Long-term follow-up of high-risk neuroblastoma survivors treated with high-dose chemotherapy and stem cell transplantation rescue.
Journal
Bone marrow transplantation
ISSN: 1476-5365
Titre abrégé: Bone Marrow Transplant
Pays: England
ID NLM: 8702459
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
received:
20
09
2020
accepted:
23
02
2021
revised:
08
02
2021
pubmed:
8
4
2021
medline:
14
10
2021
entrez:
7
4
2021
Statut:
ppublish
Résumé
Intensive treatments including high-dose chemotherapy (HDC) with autologous stem cell rescue have improved high-risk neuroblastoma (HRNB) survival. We report the long-term health status of 145 HRNB survivors, alive and disease-free 5 years post HDC. Median follow-up was 15 years (range = 5-34). Six patients experienced late relapses, 11 developed second malignant neoplasms (SMNs), and 9 died. Event-free and overall survivals 20 years post HDC were 82% (95% CI = 70%-90%) and 89% (78%-95%), respectively. Compared with the French general population, the standardized mortality ratio was 19 (95% CI = 8.7-36.1; p < 0.0001) and the absolute excess risk was 37.6 (19.2-73.5). Late effects were observed in 135/145 patients (median = 3 events/patient); 103 had at least one severe event. SMNs arose at a median of 20 years post HDC and included carcinoma (n = 5), sarcoma (2), acute myeloid leukemia (2), melanoma (1), and malignant glioma (1). Non-oncologic health events included dental maldevelopment (60%), severe hearing loss (20% cumulative probability at 15 years), hepatic focal nodular hyperplasia (14%), thyroid (11%), cardiac (8%), and renal (7%) diseases and growth retardation (height-for-age z-score ≤ -2 for 21%). Gonadal insufficiency was near-universal after busulfan (40/43 females, 33/35 males). Severe late effects are frequent and progressive in HRNB survivors needing systematic very long-term follow-up.
Identifiants
pubmed: 33824435
doi: 10.1038/s41409-021-01258-1
pii: 10.1038/s41409-021-01258-1
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1984-1997Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Lacour B, Guyot-Goubin A, Guissou S, Bellec S, Desandes E, Clavel J. Incidence of childhood cancer in France: National Children Cancer Registries. Eur J Cancer Prev. 2010;19:173–81.
pubmed: 20361423
doi: 10.1097/CEJ.0b013e32833876c0
Cohn SL, Pearson ADJ, London WB, Monclair T, Ambros PF, Brodeur GM, et al. The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol. 2009;27:289–97.
pubmed: 19047291
pmcid: 2650388
doi: 10.1200/JCO.2008.16.6785
Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, Ramsay NK, et al. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children’s Cancer Group. N Engl J Med. 1999;341:1165–73.
pubmed: 10519894
doi: 10.1056/NEJM199910143411601
Matthay KK, Reynolds CP, Seeger RC, Shimada H, Adkins ES, Haas-Kogan D, et al. Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a children’s oncology group study. J Clin Oncol. 2009;27:1007–13.
pubmed: 19171716
pmcid: 2738615
doi: 10.1200/JCO.2007.13.8925
Berthold F, Boos J, Burdach S, Erttmann R, Henze G, Hermann J, et al. Myeloablative megatherapy with autologous stem-cell rescue versus oral maintenance chemotherapy as consolidation treatment in patients with high-risk neuroblastoma: a randomised controlled trial. Lancet Oncol. 2005;6:649–58.
pubmed: 16129365
doi: 10.1016/S1470-2045(05)70291-6
Pritchard J, Cotterill SJ, Germond SM, Imeson J, de Kraker J, Jones DR. High dose melphalan in the treatment of advanced neuroblastoma: results of a randomised trial (ENSG-1) by the European Neuroblastoma Study Group. Pediatr Blood Cancer. 2005;44:348–57.
pubmed: 15546135
doi: 10.1002/pbc.20219
Park JR, Kreissman SG, London WB, Naranjo A, Cohn SL, Hogarty MD, et al. Effect of tandem autologous stem cell transplant vs single transplant on event-free survival in patients with high-risk neuroblastoma: a randomized clinical trial. JAMA. 2019;322:746–55.
pubmed: 31454045
pmcid: 6714031
doi: 10.1001/jama.2019.11642
Ladenstein R, Pötschger U, Pearson ADJ, Brock P, Luksch R, Castel V, et al. Busulfan and melphalan versus carboplatin, etoposide, and melphalan as high-dose chemotherapy for high-risk neuroblastoma (HR-NBL1/SIOPEN): an international, randomised, multi-arm, open-label, phase 3 trial. Lancet Oncol. 2017;18:500–14.
