Abstract
Purpose
Heart myxomas have been frequently considered as benign lesions associated with Carney’s complex. However, after surgical removal, myxomas re-emerge causing dysfunctional heart.
Methods
To identify whether cardiac myxomas may develop a metastatic phenotype as occurs in malignant cancers, a profile of several proteins involved in malignancy such as oncogenes (c-MYC, K-RAS and H-RAS), cancer-associated metabolic transcriptional factors (HIF-1α, p53 and PPAR-γ) and epithelial–mesenchymal transition proteins (fibronectin, vimentin, β-catenin, SNAIL and MMP-9) were evaluated in seven samples from a cohort of patients with atrial and ventricular myxomas. The analysis was also performed in: (1) cardiac tissue surrounding the area where myxoma was removed; (2) non-cancer heart tissue (NCHT); and (3) malignant triple negative breast cancer biopsies for comparative purposes.
Results
Statistical analysis applying univariate (Kruskal–Wallis and Dunn’s tests) and multivariate analyses (PCA, principal component analysis) revealed that heart myxomas (7–15 times) and myxoma surrounding tissue (22–99 times) vs. NCHT showed high content of c-MYC, p53, vimentin, and HIF-1α, indicating that both myxoma and its surrounding area express oncogenes and malignancy-related proteins as occurs in triple negative breast cancer.
Conclusions
Based on ROC (receiver operating characteristics) statistical analysis, c-MYC, HIF-1α, p53, and vimentin may be considered potential biomarkers for malignancy detection in myxoma.
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References
Abba MC, Lacunza E, Butti M, Aldaz CM (2010) Breast cancer biomarker discovery in the functional genomic age: a systematic review of 42 gene expression signatures. Biomark Insights 5:103–118. https://doi.org/10.4137/BMI.S5740
Aguirre-Benítez EL, Porras MG, Parra L, González-Ríos J, Garduño-Torres DF, Albores-García D, Avendaño A, Ávila-Rodríguez MA, Melo AI, Jiménez-Estrada I, Mendoza-Garrido ME, Toriz C, Diaz D, Ibarra-Coronado E, Mendoza-Ángeles K, Hernández-Falcón J (2017) Disruption of behavior and brain metabolism in artificially reared rats. Dev Neurobiol 77(12):1413–1429. https://doi.org/10.1002/dneu.22548
Altundag MB, Ertas G, Ucer AR, Durmus S, Abanuz H, Calikoğlu T, Ozbagi K, Demirkasimoglu A, Kaya B, Bakkal BH, Altundag K (2005) Brain metastasis of cardiac myxoma: case report and review of the literature. J Neurooncol 75(2):181–184. https://doi.org/10.1007/s11060-005-1859-7
Anders CK, Carey LA (2009) Biology, metastatic patterns, and treatment of patients with triple-negative breast cancer. Clin Breast Cancer 9(Suppl 2):S73–S81. https://doi.org/10.3816/CBC.2009.s.008
Barh D, Kumar A, Chatterjee S, Liloglou T (2009) Molecular features, markers, drug targets, and prospective targeted therapeutics in cardiac myxoma. Curr Cancer Drug Targets 9(6):705–716. https://doi.org/10.2174/156800909789271549
Bartlett JEII, Kotrlik JW, Higginsm CC (2001) Organizational research: determining appropriate sample size in survey. Off Syst Res J 19(1):43–50. https://doi.org/10.5306/wjco.v6.i6.252
Becker RP, Ramírez MA, Zalaquett SR, Moran VS, Irarrázaval LI MJ, Arretz VC, Córdova AS, Arnaiz GP (2008) Cardiac myxoma: clinical characterization, diagnostic methods and late surgical results. Rev Med Chil 136(3):287–295
