Folate and long-chain polyunsaturated fatty acid supplementation during pregnancy has long-term effects on the attention system of 8.5-y-old offspring: A randomized controlled trial

American Journal of Clinical Nutrition

Volumn 103, Issue 1, 2016, Pages 115-127

  Catena, Andrés ^a   Angela Munoz Machicao J ^b   Torres Espínola, Francisco J ^b   Martínez Zaldívar, Cristina ^b   Diaz Piedra, Carolina ^a   Gil, Angel ^b   Haile, Gudrun ^d   Gyorei, Eszter ^e   Molloy, Anne M ^e   Decsi, Tamás ^e   Koletzko, Berthold ^c   Campoy, Cristina ^b,c  

^a CIMCYC   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^d UNIVERSITY OF PÉCS   (Hungary)

^e TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Attention; Child development; Evoked potentials; Folate; Polyunsaturated fatty acids; Prenatal nutrition

Indexed keywords

5 METHYLTETRAHYDROFOLIC ACID; FOLIC ACID; PLACEBO; 5-METHYLTETRAHYDROFOLATE; EDIBLE OIL; FISH OIL; TETRAHYDROFOLIC ACID DERIVATIVE; VITAMIN B COMPLEX;

ADULT; ARTICLE; ATTENTION; ATTENTION NETWORK TEST; CHILD; COGNITIVE FUNCTION TEST; CONTROLLED STUDY; DIET SUPPLEMENTATION; ELECTROENCEPHALOGRAPHY; EVENT RELATED POTENTIAL; FEMALE; GENETIC POLYMORPHISM; HUMAN; LOW RESOLUTION BRAIN ELECTROMAGNETIC TOMOGRAPHY; MAJOR CLINICAL STUDY; MATERNAL NUTRITION; MOTHER; MULTICENTER STUDY; PREGNANCY; PROGENY; RANDOMIZED CONTROLLED TRIAL; REACTION TIME; BRAIN; CHILD DEVELOPMENT; DIETARY SUPPLEMENT; DOUBLE BLIND PROCEDURE; EXECUTIVE FUNCTION; FETUS DEVELOPMENT; GROWTH, DEVELOPMENT AND AGING; MALE; PHYSIOLOGY;

ADULT; ATTENTION; BRAIN; CHILD; CHILD DEVELOPMENT; DIETARY FATS, UNSATURATED; DIETARY SUPPLEMENTS; DOUBLE-BLIND METHOD; EXECUTIVE FUNCTION; FEMALE; FETAL DEVELOPMENT; FISH OILS; FOLIC ACID; HUMANS; MALE; PREGNANCY; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; TETRAHYDROFOLATES; VITAMIN B COMPLEX;

EID: 84953864308     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.115.109108     Document Type: Article

References (88)

