Animal models for the effective development of atrophic vaginitis therapies: possibilities and limitations

Bibliography

• Mac Bride MB, Rhodes DJ, Shuster LT. Vulvovaginal atrophy. Mayo Clin Proc 2010;85(1):87-94
   PubMed Web of Science ®Google Scholar
• Willhite L, O'Connell M. Urogenital atrophy: prevention and treatment. Pharmacotherapy 2001;21:464-80
   PubMed Web of Science ®Google Scholar
• Crandall C, Petersen L, Ganz PA, et al. Association of breast cancer and its therapy with menopause-related symptoms. Menopause 2004;11(5):519-30
   PubMed Web of Science ®Google Scholar
• Fares E, Pyle WG, Ray G, et al. The impact of ovariectomy on calcium homeostasis and myofilament calcium sensitivity in the aging mouse heart. PLoS One 2013;8(9):e74719
   PubMedGoogle Scholar
• Kavanagh K, Koudy Williams J, Wagner JD. Naturally occurring menopause in cynomolgus monkeys: changes in hormone, lipid, and carbohydrate measures with hormonal status. J Med Primatol 2005;34(4):171-7
   PubMed Web of Science ®Google Scholar
• Walker DM, Gore AC. Transgenerational neuroendocrine disruption of reproduction. Nat Rev Endocrinol 2011;7(4):197-207
   PubMed Web of Science ®Google Scholar
• Brinton D. Minireview: translational animal models of human menopause: challenges and emerging opportunities. Endocrinology 2012;153(8):3571-8
   PubMed Web of Science ®Google Scholar
• Winneker RC, Harris HA. Progress and prospects in treating postmenopausal vaginal atrophy. Clin Pharmacol Ther 2011;89(1):129-32
   PubMed Web of Science ®Google Scholar
• Mayer LP, Devine PJ, Dyer CA, et al. The follicle-deplete mouse ovary produces androgen. Biol Reprod 2004;71(1):130-8
   PubMed Web of Science ®Google Scholar
• Jacoby R, Fox J, Davisson M. Biology and diseases of mice. In: Fox JG AL, Loew FM, Quimby FW, editors, Laboratory animal medicine. 2 edition. Academic Press, San Diego; 2002
   Google Scholar
• Baeza I, De Castro NM, Gimenez-Llort L, et al. Ovariectomy, a model of menopause in rodents, causes a premature aging of the nervous and immune systems. J Neuroimmunol 2010;219(1-2):90-9
   PubMed Web of Science ®Google Scholar
• Nelson JF, Felicio LS. Hormonal influences on reproductive aging in mice. Ann NY Acad Sci 1990;592:8-12
   PubMed Web of Science ®Google Scholar
• Gamé X, Roumiguié M, Bouali O, et al. Vaginal lubrication after cervicovaginal stimulation is facilitated by phosphodiesterase type 5 inhibition in ovariectomized mice. J Sex Med 2013;10(6):1452-60
   PubMed Web of Science ®Google Scholar
• Van Kempen TA, Milner TA, Waters EM. Accelerated ovarian failure: a novel, chemically induced animal model of menopause. Brain Res 2011;1379:176-87
   PubMed Web of Science ®Google Scholar
• Danilovich N, Babu P, Xing W, et al. Estrogen deficiency, obesity, and skeletal abnormalities in follicle-stimulating hormone receptor knockout (FORKO) female mice. Endocrinology 2000;141(11):4295-308
   PubMed Web of Science ®Google Scholar
• Maximov PY, Lee TM, Jordan VC. The discovery and development of selective estrogen receptor modulators (SERMs) for clinical practice. Curr Clin Pharmacol 2013;8(2):135-55
   PubMedGoogle Scholar
• Pinkerton JV, Stanczyk FZ. Clinical effects of selective estrogen receptor modulators on vulvar and vaginal atrophy. Menopause 2013. [ Epub ahead of print]
   Web of Science ®Google Scholar
• Luo S, Sourla A, Labrie C, et al. Effect of twenty-four-week treatment with the antiestrogen EM-800 on estrogen-sensitive parameters in intact and ovariectomized mice. Endocrinology 1998;139(5):2645-56
