Evaluation of Radiation-induced Pleural Effusions after Radiotherapy to Support Development of Animal Models of Radiation Pneumonitis.
Journal
Health physics
ISSN: 1538-5159
Titre abrégé: Health Phys
Pays: United States
ID NLM: 2985093R
Informations de publication
Date de publication:
01 10 2021
01 10 2021
Historique:
entrez:
21
9
2021
pubmed:
22
9
2021
medline:
15
3
2022
Statut:
ppublish
Résumé
Not all animal models develop radiation-induced pleural effusions (RIPEs) as a form of radiation-induced lung injury (RILI). Such effusions are also not well characterized in humans. The purpose of this study is to identify occurrences of RIPE in humans, provide justification for development of relevant animal models, and further characterize its risk factors in cancer patients. We also aim to identify dose thresholds for cardiopulmonary toxicity in humans to shed light on possible pathogenic mechanisms for RIPEs. We carried out a retrospective review of medical records of 96 cancer patients receiving thoracic irradiation (TRT) at our institution. Fifty-three (53%) patients developed a new pleural effusion post TRT; 18 (19%) had RIPE; and 67% developed RIPE ipsilateral to the site irradiated. None developed "contralateral only" effusions. Median time to development was 6 mo (IQR; 4-8 mo). Of 18, 8 patients (44%) had concomitant asymptomatic (radiographic only) or symptomatic radiation pneumonitis and pericardial effusion. Dosimetric factors, including combined and ipsilateral mean lung dose (MLD), were significantly associated with increased risk of RIPE. Angiotensin converting enzyme inhibition, steroids, or concurrent chemotherapy did not modify incidence of RIPE. Our results substantiate the occurrence and incidence of RIPEs in humans. In cancer patients, a median time to development of effusions around 6 mo also supports the onset of RIPEs concurrent with radiation pneumonitis. Future work needs to include large populations of cancer survivors in whom delayed RIPEs can be tracked and correlated with cardiovascular changes in the context of injury to multiple organs.
Identifiants
pubmed: 34546223
doi: 10.1097/HP.0000000000001462
pii: 00004032-202110000-00012
pmc: PMC8500166
mid: NIHMS1738533
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
434-443Subventions
Organisme : BLRD VA
ID : I01 BX003833
Pays : United States
Organisme : NIAID NIH HHS
ID : U01 AI107305
Pays : United States
Organisme : NIAID NIH HHS
ID : U01 AI133594
Pays : United States
Informations de copyright
Copyright © 2021 Health Physics Society.
Déclaration de conflit d'intérêts
The authors declare no conflicts of interest.
Références
American Thoracic Society (ATS) Guideline. Management of malignant pleural effusions. Am J Respir Crit Care Med 162:1987–2001; 2000.
Bachman AL, Macken K. Pleural effusions following supervoltage radiation for breast carcinoma. Radiol 72:699–709; 1959.
Borkenhagen JF, Bergom C, Rapp CT, Klawikowski SJ, Rein LE, Gore EM. Dosimetric Predictors of Cardiotoxicity in Thoracic Radiotherapy for Lung Cancer. Clin Lung Cancer. 20(6):435–441; 2019.
Deas SD, Huprikar N, Skabelund A. Radiation exposure and lung disease in today's nuclear world. Curr Opin Pulm Med 23:167–172; 2017.
Fukada J, Shigematsu N, Ohashi T, Shiraishi Y, Takeuchi H, Kawaguchi O, Kitagawa Y. Pericardial and pleural effusions after definitive radiotherapy for esophageal cancer. J Radiat Res 53:447–453; 2012.
Garofalo M, Bennett A, Farese AM, Harper J, Ward A, Taylor-Howell C, Cui W, Gibbs A, Lasio G, Jackson W, MacVittie TJ. The delayed pulmonary syndrome following acute high-dose irradiation: a rhesus macaque model. Health Phys 106:56–72; 2014.
Ghobadi G, Bartelds B, van der Veen SJ, Dickinson MG, Brandenburg S, Berger RM, Langendijk JA, Coppes RP, van Luijk P. Lung irradiation induces pulmonary vascular remodelling resembling pulmonary arterial hypertension. Thorax 67:334–341; 2012a.
Ghobadi G, van der Veen S, Bartelds B, de Boer RA, Dickinson MG, de Jong JR, Faber H, Niemantsverdriet M, Brandenburg S, Berger RM, Langendijk JA, Coppes RP, van Luijk P. Physiological interaction of heart and lung in thoracic irradiation. Int J Radiat Oncol Biol Phys 84:e639–646; 2012b.
Ghosh SN, Wu Q, Mader M, Fish BL, Moulder JE, Jacobs ER, Medhora M, Molthen RC. Vascular injury after whole thoracic x-ray irradiation in the rat. Int J Radiat Oncol Biol Phys 74:192–199; 2009.
Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, Postmus PE, Rusch V, Sobin L. (International Association for the Study of Lung Cancer International Staging Committee Participating Institutions). The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM classification of malignant tumours. J Thorac Oncol 2:706–714; 2007.
Graham MV, Purdy JA, Emami B, Harms W, Bosch W, Lockett MA, Perez CA. Clinical dose-volume histogram analysis for pneumonitis after 3D treatment for non-small cell lung cancer (NSCLC). Int J Radiat Oncol Biol Phys 45:323–329; 1999.
Jackson IL, Vujaskovic Z, Down JD. Revisiting strain-related differences in radiation sensitivity of the mouse lung: recognizing and avoiding the confounding effects of pleural effusions. Radiat Res 173:10–20; 2010.
Jackson IL, Vujaskovic Z, Down JD. A further comparison of pathologies after thoracic irradiation among different mouse strains: finding the best preclinical model for evaluating therapies directed against radiation-induced lung damage. Radiat Res 175:510–518; 2011.
Jacobs ER, Narayanan J, Fish BL, Gao F, Harmann LM, Bergom C, Gasperetti T, Strande JL, Medhora M. Cardiac remodeling and reversible pulmonary hypertension during pneumonitis in rats after 13-Gy partial-body irradiation with minimal bone marrow sparing: effect of lisinopril. Health Phys 116:558–565; 2019.
MacVittie TJ, Farese AM. Defining the concomitant multiple organ injury within the ARS and DEARE in an animal model research platform. Health Phys 119:519–526; 2020.
Medhora M, Gao F, Fish BL, Jacobs ER, Moulder JE, Szabo A. Dose-modifying factor for captopril for mitigation of radiation injury to normal lung. J Radiat Res 53:633–640; 2012.
Medhora M, Gao F, Glisch C, Narayanan J, Sharma A, Harmann LM, Lawlor MW, Snyder LA, Fish BL, Down JD, Moulder JE, Strande JL, Jacobs ER. Whole-thorax irradiation induces hypoxic respiratory failure, pleural effusions and cardiac remodeling. J Radiat Res 56:248–260; 2015.
Medhora M, Gao F, Gasperetti T, Narayanan J, Khan AH, Jacobs ER, Fish BL. Delayed effects of acute radiation exposure (DEARE) in juvenile and old rats: mitigation by lisinopril. Health Phys 116:529–545; 2019.
Morrone N, Gama e Silva Volpe VL, Dourado AM, Mitre F, Coletta EN. Bilateral pleural effusion due to mediastinal fibrosis induced by radiotherapy. Chest 104:1276–1278; 1993.
Moy MP, Levsky JM, Berko NS, Godelman A, Jain VR, Haramati LB. A new, simple method for estimating pleural effusion size on CT scans. Chest 143:1054–1059; 2013.
Rabender C, Mezzaroma E, Mauro AG, Mullangi R, Abbate A, Anscher M, Hart B, Mikkelsen R. IPW-5371 proves effective as a radiation countermeasure by mitigating radiation-induced late effects. Radiat Res 186:478–488; 2016.
Rodriguez-Garcia JL, Fraile G, Moreno MA, Sánchez-Corral JA, Penalver R. Recurrent massive pleural effusion as a late complication of radiotherapy in Hodgkin's disease. Chest 100:1165–1166; 1991.
Simone CB. Thoracic radiation normal tissue injury. Semin Radiat Oncol 27:370–377; 2017.
US Department of Health and Human Services, National Institutes of Health, National Cancer Institute. Common terminology criteria for adverse events (CTCAE Version 5.0) Washington, DC: US Government Printing Office; 2017. Available at https://ctep.cancer.gov/protocoldevelopment/electronic_applications/ctc.htm ). Accessed 24 July 2021.
van der Veen SJ, Ghobadi G, de Boer RA, Faber H, Cannon MV, Nagle PW, Brandenburg S, Langendijk JA, van Luijk P, Coppes RP. ACE inhibition attenuates radiation-induced cardiopulmonary damage. Radiother Oncol 114:96–103; 2015.
Van Dyk J, Keane TJ, Kan S, Rider WD, Fryer CJ. Radiation pneumonitis following large single dose irradiation: a re-evaluation based on absolute dose to lung. Int J Radiat Oncol Biol Phys 7:461–467; 1981.
Whitcomb ME, Schwarz MI. Pleural effusion complicating intensive mediastinal radiation therapy. Am Rev Respir Dis 103:100–107; 1971.
Zhang XJ, Sun JG, Sun J, Ming H, Wang XX, Wu L, Chen ZT. Prediction of radiation pneumonitis in lung cancer patients: a systematic review. J Cancer Res Clinical Oncol 138:2103–2116; 2012.
Zhao J, Day RM, Jin JY, Quint L, Williams H, Ferguson C, Yan L, King M, Albsheer A, Matuszak M, Kong FS. Thoracic radiation-induced pleural effusion and risk factors in patients with lung cancer. Oncotarget 8:97623–97632; 2017.