Association of puberty timing with type 2 diabetes: A systematic review and meta-analysis

English version

Autoři: Tuck Seng Cheng ^aff001; Felix R. Day ^aff001; Rajalakshmi Lakshman ^aff001; Ken K. Ong ^aff001
Působiště autorů: MRC Epidemiology Unit, Institute of Metabolic Science, University of Cambridge, Cambridge, United Kingdom ^aff001; Department of Paediatrics, University of Cambridge, Cambridge, United Kingdom ^aff002
Vyšlo v časopise: Association of puberty timing with type 2 diabetes: A systematic review and meta-analysis. PLoS Med 17(1): e1003017. doi:10.1371/journal.pmed.1003017
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1003017

Souhrn

Background

Emerging studies have investigated the association between puberty timing, particularly age at menarche (AAM), and type 2 diabetes. However, whether this association is independent of adiposity is unclear. We aimed to systematically review published evidence on the association between puberty timing and type 2 diabetes (T2D) or impaired glucose tolerance (IGT), with and without adjustment for adiposity, and to estimate the potential contribution of puberty timing to the burden of T2D in the United Kingdom (UK).

Methods and findings

We searched PubMed, Medline, and Embase databases for publications until February 2019 on the timing of any secondary sexual characteristic in boys or girls in relation to T2D/IGT. Inverse-variance-weighted random-effects meta-analysis was used to pool reported estimates, and meta-regression was used to explore sources of heterogeneity. Twenty-eight observational studies were identified. All assessed AAM in women (combined N = 1,228,306); only 1 study additionally included men. In models without adjustment for adult adiposity, T2D/IGT risk was lower per year later AAM (relative risk [RR] = 0.91, 95% CI 0.89–0.93, p < 0.001, 11 estimates, n = 833,529, I² = 85.4%) and higher for early versus later menarche (RR = 1.39, 95% CI 1.25–1.55, p < 0.001, 23 estimates, n = 1,185,444, I² = 87.8%). Associations were weaker but still evident in models adjusted for adiposity (AAM: RR = 0.97 per year, 95% CI 0.95–0.98, p < 0.001, 12 estimates, n = 852,268, I² = 51.8%; early menarche: RR = 1.19, 95% CI 1.11–1.28, p < 0.001, 21 estimates, n = 890,583, I² = 68.1%). Associations were stronger among white than Asian women, and in populations with earlier average AAM. The estimated population attributable risk of T2D in white UK women due to early menarche unadjusted and adjusted for adiposity was 12.6% (95% CI 11.0–14.3) and 5.1% (95% CI 3.6–6.7), respectively. Findings in this study are limited by residual and unmeasured confounding, and self-reported AAM.

Conclusions

Earlier AAM is consistently associated with higher T2D/IGT risk, independent of adiposity. More importantly, this research has identified that a substantial proportion of T2D in women is related to early menarche, which would be expected to increase in light of global secular trends towards earlier puberty timing. These findings highlight the need to identify the underlying mechanisms linking early menarche to T2D/IGT risk.

Klíčová slova:

Physicians – Metaanalysis – Systematic reviews – Puberty – Glucose tolerance – Menarche – diabetes mellitus – Type 2 diabetes

Zdroje

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

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

3. Ahmed ML, Ong KK, Dunger DB. Childhood obesity and the timing of puberty. Trends Endocrinol Metab. 2009;20:237–42. doi: 10.1016/j.tem.2009.02.004 19541497

4. Harries M, Walker JM, Williams DM, Hawkins S, Hughes I. Changes in the male voice at puberty. Arch Dis Child. 1997;77:445–7. doi: 10.1136/adc.77.5.445 9487971

5. Sorensen K, Mouritsen A, Aksglaede L, Hagen CP, Mogensen SS, Juul A. Recent secular trends in pubertal timing: implications for evaluation and diagnosis of precocious puberty. Horm Res Paediatr 2012;77:137–45. doi: 10.1159/000336325 22508036

6. Harrington J, Palmert MR. Clinical review: distinguishing constitutional delay of growth and puberty from isolated hypogonadotropic hypogonadism: critical appraisal of available diagnostic tests. J Clin Endocrinol Metab. 2012;97:3056–67. doi: 10.1210/jc.2012-1598 22723321

7. Hosokawa M, Imazeki S, Mizunuma H, Kubota T, Hayashi K. Secular trends in age at menarche and time to establish regular menstrual cycling in Japanese women born between 1930 and 1985. BMC Womens Health. 2012;12:19. doi: 10.1186/1472-6874-12-19 22800445

8. Cho GJ, Park HT, Shin JH, Hur JY, Kim YT, Kim SH, et al. Age at menarche in a Korean population: secular trends and influencing factors. Eur J Pediatr. 2010;169:89–94. doi: 10.1007/s00431-009-0993-1 19504269

9. van der Eng P, Sohn K. The biological standard of living in Indonesia during the 20th century: evidence from the age at menarche. Econ Hum Biol. 2019;34:216–24. doi: 10.1016/j.ehb.2018.11.004 30551996

10. Kaiser AB, Zhang N, van der Pluijm W. Global prevalence of type 2 diabetes over the next ten years (2018–2028). Diabetes. 2018;67:202-LB.

