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Applying global longitudinal strain in assessing cardiac dysfunction after radiotherapy among breast cancer patients: a systemic review and meta-analysis

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Abstract

Purpose

Radiation-induced heart disease (RIHD) has cost severe health burden to breast cancer patients. However, early thoracic radiotherapy (RT)-induced cardiac damage was hard to detect through traditional echocardiography. Therefore, we conducted this systemic review and meta-analysis to evaluate the changes of GLS, an innovative echocardiographic measurement, after thoracic radiotherapy.

Methods

We searched PubMed, Embase and Web of Science using the key words “breast cancer”, “radiotherapy” and “GLS” for relevant papers. Studies covered the difference of GLS change before and after radiotherapy were included, and the standard mean difference (SMD) and its standard error were extracted and pooled using a random-effects or fixed-effects model.

Results

A total of 11 studies comprising 18 comparisons were identified, and 1808 patients were involved. The pooled SMD of GLS before and within 6-week after radiotherapy was 0.48 (95% CI 0.34–0.61, p < 0.01), and the pooled long-term changes in GLS (over 6-month after radiotherapy) was 0.46 (95% CI 0.20–0.72, p < 0.01). No obvious publication bias were observed.

Conclusion

Breast cancer patients are facing greater risk of RIHD since they presented a better survival rate and longer life expectancy with the popularization of radiotherapy. GLS might be useful in capturing minimal cardiac changes shortly after radiotherapy or during long-term follow up visit.

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References

  1. Wei T, Cheng Y (2021) The cardiac toxicity of radiotherapy - a review of characteristics, mechanisms, diagnosis, and prevention. Int J Radiat Biol 97:1333–1340

    Article  CAS  PubMed  Google Scholar 

  2. Armenian SH, Lacchetti C, Lenihan D (2017) Prevention and monitoring of cardiac dysfunction in survivors of adult cancers: American Society of Clinical Oncology Clinical Practice Guideline Summary. J Oncol Pract 13:270–275

    Article  PubMed  Google Scholar 

  3. Weberpals J, Jansen L, Müller OJ, Brenner H (2018) Long-term heart-specific mortality among 347 476 breast cancer patients treated with radiotherapy or chemotherapy: a registry-based cohort study. Eur Heart J 39:3896–3903

    Article  CAS  PubMed  Google Scholar 

  4. Bouillon K, Haddy N, Delaloge S, Garbay JR, Garsi JP, Brindel P et al (2011) Long-term cardiovascular mortality after radiotherapy for breast cancer. J Am Coll Cardiol 57:445–452

    Article  PubMed  Google Scholar 

  5. Sardar P, Kundu A, Chatterjee S, Nohria A, Nairooz R, Bangalore S et al (2017) Long-term cardiovascular mortality after radiotherapy for breast cancer: a systematic review and meta-analysis. Clin Cardiol 40:73–81

    Article  PubMed  Google Scholar 

  6. Zhang C, Shi D, Yang P (2019) BNP as a potential biomarker for cardiac damage of breast cancer after radiotherapy: a meta-analysis. Medicine 98:e16507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. D’Errico MP, Petruzzelli MF, Gianicolo EA, Grimaldi L, Loliva F, Tramacere F et al (2015) Kinetics of B-type natriuretic peptide plasma levels in patients with left-sided breast cancer treated with radiation therapy: results after one-year follow-up. Int J Radiat Biol 91:804–809

    Article  CAS  PubMed  Google Scholar 

  8. Skyttä T, Tuohinen S, Boman E, Virtanen V, Raatikainen P, Kellokumpu-Lehtinen PL (2015) Troponin T-release associates with cardiac radiation doses during adjuvant left-sided breast cancer radiotherapy. Radiat Oncol (Lond Engl) 10:141

    Article  Google Scholar 

  9. Heidenreich PA, Hancock SL, Lee BK, Mariscal CS, Schnittger I (2003) Asymptomatic cardiac disease following mediastinal irradiation. J Am Coll Cardiol 42:743–749

