Malignant pleural effusion: current understanding and therapeutic approach.
Chest drain
Indwelling pleural catheter (IPC)
Malignant pleural effusion (MPE)
Oncology
Pleural
Pleurodesis
Thoracoscopy
Journal
Respiratory research
ISSN: 1465-993X
Titre abrégé: Respir Res
Pays: England
ID NLM: 101090633
Informations de publication
Date de publication:
19 Jan 2024
19 Jan 2024
Historique:
received:
10
12
2023
accepted:
05
01
2024
medline:
20
1
2024
pubmed:
20
1
2024
entrez:
19
1
2024
Statut:
epublish
Résumé
Malignant pleural effusion (MPE) is a common complication of thoracic and extrathoracic malignancies and is associated with high mortality and elevated costs to healthcare systems. Over the last decades the understanding of pathophysiology mechanisms, diagnostic techniques and optimal treatment intervention in MPE have been greatly advanced by recent high-quality research, leading to an ever less invasive diagnostic approach and more personalized management. Despite a number of management options, including talc pleurodesis, indwelling pleural catheters and combinations of the two, treatment for MPE remains symptom directed and centered around drainage strategy. In the next future, because of a better understanding of underlying tumor biology together with more sensitive molecular diagnostic techniques, it is likely that combined diagnostic and therapeutic procedures allowing near total outpatient management of MPE will become popular. This article provides a review of the current advances, new discoveries and future directions in the pathophysiology, diagnosis and management of MPE.
Identifiants
pubmed: 38243259
doi: 10.1186/s12931-024-02684-7
pii: 10.1186/s12931-024-02684-7
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
47Informations de copyright
© 2024. The Author(s).
Références
Aboudara M, Maldonado F. Update in the management of Pleural effusions. Med Clin North Am. 2019;103:475–85.
pubmed: 30955515
doi: 10.1016/j.mcna.2018.12.007
Villanueva A. Management of malignant pleural effusions. In: Ernst A, Herth FJ, editors. Principles and Practice of Interventional Pulmonology. New York: Springer; 2012. pp. 665–74.
Scherpereel A, Astoul P, Baas P, et al. Guidelines of the European Respiratory Society and the European Society of Thoracic Surgeons for the management of malignant pleural mesothelioma. Eur Respir J. 2010;35:479–95.
pubmed: 19717482
doi: 10.1183/09031936.00063109
Roberts ME, Rahman NM, Maskell NA, et al. British thoracic Society Guideline for pleural disease. Thorax. 2023;78:1–42.
doi: 10.1136/thorax-2022-219784
Mummadi SR, Stoller JK, Lopez R, et al. Epidemiology of adult Pleural Disease in the United States. Chest. 2021;160:1534–51.
pubmed: 34023322
doi: 10.1016/j.chest.2021.05.026
Bibby AC, Dorn P, Psallidas I, et al. ERS/EACTS statement on the management of malignant pleural effusions. Eur Respir J. 2018;52:1800349.
pubmed: 30054348
doi: 10.1183/13993003.00349-2018
Porcel JM, Gasol A, Bielsa S, et al. Clinical features and survival of lung cancer patients with pleural effusions. Respirology. 2015;20:654–9.
pubmed: 25706291
doi: 10.1111/resp.12496
Clive AO, Kahan BC, Hooper CE, et al. Predicting survival in malignant pleural effusion: development and validation of the LENT prognostic score. Thorax. 2014;69:1098–104.
pubmed: 25100651
doi: 10.1136/thoraxjnl-2014-205285
Psallidas I, Kanellakis NI, Gerry S, et al. Development and validation of response markers to predict survival and pleurodesis success in patients with malignant pleural effusion (PROMISE): a multicohort analysis. Lancet Oncol. 2018;19:930–9.
pubmed: 29908990
doi: 10.1016/S1470-2045(18)30294-8
Quek JC, Tan QL, Allen JC, et al. Malignant pleural effusion survival prognostication in an Asian population. Respirology. 2020;25:1283–91.
pubmed: 32390227
doi: 10.1111/resp.13837
Cheah HM, Lansley SM, Varano Della Vergiliana JF, et al. Malignant pleural fluid from mesothelioma has potent biological activities. Respirology. 2017;22:192–9.
pubmed: 27560254
doi: 10.1111/resp.12874
Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–74.
