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Research ArticleClinical Studies

Improved Outcome in Pediatric Acute Myeloid Leukemia: Progress With Hematopoietic Cell Transplantation

JOANNA STANKIEWICZ and JAN STYCZYNSKI
Anticancer Research September 2022, 42 (9) 4499-4504; DOI: https://doi.org/10.21873/anticanres.15951
JOANNA STANKIEWICZ
Department of Pediatric Hematology and Oncology, Collegium Medicum, Nicolaus Copernicus University Torun, Jurasz University Hospital, Bydgoszcz, Poland
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  • For correspondence: joanna.konieczek@cm.umk.pl
JAN STYCZYNSKI
Department of Pediatric Hematology and Oncology, Collegium Medicum, Nicolaus Copernicus University Torun, Jurasz University Hospital, Bydgoszcz, Poland
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Abstract

Background/Aim: Pediatric acute myeloid leukemia (AML) is a heterogenous disease; however, development of diagnostic methods has led to a better understanding of its nature and improvement in therapy outcomes. In this study, we evaluated treatment results in children with AML treated in a single oncology center in comparison with international results. Patients and Methods: Data from 77 children with AML treated in a single oncology center between 1994 and 2020 were analyzed. Patients had been treated according to five consecutive therapy protocols: AML NOPHO 88; ANLL 98; BFM AML 2004; BFM AML 2012, and BFM AML 2019. Five-year overall survival (OS), 5-year event-free survival (EFS) and 5-year relapse-free survival (RFS) were evaluated for each therapy protocol to determine prognostic factors and clarify differences between international and individual center results. Results: During the observational period, 5-year OS increased from 55.6% to 85.7%, 5-year EFS from 45.7% to 87.5% and 5-year RFS from 51.4% to 85.7%. Hematopoietic cells transplantation (HCT) introduction in early 2000’ improved treatment outcomes in the high-risk group, what has been mostly seen in the results of 5-year EFS. Treatment-related mortality was the most frequent cause of death in the analyzed group. Conclusion: Despite the significant improvement in therapy of pediatric AML, treatment outcomes remain unsatisfying. Introduction of HCT relevantly improved therapy results, especially in the high-risk group. International cooperation is crucial because of the small patient numbers in individual oncology centers.

Key Words:
  • Acute myeloid leukemia
  • children
  • therapeutic era
  • survival

During the last 30 years, significant improvement in pediatric acute myeloid leukemia (AML) treatment has been made. International collaboration is necessary in AML trials because of the small number of patients in regional oncology centers, the need of standardized risk group stratification and implementing unified protocols (1, 2). In 1983, The Polish Pediatric Leukemia/Lymphoma Study Group introduced international treatment protocols in AML therapy in Poland. Multi-aspects national transformation enabled better implementation of the treatment guidelines, which led to improvement in treatment outcomes in children with AML (3, 4). The progress can be seen nationwide as well as in individual oncology centers. The aim of the study was to determine specific prognostic factors in each therapeutic era and compare a single center performance with international results. We analyzed data from 77 patients treated in the Department of Pediatrics, Hematology and Oncology in Bydgoszcz between 1994 and 2020 with five consecutive AML protocols.

Patients and Methods

Design of the study. In this study, we retrospectively analyzed outcomes in all patients diagnosed with AML at a single children oncology center in Poland between 1994 and 2020. Treatment results were divided into specific therapeutic groups, defined by several therapy protocols.

Patients. Data of patients aged under 18 years with AML treated between 1994 and 2020 in the Department of Pediatrics, Hematology and Oncology in Bydgoszcz were analyzed. The inclusion criteria included patients with AML, including AML as myelodysplastic syndrome (MDS) transformations, patients with comorbidities or congenital malformations (including Down syndrome) and also biphenotypic or bilineage leukemia with AML component.

