THE MECHANISMS OF SECONDARY OVARIAN FAILURE AT OPERATIONS ON THE PELVIC ORGANS (EXPERIMENTAL STUDY)
https://doi.org/10.17749/2070-4968.2015.9.4.006-017
Abstract
Objective - to establish a hysterectomy role in formation of secondary ovarian failure and to estimate possibility of application of DHEA. Materials and Methods. Sexually mature female rats outbred Wistar. Main group: 1a - hysterectomy + salpingectomy (n=24), Ib - hysterectomy (n=6), Ic - salpingectomy (n=6). Group of comparison - hysterectomy + salpingectomy + DHEA for 4 weeks after surgery (n=12). Intact control (n=12). Enzyme immunoassay serum concentrations anti-Müllerian hormone (AMH) and follicle stimulating (FSH) hormone, testosterone (T). Results. Shows statistically significant reductions AMH after operation at all time experience (2-10-30-40 days), increased FSH, only the end of the experiment (day 40), only the reduction of T by 10 day of the experiment compared to the control. Hysterectomy was not significantly altering the concentration of AMH, FSH and T on day 10. Salpingectomy significantly reduced the concentration of AMH and T, and has no effect on FSH. Use of DHEA 1 mg / day for 28 days did not alter the concentrations of FSH and T significantly increases AMH compared to animals after surgery, but still significantly lower than that in the control. Conclusion. Isolated hysterectomy does not substantially affect the functional ovarian reserve. Isolated salpingectomy, and also the combined operation volume (hysterectomy + salpingectomy) result in secondary ovarian failure. Effect of DHEA on the function of the gonads (AMH) remains uncertain.
About the Authors
I. A. Petrov
Siberian State Medical University
Russian Federation
PhD, intramural doctoral student in Obstetrics and Gynecology
Russian Federation
PhD, intramural doctoral student in Obstetrics and Gynecology
O. A. Tihonovskaja
Siberian State Medical University
Russian Federation
MD, professor of obstetrics and gynecology
Russian Federation
MD, professor of obstetrics and gynecology
I. I. Kuprijanova
Siberian State Medical University
Russian Federation
Postgraduate of the Department of Histology, Cytology and Embryology
Russian Federation
Postgraduate of the Department of Histology, Cytology and Embryology
A. O. Okorokov
Siberian State Medical University
Russian Federation
PhD, Department of Obstetrics and Gynecology
Russian Federation
PhD, Department of Obstetrics and Gynecology
S. V. Logvinov
Siberian State Medical University
Russian Federation
MD, Professor, Vice-Rector for Academic Affairs, Head. Department of Histology, Cytology and Embryology
Russian Federation
MD, Professor, Vice-Rector for Academic Affairs, Head. Department of Histology, Cytology and Embryology
M. S. Petrova
Siberian State Medical University
Russian Federation
MD, Associate Professor of Obstetrics and Gynecology
Russian Federation
MD, Associate Professor of Obstetrics and Gynecology
L. A. Agarkova
Research Institute for Obstetrics, Gynecology and Perinatology
Russian Federation
MD, professor, honored doctor of the Russian Federation, Director
Russian Federation
MD, professor, honored doctor of the Russian Federation, Director
References
1. Smetnik V.P., Tumilovich L.G., ed. Nonoperational gynecology [Neoperativnaja ginekologija (In Russian)]. Moscow. 2006. 632 s.
2. Alarslan D., Sarandol A., Cengiz C., Develioglu O.H. Androgens and sexual dysfunction in naturally and surgically menopausal women. J. Obstet. Gynaecol. Res. 2011; 37 (8): 1027-34.
3. Atabekoğlu C., Taşkin S., Kahraman K. et al. The effect of total abdominal hysterectomy on serum anti-Müllerian hormone levels: a pilot study. Climacteric. 2012; 15 (4): 393-7.
4. Belaisch-Allart J., Mayenga J.-M., Castaing N., Allart J.-P. Is tubal and uterine surgery deleterious to ovarian reserve. Gynecol. Obstet. Fertil. 2006; 34 (12): 1111-7.
5. Biro J.C., Eneroth P. Inhibitory effect of the uterus on plasma and pituitary FSH in rats. J Endocrinol. 1990; 124 (2): 183-9.
6. Bricaire L., Laroche E., Bourcigaux N., Donadille B., Christin-Maitre S. Premature ovarian failures. Presse Med. 2013; 42 (11): 1500-7.
