Past, Present, and Future of Radiation-Induced Cardiotoxicity: Refinements in Targeting, Surveillance, and Risk Stratification

Carmen Bergom, Julie A Bradley, Andrea K Ng, Pamela Samson, Clifford Robinson, Juan Lopez-Mattei, Joshua D Mitchell, Carmen Bergom, Julie A Bradley, Andrea K Ng, Pamela Samson, Clifford Robinson, Juan Lopez-Mattei, Joshua D Mitchell

Abstract

Radiation therapy is an important component of cancer therapy for many malignancies. With improvements in cardiac-sparing techniques, radiation-induced cardiac dysfunction has decreased but remains a continued concern. In this review, we provide an overview of the evolution of radiotherapy techniques in thoracic cancers and associated reductions in cardiac risk. We also highlight data demonstrating that in some cases radiation doses to specific cardiac substructures correlate with cardiac toxicities and/or survival beyond mean heart dose alone. Advanced cardiac imaging, cardiovascular risk assessment, and potentially even biomarkers can help guide post-radiotherapy patient care. In addition, treatment of ventricular arrhythmias with the use of ablative radiotherapy may inform knowledge of radiation-induced cardiac dysfunction. Future efforts should explore further personalization of radiotherapy to minimize cardiac dysfunction by coupling knowledge derived from enhanced dosimetry to cardiac substructures, post-radiation regional dysfunction seen on advanced cardiac imaging, and more complete cardiac toxicity data.

Keywords: CAC, coronary artery calcium; CAD, coronary artery disease; CMRI, cardiac magnetic resonance imaging; CT, computed tomography; HL, Hodgkin lymphoma; LAD, left anterior descending artery; LV, left ventricular; MHD, mean heart dose; NSCLC, non–small cell lung cancer; RICD, radiation-induced cardiovascular disease; RT, radiation therapy; SBRT, stereotactic body radiation therapy; breast cancer; cancer survivorship; childhood cancer; esophageal cancer; imaging; lung cancer; lymphoma; radiation physics.

Conflict of interest statement

This work was supported by the National Institutes of Health (R01HL147884) and National Center for Advancing Translational Sciences of the National Institutes of Health (UL1TR002345). Dr Bergom has received research funding from the National Institutes of Health, Susan G. Komen Foundation, and Innovation Pathways. Dr Bradley has received an Ion Beam Application travel grant (April 2018) and funding from the Bankhead Coley Foundation and Ocala Royal Dames Foundation. Dr Ng has received funding from ViewRay. Dr Robinson has received research funding from the National Institutes of Health and the American Heart Association. Dr Mitchell has received research funding from Pfizer, Longer Life Foundation, and Children’s Discovery Institute and consultancy for Pfizer. All other authors have reported that they have no relationships relevant to the contents of this paper to disclose.

© 2021 Published by Elsevier on behalf of the American College of Cardiology Foundation.

Figures

Graphical abstract
Graphical abstract
Central Illustration
Central Illustration
Heart Regions Associated With Radiation-Induced Cardiovascular Disease and/or Survival First author and year of publication are listed. Highlighted colors indicate cancer type (see Key). Studies demonstrating associations between total heart doses and outcomes are not included. ∗Pericardium, not including the heart. LAD = left anterior descending artery; SVC = superior vena cava.
Figure 1
Figure 1
Evolution of RT in HL (A) Schematic representation of field design, radiation therapy (RT) doses, and radiation techniques for adult Hodgkin lymphoma (HL) as they have evolved over time. (B, C) RT plan comparison of an HL patient treated with involved-site RT to the mediastinum including colorwash dose distribution. Recreated historical mantle field (B), anterior-posterior technique, treated to a dose of 40 Gy, versus involved-site RT using IMRT (C), with deep-inspiration breath hold (note expansion of lungs and elongation of mediastinal structures, displacing lungs and heart away from target volume) with arms down on inclined board (further displacement of heart inferiorly), treated to 30 Gy with a 6-Gy boost to a level 5 node. (D) Dosimetric comparison of plans in B and C. IMRT = intensity-modulated radiation therapy; LAD = left anterior descending artery; LV = left ventricle; PET-CT = positron emission tomography–computed tomography.
