Anti-Müllerian hormone and its relationships with subclinical cardiovascular disease and renal disease in a longitudinal cohort study of women with type 1 diabetes

Catherine Kim, Yuanyuan Pan, Barbara H Braffett, Valerie L Arends, Michael W Steffes, Hunter Wessells, Aruna V Sarma, DCCT/EDIC Research Group, Catherine Kim, Yuanyuan Pan, Barbara H Braffett, Valerie L Arends, Michael W Steffes, Hunter Wessells, Aruna V Sarma, DCCT/EDIC Research Group

Abstract

Background: Reproductive age may be a risk factor for vascular disease. Anti-Müllerian hormone (AMH) is produced by viable ovarian follicles and reflects reproductive age. We examined whether AMH concentrations were associated with markers of subclinical cardiovascular disease (CVD) and kidney disease among women with type 1 diabetes.

Methods: We performed a cross-sectional analysis of the Epidemiology of Diabetes Interventions and Complications Study. Participants included women with type 1 diabetes and ≥1 AMH measurement (n = 390). In multivariable regression models which adjusted for repeated measures, we examined the associations between AMH with CVD risk factors, estimated glomerular filtration rate, and albumin excretion ratio. We also examined whether initial AMH concentrations were associated with the presence of any coronary artery calcification (CAC) or carotid intima media thickness (cIMT).

Results: After adjustment for age, AMH was not associated with waist circumference, blood pressure, lipid profiles, or renal function. Higher initial AMH concentrations had borderline but non-significant associations with the presence of CAC after adjustment for age (odds ratio [OR] 1.08, 95% confidence interval [CI] 1.00, 1.16) which were minimally altered by addition of other CVD risk factors, although women in the 3rd quartile of AMH had lower odds of CAC than women in the lowest quartile (OR 0.40, 95% CI 0.17, 0.94). After adjustment for age, higher AMH was associated with statistically significant but only slightly higher cIMT (0.005 mm, p = 0.0087) which was minimally altered by addition of other CVD risk factors.

Conclusions: Among midlife women with type 1 diabetes, AMH has slight but significant associations with subclinical measures of atherosclerosis. Future studies should examine whether these associations are clinically significant.

Trial registration: NCT00360815 and NCT00360893 Study Start Date April 1994.

Keywords: Anti-Müllerian hormone; Coronary artery calcification; Ovarian reserve; Type 1 diabetes.

Conflict of interest statement

An institutional review board at each site (n = 25) approved all study procedures, and written informed consent was obtained from study participants prior to assessments.Not applicable.The authors declare that they have no competing interests.Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Flow chart of study participants

