Age at menopause, reproductive life span, and type 2 diabetes risk: Results from the EPIC-InterAct study

Diabetes Care

Volumn 36, Issue 4, 2013, Pages 1012-1019

  Brand, Judith S ^a   Van Der Schouw, Yvonne T ^a   Onland Moret, N Charlotte ^a   Sharp, Stephen J ^b   Ong, Ken K ^b   Khaw, Kay Tee ^c   Ardanaz, Eva ^d,e   Amiano, Pilar ^e,f,g   Boeing, Heiner ^h   Chirlaque, Maria Dolores ^e,i   Clavel Chapelon, Françoise ^j   Crowe, Francesca L ^k   De Lauzon Guillain, Blandine ^j   Duell, Eric J ^l   Fagherazzi, Guy ^j   Franks, Paul W ^m,n   Grioni, Sara ^o   Groop, Leif C ^p,q   Kaaks, Rudolf ^r   Key, Timothy J ^k   Nilsson, Peter M ^p   Overvad, Kim ^s,t   Palli, Domenico ^u   Panico, Salvatore ^v   Quirós, J Ramón ^w   Rolandsson, Olov ⁿ   Sacerdote, Carlotta ^x,y   Sánchez, María José ^e,z   Slimani, Nadia ^aa   Teucher, Birgit ^r   Tjonneland, Anne ^ab   Tumino, Rosario ^ac,ad   Van Der A, Daphne L ^ae   Feskens, Edith J M ^af   Langenberg, Claudia ^b   Forouhi, Nita G ^b   Riboli, Elio ^ag   Wareham, Nicholas J ^b   more..

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d INSTITUTO DE SALUD PÚBLICA DE NAVARRA   (Spain)

^e CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^f Basque Government   (Spain)

^g BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^h GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

ⁱ DEPARTMENT OF EPIDEMIOLOGY   (Spain)

^j CENTRE FOR RESEARCH IN EPIDEMIOLOGY AND POPULATION HEALTH   (France)

^k UNIVERSITY OF OXFORD   (United Kingdom)

^l Environment and Cancer   (Spain)

^m LUND UNIVERSITY   (Sweden)

ⁿ UMEÅ UNIVERSITY   (Sweden)

^o NATIONAL CANCER INSTITUTE   (Italy)

^p LUND UNIVERSITY HOSPITAL   (Sweden)

^q UNIVERSITY OF HELSINKI   (Finland)

^r GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^s AARHUS UNIVERSITY   (Denmark)

^t AALBORG UNIVERSITY HOSPITAL   (Denmark)

^u CANCER RESEARCH AND PREVENTION INSTITUTE ISPO   (Italy)

^v UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^w Human Genetic Foundation ^*  (Spain)

^x Center for Cancer Prevention CPO Piemonte   (Italy)

^y Human Genetics Foundation   (Italy)

^z ANDALUSIAN SCHOOL OF PUBLIC HEALTH   (Spain)

^aa INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^ab DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^ac CIVILE M P AREZZO HOSPITAL   (Italy)

^ad Associazone Iblea per la Ricerca Epidemiologica Onlus   (Italy)

^ae NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^af WAGENINGEN UNIVERSITY   (Netherlands)

^ag IMPERIAL COLLEGE LONDON   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BODY MASS; COHORT ANALYSIS; CONTROLLED STUDY; EARLY MENOPAUSE; FEMALE; HUMAN; INCIDENCE; MAJOR CLINICAL STUDY; MENOPAUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; POSTMENOPAUSE; PROSPECTIVE STUDY; REPRODUCTION; RISK FACTOR; SMOKING; WAIST CIRCUMFERENCE;

AGE FACTORS; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; MENOPAUSE; MIDDLE AGED; PROSPECTIVE STUDIES; REPRODUCTIVE HISTORY; RISK FACTORS;

EID: 84875421600     PISSN: 01495992     EISSN: 19355548     Source Type: Journal    
DOI: 10.2337/dc12-1020     Document Type: Article