Diagnosis. In all cases, diagnosis was established based on bone marrow biopsy including cell morphology with the French-American-British (FAB) classification and immunophenotyping. Since 2003, cytogenetic analyses have been performed. Central verification of cell morphology, immunophenotyping, and cytogenetics have been performed since 2005. Complete blood count, ultrasonography of the liver and spleen, lumbar puncture, chest X-ray and echocardiography (ECG) were performed in all cases. Most children were also examined by an ophthalmologist and children’s neurologist for central nervous system (CNS) assessment.

Treatment protocols and risk group stratification. Patients were treated according to five therapeutic protocols: AML Nordic Society of Pediatric Hematology and Oncology (NOPHO) 88 in the period from March 1994 to March 1998 (5); ANLL 98 from March 1998 to November 2005 (3); Berlin–Frankfurt–Munster (BFM) AML 2004 from November 2005 to August 2013 (6); BFM AML 2012 from August 2013 to January 2020 (7); BFM AML 2019 from January 2020. Stratification to each risk group was performed since ANLL 98 protocol and the risk group definition for each protocol is shown in Table I. Hematopoietic cell transplantation (HCT) accessibility was limited before 2000 and in the first years, transplantation was performed in all forms (autologous, matched related, and unrelated donors), after individual assessment of the advantages and risk related to the procedure.

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Table I.

Risk group definitions.

Definitions. Complete remission was defined as ≤5% of blasts in bone marrow (BM) of normal or only slightly decreased cellularity, with signs of regeneration of normal hematopoiesis, regeneration of normal cell production in peripheral blood (PB), lack of blasts in PB and the disappearance of any extramedullary sites. Relapse was defined as reappearance of leukemic blasts in the peripheral blood, re-infiltration of BM with ≥5% blasts, or leukemic infiltration elsewhere following complete remission (CR), lasting at least 4 weeks. Second complete remission (CR2) was defined as achievement of CR after relapse. An event was defined as failure to achieve complete remission during the first 42 days of treatment, relapse, death of any causes, or secondary malignancies after AML treatment. Overall survival (OS) was defined as the time from AML diagnosis until death of any cause, relapse-free survival (RFS) was defined as the time from AML diagnosis until relapse occurrence and event-free survival (EFS) was defined as the time from diagnosis to event occurrence.

Statistical methods. Data were given as median, range and proportion. Differences between groups were calculated using Ch-squared test and in specific subgroups relative odds ratio (OR) and relative risk (RR) were determined, with 95%CI (confidence interval). The endpoints of the study were 5-year OS, 5-year EFS and 5-year RFS. Survival rates were calculated with the Kaplan-Meier methods and compared with the log-rank test. MedCalc 20.100 (MedCalc Software, Mariakerke, Belgium) statistical software was used. Data were considered statistically significant when p<0.05. The study was approved (KB 577/2021) by the Ethics Committee of Collegium Medicum, Nicolas Copernicus University, Bydgoszcz.

Results

Demographics. In the period between 1994 and 2022, overall, 77 patients were diagnosed with AML. Patient characteristics in specific therapeutic protocols are shown in Table II. The median age at diagnosis was 10.0 years (range=0.1-18.2 years). Risk group stratification was introduced in ANLL 98 protocol. Since then, out of 72 children, 32 (44.4%) have been stratified into a high-risk group (HR). Relapse occurred in 21 children. Fifteen children had isolated bone marrow (BM) relapse, two isolated CNS relapse, two combined BM and CNS relapse, and two patients had BM and localized relapse (in both cases nasopharyngeal mass). High-risk group patients had fourfold higher risk of relapse (OR=4.35, 95%CI=1.22-15.44, p=0.023) compared to other patients, but no higher risk of death was observed (OR=1.04, 95%CI=0.36-2.99, p=0.934).

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Table II.

Patient characteristics at diagnosis in five acute myeloid leukemia (AML) protocols.

Achievement of remission. CR was achieved in 67 patients (87.0%). Failure to achieve CR after two cycles of induction chemotherapy was one of the risk factors of death (OR=60.0, 95%CI=3.37-1088.9, p=0.005).