Figure 2
Figure 2
Example Breast Plans Using Different RT Techniques and Modalities Example plans using cardiac-sparing techniques and different target volumes are shown. The selection of techniques and modalities is complex, involving availability of the technology, patient anatomy, and target volumes. All plans shown prescribed 50 Gy in 2-Gy fractions, except partial breast RT was prescribed 30 Gy in 5 fractions. 3DCRT = 3-dimensional conformal radiation therapy; DIBH = deep-inspiration breath hold; IMRT = intensity-modulated radiation therapy; MHD = mean heart dose; RT = radiation therapy; VMAT = volumetric-modulated arc therapy.
Figure 3
Figure 3
Comparison of Cardiovascular Imaging Modalities for Assessment of Radiation-Induced Cardiovascular Disease Major strengths and limitations of 4 major cardiovascular imaging modalities are shown. CAD = coronary artery disease; CMR = cardiac magnetic resonance imaging; echo = echocardiography; LVEF = left ventricular ejection fraction; SPECT = single-photon emission computed tomography.

References

    1. Delaney G., Jacob S., Featherstone C., Barton M. The role of radiotherapy in cancer treatment: estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer. 2005;104:1129–1137.
    1. Darby S.C., Ewertz M., McGale P. Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med. 2013;368:987–998.
    1. van den Bogaard V.A.B., Ta B.D.P., van der Schaaf A. Validation and modification of a prediction model for acute cardiac events in patients with breast cancer treated with radiotherapy based on three-dimensional dose distributions to cardiac substructures. J Clin Oncol. 2017;35:1171–1178.
    1. Taylor C., Correa C., Duane F.K. Estimating the risks of breast cancer radiotherapy: evidence from modern radiation doses to the lungs and heart and from previous randomized trials. J Clin Oncol. 2017;35:1641–1649.
    1. Wang K., Pearlstein K.A., Patchett N.D. Heart dosimetric analysis of three types of cardiac toxicity in patients treated on dose-escalation trials for stage III nonsmall-cell lung cancer. Radiother Oncol. 2017;125:293–300.
    1. Dess R.T., Sun Y., Matuszak M.M. Cardiac events after radiation therapy: combined analysis of prospective multicenter trials for locally advanced non–small-cell lung cancer. J Clin Oncol. 2017;35:1395–1402.
    1. Beukema J.C., van Luijk P., Widder J., Langendijk J.A., Muijs C.T. Is cardiac toxicity a relevant issue in the radiation treatment of esophageal cancer? Radiother Oncol. 2015;114:85–90.
    1. Atkins K.M., Rawal B., Chaunzwa T.L. Cardiac radiation dose, cardiac disease, and mortality in patients with lung cancer. J Am Coll Cardiol. 2019;73:2976–2987.
    1. McWilliam A., Kennedy J., Hodgson C., Vasquez Osorio E., Faivre-Finn C., van Herk M. Radiation dose to heart base linked with poorer survival in lung cancer patients. Eur J Cancer. 2017;85:106–113.
    1. Stam B., Peulen H., Guckenberger M. Dose to heart substructures is associated with noncancer death after SBRT in stage I-II NSCLC patients. Radiother Oncol. 2017;123:370–375.
    1. Takeuchi Y., Murakami Y., Kameoka T. Analysis of cardiac toxicity after definitive chemoradiotherapy for esophageal cancer using a biological dose-volume histogram. J Radiat Res. 2020;61:298–306.
    1. Tamari K., Isohashi F., Akino Y. Risk factors for pericardial effusion in patients with stage i esophageal cancer treated with chemoradiotherapy. Anticancer Res. 2014;34:7389–7393.
    1. Wei X., Liu H.H., Tucker S.L. Risk factors for pericardial effusion in inoperable esophageal cancer patients treated with definitive chemoradiation therapy. Int J Radiat Oncol Biol Phys. 2008;70:707–714.
    1. Girinsky T., M’Kacher R., Lessard N. Prospective coronary heart disease screening in asymptomatic Hodgkin lymphoma patients using coronary computed tomography angiography: results and risk factor analysis. Int J Radiat Oncol Biol Phys. 2014;89:59–66.
