Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-13T03:04:39.488Z Has data issue: false hasContentIssue false
  • English
  • Français

Prenatal fish oil supplementation and early childhood development in the Upstate KIDS Study

Published online by Cambridge University Press:  24 April 2017

K. Vollet ,
A. Ghassabian ,
R. Sundaram ,
N. Chahal  and
E. H. Yeung
K. Vollet
Affiliation:
Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA
A. Ghassabian
Affiliation:
Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA Department of Pediatrics, New York University School of Medicine, New York, NY, USA
R. Sundaram
Affiliation:
Biostatistics and Bioinformatics Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA
N. Chahal
Affiliation:
Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA
E. H. Yeung*
Affiliation:
Epidemiology Branch, Division of Intramural Population Health Research, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD, USA
*
*Address for correspondence: Dr E. H. Yeung, 6710B Rockledge Dr., MSC 7004, Bethesda, MD 20817, USA. (Email yeungedw@mail.nih.gov)
Get access Rights & Permissions [Opens in a new window]

Abstract

Fish oil contains omega-3 fatty acids, which play a vital role in fetal growth and development. In utero exposure to omega-3 fatty acids is exclusively dependent on maternal nutrition. Previous studies have suggested that prenatal fish oil supplementation has positive impacts on child neurodevelopment later in life. This study examines the associations between fish oil supplementation both before pregnancy and throughout pregnancy and subsequent child development. Mother–child pairs from the Upstate KIDS Study, a birth cohort consisting of children born between 2008 and 2010, were included. Self-reported prenatal fish oil supplementation data were available for 5845 children (3807 singletons and 2038 twins). At multiple time points, from 4 months to 3 years of age, child development was reported by the parents on the Ages and Stages Questionnaire (ASQ). Five developmental domains were assessed: fine motor, gross motor, communication, personal–social functioning and problem solving. Generalized linear mixed models were used to estimate odds ratios (OR) while adjusting for covariates. Primary analyses showed that the risk of failing the ASQ problem-solving domain was significantly lower among children of women who took fish oil before pregnancy (OR 0.40, 95% confidence intervals (CI) 0.18–0.89) and during pregnancy (OR 0.43, 95% CI 0.22–0.83). Gender interaction was not statistically significant, although stratified results indicated stronger associations among girls. Similarly, associations were primarily among singletons. Prenatal fish oil supplementation may be beneficial in regards to neurodevelopment. Specifically, it is associated with a lower risk of failing the problem-solving domain up to 3 years of age.

