Maternal periconceptional folic acid intake and risk of autism spectrum disorders and developmental delay in the CHARGE (CHildhood Autism Risks from Genetics and Environment) case-control study

American Journal of Clinical Nutrition

Volumn 96, Issue 1, 2012, Pages 80-89

  Schmidt, Rebecca J ^a,b   Tancredi, Daniel J ^a   Ozonoff, Sally ^a,b   Hansen, Robin L ^a,b   Hartiala, Jaana ^c   Allayee, Hooman ^c   Schmidt, Linda C ^a   Tassone, Flora ^a,b   Hertz Picciotto, Irva ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FOLIC ACID;

ADULT; AGED; ARTICLE; AUTISM; CASE CONTROL STUDY; CEREAL; CONCEPTION; CONFIDENCE INTERVAL; CONTROLLED STUDY; ENVIRONMENT; FEMALE; FOLATE METABOLISM; GENETICS; HUMAN; MAJOR CLINICAL STUDY; MALE; MATERNAL CARE; MATERNAL NUTRITION; PREGNANCY; RISK; TELECONSULTATION; VITAMIN INTAKE;

CALIFORNIA; CASE-CONTROL STUDIES; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CHILD, PRESCHOOL; CONFOUNDING FACTORS (EPIDEMIOLOGY); DEVELOPMENTAL DISABILITIES; DIET; DIETARY SUPPLEMENTS; FEMALE; FOLIC ACID; FOLIC ACID DEFICIENCY; FOOD, FORTIFIED; GENETIC ASSOCIATION STUDIES; HUMANS; INFANT; MALE; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; METHYLENETETRAHYDROFOLATE REDUCTASE (NADPH2); POLYMORPHISM, SINGLE NUCLEOTIDE; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY TRIMESTER, FIRST; RISK;

EID: 84863600970     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.110.004416     Document Type: Article

References (66)

