Skip to main content
Top
Published in: Cancer Causes & Control 7/2016

01-07-2016 | Original paper

Maternal prenatal intake of one-carbon metabolism nutrients and risk of childhood leukemia

Authors: Amanda W. Singer, Steve Selvin, Gladys Block, Carla Golden, Suzan L. Carmichael, Catherine Metayer

Published in: Cancer Causes & Control | Issue 7/2016

Login to get access

Abstract

Purpose

Folate, vitamins B12 and B6, riboflavin, and methionine are critical nutrients for the one-carbon metabolism cycle involved in DNA synthesis and epigenetic processes. We examined the association between maternal intake of these nutrients before pregnancy and risk of childhood acute lymphoblastic leukemia (ALL) and acute myeloid leukemia (AML) in a matched case–control study.

Methods

Maternal dietary intake and vitamin supplement use in the year before pregnancy was assessed by food frequency questionnaire for 681 ALL cases, 103 AML cases, and 1076 controls. Principal component analysis was used to construct a variable representing combined nutrient intake, and conditional logistic regression estimated the odds ratio (OR) and 95% confidence interval (CI) for the association of ALL and AML with the principal component and each nutrient.

Results

Higher maternal intake of one-carbon metabolism nutrients from food and supplements combined was associated with reduced risk of ALL (OR for one-unit change in the principal component = 0.91, CI 0.84–0.99) and possibly AML (OR for the principal component = 0.83, CI 0.66–1.04). When analyzed separately, intake of supplements high in these nutrients was associated with a reduced risk of ALL in children of Hispanic women only.