   PubMed Web of Science ®Google Scholar
• Sourla A, Luo S, Labrie C, et al. Morphological changes induced by 6-month treatment of intact and ovariectomized mice with tamoxifen and the pure antiestrogen EM-800. Endocrinology 1997;138(12):5605-17
   PubMed Web of Science ®Google Scholar
• Luo S, Martel C, Sourla A, et al. Comparative effects of 28-day treatment with the new anti-estrogen EM-800 and tamoxifen on estrogen-sensitive parameters in intact mice. Int J Cancer 1997;73(3):381-91
   PubMed Web of Science ®Google Scholar
• Goldman JM, Murr AS, Cooper RL. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B Dev Reprod Toxicol 2007;80(2):84-97
   PubMed Web of Science ®Google Scholar
• Bellino FL. Nonprimate animal models of menopause: workshop report. Menopause 2000;7(1):14-24
   PubMed Web of Science ®Google Scholar
• Johnson M. Mater methods. 2012. Available from: http://goo.gl/mG8fBb [Cited 24 October 2013]
   Google Scholar
• Davis BJ, Travlos G, McShane T. Reproductive endocrinology and toxicological pathology over the life span of the female rodent. Toxicol Pathol 2001;29(1):77-83
   PubMed Web of Science ®Google Scholar
• Acosta JI, Mayer L, Talboom JS, et al. Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology 2009;150(9):4248-59
   PubMed Web of Science ®Google Scholar
• Min K, Munarriz R, Kim NN, et al. Effects of ovariectomy and estrogen replacement on basal and pelvic nerve stimulated vaginal lubrication in an animal model. J Sex Marital Ther 2003;29(Suppl 1):77-84
   PubMed Web of Science ®Google Scholar
• Otto C, Kantner I, Nubbemeyer R, et al. Estradiol release kinetics determine tissue response in ovariectomized rats. Endocrinology 2012;153(4):1725-33
   PubMed Web of Science ®Google Scholar
• Muhammad FS, Goode AK, Kock ND, et al. Effects of 4-vinylcyclohexene diepoxide on peripubertal and adult Sprague-Dawley rats: ovarian, clinical, and pathologic outcomes. Comp Med 2009;59(1):46-59
   PubMed Web of Science ®Google Scholar
• Deveci I, Surmeli M, Senem Deveci H, et al. Effects of polycystic ovary syndrome and menopause on rat soft palate and base of tongue. Otolaryngol Head Neck Surg 2013;148(4):595-601
   PubMed Web of Science ®Google Scholar
• Hoyer PB, Devine PJ, Hu X, et al. Ovarian toxicity of 4-vinylcyclohexene diepoxide: a mechanistic model. Toxicol Pathol 2001;29(1):91-9
   PubMed Web of Science ®Google Scholar
• Lynch C. Vaginal estrogen therapy for the treatment of atrophic vaginitis. J Womens Health (Larchmt) 2009;18(10):1595-606
   PubMed Web of Science ®Google Scholar
• Hofseth LJ, Raafat AM, Osuch JR, et al. Hormone replacement therapy with estrogen or estrogen plus medroxyprogesterone acetate is associated with increased epithelial proliferation in the normal postmenopausal breast. J Clin Endocrinol Metab 1999;84(12):4559-65
   PubMed Web of Science ®Google Scholar
• Doren M, Azzawi FA, Donnez J, et al. Therapeutic value and long-term safety of pulsed estrogen therapy. Maturitas 2001;38:S23-30
   PubMed Web of Science ®Google Scholar
• Rozenberg S, Pornel B, Koninckx PR, et al. Endometrium protection and acceptability of nasally administered continuously combined hormone therapy: a multicentre, multinational, double-blind trial in post-menopausal women evaluating three regimens of 17 beta-estradiol and norethisterone when compared with an orally administered 17 beta-estradiol norethisterone regimen. Hum Reprod 2009;24(7):1739-47
   PubMed Web of Science ®Google Scholar
