Skip to main content
Top
Published in: BMC Public Health 1/2024

Open Access 01-12-2024 | Research

Cross-sectional and longitudinal associations between the 24-hour movement behaviours, including muscle and bone strengthening activity, with bone and lean mass from childhood to adolescence

Authors: Annie M. Skinner, Alan R. Barker, Sarah A. Moore, Sonja Soininen, Eero A. Haapala, Juuso Väistö, Kate Westgate, Soren Brage, Timo A. Lakka, Dimitris Vlachopoulos

Published in: BMC Public Health | Issue 1/2024

Login to get access

Abstract

Background

This study aimed to assess whether moderate-to-vigorous physical activity (MVPA), sport and exercise as a proxy measure of muscle and bone strengthening activity, sedentary behaviour, and sleep were associated with total-body-less-head (TBLH) bone mineral content (BMC) and TBLH lean mass cross-sectionally and longitudinally from age 6 to 9 years and age 9 to 11 years to age 15 to 17 years.

Methods

We used longitudinal data from a population sample of Finnish children from the Physical Activity and Nutrition in Children study (age 6 to 9 years: n = 478, 229 females; age 9 to 11 years: n = 384, 197 females; age 15 to 17 years: n = 222, 103 females). Linear regression analysed the cross-sectional and longitudinal associations between accelerometer-assessed MVPA, sedentary time and sleep, and questionnaire-assessed sport and exercise participation and screen time with dual-energy X-ray absorptiometry-assessed TBLH BMC and lean mass.

Results

In females, MVPA at age 6 to 9 years was positively associated with TBLH BMC at age 15 to 17 years (β = 0.008, p = 0.010). Sport and exercise at age 9 to 11 years was positively associated with TBLH BMC (β = 0.020, p = 0.002) and lean mass (β = 0.343, p = 0.040) at age 15 to 17 years. MVPA at age 9 to 11 years was positively associated with TBLH lean mass (β = 0.272, p = 0.004) at age 15 to 17 years. In males, sleep at age 6 to 9 years was positively associated with TBLH lean mass (β = 0.382, p = 0.003) at age 15 to 17 years. Sport and exercise at age 9 to 11 years was positively associated with TBLH BMC (β = 0.027, p = 0.012) and lean mass (β = 0.721, p < 0.001) at age 15 to 17 years.

Conclusions

Promoting engagement in the 24-hour movement behaviours in childhood, particularly sport and exercise to strengthen muscle and bone, is important in supporting bone and lean mass development in adolescence.