Conclusions

In conclusion, these data suggest that higher maternal intake of one-carbon metabolism nutrients may reduce risk of childhood leukemia.
Literature
1.
go back to reference Ross JA, Johnson KJ, Spector LG, Kersey JH (2011) Epidemiology of acute childhood leukemia. In: Reaman GH, Smith FO (eds) Childhood leukemia: a practical handbook. Springer, New York Ross JA, Johnson KJ, Spector LG, Kersey JH (2011) Epidemiology of acute childhood leukemia. In: Reaman GH, Smith FO (eds) Childhood leukemia: a practical handbook. Springer, New York
2.
go back to reference Wiemels J (2012) Childhood acute leukemia. In: Dietert RR, Luebke RW (eds) Immunotoxicity, immune dysfunction, and chronic disease. Springer, New York Wiemels J (2012) Childhood acute leukemia. In: Dietert RR, Luebke RW (eds) Immunotoxicity, immune dysfunction, and chronic disease. Springer, New York
4.
go back to reference Wiemels JL, Cazzaniga G, Daniotti M, Eden OB, Addison GM, Masera G, Saha V, Biondi A, Greaves MF (1999) Prenatal origin of acute lymphoblastic leukaemia in children. Lancet 354(9189):1499–1503PubMedCrossRef Wiemels JL, Cazzaniga G, Daniotti M, Eden OB, Addison GM, Masera G, Saha V, Biondi A, Greaves MF (1999) Prenatal origin of acute lymphoblastic leukaemia in children. Lancet 354(9189):1499–1503PubMedCrossRef
6.
go back to reference Shane B (2008) Folate and vitamin B12 metabolism: overview and interaction with riboflavin, vitamin B6, and polymorphisms. Food Nutr Bull 29(2 Suppl):S5–S16 discussion S17–S19 PubMedCrossRef Shane B (2008) Folate and vitamin B12 metabolism: overview and interaction with riboflavin, vitamin B6, and polymorphisms. Food Nutr Bull 29(2 Suppl):S5–S16 discussion S17–S19 PubMedCrossRef
9.
go back to reference Fenech M (2001) The role of folic acid and Vitamin B12 in genomic stability of human cells. Mutat Res 475(1–2):57–67PubMedCrossRef Fenech M (2001) The role of folic acid and Vitamin B12 in genomic stability of human cells. Mutat Res 475(1–2):57–67PubMedCrossRef
11.
go back to reference Wong NC, Ashley D, Chatterton Z, Parkinson-Bates M, Ng HK, Halemba MS, Kowalczyk A, Bedo J, Wang Q, Bell K, Algar E, Craig JM, Saffery R (2012) A distinct DNA methylation signature defines pediatric pre-B cell acute lymphoblastic leukemia. Epigenet Off J DNA Methylation Soc 7(6):535–541. doi:10.4161/epi.20193 CrossRef Wong NC, Ashley D, Chatterton Z, Parkinson-Bates M, Ng HK, Halemba MS, Kowalczyk A, Bedo J, Wang Q, Bell K, Algar E, Craig JM, Saffery R (2012) A distinct DNA methylation signature defines pediatric pre-B cell acute lymphoblastic leukemia. Epigenet Off J DNA Methylation Soc 7(6):535–541. doi:10.​4161/​epi.​20193 CrossRef
13.
go back to reference Thompson JR, Gerald PF, Willoughby ML, Armstrong BK (2001) Maternal folate supplementation in pregnancy and protection against acute lymphoblastic leukaemia in childhood: a case-control study. Lancet 358(9297):1935–1940. doi:10.1016/s0140-6736(01)06959-8 PubMedCrossRef Thompson JR, Gerald PF, Willoughby ML, Armstrong BK (2001) Maternal folate supplementation in pregnancy and protection against acute lymphoblastic leukaemia in childhood: a case-control study. Lancet 358(9297):1935–1940. doi:10.​1016/​s0140-6736(01)06959-8 PubMedCrossRef
14.
