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Association of objectively measured physical activity and sedentary behavior with bone stiffness in peripubertal children

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Abstract

Introduction

Physical activity (PA) is a key factor of bone mass acquisition in peripubertal children. Sedentary behavior (SB) has been shown to influence bone outcomes. This study aimed to examine the association between objectively measured PA and SB and bone stiffness in Japanese children.

Materials and Methods

Participants were fifth-grade children aged 10–11 years from Project Koshu. The stiffness index (SI) of the calcaneus was measured by quantitative ultrasound; PA and SB were evaluated by an accelerometer. Each PA parameter was divided into sex-specific tertile or stratified by recommended PA guideline [≥ 60 min/day of moderate-to-vigorous PA (MVPA)]. The SI was compared among PA and SB through analysis of covariance with Bonferroni correction.

Results

Of 174 children, complete data were obtained from 134 (60 boys and 74 girls). The SI in boys was higher in the highest tertile of MVPA than that in the other groups. A similar association was found in girls but was not significant. Children who met the PA guideline had higher SI than those who did not, but there was no significant difference. A negative relation was observed in girls, with the SI gradually decreasing along with increasing SB (p for trend = 0.038). This association was not observed among boys.

Conclusion

This study suggests that MVPA is positively associated with bone stiffness in Japanese schoolchildren in boys and SB is negatively associated with that in girls. Reducing SB might be a brief modifiable factor for preventing lower peak bone mass in girls, in addition to increasing MVPA.

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References

  1. Lazcano-Ponce E, Tamayo J, Cruz-Valdez A, Díaz R, Hernández B, Del Cueto R, Hernández-Avila M (2003) Peak bone mineral area density and determinants among females aged 9 to 24 years in Mexico. Osteoporos Int 14:539–547

    PubMed  Google Scholar 

  2. Santos L, Elliott-Sale KJ, Sale C (2017) Exercise and bone health across the lifespan. Biogerontology 18:931–946

    CAS  PubMed  PubMed Central  Google Scholar 

  3. MacKelvie KJ, Khan KM, McKay HA (2002) Is there a critical period for bone response to weight-bearing exercise in children and adolescents? a systematic review. Br J Sports Med 36:250–257

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Gunter KB, Almstedt HC, Janz KF (2012) Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev 40:13–21

    PubMed  PubMed Central  Google Scholar 

  6. Rizzoli R, Bianchi ML, Garabédian M, McKay HA, Moreno LA (2010) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46:294–305

    PubMed  Google Scholar 

  7. Weaver CM, Gordon CM, Janz KF, Kalkwarf HJ, Lappe JM, Lewis R, O’Karma M, Wallace TC, Zemel BS (2016) The National Osteoporosis Foundation’s position statement on peak bone mass development and lifestyle factors: a systematic review and implementation recommendations. Osteoporos Int 27:1281–1386

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Tan VP, Macdonald HM, Kim S, Nettlefold L, Gabel L, Ashe MC, McKay HAJ (2014) Influence of physical activity on bone strength in children and adolescents: a systematic review and narrative synthesis. J Bone Miner Res 10:2161–2181

    Google Scholar 

  9. Nikander R, Sievänen H, Heinonen A, Daly RM, Uusi-Rasi K, Kannus P (2010) Targeted exercise against osteoporosis: a systematic review and meta-analysis for optimising bone strength throughout life. BMC Med 8:47

    PubMed  PubMed Central  Google Scholar 

  10. World Health Organization (2017) Physical activity fact sheet. http://www.who.int/mediacentre/factsheets/fs385/en/. Accessed 1 Apr 2019

  11. World Health Organization (2010) Global recommendations: physical activity for health. http://www.who.int/dietphysicalactivity/publications/9789241599979/en/. Accessed 1 Apr 2019

  12. The Japan Sports Agency (2018) The report of FY2018 national survey on physical fitness, athletic performance and exercise habits. http://www.mext.go.jp/sports/b_menu/toukei/kodomo/zencyo/1411922.htm. Accessed 23 Apr 2019 (in Japanese)

