Bronchoalveolar Lavage in Malignancy

ABSTRACT

Bronchoalveolar lavage is a useful diagnostic tool in diffuse or disseminated lung malignancies that do not involve the bronchial structures visible by endoscopy. The neoplastic histotype and the intraparenchymal neoplastic growth pattern are good predictors for diagnostic yield; adenocarcinoma, and tumors with lymphangitic or lepidic growth patterns are more easily diagnosed by bronchoalveolar lavage; in these cases the diagnostic yield reported is higher than 80%. In hematologic malignancies the diagnostic yield is quite good in secondary diffuse indolent B cell lymphomas and in primary B cell lymphomas of mucosa-associated lymphoid tissue (MALT) type but low in Hodgkin disease. Morphological analysis may be implemented by immunocytochemical or molecular tests to identify the cell lineage and the presence of monoclonality. Disorders in which bronchioloalveolar cell hyperplasia/dysplasia is a significant morphological component may have cytological features in bronchoalveolar lavage fluid that mimic lung neoplasms: acute respiratory distress syndrome (ARDS), acute interstitial pneumonitis (AIP), and acute exacerbation of idiopathic pulmonary fibrosis are the most important clinical entities in this group.

KEYWORDS

Bronchoalveolar lavage - bronchioloalveolar cell carcinoma - lymphoproliferative lung disorders - carcinomatous lymphangitis - lung neoplasms

REFERENCES

• 1 Poletti V, Chilosi M, Olivieri D. Diagnostic invasive procedures in diffuse infiltrative lung diseases.  Respiration. 2004;  71 107-119
• 2 Libby D M, Smith J P, Altorki N K, Pasmantier M W, Yankelevitz D, Henschke C I. Managing the small nodule discovered by CT.  Chest. 2004;  125 1522-1529
• 3 Dail D H. Metastases to and from the lung. In: Dail DH, Hammar SP Pulmonary Pathology. New York; Springer-Verlag 1994: 1585-1615
• 4 Muller K M, Respondek M. Pulmonary metastases: pathologic anatomy.  Lung. 1990;  168(s) 1137-1144
• 5 Travis W D, Garg K, Franklin W A et al.. Evolving concepts in the pathology and computed tomography imaging of lung adenocarcinoma and bronchioloalveolar carcinoma.  J Clin Oncol. 2005;  23 3279-3287
• 6 Jacobs J A, De Brauwer E I, Ramsay G et al.. Detection of non-infectious conditions mimicking pneumonia in the intensive care setting: usefulness of bronchoalveolar fluid cytology.  Respir Med. 1999;  93 571-578
• 7 Azoulay E, Fieux F, Moreau D et al.. Acute monocytic leukemia presenting as acute respiratory failure.  Am J Respir Crit Care Med. 2003;  167 1329-1333
• 8 Chilosi M, Zinzani P L, Poletti V. Lymphoproliferative lung disorders.  Semin Respir Crit Care Med. 2005;  26 490-501
• 9 Colombat M, Stern M, Groussard O et al.. Pulmonary cystic disorder related to light chain deposition disease.  Am J Respir Crit Care Med. 2006;  173 777-780
• 10 Yi E S. Tumors of the pulmonary vasculature.  Cardiol Clin. 2004;  22 431-440
• 11 Aubry M C, Myers J L, Colby T V, Leslie K O, Tazelaar H D. Endometrial stromal sarcoma metastatic to the lung: a detailed analysis of 16 patients.  Am J Surg Pathol. 2002;  26 440-449
• 12 Mark E J. Mesenchymal cystic hamartoma of the lung.  N Engl J Med. 1986;  315 1255-1259
• 13 Poletti V, Casadei G, Boaron M et al.. Epithelioid haemangioendothelioma of the lung imitating clinical features of pulmonary histiocytosis X.  Monaldi Arch Chest Dis. 1997;  52 346-348
