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

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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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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

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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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Authors and Affiliations

  1. ISGlobal- Instituto de Salud Global de Barcelona-Campus MAR, PRBB, C. Doctor Aiguader 88, 08003, Barcelona, Spain

    Florence Gignac, Dora Romaguera, Silvia Fernández-Barrés, Raquel Garcia Esteban, Mónica López-Vicente, Mònica Guxens, Jordi Sunyer & Jordi Julvez

  2. Universitat Pompeu Fabra (UPF), Barcelona, Spain

    Florence Gignac, Dora Romaguera, Silvia Fernández-Barrés, Raquel Garcia Esteban, Mónica López-Vicente, Mònica Guxens, Jordi Sunyer & Jordi Julvez

  3. CIBER Epidemiologia y Salud Pública (CIBERESP), Madrid, Spain

    Florence Gignac, Dora Romaguera, Silvia Fernández-Barrés, Raquel Garcia Esteban, Mónica López-Vicente, Jesus Vioque, Ana Fernández-Somoano, Carmen Iñiguez, Maria-Jose Lopez-Espinosa, Manoli García de la Hera, Pilar Amiano, Jesús Ibarluzea, Mònica Guxens, Jordi Sunyer & Jordi Julvez

  4. Instituto de Investigación Sanitaria Illes Balears (IdISBa), Hospital Universitari Son Espases, Palma de Mallorca, Spain

    Dora Romaguera

  5. CIBER Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Santiago de Compostela, Spain

    Adonina Tardón & Mònica Guxens

  6. Institute for Advanced Biosciences, INSERM U1209, CNRS UMR 5309, University Grenoble Alpes, Grenoble, France

    Dora Romaguera & Claire Phillipat

  7. Nutritional Epidemiology Unit, Universidad Miguel Hernández, ISABIAL–FISABIO, Alicante, Spain

    Jesus Vioque & Manoli García de la Hera

  8. Medecine Department, University of Oviedo, Oviedo, Spain

    Ana Fernández-Somoano & Adonina Tardón

  9. Epidemiology and Environmental Health Joint Research Unit, FISABIO–Universitat Jaume I–Universitat de València, Valencia, Spain

    Carmen Iñiguez & Maria-Jose Lopez-Espinosa

  10. Department of Statistics and Computational Research, Universistat de València, Valencia, Spain

    Carmen Iñiguez

  11. Public Health Division of Gipuzkoa, Department of Health, San Sebastian, Basque Country, Spain

    Pilar Amiano & Jesús Ibarluzea

  12. BioDonostia Research Institute, San Sebastian, Basque Country, Spain

    Pilar Amiano & Jesús Ibarluzea

  13. School of Psychology, University of the Basque Country UPV/EHU, San Sebastian, Basque Country, Spain

    Jesús Ibarluzea

  14. Department of Child and Adolescent Psychiatry/Psychology, Erasmus University Medical Centre-Sophia Children’s Hospital, PO Box 2060, 3000 CB, Rotterdam, The Netherlands

    Mònica Guxens

Authors
  1. Florence Gignac
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  2. Dora Romaguera
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  3. Silvia Fernández-Barrés
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  4. Claire Phillipat
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  5. Raquel Garcia Esteban
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  6. Mónica López-Vicente
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  7. Jesus Vioque
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  8. Ana Fernández-Somoano
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  9. Adonina Tardón
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  11. Maria-Jose Lopez-Espinosa
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  12. Manoli García de la Hera
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  14. Jesús Ibarluzea
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  15. Mònica Guxens
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  16. Jordi Sunyer
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  17. Jordi Julvez
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Contributions

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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