Overall survival. Five-year OS was 62.1% for the entire group. For each protocol, 5-year OS was respectively 55.6% for AML-NOPHO88 protocol, 68.2% for ANLL98 protocol, 48.0% for BFM AML 2004 protocol, 85.7% for BFM AML 2012 protocol and 100.0% for BFM AML 2019 protocol (3 years of median follow up for BFM AML 2019 protocol). The results are shown in Figure 1A. There were no statistically significant differences between groups (p=0.416). Among 32 patients stratified into the HR group, 5-year OS rate in patients treated with HCT was 76.0% compared with 57.1% in patients treated without HCT. There was a significant difference between patients with primary AML and MDS transformation or other comorbidities in 5-year OS (65.5% vs. 42.4%, p=0.048). This was mainly due to the higher rate of death after disease progression in the second group (10.0% vs. 27.3%).

Figure 1.
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Figure 1.

Therapy outcomes for acute myeloid leukemia children treated between 1994-2022, according to 5 consecutive protocols: (A) Overall survival; (B) Event-free survival; (C) Relapse-free survival; (D) Overall survival of patients treated with chemotherapy+ hematopoietic cell transplantation (HCT) vs. chemotherapy without HCT.

Event-free survival. Five-year EFS was 51.4% for the entire group. For each protocol, 5-year EFS was 45.7% for AML-NOPHO88 protocol, 62.5% for ANLL98 protocol, 28.7% for BFM AML 2004 protocol, 85.7% for BFM AML 2012 protocol, and 87.5% for BFM AML 2019 protocol. The results are shown in Figure 1B. The differences were statistically significant (p=0.007). Among patients in the HR group, 5-year EFS was 58.0% in those who underwent HCT compared with 16.7% in those treated without HCT (p=0.007).

Relapse-free survival. In patients who relapsed, the average time to relapse was 2.45 years (range=0.1-15.3 years). Incidence of relapse was an independent risk factor of death (OR=5.66, 95%CI=1.48-21.56, p=0.01) (Table III). Five-year RFS was 62.7% for the entire group. Regarding each protocol, 5-year RFS was 51.4% for AML-NOPHO88 protocol, 68.8% for ANLL98 protocol, 42.0% for BFM AML 2004 protocol, 85.7% for BFM AML 2012 protocol, and 100.0% for BFM AML 2019 protocol. The results are shown in Figure 1C. The differences were also statistically significant (p=0.01). CR2 was achieved in 14 patients (66.7%) and HCT in CR2 was performed in 13 relapsed patients. Five-year OS in patients who underwent HCT was 48.9% compared with 25.0% in children treated without HCT. The difference was of borderline significance (p=0.078).

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Table III.

Independent risk factors of death.

Causes of death. In the entire observation period, 27 patients died (35.0%). Treatment-related mortality (TRM) was the most frequent cause of death (11 patients, 40.7%), among which 6 patients died from infections, 2 from treatment toxicity, 1 from graft versus host disease (GvHD) and 2 from other treatment-related complications. Nine patients died from disease progression and other 7 from relapse (3 in second relapse and 4 in third and further relapses). There was no impact of white blood cells (WBC), platelets (PLT) or hemoglobin (HGB) levels at diagnosis on the risk of death.

Discussion

Therapy results in children with AML have improved significantly over the last 3 decades, mostly due to the development of cytogenetics and molecular diagnostics, better supportive care, and introduction of HCT. The progress can be seen in international and nationwide reports (8). This study shows the results of a single oncology center experience in pediatric AML treatment and provides the opportunity to compare individual center results with international reports.

During the described period, OS improved from 55.6% between 1994 and 1998 to 87.5% from 2012 to early 2020. OS in patients treated since January 2020 remains 100.0%. In this group, observational period is short; however, it is worth emphasizing that there was no early death in patients treated by BFM AML 2019 protocol. OS in the majority of therapeutic protocols was slightly superior in our analysis compared to international results (55. 6% vs. 46.0% for AML-NOPHO 88, 68.2% vs. 50.0% for ANLL 98 and 85.7% vs. 82.0% for BFM AML 2012) (3, 5, 7). The only exception were the results of BFM AML 2004 protocol (48.0% vs. 74.0%), but also, in the nationwide analysis in Poland, OS was inferior in comparison to international results (3, 6). This was mostly due to the high rate of relapse and treatment-related mortality, including deaths after HCT. Because HCT accessibility in Poland was limited before 2000, poor OS in 2004-2012 could be the result of the unsatisfying results of transplantations during the first years of their performance.

