Hormone replacement therapy in young women with primary ovarian insufficiency and early menopause

Fertility and Sterility

Volumn 106, Issue 7, 2016, Pages 1588-1599

  Sullivan, Shannon D ^a   Sarrel, Philip M ^b   Nelson, Lawrence M ^c  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b YALE UNIVERSITY   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

androgen; early menopause; estrogen; hormone replacement therapy; management; menopausal hormone therapy; morbidity; mortality; premature menopause; premature ovarian failure; Primary ovarian insufficiency; progestin

Indexed keywords

ESTRADIOL; GESTAGEN; PRASTERONE; SEX HORMONE; TESTOSTERONE; FERTILITY PROMOTING AGENT;

ANXIETY; BONE DENSITY; BREAST CANCER; BREAST FEEDING; CANCER RISK; CARDIOVASCULAR DISEASE; COGNITIVE DEFECT; DEPRESSION; DISEASE ASSOCIATION; DISEASE COURSE; DRY EYE; EARLY MENOPAUSE; EMOTIONAL STABILITY; FEMALE; FEMALE INFERTILITY; FRACTURE; HORMONE DEFICIENCY; HORMONE SUBSTITUTION; HORMONE SYNTHESIS; HUMAN; MENOPAUSAL SYNDROME; MENOPAUSE; OVARIAN HORMONE DEFICIENCY; OVARY CANCER; OVARY INSUFFICIENCY; PATIENT SAFETY; PREMENOPAUSE; PRIORITY JOURNAL; PSYCHOSOCIAL CARE; QUALITY OF LIFE; REVIEW; RISK ASSESSMENT; RISK BENEFIT ANALYSIS; SEXUAL FUNCTION; TURNER SYNDROME; ADULT; ADVERSE EFFECTS; COMPLICATION; DRUG EFFECTS; ESTROGEN THERAPY; INFERTILITY, FEMALE; MIDDLE AGED; PATHOPHYSIOLOGY; PATIENT SELECTION; PRIMARY OVARIAN INSUFFICIENCY; PROCEDURES; RISK FACTOR; TREATMENT OUTCOME;

ADULT; ESTROGEN REPLACEMENT THERAPY; FEMALE; FERTILITY AGENTS, FEMALE; HUMANS; INFERTILITY, FEMALE; MENOPAUSE, PREMATURE; MIDDLE AGED; PATIENT SELECTION; PRIMARY OVARIAN INSUFFICIENCY; RISK ASSESSMENT; RISK FACTORS; TREATMENT OUTCOME;

EID: 84998892576     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2016.09.046     Document Type: Review

References (116)

1. 1 Nelson, L.M., Clinical practice. Primary ovarian insufficiency. N Engl J Med 360 (2009), 606–614.
2. 2 Coulam, C.B., Adamson, S.C., Annegers, J.F., Incidence of premature ovarian failure. Obstet Gynecol 67 (1986), 604–606.
3. 3 Sprague, B.L., Trentham-Dietz, A., Cronin, K.A., A sustained decline in postmenopausal hormone use: results from the National Health and Nutrition Examination Survey, 1999–2010. Obstet Gynecol 120 (2012), 595–603.
4. 4 Rossouw, J.E., Anderson, G.L., Prentice, R.L., LaCroix, A.Z., Kooperberg, C., Stefanick, M.L., et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288 (2002), 321–333.
5. 5 Stuenkel, C.A., Davis, S.R., Gompel, A., Lumsden, M.A., Murad, M.H., Pinkerton, J.V., et al. Treatment of symptoms of the menopause: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 100 (2015), 3975–4011.
6. 6 Neves, E.C.M., Birkhauser, M., Samsioe, G., Lambrinoudaki, I., Palacios, S., Borrego, R.S., et al. EMAS position statement: the ten point guide to the integral management of menopausal health. Maturitas 81 (2015), 88–92.
7. 7 Hoek, A., Schoemaker, J., Drexhage, H.A., Premature ovarian failure and ovarian autoimmunity. Endocr Rev 18 (1997), 107–134.
