Angiogenesis, Inflammation & Therapeutics | Online ISSN  2207-872X
RESEARCH ARTICLE   (Open Access)

Apoptotic Pathways and Anti-Müllerian Hormone affects the Ovarian Tissue Damage during Endometrioma Cystectomy

Tanzil al Hair1*, Wachyu Hadisaputra2*, Soegiharto Soebijanto3*, Primariadewi Rustamadji4

+ Author Affiliations

Journal of Angiotherapy 8(5) 1-18 https://doi.org/10.25163/angiotherapy.859690

Submitted: 31 March 2024  Revised: 14 May 2024  Published: 20 May 2024 

Abstract

Background: Endometriomas are cysts caused by endometriosis that can impair ovarian function and fertility. Anti-Müllerian hormone (AMH) is an important marker for ovarian reserve. This study aimed to determine the optimal timing of operative management for endometrioma by evaluating the impact of cyst size on ovarian tissue damage and hormone levels. Methods: The study included 32 endometrioma patients who underwent laparoscopic cystectomy between February 2018 and December 2019 at Women and Children’s YPK Hospital, Jakarta. Patient characteristics were recorded, including age, parity, BMI, and cyst diameter. Serum AMH levels were measured using ELISA before and one month after cystectomy. Immunohistochemical examination assessed apoptotic factor gene expression on the inner surface epithelium of endometriomas. Results: AMH levels declined post-cystectomy in both endometriomas ≤4 cm and >4 cm, with significant differences in the latter group. Additionally, there was increased Bax expression in >4 cm endometriomas. Correlation tests revealed a strong positive relationship between TNFR1 and Caspase-3 in both groups. Multivariate analysis suggested a connection between apoptotic factor gene expression and reduced AMH levels. Conclusion: TNF-α appears to initiate apoptosis in endometriomas through the intrinsic pathway. It is advisable to perform endometrioma surgery when the diameter is ≤4 cm and before the age of 30 to achieve optimal outcomes.

Keywords: AMH, apoptosis, caspase-3, caspase-8, caspase-9, gene expression, endometrioma, intrinsic pathway, P53, Bcl-2/Bax ratio, cytokine TNF-α.

References

Abrao, Mauricio S., Ludovico Muzii, and Riccardo Marana. 2013. “International Journal of Gynecology and Obstetrics Anatomical Causes of Female Infertility and Their Management.” International Journal of Gynecology and Obstetrics 123:S18–24. doi: 10.1016/j.ijgo.2013.09.008.

Akhtar Muhammad, Kong Yusheng. 2021. Performance , and Profitability.

Alammari, Roa, Michelle Lightfoot, and Hye-Chun Hur. 2017. “Impact of Cystectomy on Ovarian Reserve: Review of the Literature.” Journal of Minimally Invasive Gynecology 24(2):247–57. doi: https://doi.org/10.1016/j.jmig.2016.12.010.

Andres, Marina de Paula. 2014. “Endometriosis Is an Important Cause of Pelvic Pain in Adolescence.” 60(6):560–64.

Baker, Valerie L., Clarisa Gracia, Michael J. Glassner, Vicki L. Schnell, Kevin Doody, Charles C. Coddington, Sanghyuk S. Shin, Lorna A. Marshall, Michael M. Alper, Arlene J. Morales, Mary Ellen Pavone, Millie A. Behera, Edward A. Zbella, Bruce S. Shapiro, Joely A. Straseski, and Dennis L. Broyles. 2018. “Multicenter Evaluation of the Access AMH Antimüllerian Hormone Assay for the Prediction of Antral Follicle Count and Poor Ovarian Response to Controlled Ovarian Stimulation.” Fertility and Sterility 110(3):506-513.e3. doi: https://doi.org/10.1016/j.fertnstert.2018.03.031.

Ballard, K. D., H. E. Seaman, C. S. De Vries, and J. T. Wright. 2008. “Can Symptomatology Help in the Diagnosis of Endometriosis? Findings from a National Case-Control Study - Part 1.” BJOG: An International Journal of Obstetrics and Gynaecology 115(11):1382–91. doi: 10.1111/j.1471-0528.2008.01878.x.