• 14 Travis W D, Brambilla E, Muller-Hermelink H K et al.. Pathology and Genetics: Tumours of the Lung, Pleura, Thymus and Heart. Lyon; IARC 2004
• 15 Colby T V, Koss M N, Travis W D. Tumors of the Lower Respiratory Tract. Washington, DC; Armed Forces Institute of Pathology 1995 Armed Forces Institute of Pathology Fascicle, Third Series
• 16 Nind N R, Attanoos R L, Gibbs A R. Unusual intraparenchymal growth patterns of malignant pleural mesothelioma.  Histopathology. 2003;  42 150-155
• 17 Mutton A E, Hasleton P S, Curry A et al.. Differentiation of desquamative interstitial pneumonia (DIP) from pulmonary adenocarcinoma by immunocytochemistry.  Histopathology. 1998;  33 129-135
• 18 Janower M L, Blennerhassett J B. Lymphangitic spread of metastatic cancer to the lung: a radiologic-pathologic classification.  Radiology. 1971;  101 267-273
• 19 Roberts K E, Hamele-Bena D, Saqi A, Stein C A, Cole R P. Pulmonary tumor embolism: a review of the literature.  Am J Med. 2003;  115 228-232
• 20 Ko Y H, Han J H, Go J H et al.. Intravascular lymphomatosis: a clinicopathological study of two cases presenting as an interstitial lung disease.  Histopathology. 1997;  31 555-562
• 21 Colby T V. Malignancies in the lung and pleura mimicking benign processes.  Semin Diagn Pathol. 1995;  12 30-44
• 22 Webb W R. Thin-section CT of the secondary pulmonary lobule: anatomy and the image. The 2004 Fleischner Lecture.  Radiology. 2006;  239 322-338
• 23 Han D, Lee S, Franquet T et al.. Thrombotic and nonthrombotic pulmonary artery embolism: spectrum of imaging findings.  Radiographics. 2003;  23 1521-1539
• 24 Shintaku M, Hwang M H, Amitani R. Primary choriocarcinoma of the lung manifesting as diffuse alveolar damage.  Arch Pathol Lab Med. 2006;  130 540-543
• 25 Ebi N, Yamamoto H, Sakai J, Sugahara K, Arimura H, Nakanishi K. Angiosarcoma of the heart presenting as fatal pulmonary hemorrhage.  Intern Med. 1997;  36 191-193
• 26 Technical recommendations and guidelines for bronchoalveolar lavage (BAL). Report of the European Society of Pneumology Task Group.  Eur Respir J. 1989;  2 561-585
• 27 Linder J. Recent advances in thin-layer cytology.  Diagn Cytopathol. 1998;  18 24-32
• 28 Koss GL, Melamed MR Koss' Diagnostic Cytology. Philadelphia; Lippincott Williams & Wilkins 2006
• 29 Grotte D, Stanley M W, Swanson P E, Henry-Stanley M J, Davies S. Reactive type II pneumocytes in bronchoalveolar lavage fluid from adult respiratory distress syndrome can be mistaken for cells of adenocarcinoma.  Diagn Cytopathol. 1990;  6 317-322
• 30 Orfao A, Lopez A, Flores J et al.. Diagnosis of hematological malignancies: new applications for flow cytometry.  Hematology. 2006;  2 6-13 , (EHA Educ Program)
• 31 Springmeyer S C, Hackman R, Carlson J J et al.. Bronchoalveolar cell carcinoma diagnosed by bronchoalveolar lavage.  Chest. 1983;  83 278-279
• 32 Stover D E, Zaman M B, Hajdu S I, Lange M, Gold J, Armstrong D. Bronchoalveolar lavage in the diagnosis of diffuse pulmonary infiltrates in the immunosuppressed host.  Ann Intern Med. 1984;  101 1-7
• 33 Young J A, Hopkin J M, Cuthberston W P. Pulmonary infiltrates in immunocompromised patients: diagnosis by cytological examination of bronchoalveolar lavage fluid.  J Clin Pathol. 1984;  37 390-397