pubmed: 21376230
doi: 10.1016/j.cell.2011.02.013
Psallidas I, Kalomenidis I, Porcel JM, et al. Malignant pleural effusion: from bench to bedside. Eur Respir Rev. 2016;25:189–98.
pubmed: 27246596
pmcid: 9487241
doi: 10.1183/16000617.0019-2016
Stathopoulos GT, Kalomenidis I. Malignant pleural effusion: tumor-host interactions unleashed. Am J Respir Crit Care Med. 2012;186:487–92.
pubmed: 22652027
doi: 10.1164/rccm.201203-0465PP
Asciak R, Kanellakis NI, Yao X, et al. Pleural Fluid has pro-growth Biological properties which enable Cancer Cell Proliferation. Front Oncol. 2021;11:658395.
pubmed: 33996582
pmcid: 8115017
doi: 10.3389/fonc.2021.658395
Sahn SA. Pleural diseases related to metastatic malignancies. Eur Respir J. 1997;10:1907–13.
pubmed: 9272937
doi: 10.1183/09031936.97.10081907
Maker AV, Nguyen DM. Images in cardiothoracic surgery. Active malignant pleural effusion captured through the thoracoscope. Ann Thorac Surg. 2005;80:1941.
pubmed: 16242497
doi: 10.1016/j.athoracsur.2003.11.065
Sakr L, Maldonado F, Greillier L, et al. Thoracoscopic assessment of pleural tumor burden in patients with malignant pleural effusion: prognostic and therapeutic implications. J Thorac Oncol. 2011;6:592–7.
pubmed: 21258256
doi: 10.1097/JTO.0b013e318208c7c1
Light RW, Hamm H. Malignant pleural effusion: would the real cause please stand up? Eur Respir J. 1997;10:1701–2.
pubmed: 9272907
doi: 10.1183/09031936.97.10081701
Chen YM, Yang WK, Whang-Peng J, et al. Elevation of interleukin-10 levels in malignant pleural effusion. Chest. 1996;110:433–36.
pubmed: 8697847
doi: 10.1378/chest.110.2.433
Chen Y, Mathy NW, Lu H. The role of VEGF in the diagnosis and treatment of malignant pleural effusion in patients with nonsmall cell lung cancer (review). Mol Med Rep. 2018;17:8019–30.
pubmed: 29693703
pmcid: 5983970
Stathopoulos GT, Zhu Z, Everhart MB, et al. Nuclear factor-kappab affects tumor progression in a mouse model of malignant pleural effusion. Am J Respir Cell Mol Biol. 2006;34:142–50.
pubmed: 16210694
doi: 10.1165/rcmb.2005-0130OC
Yeh HH, Lai WW, Chen HH, et al. Autocrine IL-6-induced Stat3 activation contributes to the pathogenesis of lung adenocarcinoma and malignant pleural effusion. Oncogene. 2006;25:4300–9.
pubmed: 16518408
doi: 10.1038/sj.onc.1209464
Psallidas I, Stathopoulos GT, Maniatis NA, et al. Secreted phosphoprotein-1 directly provokes vascular leakage to foster malignant pleural effusion. Oncogene. 2013;32:528–35.
pubmed: 22370646
doi: 10.1038/onc.2012.57
Stathopoulos GT, Kollintza A, Moschos C, et al. Tumor necrosis factor-alpha promotes malignant pleural effusion. Cancer Res. 2007;67:9825–34.
pubmed: 17942913
doi: 10.1158/0008-5472.CAN-07-1064
Giannou AD, Marazioti A, Spella M, et al. Mast cells mediate malignant pleural effusion formation. J Clin Invest. 2015;125:2317–34.
pubmed: 25915587
pmcid: 4497757
doi: 10.1172/JCI79840
Agalioti T, Giannou AD, Krontira AC, et al. Mutant KRAS promotes malignant pleural effusion formation. Nat Commun. 2017;8:15205.
pubmed: 28508873
doi: 10.1038/ncomms15205
Mercer RM, Varatharajah R, Shepherd G, et al. Critical analysis of the utility of initial pleural aspiration in the diagnosis and management of suspected malignant pleural effusion. BMJ Open Respir Res. 2020;7:e000701.
