The effects of fatty fish intake on adolescents' nutritional status and associations with attention performance: results from the FINS-TEENS randomized controlled trial

Katina Handeland, Siv Skotheim, Valborg Baste, Ingvild E Graff, Livar Frøyland, Øyvind Lie, Marian Kjellevold, Maria W Markhus, Kjell M Stormark, Jannike Øyen, Lisbeth Dahl, Katina Handeland, Siv Skotheim, Valborg Baste, Ingvild E Graff, Livar Frøyland, Øyvind Lie, Marian Kjellevold, Maria W Markhus, Kjell M Stormark, Jannike Øyen, Lisbeth Dahl

Abstract

Background: Adolescence involves changes in dietary habits that may induce imbalances in the intake of different nutrients. Fish is an important dietary source of omega-3 (n-3) long-chain polyunsaturated fatty acids (LCPUFAs), vitamin D, several minerals and high-quality protein. By using secondary outcomes and exploratory analyses, the aims of this paper were to evaluate if nutritional biomarkers (red blood cell fatty acids, serum (s)-25(OH)D, s-ferritin and urinary iodine concentration (UIC)) were altered during a dietary intervention, and if they mediated previously reported changes in attention performance. In addition, to examine the status of the biomarkers and explore associations between dietary pattern, biomarkers and attention performance cross-sectionally at baseline.

Methods: The Fish Intervention Studies-TEENS (FINS-TEENS) was a three-armed intervention trial, including adolescents from eight secondary schools (n = 415; age: 14-15y) in Bergen, Norway. Participants were individually randomized to receive either fish meals, meat meals or n-3 LCPUFA supplements, three times a week for a total of 12 weeks. Blood and urine samples were collected pre and post intervention and attention performance was assessed with the d2 test of attention. Analyses of covariance (ANCOVA) assessed differences between groups in changes of biomarkers and linear mixed models were applied in analyses of attention performance and biomarkers. The trial is registered in ClinicalTrials.gov (NCT02350322).

Results: At baseline, the mean omega-3 index was 5.8 ± 1.3% and deficient status were identified for s-25(OH)D (54%), s-ferritin (10%) and UIC (40%). The intervention resulted in an increase in DHA and the omega-3 index which was larger in the supplement group compared to the fish and meat group (P < 0.01), and in the fish group compared to the meat group (P < 0.01). No differences between the groups were observed for changes in 25(OH)D, s-ferritin or UIC. None of the biomarkers mediated performance in the d2 test. The intake of fatty fish and a healthy dietary pattern was associated with scores in processing speed at baseline.

Conclusions: These results show that Norwegian adolescents have insufficient status of important nutrients, which may be improved with fatty fish consumption or n-3 LCPUFA supplements. However, nutritional status was not associated with scores in the d2 test of attention.

Keywords: Dietary intervention; Fatty fish; Healthy adolescents; Iodine; Iron; N-3 LCPUFA; Vitamin D.

Conflict of interest statement

Ethics approval and consent to participate

Norwegian Data Protection Official for Research project number: 41,030.

Written informed consent to participate in the trial was collected from all participants and one legal parent/caregiver before study start.

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Flow chart over participants. n-3 = omega-3