    1. Cutter D.J., Schaapveld M., Darby S.C. Risk of valvular heart disease after treatment for Hodgkin lymphoma. J Natl Cancer Inst. 2015;107
    1. Ma J.-T., Sun L., Sun X. Is pulmonary artery a dose-limiting organ at risk in nonsmall cell lung cancer patients treated with definitive radiotherapy? Radiat Oncol. 2017;12:34.
    1. Han C.-B., Wang W.-L., Quint L. Pulmonary artery invasion, high-dose radiation, and overall survival in patients with nonsmall cell lung cancer. Int J Radiat Oncol Biol Phys. 2014;89:313–321.
    1. Vivekanandan S., Landau D.B., Counsell N. The impact of cardiac radiation dosimetry on survival after radiation therapy for non-small cell lung cancer. Int J Radiat Oncol Biol Phys. 2017;99:51–60.
    1. Cella L., Liuzzi R., Conson M. Dosimetric predictors of asymptomatic heart valvular dysfunction following mediastinal irradiation for Hodgkin’s lymphoma. Radiother Oncol. 2011;101:316–321.
    1. Abouegylah M., Braunstein L.Z., Alm El-Din M.A. Evaluation of radiation-induced cardiac toxicity in breast cancer patients treated with trastuzumab-based chemotherapy. Breast Cancer Res Treat. 2019;174:179–185.
    1. Wennstig A.-K., Garmo H., Isacsson U. The relationship between radiation doses to coronary arteries and location of coronary stenosis requiring intervention in breast cancer survivors. Radiat Oncol. 2019;14:40.
    1. Yegya-Raman N., Wang K., Kim S. Dosimetric predictors of symptomatic cardiac events after conventional-dose chemoradiation therapy for inoperable NSCLC. J Thorac Oncol. 2018;13:1508–1518.
    1. Moignier A., Broggio D., Derreumaux S. Coronary stenosis risk analysis following Hodgkin lymphoma radiotherapy: a study based on patient specific artery segments dose calculation. Radiother Oncol. 2015;117:467–472.
    1. Mansouri I., Allodji R.S., Hill C. The role of irradiated heart and left ventricular volumes in heart failure occurrence after childhood cancer. Eur J Heart Fail. 2019;21:509–518.
    1. Cao L., Hu W.G., Kirova Y.M. Potential impact of cardiac dose-volume on acute cardiac toxicity following concurrent trastuzumab and radiotherapy. Cancer Radiother. 2014;18:119–124.
    1. de Ville de Goyet M., Brichard B., Robert A. Prospective cardiac MRI for the analysis of biventricular function in children undergoing cancer treatments. Pediatr Blood Cancer. 2015;62:867–874.
    1. Wong O.Y., Yau V., Kang J. Survival impact of cardiac dose following lung stereotactic body radiotherapy. Clin Lung Cancer. 2018;19:e241–e246.
    1. Atkins K.M., Chaunzwa T.L., Lamba N. Association of left anterior descending coronary artery radiation dose with major adverse cardiac events and mortality in patients with non–small cell lung cancer. JAMA Oncol. 2021;7:206–219.
    1. Cao L., Cai G., Chang C. Diastolic dysfunction occurs early in HER2-positive breast cancer patients treated concurrently with radiation therapy and trastuzumab. Oncologist. 2015;20:605–614.
    1. van der Ree M.H., Blanck O., Limpens J. Cardiac radioablation—a systematic review. Heart Rhythm. 2020;17:1381–1392.
    1. Haugnes H.S., Wethal T., Aass N. Cardiovascular risk factors and morbidity in long-term survivors of testicular cancer: a 20-year follow-up study. J Clin Oncol. 2010;28:4649–4657.
    1. Kaplan H.S. Evidence for a tumoricidal dose level in the radiotherapy of Hodgkin’s disease. Cancer Rese. 1966;26:5.
    1. Boivin J.-F., Hutchison G.B., Lubin J.H., Mauch P. Coronary artery disease mortality in patients treated for Hodgkin’s disease. Cancer. 1992;69:1241–1247.
    1. Hancock S.L., Tucker M.A., Hoppe R.T. Factors affecting late mortality from heart disease after treatment of Hodgkin’s disease. JAMA. 1993;270:1949–1955.