    Article  PubMed  Google Scholar 

  10. Thavendiranathan P, Negishi T, Coté MA, Penicka M, Massey R, Cho GY et al (2018) Single versus standard multiview assessment of global longitudinal strain for the diagnosis of cardiotoxicity during cancer therapy. JACC Cardiovasc Imaging 11:1109–1118

    Article  PubMed  Google Scholar 

  11. Lancellotti P, Nkomo VT, Badano LP, Bergler-Klein J, Bogaert J, Davin L et al (2013) 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. J Am Soc Echocardiogr Off Publ Am Soc Echocardiogr 26:1013–1032

    Article  Google Scholar 

  12. Zhu Q, Kirova YM, Cao L, Arsene-Henry A, Chen J (2018) Cardiotoxicity associated with radiotherapy in breast cancer: a question-based review with current literatures. Cancer Treat Rev 68:9–15

    Article  PubMed  Google Scholar 

  13. Farhood B, Aliasgharzadeh A, Amini P, Saffar H, Motevaseli E, Rezapoor S et al (2019) Radiation-induced dual oxidase upregulation in rat heart tissues: protective effect of melatonin. Medicina (Kaunas) 55:317

    Article  Google Scholar 

  14. Seddon M, Looi YH, Shah AM (2007) Oxidative stress and redox signalling in cardiac hypertrophy and heart failure. Heart (Br Cardiac Soc) 93:903–907

    Article  CAS  Google Scholar 

  15. Guldner L, Haddy N, Pein F, Diallo I, Shamsaldin A, Dahan M et al (2006) Radiation dose and long term risk of cardiac pathology following radiotherapy and anthracyclin for a childhood cancer. Radiother Oncol J Eur Soc Ther Radiol Oncol 81:47–56

    Article  Google Scholar 

  16. Armanious MA, Mohammadi H, Khodor S, Oliver DE, Johnstone PA, Fradley MG (2018) Cardiovascular effects of radiation therapy. Curr Probl Cancer 42:433–442

    Article  PubMed  Google Scholar 

  17. Darby SC, Cutter DJ, Boerma M, Constine LS, Fajardo LF, Kodama K et al (2010) Radiation-related heart disease: current knowledge and future prospects. Int J Radiat Oncol Biol Phys 76:656–665

    Article  PubMed  PubMed Central  Google Scholar 

  18. Gevaert SA, Halvorsen S, Sinnaeve PR, Sambola A, Gulati G, Lancellotti P et al (2021) Evaluation and management of cancer patients presenting with acute cardiovascular disease: a Consensus Document of the Acute CardioVascular Care (ACVC) association and the ESC council of Cardio-Oncology-Part 1: acute coronary syndromes and acute pericardial diseases. Eur Heart J Acute Cardiovasc Care 10:947–959

    Article  PubMed  Google Scholar 

  19. Piroth MD, Baumann R, Budach W, Dunst J, Feyer P, Fietkau R et al (2019) Heart toxicity from breast cancer radiotherapy: current findings, assessment, and prevention. Strahlentherapie und Onkologie : Organ der Deutschen Rontgengesellschaft [et al] 195:1–12

    Article  Google Scholar 

  20. Sritharan HP, Delaney GP, Lo Q, Batumalai V, Xuan W, Thomas L (2017) Evaluation of traditional and novel echocardiographic methods of cardiac diastolic dysfunction post radiotherapy in breast cancer. Int J Cardiol 243:204–208

    Article  PubMed  Google Scholar 

  21. Erven K, Florian A, Slagmolen P, Sweldens C, Jurcut R, Wildiers H et al (2013) Subclinical cardiotoxicity detected by strain rate imaging up to 14 months after breast radiation therapy. Int J Radiat Oncol Biol Phys 85:1172–1178

    Article  PubMed  Google Scholar 

  22. Stanton T, Leano R, Marwick TH (2009) Prediction of all-cause mortality from global longitudinal speckle strain: comparison with ejection fraction and wall motion scoring. Circ Cardiovasc Imaging 2:356–364