References

    1. EFSA: Scientific Opinion on health benefits of seafood (fish and shellfish) consumption in relation to health risks associated with exposure to methylmercury. 2014. []. Accessed 24 Jan 2018.
    1. Dahl L, Bjorkkjaer T, Graff IE, Malde MK, Klementsen B. Fish-more than just omega 3. Tidsskr Nor Laegeforen. 2006;126:309–311.
    1. Moreno LA, Gottrand F, Huybrechts I, Ruiz JR, González-Gross M, DeHenauw S. Nutrition and lifestyle in european adolescents: the HELENA (healthy lifestyle in Europe by nutrition in adolescence) study. Adv Nutr. 2014;5:615S–623S. doi: 10.3945/an.113.005678.
    1. González-Gross M, Valtueña J, Breidenassel C, Moreno LA, Ferrari M, Kersting M, De Henauw S, Gottrand F, Azzini E, Widhalm K, et al. Vitamin D status among adolescents in Europe: the healthy lifestyle in Europe by nutrition in adolescence study. Br J Nutr. 2012;107:755–764. doi: 10.1017/S0007114511003527.
    1. Braegger C, Campoy C, Colomb V, Decsi T, Domellof M, Fewtrell M, Hojsak I, Mihatsch W, Molgaard C, Shamir R, et al. Vitamin D in the healthy European paediatric population. J Pediatr Gastroenterol Nutr. 2013;56:692–701. doi: 10.1097/MPG.0b013e31828f3c05.
    1. Harris WS, Von Schacky C. The Omega-3 index: a new risk factor for death from coronary heart disease? Prev Med. 2004;39:212–220. doi: 10.1016/j.ypmed.2004.02.030.
    1. Harris WS. The omega-3 index as a risk factor for coronary heart disease. Am J Clin Nutr. 2008;87:1997S–2002S. doi: 10.1093/ajcn/87.6.1997S.
    1. O’Sullivan TA, Ambrosini GL, Mori TA, Beilin LJ, Oddy WH. Omega-3 index correlates with healthier food consumption in adolescents and with reduced cardiovascular disease risk factors in adolescent boys. Lipids. 2011;46:59–67. doi: 10.1007/s11745-010-3499-8.
    1. EFSA: Scientific Opinion on Dietary Reference Values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. 2010. []. Accessed 11 Apr 2017.
    1. Hansen LB, Myhre JB, Johansen AMW, Paulsen MM, Andersen LF: UNGKOST 3 Landsomfattende kostholdsundersøkelse blant elever i 4. -og 8. klasse i Norge, 2015 [UNGKOST 3 Nationwide dietary survey among pupils in 4th -and 8th grade in Norway, 2015]. 2016. []. Accessed 16 Dec 2016.
    1. Casey B, Jones RM, Hare TA. The adolescent brain. Ann N Y Acad Sci. 2008;1124:111–126. doi: 10.1196/annals.1440.010.
    1. Isaacs E, Oates J. Nutrition and cognition: assessing cognitive abilities in children and young people. Eur J Nutr. 2008;47:4–24. doi: 10.1007/s00394-008-3002-y.
    1. Jl K, Winkvist A, Åberg MA, Åberg N, Sundberg R, Torén K, Brisman J. Fish consumption and school grades in Swedish adolescents: a study of the large general population. Acta Paediatr. 2010;99:72–77.
    1. Åberg MA, Åberg N, Brisman J, Sundberg R, Winkvist A, Torén K. Fish intake of Swedish male adolescents is a predictor of cognitive performance. Acta Paediatr. 2009;98:555–560. doi: 10.1111/j.1651-2227.2008.01103.x.
    1. de Groot RHM, Ouwehand C, Jolles J. Eating the right amount of fish: inverted U-shape association between fish consumption and cognitive performance and academic achievement in Dutch adolescents. Prostaglandins Leukot Essent Fatty Acids. 2012;86:113–117. doi: 10.1016/j.plefa.2012.01.002.
    1. Handeland K, Oyen J, Skotheim S, Graff IE, Baste V, Kjellevold M, Froyland L, Lie O, Dahl L, Stormark KM. Fatty fish intake and attention performance in 14-15 year old adolescents: FINS-TEENS - a randomized controlled trial. Nutr J. 2017;16:64. doi: 10.1186/s12937-017-0287-9.
    1. Skotheim S, Dahl L, Handeland K, Frøyland L, Lie Ø, Øyen J, Kjellevold M, Stormark KM, Graff IE. Design of the FINS-TEENS study: a randomized controlled trial assessing the impact of fatty fish on cognitive performance in adolescents. Scand J Public Health. 2017;45:621–629. doi: 10.1177/1403494817717408.