References

    1. Harlow S, Gass M, Hall J, Lobo R, Maki P, Rebar R, et al. Executive summary of the stages of reproductive aging workshop + 10; addressing the unfinished agenda of staging reproductive aging. J Clin Endocrinol Metab. 2012;97(4):1159–1168. doi: 10.1210/jc.2011-3362.
    1. Wellons M, Ouyang P, Schreiner P, Herrington D, Vaidya D. Early menopause predicts future coronary heart disease and stroke: the multi-ethnic study of atherosclerosis (MESA) Menopause. 2012;19(10):1081–1087. doi: 10.1097/gme.0b013e3182517bd0.
    1. Sjoberg L, Pitkaniemi J, Harjutsalo V, Haapala L, Tiitinen A, Tuomilehto J, et al. Menopause in women with type 1 diabetes. Menopause. 2011;18(2):158–163.
    1. de Kat A, Broekmans F, Laven J, van der Schouw Y. Anti-Mullerian hormone as a marker of ovarian reserve in relation to cardiometabolic health: a narrative review. Maturitas. 2015;80:251–257. doi: 10.1016/j.maturitas.2014.12.010.
    1. Aksglaede L, Sorensen K, Boas M, Mouritsen A, Hagen C, Jensen R, et al. Changes in anti-Mullerian hormone (AMH) throughout the lifespan: a population-based study of 1027 healthy males from birth (cord blood) to the age of 69 years. J Clin Endocrinol Metab. 2010;95:5357–5364. doi: 10.1210/jc.2010-1207.
    1. Figueroa-Vega N, Moreno-Frias C, Malacara J. Alterations in adhesion molecules, pro-inflammatory cytokines and cell-derived microparticles contribute to intima-media thickness and symptoms in postmenopausal women. PLoS One. 2015;10(5):e0120990. doi: 10.1371/journal.pone.0120990.
    1. Dolleman M, Depmann M, Eijkemans M, Heimensem J, Broer S, van der STroom E, et al. Antimullerian hormone is a more accurate predictor of individual time to menopause than mother’s age at menopause. Hum Reprod. 2014;29(3):584–591. doi: 10.1093/humrep/det446.
    1. Broer S, Eijkemans M, Scheffer G, van Rooij I, de Vet A, Themmen A, et al. Anti-mullerian hormone predicts menopause: a long-term follow-up study in normoovulatory women. J Clin Endocrinol Metab. 2011;96(8):2532–2539. doi: 10.1210/jc.2010-2776.
    1. Dewailly D, Andersen C, Balen A, Broekmans F, Dilaver N, Fanchin R, et al. The physiology and clinical utility of anti-Mullerian hormone in women. Hum Reprod. 2013;20(3):370–385. doi: 10.1093/humupd/dmt062.
    1. Tehrani F, Solaymani-Dodaran M, Tohidi M, Goharai M, Azizi F. Modeling age at menopause using serum concentration of anti-Mullerian hormone. J Clin Endocrinol Metab. 2013;98:729–735. doi: 10.1210/jc.2012-3176.
    1. Nair S, Slaughter J, Terry J, Appiah D, Ebong I, Wang E, et al. Anti-mullerian hormone (AMH) is associated with natural menopause in a population-based sample: the CARDIA Women’s study. Maturitas. 2015;81:493–498. doi: 10.1016/j.maturitas.2015.06.026.
    1. Bleil M, Gregorich S, McConnell D, Rosen M, Cedars M. Does accelerated reproductive aging underlie premenopausal risk for cardiovascular disease. Menopause. 2013;20(11):1139–1146. doi: 10.1097/GME.0b013e31828950fa.
    1. Yarde F, Spiering W, Franx A, Visseren F, Eijkemans M, de Valk H, et al. Association between vascular health and ovarian ageing in type 1 diabetes mellitus. Hum Reprod. 2016;31(6):1354–1362. doi: 10.1093/humrep/dew063.
    1. Tehrani F, Erfani H, Cheraghi L, Tohidi M, Azizi F. Lipid profiles and ovarian reserve status: a longitudinal study. Hum Reprod. 2014;29(11):2522–2529. doi: 10.1093/humrep/deu249.
    1. Kim C, Dunn R, Braffett B, Cleary P, Arends V, Steffes M et al. Ovarian reserve in women with type 1 diabetes in the DCCT/EDIC Study. Diabet Med. 2015;33(5):691–2.
    1. Appt S, Chen H, Clarkson T, Kaplan J. Premenopausal antimullerian hormone concentration is associated with subsequent atherosclerosis. Menopause. 2012;19(12):1353–1359. doi: 10.1097/gme.0b013e31825b4fe2.
    1. Looby S, Fitch K, Srinivasa S, Lo J, Rafferty D, Martin A, et al. Reduced ovarian reserve relates to monocyte activation and subclinical coronary artherosclerotic plaque in women with HIV. AIDS. 2016;30:383–393.
    1. Orchard T, Dorman J, Maser R, Becker D, Drash A, Ellis D, et al. Prevalence of complications in IDDM by sex and duration. Pittsburgh epidemiology of diabetes complications study II. Diabetes. 1990;39(9):1116–1124. doi: 10.2337/diab.39.9.1116.
    1. DCCT/EDIC Research Group. Nathan D, Zinman B, Cleary P, Backlund J, Genuth S, et al. Modern-day clinical course of type 1 diabetes mellitus after 30 years’ duration: the diabetes control and complications trial/epidemiology of diabetes interventions and complications and Pittsburgh epidemiology of diabetes complications experience (1983-2005) Arch Intern Med. 2009;169(14):1307–1316. doi: 10.1001/archinternmed.2009.193.
    1. Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. The Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. N Engl J Med. 2000;342(6):381–9.
    1. Kim C, Cleary P, Cowie C, Braffett B, Dunn R, Larkin M, et al. Effect of glycemic treatment and microvascular complications on menopause in women with type 1 diabetes in the diabetes control and complications trial/epidemiology of diabetes interventions and complications (DCCT/EDIC) cohort. Diabetes Care. 2014;37(3):701–708. doi: 10.2337/dc13-1746.
