Maternal nut intake in pregnancy and child neuropsychological development up to 8 years old: a population-based cohort study in Spain

Abstract

There is scientific evidence on the protective effects of nut intake against cognitive decline in the elderly; however, this effect has been less explored in child neurodevelopment and no studies have explored the potential longitudinal association with nut intake during pregnancy. We aimed to analyze the association of maternal nut intake during pregnancy with child neuropsychological outcomes. We included 2208 mother–child pairs from a population-based birth cohort in four regions of Spain. The follow up settings were during pregnancy (first and third trimesters), birth, 1.5, 5 and 8 years. Neuropsychological examinations were based on Bayley Scales of Infant Development (1.5 years), McCarthy scales of Children’s Abilities (5 year), Attention Network Test (ANT, 8 year) and N-Back test (8 year). Nut intake in pregnancy was reported through a validated food frequency questionnaire during the first and the third trimester. Multivariable regressions analyzed associations after controlling for priori selected confounders notably maternal education, social class, body mass index, energy intake, fish intake, omega-3 supplements, alcohol consumption and smoking habits during pregnancy. Children within the highest tertile of maternal nut consumption during first pregnancy trimester (> 32 g/week) had a decrease of 13.82 ms [95% confidence interval (CI) − 23.40, − 4.23] in the ANT—hit reaction time standard error, compared to the first tertile (median 0 g/w). A similar protective association pattern was observed with the other cognitive scores at the different child ages. After correcting for multiple testing using Bonferroni familywise error rate (FWER), Hochberg FWER and Simes false discovery rate, ANT—hit reaction time standard error remained significant. Final model estimates by inverse probability weighting did not change results. Third pregnancy trimester nut intake showed weaker associations. These data indicate that nut intake during early pregnancy is associated with long-term child neuropsychological development. Future cohort studies and randomized clinical trials are needed to confirm this association pattern in order to further extend nutrition guidelines among pregnant women.

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Fig. 1

Abbreviations

ALA:

Alpha-linolenic acid

ANT:

Attention Network Test

BNDF:

Brain-derived neurotrophic factor

BMI:

Body mass index

BSID:

Bayley Scales of Infant Development

CI:

Confidence interval

DAG:

Directed Acyclic Graph

DALYs:

Disability adjusted life-years

DHA:

Docosahexaenoic acid

EPA:

Eicosapentaenoic acid

FDR:

False discovery rate

FFQ:

Food frequency questionnaire

FWER:

Familywise error rate

HRT-SE:

Hit reaction time standard error

IQ:

Intelligence quotient

INMA:

Infancia y Medio Ambiente (Environment and Childhood)

IQR:

Interquartile range

IPW:

Inverse probability weighting

MSCA:

McCarthy Scales of Children’s Abilities

PREDIMED:

Prevention with Mediterranean Diet

PUFAs:

Polyunsaturated fatty acids

rMED:

Relative Mediterranean diet score

SD:

Standard deviation

References

  1. 1.

    Gakidou E, Afshin A, Abajobir AA, et al. Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390(10100):1345–422.

    Article  Google Scholar 

  2. 2.

    Eslamparast T, Sharafkhah M, Poustchi H, et al. Nut consumption and total and cause-specific mortality: results from the Golestan Cohort Study. Int J Epidemiol. 2016;46(1):75–85.

    PubMed Central  Google Scholar 

  3. 3.

    Bao Y, Han J, Hu FB, et al. Association of nut consumption with total and cause-specific mortality. N Engl J Med. 2013;369(21):2001–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 4.

    Pribis P, Shukitt-Hale B. Cognition: the new frontier for nuts and berries. Am J Clin Nutr. 2014;100(SUPPL. 1):347–51.

    Article  CAS  Google Scholar 

  5. 5.

    Klimova B, Kuca K, Valis M, Hort J. Role of nut consumption in the management of cognitive decline—a mini-review. Curr Alzheimer Res. 2018;15(9):877–82.

    Article  CAS  PubMed  Google Scholar 

  6. 6.

    Valls-Pedret C, Sala-Vila A, Serra-Mir M, et al. Mediterranean diet and age-related cognitive decline. JAMA Intern Med. 2015;175(7):1–10.

    Article  Google Scholar 

  7. 7.

    Grosso G, Estruch R. Nut consumption and age-related disease. Maturitas. 2016;84:11–6.