Trial registration

NCT01803776; first trial registration date: 04/03/2013.
Literature
1.
go back to reference Baxter-Jones AD, Kontulainen SA, Faulkner RA, Bailey DA. A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone. 2008;43(6):1101–7.PubMedCrossRef Baxter-Jones AD, Kontulainen SA, Faulkner RA, Bailey DA. A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone. 2008;43(6):1101–7.PubMedCrossRef
2.
go back to reference Janz KF, Letuchy EM, Eichenberger Gilmore JM, Burns TL, Torner JC, Willing MC, et al. Early physical activity provides sustained bone health benefits later in childhood. Med Sci Sports Exerc. 2010;42(6):1072–8.PubMedPubMedCentralCrossRef Janz KF, Letuchy EM, Eichenberger Gilmore JM, Burns TL, Torner JC, Willing MC, et al. Early physical activity provides sustained bone health benefits later in childhood. Med Sci Sports Exerc. 2010;42(6):1072–8.PubMedPubMedCentralCrossRef
3.
go back to reference Elhakeem A, Heron J, Tobias JH, Lawlor DA. Physical Activity Throughout Adolescence and Peak Hip Strength in Young Adults. JAMA Netw Open. 2020;3(8): e2013463.PubMedPubMedCentralCrossRef Elhakeem A, Heron J, Tobias JH, Lawlor DA. Physical Activity Throughout Adolescence and Peak Hip Strength in Young Adults. JAMA Netw Open. 2020;3(8): e2013463.PubMedPubMedCentralCrossRef
4.
go back to reference Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res. 2011;26(8):1729–39.PubMedCrossRef Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res. 2011;26(8):1729–39.PubMedCrossRef
5.
go back to reference Schoenau E, Frost H. The" muscle-bone unit" in children and adolescents. Calcif Tissue Int. 2002;70(5):405–7.PubMedCrossRef Schoenau E, Frost H. The" muscle-bone unit" in children and adolescents. Calcif Tissue Int. 2002;70(5):405–7.PubMedCrossRef
6.
go back to reference Baxter-Jones ADG, Mirwald RL, McKay HA, Bailey DA. A longitudinal analysis of sex differences in bone mineral accrual in healthy 8–19-year-old boys and girls. Ann Hum Biol. 2003;30(2):160–75.PubMedCrossRef Baxter-Jones ADG, Mirwald RL, McKay HA, Bailey DA. A longitudinal analysis of sex differences in bone mineral accrual in healthy 8–19-year-old boys and girls. Ann Hum Biol. 2003;30(2):160–75.PubMedCrossRef
7.
go back to reference Iuliano-Burns S, Mirwald RL, Bailey DA. Timing and magnitude of peak height velocity and peak tissue velocities for early, average, and late maturing boys and girls. Am J Hum Biol. 2001;13(1):1–8.PubMedCrossRef Iuliano-Burns S, Mirwald RL, Bailey DA. Timing and magnitude of peak height velocity and peak tissue velocities for early, average, and late maturing boys and girls. Am J Hum Biol. 2001;13(1):1–8.PubMedCrossRef
8.
go back to reference Sioen I, Lust E, De Henauw S, Moreno LA, Jimenez-Pavon D. Associations between body composition and bone health in children and adolescents: a systematic review. Calcif Tissue Int. 2016;99(6):557–77.PubMedCrossRef Sioen I, Lust E, De Henauw S, Moreno LA, Jimenez-Pavon D. Associations between body composition and bone health in children and adolescents: a systematic review. Calcif Tissue Int. 2016;99(6):557–77.PubMedCrossRef
9.
go back to reference Tremblay MS, Carson V, Chaput J-P, Gorber SC, Dinh T, Duggan M, et al. Canadian 24-Hour Movement Guidelines for Children and Youth: An Integration of Physical Activity, Sedentary Behaviour, and Sleep. Appl Physiol Nutr Metab. 2016;41(6 (Suppl. 3)):S311-S27. Tremblay MS, Carson V, Chaput J-P, Gorber SC, Dinh T, Duggan M, et al. Canadian 24-Hour Movement Guidelines for Children and Youth: An Integration of Physical Activity, Sedentary Behaviour, and Sleep. Appl Physiol Nutr Metab. 2016;41(6 (Suppl. 3)):S311-S27.
10.
go back to reference Tremblay MS, Carson V, Chaput JP. Introduction to the Canadian 24-hour movement guidelines for children and youth: an integration of physical activity, sedentary behaviour, and sleep. Appl Physiol Nutr Metab. 2016;41(6 Suppl 3):iii–iv.PubMedCrossRef Tremblay MS, Carson V, Chaput JP. Introduction to the Canadian 24-hour movement guidelines for children and youth: an integration of physical activity, sedentary behaviour, and sleep. Appl Physiol Nutr Metab. 2016;41(6 Suppl 3):iii–iv.PubMedCrossRef
11.
go back to reference Okely AD, Ghersi D, Loughran SP, Cliff DP, Shilton T, Jones RA, et al. A collaborative approach to adopting/adapting guidelines. The Australian 24-hour movement guidelines for children (5-12 years) and young people (13-17 years): An integration of physical activity, sedentary behaviour, and sleep. Int J Behav Nutr Phys Activity. 2022;19(1):2. Okely AD, Ghersi D, Loughran SP, Cliff DP, Shilton T, Jones RA, et al. A collaborative approach to adopting/adapting guidelines. The Australian 24-hour movement guidelines for children (5-12 years) and young people (13-17 years): An integration of physical activity, sedentary behaviour, and sleep. Int J Behav Nutr Phys Activity. 2022;19(1):2.
12.
go back to reference Chaput J-P, Willumsen J, Bull F, Chou R, Ekelund U, Firth J, et al. 2020 WHO guidelines on physical activity and sedentary behaviour for children and adolescents aged 5–17 years: summary of the evidence. Int J Behav Nutr Phys Act. 2020;17(1):141.PubMedPubMedCentralCrossRef Chaput J-P, Willumsen J, Bull F, Chou R, Ekelund U, Firth J, et al. 2020 WHO guidelines on physical activity and sedentary behaviour for children and adolescents aged 5–17 years: summary of the evidence. Int J Behav Nutr Phys Act. 2020;17(1):141.PubMedPubMedCentralCrossRef
13.
go back to reference Moore SA, Cumming SP, Balletta G, Ramage K, Eisenmann JC, Baxter-Jones ADG, et al. Exploring the relationship between adolescent biological maturation, physical activity, and sedentary behaviour: a systematic review and narrative synthesis. Ann Hum Biol. 2020;47(4):365–83.PubMedCrossRef Moore SA, Cumming SP, Balletta G, Ramage K, Eisenmann JC, Baxter-Jones ADG, et al. Exploring the relationship between adolescent biological maturation, physical activity, and sedentary behaviour: a systematic review and narrative synthesis. Ann Hum Biol. 2020;47(4):365–83.PubMedCrossRef