• 34 Sestini P, Rottoli L, Gotti G et al.. Bronchoalveolar lavage diagnosis of bronchioloalveolar carcinoma.  Eur J Respir Dis. 1985;  66 55-58
• 35 Rossi G A, Balbi B, Risso M, Repetto M, Ravazzoni C. Acute myelomonocytic leukemia: demonstration of pulmonary involvement by bronchoalveolar lavage.  Chest. 1985;  87 259-260
• 36 Weynants P, Cordier J F, Chapuis Collier C et al.. Primary immunocytoma of the lung: the diagnostic value of bronchoalveolar lavage.  Thorax. 1985;  40 542-543
• 37 Linder J, Radio S J, Robbins R A et al.. Bronchoalveolar lavage in the cytologic diagnosis of carcinoma of the lung.  Acta Cytol. 1987;  31 796-801
• 38 Morales F M, Matthews J I. Diagnosis of parenchymal Hodgkin's disease using bronchoalveolar lavage.  Chest. 1987;  91 785-787
• 39 Davis W B, Gadek J E. Detection of pulmonary lymphoma by bronchoalveolar lavage.  Chest. 1987;  91 787-790
• 40 Oka M, Kawano K, Kanda T et al.. Bronchoalveolar lavage in primary pulmonary lymphoma with monoclonal gammopathy.  Am Rev Respir Dis. 1988;  137 957-959
• 41 Poletti V, Patelli M, Poggi S, Bertanti T, Spiga L, Ferracini R. Transbronchial lung biopsy and bronchoalveolar lavage in diagnosis of diffuse infiltrative lung diseases.  Respiration. 1988;  54(s) 66-72
• 42 Levy H, Horak D A, Lewis M I. The value of bronchial washing and bronchoalveolar lavage in the diagnosis of lymphangitic carcinomatosis.  Chest. 1988;  94 1028-1030
• 43 Radio S J, Rennard S I, Kessinger A et al.. Breast carcinoma in bronchoalveolar lavage: a cytologic and immunohistochemical study.  Arch Pathol Lab Med. 1989;  113 333-336
• 44 Wisecarver J, Ness M J, Rennard S I, Thompson A B, Armitage J O, Linder L. Bronchoalveolar lavage in the assessment of pulmonary Hodgkin disease.  Acta Cytol. 1989;  33 527-532
• 45 Rennard S I, Albera C, Carratu L et al.. Clinical guidelines and indications for bronchoalveolar lavage (BAL): pulmonary malignancies.  Eur Respir J. 1990;  8 956-969
• 46 Pirozynski M. Bronchoalveolar lavage in the diagnosis of peripheral, primary lung cancer.  Chest. 1992;  102 372-374
• 47 de Garcia J, Bravo C, Miravitlles M et al.. Diagnostic value of bronchoalveolar lavage in peripheral lung cancer.  Am Rev Respir Dis. 1993;  147 649-652
• 48 Wongsurakiat P, Wongbunnate S, Dejsomritrutai W et al.. Diagnostic value of bronchoalveolar lavage and postbronchoscopic sputum cytology in peripheral lung cancer.  Respirology. 1998;  3 131-137
• 49 Gasparini S, Ferretti M, Secchi E B, Baldelli S, Zuccatosta L, Guselli P. Integration of transbronchial and percutaneous approach in the diagnosis of peripheral pulmonary nodules or masses: experience with 1,027 consecutive cases.  Chest. 1995;  108 131-137
• 50 Clark B D, Vezza P R, Copeland C, Wilder A M, Abati A. Diagnostic sensitivity of bronchoalveolar versus lung fine needle aspirate.  Mod Pathol. 2002;  15 1259-1265
• 51 Semenzato G, Poletti V. Bronchoalveolar lavage in lung cancer.  Respiration. 1992;  59(s) 44-46
• 52 Poletti V, Romagna M, Allen K A, Gasponi A, Spiga L. Bronchoalveolar lavage in the diagnosis of disseminated lung tumors.  Acta Cytol. 1995;  39 472-477
• 53 Costabel U. Atlas of Bronchoalveolar Lavage. London; Chapman & Hall Medical 1998: 41-46