    1. Norges forskningsråd [Norwegian Research Council]: Hva spiser elevene på skolen? [What do students eat at school?]. 2011. []. Accessed 23 Mar 2017.
    1. Markhus MW, Graff IE, Dahl L, Seldal CF, Skotheim S, Braarud HC, Stormark KM, Malde MK. Establishment of a seafood index to assess the seafood consumption in pregnant women. Food Nutr Res. 2013;57
    1. Dahl L, Maeland CA, Bjorkkjaer T. A short food frequency questionnaire to assess intake of seafood and n-3 supplements: validation with biomarkers. Nutr J. 2011;10:127. doi: 10.1186/1475-2891-10-127.
    1. Handeland K, Kjellevold M, Wik Markhus M, Eide Graff I, Frøyland L, Lie Ø, Skotheim S, Stormark KM, Dahl L, Øyen J. A diet score assessing Norwegian Adolescents' adherence to dietary recommendations-development and test-retest reproducibility of the score. Nutrients. 2016;8
    1. Kissmeyer A-M, Sonne K, Binderup E. Determination of the vitamin D analog EB 1089 (seocalcitol) in human and pig serum using liquid chromatography–tandem mass spectrometry. J Chromatogr B Biomed Sci Appl. 2000;740:117–128. doi: 10.1016/S0378-4347(00)00091-8.
    1. Dahl L, Meltzer HM, Opsahl JA, Julshamn K. Iodine intake and status in two groups of Norwegians. Food Nutr Res. 2003;47
    1. Brickenkamp R, Zillmer E. d2 test of attention manual. Göttingen: Hogrefe & Huber Publishers; 2003.
    1. Skotheim S, Handeland K, Kjellevold M, Oyen J, Froyland L, Lie O, Eide Graff I, Baste V, Stormark KM, Dahl L. The effect of school meals with fatty fish on adolescents' self-reported symptoms for mental health: FINS-TEENS - a randomized controlled intervention trial. Food Nutr Res. 2017;61:1383818. doi: 10.1080/16546628.2017.1383818.
    1. Bates ME, Lemay EP. The d2 test of attention: construct validity and extensions in scoring techniques. J Inter Neuropsych Soc. 2004;10:392–400. doi: 10.1017/S135561770410307X.
    1. Baron RM, Kenny DA. The moderator-mediator distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986;51:1173–1182. doi: 10.1037/0022-3514.51.6.1173.
    1. WHO: Urinary iodine concentrations for determining iodine status deficiency in populations. 2013. []. Accessed 14 Mar 2017.
    1. WHO: Serum ferritin concentrations for the assessment of iron status and iron deficiency in populations. 2011. []. Accessed 31 Mar 2017.
    1. Stonehouse W, Pauga MR, Kruger R, Thomson CD, Wong M, Kruger MC. Consumption of salmon v. Salmon oil capsules: effects on n −3 PUFA and selenium status. Br J Nutr. 2011;106:1231–1239. doi: 10.1017/S000711451100153X.
    1. Christensen MH, Lien EA, Hustad S, Almas B. Seasonal and age-related differences in serum 25-hydroxyvitamin D, 1,25-dihydroxyvitamin D and parathyroid hormone in patients from western Norway. Scand J Clin Lab Invest. 2010;70:281–286. doi: 10.3109/00365511003797172.
    1. Lehmann U, Gjessing HR, Hirche F, Mueller-Belecke A, Gudbrandsen OA, Ueland PM, Mellgren G, Lauritzen L, Lindqvist H, Hansen AL, et al. Efficacy of fish intake on vitamin D status: a meta-analysis of randomized controlled trials. Am J Clin Nutr. 2015;102:837. doi: 10.3945/ajcn.114.105395.
    1. Gunnarsdottir I, Gunnarsdottir BE, Steingrimsdottir L, Maage A, Johannesson AJ, Thorsdottir I. Iodine status of adolescent girls in a population changing from high to lower fish consumption. Eur J Clin Nutr. 2010;64:958–964. doi: 10.1038/ejcn.2010.100.
    1. NIFES: Seafood data. []. Accessed 29 June 2017.
    1. Sørensen LB, Damsgaard CT, Dalskov SM, Petersen RA, Egelund N, Dyssegaard CB, Stark KD, Andersen R, Tetens I, Astrup A. Diet-induced changes in iron and n-3 fatty acid status and associations with cognitive performance in 8–11-year-old Danish children: secondary analyses of the optimal well-being, development and health for Danish children through a healthy new Nordic diet school meal study. Br J Nutr. 2015;114:1623–1637. doi: 10.1017/S0007114515003323.
