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Foods contributing to vitamin B6, folate, and vitamin B12 intakes and biomarkers status in European adolescents: The HELENA study

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Abstract

Purpose

To examine the association between food groups consumption and vitamin B6, folate and B12 intakes and biomarkers in adolescents.

Methods

In total 2189 individuals participating in the cross-sectional Healthy Lifestyle in Europe by Nutrition in Adolescence study met the eligibility criteria for analysis of dietary intakes (46 % males) and 632 for biomarker analysis (47 % males). Food intakes were assessed by two non-consecutive 24-h recalls. Biomarkers were measured by chromatography and immunoassay. Food groups which best discriminated participants in the extreme tertiles of the distribution of vitamins were identified by discriminant analyses. Food groups with standardised canonical coefficients higher or equal to 0.3 were selected as valid discriminators of vitamins intake and biomarkers extreme tertiles. Linear mixed model elucidated the association between food groups and vitamins intakes and biomarkers.

Results

Vitamin B6 intakes and biomarkers were best discriminated by meat (males and females), margarine and mixed origin lipids only in males and breakfast cereals (females). Breakfast cereals (males), and fruits, margarine and mixed origin lipids, vegetables excluding potatoes, breakfast cereals, and soups/bouillon (females) determined the most folate intakes and biomarkers. Considering vitamin B12 intakes and biomarkers, meat, and white and butter milk (males and females), snacks (males), and dairy products (females) best discriminated individual in the extremes of the distribution. Fewer associations were obtained with mixed model for biomarkers than for vitamins intakes with food groups.

Conclusions

Whereas B-vitamin intakes were associated with their food sources, biomarkers did with overall food consumption. Low-nutrient-density foods may compromise adolescents’ vitamin status.

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Abbreviations

HELENA:

Healthy Lifestyle in Europe by Nutrition in Adolescence

Cbl:

Cobalamin

MSM:

Multiple-source method

PLP:

Pyridoxal 5′-phosphate

EDTA:

Ethylenediaminetetraacetic acid

HPLC:

High-performance liquid chromatography

CV:

Coefficient of variation

RBC-folate:

Red blood cell folate

HoloTC:

Holotranscobalamin

SD:

Standard deviations

BMI:

Body mass index

FCDB:

Food composition databases

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Acknowledgments

HELENA study received funding from the European Union’s Sixth RTD Framework Programme (Contract FOODCT-2005-007034). Additional support from the Spanish Ministry of Education (AGL2007-29784-E/ALI), Axis-Shield Diagnostics Ltd (Oslo, Norway), Abbot Científica S.A. (Spain). The first author was financially supported by EURRECA-Network of Excellence-. This analysis was also supported by the Spanish Ministry of Science and Innovation (JCI-2010-07055) with the contribution of the European Regional Development Fund (FEDER). The authors would like to acknowledge all the adolescents who made possible the HELENA study with their participation. Many thanks to Petra Pickert, Rosa Torres and Ulrike Albers for their contribution to laboratory work.

HELENA Study Group

Co-ordinator

Luis A. Moreno.

Core Group members

Luis A. Moreno, Fréderic Gottrand, Stefaan De Henauw, Marcela González-Gross, Chantal Gilbert.

Steering Committee

Anthony Kafatos (President), Luis A. Moreno, Christian Libersa, Stefaan De Henauw, Sara Castelló, Fréderic Gottrand, Mathilde Kersting, Michael Sjöstrom, Dénes Molnár, Marcela González-Gross, Jean Dallongeville, Chantal Gilbert, Gunnar Hall, Lea Maes, Luca Scalfi.

Project Manager

Pilar Meléndez.

Universidad de Zaragoza (Spain)

Luis A. Moreno, Jesús Fleta, José A. Casajús, Gerardo Rodríguez, Concepción Tomás, María I. Mesana, Germán Vicente-Rodríguez, Adoración Villarroya, Carlos M. Gil, Ignacio Ara, Juan Fernández Alvira, Gloria Bueno, Aurora Lázaro, Olga Bueno, Juan F. León, Jesús Mª Garagorri, Manuel Bueno, Idoia Labayen, Iris Iglesia, Silvia Bel, Luis A. Gracia Marco, Theodora Mouratidou, Alba Santaliestra-Pasías, Iris Iglesia, Esther González-Gil, Pilar De Miguel-Etayo, Cristina Julián Almárcegui, Mary Miguel-Berges, Isabel Iguacel.