1. Anjos T, Altmäe S, Emmett P, Tiemeier H, Closa-Monasterolo R, Luque V, Wiseman S, Pérez-García M, Lattka E, Demmelmair H, et al. Nutrition and neurodevelopment in children: focus on NUTRIMENTHE project. Eur J Nutr 2013;52:1825-42.
2. Elmadfa I, Meyer AL. Vitamins for the first 1000 days: preparing for life. Int J Vitam Nutr Res 2012;82(5):342-7.
3. Innis SM. Perinatal biochemistry and physiology of long-chain poly-unsaturated fatty acids. J Pediatr 2003;143(4 Suppl):S1-8.
4. Julvez J, Fortuny J, Mendez M, Torrent M, Ribas-Fitó 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;23:199-206.
5. Antonow-Schlorke I, Schwab M, Cox LA, Li C, Stuchlik K, Witte OW, Nathanielsz PW, McDonald TJ. Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. Proc Natl Acad Sci USA 2011;108:3011-6.
6. Campoy C, Escolano-Margarit MV, Anjos T, Szajewska H, Uauy R. Omega 3 fatty acids on child growth, visual acuity and neuro-development. Br J Nutr 2012;107(Suppl 2):S85-106.
7. Innis SM. Dietary (n-3) fatty acids and brain development. J Nutr 2007; 137:855-9.
8. Koletzko B, Boey CCM, Campoy C, Carlson SE, Chang N, Guillermo-Tuazon MA, Joshi S, Prell C, Quak SH, Sjarif DR, et al. Current information and Asian perspectives on long-chain polyunsaturated fatty acids in pregnancy, lactation, and infancy: systematic review and practice recommendations from an Early Nutrition Academy Workshop. Ann Nutr Metab 2014;65:49-80.
9. Stillwell W, Shaikh SR, Zerouga M, Siddiqui R, Wassall S.R. Doco-sahexaenoic acid affects cell signaling by altering lipid rafts. Reprod Nutr Dev 2005;45:559-79.
10. Kitajka K, Puskás LG, Zvara A, Hackler L, Barceló-Coblijn G, Ye o YK, Farkas T. The role of n-3 polyunsaturated fatty acids in brain: modulation of rat brain gene expression by dietary n-3 fatty acids. Proc Natl Acad Sci USA 2002;99:2619-24.
11. Coti Bertrand P, O'Kusky JR, Innis SM. Maternal dietary (n-3) fatty acid deficiency alters neurogenesis in the embryonic rat brain. J Nutr 2006;136:1570-5.
12. Lauritzen L, Jørgensen MH, Olsen SF, Straarup EM, Michaelsen KF. Maternal fish oil supplementation in lactation: effect on developmental outcome in breast-fed infants. Reprod Nutr Dev 2005;45:535-47.
13. Campoy C, Escolano-Margarit MV, Ramos R, Parrilla-Roure M, Csábi G, Beyer J, Ramirez-Tortosa MC, Molloy AM, Decsi T, Koletzko BV. Effects of prenatal fish-oil and 5-methyltetrahydrofolate supplemen-tation on cognitive development of children at 6.5 y of age. Am J Clin Nutr 2011;94(6 Suppl):1880S-8S.
14. Escolano-Margarit MV, Ramos R, Beyer J, Csábi G, Parrilla-Roure M, Cruz F, Perez-Garcia M, Hadders-Algra M, Gil A, Decsi T, et al. Prenatal DHA status and neurological outcome in children at age 5.5 years are positively associated. J Nutr 2011;141:1216-23.
15. Helland IB, Smith L, Blomén B, Saarem K, Saugstad OD, Drevon CA. Effect of supplementing pregnant and lactating mothers with n-3 very-long-chain fatty acids on children's IQ and body mass index at 7 years of age. Pediatrics 2008;122:e472-9.
16. Smithers LG, Gibson RA, Makrides M. Maternal supplementation with docosahexaenoic acid during pregnancy does not affect early visual development in the infant: a randomized controlled trial. Am J Clin Nutr 2011;93:1293-9.
17. Gould JF, Makrides M, Colombo J, Smithers LG. Randomized controlled trial of maternal omega-3 long-chain PUFA supplementation during pregnancy and early childhood development of attention, working memory, and inhibitory control. Am J Clin Nutr 2014;99:851-9.
18. McNamara RK, Able J, Jandacek R, Rider T, Tso P, Eliassen JC, Alfieri D, Weber W, Jarvis K, DelBello MP, et al. Docosahexaenoic acid supplementation increases prefrontal cortex activation during sustained attention in healthy boys: a placebo-controlled, dose-ranging, functional magnetic resonance imaging study. Am J Clin Nutr 2010;91: 1060-7.
19. Colombo J, Kannass KN, Shaddy DJ, Kundurthi S, Maikranz JM, Anderson CJ, Blaga OM, Carlson SE. Maternal DHA and the development of attention in infancy and toddlerhood. Child Dev 2004;75: 1254-67.
20. Sagiv SK, Thurston SW, Bellinger DC, Amarasiriwardena C, Korrick SA. Prenatal exposure to mercury and fish consumption during pregnancy and attention-deficit/hyperactivity disorder-related behavior in children. Arch Pediatr Adolesc Med 2012;166:1123-31.