• 54 Wislez M, Massiani M A, Melleron B et al.. Clinical characteristics of pneumonic-type adenocarcinoma of the lung.  Chest. 2003;  123 1868-1877
• 55 Yang S P, Lin C C. Lymphangitic carcinomatosis of the lungs: the clinical significance of its roentgenologic classification.  Chest. 1972;  62 179-187
• 56 Subramanian J, Govindan R. Lung cancer in never smokers: a review.  J Clin Oncol. 2007;  25 561-570
• 57 Lower E E, Baughman R P. Pulmonary lymphangitic metastasis from breast cancer: lymphocytic alveolitis is associated with favorable prognosis.  Chest. 1992;  102 1113-1117
• 58 Bellocq A, Antoine M, Flahault A et al.. Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome.  Am J Pathol. 1998;  152 83-92
• 59 Aubry M C, Myers J L, Douglas W W et al.. Primary pulmonary carcinoma in patients with idiopathic pulmonary fibrosis.  Mayo Clin Proc. 2002;  77 763-770
• 60 Yang Y, Fujita J, Tokuda M, Bandoh S, Ishida T. Lung cancer associated with several connective tissue diseases: with a review of literature.  Rheumatol Int. 2001;  21 106-111
• 61 Ioachimescu O C, Metha A C. From cystic pulmonary airway malformation, to bronchioloalveolar carcinoma and adenocarcinoma of the lung.  Eur Respir J. 2005;  26 1181-1187
• 62 Takahashi K, Ishida T, Ogura G et al.. Diagnostic usefulness of bronchoalveolar lavage in Hermanski-Pudlak syndrome: a case with double lung cancers.  Intern Med. 2004;  43 972-976
• 63 Biyoudi-Vouenze R, Tazi A, Hance A J, Chastre J, Basset F, Soler P. Abnormal epithelial cells recovered by bronchoalveolar lavage: are they malignant?.  Am Rev Respir Dis. 1990;  142 686-690
• 64 Chilosi M, Zamò A, Doglioni C et al.. Migratory marker expression in fibroblast foci of idiopathic pulmonary fibrosis.  Respir Res. 2006;  7 95
• 65 Chilosi M, Zinzani P L, Poletti V. Lymphoproliferative lung disorders.  Semin Respir Crit Care Med. 2005;  26 490-501
• 66 Koh T T, Colby T V, Muller N L. Myeloid leukemias and lung involvement.  Semin Respir Crit Care Med. 2005;  26 514-519
• 67 Bertoni F, Zucca E. Delving deeper into MALT lymphoma biology.  J Clin Invest. 2006;  116 22-26
• 68 Sverzellati N, Poletti V, Chilosi M, Casoni G, Hansell D, Zompatori M. The crazy paving pattern in granulomatous mycosis fungoides: high resolution computer tomography-pathological correlation.  J Comput Assist Tomogr. 2006;  30 843-845
• 69 Chetty R, Slavin J L, O'Leary J J, Ansari N A, Gatter K C. Primary Hodgkin's disease of the lung.  Pathology. 1995;  27 111-114
• 70 Zinzani P L, Tani M, Gabriele A et al.. Extranodal marginal zone B-cell lymphoma of MALT-type of the lung: single-center experience with 12 patients.  Leuk Lymphoma. 2003;  44 821-824
• 71 Poletti V, Romagna M, Gasponi A, Baruzzi G, Allen K A. Bronchoalveolar lavage in the diagnosis of low-grade, MALT type, B-cell lymphoma in the lung.  Monaldi Arch Chest Dis. 1995;  50 191-194
• 72 Keicho N, Oka T, Takeuchi K, Yamane A, Yazaki Y, Yotsumoto H. Detection of lymphomatous involvement of the lung by bronchoalveolar lavage: application of immunophenotypic and gene rearrangement analysis.  Chest. 1994;  105 458-462
• 73 Zompi S, Couderc L J, Cadranel J et al.. Clonality analysis of alveolar B lymphocytes contributes to the diagnostic strategy in clinical suspicion of pulmonary lymphoma.  Blood. 2004;  103 3208-3215
