Skip to main content
Top

Open Access 08-06-2024 | Obesity | Original Article

Children with obesity have poorer circadian health as assessed by a global circadian health score

Authors: María Rodríguez-Martín, Nuria Martínez-Lozano, Vicente Santaclara-Maneiro, Antonio Gris-Peñas, Diego Salmerón, Rafael Ríos, Asta Tvarijonaviciute, Marta Garaulet

Published in: World Journal of Pediatrics

Login to get access

Abstract

Background

Circadian health refers to individuals’ well-being and balance in terms of their circadian rhythm. It is influenced by external cues. In adults, a close relationship between circadian-related alterations and obesity has been described. However, studies in children are scarce, and circadian health and its association with obesity have not been evaluated globally. We aimed to assess whether circadian health differed between children with and without obesity as determined by a global circadian score (GCS) in a school-age population.

Methods

Four hundred and thirty-two children (7–12 years) were recruited in Spain. Non-invasive tools were used to calculate the GCS: (1) 7-day rhythm of wrist temperature (T), activity (A), position (P), an integrative variable that combines T, A, and P (TAP); (2) cortisol; and (3) 7-day food and sleep records. Body mass index, body fat percentage, waist circumference (WC), melatonin concentration, and cardiometabolic marker levels were determined.

Results

Circadian health, as assessed by the GCS, differed among children with obesity, overweight, and normal weight, with poorer circadian health among children with obesity. Children with obesity and abdominal obesity had 3.54 and 2.39 greater odds of having poor circadian health, respectively, than did those with normal weight or low WC. The percentage of rhythmicity, a marker of the robustness of the TAP rhythm, and the amplitude, both components of the GCS, decreased with increasing obesity. Different lifestyle behaviors were involved in the association between circadian health and obesity, particularly protein intake (P = 0.024), physical activity level (P = 0.076) and chronotype (P = 0.029).

