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Maternal smoking during pregnancy, genetic polymorphisms of metabolic enzymes, and childhood acute leukemia: the ESCALE Study (SFCE)

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Abstract

Purpose

This study explored interactions between prenatal exposure to maternal smoking and polymorphisms in metabolic genes in the risk of childhood acute leukemia (AL).

Methods

The data were generated by the ESCALE study, which included 764 AL cases and 1,681 controls in 2003–2004. The data on maternal smoking during pregnancy were obtained by standardized telephone interview of the cases’ and controls’ mothers. The genotypes CYP1A1*2A/2B (rs4646903), CYP2E1*5 (rs2031920, rs3813867), NQO1*2 (rs1800566), NAT2*5 (rs1801280), and EPHX1 exon 3 (rs1051740) and exon 4 (rs2234922) were obtained using a high-throughput platform and imputation for untyped polymorphisms. The analyses were restricted to the 493 cases (433 cases of lymphoblastic (ALL) and 51 of myeloblastic (AML) leukemia) and 441 controls with at least 2 grandparents born in Europe, who were genotyped with individual call rates greater than 95%. Odds ratios were estimated by logistic regression in case–control analyses and, for gene–gene and gene–environment interactions, by case-only analyses.

Results

ALL and AML were not associated with either maternal smoking during pregnancy or candidate polymorphisms in CYP1A1, CYP2E1, EPHX1, and NQO1. Carrying two NAT2*5 alleles was significantly associated with ALL (OR = 1.8 [1.3–2.5]). The analyses also suggested an interaction between three genes involved in benzene metabolism CYP2E1, NQO1, and EPHX1. There was no interaction between maternal smoking and any of the polymorphisms under study.

Conclusions

The ESCALE study did not evidence the interaction between CYP1A1*2A/2B and maternal smoking suggested previously. The association with NAT2*5 and the gene–gene interactions need to be replicated.

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Abbreviations

AL:

Acute leukemia

ALL:

Acute lymphoblastic leukemia

AML:

Acute myeloblastic leukemia

CEU:

Utah residents with Northern and Western European ancestry from the CEPH collection

CEPH:

Centre d’Etude du Polymorphisme Humain

EPHX1:

Epoxide hydrolase 1

CYP1A1:

Cytochrome P450 1A1

CYP2E1:

Cytochrome P450 2E1

NAT2:

N-Acetyltransferase 2

NQO1:

NAD(P)H dehydrogenase quinone type 1

PAH:

Polycyclic aromatic hydrocarbons

References

  1. Little J (1999) Lifestyle. In: Epidemiology of childhood cancer, vol 149. IARC Scientific Publications. International Agency for Research on Cancer, Lyon, pp 245–247

  2. Chang JS (2009) Parental smoking and childhood leukemia. Methods Mol Biol 472:103–137. doi:10.1007/978-1-60327-492-0_5

    Article  PubMed  Google Scholar 

  3. Neutel CI, Buck C (1971) Effect of smoking during pregnancy on the risk of cancer in children. J Natl Cancer Inst 47(1):59–63

    PubMed  CAS  Google Scholar 

  4. van Steensel-Moll HA, Valkenburg HA, Vandenbroucke JP, van Zanen GE (1985) Are maternal fertility problems related to childhood leukaemia? Int J Epidemiol 14(4):555–559

    Article  PubMed  Google Scholar 

  5. McKinney PA, Cartwright RA, Saiu JM, Mann JR, Stiller CA, Draper GJ, Hartley AL, Hopton PA, Birch JM, Waterhouse JA et al (1987) The inter-regional epidemiological study of childhood cancer (IRESCC): a case control study of aetiological factors in leukaemia and lymphoma. Arch Dis Child 62(3):279–287

    Article  PubMed  CAS  Google Scholar 

  6. Pershagen G, Ericson A, Otterblad-Olausson P (1992) Maternal smoking in pregnancy: does it increase the risk of childhood cancer? Int J Epidemiol 21(1):1–5

    Article  PubMed  CAS  Google Scholar 

  7. Severson RK, Buckley JD, Woods WG, Benjamin D, Robison LL (1993) Cigarette smoking and alcohol consumption by parents of children with acute myeloid leukemia: an analysis within morphological subgroups—a report from the Childrens Cancer Group. Cancer Epidemiol Biomarkers Prev 2(5):433–439

