Human uterine vascular structures in normal and diseased states

Microscopy Research and Technique

Volumn 60, Issue 4, 2003, Pages 377-389

  Hickey, Martha ^a   Fraser, Ian ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Breakthrough bleeding; Menstruation; Progestogen; Uterus; Vascular

Indexed keywords

BLEEDING DISORDER; BLEEDINGS; BREAKTHROUGH BLEEDING; MENSTRUATION; PROGESTOGEN; SEX STEROIDS; UTERUS; VASCULAR; VASCULAR GROWTHS; VASCULAR STRUCTURES;

ESTROGEN; ESTROGEN RECEPTOR; ETONOGESTREL; GESTAGEN; LEVONORGESTREL; MEDROXYPROGESTERONE ACETATE; ORAL CONTRACEPTIVE AGENT; PROGESTERONE; PROGESTERONE RECEPTOR; SEX HORMONE;

ADENOMYOSIS; ANGIOGENESIS; ARTERIOVENOUS MALFORMATION; ARTICLE; BREAKTHROUGH BLEEDING; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MENSTRUAL CYCLE; MENSTRUATION DISORDER; METRORRHAGIA; NIDATION; PRIORITY JOURNAL; UTERINE BLOOD VESSEL; VASCULAR FRAGILITY;

EID: 0037363391     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jemt.10276     Document Type: Article

References (111)

1. Abulafia O, Sherer DM. 1999. Angiogenesis of the endometrium. Obstet Gynecol 94:148-153.
2. Adelentado JM, Rees MCP, Lopez Bernal A, et al. 1988. Increased uterine prostaglandin E receptors in menorrhagic women. Br J Obstet Gynaecol 95:162-165.
3. Au CL, Rogers PAW. 1993. Immunohistochemical staining of von Willebrand factor in human endometrium during the normal menstrual cycle. Hum Reprod 8:17-23.
4. Bartelmez GW. 1957. The form and the functions of the uterine blood vessels in the rhesus monkey. Contrib Embryol Carnegie Inst 249:155-208.
5. Blackwell PM, Fraser IS. 1981. Superficial lymphatics in the functional zone of normal human endometrium. Microvasc Res 21:142-152.
6. Blackwell PM, Fraser IS (1988). A morphometric and ultrastructural study of microvessels of the functional zone of normal human endometrium with some notions on possible secretory functions of the endothelial cells. Asia-Oceania J Obstet Gynaecol 14:233-50.
7. Brewer JI. 1938. Rhythmic changes in skin capillaries and their relation to menstruation. Am J Obstet Gynecol 36:597-612.
8. Brosens JJ, Brosens IA. 1998. Adenomyosis uteri. In: Cameron IT, Fraser IS, Smith SK, editors. Clinical disorders of the endometrium and menstrual cycle. Oxford: Oxford University Press. p 297-312.
9. Bulmer JN, Jones RK, Searle RF. 1998. Intraepithelial leukocytes in endometriosis and adenomyosis: comparison of eutopic and ectopic endometrium with normal endometrium. Hum Reprod 13:2910-2915.
10. Burri PH, Tarek MR. 1990. A novel mechanism of capillary growth in the rat pulmonary circulation. Anat Rec 228:35-45.
11. Cameron IT, Plumpton C, Champeney R, van Papendorp C, Ashby MJ, Davenport AP 1993. Identification of endothelin-1, endothelin-2 and endothelin-3 in human endometrium. J Reprod Fertil 97:251-255.
12. Carduff JH, Fischer LC, Burri PH. 1986. Scanning electron microscope study of the developing microvasculature in the postnatal rat lung. Anat Rec 216:154-164.
13. Casey ML, MacDonald PC. 1996. The endothelin-parathyroid hormone-related protein vasoactive peptide system in human endometrium: modulation by transforming growth factor-beta. In: Findlay J, Affandi B, editors. Menstrual disorders and progestin contraception. Hum Reprod 11(Suppl 2):62-82.
14. Casper RF. 1996. Regulation of estrogen/progestogen receptors in the endometrium. Int J Fertil Menopausal Stud 41:16-21.