8. 8 Rafique, S., Sterling, E.W., Nelson, L.M., A new approach to primary ovarian insufficiency. Obstet Gynecol Clin North Am 39 (2012), 567–586.
9. 9 Murray, A., Schoemaker, M.J., Bennett, C.E., Ennis, S., Macpherson, J.N., Jones, M., et al. Population-based estimates of the prevalence of FMR1 expansion mutations in women with early menopause and primary ovarian insufficiency. Genet Med 16 (2014), 19–24.
10. 10 Bondy, C.A., Care of girls and women with Turner syndrome: a guideline of the Turner Syndrome Study Group. J Clin Endocrinol Metab 92 (2007), 10–25.
11. 11 Graziottin, A., Basson, R., Sexual dysfunction in women with premature menopause. Menopause 11 (2004), 766–777.
12. 12 Kalantaridou, S.N., Vanderhoof, V.H., Calis, K.A., Corrigan, E.C., Troendle, J.F., Nelson, L.M., Sexual function in young women with spontaneous 46,XX primary ovarian insufficiency. Fertil Steril 90 (2008), 1805–1811.
13. 13 de Almeida, D.M., Benetti-Pinto, C.L., Makuch, M.Y., Sexual function of women with premature ovarian failure. Menopause 18 (2011), 262–266.
14. 14 van der Stege, J.G., Groen, H., van Zadelhoff, S.J., Lambalk, C.B., Braat, D.D., van Kasteren, Y.M., et al. Decreased androgen concentrations and diminished general and sexual well-being in women with premature ovarian failure. Menopause 15 (2008), 23–31.
15. 15 Kalantaridou, S.N., Calis, K.A., Vanderhoof, V.H., Bakalov, V.K., Corrigan, E.C., Troendle, J.F., et al. Testosterone deficiency in young women with 46,XX spontaneous premature ovarian failure. Fertil Steril 86 (2006), 1475–1482.
16. 16 Thurston, R.C., el Khoudary, S.R., Sutton-Tyrrell, K., Crandall, C.J., Gold, E., Sternfeld, B., et al. Are vasomotor symptoms associated with alterations in hemostatic and inflammatory markers? Findings from the Study of Women's Health Across the Nation. Menopause 18 (2011), 1044–1051.
17. 17 Wierman, M.E., Basson, R., Davis, S.R., Khosla, S., Miller, K.K., Rosner, W., et al. Androgen therapy in women: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 91 (2006), 3697–3710.
18. 18 Nachtigall, L., Casson, P., Lucas, J., Schofield, V., Melson, C., Simon, J.A., Safety and tolerability of testosterone patch therapy for up to 4 years in surgically menopausal women receiving oral or transdermal oestrogen. Gynecol Endocrinol 27 (2011), 39–48.
19. 19 Shifren, J.L., Braunstein, G.D., Simon, J.A., Casson, P.R., Buster, J.E., Redmond, G.P., et al. Transdermal testosterone treatment in women with impaired sexual function after oophorectomy. N Engl J Med 343 (2000), 682–688.
20. 20 Braunstein, G.D., Sundwall, D.A., Katz, M., Shifren, J.L., Buster, J.E., Simon, J.A., et al. Safety and efficacy of a testosterone patch for the treatment of hypoactive sexual desire disorder in surgically menopausal women: a randomized, placebo-controlled trial. Arch Intern Med 165 (2005), 1582–1589.
21. 21 Davis, S.R., van der Mooren, M.J., van Lunsen, R.H., Lopes, P., Ribot, C., Rees, M., et al. Efficacy and safety of a testosterone patch for the treatment of hypoactive sexual desire disorder in surgically menopausal women: a randomized, placebo-controlled trial. Menopause 13 (2006), 387–396.
22. 22 Floter, A., Nathorst-Boos, J., Carlstrom, K., von Schoultz, B., Addition of testosterone to estrogen replacement therapy in oophorectomized women: effects on sexuality and well-being. Climacteric 5 (2002), 357–365.
23. 23 Gallagher, J.C., Effect of early menopause on bone mineral density and fractures. Menopause 14 (2007), 567–571.
