Вопросы гематологии/онкологии и иммунопатологии в педиатрии. 2021; 20: 97-110
Гиподиплоидный кариотип при острых лимфобластных лейкозах из В-линейных предшественников у детей
https://doi.org/10.24287/1726-1708-2021-20-2-97-110Аннотация
Выявление генетических маркеров неблагоприятного прогноза имеет принципиальное значение для выбора тактики терапии острых лимфобластных лейкозов из В-линейных предшественников (ВП-ОЛЛ). Гиподиплоидный кариотип при ВП-ОЛЛ имеет крайне неблагоприятное значение и является критерием стратификации пациентов в группу высокого риска. Несмотря на это, показатели выживаемости пациентов с гиподиплоидным кариотипом остаются невысокими. В отечественных протоколах терапии острых лимфобластных лейкозов у детей гиподиплоидный кариотип не входит в критерии стратификации пациентов на группы риска. С целью определить прогностическое значение и клинические характеристики ВП-ОЛЛ с гиподиплоидным кариотипом нами были проанализированы показатели выживаемости 2700 пациентов, включенных в многоцентровое исследование. Данное исследование одобрено независимым этическим комитетом и утверждено решением ученого совета ФГБУ «НМИЦ ДГОИ им. Дмитрия Рогачева» Минздрава России. Всем больным было проведено исследование методами кариотипирования и флуоресцентной in situгибридизации (FISH). У 27 пациентов был выявлен гиподиплоидный кариотип. У 18 из 27 больных имел место гипоплоидный клон по данным кариотипирования, у 2 – удвоение окологаплоидного клона по данным кариотипирования и FISH, у 7 пациентов с нормальным кариотипом или отсутствием митозов гиподиплоидия была установлена только на основании результатов исследования методом FISH. Для ВП-ОЛЛ с гиподиплоидией характерно повышенное число лейкоцитов в дебюте заболевания. Медиана количества лейкоцитов составила 24,2 (3,4–206,0) × 109/л против 10,3 (0,2–1290,0) × 109/л в контрольной группе. Число пациентов с инициальным лейкоцитозом менее 30 × 109/л было достоверно ниже, чем в контрольной группе (p< 0,0062). Ремиссия была достигнута у 26 из 27 больных. Бессобытийная выживаемость пациентов с гиподиплоидией была существенно ниже, чем в группе больных без гиподиплоидии: 50 ± 11% против 72 ± 8% (p< 0,0001). Общая выживаемость составила 64 ± 10% и 90 ± 1% соответственно (p< 0,0001). Кумулятивная вероятность развития рецидива при гиподиплоидном кариотипе составила 42,6 ± 10,9% против 22,3 ± 8,1% в контрольной группе (p< 0,0001). Пациенты, получавшие более интенсивную терапию согласно группам промежуточного и высокого риска, имели более высокие показатели выживаемости, нежели больные из группы стандартного риска: 62 ± 13% против 40 ± 15% (р= 0,59), кумулятивная вероятность развития рецидива в зависимости от группы риска составила 26,4 ± 12,1% и 60 ± 16,9% соответственно (р= 0,19). Наибольший риск развития рецидива наблюдался в группе, объединяющей пациентов с окологаплоидным набором хромосом и низкой гиподиплоидией (26–39 хромосом; 52,9 ± 14,4%), бессобытийная выживаемость в этой группе составила 36 ± 13%. Результаты терапии пациентов с ВП-ОЛЛ и гиподиплоидией по отечественному протоколу оказались сравнимы с общемировыми. Пациенты с ВП-ОЛЛ и гиподиплоидией изначально должны быть стратифицированы на наиболее интенсивную ветвь терапии. Для выявления гиподиплоидии обязательно выполнение стандартного кариотипирования, при необходимости дополняемого исследованием методом FISH.
