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Influence of sex, age, pubertal maturation and body mass index on circulating white blood cell counts in healthy European adolescents—the HELENA study

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Abstract

Percentiles 10th, 25th, 50th, 75th and 90th are presented for circulating white blood cells (WBC), neutrophils, lymphocytes, monocytes, eosinophils and basophils in healthy European adolescents (12.5–17.5 years, n = 405, 48.9 % boys), considering age, sex, puberty and body mass index (BMI). CD3+ (mature T cells), CD4+ (T helper), CD8+ (T cytotoxic), CD16+56+ (natural killer), CD19+ (B cells), CD3+CD45RA+, CD4+CD45RA+, CD8+CD45RA+ (naïve), CD3+CD45RO+, CD4+CD45RO+ and CD8+CD45RO+ (memory) lymphocytes were also analysed by immunophenotyping. Girls presented higher WBC, neutrophil, CD3+CD45RO+ and CD4+CD45RO+ cell counts and CD3+/CD19+ ratio, and lower CD3+CD45RA+ and CD4+CD45RA+ counts than boys. Age was associated with higher neutrophil counts and CD3+/CD19+, and lower CD19+ counts; in boys, with lower CD3+CD45RA+, CD4+CD45RA+ and CD8+CD45RA+ counts as well; in girls, with higher WBC, CD3+CD45RO+ and CD4+CD45RO+ counts. Pubertal maturation in boys was associated with lower WBC and lymphocyte counts; in girls, with higher basophil, CD3+CD45RO+ and CD4+CD45RO+ values. BMI was associated with higher WBC counts; in boys, also with higher lymphocyte counts; in girls, with higher neutrophil, CD4+, CD3+CD45RO+ and CD4+CD45RO+ counts.

Conclusion: Our study provides normative values for circulating immune cells in adolescents, highlighting the importance of considering sex, age, pubertal maturation and BMI when establishing reference ranges for WBC in paediatric populations.

What is known:

• Reference values for white blood cell counts and immunophenotyping of lymphocyte subsets can constitute useful clinical tools and health indicators in both adult and paediatric populations.

• Immune cell counts vary between childhood and adulthood.

What is new:

• Age and female sex were associated with higher WBC, neutrophil and T memory cell values.

• Pubertal maturation was associated,with lower WBC and lymphocytes in boys and higher T memory cell counts in girls, while BMI was associated with higher WBC, mainly due to greater lymphocyte counts in boys, and to neutrophil and T memory cell counts in girls.

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Abbreviations

BMI:

Body mass index

WBC:

White blood cells

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Acknowledgments

The authors wished to dedicate this work to the memory of Dr. Javier Romeo, and to acknowledge his personal and professional contribution to our group.

The present study was performed as part of the HELENA study (www.helenastudy.com). The authors gratefully acknowledge the participation of all HELENA Study members (listed in the Appendix), as well as the financial support of the European Community 6th RTD Framework Programme (contract FOOD-CT-2005-007034). F.P.d.H. acknowledges funding from a JAE-Doc contract cofounded by the Spanish National Research Council (CSIC) and the European Social Fund. K.V. acknowledges funding from the Research Foundation Flanders (Brussels, Belgium).

Conflict of interest

None of the authors had a personal or financial conflict of interest.

Author’s contributions

L.A.M., F.G., M.G.G., E.N. and A.M. designed the research. S.G.M., L.E.D., A.M.V., J.W. and E.N. performed the sample processing and database building. F.P.d.H. performed the data cleaning and the statistical analysis. F.P.d.H., S.G.M., L.E.D., A.M.V. and E.N. wrote the paper and A.M. edited the manuscript. F.P.d.H. and S.G.M. have primary responsibility for the final content. All authors read and approved the final manuscript.