1. Greenblatt JM, Huffman LC, Reiss AL. Folic acid in neurodevelopment and child psychiatry. Prog Neuropsychopharmacol Biol Psychiatry 1994;18:647-60. (Pubitemid 24238872)
2. Medical Research Council Vitamin Study Research Group. Prevention of neural tube defects: results of the Medical Research Council Vitamin Study. Lancet 1991;338:131-7.
3. Centers for Disease Control and Prevention. Recommendations for the use of folic acid to reduce the number of cases of spina bifida and other neural tube defects. MMWR Morb Mortal Wkly Rep 1992;41(RR-14):1-7.
4. Henshaw SK. Unintended pregnancy in the United States. Fam Plann Perspect 1998;30:24-9, 46.
5. US Food and Drug Administration. Food standards: amendment of standards of identity for enriched grain products to require addition of folic acid. Fed Regist 1996;61:8781-97.
6. Honein MA, Paulozzi LJ, Mathews TJ, Erickson JD, Wong LY. Impact of folic acid fortification of the US food supply on the occurrence of neural tube defects. JAMA 2001;285(23):2981-6. (Pubitemid 32550116)
7. Boulet SL, Yang Q, Mai C, Kirby RS, Collins JS, Robbins JM, Meyer R, Canfield MA, Mulinare J. Trends in the postfortification prevalence of spina bifida and anencephaly in the United States. Birth Defects Res A Clin Mol Teratol 2008;82:527-32. (Pubitemid 352032357)
8. Rodier PM, Ingram JL, Tisdale B, Nelson S, Romano J. Embryological origin for autism: developmental anomalies of the cranial nerve motor nuclei. J Comp Neurol 1996;370:247-61. (Pubitemid 26227148)
9. Froster-Iskenius U, Bodeker K, Oepen T, Matthes R, Piper U, Schwinger E. Folic acid treatment in males and females with fragile-(X)-syndrome. Am J Med Genet 1986;23:273-89. (Pubitemid 16139734)
10. Ramaekers VT, Blau N. Cerebral folate deficiency. Dev Med Child Neurol 2004;46:843-51. (Pubitemid 39549660)
11. Moretti P, Peters SU, Del Gaudio D, Sahoo T, Hyland K, Bottiglieri T, Hopkin RJ, Peach E, Min SH, Goldman D, et al. Brief report: autistic symptoms, developmental regression, mental retardation, epilepsy, and dyskinesias in CNS folate deficiency. J Autism Dev Disord 2008;38:1170-7.
12. Ramaekers VT, Blau N, Sequeira JM, Nassogne MC, Quadros EV. Folate receptor autoimmunity and cerebral folate deficiency in low-functioning autism with neurological deficits. Neuropediatrics 2007;38:276-81. (Pubitemid 351737986)
13. Frye RE, Sequeira JM, Quadros EV, James SJ, Rossignol DA. Cerebral folate receptor autoantibodies in autism spectrum disorder. Mol Psychiatry 2012;Jan 10 (Epub ahead of print; DOI:10.1038/mp.2011.175).
14. James SJ, Melnyk S, Fuchs G, Reid T, Jernigan S, Pavliv O, Hubanks A, Gaylor DW. Efficacy of methylcobalamin and folinic acid treatment on glutathione redox status in children with autism. Am J Clin Nutr 2009;89:425-30.
15. Rogers EJ. Has enhanced folate status during pregnancy altered natural selection and possibly autism prevalence? A closer look at a possible link. Med Hypotheses 2008;71:406-10.
16. Muñoz-Moran E, Dieguez-Lucena JL, Fernandez-Arcas N, Peran-Mesa S, Reyes-Engel A. Genetic selection and folate intake during pregnancy. Lancet 1998;352:1120-1. (Pubitemid 28448525)
17. Reyes-Engel A, Munoz E, Gaitan MJ, Fabre E, Gallo M, Dieguez JL, Ruiz M, Morell M. Implications on human fertility of the 677C → T and 1298A → C polymorphisms of the MTHFR gene: consequences of a possible genetic selection. Mol Hum Reprod 2002;8:952-7. (Pubitemid 35174931)
18. Haggarty P, Campbell DM, Duthie S, Andrews K, Hoad G, Piyathilake C, Fraser I, McNeill G. Folic acid use in pregnancy and embryo selection. BJOG 2008;115:851-6. (Pubitemid 351693016)
19. James SJ, Melnyk S, Jernigan S, Cleves MA, Halsted CH, Wong DH, Cutler P, Bock K, Boris M, Bradstreet JJ, et al. Metabolic endophenotype and related genotypes are associated with oxidative stress in children with autism. Am J Med Genet B Neuropsychiatr Genet 2006;141B:947-56. (Pubitemid 44905454)
20. James SJ, Melnyk S, Jernigan S, Pavliv O, Trusty T, Lehman S, Seidel L, Gaylor DW, Cleves MA. A functional polymorphism in the reduced folate carrier gene and DNA hypomethylation in mothers of children with autism. Am J Med Genet B Neuropsychiatr Genet 2010;153B:1209-20.