7. Chalmers C., Lindsay M., Usher D., Warner P., Evans D., Ferguson M. Hysterectomy and ovarian function: levels of follicle stimulating hormone and incidence of menopausalsymptoms are not affected by hysterectomy in women under age 45 years. Climacteric. 2002; 5 (4): 366-73.
8. Ciarmela P., Islam M.S., Reis F.M. et al. Growth factors and myometrium: biological effects in uterine fibroid and possible clinical implications. Hum. Reprod. Update. 2011; 17 (6): 772-90.
9. Cohen S.L., Vitonis A.F., Einarsson J.I. Updated hysterectomy surveillance and factors associated with minimally invasive hysterectomy. JSLS . 2014; 18 (3): e2014.00096.
10. Davis S.R., Panjari M., Stanczyk F.Z. Clinical review: DHEA replacement for postmenopausal woman. J. Clin. Endocrinol. Metab. 2011; 96 (6): 1642-53.
11. Findley A.D., Siedhoff M.T., Hobbs K.A. et al. Short-term effects of salpingectomy during laparoscopic hysterectomy on ovarian reserve: a pilot randomized controlled trial. Fertil. Steril. 2013; 100 (6): 1704-8.
12. Fogle R.H., Stanczyk F.Z., Zhang X., Paulson R.J. Ovarian androgen production in postmenopausal women. J. Clin. Endocrinol. Metab. 2007; 92 (8): 3040-3.
13. Fouany M.R., Sharara F.I. Is there a role for DHEA supplementation in women with diminished ovarian reserve? J. Assist. Reprod. Genet. 2013; 30 (9): 1239-44.
14. Gleicher N., Barad D.H. Dehydroepiandrosterone (DHEA) supplementation in diminished ovarian reserve (DOR). Reprod. Biol. Endocrinol. 2011; 9: 67.
15. Gleicher N., Weghofer A., Barad D.H. Defining ovarian reserve to better understand ovarian aging. Reprod. Biol. Endocrinol. 2011; 9: 23.
16. Gökgözoğlu L., Islimye M., Topçu H.O., Ozcan U.3. The Effects of total abdominal hysterectomy on ovarian function – serial changes in serum anti-Müllerian hormone, FSH and estradiol levels. Adv. Clin. Exp. Med. 2014; 23 (5): 821-5.
17. Grynnerup A.G., Lindhard A., Sørensen S. AntiMüllerian hormone levels in salpingectomized compared with nonsalpingectomized women with tubal factor infertility and women with unexplained infertility. Acta Obstet. Gynecol. Scand. 2013; 92 (11): 1297-303.
18. Harlow S.D., Gass M., Hall J.E. et al. Executive summary of STRAW+10: addressing the unfinished agenda of staging reproductive aging. Climacteric. 2012; 15 (2): 105-14.
19. Hassa H., Tanir H.M., Ardic N. Early postoperative changes in testosterone, dehydroepiandrosterone sulfate, and sex hormone-binding globulin after hysterectomy with or without concomitant oophorectomy. Fertil. Steril. 2006; 86 (4): 981-9.
20. Hehenkamp W.J., Volkers N.A., Broekmans F.J. et al. Loss of ovarian reserve after uterine artery embolization: a randomized comparison with hysterectomy. Hum. Reprod. 2007; 22 (7): 1996-2005.
21. Hyman J.H., Margalioth E.J., Rabinowitz R. et al. DHEA supplementation may improve IVF outcome in poor responders: a proposed mechanism. Eur. J. Obstet. Gynecol. Reprod. Biol. 2013; 168 (1): 49-53.
22. Ikeda K., Baba T., Morishita M. et al. Long-term treatment with dehydroepiandrosterone may lead to follicular atresia through interaction with anti-Mullerian hormone. J. Ovarian Res. 2014; 7: 46.
23. Iwase A., Nakamura T., Nakahara T., Goto M., Kikkawa F. Assessment of ovarian reserve using anti-Müllerian hormone levels in benign gynecologic conditions and surgical interventions: a systematic narrative review. Reprod. Biol. Endocrinol. 2014; 12 (1): 125.
24. Janse F., Tanahatoe S.J., Eijkemans M.J., Fauser B.C. Testosterone concentrations, using different assays, in different types of ovarian insufficiency: a systematic review and metaanalysis. Hum. Reprod. Up. 2012; 18 (4): 405-19.