14.
go back to reference Zymbal V, Baptista F, Letuchy EM, Janz KF, Levy SM. Mediating effect of muscle on the relationship of physical activity and bone. Med Sci Sports Exerc. 2019;51(1):202–10.PubMedPubMedCentralCrossRef Zymbal V, Baptista F, Letuchy EM, Janz KF, Levy SM. Mediating effect of muscle on the relationship of physical activity and bone. Med Sci Sports Exerc. 2019;51(1):202–10.PubMedPubMedCentralCrossRef
15.
go back to reference Piercy KL, Troiano RP, Ballard RM, Carlson SA, Fulton JE, Galuska DA, et al. The physical activity guidelines for Americans. JAMA. 2018;320(19):2020–8.PubMedPubMedCentralCrossRef Piercy KL, Troiano RP, Ballard RM, Carlson SA, Fulton JE, Galuska DA, et al. The physical activity guidelines for Americans. JAMA. 2018;320(19):2020–8.PubMedPubMedCentralCrossRef
16.
go back to reference Department of Health and Social Care. UK Chief Medical Officers’ Physical Activity Guidelines. 2019. Department of Health and Social Care. UK Chief Medical Officers’ Physical Activity Guidelines. 2019.
17.
go back to reference Faigenbaum AD, MacDonald JP, Stracciolini A, Rebullido TR. Making a Strong Case for Prioritizing Muscular Fitness in Youth Physical Activity Guidelines. Curr Sports Med Rep. 2020;19(12). Faigenbaum AD, MacDonald JP, Stracciolini A, Rebullido TR. Making a Strong Case for Prioritizing Muscular Fitness in Youth Physical Activity Guidelines. Curr Sports Med Rep. 2020;19(12).
18.
go back to reference Strain T, Milton K, Dall P, Standage M, Mutrie N. How are we measuring physical activity and sedentary behaviour in the four home nations of the UK? A narrative review of current surveillance measures and future directions. Br J Sports Med. 2020;54(21):1269–76.PubMedCrossRef Strain T, Milton K, Dall P, Standage M, Mutrie N. How are we measuring physical activity and sedentary behaviour in the four home nations of the UK? A narrative review of current surveillance measures and future directions. Br J Sports Med. 2020;54(21):1269–76.PubMedCrossRef
19.
go back to reference Gunter KB, Almstedt HC, Janz KF. Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev. 2012;40(1):13–21.PubMedPubMedCentralCrossRef Gunter KB, Almstedt HC, Janz KF. Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev. 2012;40(1):13–21.PubMedPubMedCentralCrossRef
20.
go back to reference Public Health England. Muscle and bone strengthening activities for children and young people (5 to 18 years): a rapid evidence review. 2021. Public Health England. Muscle and bone strengthening activities for children and young people (5 to 18 years): a rapid evidence review. 2021.
21.
go back to reference Sport England. Active Lives Children and Young People Survey - Academic year 2021-22. 2022. Sport England. Active Lives Children and Young People Survey - Academic year 2021-22. 2022.
22.
go back to reference Pereira JR, Cliff DP, Sousa-Sa E, Zhang Z, Santos R. Prevalence of objectively measured sedentary behavior in early years: Systematic review and meta-analysis. Scand J Med Sci Sports. 2019;29(3):308–28.PubMedCrossRef Pereira JR, Cliff DP, Sousa-Sa E, Zhang Z, Santos R. Prevalence of objectively measured sedentary behavior in early years: Systematic review and meta-analysis. Scand J Med Sci Sports. 2019;29(3):308–28.PubMedCrossRef
23.
go back to reference Koedijk J, van Rijswijk J, Oranje W, van den Bergh J, Bours S, Savelberg H, et al. Sedentary behaviour and bone health in children, adolescents and young adults: a systematic review. Osteoporos Int. 2017;28(9):2507–19.PubMedPubMedCentralCrossRef Koedijk J, van Rijswijk J, Oranje W, van den Bergh J, Bours S, Savelberg H, et al. Sedentary behaviour and bone health in children, adolescents and young adults: a systematic review. Osteoporos Int. 2017;28(9):2507–19.PubMedPubMedCentralCrossRef
24.
go back to reference Fulton JE, Dai S, Steffen LM, Grunbaum JA, Shah SM, Labarthe DR. Physical Activity, Energy Intake, Sedentary Behavior, and Adiposity in Youth. Am J Prev Med. 2009;37(1, Supplement):S40-S9. Fulton JE, Dai S, Steffen LM, Grunbaum JA, Shah SM, Labarthe DR. Physical Activity, Energy Intake, Sedentary Behavior, and Adiposity in Youth. Am J Prev Med. 2009;37(1, Supplement):S40-S9.
25.
go back to reference Riso E-M, Kull M, Mooses K, Jürimäe J. Physical activity, sedentary time and sleep duration: associations with body composition in 10–12-year-old Estonian schoolchildren. BMC Public Health. 2018;18(1):496.PubMedPubMedCentralCrossRef Riso E-M, Kull M, Mooses K, Jürimäe J. Physical activity, sedentary time and sleep duration: associations with body composition in 10–12-year-old Estonian schoolchildren. BMC Public Health. 2018;18(1):496.PubMedPubMedCentralCrossRef
26.
go back to reference Swanson CM, Kohrt WM, Buxton OM, Everson CA, Wright KP, Orwoll ES, et al. The importance of the circadian system & sleep for bone health. Metabolism. 2018;84:28–43.PubMedCrossRef Swanson CM, Kohrt WM, Buxton OM, Everson CA, Wright KP, Orwoll ES, et al. The importance of the circadian system & sleep for bone health. Metabolism. 2018;84:28–43.PubMedCrossRef
27.
go back to reference Swanson CM, Blatchford PJ, Stone KL, Cauley JA, Lane NE, Rogers-Soeder TS, et al. Sleep duration and bone health measures in older men. Osteoporos Int. 2021;32(3):515–27.PubMedCrossRef Swanson CM, Blatchford PJ, Stone KL, Cauley JA, Lane NE, Rogers-Soeder TS, et al. Sleep duration and bone health measures in older men. Osteoporos Int. 2021;32(3):515–27.PubMedCrossRef
28.
go back to reference Cheng L, Pohlabeln H, Ahrens W, Russo P, Veidebaum T, Hadjigeorgiou C, et al. Cross-sectional and longitudinal associations between sleep duration, sleep quality, and bone stiffness in European children and adolescents. Osteoporos Int. 2021;32(5):853–63.PubMedCrossRef Cheng L, Pohlabeln H, Ahrens W, Russo P, Veidebaum T, Hadjigeorgiou C, et al. Cross-sectional and longitudinal associations between sleep duration, sleep quality, and bone stiffness in European children and adolescents. Osteoporos Int. 2021;32(5):853–63.PubMedCrossRef
