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Liquid biomarkers for the management of paediatric neuroblastoma: an approach to personalised and targeted cancer therapy

Published online by Cambridge University Press:  27 February 2020

Ernest Osei Open the ORCID record for Ernest Osei [Opens in a new window] ,
Nidaa Al-Ani ,
Aladdin Al-Asady  and
Susan Dang
Ernest Osei*
Affiliation:
Department of Medical Physics, Grand River Regional Cancer Centre, Kitchener, ON, Canada Department of Physics and Astronomy, University of Waterloo, Waterloo, ON, Canada Department of Systems Design Engineering, University of Waterloo, Waterloo, ON, Canada Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada
Nidaa Al-Ani
Affiliation:
Department of Medical Physics, Grand River Regional Cancer Centre, Kitchener, ON, Canada
Aladdin Al-Asady
Affiliation:
Department of Medical Physics, Grand River Regional Cancer Centre, Kitchener, ON, Canada
Susan Dang
Affiliation:
Department of Physics and Astronomy, University of Waterloo, Waterloo, ON, Canada
*
Author for correspondence: Ernest Osei, Department of Medical Physics, Grand River Regional Cancer Centre, Kitchener, ON, Canada. E-mail: [email protected]
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Abstract

Background:

Neuroblastoma is the most common extracranial solid tumour of infancy and accounts for about 6–10% of paediatric cancers. It has a biologically and clinically heterogeneous behaviour that ranges from spontaneous regression to cases of highly aggressive metastatic disease that could be unresponsive to standard therapy. In recent years, there have been several investigations into the development of various diagnostic, predictive and prognostic biomarkers towards personalised and targeted management of the disease.

Materials and Methods:

This paper reports on the review of current clinical and emerging biomarkers used in risk assessment, screening for early detection and diagnosis, prognostication and monitoring of the response of treatment of neuroblastoma in paediatric patients.

Conclusions:

Tumour markers can significantly improve diagnosis; however, the invasive, unpleasant and inconvenient nature of current tissue biopsies limits their applications, especially in paediatric patients. Therefore, the development of a non-invasive, reliable high accurate and personalised diagnostic tool capable of early detection and rapid response is the most promising step towards advanced cancer management from tumour diagnosis, therapy to patient monitoring and represents an important step towards the promise of precision, personalised and targeted medicine. Liquid biopsy assay with wide ranges of clinical applications is emerging to hold incredible potential for advancing cancer treatment and has greater promise for diagnostic purposes, identification and tracking of tumour-specific alterations during the course of the disease and to guide therapeutic decisions.

Keywords

Liquid biopsyneuroblastomabiomarkerspaediatric cancerspersonalised treatment
Type
Literature Review
Information
Journal of Radiotherapy in Practice , Volume 20 , Issue 2 , June 2021 , pp. 217 - 229
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Copyright
© The Author(s), 2020. Published by Cambridge University Press

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References

Thompson, D, Vo, KT, London, WB, et al. Identification of patient subgroups with markedly disparate rates of MYCN amplification in neuroblastoma: a report from the International Neuroblastoma Risk Group project. Cancer 2016; 122, 935–945. doi: 10.1002/cncr.29848.CrossRefGoogle ScholarPubMed
Verly, IR, van Kuilenburg, AB, Abeling, NG, et al. Catecholamines profiles at diagnosis: increased diagnostic sensitivity and correlation with biological and clinical features in neuroblastoma patients. Eur J Cancer 2017; 72, 235–243. doi: 10.1016/j.ejca.2016.12.002.CrossRefGoogle ScholarPubMed
Zambrano, E, Reyes-Múgica, M. Hormonal activity may predict aggressive behavior in neuroblastoma. Pediatr Devel Pathol 2002; 5(2):190–9. doi: 10.1007/s10024-001-0145-8.CrossRefGoogle ScholarPubMed
Wang, X, Wang, L, Su, Y, et al. Plasma cell-free DNA quantification is highly correlated to tumor burden in children with neuroblastoma. Cancer Med 2018; 7, 3022–3030. doi: 10.1002/cam4.1586.CrossRefGoogle Scholar
Maris, JM. The biologic basis for neuroblastoma heterogeneity and risk stratification. Curr Opin Pediatr 2005; 17, 7–13. doi: 10.1097/01.mop.0000150631.60571.89.CrossRefGoogle ScholarPubMed
