Cited by 229Endometriosis Research and TreatmentReproductive Biology and FertilityOvarian function and disorders

Enhanced follicular recruitment and atresia in cortex derived from ovaries with endometriomas

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Kitajima, Michio, Dolmans, Marie-Madeleine, Donnez, Olivier, Masuzaki, Hideaki, Soares, Michelle, Donnez, Jacques·2014·Fertility and Sterility

Abstract

Objective To evaluate the effects of endometriomas on the regulation of early follicular development. Design Histologic analysis of prospectively collected biopsy samples. Setting Research unit in a university hospital. Patient(s) Women <40 years of age who have ovarian endometriomas. Intervention(s) Biopsy of healthy cortex from ovaries affected by endometriomas (≤ 4 cm) and contralateral ovaries without cysts. Main outcome measure(s) Histomorphological staging of early follicles, measurement of follicle, oocyte, and oocyte nucleus diameters, immunohistochemistry of proliferating cell nuclear antigen, and caspase-3. Result(s) Thirteen cortical samples from ovaries with endometriomas and 13 samples from contralateral ovaries without endometriomas were evaluated. Cortex from ovaries with endometriomas contained significantly more morphologically atretic early follicles than cortex from contralateral ovaries without cysts. These follicles showed cleaved caspase-3 immunostaining. Diameters of primordial follicles and oocytes were decreased in cortex from ovaries with endometriomas, whereas early follicles with proliferating cell nuclear antigen-positive granulosa cells (GCs) were significantly increased in number. Conclusion(s) Ovaries with endometriomas, which may be more prone to local pelvic inflammation, showed activated follicular recruitment and atresia of early follicles. The potential contribution of inflammation to follicle "burnout" in case of endometriomas is discussed.

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Crossref · 10.1016/j.fertnstert.2013.12.049

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  • In ovaries affected by endometriosis, a higher proportion of primordial follicles are recruited into the growing pool and a greater number of maturing follicles degenerate, resulting in quicker depletion of ovarian reserve.

    “In ovaries affected by endometriosis, a higher proportion of primordial follicles are recruited into the growing pool and a greater number of maturing follicles degenerate, resulting in quicker depletion of ovarian reserve (Kitajima et al., 2014; Takeuchi et al., 2019).”

    From Endometriosis and polycystic ovary syndrome are diametric disorders (2021) · cites this paper as Kitajima et al., 2014

    The Discussion reports increased early-follicle recruitment and atresia in ovaries with endometriomas, which the authors say may result in focal exhaustion of the primordial-follicle reserve. The claim extends this finding to ovaries affected by endometriosis generally and states quicker reserve depletion as a definite result, whereas the study examined ovaries with 1–4 cm endometriomas and hedges that conclusion. (LLM, conf=0.86)

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  • Lower testosterone in women with endometriosis contributes to a faster pace of follicular recruitment and death.

    “Lower testosterone in women with endometriosis shows evidence of contributing to a faster pace of follicular recruitment and death, across several studies.”

    From Endometriosis and polycystic ovary syndrome are diametric disorders (2021) · cites this paper as Kitajima et al., 2014

    The Discussion reports increased follicular recruitment and atresia in ovaries with endometriomas compared with contralateral ovaries without cysts. The paper discusses local inflammation, fibrosis, and anti-Müllerian hormone as possible contributors, but the searched passages do not link lower testosterone to these changes. The findings also concern ovaries with endometriomas, rather than all women with endometriosis. (LLM, conf=0.88)

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References 24 · Cited by 229