pubmed: 32963027
pmcid: 7509958
doi: 10.1136/bmjresp-2020-000701
Qureshi NR, Rahman NM, Gleeson FV. Thoracic ultrasound in the diagnosis of malignant pleural effusion. Thorax. 2009;64:139–43.
pubmed: 18852159
doi: 10.1136/thx.2008.100545
Bandi V, Lunn W, Ernst A, et al. Ultrasound vs. CT in detecting chest wall invasion by tumor: a prospective study. Chest. 2008;133:881–6.
pubmed: 17951616
doi: 10.1378/chest.07-1656
Asciak R, Bedawi EO, Bhatnagar R, et al. British thoracic Society Clinical Statement on pleural procedures. Thorax. 2023;78:43–68.
doi: 10.1136/thorax-2022-219371
Diacon AH, Brutsche MH, Soler M. Accuracy of pleural puncture sites: a prospective comparison of clinical examination with ultrasound. Chest. 2003;123:436–41.
pubmed: 12576363
doi: 10.1378/chest.123.2.436
Jones PW, Moyers JP, Rogers JT, et al. Ultrasound-guided thoracentesis: is it a safer method? Chest. 2003;123:418–23.
pubmed: 12576360
doi: 10.1378/chest.123.2.418
Salamonsen M, Dobeli K, McGrath D, et al. Physician-performed ultrasound can accurately screen for a vulnerable intercostal artery prior to chest drainage procedures. Respirology. 2013;18:942–7.
pubmed: 23521021
doi: 10.1111/resp.12088
Marchetti G, Valsecchi A, Indellicati D, et al. Ultrasound-guided medical thoracoscopy in the absence of pleural effusion. Chest. 2015;147:1008–12.
pubmed: 25188712
doi: 10.1378/chest.14-0637
Hassan M, Asciak R, Mercer RM, et al. Echogenic swirling seen on Ultrasound and Outcome of Pleurodesis in Malignant Pleural Effusion. Arch Bronconeumol (Engl Ed). 2019;55:659–61.
pubmed: 31204005
doi: 10.1016/j.arbr.2019.05.018
Hallifax RJ, Talwar A, Wrightson JM, et al. State-of-the-art: radiological investigation of pleural disease. Respir Med. 2017;124:88–99.
pubmed: 28233652
doi: 10.1016/j.rmed.2017.02.013
Leung AN, Muller NL, Miller RR. CT in differential diagnosis of diffuse pleural disease. AJR Am J Roentgenol. 1990;154:487–92.
pubmed: 2106209
doi: 10.2214/ajr.154.3.2106209
Porcel JM, Pardina M, Bielsa S, et al. Derivation and validation of a CT scan scoring system for discriminating malignant from benign pleural effusions. Chest. 2015;147:513–9.
pubmed: 25255186
doi: 10.1378/chest.14-0013
Woolhouse I, Bishop L, Darlison L, et al. British Thoracic Society Guideline for the investigation and management of malignant pleural mesothelioma. Thorax. 2018;73:i1–30.
pubmed: 29444986
doi: 10.1136/thoraxjnl-2017-211321
Corcoran JP, Acton L, Ahmed A, et al. Diagnostic value of radiological imaging pre- and post-drainage of pleural effusions. Respirology. 2016;21:392–5.
pubmed: 26545413
doi: 10.1111/resp.12675
Nguyen NC, Tran I, Hueser CN, et al. F-18 FDG PET/CT characterization of talc pleurodesis-induced pleural changes over time: a retrospective study. Clin Nucl Med. 2009;34:886–90.
pubmed: 20139823
doi: 10.1097/RLU.0b013e3181bece11
Kwek BH, Aquino SL, Fischman AJ. Fluorodeoxyglucose positron emission tomography and CT after talc pleurodesis. Chest. 2004;125:2356–60.
pubmed: 15189963
doi: 10.1378/chest.125.6.2356
Porcel JM, Hernandez P, Martinez-Alonso M, et al. Accuracy of fluorodeoxyglucose-PET imaging for differentiating benign from malignant pleural effusions: a meta-analysis. Chest. 2015;147:502–12.
pubmed: 25188411
doi: 10.1378/chest.14-0820
Fjaellegaard K, Koefod Petersen J, Reuter S, et al. Positron emission tomography-computed tomography (PET-CT) in suspected malignant pleural effusion. An updated systematic review and meta-analysis. Lung Cancer. 2021;162:106–18.
pubmed: 34775214
doi: 10.1016/j.lungcan.2021.10.018
De Fonseka D, Arnold DT, Smartt HJM, et al. PET-CT guided versus CT-guided biopsy in suspected malignant pleural thickening; a randomised trial. Eur Respir J. 2023. In press. https://doi.org/10.1183/13993003.01295-2023 .