Conclusions

The GCS can capture the relationship between circadian health and obesity in school-age children. Protein intake, physical activity level, and chronotype were involved in this association. Early intervention based on improving circadian health may help to prevent childhood obesity.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kostovski M, Tasic V, Laban N, Polenakovic M, Danilovski D, Gucev Z. Obesity in childhood and adolescence, genetic factors. Pril (Makedon Akad Nauk Umet Odd Med Nauki). 2017;38:121–33.PubMed Kostovski M, Tasic V, Laban N, Polenakovic M, Danilovski D, Gucev Z. Obesity in childhood and adolescence, genetic factors. Pril (Makedon Akad Nauk Umet Odd Med Nauki). 2017;38:121–33.PubMed
2.
go back to reference Simmonds M, Llewellyn A, Owen CG, Woolacott N. Predicting adult obesity from childhood obesity: a systematic review and meta-analysis. Obes Rev. 2016;17:95–107.PubMedCrossRef Simmonds M, Llewellyn A, Owen CG, Woolacott N. Predicting adult obesity from childhood obesity: a systematic review and meta-analysis. Obes Rev. 2016;17:95–107.PubMedCrossRef
3.
go back to reference Ryder JR, Fox CK, Kelly AS. Treatment options for severe obesity in the pediatric population: current limitations and future opportunities. Obesity (Silver Spring). 2018;26:951–60.PubMedCrossRef Ryder JR, Fox CK, Kelly AS. Treatment options for severe obesity in the pediatric population: current limitations and future opportunities. Obesity (Silver Spring). 2018;26:951–60.PubMedCrossRef
4.
go back to reference Laermans J, Depoortere I. Chronobesity: role of the circadian system in the obesity epidemic. Obes Rev. 2016;17:108–25.PubMedCrossRef Laermans J, Depoortere I. Chronobesity: role of the circadian system in the obesity epidemic. Obes Rev. 2016;17:108–25.PubMedCrossRef
5.
go back to reference Broussard JL, Van Cauter E. Disturbances of sleep and circadian rhythms: novel risk factors for obesity. Curr Opin Endocrinol Diabetes Obes. 2016;23:353–9.PubMedPubMedCentralCrossRef Broussard JL, Van Cauter E. Disturbances of sleep and circadian rhythms: novel risk factors for obesity. Curr Opin Endocrinol Diabetes Obes. 2016;23:353–9.PubMedPubMedCentralCrossRef
6.
go back to reference Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol. 2010;72:517–49.PubMedCrossRef Dibner C, Schibler U, Albrecht U. The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu Rev Physiol. 2010;72:517–49.PubMedCrossRef
7.
go back to reference Klerman EB, Brager A, Carskadon MA, Depner CM, Foster R, Goel N, et al. Keeping an eye on circadian time in clinical research and medicine. Clin Transl Med. 2022;12:e1131.PubMedPubMedCentralCrossRef Klerman EB, Brager A, Carskadon MA, Depner CM, Foster R, Goel N, et al. Keeping an eye on circadian time in clinical research and medicine. Clin Transl Med. 2022;12:e1131.PubMedPubMedCentralCrossRef
8.
go back to reference Pereira LR, Moreira FP, Reyes AN, Bach SL, Amaral PLD, Motta JDS, et al. Biological rhythm disruption associated with obesity in school children. Child Obes. 2019;15:200–5.PubMedCrossRef Pereira LR, Moreira FP, Reyes AN, Bach SL, Amaral PLD, Motta JDS, et al. Biological rhythm disruption associated with obesity in school children. Child Obes. 2019;15:200–5.PubMedCrossRef
9.
go back to reference Zhou M, Lalani C, Banda JA, Robinson TN. Sleep duration, timing, variability and measures of adiposity among 8- to 12-year-old children with obesity. Obes Sci Pract. 2018;4:535–44.PubMedPubMedCentralCrossRef Zhou M, Lalani C, Banda JA, Robinson TN. Sleep duration, timing, variability and measures of adiposity among 8- to 12-year-old children with obesity. Obes Sci Pract. 2018;4:535–44.PubMedPubMedCentralCrossRef
10.