    PubMed  CAS  Google Scholar 

  8. Brondum J, Shu XO, Steinbuch M, Severson RK, Potter JD, Robison LL (1999) Parental cigarette smoking and the risk of acute leukemia in children. Cancer 85(6):1380–1388

    Article  PubMed  CAS  Google Scholar 

  9. Cnattingius S, Zack MM, Ekbom A, Gunnarskog J, Kreuger A, Linet M, Adami HO (1995) Prenatal and neonatal risk factors for childhood lymphatic leukemia. J Natl Cancer Inst 87(12):908–914

    Article  PubMed  CAS  Google Scholar 

  10. Cnattingius S, Zack M, Ekbom A, Gunnarskog J, Linet M, Adami HO (1995) Prenatal and neonatal risk factors for childhood myeloid leukemia. Cancer Epidemiol Biomarkers Prev 4(5):441–445

    PubMed  CAS  Google Scholar 

  11. Sorahan T, Lancashire R, Prior P, Peck I, Stewart A (1995) Childhood cancer and parental use of alcohol and tobacco. Ann Epidemiol 5(5):354–359

    Article  PubMed  CAS  Google Scholar 

  12. Klebanoff MA, Clemens JD, Read JS (1996) Maternal smoking during pregnancy and childhood cancer. Am J Epidemiol 144(11):1028–1033

    PubMed  CAS  Google Scholar 

  13. Petridou E, Trichopoulos D, Kalapothaki V, Pourtsidis A, Kogevinas M, Kalmanti M, Koliouskas D, Kosmidis H, Panagiotou JP, Piperopoulou F, Tzortzatou F (1997) The risk profile of childhood leukaemia in Greece: a nationwide case–control study. Br J Cancer 76(9):1241–1247

    Article  PubMed  CAS  Google Scholar 

  14. Schuz J, Kaatsch P, Kaletsch U, Meinert R, Michaelis J (1999) Association of childhood cancer with factors related to pregnancy and birth. Int J Epidemiol 28(4):631–639

    Article  PubMed  CAS  Google Scholar 

  15. Infante-Rivard C, Krajinovic M, Labuda D, Sinnett D (2000) Parental smoking, CYP1A1 genetic polymorphisms and childhood leukemia (Quebec, Canada). Cancer Causes Control 11(6):547–553

    Article  PubMed  CAS  Google Scholar 

  16. Okcu MF, Goodman KJ, Carozza SE, Weiss NS, Burau KD, Bleyer WA, Cooper SP (2002) Birth weight, ethnicity, and occurrence of cancer in children: a population-based, incident case–control study in the State of Texas, USA. Cancer Causes Control 13(7):595–602

    Article  PubMed  Google Scholar 

  17. Clavel J, Bellec S, Rebouissou S, Menegaux F, Feunteun J, Bonaiti-Pellie C, Baruchel A, Kebaili K, Lambilliotte A, Leverger G, Sommelet D, Lescoeur B, Beaune P, Hemon D, Loriot MA (2005) Childhood leukaemia, polymorphisms of metabolism enzyme genes, and interactions with maternal tobacco, coffee and alcohol consumption during pregnancy. Eur J Cancer Prev 14(6):531–540

    Article  PubMed  Google Scholar 

  18. Menegaux F, Ripert M, Hemon D, Clavel J (2007) Maternal alcohol and coffee drinking, parental smoking and childhood leukaemia: a French population-based case–control study. Paediatr Perinat Epidemiol 21(4):293–299

    Article  PubMed  Google Scholar 

  19. MacArthur AC, McBride ML, Spinelli JJ, Tamaro S, Gallagher RP, Theriault G (2008) Risk of childhood leukemia associated with parental smoking and alcohol consumption prior to conception and during pregnancy: the cross-Canada childhood leukemia study. Cancer Causes Control 19(3):283–295

    Article  PubMed  Google Scholar 

  20. Rudant J, Menegaux F, Leverger G, Baruchel A, Lambilliotte A, Bertrand Y, Patte C, Pacquement H, Verite C, Robert A, Michel G, Margueritte G, Gandemer V, Hemon D, Clavel J (2008) Childhood hematopoietic malignancies and parental use of tobacco and alcohol: the ESCALE study (SFCE). Cancer Causes Control 19(10):1277–1290