Kaul V, McCracken DJ, Rahman NM, et al. Contemporary Approach to the diagnosis of malignant pleural effusion. Ann Am Thorac Soc. 2019;16:1099–106.
pubmed: 31216176
doi: 10.1513/AnnalsATS.201902-189CME
Porcel JM, Esquerda A, Vives M, et al. Etiology of pleural effusions: analysis of more than 3,000 consecutive thoracenteses. Arch Bronconeumol. 2014;50:161–5.
pubmed: 24360987
doi: 10.1016/j.arbres.2013.11.007
Arnold DT, De Fonseka D, Perry S, et al. Investigating unilateral pleural effusions: the role of cytology. Eur Respir J. 2018;52:1801254.
pubmed: 30262573
doi: 10.1183/13993003.01254-2018
Abouzgheib W, Bartter T, Dagher H, et al. A prospective study of the volume of pleural fluid required for accurate diagnosis of malignant pleural effusion. Chest. 2009;135:999–1001.
pubmed: 19017891
doi: 10.1378/chest.08-2002
Rooper LM, Ali SZ, Olson MT. A minimum fluid volume of 75 mL is needed to ensure adequacy in a pleural effusion: a retrospective analysis of 2540 cases. Cancer Cytopathol. 2014;122:657–65.
pubmed: 25060164
doi: 10.1002/cncy.21452
Porcel JM. Diagnosis and characterization of malignant effusions through pleural fluid cytological examination. Curr Opin Pulm Med. 2019;25:362–8.
pubmed: 31082996
doi: 10.1097/MCP.0000000000000593
Sorolla MA, Sorolla A, Parisi E, et al. Diving into the Pleural Fluid: Liquid Biopsy for metastatic malignant pleural effusions. Cancers (Basel). 2021;13:2798.
pubmed: 34199799
doi: 10.3390/cancers13112798
Porcel JM, Sorolla A, Parisi E, et al. Cell-free DNA concentration and pattern fragmentation in Pleural Fluid and plasma to detect malignant effusions. Ann Am Thorac Soc. 2022;19:854–6.
pubmed: 34813415
doi: 10.1513/AnnalsATS.202107-810RL
Rahman NM, Gleeson FV. Image-guided pleural biopsy. Curr Opin Pulm Med. 2008;14:331–6.
pubmed: 18520268
doi: 10.1097/MCP.0b013e3282fe9a04
Mei F, Bonifazi M, Rota M, et al. Diagnostic yield and safety of image-guided pleural biopsy: a systematic review and Meta-analysis. Respiration. 2021;100:77–87.
pubmed: 33373985
doi: 10.1159/000511626
Mychajlowycz M, Alabousi A, Mironov O. Ultrasound- versus CT-Guided Subpleural Lung and Pleural Biopsy: an analysis of wait Times, Procedure Time, Safety, and diagnostic adequacy. Can Assoc Radiol J. 2021;72:883–9.
pubmed: 32673070
doi: 10.1177/0846537120939073
Sconfienza LM, Mauri G, Grossi F, et al. Pleural and peripheral lung lesions: comparison of US- and CT-guided biopsy. Radiology. 2013;266:930–5.
pubmed: 23204543
doi: 10.1148/radiol.12112077
Rahman NM, Ali NJ, Brown G, et al. Local anaesthetic thoracoscopy: British thoracic Society Pleural Disease Guideline 2010. Thorax. 2010;65(Suppl 2):ii54–60.
pubmed: 20696694
doi: 10.1136/thx.2010.137018
Harris RJ, Kavuru MS, Mehta AC, et al. The impact of thoracoscopy on the management of pleural disease. Chest. 1995;107:845–52.
pubmed: 7874962
doi: 10.1378/chest.107.3.845
Boutin C, Rey F. Thoracoscopy in pleural malignant mesothelioma: a prospective study of 188 consecutive patients. Part 1: diagnosis. Cancer. 1993;72:389–93.