    1. Galper S.L., Yu J.B., Mauch P.M. Clinically significant cardiac disease in patients with Hodgkin lymphoma treated with mediastinal irradiation. Blood. 2011;117:412–418.
    1. van Nimwegen F.A., Schaapveld M., Janus C.P.M. Cardiovascular disease after Hodgkin lymphoma treatment: 40-year disease risk. JAMA Intern Med. 2015;175:1007–1017.
    1. Schellong G., Riepenhausen M., Bruch C. Late valvular and other cardiac diseases after different doses of mediastinal radiotherapy for Hodgkin disease in children and adolescents: report from the longitudinal GPOH follow-up project of the German-Austrian DAL-HD studies. Pediatr Blood Cancer. 2010;55:1145–1152.
    1. Mulrooney D.A., Yeazel M.W., Kawashima T. Cardiac outcomes in a cohort of adult survivors of childhood and adolescent cancer: retrospective analysis of the Childhood Cancer Survivor Study cohort. BMJ. 2009;339:b4606.
    1. Bhakta N., Liu Q., Yeo F. Cumulative burden of cardiovascular morbidity in paediatric, adolescent, and young adult survivors of Hodgkin’s lymphoma: an analysis from the St Jude Lifetime Cohort Study. Lancet Oncol. 2016;17:1325–1334.
    1. Maraldo M.V., Giusti F., Vogelius I.R. Cardiovascular disease after treatment for Hodgkin’s lymphoma: an analysis of nine collaborative EORTC-LYSA trials. Lancet Haematol. 2015;2:e492–e502.
    1. van Nimwegen F.A., Schaapveld M., Cutter D.J. Radiation dose-response relationship for risk of coronary heart disease in survivors of Hodgkin lymphoma. J Clin Oncol. 2016;34:235–243.
    1. van Nimwegen F.A., Ntentas G., Darby S.C. Risk of heart failure in survivors of Hodgkin lymphoma: effects of cardiac exposure to radiation and anthracyclines. Blood. 2017;129:2257–2265.
    1. Specht L., Yahalom J., Illidge T. Modern radiation therapy for Hodgkin lymphoma: field and dose guidelines from the International Lymphoma Radiation Oncology Group (ILROG) Int J Radiat Oncol Biol Phys. 2014;89:854–862.
    1. Wirth A., Mikhaeel N.G., Aleman B.M.P. Involved site radiation therapy in adult lymphomas: an overview of International Lymphoma Radiation Oncology Group guidelines. Int J Radiat Oncol Biol Phys. 2020;107:909–933.
    1. Bortfeld T., Jeraj R. The physical basis and future of radiation therapy. Br J Radiol. 2011;84:485–498.
    1. Campbell B.A., Voss N., Pickles T. Involved-nodal radiation therapy as a component of combination therapy for limited-stage Hodgkin’s lymphoma: a question of field size. J Clin Oncol. 2008;26:5170–5174.
    1. Koeck J., Abo-Madyan Y., Lohr F. Radiotherapy for early mediastinal Hodgkin lymphoma according to the German Hodgkin Study Group (GHSG): the roles of intensity-modulated radiotherapy and involved-node radiotherapy. Int J Radiat Oncol. Biol Phys. 2012;83:268–276.
    1. Maraldo M.V., Brodin N.P., Vogelius I.R. Risk of developing cardiovascular disease after involved node radiotherapy versus mantle field for Hodgkin lymphoma. Int J Radiat Oncol Biol Phys. 2012;83:1232–1237.
    1. Voong K.R., McSpadden K., Pinnix C.C. Dosimetric advantages of a “butterfly” technique for intensity-modulated radiation therapy for young female patients with mediastinal Hodgkin’s lymphoma. Radiat Oncol. 2014;9:94.
    1. Mulrooney D.A., Hyun G., Ness K.K. Major cardiac events for adult survivors of childhood cancer diagnosed between 1970 and 1999: report from the Childhood Cancer Survivor Study cohort. BMJ. 2020;368:l6794.
    1. Bates J.E., Howell R.M., Liu Q. Therapy-related cardiac risk in childhood cancer survivors: an analysis of the Childhood Cancer Survivor Study. J Clin Oncol. 2019;37:1090–1101.