25. Janson P.O., Jansson I. The acute effect of hysterectomy on ovarian blood flow. Am. J. Obstet. Gynecol. 1977; 127 (4): 349-52.
26. Kalampokas T., Kamath M.S., Kalampokas E. AMH after laparoscopic surgery of the ovaries: a review. Gynecol. Endocrinol. 2013; 29 (5): 408-11.
27. Kotsopoulos J., Shafrir A.L., Rice M. et al. The relationship between bilateral oophorectomy and plasma hormone levels in postmenopausal women. Horm. Cancer. 2015; 6 (1): 54-63.
28. Lee D.Y., Park H.J., Kim B.G., Bae D.S., Yoon B.K., Choi D. Change in the ovarian environment after hysterectomy as assessed by ovarian arterial blood flow indices and serum antiMüllerian hormone levels. Eur. J. Obstet. Gynecol. Reprod. Biol. 2010; 151 (1): 82-5.
29. Mamas. L., Mamas E. Dehydroepiandrosterone supplementation in assisted reproduction: rationale and results. Curr. Opin. Obstet. Gynecol. 2009; 21 (4): 306-8.
30. McGee E.A., Hsueh A.J. Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 2000; 21 (2): 200-14.
31. Moorman P.G., Myers E.R., Schildkraut J.M., Iversen E.S., Wang F., Warren N. Effect of hysterectomy with ovarian preservation on ovarian function. Obstet. Gynecol. 2011; 118 (6): 1271-9.
32. Morelli M., Venturella R., Mocciaro R. et al. Prophylactic salpingectomy in premenopausal low-risk women for ovarian cancer: primum non nocere. Gynecol. Oncol. 2013; 129 (3): 448-51.
33. Nahás E., Pontes A., Traiman P., NahásNeto J., Dalben I., De Luca L. Inhibin B and ovarian function after total abdominal hysterectomy in women of reproductive age. Gynecol. Endocrinol. 2003; 17 (2): 125-31.
34. Neill J.D., Smith M.S. Pituitary-Ovarian Interrelationships in the Rat. In: V.H.T. James, L. Martini (eds). Current Topics in Experimental Endocrinology. New York: Academic Press, 1974. p. 73-107.
35. Nelson S.M., Telfer E.E., Anderson R.A. The ageing ovary and uterus: new biological insights. Hum. Reprod. Upd. 2013; 19 (1): 67-83.
36. Ni L., Sadiq S., Mao Y., Cui Y., Wang W., Liu J. Influence of various tubal surgeries to serum antimullerian hormone level and outcome of the subsequent IVF-ET treatment. Gynecol. Endocrinol. 2013; 29 (4): 345-9.
37. Otala M., Mäkinen S., Tuuri T. et al. Effects of testosterone, dihydrotestosterone, and 17 beta-estradiol on human ovarian tissue survival in culture. Fertil. Steril. 2004; 82 (3): 1077-85.
38. Raffi F., Metwally M., Amer S. The impact of excision of ovarian endometrioma on ovarian reserve: a systematic review and metaanalysis. J.Clin. Endocrinol. Metab. 2012; 97 (9): 3146-54.
39. Rashid S., Khaund A., Murray L.S. et al. The effects of uterine artery embolisation and surgical treatment on ovarian function in women with uterine fibroids. BJOG. 2010; 117 (8): 985-9.
40. Read M.D., Edey K.A., Hapeshi J., Foy C. The age of ovarian failure following premenopausal hysterectomy with ovarian conservation. Menopause Int. 2010. 16 (2): 56-9.
41. Schmidt P. The 2012 hormone therapy position statement of the North American menopause society. Menopause. 2012; 19 (3): 257-71.
42. Sen A., Hammes S.R. Granulosa cell-specific androgen receptors are critical regulators of ovarian development and function. Mol. Endocrinol. 2010; 24 (7): 1393-403.
43. Shifren J.L., Braunstein G.D., Simon J.A. et al. Transdermal testosterone treatment in women with impaired sexual function after oophorectomy. N. Engl. J. Med. 2000; 343 (10): 682-8.
44. Sluijmer A.V., Heineman M.J., De Jong F.H., Evers J.L. Endocrine activity of the postmenopausal ovary: the effects of pituitary down-regulation and oophorectomy. J. Clin. Endocrinol. Metab. 1995; 80 (7): 2163-7.