    1. Sowers M, Eyvazzadeh A, McConnell D, Yosef M, Jannausch M, Zhang D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab. 2008;93(9):3478–3483. doi: 10.1210/jc.2008-0567.
    1. Epidemiology of Diabetes Interventions and Complications (EDIC) Group Design, implementation, and preliminary results of a long-term follow-up of the diabetes control and complications trial cohort. Diabetes Care. 1999;22:99–111. doi: 10.2337/diacare.22.1.99.
    1. Steffes M, Cleary P, Goldstein D, Little R, Wiedmeyer HM, Rohlfing C, et al. Hemoglobin A1c measurements over nearly two decades: sustaining comparable values throughout the diabetes control and complications trial and the epidemiology of diabetes interventions and complications study. Clin Chem. 2005;51(4):753–758. doi: 10.1373/clinchem.2004.042143.
    1. Friedewald W, Levy R, Fredrickson D. Estimation of low-density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem. 1972;18:499–502.
    1. Kumar A, Kalra B, Patel A, McDavid L, Roudebush W. Development of a second generation anti-Müllerian hormone (AMH) ELISA. J Immunol Methods. 2010;362:51–59. doi: 10.1016/j.jim.2010.08.011.
    1. Broer S, Broekmans F, Laven J, Fauser B. Anti-Mullerian hormone: ovarian reserve testing and its potential clinical implications. Hum Reprod Update. 2014;20(5):688–701. doi: 10.1093/humupd/dmu020.
    1. Purnell J, Zinman B, Brunzell J. The effect of excess weight gain with intensive diabetes mellitus treatment on cardiovascular disease risk factors and atherosclerosis in type 1 diabetes mellitus: results from the diabetes control and complications trial/epidemiology of diabetes interventions and complications study (DCCT/EDIC) study. Circulation. 2013;127:180–187. doi: 10.1161/CIRCULATIONAHA.111.077487.
    1. Strotmeyer E, Steenkiste A, Foley T, Jr, Berga S, Dorman J. Menstrual cycle differences between women with type 1 diabetes and women without diabetes. Diabetes Care. 2003;26:1016–1021. doi: 10.2337/diacare.26.4.1016.
    1. Jonasson J, Brismar K, Sparen P, Lambe M, Myren O, Ostenson C, et al. Fertility in women with type 1 diabetes: a population-based cohort study in Sweden. Diabetes Care. 2007;30:2271–2276. doi: 10.2337/dc06-2574.
    1. Escobar-Morreale H, Roldan-Martin M. Type 1 diabetes and polycystic ovary syndrome: systematic review and meta-analysis. Diabetes Care. 2016;39:639–648. doi: 10.2337/dc15-2577.
    1. Cui L, Qin Y, Gao X, Lu J, Geng L, Ding L, et al. Anti-Mullerian hormone: correlation with age and androgenic and metabolic factors in women from birth to postmenopause. Fertil Steril. 2016;105(2):481–485. doi: 10.1016/j.fertnstert.2015.10.017.
    1. Fang Y, Lu X, Liu L, Lin X, Sun M, Fu J, et al. Vascular endothelial growth factor induces anti-Mullerian hormone receptor 2 overexpression in ovarian granulosa cells of in vitro fertilization/intracytoplasmic sperm injection patients. Mol Med Rep. 2016;13(6):5157–5162.
    1. Kaess B, Preis S, Beiser A, Sawyer D, Chen T, Seshadri S, et al. Circulating vascular endothelial growth factor and the risk of cardiovascular events. Heart. 2015;102(23):1898–1901. doi: 10.1136/heartjnl-2015-309155.
    1. Paradisi R, Vicenti R, Macciocca M, Seracchioli R, Rossi S, Fabbri R. High cytokine expression and reduced ovarian reserve in patients with Hodkin lymphoma or non-Hodgkin lymphoma. Fertil Steril. 2016;106(5):1176–1182. doi: 10.1016/j.fertnstert.2016.06.035.
    1. Looker H, Colombo M, Agakov F, Zeller T, Groop L, Thorand B, et al. Protein biomarkers for the prediction of cardiovascular disease in type 2 diabetes. Diabetologia. 2015;57(2):1363–1371. doi: 10.1007/s00125-015-3535-6.
    1. Sowers M, McConnell D, Yosef M, Jannausch M, Harlow S, Randolph J., Jr Relating smoking, obesity, insulin resistance, and ovarian biomarker changes to the final menstrual period. Ann N Y Acad Sci. 2010;1204:95–103. doi: 10.1111/j.1749-6632.2010.05523.x.
    1. Freeman E, Sammel M, Lin H, Gracia C. Anti-mullerian hormone as a predictor of time to menopause in late reprodutive age women. J Clin Endocrinol Metab. 2012;97(5):1673–1680. doi: 10.1210/jc.2011-3032.
    1. Kim C, Pan H, Braffett B, Cleary P, Arends V, Steffes M, et al. AMH in women with and without type 1 diabetes in the EDIC and MBHMS cohorts. Fertil Steril. 2016;106(6):1446–1452. doi: 10.1016/j.fertnstert.2016.07.009.
    1. DCCT/EDIC Research Group. de Boer I, Sun W, Cleary P, Lachin J, Molitch M, et al. Intensive diabetes therapy and glomerular filtration rate in type 1 diabetes. N Engl J Med. 2011;365(25):2366–2376. doi: 10.1056/NEJMoa1111732.
    1. Kim C, Cushman M, Khodneva Y, Lisabeth L, Judd S, Kleindorfer D, et al. Risk of incident coronary heart disease events in men compared to women by menopause type and race. J Am Heart Assoc. 2015;4(7):piie001881. doi: 10.1161/JAHA.115.001881.
    1. Cauley J. Bone health after menopause. Curr Opinn Endocrinol Diabetes Obes. 2015;22(6):490–494. doi: 10.1097/MED.0000000000000204.
    1. Palacios S, Meija A, Neyro J. Treatment of the genitourinary syndrome of menopause. Climacteric. 2015;1:23–29. doi: 10.3109/13697137.2015.1079100.

Source: PubMed

Подписаться