AML is a heterogenous disease and the diagnosis relies predominantly on the identification of mutations in myeloid cells. Immunophenotyping and cytogenetics became available in Poland after 2005, and since then, most patients have been stratified according to immunophenotype and characteristic mutations in blast cells, which allows the adjustment of therapy in some patient group. It is worth noting, that the biggest progress in childhood AML treatment has been made in specific subgroups of patients, who received targeted therapy (AML M3, patients with Down syndrome). Unfortunately, therapeutic outcomes in some subgroups remain highly unsatisfying (secondary AML, patients with FTL3 mutation) (9, 10).

AML remains the most frequent cause of HCT performance (11). Despite the controversial role of HCT in first remission in non-HR patients, undoubtedly it has improved outcomes in this particular group (1, 12). In our analysis, HCT had relevant impact on therapy results in the HR group and almost doubled chances of survival in relapsed patients.

The obvious limitation of the study was its small group size. Childhood AML is a rare disease with an incidence of 5-8/1,000000, which leads to insufficient patient numbers treated in separated centers; therefore, international cooperation is necessary (13). Other limitations include its retrospective nature and lack of complete data (e.g., uniformed genetic diagnosis before 2005) in some patients. However, the data and therapy results reflect the gradual progress in the diagnostic and therapeutic capability of oncology centers in Poland.

In conclusion, despite the fact that therapeutic results in pediatric patients with AML remain unsatisfying, we can observe significant progress, especially in some patients with well-defined mutations in blast cells and targeted therapy. Further research and international collaborations are needed to obtain a better understanding of the disease and improve outcomes.

Acknowledgements

The Authors would like to thank: Dr. Ewa Demidowicz, Dr. Krzysztof Czyżewski, Dr. Robert Dębski, Dr. Monika Pogorzała, Dr. Andrzej Kołtan, Dr. Natalia Bartoszewicz, Dr. Monika Richert-Przygońska, Dr. Barbara Tejza, Dr. Piotr Księżniakiewicz, Dr. Joanna Cisek, Dr. Agnieszka Jatczak-Gaca, Prof. Sylwia Kołtan, Dr. Anna Dąbrowska, Dr. Elżbieta Grześk, Dr. Anna Urbańczyk, Dr. Kamila Jaremek, Dr. Eugenia Winogrodzka, Dr. Dominika Kołuda, Dr. Monika Łęcka, Dr. Sandra Wałach, Dr. Agata Marjańska, Dr. Magdalena Dziedzic, Dr. Katarzyna Balci, Dr. Sonia Tarasenko, Dr. Oliwia Grochowska, Dr. Hanna Żołnowska, Prof. Mariusz Wysocki, Ewa Dembna and the nurses team, for the continuous excellent care of children with malignancies.

Footnotes

  • Authors’ Contributions

    Joanna Stankiewicz– data collection and interpretation, statistical analysis, writing the manuscript, Jan Styczyński - critical review, acceptance of final version for publication.

  • Conflicts of Interest

    The Authors declare no conflicts of interest in relation to this study.

  • Received April 27, 2022.
  • Revision received July 14, 2022.
  • Accepted July 18, 2022.
  • Copyright © 2022 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.

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Improved Outcome in Pediatric Acute Myeloid Leukemia: Progress With Hematopoietic Cell Transplantation
JOANNA STANKIEWICZ, JAN STYCZYNSKI
Anticancer Research Sep 2022, 42 (9) 4499-4504; DOI: 10.21873/anticanres.15951

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Improved Outcome in Pediatric Acute Myeloid Leukemia: Progress With Hematopoietic Cell Transplantation
JOANNA STANKIEWICZ, JAN STYCZYNSKI
Anticancer Research Sep 2022, 42 (9) 4499-4504; DOI: 10.21873/anticanres.15951
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