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Diet as a moderator in the association of sedentary behaviors with inflammatory biomarkers among adolescents in the HELENA study

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Abstract

Aim

To assess if a healthy diet might attenuate the positive sedentary–inflammation relation, whereas an unhealthy diet may increase the effect of sedentary behaviors on inflammatory biomarkers.

Methods

In 618 adolescents (13–17 years) of the European HELENA study, data were available on body composition, a set of inflammation markers, and food intake assessed by a self-administered computerized 24 h dietary recall for 2 days. A 9-point Mediterranean diet score and an antioxidant-rich diet z-score were used as dietary indices and tested as moderators. A set of low-grade inflammatory characteristics was used as outcome: several cytokines in an inflammatory ratio (IL-6, IL-10, TNF-α, TGFβ-1), C-reactive protein, three cell-adhesion molecules (sVCAM-1, sICAM-1, sE-selectin), three cardiovascular risk markers (GGT, ALT, homocysteine) and three immune cell types (white blood cells, lymphocytes, CD3). Sedentary behaviors were self-reported and analyzed as total screen time. Multiple linear regression analyses tested moderation by diet in the sedentary behaviors–inflammation association adjusted for age, sex, country, adiposity (sum of six skinfolds), parental education, and socio-economic status.

Results

Both diet scores, Mediterranean and antioxidant-rich diet, were significant protective moderators in the effect of sedentary behaviors on alanine-transaminase enzyme (P = 0.014; P = 0.027), and on the pro/anti-inflammatory cytokine ratio (P = 0.001; P = 0.004), but not on other inflammatory parameters.

Conclusion

A higher adherence to the Mediterranean diet or an antioxidant-rich diet may attenuate the onset of oxidative stress signs associated by sedentary behaviors, whereas a poor diet seems to increase inflammation.

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Acknowledgements

The HELENA Study was carried out with the financial support of the European Community Sixth RTD Framework Programme (Contract FOODCT-2005-007034). The writing group takes sole responsibility for the content of this article. The European Community is not liable for any use that may be made of the information contained therein.

The HELENA Study Group: Luis A. Moreno, Fréderic Gottrand, Stefaan De Henauw, Marcela González-Gross, Chantal Gilbert, Anthony Kafatos, Christian Libersa, Sara Castelló, Mathilde Kersting, Michael Sjöstrom, Dénes Molnár, Jean Dallongeville, Gunnar Hall, Lea Maes, Luca Scalfi, Pilar Meléndez, José A. Casajús, Jesús Fleta, Gerardo Rodríguez, Concepción Tomás, María I. Mesana, Germán Vicente-Rodríguez, Adoración Villarroya, Carlos M. Gil, Ignacio Ara, Juan Fernández Alvira, Gloria Bueno, Olga Bueno, Juan F. León, Jesús Mª Garagorri, Idoia Labayen, Silvia Bel, Luis A. Gracia Marco, Theodora Mouratidou, Alba Santaliestra-Pasías, Iris Iglesia, Esther González-Gil, Pilar De Miguel-Etayo, Cristina Julián, Mary Miguel-Berges, Isabel Iguacel, Azahara Rupérez, Ascensión Marcos, Julia Wärnberg, Esther Nova, Sonia Gómez, Ligia Esperanza Díaz, Javier Romeo, Ana Veses, Belén Zapatera, Tamara Pozo, David Martínez, Laurent Beghin, Frédéric Gottrand, Catalina Iliescu, Juliana Von Berlepsch, Wolfgang Sichert-Hellert, Ellen Koeppen, Eva Erhardt, Katalin Csernus, Katalin Török, Szilvia Bokor, Mrs. Angster, Enikö Nagy, Orsolya Kovács, Judit Répasi, 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, 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, Paola Vitaglione, Concetta Montagnese, Ilse De Bourdeaudhuij, Tineke De Vriendt, 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, Aline Meirhaeghe, María Hagströmer, Anita Hurtig Wennlöf, Lena Hallström, Emma Patterson, Lydia Kwak, Julia Wärnberg, Nico Rizzo, Jackie Sánchez-Molero, 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, 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, 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.

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Authors and Affiliations

  1. Department of Public Health, Faculty of Medicine and Health Sciences, Ghent University, De Pintelaan 185, Block K3-4th floor, 9000, Ghent, Belgium

    Aline B. Arouca, Inge Huybrechts, Stefaan De Henauw & Nathalie Michels

  2. GENUD: “Growth, Exercise, Nutrition and Development” Research Group, Facultad de Ciencias de la Salud, University of Zaragoza, Instituto Agroalimentario de Aragón (IA2), Instituto de Investigación Sanitaria Aragón (IIS Aragón), Zaragoza, Spain

    Alba M. Santaliestra-Pasías & Luis A. Moreno

  3. Department of Metabolism and Nutrition, Institute of Food Science and Technology and Nutrition, Madrid, Spain

    Ascensión Marcos

  4. Department of Pediatrics, Div. Nutrition and Metabolism, Medical University of Vienna, Vienna, Austria

    Kurt Widhalm

  5. Department of Pediatrics, Medical Faculty, University of Pécs, Pécs, Hungary

    Dénes Molnár

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

    Yannis Manios

  7. Faculty of Medicine, University Lille, Lille, France

    Frederic Gottrand

  8. Faculty of Medicine, University of Crete, Crete, Greece

    Anthony Kafatos

  9. Research Department of Child Nutrition, Pediatric University Clinic, Ruhr-University Bochum, Bochum, Germany

    Mathilde Kersting

  10. Department of Biosciences, Unit for Preventive Nutrition, Karolinska Institutet, Huddinge, Sweden

    Michael Sjöström

  11. Department of Physiology, School of Medicine, Granada University, Granada, Spain

    Ángel Gutiérrez Sáinz

  12. Council for Agricultural Research and Economics, Research Center for Food and Nutrition, Rome, Italy

    Marika Ferrari

  13. International Agency for Research on Cancer, Lyon, France

    Inge Huybrechts

  14. ImFINE Research Group. Department of Health and Human Performance, Facultad de Ciencias de la Actividad Física y del Deporte-INEF, Universidad Politécnica de Madrid, Madrid, Spain