pubmed: 28259608
doi: 10.1016/S1470-2045(17)30070-0
de Vathaire F, Hardiman C, Shamsaldin A, Campbell S, Grimaud E, Hawkins M, et al. Thyroid carcinomas after irradiation for a first cancer during childhood. Arch Intern Med. 1999;159:2713–9.
pubmed: 10597762
doi: 10.1001/archinte.159.22.2713
Veres C, Allodji RS, Llanas D, Vu Bezin J, Chavaudra J, Mège JP, et al. Retrospective reconstructions of active bone marrow dose-volume histograms. Int J Radiat Oncol Biol Phys. 2014;90:1216–24.
pubmed: 25442047
doi: 10.1016/j.ijrobp.2014.08.335
Demoor-Goldschmidt C, Allodji RS, Journy N, Rubino C, Zrafi WS, Debiche G, et al. Risk factors for small adult height in childhood cancer survivors. J Clin Oncol. 2020;38:1785–96.
Brock PR, Bellman SC, Yeomans EC, Pinkerton CR, Pritchard J. Cisplatin ototoxicity in children: a practical grading system. Med Pediatr Oncol. 1991;19:295–300.
pubmed: 2056973
doi: 10.1002/mpo.2950190415
Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958;53:457–81.
doi: 10.1080/01621459.1958.10501452
Rothman KJ. Estimation of confidence limits for the cumulative probability of survival in life table analysis. J Chronic Dis. 1978;31:557–60.
pubmed: 711848
doi: 10.1016/0021-9681(78)90043-7
Schemper M, Smith TL. A note on quantifying follow-up in studies of failure time. Control Clin Trials. 1996;17:343–6.
pubmed: 8889347
doi: 10.1016/0197-2456(96)00075-X
Breslow NE, Day NE. Statistical methods in cancer research. Volume II—the design and analysis of cohort studies. IARC Sci Publ. 1987;82:1–406.
Teepen JC, van Leeuwen FE, Tissing WJ, van Dulmen-den Broeder E, van den Heuvel-Eibrink MM, van der Pal HJ, et al. Long-term risk of subsequent malignant neoplasms after treatment of childhood cancer in the DCOG later study cohort: role of chemotherapy. J Clin Oncol. 2017;35:2288–98.
pubmed: 28530852
doi: 10.1200/JCO.2016.71.6902
Sanders JE, Hawley J, Levy W, Gooley T, Buckner CD, Deeg HJ, et al. Pregnancies following high-dose cyclophosphamide with or without high-dose busulfan or total-body irradiation and bone marrow transplantation. Blood. 1996;87:3045–52.
pubmed: 8639928
doi: 10.1182/blood.V87.7.3045.bloodjournal8773045
Teinturier C, Hartmann O, Valteau-Couanet D, Benhamou E, Bougneres PF. Ovarian function after autologous bone marrow transplantation in childhood: high-dose busulfan is a major cause of ovarian failure. Bone Marrow Transplant. 1998;22:989–94.
pubmed: 9849696
doi: 10.1038/sj.bmt.1701483
Thibaud E, Rodriguez-Macias K, Trivin C, Espérou H, Michon J, Brauner R. Ovarian function after bone marrow transplantation during childhood. Bone Marrow Transplant. 1998;21:287–90.
pubmed: 9489652
doi: 10.1038/sj.bmt.1701075
Cohen A, Békássy AN, Gaiero A, Faraci M, Zecca S, Tichelli A, et al. Endocrinological late complications after hematopoietic SCT in children. Bone Marrow Transplant. 2008;41:S43–8.
pubmed: 18545244
doi: 10.1038/bmt.2008.54
Borgmann-Staudt A, Rendtorff R, Reinmuth S, Hohmann C, Keil T, Schuster FR, et al. Fertility after allogeneic haematopoietic stem cell transplantation in childhood and adolescence. Bone Marrow Transplant. 2012;47:271–6.
pubmed: 21478918
doi: 10.1038/bmt.2011.78
Bresters D, Emons JAM, Nuri N, Ball LM, Kollen WJW, Hannema SE, et al. Ovarian insufficiency and pubertal development after hematopoietic stem cell transplantation in childhood. Pediatr Blood Cancer. 2014;61:2048–53.
pubmed: 25111958
doi: 10.1002/pbc.25162
Panasiuk A, Nussey S, Veys P, Amrolia P, Rao K, Krawczuk-Rybak M, et al. Gonadal function and fertility after stem cell transplantation in childhood: comparison of a reduced intensity conditioning regimen containing melphalan with a myeloablative regimen containing busulfan. Br J Haematol. 2015;170:719–26.