24. 24 Mallmin, H., Ljunghall, S., Persson, I., Bergstrom, R., Risk factors for fractures of the distal forearm: a population-based case-control study. Osteoporos Int 4 (1994), 298–304.
25. 25 Vega, E.M., Egea, M.A., Mautalen, C.A., Influence of the menopausal age on the severity of osteoporosis in women with vertebral fractures. Maturitas 19 (1994), 117–124.
26. 26 Tuppurainen, M., Kroger, H., Honkanen, R., Puntila, E., Huopio, J., Saarikoski, S., et al. Risks of perimenopausal fractures—a prospective population-based study. Acta Obstet Gynecol Scand 74 (1995), 624–628.
27. 27 Johansson, C., Mellstrom, D., An earlier fracture as a risk factor for new fracture and its association with smoking and menopausal age in women. Maturitas 24 (1996), 97–106.
28. 28 van Der Voort, D.J., van Der Weijer, P.H., Barentsen, R., Early menopause: increased fracture risk at older age. Osteoporos Int 14 (2003), 525–530.
29. 29 van der Klift, M., de Laet, C.E., McCloskey, E.V., Johnell, O., Kanis, J.A., Hofman, A., et al. Risk factors for incident vertebral fractures in men and women: the Rotterdam Study. J Bone Miner Res 19 (2004), 1172–1180.
30. 30 Anasti, J.N., Kalantaridou, S.N., Kimzey, L.M., Defensor, R.A., Nelson, L.M., Bone loss in young women with karyotypically normal spontaneous premature ovarian failure. Obstet Gynecol 91 (1998), 12–15.
31. 31 Ohta, H., Sugimoto, I., Masuda, A., Komukai, S., Suda, Y., Makita, K., et al. Decreased bone mineral density associated with early menopause progresses for at least ten years: cross-sectional comparisons between early and normal menopausal women. Bone 18 (1996), 227–231.
32. 32 Leite-Silva, P., Bedone, A., Pinto-Neto, A.M., Costa, J.V., Costa-Paiva, L., Factors associated with bone density in young women with karyotypically normal spontaneous premature ovarian failure. Arch Gynecol Obstet 280 (2009), 177–181.
33. 33 Popat, V.B., Calis, K.A., Vanderhoof, V.H., Cizza, G., Reynolds, J.C., Sebring, N., et al. Bone mineral density in estrogen-deficient young women. J Clin Endocrinol Metab 94 (2009), 2277–2283.
34. 34 Alzubaidi, N.H., Chapin, H.L., Vanderhoof, V.H., Calis, K.A., Nelson, L.M., Meeting the needs of young women with secondary amenorrhea and spontaneous premature ovarian failure. Obstet Gynecol 99 (2002), 720–725.
35. 35 Holick, M.F., Binkley, N.C., Bischoff-Ferrari, H.A., Gordon, C.M., Hanley, D.A., Heaney, R.P., et al. Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 96 (2011), 1911–1930.
36. 36 Popat, V.B., Calis, K.A., Kalantaridou, S.N., Vanderhoof, V.H., Koziol, D., Troendle, J.F., et al. Bone mineral density in young women with primary ovarian insufficiency: results of a three-year randomized controlled trial of physiological transdermal estradiol and testosterone replacement. J Clin Endocrinol Metab 99 (2014), 3418–3426.
37. 37 Crofton, P.M., Evans, N., Bath, L.E., Warner, P., Whitehead, T.J., Critchley, H.O., et al. Physiological versus standard sex steroid replacement in young women with premature ovarian failure: effects on bone mass acquisition and turnover. Clin Endocrinol (Oxf) 73 (2010), 707–714.
38. 38 Cartwright, B., Robinson, J., Seed, P.T., Fogelman, I., Rymer, J., Hormone replacement therapy versus the combined oral contraceptive pill in premature ovarian failure: a randomised controlled trial of the effects on bone mineral density. J Clin Endocrinol Metab 101 (2016), 3497–3505.