    1. van der Pal H.J., van Dalen E.C., van Delden E. High risk of symptomatic cardiac events in childhood cancer survivors. J Clin Oncol. 2012;30:1429–1437.
    1. Feijen E.A.M., van Dalen E.C., van der Pal H.J.H. Increased risk of cardiac ischaemia in a pan-European cohort of 36 205 childhood cancer survivors: a PanCareSurFup study. Heart. 2021;107:33–40.
    1. Lipshultz S.E., Adams M.J., Colan S.D. Long-term cardiovascular toxicity in children, adolescents, and young adults who receive cancer therapy: pathophysiology, course, monitoring, management, prevention, and research directions: A scientific statement from the American Heart Association. Circulation. 2013;128:1927–1995.
    1. Shankar S.M., Marina N., Hudson M.M. Monitoring for cardiovascular disease in survivors of childhood cancer: report from the Cardiovascular Disease Task Force of the Children’s Oncology Group. Pediatrics. 2008;121:e387–e396.
    1. Armenian S.H., Hudson M.M., Mulder R.L. Recommendations for cardiomyopathy surveillance for survivors of childhood cancer: a report from the International Late Effects of Childhood Cancer Guideline Harmonization Group. Lancet Oncol. 2015;16:e123–e136.
    1. Clarke M., Collins R., Darby S. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;366:2087–2106.
    1. Boekel N.B., Schaapveld M., Gietema J.A. Cardiovascular disease risk in a large, population-based cohort of breast cancer survivors. Int J Radiat Oncol Biol Phys. 2016;94:1061–1072.
    1. Vicini F.A., Cecchini R.S., White J.R. Long-term primary results of accelerated partial breast irradiation after breast-conserving surgery for early-stage breast cancer: a randomised, phase 3, equivalence trial. Lancet. 2019;394:2155–2164.
    1. NRG Oncology RTOG 1005: a phase III trial of accelerated whole breast irradiation with hypofractionation plus concurrent boost versus standard whole breast irradiation plus sequential boost for early-stage breast cancer. Accessed January 25, 2021.
    1. Gee H.E., Moses L., Stuart K. Contouring consensus guidelines in breast cancer radiotherapy: comparison and systematic review of patterns of failure. J Med Imaging. Radiat Oncol. 2019;63:102–115.
    1. Bradley J.A., Mendenhall N.P. Novel radiotherapy techniques for breast cancer. Annu Rev Med. 2018;69:277–288.
    1. Jacobse J.N., Duane F.K., Boekel N.B. Radiation dose-response for risk of myocardial infarction in breast cancer survivors. Int J Radiat Oncol Biol Phys. 2019;103:595–604.
    1. Duane F.K., McGale P., Brønnum D. Cardiac structure doses in women irradiated for breast cancer in the past and their use in epidemiological studies. Pract Radiat Oncol. 2019;9:158–171.
    1. Piroth M.D., Baumann R., Budach W. Heart toxicity from breast cancer radiotherapy: current findings, assessment, and prevention. Strahlenther Onkol. 2019;195:1–12.
    1. Witt J.S., Jagodinsky J.C., Liu Y. Cardiac toxicity in operable esophageal cancer patients treated with or without chemoradiation. Am J Clin Oncol. 2019;42:662–667.
    1. Chun S.G., Hu C., Choy H. Impact of intensity-modulated radiation therapy technique for locally advanced non–small-cell lung cancer: a secondary analysis of the NRG Oncology RTOG 0617 randomized clinical trial. J Clin Oncol. 2017;35:56–62.
    1. Morota M., Gomi K., Kozuka T. Late toxicity after definitive concurrent chemoradiotherapy for thoracic esophageal carcinoma. Int J Radiat Oncol Biol Phys. 2009;75:122–128.
    1. Niska J.R., Thorpe C.S., Allen S.M. Radiation and the heart: systematic review of dosimetry and cardiac end points. Expert Rev Cardiovasc Ther. 2018;16:931–950.
    1. Polk A., Vaage-Nilsen M., Vistisen K., Nielsen D.L. Cardiotoxicity in cancer patients treated with 5-fluorouracil or capecitabine: a systematic review of incidence, manifestations and predisposing factors. Cancer Treat Rev. 2013;39:974–984.
