Challenges and considerations for antifungal prophylaxis in children with acute myeloid leukemia

References

• Yeoh DK, Haeusler GM, McMullan BJ, Butters C, Bryant PA, Clark JE, et al.. Antifungal use in children with acute leukaemia: state of current evidence and directions for future research. Journal of Antimicrobial Chemotherapy. 2022;77(6):1508–1524. doi: 10.1093/jac/dkac060
   PubMedGoogle Scholar
• Bartlett AW, Cann MP, Yeoh DK, Bernard A, Ryan AL, Blyth CC, et al.. Epidemiology of invasive fungal infections in immunocompromised children; an Australian national 10-year review. Pediatric blood & cancer. 2019;66(4):e27564. doi: 10.1002/pbc.27564
   PubMedGoogle Scholar
• *Groll AH, Pana D, Lanternier F, Mesini A, Ammann RA, Averbuch D, et al. 8th European Conference on Infections in Leukaemia: 2020 guidelines for the diagnosis, prevention, and treatment of invasive fungal diseases in paediatric patients with cancer or post-haematopoietic cell transplantation. The Lancet Oncology. 2021;22(6):e254–e69.
   Google Scholar
• Teh BW, Yeoh DK, Haeusler GM, et al. Consensus guidelines for antifungal prophylaxis in haematological malignancy and haemopoietic stem cell transplantation, 2021. Intern Med J. 2021;51(S7):67–88. doi: 10.1111/imj.15588
   PubMedGoogle Scholar
• *Lehrnbecher T, Fisher BT, Phillips B, Beauchemin M, Carlesse F, Castagnola E, et al. Clinical Practice Guideline for Systemic Antifungal Prophylaxis in Pediatric Patients With Cancer and Hematopoietic Stem-Cell Transplantation Recipients. J Clin Oncol. 2020;38(27):3205–3216.10.1200/JCO.20.00158
   PubMed Web of Science ®Google Scholar
• Egan G, Tasian SK. Relapsed pediatric acute myeloid leukaemia: state-of-the-art in 2023. Haematologica. 2023;108(9):2275–2288. doi: 10.3324/haematol.2022.281106
   PubMedGoogle Scholar
• Conneely SE, Stevens AM. Acute myeloid leukemia in children: emerging paradigms in genetics and new approaches to therapy. Curr Oncol Rep. 2021;23(2):16. doi: 10.1007/s11912-020-01009-3
   PubMed Web of Science ®Google Scholar
• Lehrnbecher T, Schöning S, Poyer F, et al. Incidence and outcome of invasive fungal diseases in children with hematological malignancies and/or allogeneic hematopoietic stem cell transplantation: results of a prospective multicenter study. Front Microbiol. 2019;10(681):681. doi: 10.3389/fmicb.2019.00681
   PubMedGoogle Scholar
• Kazakou N, Vyzantiadis TA, Gambeta A, et al. Invasive fungal infections in a pediatric hematology-oncology department: a 16-year retrospective study. Curr Med Mycol. 2020;6(2):37–42. doi: 10.18502/cmm.6.2.2840
   PubMedGoogle Scholar
• Mor M, Gilad G, Kornreich L, et al. Invasive fungal infections in pediatric oncology. Pediatr Blood Cancer. 2011;56(7):1092–1097. doi: 10.1002/pbc.23005
   PubMedGoogle Scholar
• Cesaro S, Tridello G, Castagnola E, et al. Retrospective study on the incidence and outcome of proven and probable invasive fungal infections in high-risk pediatric onco-hematological patients. Eur J Haematol. 2017;99(3):240–248. doi: 10.1111/ejh.12910
   PubMed Web of Science ®Google Scholar
• Czyzewski K, Galazka P, Fraczkiewicz J, et al. Epidemiology and outcome of invasive fungal disease in children after hematopoietic cell transplantation or treated for malignancy: impact of national programme of antifungal prophylaxis. Mycoses. 2019;62(11):990–998. doi: 10.1111/myc.12990
   PubMedGoogle Scholar
• Ducassou S, Rivaud D, Auvrignon A, et al. Invasive fungal infections in pediatric acute myelogenous leukemia. Pediatr Infect Dis J. 2015;34(11):1262–1264. doi: 10.1097/INF.0000000000000875
   PubMedGoogle Scholar
• Lin G-L, Chang H-H, Lu C-Y, Chen C-M, Lu M-Y, Lee P-I, et al.. Clinical characteristics and outcome of invasive fungal infections in pediatric acute myeloid leukemia patients in a medical center in Taiwan. Journal of Microbiology, Immunology and Infection. 2018;51(2):251–259. doi: 10.1016/j.jmii.2016.08.011
   Google Scholar
• Yeoh DK, Moore AS, Kotecha RS, et al. Invasive fungal disease in children with acute myeloid leukaemia: an Australian multicentre 10-year review. Pediatr Blood Cancer. 2021;68(11):e29275. doi: 10.1002/pbc.29275
   PubMedGoogle Scholar
• Kobayashi R, Hori D, Sano H, et al. Risk factors for invasive fungal infection in children and adolescents with hematologic and malignant diseases: a 10-year analysis in a single institute in Japan. Pediatr Infect Dis J. 2018;37(12):1282–1285. doi: 10.1097/INF.0000000000002010
   PubMed Web of Science ®Google Scholar
• Ávila Montiel D, Saucedo Campos A, Avilés Robles M, Murillo Maldonado MA, Jiménez Juárez R, Silva Dirzo M, et al. Fungal infections in pediatric patients with acute myeloid leukemia in a tertiary hospital. Front Public Health. 2023;11.
