Greater male variability in daily energy expenditure develops through puberty

Lewis G Halsey¹, Vincent Careau², Philip N Ainslie³, Heliodoro Alemán-Mateo⁴, Lene F Andersen⁵, Liam J Anderson^{3

6}, Leonore Arab⁷, Issad Baddou⁸, Linda Bandini⁹, Kweku Bedu-Addo¹⁰, Ellen E Blaak¹¹, Stephane Blanc¹², Alberto G Bonomi¹³, Carlijn V C Bouten¹⁴, Pascal Bovet¹⁵, Soren Brage¹⁶, Maciej S Buchowski¹⁷, Nancy Butte¹⁸, Stephan G Camps¹⁹, Regian Casper²⁰, Graeme L Close³, Lisa H Colbert²¹, Jamie A Cooper²², Richard Cooper²³, Prasangi Dabare²⁴, Sai Krupa Das²⁵, Peter S W Davies²⁶, Sanjoy Deb^{27

28}, Christine Delisle Nyström²⁹, William Dietz³⁰, Lara R Dugas^{23

31}, Simon Eaton³², Ulf Ekelund³³, Asmaa El Hamdouchi⁸, Sonja Entringer^{34

35}, Terrence Forrester³⁶, Barry W Fudge³⁷, Melanie Gillingham³⁸, Annelies H Goris¹⁹, Michael Gurven³⁹, Hinke Haisma⁴⁰, Catherine Hambly⁴¹, Daniel Hoffman⁴², Marije B Hoos¹⁹, Sumei Hu⁴³, Noorjehan Joonas⁴⁴, Annemiek Joosen¹⁹, Peter Katzmarzyk⁴⁵, Kitty P Kempen¹⁹, Misaka Kimura⁴⁶, William E Kraus⁴⁷, Wantanee Kriengsinyos⁴⁸, Rebecca Kuriyan⁴⁹, Robert F Kushner⁵⁰, Estelle V Lambert⁵¹, Pulani Lanerolle⁵², Christel L Larsson⁵³, Nader Lessan⁵⁴, Marie Löf²⁸, Corby Martin⁴⁵, Eric Matsiko⁵⁵, Gerwin A Meijer¹¹, James C Morehen^{3

56}, James P Morton³, Aviva Must⁵⁷, Marian Neuhouser⁵⁸, Theresa A Nicklas¹⁸, Robert M Ojiambo^{59

60}, Kirsi H Pietilainen⁶¹, Yannis P Pitsiladis⁶², Jacob Plange-Rhule¹⁰, Guy Plasqui⁶³, Ross L Prentice⁶³, Roberto Rabinovich⁶⁴, Susan B Racette⁶⁵, David A Raichen⁶⁶, Eric Ravussin⁴⁵, Leanne Redman⁴⁵, John J Reilly⁶⁷, Rebecca Reynolds⁶⁸, Susan Roberts²⁵, Jennifer C Rood⁴⁵, Dulani Samaranayake⁶⁹, Luís B Sardinha⁷⁰, Albertine J Scuitt⁷¹, Analiza M Silva⁷⁰, Srishti Sinha⁴⁹, Anders M Sjödin⁷², Eric Stice⁷³, Albert Stunkard⁷⁴, Samuel S Urlacher⁷⁵, Mauro Eduardo Valencia⁴, Giulio Valenti¹⁹, Ludo M van Etten¹⁹, Edgar A Van Mil⁷⁶, Jeanine A Verbunt¹⁹, Jonathan C K Wells⁷⁷, George Wilson³, Brian Wood^{41

78

79}, Tsukasa Yoshida⁸⁰, Xueying Zhang^{81

82

83}, Alexia Murphy-Alford⁸⁴, Cornelia Loechl⁸⁴, Amy Luke^{31

85}, Herman Pontzer^{86

87}, Jennifer Rood⁴⁵, Hiroyuki Sagayama⁸⁸, Klaas R Westerterp¹¹, William W Wong¹⁸, Yosuke Yamada^{46

