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Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis

Abstract

Obesity has complex multifactorial aetiology. It has been suggested by many, but not all, reports that earlier pubertal maturation may increase adult obesity risk. We conducted a systemic review and meta-analysis in both women and men, and hypothesised that any association between pubertal timing and adult obesity is likely to be confounded by childhood adiposity. In addition, we investigated whether pubertal timing is related to other cardiometabolic risk and long-term cardiovascular morbidity/mortality. Literature search was undertaken using MEDLINE, EMBASE, Web of Knowledge and TRIP databases, with a hand search of references. Both authors independently reviewed and extracted pre-defined data from all selected papers. Meta-analyses were conducted using Review Manager (RevMan) 5.0.24. A total of 48 papers were identified. Out of 34 studies, 30 reported an inverse relationship between pubertal timing and adult body mass index (BMI), the main adiposity measure used. Meta-analysis of 10 cohorts showed association between early menarche (menarche <12 vs 12 years) and increased adult BMI, with a standardised mean difference of 0.34 kg m−2 (95% confidence interval: 0.33–0.34). Heterogeneity was large (I2=92%) but reduced significantly when grouped by outcome age. Late menarche (menarche 15 vs <15 years) was associated with decreased adult BMI, with a standardised mean difference of −0.26 kg m−2 (95% confidence interval: −0.36, −0.21) (seven cohorts). Only eight papers included data on childhood BMI; the majority reported that childhood BMI only partially attenuated association between early menarche and later obesity. Although not suitable for meta-analysis, data on cardiometabolic risk factors and puberty suggested negative association between earlier pubertal timing and cardiovascular mortality, hypertension, metabolic syndrome (MetS) and abnormal glycaemia. Earlier pubertal timing is predictive of higher adult BMI and greater risk of obesity. This effect appears to be partially independent of childhood BMI. Earlier pubertal development appears to also be inversely correlated with risk of other cardiometabolic risk factors and cardiovascular mortality. Further work is needed to examine potential mechanisms and the level at which interventions may be targeted.

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References

  1. Parsons TJ, Power C, Logan S, Summerbell CD . Childhood predictors of adult obesity: a systematic review. Int J Obes Relat Metab Disord 1999; 23 (Suppl 8): S1–S107.

    PubMed  Google Scholar 

  2. Kaplowitz P . Pubertal development in girls: secular trends. Curr Opin Obstet Gynecol 2006; 18: 487–491.

    Article  PubMed  Google Scholar 

  3. Sorensen K, Aksglaede L, Petersen JH, Juul A . Recent changes in pubertal timing in healthy Danish boys: associations with body mass index. J Clin Endocrinol Metab 2010; 95: 263–270.

    Article  PubMed  Google Scholar 

  4. Ong KK, Emmett P, Northstone K, Golding J, Rogers I, Ness AR et al. Infancy weight gain predicts childhood body fat and age at menarche in girls. J Clin Endocrinol Metab 2009; 94: 1527–1532.

    CAS  Article  PubMed  Google Scholar 

  5. Ong KK . Early determinants of obesity. Endocr Dev 2010; 19: 53–61.

    Article  PubMed  Google Scholar 

  6. Burt Solorzano CM, McCartney CR . Obesity and the pubertal transition in girls and boys. Reproduction 2010; 140: 399–410.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hartge P . Genetics of reproductive lifespan. Nat Genet 2009; 41: 637–638.

    CAS  Article  PubMed  Google Scholar 

  8. Golub MS, Collman GW, Foster PM, Kimmel CA, Rajpert-De Meyts E, Reiter EO et al. Public health implications of altered puberty timing. Pediatrics 2008; 121 (Suppl 3): S218–S230.

    Article  PubMed  Google Scholar 

  9. Walvoord EC . The timing of puberty: is it changing? Does it matter? J Adolesc Health 2010; 47: 433–439.

    Article  PubMed  Google Scholar 

  10. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2010; 283: 2008–2012.

    Article  Google Scholar 

  11. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP . The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007; 370: 1453–1457.

    Article  PubMed  Google Scholar 

  12. Moher D, Liberati A, Tetzlaff J, Altman DG . Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009; 62: 1006–1012.

    Article  PubMed  Google Scholar 

  13. Altman DG . Systematic reviews of evaluations of prognostic variables. BMJ 2001; 323: 224–228.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Mi J, Chen FF, Wang YF, Cheng H, Hou DQ, Zhao XY . Impact of early menarche on adiposity during late puberty and mid-life. Zhonghua Liu Xing Bing Xue Za Zhi 2007; 28: 833–837.