• Lopez-Belmonte J, Nieto C, Estevez J, et al. Comparative uterine effects on ovariectomized rats after repeated treatment with different vaginal estrogen formulations. Maturitas 2012;72(4):353-8
   PubMed Web of Science ®Google Scholar
• Laws SC, Carey SA, Ferrell JM, et al. Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol Sci 2000;54(1):154-67
   PubMed Web of Science ®Google Scholar
• Moore DH, Chasseaud LF, Darragh A, et al. The percutaneous absorption and excretion of promestriene (3-propoxy-17 beta-methoxy-1,3,5(10)-estratriene) in rats and humans. Steroids 1983;41(1):15-22
   PubMed Web of Science ®Google Scholar
• Berger L, El-Alfy M, Martel C, et al. Effects of dehydroepiandrosterone, Premarin and Acolbifene on histomorphology and sex steroid receptors in the rat vagina. J Steroid Biochem Mol Biol 2005;96(2):201-15
   PubMed Web of Science ®Google Scholar
• Sourla A, Flamand M, Belanger A, et al. Effect of dehydroepiandrosterone on vaginal and uterine histomorphology in the rat. J Steroid Biochem Mol Biol 1998;66(3):137-49
   PubMed Web of Science ®Google Scholar
• Labrie F, Archer D, Bouchard C, et al. High internal consistency and efficacy of intravaginal DHEA for vaginal atrophy. Gynecol Endocrinol 2010;26(7):524-32
   PubMed Web of Science ®Google Scholar
• Panjari M, Davis SR. Vaginal DHEA to treat menopause related atrophy: a review of the evidence. Maturitas 2011;70(1):22-5
   PubMed Web of Science ®Google Scholar
• Wang XN, Simmons HA, Salatto CT, et al. Lasofoxifene enhances vaginal mucus formation without causing hypertrophy and increases estrogen receptor beta and androgen receptor in rats. Menopause 2006;13(4):609-20
   PubMed Web of Science ®Google Scholar
• Unkila M, Kari S, Yatkin E, et al. Vaginal effects of ospemifene in the ovariectomized rat preclinical model of menopause. J Steroid Biochem Mol Biol 2013;138C:107-15
   Google Scholar
• Wurz GT, Soe LH, Degregorio MW. Ospemifene, vulvovaginal atrophy, and breast cancer. Maturitas 2013. [ Epub ahead of print]
   PubMed Web of Science ®Google Scholar
• Kim DI, Choi MS, Pak SC, et al. The effects of Sutaehwan-Gami on menopausal symptoms induced by ovariectomy in rats. BMC Complement Altern Med 2012;12:227
   PubMed Web of Science ®Google Scholar
• Komi J, Lankinen KS, Harkonen P, et al. Effects of ospemifene and raloxifene on hormonal status, lipids, genital tract, and tolerability in postmenopausal women. Menopause 2005;12(2):202-9
   PubMed Web of Science ®Google Scholar
• Hascalik S, Celik O, Tamser M, et al. Effects of resveratrol, raloxifene, tibolone and conjugated equine estrogen on vaginal squamous cell maturation of ovariectomized rats. Gynecol Obstet Invest 2005;60(4):186-91
   PubMed Web of Science ®Google Scholar
• Cherdshewasart W, Kitsamai Y, Malaivijitnond S. Evaluation of the estrogenic activity of the wild Pueraria mirifica by vaginal cornification assay. J Reprod Dev 2007;53(2):385-93
   PubMed Web of Science ®Google Scholar
• Ateba SB, Njamen D, Medjakovic S, et al. Eriosema laurentii De Wild (Leguminosae) methanol extract has estrogenic properties and prevents menopausal symptoms in ovariectomized Wistar rats. J Ethnopharmacol 2013;150(1):298-307
   PubMed Web of Science ®Google Scholar
• Bahr JM, Nakai M, Rivera A, et al. Dietary soy protein and isoflavones: minimal beneficial effects on bone and no effect on the reproductive tract of sexually mature ovariectomized Sprague-Dawley rats. Menopause 2005;12(2):165-73
   PubMed Web of Science ®Google Scholar
