Age-related trends in anti-Mullerian hormone serum level in women with unilateral and bilateral ovarian endometriomas prior to surgery

Reproductive Biology and Endocrinology

Robert Jach¹  Artur Ludwin⁴  Grzegorz Juszczyk²  Oliwia Grabowska⁵  Tomasz Banas⁴  Kazimierz Pitynski⁴  Iwona Hajdyla-Banas³  Dorota Nieweglowska⁴ 

[1] Department of Gynecological Endocrinology, Jagiellonian University Medical College, Krakow, Poland;Department of Public Health, Medical University of Warsaw, Warsaw, Poland;Center of Rheumatology, Immunology and Rehabilitation, Dietl Specialistic Hospital, Krakow, Poland;Department of Gynecology and Oncology, Jagiellonian University, Chair of Gynecology and Obstetrics, Krakow, 21 Kopernika Str, Krakow, 30-501, Poland;Nuffield Division of Clinical Laboratory Science, University of Oxford, Level 4, John Radcliffe Hospital, Headington, Oxford, OX3 9DU, UK

关键词: Endometriosis;    Ovarian endometrioma;    AMH;    Anti-Mullerian hormone;   

Others  :  1234164
DOI  :  10.1186/s12958-015-0125-x

 received in 2015-09-16, accepted in 2015-11-17,  发布年份 2015

【 摘 要 】

Background

Endometriosis is a well-known cause of infertility, and the anti-Mullerian hormone (AMH) is an accepted biomarker of ovarian reserve and response to artificial reproductive technology procedures. The present study was a prospective analysis of age-dependent AMH serum concentration in women with bilateral and unilateral ovarian endometriomas before therapy onset compared with healthy controls.

Methods

This prospective cross-sectional study included 384 women aged 18–48 years. AMH serum concentration was assessed between days 3 and 6 of the menstrual cycle in 78 patients with bilateral and 157 patients with unilateral ovarian endometriomas and compared with 149 healthy controls. Ovarian endometriosis was confirmed histopathologically, and data were presented as medians with interquartile range (IQR).

Results

Stage III endometriosis was diagnosed in 53.2 %, stage IV in 18.3 %, stage V in 23.4 % and stage VI in 5.4 % of the patients. Patients with bilateral ovarian endometriomas showed the lowest median AMH levels compared with patients suffering from unilateral ovarian endometriosis (0.55; IQR: 0.59 vs. 2.00; IQR: 2.80; p < 0.001) and the control group (0.55; IQR: 0.59 vs. 2.84; IQR: 3.2; p < 0.001). Median AMH concentration values were not significantly different between patients with unilateral ovarian endometriosis and the healthy controls (2.00; IQR: 2.80 vs. 2.84; IQR: 3.2; p = 0.182). A strongly negative correlation between AMH levels and age was confirmed in healthy individuals (R = −0.834; p < 0.001) and women with unilateral ovarian endometriomas (R = −0.774; p < 0.001). Patients with bilateral ovarian endometriosis showed a significantly negative but only moderate correlation between AMH levels and age (R = −0.633; p < 0.001), which was significantly lower than in the healthy controls (R = −0.633 vs. R = −0.834; p = 0.006) but not in the patients with unilateral ovarian endometriosis (R = −0.663 vs. R-0.774; p = 0.093). Based on a multivariate regression analysis, only bilateral localization of ovarian endometrial cysts (p = 0.003) and patient age (p < 0.001), but not left/right localization of unilateral cyst or cyst volume, were negatively associated with AMH serum concentration.

Conclusion

According to our data, unilateral ovarian endometriosis had a moderately negative and nonsignificant effect on AMH-based ovarian reserve evaluated prior to surgery, irrespective of age. In contrast, the ovarian reserve was significantly reduced in women with bilateral ovarian endometriomas.