29.
go back to reference Casazza K, Hanks LJ, Fernandez JR. Shorter sleep may be a risk factor for impaired bone mass accrual in childhood. J Clin Densitometry. 2011;14(4):453–7.CrossRef Casazza K, Hanks LJ, Fernandez JR. Shorter sleep may be a risk factor for impaired bone mass accrual in childhood. J Clin Densitometry. 2011;14(4):453–7.CrossRef
30.
go back to reference Buchmann N, Spira D, Norman K, Demuth I, Eckardt R, Steinhagen-Thiessen E. Sleep, muscle mass and muscle function in older people. Dtsch Arztebl Int. 2016;113(15):253–60.PubMedPubMedCentral Buchmann N, Spira D, Norman K, Demuth I, Eckardt R, Steinhagen-Thiessen E. Sleep, muscle mass and muscle function in older people. Dtsch Arztebl Int. 2016;113(15):253–60.PubMedPubMedCentral
31.
go back to reference Carter PJ, Taylor BJ, Williams SM, Taylor RW. Longitudinal analysis of sleep in relation to BMI and body fat in children: the FLAME study. BMJ. 2011;342:d2712.PubMedPubMedCentralCrossRef Carter PJ, Taylor BJ, Williams SM, Taylor RW. Longitudinal analysis of sleep in relation to BMI and body fat in children: the FLAME study. BMJ. 2011;342:d2712.PubMedPubMedCentralCrossRef
32.
go back to reference Baird J, Hill CM, Harvey NC, Crozier S, Robinson SM, Godfrey KM, et al. Duration of sleep at 3 years of age is associated with fat and fat-free mass at 4 years of age: the Southampton Women’s Survey. J Sleep Res. 2016;25(4):412–8.PubMedPubMedCentralCrossRef Baird J, Hill CM, Harvey NC, Crozier S, Robinson SM, Godfrey KM, et al. Duration of sleep at 3 years of age is associated with fat and fat-free mass at 4 years of age: the Southampton Women’s Survey. J Sleep Res. 2016;25(4):412–8.PubMedPubMedCentralCrossRef
33.
go back to reference Soininen S, Sidoroff V, Lindi V, Mahonen A, Kroger L, Kroger H, et al. Body fat mass, lean body mass and associated biomarkers as determinants of bone mineral density in children 6–8years of age - The Physical Activity and Nutrition in Children (PANIC) study. Bone. 2018;108:106–14.PubMedCrossRef Soininen S, Sidoroff V, Lindi V, Mahonen A, Kroger L, Kroger H, et al. Body fat mass, lean body mass and associated biomarkers as determinants of bone mineral density in children 6–8years of age - The Physical Activity and Nutrition in Children (PANIC) study. Bone. 2018;108:106–14.PubMedCrossRef
34.
go back to reference Eloranta AM, Lindi V, Schwab U, Tompuri T, Kiiskinen S, Lakka HM, et al. Dietary factors associated with overweight and body adiposity in Finnish children aged 6–8 years: the PANIC Study. Int J Obes (Lond). 2012;36(7):950–5.PubMedCrossRef Eloranta AM, Lindi V, Schwab U, Tompuri T, Kiiskinen S, Lakka HM, et al. Dietary factors associated with overweight and body adiposity in Finnish children aged 6–8 years: the PANIC Study. Int J Obes (Lond). 2012;36(7):950–5.PubMedCrossRef
35.
go back to reference Lakka TA, Lintu N, Vaisto J, Viitasalo A, Sallinen T, Haapala EA, et al. A 2 year physical activity and dietary intervention attenuates the increase in insulin resistance in a general population of children: the PANIC study. Diabetologia. 2020;63(11):2270–81.PubMedPubMedCentralCrossRef Lakka TA, Lintu N, Vaisto J, Viitasalo A, Sallinen T, Haapala EA, et al. A 2 year physical activity and dietary intervention attenuates the increase in insulin resistance in a general population of children: the PANIC study. Diabetologia. 2020;63(11):2270–81.PubMedPubMedCentralCrossRef
36.
go back to reference Constable AM, Vlachopoulos D, Barker AR, Moore SA, Soininen S, Haapala EA, et al. The independent and interactive associations of physical activity intensity and vitamin D status with bone mineral density in prepubertal children: the PANIC Study. Osteoporos Int. 2021;32(8):1609–20.PubMedCrossRef Constable AM, Vlachopoulos D, Barker AR, Moore SA, Soininen S, Haapala EA, et al. The independent and interactive associations of physical activity intensity and vitamin D status with bone mineral density in prepubertal children: the PANIC Study. Osteoporos Int. 2021;32(8):1609–20.PubMedCrossRef
37.
go back to reference Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, et al. The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int. 2016;27(4):1281–386.PubMedPubMedCentralCrossRef Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, et al. The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int. 2016;27(4):1281–386.PubMedPubMedCentralCrossRef
38.
go back to reference Tanner JM. Normal growth and techniques of growth assessment. Clin Endocrinol Metab. 1986;15(3):411–51.PubMedCrossRef Tanner JM. Normal growth and techniques of growth assessment. Clin Endocrinol Metab. 1986;15(3):411–51.PubMedCrossRef
39.
go back to reference Saari A, Sankilampi U, Hannila M-L, Kiviniemi V, Kesseli K, Dunkel L. New Finnish growth references for children and adolescents aged 0 to 20 years: Length/height-for-age, weight-for-length/height, and body mass index-for-age. Ann Med. 2011;43(3):235–48.PubMedCrossRef Saari A, Sankilampi U, Hannila M-L, Kiviniemi V, Kesseli K, Dunkel L. New Finnish growth references for children and adolescents aged 0 to 20 years: Length/height-for-age, weight-for-length/height, and body mass index-for-age. Ann Med. 2011;43(3):235–48.PubMedCrossRef
40.
go back to reference Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes. 2012;7(4):284–94.PubMedCrossRef Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes. 2012;7(4):284–94.PubMedCrossRef
41.
go back to reference Wren TA, Liu X, Pitukcheewanont P, Gilsanz V. Bone acquisition in healthy children and adolescents: comparisons of dual-energy x-ray absorptiometry and computed tomography measures. J Clin Endocrinol Metab. 2005;90(4):1925–8.PubMedCrossRef Wren TA, Liu X, Pitukcheewanont P, Gilsanz V. Bone acquisition in healthy children and adolescents: comparisons of dual-energy x-ray absorptiometry and computed tomography measures. J Clin Endocrinol Metab. 2005;90(4):1925–8.PubMedCrossRef
