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Prevention and Epidemiology

Correlates of Prenatal and Early-Life Tobacco Smoke Exposure and Frequency of Common Gene Deletions in Childhood Acute Lymphoblastic Leukemia

Adam J. de Smith, Maneet Kaur, Semira Gonseth, Alyson Endicott, Steve Selvin, Luoping Zhang, Ritu Roy, Xiaorong Shao, Helen M. Hansen, Alice Y. Kang, Kyle M. Walsh, Gary V. Dahl, Roberta McKean-Cowdin, Catherine Metayer and Joseph L. Wiemels
Adam J. de Smith
Department of Epidemiology and Biostatistics, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.
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  • For correspondence: adam.desmith@ucsf.edu
Maneet Kaur
School of Public Health, University of California Berkeley, Berkeley, California.
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Semira Gonseth
School of Public Health, University of California Berkeley, Berkeley, California.
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Alyson Endicott
Department of Epidemiology and Biostatistics, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.
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Steve Selvin
School of Public Health, University of California Berkeley, Berkeley, California.
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Luoping Zhang
School of Public Health, University of California Berkeley, Berkeley, California.
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Ritu Roy
Computational Biology Core, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.
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Xiaorong Shao
School of Public Health, University of California Berkeley, Berkeley, California.
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Helen M. Hansen
Department of Neurological Surgery, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.
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Alice Y. Kang
School of Public Health, University of California Berkeley, Berkeley, California.
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Kyle M. Walsh
Department of Epidemiology and Biostatistics, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.Department of Neurological Surgery, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.
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Gary V. Dahl
Stanford University School of Medicine, Stanford, California.
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Roberta McKean-Cowdin
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California.
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Catherine Metayer
School of Public Health, University of California Berkeley, Berkeley, California.
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Joseph L. Wiemels
Department of Epidemiology and Biostatistics, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.Department of Neurological Surgery, Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, California.
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DOI: 10.1158/0008-5472.CAN-16-2571
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Abstract

Tobacco smoke exposure has been associated with risk of childhood acute lymphoblastic leukemia (ALL). Understanding the relationship between tobacco exposures and specific mutations may yield etiologic insights. We carried out a case-only analysis to explore whether prenatal and early-life tobacco smoke exposure influences the formation of leukemogenic genomic deletions. Somatic copy number of 8 genes frequently deleted in ALL (CDKN2A, ETV6, IKZF1, PAX5, RB1, BTG1, PAR1 region, and EBF1) was assessed in 559 pretreatment tumor samples from the California Childhood Leukemia Study. Parent and child's passive tobacco exposure was assessed using interview-assisted questionnaires as well as DNA methylation in aryl-hydrocarbon receptor repressor (AHRR), a sentinel epigenetic biomarker of exposure to maternal smoking during pregnancy. Multivariable Poisson regressions were used to test the association between the smoking exposures and total number of deletions. Deletion burden varied by subtype, with a lower frequency in high-hyperdiploid and higher frequency in ETV6–RUNX1 fusion ALL. The total number of deletions per case was positively associated with tobacco smoke exposure, in particular for maternal ever-smoking (ratio of means, RM, 1.31; 95% CI, 1.08–1.59), maternal smoking during pregnancy (RM, 1.48; 95% CI, 1.12–1.94), and during breastfeeding (RM, 2.11; 95% CI, 1.48–3.02). The magnitude of association with maternal ever-smoking was stronger in male children compared with females (P interaction = 0.04). The total number of deletions was also associated with DNA methylation at the AHRR epigenetic biomarker (RM, 1.32; 95% CI, 1.02–1.69). Our results suggest that prenatal and early-life tobacco smoke exposure increase the frequency of somatic deletions in children who develop ALL. Cancer Res; 77(7); 1–10. ©2017 AACR.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Research Online (http://cancerres.aacrjournals.org/).

  • C. Metayer and J.L. Wiemels codirected this work.

  • Received September 19, 2016.
  • Revision received December 22, 2016.
  • Accepted January 11, 2017.
  • ©2017 American Association for Cancer Research.
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Published OnlineFirst March 22, 2017
doi: 10.1158/0008-5472.CAN-16-2571

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Correlates of Prenatal and Early-Life Tobacco Smoke Exposure and Frequency of Common Gene Deletions in Childhood Acute Lymphoblastic Leukemia
Adam J. de Smith, Maneet Kaur, Semira Gonseth, Alyson Endicott, Steve Selvin, Luoping Zhang, Ritu Roy, Xiaorong Shao, Helen M. Hansen, Alice Y. Kang, Kyle M. Walsh, Gary V. Dahl, Roberta McKean-Cowdin, Catherine Metayer and Joseph L. Wiemels
Cancer Res March 22 2017 DOI: 10.1158/0008-5472.CAN-16-2571

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Correlates of Prenatal and Early-Life Tobacco Smoke Exposure and Frequency of Common Gene Deletions in Childhood Acute Lymphoblastic Leukemia
Adam J. de Smith, Maneet Kaur, Semira Gonseth, Alyson Endicott, Steve Selvin, Luoping Zhang, Ritu Roy, Xiaorong Shao, Helen M. Hansen, Alice Y. Kang, Kyle M. Walsh, Gary V. Dahl, Roberta McKean-Cowdin, Catherine Metayer and Joseph L. Wiemels
Cancer Res March 22 2017 DOI: 10.1158/0008-5472.CAN-16-2571
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Cancer Research Online ISSN: 1538-7445
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