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Systematic review and meta-analysis of age at menarche and risk of type 2 diabetes

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Abstract

The relation of early menarche with type 2 diabetes mellitus (T2DM) remains inconsistent across studies. The objective of this systematic review and meta-analysis of published population-based observational studies was to assess the association between age at menarche and T2DM risk. We searched online data bases through December 2013 and examined the reference lists of pertinent articles. Summary relative risks (RRs) with 95 % confidence intervals (CIs) were calculated with a random-effects model. A total of 14 effect estimates from 10 eligible studies (three cross-sectional and seven cohort studies) included 315,428 participants and 22,085 cases of T2DM. Compared with the highest or middle category, women in the lowest category of age at menarche had higher risk of T2DM [summary RR (95 % CI) 1.22 (1.17, 1.28)]. These results were consistent between studies that conducted in the United States and in Europe. The association between age at menarche and T2DM was slightly stronger for cohort than for cross-sectional studies. These findings strongly support an association between younger age at menarche and increased risk of T2DM. Age at menarche may help identify women with increased risk of developing T2DM.

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References

  1. Euling SY, Herman-Giddens ME, Lee PA, Lee PA, Selevan SG, Juul A et al (2008) Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics 121(Suppl 3):S172–S191

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  3. Hu FB (2003) Overweight and obesity in women: health risks and consequences. J Women Health 12:163–172

    Article  Google Scholar 

  4. Colagiuri S, Borch-Johnsen K, Glümer C, Vistisen D (2005) There really is an epidemic of type 2 diabetes. Diabetologia 48:1459–1463

    Article  CAS  PubMed  Google Scholar 

  5. Coleman L, Coleman J (2002) The measurement of puberty: a review. J Adolesc 25:535–550

    Article  PubMed  Google Scholar 

  6. Must A, Phillips SM, Naumova EN, Blum M, Harris S, Dawson-Hughes B et al (2002) Recall of early menstrual history and menarcheal body size: after 30 years, how well do women remember? Am J Epidemiol 155:672–679

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Lakshman R, Forouhi N, Luben R, Bingham S, Khaw K, Wareham N et al (2008) Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia 51:781–786

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  10. Saquib N, Kritz-Silverstein D, Barrett-Connor E (2005) Age at menarche, abnormal glucose tolerance and type 2 diabetes mellitus: the Rancho Bernardo Study. Climacteric 8:76–82

    Article  CAS  PubMed  Google Scholar 

  11. Frontini MG, Srinivasan SR, Berenson GS (2003) 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 27:1398–1404

    Article  CAS  PubMed  Google Scholar 

  12. Heys M, Schooling CM, Jiang C, Cowling BJ, Lao X, Zhang W, Cheng KK et al (2007) Age of menarche and the metabolic syndrome in China. Epidemiology 18:740–746

    Article  PubMed  Google Scholar 

  13. Remsberg KE, Demerath EW, Schubert CM, Chumlea WC, Sun SS, Siervogel RM (2005) Early menarche and the development of cardiovascular disease risk factors in adolescent girls: the Fels Longitudinal Study. J Clin Endocrinol Metab 90:2718–2724

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Kivimäki M, Lawlor DA, Smith GD, Elovainio M, Jokela M, Keltikangas-Järvinen L et al (2008) 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 87:1876–1882

    PubMed  Google Scholar 

  16. Chen L, Zhang C, Yeung E, Ye A, Mumford SL, Wactawski-Wende J, Schisterman EF (2011) Age at menarche and metabolic markers for type 2 diabetes in premenopausal women: the BioCycle Study. J Clin Endocrinol Metab 96:E1007–E1012

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Dreyfus JG, Lutsey PL, Huxley R, Pankow JS, Selvin E, Fernández-Rhodes L et al (2012) Age at menarche and risk of type 2 diabetes among African–American and white women in the Atherosclerosis Risk in Communities (ARIC) study. Diabetologia 55:2371–2380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Pierce MB, Kuh D, Hardy R (2012) The role of BMI across the life course in the relationship between age at menarche and diabetes, in a British Birth Cohort. Diabet Med 29:600–603

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Stockl D, Doring A, Peters A, Thorand B, Heier M, Huth C et al (2012) Age at menarche is associated with prediabetes and diabetes in women (aged 32–81 years) from the general population: the KORA F4 Study. Diabetologia 55:681–688

    Article  CAS  PubMed  Google Scholar 

  20. Qiu C, Chen H, Wen J, Zhu P, Lin F, Huang B et al (2013) Associations between age at menarche and menopause with cardiovascular disease, diabetes, and osteoporosis in Chinese women. J Clin Endocrinol Metab 98:1612–1621