    PubMed  Google Scholar 

  15. Kirchengast S, Gruber D, Sator M, Huber J . Impact of the age at menarche on adult body composition in healthy pre- and postmenopausal women. Am J Phys Anthropol 1998; 105: 9–20.

    CAS  Article  PubMed  Google Scholar 

  16. Pierce MB, Leon DA . Age at menarche and adult BMI in the Aberdeen children of the 1950s cohort study. Am J Clin Nutr 2005; 82: 733–739.

    CAS  Article  PubMed  Google Scholar 

  17. Laitinen J, Power C, Jarvelin MR . Family social class, maternal body mass index, childhood body mass index, and age at menarche as predictors of adult obesity. Am J Clin Nutr 2001; 74: 287–294.

    CAS  Article  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Power C, Lake JK, Cole TJ . Body mass index and height from childhood to adulthood in the 1958 British born cohort. Am J Clin Nutr 1997; 66: 1094–1101.

    CAS  Article  PubMed  Google Scholar 

  20. Sandhu J, Ben-Shlomo Y, Cole TJ, Holly J, Davey Smith G . The impact of childhood body mass index on timing of puberty, adult stature and obesity: a follow-up study based on adolescent anthropometry recorded at Christ’s Hospital (1936–1964). Int J Obes (Lond) 2006; 30: 14–22.

    CAS  Article  Google Scholar 

  21. He C, Zhang C, Hunter DJ, Hankinson SE, Buck Louis GM, Hankinson SE et al. Age at menarche and risk of type 2 diabetes: results from 2 large prospective cohort studies. Am J Epidemiol 2010; 171: 334–344.

    Article  PubMed  Google Scholar 

  22. Kivimaki M, Lawlor DA, Smith GD, Elovainio M, Jokela M, Keltikangas-Jarvinen L et al. Association of age at menarche with cardiovascular risk factors, vascular structure, and function in adulthood: the Cardiovascular Risk in Young Finns study. Am J Clin Nutr 2008; 87: 1876–1882.

    CAS  Article  PubMed  Google Scholar 

  23. Hulanicka B, Lipowicz A, Koziel S, Kowalisko A . Relationship between early puberty and the risk of hypertension/overweight at age 50: evidence for a modified Barker hypothesis among Polish youth. Econ Hum Biol 2007; 5: 48–60.

    Article  PubMed  Google Scholar 

  24. Hardy R, Kuh D, Whincup PH, Wadsworth ME . Age at puberty and adult blood pressure and body size in a British birth cohort study. J Hypertens 2006; 24: 59–66.

    CAS  Article  PubMed  Google Scholar 

  25. van Lenthe FJ, Kemper CG, van Mechelen W . Rapid maturation in adolescence results in greater obesity in adulthood: the Amsterdam Growth and Health Study. Am J Clin Nutr 1996; 64: 18–24.

    CAS  Article  PubMed  Google Scholar 

  26. Beunen G, Malina RM, Lefevre J, Claessens AL, Renson R, Simons J et al. Size, fatness and relative fat distribution of males of contrasting maturity status during adolescence and as adults. Int J Obes Relat Metab Disord 1994; 18: 670–678.

    CAS  PubMed  Google Scholar 

  27. Sun SS, Schubert CM . Prolonged juvenile States and delay of cardiovascular and metabolic risk factors: the Fels Longitudinal study. J Pediatr 2009; 155: e1–e6.

    Article  Google Scholar 

  28. Taeymans J, Hebbelinck M, Borms J, Clarys P, Abidi H, Duquet W . Tracking of adult adiposity in early, average and late maturing children: a thirty year longitudinal growth study. J Sports Med Phys Fitness 2008; 48: 326–334.

    CAS  PubMed  Google Scholar 

  29. Lakshman R, Forouhi NG, Sharp SJ, Luben R, Bingham SA, Khaw KT et al. Early age at menarche associated with cardiovascular disease and mortality. J Clin Endocrinol Metab 2009; 94: 4953–4960.

    CAS  Article  PubMed  Google Scholar 

  30. Cooper GS, Ephross SA, Weinberg CR, Baird DD, Whelan EA, Sandler DP et al. Menstrual and reproductive risk factors for ischemic heart disease. Epidemiology 1999; 10: 255–259.

    CAS  Article  PubMed  Google Scholar 

  31. La Vecchia C, Decarli A, Franceschi S, Gentile A, Negri E, Parazzini F . Menstrual and reproductive factors and the risk of myocardial infarction in women under fifty-five years of age. Am J Obstet Gynecol 1987; 157: 1108–1112.

    CAS  Article  PubMed  Google Scholar 

  32. Jacobsen BK, Oda K, Knutsen SF, Fraser GE . Age at menarche, total mortality and mortality from ischaemic heart disease and stroke: the Adventist Health Study, 1976-88. Int J Epidemiol 2009; 38: 245–252.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 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: 740–746.