Barnhart, Kurt, Rebecca Dunsmoor-Su, and Christos Coutifaris. 2002. “Effect of Endometriosis on in Vitro Fertilization.” Fertility and Sterility 77(6):1148–55. doi: https://doi.org/10.1016/S0015-0282(02)03112-6.

Bast, R. C. 2011. “Molecular Approaches to Personalizing Management of Ovarian Cancer.” Annals of Oncology 22:viii5–15. doi: https://doi.org/10.1093/annonc/mdr516.

Bateman, Alexis H., Edgar E. Blanco, and Yossi Sheffi. 2017. “Disclosing and Reporting Environmental Sustainability of Supply Chains.” Springer Series in Supply Chain Management 4:119–44. doi: 10.1007/978-3-319-29791-0_6.

Benagiano, Giuseppe, Felice Petraglia, Stephan Gordts, and Ivo Brosens. 2016. “A New Approach to the Management of Ovarian Endometrioma to Prevent Tissue Damage and Recurrence.” Reproductive BioMedicine Online 32(6):556–62. doi: 10.1016/j.rbmo.2016.03.001.

Briley, Shawn M., Susmita Jasti, Jennifer M. McCracken, Jessica E. Hornick, Barbara Fegley, Michele T. Pritchard, and Francesca E. Duncan. 2016. “Reproductive Age-Associated Fibrosis in the Stroma of the Mammalian Ovary.” Reproduction (Cambridge, England) 152(3):245–60. doi: 10.1530/REP-16-0129.

Brilhante, Aline Veras Morais, Kathiane Lustosa Augusto, Manuela Cavalcante Portela, Luiz Carlos Gabriele Sucupira, Luiz Adriano Freitas Oliveira, Ana Juariana Magalhães Veríssimo Pouchaim, Lívia Rocha Mesquita Nóbrega, Thaís Fontes de Magalhães, and Leonardo Robson Pinheiro Sobreira. 2017. “Endometriosis and Ovarian Cancer: An Integrative Review (Endometriosis and  Ovarian Cancer).” Asian Pacific Journal of Cancer Prevention?: APJCP 18(1):11–16. doi: 10.22034/APJCP.2017.18.1.11.

Brosens, I., P. Puttemans, Sy Gordts, R. Campo, S Gordts, and G. Benagiano. 2013. “Early Stage Management of Ovarian Endometrioma to Prevent Infertility.” FVV In OBGyn 5(4):309–14.

Brosens, Ivo, Stephan Gordts, Patrick Puttemans, and Giuseppe Benagiano. 2014. “Pathophysiology Proposed as the Basis for Modern Management of the Ovarian Endometrioma.” Reproductive BioMedicine Online 28(2):232–38. doi: 10.1016/j.rbmo.2013.09.024.

Brosens, Ivo, Patrick Puttemans, Rudi Campo, Stephan Gordts, and Karen Kinkel. 2004. “Diagnosis of Endometriosis: Pelvic Endoscopy and Imaging Techniques.” Best Practice & Research Clinical Obstetrics & Gynaecology 18(2):285–303. doi: https://doi.org/10.1016/j.bpobgyn.2004.03.002.

Busacca, Mauro, and Michele Vignali. 2009. “Endometrioma Excision and Ovarian Reserve: A Dangerous Relation.” Journal of Minimally Invasive Gynecology 16(2):142–48. doi: https://doi.org/10.1016/j.jmig.2008.12.013.

Canis, M., J. L. Pouly, S. Tamburro, G. Mage, A. Wattiez, and M. A. Bruhat. 2001. “Ovarian Response during IVF – Embryo Transfer Cycles after Laparoscopic Ovarian Cystectomy for Endometriotic Cysts of > 3 Cm in Diameter.” 16(12):2583–86.

Cardoso, Jéssica Vilarinho. 2020. “Epidemiological Profile of Women with Endometriosis?: A Retrospective Descriptive Study.” Revista Brasileira de Saúde Materno Infantil 20(4):1057–67.