• Manjanatha M, Shelton S, Bishop M, et al. Dietary effects of soy isoflavones daidzein and genistein on 7,12-dimethylbenz [a] anthracene-induced mammary mutagenesis and carcinogenesis in ovariectomized Big Blue transgenic rats. Carcinogenesis 2006;27(10):1970-9
   PubMed Web of Science ®Google Scholar
• Rimoldi G, Christoffel J, Seidlova-Wuttke D, et al. Effects of chronic genistein treatment in mammary gland, uterus, and vagina. Environ Health Perspect 2007;115(Suppl 1):62-8
   PubMedGoogle Scholar
• Abramov Y, Golden B, Sullivan M, et al. Vaginal incisional wound healing in a rabbit menopause model: a histologic analysis. Int Urogynecol J 2012;23(12):1763-9
   PubMed Web of Science ®Google Scholar
• Abramov Y, Hirsch E, Ilievski V, et al. Transforming growth factor beta1 gene expression during vaginal wound healing in a rabbit menopause model. BJOG 2013;120(2):251-6
   PubMed Web of Science ®Google Scholar
• Acarturk F, Robinson JR. Vaginal permeability and enzymatic activity studies in normal and ovariectomized rabbits. Pharm Res 1996;13(5):779-83
   PubMed Web of Science ®Google Scholar
• Higgins EW, Rao A, Baumann SS, et al. Effect of estrogen replacement on the histologic response to polypropylene mesh implanted in the rabbit vagina model. Am J Obstet Gynecol 2009;201(5):505; e1-9
   PubMedGoogle Scholar
• Quintela LA, Pena AI, Vega MD, et al. Reproductive performance of rabbit does artificially inseminated via intravaginal administration of [des-Gly 10, D-Ala6]-LHRH ethylamide as ovulation inductor. Reprod Domest Anim 2009;44(5):829-33
   PubMed Web of Science ®Google Scholar
• Phillips A, Hahn DW, McGuire JL. Comparative effect of estriol and equine conjugated estrogens on the uterus and the vagina. Maturitas 1984;5(3):147-52
   PubMed Web of Science ®Google Scholar
• Adaikan PG, Srilatha B, Wheat AJ. Efficacy of red clover isoflavones in the menopausal rabbit model. Fertil Steril 2009;92(6):2008-13
   PubMed Web of Science ®Google Scholar
• Suzuki O, Koura M, Noguchi Y, et al. Optimization of superovulation induction by human menopausal gonadotropin in guinea pigs based on follicular waves and FSH-receptor homologies. Mol Reprod Dev 2003;64(2):219-25
   PubMed Web of Science ®Google Scholar
• Zern TL, West KL, Fernandez ML. Grape polyphenols decrease plasma triglycerides and cholesterol accumulation in the aorta of ovariectomized guinea pigs. J Nutr 2003;133(7):2268-72
   PubMed Web of Science ®Google Scholar
• Lilley KG, Epping RJ, Hafner LM. The guinea pig estrous cycle: correlation of vaginal impedance measurements with vaginal cytologic findings. Lab Anim Sci 1997;47(6):632-7
   PubMedGoogle Scholar
• Shideler SE, Gee NA, Chen J, et al. Estrogen and progesterone metabolites and follicle-stimulating hormone in the aged macaque female. Biol Reprod 2001;65(6):1718-25
   PubMed Web of Science ®Google Scholar
• Bellino FL, Wise PM. Nonhuman primate models of menopause workshop. Biol Reprod 2003;68(1):10-18
   PubMed Web of Science ®Google Scholar
• Walker ML, Herndon JG. Menopause in nonhuman primates? Biol Reprod 2008;79(3):398-406
   PubMed Web of Science ®Google Scholar
• Graham C. Reproductive function in aged female chimpanzees. Am J Phys Anthropol 1979;50:291-300
   PubMed Web of Science ®Google Scholar
• Packer C, Tatar M, Collins A. Reproductive cessation in female mammals. Nature 1998;392:807-11
   PubMed Web of Science ®Google Scholar
• Gilardi KV, Shideler SE, Valverde CR, et al. Characterization of the onset of menopause in the rhesus macaque. Biol Reprod 1997;57(2):335-40