45. Souza A.Z., Fonseca A.M., Izzo V.M., Clauzet R.M., Salvatore C.A. Ovarian histology and function after total abdominal hysterectomy. Obstet. Gynecol. 1986; 68 (6): 847-9.
46. Takae S., Kawamura K., Sato Y. et. al. Analysis of late-onset ovarian insufficiency after ovarian surgery: retrospective study with 75 patients of post-surgical ovarian insufficiency. PLoS One. 2014; 9 (5): e98174.
47. Tapisiz O.L., Gungor T., Aytan H. et al. Does hysterectomy affect ovarian function? Histopathologic evaluation and serum FSH, inhibin A, and inhibin B levels in an experimental rat model. Eur. J. Obstet. Gynecol. Reprod. Biol. 2008; 140 (1): 61-6.
48. Ulug P., Oner G. Evaluation of the effects of single or multiple dose methotrexate administration, salpingectomy on ovarian reserve of rat with the measurement of antiMüllerian hormone (AMH) levels and histological analysis. Eur. J. Obstet. Gynecol. Reprod. Biol. 2014; 181: 205-9.
49. Vlahos N., Papalouka M., Triantafyllidou O.3. et al. Dehydroepiandrosterone administration before IVF in poor responders: a prospective cohort study. Reprod. Biomed. Online. 2015; 30 (2): 191-6.
50. Vuorento T., Mäenpää J., Huhtaniemi I. Followup of ovarian endocrine function in premenopausal women after hysterectomy by daily measurements ofsalivary progesterone. Clin. Endocrinol. (Oxf). 1992; 36 (5): 505-10.
51. Vural B., Cakiroglu Y., Vural F., Filiz S. Hormonal and functional biomarkers in ovarian response. Arch. Gynecol. Obstet. 2014; 289 (6): 1355-61.
52. Wang H.Y., Quan S., Zhang R.L. et al. Comparison of serum anti-Mullerian hormone levels following hysterectomy and myomectomy for benign gynaecological conditions. Eur. J. Obstet. Gynecol. Reprod. Biol. 2013; 171 (2): 368-71.
53. Wiser A., Gonen O., Ghetler Y., Shavit T., Berkovitz A., Shulman A. Addition of dehydroepiandrosterone (DHEA) for poorresponder patients before and during IVF treatment improves the pregnancy rate: a randomized prospective study. Hum. Reprod. 2010; 25 (10): 2496-500.
54. Ye X.P., Yang Y.Z., Sun X.X. A retrospective analysis of the effect of salpingectomy on serum antiMüllerian hormone level and ovarian reserve. Am. J. Obstet. Gynecol. 2015; 212 (1): 53.e1-10.
55. Yi Q.H., Ling S.R., Chen K.M., He W.R., Li L., Yi C.J. Evaluation of the clinical value of simultaneous hysterectomy and bilateral salpingectomy in perimenopausal women. Zhonghua Fu Chan Ke Za Zhi. 2012; 47 (2): 110-4.
56. Yuan H., Wang C., Wang D., Wang Y.3. Comparison of the effect of laparoscopic supracervical and total hysterectomy for uterine fibroids on ovarian reserve by assessing serum anti-Mullerian hormone levels: a prospective cohort study. J. Minim. Invasive Gynecol. 2015. PII: S1553-4650 (15) 00090-4.
57. Zhang H.H., Xu P.Y., Wu J. et al. Dehydroepiandrosterone improves follicular fluid bone morphogenetic protein-15 and accumulated embryo score of infertility patients with diminished ovarian reserve undergoing in vitro fertilization: a randomized controlled trial. J. Ovarian Res. 2014; 7 (1): 93.
58.
59.
Review
For citations:
Petrov I.A., Tihonovskaja O.A., Kuprijanova I.I., Okorokov A.O., Logvinov S.V., Petrova M.S., Agarkova L.A. THE MECHANISMS OF SECONDARY OVARIAN FAILURE AT OPERATIONS ON THE PELVIC ORGANS (EXPERIMENTAL STUDY). Obstetrics, Gynecology and Reproduction. 2015;9(4):6-17. (In Russ.) https://doi.org/10.17749/2070-4968.2015.9.4.006-017
Views:
562
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Email this article 