go back to reference Martinez-Lozano N, Tvarijonaviciute A, Rios R, Baron I, Scheer F, Garaulet M. Late eating is associated with obesity, inflammatory markers and circadian-related disturbances in school-aged children. Nutrients. 2020;12:2881.PubMedPubMedCentralCrossRef Martinez-Lozano N, Tvarijonaviciute A, Rios R, Baron I, Scheer F, Garaulet M. Late eating is associated with obesity, inflammatory markers and circadian-related disturbances in school-aged children. Nutrients. 2020;12:2881.PubMedPubMedCentralCrossRef
11.
go back to reference Barraco GM, Martinez-Lozano N, Vales-Villamarin C, Del Carmen BM, Rios R, Madrid JA, et al. Circadian health differs between boys and girls as assessed by non-invasive tools in school-aged children. Clin Nutr. 2019;38:774–81.PubMedCrossRef Barraco GM, Martinez-Lozano N, Vales-Villamarin C, Del Carmen BM, Rios R, Madrid JA, et al. Circadian health differs between boys and girls as assessed by non-invasive tools in school-aged children. Clin Nutr. 2019;38:774–81.PubMedCrossRef
12.
go back to reference Krauchi K, Cajochen C, Werth E, Wirz-Justice A. Functional link between distal vasodilation and sleep-onset latency? Am J Physiol Regul Integr Comp Physiol. 2000;278:R741–8.PubMedCrossRef Krauchi K, Cajochen C, Werth E, Wirz-Justice A. Functional link between distal vasodilation and sleep-onset latency? Am J Physiol Regul Integr Comp Physiol. 2000;278:R741–8.PubMedCrossRef
13.
go back to reference Martoni M, Carissimi A, Fabbri M, Filardi M, Tonetti L, Natale V. 24-h actigraphic monitoring of motor activity, sleeping and eating behaviors in underweight, normal weight, overweight and obese children. Eat Weight Disord. 2016;21:669–77.PubMedCrossRef Martoni M, Carissimi A, Fabbri M, Filardi M, Tonetti L, Natale V. 24-h actigraphic monitoring of motor activity, sleeping and eating behaviors in underweight, normal weight, overweight and obese children. Eat Weight Disord. 2016;21:669–77.PubMedCrossRef
14.
go back to reference Ortiz-Tudela E, Martinez-Nicolas A, Campos M, Rol MA, Madrid JA. A new integrated variable based on thermometry, actimetry and body position (TAP) to evaluate circadian system status in humans. PLoS Comput Biol. 2010;6:e1000996.PubMedPubMedCentralCrossRef Ortiz-Tudela E, Martinez-Nicolas A, Campos M, Rol MA, Madrid JA. A new integrated variable based on thermometry, actimetry and body position (TAP) to evaluate circadian system status in humans. PLoS Comput Biol. 2010;6:e1000996.PubMedPubMedCentralCrossRef
15.
go back to reference Garaulet M, Madrid JA. Methods for monitoring the functional status of the circadian system in dietary surveys studies: application criteria and interpretation of results. Nutr Hosp. 2015;31(Suppl 3):279–89.PubMed Garaulet M, Madrid JA. Methods for monitoring the functional status of the circadian system in dietary surveys studies: application criteria and interpretation of results. Nutr Hosp. 2015;31(Suppl 3):279–89.PubMed
16.
go back to reference Tvarijonaviciute A, Martinez-Lozano N, Rios R, Marcilla de Teruel MC, Garaulet M, Ceron JJ. Saliva as a non-invasive tool for assessment of metabolic and inflammatory biomarkers in children. Clin Nutr. 2020;39:2471–8.PubMedCrossRef Tvarijonaviciute A, Martinez-Lozano N, Rios R, Marcilla de Teruel MC, Garaulet M, Ceron JJ. Saliva as a non-invasive tool for assessment of metabolic and inflammatory biomarkers in children. Clin Nutr. 2020;39:2471–8.PubMedCrossRef
17.
go back to reference Martinez-Lozano N, Barraco GM, Rios R, Ruiz MJ, Tvarijonaviciute A, Fardy P, et al. Evening types have social jet lag and metabolic alterations in school-age children. Sci Rep. 2020;10:16747.PubMedPubMedCentralCrossRef Martinez-Lozano N, Barraco GM, Rios R, Ruiz MJ, Tvarijonaviciute A, Fardy P, et al. Evening types have social jet lag and metabolic alterations in school-age children. Sci Rep. 2020;10:16747.PubMedPubMedCentralCrossRef
