Pubertal timing and adult fracture risk in men: A population-based cohort study


Autoři: Liesbeth Vandenput aff001;  Jenny M. Kindblom aff001;  Maria Bygdell aff001;  Maria Nethander aff001;  Claes Ohlsson aff001
Působiště autorů: Centre for Bone and Arthritis Research, Department of Internal Medicine and Clinical Nutrition, Institute of Medicine, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden aff001;  Bioinformatics Core Facility, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden aff002
Vyšlo v časopise: Pubertal timing and adult fracture risk in men: A population-based cohort study. PLoS Med 16(12): e1002986. doi:10.1371/journal.pmed.1002986
Kategorie: Research Article
doi: 10.1371/journal.pmed.1002986

Souhrn

Background

Puberty is a critical period for bone mass accrual, and late puberty in boys is associated with reduced bone mass in adult men. The role of variations in pubertal timing within the normal range for adult fracture risk in men is, however, unknown. We, therefore, assessed the association between age at peak height velocity (PHV), an objective measure of pubertal timing, and fracture risk in adult men.

Methods and findings

In the BMI Epidemiology Study Gothenburg, 31,971 Swedish men born between January 1, 1945, and December 31, 1961, with detailed growth data (height and weight) available from centrally archived school healthcare records and the conscription register were followed until December 31, 2016. Age at PHV was calculated according to a modified infancy–childhood–puberty model, and fracture information was retrieved from the Swedish National Patient Register. The mean ± SD age at PHV was 14.1 ± 1.1 years. In total, 5,872 men (18.4%) sustained at least 1 fracture after 20 years of age and 5,731 men (17.9%) sustained a non-vertebral fracture after 20 years of age during a mean ± SD follow-up of 37.3 ± 11.7 years. Cox proportional hazards models adjusted for birth year and country of origin revealed that age at PHV was associated with the risk of any fracture and non-vertebral fracture. Participants with age at PHV in the highest tertile (after 14.5 years of age) were at greater risk of any fracture (hazard ratio [HR] 1.15, 95% confidence interval [CI] 1.08–1.22, P < 0.001) and non-vertebral fracture (HR 1.16, 95% CI 1.09–1.24, P < 0.001) compared with those with age at PHV in the lowest tertile (at 13.6 years of age or younger). Additional adjustments for birthweight, childhood BMI, adult educational level, and young adult height did not attenuate the associations between age at PHV and adult fracture risk. Limitations of this study include the inability to adjust for important risk factors for fracture, inadequate power to assess the relation between pubertal timing and specific fracture types, and the limited generalizability to other populations.

Conclusions

In this study, we observed that late pubertal timing was associated with increased adult fracture risk in men. These findings suggest that information on pubertal timing might aid in the identification of those men at greatest risk of fracture.

Klíčová slova:

Adults – Bone fracture – Cohort studies – Educational attainment – Puberty – Schools – Sweden – Young adults


Zdroje

1. Bonjour JP, Chevalley T. Pubertal timing, bone acquisition, and risk of fracture throughout life. Endocr Rev. 2014;35(5):820–47. doi: 10.1210/er.2014-1007 25153348

2. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969;44(235):291–303. doi: 10.1136/adc.44.235.291 5785179

3. Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970;45(239):13–23. doi: 10.1136/adc.45.239.13 5440182

4. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev. 2003;24(5):668–93. doi: 10.1210/er.2002-0019 14570750

5. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R. Influence of age at menarche on forearm bone microstructure in healthy young women. J Clin Endocrinol Metab. 2008;93(7):2594–601. doi: 10.1210/jc.2007-2644 18430772

6. Gilsanz V, Chalfant J, Kalkwarf H, Zemel B, Lappe J, Oberfield S, et al. Age at onset of puberty predicts bone mass in young adulthood. J Pediatr. 2011;158(1):100–5. doi: 10.1016/j.jpeds.2010.06.054 20797727

7. Jackowski SA, Erlandson MC, Mirwald RL, Faulkner RA, Bailey DA, Kontulainen SA, et al. Effect of maturational timing on bone mineral content accrual from childhood to adulthood: evidence from 15 years of longitudinal data. Bone. 2011;48(5):1178–85. doi: 10.1016/j.bone.2011.02.010 21338727

8. Chevalley T, Bonjour JP, van Rietbergen B, Rizzoli R, Ferrari S. Fractures in healthy females followed from childhood to early adulthood are associated with later menarcheal age and with impaired bone microstructure at peak bone mass. J Clin Endocrinol Metab. 2012;97(11):4174–81. doi: 10.1210/jc.2012-2561 22948760