42.
go back to reference Leonard MB, Shults J, Elliott DM, Stallings VA, Zemel BS. Interpretation of whole body dual energy X-ray absorptiometry measures in children: comparison with peripheral quantitative computed tomography. Bone. 2004;34(6):1044–52.PubMedCrossRef Leonard MB, Shults J, Elliott DM, Stallings VA, Zemel BS. Interpretation of whole body dual energy X-ray absorptiometry measures in children: comparison with peripheral quantitative computed tomography. Bone. 2004;34(6):1044–52.PubMedCrossRef
43.
go back to reference Binkovitz LA, Henwood MJ. Pediatric DXA: technique and interpretation. Pediatr Radiol. 2007;37(1):21–31.PubMedCrossRef Binkovitz LA, Henwood MJ. Pediatric DXA: technique and interpretation. Pediatr Radiol. 2007;37(1):21–31.PubMedCrossRef
44.
go back to reference Jaworski M, Pludowski P. Precision errors, least significant change, and monitoring time interval in pediatric measurements of bone mineral density, body composition, and mechanostat parameters by GE lunar prodigy. J Clin Densitom. 2013;16(4):562–9.PubMedCrossRef Jaworski M, Pludowski P. Precision errors, least significant change, and monitoring time interval in pediatric measurements of bone mineral density, body composition, and mechanostat parameters by GE lunar prodigy. J Clin Densitom. 2013;16(4):562–9.PubMedCrossRef
45.
go back to reference Corder K, Brage S, Mattocks C, Ness A, Riddoch C, Wareham NJ, et al. Comparison of two methods to assess PAEE during six activities in children. Med Sci Sports Exerc. 2007;39(12):2180–8.PubMedCrossRef Corder K, Brage S, Mattocks C, Ness A, Riddoch C, Wareham NJ, et al. Comparison of two methods to assess PAEE during six activities in children. Med Sci Sports Exerc. 2007;39(12):2180–8.PubMedCrossRef
46.
go back to reference Brage S, Brage N, Franks PW, Ekelund U, Wareham NJ. Reliability and validity of the combined heart rate and movement sensor Actiheart. Eur J Clin Nutr. 2005;59(4):561–70.PubMedCrossRef Brage S, Brage N, Franks PW, Ekelund U, Wareham NJ. Reliability and validity of the combined heart rate and movement sensor Actiheart. Eur J Clin Nutr. 2005;59(4):561–70.PubMedCrossRef
47.
go back to reference Collings PJ, Westgate K, Väistö J, Wijndaele K, Atkin AJ, Haapala EA, et al. Cross-Sectional Associations of Objectively-Measured Physical Activity and Sedentary Time with Body Composition and Cardiorespiratory Fitness in Mid-Childhood: The PANIC Study. Sports Med. 2017;47(4):769–80.PubMedCrossRef Collings PJ, Westgate K, Väistö J, Wijndaele K, Atkin AJ, Haapala EA, et al. Cross-Sectional Associations of Objectively-Measured Physical Activity and Sedentary Time with Body Composition and Cardiorespiratory Fitness in Mid-Childhood: The PANIC Study. Sports Med. 2017;47(4):769–80.PubMedCrossRef
48.
go back to reference Skinner AM, Vlachopoulos D, Barker AR, Moore SA, Rowlands AV, Soininen S, et al. Physical activity volume and intensity distribution in relation to bone, lean and fat mass in children. Scand J Med Sci Sports. 2023;33(3):267–82.PubMedCrossRef Skinner AM, Vlachopoulos D, Barker AR, Moore SA, Rowlands AV, Soininen S, et al. Physical activity volume and intensity distribution in relation to bone, lean and fat mass in children. Scand J Med Sci Sports. 2023;33(3):267–82.PubMedCrossRef
49.
go back to reference Stegle O, Fallert SV, MacKay DJ, Brage S. Gaussian process robust regression for noisy heart rate data. IEEE Trans Biomed Eng. 2008;55(9):2143–51.PubMedCrossRef Stegle O, Fallert SV, MacKay DJ, Brage S. Gaussian process robust regression for noisy heart rate data. IEEE Trans Biomed Eng. 2008;55(9):2143–51.PubMedCrossRef
50.
go back to reference Brage S, Ekelund U, Brage N, Hennings MA, Froberg K, Franks PW, et al. Hierarchy of individual calibration levels for heart rate and accelerometry to measure physical activity. J Appl Physiol (1985). 2007;103(2):682-92. Brage S, Ekelund U, Brage N, Hennings MA, Froberg K, Franks PW, et al. Hierarchy of individual calibration levels for heart rate and accelerometry to measure physical activity. J Appl Physiol (1985). 2007;103(2):682-92.
51.
go back to reference Brage S, Brage N, Franks PW, Ekelund U, Wong MY, Andersen LB, et al. Branched equation modeling of simultaneous accelerometry and heart rate monitoring improves estimate of directly measured physical activity energy expenditure. J Appl Physiol (1985). 2004;96(1):343-51. Brage S, Brage N, Franks PW, Ekelund U, Wong MY, Andersen LB, et al. Branched equation modeling of simultaneous accelerometry and heart rate monitoring improves estimate of directly measured physical activity energy expenditure. J Appl Physiol (1985). 2004;96(1):343-51.
52.
go back to reference Corder K, Brage S, Wareham NJ, Ekelund U. Comparison of PAEE from combined and separate heart rate and movement models in children. Med Sci Sports Exerc. 2005;37(10):1761–7.PubMedCrossRef Corder K, Brage S, Wareham NJ, Ekelund U. Comparison of PAEE from combined and separate heart rate and movement models in children. Med Sci Sports Exerc. 2005;37(10):1761–7.PubMedCrossRef
53.
go back to reference Trost SG, Loprinzi PD, Moore R, Pfeiffer KA. Comparison of accelerometer cut points for predicting activity intensity in youth. Med Sci Sports Exerc. 2011;43(7):1360–8.PubMedCrossRef Trost SG, Loprinzi PD, Moore R, Pfeiffer KA. Comparison of accelerometer cut points for predicting activity intensity in youth. Med Sci Sports Exerc. 2011;43(7):1360–8.PubMedCrossRef
54.