pubmed: 25974284
doi: 10.1111/bjh.13497
van As JW, van den Berg H, van Dalen EC. Platinum-induced hearing loss after treatment for childhood cancer. Cochrane Database Syst Rev. 2016;2016:CD010181.
pmcid: 6466671
Brock PR, Knight KR, Freyer DR, Campbell KCM, Steyger PS, Blakley BW, et al. Platinum-induced ototoxicity in children: a consensus review on mechanisms, predisposition, and protection, including a new International Society of Pediatric Oncology Boston ototoxicity scale. J Clin Oncol. 2012;30:2408–17.
pubmed: 22547603
pmcid: 3675696
doi: 10.1200/JCO.2011.39.1110
Whelan K, Stratton K, Kawashima T, Leisenring W, Hayashi S, Waterbor J, et al. Auditory complications in childhood cancer survivors: a report from the childhood cancer survivor study. Pediatr Blood Cancer. 2011;57:126–34.
pubmed: 21328523
pmcid: 3091978
doi: 10.1002/pbc.23025
Grewal S, Merchant T, Reymond R, McInerney M, Hodge C, Shearer P. Auditory late effects of childhood cancer therapy: a report from the Children’s Oncology Group. Pediatrics. 2010;125:e938–50.
pubmed: 20194279
doi: 10.1542/peds.2009-1597
Li Y, Womer RB, Silber JH. Predicting cisplatin ototoxicity in children: the influence of age and the cumulative dose. Eur J Cancer. 2004;40:2445–51.
pubmed: 15519518
doi: 10.1016/j.ejca.2003.08.009
van As JW, van den Berg H, van Dalen EC. Different infusion durations for preventing platinum-induced hearing loss in children with cancer. Cochrane Database Syst Rev. 2018;7:CD010885.
pubmed: 29975402
Schell MJ, McHaney VA, Green AA, Kun LE, Hayes FA, Horowitz M, et al. Hearing loss in children and young adults receiving cisplatin with or without prior cranial irradiation. J Clin Oncol. 1989;7:754–60.
pubmed: 2715805
doi: 10.1200/JCO.1989.7.6.754
Bertolini P, Lassalle M, Mercier G, Raquin MA, Izzi G, Corradini N, et al. Platinum compound-related ototoxicity in children: long-term follow-up reveals continuous worsening of hearing loss. J Pediatr Hematol Oncol. 2004;26:649–55.
pubmed: 27811606
doi: 10.1097/01.mph.0000141348.62532.73
Bitner-Glindzicz M, Rahman S. Ototoxicity caused by aminoglycosides. BMJ. 2007;335:784–5.
pubmed: 17947747
pmcid: 2034737
doi: 10.1136/bmj.39301.680266.AE
Gallagher KL, Jones JK. Furosemide-induced ototoxicity. Ann Intern Med. 1979;91:744–5.
pubmed: 496112
doi: 10.7326/0003-4819-91-5-744
Parsons SK, Neault MW, Lehmann LE, Brennan LL, Eickhoff CE, Kretschmar CS, et al. Severe ototoxicity following carboplatin-containing conditioning regimen for autologous marrow transplantation for neuroblastoma. Bone Marrow Transplant. 1998;22:669–74.
pubmed: 9818694
doi: 10.1038/sj.bmt.1701391
Knight KRG, Kraemer DF, Neuwelt EA. Ototoxicity in children receiving platinum chemotherapy: underestimating a commonly occurring toxicity that may influence academic and social development. J Clin Oncol. 2005;23:8588–96.
pubmed: 16314621
doi: 10.1200/JCO.2004.00.5355
Weiss A, Sommer G, Kasteler R, Scheinemann K, Grotzer M, Kompis M, et al. Long-term auditory complications after childhood cancer: a report from the Swiss Childhood Cancer Survivor Study. Pediatr Blood Cancer. 2017;64:364–73.
pubmed: 27650356
doi: 10.1002/pbc.26212
Landier W, Knight K, Wong FL, Lee J, Thomas O, Kim H, et al. Ototoxicity in children with high-risk neuroblastoma: prevalence, risk factors, and concordance of grading scales-a report from the Children’s Oncology Group. J Clin Oncol. 2014;32:527–34.
pubmed: 24419114
pmcid: 3918536
doi: 10.1200/JCO.2013.51.2038
Laverdière C, Cheung N-KV, Kushner BH, Kramer K, Modak S, LaQuaglia MP, et al. Long-term complications in survivors of advanced stage neuroblastoma. Pediatr Blood Cancer. 2005;45:324–32.
