington C B. Bronchiolitis and bronchitis in connective tissue disease: A possible relationship to the use of penicillamine.  JAMA . 1979;  242 528-532
  • 48 Bégin R, Massé S, Cantin A, Menard H A, Bureau M A. Airway disease in a subset of nonsmoking rheumatoid patients: Characterization of the disease and evidence for an autoimmune pathogenesis.  Am J Med . 1982;  72 743-750
  • 49 Penny W J, Knight R K, Rees A M, Thomas A L, Smith A P. Obliterative bronchiolitis in rheumatoid arthritis.  Ann Rheum Dis . 1982;  41 469-472
  • 50 Van de Laar M F J A, Westermann C JJ, Wagenaar S S, Dinant H J. Beneficial effect of intravenous cyclophosphamide and oral prednisolone on d-penicillamine-associated bronchiolitis obliterans.  Arthritis Rheum . 1985;  28 93-97
  • 51 Van Thiel J R, van der Burg S, Groote A D, Nossent G D, Wills S H. Bronchiolitis obliterans organizing pneumonia and rheumatoid arthritis.  Eur Respir J . 1991;  4 905-911
  • 52 Fortoul T I, Cano-Valle F, Oliva E, Barrios E. Follicular bronchiolitis in association with connective tissue diseases.  Lung . 1985;  163 305-314
  • 53 Yousem S A, Colby T V, Carrington C B. Follicular bronchitis/bronchiolitis.  Hum Pathol . 1985;  16 700-706
  • 54 Bjerke R D, Tashkin D P, Clements P J. Small airways in progressive systemic sclerosis (PSS).  Am J Med . 1979;  66 201-209
  • 55 Weaver A L, Divertie M B, Titus J L. Pulmonary scleroderma.  Dis Chest . 1968;  54 4-12
  • 56 Davison A G, Epstein D. Relapsing organizing pneumonitis in a man with primary biliary cirrhosis, CREST syndrome, and chronic pancreatitis.  Thorax . 1983;  38 316-317
  • 57 Min J K, Hong Y S, Park S H. Bronchiolitis obliterans organizing pneumonia as an initial manifestation in patients with systemic lupus erythematosus.  J Rheumatol . 1997;  24 2254-2257
  • 58 Otsuka F, Amano T, Hashimoto N, Ogura T, Ishikawa A, Takahashi T. Bronchiolitis obliterans organizing pneumonia associated with systemic lupus erythematosus with antiphospholipid antibody.  Intern Med . 1996;  35 341-344
  • 59 Tazelaar H D, Viggiano R W, Pickersgill J. Interstitial lung disease in polymyositis and dermatomyositis: Clinical features and prognosis as correlated with histologic findings.  Am Rev Respir Dis . 1990;  141 727-733
  • 60 Imasaki T, Yoshii A, Tanaka S. Polymyositis and Sjogren's syndrome associated with bronchiolitis obliterans organizing pneumonia.  Intern Med . 1996;  35 231-235
  • 61 Knoell K A, Hook M, Grice D P, Hendrix Jr D J. Dermatomyositis associated with bronchiolitis obliterans organizing pneumonia (BOOP).  J Am Acad Dermatol . 1999;  40 328-330
  • 62 Akira M, Hara H, Sakatani M. Interstitial lung disease in association with polymyositis-dermatomyositis: Long-term follow-up CT evaluation in seven patients.  Radiology . 1999;  210 333-338
  • 63 Smith C B, Overall C JJ. Clinical and epidemiological clues to the diagnosis of respiratory infections.  Radiol Clin North Am . 1973;  11 261-278
  • 64 Penn C C, Liu C. Bronchiolitis following infection in adults and children.  Clin Chest Med . 1993;  14 645-654
  • 65 Philit F, Wiesendanger T, Archimbaud E, Mornex J-F, Brune J, Cordier J-F. Post-transplant obstructive lung disease (``bronchiolitis obliterans''): A clinical comparative study of bone marrrow and lung transplant patients.  Eur Respir J . 1995;  8 551-558