    Article  PubMed  Google Scholar 

  34. Feng Y, Hong X, Wilker E, Li Z, Zhang W, Jin D et al. Effects of age at menarche, reproductive years, and menopause on metabolic risk factors for cardiovascular diseases. Atherosclerosis 2008; 196: 590–597.

    CAS  Article  PubMed  Google Scholar 

  35. Emaus A, Espetvedt S, Veierod MB, Ballard-Barbash R, Furberg AS, Ellison PT et al. 17-Beta-estradiol in relation to age at menarche and adult obesity in premenopausal women. Hum Reprod 2008; 23: 919–927.

    CAS  Article  PubMed  Google Scholar 

  36. Frontini MG, Srinivasan SR, Berenson GS . Longitudinal changes in risk variables underlying metabolic Syndrome X from childhood to young adulthood in female subjects with a history of early menarche: the Bogalusa Heart Study. Int J Obes Relat Metab Disord 2003; 27: 1398–1404.

    CAS  Article  PubMed  Google Scholar 

  37. Cho GJ, Park HT, Shin JH, Kim T, Hur JY, Kim YT et al. The relationship between reproductive factors and metabolic syndrome in Korean postmenopausal women: Korea National Health and Nutrition Survey 2005. Menopause 2009; 16: 998–1003.

    Article  PubMed  Google Scholar 

  38. Santos AC, Ebrahim S, Barros H . Gender, socio-economic status and metabolic syndrome in middle-aged and old adults. BMC Public Health 2008; 8: 62.

    Article  PubMed  PubMed Central  Google Scholar 

  39. 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.

    CAS  Article  PubMed  Google Scholar 

  40. de Kleijn MJ, van der Schouw YT, van der Graaf Y . Reproductive history and cardiovascular disease risk in postmenopausal women: a review of the literature. Maturitas 1999; 33: 7–36.

    CAS  Article  PubMed  Google Scholar 

  41. Cheng G, Buyken AE, Shi L, Karaolis-Danckert N, Kroke A et al. Beyond overweight: nutrition as an important lifestyle factor influencing timing of puberty. Nutr Rev 2012; 70: 133–152.

    Article  PubMed  Google Scholar 

  42. Elks CE, Perry JR, Sulem P, Chasman DI, Franceschini N, He C et al. Thirty new loci for age at menarche identified by a meta-analysis of genome-wide association studies. Nat Genet 2010; 42: 1077–1085.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 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: 993–997.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 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: 672–679.

    CAS  Article  PubMed  Google Scholar 

  45. Patton GC, Viner R . Pubertal transitions in health. Lancet 2007; 369: 1130–1139.

    Article  PubMed  Google Scholar 

  46. Keim SA, Branum AM, Klebanoff MA, Zemel BS . Maternal body mass index and daughters’ age at menarche. Epidemiology 2009; 20: 677–681.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Ong KK, Northstone K, Wells JC, Rubin C, Ness AR, Golding J et al. Earlier mother’s age at menarche predicts rapid infancy growth and childhood obesity. PLoS Med 2007; 4: e132.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Harris MA, Prior JC, Koehoorn M . Age at menarche in the Canadian population: secular trends and relationship to adulthood BMI. J Adolesc Health 2008; 43: 548–554.

    Article  PubMed  Google Scholar 

  49. Cui R, Iso H, Toyoshima H, Date C, Yamamoto A, Kikuchi S et al. Relationships of age at menarche and menopause, and reproductive year with mortality from cardiovascular disease in Japanese postmenopausal women: the JACC study. J Epidemiol 2006; 16: 177–184.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Must A, Naumova EN, Phillips SM, Blum M, Dawson-Hughes B, Rand WM et al. Childhood overweight and maturational timing in the development of adult overweight and fatness: the Newton Girls Study and its follow-up. Pediatrics 2005; 116: 620–627.

    Article  PubMed  Google Scholar 

  51. Newby PK, Dickman PW, Adami HO, Wolk A . Early anthropometric measures and reproductive factors as predictors of body mass index and obesity among older women. Int J Obes (Lond) 2005; 29: 1084–1092.

    CAS  Article  Google Scholar 

  52. Wen W, Gao YT, Shu XO, Yang G, Li HL, Jin F et al. Sociodemographic, behavioral, and reproductive factors associated with weight gain in Chinese women. Int J Obes Relat Metab Disord 2003; 27: 933–940.

    CAS  Article  PubMed  Google Scholar 

  53. Lahmann PH, Lissner L, Gullberg B, Berglund G . Sociodemographic factors associated with long-term weight gain, current body fatness and central adiposity in Swedish women. Int J Obes Relat Metab Disord 2000; 24: 685–694.