    Marcela González-Gross

  15. School of Education, Health and Social Studies, Dalarna University, Falun, Sweden

    Maria Forsner

  16. Department of Nursing, Umeå University, Umeå, Sweden

    Maria Forsner

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

    Luis A. Moreno & Marcela González-Gross

Authors
  1. Aline B. Arouca
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  2. Alba M. Santaliestra-Pasías
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  3. Luis A. Moreno
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  4. Ascensión Marcos
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  5. Kurt Widhalm
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  6. Dénes Molnár
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  7. Yannis Manios
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  8. Frederic Gottrand
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  9. Anthony Kafatos
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  10. Mathilde Kersting
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  11. Michael Sjöström
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  12. Ángel Gutiérrez Sáinz
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  13. Marika Ferrari
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  14. Inge Huybrechts
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  15. Marcela González-Gross
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  16. Maria Forsner
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  17. Stefaan De Henauw
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  18. Nathalie Michels
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Consortia

the HELENA study group

  • Luis A. Moreno
  • , Fréderic Gottrand
  • , Stefaan De Henauw
  • , Marcela González-Gross
  • , Chantal Gilbert
  • , Anthony Kafatos
  • , Christian Libersa
  • , Sara Castelló
  • , Mathilde Kersting
  • , Michael Sjöstrom
  • , Dénes Molnár
  • , Jean Dallongeville
  • , Gunnar Hall
  • , Lea Maes
  • , Luca Scalfi
  • , Pilar Meléndez
  • , José A. Casajús
  • , Jesús Fleta
  • , Gerardo Rodríguez
  • , Concepción Tomás
  • , María I. Mesana
  • , Germán Vicente-Rodríguez
  • , Adoración Villarroya
  • , Carlos M. Gil
  • , Ignacio Ara
  • , Juan Fernández Alvira
  • , Gloria Bueno
  • , Olga Bueno
  • , Juan F. León
  • , Jesús Mª Garagorri
  • , Idoia Labayen
  • , Silvia Bel
  • , Luis A. Gracia Marco
  • , Theodora Mouratidou
  • , Alba Santaliestra-Pasías
  • , Iris Iglesia
  • , Esther González-Gil
  • , Pilar De Miguel-Etayo
  • , Cristina Julián
  • , Mary Miguel-Berges
  • , Isabel Iguacel
  • , Azahara Rupérez
  • , Ascensión Marcos
  • , Julia Wärnberg
  • , Esther Nova
  • , Sonia Gómez
  • , Ligia Esperanza Díaz
  • , Javier Romeo
  • , Ana Veses
  • , Belén Zapatera
  • , Tamara Pozo
  • , David Martínez
  • , Laurent Beghin
  • , Frédéric Gottrand
  • , Catalina Iliescu
  • , Juliana Von Berlepsch
  • , Wolfgang Sichert-Hellert
  • , Ellen Koeppen
  • , Eva Erhardt
  • , Katalin Csernus
  • , Katalin Török
  • , Szilvia Bokor
  • ,  Angster
  • , Enikö Nagy
  • , Orsolya Kovács
  • , Judit Répasi
  • , 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
  • , 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
  • , Paola Vitaglione
  • , Concetta Montagnese
  • , Ilse De Bourdeaudhuij
  • , Tineke De Vriendt
  • , 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
  • , Aline Meirhaeghe
  • , María Hagströmer
  • , Anita Hurtig Wennlöf
  • , Lena Hallström
  • , Emma Patterson
  • , Lydia Kwak
  • , Julia Wärnberg
  • , Nico Rizzo
  • , Jackie Sánchez-Molero
  • , 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
  • , 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
  • , 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

Contributions

ABA formulated the research question, has analyzed the data and wrote a draft of the paper. NM helped in formulating the research question, analyzing the data and did editing of the first draft. NM and SDH are co-supervisor and supervisor of ABA; LAM was coordinator of the HELENA project. All other authors were involved in the HELENA project (coordinator or data collection). AM was responsible for the inflammatory parameter analyses. IH developed the Mediterranean diet Score. MG was responsible for the complete blood sampling and collection. The authors would like to thank Anke Carstensen and Petra Pickert for their contribution to laboratory work. All authors have read the draft and agreed on the final version.

Corresponding author

Correspondence to Aline B. Arouca.

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Conflict of interest

The author declares that there is no competing interest.

Additional information

The members of the HELENA Study Group are listed in Acknowledgements.

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Arouca, A.B., Santaliestra-Pasías, A.M., Moreno, L.A. et al. Diet as a moderator in the association of sedentary behaviors with inflammatory biomarkers among adolescents in the HELENA study. Eur J Nutr 58, 2051–2065 (2019). https://doi.org/10.1007/s00394-018-1764-4

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  • DOI: https://doi.org/10.1007/s00394-018-1764-4

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