    Article  PubMed  Google Scholar 

  23. Marwick TH (2022) Global longitudinal strain monitoring to guide cardioprotective medications during anthracycline treatment. Curr Oncol Rep. https://doi.org/10.1007/s11912-022-01242-y

    Article  PubMed  PubMed Central  Google Scholar 

  24. Thavendiranathan P, Poulin F, Lim KD, Plana JC, Woo A, Marwick TH (2014) Use of myocardial strain imaging by echocardiography for the early detection of cardiotoxicity in patients during and after cancer chemotherapy: a systematic review. J Am Coll Cardiol 63:2751–2768

    Article  PubMed  Google Scholar 

  25. Haugaa KH, Dejgaard LA (2018) Global longitudinal strain: ready for clinical use and guideline implementation. J Am Coll Cardiol 71:1958–1959

    Article  PubMed  Google Scholar 

  26. Tarantini L, Gulizia MM, Di Lenarda A, Maurea N, Giuseppe Abrignani M, Bisceglia I et al (2017) ANMCO/AIOM/AICO Consensus Document on clinical and management pathways of cardio-oncology: executive summary. Eur Heart J Suppl J Eur Soc Cardiol 19:D370–D379

    Article  CAS  Google Scholar 

  27. Escher F, Westermann D, Gaub R, Pronk J, Bock T, Al-Saadi N et al (2011) Development of diastolic heart failure in a 6-year follow-up study in patients after acute myocarditis. Heart 97:709–714

    Article  PubMed  Google Scholar 

  28. Di Bella G, Coglitore S, Zimbalatti C, Minutoli F, Zito C, Patane S et al (2008) Strain Doppler echocardiography can identify longitudinal myocardial dysfunction derived from edema in acute myocarditis. Int J Cardiol 126:279–280

    Article  PubMed  Google Scholar 

  29. Di Bella G, Gaeta M, Pingitore A, Oreto G, Zito C, Minutoli F et al (2010) Myocardial deformation in acute myocarditis with normal left ventricular wall motion—a cardiac magnetic resonance and 2-dimensional strain echocardiographic study. Circ J 74:1205–1213

    Article  PubMed  Google Scholar 

  30. Haland TF, Almaas VM, Hasselberg NE, Saberniak J, Leren IS, Hopp E et al (2016) Strain echocardiography is related to fibrosis and ventricular arrhythmias in hypertrophic cardiomyopathy. Eur Heart J Cardiovasc Imaging 17:613–621

    Article  PubMed  PubMed Central  Google Scholar 

  31. Sung H, Ferlay J, Siegel RL (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249

    Article  PubMed  Google Scholar 

  32. Wright JL, Parekh A (2017) Updates in postmastectomy radiation. Surg Oncol Clin N Am 26:383–392

    Article  PubMed  Google Scholar 

  33. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić M et al (2018) Global surveillance of trends in cancer survival 2000–14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet (Lond Engl) 391:1023–1075

    Article  Google Scholar 

  34. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097

    Article  PubMed  PubMed Central  Google Scholar 

  35. Senkus E, Kyriakides S, Ohno S, Penault-Llorca F, Poortmans P, Rutgers E et al (2015) Primary breast cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 26(Suppl 5):v8-30

    Article  PubMed  Google Scholar 

  36. Siegel RL, Miller KD (2021) Cancer statistics, 2021. CA Cancer J Clin 71:7–33

    Article  PubMed  Google Scholar 

  37. Donnellan E, Phelan D, McCarthy CP, Collier P, Desai M, Griffin B (2016) Radiation-induced heart disease: a practical guide to diagnosis and management. Cleve Clin J Med 83:914–922

    Article  PubMed  Google Scholar 

  38. Galper SL, Yu JB, Mauch PM, Strasser JF, Silver B, Lacasce A et al (2011) Clinically significant cardiac disease in patients with Hodgkin lymphoma treated with mediastinal irradiation. Blood 117:412–418

