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Published in: Journal of Ovarian Research 1/2014

Open Access 01-12-2014 | Research

The impact of endometrioma and laparoscopic cystectomy on ovarian reserve and the exploration of related factors assessed by serum anti-Mullerian hormone: a prospective cohort study

Authors: Yuqing Chen, Huihui Pei, Yajie Chang, Minghui Chen, Haihe Wang, Hongzhe Xie, Shuzhong Yao

Published in: Journal of Ovarian Research | Issue 1/2014

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Abstract

Background

To evaluate the impact of the presence of endometrioma and laparoscopic cystectomy on ovarian reserve as assessed by serum anti-Müllerian hormone (AMH) level. In addition, factors related to the decline in ovarian reserve were analyzed.

Methods

From June 2013 to January 2014, we prospectively included 40 women with endometriomas as the study group (group A), 36 women with tubal factor infertilities as control group 1 (group B) and 22 women with the other benign ovarian cysts as control group 2 (group C). The women with ovarian cysts underwent laparoscopic cystectomy. Serum AMH levels were determined preoperatively and at 1 month after surgery.

Results

The endometrioma group had lower AMH levels (1.53 ± 1.37 ng/ml) compared with the other benign ovarian cyst group (2.20 ± 1.23 ng/ml) and the tubal factor infertility group (2.82 ± 1.74 ng/ml). The rate of serum AMH decline 1 month after surgery in the endometrioma group (0.62 ± 0.35) was larger than the decline in the other benign ovarian cyst group (0.32 ± 0.30). The preoperative AMH level showed a significant correlation with patient age (group A, r = −0.32; group B, r = −0.54; group C, r = −0.71); there was a statistically significant correlation between the rate of serum AMH decline and endometrioma diameter as well as with the preoperative serum AMH level. In addition, the rate of serum AMH decline was larger for bilateral endometriomas than for unilateral endometriomas, but there was no similar correlation in the other benign ovarian cyst group. The rate of AMH decline after surgery in the subgroup of >7 cm was significantly higher than in the subgroup of ≤7 cm.