    Article  PubMed  Google Scholar 

  21. John EM, Savitz DA, Sandler DP (1991) Prenatal exposure to parents’ smoking and childhood cancer. Am J Epidemiol 133(2):123–132

    PubMed  CAS  Google Scholar 

  22. Stjernfeldt M, Berglund K, Lindsten J, Ludvigsson J (1986) Maternal smoking during pregnancy and risk of childhood cancer. Lancet 1(8494):1350–1352

    Article  PubMed  CAS  Google Scholar 

  23. Mucci LA, Granath F, Cnattingius S (2004) Maternal smoking and childhood leukemia and lymphoma risk among 1,440,542 Swedish children. Cancer Epidemiol Biomarkers Prev 13(9):1528–1533

    PubMed  CAS  Google Scholar 

  24. Shu XO, Ross JA, Pendergrass TW, Reaman GH, Lampkin B, Robison LL (1996) Parental alcohol consumption, cigarette smoking, and risk of infant leukemia: a Childrens Cancer Group study. J Natl Cancer Inst 88(1):24–31

    Article  PubMed  CAS  Google Scholar 

  25. Pang D, McNally R, Birch JM (2003) Parental smoking and childhood cancer: results from the United Kingdom Childhood Cancer Study. Br J Cancer 88(3):373–381

    Article  PubMed  CAS  Google Scholar 

  26. Lang M, Pelkonen O (1999) Metabolism of xenobiotics and chemical carcinogenesis. In: Vineis P, Malats N, Lang M, d’Errico A, Caporaso N, Cuzick J, Boffetta P (eds) Metabolic polymorphisms and susceptibility to cancer, vol 148. IARC Scientific Publications. International Agency for Research on Cancer, Lyon, pp 13–22

  27. Vijayakrishnan J, Houlston RS (2010) Candidate gene association studies and risk of childhood acute lymphoblastic leukemia: a systematic review and meta-analysis. Haematologica 95(8):1405–1414. doi:10.3324/haematol.2010.022095

    Article  PubMed  CAS  Google Scholar 

  28. Traver RD, Siegel D, Beall HD, Phillips RM, Gibson NW, Franklin WA, Ross D (1997) Characterization of a polymorphism in NAD(P)H: quinone oxidoreductase (DT-diaphorase). Br J Cancer 75(1):69–75

    Article  PubMed  CAS  Google Scholar 

  29. Guha N, Chang JS, Chokkalingam AP, Wiemels JL, Smith MT, Buffler PA (2008) NQO1 polymorphisms and de novo childhood leukemia: a HuGE review and meta-analysis. Am J Epidemiol 168(11):1221–1232

    Article  PubMed  Google Scholar 

  30. Silveira Vda S, Canalle R, Scrideli CA, Queiroz RG, Tone LG (2010) Role of the CYP2D6, EPHX1, MPO, and NQO1 genes in the susceptibility to acute lymphoblastic leukemia in Brazilian children. Environ Mol Mutagen 51(1):48–56

    PubMed  Google Scholar 

  31. Arylamine N-acetyltransferase Gene Nomenclature Committee. Human NAT2 alleles/haplotypes. (2010) http://louisville.edu/medschool/pharmacology/consensus-human-arylamine-n-acetyltransferase-gene-nomenclature/nat_pdf_files/Human_NAT2_alleles.pdf

  32. Grant DM, Hughes NC, Janezic SA, Goodfellow GH, Chen HJ, Gaedigk A, Yu VL, Grewal R (1997) Human acetyltransferase polymorphisms. Mutat Res 376(1–2):61–70

    PubMed  CAS  Google Scholar 

  33. Krajinovic M, Richer C, Sinnett H, Labuda D, Sinnett D (2000) Genetic polymorphisms of N-acetyltransferases 1 and 2 and gene–gene interaction in the susceptibility to childhood acute lymphoblastic leukemia. Cancer Epidemiol Biomarkers Prev 9(6):557–562

    PubMed  CAS  Google Scholar 

  34. Zanrosso CW, Emerenciano M, Goncalves BA, Faro A, Koifman S, Pombo-de-Oliveira MS (2010) N-acetyltransferase 2 polymorphisms and susceptibility to infant leukemia with maternal exposure to dipyrone during pregnancy. Cancer Epidemiol Biomarkers Prev 19(12):3037–3043. doi:10.1158/1055-9965.epi-10-0508