15. Casslen B, Astedt B. 1983. Reduced plasminogen activator content of endometrium in oral contraceptive users. Contraception 28:181-188.
16. Chiang CH, Chang MY, Hsu JJ, et al. 1999. Tumor vascular pattern and blood flow impedance in the differential diagnosis of leiomyoma and adenomyosis by color Doppler sonography. J Assist Reprod Genet 16:268-275.
17. Clark DA, Wang S, Rogers PAW, et al. 1996. Endometrial lymphomyeloid cells in abnormal uterine bleeding due to levonorgestrel (Norplant). Hum Reprod 11:1438-1444.
18. Clemetson CA, Blair L, Brown AB. 1962. Capillary strength and the menstrual cycle. Ann NY Acad Sci 93:279-299.
19. Critchley HOD, Abberton KM, Taylor NH, et al. 1994. Endometrial sex steroid receptor expression in women with menorrhagia. Br J Obstet Gynaecol 101:428-434.
20. Dallenbach-Hellweg G. 1988. The endometrium in natural and artificial luteal phases. Hum Reprod 3:165-168.
21. Das SK, Chakraborty I, Wang J, et al. 1997. Expression of vascular endothelial growth factor (VEGF) and VEGF-receptor messenger ribonucleic acids in the peri-implantation rabbit uterus. Biol Reprod 56:1390-1399.
22. Enders AC, Blankenship TN. 1997. Modification of endometrial arteries during invasion by cytotrophoblast cells in the pregnant macaque. Acta Anat (Basel) 159:169-193.
23. Farrer-Brown G, Beilby JO, Tarbit MH. 1970. The blood supply of the uterus. 1. Arterial vasculature. J Obstet Gynaecol Br Commonw 77:673-681
24. Farrer-Brown G, Beilby JOW, Tarbit MH. 1971. Venous changes in the endometrium of myomatous uteri. Obstet Gynecol 38:743-751.
25. Ferenczy A. 1998. Pathophysiology of adenomyosis. Human Reprod Update 4:313-322.
26. Fleming H, Ostor AG, Pickel H, Fortune DW. 1989. Arteriovenous malformations of the uterus. Obstet Gynecol 73:209-213.
27. Foley ME, Griffin BD, Zugel M. 1978. Heparin-like activity in uterine fluid. Br Med J11:322-324.
28. Foley ME, Griffin BD, Zuzel M, Aparicio SR, Bradbury K, Bird CC, Clayton JK, Jenkins DM, Scott JS, Rajah SM, McNichol GP. 1978. Heparin-like activity in uterine fluid. Br Med J 2:322-324.
29. Fraser IS, Hickey M. 2000. Endometrial vascular changes and bleeding disturbances with long-acting progestins. Steroids 65:665-671.
30. Fraser IS, McCarron G, Markham R, Resta T. 1985. Blood and total fluid content of menstrual discharge. Obstet Gynecol 65:194-198.
31. Fraser IS, McCarron G, Markham R, et al. 1986. Objective measurement of menstrual blood loss in women with a complaint of menorrhagia associated with pelvic disease or a coagulation disorder. Obstet Gynecol 68:630-633.
32. Fraser IS, McCarron G, Hutton BF, Macey D. 1987. Endometrial blood flow measured by xenon-133 clearance in women with normal menstrual cycles and dysfunctional uterine bleeding. Am J Obstet Gynecol 156:158-166.
33. Fraser IS, Hickey M, Song JY. 1996. A comparison of mechanisms underlying disturbances of bleeding caused by spontaneous dysfunctional uterine bleeding or hormonal contraception. Hum Reprod 11(Suppl 2):165-178.
34. Gargett CE, Lederman FL, Lau TM, Taylor NH, Rogers PA. 1999. Lack of correlation between vascular endothelial growth factor production and endothelial cell proliferation in the human endometrium. Hum Reprod 14:2080-2088.