80}, John R Speakman^{85

86}; IAEA DLW Database Consortium

Affiliations

¹ School of Life and Health Sciences, University of Roehampton, London SW15 4JD, UK.
² Department of Biology, University of Ottawa, Ottawa, Ontario, Canada.
³ Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, UK.
⁴ Centro de Investigación en Alimentación y Desarrollo, A.C., Mexico.
⁵ Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, 0317 Oslo, Norway.
⁶ School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK.
⁷ David Geffen School of Medicine, University of California, Los Angeles, CA, USA.
⁸ Unité Mixte de Recherche en Nutrition et Alimentation, CNESTEN-Université Ibn Tofail URAC39, Morocco.
⁹ University of Massachusetts Chan Medical School, Worcester, MA, USA.
¹⁰ Department of Physiology, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana.
¹¹ Nutrition and Translational Research in Metabolism (NUTRIM), Maastricht University Medical Centre, Maastricht, Netherlands.
¹² Institut Pluridisciplinaire Hubert Curien, CNRS Université de Strasbourg, Strasbourg, France.
¹³ Phillips Research, Eindhoven, The Netherlands.
¹⁴ Department of Biomedical Engineering and Institute for Complex Molecular Systems, Eindhoven Unversity of Technology, Eindhoven, The Netherlands.
¹⁵ University Center for promary care and public health (Unisante), Lausanne, Sweitzerland.
¹⁶ MRC Epidemiology Unit, University of Cambridge, Cambridge, UK.
¹⁷ Division of Gastroenterology, Hepatology and Nutrition, Department of Medicine, Vanderbilt University, Nashville, TN, USA.
¹⁸ Department of Pediatrics, Baylor College of Medicine, USDA/ARS Children's Nutrition Research Center, Houston, TX, USA.
¹⁹ Maastricht University, Maastricht, The Netherlands.
²⁰ Department of Psychiatry, University of Chicago, IL, USA.
²¹ Kinesiology, University of Wisconsin, Madison, WI, USA.
²² Nutritional Sciences, University of Wisconsin, USA.
²³ Department of Public Health Sciences, Parkinson School of Health Sciences and Public Health, Maywood, IL, USA.
²⁴ Department of Physiotherapy, Faculty of Allied Health Sciences, General Sir John Kotelawala Defence University, Sri Lanka.
²⁵ Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA, USA.
²⁶ Child Health Research Centre, Level 6 Centre for Children's Health Research, University of Queensland, 62 Graham Street, South Brisbane, Queensland.
²⁷ Centre for Nutraceuticals, School of Life Sciences, University of Westminster, London, UK.
²⁸ Department of Circulation and Medical Imaging, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
²⁹ Department of Biosciences and Nutrition, Karolinska Institute, Stockholm, Sweden.
³⁰ George Washington University, Washington, DC, USA.
³¹ Division of Epidemiology and Biostatistics, School of Public Health and Family Medicine, University of Cape Town, Cape Town, South Africa.
³² UCL, Great Ormond Street Institute of Child Health, London, UK.
³³ Department of Sport Medicine, Norwegian School of Sport Sciences, Oslo, Norway.
³⁴ Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health (BIH), Institute of Medical Psychology, Berlin, Germany.
³⁵ University of California Irvine, Irvine, CA, USA.
³⁶ Solutions for Developing Countries, University of the West Indies, Mona, Kingston, Jamaica.
³⁷ University of Glasgow, Glasgow, UK.
³⁸ Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, OR.
³⁹ Department of Anthropology, University of California Santa Barbara, Santa Barbara, CA, USA.
⁴⁰ Population Research Centre, Faculty of Spatial Sciences, University of Groningen, The Netherlands.
⁴¹ Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, UK.
⁴² Department of Nutritional Sciences, Program in International Nutrition, Rutgers University, New Brunswick, NJ, USA.
⁴³ Institute of Genetics and development Biology, Chinese Academy of Sciences, Beichen Xi lu, Beijing, People's Republic of China.
⁴⁴ Central health Laboratory, Ministry of Health and Wellness, Port Louis, Mauritius.
⁴⁵ Pennington Biomedical Research Center, Baton Rouge, LA, USA.
⁴⁶ Institute for Active Health, Kyoto University of Advanced Science, Kyoto, Japan.
⁴⁷ Department of Medicine, Duke University, Durham, NC, USA.
⁴⁸ Institute of Nutrition, Mahidol University, Salaya, Thailand.
⁴⁹ Division of Nutrition, St John's Research Institute, Bangalore, India.
⁵⁰ Northwestern University, Chicago, IL, USA.
⁵¹ Health through Physical Activity, Lifestyle and Sport Research Centre, Division of Exercise Science and Sports Medicine (ESSM), FIMS International Collaborating Centre of Sports Medicine, Department of Human Biology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa.
⁵² Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka.
⁵³ University of Gothenburg, Gothenburg, Sweden.
⁵⁴ Imperial College London Diabetes Centre, Abu Dhabi, United Arab Emirates.
⁵⁵ Department of Human Nutrition and Dietetics, University of Rwanda, Kigali, Rwanda.
⁵⁶ The FA Group, Burton-Upon-Trent, Staffordshire, UK.
⁵⁷ Tufts University School of Medicine, Boston, USA.
⁵⁸ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center and School of Public Health, University of Washington, Seattle, WA, USA.
⁵⁹ Moi University, Eldoret, Kenya.
⁶⁰ University of Global Health Equity, Rwanda.
⁶¹ Helsinki University Central Hospital, Helsinki, Finland.
⁶² University of Brighton, Eastbourne, UK.
⁶³ Department of Nutrition and Movement Sciences, Maastricht University, Maastricht, The Netherlands.
⁶⁴ University of Edinburgh, Edinburgh, UK.
⁶⁵ Arizona State University, Phoenix, AZ, USA.
⁶⁶ Biological Sciences and Anthropology, University of Southern California, CA, USA.
⁶⁷ Physical activity for Health group, School of Psychological Sciences and Health, University of Strathclyde, Glasgow, UK.
⁶⁸ Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.
⁶⁹ Department of Community Medicine, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka.
⁷⁰ Exercise and health laboratory, CIPER, Faculdade Motricidade Humana, Universidade de Lisboa, Portugal.
⁷¹ University of Wageningen, Wageningen, The Netherlands.
⁷² Department of Nutrition, Exercise and Sports, Copenhagen University, Copenhagen, Denmark.
⁷³ Stanford University, Stanford CA, USA.
⁷⁴ University of Pennsylvania Perelman School of Medicine Department of Psychiatry.
⁷⁵ Department of Anthropology, Baylor University, Waco, TX, USA.
⁷⁶ Maastricht and Lifestyle Medicine Center for Children, Jeroen Bosch Hospital 's-Hertogenbosch, Maastricht University, Maastricht, The Netherlands.
⁷⁷ Population, Policy and Practice Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London, UK.
⁷⁸ University of California Los Angeles, Los Angeles, USA.
⁷⁹ Department of Human Behavior, Ecology, and Culture, Max Planck Institute for Evolutionary Anthropology.
⁸⁰ National Institute of Health and Nutrition, National Institutes of Biomedical Innovation, Health and Nutrition, Tokyo, Japan.
⁸¹ Center for Energy Metabolism and Reproduction, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, People's Republic of China.
⁸² China medical University, Shenyang, Liaoning, People's Republic of China.
⁸³ CAS Center of Excellence in Animal Evolution and Genetics, Kunming, People's Republic of China.
⁸⁴ Nutritional and Health Related Environmental Studies Section, Division of Human Health, International Atomic Energy Agency, Vienna, Austria.
⁸⁵ Division of Epidemiology, Department of Public Health Sciences, Loyola University School of Medicine, Maywood IL, USA.
⁸⁶ Department of Evolutionary Anthropology, Duke University, Durham, NC, USA.
⁸⁷ Duke Global Health Institute, Duke University, Durham, NC, USA.
⁸⁸ Faculty of Health and Sport Sciences, University of Tsukuba, Ibaraki, Japan.