18.
go back to reference Qian J, Martinez-Lozano N, Tvarijonaviciute A, Rios R, Scheer F, Garaulet M. Blunted rest-activity rhythms link to higher body mass index and inflammatory markers in children. Sleep. 2021;44:zsaa256.PubMedCrossRef Qian J, Martinez-Lozano N, Tvarijonaviciute A, Rios R, Scheer F, Garaulet M. Blunted rest-activity rhythms link to higher body mass index and inflammatory markers in children. Sleep. 2021;44:zsaa256.PubMedCrossRef
19.
go back to reference de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85:660–7.PubMedPubMedCentralCrossRef de Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull World Health Organ. 2007;85:660–7.PubMedPubMedCentralCrossRef
20.
go back to reference Sarabia JA, Rol MA, Mendiola P, Madrid JA. Circadian rhythm of wrist temperature in normal-living subjects A candidate of new index of the circadian system. Physiol Behav. 2008;95:570–80.PubMedCrossRef Sarabia JA, Rol MA, Mendiola P, Madrid JA. Circadian rhythm of wrist temperature in normal-living subjects A candidate of new index of the circadian system. Physiol Behav. 2008;95:570–80.PubMedCrossRef
21.
go back to reference Naismith SL, Rogers NL, Mackenzie J, Hickie IB, Lewis SJ. The relationship between actigraphically defined sleep disturbance and REM sleep behaviour disorder in Parkinson’s Disease. Clin Neurol Neurosurg. 2010;112:420–3.PubMedCrossRef Naismith SL, Rogers NL, Mackenzie J, Hickie IB, Lewis SJ. The relationship between actigraphically defined sleep disturbance and REM sleep behaviour disorder in Parkinson’s Disease. Clin Neurol Neurosurg. 2010;112:420–3.PubMedCrossRef
22.
go back to reference Roenneberg T, Kuehnle T, Juda M, Kantermann T, Allebrandt K, Gordijn M, et al. Epidemiology of the human circadian clock. Sleep Med Rev. 2007;11:429–38.PubMedCrossRef Roenneberg T, Kuehnle T, Juda M, Kantermann T, Allebrandt K, Gordijn M, et al. Epidemiology of the human circadian clock. Sleep Med Rev. 2007;11:429–38.PubMedCrossRef
23.
go back to reference Roenneberg T, Pilz LK, Zerbini G, Winnebeck EC. Chronotype and social jetlag: a (self-) critical review. Biology (Basel). 2019;8:54.PubMed Roenneberg T, Pilz LK, Zerbini G, Winnebeck EC. Chronotype and social jetlag: a (self-) critical review. Biology (Basel). 2019;8:54.PubMed
24.
go back to reference Azevedo CSI, Paul K, MacLeish M, Mondejar M, Sarabia J, et al. Teaching chronobiology and sleep habits in school and university. Mind Brain Educ. 2008;2:34–47.CrossRef Azevedo CSI, Paul K, MacLeish M, Mondejar M, Sarabia J, et al. Teaching chronobiology and sleep habits in school and university. Mind Brain Educ. 2008;2:34–47.CrossRef
25.
go back to reference Perez-Llamas F, Garaulet M, Torralba C, Zamora S. Development of a current version of a software application for research and practice in human nutrition (GRUNUMUR 2.0). Nutr Hosp. 2012;27:1576–82 (in Spanish).PubMed Perez-Llamas F, Garaulet M, Torralba C, Zamora S. Development of a current version of a software application for research and practice in human nutrition (GRUNUMUR 2.0). Nutr Hosp. 2012;27:1576–82 (in Spanish).PubMed
26.
go back to reference Moreiras O, Carvajal A, Cabrera, L. Table of composition of Spanish foods. Madrid, Spain: Pirámide; 1995 (in Spanish). Moreiras O, Carvajal A, Cabrera, L. Table of composition of Spanish foods. Madrid, Spain: Pirámide; 1995 (in Spanish).
27.
go back to reference Bonmati-Carrion MA, Middleton B, Revell VL, Skene DJ, Rol MA, Madrid JA. Validation of an innovative method, based on tilt sensing, for the assessment of activity and body position. Chronobiol Int. 2015;32:701–10.PubMedCrossRef Bonmati-Carrion MA, Middleton B, Revell VL, Skene DJ, Rol MA, Madrid JA. Validation of an innovative method, based on tilt sensing, for the assessment of activity and body position. Chronobiol Int. 2015;32:701–10.PubMedCrossRef