Keywords

child developmentfish oilomega-3 fatty acidsprenatalproblem solving
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 4: Themed Issue: Assisted Reproductive Treatments (ART) and DOHAD , August 2017 , pp. 465 - 473
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Barker, DJ, Clark, PM. Fetal undernutrition and disease in later life. Rev Reprod. 1997; 2, 105–112.CrossRefGoogle ScholarPubMed
2. Schlotz, W, Phillips, DI. Fetal origins of mental health: evidence and mechanisms. Brain Behav Immun. 2009; 23, 905–916.CrossRefGoogle ScholarPubMed
3. Bale, TL, Baram, TZ, Brown, AS, et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010; 68, 314–319.CrossRefGoogle ScholarPubMed
4. Weiser, MJ, Butt, CM, Mohajeri, MH. Docosahexaenoic acid and cognition throughout the lifespan. Nutrients. 2016; 8, 99.CrossRefGoogle ScholarPubMed
5. Karr, JE, Alexander, JE, Winningham, RG. Omega-3 polyunsaturated fatty acids and cognition throughout the lifespan: a review. Nutr Neurosci. 2011; 14, 216–225.CrossRefGoogle ScholarPubMed
6. Lauritzen, L, Hansen, HS, Jørgensen, MH, Michaelsen, KF. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res. 2001; 40, 1–94.Google Scholar
7. Yehuda, S, Rabinovitz, S, Mostofsky, DI. Essential fatty acids and the brain: from infancy to aging. Neurobiol Aging. 2005; 26(Suppl. 1), 98–102.Google Scholar
8. Coletta, JM, Bell, SJ, Roman, AS. Omega-3 fatty acids and pregnancy. Rev Obstet Gynecol. 2010; 3, 163–171.Google ScholarPubMed
9. Gow, RV, Hibbeln, JR. Omega-3 fatty acid and nutrient deficits in adverse neurodevelopment and childhood behaviors. Child Adolesc Psychiatr Clin N Am. 2014; 23, 555–590.CrossRefGoogle ScholarPubMed
10. Uauy, R, Mena, P, Wegher, B, Nieto, S, Salem, N. Long chain polyunsaturated fatty acid formation in neonates: effect of gestational age and intrauterine growth. Pediatr Res. 2000; 47, 127–135.CrossRefGoogle ScholarPubMed
11. Bobiński, R, Mikulska, M. The ins and outs of maternal-fetal fatty acid metabolism. Acta Biochim Pol. 2015; 62, 499–507.Google Scholar
12. Hadders-Algra, M. The neuromotor examination of the preschool child and its prognostic significance. Ment Retard Dev Disabil Res Rev. 2005; 11, 180–188.Google Scholar
13. 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, 531–544.CrossRefGoogle ScholarPubMed
14. Arterburn, LM, Hall, EB, Oken, H. Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr. 2006; 83(Suppl.), 1467S–1476S.Google Scholar
15. Koletzko, B, Larqué, E, Demmelmair, H. Placental transfer of long-chain polyunsaturated fatty acids (LC-PUFA). J Perinat Med. 2007; 35(Suppl. 1), S5–S11.CrossRefGoogle ScholarPubMed
16. Muldoon, MF, Ryan, CM, Yao, JK, Conklin, SM, Manuck, SB. Long-chain omega-3 fatty acids and optimization of cognitive performance. Mil Med. 2014; 179(Suppl.), 95–105.CrossRefGoogle ScholarPubMed
17. Dunstan, JA, Simmer, K, Dixon, G, Prescott, SL. Cognitive assessment of children at age 2(1/2) years after maternal fish oil supplementation in pregnancy: a randomised controlled trial. Arch Dis Child Fetal Neonatal Ed. 2008; 93, F45–F50.Google Scholar
18. Hibbeln, JR, Davis, JM, Steer, C, et al. Maternal seafood consumption in pregnancy and neurodevelopmental outcomes in childhood (ALSPAC study): an observational cohort study. Lancet. 2007; 369, 578–585.Google Scholar
19. Jacobson, JL, Jacobson, SW, Muckle, G, et al. Beneficial effects of a polyunsaturated fatty acid on infant development: evidence from the inuit of arctic Quebec. J Pediatr. 2008; 152, 356–364.Google Scholar
20. Boucher, O, Burden, MJ, Muckle, G, et al. Neurophysiologic and neurobehavioral evidence of beneficial effects of prenatal omega-3 fatty acid intake on memory function at school age. Am J Clin Nutr. 2011; 93, 1025–1037.Google Scholar
21. Lauritzen, L, Brambilla, P, Mazzocchi, A, et al. DHA effects in brain development and function. Nutrients. 2016; 8, 6.Google Scholar
22. Suganuma, H, Arai, Y, Kitamura, Y, et al. Maternal docosahexaenoic acid-enriched diet prevents neonatal brain injury. Neuropathology. 2010; 30, 597–605.CrossRefGoogle ScholarPubMed