  13. The Japan Pediatric Association (2004) Proposal for children’s media use. https://www.jpa-web.org/dcms_media/other/ktmedia_teigenzenbun.pdf. Accessed 23 Apr 2019 (in Japanese)

  14. Patterson R, McNamara E, Tainio M, de Sá TH, Smith AD, Sharp SJ, Edwards P, Woodcock J, Brage S, Wijndaele K (2018) Sedentary behaviour and risk of all-cause, cardiovascular and cancer mortality, and incident type 2 diabetes: a systematic review and dose response meta-analysis. Eur J Epidemiol 33:811–829

    PubMed  PubMed Central  Google Scholar 

  15. Biswas A, Oh PI, Faulkner GE, Bajaj RR, Silver MA, Mitchell MS, Alter DA (2015) Sedentary time and its association with risk for disease incidence, mortality, and hospitalization in adults: a systematic review and meta-analysis. Ann Intern Med 162:123–132

    PubMed  Google Scholar 

  16. Tremblay MS, LeBlanc AG, Kho ME, Saunders TJ, Larouche R, Colley RC, Goldfield G, Connor Gorber S (2011) Systematic review of sedentary behaviour and health indicators in school-aged children and youth. Int J Behav Nutr Phys Act 8:98

    PubMed  PubMed Central  Google Scholar 

  17. Tremblay MS, Colley RC, Saunders TJ, Healy GN, Owen N (2010) Physiological and health implications of a sedentary lifestyle. Appl Physiol Nutr Metab 35:725–740

    PubMed  Google Scholar 

  18. Koedijk JB, van Rijswijk J, Oranje WA, van den Bergh JP, Bours SP, Savelberg HH, Schaper NC (2017) Sedentary behaviour and bone health in children, adolescents and young adults: a systematic review. Osteoporos Int 28:2507–2519

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Xu Y, Guo B, Gong J, Xu H, Bai Z (2014) The correlation between calcaneus stiffness index calculated by QUS and total body BMD assessed by DXA in Chinese children and adolescents. J Bone Miner Metab 32:159–166

    CAS  PubMed  Google Scholar 

  20. Babatunde OO, Forsyth JJ (2013) Quantitative ultrasound and bone’s response to exercise: a meta analysis. Bone 53:311–318

    CAS  PubMed  Google Scholar 

  21. Suzuki K (2015) Longitudinal analyses of childhood growth: evidence from Project Koshu. J Epidemiol 25:2–7

    PubMed  Google Scholar 

  22. McClain JJ, Sisson SB, Washington TL, Craig CL, Tudor-Locke C (2007) Comparison of Kenz Lifecorder EX and ActiGraph accelerometers in 10-yr-old children. Med Sci Sports Exerc 39:630–638

    PubMed  Google Scholar 

  23. Kumahara H, Schutz Y, Ayabe M, Yoshioka M, Yoshitake Y, Shindo M, Ishii K, Tanaka H (2004) The use of uniaxial accelerometry for the assessment of physical activity-related energy expenditure: a validation study against whole-body indirect calorimetry. Br J Nutr 91:235–243

    CAS  PubMed  Google Scholar 

  24. Arabi A, Nabulsi M, Maalouf J, Choucair M, Khalifé H, Vieth R, El-Hajj Fuleihan G (2004) Bone mineral density by age, gender, pubertal stages, and socioeconomic status in healthy Lebanese children and adolescents. Bone 35:1169–1179

    PubMed  Google Scholar 

  25. Ishii M, Uenishi K, Ishida H, Kushima Y (2005) Development of the “self-assessment table for calcium intake” and evaluation of its validity. Osteoporos Jpn 13:497–502 (in Japanese)

    Google Scholar 

  26. Miyoshi M, Tsuboyama-Kasaoka N, Nishi N (2012) School-based “Shokuiku” program in Japan: application to nutrition education in Asian countries. Asia Pac J Clin Nutr 21:159–162

    PubMed  Google Scholar 

  27. Currie C, Molcho M, Boyce W, Holstein B, Torsheim T, Richter M (2008) Researching health inequalities in adolescents: the development of the health behaviour in school-aged children (HBSC) family affluence scale. Soc Sci Med 66:1429–1436