    1. Bradley J.D., Paulus R., Komaki R. Standard-dose versus high-dose conformal radiotherapy with concurrent and consolidation carboplatin plus paclitaxel with or without cetuximab for patients with stage IIIA or IIIB nonsmall-cell lung cancer (RTOG 0617): a randomised, two-by-two factorial phase 3 study. Lancet Oncol. 2015;16:187–199.
    1. Wang K., Eblan M.J., Deal A.M. Cardiac toxicity after radiotherapy for stage III non–small-cell lung cancer: pooled analysis of dose-escalation trials delivering 70 to 90 Gy. J Clin Oncol. 2017;35:1387–1394.
    1. Reshko L.B., Kalman N.S., Hugo G.D., Weiss E. Cardiac radiation dose distribution, cardiac events and mortality in early-stage lung cancer treated with stereotactic body radiation therapy (SBRT) J Thorac Dis. 2018;10:2346–2356.
    1. Mulrooney D.A., Armstrong G.T., Huang S. Cardiac outcomes in adult survivors of childhood cancer exposed to cardiotoxic therapy: a cross-sectional study from the St. Jude Lifetime Cohort. Ann Intern Med. 2016;164:93–101.
    1. Hooning M.J., Botma A., Aleman B.M.P. Long-term risk of cardiovascular disease in 10-year survivors of breast cancer. J Natl Cancer Inst. 2007;99:365–375.
    1. Wethal T., Nedregaard B., Andersen R. Atherosclerotic lesions in lymphoma survivors treated with radiotherapy. Radiother Oncol. 2014;110:448–454.
    1. Armstrong G.T., Oeffinger K.C., Chen Y. Modifiable risk factors and major cardiac events among adult survivors of childhood cancer. J Clin Oncol. 2013;31:3673–3680.
    1. Yeboah J., McClelland R.L., Polonsky T.S. Comparison of novel risk markers for improvement in cardiovascular risk assessment in intermediate-risk individuals. JAMA. 2012;308:788.
    1. Roos C.T.G., van den Bogaard V.A.B., Greuter M.J.W. Is the coronary artery calcium score associated with acute coronary events in breast cancer patients treated with radiotherapy? Radiother Oncol. 2018;126:170–176.
    1. Xie X., Zhao Y., de Bock G.H. Validation and prognosis of coronary artery calcium scoring in nontriggered thoracic computed tomography: systematic review and meta-analysis. Circ Cardiovasc Imaging. 2013;6:514–521.
    1. Lancellotti P., Nkomo V.T., Badano L.P. Expert consensus for multi-modality imaging evaluation of cardiovascular complications of radiotherapy in adults: a report from the European Association of Cardiovascular Imaging and the American Society of Echocardiography. Eur Heart J Cardiovasc Imaging. 2013;14:721–740.
    1. Armenian S.H., Lacchetti C., Barac A. Prevention and monitoring of cardiac dysfunction in survivors of adult cancers: American Society of Clinical Oncology clinical practice guideline. J Clin Oncol. 2017;35:893–911.
    1. Curigliano G., Lenihan D., Fradley M. Management of cardiac disease in cancer patients throughout oncological treatment: ESMO consensus recommendations. Ann Oncol. 2020;31:171–190.
    1. Mitchell J.D., Cehic D.A., Morgia M. Cardiovascular manifestations from therapeutic radiation: a multidisciplinary expert consensus statement from the international cardio-oncology society. J Am Coll Cardiol CardioOnc. 2021;3:360–380.
    1. Children’s Oncology Group Long-term follow-up guidelines for survivors of childhood, adolescent and young adult cancers. Version 5.0, October 2018. Accessed June 2, 2021.
    1. Ganatra Sarju, Chatur Safia, Nohria Anju. How to diagnose and manage radiation cardiotoxicity. J Am Coll Cardiol CardioOnc. 2020;2:655–660.
    1. Donnellan E., Masri A., Johnston D.R. Long-term outcomes of patients with mediastinal radiation-associated severe aortic stenosis and subsequent surgical aortic valve replacement: a matched cohort study. J Am Heart Assoc. 2017;6
    1. Dolmaci O.B., Farag E.S., Boekholdt S.M., van Boven W.J.P., Kaya A. Outcomes of cardiac surgery after mediastinal radiation therapy: a single-center experience. J Card Surg. 2020;35:612–619.