Conclusions

Ovarian endometriomas per se may damage ovarian reserve, and cystectomy of endometriomas may cause greater damage to ovarian reserve compared with other benign ovarian cysts. The operation-related damage to the ovarian reserve was positively related to whether the endometriomas were bilateral, as well as cyst size (especially for cysts >7 cm), but was negatively related to the preoperative serum AMH level. Age was a negative factor that affected the ovarian reserve.
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Literature
1.
go back to reference de Ziegler D, Borghese B, Chapron C: Endometriosis and infertility: pathophysiology and management. Lancet 2010,376(9742):730–738. 10.1016/S0140-6736(10)60490-4CrossRefPubMed de Ziegler D, Borghese B, Chapron C: Endometriosis and infertility: pathophysiology and management. Lancet 2010,376(9742):730–738. 10.1016/S0140-6736(10)60490-4CrossRefPubMed
2.
go back to reference Busacca M, Vignali M: Endometrioma excision and ovarian reserve: a dangerous relation. J Minim Invasive Gynecol 2009,16(2):142–148. 10.1016/j.jmig.2008.12.013CrossRefPubMed Busacca M, Vignali M: Endometrioma excision and ovarian reserve: a dangerous relation. J Minim Invasive Gynecol 2009,16(2):142–148. 10.1016/j.jmig.2008.12.013CrossRefPubMed
3.
go back to reference Ruiz-Flores FJ, Garcia-Velasco JA: Is there a benefit for surgery in endometrioma-associated infertility? Curr Opin Obstet Gynecol 2012,24(3):136–140. 10.1097/GCO.0b013e32835175d9CrossRefPubMed Ruiz-Flores FJ, Garcia-Velasco JA: Is there a benefit for surgery in endometrioma-associated infertility? Curr Opin Obstet Gynecol 2012,24(3):136–140. 10.1097/GCO.0b013e32835175d9CrossRefPubMed
4.
go back to reference Fanchin R, Schonauer LM, Righini C, Guibourdenche J, Frydman R, Taieb J: Serum anti-Mullerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3. Hum Reprod 2003,18(2):323–327. 10.1093/humrep/deg042CrossRefPubMed Fanchin R, Schonauer LM, Righini C, Guibourdenche J, Frydman R, Taieb J: Serum anti-Mullerian hormone is more strongly related to ovarian follicular status than serum inhibin B, estradiol, FSH and LH on day 3. Hum Reprod 2003,18(2):323–327. 10.1093/humrep/deg042CrossRefPubMed
5.
go back to reference Hehenkamp WJ, Looman CW, Themmen AP, de Jong FH, Te VE, Broekmans FJ: Anti-Mullerian hormone levels in the spontaneous menstrual cycle do not show substantial fluctuation. J Clin Endocrinol Metab 2006,91(10):4057–4063. 10.1210/jc.2006-0331CrossRefPubMed Hehenkamp WJ, Looman CW, Themmen AP, de Jong FH, Te VE, Broekmans FJ: Anti-Mullerian hormone levels in the spontaneous menstrual cycle do not show substantial fluctuation. J Clin Endocrinol Metab 2006,91(10):4057–4063. 10.1210/jc.2006-0331CrossRefPubMed
6.
go back to reference La Marca A, Stabile G, Artenisio AC, Volpe A: Serum anti-Mullerian hormone throughout the human menstrual cycle. Hum Reprod 2006,21(12):3103–3107. 10.1093/humrep/del291CrossRefPubMed La Marca A, Stabile G, Artenisio AC, Volpe A: Serum anti-Mullerian hormone throughout the human menstrual cycle. Hum Reprod 2006,21(12):3103–3107. 10.1093/humrep/del291CrossRefPubMed
7.
go back to reference Deb S, Campbell BK, Pincott-Allen C, Clewes JS, Cumberpatch G, Raine-Fenning NJ: Quantifying effect of combined oral contraceptive pill on functional ovarian reserve as measured by serum anti-Mullerian hormone and small antral follicle count using three-dimensional ultrasound. Ultrasound Obstet Gynecol 2012,39(5):574–580. 10.1002/uog.10114CrossRefPubMed Deb S, Campbell BK, Pincott-Allen C, Clewes JS, Cumberpatch G, Raine-Fenning NJ: Quantifying effect of combined oral contraceptive pill on functional ovarian reserve as measured by serum anti-Mullerian hormone and small antral follicle count using three-dimensional ultrasound. Ultrasound Obstet Gynecol 2012,39(5):574–580. 10.1002/uog.10114CrossRefPubMed
8.