Tolaney, SM, Toi, M, Neven, P, et al. Clinical significance of PIK3CA and ESR1 mutations in ctDNA and FFPE samples from the MONARCH 2 study of abemaciclib plus fulvestrant [abstract]. Proceedings of the American Association for Cancer Research Annual Meeting 2019; 2019 Mar 29–Apr 3; Atlanta, GA. Philadelphia (PA): AACR; Cancer Res 2019; 79 (13 Suppl): Abstract nr 4458.CrossRefGoogle Scholar
World Health Organization report 2018. Latest global cancer data. Geneva, Switzerland, 12 September 2018.Google Scholar
Steliarova-Foucher, E, Colombet, M, Ries, LAG, et al. International incidence of childhood cancer, 2001–10: a population-based registry study. Lancet Oncol 2017; 18 (6), 719–731. doi: 10.1016/S1470-2045(17)30186-9. Epub 2017 Apr 11.CrossRefGoogle ScholarPubMed
Siegel, RL, Miller, KD, Jemal, A. Cancer Stat 2017; 67 (1), 7–30. doi: 10.3322/caac.21387. Epub 2017 Jan 5.Google Scholar
Louis, CU, Shohet, JM. Neuroblastoma: molecular pathogenesis and therapy. Ann Rev Med 2015; 66, 49–63. doi: 10.1146/annurev-med-011514-023121. Epub 2014 Oct 27. PMID: 25386934.; PMCID: PMC4418018.CrossRefGoogle ScholarPubMed
Park, JR, Bagatell, R, London, WB, et al. Children’s Oncology Group’s 2013 blueprint for research: neuroblastoma. Pediatr Blood Cancer 2013; 985–993. doi: 10.1002/pbc.24433.CrossRefGoogle ScholarPubMed
Monsaingeon, M, Perel, Y, Simonnet, G, et al. Comparative values of catecholamines and metabolites for the diagnosis of neuroblastoma. Eur. J Pediatr 2003; 162 (6):397–402. doi: 10.1007/s00431-003-1175-1.CrossRefGoogle Scholar
Spix, C, Pastore, G, Sankila, R, et al. Neuroblastoma incidence and survival in European children (1978–1997): report from the Automated Childhood Cancer Information System project. Eur J Cancer 2006; 42 (13), 2081–2091. PMID: 16919772. doi: 10.1016/j.ejca.2006.05.008.CrossRefGoogle ScholarPubMed
Shinagawa, T, Kitamura, T, Katanoda, K, et al. The incidence and mortality rates of neuroblastoma cases before and after the cessation of the mass screening program in Japan: A descriptive study. Int J Cancer 2017; 140 (3), 618–625. doi: 10.1002/ijc.30482. Epub 2016 Nov 7.CrossRefGoogle ScholarPubMed
American cancer society. Cancer Facts and figures. January 9th 2019. Google Scholar
Maris, JM, Hogarty, MD, Bagatell, R, et al. Neuroblastoma Lancet 2007; 369 (9579), 2106–2120. doi: 10.1016/S0140–6736(07)60983–0. PMID: 17586306.CrossRefGoogle Scholar
Castel, V, Segura, V, Berlanga, P. Emerging drugs for neuroblastoma. Exp Opin Emer Drugs 2013; 18 (2), 155–171. doi: 10.1517/14728214.2013.796927.CrossRefGoogle ScholarPubMed
Schmidt, ML, Lukens, JN, Seeger, RC, et al. Biologic factors determine prognosis in infants with stage IV neuroblastoma: a prospective Children’s Cancer Group study. J Clin Oncol 2000; 18, 1260–1268. doi: 10.1097/01.mop.0000150631.60571.89.CrossRefGoogle ScholarPubMed
Brodeur, GM. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 2003; 3 (3), 203–216. doi: 10.1038/nrc1014. PMID:12612655.CrossRefGoogle ScholarPubMed
Brodeur, GM, Bagatell, R. Mechanisms of neuroblastoma regression. Nat Rev Clin Oncol 2014; 11, 704–713. doi: 10.1038/nrclinonc.2014.168.CrossRefGoogle ScholarPubMed
Hero, B, Simon, T, Spiz, R, et al. Localized infant neuroblastomas often show spontaneous regression: results of the prospective trials NB95-S and NB97. J Clin Oncol 2008; 26, 1504–1510. doi: 10.1200/JCO.2007.12.3349.CrossRefGoogle ScholarPubMed
Fritsch, P, Kerbl, R, Lackner, H, et al. ‘Wait and see’ strategy in localized neuroblastoma in infants: an option not only for cases detected by mass screening. Pediatr Blood Cancer 2004; 43, 679–682. doi: 10.1002/pbc.20126.CrossRefGoogle Scholar
Mosse, YP, Laundenslager, M, Longo, L, et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008; 455, 930–935. doi: 10.1038/nature07261.CrossRefGoogle ScholarPubMed
Yáñez, Y, Grau, E, Oltra, S, et al. Minimal disease detection in peripheral blood and bone marrow from patients with non-metastatic neuroblastoma. J Cancer Res Clin Oncol 2001; 137, 1263–1272. doi: 10.1007/s00432-011-0997-x.CrossRefGoogle Scholar
Pinto, NR, Applebaum, MA, Volchenboum, SL, et al. Advances in risk classification and treatment strategies for neuroblastoma. J Clin Oncol 2015; 33, 3008–3017. doi: 10.1200/JCO.2014.59.4648.CrossRefGoogle ScholarPubMed
Monclair, T, Brodeur, GM, Ambros, PF, et al. The International Neuroblastoma Risk Group (INRG) staging system: an INRG Task Force report. J Clin Oncol 2009; 27 (2), 298–303. doi: 10.1200/JCO.2008.16.6876.CrossRefGoogle ScholarPubMed
Cohn, SL, Pearson, AD, London, WB, et al. The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol 2009; 27, 289–297. doi: 10.1200/JCO.2008.16.6785.CrossRefGoogle ScholarPubMed