23. Tuzun, F, Kumral, A, Ozbal, S, et al. Maternal prenatal omega-3 fatty acid supplementation attenuates hyperoxia-induced apoptosis in the developing rat brain. Int J Dev Neurosci. 2012; 30, 315–323.Google Scholar
24. Feng, Z, Zou, X, Jia, H, et al. Maternal docosahexaenoic acid feeding protects against impairment of learning and memory and oxidative stress in prenatally stressed rats: possible role of neuronal mitochondria metabolism. Antioxid Redox Signal. 2012; 16, 275–289.Google Scholar
25. Judge, MP, Cong, X, Harel, O, Courville, AB, Lammi-Keefe, CJ. Maternal consumption of a DHA-containing functional food benefits infant sleep patterning: an early neurodevelopmental measure. Early Hum Dev. 2012; 88, 531–537.Google Scholar
26. Escolano-Margarit, MV, Ramos, R, Beyer, J, et al. Prenatal DHA status and neurological outcome in children at age 5.5 years are positively associated. J Nutr. 2011; 141, 1216–1223.Google Scholar
27. Helland, IB, Smith, L, Saarem, K, Saugstad, OD, Drevon, CA. Maternal supplementation with very-long-chain n-3 fatty acids during pregnancy and lactation augments children’s IQ at 4 years of age. Pediatrics. 2003; 111, e39–e44.Google Scholar
28. Campoy, C, Escolano-Margarit, MV, Ramos, R, et al. Effects of prenatal fish-oil and 5-methyltetrahydrofolate supplementation on cognitive development of children at 6.5 y of age. Am J Clin Nutr. 2011; 94(Suppl.), 1880S–1888S.Google Scholar
29. Makrides, M, Gibson, RA, McPhee, AJ, et al. Effect of DHA supplementation during pregnancy on maternal depression and neurodevelopment of young children: a randomized controlled trial. JAMA. 2010; 304, 1675–1683.CrossRefGoogle ScholarPubMed
30. Meldrum, S, Dunstan, JA, Foster, JK, Simmer, K, Prescott, SL. Maternal fish oil supplementation in pregnancy: a 12 year follow-up of a randomised controlled trial. Nutrients. 2015; 7, 2061–2067.CrossRefGoogle ScholarPubMed
31. McFadyen, M, Farquharson, J, Cockburn, F. Maternal and umbilical cord erythrocyte omega-3 and omega-6 fatty acids and haemorheology in singleton and twin pregnancies. Arch Dis Child Fetal Neonatal Ed. 2003; 88, F134–F138.Google Scholar
32. Wadhawan, R, Oh, W, Vohr, BR, et al. Neurodevelopmental outcomes of triplets or higher-order extremely low birth weight infants. Pediatrics. 2011; 127, e654–e660.Google Scholar
33. Buck Louis, GM, Hediger, ML, Bell, EM, et al. Methodology for establishing a population-based birth cohort focusing on couple fertility and children’s development, the Upstate KIDS Study. Paediatr Perinat Epidemiol. 2014; 28, 191–202.Google Scholar
34. Squires, J, Bricker, D. Ages & Stages Questionnaires®, (ASQ-3™): A Parent-Completed Child-Monitoring System. 2009. Brookes Publishing Company: Baltimore, MD.Google Scholar
35. Gollenberg, AL, Lynch, CD, Jackson, LW, McGuinness, BM, Msall, ME. Concurrent validity of the parent-completed Ages and Stages Questionnaires, 2nd Ed. with the Bayley Scales of Infant Development II in a low-risk sample. Child Care Health Dev. 2010; 36, 485–490.Google Scholar
36. Squires, JPL, Bricker, D. The ASQ User’s Guide for the Ages & Stages Questionnaire: A Parent-Completed, Child-Monitoring System. 1999. Paul H. Brookes Publishing Co: Baltimore, MD.Google Scholar
37. WHO. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser. 2000; 894, i–xii, 1–253.Google Scholar
38. Hauser, RM. Measuring socioeconomic status in studies of child development. Child Dev. 1994; 65, 1541–1545.Google Scholar
39. Chin-Lun Hung, G, Hahn, J, Alamiri, B, et al. Socioeconomic disadvantage and neural development from infancy through early childhood. Int J Epidemiol. 2015; 44, 1889–1899.CrossRefGoogle ScholarPubMed
40. Yolton, K, Khoury, J, Xu, Y, et al. Low-level prenatal exposure to nicotine and infant neurobehavior. Neurotoxicol Teratol. 2009; 31, 356–363.CrossRefGoogle ScholarPubMed
41. Rubin, DB. Multiple Imputation for Nonresponse in Surveys. 2004. John Wiley & Sons: New York.Google Scholar