go back to reference Amigou A, Rudant J, Orsi L, Goujon-Bellec S, Leverger G, Baruchel A, Bertrand Y, Nelken B, Plat G, Michel G, Haouy S, Chastagner P, Ducassou S, Rialland X, Hemon D, Clavel J (2012) Folic acid supplementation, MTHFR and MTRR polymorphisms, and the risk of childhood leukemia: the ESCALE study (SFCE). Cancer Causes Control 23(8):1265–1277. doi:10.1007/s10552-012-0004-0 PubMedCrossRef Amigou A, Rudant J, Orsi L, Goujon-Bellec S, Leverger G, Baruchel A, Bertrand Y, Nelken B, Plat G, Michel G, Haouy S, Chastagner P, Ducassou S, Rialland X, Hemon D, Clavel J (2012) Folic acid supplementation, MTHFR and MTRR polymorphisms, and the risk of childhood leukemia: the ESCALE study (SFCE). Cancer Causes Control 23(8):1265–1277. doi:10.​1007/​s10552-012-0004-0 PubMedCrossRef
15.
go back to reference Bailey HD, Miller M, Langridge A, de Klerk NH, van Bockxmeer FM, Attia J, Scott RJ, Armstrong BK, Milne E (2012) Maternal dietary intake of folate and vitamins b6 and B12 during pregnancy and the risk of childhood acute lymphoblastic leukemia. Nutr Cancer 64(7):1122–1130. doi:10.1080/01635581.2012.707278 PubMedCrossRef Bailey HD, Miller M, Langridge A, de Klerk NH, van Bockxmeer FM, Attia J, Scott RJ, Armstrong BK, Milne E (2012) Maternal dietary intake of folate and vitamins b6 and B12 during pregnancy and the risk of childhood acute lymphoblastic leukemia. Nutr Cancer 64(7):1122–1130. doi:10.​1080/​01635581.​2012.​707278 PubMedCrossRef
16.
go back to reference Milne E, Royle JA, Miller M, Bower C, de Klerk NH, Bailey HD, van Bockxmeer F, Attia J, Scott RJ, Norris MD, Haber M, Thompson JR, Fritschi L, Marshall GM, Armstrong BK (2010) Maternal folate and other vitamin supplementation during pregnancy and risk of acute lymphoblastic leukemia in the offspring. Int J Cancer 126(11):2690–2699. doi:10.1002/ijc.24969 PubMed Milne E, Royle JA, Miller M, Bower C, de Klerk NH, Bailey HD, van Bockxmeer F, Attia J, Scott RJ, Norris MD, Haber M, Thompson JR, Fritschi L, Marshall GM, Armstrong BK (2010) Maternal folate and other vitamin supplementation during pregnancy and risk of acute lymphoblastic leukemia in the offspring. Int J Cancer 126(11):2690–2699. doi:10.​1002/​ijc.​24969 PubMed
20.
go back to reference Kwan ML, Jensen CD, Block G, Hudes ML, Chu LW, Buffler PA (2009) Maternal diet and risk of childhood acute lymphoblastic leukemia. Public Health Rep 124(4):503–514PubMedPubMedCentral Kwan ML, Jensen CD, Block G, Hudes ML, Chu LW, Buffler PA (2009) Maternal diet and risk of childhood acute lymphoblastic leukemia. Public Health Rep 124(4):503–514PubMedPubMedCentral
21.
go back to reference Metayer C, Scelo G, Chokkalingam AP, Barcellos LF, Aldrich MC, Chang JS, Guha N, Urayama KY, Hansen HM, Block G, Kiley V, Wiencke JK, Wiemels JL, Buffler PA (2011) Genetic variants in the folate pathway and risk of childhood acute lymphoblastic leukemia. Cancer Causes Control 22(9):1243–1258. doi:10.1007/s10552-011-9795-7 PubMedPubMedCentralCrossRef Metayer C, Scelo G, Chokkalingam AP, Barcellos LF, Aldrich MC, Chang JS, Guha N, Urayama KY, Hansen HM, Block G, Kiley V, Wiencke JK, Wiemels JL, Buffler PA (2011) Genetic variants in the folate pathway and risk of childhood acute lymphoblastic leukemia. Cancer Causes Control 22(9):1243–1258. doi:10.​1007/​s10552-011-9795-7 PubMedPubMedCentralCrossRef
22.
go back to reference Metayer C, Milne E, Dockerty JD, Clavel J, Pombo-de-Oliveira MS, Wesseling C, Spector LG, Schuz J, Petridou E, Ezzat S, Armstrong BK, Rudant J, Koifman S, Kaatsch P, Moschovi M, Rashed WM, Selvin S, McCauley K, Hung RJ, Kang AY, Infante-Rivard C (2014) Maternal supplementation with folic acid and other vitamins and risk of leukemia in offspring: a childhood leukemia international consortium study. Epidemiology (Cambridge, Mass) 25(6):811–822. doi:10.1097/EDE.0000000000000141 CrossRef Metayer C, Milne E, Dockerty JD, Clavel J, Pombo-de-Oliveira MS, Wesseling C, Spector LG, Schuz J, Petridou E, Ezzat S, Armstrong BK, Rudant J, Koifman S, Kaatsch P, Moschovi M, Rashed WM, Selvin S, McCauley K, Hung RJ, Kang AY, Infante-Rivard C (2014) Maternal supplementation with folic acid and other vitamins and risk of leukemia in offspring: a childhood leukemia international consortium study. Epidemiology (Cambridge, Mass) 25(6):811–822. doi:10.​1097/​EDE.​0000000000000141​ CrossRef