    1. Whelan T.J., Olivotto I.A., Parulekar W.R. Regional nodal irradiation in early-stage breast cancer. N Engl J Med. 2015;373:307–316.
    1. Saiki H., Petersen I.A., Scott C.G. Risk of heart failure with preserved ejection fraction in older women after contemporary radiotherapy for breast cancer. Circulation. 2017;135:1388–1396.
    1. Heidenreich P.A., Schnittger I., Strauss H.W. Screening for coronary artery disease after mediastinal irradiation for Hodgkin’s disease. J Clin Oncol. 2007;25:43–49.
    1. Tuohinen S.S., Skyttä T., Virtanen V. Detection of radiotherapy-induced myocardial changes by ultrasound tissue characterisation in patients with breast cancer. Int J Cardiovasc Imaging. 2016;32:767–776.
    1. Tuohinen S.S., Skyttä T., Virtanen V., Luukkaala T., Kellokumpu-Lehtinen P.-L., Raatikainen P. Early effects of adjuvant breast cancer radiotherapy on right ventricular systolic and diastolic function. Anticancer Res. 2015;35:2141–2147.
    1. Trivedi S.J., Choudhary P., Lo Q. Persistent reduction in global longitudinal strain in the longer term after radiation therapy in patients with breast cancer. Radiother Oncol. 2019;132:148–154.
    1. Chirakarnjanakorn S., Popović Z.B., Wu W. Impact of long-axis function on cardiac surgical outcomes in patients with radiation-associated heart disease. J Thorac Cardiovasc Surg. 2015;149:1643–1651.e2.
    1. Walker V., Lairez O., Fondard O. Early detection of subclinical left ventricular dysfunction after breast cancer radiation therapy using speckle-tracking echocardiography: association between cardiac exposure and longitudinal strain reduction (BACCARAT study) Radiat Oncol. 2019;14:204.
    1. Desai M.Y., Wu W., Masri A. Increased aorto-mitral curtain thickness independently predicts mortality in patients with radiation-associated cardiac disease undergoing cardiac surgery. Ann Thorac Surg. 2014;97:1348–1355.
    1. Armstrong G.T., Plana J.C., Zhang N. Screening adult survivors of childhood cancer for cardiomyopathy: comparison of echocardiography and cardiac magnetic resonance imaging. J Clin Oncol. 2012;30:2876–2884.
    1. Kim R.J., Wu E., Rafael A. The use of contrast-enhanced magnetic resonance imaging to identify reversible myocardial dysfunction. N Engl J Med. 2000;343:1445–1453.
    1. Haaf P., Garg P., Messroghli D.R., Broadbent D.A., Greenwood J.P., Plein S. Cardiac T1 mapping and extracellular volume (ECV) in clinical practice: a comprehensive review. J Cardiovasc Magn Reason. 2016;18:89.
    1. Lopez-Mattei J.C., Shah D.J. The role of cardiac magnetic resonance in valvular heart disease. Methodist DeBakey Cardiovasc J. 2013;9:142–148.
    1. Ariyarajah V., Jassal D.S., Kirkpatrick I., Kwong R.Y. The utility of cardiovascular magnetic resonance in constrictive pericardial disease. Cardiol Rev. 2009;17:77–82.
    1. Veinot J.P., Edwards W.D. Pathology of radiation-induced heart disease: a surgical and autopsy study of 27 cases. Hum Pathol. 1996;27:766–773.
    1. Gould K.L., Johnson N.P., Bateman T.M. Anatomic versus physiologic assessment of coronary artery disease. Role of coronary flow reserve, fractional flow reserve, and positron emission tomography imaging in revascularization decision-making. J Am Coll Cardiol. 2013;62:1639–1653.
    1. Hardenbergh P.H., Munley M.T., Bentel G.C. Cardiac perfusion changes in patients treated for breast cancer with radiation therapy and doxorubicin: preliminary results. Int J Radiat Oncol Biol Phy.s. 2001;49:1023–1028.
    1. Prosnitz R.G., Hubbs J.L., Evans E.S. Prospective assessment of radiotherapy-associated cardiac toxicity in breast cancer patients: analysis of data 3 to 6 years after treatment. Cancer. 2007;110:1840–1850.