Consejo Superior de Investigaciones Científicas (Spain)

Ascensión Marcos, Julia Wärnberg, Esther Nova, Sonia Gómez, Ligia Esperanza Díaz, Javier Romeo, Ana Veses, Belén Zapatera, Tamara Pozo, David Martínez.

Université de Lille 2 (France)

Laurent Beghin, Christian Libersa, Frédéric Gottrand, Catalina Iliescu, Juliana Von Berlepsch.

Research Institute of Child Nutrition Dortmund, Rheinische Friedrich-Wilhelms-Universität Bonn (Germany)

Mathilde Kersting, Wolfgang Sichert-Hellert, Ellen Koeppen.

Pécsi Tudományegyetem (University of Pécs) (Hungary)

Dénes Molnar, Eva Erhardt, Katalin Csernus, Katalin Török, Szilvia Bokor, Mrs. Angster, Enikö Nagy, Orsolya Kovács, Judit Répasi.

University of Crete School of Medicine (Greece)

Anthony Kafatos, Caroline Codrington, María Plada, Angeliki Papadaki, Katerina Sarri, Anna Viskadourou, Christos Hatzis, Michael Kiriakakis, George Tsibinos, Constantine Vardavas, Manolis Sbokos, Eva Protoyeraki, Maria Fasoulaki.

Institut für Ernährungs- und Lebensmittelwissenschaften – Ernährungphysiologie. Rheinische Friedrich Wilhelms Universität (Germany)

Peter Stehle, Klaus Pietrzik, Marcela González-Gross, Christina Breidenassel, Andre Spinneker, Jasmin Al-Tahan, Miriam Segoviano, Anke Berchtold, Christine Bierschbach, Erika Blatzheim, Adelheid Schuch, Petra Pickert.

University of Granada (Spain)

Manuel J. Castillo, Ángel Gutiérrez, Francisco B Ortega, Jonatan R Ruiz, Enrique G Artero, Vanesa España, David Jiménez-Pavón, Palma Chillón, Cristóbal Sánchez-Muñoz, Magdalena Cuenca.

Istituto Nazionalen di Ricerca per gli Alimenti e la Nutrizione (Italy)

Davide Arcella, Elena Azzini, Emma Barrison, Noemi Bevilacqua, Pasquale Buonocore, Giovina Catasta, Laura Censi, Donatella Ciarapica, Paola D’Acapito, Marika Ferrari, Myriam Galfo, Cinzia Le Donne, Catherine Leclercq, Giuseppe Maiani, Beatrice Mauro, Lorenza Mistura, Antonella Pasquali, Raffaela Piccinelli, Angela Polito, Romana Roccaldo, Raffaella Spada, Stefania Sette, Maria Zaccaria.

University of Napoli “Federico II” Dept of Food Science (Italy)

Luca Scalfi, Paola Vitaglione, Concetta Montagnese.

Ghent University (Belgium)

Ilse De Bourdeaudhuij, Stefaan De Henauw, Tineke De Vriendt, Lea Maes, Christophe Matthys, Carine Vereecken, Mieke de Maeyer, Charlene Ottevaere, Inge Huybrechts.

Medical University of Vienna (Austria)

Kurt Widhalm, Katharina Phillipp, Sabine Dietrich, Birgit Kubelka, Marion Boriss-Riedl.

Harokopio University (Greece)

Yannis Manios, Eva Grammatikaki, Zoi Bouloubasi, Tina Louisa Cook, Sofia Eleutheriou, Orsalia Consta, George Moschonis, Ioanna Katsaroli, George Kraniou, Stalo Papoutsou, Despoina Keke, Ioanna Petraki, Elena Bellou, Sofia Tanagra, Kostalenia Kallianoti, Dionysia Argyropoulou, Stamatoula Tsikrika, Christos Karaiskos.

Institut Pasteur de Lille (France)

Jean Dallongeville, Aline Meirhaeghe.

Karolinska Institutet (Sweden)

Michael Sjöstrom, Jonatan R Ruiz, Francisco B. Ortega, María Hagströmer, Anita Hurtig Wennlöf, Lena Hallström, Emma Patterson, Lydia Kwak, Julia Wärnberg, Nico Rizzo.