go back to reference Brage S, Westgate K, Wijndaele K, Godinho J, Griffin S, Wareham N, editors. Evaluation of a method for minimizing diurnal information bias in objective sensor data. International Conference on Ambulatory Monitoring of Physical Activity and Movement; Massachusetts. 2013. Brage S, Westgate K, Wijndaele K, Godinho J, Griffin S, Wareham N, editors. Evaluation of a method for minimizing diurnal information bias in objective sensor data. International Conference on Ambulatory Monitoring of Physical Activity and Movement; Massachusetts. 2013.
55.
go back to reference Lampinen EK, Eloranta AM, Haapala EA, Lindi V, Vaisto J, Lintu N, et al. Physical activity, sedentary behaviour, and socioeconomic status among Finnish girls and boys aged 6–8 years. Eur J Sport Sci. 2017;17(4):462–72.PubMedCrossRef Lampinen EK, Eloranta AM, Haapala EA, Lindi V, Vaisto J, Lintu N, et al. Physical activity, sedentary behaviour, and socioeconomic status among Finnish girls and boys aged 6–8 years. Eur J Sport Sci. 2017;17(4):462–72.PubMedCrossRef
56.
go back to reference Vaisto J, Eloranta AM, Viitasalo A, Tompuri T, Lintu N, Karjalainen P, et al. Physical activity and sedentary behaviour in relation to cardiometabolic risk in children: cross-sectional findings from the Physical Activity and Nutrition in Children (PANIC) Study. Int J Behav Nutr Phys Act. 2014;11:55.PubMedPubMedCentralCrossRef Vaisto J, Eloranta AM, Viitasalo A, Tompuri T, Lintu N, Karjalainen P, et al. Physical activity and sedentary behaviour in relation to cardiometabolic risk in children: cross-sectional findings from the Physical Activity and Nutrition in Children (PANIC) Study. Int J Behav Nutr Phys Act. 2014;11:55.PubMedPubMedCentralCrossRef
57.
go back to reference Soininen S, Eloranta A-M, Schwab U, Lakka TA. Sources of vitamin D and determinants of serum 25-hydroxyvitamin D in Finnish adolescents. Eur J Nutr. 2023;62(2):1011–25.PubMed Soininen S, Eloranta A-M, Schwab U, Lakka TA. Sources of vitamin D and determinants of serum 25-hydroxyvitamin D in Finnish adolescents. Eur J Nutr. 2023;62(2):1011–25.PubMed
58.
go back to reference Hyde ET, Watson KB, Omura JD, Janz KF, Lee SM, Fulton JE, et al. Surveillance of Meeting the Youth Physical Activity Guideline: Impact of Including Vigorous-Intensity and Bone-Strengthening Activities. Res Q Exerc Sport. 2021;93(4):728–33.PubMedCrossRef Hyde ET, Watson KB, Omura JD, Janz KF, Lee SM, Fulton JE, et al. Surveillance of Meeting the Youth Physical Activity Guideline: Impact of Including Vigorous-Intensity and Bone-Strengthening Activities. Res Q Exerc Sport. 2021;93(4):728–33.PubMedCrossRef
59.
go back to reference Recommendation on physical activity for children and adolescents aged 7 to 17 years. Finland: Ministry of Education and Culture of Finland; 2021. Recommendation on physical activity for children and adolescents aged 7 to 17 years. Finland: Ministry of Education and Culture of Finland; 2021.
60.
go back to reference Leppänen MH, Haapala EA, Väistö J, Ekelund U, Brage S, Kilpeläinen TO, et al. Longitudinal and cross-sectional associations of adherence to 24-hour movement guidelines with cardiometabolic risk. Scand J Med Sci Sports. 2022;32(1):255–66.PubMedCrossRef Leppänen MH, Haapala EA, Väistö J, Ekelund U, Brage S, Kilpeläinen TO, et al. Longitudinal and cross-sectional associations of adherence to 24-hour movement guidelines with cardiometabolic risk. Scand J Med Sci Sports. 2022;32(1):255–66.PubMedCrossRef
61.
go back to reference Lubans DR, Hesketh K, Cliff DP, Barnett LM, Salmon J, Dollman J, et al. A systematic review of the validity and reliability of sedentary behaviour measures used with children and adolescents. Obes Rev. 2011;12(10):781–99.PubMedCrossRef Lubans DR, Hesketh K, Cliff DP, Barnett LM, Salmon J, Dollman J, et al. A systematic review of the validity and reliability of sedentary behaviour measures used with children and adolescents. Obes Rev. 2011;12(10):781–99.PubMedCrossRef
62.
go back to reference Roberts KC, Yao X, Carson V, Chaput J-P, Janssen I, Tremblay MS. Meeting the Canadian 24-hour movement guidelines for children and youth. Health Rep. 2017;28(10):3–7.PubMed Roberts KC, Yao X, Carson V, Chaput J-P, Janssen I, Tremblay MS. Meeting the Canadian 24-hour movement guidelines for children and youth. Health Rep. 2017;28(10):3–7.PubMed
63.
go back to reference Janssen I, Roberts KC, Thompson W. Adherence to the 24-Hour Movement Guidelines among 10- to 17-year-old Canadians. Health Promot Chronic Dis Prev Can. 2017;37(11):369–75.PubMedCrossRef Janssen I, Roberts KC, Thompson W. Adherence to the 24-Hour Movement Guidelines among 10- to 17-year-old Canadians. Health Promot Chronic Dis Prev Can. 2017;37(11):369–75.PubMedCrossRef
64.
go back to reference Riddoch CJ, Boreham CAG. The Health-Related Physical Activity of Children. Sports Med. 1995;19(2):86–102.PubMedCrossRef Riddoch CJ, Boreham CAG. The Health-Related Physical Activity of Children. Sports Med. 1995;19(2):86–102.PubMedCrossRef
65.
go back to reference Klitsie T, Corder K, Visscher TLS, Atkin AJ, Jones AP, van Sluijs EMF. Children’s sedentary behaviour: descriptive epidemiology and associations with objectively-measured sedentary time. BMC Public Health. 2013;13(1):1092.PubMedPubMedCentralCrossRef Klitsie T, Corder K, Visscher TLS, Atkin AJ, Jones AP, van Sluijs EMF. Children’s sedentary behaviour: descriptive epidemiology and associations with objectively-measured sedentary time. BMC Public Health. 2013;13(1):1092.PubMedPubMedCentralCrossRef
66.
go back to reference Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, et al. Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for black and non-black children: results of the bone mineral density in childhood study. J Clin Endocrinol Metab. 2011;96(10):3160–9.PubMedPubMedCentralCrossRef Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, et al. Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for black and non-black children: results of the bone mineral density in childhood study. J Clin Endocrinol Metab. 2011;96(10):3160–9.PubMedPubMedCentralCrossRef
67.
