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Effect of walnut consumption on neuropsychological development in healthy adolescents: a multi-school randomised controlled trial.

Institut d'Investigació Sanitària Pere Virgili (IISPV), Clinical and Epidemiological Neuroscience Group (NeuroÈpia), 43204 Reus (Tarragona), Catalonia, Spain. Universitat Pompeu Fabra (UPF), Barcelona, Catalonia, Spain. ISGlobal, Barcelona, Spain. Agència de Salut Pública de Barcelona, Pl. Lesseps 1, 08023, Barcelona, Spain. Instituto de Investigación Sanitaria Illes Balears (IdISBa), Hospital Universitari Son Espases, Palma de Mallorca, Spain. Consorcio CIBER, M.P. Fisiopatología de la Obesidad y Nutrición (CIBERObn), Instituto de Salud Carlos III (ISCIII), Madrid, Spain. The Fatty Acid Research Institute, Sioux Falls, SD, USA. Cardiovascular Risk and Nutrition, IMIM-Hospital del Mar Medical Research Institute, Barcelona, Catalonia, Spain. Centre de Recherche du Centre Hospitalier de l'Université de Montreal (CHUM), Montreal, QC, Canada. CIBER Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III (ISCIII), Madrid, Spain. University of Barcelona, Barcelona, Spain. Nutrition and Public Health Unit, Research Group on Nutrition and Mental Health (NUTRISAM), Faculty of Medicine and Health Science, Universitat Rovira I Virgili, 43201 Reus, Spain. Lipid Clinic, Endocrinology and Nutrition Service, Hospital Clínic, Biomedical Research Institute August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain. Institut d'Investigació Sanitària Pere Virgili (IISPV), Hospital Universitari Sant Joan de Reus, 43204 Reus, Catalonia, Spain. Universitat Rovira i Virgili, Departament de Bioquímica i Biotecnologia, Unitat de Nutrició Humana, Reus, Spain. Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, 02115, USA.

EClinicalMedicine. 2023;:101954
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Abstract

BACKGROUND Omega-3 fatty acids are critical for neuropsychological functioning. Adolescence is increasingly believed to entail brain vulnerability to dietary intake. The potential benefit on adolescent neurodevelopment of consuming walnuts, a source of omega-3 alpha-linolenic acid (ALA), remains unclear. METHODS We conducted a 6-month multi-school-based randomised controlled nutrition intervention trial to assess whether walnut consumption has beneficial effects on the neuropsychological and behavioural development of adolescents. The study took place between 04/01/2016 and 06/30/2017 in twelve different high schools in Barcelona, Spain (ClinicalTrials.gov Identifier: NCT02590848). A total of 771 healthy teenagers aged 11-16 years were randomised into two equal groups (intervention or control). The intervention group received 30 g/day of raw walnut kernels to be incorporated into their diet for 6 months. Multiple primary endpoints concerning neuropsychological (working memory, attention, fluid intelligence, and executive function) and behavioural (socio-emotional and attention deficit hyperactivity disorder [ADHD] symptoms) development were assessed at baseline and after intervention. Red blood cell (RBC) ALA status was determined at baseline and 6 months as a measure of compliance. Main analyses were based on intention-to-treat using a linear mixed-effects model. A per-protocol effect of the intervention was analysed using inverse-probability weighting to account for post-randomisation prognostic factors (including adherence) using generalised estimating equations. FINDINGS In intention-to-treat analyses, at 6 months there were no statistically significant changes between the intervention and control groups for all primary endpoints. RBC ALA (%) significantly increased only in the intervention group, coefficient = 0.04 (95% Confidence Interval (CI) = 0.03, 0.06; p < 0.0001). The per-protocol (adherence-adjusted) effect on improvement in attention score (hit reaction time variability) was -11.26 ms (95% CI = -19.92, -2.60; p = 0.011) for the intervention group as compared to the control group, improvement in fluid intelligence score was 1.78 (95% CI = 0.90, 2.67; p < 0.0001), and reduction of ADHD symptom score was -2.18 (95% CI = -3.70, -0.67; p = 0.0050). INTERPRETATION Our study suggested that being prescribed eating walnuts for 6 months did not improve the neuropsychological function of healthy adolescents. However, improved sustained attention, fluid intelligence, and ADHD symptoms were observed in participants who better complied with the walnut intervention. This study provides a foundation for further clinical and epidemiological research on the effect of walnuts and ALA on neurodevelopment in adolescents. FUNDING This study was supported by Instituto de Salud Carlos III through the projects 'CP14/00108, PI16/00261, PI21/00266' (co-funded by European Union Regional Development Fund 'A way to make Europe'). The California Walnut Commission (CWC) has given support by supplying the walnuts for free for the Walnuts Smart Snack Dietary Intervention Trial.