39. 39 Colditz, G.A., Willett, W.C., Stampfer, M.J., Rosner, B., Speizer, F.E., Hennekens, C.H., Menopause and the risk of coronary heart disease in women. N Engl J Med 316 (1987), 1105–1110.
40. 40 Muka, T., Oliver-Williams, C., Kunutsor, S., Laven, J.S., Fauser, B.C., Chowdhury, R., et al. Association of age at onset of menopause and time since onset of menopause with cardiovascular outcomes, intermediate vascular traits, and all-cause mortality: a systematic review and meta-analysis. JAMA Cardiol, 2016.
41. 41 Kalantaridou, S.N., Naka, K.K., Papanikolaou, E., Kazakos, N., Kravariti, M., Calis, K.A., et al. Impaired endothelial function in young women with premature ovarian failure: normalization with hormone therapy. J Clin Endocrinol Metab 89 (2004), 3907–3913.
42. 42 Hu, F.B., Grodstein, F., Hennekens, C.H., Colditz, G.A., Johnson, M., Manson, J.E., et al. Age at natural menopause and risk of cardiovascular disease. Arch Intern Med 159 (1999), 1061–1066.
43. 43 Jacobsen, B.K., Knutsen, S.F., Fraser, G.E., Age at natural menopause and total mortality and mortality from ischemic heart disease: the Adventist Health Study. J Clin Epidemiol 52 (1999), 303–307.
44. 44 Rivera, C.M., Grossardt, B.R., Rhodes, D.J., Brown, R.D. Jr., Roger, V.L., Melton, L.J. 3rd, et al. Increased cardiovascular mortality after early bilateral oophorectomy. Menopause 16 (2009), 15–23.
45. 45 Lokkegaard, E., Jovanovic, Z., Heitmann, B.L., Keiding, N., Ottesen, B., Pedersen, A.T., The association between early menopause and risk of ischaemic heart disease: influence of hormone therapy. Maturitas 53 (2006), 226–233.
46. 46 Archer, D.F., Premature menopause increases cardiovascular risk. Climacteric 12:Suppl 1 (2009), 26–31.
47. 47 van der Schouw, Y.T., van der Graaf, Y., Steyerberg, E.W., Eijkemans, J.C., Banga, J.D., Age at menopause as a risk factor for cardiovascular mortality. Lancet 347 (1996), 714–718.
48. 48 Rocca, W.A., Grossardt, B.R., Miller, V.M., Shuster, L.T., Brown, R.D. Jr., Premature menopause or early menopause and risk of ischemic stroke. Menopause 19 (2012), 272–277.
49. 49 Orshan, S.A., Ventura, J.L., Covington, S.N., Vanderhoof, V.H., Troendle, J.F., Nelson, L.M., Women with spontaneous 46,XX primary ovarian insufficiency (hypergonadotropic hypogonadism) have lower perceived social support than control women. Fertil Steril 92 (2009), 688–693.
50. 50 Schmidt, P.J., Cardoso, G.M., Ross, J.L., Haq, N., Rubinow, D.R., Bondy, C.A., Shyness, social anxiety, and impaired self-esteem in Turner syndrome and premature ovarian failure. JAMA 295 (2006), 1374–1376.
51. 51 Schmidt, P.J., Luff, J.A., Haq, N.A., Vanderhoof, V.H., Koziol, D.E., Calis, K.A., et al. Depression in women with spontaneous 46, XX primary ovarian insufficiency. J Clin Endocrinol Metab 96 (2011), E278–E287.
52. 52 Freeman, E.W., Sammel, M.D., Liu, L., Gracia, C.R., Nelson, D.B., Hollander, L., Hormones and menopausal status as predictors of depression in women in transition to menopause. Arch Gen Psychiatry 61 (2004), 62–70.
53. 53 Cohen, L.S., Soares, C.N., Vitonis, A.F., Otto, M.W., Harlow, B.L., Risk for new onset of depression during the menopausal transition: the Harvard study of moods and cycles. Arch Gen Psychiatry 63 (2006), 385–390.