go back to reference Shepherd JA, Fan B, Lu Y, Wu XP, Wacker WK, Ergun DL, et al. A multinational study to develop universal standardization of whole-body bone density and composition using GE Healthcare Lunar and Hologic DXA systems. J Bone Miner Res. 2012;27(10):2208–16.PubMedCrossRef Shepherd JA, Fan B, Lu Y, Wu XP, Wacker WK, Ergun DL, et al. A multinational study to develop universal standardization of whole-body bone density and composition using GE Healthcare Lunar and Hologic DXA systems. J Bone Miner Res. 2012;27(10):2208–16.PubMedCrossRef
68.
go back to reference Weber DR, Moore RH, Leonard MB, Zemel BS. Fat and lean BMI reference curves in children and adolescents and their utility in identifying excess adiposity compared with BMI and percentage body fat. Am J Clin Nutr. 2013;98(1):49–56.PubMedPubMedCentralCrossRef Weber DR, Moore RH, Leonard MB, Zemel BS. Fat and lean BMI reference curves in children and adolescents and their utility in identifying excess adiposity compared with BMI and percentage body fat. Am J Clin Nutr. 2013;98(1):49–56.PubMedPubMedCentralCrossRef
69.
go back to reference Guinhouya BC, Samouda H, de Beaufort C. Level of physical activity among children and adolescents in Europe: a review of physical activity assessed objectively by accelerometry. Public Health. 2013;127(4):301–11.PubMedCrossRef Guinhouya BC, Samouda H, de Beaufort C. Level of physical activity among children and adolescents in Europe: a review of physical activity assessed objectively by accelerometry. Public Health. 2013;127(4):301–11.PubMedCrossRef
70.
go back to reference Roman-Vinas B, Chaput JP, Katzmarzyk PT, Fogelholm M, Lambert EV, Maher C, et al. Proportion of children meeting recommendations for 24-hour movement guidelines and associations with adiposity in a 12-country study. Int J Behav Nutr Phys Act. 2016;13(1):123.PubMedPubMedCentralCrossRef Roman-Vinas B, Chaput JP, Katzmarzyk PT, Fogelholm M, Lambert EV, Maher C, et al. Proportion of children meeting recommendations for 24-hour movement guidelines and associations with adiposity in a 12-country study. Int J Behav Nutr Phys Act. 2016;13(1):123.PubMedPubMedCentralCrossRef
71.
go back to reference Bland VL, Heatherington-Rauth M, Howe C, Going SB, Bea JW. Association of objectively measured physical activity and bone health in children and adolescents: a systematic review and narrative synthesis. Osteoporos Int. 2020;31(10):1865–94.PubMedCrossRef Bland VL, Heatherington-Rauth M, Howe C, Going SB, Bea JW. Association of objectively measured physical activity and bone health in children and adolescents: a systematic review and narrative synthesis. Osteoporos Int. 2020;31(10):1865–94.PubMedCrossRef
72.
go back to reference Rowlands AV, Stiles VH. Accelerometer counts and raw acceleration output in relation to mechanical loading. J Biomech. 2012;45(3):448–54.PubMedCrossRef Rowlands AV, Stiles VH. Accelerometer counts and raw acceleration output in relation to mechanical loading. J Biomech. 2012;45(3):448–54.PubMedCrossRef
73.
go back to reference Hart NH, Nimphius S, Rantalainen T, Ireland A, Siafarikas A, Newton RU. Mechanical basis of bone strength: influence of bone material, bone structure and muscle action. J Musculoskelet Neuronal Interact. 2017;17(3):114–39.PubMedPubMedCentral Hart NH, Nimphius S, Rantalainen T, Ireland A, Siafarikas A, Newton RU. Mechanical basis of bone strength: influence of bone material, bone structure and muscle action. J Musculoskelet Neuronal Interact. 2017;17(3):114–39.PubMedPubMedCentral
74.
go back to reference Haapala EA, Rantalainen T, Hesketh KD, Rodda CP, Duckham RL. Accelerometer-based osteogenic indices, moderate-to-vigorous and vigorous physical activity, and bone traits in adolescents. J Musculoskelet Neuronal Interact. 2022;22(4):514–23.PubMedPubMedCentral Haapala EA, Rantalainen T, Hesketh KD, Rodda CP, Duckham RL. Accelerometer-based osteogenic indices, moderate-to-vigorous and vigorous physical activity, and bone traits in adolescents. J Musculoskelet Neuronal Interact. 2022;22(4):514–23.PubMedPubMedCentral
75.
go back to reference Córdoba-Rodríguez DP, Iglesia I, Gómez-Bruton A, Miguel-Berges ML, Flores-Barrantes P, Casajús JA, et al. Associations between Spanish children’s physical activity and physical fitness with lean body mass: The CALINA study. J Sports Sci. 2022;40(4):401–12.PubMedCrossRef Córdoba-Rodríguez DP, Iglesia I, Gómez-Bruton A, Miguel-Berges ML, Flores-Barrantes P, Casajús JA, et al. Associations between Spanish children’s physical activity and physical fitness with lean body mass: The CALINA study. J Sports Sci. 2022;40(4):401–12.PubMedCrossRef
76.
go back to reference Moliner-Urdiales D, Ortega FB, Vicente-Rodriguez G, Rey-Lopez JP, Gracia-Marco L, Widhalm K, et al. Association of physical activity with muscular strength and fat-free mass in adolescents: the HELENA study. Eur J Appl Physiol. 2010;109(6):1119–27.PubMedCrossRef Moliner-Urdiales D, Ortega FB, Vicente-Rodriguez G, Rey-Lopez JP, Gracia-Marco L, Widhalm K, et al. Association of physical activity with muscular strength and fat-free mass in adolescents: the HELENA study. Eur J Appl Physiol. 2010;109(6):1119–27.PubMedCrossRef
77.
go back to reference Ness AR, Leary SD, Mattocks C, Blair SN, Reilly JJ, Wells J, et al. Objectively measured physical activity and fat mass in a large cohort of children. PLOS Med. 2007;4(3):e97.PubMedPubMedCentralCrossRef Ness AR, Leary SD, Mattocks C, Blair SN, Reilly JJ, Wells J, et al. Objectively measured physical activity and fat mass in a large cohort of children. PLOS Med. 2007;4(3):e97.PubMedPubMedCentralCrossRef
78.
go back to reference Janz KF, Medema-Johnson HC, Letuchy EM, Burns TL, Gilmore JME, Torner JC, et al. Subjective and objective measures of physical activity in relationship to bone mineral content during late childhood: the Iowa Bone Development Study. Br J Sports Med. 2008;42(8):658.PubMedCrossRef Janz KF, Medema-Johnson HC, Letuchy EM, Burns TL, Gilmore JME, Torner JC, et al. Subjective and objective measures of physical activity in relationship to bone mineral content during late childhood: the Iowa Bone Development Study. Br J Sports Med. 2008;42(8):658.PubMedCrossRef