Shimada, H, Umehara, S, Monobe, Y, et al. International neuroblastoma pathology classification for prognostic evaluation of patients with peripheral neuroblastic tumors: A report from the Children’s Cancer Group. Cancer. 2001; 92 (9), 2451–2461. doi: 10.1002/1097-0142(20011101)92:9 <2451:aid-cncr1595>3.0.co;2-s.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Look, AT, Hayes, FA, Shuster, JJ, et al. Clinical relevance of tumor cell ploidy and N-myc gene amplification in childhood neuroblastoma: a Pediatric Oncology Group study. J Clin Oncol 1991; 9 (4), 581–591. doi: 10.1200/JCO.1991.9.4.581.CrossRefGoogle ScholarPubMed
Jiang, M, Stanke, J, Lahti, JM. The connections between neural crest development and neuroblastoma. In: Michael, AD (ed.) Current Topics in Developmental Biology. 2011; 94, 77–127. doi: 10.1016/B978-0-12-380916-2.00004-8.CrossRefGoogle Scholar
Cheung, NK, Dyer, MA. Neuroblastoma: developmental biology, cancer genomics and immunotherapy. Nat Rev Cancer 2013; 13, 397–411. doi: 10.1038/nrc3526.CrossRefGoogle ScholarPubMed
Maris, JM. Recent advances in neuroblastoma. N Engl J Med 2010; 362 (23), 2202–2211. doi: 10.1056/NEJMra0804577.CrossRefGoogle ScholarPubMed
Ambros, PF, Ambros, IM, Brodeur, GM, et al. International consensus for neuroblastoma molecular diagnostics: report from the International Neuroblastoma Risk Group (INRG) Biology Committee. Br J Cancer 2009; 100, 1471–1482. doi: 10.1038/sj.bjc.6605014.CrossRefGoogle ScholarPubMed
Osei, E, Lumini, J, Gunasekara, D, et al. A review of predictive, prognostic and diagnostic biomarkers for non-small-cell lung cancer: towards personalised and targeted cancer therapy. J Radiother Pract 2019; 1–15. doi: 10.1017/S1460396919000876.Google Scholar
Osei, E, Walters, P, Masella, O, et al. A review of predictive, prognostic and diagnostic biomarkers for brain tumors: towards personalised and targeted cancer therapy. J Radiother Pract Accepted for publication 2019.CrossRefGoogle Scholar
Utnes, P, Løkke, , C, Flægstad, , T, et al. Clinically relevant biomarker discovery in high-risk recurrent neuroblastoma. Cancer Inform 2019; 18. doi: 10.1177/1176935119832910.CrossRefGoogle ScholarPubMed
Goossens, N, Nakagawa, , S, Sun, X, et al. Cancer biomarker discovery and validation. Transl Cancer Res 2015; 4 (3), 256–269. doi: 10.3978/j.issn.2218.-676X.2015.06.04.PMID:26213686.Google Scholar
World Health Organization & International Programme on Chemical Safety. 2001. Biomarkers in risk assessment: validity and validation. The World Health Organization. https://apps.who.int/iris/handle/10665/42363 Google Scholar
Sawyers, CL. The cancer biomarker problem. Nature. 2008; 452 (7187), 548–552. doi: 10.1038/nature06913. PMID: 18385728.CrossRefGoogle ScholarPubMed
Paik, S, Shak, S, Tang, G, et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 2004; 351 (27), 2817–2826. PMID: 15591335. doi: 10.1056/NEJMoa041588.CrossRefGoogle ScholarPubMed
He, WG, Yan, Y, Tang, W, et al. Clinical and biological features of neuroblastic tumors: a comparison of neuroblastoma and ganglioneuroblastoma. Oncotarget 2017; 8 (23), 37730.CrossRefGoogle ScholarPubMed
Singal, AK, Agarwala, S. Tumour markers in pediatric solid tumours. J Indian Assoc Pediatr Surg 2005; 10 (3), 183–190.Google Scholar
Crowley, E, Di Nicolantonio, F, Loupakis, F, et al. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol 2013; 10 (8), 472–484. doi: 10.1038/nrclinonc.2013.110. PMID: 23836314.CrossRefGoogle ScholarPubMed
Tadimety, A, Closson, A, Li, C, et al. Advances in liquid biopsy on-chip for cancer management: technologies, biomarkers, and clinical analysis. Crit Rev Clin Lab Sci 2018; 55 (3), 140–162. doi: 10.1080/10408363.2018.1425976. PMID: 29388456. PMCID: PMC6101655.CrossRefGoogle ScholarPubMed
Wan, JCM, Massie, C, Garcia-Corbacho, J, et al. Liquid biopsies come of age: towards implementation of circulating tumour DNA. Nat Rev Cancer 2017; 17 (4), 223–238. doi: 10.1038/nrc.2017.7. PMID: 28233803.CrossRefGoogle ScholarPubMed
Siravegna, G, Marsoni, S, Siena, S, et al. Integrating liquid biopsies into the management of cancer. Nat Rev Clin Oncol 2017; 14 (9), 531–548. doi: 10.1038/nrclinonc.2017.14. PMID: 28252003.CrossRefGoogle ScholarPubMed
Hao, N, Zhang, JXJ. Microfluidic screening of circulating tumor biomarkers toward liquid biopsy. Sep Purif Rev 2018; 47 (1), 1–30.CrossRefGoogle Scholar
Chen, X, Ba, Y, Ma, L, et al. Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 2008; 18 (10), 997–1006. doi: 10.1038/cr.2008.282. PMID: 18766170.CrossRefGoogle ScholarPubMed
Sausen, M, Parpart, S, Diaz, LA. Circulating tumor DNA moves further into the spotlight. Genome Med 2014; 6 (5), 35. 2014 May 28. doi: 10.1186/gm552. PMCID: PMC4062042. PMID: 24944584.CrossRefGoogle ScholarPubMed