    Article  CAS  PubMed  Google Scholar 

  21. Vazquez G, Duval S, Jacobs DR Jr, Silventoinen K (2007) Comparison of body mass index, waist circumference, and waist/hip ratio in predicting incident diabetes: a meta-analysis. Epidemiol Rev 29:115–128

    Article  PubMed  Google Scholar 

  22. Janghorbani M, Amini M (2010) Comparison of body mass index with abdominal obesity indicators and waist-to-stature ratio for prediction of type 2 diabetes: the Isfahan Diabetes Prevention Study. Obes Res Clin Pract 4:e25–e32

    Article  Google Scholar 

  23. Himes JH, Obarzanek E, Baranowski T, Wilson DM, Rochon J, McClanahan BS (2004) Early sexual maturation, body composition, and obesity in African–American girls. Obes Res 12(Suppl):64S–72S

    Article  PubMed  Google Scholar 

  24. Demerath EW, Li J, Sun SS, Chumlea WC, Remsberg KE, Czerwinski SA et al (2004) Fifty-year trends in serial body mass index during adolescence in girls: the Fels Longitudinal Study. Am J Clin Nutr 80:441–446

    CAS  PubMed  Google Scholar 

  25. Adair LS, Gordon-Larsen P (2001) Maturational timing and overweight prevalence in US adolescent girls. Am J Public Health 91:642–644

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012

    Article  CAS  PubMed  Google Scholar 

  27. Elks CE, Ong KK, Scott RA, van der Schouw YT, Brand JS, Wark PA et al (2013) Age at menarche and type 2 diabetes risk: the EPIC-InterAct study. Diabetes Care 36:3526–3534

    Article  PubMed  Google Scholar 

  28. Conway BN, Shu XO, Zhang X, Xiang YB, Cai H, Li H, Yang G et al (2012) 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 7:e30625

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30

    CAS  PubMed  Google Scholar 

  30. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  CAS  PubMed  Google Scholar 

  31. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  PubMed  Google Scholar 

  32. Higgins JP, Green S, eds (2011) Cochrane handbook for systematic reviews of interventions. Version 5.1.0. The Cochran Collaboration 2011. www.cochrane-handbook.org

  33. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Br Med J 315:629–634

    Article  CAS  Google Scholar 

  34. Egger M, Smith GD, Altman DG (2001) Systematic reviews in health care: meta-analysis in context. BMJ Publishing Group, London

    Book  Google Scholar 

  35. Sutton AJ, Duval SJ, Tweedie RL, Abrams KR, Jones DR (2000) Empirical assessment of effect of publication bias on meta-analyses. Br Med J 320:1574–1577

    Article  CAS  Google Scholar 

  36. Strotmeyer ES, Steenkiste AR, Foley TP Jr, Berga SL, Dorman JS (2003) Menstrual cycle differences between women with type 1 diabetes and women without diabetes. Diabetes Care 26:1016–1021

    Article  PubMed  Google Scholar 

  37. Casey VA, Dwyer JT, Coleman KA, Krall EA, Gardner J, Valadian I (1991) Accuracy of recall by middle-aged participants in a longitudinal study of their body size and indices of maturation earlier in life. Ann Hum Biol 18:155–166

    Article  CAS  PubMed  Google Scholar 

  38. Ding EL, Song Y, Malik VS, Liu S (2006) Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 295:1288–1299

    Article  CAS  PubMed  Google Scholar 

  39. Vikan T, Schirmer H, Njølstad I, Svartberg J (2010) Low testosterone and sex hormone-binding globulin levels and high estradiol levels are independent predictors of type 2 diabetes in men. Eur J Endocrinol 162:747–754

    Article  CAS  PubMed  Google Scholar 

  40. Zhu H, Shyh-Chang N, Segrè AV et al (2011) The Lin28/let-7 axis regulates glucose metabolism. Cell 147:81–94

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Conflict of interest

Mohsen Janghorbani, Marjan Mansourian and Elham Hosseini declare they have no conflict of interest.

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This article does not contain any studies with human or animal subjects performed by the any of the authors.

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Authors and Affiliations

  1. Department of Epidemiology and Biostatistics, School of Public Health, Isfahan University of Medical Sciences, Esfahān, Iran

    Mohsen Janghorbani & Marjan Mansourian

  2. Isfahan Endocrine and Metabolism Research Center, Isfahan University of Medical Sciences, Esfahān, Iran

    Mohsen Janghorbani & Elham Hosseini

Authors
  1. Mohsen Janghorbani
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  2. Marjan Mansourian
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  3. Elham Hosseini
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Correspondence to Mohsen Janghorbani.

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Janghorbani, M., Mansourian, M. & Hosseini, E. Systematic review and meta-analysis of age at menarche and risk of type 2 diabetes. Acta Diabetol 51, 519–528 (2014). https://doi.org/10.1007/s00592-014-0579-x

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  • DOI: https://doi.org/10.1007/s00592-014-0579-x

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