Список литературы
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22. Safavi S., Olsson L., Biloglav A., Veerla S., Blendberg M., Tayebwa J., et al. Genetic and epigenetic characterization of hypodiploid acute lymphoblastic leukemia. Oncotarget 2015; 6 (40): 42793–802. DOI: 10.18632/oncotarget.6000
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29. Gibbons B., MacCallum P., Watts E., Rohatiner A.Z., Webb D., Katz F.E., et al. Near haploid acute lymphoblastic leukemia: seven new cases and a review of the literature. Leukemia 1991; 5 (9): 738–43.
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31. Misawa S., Oguma N., Testa J.R. A case of acute lymphoblastic leukemia with severe hypodiploidy. Cancer Genet Cytogenet 1985; 16 (2): 137–43. DOI: 10.1016/0165-4608(85)90007-x
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Pediatric Hematology/Oncology and Immunopathology. 2021; 20: 97-110
A hypodiploid karyotype in childhood B-cell precursor acute lymphoblastic leukemia
https://doi.org/10.24287/1726-1708-2021-20-2-97-110Abstract
The detection of genetic markers associated with poor prognosis is crucial to the selection of an appropriate treatment plan for B-cell precursor acute lymphoblastic leukemia (BCP-ALL). A hypodiploid karyotype in patients with BCP-ALL has an unfavorable impact and serves as a criterion for the stratification of patients into a high-risk group. However, the survival rates of patients with a hypodiploid karyotype remain poor. Russian treatment protocols for childhood acute lymphoblastic leukemia do not include a hypodiploid karyotype in risk stratification criteria. In order to determine the prognostic value of a hypodiploid karyotype and the clinical characteristics of BCP-ALL in patients with a hypodiploid karyotype, we analyzed the survival rates of 2,700 patients included in a multicenter study. Our study was approved by the Independent Ethics Committee and the Scientific Council of the D. Rogachev NMRCPHOI of the Ministry of Healthcare of the Russian Federation. All patients underwent karyotyping and fluorescence in situhybridization (FISH) testing. A hypodiploid karyotype was detected in 27 patients. Eighteen out of 27 patients had a hypoploid clone (according to karyotyping results), 2 patients had a doubled near-haploid clone (according to karyotyping and FISH results); in 7 patients with a normal karyotype or in the absence of mitosis, hypodiploidy was determined only by FISH test. BCP-ALL with hypodiploidy is usually associated with increased WBC count at disease onset. The median WBC count in the study group was 24.2 (3.4–206.0) × 109/l vs 10.3 (0.2–1290.0) × 109/l in the control group. The number of patients with initial leukocytosis < 30 × 109/l in the study group was significantly lower than in the control group (p< 0.062). Remission was achieved in 26/27 patients. The event-free survival rates in patients with hypodiploidy were significantly lower than in those without hypodiploidy: 50 ± 11% vs 72 ± 8% (p< 0.0001). The overall survival was 64 ± 10% and 90 ± 1%, respectively (p< 0.0001). The cumulative incidence of relapse in patients with a hypodiploid karyotype was higher (42.6 ± 10.9%) than in the controls (22.3 ± 8.1%) (p< 0.0001). The patients who received more intense treatment for intermediate- and high-risk groups showed better survival rates than those in the standard-risk group: 62 ± 13% vs 40 ± 15% (р= 0.59); the cumulative incidence of relapse according to the risk group was 26.4 ± 12.1% and 60 ± 16.9%, respectively (р= 0.19).The highest risk of relapse was observed in a group that included patients with near-haploidy and low hypodiploidy (26–39 chromosomes; 52.9 ± 14.4%). The event-free survival in this group was 36 ± 13%. The results of treatment of patients with BCP-ALL and hypodiploidy according to the national guidelines turned out to be comparable to the international ones. Patients with BCP-ALL and hypodiploidy should be initially stratified to the most intense treatment arm. In order to identify patients with hypoploidy, standard karyotyping is required; where needed, it can be supplemented by FISH analysis
References
1. McNeer J.L., Devidas M., Dai Y., Carroll A.J., Heerema N.A., Gastier-Foster J.M., et al. Hematopoietic Stem-Cell Transplantation Does Not Improve the Poor Outcome of Children With Hypodiploid Acute Lymphoblastic Leukemia: A Report From Children's Oncology Group. J Clin Oncol 2019; 37 (10): 780–9. DOI: 10.1200/JCO.18.00884
2. Pui C.H., Rebora P., Schrappe M., Attarbaschi A., Baruchel A., Basso G., et al. Ponte di Legno Childhood ALL Working Group. Outcome of Children With Hypodiploid Acute Lymphoblastic Leukemia: A Retrospective Multinational Study. J Clin Oncol 2019; 37 (10): 770–9. DOI: 10.1200/JCO.18.00822. Epub 2019 Jan 18.