28.
go back to reference Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ. 2000;320:1240–3.PubMedPubMedCentralCrossRef Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ. 2000;320:1240–3.PubMedPubMedCentralCrossRef
29.
go back to reference Martinez-Nicolas A, Martinez-Madrid MJ, Almaida-Pagan PF, Bonmati-Carrion MA, Madrid JA, Rol MA. Assessing chronotypes by ambulatory circadian monitoring. Front Physiol. 2019;10:1396.PubMedPubMedCentralCrossRef Martinez-Nicolas A, Martinez-Madrid MJ, Almaida-Pagan PF, Bonmati-Carrion MA, Madrid JA, Rol MA. Assessing chronotypes by ambulatory circadian monitoring. Front Physiol. 2019;10:1396.PubMedPubMedCentralCrossRef
30.
go back to reference Calogiuri G, Weydahl A, Carandente F. Methodological issues for studying the rest-activity cycle and sleep disturbances: a chronobiological approach using actigraphy data. Biol Res Nurs. 2013;15:5–12.PubMedCrossRef Calogiuri G, Weydahl A, Carandente F. Methodological issues for studying the rest-activity cycle and sleep disturbances: a chronobiological approach using actigraphy data. Biol Res Nurs. 2013;15:5–12.PubMedCrossRef
32.
go back to reference Corbalan-Tutau MD, Madrid JA, Ordovas JM, Smith CE, Nicolas F, Garaulet M. Differences in daily rhythms of wrist temperature between obese and normal-weight women: associations with metabolic syndrome features. Chronobiol Int. 2011;28:425–33.PubMedPubMedCentralCrossRef Corbalan-Tutau MD, Madrid JA, Ordovas JM, Smith CE, Nicolas F, Garaulet M. Differences in daily rhythms of wrist temperature between obese and normal-weight women: associations with metabolic syndrome features. Chronobiol Int. 2011;28:425–33.PubMedPubMedCentralCrossRef
33.
go back to reference Quante M, Cespedes Feliciano EM, Rifas-Shiman SL, Mariani S, Kaplan ER, Rueschman M, et al. Association of daily rest-activity patterns with adiposity and cardiometabolic risk measures in teens. J Adolesc Health. 2019;65:224–31.PubMedPubMedCentralCrossRef Quante M, Cespedes Feliciano EM, Rifas-Shiman SL, Mariani S, Kaplan ER, Rueschman M, et al. Association of daily rest-activity patterns with adiposity and cardiometabolic risk measures in teens. J Adolesc Health. 2019;65:224–31.PubMedPubMedCentralCrossRef
34.
go back to reference Hoopes EK, Witman MA, D’Agata MN, Berube FR, Brewer B, Malone SK, et al. Rest-activity rhythms in emerging adults: implications for cardiometabolic health. Chronobiol Int. 2021;38:543–56.PubMedPubMedCentralCrossRef Hoopes EK, Witman MA, D’Agata MN, Berube FR, Brewer B, Malone SK, et al. Rest-activity rhythms in emerging adults: implications for cardiometabolic health. Chronobiol Int. 2021;38:543–56.PubMedPubMedCentralCrossRef
35.
go back to reference Sohail S, Yu L, Bennett DA, Buchman AS, Lim AS. Irregular 24-hour activity rhythms and the metabolic syndrome in older adults. Chronobiol Int. 2015;32:802–13.PubMedPubMedCentralCrossRef Sohail S, Yu L, Bennett DA, Buchman AS, Lim AS. Irregular 24-hour activity rhythms and the metabolic syndrome in older adults. Chronobiol Int. 2015;32:802–13.PubMedPubMedCentralCrossRef
36.
go back to reference Corbalan-Tutau MD, Gomez-Abellan P, Madrid JA, Canteras M, Ordovas JM, Garaulet M. Toward a chronobiological characterization of obesity and metabolic syndrome in clinical practice. Clin Nutr. 2015;34:477–83.PubMedCrossRef Corbalan-Tutau MD, Gomez-Abellan P, Madrid JA, Canteras M, Ordovas JM, Garaulet M. Toward a chronobiological characterization of obesity and metabolic syndrome in clinical practice. Clin Nutr. 2015;34:477–83.PubMedCrossRef
37.