    Article  PubMed  CAS  Google Scholar 

  35. Zanrosso CW, Emerenciano M, Faro A, de Aguiar Goncalves BA, Mansur MB, Pombo-de-Oliveira MS (2011) Genetic variability in N-Acetyltransferase 2 gene determines susceptibility to childhood lymphoid or myeloid leukemia in Brazil. Leuk Lymphoma. doi:10.3109/10428194.2011.619605

  36. Krajinovic M, Sinnett H, Richer C, Labuda D, Sinnett D (2002) Role of NQO1, MPO and CYP2E1 genetic polymorphisms in the susceptibility to childhood acute lymphoblastic leukemia. Int J Cancer 97(2):230–236

    Article  PubMed  CAS  Google Scholar 

  37. Canalle R, Burim RV, Tone LG, Takahashi CS (2004) Genetic polymorphisms and susceptibility to childhood acute lymphoblastic leukemia. Environ Mol Mutagen 43(2):100–109. doi:10.1002/em.20003

    Article  PubMed  CAS  Google Scholar 

  38. Thomas D (2010) Methods for investigating gene-environment interactions in candidate pathway and genome-wide association studies. Annu Rev Public Health 31:21–36. doi:10.1146/annurev.publhealth.012809.103619

    Article  PubMed  Google Scholar 

  39. Mallol-Mesnard N, Menegaux F, Auvrignon A, Auclerc MF, Bertrand Y, Nelken B, Robert A, Michel G, Margueritte G, Perel Y, Mechinaud F, Bordigoni P, Leverger G, Baruchel A, Hemon D, Clavel J (2007) Vaccination and the risk of childhood acute leukaemia: the ESCALE study (SFCE). Int J Epidemiol 36(1):110–116. doi:10.1093/ije/dyl270

    Article  PubMed  Google Scholar 

  40. Rudant J, Menegaux F, Leverger G, Baruchel A, Nelken B, Bertrand Y, Hartmann O, Pacquement H, Verite C, Robert A, Michel G, Margueritte G, Gandemer V, Hemon D, Clavel J (2007) Family history of cancer in children with acute leukemia, Hodgkin’s lymphoma or non-Hodgkin’s lymphoma: the ESCALE study (SFCE). Int J Cancer 121(1):119–126. doi:10.1002/ijc.22624

    Article  PubMed  CAS  Google Scholar 

  41. Rudant J, Menegaux F, Leverger G, Baruchel A, Nelken B, Bertrand Y, Patte C, Pacquement H, Verite C, Robert A, Michel G, Margueritte G, Gandemer V, Hemon D, Clavel J (2007) Household exposure to pesticides and risk of childhood hematopoietic malignancies: the ESCALE study (SFCE). Environ Health Perspect 115(12):1787–1793. doi:10.1289/ehp.10596

    Article  PubMed  Google Scholar 

  42. Brosselin P, Rudant J, Orsi L, Leverger G, Baruchel A, Bertrand Y, Nelken B, Robert A, Michel G, Margueritte G, Perel Y, Mechinaud F, Bordigoni P, Hemon D, Clavel J (2009) Acute childhood leukaemia and residence next to petrol stations and automotive repair garages: the ESCALE study (SFCE). Occup Environ Med 66(9):598–606. doi:10.1136/oem.2008.042432

    Article  PubMed  CAS  Google Scholar 

  43. Rudant J, Orsi L, Menegaux F, Petit A, Baruchel A, Bertrand Y, Lambilliotte A, Robert A, Michel G, Margueritte G, Tandonnet J, Mechinaud F, Bordigoni P, Hemon D, Clavel J (2010) Childhood acute leukemia, early common infections, and allergy: the ESCALE Study. Am J Epidemiol 172(9):1015–1027. doi:10.1093/aje/kwq233

    Article  PubMed  Google Scholar 

  44. Amigou A, Sermage-Faure C, Orsi L, Leverger G, Baruchel A, Bertrand Y, Nelken B, Robert A, Michel G, Margueritte G, Perel Y, Mechinaud F, Bordigoni P, Hemon D, Clavel J (2011) Road traffic and childhood leukemia: the ESCALE study (SFCE). Environ Health Perspect 119(4):566–572. doi:10.1289/ehp.1002429