go back to reference Kristensen SL, Ramlau-Hansen CH, Andersen CY, Ernst E, Olsen SF, Bonde JP, Vested A, Toft G: The association between circulating levels of antimullerian hormone and follicle number, androgens, and menstrual cycle characteristics in young women. Fertil Steril 2012,97(3):779–785. 10.1016/j.fertnstert.2011.12.017CrossRefPubMed Kristensen SL, Ramlau-Hansen CH, Andersen CY, Ernst E, Olsen SF, Bonde JP, Vested A, Toft G: The association between circulating levels of antimullerian hormone and follicle number, androgens, and menstrual cycle characteristics in young women. Fertil Steril 2012,97(3):779–785. 10.1016/j.fertnstert.2011.12.017CrossRefPubMed
9.
go back to reference Kuroda M, Kuroda K, Arakawa A, Fukumura Y, Kitade M, Kikuchi I, Kumakiri J, Matsuoka S, Brosens IA, Brosens JJ, Takeda S, Yao T: Histological assessment of impact of ovarian endometrioma and laparoscopic cystectomy on ovarian reserve. J Obstet Gynaecol Res 2012,38(9):1187–1193. 10.1111/j.1447-0756.2012.01845.xCrossRefPubMed Kuroda M, Kuroda K, Arakawa A, Fukumura Y, Kitade M, Kikuchi I, Kumakiri J, Matsuoka S, Brosens IA, Brosens JJ, Takeda S, Yao T: Histological assessment of impact of ovarian endometrioma and laparoscopic cystectomy on ovarian reserve. J Obstet Gynaecol Res 2012,38(9):1187–1193. 10.1111/j.1447-0756.2012.01845.xCrossRefPubMed
10.
go back to reference Pacchiarotti A, Frati P, Milazzo GN, Catalano A, Gentile V, Moscarini M: Evaluation of serum anti-Mullerian hormone levels to assess the ovarian reserve in women with severe endometriosis. Eur J Obstet Gynecol Reprod Biol 2014, 172: 62–64. 10.1016/j.ejogrb.2013.10.003CrossRefPubMed Pacchiarotti A, Frati P, Milazzo GN, Catalano A, Gentile V, Moscarini M: Evaluation of serum anti-Mullerian hormone levels to assess the ovarian reserve in women with severe endometriosis. Eur J Obstet Gynecol Reprod Biol 2014, 172: 62–64. 10.1016/j.ejogrb.2013.10.003CrossRefPubMed
11.
go back to reference Streuli I, de Ziegler D, Gayet V, Santulli P, Bijaoui G, de Mouzon J, Chapron C: In women with endometriosis anti-Mullerian hormone levels are decreased only in those with previous endometrioma surgery. Hum Reprod 2012,27(11):3294–3303. 10.1093/humrep/des274CrossRefPubMed Streuli I, de Ziegler D, Gayet V, Santulli P, Bijaoui G, de Mouzon J, Chapron C: In women with endometriosis anti-Mullerian hormone levels are decreased only in those with previous endometrioma surgery. Hum Reprod 2012,27(11):3294–3303. 10.1093/humrep/des274CrossRefPubMed
12.
go back to reference Benaglia L, Pasin R, Somigliana E, Vercellini P, Ragni G, Fedele L: Unoperated ovarian endometriomas and responsiveness to hyperstimulation. Hum Reprod 2011,26(6):1356–1361. 10.1093/humrep/der097CrossRefPubMed Benaglia L, Pasin R, Somigliana E, Vercellini P, Ragni G, Fedele L: Unoperated ovarian endometriomas and responsiveness to hyperstimulation. Hum Reprod 2011,26(6):1356–1361. 10.1093/humrep/der097CrossRefPubMed
13.
go back to reference Muzii L, Bianchi A, Croce C, Manci N, Panici PB: Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure? Fertil Steril 2002,77(3):609–614. 10.1016/S0015-0282(01)03203-4CrossRefPubMed Muzii L, Bianchi A, Croce C, Manci N, Panici PB: Laparoscopic excision of ovarian cysts: is the stripping technique a tissue-sparing procedure? Fertil Steril 2002,77(3):609–614. 10.1016/S0015-0282(01)03203-4CrossRefPubMed
14.
go back to reference Stilley JA, Birt JA, Sharpe-Timms KL: Cellular and molecular basis for endometriosis-associated infertility. Cell Tissue Res 2012,349(3):849–862. 10.1007/s00441-011-1309-0PubMedCentralCrossRefPubMed Stilley JA, Birt JA, Sharpe-Timms KL: Cellular and molecular basis for endometriosis-associated infertility. Cell Tissue Res 2012,349(3):849–862. 10.1007/s00441-011-1309-0PubMedCentralCrossRefPubMed
15.
go back to reference Tehrani FR, Mansournia MA, Solaymani-Dodaran M, Azizi F: Age-specific serum anti-Mullerian hormone levels: estimates from a large population-based sample. Climacteric 2014,17(5):591–597. 10.3109/13697137.2014.912262CrossRefPubMed Tehrani FR, Mansournia MA, Solaymani-Dodaran M, Azizi F: Age-specific serum anti-Mullerian hormone levels: estimates from a large population-based sample. Climacteric 2014,17(5):591–597. 10.3109/13697137.2014.912262CrossRefPubMed