21. Crider KS, Devine O, Hao L, Dowling NF, Li S, Molloy AM, Li Z, Zhu J, Berry RJ. Population red blood cell folate concentrations for prevention of neural tube defects: Bayesian model. BMJ 2014;349:g4554.
22. Mattson MP, Shea TB. Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders. Trends Neurosci 2003;26: 137-46.
23. Pérez-Dueñas B, Ormazábal A, Toma C, Torrico B, Cormand B, Serrano M, Sierra C, De Grandis E, Marfa MP, García-Cazorla A, et al. Cerebral folate deficiency syndromes in childhood: clinical, analytical, and etiologic aspects. Arch Neurol 2011;68:615-21.
24. Sram RJ, Binkova B, Lnenickova Z, Solansky I, Dejmek J. The impact of plasma folate levels of mothers and newborns on intrauterine growth retardation and birth weight. Mutat Res 2005;591:302-10.
25. Trabetti E. Homocysteine, MTHFR gene polymorphisms, and cardio-cerebrovascular risk. J Appl Genet 2008;49:267-82.
26. Roza SJ, van Batenburg-Eddes T, Steegers EAP, Jaddoe VWV, 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.
27. Schlotz W, Jones A, Phillips DIW, 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 Psy-chol Psychiatry 2010;51:594-602.
28. Nguyen CT, Gracely EJ, Lee BK. Serum folate but not vitamin B-12 concentrations are positively associated with cognitive test scores in children aged 6-16 years. J Nutr 2013;143:500-4.
29. Veena SR, Krishnaveni GV, Srinivasan K, Wills AK, Muthayya S, Kurpad AV, Yajnik CS, Fall C.H. Higher maternal plasma folate but not vitamin B-12 concentrations during pregnancy are associated with better cognitive function scores in 9-to 10-year-old children in South India. J Nutr 2010;140:1014-22.
30. Skórka A, Gieruszczak-Bialek D, Piescik M, Szajewska H. Effects of prenatal and/or postnatal (maternal and/or child) folic acid supple-mentation on the mental performance of children. Crit Rev Food Sci Nutr 2012;52:959-64.
31. Petersen SE, Posner MI. The attention system of the human brain: 20 years after. Annu Rev Neurosci 2012;35:73-89.
32. Raz A, Buhle J. Typologies of attentional networks. Nat Rev Neurosci 2006;7:367-79.
33. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD. Conflict monitoring and cognitive control. Psychol Rev 2001;108:624-52.
34. MacDonald AW, Cohen JD, Stenger VA, Carter CS. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 2000;288:1835-8.
35. Shenhav A, Botvinick MM, Cohen JD. The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 2013;79:217-40.
36. Karch S, Feuerecker R, Leicht G, Meindl T, Hantschk I, Kirsch V, Ertl M, Lutz J, Pogarell O, Mulert C. Separating distinct aspects of the voluntary selection between response alternatives: N2-and P3-related BOLD responses. Neuroimage 2010;51:356-64.
37. Albert J, López-Martín S, Hinojosa JA, Carretié L. Spatiotemporal characterization of response inhibition. Neuroimage 2013;76:272-81.
38. Isaacs EB. Neuroimaging, a new tool for investigating the effects of early diet on cognitive and brain development. Front Hum Neurosci 2013;7:445.
39. Paus T. A primer for brain imaging: a tool for evidence-based studies of nutrition? Nutr Rev 2010;68(Suppl 1):S29-37.
40. Sizonenko SV, Babiloni C, Sijben JW, Walhovd KB. Brain imaging and human nutrition: which measures to use in intervention studies? Adv Nutr 2013;4:554-6.
41. Ambrosini E, Vastano R, Montefinese M, Ciavarro M. Functional specificity of the locus coeruleus-norepinephrine system in the atten-tional networks. Front Behav Neurosci 2013;7:201.
42. Chica AB, Bartolomeo P, Valero-Cabré A. Dorsal and ventral parietal contributions to spatial orienting in the human brain. J Neu-rosci 2011;31:8143-9.
43. Krauss-Etschmann S, Shadid R, Campoy C, Hoster E, Demmelmair H, Jiménez M, Gil A, Rivero M, Veszprémi B, Decsi T, et al; Nutrition and Health Lifestyle (NUHEAL) Study Group. Effects of fish-oil and folate supplementation of pregnant women on maternal and fetal plasma concentrations of docosahexaenoic acid and eicosapentaenoic acid: a European randomized multicenter trial. Am J Clin Nutr 2007;85:1392-400.
44. Kolarovic L, Fournier NC. A comparison of extraction methods for the isolation of phospholipids from biological sources. Anal Biochem 1986;156:244-50.