    Article  PubMed  CAS  Google Scholar 

  45. Howie BN, Donnelly P, Marchini J (2009) A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet 5(6):e1000529. doi:10.1371/journal.pgen.1000529

  46. Baxter SW, Choong DY, Campbell IG (2002) Microsomal epoxide hydrolase polymorphism and susceptibility to ovarian cancer. Cancer Lett 177(1):75–81

    Article  PubMed  CAS  Google Scholar 

  47. Li X, Hu Z, Qu X, Zhu J, Li L, Ring BZ, Su L (2011) Putative EPHX1 enzyme activity is related with risk of lung and upper aerodigestive tract cancers: a comprehensive meta-analysis. PLoS One 6(3):e14749. doi:10.1371/journal.pone.0014749

  48. Ross D, Siegel D (2004) NAD(P)H: quinone oxidoreductase 1 (NQO1, DT-diaphorase), functions and pharmacogenetics. Methods Enzymol 382:115–144

    Article  PubMed  CAS  Google Scholar 

  49. Blondel B, Breart G, du Mazaubrun C, Badeyan G, Wcislo M, Lordier A, Matet N (1997) The perinatal situation in France. Trends between 1981 and 1995. J Gynecol Obstet Biol Reprod (Paris) 26(8):770–780

    CAS  Google Scholar 

  50. Blondel B, Norton J, du Mazaubrun C, Breart G (2001) Development of the main indicators of perinatal health in metropolitan France between 1995 and 1998. Results of the national perinatal survey. J Gynecol Obstet Biol Reprod (Paris) 30(6):552–564

    CAS  Google Scholar 

  51. Blondel B, Supernant K, Du Mazaubrun C, Breart G (2006) Trends in perinatal health in metropolitan France between 1995 and 2003: results from the national perinatal surveys. J Gynecol Obstet Biol Reprod (Paris) 35(4):373–387

    CAS  Google Scholar 

  52. McCarver DG, Hines RN (2002) The ontogeny of human drug-metabolizing enzymes: phase II conjugation enzymes and regulatory mechanisms. J Pharmacol Exp Ther 300(2):361–366

    Article  PubMed  CAS  Google Scholar 

  53. Hines RN, McCarver DG (2002) The ontogeny of human drug-metabolizing enzymes: phase I oxidative enzymes. J Pharmacol Exp Ther 300(2):355–360

    Article  PubMed  CAS  Google Scholar 

  54. Yang Q, Khoury MJ, Flanders WD (1997) Sample size requirements in case-only designs to detect gene-environment interaction. Am J Epidemiol 146(9):713–720

    PubMed  CAS  Google Scholar 

  55. Khoury MJ, Flanders WD (1996) Nontraditional epidemiologic approaches in the analysis of gene-environment interaction: case–control studies with no controls! Am J Epidemiol 144(3):207–213

    PubMed  CAS  Google Scholar 

  56. Smith MT (2010) Advances in understanding benzene health effects and susceptibility. Annu Rev Public Health 31:133–148 (2 p following 148). doi:10.1146/annurev.publhealth.012809.103646

    Google Scholar 

  57. Dougherty D, Garte S, Barchowsky A, Zmuda J, Taioli E (2008) NQO1, MPO, CYP2E1, GSTT1 and GSTM1 polymorphisms and biological effects of benzene exposure–a literature review. Toxicol Lett 182(1–3):7–17. doi:10.1016/j.toxlet.2008.09.008

    Article  PubMed  CAS  Google Scholar 

  58. Krajinovic M, Labuda D, Richer C, Karimi S, Sinnett D (1999) Susceptibility to childhood acute lymphoblastic leukemia: influence of CYP1A1, CYP2D6, GSTM1, and GSTT1 genetic polymorphisms. Blood 93(5):1496–1501

    PubMed  CAS  Google Scholar 

  59. Balta G, Yuksek N, Ozyurek E, Ertem U, Hicsonmez G, Altay C, Gurgey A (2003) Characterization of MTHFR, GSTM1, GSTT1, GSTP1, and CYP1A1 genotypes in childhood acute leukemia. Am J Hematol 73(3):154–160. doi:10.1002/ajh.10339