   Google Scholar
• Johnston DL, Lewis V, Yanofsky R, et al. Invasive fungal infections in paediatric acute myeloid leukaemia. Mycoses. 2013;56(4):482–487. doi: 10.1111/myc.12063
   PubMed Web of Science ®Google Scholar
• Calle-Miguel L, Garrido-Colino C, Santiago-García B, et al. Changes in the epidemiology of invasive fungal disease in a pediatric hematology and oncology unit: the relevance of breakthrough infections. BMC Infect Dis. 2023;23(1):348. doi: 10.1186/s12879-023-08314-9
   PubMed Web of Science ®Google Scholar
• Sung L, Aplenc R, Alonzo TA, Gerbing RB, Meshinchi S, Burden L, et al. Severe Toxicities During Pediatric Acute Myeloid Leukemia Chemotherapy: A Report From the Children’s Oncology Group. Blood. 2010;116(21):1071.
   Google Scholar
• Sung L, Aplenc R, Alonzo TA, et al. Effectiveness of supportive care measures to reduce infections in pediatric AML: a report from the Children’s oncology group. Blood. 2013;121(18):3573–3577. doi: 10.1182/blood-2013-01-476614
   PubMed Web of Science ®Google Scholar
• Bochennek K, Hassler A, Perner C, et al. Infectious complications in children with acute myeloid leukemia: decreased mortality in multicenter trial AML-BFM 2004. Blood Cancer J. 2016;6(1):e382. doi: 10.1038/bcj.2015.110
   PubMedGoogle Scholar
• Sung L, Gamis A, Alonzo TA, et al. Infections and association with different intensity of chemotherapy in children with acute myeloid leukemia. Cancer. 2009;115(5):1100–1108. doi: 10.1002/cncr.24107
   PubMed Web of Science ®Google Scholar
• Dix D, Cellot S, Price V, Gillmeister B, Ethier M-C, Johnston DL, et al.. Association Between Corticosteroids and Infection, Sepsis, and Infectious Death in Pediatric Acute Myeloid Leukemia (AML): Results From the Canadian Infections in AML Research Group. Clinical Infectious Diseases. 2012;55(12):1608–1614. doi: 10.1093/cid/cis774
   PubMed Web of Science ®Google Scholar
• Pagano L, Stamouli M, Tumbarello M, et al. Risk of invasive fungal infection in patients affected by acute promyelocytic leukaemia. A report by the SEIFEM-D registry. Br J Haematol. 2015;170(3):434–439. doi: 10.1111/bjh.13308
   PubMedGoogle Scholar
• Cellot S, Johnston D, Dix D, et al. Infections in pediatric acute promyelocytic leukemia: from the Canadian infections in acute myeloid leukemia research group. BMC Cancer. 2013;13(1):276. doi: 10.1186/1471-2407-13-276
   PubMedGoogle Scholar
• Pana ZD, Roilides E, Warris A, et al. Epidemiology of invasive fungal disease in children. J Pediatric Infect Dis Soc. 2017;6(suppl_1):S3–s11. doi: 10.1093/jpids/pix046
   PubMed Web of Science ®Google Scholar
• Otto WR, Green AM. Fungal infections in children with haematologic malignancies and stem cell transplant recipients. Br J Haematol. 2020;189(4):607–624. doi: 10.1111/bjh.16452
   PubMed Web of Science ®Google Scholar
• Cornely OA, Maertens J, Winston DJ, et al. Posaconazole vs. fluconazole or itraconazole prophylaxis in patients with neutropenia. N Engl J Med. 2007;356(4):348–359. doi: 10.1056/NEJMoa061094
   PubMed Web of Science ®Google Scholar
• Fisher BT, Zaoutis T, Dvorak CC, et al. Effect of Caspofungin vs Fluconazole Prophylaxis on Invasive Fungal disease Among Children and young adults with acute myeloid leukemia: a randomized clinical trial. JAMA. 2019;322(17):1673–1681. doi: 10.1001/jama.2019.15702
   PubMed Web of Science ®Google Scholar
• Lai T, Alffenaar J-W, Kesson A, Bandodkar S, Roberts JA. Evaluation of target attainment of oral posaconazole suspension in immunocompromised children. Journal of Antimicrobial Chemotherapy. 2019;75(3):726–9.