79.
go back to reference McVeigh JA, Howie EK, Zhu K, Walsh JP, Straker L. Organized Sport participation from childhood to adolescence is associated with bone mass in young adults from the raine study. J Bone Miner Res. 2019;34(1):67–74.PubMedCrossRef McVeigh JA, Howie EK, Zhu K, Walsh JP, Straker L. Organized Sport participation from childhood to adolescence is associated with bone mass in young adults from the raine study. J Bone Miner Res. 2019;34(1):67–74.PubMedCrossRef
80.
go back to reference Nogueira RC, Weeks BK, Beck BR. Exercise to Improve Pediatric Bone and Fat: A Systematic Review and Meta-analysis. Med Sci Sports Exerc. 2014;46(3):610–21.PubMedCrossRef Nogueira RC, Weeks BK, Beck BR. Exercise to Improve Pediatric Bone and Fat: A Systematic Review and Meta-analysis. Med Sci Sports Exerc. 2014;46(3):610–21.PubMedCrossRef
81.
go back to reference Diethelm K, Bolzenius K, Cheng G, Remer T, Buyken AE. Longitudinal associations between reported sleep duration in early childhood and the development of body mass index, fat mass index and fat free mass index until age 7. Int J Pediatr Obes. 2011;6(2–2):e114-23.PubMedCrossRef Diethelm K, Bolzenius K, Cheng G, Remer T, Buyken AE. Longitudinal associations between reported sleep duration in early childhood and the development of body mass index, fat mass index and fat free mass index until age 7. Int J Pediatr Obes. 2011;6(2–2):e114-23.PubMedCrossRef
82.
go back to reference Butte NF, Puyau MR, Wilson TA, Liu Y, Wong WW, Adolph AL, et al. Role of physical activity and sleep duration in growth and body composition of preschool-aged children. Obesity. 2016;24(6):1328–35.PubMedCrossRef Butte NF, Puyau MR, Wilson TA, Liu Y, Wong WW, Adolph AL, et al. Role of physical activity and sleep duration in growth and body composition of preschool-aged children. Obesity. 2016;24(6):1328–35.PubMedCrossRef
83.
go back to reference Hernandez CJ, Beaupre GS, Carter DR. A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos Int. 2003;14(10):843–7.PubMedCrossRef Hernandez CJ, Beaupre GS, Carter DR. A theoretical analysis of the relative influences of peak BMD, age-related bone loss and menopause on the development of osteoporosis. Osteoporos Int. 2003;14(10):843–7.PubMedCrossRef
84.
go back to reference Smith JJ, Diallo TMO, Bennie JA, Tomkinson GR, Lubans DR. Factors associated with adherence to the muscle-strengthening activity guideline among adolescents. Psychol Sport Exerc. 2020;51:101747.CrossRef Smith JJ, Diallo TMO, Bennie JA, Tomkinson GR, Lubans DR. Factors associated with adherence to the muscle-strengthening activity guideline among adolescents. Psychol Sport Exerc. 2020;51:101747.CrossRef
85.
go back to reference Bennie JA, Smith JJ, Qian W, Leatherdale ST, Faulkner G. Longitudinal trends and predictors of muscle-strengthening activity guideline adherence among Canadian youths. J Sci Med Sport. 2022;25(3):230–4.PubMedCrossRef Bennie JA, Smith JJ, Qian W, Leatherdale ST, Faulkner G. Longitudinal trends and predictors of muscle-strengthening activity guideline adherence among Canadian youths. J Sci Med Sport. 2022;25(3):230–4.PubMedCrossRef
86.
go back to reference Fraser BJ, Alishah Z, Magnussen CG, Venn AJ, Dwyer T, Cleland V. Factors associated with change and stability in adherence to muscle-strengthening guidelines among young Australian adults: a longitudinal study. J Sci Med Sport. 2021;24(12):1261–6.PubMedCrossRef Fraser BJ, Alishah Z, Magnussen CG, Venn AJ, Dwyer T, Cleland V. Factors associated with change and stability in adherence to muscle-strengthening guidelines among young Australian adults: a longitudinal study. J Sci Med Sport. 2021;24(12):1261–6.PubMedCrossRef
87.
go back to reference Foster C, Armstrong MEG. What types of physical activities are effective in developing muscle and bone strength and balance? J Frailty Sarcopenia Falls. 2018;3(2):58–65.PubMedPubMedCentralCrossRef Foster C, Armstrong MEG. What types of physical activities are effective in developing muscle and bone strength and balance? J Frailty Sarcopenia Falls. 2018;3(2):58–65.PubMedPubMedCentralCrossRef
88.
go back to reference Lehtonen K, Oja S, Hakamäki M. Equality in sports and physical activity in Finland in 2021. 2022. Lehtonen K, Oja S, Hakamäki M. Equality in sports and physical activity in Finland in 2021. 2022.
89.
go back to reference Edwardson CL, Gorely T. Epoch length and its effect on physical activity intensity. Med Sci Sports Exerc. 2010;42(5):928–34.PubMedCrossRef Edwardson CL, Gorely T. Epoch length and its effect on physical activity intensity. Med Sci Sports Exerc. 2010;42(5):928–34.PubMedCrossRef
90.
go back to reference Skinner AM, Rowlands AV, Vlachopoulos D, Barker AR, Janz KF, Moore SA. The influence of accelerometer epoch length on associations of physical activity intensity and volume with bone outcomes. J Sports Sci Med. 2023;22:117–32.PubMedPubMedCentralCrossRef Skinner AM, Rowlands AV, Vlachopoulos D, Barker AR, Janz KF, Moore SA. The influence of accelerometer epoch length on associations of physical activity intensity and volume with bone outcomes. J Sports Sci Med. 2023;22:117–32.PubMedPubMedCentralCrossRef
Metadata
Title
Cross-sectional and longitudinal associations between the 24-hour movement behaviours, including muscle and bone strengthening activity, with bone and lean mass from childhood to adolescence
Authors
Annie M. Skinner
Alan R. Barker
Sarah A. Moore
Sonja Soininen
Eero A. Haapala
Juuso Väistö
Kate Westgate
Soren Brage
Timo A. Lakka
Dimitris Vlachopoulos
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2024
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-024-17711-x

Other articles of this Issue 1/2024

BMC Public Health 1/2024 Go to the issue