Abbou, SD, Shulman, DS, DuBois, SG, et al. Assessment of circulating tumor DNA in pediatric solid tumors: the promise of liquid biopsies. Pediatr Blood Cancer 2019; 66 (5), e27595. doi: 10.1002/pbc.27595. Epub 2019 Jan 6. PMID: 30614191; PMCID: PMC6550461.CrossRefGoogle ScholarPubMed
Perakis, S, Speicher, MR. Emerging concepts in liquid biopsies. BMC Med 2017; 15, 75. doi: 10.1186/s12916-017-0840-6.CrossRefGoogle ScholarPubMed
Jahr, S, Hentze, H, Englisch, S, et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res 2001; 61 (4), 1659–1665. PMID: 11245480.Google ScholarPubMed
Liu, R, Cao, J, Gao, X, et al. Overall survival of cancer patients with serum lactate dehydrogenase greater than 1000 IU/L. Tumor Biol 2016; 37 (10), 14083–14088. doi: 10.1007/s13277-016-5228-2.CrossRefGoogle ScholarPubMed
Petrelli, F, Cabiddu, M, Coinu, A, et al. Prognostic role of lactate dehydrogenase in solid tumors: a systematic review and meta-analysis of 76 studies. Acta Oncolog 2015; 54 (7), 961–970. doi: 10.3109/0284186X.2015.1043026.CrossRefGoogle ScholarPubMed
Wulaningsih, W, Holmberg, L, Garmo, H, et al. Serum lactate dehydrogenase and survival following cancer diagnosis. Br J Cancer 2015; 113 (9), 1389–1396. doi: 10.1038/bjc.2015.361.CrossRefGoogle ScholarPubMed
Morgenstern, DA, London, WB, Stephens, D, et al. Prognostic significance of pattern and burden of metastatic disease in patients with stage 4 neuroblastoma: a study from the International Neuroblastoma Risk Group database. Eur J Cancer 2016; 65, 1–10. doi: 10.1016/j.ejca.2016.06.005. PMID: 27434878.CrossRefGoogle ScholarPubMed
Shuster, JJ, McWilliams, NB, Castleberry, R, et al. Serum lactate dehydrogenase in childhood neuroblastoma. A Pediatric Oncology Group recursive partitioning study. Amer J Clin Oncol 1992; 15, 295–303. doi: 10.1097/00000421-199208000-00004.CrossRefGoogle ScholarPubMed
Cangemi, G et al. Prognostic value of ferritin, neuron-specific enolase, lactate dehydrogenase, and urinary and plasmatic catecholamine metabolites in children with neuroblastoma. Onco Targets Ther 2012; 5, 417–423. doi: 10.2147/OTT.S36366.Google ScholarPubMed
Morgenstern, DA, Potschger, U, Moreno, L, et al. Risk stratification of high-risk metastatic neuroblastoma: a report from the HR-NBL-1/SIOPEN study. Pediatr Blood Cancer 2018; 65 (11), e27363. doi: 10.1002/pbc.27363.CrossRefGoogle ScholarPubMed
Hann, HW, Levy, HM, Evans, AE. Serum ferritin as a guide to therapy in neuroblastoma. Cancer Res 1980; 40 (5), 1411–1413. PMID: 6245792.Google ScholarPubMed
Hann, HW, Evans, AE, Cohen, IJ, et al. Biologic differences between neuroblastoma stages IV-S and IV: measurement of serum ferritin and E-rosette inhibition in 30 children. N Engl J Med 1981; 305, 425–429. doi: 10.1056/NEJM198108203050803.CrossRefGoogle ScholarPubMed
Meany, HJ, London, WB, Ambros, PF, et al. Significance of clinical and biologic features in stage 3 neuroblastoma: a report from the International Neuroblastoma Risk Group project. Pediatr Blood Cancer. 2014; 61, 1932–1939. doi: 10.1002/pbc.25134.CrossRefGoogle ScholarPubMed
Hann, HW, Stahlhut, MW, Evans, AE. Source of increased ferritin in neuroblastoma: studies with concanavalin A-sepharose binding. J Nat Cancer Inst 1986; 76, 1031–1033. PMID: 3986811.Google ScholarPubMed
Hann, HW, Evans, AE, Siegel, SE, et al. Prognostic importance of serum ferritin in patients with stages III and IV neuroblastoma: the childrens cancer study group experience. Cancer Res 1985; 45, 2843–2848. PMID: 3986811.Google ScholarPubMed
Isgro, MA, Bottoni, P, Scatena, R. 2015. Neuron-specific enolase as a biomarker: biochemical and clinical aspects. Adv Exp Med Biol 2015; 867, 125–143. doi: 10.1007/978-94-017-7215-0_9.CrossRefGoogle ScholarPubMed
Zeltzer, PM, Marangos, PJ, Parma, AM, et al. Raised neuron-specific enolase in serum of children with metastatic neuroblastoma: a report from the Children’s Cancer Study Group. Lancet 1983; 2, 361–363. doi 10.1016/S0140-6736(83)90342-2.CrossRefGoogle ScholarPubMed
Tsuchida, Y, Honna, T, Iwanaka, T, et al. Serial determination of serum neuron-specific enolase in patients with neuroblastoma and other pediatric tumors. J Pediatr Surg 1987; 22 (5), 419–424. doi: 10.1016/s0022-3468(87)80261-0.CrossRefGoogle ScholarPubMed
Massaron, S, Seregni, E, Luksch, R, et al. Neuron-specific enolase evaluation in patients with neuroblastoma. Tumour Biol 1998; 19 (4), 261–268. doi: 10.1159/000030016.CrossRefGoogle ScholarPubMed
Kintzel, K, Sonntag, J, Strauss, E, et al. Neuron specific enolase: reference values in cord blood. Clin Chem Lab Med 1998; 36 (4), 245–247. doi: 10.1515/CCLM.1998.042.CrossRefGoogle ScholarPubMed