3. Harrison C.J., Moorman A.V., Broadfield Z.J., Cheung K.L., Harris R.L., Reza Jalali G., et al. Childhood and Adult Leukaemia Working Parties. Three distinct subgroups of hypodiploidy in acute lymphoblastic leukaemia Br J Haematol 2004; 125 (5): 552–9. DOI: 10.1111/j.1365-2141.2004.04948.x
4. The Mitelman Database of Chromosome Aberrations and Gene Fusions in Cancer. Dostupno po: https://mitelmandatabase.isb-cgc.org/. Ssylka aktivna na 5.04.2021.
5. Pui C.H., Carroll A.J., Raimondi S.C., Land V.J., Crist W.M., Shuster J.J., et al. Clinical presentation, karyotypic characterization, and treatment outcome of childhood acute lymphoblastic leukemia with a near-haploid or hypodiploid less than 45 line. Blood 1990; 75 (5): 1170–7.
6. Charrin C., Thomas X., Ffrench M., Le Q.H., Andrieux J., Mozziconacci M.J., et al. A report from the LALA-94 and LALA-SA groups on hypodiploidy with 30 to 39 chromosomes and near-triploidy: 2 possible expressions of a sole entity conferring poor prognosis in adult acute lymphoblastic leukemia (ALL) Blood 2004; 104 (8): 2444–51. DOI: 10.1182/blood-2003-04-1299
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8. Bennett J., Catovsky D., Daniel M., Flandrin G., Galton D., Gralnick H., et al. Proposals for the classification of the acute leukaemias. French-American-British (FAB) co-operative group. Br J Haematol 1976; 33 (4): 451–8.
9. Bene M.C., Castoldi G., Knapp W., Ludwig W.D., Matutes E., Orfao A., et al. Proposals for the immunological classification of acute leukemias. European Group for the Immunological Characterization of Leukemias (EGIL). Leukemia 1995; 9 (10): 1783–6.
10. Béné M.C., Nebe T., Bettelheim P., Buldini B., Bumbea H., Kern W., et al. Immunophenotyping of acute leukemia and lymphoproliferative disorders: a consensus proposal of the European Leukemia Net Work Package 10. Leukemia 2011; 25 (4): 567–74. DOI: 10.1038/leu.2010.312
11. Czepulkowski B., Bhatt B., Rooney D. Malignancy and acquired abnormalities. Ed. 2 nd. Vol. 2. New York, NY: Oxford University Press; 1992. Analysis of Chromosomes from Bone marrow and Leukaemic Blood. In: Human cytogenetics. A practical approach; pp. 1–25.
12. ISCN 2016: An International System for Human Cytogenomic Nomenclature (2016) Jean McGowan-Jordan, A. Simons, Michael Schmid. Basel: Karger; 2016.
13. Kaplan E.L., Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc 1958; 53: 457–81.
14. Mantel N. Evaluation of survival data and two new rank order statistics arising in its consideration. Cancer Chemother Rep 1966; 50: 163–70.
15. Kalbfleisch J., Prentice R. The statistical analysis of failure time data. New York: John Wiley&Sons; 1980.
16. Gray R.J. A class of k-sample tests for comparing the cumulative incidence of a competing risk. Ann Stat 1988; 16: 1141–54.