45. Agren JJ, Julkunen A, Penttilä I. Rapid separation of serum lipids for fatty acid analysis by a single aminopropyl column. J Lipid Res 1992;33:1871-6.
46. Lepage G, Roy CC. Direct transesterification of all classes of lipids in a one-step reaction. J Lipid Res 1986;27:114-20.
47. Molloy AM, Scott JM. Microbiological assay for serum, plasma, and red cell folate using cryopreserved, microtiter plate method. Methods Enzymol 1997;281:43-53.
48. Fazili Z, Pfeiffer CM, Zhang M, Jain R. Erythrocyte folate extraction and quantitative determination by liquid chromatography-tandem mass spectrometry: comparison of results with microbiologic assay. Clin Chem 2005;51:2318-25.
49. Pfeiffer CM, Fazili Z, McCoy L, Zhang M, Gunter EW. Determination of folate vitamers in human serum by stable-isotope-dilution tandem mass spectrometry and comparison with radioassay and microbiologic assay. Clin Chem 2004;50:423-32.
50. Windelberg A, Arseth O, Kvalheim G, Ueland PM. Automated assay for the determination of methylmalonic acid, total homocysteine, and related amino acids in human serum or plasma by means of methyl-chloroformate derivatization and gas chromatography-mass spectrom-etry. Clin Chem 2005;51:2103-9.
51. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for ex-tracting DNA from human nucleated cells. Nucleic Acids Res 1988;16:1215.
52. Rueda MR, Fan J, McCandliss BD, Halparin JD, Gruber DB, Lercari LP, Posner MI. Development of attentional networks in childhood. Neuropsychologia 2004;42:1029-40.
53. Fan J, McCandliss BD, Sommer T, Raz A, Posner MI. Testing the efficiency and independence of attentional networks. J Cogn Neurosci 2002;14:340-7.
54. Belouchrani A, Abed-Meraim K, Cardoso J-F, Moulines E. A blind source separation technique using second-order statistics. IEEE Trans Signal Process 1997;45:434-44.
55. Tang AC, Sutherland MT, McKinney CJ. Validation of SOBI components from high-density EEG. Neuroimage 2005;25:539-53.
56. Mognon A, Jovicich J, Bruzzone L, Buiatti M. ADJUST: an automatic EEG artifact detector based on the joint use of spatial and temporal features. Psychophysiology 2011;48:229-40.
57. Groppe DM, Urbach TP, Kutas M. Mass univariate analysis of event-related brain potentials/fields I: a critical tutorial review. Psychophys-iology 2011;48:1711-25.
58. Pascual-Marqui RD. Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 2002;24(Suppl D):5-12.
59. Braver TS, Barch DM, Gray JR, Molfese DL, Snyder A. Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. Cereb Cortex. 2001;11(9):825-36.
60. Falkenstein M, Hoormann J, Hohnsbein J. ERP components in Go/Nogo tasks and their relation to inhibition. Acta Psychol (Amst) 1999;101:267-91.
61. Folstein JR, Van Petten C. Influence of cognitive control and mismatch on the N2 component of the ERP: a review. Psychophysiology 2008; 45:152-70.
62. Jones AD, Cho RY, Nystrom LE, Cohen JD, Braver TS. A computa-tional model of anterior cingulate function in speeded response tasks: effects of frequency, sequence, and conflict. Cogn Affect Behav Neu-rosci 2002;2:300-17.
63. Lo Y-H, Liang W-K, Lee H-W, Wang C-H, Tzeng OJL, Hung DL, Cheng SK, Juan C.H. The neural development of response inhibition in 5-and 6-year-old preschoolers: an ERP and EEG study. Dev Neuro-psychol 2013;38:301-16.
64. Patel SH, Azzam PN. Characterization of N200 and P300: selected studies of the event-related potential. Int J Med Sci 2005;2:147-54.
65. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, Greenstein D, Clasen L, Evans A, Rapoport JL, et al. Neuro-developmental trajectories of the human cerebral cortex. J Neurosci 2008;28:3586-94.
66. Abundis-Gutiérrez A, Checa P, Castellanos C, Rosario Rueda M. Electrophysiological correlates of attention networks in childhood and early adulthood. Neuropsychologia 2014;57:78-92.
67. Espinet SD, Anderson JE, Zelazo PD. Reflection training improves executive function in preschool-age children: behavioral and neural effects. Dev Cogn Neurosci 2013;4:3-15.
68. Fedorenko E, Duncan J, Kanwisher N. Broad domain generality in focal regions of frontal and parietal cortex. Proc Natl Acad Sci USA 2013;110:16616-21.
69. van Meel CS, Heslenfeld DJ, Rommelse NN, Oosterlaan J, Sergeant JA. Developmental trajectories of neural mechanisms supporting con-flict and error processing in middle childhood. Dev Neuropsychol 2012;37:358-78.