Biddlestone J, Bandarra D, Rocha S (2015) The role of hypoxia in inflammatory disease (review). Int J Mol Med 35(4):859–869. https://doi.org/10.3892/ijmm.2015.2079
Björklund M, Koivunen E (2005) Gelatinase-mediated migration and invasion of cancer cells. Biochim Biophys Acta 1755(1):37–69. https://doi.org/10.1016/j.bbcan.2005.03.001
Blackmon SH, Kassis ES, Ge Y, Goldfarb R, Reardon M (2010) Left atrial myxoma embolus to the renal artery: should a nephrectomy be advised? Ann Thorac Surg 90(1):289–292. https://doi.org/10.1016/j.athoracsur.2009.11.059
Burke A, Jeudy J, Virmani R (2007) Textbook of cardiovascular medicine. Lippincott Williams and Wilkins, Philadelphia
Cardoso F, Harbeck N, Fallowfield L, Kyriakides S, Senkus E, ESMO Guidelines Working Group (2012) Locally recurrent or metastatic breast cancer: ESMO clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 23(Suppl 7):vii11–9. https://doi.org/10.1093/annonc/mds232
Carney JA (1985) Differences between non-familial and familial cardiac myxoma. Am J Surg Pathol 9(1):53–55. https://doi.org/10.1097/00000478-198501000-00009
Chambers JM, Cleveland WS, Kleiner B, Tukey PA (1983) Graphical methods for data analysis. Chapman and Hall/Cole Publishing Company, London
Chen Y, Olopade OI (2008) MYC in breast tumor progression. Expert Rev Anticancer Ther 8(10):1689–1698. https://doi.org/10.1586/14737140.8.10.1689
Collignon J, Lousberg L, Schroeder H, Jerusalem G (2016) Triple-negative breast cancer: treatment challenges and solutions. Breast Cancer (Dove Med Press) 8:93–107. https://doi.org/10.2147/BCTT.S69488
Diaz D, Vazquez-Polanco AM, Argueta-Donohué J, Stephens CR, Jimenez-Trejo F, Ceballos-Liceaga SE, Mantilla-Beniers N (2018) Incidence of intestinal infectious disease due to protozoa and bacteria in Mexico: analysis of national surveillance records from 2003 to 2012. BioMed Res Int 2018:22. https://doi.org/10.1155/2018/2893012
Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6:241–252. https://doi.org/10.1080/00401706.1964.10490181
Foulkes WD, Smith IE, Reis-Filho JS (2010) Triple-negative breast cancer. N Engl J Med 363(20):1938–1948. https://doi.org/10.1056/NEJMra1001389
Fyke FE 3rd, Seqard JB, Edwards WD, Miller FA Jr, Reeder GS, Schattenberg TT, Schub C, Callahan JA, Tajik AJ (1985) Primary cardiac tumors: experience with 30 consecutive patients since the introduction of two-dimensional echocardiography. J Am Coll Cardiol 5(6):1465–1473. https://doi.org/10.1016/S0735-1097(85)80364-8
Gallardo-Pérez JC, Rivero-Segura NA, Marín-Hernández A, Moreno-Sánchez R, Rodríguez-Enríquez S (2014) GPI/AMF inhibition blocks the development of the metastatic phenotype of mature multi-cellular tumor spheroids. Biochim Biophys Acta 1843(6):1043–1053. https://doi.org/10.1016/j.bbamcr.2014.01.013
Gao L, Chen Q, Zhou X, Fan L (2012) The role of hypoxia-inducible factor 1 in atherosclerosis. J Clin Pathol 65(10):872–876. https://doi.org/10.1136/jclinpath-2012-200828
Goossens N, Nakagawa S, Sun X, Hoshida Y (2015) Cancer biomarker discovery and validation. Transl Cancer Res 4(3):256–269. https://doi.org/10.3978/j.issn.2218-676X.2015.06.04
Gošev I, Paić F, Durić Z, Gošev M, Ivčević S, Jakuš FB, Biočina B (2013) Cardiac myxoma the great imitators: comprehensive histopathological and molecular approach. Int J Cardiol 164(1):7–20. https://doi.org/10.1016/j.ijcard.2011.12.052