9. Elhakeem A, Frysz M, Tilling K, Tobias JH, Lawlor DA. Association between age at puberty and bone accrual from 10 to 25 years of age. JAMA Network Open. 2019;2(8):e198918. doi: 10.1001/jamanetworkopen.2019.8918 31397863

10. Ito M, Yamada M, Hayashi K, Ohki M, Uetani M, Nakamura T. Relation of early menarche to high bone mineral density. Calcif Tissue Int. 1995;57(1):11–4. doi: 10.1007/bf00298989 7671158

11. Rosenthal DI, Mayo-Smith W, Hayes CW, Khurana JS, Biller BM, Neer RM, et al. Age and bone mass in premenopausal women. J Bone Miner Res. 1989;4(4):533–8. doi: 10.1002/jbmr.5650040412 2816502

12. Chevalley T, Bonjour JP, Ferrari S, Rizzoli R. Deleterious effect of late menarche on distal tibia microstructure in healthy 20-year-old and premenopausal middle-aged women. J Bone Miner Res. 2009;24(1):144–52. doi: 10.1359/jbmr.080815 19086917

13. Day FR, Elks CE, Murray A, Ong KK, Perry JR. Puberty timing associated with diabetes, cardiovascular disease and also diverse health outcomes in men and women: the UK Biobank study. Sci Rep. 2015;5:11208. doi: 10.1038/srep11208 26084728

14. Chang HK, Chang DG, Myong JP, Kim JH, Lee SJ, Lee YS, et al. Bone mineral density among Korean females aged 20–50 years: influence of age at menarche (The Korea National Health and Nutrition Examination Survey 2008–2011). Osteoporos Int. 2017;28(7):2129–36. doi: 10.1007/s00198-017-3997-0 28293690

15. Johnell O, Gullberg B, Kanis JA, Allander E, Elffors L, Dequeker J, et al. Risk factors for hip fracture in European women: the MEDOS Study. Mediterranean Osteoporosis Study. J Bone Miner Res. 1995;10(11):1802–15. doi: 10.1002/jbmr.5650101125 8592959

16. Roy DK, O’Neill TW, Finn JD, Lunt M, Silman AJ, Felsenberg D, et al. Determinants of incident vertebral fracture in men and women: results from the European Prospective Osteoporosis Study (EPOS). Osteoporos Int. 2003;14(1):19–26. doi: 10.1007/s00198-002-1317-8 12577181

17. Silman AJ. Risk factors for Colles’ fracture in men and women: results from the European Prospective Osteoporosis Study. Osteoporos Int. 2003;14(3):213–8. doi: 10.1007/s00198-002-1364-1 12730767

18. Cousminer DL, Mitchell JA, Chesi A, Roy SM, Kalkwarf HJ, Lappe JM, et al. Genetically determined later puberty impacts lowered bone mineral density in childhood and adulthood. J Bone Miner Res. 2018;33(3):430–6. doi: 10.1002/jbmr.3320 29068475

19. Zhang Q, Greenbaum J, Zhang WD, Sun CQ, Deng HW. Age at menarche and osteoporosis: a Mendelian randomization study. Bone. 2018;117:91–7. doi: 10.1016/j.bone.2018.09.015 30240960

20. Karlberg J. On the modelling of human growth. Stat Med. 1987;6(2):185–92. doi: 10.1002/sim.4780060210 3589247

21. Kindblom JM, Lorentzon M, Norjavaara E, Hellqvist A, Nilsson S, Mellstrom D, et al. Pubertal timing predicts previous fractures and BMD in young adult men: the GOOD study. J Bone Miner Res. 2006;21(5):790–5. doi: 10.1359/jbmr.020602 16734395

22. Kuh D, Muthuri SG, Moore A, Cole TJ, Adams JE, Cooper C, et al. Pubertal timing and bone phenotype in early old age: findings from a British birth cohort study. Int J Epidemiol. 2016;45(4):1113–24. doi: 10.1093/ije/dyw131 27401728

23. Ohlsson C, Bygdell M, Sonden A, Rosengren A, Kindblom JM. Association between excessive BMI increase during puberty and risk of cardiovascular mortality in adult men: a population-based cohort study. Lancet Diabetes Endocrinol. 2016;4(12):1017–24. doi: 10.1016/S2213-8587(16)30273-X 27815089

24. Ohlsson C, Bygdell M, Sonden A, Jern C, Rosengren A, Kindblom JM. BMI increase through puberty and adolescence is associated with risk of adult stroke. Neurology. 2017;89(4):363–9. doi: 10.1212/WNL.0000000000004158 28659423