Asociación de Investigación de la Industria Agroalimentaria (Spain)

Jackie Sánchez-Molero, Sara Castelló, Elena Picó, Maite Navarro, Blanca Viadel, José Enrique Carreres, Gema Merino, Rosa Sanjuán, María Lorente, María José Sánchez.

Campden BRI (United Kingdom)

Chantal Gilbert, Sarah Thomas, Elaine Allchurch, Peter Burgess.

SIK - Institutet foer Livsmedel och Bioteknik (Sweden)

Gunnar Hall, Annika Astrom, Anna Sverkén, Agneta Broberg.

Meurice Recherche & Development asbl (Belgium)

Annick Masson, Claire Lehoux, Pascal Brabant, Philippe Pate, Laurence Fontaine.

Campden & Chorleywood Food Development Institute (Hungary)

Andras Sebok, Tunde Kuti, Adrienn Hegyi.

Productos Aditivos SA (Spain)

Cristina Maldonado, Ana Llorente.

Cárnicas Serrano SL (Spain)

Emilio García.

Cederroth International AB (Sweden)

Holger von Fircks, Marianne Lilja Hallberg, Maria Messerer.

Lantmännen Food R&D (Sweden)

Mats Larsson, Helena Fredriksson, Viola Adamsson, Ingmar Börjesson.

European Food Information Council (Belgium)

Laura Fernández, Laura Smillie, Josephine Wills.

Universidad Politécnica de Madrid (Spain)

Marcela González-Gross, Raquel Pedrero-Chamizo, Agustín Meléndez, Jara Valtueña, David Jiménez-Pavón, Ulrike Albers, Pedro J. Benito, Juan José Gómez Lorente, David Cañada, Alejandro Urzanqui, Rosa María Torres, Paloma Navarro.

Author information

Authors and Affiliations

  1. GENUD (Growth, Exercise, Nutrition and Development) Research group, Instituto Agroalimentario de Aragón (IA2), Instituto de Investigación Sanitaria Aragón (IIS Aragón), Universidad de Zaragoza, C/Pedro Cerbuna, 12, SAI Building (Servicio de Apoyo a la Investigación), 2nd floor, 50009, Zaragoza, Spain

    Iris Iglesia, Theodora Mouratidou & Luis A. Moreno

  2. Red de Salud Materno-infantil y del Desarrollo (SAMID), Madrid, Spain

    Iris Iglesia

  3. ImFINE Research Group, Department of Health and Human Performance, Universidad Politécnica de Madrid, Madrid, Spain

    Marcela González-Gross & Christina Breidenassel

  4. Department of Public Health, Ghent University, Ghent, Belgium

    Inge Huybrechts & Stefaan De Henauw

  5. International Agency for Research on Cancer (IARC), 150 Cours Albert Thomas, 69372, Lyon Cedex 08, France

    Inge Huybrechts

  6. Department of Nutrition and Food Science, University of Bonn, 53115, Bonn, Germany

    Christina Breidenassel & Peter Stehle

  7. Department of Preventive Medicine and Public Health, Universidad de Zaragoza, Zaragoza, Spain

    Javier Santabárbara

  8. Immunonutrition Research Group, Department of Metabolism and Nutrition, Institute of Food Science, Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain

    Ligia-Esperanza Díaz

  9. Unit for Preventive Nutrition, Department of Biosciences and Nutrition, Karolinska Institute, Stockholm (Huddinge), Sweden

    Lena Hällström

  10. Sweden and School of Health, Care and Social Welfare Mälardalens University, Västerås, Sweden

    Lena Hällström

  11. Inserm U995, Faculté de Médecine, Université Lille 2, Lille, France

    Frédéric Gottrand

  12. University of Crete School of Medicine, 71033, Crete, Greece

    Anthony Kafatos

  13. Division of Clinical Nutrition and Prevention, Department of Pediatrics, Medical University of Vienna, Vienna, Austria

    Kurt Widhalm

  14. Department of Nutrition- and Dietetics, School of Health Science and Education, Harokopio University, Athens, Greece

    Yannis Manios

  15. Department of Paediatrics, University of Pécs, Pécs, Hungary

    Denes Molnar

  16. Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y Nutrición (CIBERObn), Madrid, Spain