PMID: 37727077
PMCID: PMC10509569
DOI: 10.1098/rsbl.2023.0152

Greater male variability in daily energy expenditure develops through puberty

Lewis G Halsey et al. Biol Lett. 2023 Sep.

. 2023 Sep;19(9):20230152.

doi: 10.1098/rsbl.2023.0152. Epub 2023 Sep 20.

Authors

Affiliations

¹ School of Life and Health Sciences, University of Roehampton, London SW15 4JD, UK.
² Department of Biology, University of Ottawa, Ottawa, Ontario, Canada.
³ Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, UK.
⁴ Centro de Investigación en Alimentación y Desarrollo, A.C., Mexico.
⁵ Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, 0317 Oslo, Norway.
⁶ School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, UK.
⁷ David Geffen School of Medicine, University of California, Los Angeles, CA, USA.
⁸ Unité Mixte de Recherche en Nutrition et Alimentation, CNESTEN-Université Ibn Tofail URAC39, Morocco.
⁹ University of Massachusetts Chan Medical School, Worcester, MA, USA.
¹⁰ Department of Physiology, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana.
¹¹ Nutrition and Translational Research in Metabolism (NUTRIM), Maastricht University Medical Centre, Maastricht, Netherlands.
¹² Institut Pluridisciplinaire Hubert Curien, CNRS Université de Strasbourg, Strasbourg, France.
¹³ Phillips Research, Eindhoven, The Netherlands.
¹⁴ Department of Biomedical Engineering and Institute for Complex Molecular Systems, Eindhoven Unversity of Technology, Eindhoven, The Netherlands.
¹⁵ University Center for promary care and public health (Unisante), Lausanne, Sweitzerland.
¹⁶ MRC Epidemiology Unit, University of Cambridge, Cambridge, UK.
¹⁷ Division of Gastroenterology, Hepatology and Nutrition, Department of Medicine, Vanderbilt University, Nashville, TN, USA.
¹⁸ Department of Pediatrics, Baylor College of Medicine, USDA/ARS Children's Nutrition Research Center, Houston, TX, USA.
¹⁹ Maastricht University, Maastricht, The Netherlands.
²⁰ Department of Psychiatry, University of Chicago, IL, USA.
²¹ Kinesiology, University of Wisconsin, Madison, WI, USA.
²² Nutritional Sciences, University of Wisconsin, USA.
²³ Department of Public Health Sciences, Parkinson School of Health Sciences and Public Health, Maywood, IL, USA.
²⁴ Department of Physiotherapy, Faculty of Allied Health Sciences, General Sir John Kotelawala Defence University, Sri Lanka.
²⁵ Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, Boston, MA, USA.
²⁶ Child Health Research Centre, Level 6 Centre for Children's Health Research, University of Queensland, 62 Graham Street, South Brisbane, Queensland.
²⁷ Centre for Nutraceuticals, School of Life Sciences, University of Westminster, London, UK.
²⁸ Department of Circulation and Medical Imaging, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway.
²⁹ Department of Biosciences and Nutrition, Karolinska Institute, Stockholm, Sweden.
³⁰ George Washington University, Washington, DC, USA.
³¹ Division of Epidemiology and Biostatistics, School of Public Health and Family Medicine, University of Cape Town, Cape Town, South Africa.
³² UCL, Great Ormond Street Institute of Child Health, London, UK.
³³ Department of Sport Medicine, Norwegian School of Sport Sciences, Oslo, Norway.
³⁴ Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health (BIH), Institute of Medical Psychology, Berlin, Germany.
³⁵ University of California Irvine, Irvine, CA, USA.
³⁶ Solutions for Developing Countries, University of the West Indies, Mona, Kingston, Jamaica.
³⁷ University of Glasgow, Glasgow, UK.
³⁸ Department of Molecular and Medical Genetics, Oregon Health & Science University, Portland, OR.
³⁹ Department of Anthropology, University of California Santa Barbara, Santa Barbara, CA, USA.
⁴⁰ Population Research Centre, Faculty of Spatial Sciences, University of Groningen, The Netherlands.
⁴¹ Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, UK.
⁴² Department of Nutritional Sciences, Program in International Nutrition, Rutgers University, New Brunswick, NJ, USA.