35. Gargett CE, Lederman F, Heryanto B, Gambino LS, Rogers PA. 2001. Focal vascular endothelial growth factor correlates with angiogenesis in human endometrium. Role of intravascular neutrophils. Hum Reprod 16:1065-1075.
36. Hampton AL, Salamonsen L. 1994. Expression of messenger ribonucleic acid encoding matrix metalloproteinases and their tissue inhibitors is related to menstrution. J Endocrin 141:R1-R3.
37. Hickey M, Fraser IS, Dwarte D, Graham S. 1996. Endometrial vasculature in Norplant users: preliminary results from a hysteroscopic study. Hum Reprod 11 Suppl2:35-44.
38. Hickey M, Simbar M, Markham R, et al. 1999a. Changes in endometrial vascular density in Norplant users. Contraception 59:123-129.
39. Hickey M, Simbar M, Markham R, et al. 1999b. Changes in vascular basement membrane in the endometrium of Norplant users. Hum Reprod 14:716-721.
40. Hickey M, Higham J, Sullivan M, Miles L, Fraser IS. 2001. Endometrial bleeding in HRT users: Preliminary findings regarding the role of MMP-9 and TIMP-1. Fertil Steril 75:288-296.
41. Hirschi KK, d'Amore PA. 1996. Pericytes in the microvasculature. Cardiovasc Res 32:687-698.
42. Hoffman MK, Meilstrup JW, Shackelford DP, Kaminski PF. 1997. Arteriovenous malformations of the uterus: an uncommon cause of vaginal bleeding. Obstet Gynecol Surv 52:736-740.
43. Hourihan HM, Sheppard BL, Bonnar J. 1986. A morphometric study of the effect of oral norethisterone or levonorgestrel on endometrial blood vessels. Contraception 38:603-612.
44. Hourihan HM, Sheppard BL, Bonnar J. 1989. The morphologic characteristics of menstrual haemostasis in patients with unexplained menorrhagia. Int J Gynecol Pathol 8:221-229.
45. Huang MW, Muradali D, Thurston WA, Burns PN, Wilson SR. 1998. Uterine arteriovenous malformations: gray-scale and Doppler US features with MR imaging correlation. Radiology 206:115-123.
46. Kasonde JM, Bonnar J. 1976. Plasminogen activators in the endometrium of women using intrauterine contraceptive devices. Br J Obstet Gynaecol 83:315-319.
47. Koga K, Osuga Y, Tsutsumi O, Yano T, Yoshino O, Takai Y, Matsumi H, Hiroi H, Kugu K, Momoeda M, Fujiwara T, Taketani Y. 2001. Demonstration of angiogenin in human endometrium and its enhanced expression in endometrial tissues in the secretory phase and the decidua. J Clin Endocrinol Metab 86:5609-5614.
48. Korkorine I, Marbaix E, Henriet P, Okada Y, Donnez J, Eeckhout Y, Courtoy PJ. 1996. Focal cellular origin and regulation of interstitial collagenase (matrix metalloproteinase-1) are related to menstrual breakdown in the human endometrium. J Cell Sci 109:2151-2160.
49. Lakhani KP, Marsh MS, Purcell W, Hardiman. 1998. Uterine artery blood flow parameters in women with dysfunctional uterine bleeding and uterine fibroids: the effects of tranexamic acid. Ultrasound Obstet Gynecol 11:283-285.
50. Landgren BM, Johannisson E, Masirono B, Diczfalusy E. 1982. Pharmacokinetic and pharmacodynamic investigations with vaginal devices releasing levonorgestrel at a constant, near zero order. Contraception 26:567-585.
51. Lessey BA, Arnold JT 1998. Paracrine signaling in the endometrium: integrins and the establishment of uterine receptivity. J Reprod Immunol:105-116
52. Li XF, Charnock-Jones DS, Zhang E, Hiby S, Malik S, Day K, Licence D, Bowen JM, Gardner L, King A, Loke YW, Smith SK. 2001. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J Clin Endocrinol Metab 86:1823-1834
53. Lockwood CJ, Krikun G, Hausknecht V, et al 1997. Decidual cell regulation of hemostasis during implantation and menstruation. Ann NY Acad Sci 828:188-193.