pubmed: 8319170
doi: 10.1002/1097-0142(19930715)72:2<389::AID-CNCR2820720213>3.0.CO;2-V
Dhooria S, Singh N, Aggarwal AN, et al. A randomized trial comparing the diagnostic yield of rigid and semirigid thoracoscopy in undiagnosed pleural effusions. Respir Care. 2014;59:756–64.
pubmed: 24106326
doi: 10.4187/respcare.02738
Chen CH, Cheng WC, Wu BR, et al. Feasibility and safety of Pleuroscopic Cryobiopsy of the Pleura: a prospective study. Can Respir J. 2018;2018:6746470.
pubmed: 29610630
pmcid: 5828474
doi: 10.1155/2018/6746470
Dhooria S, Bal A, Sehgal IS, et al. Pleural Cryobiopsy versus flexible forceps biopsy in subjects with undiagnosed Exudative Pleural effusions Undergoing Semirigid Thoracoscopy: a crossover randomized trial (COFFEE trial). Respiration. 2019;98:133–41.
pubmed: 31018210
doi: 10.1159/000497212
Shafiq M, Sethi J, Ali MS, et al. Pleural Cryobiopsy: a systematic review and Meta-analysis. Chest. 2020;157:223–30.
pubmed: 31610161
doi: 10.1016/j.chest.2019.09.023
Giri M, Dai H, Guo S, et al. Efficacy and Safety of Pleural Cryobiopsy vs. forceps biopsy for evaluation of undiagnosed Pleural Effusion: a systematic review and Meta-analysis. Front Med (Lausanne). 2022;9:847146.
pubmed: 35479946
doi: 10.3389/fmed.2022.847146
Koegelenberg CF, Diacon AH. Pleural controversy: close needle pleural biopsy or thoracoscopy-which first? Respirology. 2011;16:738–46.
pubmed: 21435098
doi: 10.1111/j.1440-1843.2011.01973.x
MacDuff A, Arnold A, Harvey J, et al. Management of spontaneous pneumothorax: British thoracic Society Pleural Disease Guideline 2010. Thorax. 2010;65(Suppl 2):ii18–31.
pubmed: 20696690
doi: 10.1136/thx.2010.136986
Rahman NM, Pepperell J, Rehal S, et al. Effect of opioids vs NSAIDs and larger vs smaller chest tube size on Pain Control and Pleurodesis Efficacy among patients with malignant pleural effusion: the TIME1 Randomized Clinical Trial. JAMA. 2015;314:2641–53.
pubmed: 26720026
doi: 10.1001/jama.2015.16840
Bhatnagar R, Piotrowska HEG, Laskawiec-Szkonter M, et al. Effect of Thoracoscopic Talc Poudrage vs talc slurry via Chest Tube on Pleurodesis failure rate among patients with malignant pleural effusions: a Randomized Clinical Trial. JAMA. 2020;323:60–9.
pubmed: 31804680
doi: 10.1001/jama.2019.19997
Davies HE, Mishra EK, Kahan BC, et al. Effect of an indwelling pleural catheter vs chest tube and talc pleurodesis for relieving dyspnea in patients with malignant pleural effusion: the TIME2 randomized controlled trial. JAMA. 2012;307:2383–9.
pubmed: 22610520
doi: 10.1001/jama.2012.5535
Thomas R, Fysh ETH, Smith NA, et al. Effect of an Indwelling Pleural Catheter vs Talc Pleurodesis on hospitalization days in patients with malignant pleural effusion: the AMPLE randomized clinical trial. JAMA. 2017;318:1903–12.
pubmed: 29164255
pmcid: 5820726
doi: 10.1001/jama.2017.17426
Wahidi MM, Reddy C, Yarmus L, et al. Randomized Trial of Pleural Fluid Drainage frequency in patients with malignant pleural effusions. The ASAP trial. Am J Respir Crit Care Med. 2017;195:1050–7.
pubmed: 27898215
doi: 10.1164/rccm.201607-1404OC
Muruganandan S, Azzopardi M, Fitzgerald DB, et al. Aggressive versus symptom-guided drainage of malignant pleural effusion via indwelling pleural catheters (AMPLE-2): an open-label randomised trial. Lancet Respir Med. 2018;6:671–80.