⁴³ Institute of Genetics and development Biology, Chinese Academy of Sciences, Beichen Xi lu, Beijing, People's Republic of China.
⁴⁴ Central health Laboratory, Ministry of Health and Wellness, Port Louis, Mauritius.
⁴⁵ Pennington Biomedical Research Center, Baton Rouge, LA, USA.
⁴⁶ Institute for Active Health, Kyoto University of Advanced Science, Kyoto, Japan.
⁴⁷ Department of Medicine, Duke University, Durham, NC, USA.
⁴⁸ Institute of Nutrition, Mahidol University, Salaya, Thailand.
⁴⁹ Division of Nutrition, St John's Research Institute, Bangalore, India.
⁵⁰ Northwestern University, Chicago, IL, USA.
⁵¹ Health through Physical Activity, Lifestyle and Sport Research Centre, Division of Exercise Science and Sports Medicine (ESSM), FIMS International Collaborating Centre of Sports Medicine, Department of Human Biology, Faculty of Health Sciences, University of Cape Town, Cape Town, South Africa.
⁵² Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka.
⁵³ University of Gothenburg, Gothenburg, Sweden.
⁵⁴ Imperial College London Diabetes Centre, Abu Dhabi, United Arab Emirates.
⁵⁵ Department of Human Nutrition and Dietetics, University of Rwanda, Kigali, Rwanda.
⁵⁶ The FA Group, Burton-Upon-Trent, Staffordshire, UK.
⁵⁷ Tufts University School of Medicine, Boston, USA.
⁵⁸ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center and School of Public Health, University of Washington, Seattle, WA, USA.
⁵⁹ Moi University, Eldoret, Kenya.
⁶⁰ University of Global Health Equity, Rwanda.
⁶¹ Helsinki University Central Hospital, Helsinki, Finland.
⁶² University of Brighton, Eastbourne, UK.
⁶³ Department of Nutrition and Movement Sciences, Maastricht University, Maastricht, The Netherlands.
⁶⁴ University of Edinburgh, Edinburgh, UK.
⁶⁵ Arizona State University, Phoenix, AZ, USA.
⁶⁶ Biological Sciences and Anthropology, University of Southern California, CA, USA.
⁶⁷ Physical activity for Health group, School of Psychological Sciences and Health, University of Strathclyde, Glasgow, UK.
⁶⁸ Centre for Cardiovascular Sciences, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.
⁶⁹ Department of Community Medicine, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka.
⁷⁰ Exercise and health laboratory, CIPER, Faculdade Motricidade Humana, Universidade de Lisboa, Portugal.
⁷¹ University of Wageningen, Wageningen, The Netherlands.
⁷² Department of Nutrition, Exercise and Sports, Copenhagen University, Copenhagen, Denmark.
⁷³ Stanford University, Stanford CA, USA.
⁷⁴ University of Pennsylvania Perelman School of Medicine Department of Psychiatry.
⁷⁵ Department of Anthropology, Baylor University, Waco, TX, USA.
⁷⁶ Maastricht and Lifestyle Medicine Center for Children, Jeroen Bosch Hospital 's-Hertogenbosch, Maastricht University, Maastricht, The Netherlands.
⁷⁷ Population, Policy and Practice Research and Teaching Department, UCL Great Ormond Street Institute of Child Health, London, UK.
⁷⁸ University of California Los Angeles, Los Angeles, USA.
⁷⁹ Department of Human Behavior, Ecology, and Culture, Max Planck Institute for Evolutionary Anthropology.
⁸⁰ National Institute of Health and Nutrition, National Institutes of Biomedical Innovation, Health and Nutrition, Tokyo, Japan.
⁸¹ Center for Energy Metabolism and Reproduction, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen, People's Republic of China.
⁸² China medical University, Shenyang, Liaoning, People's Republic of China.
⁸³ CAS Center of Excellence in Animal Evolution and Genetics, Kunming, People's Republic of China.
⁸⁴ Nutritional and Health Related Environmental Studies Section, Division of Human Health, International Atomic Energy Agency, Vienna, Austria.
⁸⁵ Division of Epidemiology, Department of Public Health Sciences, Loyola University School of Medicine, Maywood IL, USA.
⁸⁶ Department of Evolutionary Anthropology, Duke University, Durham, NC, USA.
⁸⁷ Duke Global Health Institute, Duke University, Durham, NC, USA.
⁸⁸ Faculty of Health and Sport Sciences, University of Tsukuba, Ibaraki, Japan.