    Article  CAS  PubMed  Google Scholar 

  39. Yu AF, Raikhelkar J, Zabor EC, Tonorezos ES, Moskowitz CS, Adsuar R et al (2016) Two-dimensional speckle tracking echocardiography detects subclinical left ventricular systolic dysfunction among adult survivors of childhood, adolescent, and young adult cancer. Biomed Res Int 2016:9363951

    PubMed  PubMed Central  Google Scholar 

  40. Desai MY, Jellis CL, Kotecha R, Johnston DR, Griffin BP (2018) Radiation-associated cardiac disease: a practical approach to diagnosis and management. JACC Cardiovasc Imaging 11:1132–1149

    Article  PubMed  Google Scholar 

  41. Fuentes E, Gibbins JM, Holbrook LM, Palomo I (2018) NADPH oxidase 2 (NOX2): a key target of oxidative stress-mediated platelet activation and thrombosis. Trends Cardiovasc Med 28:429–434

    Article  CAS  PubMed  Google Scholar 

  42. Ping Z, Peng Y, Lang H, Xinyong C, Zhiyi Z, Xiaocheng W et al (2020) Oxidative stress in radiation-induced cardiotoxicity. Oxid Med Cell Longev 2020:3579143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Alam K, Moinuddin, Jabeen S (2007) Immunogenicity of mitochondrial DNA modified by hydroxyl radical. Cell Immunol 247:12–17

    Article  CAS  PubMed  Google Scholar 

  44. Wei YH (1998) Oxidative stress and mitochondrial DNA mutations in human aging. Proc Soc Exp Biol Med Soc Exp Biol Med (New York, NY) 217:53–63

    Article  CAS  Google Scholar 

  45. Gajowik A, Dobrzyńska MM (2014) Lycopene—antioxidant with radioprotective and anticancer properties. A review. Rocz Panstw Zakl Hig 65:263–271

    PubMed  Google Scholar 

  46. Meng G, Tang X, Yang Z, Benesch MGK, Marshall A, Murray D et al (2017) Implications for breast cancer treatment from increased autotaxin production in adipose tissue after radiotherapy. FASEB J 31:4064–4077

    Article  CAS  PubMed  Google Scholar 

  47. Zhang K, He X, Zhou Y, Gao L, Qi Z, Chen J et al (2015) Atorvastatin ameliorates radiation-induced cardiac fibrosis in rats. Radiat Res 184:611–620

    Article  CAS  PubMed  Google Scholar 

  48. van der Veen SJ, Ghobadi G, de Boer RA, Faber H, Cannon MV, Nagle PW et al (2015) ACE inhibition attenuates radiation-induced cardiopulmonary damage. Radiother Oncol 114:96–103

    Article  PubMed  CAS  Google Scholar 

  49. O’Herron T, Lafferty J (2018) Prophylactic use of colchicine in preventing radiation induced coronary artery disease. Med Hypotheses 111:58–60

    Article  CAS  PubMed  Google Scholar 

  50. Escher F, Kasner M, Kühl U, Heymer J, Wilkenshoff U, Tschöpe C et al (2013) New echocardiographic findings correlate with intramyocardial inflammation in endomyocardial biopsies of patients with acute myocarditis and inflammatory cardiomyopathy. Mediat Inflamm 2013:875420

    Article  Google Scholar 

  51. Schwuchow-Thonke S, Göbel S, Emrich T, Schmitt VH, Fueting F, Klank C et al (2021) Increased C reactive protein, cardiac troponin I and GLS are associated with myocardial inflammation in patients with non-ischemic heart failure. Sci Rep 11:3008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sperry BW, Ibrahim A, Negishi K, Negishi T, Patel P, Popović ZB et al (2017) Incremental prognostic value of global longitudinal strain and 18F-fludeoxyglucose positron emission tomography in patients with systemic sarcoidosis. Am J Cardiol 119:1663–1669

