Postmenopausal hormone therapy increases retinal blood flow and protects the retinal nerve fiber layer

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 5, 2010, Pages 2587-2600

  Deschênes, Micheline C ^a,b   Descovich, Denise ^b   Moreau, Michèle ^a   Granger, Louis ^a   Kuchel, George A ^c   Mikkola, Tomi S ^d   Fick, Gordon H ^e   Chemtob, Sylvain ^f   Vaucher, Elvire ^a   Lesk, Mark R ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e UNIVERSITY OF CALGARY   (Canada)

^f UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CONJUGATED ESTROGEN; CONJUGATED ESTROGEN PLUS MEDROXYPROGESTERONE; CONJUGATED ESTROGEN PLUS PROGESTERONE; ESTRADIOL; ESTRADIOL PLUS LEVONORGESTREL; ESTRADIOL PLUS MEDROXYPROGESTERONE; ESTRADIOL PLUS NORETHISTERONE ACETATE; ESTROGEN; ETHINYLESTRADIOL PLUS NORETHISTERONE ACETATE; GESTAGEN; KLIMAVAG; PIPERAZINE ESTRONE SULFATE PLUS PROGESTERONE; PLACEBO; UNCLASSIFIED DRUG;

ADULT; AGE; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; FEMALE; HORMONAL THERAPY; HUMAN; MAJOR CLINICAL STUDY; MENARCHE; MENOPAUSAL SYNDROME; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA ARTERY; RETINA BLOOD FLOW; RETINA CELL; RETINA GANGLION CELL; RETINA NERVE FIBER LAYER; TISSUE PERFUSION; VISUAL NERVOUS SYSTEM; ANIMAL; AUTORADIOGRAPHY; BLOOD FLOW; BLOOD FLOW VELOCITY; BROWN NORWAY RAT; ELECTRORETINOGRAPHY; ESTROGEN THERAPY; LASER DOPPLER FLOWMETRY; MIDDLE AGED; NERVE FIBER; OPTIC DISK; OVARIECTOMY; PHYSIOLOGY; POSTMENOPAUSE; VASCULARIZATION;

AGED; ANIMALS; AUTORADIOGRAPHY; BLOOD FLOW VELOCITY; ELECTRORETINOGRAPHY; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; FEMALE; HUMANS; LASER-DOPPLER FLOWMETRY; MIDDLE AGED; NERVE FIBERS; OPTIC DISK; OVARIECTOMY; POSTMENOPAUSE; PROGESTINS; RATS; RATS, INBRED BN; REGIONAL BLOOD FLOW; RETINAL ARTERY; RETINAL GANGLION CELLS;

EID: 77952529477     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-3710     Document Type: Article

References (90)

1. Samsioe G, Dören M, Lobo RA. Menopause. London: Elsevier; 203:9.
2. Tostes RC, Nigro D, Fortes ZB, Carvalho MHC. Effects of estrogen on the vascular system. Braz J Med Biol Res. 2003;36:1143-1158.
3. Green PS, Simpkins JW. Neuroprotective effects of estrogens: potential mechanisms of action. Int J Dev Neurosci. 2000;18:347-358.
4. Riedel M, Oeltermann A, Mügge A, et al. Vascular responses to 17β-oestradiol in postmenopausal women. Eur J Clin Invest. 1995; 25:44-47.
5. Ohkura T, Teshima Y, Isse K, et al. Estrogen increases cerebral and cerebellar blood flows in postmenopausal women. Menopause. 1995;2:13-18.
6. Maki PM, Resnick SM. Longitudinal effects of estrogen replacement therapy on PET cerebral blood flow and cognition. Neurobiol Aging. 2000;21:373-383.
7. De Leo V, la Marca A, Orlandi R, et al. Effects of estradiol alone or in combination with cyproterone acetate on carotid artery pulsatility index in postmenopausal women. Maturitas. 2003;46:219-224.
8. Gangar KF, Vyas S, Whitehead M, et al. Pulsatility index in internal carotid artery in relation to transdermal oestradiol and time since menopause. Lancet. 1991;338:839-842.