• 74 Trisolini R, Lazzari Agli L, Poletti V. Bronchiolocentric pulmonary involvement due to chronic lymphocytic leukaemia.  Haematologica. 2000;  85 1097
• 75 Marrucchella A, Epis R, Camerone G, Tondini M. Association between chronic lymphocytic leukaemia and sarcoidosis: clinical value of bronchoalveolar lavage.  Sarcoidosis Vasc Diffuse Lung Dis. 1999;  16 101-103
• 76 Kamble R, Rosenzweig T. Diffuse pulmonary parenchymal involvement in multiple myeloma: antemortem diagnosis.  Int J Hematol. 2006;  83 259-261
• 77 Kovalski R, Hansen-Flaschen J, Lodato R F, Pietra G G. Localized leukemic pulmonary infiltrates: diagnosis by bronchoscopy and resolution with therapy.  Chest. 1990;  97 674-678
• 78 Linder J, Rennard S I. Bronchoalveolar Lavage. Chicago; American Society of Clinical Pathologists Press 1988
• 79 Tamm M, Reichenberger T M, McGandy C E et al.. Diagnosis of pulmonary Kaposi's sarcoma by detection of human herpes virus 8 in bronchoalveolar lavage.  Am J Respir Crit Care Med. 1998;  157 458-463
• 80 Chilosi M, Poletti V, Murer B et al.. Abnormal re-epithelization and lung remodeling in idiopathic pulmonary fibrosis: the role of deltaN-p63.  Lab Invest. 2002;  82 1335-1345
• 81 Linssen K C, Jacobs J A, Poletti V et al.. Reactive type II pneumocytes in bronchoalveolar lavage fluid.  Acta Cytol. 2004;  48 497-504
• 82 Stanley M W, Henry-Stanley M J, Gajl-Peczalska K J, Bitterman P B. Hyperplasia of type II pneumocytes in acute lung injury.  Am J Clin Pathol. 1992;  97 669-677
• 83 Beskow C O, Drachenberg C B, Bourquin P M et al.. Diffuse alveolar damage: morphologic features in bronchoalveolar lavage fluid.  Acta Cytol. 2000;  44 640-646
• 84 Bonaccorsi A, Cancellieri A, Chilosi M et al.. Acute interstitial pneumonia: report of a series.  Eur Respir J. 2003;  21 187-191
• 85 Ambrosini V, Cancellieri A, Chilosi M et al.. Acute exacerbation of idiopathic pulmonary fibrosis: report of a series.  Eur Respir J. 2003;  22 821-826
• 86 Trisolini R, Cancellieri A, Bonaccorsi A, Poletti V. Bronchoalveolar lavage suggesting diffuse alveolar damage in a patient with acute eosinophilic pneumonia.  Sarcoidosis Vasc Diffuse Lung Dis. 2001;  18 311-312
• 87 Waeker T, Mukerjee D, Levine T S. Bronchial epithelial atypia mimicking squamous cell carcinoma secondary to cyclophosphamide therapy.  Cytopathology. 2002;  13 330-332
• 88 Cazzato S, Zompatori M, Baruzzi G et al.. Bronchiolitis obliterans-organizing pneumonia: an Italian experience.  Respir Med. 2000;  94 702-708
• 89 Masih A S, Woods G L, Thiele G M et al.. Detection of cytomegalovirus in bronchoalveolar lavage: a comparison of techniques.  Mod Pathol. 1991;  4 108-112
• 90 Greenwald P. A favourable view: progress in cancer prevention and screening.  Recent Results Cancer Res. 2007;  174 3-17
• 91 de Fraipont F, Moro-Sibilot D, Michelland S, Brambilla E, Brambilla C, Favrot M C. Promoter methylation of genes in bronchial lavages: a marker for early diagnosis of primary and relapsing non-small cell lung cancer?.  Lung Cancer. 2005;  50 199-209
• 92 Phillips M, Cataneo R N, Cummin A R et al.. Detection of lung cancer with volatile markers in the breath.  Chest. 2003;  123 2115-2123
• 93 Poli D, Carbognani P, Corradi M et al.. Exhaled volatile organic compounds in patients with non-small cell lung cancer: cross sectional and nested short-term follow-up study.  Respir Res. 2005;  6 71-80