    Article  PubMed  CAS  Google Scholar 

  60. Pakakasama S, Mukda E, Sasanakul W, Kadegasem P, Udomsubpayakul U, Thithapandha A, Hongeng S (2005) Polymorphisms of drug-metabolizing enzymes and risk of childhood acute lymphoblastic leukemia. Am J Hematol 79(3):202–205

    Article  PubMed  CAS  Google Scholar 

  61. Joseph T, Kusumakumary P, Chacko P, Abraham A, Radhakrishna Pillai M (2004) Genetic polymorphism of CYP1A1, CYP2D6, GSTM1 and GSTT1 and susceptibility to acute lymphoblastic leukaemia in Indian children. Pediatr Blood Cancer 43(5):560–567. doi:10.1002/pbc.20074

    Article  PubMed  Google Scholar 

  62. Aydin-Sayitoglu M, Hatirnaz O, Erensoy N, Ozbek U (2006) Role of CYP2D6, CYP1A1, CYP2E1, GSTT1, and GSTM1 genes in the susceptibility to acute leukemias. Am J Hematol 81(3):162–170. doi:10.1002/ajh.20434

    Article  PubMed  CAS  Google Scholar 

  63. Bolufer P, Collado M, Barragan E, Cervera J, Calasanz MJ, Colomer D, Roman-Gomez J, Sanz MA (2007) The potential effect of gender in combination with common genetic polymorphisms of drug-metabolizing enzymes on the risk of developing acute leukemia. Haematologica 92(3):308–314

    Article  PubMed  CAS  Google Scholar 

  64. Lee KM, Ward MH, Han S, Ahn HS, Kang HJ, Choi HS, Shin HY, Koo HH, Seo JJ, Choi JE, Ahn YO, Kang D (2009) Paternal smoking, genetic polymorphisms in CYP1A1 and childhood leukemia risk. Leuk Res 33(2):250–258. doi:10.1016/j.leukres.2008.06.031

    Article  PubMed  CAS  Google Scholar 

  65. Ulusoy G, Adali O, Tumer TB, Sahin G, Gozdasoglu S, Arinc E (2007) Significance of genetic polymorphisms at multiple loci of CYP2E1 in the risk of development of childhood acute lymphoblastic leukemia. Oncology 72(1–2):125–131

    Article  PubMed  CAS  Google Scholar 

  66. Wiemels JL, Pagnamenta A, Taylor GM, Eden OB, Alexander FE, Greaves MF (1999) A lack of a functional NAD(P)H: quinone oxidoreductase allele is selectively associated with pediatric leukemias that have MLL fusions United Kingdom Childhood Cancer Study Investigators. Cancer Res 59(16):4095–4099

    PubMed  CAS  Google Scholar 

  67. Smith MT, Wang Y, Skibola CF, Slater DJ, Lo Nigro L, Nowell PC, Lange BJ, Felix CA (2002) Low NAD(P)H: quinone oxidoreductase activity is associated with increased risk of leukemia with MLL translocations in infants and children. Blood 100(13):4590–4593. doi:10.1182/blood-2001-12-0264

    Article  PubMed  CAS  Google Scholar 

  68. Kracht T, Schrappe M, Strehl S, Reiter A, Elsner HA, Trka J, Cario G, Viehmann S, Harbott J, Borkhardt A, Metzler M, Langer T, Repp R, Marschalek R, Welte K, Haas OA, Stanulla M (2004) NQO1 C609T polymorphism in distinct entities of pediatric hematologic neoplasms. Haematologica 89(12):1492–1497

    PubMed  CAS  Google Scholar 

  69. Sirma S, Agaoglu L, Yildiz I, Cayli D, Horgusluoglu E, Anak S, Yuksel L, Unuvar A, Celkan T, Apak H, Karakas Z, Devecioglu O, Ozbek U (2004) NAD(P)H: quinone oxidoreductase 1 null genotype is not associated with pediatric de novo acute leukemia. Pediatr Blood Cancer 43(5):568–570. doi:10.1002/pbc.20098