    1. Gayed I.W., Liu H.H., Yusuf S.W. The prevalence of myocardial ischemia after concurrent chemoradiation therapy as detected by gated myocardial perfusion imaging in patients with esophageal cancer. J Nucl Med. 2006;47:1756–1762.
    1. Gayed I., Gohar S., Liao Z., McAleer M., Bassett R., Yusuf S.W. The clinical implications of myocardial perfusion abnormalities in patients with esophageal or lung cancer after chemoradiation therapy. Int J Cardiovasc Imaging. 2009;25:487–495.
    1. Layoun M.E., Yang E.H., Herrmann J. Applications of cardiac computed tomography in the cardio-oncology population. Curr Treat Options Oncol. 2019;20:47.
    1. Milgrom S.A., Varghese B., Gladish G.W. Coronary artery dose-volume parameters predict risk of calcification after radiation therapy. J. Cardiovasc. Imaging. 2019;27:268–279.
    1. Yakupovich A., Davison M.A., Kharouta M.Z. Heart dose and coronary artery calcification in patients receiving thoracic irradiation for lung cancer. J Thorac Dis. 2020;12:223–231.
    1. Tomizawa N. Could coronary calcification identified at nongated chest CT be a predictor for cardiovascular events in breast cancer patients? Int J Cardiol. 2019;282:108–109.
    1. Mitchell J.D., Fergestrom N., Gage B.F. Impact of statins on cardiovascular outcomes following coronary artery calcium scoring. J Am Coll Cardiol. 2018;72:3233–3242.
    1. Cuddy S., Payne D.L., Murphy D.J. Incidental coronary artery calcification in cancer imaging. J Am Coll Cardiol CardioOnc. 2019;1:135–137.
    1. Phillips W.J., Johnson C., Law A. Reporting of coronary artery calcification on chest CT studies in breast cancer patients at high risk of cancer therapy related cardiac events. Int J Cardiol Heart Vasc. 2018;18:12–16.
    1. Gernaat S.A.M., Išgum I., de Vos B.D. Automatic coronary artery calcium scoring on radiotherapy planning CT scans of breast cancer patients: reproducibility and association with traditional cardiovascular risk factors. PLoS One. 2016;11
    1. Mast M.E., Heijenbrok M.W., Petoukhova A.L., Scholten A.N., Schreur J.H.M., Struikmans H. Preradiotherapy calcium scores of the coronary arteries in a cohort of women with early-stage breast cancer: a comparison with a cohort of healthy women. Int J Radiat Oncol Biol Phy.s. 2012;83:853–858.
    1. Demissei B.G., Freedman G., Feigenberg S.J. Early changes in cardiovascular biomarkers with contemporary thoracic radiation therapy for breast cancer, lung cancer, and lymphoma. Int J Radiat Oncol Biol Phys. 2019;103:851–860.
    1. Chalubinska-Fendler J., Graczyk L., Piotrowski G. Lipopolysaccharide-binding protein is an early biomarker of cardiac function after radiation therapy for breast cancer. Int J Radiat Oncol Biol Phys. 2019;104:1074–1083.
    1. Dixon S.B., Howell C.R., Lu L. Cardiac biomarkers and association with subsequent cardiomyopathy and mortality among adult survivors of childhood cancer: a report from the St. Jude Lifetime Cohort. Cancer. 2021;127:458–466.
    1. Zei P.C., Wong D., Gardner E., Fogarty T., Maguire P. Safety and efficacy of stereotactic radioablation targeting pulmonary vein tissues in an experimental model. Heart Rhythm. 2018;15:1420–1427.
    1. Lehmann H.I., Deisher A.J., Takami M. External arrhythmia ablation using photon beams: ablation of the atrioventricular junction in an intact animal model. Circ Arrhythm Electrophysiol. 2017;10
    1. Robinson C.G., Samson P.P., Moore K.M.S. Phase I/II trial of electrophysiology-guided noninvasive cardiac radioablation for ventricular tachycardia. Circulation. 2019;139:313–321.
    1. Hall D., Robinson C., Cuculich P.S. Cardiac function after noninvasive radioablation [abstract] Heart Rhythm Society Annual Meeting. 2019

Source: PubMed

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