pubmed: 30037711
doi: 10.1016/S2213-2600(18)30288-1
Bhatnagar R, Kahan BC, Morley AJ, et al. The efficacy of indwelling pleural catheter placement versus placement plus talc sclerosant in patients with malignant pleural effusions managed exclusively as outpatients (IPC-PLUS): study protocol for a randomised controlled trial. Trials. 2015;16:48.
pubmed: 25880969
pmcid: 4333179
doi: 10.1186/s13063-015-0563-y
Fitzgerald DB, Sidhu C, Budgeon C, et al. Australasian Malignant PLeural Effusion (AMPLE)-3 trial: study protocol for a multi-centre randomised study comparing indwelling pleural catheter (+/-talc pleurodesis) versus video-assisted thoracoscopic surgery for management of malignant pleural effusion. Trials. 2022;23:530.
pubmed: 35761341
pmcid: 9235203
doi: 10.1186/s13063-022-06405-7
Dipper A, Jones HE, Bhatnagar R, et al. Interventions for the management of malignant pleural effusions: an updated network meta-analysis. Eur Respir Rev. 2021;30:210025.
pubmed: 33952602
pmcid: 9488663
doi: 10.1183/16000617.0025-2021
Dresler CM, Olak J, Herndon JE, et al. Phase III intergroup study of talc poudrage vs talc slurry sclerosis for malignant pleural effusion. Chest. 2005;127:909–15.
pubmed: 15764775
doi: 10.1378/chest.127.3.909
Rintoul RC. The MesoVATS trial: is there a future for video-assisted thoracoscopic surgery partial pleurectomy? Future Oncol. 2015;11:15–7.
pubmed: 26638917
doi: 10.2217/fon.15.274
Psallidas I, Hassan M, Yousuf A, et al. Role of thoracic ultrasonography in pleurodesis pathways for malignant pleural effusions (SIMPLE): an open-label, randomised controlled trial. Lancet Respir Med. 2022;10:139–48.
pubmed: 34634246
doi: 10.1016/S2213-2600(21)00353-2
Addala DN, Kanellakis NI, Bedawi EO, et al. Malignant pleural effusion: updates in diagnosis, management and current challenges. Front Oncol. 2022;12:1053574.
pubmed: 36465336
pmcid: 9712949
doi: 10.3389/fonc.2022.1053574
Mitchell MA, Deschner E, Dhaliwal I, et al. Patient perspectives on the use of indwelling pleural catheters in malignant pleural effusions. Thorax. 2023;78:1111–7.
pubmed: 37173137
doi: 10.1136/thorax-2022-219449
Peddle-McIntyre CJ, Muruganandan S, McVeigh J, et al. Device assessed activity behaviours in patients with indwelling pleural catheter: a sub-study of the Australasian Malignant PLeural Effusion (AMPLE)-2 randomized trial. Respirology. 2023;28:561–70.
pubmed: 36642702
doi: 10.1111/resp.14451
Shrager JB, Bhatnagar R, Kearney CT, et al. Silver nitrate-coated versus standard indwelling Pleural Catheter for malignant effusions: the SWIFT Randomized Trial. Ann Am Thorac Soc. 2022;19:1722–9.
pubmed: 35363591
doi: 10.1513/AnnalsATS.202111-1301OC
Mishra EK, Clive AO, Wills GH, et al. Randomized Controlled Trial of Urokinase versus Placebo for Nondraining Malignant Pleural Effusion. Am J Respir Crit Care Med. 2018;197:502–8.
pubmed: 28926296
doi: 10.1164/rccm.201704-0809OC
Addala DN, Rahman NM, Maldonado F. Personalized prognostication in malignant pleural effusion: the next step? Chest. 2021;160:805–6.
pubmed: 34488957
doi: 10.1016/j.chest.2021.04.042
Peel AM, Mishra EK. The Psychosocial Impact of Indwelling Pleural catheters: a scoping review. Cureus. 2023;15:e41689.
pubmed: 37575731
pmcid: 10413413
Molina S, Martinez-Zayas G, Sainz PV, et al. Breast and lung effusion survival score models: improving survival prediction in patients with malignant pleural effusion and metastasis. Chest. 2021;160:1075–94.
pubmed: 33852918
pmcid: 8449006
doi: 10.1016/j.chest.2021.03.059