    PubMed  Google Scholar 

  28. Oh IH, Cho Y, Park SY, Oh C, Choe BK, Choi JM, Yoon TY (2011) Relationship between socioeconomic variables and obesity in Korean adolescents. J Epidemiol 21:263–270

    PubMed  PubMed Central  Google Scholar 

  29. Elgar FJ, Pförtner TK, Moor I, De Clercq B, Stevens GW, Currie C (2015) Socioeconomic inequalities in adolescent health 2002–2010: a time-series analysis of 34 countries participating in the health behaviour in school-aged children study. Lancet 385:2088–2095

    PubMed  Google Scholar 

  30. Nogueira RC, Weeks BK, Beck BR (2014) Exercise to improve pediatric bone and fat: a systematic review and meta-analysis. Med Sci Sports Exerc 46:610–621

    PubMed  Google Scholar 

  31. Zymbal V, Baptista F, Letuchy EM, Janz KF, Levy SM (2019) Mediating effect of muscle on the relationship of physical activity and bone. Med Sci Sports Exerc 51:202–210

    PubMed  PubMed Central  Google Scholar 

  32. Osborn W, Simm P, Olds T, Lycett K, Mensah FK, Muller J, Fraysse F, Ismail N, Vlok J, Burgner D, Carlin JB, Edwards B, Dwyer T, Azzopardi P, Ranganathan S, Wake M (2018) Bone health, activity and sedentariness at age 11–12 years: cross-sectional Australian population-derived study. Bone 112:153–160

    PubMed  Google Scholar 

  33. Gabel L, Macdonald HM, Nettlefold LA, McKay HA (2018) Sex-, ethnic-, and age-specific centile curves for pQCT- and HR-pQCT-derived measures of bone structure and strength in adolescents and young adults. J Bone Miner Res 33:987–1000

    CAS  PubMed  Google Scholar 

  34. Ivuškāns A, Mäestu J, Jürimäe T, Lätt E, Purge P, Saar M, Maasalu K, Jürimäe J (2015) Sedentary time has a negative influence on bone mineral parameters in peripubertal boys: a 1-year prospective study. J Bone Miner Metab 33:85–92

    PubMed  Google Scholar 

  35. Janz KF, Letuchy EM, Burns TL, Eichenberger Gilmore JM, Torner JC, Levy SM (2014) Objectively measured physical activity trajectories predict adolescent bone strength: Iowa Bone Development Study. Br J Sports Med 48:1032–1036

    PubMed  Google Scholar 

  36. Chastin SF, Mandrichenko O, Skelton DA (2014) The frequency of osteogenic activities and the pattern of intermittence between periods of physical activity and sedentary behaviour affects bone mineral content: the cross-sectional NHANES study. BMC Public Health 6:4

    Google Scholar 

  37. Vaitkeviciute D, Lätt E, Mäestu J, Jürimäe T, Saar M, Purge P, Maasalu K, Jürimäe J (2014) Physical activity and bone mineral accrual in boys with different body mass parameters during puberty: a longitudinal study. PLoS One 9:e107759

    PubMed  PubMed Central  Google Scholar 

  38. Heidemann M, Mølgaard C, Husby S, Schou AJ, Klakk H, Møller NC, Holst R, Wedderkopp N (2013) The intensity of physical activity influences bone mineral accrual in childhood: the childhood health, activity and motor performance school (the CHAMPS) study, Denmark. BMC Pediatr 2:32

    Google Scholar 

  39. Herrmann D, Buck C, Sioen I, Kouride Y, Marild S, Molnár D, Mouratidou T, Pitsiladis Y, Russo P, Veidebaum T, Ahrens W, IDEFICS consortium (2015) Impact of physical activity, sedentary behaviour and muscle strength on bone stiffness in 2-10-year-old children-cross-sectional results from the IDEFICS study. Int J Behav Nutr Phys Act 17:112

    Google Scholar 

  40. Herrmann D, Pohlabeln H, Gianfagna F, Konstabel K, Lissner L, Mårild S, Molnar D, Moreno LA, Siani A, Sioen I, Veidebaum T, Ahrens W, IDEFICS Consortium (2015) Association between bone stiffness and nutritional biomarkers combined with weight-bearing exercise, physical activity, and sedentary time in preadolescent children. A case–control study. Bone 78:142–149