【 授权许可】

   
2015 Nieweglowska et al.

【 图 表 】

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【 参考文献 】

• [1]Thoma ME, McLain AC, Louis JF, King RB, Trumble AC, Sundaram R et al.. Prevalence of infertility in the United States as estimated by the current duration approach and a traditional constructed approach. Fertil Steril. 2013; 99:1324-31.
• [2]Tarín JJ, García-Pérez MA, Hamatani T, Cano A. Infertility etiologies are genetically and clinically linked with other diseases in single meta-diseases. Reprod Biol Endocrinol. 2015; 13:31. BioMed Central Full Text
• [3]Giudice LC. Clinical practice. Endometriosis N Engl JMed. 2010; 362:2389-98.
• [4]Ozkan S, Murk W, Arici A. Endometriosis and infertility: epidemiology and evidence-based treatments. Ann N Y Acad Sci. 2008; 1127:92-100.
• [5]Bulletti C, Coccia ME, Battistoni S, Borini A. Endometriosis and infertility. Assist Reprod Genet. 2010; 27:441-7.
• [6]Haydardedeoglu B, Zeyneloglu HB. The impact of endometriosis on fertility. Womens Health (Lond Engl). 2015. doi:10.2217/whe.15.48.
• [7]Hughesdon PE. The structure of endometrial cysts of the ovary. J Obstet Gynaecol Br Emp. 1957; 64:481-7.
• [8]Sanchez AM, Viganò P, Somigliana E, Panina-Bordignon P, Vercellini P, Candiani M. The distinguishing cellular and molecular features of the endometriotic ovarian cyst: from pathophysiology to the potential endometrioma-mediated damage to the ovary. Hum Reprod Update. 2014; 20:217-30.
• [9]Matsuzaki S, Schubert B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertil Steril. 2010; 93:2431-2.
• [10]Csanyi G, Yao M, Rodriguez AI, Al Ghouleh I, Sharifi-Sanjani M, Frazziano G et al.. Thrombospondin-1 regulates blood flow via CD47 receptor-mediated activation of NADPH oxidase 1. Arterioscler Thromb Vasc Biol. 2012; 32:2966-73.
• [11]Hock DL, Sharafi K, Dagostino L, Kemmann E, Seifer DB. Contribution of diminished ovarian reserve to hypofertility associated with endometriosis. J Reprod Med. 2001; 46:7-10.
• [12]Shebl O, Ebner T, Sommergruber M, Sir A, Tews G. Anti Muellerian hormone serum levels in women with endometriosis: a case–control study. Gynecol Endocrinol. 2009; 25:713-6.
• [13]Wahd SA, Alalaf SK, Al-Shawaf T, Al-Tawil NG. Ovarian reserve markers and assisted reproductive technique (ART) outcomes in women with advanced endometriosis. Reprod Biol Endocrinol. 2014; 12:120. BioMed Central Full Text
• [14]Ledger WL. Clinical utility of measurement of anti-mullerian hormone in reproductive endocrinology. J Clin Endocrinol Metab. 2010; 95:5144-54.
• [15]Fridén B, Sjöblom P, Menezes J. Using anti-Müllerian hormone to identify a good prognosis group in women of advanced reproductive age. Aust N Z J Obstet Gynaecol. 2011; 51:411-5.
• [16]Pepinsky RB, Sinclair LK, Chow EP, Mattaliano RJ, Manganaro TF, Donahoe PK et al.. Proteolytic processing of Mullerian inhibiting substance produces a transforming growth factor-b-like fragment. J Biol Chem. 1988; 263:18961-4.
• [17]La Marca A, Volpe A. Anti-Müllerian hormone (AMH) in female reproduction: is measurement of circulating AMH a useful tool? Clin Endocrinol. 2006; 64:603-10.
• [18]Sadeu JC, Adriaenssens T, Smitz J. Expression of growth differentiation factor 9, bone morphogenetic protein 15, and anti-Mullerian hormone in cultured mouse primary follicles. Reproduction. 2008; 136:195-203.
• [19]de Vet A, Laven JS, de Jong FH, Themmen AP, Fauser BC. Antimu¨ llerian hormone serum levels: a putative marker for ovarian aging. Fertil Steril. 2002; 77:357-62.
• [20]Lee MM, Donahoe PK, Hasegawa T, Silverman B, Crist GB, Best S et al.. Mullerian inhibiting substance in humans: normal levels from infancy to adulthood. J Clin Endocrinol Metab. 1996; 81:571-6.
• [21]La Marca A, Stabile G, Artenisio AC, Volpe A. Serum anti-Mullerian hormone throughout the human menstrual cycle. Hum Reprod. 2006; 21:3103-7.