   Google Scholar
• Tragiannidis A, Herbrüggen H, Ahlmann M, Vasileiou E, Gastine S, Thorer H, et al.. Plasma exposures following posaconazole delayed-release tablets in immunocompromised children and adolescents. Journal of Antimicrobial Chemotherapy. 2019;74(12):3573–3578. doi: 10.1093/jac/dkz359
   PubMed Web of Science ®Google Scholar
• Bio LL, Hiroshima L, Schwenk HT, Green S. Successful enteral administration of crushed posaconazole delayed-release tablets in children. Pediatric blood & cancer. 2024;71(2):e30782. doi: 10.1002/pbc.30782
   PubMedGoogle Scholar
• Groll AH, Abdel-Azim H, Lehrnbecher T, et al. Pharmacokinetics and safety of posaconazole intravenous solution and powder for oral suspension in children with neutropenia: an open-label, sequential dose-escalation trial. Int J Antimicrob Agents. 2020;56(3):106084. doi: 10.1016/j.ijantimicag.2020.106084
   PubMed Web of Science ®Google Scholar
• Boast A, Curtis N, Cranswick N, et al. Voriconazole dosing and therapeutic drug monitoring in children: experience from a paediatric tertiary care centre. J Antimicrob Chemother. 2016;71(7):2031–2036. doi: 10.1093/jac/dkw056
   PubMed Web of Science ®Google Scholar
• Leong YH, Boast A, Cranswick N, et al. Itraconazole dosing and drug monitoring at a tertiary Children’s hospital. Pediatr Infect Dis J. 2019;38(1):60–64. doi: 10.1097/INF.0000000000002048
   PubMed Web of Science ®Google Scholar
• Lindsay J, Othman J, Kong Y, et al. SUBA-Itraconazole for primary antifungal prophylaxis after Allogeneic Hematopoietic Cell Transplantation. Open Forum Infect Dis. 2021;8(11):ofab502. doi: 10.1093/ofid/ofab502
   PubMed Web of Science ®Google Scholar
• Nield B, Larsen SR, van Hal SJ. Clinical experience with new formulation SUBA®-itraconazole for prophylaxis in patients undergoing stem cell transplantation or treatment for haematological malignancies. J Antimicrob Chemother. 2019;74(10):3049–3055. doi: 10.1093/jac/dkz303
   PubMed Web of Science ®Google Scholar
• Abbotsford J, Foley DA, Goff Z, et al. Clinical experience with SUBA-itraconazole at a tertiary paediatric hospital. J Antimicrob Chemother. 2021;76(1):249–252. doi: 10.1093/jac/dkaa382
   PubMed Web of Science ®Google Scholar
• van Burik JA, Ratanatharathorn V, Stepan DE, Miller CB, Lipton JH, Vesole DH, et al. Micafungin versus fluconazole for prophylaxis against invasive fungal infections during neutropenia in patients undergoing hematopoietic stem cell transplantation. Clin Infect Dis. 2004;39(10):1407–16.
   PubMedGoogle Scholar
• Gil-Navarro MV, Luque-Marquez R, Báez-Gutiérrez N, Álvarez-Marín R, Navarro-Amuedo Mª D, Praena-Segovia J, et al. Antifungal treatment administered in OPAT programs is a safe and effective option in selected patients. Enferm Infecc Microbiol Clin (Engl Ed). 2020;38(10):479–84.
   PubMedGoogle Scholar
• Lehrnbecher T, Bochennek K, Klingebiel T, et al. Extended dosing regimens for fungal prophylaxis. Clin Microbiol Rev. 2019;32(3):e00010–19. doi: 10.1128/CMR.00010-19
   PubMedGoogle Scholar
• Bury D, Wolfs TFW, Muilwijk EW, Fiocco M, Pieters R, Brüggemann RJ, et al. Micafungin twice-a-week for prophylaxis of invasive Aspergillus infections in children with acute lymphoblastic leukaemia: A controlled cohort study. Int J Antimicrob Agents. 2023;63(1):107058.