Research works printed but not linked: 21

  1. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometri- osis. Fertil Steril 2012;98:511-9.
  2. Donnez J. Endometriosis: enigmatic in the pathogenesis and controversial in its therapy. Fertil Steril 2012;98:509-10.
  3. Donnez J, Lousse JC, Jadoul P, Donnez O, Squifflet J. Laparoscopic manage- ment of endometriomas using a combined technique of excisional (cystec- tomy) and ablative surgery. Fertil Steril 2010;94:28-32.
  4. Busacca M, Vignali M. Endometrioma excision and ovarian reserve: a dangerous relation. J Minim Invasive Gynecol 2009;16:142-8.
  5. Jadoul P, Kitajima M, Donnez O, Squifflet J, Donnez J. Surgical treatment of ovarian endometriomas: state of the art? Fertil Steril 2012;98:556-63.
  6. Uncu G, Kasapoglu I, Ozerkan K, Seyhan A, Oral Yilmaztepe A, Ata B. Pro- spective assessment of the impact of endometriomas and their removal on ovarian reserve and determinants of the rate of decline in ovarian reserve. Hum Reprod 2013;28:2140-5.
  7. Somigliana E, Berlanda N, Benaglia L, Vigan o P, Vercellini P, Fedele L. Surgical excision of endometriomas and ovarian reserve: a systematic review on serum antim€ ullerian hormone level modifications. Fertil Steril 2012;98:1531-8.
  8. Kitajima M, Khan KN, Hiraki K, Inoue T, Fujishita A, Masuzaki H. Changes in serum anti-M€ ullerian hormone levels may predict damage to residual normal ovarian tissue after laparoscopic surgery for women with ovarian endome- trioma. Fertil Steril 2011;95:2589-2591.e1.
  9. Kitajima M, Defr ere S, Dolmans MM, Colette S, Squifflet J, Van Langendonckt A, et al. Endometriomas as a possible cause of reduced ovarian reserve in women with endometriosis. Fertil Steril 2011;96:685-91.
  10. Gougeon A, Chainy G. Morphometric studies of small follicles in ovaries of women at different ages. J Reprod Fertil 1987;81:433-42.
  11. Westergaard CG, Byskov AG, Andersen CY. Morphometric characteristics of the primordial to primary follicle transition in the human ovary in relation to age. Hum Reprod 2007;22:2225-31.
  12. Dolmans MM, Martinez-Madrid B, Gadisseux E, Guiot Y, Yuan WY, Torre A, et al. Short-term transplantation of isolated human ovarian follicles and cortical tissue into nude mice. Reproduction 2007;134:253-62.
  13. David A, Van Langendonckt A, Gilliaux S, Dolmans MM, Donnez J, Amorim CA. Effect of cryopreservation and transplantation on the expres- sion of kit ligand and anti-Mullerian hormone in human ovarian tissue. Hum Reprod 2012;27:1088-95.
  14. Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex sur- rounding ovarian endometriosis. Fertil Steril 2010;93:2431-2.
  15. Gougeon A. Dynamics of human follicular growth: morphologic, dynamic, and functional aspects. In: Leung P, Adashi E, editors. The ovary. 2nd ed. New York: Elsevier Academic Press; 2004:25-43.
  16. Hurst PR, Mora JM, Fenwick MA. Caspase-3, TUNEL and ultrastructural studies of small follicles in adult human ovarian biopsies. Hum Reprod 2006;21:1974-80.
  17. Depalo R, Nappi L, Loverro G, Bettocchi S, Caruso ML, Valentini AM, et al. Evidence of apoptosis in human primordial and primary follicles. Hum Re- prod 2003;18:2678-82.
  18. Martinez-Madrid B, Camboni A, Dolmans MM, Nottola S, Van Langendonckt A, Donnez J. Apoptosis and ultrastructural assessment after cryopreservation of whole human ovaries with their vascular pedicle. Fertil Steril 2007;87:1153-65.
  19. Opøien HK, Fedorcsak P, Polec A, Stensen MH, Abyholm T, Tanbo T. Do en- dometriomas induce an inflammatory reaction in nearby follicles? Hum Re- prod 2013;28:1837-45.
  20. Sobinoff AP, Pye V, Nixon B, Roman SD, McLaughlin EA. Jumping the gun: smoking constituent BaP causes premature primordial follicle activation and impairs oocyte fusibility through oxidative stress. Toxicol Appl Pharmacol 2012;260:70-80.
  21. Kalich-Philosoph L, Roness H, Carmely A, Fishel-Bartal M, Ligumsky H, Paglin S, et al. Cyclophosphamide triggers follicle activation and ''burnout''; AS101 prevents follicle loss and preserves fertility. Sci Transl Med 2013;5: 185ra62.

Authors
Kitajima, M., Dolmans, M.-M., Donnez, O., Masuzaki, H., Soares, M., & Donnez, J.
Affiliations
  • Nagasaki University (JP)
  • UCLouvain (BE)
Corresponding author
Dolmans, Marie-Madeleine
Venue
Fertility and Sterility
Publisher
Elsevier BV
Published
2014-04
Volume
101
Issue
4
Pages
1031-1037
ISSN
0015-0282 (ISSN-L)
OpenAlex
W1997742717
Cited by
229
References
24
Citations by year
2026: 12 · 2025: 24 · 2024: 19 · 2023: 19 · 2022: 27 · 2021: 31 · 2020: 27 · 2019: 14 · 2018: 18 · 2017: 17 · 2016: 9 · 2015: 10 · 2014: 2
FWCI
15.38
Type
journal article
Language
en
Open access
Locations
  • Fertility and Sterility (publishedVersion)
  • PubMed (publishedVersion)
  • Digital Access to Libraries (Université catholique de Louvain (UCL), l'Université de Namur (UNamur) and the Université Saint-Louis (USL-B)) (submittedVersion)
  • VUBIR (Vrije Universiteit Brussel) (submittedVersion)
Funders
  • Fonds De La Recherche Scientifique - FNRS
  • Japan Society for the Promotion of Science (24592475)
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
  • Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
Keywords
endometrioma, follicular atresia, follicle recruitment, primordial follicles, oocyte size, granulosa cells, proliferating cell nuclear antigen, caspase-3, ovarian inflammation, ovarian cortex
MeSH terms
Adult, Endometriosis, Female, Follicular Atresia, Ovarian Follicle, Humans, Young Adult

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