Abstract
Purpose
This study aimed to analyze the associations between childhood acute leukemia (AL) and maternal caffeinated beverage consumption during pregnancy, and to explore interactions between caffeinated and alcoholic beverage consumption and polymorphisms of enzymes involved in caffeine and ethanol metabolisms.
Methods
The data were generated by the French ESCALE study, which included 764 AL cases and 1,681 controls in 2003–2004. The case and control mothers were interviewed on their consumption habits during pregnancy using a standardized questionnaire. Genotypes of the candidate alleles (NAT2*5 rs1801280, ADH1C*2 rs698 and rs1693482, CYP2E1*5 rs2031920 and rs3813867) were obtained using high-throughput genotyping and imputation data for 493 AL cases and 549 controls with at least two grandparents born in Europe.
Results
Maternal regular coffee consumption during pregnancy was associated with childhood AL (OR = 1.2 [1.0–1.5], p = 0.02); the odds ratios increased linearly with daily intake (p for trend <0.001; >2 cups per day vs. no or less than 1 cup per week: AL: OR = 1.6 [1.2–2.1], lymphoblastic AL: OR = 1.5 [1.1–2.0], myeloblastic AL: OR = 2.4 [1.3–4.3]). The association was slightly more marked for children born to non-smoking mothers. Lymphoblastic AL was also associated with cola soda drinking (OR = 1.3 [1.0–1.5], p = 0.02). No significant gene–environment interactions with coffee, tea, cola soda, or alcohol drinking were observed.
Conclusion
This study provides additional evidence that maternal coffee consumption during pregnancy may be associated with childhood AL. Coffee consumption is a prevalent habit and its potential involvement in childhood AL needs to be considered further.
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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
- CYP2E1:
-
Cytochrome P450 2E1
- NAT2:
-
N-acetyltransferase 2
- ADH:
-
Alcohol dehydrogenase
References
Menegaux F, Steffen C, Bellec S, Baruchel A, Lescoeur B, Leverger G, Nelken B, Philippe N, Sommelet D, Hemon D, Clavel J (2005) Maternal coffee and alcohol consumption during pregnancy, parental smoking and risk of childhood acute leukaemia. Cancer Detect Prev 29(6):487–493
Ross JA, Potter JD, Reaman GH, Pendergrass TW, Robison LL (1996) Maternal exposure to potential inhibitors of DNA topoisomerase II and infant leukemia (United States): a report from the Children’s Cancer Group. Cancer Causes Control 7(6):581–590
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
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
Milne E, Royle JA, Bennett LC, de Klerk NH, Bailey HD, Bower C, Miller M, Attia J, Scott RJ, Kirby M, Armstrong BK (2011) Maternal consumption of coffee and tea during pregnancy and risk of childhood ALL: results from an Australian case–control study. Cancer Causes Control 22(2):207–218. doi:10.1007/s10552-010-9688-1
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
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
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
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
Bonaventure A, Goujon-Bellec S, Rudant J, Orsi L, Leverger G, Baruchel A, Bertrand Y, Nelken B, Pasquet M, Michel G, Sirvent N, Bordigoni P, Ducassou S, Rialland X, Zelenika D, Hemon D, Clavel J (2012) Maternal smoking during pregnancy, genetic polymorphisms of metabolic enzymes, and childhood acute leukemia: the ESCALE Study (SFCE). Cancer Causes Control 23(2):329–345. doi:10.1007/s10552-011-9882-9
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
Latino-Martel P, Chan DS, Druesne-Pecollo N, Barrandon E, Hercberg S, Norat T (2010) Maternal alcohol consumption during pregnancy and risk of childhood leukemia: systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev 19(5):1238–1260
Edenberg HJ (2007) The genetics of alcohol metabolism: role of alcohol dehydrogenase and aldehyde dehydrogenase variants. Alcohol Res Health 30(1):5–13
IARC (1999) Metabolic polymorphisms & susceptibility to cancer, chap 3. IARC monograph 148, IARC, Lyon
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
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
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
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
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
Infante-Rivard C, Krajinovic M, Labuda D, Sinnett D (2002) Childhood acute lymphoblastic leukemia associated with parental alcohol consumption and polymorphisms of carcinogen-metabolizing genes. Epidemiology 13(3):277–281
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
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
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
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
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
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
Ferguson LR, Philpott M (2008) Nutrition and mutagenesis. In: Annual review of nutrition, vol 28. Annual review of nutrition. Annual Reviews, Palo Alto, pp 313–329. doi:10.1146/annurev.nutr.28.061807.155449
IARC (1991) IARC monographs on the evaluation of carcinogenic risks to humans, vol 51. In: Coffee, tea, mate, methylxanthines and methylglyoxal. IARC, Lyon, pp 291–390
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
Hines RN, McCarver DG (2002) The ontogeny of human drug-metabolizing enzymes: phase I oxidative enzymes. J Pharmacol Exp Ther 300(2):355–360
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 the 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.
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An erratum to this article is available at http://dx.doi.org/10.1007/s10552-014-0403-5.
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Bonaventure, A., Rudant, J., Goujon-Bellec, S. et al. Childhood acute leukemia, maternal beverage intake during pregnancy, and metabolic polymorphisms. Cancer Causes Control 24, 783–793 (2013). https://doi.org/10.1007/s10552-013-0161-9
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DOI: https://doi.org/10.1007/s10552-013-0161-9