   PubMedGoogle Scholar
• Bury D, Wolfs TFW, Ter Heine R, et al. Pharmacokinetic evaluation of twice-a-week micafungin for prophylaxis of invasive fungal disease in children with acute lymphoblastic leukaemia: a prospective observational cohort study. J Antimicrob Chemother. 2022;77(3):699–703. doi: 10.1093/jac/dkab467
   PubMedGoogle Scholar
• Thompson GR, III, Soriano A, Cornely OA, Kullberg BJ, Kollef M, Vazquez J, et al.. Rezafungin versus caspofungin for treatment of candidaemia and invasive candidiasis (ReSTORE): a multicentre, double-blind, double-dummy, randomised phase 3 trial. The Lancet. 2023;401(10370):49–59. doi: 10.1016/S0140-6736(22)02324-8
   PubMed Web of Science ®Google Scholar
• Mattiuzzi GN, Estey E, Raad I, et al. Liposomal amphotericin B versus the combination of fluconazole and itraconazole as prophylaxis for invasive fungal infections during induction chemotherapy for patients with acute myelogenous leukemia and myelodysplastic syndrome. Cancer. 2003;97(2):450–456. doi: 10.1002/cncr.11094
   PubMed Web of Science ®Google Scholar
• Cornely OA, Leguay T, Maertens J, et al. Randomized comparison of liposomal amphotericin B versus placebo to prevent invasive mycoses in acute lymphoblastic leukaemia. J Antimicrob Chemother. 2017;72(8):2359–2367. doi: 10.1093/jac/dkx133
   PubMed Web of Science ®Google Scholar
• Bochennek K, Tramsen L, Schedler N, et al. Liposomal amphotericin B twice weekly as antifungal prophylaxis in paediatric haematological malignancy patients. Clin Microbiol Infect. 2011;17(12):1868–1874. doi: 10.1111/j.1469-0691.2011.03483.x
   PubMed Web of Science ®Google Scholar
• Meryk A, Kropshofer G, Hutter J, et al. Benefits of risk-adapted and mould-specific antifungal prophylaxis in childhood leukaemia. Br J Haematol. 2020;191(5):816–824. doi: 10.1111/bjh.16931
   PubMedGoogle Scholar
• Lindsay J, Teh BW, Micklethwaite K, et al. Azole antifungals and new targeted therapies for hematological malignancy. Curr Opin Infect Dis. 2019;32(6):538–545. doi: 10.1097/QCO.0000000000000611
   PubMed Web of Science ®Google Scholar
• Stemler J, Cornely OA. Antifungal Prophylaxis in Acute Myeloid Leukemia: New Drugs, New Challenges?: Summary of the EHA Guideline on Antifungal Prophylaxis in Adult Patients With Acute Myeloid Leukemia Treated With Novel-targeted Therapies. Hemasphere. 2022;6(7):e742. doi: 10.1097/HS9.0000000000000742
   PubMedGoogle Scholar
• Karol SE, Alexander TB, Budhraja A, Pounds SB, Canavera K, Wang L, et al.. Venetoclax in combination with cytarabine with or without idarubicin in children with relapsed or refractory acute myeloid leukaemia: a phase 1, dose-escalation study. The Lancet Oncology. 2020;21(4):551–560. doi: 10.1016/S1470-2045(20)30060-7
   PubMed Web of Science ®Google Scholar
• Karol SE, Bittencourt H, Morgenstern DA, et al. Venetoclax alone or in combination with chemotherapy: responses in pediatric patients with Relapsed/Refractory acute myeloid leukemia with heterogeneous genomic profiles. Blood. 2020;136(Supplement 1):30–31. doi: 10.1182/blood-2020-136999
   Google Scholar
• DiNardo CD, Lachowiez CA, Takahashi K, et al. Venetoclax combined with FLAG-IDA induction and consolidation in newly diagnosed and relapsed or refractory acute myeloid leukemia. J Clin Oncol. 2021;39(25):2768–2778. doi: 10.1200/JCO.20.03736
   PubMed Web of Science ®Google Scholar
• Kadia TM, Reville PK, Borthakur G, Yilmaz M, Kornblau S, Alvarado Y, et al. Venetoclax plus intensive chemotherapy with cladribine, idarubicin, and cytarabine in patients with newly diagnosed acute myeloid leukaemia or high-risk myelodysplastic syndrome: a cohort from a single-centre, single-arm, phase 2 trial. Lancet Haematol. 2021;8(8):e552–e61.