54. Lumsden MA. 1998. Clinical presentation of uterine fibroids. Bailliere's Clin Obstet Gynaecol 12:177-195.
55. Maas JW, Groothuis PG, Dunselman GA, de Goeij AF, Boudier HA, Evers JL. 2001. Endometrial angiogenesis throughout the human menstrual cycle. Hum Reprod 16:1557-1561.
56. Maqueo M. Vascular and perivascular changes in the endometrium of women using steroidal contraceptives. 1980. In: Diczfalusy E, Fraser IS, Webb FTG, editors. Endometrial bleeding and steroidal contraception. Bath: Pitman Press p138-152.
57. Marbaix E, Kokorine I, Henriet et al. 1995. The expression of interstitial colaginase in human endometrium is controlled by progesterone and by oestradiol and is related to menstruation. Biochem J 305:1027-1030.
58. Marbaix E, Vekemans M, Galant C, Rigot V, Lemoine P, Dubois D, Picquet C, Henriet P, Twagirayezu P, Sufi S, Eeckhout Y, Courtoy PJ. 2000. Circulating sex hormones and endometrial stromelysin-1 (matrix metalloproteinase-3) at the start of bleeding episodes in levonorgestrel-implant users. Hum Reprod 15(Suppl 3):120-134.
59. Markee JE. 1940. Menstruation in intraocular endometrial transplants in the rhesus monkey. Contrib Embryol Carnegie Inst Wash 177:220-306.
60. Marsh MM, Findlay JK, Salamonsen LA. 1996. Endothelin and menstruation. Hum Reprod 11(Suppl 2):83-89.
61. Matsuda M, Sasabe H, Adachi Y, Suzuki T, Mori T. 2001. Increased invasion activity of endometrial stromal cells and elevated expression of matrix metalloproteinase messenger RNA in the uterine tissues of mice with experimentally induced adenomyosis. Am J Obstet Gynecol 185:1374-1380.
62. Matsumo Y, Iwasaka T, Yamasaki F, et al. 1999. Apoptosis and Ki-67 expression in adenomyotic lesions and in the corresponding eutopic endometrium. Obstet Gynecol 94:71-77.
63. Odlind V, Fraser IS. 1990. Contraception and menstrual bleeding disturbances: a clinical overview. In: d'Arcangues C, Fraser IS, Newton JR, Odlind V, editors. Contraception and mechanisms of endometrial bleeding. Cambridge: Cambridge University Press. p 5-31.
64. Osteen KG, Keller NR, Feltus FA, Melner MH. 1999. Paracrine regulation of matrix metalloproteinase expression in the normal human endometrium. Gynecol Obstet Invest 48(Suppl 1):2-13
65. Ota H, Igarashi S, Tanaka T. 1998. Morphometric evaluation of stromal vascularization in the endometrium of adenomyosis. Hum Reprod 13:715-719.
66. Pepper MS, Vassalli JD, Orci L, Montesano R. 1993. Angiogenesis in vitro: cytokine interactions and balanced extracellular proteolysis. In: Maragouakis ME, Gullino PM, Lelkes PI, editors. Angiogenesis: molecular biology, clinical aspects. New York: Plenum Press p 149-171.
67. Perrot-Applanat M, Groyer-Pickard MT, Garcia E, Lorenzo F, Milgrom E. 1988. Immunocytochemical demonstration of estrogen and progesterone receptors in muscle cells of uterine arteries in rabbits and humans. Endocrinology 123:1511-1519.
68. Purcell TL, Given R, Chwalisz K, et al. 1999. Nitric oxide synthetase distribution during implantation in the mouse. Mol Hum Reprod 5:467-475.
69. Rai R, Regan L. 1998. Antiphospholipid syndrome and pregnancy loss. Hosp Med 59:637-639
70. Ramsey EM. 1982. Vascular anatomy. In: Wynn RM, editor. Biology of the uterus, 2nd ed. New York: Plenum Press. p 59-76.