Riley, RD, Heney, D, Jones, DR et al. A systematic review of molecular and biological tumor markers in neuroblastoma. Clin Cancer Res 2004; 10 (1 Pt 1), 4–12. doi: 10.1158/1078-0432.ccr-1051-2.CrossRefGoogle ScholarPubMed
Zeltzer, PM, Marangos, PJ, Evans, AE, et al. Serum neuron-specific enolase in children with neuroblastoma. Relationship to stage and disease course Cancer 1986; 57 (6), 1230–1234. doi: 10.1002/1097-0142(19860315)57:6<1230:aid-cncr 2820570628>3.0.co;2-#.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Berthold, F, Engelhardt-Fahrner, U, Schneider, A, et al. Age dependence and prognostic impact of neuron specific enolase (NSE) in children with Neuroblastoma. In Vivo 1991; 5 (3), 245–247. PMID: 1893081.Google ScholarPubMed
Schilling, FH, Spix, C, Berthold, F, et al. Neuroblastoma screening at one year of age. N Engl J Med 2002; 346, 1047–1053. doi: 10.1056/NEJMoa012277.CrossRefGoogle ScholarPubMed
Bond, JV. Clinical significance of catecholamine excretion levels in diagnosis and treatment of neuroblastoma. Arch Dis Childhood 1975; 50, 691–695. doi: 10.1136/adc.50.9.691.CrossRefGoogle ScholarPubMed
LaBrosse, EH, Com-Nougue, C, Zucker, JM, et al. Urinary excretion of 3-methoxy-4-hydroxymandelic acid and 3-methoxy-4-hydroxyphenylacetic acid by 288 patients with neuroblastoma and related neural crest tumors. Cancer Res 1980; 40 (6), 1995–2001. PMID: 7371035.Google ScholarPubMed
Strenger, V, Kerbl, R, Dornbusch, HJ, et al. Diagnostic and prognostic impact of urinary catecholamines in neuroblastoma patients. Pediatr Blood Cancer 2007; 48, 504–509. doi: 10.1002/pbc.20888.CrossRefGoogle ScholarPubMed
Tsubono, Y, Hisamichi, S. A halt to neuroblastoma screening in Japan. N Engl J Med 2004; 350, 2010–2011. doi: 10.1056/NEJM200405063501922.CrossRefGoogle ScholarPubMed
Laug, WE, Siegel, SE, Shaw, KN, et al. Initial urinary catecholamine metabolite concentrations and prognosis in neuroblastoma. Pediatrics 1978; 62, 77–83. doi: 10.1203/00006450–197610000–00158.Google ScholarPubMed
Woods, WG, Gao, RN, Shuster, JJ, et al. Screening of infants and mortality due to neuroblastoma. N Engl J Med 2002; 346, 1041–1046. doi: 10.1056/NEJMoa012387.CrossRefGoogle ScholarPubMed
Berthold, F, Hunneman, DH, Harms, D, et al. Serum vanillylmandelic acid/homovanillic acid contributes to prognosis estimation in patients with localised but not with metastatic neuroblastoma. Eur J Cancer 1992; 28A: 1950–1954. doi: 10.1016/0959-8049(92)90234-s.CrossRefGoogle Scholar
Bettegowda, C, Sausen, M, Leary, RJ, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 2014; 6, 224ra224. doi: 10.1126/scitranslmed.3007094.CrossRefGoogle ScholarPubMed
Trigg, RM, Martinson, LJ, Parpart-Li, S, et al. Factors that influence quality and yield of circulating-free DNA: a systematic review of the methodology literature. Heliyon. 2018; 4, e00699. doi: 10.1016/j.heliyon.2018.e00699.CrossRefGoogle ScholarPubMed
Combaret, V, Hogarty, MD, London, WB, et al. Influence of neuroblastoma stage on serum-based detection of MYCN amplification. Pediatr Blood Cancer 2009; 53, 329–331.CrossRefGoogle ScholarPubMed
Chicard, M, Colmet-Daage, L, Clement, N, et al. Whole-exome sequencing of cell-free DNA reveals temporo-spatial heterogeneity and identifies treatment-resistant clones in neuroblastoma. Clin Cancer Res 2018; 24, 939–949. doi: 10.1158/1078-0432.CCR-17-1586.CrossRefGoogle ScholarPubMed
Janoueix-Lerosey, I, Schleiermacher, G, Michels, E, et al. Overall genomic pattern is a predictor of outcome in neuroblastoma. J Clin Oncol 2009; 27 (7), 1026–1033.CrossRefGoogle ScholarPubMed
Kurihara, S, Ueda, Y, Onitake, Y, et al. Circulating free DNA as non-invasive diagnostic biomarker for childhood solid tumors. J Pediatr Surg 2015; 50, 2094–2097. doi: 10.1016/j.jpedsurg.2015.08.033.CrossRefGoogle ScholarPubMed
Chicard, M, Boyault, S, Daage, LC, et al. Genomic copy number profiling using circulating free tumor DNA highlights heterogeneity in neuroblastoma. Clin Cancer Res 2016; 22, 5564–5573. doi: 10.1158/1078-0432.CCR-16-0500.CrossRefGoogle ScholarPubMed
Okubo, T, Knoepfler, PS, Eisenman, RN, et al. Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 2005; 132, 1363–1374. doi: 10.1242/dev.01678.CrossRefGoogle ScholarPubMed
Kaczówka, P, Wieczorek, A, Czogała, M, et al. The role of N-Myc gene amplification in neuroblastoma childhood tumour – single-centre experience. Contemp Oncol 2018; 22 (4), 223–228. doi: 10.5114/wo.2018.81402.Google ScholarPubMed
Pezzolo, A, Rossi, E, Gimelli, S, et al. Presence of 1q gain and absence of 7p gain are new predictors of local or metastatic relapse in localized resectable neuroblastoma. Neuro-Oncol 2009; 11 (2), 192–200. doi: 10.1215/15228517-2008-086.CrossRefGoogle ScholarPubMed