16.
go back to reference Chapron C, Fauconnier A, Goffinet F, Breart G, Dubuisson JB: Laparoscopic surgery is not inherently dangerous for patients presenting with benign gynaecologic pathology. Results of a meta-analysis. Hum Reprod 2002,17(5):1334–1342. 10.1093/humrep/17.5.1334CrossRefPubMed Chapron C, Fauconnier A, Goffinet F, Breart G, Dubuisson JB: Laparoscopic surgery is not inherently dangerous for patients presenting with benign gynaecologic pathology. Results of a meta-analysis. Hum Reprod 2002,17(5):1334–1342. 10.1093/humrep/17.5.1334CrossRefPubMed
17.
go back to reference Litta P, D’Agostino G, Conte L, Saccardi C, Cela V, Angioni S, Plebani M: Anti-Mullerian hormone trend after laparoscopic surgery in women with ovarian endometrioma. Gynecol Endocrinol 2013,29(5):452–454. 10.3109/09513590.2012.758704CrossRefPubMed Litta P, D’Agostino G, Conte L, Saccardi C, Cela V, Angioni S, Plebani M: Anti-Mullerian hormone trend after laparoscopic surgery in women with ovarian endometrioma. Gynecol Endocrinol 2013,29(5):452–454. 10.3109/09513590.2012.758704CrossRefPubMed
18.
go back to reference Takashima A, Takeshita N, Otaka K, Kinoshita T: Effects of bipolar electrocoagulation versus suture after laparoscopic excision of ovarian endometrioma on the ovarian reserve and outcome of in vitro fertilization. J Obstet Gynaecol Res 2013,39(7):1246–1252. 10.1111/jog.12056CrossRefPubMed Takashima A, Takeshita N, Otaka K, Kinoshita T: Effects of bipolar electrocoagulation versus suture after laparoscopic excision of ovarian endometrioma on the ovarian reserve and outcome of in vitro fertilization. J Obstet Gynaecol Res 2013,39(7):1246–1252. 10.1111/jog.12056CrossRefPubMed
19.
go back to reference Sugita A, Iwase A, Goto M, Nakahara T, Nakamura T, Kondo M, Osuka S, Mori M, Saito A, Kikkawa F: One-year follow-up of serum antimullerian hormone levels in patients with cystectomy: are different sequential changes due to different mechanisms causing damage to the ovarian reserve? Fertil Steril 2013,100(2):516–522. 10.1016/j.fertnstert.2013.03.032CrossRefPubMed Sugita A, Iwase A, Goto M, Nakahara T, Nakamura T, Kondo M, Osuka S, Mori M, Saito A, Kikkawa F: One-year follow-up of serum antimullerian hormone levels in patients with cystectomy: are different sequential changes due to different mechanisms causing damage to the ovarian reserve? Fertil Steril 2013,100(2):516–522. 10.1016/j.fertnstert.2013.03.032CrossRefPubMed
20.
go back to reference Muzii L, Di Tucci C, Di Feliciantonio M, Marchetti C, Perniola G, Panici PB: The effect of surgery for endometrioma on ovarian reserve evaluated by antral follicle count: a systematic review and meta-analysis. Hum Reprod 2014, 29: 2190–2198. 10.1093/humrep/deu199CrossRefPubMed Muzii L, Di Tucci C, Di Feliciantonio M, Marchetti C, Perniola G, Panici PB: The effect of surgery for endometrioma on ovarian reserve evaluated by antral follicle count: a systematic review and meta-analysis. Hum Reprod 2014, 29: 2190–2198. 10.1093/humrep/deu199CrossRefPubMed
21.
go back to reference Lee DY, Young KN, Jae KM, Yoon BK, Choi D: Effects of laparoscopic surgery on serum anti-Mullerian hormone levels in reproductive-aged women with endometrioma. Gynecol Endocrinol 2011,27(10):733–736. 10.3109/09513590.2010.538098CrossRefPubMed Lee DY, Young KN, Jae KM, Yoon BK, Choi D: Effects of laparoscopic surgery on serum anti-Mullerian hormone levels in reproductive-aged women with endometrioma. Gynecol Endocrinol 2011,27(10):733–736. 10.3109/09513590.2010.538098CrossRefPubMed
22.