    Article  PubMed  Google Scholar 

  70. Eguchi-Ishimae M, Eguchi M, Ishii E, Knight D, Sadakane Y, Isoyama K, Yabe H, Mizutani S, Greaves M (2005) The association of a distinctive allele of NAD(P)H: quinone oxidoreductase with pediatric acute lymphoblastic leukemias with MLL fusion genes in Japan. Haematologica 90(11):1511–1515

    PubMed  CAS  Google Scholar 

  71. Lanciotti M, Dufour C, Corral L, Di Michele P, Pigullo S, De Rossi G, Basso G, Leszl A, Luciani M, Lo Nigro L, Micalizzi C, Valsecchi MG, Biondi A, Haupt R (2005) Genetic polymorphism of NAD(P)H: quinone oxidoreductase is associated with an increased risk of infant acute lymphoblastic leukemia without MLL gene rearrangements. Leukemia 19(2):214–216. doi:10.1038/sj.leu.2403613

    Article  PubMed  CAS  Google Scholar 

  72. Infante-Rivard C, Vermunt JK, Weinberg CR (2007) Excess transmission of the NAD(P)H: quinone oxidoreductase 1 (NQO1) C609T polymorphism in families of children with acute lymphoblastic leukemia. Am J Epidemiol 165(11):1248–1254. doi:10.1093/aje/kwm022

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to Claire Mulot, who was in charge of the biological collection at the Biological Resource Center of Saints-Pères, INSERM U775; the CEPH and the Centre National du Génotypage, which genotyped the cases; and IntegraGen, which genotyped the controls. The authors would also like to express their gratitude to Marie-Hélène Da Silva, Christophe Steffen and Florence Menegaux (INSERM U1018, Environmental Epidemiology of Cancer), who contributed to the recruitment of the cases; Aurélie Guyot-Goubin and the staff of the French National Registry of Childhood Blood Malignancies, who contributed to case detection and verification; Sabine Mélèze and Marie-Anne Noel (Institut CSA), who coordinated the selection of the controls and the interviews; and Catherine Tricoche (Callson) and the team of interviewers, who interviewed the cases and controls. The authors would also like to thank all of the Société Française de lutte contre les Cancers de l’Enfant et de l’Adolescent (SFCE) principal investigators: André Baruchel (Hôpital Saint-Louis/Hôpital Robert Debré, Paris), Claire Berger (Centre Hospitalier Universitaire, Saint-Etienne), Christophe Bergeron (Centre Léon Bérard, Lyon), Jean-Louis Bernard (Hôpital La Timone, Marseille), Yves Bertrand (Hôpital Debrousse, Lyon), Pierre Bordigoni (Centre Hospitalier Universitaire, Nancy), Patrick Boutard (Centre Hospitalier Régional Universitaire, Caen), Gérard Couillault (Hôpital d’Enfants, Dijon), Christophe Piguet (Centre Hospitalier Régional Universitaire, Limoges), Anne-Sophie Defachelles (Centre Oscar Lambret, Lille), François Demeocq (Hôpital Hôtel-Dieu, Clermont-Ferrand), Alain Fischer (Hôpital des Enfants Malades, Paris), Virginie Gandemer (Centre Hospitalier Universitaire—Hôpital Sud, Rennes), Dominique Valteau-Couanet (Institut Gustave Roussy, Villejuif), Jean-Pierre Lamagnere (Centre Gatien de Clocheville, Tours), Françoise Lapierre (Centre Hospitalier Universitaire Jean Bernard, Poitiers), Guy Leverger (Hôpital Armand-Trousseau, Paris), Patrick Lutz (Hôpital de Hautepierre, Strasbourg), Geneviève Margueritte (Hôpital Arnaud de Villeneuve, Montpellier), Françoise Mechinaud (Hôpital Mère et Enfants, Nantes), Gérard Michel (Hôpital La Timone, Marseille), Frédéric Millot (Centre Hospitalier Universitaire Jean Bernard, Poitiers), Martine Münzer (American Memorial Hospital, Reims), Brigitte Nelken (Hôpital Jeanne de Flandre, Lille), Hélène Pacquement (Institut Curie, Paris), Brigitte Pautard (Centre Hospitalier Universitaire, Amiens), Yves Perel (Hôpital Pellegrin Tripode, Bordeaux), Alain Pierre-Kahn (Hôpital Enfants Malades, Paris), Emmanuel Plouvier (Centre Hospitalier Régional, Besançon), Xavier Rialland (Centre Hospitalier Universitaire, Angers), Alain Robert (Hôpital des Enfants, Toulouse), Hervé Rubie (Hôpital des Enfants, Toulouse), Nicolas Sirvent (L’Archet, Nice), Christine Soler (Fondation Lenval, Nice), and Jean-Pierre Vannier (Hôpital Charles Nicolle, Rouen). This work was supported by grants from INSERM, the Fondation de France, the Association pour la Recherche sur le Cancer (ARC), the Agence Française de Sécurité Sanitaire des Produits de Santé (AFSSAPS), the Agence Française de Sécurité Sanitaire de l’Environnement et du Travail (AFSSET), the association Cent pour sang la vie, the Institut National du Cancer (INCa), the Agence Nationale de la Recherche (ANR), and Cancéropôle Ile de France. Audrey Bonaventure was funded by the Fondation pour la Recherche Médicale.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Inserm, UMRS 1018, CESP, Team 6 Environmental Epidemiology of Cancer, 16, Avenue Paul Vaillant-Couturier, Bâtiment 15/16, 94807, Villejuif Cedex, France