Van Roy, N, Van Der Linden, M, Menten, B, et al. Shallow whole genome sequencing on circulating cell-free DNA allows reliable noninvasive copy-number profiling in neuroblastoma patients. Clin Cancer Res 2017; 23, 6305–6314. doi: 10.1158/1078-0432.CCR-17-0675.CrossRefGoogle ScholarPubMed
Su, Y, Wang, L, Wang, X, et al. Dynamic alterations of plasma cell free DNA in response to chemotherapy in children with neuroblastoma. Cancer Med 2019; 8 (4), 1558–1566.CrossRefGoogle ScholarPubMed
Kojima, M, Hiyama, E, Fukuba, I, et al. Detection of MYCN amplification using blood plasma: noninvasive therapy evaluation and prediction of prognosis in neuroblastoma. Pediatr Surg Int 2013; 29, 1139–1145. doi: 10.1007/s00383-013-3374-9.CrossRefGoogle ScholarPubMed
Yagyu, S, Iehara, T, Tanaka, S, et al. Serum-based quantification of MYCN gene amplification in young patients with neuroblastoma: potential utility as a surrogate biomarker for neuroblastoma. PLoS One 2016; 11, e0161039. doi: 10.1371/journal.pone.0161039.CrossRefGoogle ScholarPubMed
Ma, Y, Lee, JW, Park, SJ, et al. Detection of MYCN amplification in serum DNA using conventional polymerase chain reaction. J Korean Med Sci 2016; 31, 1392–1396. doi: 10.3346/jkms.2016.31.9.1392.CrossRefGoogle ScholarPubMed
De Bernardi, B, Gerrard, M, Boni, L, et al. Excellent outcome with reduced treatment for infants with disseminated neuroblastoma without MYCN gene amplification. J Clin Oncol 2009; 27 (7), 1034–1040. doi: 10.1200/JCO.2008.17.5877. Epub 2009 Jan 26.CrossRefGoogle ScholarPubMed
George, RE, London, WB, Cohn, SL, et al. Hyperdiploidy plus nonamplified MYCN confers a favorable prognosis in children 12 to 18 months old with disseminated neuroblastoma: a pediatric oncology group study. J Clin Oncol 2005; 23, 6466–6473. doi: 10.1200/JCO.2005.05.582.CrossRefGoogle ScholarPubMed
Combaret, V, Audoynaud, C, Iacono, I, et al. Circulating MYCN DNA predicts MYCN-amplification in neuroblastoma. J Clin Oncol 2005; 23, 8919–8920. doi: 10.1200/JCO.2005.04.0170.CrossRefGoogle ScholarPubMed
Schneiderman, J, London, WB, Brodeur, GM, et al. Clinical significance of MYCN amplification and ploidy in favorable-stage neuroblastoma: a report from the children’s oncology group. J Clin Oncol 2008; 26, 913–918. doi: 10.1200/JCO.2007.13.9493.Google Scholar
Lee, JW, Son, MH, Cho, HW, et al. Clinical significance of MYCN amplification in patients with high-risk neuroblastoma. Pediatr Blood Cancer 2018; 65 (10), e27257. doi: 10.1002/pbc.27257. Epub 2018 May 24.CrossRefGoogle ScholarPubMed
Marrano, P, Irwin, MS, Thorner, PS. Heterogeneity of MYCN amplification in neuroblastoma at diagnosis, treatment, relapse, and metastasis. Gene Chromosome Cancer 2017; 56 (1), 28–41. doi: 10.1002/gcc.22398.CrossRefGoogle Scholar
Lodrini, M, Sprussel, A, Astrahantseff, K et al. Using droplet digital PCR to analyze MYCN and ALK copy number in plasma from patients with neuroblastoma. Oncotarget 2017; 8, 85 234–85 251. doi: 10.18632/oncotarget.19076.CrossRefGoogle ScholarPubMed
Combaret, V, Audoynaud, C, Iacono, I, et al. Circulating MYCN DNA as a tumor-specific marker in neuroblastoma patients. Cancer Research. 2002; 62 (13), 3646–3648.Google ScholarPubMed
Yagyu, S, Iehara, T, Gotoh, T, et al. Preoperative analysis of 11q loss using circulating tumor-released DNA in serum: a novel diagnostic tool for therapy stratification of neuroblastoma. Cancer Lett 2011; 309, 185–189. doi: 10.1016/j.canlet.2011.05.032.CrossRefGoogle ScholarPubMed
Combaret, V, Brejon, S, Iacono, I, et al. Determination of 17q gain in patients with neuroblastoma by analysis of circulating DNA. Pediatr Blood Cancer 2011; 56, 757–761. doi: 10.1002/pbc.22816.CrossRefGoogle ScholarPubMed
Schleiermacher, G, Mosseri, V, London, WB, et al. Segmental chromosomal alterations have prognostic impact in neuroblastoma: a report from the INRG project. Br J Cancer 2012; 107, 1418–1422. doi: 10.1038/bjc.2012.375.CrossRefGoogle ScholarPubMed
George, RE, Attiyeh, EF, Li, S, et al. Genome-wide analysis of neuroblastomas using high-density single nucleotide polymorphism arrays. PLoS One 2007; 2, e255. doi: 10.1371/journal.pone.0000255.CrossRefGoogle ScholarPubMed
Wang, M, Zhou, C, Sun, Q, et al. ALK amplification and protein expression predict inferior prognosis in neuroblastomas. Exp Mol Pathol 2013; 95 (2), 124–130. doi: 10.1016/j.yexmp.CrossRefGoogle ScholarPubMed
Janoueix-Lerosey, I, Lequin, D, Brugieres, L, et al. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 2008; 455, 967–970. doi: 10.1038/nature07398.CrossRefGoogle ScholarPubMed