11. Janghorbani M, Mansourian M, Hosseini E. Systematic review and meta-analysis of age at menarche and risk of type 2 diabetes. Acta Diabetol. 2014;51:519–28. doi: 10.1007/s00592-014-0579-x 24671509

12. Yang L, Li L, Peters SAE, Clarke R, Guo Y, Chen Y, et al. Age at menarche and incidence of diabetes: a prospective study of 300,000 women in China. Am J Epidemiol. 2018;187:190–8. doi: 10.1093/aje/kwx219 28605451

13. Au Yeung SL, Jiang C, Cheng KK, Xu L, Zhang W, Lam TH, et al. Age at menarche and cardiovascular risk factors using Mendelian randomization in the Guangzhou Biobank Cohort Study. Prev Med. 2017;101:142–8. doi: 10.1016/j.ypmed.2017.06.006 28601624

14. Evensen E, Wilsgaard T, Furberg AS, Skeie G. Tracking of overweight and obesity from early childhood to adolescence in a population-based cohort—the Tromso Study, Fit Futures. BMC Pediatr. 2016;16:64. doi: 10.1186/s12887-016-0599-5 27165270

15. Freedman DS, Khan LK, Serdula MK, Dietz WH, Srinivasan SR, Berenson GS. The relation of menarcheal age to obesity in childhood and adulthood: the Bogalusa heart study. BMC Pediatr. 2003;3:3. doi: 10.1186/1471-2431-3-3 12723990

16. Scottish Intercollegiate Guidelines Network. Search filters. Edinburgh: Scottish Intercollegiate Guidelines Network; 2019 [cited 2019 Feb 28]. Available from: https://www.sign.ac.uk/search-filters.html.

17. Dreyfus J, Jacobs DR Jr, Mueller N, Schreiner PJ, Moran A, Carnethon MR, et al. Age at menarche and cardiometabolic risk in adulthood: the Coronary Artery Risk Development in Young Adults Study. J Pediatr. 2015;167:344–52.e1. doi: 10.1016/j.jpeds.2015.04.032 25962931

18. Saquib N, Kritz-Silverstein D, Barrett-Connor E. Age at menarche, abnormal glucose tolerance and type 2 diabetes mellitus: the Rancho Bernardo Study. Climacteric. 2005;8:76–82. doi: 10.1080/13697130500062688 15804735

19. Lakshman R, Forouhi N, Luben R, Bingham S, Khaw K, Wareham N, et al. Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia. 2008;51:781–6. doi: 10.1007/s00125-008-0948-5 18320165

20. Conway BN, Shu XO, Zhang X, Xiang YB, Cai H, Li H, et al. Age at menarche, the leg length to sitting height ratio, and risk of diabetes in middle-aged and elderly Chinese men and women. PLoS ONE. 2012;7(3):e30625. doi: 10.1371/journal.pone.0030625 22448212

21. Cao X, Zhou J, Yuan H, Chen Z. Duration of reproductive lifespan and age at menarche in relation to metabolic syndrome in postmenopausal Chinese women. J Obstet Gynaecol Res. 2016;42:1581–7. doi: 10.1111/jog.13093 27718299

22. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36:1–48.

23. Levine B. What does the population attributable fraction mean? Prev Chronic Dis. 2007;4:A14-A.

24. 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

25. Stang A. Critical evaluation of the Newcastle–Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25:603–5. doi: 10.1007/s10654-010-9491-z 20652370

26. Pierce MB, Kuh D, Hardy R. The role of BMI across the life course in the relationship between age at menarche and diabetes, in a British birth cohort. Diabet Med. 2012;29:600–3. doi: 10.1111/j.1464-5491.2011.03489.x 21999522

27. Cooper GS, Ephross SA, Sandler DP. Menstrual patterns and risk of adult-onset diabetes mellitus. J Clin Epidemiol. 2000;53:1170–3. doi: 10.1016/s0895-4356(00)00240-7 11106892

28. Stockl D, Doring A, Peters A, Thorand B, Heier M, Huth C, et al. Age at menarche is associated with prediabetes and diabetes in women (aged 32–81 years) from the general population: the KORA F4 Study. Diabetologia. 2012;55:681–8. doi: 10.1007/s00125-011-2410-3 22170465