go back to reference Celik HG, Dogan E, Okyay E, Ulukus C, Saatli B, Uysal S, Koyuncuoglu M: Effect of laparoscopic excision of endometriomas on ovarian reserve: serial changes in the serum antimullerian hormone levels. Fertil Steril 2012,97(6):1472–1478. 10.1016/j.fertnstert.2012.03.027CrossRefPubMed Celik HG, Dogan E, Okyay E, Ulukus C, Saatli B, Uysal S, Koyuncuoglu M: Effect of laparoscopic excision of endometriomas on ovarian reserve: serial changes in the serum antimullerian hormone levels. Fertil Steril 2012,97(6):1472–1478. 10.1016/j.fertnstert.2012.03.027CrossRefPubMed
23.
go back to reference Tsolakidis D, Pados G, Vavilis D, Athanatos D, Tsalikis T, Giannakou A, Tarlatzis BC: 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(1):71–77. 10.1016/j.fertnstert.2009.01.138CrossRefPubMed Tsolakidis D, Pados G, Vavilis D, Athanatos D, Tsalikis T, Giannakou A, Tarlatzis BC: 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(1):71–77. 10.1016/j.fertnstert.2009.01.138CrossRefPubMed
24.
go back to reference Durlinger AL, Visser JA, Themmen AP: Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 2002,124(5):601–609. 10.1530/rep.0.1240601CrossRefPubMed Durlinger AL, Visser JA, Themmen AP: Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 2002,124(5):601–609. 10.1530/rep.0.1240601CrossRefPubMed
25.
go back to reference Nelson SM, Anderson RA, Broekmans FJ, Raine-Fenning N, Fleming R, La Marca A: Anti-Mullerian hormone: clairvoyance or crystal clear? Hum Reprod 2012,27(3):631–636. 10.1093/humrep/der446CrossRefPubMed Nelson SM, Anderson RA, Broekmans FJ, Raine-Fenning N, Fleming R, La Marca A: Anti-Mullerian hormone: clairvoyance or crystal clear? Hum Reprod 2012,27(3):631–636. 10.1093/humrep/der446CrossRefPubMed
26.
go back to reference Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM, Nagle CM, Doherty JA, Cushing-Haugen KL, Wicklund KG, Chang-Claude J, Hein R, Lurie G, Wilkens LR, Carney ME, Goodman MT, Moysich K, Kjaer SK, Hogdall E, Jensen A, Goode EL, Fridley BL, Larson MC, Schildkraut JM, Palmieri RT, Cramer DW, Terry KL, Vitonis AF, Titus LJ, Ziogas A, et al.: Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies. Lancet Oncol 2012,13(4):385–394. 10.1016/S1470-2045(11)70404-1PubMedCentralCrossRefPubMed Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM, Nagle CM, Doherty JA, Cushing-Haugen KL, Wicklund KG, Chang-Claude J, Hein R, Lurie G, Wilkens LR, Carney ME, Goodman MT, Moysich K, Kjaer SK, Hogdall E, Jensen A, Goode EL, Fridley BL, Larson MC, Schildkraut JM, Palmieri RT, Cramer DW, Terry KL, Vitonis AF, Titus LJ, Ziogas A, et al.: Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies. Lancet Oncol 2012,13(4):385–394. 10.1016/S1470-2045(11)70404-1PubMedCentralCrossRefPubMed
27.
go back to reference Nargund G, Parsons J: Infected endometriotic cysts secondary to oocyte aspiration for in-vitro fertilization. Hum Reprod 1995,10(6):1555. 10.1093/HUMREP/10.6.1555-aCrossRefPubMed Nargund G, Parsons J: Infected endometriotic cysts secondary to oocyte aspiration for in-vitro fertilization. Hum Reprod 1995,10(6):1555. 10.1093/HUMREP/10.6.1555-aCrossRefPubMed
28.
go back to reference Kitajima M, Khan KN, Hiraki K, Inoue T, Fujishita A, Masuzaki H: Changes in serum anti-Mullerian hormone levels may predict damage to residual normal ovarian tissue after laparoscopic surgery for women with ovarian endometrioma. Fertil Steril 2011,95(8):2589–2591. 10.1016/j.fertnstert.2011.01.036CrossRefPubMed Kitajima M, Khan KN, Hiraki K, Inoue T, Fujishita A, Masuzaki H: Changes in serum anti-Mullerian hormone levels may predict damage to residual normal ovarian tissue after laparoscopic surgery for women with ovarian endometrioma. Fertil Steril 2011,95(8):2589–2591. 10.1016/j.fertnstert.2011.01.036CrossRefPubMed
Metadata
Title
The impact of endometrioma and laparoscopic cystectomy on ovarian reserve and the exploration of related factors assessed by serum anti-Mullerian hormone: a prospective cohort study
Authors
Yuqing Chen
Huihui Pei
Yajie Chang
Minghui Chen
Haihe Wang
Hongzhe Xie
Shuzhong Yao
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2014
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/s13048-014-0108-0

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