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Review

The relevance of bronchoalveolar lavage fluid analysis for lung cancer patients

Pages 329-337 | Received 19 Aug 2019, Accepted 20 Dec 2019, Published online: 25 Dec 2019

References

  • Reynolds HY, Newball HH. Analysis of proteins and respiratory cells obtained from human lungs by bronchial lavage. J Lab Clin Med. 1974;84(4):559–573.
  • Reynolds HY. Use of bronchoalveolar lavage in humans–past necessity and future imperative. Lung. 2000;178(5):271–293.
  • Technical recommendations and guidelines for bronchoalveolar lavage (BAL). Report of the European society of pneumology task group. Eur Respir J. 1989 Jun;2(6):561–585.
  • Bronchoalveolar lavage constituents in healthy individuals, idiopathic pulmonary fibrosis, and selected comparison groups. The BAL cooperative group steering committee. Am Rev Respir Dis. 1990;141:S169–S202.
  • Clinical guidelines and indications for bronchoalveolar lavage (BAL): report of the European society of pneumology task group on BAL. Eur Respir J. 1990;3(8):937–976.
  • Chcialowski A, Chorostkowska-Wynimko J, Fal A, et al. Recommendation of the Polish Respiratory Society for bronchoalveolar lavage (BAL) sampling, processing and analysis methods. Pneumonol Alergol Pol. 2011;79(2):75–98.
  • Baughman RP. Technical aspects of bronchoalveolar lavage: recommendations for a standard procedure. Semin Respir Crit Care Med. 2007 Oct;28(5):475–485.
  • Costabel U. Atlas of bronchoalveolar lavage. Chapman and Hall Medical; 1998.
  • Linder J, Radio SJ, Robbins RA, et al. Bronchoalveolar lavage in the cytologic diagnosis of carcinoma of the lung. Acta Cytol. 1987 Nov;31(6):796–801.
  • Poletti V, Poletti G, Murer B, et al. Bronchoalveolar lavage in malignancy. Semin Respir Crit Care Med. 2007 Oct;28(5):534–545.
  • Yoss EB, Berd D, Cohn Jr, et al. Flow cytometric evaluation of bronchoscopic washings and lavage fluid for DNA aneuploidy as an adjunct in the diagnosis of lung cancer and tumors metastatic to the lung. Chest. 1989 Jul;96(1):54–59.
  • Dauber JH, Wagner M, Brunsvold S, et al. Flow cytometric analysis of lymphocyte phenotypes in bronchoalveolar lavage fluid: comparison of a two-color technique with a standard immunoperoxidase assay. Am J Respir Cell Mol Biol. 1992 Nov;7(5):531–541.
  • Morgan E, Varro R, Sepulveda H, et al. Cytometric bead array: a multiplexed assay platform with applications in various areas of biology. Clin Immunol. 2004 Mar;110(3):252–266.
  • Marsan C, Chosia M. Diagnostic value of bronchoalveolar lavage in immunodepressed patients. Patologia Polska. 1990;41(4):178–182.
  • de Gracia J, Bravo C, Miravitlles M, et al. Diagnostic value of bronchoalveolar lavage in peripheral lung cancer. Am Rev Respir Dis. 1993;147(3):649–652.
  • Pirozynski M. Bronchoalveolar lavage in the diagnosis of peripheral, primary lung cancer. Chest. 1992;102(2):372–374.
  • Poletti V, Romagna M, Gasponi A, et al. Bronchoalveolar lavage in the diagnosis of low-grade, MALT type, B-cell lymphoma in the lung. Monaldi Arch Chest Dis. 1995;50(3):191–194.
  • Debeljak A, Mermolja M, Sorli J, et al. Bronchoalveolar lavage in the diagnosis of peripheral primary and secondary malignant lung tumors. Respiration. 1994;61(4):226–230.
  • Rennard SI, Albera C, Carratu L, et al. Clinical guidelines and indications for bronchoalveolar lavage (BAL): pulmonary malignancies. Eur Respir J. 1990;3(8):956–959.
  • Schreiber G, McCrory DC. Performance characteristics of different modalities for diagnosis of suspected lung cancer: summary of published evidence. Chest. 2003;123(1Suppl):115S–28S.
  • Han S, Yang W, Li H. A study of the application of fiberoptic bronchoscopy combined with liquid-based cytology test in the early diagnosis of lung cancer. Oncol Lett. 2018;16(5):5807–5812.