21. Hertz-Picciotto I, Croen LA, Hansen R, Jones CR, van de Water J, Pessah IN. The CHARGE study: an epidemiologic investigation of genetic and environmental factors contributing to autism. Environ Health Perspect 2006;114:1119-25. (Pubitemid 44018911)
22. Mullen EM. Scales of Early Learning. Circle Pines, MN: American Guidance Services Inc, 1995.
23. Sparrow SS, Balla DA, Cicchetti DV. Vineland Adaptive Behavior Scales: interview edition, expanded form manual. Circle Pines, MN: American Guidance Services Inc, 1984.
24. Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 1994;24:659-85. (Pubitemid 24309810)
25. Lord C, Pickles A, McLennan J, Rutter M, Bregman J, Folstein S, Fombonne E, Leboyer M, Minshew N. Diagnosing autism: analyses of data from the Autism Diagnostic Interview. J Autism Dev Disord 1997;27:501-17. (Pubitemid 27513149)
26. Lord C, Rutter M, DiLavore PC, Risi S. The Autism Diagnostic Observation Schedule (ADOS). Los Angeles, CA: Western Psychological Services, 2000.
27. Lord C, Rutter M, DiLavore PC, Risi S. Autism Diagnostic Observation Schedule manual. Los Angeles, CA: Western Psychological Services, 2003.
28. Risi S, Lord C, Gotham K, Corsello C, Chrysler C, Szatmari P, Cook EH Jr, Leventhal BL, Pickles A. Combining information from multiple sources in the diagnosis of autism spectrum disorders. J Am Acad Child Adolesc Psychiatry 2006;45(9):1094-103. (Pubitemid 44343065)
29. American Psychiatric Association. DSM-5 development: A 05 autism spectrum disorder. Arlington, VA: American Psychiatric Association. Available from: http://www.dsm5.org/ProposedRevisions/Pages/proposedrevision.aspx?rid=94# (cited 11 May 2012).
30. Schmidt RJ, Hansen RL, Hartiala J, Allayee H, Schmidt LC, Tancredi DJ, Tassone F, Hertz-Picciotto I. Prenatal vitamins, functional one-carbon metabolism gene variants, and risk for autism in the CHARGE Study. 2011.
31. US Department of Agriculture, Agricultural Research Service. USDA national nutrient database for standard reference, release 23. Nutrient Data Laboratory homepage. 2010. Available from: http://www.ars.usda.gov/ba/bhnrc/ndl (cited 11 May 2012).
32. Schmidt RJ, Hansen RL, Hartiala J, Allayee H, Schmidt LC, Tancredi DJ, Tassone F, Hertz-Picciotto I. Prenatal vitamins, one-carbon metabolism gene variants, and risk for autism. Epidemiology 2011;22:476-85.
33. Weinberg CR, Umbach DM. A hybrid design for studying genetic influences on risk of diseases with onset early in life. Am J Hum Genet 2005;77:627-36. (Pubitemid 41361609)
34. Agresti A. Categorical data analysis. 2nd ed. New York, NY: Wiley-Interscience, 2002.
35. Selvin S. Statistical analysis of epidemiologic data. 3rd ed. Oxford, United Kingdom: Oxford University Press, 2004.
36. MacKinnon DP, Krull JL, Lockwood CM. Equivalence of the mediation, confounding and suppression effect. Prev Sci 2000;1:173-81.
37. Schafer JL. Analysis of incomplete multivariate data. London, United Kingdom: Chapman & Hall, 1997.
38. Roza SJ, van Batenburg-Eddes T, Steegers EA, Jaddoe VW, Mackenbach JP, Hofman A, Verhulst FC, Tiemeier H. Maternal folic acid supplement use in early pregnancy and child behavioural problems: the Generation R Study. Br J Nutr 2010;103:445-52.
39. Roth C, Magnus P, Schjolberg S, Stoltenberg C, Suren P, McKeague IW, Davey Smith G, Reichborn-Kjennerud T, Susser E. Folic acid supplements in pregnancy and severe language delay in children. JAMA 2011;306(14):1566-73.
40. Julvez J, Fortuny J, Mendez M, Torrent M, Ribas-Fito N, Sunyer J. Maternal use of folic acid supplements during pregnancy and four-year-old neurodevelopment in a population-based birth cohort. Paediatr Perinat Epidemiol 2009;23(3):199-206.
41. Schlotz W, Jones A, Phillips DI, Gale CR, Robinson SM, Godfrey KM. Lower maternal folate status in early pregnancy is associated with childhood hyperactivity and peer problems in offspring. J Child Psychol Psychiatry 2010;51(5):594-602.
42. James SJ, Melnyk S, Jernigan S, Hubanks A, Rose S, Gaylor DW. Abnormal transmethylation/transsulfuration metabolism and DNA hypomethylation among parents of children with autism. J Autism Dev Disord 2008;38:1976.