pubmed: 15714447
doi: 10.1002/pbc.20331
Ladenstein R, Pötschger U, Pearson ADJ, Brock P, Luksch R, Castel V, et al. Busulfan and melphalan versus carboplatin, etoposide, and melphalan as high-dose chemotherapy for high-risk neuroblastoma (HR-NBL1/SIOPEN): an international, randomised, multi-arm, open-label, phase 3 trial. Lancet Oncol. 2017;18:500–14.
pubmed: 28259608
doi: 10.1016/S1470-2045(17)30070-0
Reddel RR, Kefford RF, Grant JM, Coates AS, Fox RM, Tattersall MH. Ototoxicity in patients receiving cisplatin: importance of dose and method of drug administration. Cancer Treat Rep. 1982;66:19–23.
pubmed: 7198012
Coze C, Hartmann O, Michon J, Frappaz D, Dusol F, Rubie H, et al. NB87 induction protocol for stage 4 neuroblastoma in children over 1 year of age: a report from the French Society of Pediatric Oncology. J Clin Oncol. 1997;15:3433–40.
pubmed: 9396394
doi: 10.1200/JCO.1997.15.12.3433
Trahair TN, Vowels MR, Johnston K, Cohn RJ, Russell SJ, Neville KA, et al. Long-term outcomes in children with high-risk neuroblastoma treated with autologous stem cell transplantation. Bone Marrow Transplant. 2007;40:741–6.
pubmed: 17724446
doi: 10.1038/sj.bmt.1705809
Elzembely MM, Dahlberg AE, Pinto N, Leger KJ, Chow EJ, Park JR, et al. Late effects in high-risk neuroblastoma survivors treated with high-dose chemotherapy and stem cell rescue. Pediatr Blood Cancer. 2018;66:e27421.
pubmed: 30151986
doi: 10.1002/pbc.27421
Kohler JA, Ellershaw C, Machin D, Neuroblastoma Working Group of the Children’s Cancer and Leukaemia Group. Response to N7 induction chemotherapy in children more than one year of age diagnosed with metastatic neuroblastoma treated in UKCCSG centers. Pediatr Blood Cancer. 2007;49:234–9.
pubmed: 17252561
doi: 10.1002/pbc.21139
Moreno L, Vaidya SJ, Pinkerton CR, Lewis IJ, Imeson J, Machin D, et al. Long-term follow-up of children with high-risk neuroblastoma: the ENSG5 trial experience. Pediatr Blood Cancer. 2013;60:1135–40.
pubmed: 23281263
doi: 10.1002/pbc.24452
Pearson ADJ, Pinkerton CR, Lewis IJ, Imeson J, Ellershaw C, Machin D, et al. High-dose rapid and standard induction chemotherapy for patients aged over 1 year with stage 4 neuroblastoma: a randomised trial. Lancet Oncol. 2008;9:247–56.
pubmed: 18308250
doi: 10.1016/S1470-2045(08)70069-X
Clemens E, de Vries AC, Pluijm SF, Am Zehnhoff-Dinnesen A, Tissing WJ, Loonen JJ, et al. Determinants of ototoxicity in 451 platinum-treated Dutch survivors of childhood cancer: a DCOG late-effects study. Eur J Cancer. 2016;69:77–85.
pubmed: 27821322
doi: 10.1016/j.ejca.2016.09.023
Dean JB, Hayashi SS, Albert CM, King AA, Karzon R, Hayashi RJ. Hearing loss in pediatric oncology patients receiving carboplatin-containing regimens. J Pediatr Hematol Oncol. 2008;30:130–4.
pubmed: 18376265
doi: 10.1097/MPH.0b013e31815d1d83
Hobbie WL, Moshang T, Carlson CA, Goldmuntz E, Sacks N, Goldfarb SB, et al. Late effects in survivors of tandem peripheral blood stem cell transplant for high-risk neuroblastoma. Pediatr Blood Cancer. 2008;51:679–83.
pubmed: 18623215
pmcid: 2888471
doi: 10.1002/pbc.21683
Cohen LE, Gordon JH, Popovsky EY, Gunawardene S, Duffey-Lind E, Lehmann LE, et al. Late effects in children treated with intensive multimodal therapy for high-risk neuroblastoma: high incidence of endocrine and growth problems. Bone Marrow Transplant. 2014;49:502–8.
pubmed: 24442245
doi: 10.1038/bmt.2013.218
Lackner H, Urban C, Sovinz P, Nebl A, Schmidt S, Benesch M, et al. Hypothyroidism after treatment of metastatic neuroblastoma. Pediatr Blood Cancer. 2010;55:768.