9. Penotti M, Farina M, Castiglioni E, et al. Alteration in the pulsatility index values of the internal carotid and middle cerebral arteries after suspension of postmenopausal hormone replacement therapy: a randomized crossover study. Am J Obstet Gynecol. 1996;175:606-611.
10. Battaglia C, Mancini F, Regnani G, et al. Hormone therapy and ophthalmic artery blood flow changes in women with primary open-angle glaucoma. Menopause. 2004;11:69-77.
11. Eberling JL, Wu C, Haan MN, et al. Preliminary evidence that estrogen protects against age-related hippocampal atrophy. Neurobiol Aging. 2003;24:725-732.
12. Raz N, Rodrigue KM, Kennedy KM, Acker JD. Hormone replacement therapy and age-related brain shrinkage: regional effects. Neuroreport. 2004;15:2531-2534.
13. Flammer J, Orgül S, Costa VP, et al. The impact of ocular blood flow in glaucoma. Prog Retin Eye Res. 2002;21:359-393.
14. Harris A, Chung HS, Ciulla TA, Kagemann L. Progress in measurement of ocular blood flow and relevance to our understanding of glaucoma and age-related macular degeneration. Prog Retin Eye Res. 1999;18:669-687.
15. Hulsman CAA, Westendorp ICD, Ramrattan RS, et al. Is open-angle glaucoma associated with early menopause? The Rotterdam Study. Am J Epidemiol. 2001;154:138-144.
16. Lee AJ, Mitchell P, Rochtchina E, Healey PR. Female reproductive factors and open angle glaucoma: the Blue Mountains Eye Study. Br J Ophthalmol. 2003;87:1324-1328.
17. Smith W, Mitchell P, Wang JJ. Gender, oestrogen, hormone replacement and age-related macular degeneration: Results from the Blue Mountains Eye Study. Aust N Z J Ophthalmol. 1997;25(suppl 1):S13-S15.
18. Abramov Y, Borik S, Yahalom C, et al. Does postmenopausal hormone replacement therapy affect intraocular pressure. J Glaucoma. 2005;14:271-275.
19. Snow KK, Cote J, Yang W, Davis NJ, Seddon JM. Association between reproductive and hormonal factors and age-related maculopathy in postmenopausal women. Am J Ophthalmol. 2002;134:842-848.
20. Haan MN, Klein R, Klein BE, et al. Hormone therapy and agerelated macular degeneration. Arch Ophthalmol. 2006;124:988-992.
21. Seitzman RL, Mangione C, Ensrund KE, et al. Postmenopausal hormone therapy and age-related maculopathy in older women. Ophthalmic Epidemiol. 2008;15:308-316.
22. Cheifitz RL. Cardiovascular disease: hormone replacement therapy and the window of opportunity. Cardiovasc J S Afr. 2005;16:229-230.
23. Hodis HN, Mack WJ. Postmenopausal hormone therapy and cardiovascular disease in perspective. Clin Obstet Gynecol. 2008;51.
24. Ogueta SB, Schwartz SD, Yamashita CK, Farber DB. Estrogen receptor in the human eye: Influence of gender and age on gene expression. Invest Ophthalmol Vis Sci. 1999;40:1906-2011.
25. Wickham LA, Gao J, Toda I, et al. Identification of androgen, estrogen and P receptor mRNAs in the eye. Acta Ophthalmol Scand. 2000;78:146-153.
26. Munaut C, Lambert V, Noël A, et al. Presence of oestrogen receptor type β in human retina. Br J Ophthalmol. 2001;85:877-882.
27. Belfort MA, Saade GR, Snabes M, et al. Hormonal status affects the reactivity of the cerebral vasculature. Am J Obstet Gynecol. 1995; 172:1273-1278.
28. Hata K, Hata T. Effects of oophorectomy and hormone replacement therapy on ophthalmic artery blood flow velocity waveforms. J Ultrasound Med. 1997;16:737-741.