  • Canberk S, Montezuma D, Aydin O, et al. The new guidelines of Papanicolaou society of cytopathology for respiratory specimens: assessment of risk of malignancy and diagnostic yield in different cytological modalities. Diagn Cytopathol. 2018;46(9):725–729.
  • Ebert W, Dienemann H, Fateh-Moghadam A. et al. Cytokeratin 19 fragment CYFRA 21-1 compared with carcinoembryonic antigen, squamous cell carcinoma antigen and neuron-specific enolase in lung cancer. Results of an international multicentre study. Eur J Clin Chem Clin Biochem. 1994;32(3):189–199.
  • Niklinski J, Chyczewska E, Furman M, et al. Usefulness of a multiple biomarker assay in bronchoalveolar lavage (BAL) and serum for the diagnosis of small cell lung cancer. Neoplasma. 1993;40(5):305–308.
  • Niklinski J, Chyczewska E, Furman M, et al. Value of CEA and SCC-Ag in bronchoalveolar lavage (BAL) and serum of patients with lung carcinoma. Neoplasma. 1992;39(5):283–285.
  • Calabrese F, Lunardi F, Pezzuto F, et al. Are there new biomarkers in tissue and liquid biopsies for the early detection of non-small cell lung cancer? J Clin Med. 2019 26;8(3):414. .
  • Rolfo C, Castiglia M, Hong D, et al. Liquid biopsies in lung cancer: the new ambrosia of researchers. Biochim Biophys Acta. 2014;1846(2):539–546.
  • Rolfo C, Mack PC, Scagliotti GV, et al. Liquid biopsy for advanced non-small cell lung cancer (NSCLC): a statement paper from the IASLC. J Thorac Oncol. 2018;13(9):1248–1268.
  • Lindeman NI, Cagle PT, Aisner DL, et al. Updated molecular testing guideline for the selection of lung cancer patients for treatment with targeted tyrosine kinase inhibitors: guideline from the college of American pathologists, the international association for the study of lung cancer, and the association for molecular pathology. J Mol Diagn. 2018;20(2):129–159.
  • Travis WD, Brambilla E, Noguchi M, et al. Diagnosis of lung cancer in small biopsies and cytology: implications of the 2011 international association for the study of lung cancer/American thoracic society/European respiratory society classification. Arch Pathol Lab Med. 2013;137(5):668–684.
  • Koss LG, Woyke S, Olszewski WT. Aspiration biopsy, cytology interpretation and histological bases. II ed. New York: Igaku Shoin; 1992.
  • Travis WD, Brambilla E, Noguchi M, et al. International association for the study of lung cancer/American thoracic society/European respiratory society: international multidisciplinary classification of lung adenocarcinoma: executive summary. Proc Am Thorac Soc. 2011;8(5):381–385.
  • Travis WD, Brambilla E, Nicholson AG, et al. The 2015 World Health Organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol. 2015;10(9):1243–1260.
  • Metovic J, Righi L, Delsedime L, et al. Role of immunocytochemistry in the cytological diagnosis of pulmonary tumors. Acta Cytol. 2019;15:1–14.
  • Choo R, Naser NSH, Nadkarni NV, et al. Utility of bronchoalveolar lavage in the management of immunocompromised patients presenting with lung infiltrates. BMC Pulm Med. 2019;19(1):51.
  • Costabel U, Bross KJ, Reuter C, et al. Alterations in immunoregulatory T-cell subsets in cigarette smokers. A phenotypic analysis of bronchoalveolar and blood lymphocytes. Chest. 1986;90(1):39–44.
  • Mancini NM, Bene MC, Gerard H, et al. Early effects of short-time cigarette smoking on the human lung: a study of bronchoalveolar lavage fluids. Lung. 1993;171(5):277–291.
  • Hoser G, Domagala-Kulawik J, Droszcz P, et al. Lymphocyte subsets differences in smokers and nonsmokers with primary lung cancer: a flow cytometry analysis of bronchoalveolar lavage fluid cells. Med Sci Monit. 2003;9(8):BR310–BR315.
  • Grotte D, Stanley MW, Swanson PE, et al. Reactive type II pneumocytes in bronchoalveolar lavage fluid from adult respiratory distress syndrome can be mistaken for cells of adenocarcinoma. Diagn Cytopathol. 1990;6(5):317–322.
  • Domagala-Kulawik J, Droszcz P. Squamous metaplasia of the bronchial micosa-significance in pulmonary tumor diagnosis and its relationship to smoking. Med Sci Monit. 1998;4(6):993–996.
  • Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373(2):123–135.
  • Reck M, Rabe KF. Advanced non-small-cell lung cancer. N Engl J Med. 2017;377(20):1999.
  • Aerts JG, Hegmans JP. Tumor-specific cytotoxic T cells are crucial for efficacy of immunomodulatory antibodies in patients with lung cancer. Cancer Res. 2013;73(8):2381–2388.
  • Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480(7378):480–489.
  • Domagala-Kulawik J. Immune checkpoint inhibitors in non-small cell lung cancer - towards daily practice. Adv Respir Med. 2018;86(3):144–150.
  • Peters S, Reck M, Smit EF, et al. How to make the best use of immunotherapy as first-line treatment for advanced/metastatic non-small-cell lung cancer. Ann Oncol. 2019;26. DOI:10.1093/annonc/mdz109.
  • Chen DS, Mellman I. Elements of cancer immunity and the cancer-immune set point. Nature. 2017;541(7637):321–330.
  • Teng MW, Ngiow SF, Ribas A, et al. Classifying cancers based on T-cell infiltration and PD-L1. Cancer Res. 2015;75(11):2139–2145.
  • Bedognetti D, Ceccarelli M, Galluzzi L, et al. Toward a comprehensive view of cancer immune responsiveness: a synopsis from the SITC workshop. J Immunother Cancer. 2019;7(1):131.
  • Galon J, Pages F, Marincola FM, et al. The immune score as a new possible approach for the classification of cancer. J Transl Med. 2012;10:1.
  • Domagala-Kulawik J, Raniszewska A. How to evaluate the immune status of lung cancer patients before immunotherapy. Breathe (Sheff). 2017;13(4):291–296.
  • Fracchia A, Ubbiali A, El Bitar O, et al. A comparative study on ferritin concentration in serum and bilateral bronchoalveolar lavage fluid of patients with peripheral lung cancer versus control subjects. Oncology. 1999;56(3):181–188.
  • Olsen GN, Gangemi JD. Bronchoalveolar lavage and the immunology of primary lung cancer. Chest. 1985;87(5):677–683.
  • Piazza C, Gilardini Montani MS, Moretti S, et al. Cutting edge: CD4+ T cells kill CD8+ T cells via Fas/Fas ligand- mediated apoptosis. J Immunol. 1997;158(4):1503–1506.
  • Domagala-Kulawik J, Guzman J, Costabel U. Immune cells in bronchoalveolar lavage in peripheral lung cancer–analysis of 140 cases. Respiration. 2003;70(1):43–48.
  • Domagala-Kulawik J, Hoser G, Droszcz P, et al. T-cell subtypes in bronchoalveolar lavage fluid and in peripheral blood from patients with primary lung cancer. Diagn Cytopathol. 2001;25(4):208–213.
  • Hoser G, Kawiak J, Domagala-Kulawik J, et al. Flow cytometric evaluation of lymphocyte subpopulations in BALF of healthy smokers and nonsmokers. Folia Histochem Cytobiol. 1999;37(1):25–30.
  • Domagala-Kulawik J, Maskey-Warzecowska M. T-regulatory cells in COPD or tumour environment. Eur Respir J. 2009 Jul;34(1):284–286.
  • Yoshino I, Yano T, Murata M, et al. Phenotypes of lymphocytes infiltrating non-small cell lung cancer tissues and its variation with histological types of cancer. Lung Cancer. 1993;10(1–2):13–19.
  • Osinska I, Stelmaszczyk-Emmel A, Polubiec-Kownacka M, et al. CD4+/CD25high/FoxP3+/CD127-regulatory T cells in bronchoalveolar lavage fluid of lung cancer patients. Hum Immunol. 2016;77(10):912–915.
  • Erfani N, Mehrabadi SM, Ghayumi MA, et al. Increase of regulatory T cells in metastatic stage and CTLA-4 over expression in lymphocytes of patients with non-small cell lung cancer (NSCLC). Lung Cancer. 2012;77(2):306–311.
  • Schneider T, Kimpfler S, Warth A, et al. Foxp3(+) regulatory T cells and natural killer cells distinctly infiltrate primary tumors and draining lymph nodes in pulmonary adenocarcinoma. J Thorac Oncol. 2011;6(3):432–438.
  • Kwiecien I, Stelmaszczyk-Emmel A, Polubiec-Kownacka M, et al. Elevated regulatory T cells, surface and intracellular CTLA-4 expression and interleukin-17 in the lung cancer microenvironment in humans. Cancer Immunol Immunother. 2016;11(4):pii: E567.
