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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

  • Florence Gignac
  • Dora Romaguera
  • Silvia Fernández-Barrés
  • Claire Phillipat
  • Raquel Garcia Esteban
  • Mónica López-Vicente
  • Jesus Vioque
  • Ana Fernández-Somoano
  • Adonina Tardón
  • Carmen Iñiguez
  • Maria-Jose Lopez-Espinosa
  • Manoli García de la Hera
  • Pilar Amiano
  • Jesús Ibarluzea
  • Mònica Guxens
  • Jordi Sunyer
  • Jordi JulvezEmail author
DEVELOPMENTAL EPIDEMIOLOGY

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.

Keywords

Nut Maternal diet Children Neurodevelopment Population-based cohort 

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

Notes

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.

Authors’ 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.

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.

Compliance with ethical standards

Conflict of interest

The authors have indicated they have no potential conflicts of interest to disclose.

Supplementary material

10654_2019_521_MOESM1_ESM.docx (387 kb)
Supplementary material 1 (DOCX 377 kb)

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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Florence Gignac
    • 1
    • 2
    • 3
  • Dora Romaguera
    • 1
    • 2
    • 3
    • 4
    • 6
  • Silvia Fernández-Barrés
    • 1
    • 2
    • 3
  • Claire Phillipat
    • 6
  • Raquel Garcia Esteban
    • 1
    • 2
    • 3
  • Mónica López-Vicente
    • 1
    • 2
    • 3
  • Jesus Vioque
    • 3
    • 7
  • Ana Fernández-Somoano
    • 3
    • 8
  • Adonina Tardón
    • 5
    • 8
  • Carmen Iñiguez
    • 3
    • 9
    • 10
  • Maria-Jose Lopez-Espinosa
    • 3
    • 9
  • Manoli García de la Hera
    • 3
    • 7
  • Pilar Amiano
    • 3
    • 11
    • 12
  • Jesús Ibarluzea
    • 3
    • 11
    • 12
    • 13
  • Mònica Guxens
    • 1
    • 2
    • 3
    • 5
    • 14
  • Jordi Sunyer
    • 1
    • 2
    • 3
  • Jordi Julvez
    • 1
    • 2
    • 3
    Email author
  1. 1.ISGlobal- Instituto de Salud Global de Barcelona-Campus MAR, PRBBBarcelonaSpain
  2. 2.Universitat Pompeu Fabra (UPF)BarcelonaSpain
  3. 3.CIBER Epidemiologia y Salud Pública (CIBERESP)MadridSpain
  4. 4.Instituto de Investigación Sanitaria Illes Balears (IdISBa), Hospital Universitari Son EspasesPalma de MallorcaSpain
  5. 5.CIBER Fisiopatología de la Obesidad y Nutrición (CIBEROBN)Santiago de CompostelaSpain
  6. 6.Institute for Advanced Biosciences, INSERM U1209, CNRS UMR 5309University Grenoble AlpesGrenobleFrance
  7. 7.Nutritional Epidemiology UnitUniversidad Miguel Hernández, ISABIAL–FISABIOAlicanteSpain
  8. 8.Medecine DepartmentUniversity of OviedoOviedoSpain
  9. 9.Epidemiology and Environmental Health Joint Research UnitFISABIO–Universitat Jaume I–Universitat de ValènciaValenciaSpain
  10. 10.Department of Statistics and Computational ResearchUniversistat de ValènciaValenciaSpain
  11. 11.Public Health Division of GipuzkoaDepartment of HealthSan SebastianSpain
  12. 12.BioDonostia Research InstituteSan SebastianSpain
  13. 13.School of PsychologyUniversity of the Basque Country UPV/EHUSan SebastianSpain
  14. 14.Department of Child and Adolescent Psychiatry/PsychologyErasmus University Medical Centre-Sophia Children’s HospitalRotterdamThe Netherlands

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