24.
go back to reference Lim JY, Bhatia S, Robison LL, Yang JJ (2013) Genomics of racial and ethnic disparities in childhood acute lymphoblastic leukemia. Cancer. doi:10.1002/cncr.28531 Lim JY, Bhatia S, Robison LL, Yang JJ (2013) Genomics of racial and ethnic disparities in childhood acute lymphoblastic leukemia. Cancer. doi:10.​1002/​cncr.​28531
26.
go back to reference Ma X, Buffler PA, Wiemels JL, Selvin S, Metayer C, Loh M, Does MB, Wiencke JK (2005) Ethnic difference in daycare attendance, early infections, and risk of childhood acute lymphoblastic leukemia. Cancer Epidemiol Biomark Prev Publ Am Asso Cancer Research Cosponsored Am Soc Prev Oncol 14(8):1928–1934. doi:10.1158/1055-9965.EPI-05-0115 CrossRef Ma X, Buffler PA, Wiemels JL, Selvin S, Metayer C, Loh M, Does MB, Wiencke JK (2005) Ethnic difference in daycare attendance, early infections, and risk of childhood acute lymphoblastic leukemia. Cancer Epidemiol Biomark Prev Publ Am Asso Cancer Research Cosponsored Am Soc Prev Oncol 14(8):1928–1934. doi:10.​1158/​1055-9965.​EPI-05-0115 CrossRef
27.
go back to reference Francis SS, Selvin S, Metayer C, Wallace AD, Crouse V, Moore TB, Wiemels JL, Buffler PA (2014) Mode of delivery and risk of childhood leukemia. Cancer Epidemiol Biomark Prev Publ Am Asso Cancer Research Cosponsored Am Soc Prev Oncol 23(5):876–881. doi:10.1158/1055-9965.EPI-13-1098 CrossRef Francis SS, Selvin S, Metayer C, Wallace AD, Crouse V, Moore TB, Wiemels JL, Buffler PA (2014) Mode of delivery and risk of childhood leukemia. Cancer Epidemiol Biomark Prev Publ Am Asso Cancer Research Cosponsored Am Soc Prev Oncol 23(5):876–881. doi:10.​1158/​1055-9965.​EPI-13-1098 CrossRef
28.
go back to reference Urayama KY, Ma X, Selvin S, Metayer C, Chokkalingam AP, Wiemels JL, Does M, Chang J, Wong A, Trachtenberg E, Buffler PA (2011) Early life exposure to infections and risk of childhood acute lymphoblastic leukemia. Int J Cancer 128(7):1632–1643. doi:10.1002/ijc.25752 PubMedCrossRef Urayama KY, Ma X, Selvin S, Metayer C, Chokkalingam AP, Wiemels JL, Does M, Chang J, Wong A, Trachtenberg E, Buffler PA (2011) Early life exposure to infections and risk of childhood acute lymphoblastic leukemia. Int J Cancer 128(7):1632–1643. doi:10.​1002/​ijc.​25752 PubMedCrossRef
29.
go back to reference Xu H, Cheng C, Devidas M, Pei D, Fan Y, Yang W, Neale G, Scheet P, Burchard EG, Torgerson DG, Eng C, Dean M, Antillon F, Winick NJ, Martin PL, Willman CL, Camitta BM, Reaman GH, Carroll WL, Loh M, Evans WE, Pui CH, Hunger SP, Relling MV, Yang JJ (2012) ARID5B genetic polymorphisms contribute to racial disparities in the incidence and treatment outcome of childhood acute lymphoblastic leukemia. J Clin Oncol Off J Am Soc Clin Oncol 30(7):751–757. doi:10.1200/JCO.2011.38.0345 CrossRef Xu H, Cheng C, Devidas M, Pei D, Fan Y, Yang W, Neale G, Scheet P, Burchard EG, Torgerson DG, Eng C, Dean M, Antillon F, Winick NJ, Martin PL, Willman CL, Camitta BM, Reaman GH, Carroll WL, Loh M, Evans WE, Pui CH, Hunger SP, Relling MV, Yang JJ (2012) ARID5B genetic polymorphisms contribute to racial disparities in the incidence and treatment outcome of childhood acute lymphoblastic leukemia. J Clin Oncol Off J Am Soc Clin Oncol 30(7):751–757. doi:10.​1200/​JCO.​2011.​38.​0345 CrossRef
30.