Carnahan, Molly, Jennifer Fedor, Ashok Agarwal, and Sajal Gupta. 2013. “Ovarian Endometrioma: Guidelines for Selection of Cases for Surgical Treatment or Expectant Management.” Expert Review of Obstetrics and Gynecology 8(1):29–55. doi: 10.1586/eog.12.75.

Celik, Hale Goksever, Erbil Dogan, Emre Okyay, Cagnur Ulukus, Bahadir Saatli, Sezer Uysal, and Meral Koyuncuoglu. 2012. “Effect of Laparoscopic Excision of Endometriomas on Ovarian Reserve: Serial Changes in the Serum Antimüllerian Hormone Levels.” Fertility and Sterility 97(6):1472–78. doi: https://doi.org/10.1016/j.fertnstert.2012.03.027.

Chen, Yuqing, Huihui Pei, Yajie Chang, Minghui Chen, Haihe Wang, Hongzhe Xie, and Shuzhong Yao. 2014. “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.” 1–8. doi: 10.1186/s13048-014-0108-0.

Chiu, Chui-Ching, Teh-Fu Hsu, Ling-Yu Jiang, I. San Chan, Ying-Chu Shih, Yen-Hou Chang, Peng-Hui Wang, and Yi-Jen Chen. 2022. “Maintenance Therapy for Preventing Endometrioma Recurrence after Endometriosis Resection Surgery – A Systematic Review and Network Meta-Analysis.” Journal of Minimally Invasive Gynecology 29(5):602–12. doi: https://doi.org/10.1016/j.jmig.2021.11.024.

Coccia, Maria Elisabetta, Francesca Rizzello, Stefano Barone, Sara Pinelli, Erika Rapalini, Cristiana Parri, Domenico Caracciolo, Savvas Papageorgiou, Gianpaolo Cima, and Loredana Gandini. 2014. “Is There a Critical Endometrioma Size Associated with Reduced Ovarian  Responsiveness in Assisted Reproduction Techniques?” Reproductive Biomedicine Online 29(2):259–66. doi: 10.1016/j.rbmo.2014.04.019.

Davies, Melanie J., Caroline A. Kristunas, Abualbishr Alshreef, Simon Dixon, Helen Eborall, Agnieszka Glab, Lisa Huddlestone, Nicky Hudson, Kamlesh Khunti, Graham Martin, Alison Northern, Mike Patterson, Rebecca Pritchard, Sally Schreder, Bernie Stribling, Jessica Turner, and Laura J. Gray. 2019. “The Impact of an Intervention to Increase Uptake to Structured Self-Management Education for People with Type 2 Diabetes Mellitus in Primary Care (the Embedding Package), Compared to Usual Care, on Glycaemic Control: Study Protocol for a Mixed Methods Stu.” BMC Family Practice 20(1):152. doi: 10.1186/s12875-019-1038-0.

Depalo, Raffaella, Aldo Cavallini, Filomenamila Lorusso, Emma Bassi, Ilaria Totaro, and Andrea Marzullo. 2009. “Article Apoptosis in Normal Ovaries of Women with and without Endometriosis.” Reproductive BioMedicine Online 19(6):808–15. doi: 10.1016/j.rbmo.2009.09.024.

Dufournet, Charlotte, Catherine Uzan, Raffaèle Fauvet, Annie Cortez, Jean-Pierre Siffroi, and Emile Daraï. 2006. “Expression of Apoptosis-Related Proteins in Peritoneal, Ovarian and Colorectal Endometriosis.” Journal of Reproductive Immunology 70(1):151–62. doi: https://doi.org/10.1016/j.jri.2005.11.003.

Fassbender, Amelie, Richard O. Burney, Dorien F. O, Thomas D’Hooghe, and Linda Giudice. 2015. “Update on Biomarkers for the Detection of Endometriosis-Protein and Contraction.” BioMed Research International 2015.

Fauvet, Raffaèle, Charlotte Dufournet, Christophe Poncelet, Catherine Uzan, Danièle Hugol, and Emile Daraï. 2005. “Expression of Pro-Apoptotic (P53, P21, Bax, Bak and Fas) and Anti-Apoptotic (Bcl-2 and Bcl-x) Proteins in Serous versus Mucinous Borderline Ovarian Tumours.” Journal of Surgical Oncology 92(4):337–43. doi: https://doi.org/10.1002/jso.20424.