71. Rand JH. 1998. Antiphospholipid antibody syndrome: new insights on thrombogenic mechanisms. Am J Med Sci 316:142-51.
72. Rand JH, Wu XX, Andree HA, et al. 1997. Pregnancy loss in the antiphospholipid-antibody syndrome: a possible thrombogenic mechanism. N Engl J Med 337:154-60.
73. Ravina JA, Herbreteau D, Ciraru-Vigneron et al. 1995. Arterial embolisation to treat uterine myomata. Lancet 346:671-672.
74. Rees MCP, Demers LM, Anderson ABM, et al. 1984a. A functional study of platelets in menstrual fluid. Br J Obstet Gynaecol 91:667-672.
75. Rees MCP, Dunhill MS, Anderson ABM, et al. 1984b. Quantitative uterine histology during the menstrual cycle related to measured blood loss. Br J Obstet Gynaecol 91:662-666.
76. Rees MCP, Cederholm-Williams SA, Turnbull AC. 1985. Coagulation factors and fibrinolytic proteins in menstrual fluid collected from normal and menorrhagic women. Br J Obstet Gynaecol 92:1164-1168.
77. Rees MCP, Canete-Soler R, Lopez-Bernal A, et al. 1988. Effect of fenamates on prostaglandin E receptor binding. Lancet ii:541-542.
78. Rein MS, Barbieri RL, Friedman AJ. 1995. Progesterone: a critical role in the pathogenesis of uterine myomas. Am J Obstet Gynecol 172:14-18.
79. Roberts DK, Parmley TH, Walker NJ, Horbelt DV. 1992. Ultrastructure of the microvasculature in the human endometrium throughout the normal menstrual cycle. Am J Obstet Gynecol 166:1393-406.
80. Rogers PAW. 1995. Current studies on human implantation. Reprod Fertil Devel 7:1395-1399.
81. Rogers PAW. 2000. Growth and regression of the endometrial vasculature. In: Rogers PAW, Smith SK, editors. Steroids and endometrial breakthrough bleeding. Hum Reprod Suppl (in press).
82. Rogers PAW, Au CL, Affandi B. 1993. Endometrial microvascular density during the normal menstrual cycle and following exposure to long-term levonorgestrel. Hum Reprod 8:1396-1404.
83. Rogers PA, Lederman F, Kooy J, Taylor NH, Healy DL. 1996. Endometrial vascular smooth muscle oestrogen and progesterone receptor distribution in women with and without menorrhagia. Hum Reprod 11:2003-2008.
84. Rogers PAW, Lederman F, Taylor N. 1998. Endometrial microvascular growth in normal and dysfunctional states. Hum Reprod Update 4:503-508.
85. Rogers PAW, Plunkett D, Affandi B. 2000. Perivascular smooth muscle -actin is reduced in the endometrium of women with progestin-only contraceptive breakthrough bleeding. Hum Reprod 15(Suppl 3):78-84.
86. Rybo G, Leman J, Tibblin E. 1985. Epidemiology of menstrual blood loss. In: Baird DT, Michie EA, editors. Mechanism of menstrual bleeding. New York: Raven Press. p181-194.
87. Salamonsen LA, Woolley DE. 1996. Matrix metalloproteinases in normal menstruation. Hum Reprod 11(Suppl 2):124-133.
88. Salamonsen LA, Marsh MM, Findlay JK. 1999. Endometrial endothelin: regulator of uterine bleeding and endometrial repair. Clin Exp Pharmacol Physiol 26:154-157.
89. Sapozhnikov AG. 1987. Structure of the blood microcirculatory bed in intramural uterine myomas. Vopr Onkol 33:43-48.
90. Searle RF, Jones RK, Bulmer JN. 1999. Phenotypic analysis and proliferative responses of human endometrial granulated lymphocytes during the menstrual cycle. Biol Reprod 60:871-878.
91. Sheppard BL. 1990. Coagulation and electron microscopy studies in menorrhagia. In: Shaw RW, editor. Advances in reproductive endocrinology, Vol. 2. Carnforth: Parthenon Press. p 25-42.