Author information

Author notes

    Authors and Affiliations

    1. School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Byrom Street, Liverpool, L3 3AF, UK

      Fátima Pérez-de-Heredia

    2. Institute of Food Science, Technology and Nutrition (ICTAN), Spanish National Research Council (CSIC), Madrid, Spain

      Fátima Pérez-de-Heredia, Sonia Gómez-Martínez, Ligia-Esperanza Díaz, Ana M. Veses, Esther Nova & Ascensión Marcos

    3. Unit for Preventive Nutrition, Department of Biosciences and Nutrition at Novum, Karolinska Institutet, Stockholm, Sweden

      Julia Wärnberg, Acki Wastlund & Michael Sjöstrom

    4. Department of Public Health, Faculty of Medicine and Health Sciences, University of Ghent, Ghent, Belgium

      Inge Huybrechts & Krishna Vyncke

    5. International Agency for Research on Cancer, Dietary Exposure Assessment Group, Lyon, France

      Inge Huybrechts

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

      Odysseas Androutsos & Yannis Manios

    7. CRA-NUT, Food and Nutrition Research Center, Agricultural Research Council Roma, Rome, Italy

      Marika Ferrari

    8. ImFine Research Group, Faculty of Physical Activity and Sport Sciences, Technical University of Madrid, Madrid, Spain

      Gonzalo Palacios & Marcela González-Gross

    9. Department of Pediatrics, University of Pécs, Pécs, Hungary

      Éva Kovács & Denes Molnár

    10. Institute for Medical Information Processing, Biometrics and Epidemiology and German Centre for Vertigo and Balance Disorders, Ludwig-Maximilians-Universität, Munich, Germany

      Éva Kovács

    11. Hôpital J de Flandre CHRU de Lille, Inserm U995, IFR114, Faculté de Médecine, Université de Lille 2, Lille, France

      Frédéric Gottrand

    12. Department of Nutrition and Food Sciences, Nutritional Physiology, University of Bonn, Bonn, Germany

      Marcela González-Gross

    13. Department of Medical Physiology, Faculty of Medicine, University of Granada, Granada, Spain

      Manuel J. Castillo

    14. University of Crete School of Medicine, Department of Social Medicine, Preventive Medicine and Nutrition Clinic, Heraklion, Crete, Greece

      Anthony Kafatos

    15. Department of Pediatrics, Private Medical University Salzburg, Salzburg, Austria

      Kurt Widhalm

    16. GENUD (Growth, Exercise, Nutrition and Development) Research Group, University of Zaragoza, Zaragoza, Spain

      Luis A. Moreno

    Authors
    1. Fátima Pérez-de-Heredia
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    2. Sonia Gómez-Martínez
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    3. Ligia-Esperanza Díaz
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    4. Ana M. Veses
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    5. Esther Nova
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    6. Julia Wärnberg
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    7. Inge Huybrechts
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    8. Krishna Vyncke
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    9. Odysseas Androutsos
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    10. Marika Ferrari
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    11. Gonzalo Palacios
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    12. Acki Wastlund
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    13. Éva Kovács
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    14. Frédéric Gottrand
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    15. Marcela González-Gross
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    16. Manuel J. Castillo
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    17. Michael Sjöstrom
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    18. Yannis Manios
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    19. Anthony Kafatos
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    20. Denes Molnár
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    21. Kurt Widhalm
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    22. Luis A. Moreno
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    23. Ascensión Marcos
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    Consortia

    on behalf of the HELENA Study Group

    Corresponding author

    Correspondence to Fátima Pérez-de-Heredia.

    Additional information

    Communicated by David Nadal

    Fátima Pérez-de-Heredia and Sonia Gómez-Martínez contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary Table 1

    Relative values (%) of white blood cell types in European adolescents, according to age categories and stratified for sex. (DOCX 27 kb)

    Supplementary Table 2

    Relative counts (%) of selected lymphocyte subsets in European adolescents, according to age and stratified for sex. (DOCX 33 kb)

    Supplementary Table 3

    Relative values (%) of white blood cell types in European adolescents, according to Tanner stages and stratified for sex. (DOCX 25 kb)

    Supplementary Table 4

    Relative counts (%) of selected lymphocyte subsets in European adolescents, according to Tanner stages and stratified for sex. (DOCX 30 kb)

    Supplementary Table 5

    Relative values (%) of white blood cell types in European adolescents, according to BMI z-scores and stratified for sex. (DOCX 26 kb)

    Supplementary Table 6

    Relative counts (%) of selected lymphocyte subsets in European adolescents, according to BMI z-scores and stratified for sex (DOCX 34 kb)

    APPENDIX: HELENA Study Group

    APPENDIX: 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.

    1. 1.