Goswami SK, Das DK (2010) Oxygen sensing, cardiac ischemia, HIF-1α and some emerging concepts. Curr Cardiol Rev 6(4):265–273. https://doi.org/10.2174/157340310793566136
Haffty BG, Yang Q, Reiss M, Kearney T, Higgins SA, Weidhaas J, Harris L, Hait W, Toppmeyer D (2006) Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol 24(36):5652–5657. https://doi.org/10.1200/JCO.2006.06.5664
Hannah H 3rd, Eisemann G, Hiszcznskyj R, Winsky M, Cohen L (1982) Invasive atrial myxoma: documentation of malignant potential of cardiac myxomas. Am Heart J 104(4 Pt 1):881–883. https://doi.org/10.1016/0002-8703(82)90031-X
Hasegawa T, Nakagawa S, Chino M, Kunihiro T, Ui S, Kimura M (2002) Primary cardiac sarcoma mimicking benign myxoma: a case report. J Cardiol 39(6):321–325
Henry NL, Hayes DF (2012) Cancer biomarkers. Mol Oncol 6(2):140–146. https://doi.org/10.1016/j.molonc.2012.01.010
Hoffmeier A, Sindermann JR, Scheld HH, Martens S (2014) Cardiac tumors—diagnosis and surgical treatment. Dtsch Arztebl Int 111(12):205–211. https://doi.org/10.3238/arztebl.2014.0205
Hong OY, Noh EM, Jang HY, Lee YR, Lee BK, Jung SH, Kim JS, Youn HJ (2017) Epigallocatechin gallate inhibits the growth of MDA-MB-231 breast cancer cells via inactivation of the β-catenin signaling pathway. Oncol Lett 14(1):441–446. https://doi.org/10.3892/ol.2017.6108
Hou YC, Chang S, Lo HM, Hsiao CH, Lin FY (2001) Recurrent cardiac myxoma with multiple distant metastasis and malignant change. J Formos Med Assoc 100(1):63–65
Ibarra-Coronado EG, Velazquéz-Moctezuma J, Diaz D, Becerril-Villanueva LE, Pavón L, Morales-Montor J (2015) Sleep deprivation induces changes in immunity in Trichinella spiralis-infected rats. Int J Biol Sci 11(8):901–912. https://doi.org/10.7150/ijbs.11907
Isobe S, Murohara T (2015) Editorial: cardiac tumors: histopathological aspects and assessments with cardiac noninvasive imaging. J Cardiol Cases 12:37–38. https://doi.org/10.1016/j.jccase.2015.04.008
Iurlaro R, León-Annicchiarico CL, Muñoz-Pinedo C (2014) Regulation of cancer metabolism by oncogenes and tumor suppressors. Methods Enzymol 542:59–80. https://doi.org/10.1016/B978-0-12-416618-9.00003-0
Jackson T, Allard MF, Sreenan CM, Doss LK, Bishop SP, Swain JL (1990) The c-myc proto-oncogene regulates cardiac development in transgenic mice. Mol Cell Biol 10(7):3709–3716. https://doi.org/10.1128/MCB.10.7.3709
Kalia M (2015) Biomarkers for personalized oncology: recent advances and future challenges. Metabolism 64(3 Suppl 1):S16–S21. https://doi.org/10.1016/j.metabol.2014.10.027
Kaul P, Paniagua R, Balaji S, Batin P (2013) Large mass in right atrium after CABG—myxoma, adrenal metastasis or in-transit thrombus? Br J Cardiol 20:79. https://doi.org/10.5837/bjc.2013.19
Kaynak K, Beşirli K, Arslan C, Ozgüroğlu M, Oz B (2001) Metastatic cardiac myxoma. Ann Thorac Surg 72(2):623–625. https://doi.org/10.1016/S0003-4975(00)02408-5
Kidd ME, Shumaker DK, Ridge KM (2014) The role of vimentin intermediate filaments in the progression of lung cancer. Am J Respir Cell Mol Biol 50(1):1–6. https://doi.org/10.1165/rcmb.2013-0314TR