    PubMed  Google Scholar 

  41. De Smet S, Michels N, Polfliet C, D’Haese S, Roggen I, De Henauw S, Sioen I (2015) The influence of dairy consumption and physical activity on ultrasound bone measurements in Flemish children. J Bone Miner Metab 33:192–200

    PubMed  Google Scholar 

  42. Sayers A, Mattocks C, Deere K, Ness A, Riddoch C, Tobias JH (2011) Habitual levels of vigorous, but not moderate or light, physical activity is positively related to cortical bone mass in adolescents. J Clin Endocrinol Metab 96:E793–E802

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Sardinha LB, Baptista F, Ekelund U (2008) Objectively measured physical activity and bone strength in 9-year-old boys and girls. Pediatrics 122:e728–e736

    PubMed  Google Scholar 

  44. Gracia-Marco L, Moreno LA, Ortega FB, León F, Sioen I et al (2011) Levels of physical activity that predict optimal bone mass in adolescents: the HELENA study. Am J Prev Med 40:599–607

    PubMed  Google Scholar 

  45. Thomsen K, Jepsen DB, Matzen L, Hermann AP, Masud T, Ryg J (2015) Is calcaneal quantitative ultrasound useful as prescreen stratification tool for osteoporosis? Osteoporos Int 26:1459–1475

    CAS  PubMed  Google Scholar 

  46. Wang KC, Wang KC, Amirabadi A, Cheung E, Uleryk E, Moineddin R, Doria AS (2014) Evidence-based outcomes on diagnostic accuracy of quantitative ultrasound for assessment of pediatric osteoporosis—a systematic review. Pediatr Radiol 44:1573–1587

    PubMed  Google Scholar 

  47. Moayyeri A, Adams JE, Adler RA, Krieg MA, Hans D, Compston J, Lewiecki EM (2012) Quantitative ultrasound of the heel and fracture risk assessment: an updated meta-analysis. Osteoporos Int 23:143–153

    CAS  PubMed  Google Scholar 

  48. Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51:170–179

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the study participants for the use of their personal data. We also thank the principal, vice principal, and homeroom teachers at the elementary schools. We are extremely grateful to the school nurses of each school for their support. This study was supported by JSPS KAKENHI (Grant numbers 26750335, 17K01794, 15K08801, 24590788, 23390173, 18H03037, 18K10064, and 18K17375) and Kitasato University Research Grant for Young Researchers.

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Authors and Affiliations

  1. College of Liberal Arts and Sciences, Kitasato University, Sagamihara, Kanagawa, 252-0373, Japan

    Mitsuya Yamakita

  2. Division of Human Sciences, Faculty of Education, Graduate School Department of Interdisciplinary Research, University of Yamanashi, Kofu, Yamanashi, Japan

    Daisuke Ando

  3. Division of Medicine, Department of Health Sciences, Basic Science for Clinical Medicine, Graduate School Department of Interdisciplinary Research, University of Yamanashi, Chuo, Yamanashi, Japan

    Yuka Akiyama & Zentaro Yamagata

  4. Center for Birth Cohort Studies, Graduate School Department of Interdisciplinary Research, University of Yamanashi, Chuo, Yamanashi, Japan

    Miri Sato & Zentaro Yamagata

  5. Department of Health and Psychosocial Medicine, Aichi Medical University School of Medicine, Nagakute, Aichi, Japan

    Kohta Suzuki

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Contributions

Study design: MY, DA, MS, and ZY. Study conduct and data collection: MY, DA, YA, MS, and KS. Data analysis: MY and AY. Data interpretation and drafting manuscript: all authors. MY and AY take responsibility for the integrity of the data analysis. All authors read, revised, and approved the final manuscript.

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Correspondence to Mitsuya Yamakita.

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Yamakita, M., Ando, D., Akiyama, Y. et al. Association of objectively measured physical activity and sedentary behavior with bone stiffness in peripubertal children. J Bone Miner Metab 37, 1095–1103 (2019). https://doi.org/10.1007/s00774-019-01021-z

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