    CAS  Article  PubMed  Google Scholar 

  54. van Lenthe FJ, Kemper HC, van Mechelen W, Post GB, Twisk JW, Welten DC et al. Biological maturation and the distribution of subcutaneous fat from adolescence into adulthood: the Amsterdam Growth and Health Study. Int J Obes Relat Metab Disord 1996; 20: 121–129.

    CAS  PubMed  Google Scholar 

  55. Troisi RJ, Wolf AM, Mason JE, Klingler KM, Colditz GA . Relation of body fat distribution to reproductive factors in pre- and postmenopausal women. Obes Res 1995; 3: 143–151.

    CAS  Article  PubMed  Google Scholar 

  56. Helm P, Munster K, Schmidt L . Recalled menarche in relation to infertility and adult weight and height. Acta Obstet Gynecol Scand 1995; 74: 718–722.

    CAS  Article  PubMed  Google Scholar 

  57. Burke GL, Savage PJ, Manolio TA, Sprafka JM, Wagenknecht LE, Sidney S et al. Correlates of obesity in young black and white women: the CARDIA Study. Am J Public Health 1992; 82: 1621–1625.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. den Tonkelaar I, Seidell JC, van Noord PA, Baanders-van Halewijn EA, Ouwehand IJ . Fat distribution in relation to age, degree of obesity, smoking habits, parity and estrogen use: a cross-sectional study in 11,825 Dutch women participating in the DOM-project. Int J Obes 1990; 14: 753–761.

    CAS  PubMed  Google Scholar 

  59. Kaye SA, Folsom AR, Prineas RJ, Potter JD, Gapstur SM . The association of body fat distribution with lifestyle and reproductive factors in a population study of postmenopausal women. Int J Obes 1990; 14: 583–591.

    CAS  PubMed  Google Scholar 

  60. Frisancho AR, Housh CH . The relationship of maturity rate to body size and body proportions in children and adults. Hum Biol 1988; 60: 759–770.

    CAS  PubMed  Google Scholar 

  61. Bjorkelund C, Lissner L, Andersson S, Lapidus L, Bengtsson C . Reproductive history in relation to relative weight and fat distribution. Int J Obes Relat Metab Disord 1996; 20: 213–219.

    CAS  PubMed  Google Scholar 

  62. Garn SM, LaVelle M, Rosenberg KR, Hawthorne VM . Maturational timing as a factor in female fatness and obesity. Am J Clin Nutr 1986; 43: 879–883.

    CAS  Article  PubMed  Google Scholar 

  63. Sherman B, Wallace R, Bean J, Schlabaugh L . Relationship of body weight to menarcheal and menopausal age: implications for breast cancer risk. J Clin Endocrinol Metab 1981; 52: 488–493.

    CAS  Article  PubMed  Google Scholar 

  64. Bertuccio P, Tavani A, Gallus S, Negri E, La Vecchia C . Menstrual and reproductive factors and risk of non-fatal acute myocardial infarction in Italy. Eur J Obstet Gynecol Reprod Biol 2007; 134: 67–72.

    Article  PubMed  Google Scholar 

  65. Rosenberg L, Palmer JR, Rao RS, Adams-Campbell LL . Risk factors for coronary heart disease in African American women. Am J Epidemiol 1999; 150: 904–909.

    CAS  Article  PubMed  Google Scholar 

  66. Palmer JR, Rosenberg L, Shapiro S . Reproductive factors and risk of myocardial infarction. Am J Epidemiol 1992; 136: 408–416.

    CAS  Article  PubMed  Google Scholar 

  67. Colditz GA, Willett WC, Stampfer MJ, Rosner B, Speizer FE, Hennekens CH et al. A prospective study of age at menarche, parity, age at first birth, and coronary heart disease in women. Am J Epidemiol 1987; 126: 861–870.

    CAS  Article  PubMed  Google Scholar 

  68. Oliver MF . Ischaemic heart disease in young women. BMJ 1974; 4: 253–259.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Cooper GS, Ephross SA, Sandler DP . Menstrual patterns and risk of adult-onset diabetes mellitus. J Clin Epidemiol 2000; 53: 1170–1173.

    CAS  Article  PubMed  Google Scholar 

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Correspondence to P Prentice.

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PP and RV both contributed substantially to the conception and design of the review, and the acquisition, analysis and interpretation of data. Both authors wrote and approved the paper for publication.

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Prentice, P., Viner, R. Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis. Int J Obes 37, 1036–1043 (2013). https://doi.org/10.1038/ijo.2012.177

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Keywords

  • puberty
  • cardiovascular disease
  • metabolic syndrome

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