References (40)

1. Atsma F, Bartelink ML, Grobbee DE, van der Schouw YT. Postmenopausal status and early menopause as independent risk factors for cardiovascular disease: a metaanalysis. Menopause 2006;13:265-279
2. van Der Voort DJ, van Der Weijer PH, Barentsen R. Early menopause: increased fracture risk at older age. Osteoporos Int 2003;14:525-530
3. van der Klift M, de Laet CE, McCloskey EV, et al. Risk factors for incident vertebral fractures in men and women: the Rotterdam Study. J Bone Miner Res 2004;19: 1172-1180
4. Monninkhof EM, van der Schouw YT, Peeters PH. Early age at menopause and breast cancer: are leaner women more protected? A prospective analysis of the Dutch DOM cohort. Breast Cancer Res Treat 1999;55:285-291
5. Trichopoulos D, MacMahon B, Cole P. Menopause and breast cancer risk. J Natl Cancer Inst 1972;48:605-613
6. Dossus L, Allen N, Kaaks R, et al. Reproductive risk factors and endometrial cancer: the European Prospective Investigation into Cancer and Nutrition. Int J Cancer 2010;127:442-451
7. Tsilidis KK, Allen NE, Key TJ, et al. Oral contraceptive use and reproductive factors and risk of ovarian cancer in the European Prospective Investigation into Cancer and Nutrition. Br JCancer 2011;105:1436-1442
8. Kelsey JL, Gammon MD, John EM. Reproductive factors and breast cancer. Epidemiol Rev 1993;15:36-47
9. van der Graaf Y, de Kleijn MJ, van der Schouw YT. Menopause and cardiovascular disease. J Psychosom Obstet Gynaecol 1997;18:113-120
10. Kritz-Silverstein D, Barrett-Connor E, Wingard DL. Hysterectomy, oophorectomy, and heart disease risk factors in older women. Am J Public Health 1997;87:676-680
11. Pirimoglu ZM, Arslan C, Buyukbayrak EE, et al. Glucose tolerance of premenopausal women after menopause due to surgical removal of ovaries. Climacteric 2011;14: 453-457
12. Malacara JM, Huerta R, Rivera B, Esparza S, Fajardo ME. Menopause in normal and uncomplicated NIDDM women: physical and emotional symptoms and hormone profile. Maturitas 1997;28:35-45
13. Di Donato P, Giulini NA, Bacchi Modena A, et al.; Gruppo di Studio Progetto Menopausa Italia. Risk factors for type 2 diabetes in women attending menopause clinics in Italy: a cross-sectional study. Climacteric 2005;8:287-293
14. Luborsky JL, Meyer P, Sowers MF, Gold EB, Santoro N. Premature menopause in a multi-ethnic population study of the menopause transition. Hum Reprod 2003; 18:199-206
15. Langenberg C, Sharp S, Forouhi NG, et al.; InterAct Consortium. Design and cohort description of the InterAct Project: an examination of the interaction of genetic and lifestyle factors on the incidence of type 2 diabetes in the EPIC Study. Diabetologia 2011;54:2272-2282
16. White IR, Royston P. Imputing missing covariate values for the Cox model. Stat Med 2009;28:1982-1998
17. Prentice RL. A case-cohort design for epidemiologic cohort studies and disease prevention trials. Biometrika 1986;73:1-11
18. Hu FB, Grodstein F, Hennekens CH, et al. Age at natural menopause and risk of cardiovascular disease. Arch Intern Med 1999;159:1061-1066
19. Kampert JB, Whittemore AS, Paffenbarger RS Jr. Combined effect of childbearing, menstrual events, and body size on agespecific breast cancer risk. Am J Epidemiol 1988;128:962-979
20. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7: 177-188
21. den Tonkelaar I. Validity and reproducibility of self-reported age at menopause in women participating in the DOM-project. Maturitas 1997;27:117-123