pubmed: 20806369
doi: 10.1002/pbc.22593
Perwein T, Lackner H, Sovinz P, Benesch M, Schmidt S, Schwinger W, et al. Survival and late effects in children with stage 4 neuroblastoma. Pediatr Blood Cancer. 2011;57:629–35.
pubmed: 21319289
doi: 10.1002/pbc.23036
Zheng L, Yan W, Kong Y, Liang P, Mu Y. An epidemiological study of risk factors of thyroid nodule and goiter in Chinese women. Int J Clin Exp Med. 2015;8:11379–87.
pubmed: 26379953
pmcid: 4565336
Michel G, Socié G, Gebhard F, Bernaudin F, Thuret I, Vannier JP, et al. Late effects of allogeneic bone marrow transplantation for children with acute myeloblastic leukemia in first complete remission: the impact of conditioning regimen without total-body irradiation-a report from the Société Française de Greffe de Moelle. J Clin Oncol. 1997;15:2238–46.
pubmed: 9196136
doi: 10.1200/JCO.1997.15.6.2238
Cohen A, Rovelli A, Bakker B, Uderzo C, van Lint MT, Esperou H, et al. Final height of patients who underwent bone marrow transplantation for hematological disorders during childhood: a study by the Working Party for Late Effects-EBMT. Blood. 1999;93:4109–15.
pubmed: 10361107
doi: 10.1182/blood.V93.6.2013.406k25_2013_2024
Huma Z, Boulad F, Black P, Heller G, Sklar C. Growth in children after bone marrow transplantation for acute leukemia. Blood. 1995;86:819–24.
pubmed: 7606013
doi: 10.1182/blood.V86.2.819.bloodjournal862819
Giorgiani G, Bozzola M, Locatelli F, Picco P, Zecca M, Cisternino M, et al. Role of busulfan and total body irradiation on growth of prepubertal children receiving bone marrow transplantation and results of treatment with recombinant human growth hormone. Blood. 1995;86:825–31.
pubmed: 7606014
doi: 10.1182/blood.V86.2.825.bloodjournal862825
Hovi L, Rajantie J, Perkkiö M, Sainio K, Sipilä I, Siimes MA. Growth failure and growth hormone deficiency in children after bone marrow transplantation for leukemia. Bone Marrow Transplant. 1990;5:183–6.
pubmed: 2331538
Clement-De Boers A, Oostdijk W, Van Weel-Sipman MH, Van den Broeck J, Wit JM, Vossen JM. Final height and hormonal function after bone marrow transplantation in children. J Pediatr. 1996;129:544–50.
pubmed: 8859261
doi: 10.1016/S0022-3476(96)70119-1
Sanders JE, Guthrie KA, Hoffmeister PA, Woolfrey AE, Carpenter PA, Appelbaum FR. Final adult height of patients who received hematopoietic cell transplantation in childhood. Blood. 2005;105:1348–54.
pubmed: 15454481
doi: 10.1182/blood-2004-07-2528
Thomas BC, Stanhope R, Plowman PN, Leiper AD. Endocrine function following single fraction and fractionated total body irradiation for bone marrow transplantation in childhood. Acta Endocrinol. 1993;128:508–12.
doi: 10.1530/acta.0.1280508
Allodji RS, Diallo I, El-Fayech C, Kahlouche A, Dumas A, Schwartz B, et al. Association of radiation dose to the eyes with the risk for cataract after nonretinoblastoma solid cancers in childhood. JAMA Ophthalmol. 2016;134:390–7.
pubmed: 26868620
doi: 10.1001/jamaophthalmol.2015.6088
Suesskind D, Schrader M, Foerster MH, Ernemann U, Aisenbrey S. Cataract formation: a possible complication of intra-arterial chemotherapy for retinoblastoma. Eur J Ophthalmol. 2014;24:449–53.
pubmed: 24242220
doi: 10.5301/ejo.5000393
Stuber ML, Meeske KA, Krull KR, Leisenring W, Stratton K, Kazak AE, et al. Prevalence and predictors of posttraumatic stress disorder in adult survivors of childhood cancer. Pediatrics. 2010;125:e1124–34.
pubmed: 20435702
doi: 10.1542/peds.2009-2308
Poulet-Coulibando P, Testas A. Le niveau d’études de la population et des jeunes. État de l’Enseignement supérieur et de la Recherche en France - 49 indicateurs. 2017. https://publication.enseignementsup-recherche.gouv.fr/eesr/10/EESR10_ES_20-le_niveau_d_etudes_de_la_population_et_des_jeunes.php . Accessed 26 Jan 2021.