43. Christensen B, Arbour L, Tran P, Leclerc D, Sabbaghian N, Platt R, Gilfix BM, Rosenblatt DS, Gravel RA, Forbes P, et al. Genetic polymorphisms in methylenetetrahydrofolate reductase and methionine synthase, folate levels in red blood cells, and risk of neural tube defects. Am J Med Genet 1999;84:151-7. (Pubitemid 29201082)
44. Daly S, Mills JL, Molloy AM, Conley M, McPartlin J, Lee YJ, Young PB, Kirke PN, Weir DG, Scott JM. Low-dose folic acid lowers plasma homocysteine levels in women of child-bearing age. QJM 2002;95:733-40. (Pubitemid 35276994)
45. Solon O, Riddell TJ, Quimbo SA, Butrick E, Aylward GP, Lou Bacate M, Peabody JW. Associations between cognitive function, blood lead concentration, and nutrition among children in the central Philippines. J Pediatr 2008;152:237-43.
46. Pufulete M, Al-Ghnaniem R, Khushal A, Appleby P, Harris N, Gout S, Emery PW, Sanders TA. Effect of folic acid supplementation on genomic DNA methylation in patients with colorectal adenoma. Gut 2005;54:648-53. (Pubitemid 40559249)
47. Schanen NC. Epigenetics of autism spectrum disorders. Hum Mol Genet 2006;15(2):R138-50. (Pubitemid 44446787)
48. Van den Veyver IB. Genetic effects of methylation diets. Annu Rev Nutr 2002;22:255-82. (Pubitemid 35221462)
49. Moretti R, Torre P, Antonello RM, Cattaruzza T, Cazzato G, Bava A. Vitamin B12 and folate depletion in cognition: a review. Neurol India 2004;52:310-8. (Pubitemid 39430183)
50. Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr 2002;132(suppl):2393S-400S. (Pubitemid 34848114)
51. Reik W, Walter J. Genomic imprinting: parental influence on the genome. Nat Rev Genet 2001;2:21-32. (Pubitemid 33674766)
52. Steegers-Theunissen RP, Obermann-Borst SA, Kremer D, Lindemans J, Siebel C, Steegers EA, Slagboom PE, Heijmans BT. 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 2009;4:e7845.
53. Blom HJ. Folic acid, methylation and neural tube closure in humans. Birth Defects Res A Clin Mol Teratol 2009;85:295-302.
54. Iskandar BJ, Rizk E, Meier B, Hariharan N, Bottiglieri T, Finnell RH, Jarrard DF, Banerjee RV, Skene JH, Nelson A, et al. Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J Clin Invest 2010;120(5):1603-16.
55. Yang QH, Carter HK, Mulinare J, Berry RJ, Friedman JM, Erickson JD. 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 2007;85:1409-16. (Pubitemid 46740486)
56. Yeung L, Yang Q, Berry RJ. Contributions of total daily intake of folic acid to serum folate concentrations. JAMA 2008;300:2486-7.
57. Gregory JF III. Case study: folate bioavailability. J Nutr 2001;131(suppl):1376S-82S.
58. Choumenkovitch SF, Selhub J, Wilson PW, Rader JI, Rosenberg IH, Jacques PF. Folic acid intake from fortification in United States exceeds predictions. J Nutr 2002;132:2792-8. (Pubitemid 35013272)
59. Burton A, Wilson S, Gillies AJ. Folic acid: is self reported use of supplements accurate? J Epidemiol Community Health 2001;55:841-2. (Pubitemid 32980466)
60. Brantsaeter AL, Haugen M, Hagve TA, Aksnes L, Rasmussen SE, Julshamn K, Alexander J, Meltzer HM. Self-reported dietary supplement use is confirmed by biological markers in the Norwegian Mother and Child Cohort Study (MoBa). Ann Nutr Metab 2007;51(2):146-54. (Pubitemid 46975993)
61. Jurek AM, Maldonado G, Spector LG, Ross JA. Periconceptional maternal vitamin supplementation and childhood leukaemia: an uncertainty analysis. J Epidemiol Community Health 2009;63(2):168-72.
62. Werler MM, Pober BR, Nelson K, Holmes LB. Reporting accuracy among mothers of malformed and nonmalformed infants. Am J Epidemiol 1989;129:415-21. (Pubitemid 19047007)
63. Bosco JL, Tseng M, Spector LG, Olshan AF, Bunin GR. Reproducibility of reported nutrient intake and supplement use during a past pregnancy: a report from the Children's Oncology Group. Paediatr Perinat Epidemiol 2010;24(1):93-101.
64. Dror DK, Allen LH. Effect of vitamin B12 deficiency on neurodevelopment in infants: current knowledge and possible mechanisms. Nutr Rev 2008;66:250-5. (Pubitemid 351623969)
65. Zeisel SH. Importance of methyl donors during reproduction. Am J Clin Nutr 2009;89:673S-7S.
66. Beard J. Recent evidence from human and animal studies regarding iron status and infant development. J Nutr 2007;137:524S-30S. (Pubitemid 46213476)