    Article  CAS  PubMed  Google Scholar 

  8. 8.

    Cusick SE, Georgieff MK. The Role of nutrition in brain development: the golden opportunity of the “first 1000 days”. J Pediatr. 2016;175:16–21.

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Davidson PW, Cory-Slechta DA, Thurston SW, et al. Fish consumption and prenatal methylmercury exposure: cognitive and behavioral outcomes in the main cohort at 17 years from the Seychelles child development study. Neurotoxicology. 2011;32(6):711–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Forns J, Aranbarri A, Grellier J, Julvez J, Vrijheid M, Sunyer J. A conceptual framework in the study of neuropsychological development in epidemiological studies. Neuroepidemiology. 2012;38:203–8.

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Nyaradi A, Li J, Hickling S, Foster J, Oddy WH. The role of nutrition in children’s neurocognitive development, from pregnancy through childhood. Front Hum Neurosci. 2013;7(97):1–16.

    Google Scholar 

  12. 12.

    Anjos T, Altmae 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(8):1825–42.

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Guxens M, Ballester F, Espada M, et al. Cohort profile: the INMA—INfancia y Medio Ambiente—(Environment and Childhood) Project. Int J Epidemiol. 2012;41(4):930–40.

    Article  PubMed  Google Scholar 

  14. 14.

    Willett W, Sampson L, Stampfer M, Rosner B, Bain C. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol. 1985;122:51–65.

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Vioque J, Gimenez-monzó D, García-de-la-hera M, Iñiguez C, Study IC. Reproducibility and validity of a food frequency questionnaire among pregnant women in a Mediterranean area. Nutr J. 2013;12(26):1–9.

    Google Scholar 

  16. 16.

    US Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory. USDA National Nutrient Database for Standard Reference, Legacy. Version Current: April 2018. Internet:/nea/bhnrc/ndl.

  17. 17.

    Rodríguez-Bernal C, Rebagliato M, Iniguez C, et al. Diet quality in early pregnancy and its effects on fetal growth outcomes: the Infancia y Medio Ambiente (Childhood and Environment) Mother and Child Cohort Study in Spain. Am J Clin Nutr. 2010;91(6):1659–66.

    Article  CAS  PubMed  Google Scholar 

  18. 18.

    Palma I, Farran A, Cantós D. Tablas de Composición de Alimentos Por Medidas Caseras de Consumo Habitual En España. Spain: McGraw-Hill. Madrid; 2008.

    Google Scholar 

  19. 19.

    Koletzko B, Muller J. Cis- and trans-isometric fatty acids in plasma lipids of newborn infants and their mothers. Biol Neonates. 1990;57:172–8.

    Article  CAS  Google Scholar 

  20. 20.

    Willett WC, Howe GR, Kushi L. Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr. 1997;65(SUPPL.):1220S–8S.

    Article  CAS  PubMed  Google Scholar 

  21. 21.

    Hörnell A, Berg C, Forsum E, et al. Perspective: an extension of the STROBE statement for observational studies in nutritional epidemiology (STROBE-nut): explanation and elaboration. Adv Nutr. 2017;8(5):652–78.

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Textor J, Hardt J, Knüppel S. DAGitty: a graphical tool for analyzing causal diagrams. Epidemiology. 2011;5(22):745.

    Article  Google Scholar 

  23. 23.

    González de Rivera JL, Derogatis L, de las Cuevas C. The Spanish version of the SCL-90-R: normative data in general population. Baltimore: Towson; 1989.

    Google Scholar 

  24. 24.

    Weschler D, Kaufman A. WAIS-III. Escala de Inteligencia de Wechsler Para Adultos (III). Madrid: TEA Ediciones; 2001.

    Google Scholar 

  25. 25.

    Axelrod B. Validity of the Wechsler abbreviated scale of intelligence and other very short forms of estimating intellectual functioning. Assessment. 2002;9(1):17–23.

    Article  PubMed  Google Scholar 

  26. 26.

    Fernández-Barrés S, Romaguera D, Valvi D, et al. Mediterranean dietary pattern in pregnant women and offspring risk of overweight and abdominal obesity in early childhood: the INMA birth cohort study. Pediatr Obes. 2016;11(6):491–9.

    Article  PubMed  Google Scholar 

  27. 27.