17. Shabtai F., Lewinski U.H., HarZahav L., Gafter U., Halbrecht I., Djaldetti M. A hypodiploid clone and its duplicate in acute lymphoblastic leukemia. Am J Clin Pathol 1979; 72 (6): 1018–24. DOI: 10.1093/ajcp/72.6.1018
18. Pui C.H., Williams D.L., Raimondi S.C., Rivera G.K., Look A.T., Dodge R.K., at al. Hypodiploidy is associated with a poor prognosis in childhood acute lymphoblastic leukemia. Blood 1987; 70 (1): 247–53.
19. Nordenson I., Adrian B.A., Holmgren G., Roos G., Rudolphi O., Wahlqvist O., et al. Near-haploidy in childhood leukemia: a high-risk component. Pediatr Hematol Oncol 1988; 5 (4): 309–14. DOI: 10.3109/08880018809037371
20. Secker-Walker L.M., Chessels J.M., Stewart E.L., Swansbury G.J., Richards S., Lawler S.D. Chromosomes and other prognostic factors in lymphoblastic leukemia: a long-term follow-up. Br J Haematol 1989; 72 (3): 336–42. DOI: 10.1111/j.1365-2141.1989.tb07713.x
21. Raimondi S.C., Mathew S. Conventional cytogenetic techniques in the diagnosis of childhood acute lymphoblastic leukemia. Methods Mol Biol 2003; 220: 73–82. DOI: 10.1385/1-59259-363-1:073
22. Safavi S., Olsson L., Biloglav A., Veerla S., Blendberg M., Tayebwa J., et al. Genetic and epigenetic characterization of hypodiploid acute lymphoblastic leukemia. Oncotarget 2015; 6 (40): 42793–802. DOI: 10.18632/oncotarget.6000
23. Pui C.H., Yang J.J., Bhakta N., Rodrigez-Galindo C. Global effort toward the cure of childhood acute lymphoblastic leukemia. Lancet Child Adolesc Health 2018; 2 (6): 440–54. DOI: 101016/S2352-4642(18)30066-X
24. Holmfeldt L., Wei L., Diaz-Flores E., Walsh M., Zhang J., Ding L., et al. The genomic landscape of hypodiploid acute lymphoblastic leukemia. Nat Genet 2013; 45 (3): 242–52. DOI: 10.1038/ng.2532. Epub 2013 Jan 20.
25. Nachman J.B., Heerema N.A., Sather H., Camitta B., Forestier E., Harrison C.J., et al. Outcome of treatment in children with hypodiploid acute lymphoblastic leukemia. Blood 2007; 110 (4): 1112–5. DOI: 10.1182/blood-2006-07-038299
26. Moorman A.V., Chilton L., Wilkinson J., Ensor H.M., Bown N., Proctor S.J. A population-based cytogenetic study of adults with acute lymphoblastic leukemia. Blood 2010; 115 (2): 206–14. DOI: 10.1182/blood-2009-07-232124
27. Safavi S., Paulsson K. Near-haploid and low-hypodiploid acute lymphoblastic leukemia: two distinct subtypes with consistently poor prognosis. Blood 2017; 129 (4): 420–3. DOI: 10.1182/blood-2016-10-743765
28. Callen D.F., Raphael K., Michael P.M., Garson O.M. Acute lymphoblastic leukemia with a hypodiploid karyotype with less than 40 chromosomes: the basis for division into two subgroups. Leukemia 1989; 3 (10): 749–52.
29. Gibbons B., MacCallum P., Watts E., Rohatiner A.Z., Webb D., Katz F.E., et al. Near haploid acute lymphoblastic leukemia: seven new cases and a review of the literature. Leukemia 1991; 5 (9): 738–43.
30. Ma S.K., Chan G.C., Wan T.S., Lam C.K., Ha S.Y., Lau Y.L., et al. Near-haploid common acute lymphoblastic leukaemia of childhood with a second hyperdiploid line: a DNA ploidy and fluorescence in-situ hybridization study. Br J Haematol 1998; 103 (3): 750–5. DOI: 10.1046/j.1365-2141.1998.01044.x
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