Kim SA, Inamura K, Yamauchi M, Nishihara R, Mima K, Sukawa Y, Li T, Yasunari M, Morikawa T, Fitzgerald KC, Fuchs CS, Wu K, Chan AT, Zhang X, Ogino S, Qian ZR (2016) Loss of CDH1 (E-cadherin) expression is associated with infiltrative tumour growth and lymph node metastasis. Br J Cancer 114(2):199–206. https://doi.org/10.1038/bjc.2015.347
Köhrmann A, Kammerer U, Kapp M, Dietl J, Anacker J (2009) Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: New findings and review of the literature. BMC Cancer 9:188. https://doi.org/10.1186/1471-2407-9-188
Kothari J, Lakhia K, Solanki P, Panchal J, Shah P (2016) Recurrent left atrial myxoma in a young patient: a rare entity. J Clin Diagn Res 10(8):PD05–P7. https://doi.org/10.7860/JCDR/2016/20425.8321
Lee VH, Connolly HM, Brown RD Jr (2007) Central nervous system manifestations of cardiac myxoma. Arch Neurol 64(8):1115–1120. https://doi.org/10.1001/archneur.64.8.1115
Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 121(7):2750–2767. https://doi.org/10.1172/JCI45014
Lin SY, Xia W, Wang JC, Kwong KY, Spohn B, Wen Y, Pestell RG, Hung MC (2000) Beta-catenin, a novel prognostic marker for breast cancer: its roles in cyclin D1 expression and cancer progression. Proc Natl Acad Sci USA 97(8):4262–4266. https://doi.org/10.1073/pnas.060025397
Locker GY, Hamilton S, Harris J, Jessup JM, Kemeny N, Macdonald JS, Somerfield MR, Hayes DF, Bast RC Jr, ASCO (2006) ASCO 2006 update of recommendations for the use of tumor markers in gastrointestinal cancer. J Clin Oncol 24(33):5313–5327. https://doi.org/10.1200/JCO.2006.08.2644
Loor G, Schumacker PT (2008) Role of hypoxia-inducible factor in cell survival during myocardial ischemia-reperfusion. Cell Death Differ 15(4):686–690. https://doi.org/10.1038/cdd.2008.13
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275
McCarthy PM, Schaff HV, Winkler HZ, Lieber MM, Carney JA (1989) Deoxyribonucleic acid ploidy pattern of cardiac myxomas. Another predictor of biologically unusual myxomas. J Thorac Cardiovasc Surg 98(6):1083–1086
Mendoza C, Bernstein E, Ferreira A (2007) Multiple recurrences of nonfamilial cardiac myxomas: a report of two cases. Tex Heart Inst J 34(2):236–239
Mohajeri G, Sanei MH, Tabatabaee SA, Hashemi SM, Amjad E, Mohajeri MR, Shemshaki H, Jazi AH, Kolahdouzan M (2012) Micrometastasis in non-small-cell lung cancer: detection and staging. Ann Thorac Med 7(3):149–152. https://doi.org/10.4103/1817-1737.98848
Nieto MA, Huang RY, Jackson RA, Thiery JP (2016) EMT: 2016. Cell 166:21–45. https://doi.org/10.1016/j.cell.2016.06.028
Pacheco-Velázquez SC, Gallardo-Pérez JC, Aguilar-Ponce JL, Villarreal P, Ruiz-Godoy L, Pérez-Sánchez M, Marín-Hernández A, Ruiz-García E, Meneses-García A, Moreno-Sánchez R, Rodríguez-Enríquez S (2014) Identification of a metabolic and canonical biomarker signature in Mexican HR+/HER2-, triple positive and triple-negative breast cancer patients. Int J Oncol 45(6):2549–2559. https://doi.org/10.3892/ijo.2014.2676
Pateras IS, Evangelou K, Tsimaratou K, Liontos M, Sakellariou S, Barlogiannis T, Karakitsos P, Papalois A, Kotsinas A, Gorgoulis VG (2012) Detection of herplex simplex virus-1 and -2 in cardiac myxomas. J Biomed Biotechnol 2012:823949. https://doi.org/10.1155/2012/823949
Pérez-Andreu J, Parrilla G, Arribas JM, García-Villalba B, Lucas JJ, Garci- Navarro M, Marín F, Gutierrez F, Moreno A (2013) Neurological manifestations of cardiac myxoma: experience in a referral hospital. Neurologia 28(9):529–534. https://doi.org/10.1016/j.nrl.2013.03.006