    Luis A. Moreno

Authors
  1. Iris Iglesia
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  2. Theodora Mouratidou
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  3. Marcela González-Gross
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  4. Inge Huybrechts
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  5. Christina Breidenassel
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  6. Javier Santabárbara
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  7. Ligia-Esperanza Díaz
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  8. Lena Hällström
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  9. Stefaan De Henauw
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  10. Frédéric Gottrand
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  11. Anthony Kafatos
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  12. Kurt Widhalm
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  13. Yannis Manios
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  14. Denes Molnar
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  15. Peter Stehle
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  16. Luis A. Moreno
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Consortia

on the behalf of HELENA study group

  • Luis A. Moreno
  • , Jesús Fleta
  • , José A. Casajús
  • , Gerardo Rodríguez
  • , Concepción Tomás
  • , María I. Mesana
  • , Germán Vicente-Rodríguez
  • , Adoración Villarroya
  • , Carlos M. Gil
  • , Ignacio Ara
  • , Juan Fernández Alvira
  • , Gloria Bueno
  • , Aurora Lázaro
  • , Olga Bueno
  • , Juan F. León
  • , Jesús Mª Garagorri
  • , Manuel Bueno
  • , Idoia Labayen
  • , Iris Iglesia
  • , Silvia Bel
  • , Luis A. Gracia Marco
  • , Theodora Mouratidou
  • , Alba Santaliestra-Pasías
  • , Iris Iglesia
  • , Esther González-Gil
  • , Pilar De Miguel-Etayo
  • , Cristina Julián Almárcegui
  • , Mary Miguel-Berges
  • , Isabel Iguacel
  • , Ascensión Marcos
  • , Julia Wärnberg
  • , Esther Nova
  • , Sonia Gómez
  • , Ligia Esperanza Díaz
  • , Javier Romeo
  • , Ana Veses
  • , Belén Zapatera
  • , Tamara Pozo
  • , David Martínez
  • , Laurent Beghin
  • , Christian Libersa
  • , Frédéric Gottrand
  • , Catalina Iliescu
  • , Juliana Von Berlepsch
  • , Mathilde Kersting
  • , Wolfgang Sichert-Hellert
  • , Ellen Koeppen
  • , Dénes Molnar
  • , Eva Erhardt
  • , Katalin Csernus
  • , Katalin Török
  • , Szilvia Bokor
  • , Mrs. Angster
  • , Enikö Nagy
  • , Orsolya Kovács
  • , Judit Répasi
  • , Anthony Kafatos
  • , Caroline Codrington
  • , María Plada
  • , Angeliki Papadaki
  • , Katerina Sarri
  • , Anna Viskadourou
  • , Christos Hatzis
  • , Michael Kiriakakis
  • , George Tsibinos
  • , Constantine Vardavas
  • , Manolis Sbokos
  • , Eva Protoyeraki
  • , Maria Fasoulaki
  • , Peter Stehle
  • , Klaus Pietrzik
  • , Marcela González-Gross
  • , Christina Breidenassel
  • , Andre Spinneker
  • , Jasmin Al-Tahan
  • , Miriam Segoviano
  • , Anke Berchtold
  • , Christine Bierschbach
  • , Erika Blatzheim
  • , Adelheid Schuch
  • , Petra Pickert
  • , Manuel J. Castillo
  • , Ángel Gutiérrez
  • , Francisco B. Ortega
  • , Jonatan R. Ruiz
  • , Enrique G. Artero
  • , Vanesa España
  • , David Jiménez-Pavón
  • , Palma Chillón
  • , Cristóbal Sánchez-Muñoz
  • , Magdalena Cuenca
  • , Davide Arcella
  • , Elena Azzini
  • , Emma Barrison
  • , Noemi Bevilacqua
  • , Pasquale Buonocore
  • , Giovina Catasta
  • , Laura Censi
  • , Donatella Ciarapica
  • , Paola D’Acapito
  • , Marika Ferrari
  • , Myriam Galfo
  • , Cinzia Le Donne
  • , Catherine Leclercq
  • , Giuseppe Maiani
  • , Beatrice Mauro