    Article  PubMed  Google Scholar 

  53. Palmieri V, Innocenti F, Guzzo A, Guerrini E, Vignaroli D, Pini R (2015) Left ventricular systolic longitudinal function as predictor of outcome in patients with sepsis. Circ Cardiovasc Imaging 8:e003865 (discussion e)

    Article  PubMed  Google Scholar 

  54. Wynn TA (2004) Fibrotic disease and the T(H)1/T(H)2 paradigm. Nat Rev Immunol 4:583–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Veinot JP, Edwards WD (1996) Pathology of radiation-induced heart disease: a surgical and autopsy study of 27 cases. Hum Pathol 27:766–773

    Article  CAS  PubMed  Google Scholar 

  56. Xu P, Yi Y, Luo Y, Liu Z, Xu Y, Cai J et al (2021) Radiation-induced dysfunction of energy metabolism in the heart results in the fibrosis of cardiac tissues. Mol Med Rep. https://doi.org/10.3892/mmr.2021.12482

    Article  PubMed  PubMed Central  Google Scholar 

  57. Yarnold J, Brotons MC (2010) Pathogenetic mechanisms in radiation fibrosis. Radiother Oncol 97:149–161

    Article  CAS  PubMed  Google Scholar 

  58. Weigel C, Schmezer P, Plass C, Popanda O (2015) Epigenetics in radiation-induced fibrosis. Oncogene 34:2145–2155

    Article  CAS  PubMed  Google Scholar 

  59. Rodemann HP, Peterson HP, Schwenke K, von Wangenheim KH (1991) Terminal differentiation of human fibroblasts is induced by radiation. Scan Microsc 5:1135–1142 (discussion 42–3)

    CAS  Google Scholar 

  60. Chimura M, Onishi T, Tsukishiro Y, Sawada T, Kiuchi K, Shimane A et al (2017) Longitudinal strain combined with delayed-enhancement magnetic resonance improves risk stratification in patients with dilated cardiomyopathy. Heart 103:679–686

    Article  CAS  PubMed  Google Scholar 

  61. Cui Y, Cao Y, Song J, Dong N, Kong X, Wang J et al (2018) Association between myocardial extracellular volume and strain analysis through cardiovascular magnetic resonance with histological myocardial fibrosis in patients awaiting heart transplantation. J Cardiovasc Magn Reson 20:25

    Article  PubMed  PubMed Central  Google Scholar 

  62. Xu HY, Yang ZG, Zhang Y, Peng WL, Xia CC, Li ZL et al (2020) Prognostic value of heart failure in hemodialysis-dependent end-stage renal disease patients with myocardial fibrosis quantification by extracellular volume on cardiac magnetic resonance imaging. BMC Cardiovasc Disord 20:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Huttin O, Zhang L, Lemarié J, Mandry D, Juillière Y, Lemoine S et al (2015) Global and regional myocardial deformation mechanics of microvascular obstruction in acute myocardial infarction: a three dimensional speckle-tracking imaging study. Int J Cardiovasc Imaging 31:1337–1346

    Article  PubMed  Google Scholar 

  64. Cameli M, Mondillo S, Righini FM, Lisi M, Dokollari A, Lindqvist P et al (2016) Left ventricular deformation and myocardial fibrosis in patients with advanced heart failure requiring transplantation. J Card Fail 22:901–907

    Article  PubMed  Google Scholar 

  65. Lisi M, Cameli M, Righini FM, Malandrino A, Tacchini D, Focardi M et al (2015) RV Longitudinal Deformation Correlates With Myocardial Fibrosis in Patients With End-Stage Heart Failure. JACC Cardiovasc Imaging 8:514–522

    Article  PubMed  Google Scholar 

  66. Yeboa DN, Evans SB (2016) Contemporary breast radiotherapy and cardiac toxicity. Semin Radiat Oncol 26:71–78

    Article  PubMed  Google Scholar 

  67. Dell’Oro M, Giles E, Sharkey A, Borg M (2019) A retrospective dosimetric study of radiotherapy patients with left-sided breast cancer; patient selection criteria for deep inspiration breath hold technique. Cancers (Basel) 11:259

