To the Editor:
We read with great interest the article by Celik et al. (1) about the reduction of ovarian reserve in patients submitted to laparoscopic ovarian endometrioma excision. The topic of endometriosis and ovarian reserve is extremely interesting and has been extensively debated in the literature. Our group was the first to report a reduction of AMH levels in patients with endometriosis (2), and others have shown also a significant reduction of ovarian reserve after surgery in this group of patients (3). However, what caught our attention in this paper was the finding that after endometrioma excision, patients presented significantly lower levels of AMH while a significantly higher number of antral follicles was observed.
Nevertheless, the authors did not reach a physiological explanation for this finding. Therefore, we think that this finding could be, somewhat, compared to the accelerated dominant follicle development phenomenon described formerly by Nancy Klein in older women (4). If these patients were suffering from a type of reduction of ovarian reserve, it would be plausible to accept that higher FSH levels in the luteal-follicular transition, also demonstrated by the authors, and the reactive response of ovarian tissue after surgery have lead to the production of larger follicles. It is well known that follicles in more advanced stages of maturation do not produce AMH. It would justify a reduction in AMH levels and augmentation in the number of follicles counted.
To confirm this hypothesis, it would be necessary to have the size of all follicles measured by ultrasound before and after surgery. This model could provide us with valuable information about follicular dynamics in the remaining ovarian tissue after endometrioma excision.
Vanessa K. Genro, Ph.D.
Carlos A. B. Souza
João Sabino Cunha-Filho
Universidade Federal do Rio Grande do Sul
Ramiro Barcelos, Brazil
1. Celik HG, Dogan E, Okyay E, Ulukus C, Saatli B, Uysal S, et al. Effect of laparoscopic excision of endometriomas on ovarian reserve: serial changes in the serum antimüllerian hormone levels. Fertil Steril 2012;97:1472-8.
2. Lemos NA, Arbo E, Scalco R, Weiler E, Rosa V, Cunha-Filho JS. Decreased anti-Mullerian hormone and altered ovarian follicular cohort in infertile patients with mild/minimal endometriosis. Fertil Steril 2008;89:1064-8.
3. Exacoustos C, Zupi E, Amadio A, Szabolcs B, De Vivo B, Marconi D, et al. Laparoscopic removal of endometriomas: sonographic evaluation of residual functioning ovarian tissue. Am J Obstet Gynecol 2004;191:68-72.
4. Klein NA, Harper AJ, Houmard BS, Sluss PM, Soules MR. Is the short follicular phase in older women secondary to advanced or accelerated dominant follicle development? J Clin Endocrinol Metab 2002;87:5746-50.
Published online in Fertility and Sterility doi:10.1016/j.fertnstert.2012.09.007
The authors respond:
We read with interest the letter by Genro et al. commenting on our article “Effect of laparoscopic excision of endometriomas on ovarian reserve: serial changes in the serum antimüllerian hormone levels” (1).
In the letter Dr. Genro questions the unexpected increase in the antral follicle count (AFC) while antimüllerian hormone (AMH) levels were decreasing after endometrioma excision. We agree that there was an unexpected increase in AFC in our study. In the discussion section of our article we speculate that this finding may be either due to a reactive response of ovarian parenchyma after surgery, or due to the presence of endometriomas, which prevents the correct measurement of AFC preoperatively, and underestimating of AFC. In clinical practice we have seen that large endometriomas may prevent the visualization of the normal ovarian cortex. This increased AFC after endometrioma surgery was also reported by Tsolakidis et al. (2) in the three-step laser vaporization group of their study population. Similar results were also reported by Pados et al. (4). They compared one-stage laparoscopic cystectomy with “three-stage management” (laparoscopic drainage, followed by 3 months of GnRH agonist treatment, and then laser vaporization of the cyst wall during a second laparoscopic surgery) in 20 patients with ovarian endometriomas. Interestingly, AFC on the operated ovary was significantly increased after 6 months of surgery in the three-stage management group compared with the one-stage laparoscopy group.
In their letter, Genro et al. refer to an article by Klein et al. (3) for the physiologic explanation of this increase in AFC. We agree that the reactive response of ovarian tissue after surgery may have lead to the production of larger follicles because of the high luteo-follicular phase FSH levels. This may also be a plausible explanation for the AFC increase. Since more advanced stages of maturation do not produce AMH, higher numbers of antral follicles and lower levels of AMH may be encountered after endometrioma excision.
In our article, because of this unexpected increase in AFC, we conclude that AFC may not be a suitable ovarian reserve marker in patients undergoing endometrioma surgery. AFC may be measured as erroneously increased after surgery, whereas AMH is truly decreased. Obviously, more studies with longer follow-up periods are needed to better understand the impact of laparoscopic endometrioma excision on ovarian reserve.
Hale Goksever Celik, M.D.
Department of Obstetrics and Gynecology, Kayseri Develi General Hospital
Erbil Dogan, M.D.
Department of Obstetrics and Gynecology, Dokuz Eylul University
Inciralti, Izmir, Turkey
1. Celik HG, Dogan E, Okyay E, Ulukus C, Saatli B, Uysal S, et al. Effect of laparoscopic excision of endometriomas on ovarian reserve: serial changes in the serum antimüllerian hormone levels. Fertil Steril 2012; 97:1472-8.
2. Tsolakidis D, Pados G, Vavilis D, Athanatos D, Tsalikis T, Giannakou A, et al. The impact on ovarian reserve after laparoscopic ovarian cystectomy versus three-stage management in patients with endometriomas: a prospective randomized study. Fertil Steril 2010; 94:71–77.
3. Klein NA, Harper AJ, Houmard BS, Sluss PM, Soules MR. Is the short follicular phase in older women secondary to advanced or accelerated dominant follicle development? J Clin Endocrinol Metab 2002; 87:5746-50.
4. Pados G, Tsolakidis D, Assimakopoulos E, Athanatos D, Tarlatzis B. Sonographic changes after laparoscopic cystectomy compared with three-stage management in patients with ovarian endometriomas: a prospective randomized study. Hum Reprod 2010; 25:672–677.
Published online in Fertility and Sterility doi:10.1016/j.fertnstert.2012.09.008