Journal of Reproduction & Infertility

Journal of Reproduction & Infertility

Uterine Artery Interruption: Evidence for Follicular Growth and Histochemical and Biochemical Changes

Authors
Kaveh Akhtari 1
Mazdak Razi 2
Hassan Malekinejad 3
1 Department of Clinical Science, Faculty of Veterinary Medicine, Islamic Azad University, Urmia Branch, Urmia, Iran
2 Department of Comparative Histology and Embryology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
3 Department of Pharmacology and Toxicology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
Abstract
Background: The present study was conducted in order to evaluate the effects of bilateral uterine artery ligation (BUAL) on the ovarian follicular fate, and alterations in carbohydrate, lipid, lipase and serum levels of F9SH, LH, prolactin, estrogen and progesterone. Methods: Twenty-four mature female rabbits divided into two test and control-sham groups. The animals underwent ovariohystrectomy on days 23, 43 and 63 after BUAL. Later serum and tissue samples were processed for histological and biochemical analyses. Two-way ANOVA test was used for statistical analyses and p < 0.05 was considered as significant. Results: The ovaries from the case groups exhibited markedly increased atretic follicles, which were characterized by early antrum formation, ooplasmic vacoulation, granulosa cells dissociation and oocyte deformation. Lipid foci were remarkably present in the cytoplasm of oocytes, granulosa and theca cells in BUAL rabbits. Smaller sized atretic follicles showed higher lipid reactions than large ones. The PAS reaction was highly positive in zona pellucida (ZP), basement membrane, granulosa cells and follicular fluid of atretic follicles. Early atresiated follicles showed remarkable reaction sites for lipase. Significant (p < 0.05) increase in serum levels of FSH, LH, progesterone, and prolactin was revealed in BUAL rabbits compared to the control group while serum levels of estrogen decreased time-dependently in the test groups. Conclusion: The current study suggests the critical role of the uterine artery in controlling ovulation and follicular growth. Moreover atresia processes might relate to lipid accumulation in the cells along with attenuation of lipase activity.
Keywords
Atresia
follicle
Gonadal hormones
Ligation
Uterine Artery
  1. Kuscu E, Duran HE, Zeyneloglu HB, Demirhan B, Bagis T, Saygili E. The effect of surgical sterilization on ovarian function: a rat model. Eur J Obstet Gynecol Reprod Biol. 2002;100(2):204-7.
  2. Kelekci S, Yorgancioglu Z, Yilmaz B, Yasar L, Savan K, Sonmez S, et al. Effect of tubal ligation on ovarian reserve and the ovarian stromal blood supply. Aust N Z J Obstet Gynaecol. 2004;44(5):449-51.
  3. Bulent Tiras M, Noyan V, Ozdemir H, Guner H, Yi-ldiz A, Yildirim M. The changes in ovarian hormone levels and ovarian artery blood flow rate after laparoscopic tubal sterilization. Eur J Obstet Gynecol Reprod Biol. 2001;99(2):219-21.
  4. Ozdamar S, Ulger H, Sorkun HC, Müderris I. Effects of hysterectomy on ovarian morphology and serum FSH level in rats. Maturitas. 2005;52(1):60-4.
  5. Kim HS, Thonse VR, Judson K, Vang R. Utero-ovarian anastomosis: histopathologic correlation after uterine artery embolization with or without ovarian artery embolization. J Vasc Interv Radiol. 2007; 18(1 Pt 1):31-9.
  6. Petri Nahás EA, Pontes A, Nahas-Neto J, Borges VT, Dias R, Traiman P. Effect of total abdominal hysterectomy on ovarian blood supply in women of reproductive age. J Ultrasound Med. 2005;24(2): 169-74.
  7. Ahn EH, Bai SW, Song CH, Kim JY, Jeong KA, Kim SK, et al. Effect of hysterectomy on conserved ovarian function. Yonsei Med J. 2002;43(1):53-8.
  8. Kelekci S, Yorgancioglu Z, Yilmaz B, Yasar L, Sa-van K, Sonmez S, et al. Effect of tubal ligation on ovarian reserve and the ovarian stromal blood supply. Aust N Z J Obstet Gynaecol. 2004;44(5):449-51.
  9. Camprubí M, Ortega A, Balaguer A, Iglesias I, Girabent M, Callejo J, et al. Cauterization of meso-ovarian vessels, a new model of intrauterine growth restriction in rats. Placenta. 2009;30(9):761-6.
  10. Zackrisson U, Mikuni M, Peterson MC, Nilsson B, Janson PO, Brännström M. Evidence for the involvement of blood flow-related mechanisms in the ovulatory process of the rat. Hum Reprod. 2000;15 (2):264-72.
  11. Wehrenberg WB, Dierschke DJ, Wolf RC, Meyer RK. The effect of ligating the ovarian and uterine arteries on ovarian function in cyclic rhesus monkeys. Biol Reprod. 1979;20(3):596-600.
  12. Luukkainen T. Contraception after thirty-five. Acta Obstet Gynecol Scand. 1992;71(3):169-74.
  13. Hulka JF, Phillips JM, Peterson HB, Surrey MW. American association of gynecologic laparoscopic 1993 membership survey. J Reprod Med. 1990;35: 5846.