   PubMed Web of Science ®Google Scholar
• Appt SE, Kaplan JR, Clarkson TB, et al. Destruction of primordial ovarian follicles in adult cynomolgus macaques after exposure to 4-vinylcyclohexene diepoxide: a nonhuman primate model of the menopausal transition. Fertil Steril 2006;86:1210-16
   PubMed Web of Science ®Google Scholar
• Appt SE, Clarkson TB, Lees CJ, et al. Low dose estrogens inhibit coronary artery atherosclerosis in postmenopausal monkeys. Maturitas 2006;55(2):187-94
   PubMed Web of Science ®Google Scholar
• Wagner JD, Clarkson TB, St Clair RW, et al. Estrogen and progesterone replacement therapy reduces low density lipoprotein accumulation in the coronary arteries of surgically postmenopausal cynomolgus monkeys. J Clin Invest 1991;88(6):1995-2002
   PubMed Web of Science ®Google Scholar
• Moyer DL, de Lignieres B, Driguez P, et al. Prevention of endometrial hyperplasia by progesterone during long-term estradiol replacement: influence of bleeding pattern and secretory changes. Fertil Steril 1993;59(5):992-7
   PubMed Web of Science ®Google Scholar
• Boerrigter PJ, van de Weijer PH, Baak JP, et al. Endometrial response in estrogen replacement therapy quarterly combined with a progestogen. Maturitas 1996;24(1-2):63-71
   PubMed Web of Science ®Google Scholar
• Robinson D, Rainer RO, Washburn SA, et al. Effects of estrogen and progestin replacement on the urogenital tract of the ovariectomized cynomolgus monkey. Neurourol Urodyn 1996;15(3):215-21
   PubMed Web of Science ®Google Scholar
• Wadsworth PF, Heywood R, Allen DG, et al. Treatment of rhesus monkeys (Macaca mulatta) with intravaginal rings loaded with levonorgestrel. Contraception 1979;20(6):559-67
   PubMed Web of Science ®Google Scholar
• Wood CE, Sitruk-Ware RL, Tsong YY, et al. Effects of estradiol with oral or intravaginal progesterone on risk markers for breast cancer in a postmenopausal monkey model. Menopause 2007;14(4):639-47
   PubMed Web of Science ®Google Scholar
• Cline JM, Paschold JC, Anthony MS, et al. Effects of hormonal therapies and dietary soy phytoestrogens on vaginal cytology in surgically postmenopausal macaques. Fertil Steril 1996;65(5):1031-5
   PubMed Web of Science ®Google Scholar
• Appt SE, Tormala R, Franke AA, et al. Soy-tibolone combination - effect on lipids in postmenopausal monkeys and women. Maturitas 2008;60(3-4):216-22
   PubMed Web of Science ®Google Scholar
• Wood CE, Appt SE, Clarkson TB, et al. Effects of high-dose soy isoflavones and equol on reproductive tissues in female cynomolgus monkeys. Biol Reprod 2006;75(3):477-86
   PubMed Web of Science ®Google Scholar
• Foth D, Cline JM, Romer T. [Effect of isoflavones on mammary gland and endometrium of postmenopausal macaques (Macaca fascicularis)]. Zentralbl Gynakol 2000;122(2):96-102
   PubMedGoogle Scholar
• Clarkson TB. Soy, soy phytoestrogens and cardiovascular disease. J Nutr 2002;132(3):566S-9S
   PubMed Web of Science ®Google Scholar
• Schnatz PF, Marakovits KA, O'Sullivan DM, et al. Response to an adequate dietary intake of vitamin D3 modulates the effect of estrogen therapy on bone density. J Womens Health (Larchmt) 2012;21(8):858-64
   PubMed Web of Science ®Google Scholar
• Lima SM, Yamada SS, Reis BF, et al. Effective treatment of vaginal atrophy with isoflavone vaginal gel. Maturitas 2013. [ Epub ahead of print]
   Web of Science ®Google Scholar
• Ghumman S. Atrophic vaginitis: diagnosis and treatment. J South Asian Feder Menopause Soc 2013;1(1):4-12
   Google Scholar