go back to reference Walsh KM, Chokkalingam AP, Hsu LI, Metayer C, de Smith AJ, Jacobs DI, Dahl GV, Loh ML, Smirnov IV, Bartley K, Ma X, Wiencke JK, Barcellos LF, Wiemels JL, Buffler PA (2013) Associations between genome-wide native American ancestry, known risk alleles and B-cell ALL risk in Hispanic children. Leuk Off J Leuk Soc Am Leuk Res Fund UK. doi:10.1038/leu.2013.130 Walsh KM, Chokkalingam AP, Hsu LI, Metayer C, de Smith AJ, Jacobs DI, Dahl GV, Loh ML, Smirnov IV, Bartley K, Ma X, Wiencke JK, Barcellos LF, Wiemels JL, Buffler PA (2013) Associations between genome-wide native American ancestry, known risk alleles and B-cell ALL risk in Hispanic children. Leuk Off J Leuk Soc Am Leuk Res Fund UK. doi:10.​1038/​leu.​2013.​130
33.
go back to reference Ma X, Buffler PA, Layefsky M, Does MB, Reynolds P (2004) Control selection strategies in case-control studies of childhood diseases. Am J Epidemiol 159(10):915–921PubMedCrossRef Ma X, Buffler PA, Layefsky M, Does MB, Reynolds P (2004) Control selection strategies in case-control studies of childhood diseases. Am J Epidemiol 159(10):915–921PubMedCrossRef
36.
go back to reference Dockerty JD, Draper G, Vincent T, Rowan SD, Bunch KJ (2001) Case-control study of parental age, parity and socioeconomic level in relation to childhood cancers. Int J Epidemiol 30(6):1428–1437PubMedCrossRef Dockerty JD, Draper G, Vincent T, Rowan SD, Bunch KJ (2001) Case-control study of parental age, parity and socioeconomic level in relation to childhood cancers. Int J Epidemiol 30(6):1428–1437PubMedCrossRef
40.
go back to reference Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65(4 Suppl):1220S–1228S 1229S-1231S PubMed Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65(4 Suppl):1220S–1228S 1229S-1231S PubMed
41.
go back to reference Halsted CH, Villanueva JA, Devlin AM, Chandler CJ (2002) Metabolic interactions of alcohol and folate. J Nutr 132(8 Suppl):2367S–2372SPubMed Halsted CH, Villanueva JA, Devlin AM, Chandler CJ (2002) Metabolic interactions of alcohol and folate. J Nutr 132(8 Suppl):2367S–2372SPubMed
43.
go back to reference Petridou E, Ntouvelis E, Dessypris N, Terzidis A, Trichopoulos D, Childhood Hematology-Oncology G (2005) Maternal diet and acute lymphoblastic leukemia in young children. Cancer Epidemiol Biomark Prev Publ Am Asso Cancer Research Cosponsored Am Soc Prev Oncol 14(8):1935–1939. doi:10.1158/1055-9965.EPI-05-0090 CrossRef Petridou E, Ntouvelis E, Dessypris N, Terzidis A, Trichopoulos D, Childhood Hematology-Oncology G (2005) Maternal diet and acute lymphoblastic leukemia in young children. Cancer Epidemiol Biomark Prev Publ Am Asso Cancer Research Cosponsored Am Soc Prev Oncol 14(8):1935–1939. doi:10.​1158/​1055-9965.​EPI-05-0090 CrossRef
46.
go back to reference Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA, Slagboom PE, Heijmans BT (2009) Periconceptional maternal folic acid use of 400 microg per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One 4(11):e7845. doi:10.1371/journal.pone.0007845 PubMedPubMedCentralCrossRef Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA, Slagboom PE, Heijmans BT (2009) Periconceptional maternal folic acid use of 400 microg per day is related to increased methylation of the IGF2 gene in the very young child. PLoS One 4(11):e7845. doi:10.​1371/​journal.​pone.​0007845 PubMedPubMedCentralCrossRef
47.
go back to reference Tamura T, Picciano MF (2006) Folate and human reproduction. Am J Clin Nutr 83(5):993–1016PubMed Tamura T, Picciano MF (2006) Folate and human reproduction. Am J Clin Nutr 83(5):993–1016PubMed
50.