  • Kwiecien I, Skirecki T, Polubiec-Kownacka M, et al. Immunophenotype of T cells expressing programmed death-1 and cytotoxic T cell antigen-4 in early lung cancer: local vs systemic immune response. Cancers (Basel). 2019;11:4.
  • Brcic L, Stanzer S, Krenbek D, et al. Immune cell landscape in therapy-naive squamous cell and adenocarcinomas of the lung. Virchows Arch. 2018;472(4):589–598.
  • Zikos TA, Donnenberg AD, Landreneau RJ, et al. Lung T-cell subset composition at the time of surgical resection is a prognostic indicator in non-small cell lung cancer. Cancer Immunol Immunother. 2011;60(6):819–827.
  • Staal-van den Brekel AJ, Dentener MA, Drent M, et al. The enhanced inflammatory response in non-small cell lung carcinoma is not reflected in the alveolar compartment. Respir Med. 1998;92(1):76–83.
  • Haslam PL, Baughman RP. Report of ERS task force: guidelines for measurement of acellular components and standardization of BAL. Eur Respir J. 1999 Aug;14(2):245–248.
  • Kopinski P, Wandtke T, Dyczek A, et al. Increased levels of interleukin 27 in patients with early clinical stages of non-small cell lung cancer. Pol Arch Intern Med. 2018;128(2):105–114.
  • Jakubowska K, Naumnik W, Niklinska W, et al. Clinical Significance of HMGB-1 and TGF-beta level in serum and BALF of advanced non-small cell lung cancer. Adv Exp Med Biol. 2015;852:49–58.
  • Naumnik W, Naumnik B, Niklinska W, et al. Clinical implications of hepatocyte growth factor, interleukin-20, and interleukin-22 in serum and bronchoalveolar fluid of patients with non-small cell lung cancer. Adv Exp Med Biol. 2016;952:41–49.
  • Naumnik W, Panek B, Ossolinska M, et al. B cell-attracting chemokine-1 and progranulin in bronchoalveolar lavage fluid of patients with advanced non-small cell lung cancer: new prognostic factors. Adv Exp Med Biol. 2019;1150:11–16.
  • Naumnik W, Plonska I, Ossolinska M, et al. Prognostic value of osteoprotegerin and sRANKL in bronchoalveolar lavage fluid of patients with advanced non-small cell lung cancer. Adv Exp Med Biol. 2018;1047:1–6.
  • Domagala-Kulawik J, Hoser G, Safianowska A, et al. Elevated TGF-beta1 concentration in bronchoalveolar lavage fluid from patients with primary lung cancer. Arch Immunol Ther Exp (Warsz). 2006;54(2):143–147.
  • Dabrowska M, Grubek-Jaworska H, Hoser G, et al. Effect of IFN-gamma stimulation on expression of intercellular adhesion molecule-1 (ICAM-1) on alveolar macrophages in patients with non-small cell lung cancer. J Interferon Cytokine Res. 2006;26(3):190–195.
  • Whiteside TL. Exosomes in cancer: another mechanism of tumor-induced immune suppression. Adv Exp Med Biol. 2017;1036:81–89.
  • Yang Y, Ji P, Wang X, et al. Bronchoalveolar lavage fluid-derived exosomes: a novel role contributing to lung cancer growth. Front Oncol. 2019;9:197.
  • Suresh K, Naidoo J, Lin CT, et al. Immune checkpoint immunotherapy for non-small cell lung cancer: benefits and pulmonary toxicities. Chest. 2018;154(6):1416–1423.
  • Naidoo J, Wang X, Woo KM, et al. Pneumonitis in patients treated with anti-programmed death-1/programmed death ligand 1 therapy. J Clin Oncol. 2017;35(7):709–717.
  • Martins F, Sykiotis GP, Maillard M, et al. New therapeutic perspectives to manage refractory immune checkpoint-related toxicities. Lancet Oncol. 2019;20(1):e54–e64.
  • Montaudie H, Pradelli J, Passeron T, et al. Pulmonary sarcoid-like granulomatosis induced by nivolumab. Br J Dermatol. 2017;176(4):1060–1063.
  • Tanaka K, Yanagihara T, Ikematsu Y, et al. Detection of identical T cell clones in peritumoral pleural effusion and pneumonitis lesions in a cancer patient during immune-checkpoint blockade. Oncotarget. 2018;9(55):30587–30593.

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