54. 54 Soares, C.N., Almeida, O.P., Joffe, H., Cohen, L.S., Efficacy of estradiol for the treatment of depressive disorders in perimenopausal women: a double-blind, randomized, placebo-controlled trial. Arch Gen Psychiatry 58 (2001), 529–534.
55. 55 Zweifel, J.E., O'Brien, W.H., A meta-analysis of the effect of hormone replacement therapy upon depressed mood. Psychoneuroendocrinology 22 (1997), 189–212.
56. 56 Schmidt, P.J., Nieman, L., Danaceau, M.A., Tobin, M.B., Roca, C.A., Murphy, J.H., et al. Estrogen replacement in perimenopause-related depression: a preliminary report. Am J Obstet Gynecol 183 (2000), 414–420.
57. 57 Guerrieri, G.M., Martinez, P.E., Klug, S.P., Haq, N.A., Vanderhoof, V.H., Koziol, D.E., et al. Effects of physiologic testosterone therapy on quality of life, self-esteem, and mood in women with primary ovarian insufficiency. Menopause 21 (2014), 952–961.
58. 58 Morrison, J.H., Brinton, R.D., Schmidt, P.J., Gore, A.C., Estrogen, menopause, and the aging brain: how basic neuroscience can inform hormone therapy in women. J Neurosci 26 (2006), 10332–10348.
59. 59 Maki, P.M., Resnick, S.M., Effects of estrogen on patterns of brain activity at rest and during cognitive activity: a review of neuroimaging studies. Neuroimage 14 (2001), 789–801.
60. 60 Yaffe, K., Sawaya, G., Lieberburg, I., Grady, D., Estrogen therapy in postmenopausal women: effects on cognitive function and dementia. JAMA 279 (1998), 688–695.
61. 61 LeBlanc, E.S., Janowsky, J., Chan, B.K., Nelson, H.D., Hormone replacement therapy and cognition: systematic review and meta-analysis. JAMA 285 (2001), 1489–1499.
62. 62 van Kasteren, Y.M., Schoemaker, J., Premature ovarian failure: a systematic review on therapeutic interventions to restore ovarian function and achieve pregnancy. Hum Reprod Update 5 (1999), 483–492.
63. 63 Hubayter, Z.R., Popat, V., Vanderhoof, V.H., Ndubizu, O., Johnson, D., Mao, E., et al. A prospective evaluation of antral follicle function in women with 46,XX spontaneous primary ovarian insufficiency. Fertil Steril 94 (2010), 1769–1774.
64. 64 Nelson, L.M., Anasti, J.N., Kimzey, L.M., Defensor, R.A., Lipetz, K.J., White, B.J., et al. Development of luteinized graafian follicles in patients with karyotypically normal spontaneous premature ovarian failure. J Clin Endocrinol Metab 79 (1994), 1470–1475.
65. 65 Popat, V.B., Vanderhoof, V.H., Calis, K.A., Troendle, J.F., Nelson, L.M., Normalization of serum luteinizing hormone levels in women with 46,XX spontaneous primary ovarian insufficiency. Fertil Steril 89 (2008), 429–433.
66. 66 Tartagni, M., Cicinelli, E., de Pergola, G., de Salvia, M.A., Lavopa, C., Loverro, G., Effects of pretreatment with estrogens on ovarian stimulation with gonadotropins in women with premature ovarian failure: a randomized, placebo-controlled trial. Fertil Steril 87 (2007), 858–861.
67. 67 Taylor, A.E., Adams, J.M., Mulder, J.E., Martin, K.A., Sluss, P.M., Crowley, W.F. Jr., A randomized, controlled trial of estradiol replacement therapy in women with hypergonadotropic amenorrhea. J Clin Endocrinol Metab 81 (1996), 3615–3621.
68. 68 Check, J.H., Nowroozi, K., Chase, J.S., Nazari, A., Shapse, D., Vaze, M., Ovulation induction and pregnancies in 100 consecutive women with hypergonadotropic amenorrhea. Fertil Steril 53 (1990), 811–816.