go back to reference Nygard O, Refsum H, Ueland PM, Vollset SE (1998) Major lifestyle determinants of plasma total homocysteine distribution: the Hordaland Homocysteine Study. Am J Clin Nutr 67(2):263–270PubMed Nygard O, Refsum H, Ueland PM, Vollset SE (1998) Major lifestyle determinants of plasma total homocysteine distribution: the Hordaland Homocysteine Study. Am J Clin Nutr 67(2):263–270PubMed
51.
go back to reference Jacques PF, Kalmbach R, Bagley PJ, Russo GT, Rogers G, Wilson PW, Rosenberg IH, Selhub J (2002) The relationship between riboflavin and plasma total homocysteine in the Framingham offspring cohort is influenced by folate status and the C677T transition in the methylenetetrahydrofolate reductase gene. J Nutr 132(2):283–288PubMed Jacques PF, Kalmbach R, Bagley PJ, Russo GT, Rogers G, Wilson PW, Rosenberg IH, Selhub J (2002) The relationship between riboflavin and plasma total homocysteine in the Framingham offspring cohort is influenced by folate status and the C677T transition in the methylenetetrahydrofolate reductase gene. J Nutr 132(2):283–288PubMed
52.
go back to reference Gabriel HE, Crott JW, Ghandour H, Dallal GE, Choi SW, Keyes MK, Jang H, Liu Z, Nadeau M, Johnston A, Mager D, Mason JB (2006) Chronic cigarette smoking is associated with diminished folate status, altered folate form distribution, and increased genetic damage in the buccal mucosa of healthy adults. Am J Clin Nutr 83(4):835–841PubMed Gabriel HE, Crott JW, Ghandour H, Dallal GE, Choi SW, Keyes MK, Jang H, Liu Z, Nadeau M, Johnston A, Mager D, Mason JB (2006) Chronic cigarette smoking is associated with diminished folate status, altered folate form distribution, and increased genetic damage in the buccal mucosa of healthy adults. Am J Clin Nutr 83(4):835–841PubMed
53.
go back to reference Yang QH, Botto LD, Gallagher M, Friedman JM, Sanders CL, Koontz D, Nikolova S, Erickson JD, Steinberg K (2008) Prevalence and effects of gene-gene and gene-nutrient interactions on serum folate and serum total homocysteine concentrations in the United States: findings from the third National Health and Nutrition Examination Survey DNA Bank. Am J Clin Nutr 88(1):232–246PubMed Yang QH, Botto LD, Gallagher M, Friedman JM, Sanders CL, Koontz D, Nikolova S, Erickson JD, Steinberg K (2008) Prevalence and effects of gene-gene and gene-nutrient interactions on serum folate and serum total homocysteine concentrations in the United States: findings from the third National Health and Nutrition Examination Survey DNA Bank. Am J Clin Nutr 88(1):232–246PubMed
54.
go back to reference Yang QH, Carter HK, Mulinare J, Berry RJ, Friedman JM, Erickson JD (2007) Race-ethnicity differences in folic acid intake in women of childbearing age in the United States after folic acid fortification: findings from the National Health and Nutrition Examination Survey, 2001–2002. Am J Clin Nutr 85(5):1409–1416PubMed Yang QH, Carter HK, Mulinare J, Berry RJ, Friedman JM, Erickson JD (2007) Race-ethnicity differences in folic acid intake in women of childbearing age in the United States after folic acid fortification: findings from the National Health and Nutrition Examination Survey, 2001–2002. Am J Clin Nutr 85(5):1409–1416PubMed
55.
go back to reference Bailey RL, Dodd KW, Gahche JJ, Dwyer JT, McDowell MA, Yetley EA, Sempos CA, Burt VL, Radimer KL, Picciano MF (2010) Total folate and folic acid intake from foods and dietary supplements in the United States: 2003-2006. Am J Clin Nutr 91(1):231–237. doi:10.3945/ajcn.2009.28427 PubMedCrossRef Bailey RL, Dodd KW, Gahche JJ, Dwyer JT, McDowell MA, Yetley EA, Sempos CA, Burt VL, Radimer KL, Picciano MF (2010) Total folate and folic acid intake from foods and dietary supplements in the United States: 2003-2006. Am J Clin Nutr 91(1):231–237. doi:10.​3945/​ajcn.​2009.​28427 PubMedCrossRef