29. Elks CE, Ong KK, Scott RA, van der Schouw YT, Brand JS, Wark PA, et al. Age at menarche and type 2 diabetes risk: the EPIC-InterAct study. Diabetes Care. 2013;36:3526–34. doi: 10.2337/dc13-0446 24159179

30. Farahmand M, Tehrani FR, Dovom MR, Azizi F. Menarcheal age and risk of type 2 diabetes: a community-based cohort study. J Clin Res Pediatr Endocrinol. 2017;9:156–62. doi: 10.4274/jcrpe.3370 27840328

31. Pandeya N, Huxley RR, Chung HF, Dobson AJ, Kuh D, Hardy R, et al. Female reproductive history and risk of type 2 diabetes: a prospective analysis of 126 721 women. Diabetes Obes Metab. 2018;20:2103–12. doi: 10.1111/dom.13336 29696756

32. Heys M, Schooling CM, Jiang C, Cowling BJ, Lao X, Zhang W, et al. Age of menarche and the metabolic syndrome in China. Epidemiology. 2007;18:740–6. doi: 10.1097/EDE.0b013e3181567faf 17917601

33. Akter S, Jesmin S, Islam M, Sultana SN, Okazaki O, Hiroe M, et al. Association of age at menarche with metabolic syndrome and its components in rural Bangladeshi women. Nutr Metab (Lond). 2012;9:99.

34. Qiu C, Chen H, Wen J, Zhu P, Lin F, Huang B, et al. Associations between age at menarche and menopause with cardiovascular disease, diabetes, and osteoporosis in Chinese women. J Clin Endocrinol Metab. 2013;98:1612–21. doi: 10.1210/jc.2012-2919 23471979

35. Baek TH, Lim NK, Kim MJ, Lee J, Ryu S, Chang Y, et al. Age at menarche and its association with dysglycemia in Korean middle-aged women. Menopause. 2015;22:542–8. doi: 10.1097/GME.0000000000000353 25335102

36. Hwang E, Lee KW, Cho Y, Chung HK, Shin MJ. Association between age at menarche and diabetes in Korean post-menopausal women: results from the Korea National Health and Nutrition Examination Survey (2007–2009). Endocr J. 2015;62:897–905. doi: 10.1507/endocrj.EJ15-0192 26194132

37. Lim JS, Lee HS, Kim EY, Yi KH, Hwang JS. Early menarche increases the risk of type 2 diabetes in young and middle-aged Korean women. Diabet Med. 2015;32:521–5. doi: 10.1111/dme.12653 25441051

38. Won JC, Hong JW, Noh JH, Kim DJ. Association between age at menarche and risk factors for cardiovascular diseases in Korean women: the 2010 to 2013 Korea National Health and Nutrition Examination Survey. Medicine. 2016;95:e3580. doi: 10.1097/MD.0000000000003580 27149485

39. Yang A, Liu S, Cheng N, Pu H, Dai M, Ding J, et al. Reproductive factors and risk of type 2 diabetes in an occupational cohort of Chinese women. J Diabetes Complications. 2016;30:1217–22. doi: 10.1016/j.jdiacomp.2016.06.011 27345735

40. Nanri A, Mizoue T, Noda M, Goto A, Sawada N, Tsugane S. Menstrual and reproductive factors and type 2 diabetes risk: the Japan Public Health Center-based Prospective Study. J Diabetes Investig 2019;10:147–53. doi: 10.1111/jdi.12853 29667360

41. He C, Zhang C, Hunter DJ, Hankinson SE, Buck Louis GM, Hediger ML, et al. Age at menarche and risk of type 2 diabetes: results from 2 large prospective cohort studies. Am J Epidemiol. 2010;171:334–44. doi: 10.1093/aje/kwp372 20026580

42. Dreyfus JG, Lutsey PL, Huxley R, Pankow JS, Selvin E, Fernandez-Rhodes L, et al. Age at menarche and risk of type 2 diabetes among African-American and white women in the Atherosclerosis Risk in Communities (ARIC) study. Diabetologia. 2012;55:2371–80. doi: 10.1007/s00125-012-2616-z 22760786

43. Mueller NT, Duncan BB, Barreto SM, Chor D, Bessel M, Aquino EM, et al. Earlier age at menarche is associated with higher diabetes risk and cardiometabolic disease risk factors in Brazilian adults: Brazilian Longitudinal Study of Adult Health (ELSA-Brasil). Cardiovasc Diabetol. 2014;13:22. doi: 10.1186/1475-2840-13-22 24438044

44. LeBlanc ES, Kapphahn K, Hedlin H, Desai M, Parikh NI, Liu S, et al. Reproductive history and risk of type 2 diabetes mellitus in postmenopausal women: findings from the Women’s Health Initiative. Menopause. 2017;24:64–72. doi: 10.1097/GME.0000000000000714 27465714

45. Petersohn I, Zarate-Ortiz AG, Cepeda-Lopez AC, Melse-Boonstra A. Time trends in age at menarche and related non-communicable disease risk during the 20th century in Mexico. Nutrients. 2019;11:394.