29. Harris-Yitzhak M, Harris A, Ben-Refael Z, et al. Estrogen-replacement therapy: effects on retrobulbar hemodynamics. Am J Ophthalmol. 2000;129:623-628.
30. van Baal WM, Kenemans P, Stehouwer CDA, et al. Sequentially combined hormone replacement therapy reduces impedance to flow within the uterine and central retinal arteries in healthy postmenopausal women. Am J Obstet Gynecol. 1999;181:1365-1373.
31. Rossouw JE, Anderson GL, Prentice RL, 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. 2002;288:321-333.
32. 125I]iodoamphetamine (IMP) as a practical cerebral blood flow (CBF) indicator in rats. Nucl Med Biol. 2004;31:811-814.
33. 14C]-IMP). Exp Eye Res. 2009;89(6):960-966.
34. Kobayashi K, Kobayashi H, Ueda M, Honda Y. Estrogen receptor expression in bovine and rat retinas. Invest Ophthalmol Vis Sci. 1998;39:2105-2110.
35. Alm, A. Ocular circulation. Hart WM. Adler's Physiology of the Eye. 9th ed. St-Louis: Mosby-Year Book; 1992:198-227.
36. Garcia JPS, Garcia PT, Rosen RB. Retinal blood flow in the normal human eye using the canon laser blood flowmeter. Ophthalmic Res. 2002;34:295-299.
37. Yoshida A, Feke GT, Mori F, et al. Reproducibility and clinical application of a newly developed stabilized retinal laser Doppler instrument. Am J Ophthalmol. 2003;135:356-361.
38. Riva CE, Feke GT, Eberli B, Benary V. Bidirectional LDV system for absolute measurement of blood speed in retinal vessels. Appl Opt. 1979;18:2301-2306.
39. Feke GT, Goger DG, Tagawa H, Delori FC. Laser Doppler technique for absolute measurement of blood speed in retinal vessels. IEEE Trans Biomed Eng. 1987;34:673-680.
40. Delori FC, Fitch KA, Feke GT, Deupree DM, Weiter JJ. Evaluation of micrometric and microdensitometric methods for measuring the width of retinal vessel images on fundus photographs. Graefes Arch Clin Exp Ophthalmol. 1988;226:393-399.
41. Allingham RR, Damji KF, Freedman S, Moroi SE, Shafranov G, Shields MB. Sheilds' Textbook of Glaucoma. Philadelphia: Lippincott Williams & Wilkins; 2004:88.
42. Michelson G, Schmauss B. Two dimensional mapping of the perfusion of the retina and optic nerve head. Br J Ophthalmol. 1995;79:1126-1132.
43. Michelson G, Welzenbach J, Pal I, Harazny J. Automatic full field analysis of perfusion images gained by scanning laser Doppler flowmetry. Br J Ophthalmol. 1998;82:1294-1300.
44. Hafez AS, Bizzarro RLG, Rivard M, et al. Reproducibility of retinal and optic nerve head perfusion measurements using scanning laser Doppler flowmetry. Ophthalmic Surg Lasers and Imaging. 2003; 34:422-432.
45. Lesk MR, Hafez AS, Descovich D. Relationship between central corneal thickness and changes of optic nerve head topography and blood flow after intraocular pressure reduction in open-angle glaucoma and ocular hypertension. Arch Ophthalmol. 2006;124:1568-1572.
46. Holder GE, Brigell MG, Hawlina M, et al. ISCEV standard for clinical pattern electroretinography:2007 update. Doc Ophthalmol. 2007; 114:111-116.
47. Mannino CA, South SM, Inturrisi CE, Quinones-Jenab V. Pharmacokinetics and effects of 17β-estradiol and P implants in ovariectomized rats. J Pain. 2005;6:809-816.
48. Winchell HS, Baldwin RM, Lin TH. Development of I-123-labeled amines for brain studies: localization of I-123 iodophenylalkyl amines in rat brain. J Nucl Med. 1980;21:940-946.
49. 123I]isopropyliodoamphetamine as a tracer for local cerebral blood flow using direct autoradiographic comparison. J Cereb Blood Flow Metab. 1982;2:179-185.