  14. Battaglia C, Pasini A, Mancini F, Persico N, Burnelli R, Cicognani A, et al. Utero-ovarian ultra-sonographic and Doppler flow analyses in female childhood cancer survivors with regular menstruation and normal circulating follicle-stimulating hormone levels. Fertil Steril. 2006;85(2):455-61.
  15. Sumiala S, Pirhonen J, Tuominen J, Mäenpää J. Increased uterine and ovarian vascular resistance following Filshie clip sterilization: preliminary findings obtained with color Doppler ultrasonography. J Clin Ultrasound. 1995;23(9):511-6.
  16. Campbell S, Bourne TH, Waterstone J, Reynolds KM, Crayford TJ, Jurkovic D, et al. Transvaginal color blood flow imaging of the periovulatory follicle. Fertil Steril. 1993;60(3):433-8.
  17. Robker RL, Russell DL, Espey LL, Lydon JP, O' Malley BW, Richards JS. Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L prote-ases. Proc Natl Acad Sci U S A. 2000;97(9):4689-94.
  18. Dahm-Kähler P, Löfman C, Fujii R, Axelsson M, Janson PO, Brännström M. An intravital microscopy method permitting continuous long-term observations of ovulation in vivo in the rabbit. Hum Re-prod. 2006;21(3):624-31.
  19. Acosta TJ. Studies of follicular vascularity associated with follicle selection and ovulation in cattle. J Reprod Dev. 2007;53(1):39-44.
  20. Tanaka N, Espey LL, Okamura H. Increase in ovarian blood volume during ovulation in the gonadotropin-primed immature rat. Biol Reprod. 1989;40(4): 762-8.
  21. Fénichel P, Gobert B, Carré Y, Barbarino-Monnier P, Hiéronimus S. Polycystic ovary syndrome in autoimmune disease. Lancet. 1999;353(9171):2210.
  22. Kim H, Yamanouchi K, Nishihara M. Expression of ski in the granulosa cells of atretic follicles in the rat ovary. J Reprod Dev. 2006;52(6):715-21.
  23. Corner GW. On the origin of the corpus luteum of the sow from both granulosa and theca interna. Am J Anat. 1919;26(1):116-83.doi: 10.1002/aja.1000260105/abstract
  24. Gunin AG, Sharov AA. Role of mast cells in oestradiol effects on the uterus of ovariectomized rats. J Reprod Fertil. 1998;113(1):61-8.
  25. Junqueira LC, Carneiro J, Kelley RO. Basic histology. 4th ed. California: Lange Medical Publication; 1992. p. 123-4.
  26. Najati V, Sadrkhanlou RA, Hasanzadeh SH, Far-shid AA. Histological and histochemical and electronmicroscopic study on PCO induce immature rat ovary and endometrium. Iran Vet Res J. 2005;7: 176-80.
  27. Henmi H, Endo T, Nagasawa K, Hayashi T, Chida M, Akutagawa N, et al. Lysyl oxidase and MMP-2 expression in dehydroepiandrosterone- induced polycystic ovary in rats. Biol Reprod. 2001;64(1): 157-62.
  28. Dvorak AM. New aspects of mast cell biology. Int Arch Allergy Immunol. 1997;114(1):1-9.
  29. Faulds G. Mechanism of catecholamine resistance in polycystic ovarian syndrome reviewed. Women Health Wkly. 2003;1:6-7.
  30. Jefferson WN, Padilla-Banks E, Newbold RR. Lac-toferrin is an estrogen responsive protein in the uterus of mice and rats. Reprod Toxicol. 2000;14 (2):103-10.
  31. Eagleson CA, Gingrich MB, Pastor CL, Arora TK, Burt CM, Evans WS, et al. Polycystic ovarian syndrome: evidence that flutamide restores sensitivity of the gonadotropin-releasing hormone pulse generator to inhibition by estradiol and progesterone. J Clin Endocrinol Metab. 2000;85(11): 4047-52.
  32. Zeleznik AJ, Hutchison JS, Schuler HM. Inter-ference with the gonadotropin-suppressing actions of estradiol in macaques overrides the selection of a single preovulatory follicle. Endocrinology. 1985; 117(3):991-9.
  33. Lee GY, Croop JM, Anderson E. Multidrug resistance gene expression correlates with progesterone production in dehydroepiandrosterone-induced polycystic and equine chorionic gonadotropin-stimulated ovaries of prepubertal rats. Biol Reprod. 1998;58(2):330-7.
  34. Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppä L, et al. Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab. 1999;84(8):2744-50.
  35. Carmona F, Cristóbal P, Casamitjana R, Balasch J. Effect of tubal sterilization on ovarian follicular reserve and function. Am J Obstet Gynecol. 2003; 189(2):447-52.
  36. Abbott DH, Barnett DK, Levine JE, Padmanabhan V, Dumesic DA, Jacoris S, et al. Endocrine antecedents of polycystic ovary syndrome in fetal and infant prenatally androgenized female rhesus monkeys. Biol Reprod. 2008;79(1):154-63.
  37. Ying SY, Becker A. Periodical relationship between the secretion of foolicle stimulatory hormone and production of inhibin in rat. J Reprod Fertil. 1991;27:281-2.
  38. Batth BK, Parshad RK. Mast cell dynamics in the house rat (Rattus rattus) ovary during estrus cycle, pregnancy and lactation. Eur J Morphol. 2000;38 (1):17-23.
  39. Brinton LA, Gammon MD, Coates RJ, Hoover RN. Tubal ligation and risk of breast cancer. Br J Cancer. 2000;82(9):1600-4.
Journal of Reproduction & Infertility
Volume 13, Issue 4
Autumn 2012
Pages 193-203