Combaret, V, Iacono, I, Bellini, A, et al. Detection of tumor ALK status in neuroblastoma patients using peripheral blood. Cancer Med 2015; 4, 540–550. doi: 10.1002/cam4.414.CrossRefGoogle ScholarPubMed
Trigg, RM, Shaw, JA, Turner, SD. Opportunities and challenges of circulating biomarkers in neuroblastoma. Open Biol 2019; 9 (5), 190056.CrossRefGoogle ScholarPubMed
De Brouwer, S, De Preter, K, Kumps, C, et al. Meta-analysis of neuroblastomas reveals a skewed ALK mutation spectrum in tumors with MYCN amplification. Clin Cancer Res 2010; 16, 4353–4362. doi: 10.1158/1078–0432.CCR-09–2660.CrossRefGoogle ScholarPubMed
Trigg, RM, Turner, SD. ALK in neuroblastoma: biological and therapeutic implications. Cancer 2018; 10, 113. doi: 10.3390/cancers10040113.CrossRefGoogle ScholarPubMed
Gorgannezhad, L, Umer, M, Islam, MN, et al. Circulating tumor DNA and liquid biopsy: opportunities, challenges, and recent advances in detection technologies. Lab on a Chip. 2018; 18 (8), 1174–1196. doi: 10.1039/C8LC00100F. PMID: 29569666.CrossRefGoogle ScholarPubMed
Jiang, P, Chan Cw, Chan KA, et al. Lengthening and shortening of plasma DNA in hepatocellular carcinoma patients. Proceedings of the National Academy of Sciences. 2015; 112, E1317–E1325. doi: 10.1073/pnas.1500076112.CrossRefGoogle ScholarPubMed
Klega, K, Imamovic-Tuco, A, Ha, G, et al. Detection of somatic structural variants enables quantification and characterization of circulating tumor DNA in children with solid tumors. JCO Precis Oncol 2018; 2, 1–13. doi: 10.1200/PO.17.00285.Google Scholar
Phallen, J, Sausen, M, Adleff, V, et al. Direct detection of early-stage cancers using circulating tumor DNA. Sci Transl Med 2017; 9 (403), pii: eaan2415. doi: 10.1126/scitranslmed.aan2415. PMID: 28814544. PMCID: PMC6714979.CrossRefGoogle ScholarPubMed
Gotoh, T, Hosoi, H, Iehara, T, et al. Prediction of MYCN amplification in neuroblastoma using serum DNA and real-time quantitative polymerase chain reaction. J Clin Oncol 2005; 23, 5205–5210. doi: 10.1200/JCO.2005.02.014.CrossRefGoogle ScholarPubMed
Yagyu, S, Gotoh, T, Iehara, T, et al. Circulating methylated-DCR2 gene in serum as an indicator of prognosis and therapeutic efficacy in patients with MYCN non amplified neuroblastoma. Clin Cancer Res 2008; 14, 7011–7019. doi: 10.1158/1078-0432.CCR-08-1249.CrossRefGoogle Scholar
Bosse, KR, Buongervino, S, Lane, M, et al. Serial profiling of ctDNA identifies clinically actionable genomic evolution in high-risk neuroblastoma. Proceedings: AACR Annual Meeting 2019; March 29–April 3, 2019, Atlanta, GA.CrossRefGoogle Scholar
Misawa, A, Tanaka, S, Yagyu, S, et al. RASSF1A hypermethylation in pretreatment serum DNA of neuroblastoma patients: a prognostic marker. Br J Cancer 2009; 100, 399–404. doi: 10.1038/sj.bjc.6604887.CrossRefGoogle ScholarPubMed
Sun, K, Jiang, P, Chan, KC, et al. Plasma DNA tissue mapping by genome-wide methylation sequencing for noninvasive prenatal, cancer, and transplantation assessments. Proc Natl Acad Sci U S A 2015; 112, E5503–E5512. doi: 10.1073/pnas.1508736112. Epub: 2015 Sep 21.CrossRefGoogle ScholarPubMed
Man, Y, Wang, Q, Kemmner, W. Currently used markers for CTC isolation – advantages, limitations and impact on cancer prognosis. J Clin Exp Pathol 2011; 1 (1), 1–7. doi: 10.4172/2161-0681.1000102.CrossRefGoogle Scholar
Joosse, SA, Gorges, TM, Pantel, K. Biology, Detection, and clinical implications of circulating tumor cells. EMBO Mol Med 2015; 7, 1–11. doi: 10.15252/emmm.201303698.CrossRefGoogle ScholarPubMed
Ferreira, MM, Ramani, VC,Jeffrey, SS. Circulating tumor cell technologies. Mol Oncol 2016; 10 (3), 374–394. doi: 10.1016/j.molonc.2016.01.007. PMID: 26897752. PMCID: PMC5528969.CrossRefGoogle ScholarPubMed
Liu, X, Zhang, Z, Zhang, B, et al. Circulating tumor cells detection in neuroblastoma patients by EpCAM-independent enrichment and immunostaining-fluorescence in situ hybridization. EBioMedicine. 2018; 35, 244–250. doi: 10.1016/j.ebiom.2018.08.005.CrossRefGoogle ScholarPubMed
Kurodaa, T, Morikawaa, N, Matsuoka, K, et al. Prognostic significance of circulating tumor cells and bone marrow micrometastasis in advanced neuroblastoma. J Pediatr Surg 2008; 43 (12), 2182–2185. doi: 10.1016/j.jpedsurg.2008.08.046.CrossRefGoogle Scholar
Zaporozhchenko, IA, Ponomaryova, AA, Rykova, EY, et al. The potential of circulating cell-free RNA as a cancer biomarker: challenges and opportunities. Exp Rev Mol Diagn 2018; 18 (2), 133–145.CrossRefGoogle ScholarPubMed
Feng, H, Qin, Z, Zhang, X. Opportunities and methods for studying alternative splicing in cancer with RNA-Seq. Cancer Lett. 2013; 340, 179–191.CrossRefGoogle ScholarPubMed