42. Diau, GY, Hsieh, AT, Sarkadi-Nagy, EA, et al. The influence of long chain polyunsaturate supplementation on docosahexaenoic acid and arachidonic acid in baboon neonate central nervous system. BMC Med. 2005; 3, 11.CrossRefGoogle ScholarPubMed
43. Cheatham, CL, Colombo, J, Carlson, SE. n-3 Fatty acids and cognitive and visual acuity development: methodologic and conceptual considerations. Am J Clin Nutr. 2006; 83(Suppl.), 1458S–1466S.CrossRefGoogle ScholarPubMed
44. Stonehouse, W. Does consumption of LC omega-3 PUFA enhance cognitive performance in healthy school-aged children and throughout adulthood? Evidence from clinical trials. Nutrients. 2014; 6, 2730–2758.Google Scholar
45. Drover, J, Hoffman, DR, Castañeda, YS, Morale, SE, Birch, EE. Three randomized controlled trials of early long-chain polyunsaturated fatty acid supplementation on means-end problem solving in 9-month-olds. Child Dev. 2009; 80, 1376–1384.Google Scholar
46. Cowan, N. Working memory underpins cognitive development, learning, and education. Educ Psychol Rev. 2014; 26, 197–223.Google Scholar
47. Colombo, J, Kannass, KN, Shaddy, DJ, et al. Maternal DHA and the development of attention in infancy and toddlerhood. Child Dev. 2004; 75, 1254–1267.Google Scholar
48. Catena, A, Muñoz-Machicao, JA, Torres-Espínola, FJ, et al. 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. Am J Clin Nutr. 2016; 103, 115–127.CrossRefGoogle ScholarPubMed
49. Bakker, EC, Hornstra, G, Blanco, CE, Vles, JS. Relationship between long-chain polyunsaturated fatty acids at birth and motor function at 7 years of age. Eur J Clin Nutr. 2009; 63, 499–504.Google Scholar
50. Ghassabian, A, Sundaram, R, Bell, E, et al. Gross motor milestones and subsequent development. Pediatrics. 2016; 138, e20154372.Google Scholar
51. McNamara, RK, Carlson, SE. Role of omega-3 fatty acids in brain development and function: potential implications for the pathogenesis and prevention of psychopathology. Prostaglandins Leukot Essent Fatty Acids. 2006; 75, 329–349.Google Scholar
52. Kobayashi, K. Role of catecholamine signaling in brain and nervous system functions: new insights from mouse molecular genetic study. J Investig Dermatol Symp Proc. 2001; 6, 115–121.CrossRefGoogle ScholarPubMed
53. Takeuchi, T, Fukumoto, Y, Harada, E. Influence of a dietary n-3 fatty acid deficiency on the cerebral catecholamine contents, EEG and learning ability in rat. Behav Brain Res. 2002; 131, 193–203.CrossRefGoogle ScholarPubMed
54. Luchtman, DW, Song, C. Cognitive enhancement by omega-3 fatty acids from child-hood to old age: findings from animal and clinical studies. Neuropharmacology. 2013; 64, 550–565.Google Scholar
55. Dyall, SC, Michael, GJ, Michael-Titus, AT. Omega-3 fatty acids reverse age-related decreases in nuclear receptors and increase neurogenesis in old rats. J Neurosci Res. 2010; 88, 2091–2102.Google Scholar
56. Kelly, L, Grehan, B, Chiesa, AD, et al. The polyunsaturated fatty acids, EPA and DPA exert a protective effect in the hippocampus of the aged rat. Neurobiol Aging. 2011; 32, 2318.e1–e15.CrossRefGoogle ScholarPubMed
57. Gamoh, S, Hashimoto, M, Hossain, S, Masumura, S. Chronic administration of docosahexaenoic acid improves the performance of radial arm maze task in aged rats. Clin Exp Pharmacol Physiol. 2001; 28, 266–270.CrossRefGoogle ScholarPubMed
58. Morris, MC, Evans, DA, Bienias, JL, et al. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch Neurol. 2003; 60, 940–946.CrossRefGoogle ScholarPubMed
59. Phillips, MA, Childs, CE, Calder, PC, Rogers, PJ. No effect of omega-3 fatty acid supplementation on cognition and mood in individuals with cognitive impairment and probable Alzheimer’s disease: a randomised controlled trial. Int J Mol Sci. 2015; 16, 24600–24613.Google Scholar
60. 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, 851–859.Google Scholar
61. Morse, NL. Benefits of docosahexaenoic acid, folic acid, vitamin D and iodine on foetal and infant brain development and function following maternal supplementation during pregnancy and lactation. Nutrients. 2012; 4, 799–840.Google Scholar