    Spanish Ministry of Public Works. Atlas de La Vulnerabilidad Urbana En España 2001 Y 2011: Metodologia, Contenidos Y Créditos (Edicion de Diciembre de 2015); 2012.

  28. 28.

    Seaman SR, White IR. Review of inverse probability weighting for dealing with missing data. Stat Methods Med Res. 2011;22(3):278–95.

    Article  PubMed  Google Scholar 

  29. 29.

    Dapcich V, Salvador-Castell G, Ribas-Barba L, Pérez-Rodrigo C, Aranceta-Bartrina J, Serra-Majem L. Guía de la alimentación saludable. Spain: Sociedad Española de Nutrición Comunitaria; 2004.

    Google Scholar 

  30. 30.

    Jenab M, Sabaté J, Slimani N, et al. Consumption and portion sizes of tree nuts, peanuts and seeds in the European Prospective Investigation into Cancer and Nutrition (EPIC) cohorts from 10 European countries. Br J Nutr. 2008;99(2):447–8.

    Article  CAS  Google Scholar 

  31. 31.

    Nielsen SJ, Kit BK, Ogden CL. Nut consumption among U.S. adults, 2009–2010. NCHS data brief, no 176. Hyattsville, MD: National Center for Health Statistics. 2014.

  32. 32.

    Kim JY, Kang SW. Lifestyle relationships between dietary intake and cognitive function in healthy Korean children and adolescents. J Lifestyle Med. 2017;7(1):10–7.

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Vázquez-Marrufo M, Galvao-Carmona A, González-Rosa JJ, et al. Neural correlates of alerting and orienting impairment in multiple sclerosis patients. PLoS ONE. 2014;9(5):e97226.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Martínez-Lapiscina EH, Clavero P, Toledo E, et al. Mediterranean diet improves cognition: the PREDIMED-NAVARRA randomised trial. Cognit Neurol. 2013;84:1318–25.

    Google Scholar 

  35. 35.

    Nurk E, Refsum H, Drevon CA, et al. Cognitive performance among the elderly in relation to the intake of plant foods. The Hordaland Health Study. Br J Nutr. 2010;104:1190–201.

    Article  CAS  PubMed  Google Scholar 

  36. 36.

    Nooyens ACJ, Bueno-de-Mesquita HB, van Boxtel MPJ, van Gelder BM, Verhagen H, Verschuren WMM. Fruit and vegetable intake and cognitive decline in middle-aged men and women: the Doetinchem Cohort Study. Br J Nutr. 2011;106(5):752–61.

    Article  CAS  PubMed  Google Scholar 

  37. 37.

    Pribis P, Bailey RN, Russell AA, et al. Effects of walnut consumption on cognitive performance in young adults. Br J Nutr. 2012;107:1393–401.

    Article  CAS  PubMed  Google Scholar 

  38. 38.

    Aranceta J, Rodrigo C, Naska A, Vadillo V, Trichopoulou A. Nut consumption in Spain and other countries. Br J Nutr. 2006;96(Suppl. 2):S3–11.

    Article  CAS  PubMed  Google Scholar 

  39. 39.

    Greenberg JA, Bell SJ, Van Ausdal W. Omega-3 fatty acid supplementation during pregnancy. Rev Obstet Gynecol. 2008;1(4):162–9.

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Haider S, Batool Z, Tabassum S. Effects of Walnuts (Juglans regia) on learning and memory functions. Plants Foods Hum Nutr. 2011;66:335–40.

    Article  CAS  Google Scholar 

  41. 41.

    Blondeau N, Lipsky RH, Bourourou M, Duncan MW, Gorelick PB, Marini AM. Alpha-linolenic acid: an omega-3 fatty acid with neuroprotective properties—ready for use in the stroke clinic? Biomed Res Int. 2015;2015:1–8.

    Article  CAS  Google Scholar 

  42. 42.

    Haggarty P, Page K, Abramovich DR, et al. Long-chain polyunsaturated fatty acid transport across the perfused human placenta. Placenta. 1997;18:635–42.

    Article  CAS  PubMed  Google Scholar 

  43. 43.

    Martinez M. Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr. 1992;120(4):S129–38.

    Article  CAS  PubMed  Google Scholar 

  44. 44.

    Alasalvar C, Bolling B. Review of nut phytochemicals, fat-soluble bioactives, antioxidant components and health effects. Br J Nutr. 2015;113(S2):S68–78.