   PubMed Web of Science ®Google Scholar
• Stemler J, de Jonge N, Skoetz N, Sinkó J, Brüggemann RJ, Busca A, et al. Antifungal prophylaxis in adult patients with acute myeloid leukaemia treated with novel targeted therapies: a systematic review and expert consensus recommendation from the European Hematology Association. Lancet Haematol. 2022;9(5):e361–e73.
   PubMedGoogle Scholar
• Aldoss I, Dadwal S, Zhang J, et al. Invasive fungal infections in acute myeloid leukemia treated with venetoclax and hypomethylating agents. Blood Adv. 2019;3(23):4043–4049. doi: 10.1182/bloodadvances.2019000930
   PubMed Web of Science ®Google Scholar
• Stemler J, Mellinghoff SC, Khodamoradi Y, et al. Primary prophylaxis of invasive fungal diseases in patients with haematological malignancies: 2022 update of the recommendations of the infectious diseases working party (AGIHO) of the German society for haematology and medical oncology (DGHO). J Antimicrob Chemother. 2023;78(8):1813–1826. doi: 10.1093/jac/dkad143
   PubMed Web of Science ®Google Scholar
• Agarwal SK, DiNardo CD, Potluri J, et al. Management of Venetoclax-posaconazole interaction in acute myeloid leukemia patients: evaluation of dose adjustments. Clin Ther. 2017;39(2):359–367. doi: 10.1016/j.clinthera.2017.01.003
   PubMed Web of Science ®Google Scholar
• Sun W, Triche T Jr., Malvar J, et al. A phase 1 study of azacitidine combined with chemotherapy in childhood leukemia: a report from the TACL consortium. Blood. 2018;131(10):1145–1148. doi: 10.1182/blood-2017-09-803809
   PubMed Web of Science ®Google Scholar
• Gore L, Triche TJ Jr., Farrar JE, et al. A multicenter, randomized study of decitabine as epigenetic priming with induction chemotherapy in children with AML. Clin Epigenetics. 2017;9(1):108. doi: 10.1186/s13148-017-0411-x
   PubMedGoogle Scholar
• Pommert L, Schafer ES, Malvar J, et al. Decitabine and vorinostat with FLAG chemotherapy in pediatric relapsed/refractory AML: report from the therapeutic advances in childhood leukemia and lymphoma (TACL) consortium. Am J Hematol. 2022;97(5):613–622. doi: 10.1002/ajh.26510
   PubMedGoogle Scholar
• Schafer ES, Chao K, Stevens AM, et al. Real-world experience in treating pediatric relapsed/refractory or therapy-related myeloid malignancies with decitabine, vorinostat, and FLAG therapy based on a phase 1 study run by the TACL consortium. Pediatr Blood Cancer. 2022;69(10):e29812. doi: 10.1002/pbc.29812
   PubMedGoogle Scholar
• Pollard JA, Alonzo TA, Gerbing R, Brown P, Fox E, Choi J, et al. Sorafenib in Combination With Standard Chemotherapy for Children With High Allelic Ratio FLT3/ITD+ Acute Myeloid Leukemia: A Report From the Children’s Oncology Group Protocol AAML1031. Journal of Clinical Oncology. 2022;40(18):2023–35.
   PubMed Web of Science ®Google Scholar
• Aldoss I, Issa GC, Thirman M, DiPersio J, Arellano M, Blachly JS, et al. Revumenib Monotherapy in Patients with Relapsed/Refractory KMT2Ar Acute Leukemia: Topline Efficacy and Safety Results from the Pivotal Augment-101 Phase 2 Study. Blood. 2023;142(Supplement 2):LBA-5-LBA-.
   Google Scholar
• Issa GC, Aldoss I, DiPersio J, et al. The menin inhibitor revumenib in KMT2A-rearranged or NPM1-mutant leukaemia. Nature. 2023;615(7954):920–924. doi: 10.1038/s41586-023-05812-3
   PubMed Web of Science ®Google Scholar
• Cooper TM, Alonzo TA, Tasian SK, Kutny MA, Hitzler J, Pollard JA, et al.. Children’s Oncology Group’s 2023 blueprint for research: Myeloid neoplasms. Pediatric Blood & Cancer. 2023;70(S6):e30584. doi: 10.1002/pbc.30584
   PubMedGoogle Scholar
• Gamis AS, Alonzo TA, Meshinchi S, Sung L, Gerbing RB, Raimondi SC, et al. Gemtuzumab Ozogamicin in Children and Adolescents With De Novo Acute Myeloid Leukemia Improves Event-Free Survival by Reducing Relapse Risk: Results From the Randomized Phase III Children’s Oncology Group Trial AAML0531. Journal of Clinical Oncology. 2014;32(27):3021–32.
   PubMed Web of Science ®Google Scholar