  • 66 Clark J G, Crawford S W, Madtes D K, Sullivan K M. Obstructive lung disease after allogeneic marrow transplantation: Clinical presentation and course.  Ann Intern Med . 1989;  111 368-376
  • 67 Palmas A, Tefferi A, Myers J L. Late-onset noninfectious pulmonary complications after allogeneic bone marrow transplantation.  Br J Haematol . 1998;  100 680-687
  • 68 Paz H L, Crilley P, Pachefsky A, Schiffman R L, Brodsky I. Bronchiolitis obliterans after autologous bone marrow transplantation.  Chest . 1992;  101 775-778
  • 69 Clark J G, Schwartz D A, Flournoy N, Sullivan K M, Crawford S W, Thomas E D. Risk factors for airflow obstruction in recipients of bone marrow transplants.  Ann Intern Med . 1987;  107 648-656
  • 70 Prince D S, Wingard J R, Saral R, Santos G W, Wise R A. Longitudinal changes in pulmonary function following bone marrow transplantation.  Chest . 1989;  96 301-306
  • 71 Crawford S W, Clark J G. Bronchiolitis associated with bone marrow transplantation.  Clin Chest Med . 1993;  14 741-750
  • 72 Yousem S A. The histological spectrum of pulmonary graft-versus-host disease in bone marrow transplant recipients.  Hum Pathol . 1995;  26 668-675
  • 73 Thirman M J, Devine S M, O'Toole K. Bronchiolitis obliterans organizing pneumonia as a complication of allogeneic bone marrow transplantation.  Bone Marrow Transplant . 1992;  10 307-311
  • 74 Quabeck K. The lung as a critical organ in marrow transplantation.  Bone Marrow Transplant . 1994;  14 S19-S28
  • 75 Calhoon J H, Levine S, Anzueto A, Bryan C L, Trinkle J K. Lung transplantation in a patient with a prior bone marrow transplant.  Chest . 1992;  102 948
  • 76 Hosenpud J D, Bennett L E, Keck B M, Fiol B, Boucek M M, Novick R J. The registry of the International Society for Heart and Lung Transplantation: Fifteenth official report-1998.  J Heart Lung Transplant . 1998;  17 656-668
  • 77 Trulock E P. Lung transplantation.  Am J Respir Crit Care Med . 1997;  155 789-819
  • 78 Kroshus T J, Kshettry V R, Savik K. Risk factors for the development of bronchiolitis obliterans syndrome after lung transplantation.  J Thorac Cardiovasc Surg . 1997;  114 195-202
  • 79 Bando K, Paradis I L, Similo S. Obliterative bronchiolitis after lung and heart-lung transplantation: An analysis of risk factors and management.  J Thorac Cardiovasc Surg . 1995;  110 4-14
  • 80 Scott J P, Higgenbottam T W, Sharples L. Risk factors for obliterative bronchiolitis in heart-lung transplant recipients.  Transplantation . 1991;  51 813-817
  • 81 Bando K, Paradis I L, Similo S. Obliterative bronchiolitis after lung and heart-lung transplantation: an analysis of risk factors and management.  J Thorac Cardiovasc Surg . 1995;  110 4-14
  • 82 Husain A N, Siddiqui M T, Holmea E W. Analysis of risk factors for the development of bronchiolitis obliterans syndrome.  Am J Respir Crit Care Med . 1999;  159 829-833
  • 83 Sundaresan S, Mohanakumar T, Smith M A. HLA-A locus mismatches and development of antibodies to HLA after lung transplantation correlate with the development of bronchiolitis obliterans syndrome.  Transplantation . 1998;  65 648-653
  • 84 Girgis R E, Tu I, Berry G J. Risk factors for the development of obliterative bronchiolitis after lung transplantation.  J Heart Lung Transplant . 1996;  15 1200-1208