Pinede L, Duhaut P, Loire R (2001) Clinical presentation of left atrial cardiac myxoma. A series of 112 consecutive cases. Medicine (Baltimore) 80(3):159–172
Porcaro AB, de Luyk N, Corsi P, Sebben M, Tafuri A, Tamanini I, Processali T, Cerruto MA, Migliorini F, Brunelli M, Siracusano S, Artibani W (2017) Bilateral lymph node micrometastases and seminal vesicle invasion associated with same clinical predictors in localized prostate cancer. Tumori 103(3):299–306. https://doi.org/10.5301/tj.5000546
Rathore KS, Hussenbocus S, Stuklis R, Edwards J (2008) Novel strategies for recurrent cardiac myxoma. Ann Thorac Surg 85(6):2125–2126. https://doi.org/10.1016/j.athoracsur.2007.11.080
Reynen K (1995) Cardiac myxomas. N Engl J Med 333(24):1610–1617. https://doi.org/10.1056/NEJM199512143332407
Reynen K (1996) Frequency of primary tumors of the heart. Am J Cardiol 77(1):107. https://doi.org/10.1016/S0002-9149(97)89149-7
Rodríguez-Enríquez S, Pacheco-Velázquez SC, Gallardo-Pérez JC, Marín-Hernández A, Aguilar-Ponce JL, Ruiz-García E, Ruizgodoy-Rivera LM, Meneses-García A, Moreno-Sánchez R (2011) Multi-biomarker pattern for tumor identification and prognosis. J Cell Biochem 112(10):2703–2715. https://doi.org/10.1002/jcb.23224
Roldán FJ, Vargas-Barrón J, Espinola-Zavaleta N, Keirns C, Romero-Cárdenas A (2000) Recurrent myxoma implanted in the left atrial appendage. Echocardiography 17(2):169–171. https://doi.org/10.1111/j.1540-8175.2000.tb01119.x
Siltanen P, Tuuteri L, Norio R, Tala P, Ahrenberg P, Halonen PI (1976) Atrial myxoma in a family. Am J Cardiol 38(2):252–256. https://doi.org/10.1016/0002-9149(76)90158-2
Singh S, Singh M, Kovacs D, Benatar D, Khosla S, Singh H (2015) A rare case of an intracardiac lipoma. Int J Surg Case Rep 9:105–108. https://doi.org/10.1016/j.ijscr.2015.02.024
Singhal P, Luk A, Rao V, Butany J (2014) Molecular basis of cardiac myxomas. Int J Mol Sci 15(1):1315–1337. https://doi.org/10.3390/ijms15011315
Smith M, Chaudhry MA, Lozano P, Humphrey MB (2012) Cardiac myxoma induced paraneoplastic syndromes: a review of the literature. Eur J Intern Med 23(8):669–673. https://doi.org/10.1016/j.ejim.2012.05.015
Suvarna SK, Royds JA (1996) The nature of the cardiac myxoma. Int J Cardiol 57(3):211–216. https://doi.org/10.1016/S0167-5273(96)02827-6
Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240(4857):1285–1293. https://doi.org/10.1126/science.3287615
Tachibana K, Yamasaki D, Ishimoto K, Doi T (2008) The role of PPARs in cancer. PPAR Res 2008:102737, https://doi.org/10.1155/2008/102737
Tal R (2012) The role of hypoxia and hypoxia-inducible factor-1alpha in preeclampsia pathogenesis. Biol Reprod 87(6):134. https://doi.org/10.1095/biolreprod.112.102723
Talks K, Turley H, Gatter KC (2000) The expression and distribution of hypoxia inducible factors HIF-1a and HIF-2a in normal human tissues, cancers tumor associated macrophages. Am J Pathol 157(2):411–421. https://doi.org/10.1016/S0002-9440(10)64554-3
Tarelo-Saucedo JM, Peñaloza-Guadarrama M, Villela-Caleti J, García-Cruz A, Arizmendi-Monroy DK, Reynada-Torres JL, Martinez-Ramirez L (2016) Surgical results and monitoring of postoperative atrial myxomas. Arch Cardiol Mex 86(1):35–40. https://doi.org/10.1016/j.acmx.2015.09.002
Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7(2):131–142. https://doi.org/10.1038/nrm1835
Todo T, Usui M, Nagashima K (1992) Cerebral metastasis of malignant cardiac myxoma. Surg Neurol 37(5):374–379. https://doi.org/10.1016/0090-3019(92)90007-A
Tomifuji M, Imanishi Y, Araki K, Yamashita T, Yamamoto S, Kameyama K, Shiotani A (2011) Tumor depth as a predictor of lymph node metastasis of supraglottic and hypopharyngeal cancers. Ann Surg Oncol 18(2):490–496. https://doi.org/10.1245/s10434-010-1219-5
Vargas-Alarcón G, Vargas-Barrón J, Cruz-Robles D, Pérez-Vielma N, García-Trejo JJ, Aguilar-Gaytán R, Cortés-Hernández P, Vazquez-Ortíz ZY, Romero-Cardenas A (2008) A deletion in the PRKAR1A gene is associated with Carney complex. J Pediatr Endocrinol Metab 21(7):705–709. https://doi.org/10.1515/JPEM.2008.21.7.705
Vargas-Barron J, Romero-Cardenas A, Villegas M, Keirns C, Gomez-Jaume A, Delong R, Malo-Camacho R (1991) Transthoracic and transesophageal echocardiographic diagnosis of myxomas in the four cardiac cavities. Am Heart J 121(3 Pt 1):931–933. https://doi.org/10.1016/0002-8703(91)90216-5
Villalpando-Mendoza E, Pérez-Pérez FM, Cortés-Flores AO, Velázquez-Ramírez GA, Fuentes-Orozco C, González-Ojeda A (2006) Frequency of heart tumors and their histopathological correlation. Cir Cir 74(3):183–187
Wada A, Kanda T, Hayashi R, Imai S, Suzuki T, Murata K (1993) Cardiac myxoma metastasized to the brain: potential role of endogenous interleukin-6. Cardiology 83(3):208–211. https://doi.org/10.1159/000175971
Wang C, Lisanti MP, Liao DJ (2011) Reviewing once more the c-myc and Ras collaboration: converging at the cyclin D1-CDK4 complex and challenging basic concepts of cancer biology. Cell Cycle 10(1):57–67. https://doi.org/10.4161/cc.10.1.14449
Wang S, Cheng Y, Zheng Y, He Z, Chen W, Zhou W, Duan C, Zhang C (2016) PRKAR1A is a functional tumor suppressor inhibiting ERK/Snail/E-cadherin pathway in lung adenocarcinoma. Sci Rep 6:39630. https://doi.org/10.1038/srep39630
Wittersheim M, Heydt C, Hoffmann F, Büttner R (2017) KRAS mutation in papillary fibroelastoma: a true cardiac neoplasm? J Pathol Clin Res 3(2):100–104. https://doi.org/10.1002/cjp2.66
Wu XY, Liu WT, Wu ZF, Chen C, Liu JY, Wu GN, Yao XQ, Liu FK, Li G (2016) Identification of HRAS as cancer-promoting gene in gastric carcinoma cell aggressiveness. Am J Cancer Res 6(9):1935–1948
Yadav BS, Chanana P, Jhamb S (2015) Biomarkers in triple negative breast cancer: a review. World J Clin Oncol 6(6):252–263. https://doi.org/10.5306/wjco.v6.i6.252
Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, Buechler P, Isaacs WB, Semenza GL, Simons JW (1999) Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res 59(22):5830–5835
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The present work was partially supported by CONACyT-México Grant No. 283144 to SRE.
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Pacheco-Velázquez, S.C., Gallardo-Pérez, J.C., Díaz, D. et al. Heart myxoma develops oncogenic and metastatic phenotype. J Cancer Res Clin Oncol 145, 1283–1295 (2019). https://doi.org/10.1007/s00432-019-02897-0
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DOI: https://doi.org/10.1007/s00432-019-02897-0