25. Ohlsson C, Bygdell M, Nethander M, Rosengren A, Kindblom JM. BMI change during puberty is an important determinant of adult type 2 diabetes risk in men. J Clin Endocrinol Metab. 2019;104(5):1823–32. doi: 10.1210/jc.2018-01339 30517677

26. Bygdell M, Kindblom JM, Celind J, Nethander M, Ohlsson C. Childhood BMI is inversely associated with pubertal timing in normal-weight but not overweight boys. Am J Clin Nutr. 2018;108(6):1259–63. doi: 10.1093/ajcn/nqy201 30321255

27. Liu YX, Wikland KA, Karlberg J. New reference for the age at childhood onset of growth and secular trend in the timing of puberty in Swedish. Acta Paediatr. 2000;89(6):637–43. doi: 10.1080/080352500750043918 10914954

28. Harrell FE. Regression modeling strategies. Nashville: Vanderbilt University Department of Statistics; 2019 [cited 2019 Nov 6]. Available from: http://biostat.mc.vanderbilt.edu/wiki/Main/RmS.

29. Therneau TM. survival: survival analysis. Version 2.41–3. Comprehensive R Archive Network; 2017 [cited 2019 Nov 6]. Available from: https://CRAN.R-project.org/package=survival.

30. Kassambara A, Kosinski M, Biecek P, Fabian S. survminer: drawing survival curves using ‘ggplot2’. Version 0.4.3. Comprehensive R Archive Network; 2018 [cited 2019 Nov 6]. Available from: https://CRAN.R-project.org/package=survminer.

31. Darelid A, Ohlsson C, Nilsson M, Kindblom JM, Mellstrom D, Lorentzon M. Catch up in bone acquisition in young adult men with late normal puberty. J Bone Miner Res. 2012;27(10):2198–207. doi: 10.1002/jbmr.1675 22653693

32. Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ. 1996;312(7041):1254–9. doi: 10.1136/bmj.312.7041.1254 8634613

33. Meyer HE, Tverdal A, Falch JA. Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol. 1993;137(11):1203–11. doi: 10.1093/oxfordjournals.aje.a116622 8322761

34. Cauley JA, Cawthon PM, Peters KE, Cummings SR, Ensrud KE, Bauer DC, et al. Risk factors for hip fracture in older men: the Osteoporotic Fractures in Men Study (MrOS). J Bone Miner Res. 2016;31(10):1810–9. doi: 10.1002/jbmr.2836 26988112

35. Mellström D, Vandenput L, Mallmin H, Holmberg AH, Lorentzon M, Oden A, et al. Older men with low serum estradiol and high serum SHBG have an increased risk of fractures. J Bone Miner Res. 2008;23(10):1552–60. doi: 10.1359/jbmr.080518 18518773

36. Vanderschueren D, Laurent MR, Claessens F, Gielen E, Lagerquist MK, Vandenput L, et al. Sex steroid actions in male bone. Endocr Rev. 2014;35(6):906–60. doi: 10.1210/er.2014-1024 25202834

37. Greenspan LC, Lee MM. Endocrine disrupters and pubertal timing. Curr Opin Endocrinol Diabetes Obes. 2018;25(1):49–54. doi: 10.1097/MED.0000000000000377 29135489

38. Wang Z, Li D, Miao M, Liang H, Chen J, Zhou Z, et al. Urine bisphenol A and pubertal development in boys. Int J Hyg Environ Health. 2017;220(1):43–50. doi: 10.1016/j.ijheh.2016.10.004 27769633

39. Harley KG, Rauch SA, Chevrier J, Kogut K, Parra KL, Trujillo C, et al. Association of prenatal and childhood PBDE exposure with timing of puberty in boys and girls. Environ Int. 2017;100:132–8. doi: 10.1016/j.envint.2017.01.003 28089583

40. Mieritz MG, Frederiksen H, Sorensen K, Aksglaede L, Mouritsen A, Hagen CP, et al. Urinary phthalate excretion in 555 healthy Danish boys with and without pubertal gynaecomastia. Int J Androl. 2012;35(3):227–35. doi: 10.1111/j.1365-2605.2012.01279.x 22612475

41. Ohlsson C, Bygdell M, Celind J, Sondén A, Tidblad A, Sävendahl L, et al. Secular trends in pubertal growth acceleration in Swedish boys born from 1947 to 1996. JAMA Pediatr. 2019;173(9):860–5.

42. Fuggle NR, Curtis EM, Ward KA, Harvey NC, Dennison EM, Cooper C. Fracture prediction, imaging and screening in osteoporosis. Nat Rev Endocrinol. 2019;15(9):535–47. doi: 10.1038/s41574-019-0220-8 31189982

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Interní lékařství

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PLOS Medicine


2019 Číslo 12

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