92. Simbar M, Manconi F, Markham R, Hickey M, Fraser IS. A three-dimensional study of endometrial microvessels in women using the subdermal levonorgestrel implant system, Norplant. In preparation.
93. Sixma J, Christiaens GCML, Haspels AA. 1980. The sequence of haemostatic events in the endometrium during normal menstruation. In: Diczfalusy E, Fraser IS, Webb FTG, editors. Endometrial bleeding and steroidal contraception. Bath: Pitman Press. p 86-96.
94. Skinner JL, Riley SC, Gebbie AE, Glasier AF, Critchley HO. 1999. Regulation of matrix metalloproteinase-9 in endometrium during the menstrual cycle and following administration of intrauterine levonorgestrel. Hum Reprod 14:793-799.
95. Skopichev VG, Savitskii GA. 1992. Changes in the human uterine vascular bed in myoma. Arkh Patol 54:27-30.
96. Smith SK. 1998. Angiogenesis, vascular endothelial growth factor and the endometrium. Hum Reprod Update 4:509-519.
97. 2) in excessive menstrual bleeding. Lancet I:522-524.
98. Smith SK, Abel MH, Kelly RW, et al. 1982. The synthesis of prostaglandins from persistent proliferative endometrium. J Clin Endocrinol Metab 55:284-289.
99. Song JY, Markham R, Russell P, Wong T, Young L, Fraser IS. 1995. The effect of high dose medium and long-term progestogen exposure on endometrial vessels. Hum Reprod 10:797-800
100. Song JY, Russell P, Markham R, et al. 1996. The effect of high-dose progestogens on white cells and necrosis in human endometrium. Hum Reprod 11:1713-1718.
101. Sosic A, Skuski DW, Streltzoff J, et al. 1996. Vascularity of uterine myomas: assessment by color and pulsed Doppler ultrasound. Int J Gynaecol Obstet 54:245-250.
102. Stewart CJ, Campbell-Brown M, Critchley HO, Farquharson MA. 1999. Endometrial apoptosis in patients with dysfunctional uterine bleeding. Histopathology 34:99-105
103. Stewart EA, Nowak, RA. 1996. Leiomyoma-related bleeding: a classic hypothesis updated for the molecular era. Hum Reprod Update 2:295-306.
104. Taylor RN, Lebovic DI, Hornung D, Mueller MD. 2001. Endocrine and paracrine regulation of endometrial angiogenesis. Ann NY Acad Sci 943:109-121
105. Uduwela AS, Perera MAK, Li A, Fraser IS. 2000. The endometrialmyometrial interface: relationship to adenomyosis and changes in pregnancy. Obstet Gynecol Surv Rev 55:390-400.
106. Van Herendael BJ, Stevens MJ, Flakiewicz-Kula A, et al 1987. Dating of the endometrium by microhysteroscopy. Gynecol Obstet Invest 24:114-118.
107. Vincent AJ, Malakooti N, Zhang J, et al. 1999. Endometrial breakdown in women using Norplant is associated with migratory cells expressing matrix-metalloproteinase-9 (gelatinase B). Hum Reprod 14:807-814.
108. Vincent AJ, Zhang J, Ostor A, Rogers PA, Affandi B, Kovacs G, Salamonsen LA. 2000. Matrix metalloproteinase-1 and -3 and mast cells are present in the endometrium of women using progestin-only contraceptives. Hum Reprod 15:123-30.
109. Wang IYS, Barsamian S, Cornellie FJ, et al. 2000. Endometrial lysosomal enzyme activity in ovulatory dysfunctional bleeding, IUCD users and in postpartum women. Mol Hum Reprod 6:101-106.
110. Warner P, Critchley HO, Lumsden MA, Campbell-Brown M, Douglas A, Murray G. 2001. Referral for menstrual problems: cross sectional survey of symptoms, reasons for referral, and management. BMJ 323:24-28.
111. Yang JH, Wu MY, Chen CD, et al. 1999. Association of endometrial blood flow as determined by a modified colour Doppler technique with subsequent outcome of in-vitro fertilisation. Hum Reprod 14:1606-1610.