• [22]La Marca A, Broekmans FJ, Volpe A, Fauser BC, Macklon NS. ESHRE special interest group for reproductive endocrinology–AMH round table. Anti-Mullerian hormone (AMH): what do we still need to know? Hum Reprod. 2009; 24:2264-75.
• [23]Köninger A, Kauth A, Schmidt B, Schmidt M, Yerlikaya G, Kasimir-Bauer S et al.. Anti-Mullerian-hormone levels during pregnancy and postpartum. Reprod Biol Endocrinol. 2013; 11:60. BioMed Central Full Text
• [24]Köninger A, Schmidt B, Mach P, Damaske D, Nießen S, Kimmig R et al.. Anti-Mullerian-hormone during pregnancy and peripartum using the new Beckman Coulter AMH Gen II assay. Reprod Biol Endocrinol. 2015; 13:86. BioMed Central Full Text
• [25]Hadlow N, Longhurst K, McClements A, Natalwala J, Brown SJ, Matson PL. Variation in antimüllerian hormone concentration during the menstrual cycle may change the clinical classification of the ovarian response. Fertil Steril. 2013; 99:1791-7.
• [26]Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D’Hooghe T, De Bie B et al.. ESHRE guideline: management of women with endometriosis. Hum Reprod. 2014; 29:400-12.
• [27]Shebl O, Ebner T, Sir A, Schreier-Lechner E, Mayer RB, Tews G et al.. Age-related distribution of basal serum AMH level in women of reproductive age and a presumably healthy cohort. Fertil Steril. 2011; 95:832-4.
• [28]Wiweko B, Prawesti DM, Hestiantoro A, Sumapraja K, Natadisastra M, Baziad A. Chronological age vs biological age: an age-related normogram for antral follicle count, FSH and anti-Mullerian hormone. J Assist Reprod Genet. 2013; 30:1563-7.
• [29]Nelson SM, Messow MC, Wallace AM, Fleming R, McConnachie A. Nomogram for the decline in serum antimüllerian hormone: a population study of 9,601 infertility patients. Fertil Steril. 2011; 95:736-41.
• [30]Nelson SM, Messow MC, McConnachie A, Wallace H, Kelsey T, Fleming R et al.. External validation of nomogram for the decline in serum anti-Müllerian hormone in women: a population study of 15,834 infertility patients. Reprod Biomed Online. 2011; 23:204-6.
• [31]Somigliana E, Marchese MA, Frattaruolo MP, Berlanda N, Fedele L, Vercellini P. Serum anti-mullerian hormone in reproductive aged women with benign ovarian cysts. Eur J Obstet Gynecol Reprod Biol. 2014; 180:142-7.
• [32]Chang HJ, Han SH, Lee JR, Jee BC, Lee BI, Suh CS et al.. Impact of laparoscopic cystectomy on ovarian reserve: serial changes of serum anti-Müllerian hormone levels. Fertil Steril. 2010; 94:343-9.
• [33]Uncu G, Kasapoglu I, Ozerkan K, Seyhan A, Oral Yilmaztepe A, Ata B. Prospective 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.
• [34]Kim JY, Jee BC, Suh CS, Kim SH. Preoperative serum anti-mullerian hormone level in women with ovarian endometrioma and mature cystic teratoma. Yonsei Med J. 2013; 54:921-6.
• [35]Lind T, Hammarström M, Lampic C, Rodriguez-Wallberg K. Anti-Müllerian hormone reduction after ovarian cyst surgery is dependent on the histological cyst type and preoperative anti-Müllerian hormone levels. Acta Obstet Gynecol Scand. 2015; 94:183-90.
• [36]Streuli I, de Ziegler D, Gayet V, Santulli P, Bijaoui G, de Mouzon J et al.. In women with endometriosis anti-Müllerian hormone levels are decreased only in those with previous endometrioma surgery. Hum Reprod. 2012; 27:3294-303.
• [37]Vignali M, Mabrouk M, Ciocca E, Alabiso G, Barbasetti di Prun A, Gentilini D, et al. Surgical excision of ovarian endometriomas: does it truly impair ovarian reserve? Long term anti-Müllerian hormone (AMH) changes after surgery. J Obstet Gynaecol Res. 2015. doi:10.1111/jog.12830
• [38]Angioni S, Pontis A, Cela V, Sedda F, Genazzani AD, Nappi L. Surgical technique of endometrioma excision impacts on the ovarian reserve. Single-port access laparoscopy versus multiport access laparoscopy: a case control study. Gynecol Endocrinol. 2015; 31:454-7.
• [39]Nappi L, Angioni S, Sorrentino F, Cinnella G, Lombardi M, Greco P. Anti-Mullerian hormone trend evaluation after laparoscopic surgery of monolateral endometrioma using a new dual wavelengths laser system (DWLS) for hemostasis. Gynecol Endocrinol. 2015.