    1. van der Wurff IS, von Schacky C, Berge K, Zeegers MP, Kirschner PA, de Groot RH. Association between blood Omega-3 index and cognition in typically developing Dutch adolescents. Nutrients. 2016;8. 10.3390/nu8010013
    1. Cohen JFW, Gorski MT, Gruber SA, Kurdziel LBF, Rimm EB. The effect of healthy dietary consumption on executive cognitive functioning in children and adolescents: a systematic review. Br J Nutr. 2016;116:989–1000. doi: 10.1017/S0007114516002877.
    1. Haapala EA, Eloranta AM, Venäläinen T, Schwab U, Lindi V, Lakka TA. Associations of diet quality with cognition in children–the physical activity and nutrition in children study. Br J Nutr. 2015;114:1080–1087. doi: 10.1017/S0007114515001634.
    1. Khan NA, Raine LB, Drollette ES, Scudder MR, Kramer AF, Hillman CH. Dietary fiber is positively associated with cognitive control among prepubertal children. J Nutr. 2015;145:143–149. doi: 10.3945/jn.114.198457.
    1. Nyaradi A, Foster JK, Hickling S, Li J, Ambrosini GL, Jacques A, Oddy WH. Prospective associations between dietary patterns and cognitive performance during adolescence. J Child Psychol Psychiatry. 2014;55:1017–1024. doi: 10.1111/jcpp.12209.
    1. Kirby A, Woodward A, Jackson S, Wang Y, Crawford MA. A double-blind, placebo-controlled study investigating the effects of omega-3 supplementation in children aged 8-10 years from a mainstream school population. Res Dev Disabil. 2010;31:718–730. doi: 10.1016/j.ridd.2010.01.014.
    1. Stonehouse W, Conlon CA, Podd J, Hill SR, Minihane AM, Haskell C, Kennedy D. DHA supplementation improved both memory and reaction time in healthy young adults: a randomized controlled trial. Am J Clin Nutr. 2013;97:1134–1143. doi: 10.3945/ajcn.112.053371.
    1. Kennedy DO, Jackson PA, Elliott JM, Scholey AB, Robertson BC, Greer J, Tiplady B, Buchanan T, Haskell CF. Cognitive and mood effects of 8 weeks' supplementation with 400 mg or 1000 mg of the omega-3 essential fatty acid docosahexaenoic acid (DHA) in healthy children aged 10-12 years. Nutr Neurosci. 2009;12:48–56. doi: 10.1179/147683009X388887.
    1. McNamara RK, Able J, Jandacek R, Rider T, Tso P, Eliassen JC, Alfieri D, Weber W, Jarvis K, DelBello MP. Docosahexaenoic acid supplementation increases prefrontal cortex activation during sustained attention in healthy boys: a placebo-controlled, dose-ranging, functional magnetic resonance imaging study. Am J Clin Nutr. 2010;91:1060–1067. doi: 10.3945/ajcn.2009.28549.
    1. Harris WS, Thomas RM. Biological variability of blood omega-3 biomarkers. Clin Biochem. 2010;43:338–340. doi: 10.1016/j.clinbiochem.2009.08.016.
    1. Harris WS, Varvel SA, Pottala JV, Warnick GR, McConnell JP. Comparative effects of an acute dose of fish oil on omega-3 fatty acid levels in red blood cells versus plasma: implications for clinical utility. J Clin Lipidol. 2013;7:433–440. doi: 10.1016/j.jacl.2013.05.001.
    1. Stepman HCM, Vanderroost A, Van Uytfanghe K, Thienpont LM. Candidate reference measurement procedures for serum 25-Hydroxyvitamin D3 and 25-Hydroxyvitamin D2 by using isotope-dilution liquid chromatography–tandem mass spectrometry. Clin Chem. 2011;57:441–448. doi: 10.1373/clinchem.2010.152553.
    1. Julshamn K, Dahl L, Eckhoff K. Determination of iodine in seafood by inductively coupled plasma/mass spectrometry. J AOAC Int. 2001;84:1976–1983.
    1. Katan MB, Deslypere JP, van Birgelen AP, Penders M, Zegwaard M. Kinetics of the incorporation of dietary fatty acids into serum cholesteryl esters, erythrocyte membranes, and adipose tissue: an 18-month controlled study. J Lipid Res. 1997;38:2012–2022.
    1. Cao J, Schwichtenberg KA, Hanson NQ, Tsai MY. Incorporation and clearance of omega-3 fatty acids in erythrocyte membranes and plasma phospholipids.(Lipis, Lipoproteins and Cardiovascular Risk Factors) Clin Chem. 2006;52:2265. doi: 10.1373/clinchem.2006.072322.

Source: PubMed

3
Prenumerera