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Radiation exposure and leukaemia risk among cohorts of persons exposed to low and moderate doses of external ionising radiation in childhood

British Journal of Cancer volume 129, pages 1152–1165 (2023)Cite this article

Subjects

Abstract

Background

Many high-dose groups demonstrate increased leukaemia risks, with risk greatest following childhood exposure; risks at low/moderate doses are less clear.

Methods

We conducted a pooled analysis of the major radiation-associated leukaemias (acute myeloid leukaemia (AML) with/without the inclusion of myelodysplastic syndrome (MDS), chronic myeloid leukaemia (CML), acute lymphoblastic leukaemia (ALL)) in ten childhood-exposed groups, including Japanese atomic bomb survivors, four therapeutically irradiated and five diagnostically exposed cohorts, a mixture of incidence and mortality data. Relative/absolute risk Poisson regression models were fitted.

Results

Of 365 cases/deaths of leukaemias excluding chronic lymphocytic leukaemia, there were 272 AML/CML/ALL among 310,905 persons (7,641,362 person-years), with mean active bone marrow (ABM) dose of 0.11 Gy (range 0–5.95). We estimated significant (P < 0.005) linear excess relative risks/Gy (ERR/Gy) for: AML (n = 140) = 1.48 (95% CI 0.59–2.85), CML (n = 61) = 1.77 (95% CI 0.38–4.50), and ALL (n = 71) = 6.65 (95% CI 2.79–14.83). There is upward curvature in the dose response for ALL and AML over the full dose range, although at lower doses (<0.5 Gy) curvature for ALL is downwards.

Discussion

We found increased ERR/Gy for all major types of radiation-associated leukaemia after childhood exposure to ABM doses that were predominantly (for 99%) <1 Gy, and consistent with our prior analysis focusing on <100 mGy.

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Fig. 1: Relative risk (and 95% CI) by mean whole-body-averaged cumulative active bone marrow dose by leukaemia subtype.

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Data availability

The data are available from the first author upon request.

Code availability

All Epicure [32] and R [34] code used can be obtained from the principal author upon request.

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Funding

This work was supported by the Intramural Research Program of the National Institutes of Health, National Cancer Institute, Division of Cancer Epidemiology and Genetics. The Radiation Effects Research Foundation (RERF), Hiroshima and Nagasaki, Japan is a public interest foundation funded by the Japanese Ministry of Health, Labour and Welfare (MHLW) and the US Department of Energy (DOE). The research was also funded in part through DOE award DE-HS0000031 to the National Academy of Sciences. Dr Zablotska’s work was supported by the National Cancer Institute of the National Institutes of Health under the R01CA197422 award. This publication was supported by RERF Research Protocol A1-16. The views of the authors do not necessarily reflect those of the two governments.

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Author notes

  1. These authors contributed equally: Mark P. Little, Richard Wakeford, Lydia B. Zablotska, Michael Jacob Adams, Amy Berrington de González, Martha S. Linet.

  2. Deceased: Marie Lundell.

Authors and Affiliations

  1. Radiation Epidemiology Branch, National Cancer Institute, 9609 Medical Center Drive, Bethesda, MD, 20892-9778, USA

    Mark P. Little, David Borrego, Keith T. Griffin, Choonsik Lee, Alina V. Brenner, Michele M. Doody, Amy Berrington de González & Martha S. Linet

  2. Centre for Occupational and Environmental Health, Faculty of Biology, Medicine and Health, The University of Manchester, Ellen Wilkinson Building, Oxford Road, Manchester, M13 9PL, UK

    Richard Wakeford

  3. Department of Epidemiology & Biostatistics, School of Medicine, University of California, San Francisco, 550 16th Street, 2nd floor, San Francisco, CA, 94143, USA

    Lydia B. Zablotska

  4. Equipe d’Epidémiologie des radiations, Unité 1018 INSERM, Bâtiment B2M, Institut Gustave Roussy, Villejuif, Cedex, 94805, France

    Rodrigue S. Allodji & Florent de Vathaire

  5. Information Management Services, Silver Spring, MD, 20904, USA

    Jeremy S. Miller & David Campbell

  6. Institute of Health and Society, Newcastle University, Sir James Spence Institute, Royal Victoria Infirmary, Queen Victoria Road, Newcastle upon Tyne, NE1 4LP, UK

    Mark S. Pearce

  7. NIHR Health Protection Research Unit in chemical and radiation threats and hazards, Newcastle University, Newcastle upon Tyne, UK

    Mark S. Pearce

  8. Israel Ministry of Health, Jerusalem, Israel

    Siegal Sadetzki

  9. Cancer & Radiation Epidemiology Unit, Gertner Institute for Epidemiology & Health Policy Research, Sheba Medical Center, Tel-Hashomer, Israel & Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv-Yafo, Israel

    Siegal Sadetzki

  10. Department of Oncology, Sahlgrenska University Hospital, S-413-45, Göteborg, Sweden

    Erik Holmberg

  11. Department of Medical Radiation Physics and Nuclear Medicine, Karolinska University Hospital, S-17176, Stockholm, Sweden

    Marie Lundell

  12. Department of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA

    Benjamin French

  13. University of Rochester School of Medicine and Dentistry, 265 Crittenden Boulevard, CU 420644, Rochester, NY, 14642-0644, USA

    Michael Jacob Adams

  14. Division of Genetics and Epidemiology, Institute of Cancer Research, London, UK

    Amy Berrington de González

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Contributions

All authors contributed to the study’s conception and design. Material preparation, data collection and analysis were performed by Mark Little with assistance from Jeremy Miller and David Campbell. The first draft of the manuscript was written by Mark Little and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mark P. Little.

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Competing interests

Richard Wakeford is a member of the Technical Working Party of the UK Compensation Scheme for Radiation-Linked Diseases (http://www.csrld.org.uk), for which he is paid a consultancy fee. The Technical Working Party is unaware of the contents of this article, which are entirely independent of any views held by other members of the Technical Working Party. The remaining authors declare no competing interests.

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This study cohort has been declared exempt from requiring ethical approval by the NCI Special Studies Institution Review Board because we used preexisting approved data. Because of the size and age of these cohorts, and the fact that they were retrospectively assembled in many cases, individual informed consent could not have been obtained for most studies. However, in all cases, the exemption was granted by the relevant ethical review boards.

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Little, M.P., Wakeford, R., Zablotska, L.B. et al. Radiation exposure and leukaemia risk among cohorts of persons exposed to low and moderate doses of external ionising radiation in childhood. Br J Cancer 129, 1152–1165 (2023). https://doi.org/10.1038/s41416-023-02387-8

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  • DOI: https://doi.org/10.1038/s41416-023-02387-8

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