      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 Revenga, Carmen Lachen, Juan Fernández Alvira, Gloria Bueno, Aurora Lázaro, Olga Bueno, Juan F. León, Jesús Mª Garagorri, Manuel Bueno, Juan Pablo Rey López, Iris Iglesia, Paula Velasco, Silvia Bel, Luis A. Gracia Marco, Theodora Mouratidou.

    2. 2.

      Consejo Superior de Investigaciones Científicas (Spain): Ascensión Marcos, Esther Nova, Sonia Gómez-Martínez, Ligia-Esperanza Díaz, Javier Romeo, Ana Veses, Belén Zapatera, Tamara Pozo, David Martínez.

    3. 3.

      Université de Lille 2 (France): Laurent Beghin, Christian Libersa, Frédéric Gottrand, Catalina Iliescu, Juliana Von Berlepsch.

    4. 4.

      Research Institute of Child Nutrition Dortmund, Rheinische Friedrich-Wilhelms-Universität Bonn (Germany): Mathilde Kersting, Wolfgang Sichert-Hellert, Ellen Koeppen.

    5. 5.

      Pécsi Tudományegyetem (University of Pécs) (Hungary): Dénes Molnar, Eva Erhardt, Katalin Csernus, Katalin Török, Szilvia Bokor, Enikö Nagy, Orsolya Kovács, Judit Répasi.

    6. 6.

      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.

    7. 7.

      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.

    8. 8.

      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.

    9. 9.

      Istituto Nazionale di Ricerca per gli Alimenti e la Nutrizione (Italy): Davide Arcella, Elena Azzini, Emma Barison, 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, Raffaella Spada, Stefania Sette, Maria Zaccaria, Romana Roccaldo.

    10. 10.

      University of Napoli ‘Federico II’ Department of Food Science (Italy): Luca Scalfi, Paola Vitaglione, Concetta Montagnese.

    11. 11.

      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.

    12. 12.

      Medical University of Vienna (Austria): Kurt Widhalm, Katharina Phillipp, Sabine Dietrich, Birgit Kubelka, Marion Boriss-Riedl.

    13. 13.

      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, Katerina Kondaki, Stamatoula Tsikrika, Christos Karaiskos.

    14. 14.

      Institut Pasteur de Lille (France): Jean Dallongeville, Aline Meirhaeghe.

    15. 15.

      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.

    16. 16.

      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.

    17. 17.

      Campden BRI (United Kingdom): Chantal Gilbert, Sarah Thomas, Elaine Allchurch, Peter Burgess.

    18. 18.

      SIK – Institutet foer Livsmedel och Bioteknik (Sweden): Gunnar Hall, Annika Astrom, Anna Sverkén, Agneta Broberg.

    19. 19.

      Meurice Recherche & Development asbl (Belgium): Annick Masson, Claire Lehoux, Pascal Brabant, Philippe Pate, Laurence Fontaine.

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      Campden and Chorleywood Food Development Institute (Hungary): Andras Sebok, Tunde Kuti, Adrienn Hegyi.

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      Productos Aditivos SA (Spain): Cristina Maldonado, Ana Llorente.

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      Cárnicas Serrano SL (Spain): Emilio García.

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      Cederroth International AB (Sweden): Holger von Fircks, Marianne Lilja Hallberg, Maria Messerer.

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      Lantmännen Food R&D (Sweden): Mats Larsson, Helena Fredriksson, Viola Adamsson, Ingmar Börjesson.

    25. 25.

      European Food Information Council (Belgium): Laura Fernández, Laura Smillie, Josephine Wills.

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      Universidad Politécnica de Madrid (Spain): Marcela González-Gross, Jara Valtueña, David Jiménez-Pavón, Ulrike Albers, Raquel Pedrero, Gonzalo Palacios, Agustín Meléndez, Pedro J. Benito, Juan José Gómez Lorente, David Cañada, Alejandro Urzanqui, Juan Carlos Ortiz, Francisco Fuentes, Rosa María Torres, Paloma Navarro.

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    Pérez-de-Heredia, F., Gómez-Martínez, S., Díaz, LE. et al. Influence of sex, age, pubertal maturation and body mass index on circulating white blood cell counts in healthy European adolescents—the HELENA study. Eur J Pediatr 174, 999–1014 (2015). https://doi.org/10.1007/s00431-015-2497-5

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