    Article  CAS  PubMed  Google Scholar 

  45. 45.

    Johansson L, Thelle D, Solvoll K, Bjørneboe G, Drevon C. Healthy dietary habits in relation to social determinants and lifestyle factors. Br J Nutr. 1999;81(3):211–20.

    Article  CAS  PubMed  Google Scholar 

  46. 46.

    Suades-González E, Forns J, García-Esteban R, López-Vicente M, Esnaola M, Álvarez-Pedrerol M, Julvez J, Cáceres A, Basagaña X, López-Sala A, Sunyer J. A longitudinal study on attention development in primary school children with and without teacher-reported symptoms of ADHD. Front Psychol. 2017;8:655.

    Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Freedman LS, Schatzkin A, Midthune D, Kipnis V. Dealing with dietary measurement error in nutritional cohort studies. J Natl Cancer Inst. 2011;103(14):1086–92.

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    O’Brien J, Okereke O, Devore E, Rosner B, Breteler M, Grodstein F. Long-term intake of nuts in relation to cognitive function in older women. J Nutr Health Aging. 2014;18(5):496–502.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Eslamparast T, Sharafkhah M, Poustchi H, et al. Nut consumption and total and cause-specific mortality: results from the Golestan Cohort Study. Int J Epidemiol. 2017;46(1):75–85.

    PubMed  Google Scholar 

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Acknowledgements

We would like to thank all the participants of the INMA Project for their collaboration as well as the project investigators at each cohort center as well as the coordination centers. A full roster of the INMA Project investigator can be found at http://www.PROYECTOINMA.org/. We would like to thank also Nuria Sebastian-Galles and her team who have designed the N-Back and ANT tests.

Funding

This study was funded by Grants from Spanish Institute of Health Carlos III-Ministry of Economy and Competitiveness (INMA Network G03/176, CB06/02/0041, and FIS-FEDER: PI03/1615, PI04/1436, PI08/1151, PI04/2018, PI04/1509, PI04/1112, PI04/1931, PI05/1079, PI05/1052, PI06/1213, PI06/0867, PI07/0314, PI09/02647, PS09/00090, PI09/02311, MS11/0178, PI13/1944, PI13/2032, PI13/02429, PI16/1288, and PI17/00663), Generalitat de Catalunya-CIRIT 1999SGR 00241, JCI-2011–09771–MICINN, Generalitat Valenciana (Conselleria de Sanitat-048/2010 and 060/2010 and FISABIO-UGP 15-230, 15-244, and 15-249), Alicia Koplowitz Foundation, Universidad de Oviedo, Fundación Cajastur-Liberbank, Department of Health of the Basque Government (2005111093 and 2009111069), the Provincial Government of Gipuzkoa (DFG06/004 and DFG08/001), and the Fundación Roger Torné. This study has been funded by Instituto de Salud Carlos III through the projects “CP14/00108 & PI16/00261” (Co-funded by European Regional Development Fund “A way to make Europe”). Jordi Julvez, Mònica Guxens and Maria-Jose Lopez-Espinosa hold a Miguel Servet contract (MS14/00108, MS13/00054 and MSII16/00051, respectively) awarded by the Spanish Institute of Health Carlos III (Ministry of Economy and Competitiveness). Funding sources played no role in the design and conduct of the study, including: collection, management, analysis and interpretation of the data; or the preparation, review, and approval of the manuscript. The authors would also like to acknowledge all the study participants for their generous collaboration, and the interviewers for their assistance in contacting the families and administering the questionnaires.

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DR, JS and JJ designed research. FG analyzed data, wrote the paper and is responsible for final content. CP, JJ, DR, SFB, RGE supported and revised the statistical analyses. JJ coordinated and supervised data collection. JJ and DR supervised the interpretation of the results. All authors critically reviewed the manuscript and approved the final version of the manuscript.

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Correspondence to Jordi Julvez.

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Gignac, F., Romaguera, D., Fernández-Barrés, S. et al. Maternal nut intake in pregnancy and child neuropsychological development up to 8 years old: a population-based cohort study in Spain. Eur J Epidemiol 34, 661–673 (2019). https://doi.org/10.1007/s10654-019-00521-6

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Keywords

  • Nut
  • Maternal diet
  • Children
  • Neurodevelopment
  • Population-based cohort