56.
go back to reference Solis C, Veenema K, Ivanov AA, Tran S, Li R, Wang W, Moriarty DJ, Maletz CV, Caudill MA (2008) Folate intake at RDA levels is inadequate for Mexican American men with the methylenetetrahydrofolate reductase 677TT genotype. J Nutr 138(1):67–72PubMedPubMedCentral Solis C, Veenema K, Ivanov AA, Tran S, Li R, Wang W, Moriarty DJ, Maletz CV, Caudill MA (2008) Folate intake at RDA levels is inadequate for Mexican American men with the methylenetetrahydrofolate reductase 677TT genotype. J Nutr 138(1):67–72PubMedPubMedCentral
57.
59.
go back to reference Greenland S, Schwartzbaum JA, Finkle WD (2000) Problems due to small samples and sparse data in conditional logistic regression analysis. Am J Epidemiol 151(5):531–539PubMedCrossRef Greenland S, Schwartzbaum JA, Finkle WD (2000) Problems due to small samples and sparse data in conditional logistic regression analysis. Am J Epidemiol 151(5):531–539PubMedCrossRef
60.
go back to reference Bunin GR, Gyllstrom ME, Brown JE, Kahn EB, Kushi LH (2001) Recall of diet during a past pregnancy. Am J Epidemiol 154(12):1136–1142PubMedCrossRef Bunin GR, Gyllstrom ME, Brown JE, Kahn EB, Kushi LH (2001) Recall of diet during a past pregnancy. Am J Epidemiol 154(12):1136–1142PubMedCrossRef
61.
go back to reference Willett WC (2013) Nutritional Epidemiology, vol 40. Monographs in Epidemiology and Biostatistics Oxford University Press, New York Willett WC (2013) Nutritional Epidemiology, vol 40. Monographs in Epidemiology and Biostatistics Oxford University Press, New York
62.
go back to reference Byers T (2001) Food frequency dietary assessment: how bad is good enough? Am J Epidemiol 154(12):1087–1088PubMedCrossRef Byers T (2001) Food frequency dietary assessment: how bad is good enough? Am J Epidemiol 154(12):1087–1088PubMedCrossRef
63.
go back to reference Drews CD, Kraus JF, Greenland S (1990) Recall bias in a case-control study of sudden infant death syndrome. Int J Epidemiol 19(2):405–411PubMedCrossRef Drews CD, Kraus JF, Greenland S (1990) Recall bias in a case-control study of sudden infant death syndrome. Int J Epidemiol 19(2):405–411PubMedCrossRef
64.
go back to reference Infante-Rivard C, Jacques L (2000) Empirical study of parental recall bias. Am J Epidemiol 152(5):480–486PubMedCrossRef Infante-Rivard C, Jacques L (2000) Empirical study of parental recall bias. Am J Epidemiol 152(5):480–486PubMedCrossRef
65.
go back to reference Kwan ML, Metayer C, Crouse V, Buffler PA (2007) Maternal illness and drug/medication use during the period surrounding pregnancy and risk of childhood leukemia among offspring. Am J Epidemiol 165(1):27–35. doi:10.1093/aje/kwj336 PubMedCrossRef Kwan ML, Metayer C, Crouse V, Buffler PA (2007) Maternal illness and drug/medication use during the period surrounding pregnancy and risk of childhood leukemia among offspring. Am J Epidemiol 165(1):27–35. doi:10.​1093/​aje/​kwj336 PubMedCrossRef
Metadata
Title
Maternal prenatal intake of one-carbon metabolism nutrients and risk of childhood leukemia
Authors
Amanda W. Singer
Steve Selvin
Gladys Block
Carla Golden
Suzan L. Carmichael
Catherine Metayer
Publication date
01-07-2016
Publisher
Springer International Publishing
Published in
Cancer Causes & Control / Issue 7/2016
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-016-0773-y

Other articles of this Issue 7/2016

Cancer Causes & Control 7/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine