Early and late menarche are associated with oligomenorrhea and predict metabolic syndrome 26 years later

Metabolism: Clinical and Experimental

Volumn 62, Issue 11, 2013, Pages 1597-1606

  Glueck, Charles J ^a   Morrison, John A ^a   Wang, Ping ^a   Woo, Jessica G ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Cardiometabolic abnormalities; Early menarche; Late menarche; Metabolic syndrome; Oligomenorrhea

Indexed keywords

ADOLESCENT; ADULT; ADULTHOOD; ARTICLE; BODY MASS; CHILD; DISEASE ASSOCIATION; FEMALE; HUMAN; HYPERTENSION; LIPID BLOOD LEVEL; LOGISTIC REGRESSION ANALYSIS; MAJOR CLINICAL STUDY; MENARCHE; MENSTRUAL CYCLE; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; OLIGOMENORRHEA; ONSET AGE; PRIMARY PREVENTION; PRIORITY JOURNAL; RISK FACTOR;

95% CI; 95% CONFIDENCE INTERVALS; BMI; BODY MASS INDEX; CARDIOMETABOLIC ABNORMALITIES; DBP; DIASTOLIC BLOOD PRESSURE; EARLY MENARCHE; HDLC; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LATE MENARCHE; LDLC; LIPID RESEARCH CLINICS; LOW-DENSITY LIPOPROTEIN CHOLESTEROL; LRC; METABOLIC SYNDROME; METS; ODDS RATIO; OLIGOMENORRHEA; OR; PFS; PRINCETON FOLLOW-UP STUDY; SBP; SYSTOLIC BLOOD PRESSURE; TG; TRIGLYCERIDE;

ADOLESCENT; ADULT; BIOLOGICAL MARKERS; BLOOD GLUCOSE; BLOOD PRESSURE; BODY MASS INDEX; CHILD; CHILD, PRESCHOOL; CHOLESTEROL, HDL; FEMALE; FOLLOW-UP STUDIES; HUMANS; LOGISTIC MODELS; MENARCHE; METABOLIC SYNDROME X; MIDDLE AGED; ODDS RATIO; OLIGOMENORRHEA; PREDICTIVE VALUE OF TESTS; PROSPECTIVE STUDIES; RISK FACTORS; TIME FACTORS; TRIGLYCERIDES; UNITED STATES; YOUNG ADULT;

EID: 84886435698     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2013.07.005     Document Type: Article

References (71)

1. W.A. Wattigney, S.R. Srinivasan, and W. Chen Secular trend of earlier onset of menarche with increasing obesity in black and white girls: the Bogalusa Heart Study Ethn Dis 9 1999 181 189
2. P. Kaplowitz Pubertal development in girls: secular trends Curr Opin Obstet Gynecol 18 2006 487 491 (Pubitemid 44319019)
3. R.E. Frisch Body fat, puberty and fertility Biol Rev Camb Philos Soc 59 1984 161 188
4. S.M. Garn, M. LaVelle, and K.R. Rosenberg Maturational timing as a factor in female fatness and obesity Am J Clin Nutr 43 1986 879 883 (Pubitemid 16067729)
5. A.D. Rodrigues, H. Theodoro, and K.G. Mendes Factors associated with metabolic syndrome in climacteric women of southern Brazil Climacteric 16 1 2013 96 103
6. S. Akter, S. Jesmin, and M. Islam Association of age at menarche with metabolic syndrome and its components in rural Bangladeshi women Nutr Metab (Lond) 9 2012 99
7. D. Stockl, C. Meisinger, and A. Peters Age at menarche and its association with the metabolic syndrome and its components: results from the KORA F4 study PLoS One 6 2011 e26076
8. J. Mi, F.F. Chen, and Y.F. Wang Impact of early menarche on adiposity during late puberty and mid-life Zhonghua Liu Xing Bing Xue Za Zhi 28 2007 833 837
9. D. Stockl, A. Doring, and A. Peters 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 2012 681 688
10. L. Ibanez, A. Lopez-Bermejo, and M. Diaz Early metformin therapy (age 8-12 years) in girls with precocious pubarche to reduce hirsutism, androgen excess, and oligomenorrhea in adolescence J Clin Endocrinol Metab 96 2011 E1262 E1267
11. R. Lakshman, N.G. Forouhi, and S.J. Sharp Early age at menarche associated with cardiovascular disease and mortality J Clin Endocrinol Metab 94 2009 4953 4960
12. M. Kivimaki, D.A. Lawlor, and G.D. Smith 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 2008 1876 1882 (Pubitemid 351872654)
13. S.Y. Kimm, B.A. Barton, and E. Obarzanek Racial divergence in adiposity during adolescence: the NHLBI Growth and Health Study Pediatrics 107 2001 E34
14. K. Tamakoshi, H. Yatsuya, and A. Tamakoshi Early age at menarche associated with increased all-cause mortality Eur J Epidemiol 26 2011 771 778
15. M.H. van Hooff, F.J. Voorhorst, and M.B. Kaptein Insulin, androgen, and gonadotropin concentrations, body mass index, and waist to hip ratio in the first years after menarche in girls with regular menstrual cycles, irregular menstrual cycles, or oligomenorrhea J Clin Endocrinol Metab 85 2000 1394 1400 (Pubitemid 32289479)
16. M.H. van Hooff, F.J. Voorhorst, and M.B. Kaptein Polycystic ovaries in adolescents and the relationship with menstrual cycle patterns, luteinizing hormone, androgens, and insulin Fertil Steril 74 2000 49 58 (Pubitemid 30427272)
17. C.J. Glueck, J.A. Morrison, and S. Daniels Sex hormone-binding globulin, oligomenorrhea, polycystic ovary syndrome, and childhood insulin at age 14 years predict metabolic syndrome and class III obesity at age 24 years J Pediatr 159 2011 308 313e2
18. D. Apter, and R. Vihko Endocrine determinants of fertility: serum androgen concentrations during follow-up of adolescents into the third decade of life J Clin Endocrinol Metab 71 1990 970 974
19. A.L. Southam, and R.M. Richart The prognosis for adolescents with menstrual abnormalities Am J Obstet Gynecol 94 1966 637 645
20. J.A. Morrison, C.J. Glueck, and S. Daniels Adolescent oligomenorrhea in a biracial schoolgirl cohort: a simple clinical parameter predicting impaired fasting glucose plus type 2 diabetes mellitus, insulin, glucose, insulin resistance, and centripetal obesity from age 19 to 25 years Metabolism 60 2011 1285 1293
21. M.C. Amato, M. Verghi, and A. Galluzzo The oligomenorrhoic phenotypes of polycystic ovary syndrome are characterized by a high visceral adiposity index: a likely condition of cardiometabolic risk Hum Reprod 26 2011 1486 1494
22. F. Atsma, M.L. Bartelink, and D.E. Grobbee Reproductive factors, metabolic factors, and coronary artery calcification in older women Menopause 15 2008 899 904
23. L.J. Shaw, C.N. Bairey Merz, and R. Azziz Postmenopausal women with a history of irregular menses and elevated androgen measurements at high risk for worsening cardiovascular event-free survival: results from the National Institutes of Health - National Heart, Lung, and Blood Institute sponsored Women's Ischemia Syndrome Evaluatio J Clin Endocrinol Metab 93 2008 1276 1284 (Pubitemid 351519721)
24. H. Tfayli, and S. Arslanian Menstrual health and the metabolic syndrome in adolescents Ann N Y Acad Sci 1135 2008 85 94 (Pubitemid 351862137)
25. M.C. Haver, G.J. Locksmith, and E. Emmet Irregular menses: an independent risk factor for gestational diabetes mellitus Am J Obstet Gynecol 188 2003 1189 1191 (Pubitemid 36589098)