• Cardozo L, Bachmann G, McClish D, et al. Meta-analysis of estrogen therapy in the management of urogenital atrophy in postmenopausal women: second report of the Hormones and Urogenital Therapy Committee. Obstet Gynecol 1998;92(4 Pt 2):722-7
   PubMed Web of Science ®Google Scholar
• Suckling J, Lethaby A, Kennedy R. Local oestrogen for vaginal atrophy in postmenopausal women. Cochrane Database Syst Rev 2006;2006(4):CD001500
   Google Scholar
• Karp DR, Jean-Michel M, Johnston Y, et al. A randomized clinical trial of the impact of local estrogen on postoperative tissue quality after vaginal reconstructive surgery. Female Pelvic Med Reconstr Surg 2012;18(4):211-15
   PubMedGoogle Scholar
• Gupta P, Ozel B, Stanczyk FZ, et al. The effect of transdermal and vaginal estrogen therapy on markers of postmenopausal estrogen status. Menopause 2008;15(1):94-7
   PubMed Web of Science ®Google Scholar
• Bachmann G, Lobo RA, Gut R, et al. Efficacy of low-dose estradiol vaginal tablets in the treatment of atrophic vaginitis: a randomized controlled trial. Obstet Gynecol 2008;111(1):67-76
   PubMed Web of Science ®Google Scholar
• Akrivis C, Varras M, Thodos A, et al. Action of 25 microg 17beta-oestradiol vaginal tablets in the treatment of vaginal atrophy in Greek postmenopausal women; clinical study. Clin Exp Obstet Gynecol 2003;30(4):229-34
   PubMedGoogle Scholar
• Mainini G, Scaffa C, Rotondi M, et al. Local estrogen replacement therapy in postmenopausal atrophic vaginitis: efficacy and safety of low dose 17beta-estradiol vaginal tablets. Clin Exp Obstet Gynecol 2005;32(2):111-13
   PubMedGoogle Scholar
• Handa VL, Bachus KE, Johnston WW, et al. Vaginal administration of low-dose conjugated estrogens: systemic absorption and effects on the endometrium. Obstet Gynecol 1994;84(2):215-18
   PubMed Web of Science ®Google Scholar
• Raymundo N, Yu-cheng B, Zi-yan H, et al. Treatment of atrophic vaginitis with topical conjugated equine estrogens in postmenopausal Asian women. Climacteric 2004;7(3):312-18
   PubMed Web of Science ®Google Scholar
• Bachmann G, Bouchard C, Hoppe D, et al. Efficacy and safety of low-dose regimens of conjugated estrogens cream administered vaginally. Menopause 2009;16(4):719-27
   PubMed Web of Science ®Google Scholar
• Bachmann GA, Komi JO. Ospemifene effectively treats vulvovaginal atrophy in postmenopausal women: results from a pivotal phase 3 study. Menopause 2010;17(3):480-6
   PubMed Web of Science ®Google Scholar
• Pickar JH. Emerging therapies for postmenopausal vaginal atrophy. Maturitas 2013;75(1):3-6
   PubMed Web of Science ®Google Scholar
• Management of symptomatic vulvovaginal atrophy: 2013 position statement of The North American Menopause Society. Menopause 2013:20(9):888-902
   Google Scholar
• Stovall DW, Utian WH, Gass ML, et al. The effects of combined raloxifene and oral estrogen on vasomotor symptoms and endometrial safety. Menopause 2007;14(3):510-17
   PubMed Web of Science ®Google Scholar
• Kagan R, Williams RS, Pan K, et al. A randomized, placebo- and active-controlled trial of bazedoxifene/conjugated estrogens for treatment of moderate to severe vulvar/vaginal atrophy in postmenopausal women. Menopause 2010;17(2):281-9
   PubMed Web of Science ®Google Scholar
• Moraes AB, Haidar MA, Soares Junior JM, et al. The effects of topical isoflavones on postmenopausal skin: double-blind and randomized clinical trial of efficacy. Eur J Obstet Gynecol Reprod Biol 2009;146(2):188-92
   PubMed Web of Science ®Google Scholar