46. Terry MB, Ferris JS, Tehranifar P, Wei Y, Flom JD. Birth weight, postnatal growth, and age at menarche. Am J Epidemiol 2009;170:72–9. doi: 10.1093/aje/kwp095 19439580

47. Li W, Liu Q, Deng X, Chen Y, Liu S, Story M. Association between obesity and puberty timing: a systematic review and meta-analysis. Int J Environ Res Public Health 2017;14:1266.

48. Mumby HS, Elks CE, Li S, Sharp SJ, Khaw KT, Luben RN, et al. Mendelian randomisation study of childhood BMI and early menarche. J Obes. 2011;2011:180729. doi: 10.1155/2011/180729 21773002

49. Trikudanathan S, Pedley A, Massaro JM, Hoffmann U, Seely EW, Murabito JM, et al. Association of female reproductive factors with body composition: the Framingham Heart Study. J Clin Endocrinol Metab. 2013;98:236–44. doi: 10.1210/jc.2012-1785 23093491

50. Al-Goblan AS, Al-Alfi MA, Khan MZ. Mechanism linking diabetes mellitus and obesity. Diabetes Metab Syndr Obes. 2014;7:587–91. doi: 10.2147/DMSO.S67400 25506234

51. Eriksson JG, Forsen TJ, Osmond C, Barker DJP. Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care. 2003;26:3006–10. doi: 10.2337/diacare.26.11.3006 14578231

52. Vihko R, Apter D. Endocrine characteristics of adolescent menstrual cycles: impact of early menarche. J Steroid Biochem. 1984;20:231–6. doi: 10.1016/0022-4731(84)90209-7 6231419

53. Apter D, Vihko R. Early menarche, a risk factor for breast cancer, indicates early onset of ovulatory cycles. J Clin Endocrinol Metab. 1983;57:82–6. doi: 10.1210/jcem-57-1-82 6222061

54. Thankamony A, Ong KK, Ahmed ML, Ness AR, Holly JM, Dunger DB. Higher levels of IGF-I and adrenal androgens at age 8 years are associated with earlier age at menarche in girls. J Clin Endocrinol Metab 2012;97:E786–90. doi: 10.1210/jc.2011-3261 22419724

55. Ding EL, Song Y, Malik VS, Liu S. Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA. 2006;295:1288–99. doi: 10.1001/jama.295.11.1288 16537739

56. O’Reilly MW, Glisic M, Kumarendran B, Subramanian A, Manolopoulos KN, Tahrani AA, et al. Serum testosterone, sex hormone-binding globulin and sex-specific risk of incident type 2 diabetes in a retrospective primary care cohort. Clin Endocrinol (Oxf). 2019;90:145–54.

57. Perry JR, Weedon MN, Langenberg C, Jackson AU, Lyssenko V, Sparso T, et al. Genetic evidence that raised sex hormone binding globulin (SHBG) levels reduce the risk of type 2 diabetes. Hum Mol Genet. 2010;19:535–44. doi: 10.1093/hmg/ddp522 19933169

58. Salpeter SR, Walsh JM, Ormiston TM, Greyber E, Buckley NS, Salpeter EE. Meta-analysis: effect of hormone-replacement therapy on components of the metabolic syndrome in postmenopausal women. Diabetes Obes Metab. 2006;8:538–54. doi: 10.1111/j.1463-1326.2005.00545.x 16918589

59. Clegg D, Hevener AL, Moreau KL, Morselli E, Criollo A, Van Pelt RE, et al. Sex hormones and cardiometabolic health: role of estrogen and estrogen receptors. Endocrinology. 2017;158:1095–105. doi: 10.1210/en.2016-1677 28323912

60. Must A, Phillips SM, Naumova EN, Blum M, Harris S, Dawson-Hughes B, et al. Recall of early menstrual history and menarcheal body size: after 30 years, how well do women remember? Am J Epidemiol. 2002;155:672–9. doi: 10.1093/aje/155.7.672 11914195

61. Cooper R, Blell M, Hardy R, Black S, Pollard TM, Wadsworth ME, et al. Validity of age at menarche self-reported in adulthood. J Epidemiol Community Health 2006;60:993–7. doi: 10.1136/jech.2005.043182 17053289