Zhou, D, Tang, W, Liu, X, et al. Clinical verification of plasma messenger RNA as novel noninvasive biomarker identified through bioinformatics analysis for lung cancer. Oncotarget. 2017; 8 (27), 43978–43989. doi: 10.18632/oncotarget.16701. PMID: 28410204.; PMCID: PMC5546455.CrossRefGoogle ScholarPubMed
Träger, C, Kogner, P, Lindskog, M, et al. Quantitative analysis of tyrosine hydroxylase mRNA for sensitive detection of neuroblastoma cells in blood and bone marrow. Clin Chem 2003; 49, 104–112. doi: 10.1373/49.1.104.CrossRefGoogle ScholarPubMed
Lee, NH, Son, MH, Choi, YB, et al. Clinical significance of tyrosine hydroxylase mRNA transcripts in peripheral blood at diagnosis in patients with neuroblastoma. Cancer Research and. Treatment. 2016; 48, 1399–1407. doi: 10.4143/crt.2015.481.CrossRefGoogle ScholarPubMed
Viprey, VF, Gregory, W, Corrias, MV, et al. Neuroblastoma mRNAs predict outcome in children with stage 4 neuroblastoma: a European HR-NBL1/SIOPEN Study. J Clin Oncol 2014; 32, 1074–1083. doi: 10.1200/Jco.2013.53.3604.CrossRefGoogle ScholarPubMed
Burchill, SA, Lewis, IJ, Abrams, KR, et al. Circulating neuroblastoma cells detected by reverse transcriptase polymerase chain reaction for tyrosine hydroxylase mRNA are an independent poor prognostic indicator in stage 4 neuroblastoma in children over 1 year. J Clin Oncol 2001; 19, 1795–1801. doi: 10.1200/JCO.2001.19.6.1795.CrossRefGoogle ScholarPubMed
Marachelian, A, Villablanca, JG, Liu, CW, et al. Expression of five neuroblastoma genes in bone marrow or blood of patients with relapsed/refractory neuroblastoma provides a new biomarker for disease and prognosis. Clin Cancer Res 2017; 23, 5374–5383. doi: 10.1158/1078-0432.Ccr-16-2647.CrossRefGoogle ScholarPubMed
Corrias, MV, Haupt, R, Carlini, B, et al. Multiple target molecular monitoring of bone marrow and peripheral blood samples from patients with localized neuroblastoma and healthy donors. Pediatr Blood Cancer 2012; 58, 43–49. doi: 10.1002/pbc.22960.CrossRefGoogle ScholarPubMed
Cheung, IY, Sahota, A, Cheung, NK. Measuring circulating neuroblastoma cells by quantitative reverse transcriptase–polymerase chain reaction analysis: correlation with its paired bone marrow and standard disease markers. Cancer. Interdisciplinary International Journal of the American Cancer Society 2004; 101 (10), 2303–2308.CrossRefGoogle Scholar
Burchill, SA, Lewis, IJ, Abrams, KR, et al. Circulating neuroblastoma cells detected by reverse transcriptase polymerase chain reaction for tyrosine hydroxylase mRNA are an independent poor prognostic indicator in stage 4 neuroblastoma in children over 1 year. J Clin Oncol 2001 19 (6), 1795–1801.CrossRefGoogle ScholarPubMed
Mitchell, PS, Parkin, RK, Kroh, EM,et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Nat Acad Sci 2008; 105 (30), 10513–10518. doi: 10.1073/pnas.0804549105. PMID: 18663219. PMCID: PMC2492472.CrossRefGoogle ScholarPubMed
Murray, MJ, Raby, KL, Saini, HK, et al. Solid tumors of childhood display specific serum microRNA profiles. Cancer Epidemiol Prev Biomarkers. 2015; 24, 350–360. doi: 10.1158/1055-9965.EPI-14-0669.CrossRefGoogle ScholarPubMed
O’Brien, KP, Ramphul, E, Howard, L, et al. Circulating microRNAs in cancer. Methods Mol Biol 1509, 123–139. doi: 10.1007/978-1-4939-6524-3_12.CrossRefGoogle Scholar
Galardi, A, Colletti, M, Businaro, P, et al. MicroRNAs in neuroblastoma: biomarkers with therapeutic potential. Curr Med Chem 2018; 25, 584–600. doi: 10.2174/0929867324666171003120335.CrossRefGoogle ScholarPubMed
Peng, Y, Croce, CM. The role of microRNAs in human cancer. Signal Transduction and Target Therapy. 2016; 1, 15004. doi: 10.1038/sigtrans.2015.4.CrossRefGoogle ScholarPubMed
Chen, Y, Stallings, RL. Differential patterns of microRNA expression in neuroblastoma are correlated with prognosis, differentiation, and apoptosis. Cancer Research. 2007; 67, 976–983. doi: 10.1158/0008-5472.CAN-06-3667.CrossRefGoogle Scholar
Zeka, F, Decock, A, Can Goethem, A, et al. Circulating microRNA biomarkers for metastatic disease in neuroblastoma patients. JCI Insight. 2018; 3, 97021. doi: 10.1172/jci.insight.97021.CrossRefGoogle ScholarPubMed
Ramraj, SK, Aravindan, S, Somasundaram, DB, et al. Serum-circulating miRNAs predict neuroblastoma progression in a mouse model of high-risk metastatic disease. Oncotarget 2016; 7, 18 605–18 619. doi: 10.18632/oncotarget.7615.CrossRefGoogle Scholar
Ma, R, Jiang, T, Kang, X. Circulating microRNAs in cancer: origin, function and application. J Exp Clin Cancer Res 2012; 31 (1), 38.CrossRefGoogle ScholarPubMed
Ashworth, TR. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Aust Med J 1869; 14, 146–147.Google Scholar