    Article  Google Scholar 

  68. Remouchamps VM, Vicini FA, Sharpe MB, Kestin LL, Martinez AA, Wong JW (2003) Significant reductions in heart and lung doses using deep inspiration breath hold with active breathing control and intensity-modulated radiation therapy for patients treated with locoregional breast irradiation. Int J Radiat Oncol Biol Phys 55:392–406

    Article  PubMed  Google Scholar 

  69. Salvestrini V, Iorio GC, Borghetti P, De Felice F, Greco C, Nardone V et al (2022) The impact of modern radiotherapy on long-term cardiac sequelae in breast cancer survivor: a focus on deep inspiration breath-hold (DIBH) technique. J Cancer Res Clin Oncol 148:409–417

    Article  CAS  PubMed  Google Scholar 

  70. Hjelstuen MH, Mjaaland I, Vikström J, Dybvik KI (2012) Radiation during deep inspiration allows loco-regional treatment of left breast and axillary-, supraclavicular- and internal mammary lymph nodes without compromising target coverage or dose restrictions to organs at risk. Acta Oncol (Stockholm, Sweden) 51:333–344

    Article  Google Scholar 

  71. Schönecker S, Heinz C, Söhn M, Haimerl W, Corradini S, Pazos M et al (2016) Reduction of cardiac and coronary artery doses in irradiation of left-sided breast cancer during inspiration breath hold: a planning study. Strahlentherapie und Onkologie: Organ der Deutschen Rontgengesellschaft [et al] 192:750–758

    Article  Google Scholar 

  72. Korreman SS, Pedersen AN, Nøttrup TJ, Specht L, Nyström H (2005) Breathing adapted radiotherapy for breast cancer: comparison of free breathing gating with the breath-hold technique. Radiother Oncol 76:311–318

    Article  PubMed  Google Scholar 

  73. Latty D, Stuart KE, Wang W, Ahern V (2015) Review of deep inspiration breath-hold techniques for the treatment of breast cancer. J Med Radiat Sci 62:74–81

    Article  PubMed  PubMed Central  Google Scholar 

  74. Desai MY, Windecker S, Lancellotti P, Bax JJ, Griffin BP, Cahlon O et al (2019) Prevention, diagnosis, and management of radiation-associated cardiac disease: JACC Scientific Expert Panel. J Am Coll Cardiol 74:905–927

    Article  PubMed  Google Scholar 

  75. Boero IJ, Paravati AJ, Triplett DP, Hwang L, Matsuno RK, Gillespie EF et al (2016) Modern radiation therapy and cardiac outcomes in breast cancer. Int J Radiat Oncol Biol Phys 94:700–708

    Article  PubMed  Google Scholar 

  76. Saiki H, Petersen IA, Scott CG, Bailey KR, Dunlay SM, Finley RR et al (2017) Risk of heart failure with preserved ejection fraction in older women after contemporary radiotherapy for breast cancer. Circulation 135:1388–1396

    Article  PubMed  PubMed Central  Google Scholar 

  77. Saiki H, Moulay G, Guenzel AJ, Liu WB, Decklever TD, Classic KL et al (2017) Experimental cardiac radiation exposure induces ventricular diastolic dysfunction with preserved ejection fraction. Am J Physiol Heart Circ Physiol 313:H392–H407

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This research is supported by the National Science Foundation of China, Grant No. 81970341, and the National Science Foundation of China, Grant No.81773366.

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GB conceived and designed the study. LH reviewed the indexes and extracted data. LXT performed risk of bias assessment and analyzed the data. WTH wrote the article. LSJ and YZY supervised the data synthesis, results interpretations and oversaw the entire project.

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Correspondence to Shijun Li or Zuyin Yu.

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Guan, B., Luan, H., Li, X. et al. Applying global longitudinal strain in assessing cardiac dysfunction after radiotherapy among breast cancer patients: a systemic review and meta-analysis. Clin Transl Imaging 10, 413–424 (2022). https://doi.org/10.1007/s40336-022-00493-w

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