26. Strowitzki T, Capp E, von Eye Corleta H. The degree of cycle irregularity correlates with the grade of endocrine and metabolic disorders in PCOS patients. Eur J Obstet Gynecol Reprod Biol.149:178-81.
27. Souza FA, Dias R, Fernandes CE, et al. Menstrual irregularity: a possible clinical marker of metabolic dysfunction in women with class III obesity. Gynecol Endocrinol.
28. S. Sadrzadeh, W.A. Klip, and F.J. Broekmans Birth weight and age at menarche in patients with polycystic ovary syndrome or diminished ovarian reserve, in a retrospective cohort Hum Reprod 18 2003 2225 2230 (Pubitemid 37265091)
29. P. Montero, C. Bernis, and M. Loukid Characteristics of menstrual cycles in Moroccan girls: prevalence of dysfunctions and associated behaviours Ann Hum Biol 26 1999 243 249 (Pubitemid 29235466)
30. A.D. Coviello, R.S. Legro, and A. Dunaif Adolescent girls with polycystic ovary syndrome have an increased risk of the metabolic syndrome associated with increasing androgen levels independent of obesity and insulin resistance J Clin Endocrinol Metab 91 2006 492 497 (Pubitemid 43236914)
31. M.E. Atabek, and O. Pirgon Use of metformin in obese adolescents with hyperinsulinemia: a 6-month, randomized, double-blind, placebo-controlled clinical trial J Pediatr Endocrinol Metab 21 2008 339 348 (Pubitemid 351802726)
32. B. Banaszewska, A.J. Duleba, and R.Z. Spaczynski Lipids in polycystic ovary syndrome: role of hyperinsulinemia and effects of metformin Am J Obstet Gynecol 194 2006 1266 1272
33. W. Bao, S.R. Srinivasan, and W.A. Wattigney Persistence of multiple cardiovascular risk clustering related to syndrome X from childhood to young adulthood. The Bogalusa Heart Study. Arch Intern Med 154 1994 1842 1847 (Pubitemid 24262002)
34. E. Bonora, G. Formentini, and F. Calcaterra HOMA-estimated insulin resistance is an independent predictor of cardiovascular disease in type 2 diabetic subjects: prospective data from the Verona Diabetes Complications Study Diabetes Care 25 2002 1135 1141 (Pubitemid 41071163)
35. L.E. Eberly, R. Prineas, and J.D. Cohen Metabolic syndrome: risk factor distribution and 18-year mortality in the multiple risk factor intervention trial Diabetes Care 29 2006 123 130 (Pubitemid 44033442)
36. P.W. Franks, R.L. Hanson, and W.C. Knowler Childhood predictors of young-onset type 2 diabetes Diabetes 56 2007 2964 2972 (Pubitemid 350223631)
37. P. Laskarzewski, J.A. Morrison, and M.J. Mellies Relationships of measurements of body mass to plasma lipoproteins in schoolchildren and adults Am J Epidemiol 111 1980 395 406 (Pubitemid 10021495)
38. J.A. Morrison, I. deGroot, and B.K. Edwards Plasma cholesterol and triglyceride levels in 6,775 school children, ages 6-17 Metabolism 26 1977 1199 1211 (Pubitemid 8210414)
39. J.A. Morrison, C.J. Glueck, and P. Wang The child as proband for future parental cardiometabolic disease: the 26-year prospective Princeton Lipid Research Clinics Follow-up Study J Pediatr 160 2012 590 597e3
40. J.A. Morrison, L.A. Friedman, and C. Gray-McGuire Metabolic syndrome in childhood predicts adult cardiovascular disease 25 years later: the Princeton Lipid Research Clinics Follow-up Study Pediatrics 120 2007 340 345 (Pubitemid 47219504)
41. J.A. Morrison, C.J. Glueck, and P.S. Horn Pediatric triglycerides predict cardiovascular disease events in the fourth to fifth decade of life Metabolism 58 2009 1277 1284
42. J.A. Morrison, C.J. Glueck, and P. Wang Childhood risk factors predict cardiovascular disease, impaired fasting glucose plus type 2 diabetes mellitus, and high blood pressure 26 years later at a mean age of 38 years: the Princeton-lipid research clinics follow-up study Metabolism 61 2012 531 541
43. L.A. Friedman, J.A. Morrison, and S.R. Daniels Sensitivity and specificity of pediatric lipid determinations for adult lipid status: findings from the Princeton Lipid Research Clinics Prevalence Program Follow-up Study Pediatrics 118 2006 165 172 (Pubitemid 46071159)
44. J.A. Morrison, C.J. Glueck, and P.S. Horn Childhood predictors of adult type 2 diabetes at 9- and 26-year follow-ups Arch Pediatr Adolesc Med 164 2010 53 60
45. J.A. Morrison, L.A. Friedman, and P. Wang Metabolic syndrome in childhood predicts adult metabolic syndrome and type 2 diabetes mellitus 25 to 30 years later J Pediatr 152 2008 201 206
46. L. Chiazze Jr., F.T. Brayer, and J.J. Macisco Jr. The length and variability of the human menstrual cycle JAMA 203 1968 377 380
47. J.A. Morrison, C.J. Glueck, and P.S. Horn Pre-teen insulin resistance predicts weight gain, impaired fasting glucose, and type 2 diabetes at age 18-19 y: a 10-y prospective study of black and white girls Am J Clin Nutr 88 2008 778 788
48. Obesity and cardiovascular disease risk factors in black and white girls: the NHLBI Growth and Health Study Am J Public Health 82 1992 1613 1620