PMID: 37727077
PMCID: PMC10509569
DOI: 10.1098/rsbl.2023.0152

Erratum in

Correction: 'Greater male variability in daily energy expenditure develops through puberty' (2023), by Halsey et al.
Biology Letters. Biology Letters. Biol Lett. 2023 Nov;19(11):20230482. doi: 10.1098/rsbl.2023.0482. Epub 2023 Nov 1. Biol Lett. 2023. PMID: 37909701 Free PMC article. No abstract available.

Abstract

There is considerably greater variation in metabolic rates between men than between women, in terms of basal, activity and total (daily) energy expenditure (EE). One possible explanation is that EE is associated with male sexual characteristics (which are known to vary more than other traits) such as musculature and athletic capacity. Such traits might be predicted to be most prominent during periods of adolescence and young adulthood, when sexual behaviour develops and peaks. We tested this hypothesis on a large dataset by comparing the amount of male variation and female variation in total EE, activity EE and basal EE, at different life stages, along with several morphological traits: height, fat free mass and fat mass. Total EE, and to some degree also activity EE, exhibit considerable greater male variation (GMV) in young adults, and then a decreasing GMV in progressively older individuals. Arguably, basal EE, and also morphometrics, do not exhibit this pattern. These findings suggest that single male sexual characteristics may not exhibit peak GMV in young adulthood, however total and perhaps also activity EE, associated with many morphological and physiological traits combined, do exhibit GMV most prominently during the reproductive life stages.

Keywords: age; height; inter-individual variation; morphometry; weight.

PubMed Disclaimer

Conflict of interest statement

We declare we have no competing interests.

Figures

**Figure 1.**
Top row: male (blue triangles) and female (red circles) coefficients of variance (CoV) in measures of energy expenditure and body morphometrics as a function of age category. Error bars represent 95% credible intervals (95% CI). These data are presented in electronic supplementary material, table S1. Bottom row: the ratio of male to female (M/F) CoV with 95% CI. The dashed lines represent equal variance; values above indicate greater male variance (GMV). TEE = total energy expenditure; AEE = activity energy expenditure; BEE = basal energy expenditure.

See this image and copyright information in PMC

References

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Greater male variability in daily energy expenditure develops through puberty

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Greater male variability in daily energy expenditure develops through puberty

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Erratum in

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Conflict of interest statement

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