50. Eskin, B. The Menopause: Endocrinology Basis and Management Options. 5th ed. Oxon, UK: Informa UK Ltd; 2007:253-8.
51. Micevych P, Sinchak K. Estradiol regulation of P synthesis in the brain. Mol Cell Endocrinol. 2008;290:44-50.
52. Musatov S, Chen W, Pfaff DW, et al. Silencing of estrogen receptor α in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci USA. 2007;104:2501-2506.
53. Leung H, Wang JJ, Rochtchina E, et al. Does hormone replacement therapy influence retinal microvascular caliber? Microvasc Res. 2004;67:48-54.
54. Wong TY, Knudtson MD, Klein BEK, Klein R, Hubbard LD. Estrogen replacement therapy and retinal vascular caliber. Ophthalmology. 2005;112:553-558.
55. Wong TY. Retinal vessel diameter. Ophthalmology. 2006;113:887.
56. Scuteri A, Bos AJ, Brant LJ, et al. Hormone replacement therapy and longitudinal changes in blood pressure in postmenopausal women. Ann Intern Med. 2001;135:229-238.
57. Alm A, Bill A. Ocular and optic nerve blood flow at normal and increased intraocular pressures in monkeys (Macaca irus): a study with radioactively labelled microspheres including flow determinations in brain and some other tissues. Exp Eye Res. 1973;15:15-29.
58. Bhutto IA, Amemiya T. Corrosion cast demonstration of retinal vasculature of normal Wistar-Kyoto Rats. Acta Anat. 1995;153:290-300.
59. Chakravarthy U, Stitt AW, McNally J, et al. Nitric oxide synthase activity and expression in retinal capillary endothelial cells and pericytes. Curr Eye Res. 1995;14:285-294.
60. Meyer P, Champion C, Schlötzer-Schrehardt U, Flammer J, Haefliger IO. Localization of nitric oxide synthase isoforms in porcine ocular tissues. Curr Eye Res. 1999;18:375-380.
61. Hata Y, Clermont A, Yamauchi T, et al. Retinal expression, regulation, and functional bioactivity of prostacyclin-stimulating factor. J Clin Invest. 2000;106:541-550.
62. Ju WK, Neufeld AH. Cellular localization of cyclooxygenase-1 and cyclooxygenase-2 in the normal mouse, rat, and human retina. J Comp Neurol. 2002;452:392-9.
63. Christian RC, Liu PY, Harrington S, et al. Intimal estrogen receptor (ER)β, but not ERα expression, is correlated with coronary calcification ad atherosclerosis in pre-and post-menopausal women. J Clin Endocrinol Metab. 2006;91:2713-2720.
64. Kauser K, Rubanyi GM. Potential cellular signaling mechanisms mediating upregulation of endothelial nitric oxide production by estrogen. J Vasc Res. 1997;34:229-236.
65. Mikkola T, Turunen P, Avela K, et al. 17β-estradiol stimulates prostacyclin, but not endothelin-1, production in human vascular endothelial cells. J Clin Endocrinol Metab. 1995;80:1832-1836.
66. Hermenegildo C, Oviedo PJ, Cano A. Cyclooxygenases regulation by estradiol on endothelium. Curr Pharm Des. 2006;12:205-215.
67. Haefliger IO, Flammer J, Bény JL, Lüscher TF. Endothelium-dependent vasoactive modulation in the ophthalmic circulation. Prog Retin Eye Res. 2001;20:209-225.
68. Resnik R, Brink GW, Plumer MH. The effect of P on estrogeninduced uterine blood flow. Am J Obstet Gynecol. 1977;128:251-254.
69. Caton D, Abrams RM, Clapp JF, Barron DH. The effect of exogenous P on the rate of blood flow of the uterus of ovariectomized sheep. Q J Exp Physiol. 1974;59:225-231.
70. Batra S, Bjellin L, Iosif S, Mårtensson L, Sjögren C. Effect of oestrogen and P on the blood flow in the lower urinary tract of the rabbit. Acta Physiol Scand. 1985;123:191-194.