49. D. Dabelea, R.A. Bell, and R.B. D'Agostino Jr. Incidence of diabetes in youth in the United States JAMA 297 2007 2716 2724 (Pubitemid 47001097)
50. J.M. Murabito, B.H. Nam, and R.B. D'Agostino Sr. Accuracy of offspring reports of parental cardiovascular disease history: the Framingham Offspring Study Ann Intern Med 140 2004 434 440
51. S.M. Grundy, H.B. Brewer Jr., and J.I. Cleeman Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition Circulation 109 2004 433 438 (Pubitemid 38133916)
52. S. Cook, P. Auinger, and C. Li Metabolic syndrome rates in United States adolescents, from the National Health and Nutrition Examination Survey, 1999-2002 J Pediatr 152 2008 165 170
53. S. Cook, M. Weitzman, and P. Auinger Prevalence of a metabolic syndrome phenotype in adolescents: findings from the third National Health and Nutrition Examination Survey, 1988-1994 Arch Pediatr Adolesc Med 157 2003 821 827 (Pubitemid 36988016)
54. J.A. Morrison, C.J. Glueck, and M. Umar Hyperinsulinemia and metabolic syndrome at mean age of 10 years in black and white schoolgirls and development of impaired fasting glucose and type 2 diabetes mellitus by mean age of 24 years Metabolism 60 2011 24 31
55. E.W. Demerath, J. Li, and S.S. Sun Fifty-year trends in serial body mass index during adolescence in girls: the Fels Longitudinal Study Am J Clin Nutr 80 2004 441 446 (Pubitemid 41080020)
56. P. Prentice, and R.M. Viner Pubertal timing and adult obesity and cardiometabolic risk in women and men: a systematic review and meta-analysis Int J Obes (Lond) 177 2012 [Epub ahead of print, November 20, 2012]
57. N. Lass, M. Kleber, and K. Winkel Effect of lifestyle intervention on features of polycystic ovarian syndrome, metabolic syndrome, and intima-media thickness in obese adolescent girls J Clin Endocrinol Metab 96 2011 3533 3540
58. R. Kelishadi, M. Malekahmadi, and M. Hashemipour Can a trial of motivational lifestyle counseling be effective for controlling childhood obesity and the associated cardiometabolic risk factors? Pediatr Neonatol 53 2012 90 97
59. T. Reinehr, M. Kleber, and A.M. Toschke Lifestyle intervention in obese children is associated with a decrease of the metabolic syndrome prevalence Atherosclerosis 207 2009 174 180
60. G. Lambert-Messerlian, M.B. Roberts, and S.S. Urlacher First assessment of menstrual cycle function and reproductive endocrine status in Samoan women Hum Reprod 26 2011 2518 2524
61. S.M. Camhi, and P.T. Katzmarzyk Tracking of cardiometabolic risk factor clustering from childhood to adulthood Int J Pediatr Obes 5 2010 122 129
62. J.C. Eisenmann, G.J. Welk, and E.E. Wickel Stability of variables associated with the metabolic syndrome from adolescence to adulthood: the Aerobics Center Longitudinal Study Am J Hum Biol 16 2004 690 696 (Pubitemid 39517316)
63. K. Sorensen, A. Mouritsen, and L. Aksglaede Recent secular trends in pubertal timing: implications for evaluation and diagnosis of precocious puberty Horm Res Paediatr 77 2012 137 145
64. L. Aksglaede, K. Sorensen, and J.H. Petersen Recent decline in age at breast development: the Copenhagen Puberty Study Pediatrics 123 2009 e932 e939
65. M.E. Herman-Giddens Recent data on pubertal milestones in United States children: the secular trend toward earlier development Int J Androl 29 2006 241 246 discussion 86-90
66. M.A. McDowell, D.J. Brody, and J.P. Hughes Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999-2004 J Adolesc Health 40 2007 227 231
67. L. Ibanez, C. Valls, and N. Potau Sensitization to insulin in adolescent girls to normalize hirsutism, hyperandrogenism, oligomenorrhea, dyslipidemia, and hyperinsulinism after precocious pubarche J Clin Endocrinol Metab 85 2000 3526 3530
68. S.M. Bhattacharya Prevalence of metabolic syndrome in women with polycystic ovary syndrome, using two proposed definitions Gynecol Endocrinol 26 2010 516 520
69. L. Ibanez, N. Potau, and A. Ferrer Anovulation in eumenorrheic, nonobese adolescent girls born small for gestational age: insulin sensitization induces ovulation, increases lean body mass, and reduces abdominal fat excess, dyslipidemia, and subclinical hyperandrogenism J Clin Endocrinol Metab 87 2002 5702 5705 (Pubitemid 36034379)
70. D.M. Wilson, S.H. Abrams, and T. Aye Metformin extended release treatment of adolescent obesity: a 48-week randomized, double-blind, placebo-controlled trial with 48-week follow-up Arch Pediatr Adolesc Med 164 2010 116 123
71. K. Hoeger, K. Davidson, and L. Kochman The impact of metformin, oral contraceptives, and lifestyle modification on polycystic ovary syndrome in obese adolescent women in two randomized, placebo-controlled clinical trials J Clin Endocrinol Metab 93 2008 4299 4306 (Pubitemid 352789525)