  • , Lorenza Mistura
  • , Antonella Pasquali
  • , Raffaela Piccinelli
  • , Angela Polito
  • , Romana Roccaldo
  • , Raffaella Spada
  • , Stefania Sette
  • , Maria Zaccaria
  • , Luca Scalfi
  • , Paola Vitaglione
  • , Concetta Montagnese lyName>
  • , Ilse De Bourdeaudhuij
  • , Stefaan De Henauw
  • , Tineke De Vriendt
  • , Lea Maes
  • , Christophe Matthys
  • , Carine Vereecken
  • , Mieke de Maeyer
  • , Charlene Ottevaere
  • , Inge Huybrechts
  • , Kurt Widhalm
  • , Katharina Phillipp
  • , Sabine Dietrich
  • , Birgit Kubelka
  • , Marion Boriss-Riedl
  • , Yannis Manios
  • , Eva Grammatikaki
  • , Zoi Bouloubasi
  • , Tina Louisa Cook
  • , Sofia Eleutheriou
  • , Orsalia Consta
  • , George Moschonis
  • , Ioanna Katsaroli
  • , George Kraniou
  • , Stalo Papoutsou
  • , Despoina Keke
  • , Ioanna Petraki
  • , Elena Bellou
  • , Sofia Tanagra
  • , Kostalenia Kallianoti
  • , Dionysia Argyropoulou
  • , Stamatoula Tsikrika
  • , Christos Karaiskos
  • , Jean Dallongeville
  • , Aline Meirhaeghe
  • , Michael Sjöstrom
  • , Jonatan R. Ruiz
  • , Francisco B. Ortega
  • , María Hagströmer
  • , Anita Hurtig Wennlöf
  • , Lena Hallström
  • , Emma Patterson
  • , Lydia Kwak
  • , Julia Wärnberg
  • , Nico Rizzo
  • , Jackie Sánchez-Molero
  • , Sara Castelló
  • , Elena Picó
  • , Maite Navarro
  • , Blanca Viadel
  • , José Enrique Carreres
  • , Gema Merino
  • , Rosa Sanjuán
  • , María Lorente
  • , María José Sánchez
  • , Chantal Gilbert
  • , Sarah Thomas
  • , Elaine Allchurch
  • , Peter Burgess
  • , Gunnar Hall
  • , Annika Astrom
  • , Anna Sverkén
  • , Agneta Broberg
  • , Annick Masson
  • , Claire Lehoux
  • , Pascal Brabant
  • , Philippe Pate
  • , Laurence Fontaine
  • , Andras Sebok
  • , Tunde Kuti
  • , Adrienn Hegyi
  • , Cristina Maldonado
  • , Ana Llorente
  • , Emilio García
  • , Holger von Fircks
  • , Marianne Lilja Hallberg
  • , Maria Messerer
  • , Mats Larsson
  • , Helena Fredriksson
  • , Viola Adamsson
  • , Ingmar Börjesson
  • , Laura Fernández
  • , Laura Smillie
  • , Josephine Wills
  • , Marcela González-Gross
  • , Raquel Pedrero-Chamizo
  • , Agustín Meléndez
  • , Jara Valtueña
  • , David Jiménez-Pavón
  • , Ulrike Albers
  • , Pedro J. Benito
  • , Juan José Gómez Lorente
  • , David Cañada
  • , Alejandro Urzanqui
  • , Rosa María Torres
  •  & Paloma Navarro

Corresponding author

Correspondence to Iris Iglesia.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical standard

This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving human subjects were approved by the Human Research Review Committees of the corresponding centres. Informed written consent was obtained from all the adolescents and their parents.

Appendix

Appendix

Food group

Items included, description

Dairy products

Milk and yogurt beverages

Other milk products

Desserts and puddings milk based and creams with extra amount of sugars and fats

White and butter milk

Milk (any kind of fat content), and also the liquid left behind after churning butter out of cream, which is typical for northern countries in Europe

Yogurt and white cheese

All kind of yogurts and low fat cheese

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Iglesia, I., Mouratidou, T., González-Gross, M. et al. Foods contributing to vitamin B6, folate, and vitamin B12 intakes and biomarkers status in European adolescents: The HELENA study. Eur J Nutr 56, 1767–1782 (2017). https://doi.org/10.1007/s00394-016-1221-1

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  • DOI: https://doi.org/10.1007/s00394-016-1221-1

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