70. Roffman JL, Brohawn DG, Friedman JS, Dyckman KA, Thakkar KN, Agam Y, Vangel MG, Goff DC, Manoach DS. MTHFR 677C.T effects on anterior cingulate structure and function during response monitoring in schizophrenia: a preliminary study. Brain Imaging Behav 2011;5:65-75.
71. Roffman JL, Nitenson AZ, Agam Y, Isom M, Friedman JS, Dyckman KA, Brohawn DG, Smoller JW, Goff DC, Manoach DS. A hypo-methylating variant of MTHFR, 677C.T, blunts the neural response to errors in patients with schizophrenia and healthy individuals. PLoS One 2011;6:e25253.
72. Willette AA, Gallagher C, Bendlin BB, McLaren DG, Kastman EK, Canu E, Kosmatka KJ, Field AS, Alexander AL, Colman RJ, et al. Homocysteine, neural atrophy, and the effect of caloric restriction in rhesus monkeys. Neurobiol Aging 2012;33:670-80.
73. Roffman JL, Gollub RL, Calhoun VD, Wassink TH, Weiss AP, Ho BC, White T, Clark VP, Fries J, Andreasen NC, et al. MTHFR 677C/T genotype disrupts prefrontal function in schizophrenia through an interaction with COMT 158Val/Met. Proc Natl Acad Sci USA 2008;105:17573-8.
74. Gould JF, Smithers LG, Makrides M. The effect of maternal omega-3 (n-3) LCPUFA supplementation during pregnancy on early childhood cognitive and visual development: a systematic review and meta-analysis of randomized controlled trials. Am J Clin Nutr 2013;97:531-44.
75. Cheatham CL, Nerhammer AS, Asserhøj M, Michaelsen KF, Lauritzen L. Fish oil supplementation during lactation: effects on cognition and behavior at 7 years of age. Lipids 2011;46:637-45.
76. Jackson PA, Reay JL, Scholey AB, Kennedy DO. Docosahexaenoic acid-rich fish oil modulates the cerebral hemodynamic response to cognitive tasks in healthy young adults. Biol Psychol 2012;89:183-90.
77. Yi SHL, Kable JA, Evatt ML, Singh RH. A randomized, placebo-controlled, double-blind trial of supplemental docosahexaenoic acid on cognitive processing speed and executive function in females of reproductive age with phenylketonuria: a pilot study. Prostaglandins Leukot Essent Fatty Acids 2011;85:317-27.
78. Rao S, Joshi S, Kale A, Hegde M, Mahadik S. Maternal folic acid supplementation to dams on marginal protein level alters brain fatty acid levels of their adult offspring. Metabolism 2006;55:628-34.
79. Steenweg-de Graaff J, Roza SJ, Steegers EA, Hofman A, Verhulst FC, Jaddoe VW, Tiemeier H. Maternal folate status in early pregnancy and child emotional and behavioral problems: the Generation R Study. Am J Clin Nutr 2012;95:1413-21.
80. Meher A, Joshi A, Joshi S. Differential regulation of hepatic transcription factors in the Wistar rat offspring born to dams fed folic acid, vitamin B12 deficient diets and supplemented with omega-3 fatty acids. PLoS One 2014;9(2):e90209.
81. Umhau JC, Dauphinais KM, Patel SH, Nahrwold DA, Hibbeln JR, Rawlings RR, George DT. The relationship between folate and docosahexaenoic acid in men. Eur J Clin Nutr 2006;60:352-7.
82. Callejas A, Lupiàñez J, Funes MJ, Tudela P. Modulations among the alerting, orienting and executive control networks. Exp Brain Res 2005;167:27-37.
83. Hamazaki K, Itomura M, Huan M, Nishizawa H, Sawazaki S, Tanouchi M, Watanabe S, Hamazaki T, Terasawa K, Yazawa K. Effect of omega-3 fatty acid-containing phospholipids on blood catecholamine concentrations in healthy volunteers: a randomized, placebo-controlled, double-blind trial. Nutrition 2005;21:705-10.
84. Aston-Jones G, Chiang C, Alexinsky T. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 1991;88:501-20.
85. Birnbaum S, Gobeske KT, Auerbach J, Taylor JR, Arnsten AF. A role for norepinephrine in stress-induced cognitive deficits: alpha-1-adrenoceptor mediation in the prefrontal cortex. Biol Psychiatry 1999;46:1266-74.
86. Finlay JM, Zigmond MJ, Abercrombie ED. Increased dopamine and norepinephrine release in medial prefrontal cortex induced by acute and chronic stress: effects of diazepam. Neuroscience 1995;64:619-28.
87. Rajkowski J, Kubiak P, Aston-Jones G. Locus coeruleus activity in monkey: phasic and tonic changes are associated with altered vigilance. Brain Res Bull 1994;35:607-16.
88. Usher M, Cohen JD, Servan-Schreiber D, Rajkowski J, Aston-Jones G. The role of locus coeruleus in the regulation of cognitive performance. Science 1999;283:549-54.