    Audrey Bonaventure, Stéphanie Goujon-Bellec, Jérémie Rudant, Laurent Orsi, Denis Hémon & Jacqueline Clavel

  2. Université Paris-Sud 11, UMRS 1018, Villejuif, France

    Audrey Bonaventure, Stéphanie Goujon-Bellec, Jérémie Rudant, Laurent Orsi, Denis Hémon & Jacqueline Clavel

  3. RNHE—National Registry of Childhood Hematopoietic Malignancies, Villejuif, France

    Stéphanie Goujon-Bellec & Jacqueline Clavel

  4. AP-HP, Hôpital Armand Trousseau, Paris, France

    Guy Leverger

  5. Université Paris 6 Pierre et Marie Curie, Paris, France

    Guy Leverger

  6. AP-HP, Hôpital Robert Debré, Paris, France

    André Baruchel

  7. Université Paris 7, Paris, France

    André Baruchel

  8. Institut d’Hémato-Oncologie Pédiatrique, Lyon, France

    Yves Bertrand

  9. Hôpital Jeanne de Flandre, CHRU, Lille, France

    Brigitte Nelken

  10. Université Lille Nord de France, 59000, Lille, France

    Brigitte Nelken

  11. Hôpital des Enfants, Toulouse, France

    Marlène Pasquet

  12. AP-HM, Hôpital la Timone, Marseille, France

    Gérard Michel

  13. Hôpital Arnaud de Villeneuve, Montpellier, France

    Nicolas Sirvent

  14. CHU de Nancy, Vandoeuvre, France

    Pierre Bordigoni

  15. Hematology and Oncology, Childrens’ Hospital, Pellegrin, Bordeaux University Hospital, Bordeaux, France

    Stéphane Ducassou

  16. Hôpital Mère-Enfant, CHU, Nantes, France

    Xavier Rialland

  17. CHU d’Angers, Angers, France

    Xavier Rialland

  18. Commissariat à l’Energie Atomique (CEA) Genomics Institute-Centre National de Génotypage, Evry Cedex, France

    Diana Zelenika

Authors
  1. Audrey Bonaventure
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  2. Stéphanie Goujon-Bellec
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  3. Jérémie Rudant
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  4. Laurent Orsi
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  5. Guy Leverger
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  6. André Baruchel
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  7. Yves Bertrand
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  8. Brigitte Nelken
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  9. Marlène Pasquet
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  10. Gérard Michel
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  11. Nicolas Sirvent
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  12. Pierre Bordigoni
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  13. Stéphane Ducassou
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  14. Xavier Rialland
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  15. Diana Zelenika
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  16. Denis Hémon
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  17. Jacqueline Clavel
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Corresponding author

Correspondence to Audrey Bonaventure.

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Bonaventure, A., Goujon-Bellec, S., Rudant, J. et al. Maternal smoking during pregnancy, genetic polymorphisms of metabolic enzymes, and childhood acute leukemia: the ESCALE Study (SFCE). Cancer Causes Control 23, 329–345 (2012). https://doi.org/10.1007/s10552-011-9882-9

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  • DOI: https://doi.org/10.1007/s10552-011-9882-9

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