go back to reference Garaulet M, Gomez-Abellan P. Chronobiology and obesity. Nutr Hosp. 2013;28(Suppl 5):114–20.PubMed Garaulet M, Gomez-Abellan P. Chronobiology and obesity. Nutr Hosp. 2013;28(Suppl 5):114–20.PubMed
38.
go back to reference Gomez-Abellan P, Madrid JA, Ordovas JM, Garaulet M. Chronobiological aspects of obesity and metabolic syndrome. Endocrinol Nutr. 2012;59:50–61 (in Spanish).PubMedCrossRef Gomez-Abellan P, Madrid JA, Ordovas JM, Garaulet M. Chronobiological aspects of obesity and metabolic syndrome. Endocrinol Nutr. 2012;59:50–61 (in Spanish).PubMedCrossRef
39.
go back to reference Szajewska H, Ruszczynski M. Systematic review demonstrating that breakfast consumption influences body weight outcomes in children and adolescents in Europe. Crit Rev Food Sci Nutr. 2010;50:113–9.PubMedCrossRef Szajewska H, Ruszczynski M. Systematic review demonstrating that breakfast consumption influences body weight outcomes in children and adolescents in Europe. Crit Rev Food Sci Nutr. 2010;50:113–9.PubMedCrossRef
40.
go back to reference Arnesen EK, Thorisdottir B, Lamberg-Allardt C, Barebring L, Nwaru B, Dierkes J, et al. Protein intake in children and growth and risk of overweight or obesity: a systematic review and meta-analysis. Food Nutr Res. 2022;66:8242.CrossRef Arnesen EK, Thorisdottir B, Lamberg-Allardt C, Barebring L, Nwaru B, Dierkes J, et al. Protein intake in children and growth and risk of overweight or obesity: a systematic review and meta-analysis. Food Nutr Res. 2022;66:8242.CrossRef
41.
go back to reference Wyszynska J, Ring-Dimitriou S, Thivel D, Weghuber D, Hadjipanayis A, Grossman Z, et al. Physical activity in the prevention of childhood obesity: the position of the European Childhood Obesity Group and the European Academy of Pediatrics. Front Pediatr. 2020;8:535705.PubMedPubMedCentralCrossRef Wyszynska J, Ring-Dimitriou S, Thivel D, Weghuber D, Hadjipanayis A, Grossman Z, et al. Physical activity in the prevention of childhood obesity: the position of the European Childhood Obesity Group and the European Academy of Pediatrics. Front Pediatr. 2020;8:535705.PubMedPubMedCentralCrossRef
42.
go back to reference Martinez-Nicolas A, Madrid JA, Rol MA. Day-night contrast as source of health for the human circadian system. Chronobiol Int. 2014;31:382–93.PubMedCrossRef Martinez-Nicolas A, Madrid JA, Rol MA. Day-night contrast as source of health for the human circadian system. Chronobiol Int. 2014;31:382–93.PubMedCrossRef
43.
go back to reference Akacem LD, Wright KP Jr, LeBourgeois MK. Bedtime and evening light exposure influence circadian timing in preschool-age children: a field study. Neurobiol Sleep Circadian Rhythms. 2016;1:27–31.PubMedPubMedCentralCrossRef Akacem LD, Wright KP Jr, LeBourgeois MK. Bedtime and evening light exposure influence circadian timing in preschool-age children: a field study. Neurobiol Sleep Circadian Rhythms. 2016;1:27–31.PubMedPubMedCentralCrossRef
44.
go back to reference Reiter RJ, Tan DX, Korkmaz A, Ma S. Obesity and metabolic syndrome: association with chronodisruption, sleep deprivation, and melatonin suppression. Ann Med. 2012;44:564–77.PubMedCrossRef Reiter RJ, Tan DX, Korkmaz A, Ma S. Obesity and metabolic syndrome: association with chronodisruption, sleep deprivation, and melatonin suppression. Ann Med. 2012;44:564–77.PubMedCrossRef
Metadata
Title
Children with obesity have poorer circadian health as assessed by a global circadian health score
Authors
María Rodríguez-Martín
Nuria Martínez-Lozano
Vicente Santaclara-Maneiro
Antonio Gris-Peñas
Diego Salmerón
Rafael Ríos
Asta Tvarijonaviciute
Marta Garaulet
Publication date
08-06-2024
Publisher
Springer Nature Singapore
Keywords
Obesity
Obesity
Published in
World Journal of Pediatrics
Print ISSN: 1708-8569
Electronic ISSN: 1867-0687
DOI
https://doi.org/10.1007/s12519-024-00804-3