22. Colditz GA, Stampfer MJ, Willett WC, et al. Reproducibility and validity of selfreported menopausal status in a prospective cohort study. Am J Epidemiol 1987;126:319-325
23. Must A, Phillips SM, Naumova EN, 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
24. Casey VA, Dwyer JT, Coleman KA, Krall EA, Gardner J, Valadian I. 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 1991;18:155-166
25. Cairns BJ, Liu B, Clennell S, et al. Lifetime body size and reproductive factors: comparisons of data recorded prospectively with self reports in middle age. BMC Med Res Methodol 2011;11:7
26. Dorman JS, Steenkiste AR, Foley TP, et al.; Familial Autoimmune and Diabetes (FAD) Study. Menopause in type 1 diabetic women: is it premature? Diabetes 2001; 50:1857-1862
27. Mishra GD, Carrigan G, Brown WJ, Barnett AG, Dobson AJ. Short-term weight change and the incidence of diabetes in midlife: results from the Australian Longitudinal Study on Women's Health. Diabetes Care 2007;30:1418-142
28. Soriguer F, Morcillo S, Hernando V, et al. Type 2 diabetes mellitus and other cardiovascular risk factors are no more common during menopause: longitudinal study. Menopause 2009;16:817-821
29. Kim C, Edelstein SL, Crandall JP, et al.; Diabetes Prevention Program Research Group. Menopause and risk of diabetes in the Diabetes Prevention Program. Menopause 2011;18:857-868
30. He C, Zhang C, Hunter DJ, et al. Age at menarche and risk of type 2 diabetes: results from2 large prospective cohort studies. Am J Epidemiol 2010;171:334-344
31. Lakshman R, Forouhi N, Luben R, et al. Association between age at menarche and risk of diabetes in adults: results from the EPIC-Norfolk cohort study. Diabetologia 2008;51:781-786
32. Persson I. Estrogens in the causation of breast, endometrial and ovarian cancers -evidence and hypotheses from epidemiological findings. J Steroid Biochem Mol Biol 2000;74:357-364
33. Godsland IF. Oestrogens and insulin secretion. Diabetologia 2005;48:2213-222
34. Margolis KL, Bonds DE, Rodabough RJ, et al.; Women's Health Initiative Investigators. Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the Women's Health Initiative Hormone Trial. Diabetologia 2004;47:1175-1187
35. Kanaya AM, Herrington D, Vittinghoff E, et al.; Heart and Estrogen/progestin Replacement Study. Glycemic effects of postmenopausal hormone therapy: the Heart and Estrogen/progestin Replacement Study. A randomized, double-blind, placebo-controlled trial. Ann Intern Med 2003;138:1-9
36. Kalyani RR, Franco M, Dobs AS, et al. The association of endogenous sex hormones, adiposity, and insulin resistance with incident diabetes in postmenopausal women. J Clin Endocrinol Metab 2009; 94:4127-4135
37. Ding EL, Song Y, Manson JE, Rifai N, Buring JE, Liu S. Plasma sex steroid hormones and risk of developing type 2 diabetes in women: a prospective study. Diabetologia 2007;50:2076-2084
38. Burger HG, Dudley EC, Cui J, Dennerstein L, Hopper JL. A prospective longitudinal study of serum testosterone, dehydroepiandrosterone sulfate, and sex hormone-binding globulin levels through the menopause transition. J Clin Endocrinol Metab 2000;85:2832-2838
39. Rannevik G, Jeppsson S, Johnell O, Bjerre B, Laurell-Borulf Y, Svanberg L. A longitudinal study of the perimenopausal transition: altered profiles of steroid and pituitary hormones, SHBG and bone mineral density. Maturitas 1995;21:103-113
40. Stolk L, Perry JR, Chasman DI, et al.Metaanalyses identify 13 loci associated with age at menopause and highlight DNA repair and immune pathways. Nat Genet 2012;44:260-268