  • 85 Ross D J, Marchevsky A, Kramer M, Kass R M. ``Refractoriness'' of airflow obstruction associated with isolated lymphocytic bronchiolitis/bronchitis in pulmonary allografts.  J Heart Lung Transplant . 1997;  16 832-838
  • 86 Schulman L L, Weinberg A D, McGregor C, Galantowicz M E, Suciu-Foca N M, Itescu S. Mismatches at the GLA-DR and GLA-B loci are risk factors for acute rejection after lung transplantation.  Am J Respir Crit Care Med . 1998;  157 1833-1837
  • 87 Sundaresan R S, Trulock E P, Mohanakumar T, Cooper J D, Patterson G A, Washington Universisty Lung Transplant Group. Prevalence and outcome of bronchiolitis obliterans syndrome after lung transplantation.  Ann Thorac Surg . 1995;  60 1341-1347
  • 88 Keller C A, Cagle P T, Brown R W, Noon G, Frost A E. Bronchiolitis obliterans in recipients of single, double, and heart-lung transplantation.  Chest . 1995;  107 973-980
  • 89 Patterson G M, Wilson S, Whang J L. Physiologic definitions of obliterative bronchiolitis in heart-lung and double lung transplantation: A comparison of the forced expiratory flow between 25% and 75% of the forced vital capacity and forced expiratory volume in one second.  J Heart Lung Transplant . 1996;  15 175-181
  • 90 Ikonen T, Kivisaari L, Taskinen E, Piilonen A, Harjula A LJ. High-resolution CT in long-term follow-up after lung transplantation.  Chest . 1997;  111 370-376
  • 91 Leung A n, Fisher K, Valentine V. Bronchiolitis obliterans after lung transplantation.  Chest . 1998;  113 365-370
  • 92 International Society of Heart and Lung Transplantation, Cooper J D, Billlingham M. A working formulation for the standardization of nomenclature and for clinical staging of chronic dysfunction in lung allografts.  J Heart Lung Transplant . 1993;  12 713-716
  • 93 Ross D J, Lewis M I, Kramer M, Vo A, Kass R M. FK 506 `Rescue' immunosuppression for obliterative bronchiolitis after lung transplantation.  Chest . 1997;  112 1175-1183
  • 94 Kesten S, Chaparro C, Scavuzza M, Gutierrez C. Tacrolimus as rescue therapy for bronchiolitis obliterans symdrome.  J Heart Lung Transplant . 1997;  16 905-912
  • 95 Whyte R I, Rossi S J, Mulligan M S. Mycophenolate mofetil for obliterative bronchiolitis syndrome after lung transplantation.  Ann Thorac Surg . 1997;  64 945-948
  • 96 Keenan R J, Konishi H, Kawai A. Clinical trial of tacrolimus versus cyclosporine in lung transplantation.  Ann Thorac Surg . 1995;  60 580-585
  • 97 Date H, Lynch J P, Sundaresan S, Patterson G A, Trulock E P. The impact of cytolytic therapy on bronchiolitis obliterans syndrome.  J Heart Lung Transplant . 1998;  17 869-875
  • 98 Valentine V G, Robbins R C, Berry G J. Actuarial survival of heart-lung and bilateral sequential lung transplant recipients with obliterative bronchiolitis.  J Heart Lung Transplant . 1996;  15 371-383
  • 99 Katzenstein A-L, Myers J L. Idiopathic pulmonary fibrosis.  Am J Respir Crit Care Med . 1998;  157 1301-1315
  • 100 Myers J L, Veal C F, Shin M S, Katzenstein A-L. Respiratory bronchiolitis causing interstitial lung disease: A clinicopathologic study of six cases.  Am Rev Respir Dis . 1987;  135 880-884
  • 101 Yousem S A, Colby T V, Gaensler E A. Respiratory bronchiolitis-associated interstitial lung disease and its relationship to desquamative interstitial pneumonia.  Mayo Clin Proc . 1989;  64 1373-1380
    >