62. Holman, RT. The slow discovery of the importance of omega 3 essential fatty acids in human health. J Nutr. 1998; 128(Suppl.), 427S–433S.CrossRefGoogle ScholarPubMed
63. Huffman, SL, Harika, RK, Eilander, A, Osendarp, SJ. Essential fats: how do they affect growth and development of infants and young children in developing countries? A literature review. Matern Child Nutr. 2011; 7(Suppl. 3), 44–65.Google Scholar
64. Gil, A, Gil, F. Fish, a Mediterranean source of n-3 PUFA: benefits do not justify limiting consumption. Br J Nutr. 2015; 113(Suppl. 2), S58–S67.Google Scholar
65. Grandjean, P, Landrigan, PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006; 368, 2167–2178.Google Scholar
66. Childs, CE, Romeu-Nadal, M, Burdge, GC, Calder, PC. Gender differences in the n-3 fatty acid content of tissues. Proc Nutr Soc. 2008; 67, 19–27.Google Scholar
67. Lassek, WD, Gaulin, SJ. Sex differences in the relationship of dietary fatty acids to cognitive measures in American children. Front Evol Neurosci. 2011; 3, 5.Google Scholar
68. Sedlmeier, EM, Brunner, S, Much, D, et al. Human placental transcriptome shows sexually dimorphic gene expression and responsiveness to maternal dietary n-3 long-chain polyunsaturated fatty acid intervention during pregnancy. BMC Genomics. 2014; 15, 941.Google Scholar
69. Makrides, M, Gibson, RA, McPhee, AJ, et al. Neurodevelopmental outcomes of preterm infants fed high-dose docosahexaenoic acid: a randomized controlled trial. JAMA. 2009; 301, 175–182.Google Scholar
70. Clouard, C, Souza, AS, Gerrits, WJ, et al. Maternal fish oil supplementation affects the social behavior, brain fatty acid profile, and sickness response of piglets. J Nutr. 2015; 145, 2176–2184.CrossRefGoogle ScholarPubMed
71. Lorenz, JM. Neurodevelopmental outcomes of twins. Semin Perinatol. 2012; 36, 201–212.Google Scholar
72. Ronalds, GA, De Stavola, BL, Leon, DA. The cognitive cost of being a twin: evidence from comparisons within families in the Aberdeen children of the 1950s cohort study. BMJ. 2005; 331, 1306.Google Scholar
73. Olsen, SF, Secher, NJ, Tabor, A, et al. Randomised clinical trials of fish oil supplementation in high risk pregnancies. Fish Oil Trials In Pregnancy (FOTIP) Team. BJOG. 2000; 107, 382–395.Google Scholar
74. Barker, DJ, Eriksson, JG, Forsén, T, Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002; 31, 1235–1239.CrossRefGoogle ScholarPubMed
75. Torres-Espinola, FJ, Berglund, SK, García-Valdés, LM, et al. Maternal obesity, overweight and gestational diabetes affect the offspring neurodevelopment at 6 and 18 months of age – a follow up from the PREOBE Cohort. Plos One. 2015; 10, e0133010.CrossRefGoogle ScholarPubMed
76. Clandinin, MT, Chappell, JE, Leong, S, et al. Intrauterine fatty acid accretion rates in human brain: implications for fatty acid requirements. Early Hum Dev. 1980; 4, 121–129.Google Scholar
77. Ikemoto, A, Ohishi, M, Sato, Y, et al. Reversibility of n-3 fatty acid deficiency-induced alterations of learning behavior in the rat: level of n-6 fatty acids as another critical factor. J Lipid Res. 2001; 42, 1655–1663.Google Scholar
78. Bhatia, HS, Agrawal, R, Sharma, S, et al. Omega-3 fatty acid deficiency during brain maturation reduces neuronal and behavioral plasticity in adulthood. PLoS One. 2011; 6, e28451.Google Scholar
79. Umhau, JC, Zhou, W, Carson, RE, et al. Imaging incorporation of circulating docosahexaenoic acid into the human brain using positron emission tomography. J Lipid Res. 2009; 50, 1259–1268.Google Scholar
80. Willatts, P, Forsyth, JS, DiModugno, MK, Varma, S, Colvin, M. Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age. Lancet. 1998; 352, 688–691.CrossRefGoogle ScholarPubMed
81. Saccone, G, Saccone, I, Berghella, V. Omega-3 long-chain polyunsaturated fatty acids and fish oil supplementation during pregnancy: which evidence? J Matern Fetal Neonatal Med. 2016; 29, 2389–2397.Google Scholar
Supplementary material: File

Vollet supplementary material

Vollet supplementary material

Download Vollet supplementary material(File)
File 121.6 KB