69. 69 Smith, J.A., Vitale, S., Reed, G.F., Grieshaber, S.A., Goodman, L.A., Vanderhoof, V.H., et al. Dry eye signs and symptoms in women with premature ovarian failure. Arch Ophthalmol 122 (2004), 151–156.
70. 70 Sullivan, B.D., Evans, J.E., Cermak, J.M., Krenzer, K.L., Dana, M.R., Sullivan, D.A., Complete androgen insensitivity syndrome: effect on human meibomian gland secretions. Arch Ophthalmol 120 (2002), 1689–1699.
71. 71 Sullivan, B.D., Evans, J.E., Krenzer, K.L., Reza Dana, M., Sullivan, D.A., Impact of antiandrogen treatment on the fatty acid profile of neutral lipids in human meibomian gland secretions. J Clin Endocrinol Metab 85 (2000), 4866–4873.
72. 72 Hipp, H.S., Charen, K.H., Spencer, J.B., Allen, E.G., Sherman, S.L., Reproductive and gynecologic care of women with fragile X primary ovarian insufficiency (FXPOI). Menopause 23 (2016), 993–999.
73. 73 Mishell, D.R. Jr., Nakamura, R.M., Crosignani, P.G., Stone, S., Kharma, K., Nagata, Y., et al. Serum gonadotropin and steroid patterns during the normal menstrual cycle. Am J Obstet Gynecol 111 (1971), 60–65.
74. 74 Scarabin, P.Y., Oger, E., Plu-Bureau, G., Differential association of oral and transdermal oestrogen-replacement therapy with venous thromboembolism risk. Lancet 362 (2003), 428–432.
75. 75 Canonico, M., Oger, E., Plu-Bureau, G., Conard, J., Meyer, G., Levesque, H., et al. Hormone therapy and venous thromboembolism among postmenopausal women: impact of the route of estrogen administration and progestogens: the ESTHER study. Circulation 115 (2007), 840–845.
76. 76 Canonico, M., Plu-Bureau, G., Lowe, G.D., Scarabin, P.Y., Hormone replacement therapy and risk of venous thromboembolism in postmenopausal women: systematic review and meta-analysis. BMJ 336 (2008), 1227–1231.
77. 77 Mohammed, K., abu Dabrh, A.M., Benkhadra, K., al Nofal, A., Carranza Leon, B.G., Prokop, L.J., et al. Oral vs. transdermal estrogen therapy and vascular events: a systematic review and meta-analysis. J Clin Endocrinol Metab 100 (2015), 4012–4020.
78. 78 Hemelaar, M., van der Mooren, M.J., Rad, M., Kluft, C., Kenemans, P., Effects of nonoral postmenopausal hormone therapy on markers of cardiovascular risk: a systematic review. Fertil Steril 90 (2008), 642–672.
79. 79 Post, M.S., Christella, M., Thomassen, L.G., van der Mooren, M.J., van Baal, W.M., Rosing, J., et al. Effect of oral and transdermal estrogen replacement therapy on hemostatic variables associated with venous thrombosis: a randomized, placebo-controlled study in postmenopausal women. Arterioscler Thromb Vasc Biol 23 (2003), 1116–1121.
80. 80 Renoux, C., dell'Aniello, S., Garbe, E., Suissa, S., Transdermal and oral hormone replacement therapy and the risk of stroke: a nested case-control study. BMJ, 340, 2010, c2519.
81. 81 Sidney, S., Cheetham, T.C., Connell, F.A., Ouellet-Hellstrom, R., Graham, D.J., Davis, D., et al. Recent combined hormonal contraceptives (CHCs) and the risk of thromboembolism and other cardiovascular events in new users. Contraception 87 (2013), 93–100.
82. 82 Langrish, J.P., Mills, N.L., Bath, L.E., Warner, P., Webb, D.J., Kelnar, C.J., et al. Cardiovascular effects of physiological and standard sex steroid replacement regimens in premature ovarian failure. Hypertension 53 (2009), 805–811.