71. Miyagawa K, Rösch J, Stanczyk F, Hermsmeyer K. MedroxyP interferes with ovarian steroid protection against coronary vasospasm. Nat Med. 1997;3:324-327.
72. Williams JK, Hall J, Anthony MS, et al. A comparison of tibolone and hormone replacement therapy on coronary artery and myocardial function in ovariectomized atherosclerotic monkeys. Menopause. 2002;9:41-51.
73. Dinh H, Nathan L. MedroxyP acetate does not antagonize estrogeninduced increases in endothelium-dependent vasodilation: potential clinical implications. Fertil Steril. 2002;78:122-127.
74. Faludi AA, Aldrighi JM, Bertolami MC, et al. P abolishes estrogen and/or atorvastatin endothelium dependent vasodilatory effects. Atherosclerosis. 2004;177:89-96.
75. Gerhard M, Walsh BW, Tawakol A, et al. Estradiol therapy combined with P and endothelium-dependent vasodilation in postmenopausal women. Circulation. 1998;98:1158-1163.
76. Mather KJ, Norman EG, Prior JC, Elliott TG. Preserved forearm endothelial responses with acute exposure to P: a randomized cross-over trial of 17-β estradiol, P, and 17-β estradiol with P in healthy menopausal women. J Clin Endocrinol Metab. 2000;85:4644-4649.
77. Wakatsuki A, Okatani Y, Ikenoue N, Fukawa T. Effect of medroxyP acetate on endothelium-dependent vasodilation in postmenopausal women receiving estrogen. Circulation. 2001;104:1773-1778.
78. Selles J, Polini N, Alvarez C, Massheimer V. P and 17 β-estradiol acutely stimulate nitric oxide synthase activity in rat aorta and inhibit platelet aggregation. Life Sci. 2001;69:815-827.
79. Selles J, Polini N, Alvarez C, Massheimer V. Nongenomic action of P in rat aorta: role of nitric oxide and prostaglandins. Cell Signal. 2002;14:431-436.
80. Simoncini T, Mannella P, Fornari L, et al. Differential signal transduction of P and medroxyP acetate in human endothelial cells. Endocrinology. 2004;145:5745-5756.
81. 2, COX-1, and PGIS protein expression. Biol Reprod. 2002;66:468-474.
82. Townsend R, Cringle SJ, Morgan WH, Chauhan BC, Yu D-Y. Confocal laser Doppler flowmeter measurements in a controlled flow environment in a isolated eye. Exp Eye Res. 2006;82:65-73.
83. Wang L, Cull G, Cioffi GA. Depth of penetration of scanning laser Doppler flowmetry in the primate optic nerve. Arch Ophthalmol. 2001;119:1810-1814.
84. Tamaki Y, Araie M, Fukaya Y, Ishi K. Validation of scanning laser Doppler flowmetry for retinal blood flow measurements in animal models. Curr Eye Res. 2002;24:332-340.
85. Kumar DM, Perez E, Cai ZY, et al. Role of nonfeminizing estrogen analogues in neuroprotection of rat retinal ganglion cells against glutamate-induced cytotoxicity. Free Radic Biol Med. 2005;38:1152-1163.
86. Nakazawa T, Takahashi H, Shimura M. Estrogen has a neuroprotective effect on axotomized RGCs through ERK signal transduction pathway. Brain Res. 2006;1093:141-149.
87. Nilsen J, Brinton RD. Impact of progestins on estrogen-induced neuroprotection: synergy by P and 19-norP and antagonism by medroxyP acetate. Endocrinology. 2002;143:205-212.
88. Quigley HA, Addicks EM. Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage. Arch Ophthalmol. 1981;99:137-143.
89. Javitt JC, Spaeth GL, Katz LJ, Poryzees E, Addiego R. Acquired pits of the optic nerve: increased prevalence in patients with lowtension glaucoma. Ophthalmology. 1990;97:1038-1043.
90. Parr JC, Spears GFS. General caliber of the retinal arteries expressed as the equivalent width of the central retinal artery. Am J Ophthalmol. 1974;77:472-477.