83. 83 Gibbons, W.E., Moyer, D.L., Lobo, R.A., Roy, S., Mishell, D.R. Jr., Biochemical and histologic effects of sequential estrogen/progestin therapy on the endometrium of postmenopausal women. Am J Obstet Gynecol 154 (1986), 456–461.
84. 84 Bjarnason, K., Cerin, A., Lindgren, R., Weber, T., Scandinavian Long Cycle Study Group. Adverse endometrial effects during long cycle hormone replacement therapy. Maturitas 32 (1999), 161–170.
85. 85 Darney, P.D., The androgenicity of progestins. Am J Med 98 (1995), 104S–110S.
86. 86 Writing Group for the PEPI Trial, Effects of hormone replacement therapy on endometrial histology in postmenopausal women. The Postmenopausal Estrogen/Progestin Interventions (PEPI) trial. JAMA 275 (1996), 370–375.
87. 87 Wildemeersch, D., Janssens, D., Weyers, S., Continuous combined parenteral estrogen substitution and intrauterine progestogen delivery: the ideal HST combination?. Maturitas 51 (2005), 207–214.
88. 88 Wildemeersch, D., Andrade, A., Goldstuck, N., Femilis 60 Levonorgestrel-releasing intrauterine system—a review of 10 years of clinical experience. Clin Med Insights Reprod Health 10 (2016), 19–27.
89. 89 Nahoul, K., Dehennin, L., Scholler, R., Radioimmunoassay of plasma progesterone after oral administration of micronized progesterone. J Steroid Biochem 26 (1987), 241–249.
90. 90 Barrett-Connor, E., Slone, S., Greendale, G., Kritz-Silverstein, D., Espeland, M., Johnson, S.R., et al. The Postmenopausal Estrogen/Progestin Interventions study: primary outcomes in adherent women. Maturitas 27 (1997), 261–274.
91. 91 Harman, S.M., Black, D.M., Naftolin, F., Brinton, E.A., Budoff, M.J., Cedars, M.I., et al. Arterial imaging outcomes and cardiovascular risk factors in recently menopausal women: a randomized trial. Ann Intern Med 161 (2014), 249–260.
92. 92 Abraham, G.E., Ovarian and adrenal contribution to peripheral androgens during the menstrual cycle. J Clin Endocrinol Metab 39 (1974), 340–346.
93. 93 Wierman, M.E., Arlt, W., Basson, R., Davis, S.R., Miller, K.K., Murad, M.H., et al. Androgen therapy in women: a reappraisal: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 99 (2014), 3489–3510.
94. 94 Zuckerman-Levin, N., Frolova-Bishara, T., Militianu, D., Levin, M., Aharon-Peretz, J., Hochberg, Z., Androgen replacement therapy in Turner syndrome: a pilot study. J Clin Endocrinol Metab 94 (2009), 4820–4827.
95. 95 Elias, A.N., Pandian, M.R., Rojas, F.J., Serum levels of androstenedione, testosterone and dehydroepiandrosterone sulfate in patients with premature ovarian failure to age-matched menstruating controls. Gynecol Obstet Invest 43 (1997), 47–48.
96. 96 Gleicher, N., Barad, D.H., Dehydroepiandrosterone (DHEA) supplementation in diminished ovarian reserve (DOR). Reprod Biol Endocrinol, 9, 2011, 67.
97. 97 Yilmaz, N., Uygur, D., Inal, H., Gorkem, U., Cicek, N., Mollamahmutoglu, L., Dehydroepiandrosterone supplementation improves predictive markers for diminished ovarian reserve: serum AMH, inhibin B and antral follicle count. Eur J Obstet Gynecol Reprod Biol 169 (2013), 257–260.
98. 98 Narkwichean, A., Maalouf, W., Campbell, B.K., Jayaprakasan, K., Efficacy of dehydroepiandrosterone to improve ovarian response in women with diminished ovarian reserve: a meta-analysis. Reprod Biol Endocrinol, 11, 2013, 44.
99. 99 Hanton, L., Axelrod, L., Bakalov, V., Bondy, C.A., The importance of estrogen replacement in young women with Turner syndrome. J Womens Health (Larchmt) 12 (2003), 971–977.
100. 100 Bakalov, V.K., Chen, M.L., Baron, J., Hanton, L.B., Reynolds, J.C., Stratakis, C.A., et al. Bone mineral density and fractures in Turner syndrome. Am J Med 115 (2003), 259–264.
101. 101 Hogler, W., Briody, J., Moore, B., Garnett, S., Lu, P.W., Cowell, C.T., Importance of estrogen on bone health in Turner syndrome: a cross-sectional and longitudinal study using dual-energy X-ray absorptiometry. J Clin Endocrinol Metab 89 (2004), 193–199.
102. 102 Bertelloni, S., Cinquanta, L., Baroncelli, G.I., Simi, P., Rossi, S., Saggese, G., Volumetric bone mineral density in young women with Turner's syndrome treated with estrogens or estrogens plus growth hormone. Horm Res 53 (2000), 72–76.
103. 103 Deniz, G., Antoine, C., Liebens, F., Carly, B., Pastijn, A., Rozenberg, S., Treatment of premature menopause in breast cancer patients. Acta Chir Belg 107 (2007), 263–266.
104. 104 Nappi, R.E., Cassani, C., Rossi, M., Zanellini, F., Spinillo, A., Dealing with premature menopause in women at high-risk for hereditary genital and breast cancer. Minerva Ginecol, 2016.
105. 105 Which pill to choose if breastfeeding. Fam Plann Inf Serv, 1, 1978, 17.
106. 106 Tankeyoon, M., Dusitsin, N., Chalapati, S., Koetsawang, S., Saibiang, S., Sas, M., et al. WHO Special Programme of Research, Development and Research Training in Human Reproduction Task Force on Oral Contraceptives. Effects of hormonal contraceptives on milk volume and infant growth. Contraception 30 (1984), 505–522.
107. 107 Kelsey, J.J., Hormonal contraception and lactation. J Hum Lact 12 (1996), 315–318.
108. 108 van Noord, P.A., Dubas, J.S., Dorland, M., Boersma, H., te Velde, E., Age at natural menopause in a population-based screening cohort: the role of menarche, fecundity, and lifestyle factors. Fertil Steril 68 (1997), 95–102.
109. 109 Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol 13 (2012), 1141–1151.
110. 110 Marchetti, C., Iadarola, R., Palaia, I., di Donato, V., Perniola, G., Muzii, L., et al. Hormone therapy in oophorectomized BRCA1/2 mutation carriers. Menopause 21 (2014), 763–768.
111. 111 Rebbeck, T.R., Friebel, T., Wagner, T., Lynch, H.T., Garber, J.E., Daly, M.B., et al. Effect of short-term hormone replacement therapy on breast cancer risk reduction after bilateral prophylactic oophorectomy in BRCA1 and BRCA2 mutation carriers: the PROSE Study Group. J Clin Oncol 23 (2005), 7804–7810.
112. 112 Svejme, O., Ahlborg, H.G., Nilsson, J.A., Karlsson, M.K., Early menopause and risk of osteoporosis, fracture and mortality: a 34-year prospective observational study in 390 women. BJOG 119 (2012), 810–816.
113. 113 Sioka, C., Fotopoulos, A., Georgiou, A., Xourgia, X., Papadopoulos, A., Kalef-Ezra, J.A., Age at menarche, age at menopause and duration of fertility as risk factors for osteoporosis. Climacteric 13 (2010), 63–71.
114. 114 de Kleijn, M.J., van der Schouw, Y.T., Verbeek, A.L., Peeters, P.H., Banga, J.D., van der Graaf, Y., Endogenous estrogen exposure and cardiovascular mortality risk in postmenopausal women. Am J Epidemiol 155 (2002), 339–345.
115. 115 Mondul, A.M., Rodriguez, C., Jacobs, E.J., Calle, E.E., Age at natural menopause and cause-specific mortality. Am J Epidemiol 162 (2005), 1089–1097.
116. 116 Lobo, R.A., What the future holds for women after menopause: where we have been, where we are, and where we want to go. Climacteric 17:Suppl 2 (2014), 12–17.