Feng, Guohua, Jiti Gao, and Bin Peng. 2019. “An Integrated Panel Data Approach to Modelling Economic Growth.”

Foti, Pietro Valerio, Renato Farina, Stefano Palmucci, Ilenia Anna, Agata Vizzini, Norma Libertini, Maria Coronella, Saveria Spadola, Rosario Caltabiano, Marco Iraci, Antonio Basile, Pietro Milone, Antonio Cianci, and Giovanni Carlo Ettorre. 2018. “Endometriosis?: Clinical Features , MR Imaging Findings and Pathologic Correlation.” 149–72.

Garcia-Velasco, Juan A., and Edgardo Somigliana. 2009. “Management of Endometriomas in Women Requiring IVF: To Touch or Not to Touch.” Human Reproduction (Oxford, England) 24(3):496–501. doi: 10.1093/humrep/den398.

Gardner, David K. 2011. Human Assisted Reproductive Technology.

Giacomini, Elisa, Ana M. Sanchez, Veronica Sarais, Soha Al Beitawi, Massimo Candiani, and Paola Viganò. 2017. “Characteristics of Follicular Fluid in Ovaries with Endometriomas.” European Journal of Obstetrics, Gynecology, and Reproductive Biology 209:34–38. doi: 10.1016/j.ejogrb.2016.01.032.

Gordts, Stephan, Philippe Koninckx, and Ivo Brosens. 2017. “Pathogenesis of Deep Endometriosis.” Fertility and Sterility 108(6):872-885.e1. doi: https://doi.org/10.1016/j.fertnstert.2017.08.036.

Gordts, Stephan, Patrick Puttemans, Sylvie Gordts, and Ivo Brosens. 2015. “Ovarian Endometrioma in the Adolescent: A Plea for Early-Stage Diagnosis and Full Surgical Treatment.” Gynecological Surgery 12(1):21–30. doi: 10.1007/s10397-014-0877-x.

Gupta, Sajal, Jeffrey M. Goldberg, Nabil Aziz, Eric Goldberg, Natalie Krajcir, and Ashok Agarwal. 2008. “Pathogenic Mechanisms in Endometriosis-Associated Infertility.” Fertility and Sterility 90(2):247–57. doi: https://doi.org/10.1016/j.fertnstert.2008.02.093.

Haupt, Susan, Michael Berger, Zehavit Goldberg, and Ygal Haupt. 2003. “Apoptosis – the P53 Network.” doi: 10.1242/jcs.00739.

Heca, Cancer Cell Line, Meryem I. Karagül, Derya Yetkin, Gülsen Bayrak, and Didem Çelikcan. 2018. “P53 , Bcl2 and Bax Expression and Apoptosis in Perifosine and Vitamin D-Treated Endometrial.” 25:3–7. doi: 10.3390/proceedings2251564.

Henes, Melanie, and Engler. 2018. “Ovarian Cyst Removal Influences Ovarian Reserve Dependent on Histology, Size and Type of Operation.” Women’s Health 14:1745506518778992. doi: 10.1177/1745506518778992.

Hwu, Yuh-ming, Frank Shao-ying Wu, Sheng-hsiang Li, Fang-ju Sun, Ming-huei Lin, and Robert Kuo-kuang Lee. 2011. “The Impact of Endometrioma and Laparoscopic Cystectomy on Serum Anti-Müllerian Hormone Levels.” Reproductive Biology and Endocrinology 9(1):80. doi: 10.1186/1477-7827-9-80.

Isono, Wataru, Osamu Wada-Hiraike, Nana Akino, Hiromi Terao, Miyuki Harada, Tetsuya Hirata, Yasushi Hirota, Kaori Koga, Tomoyuki Fujii, and Yutaka Osuga. 2019. “The Efficacy of Non-Assisted Reproductive Technology Treatment Might Be Limited in Infertile Patients with Advanced Endometriosis in Their 30s.” Journal of Obstetrics and Gynaecology Research 45(2):368–75. doi: 10.1111/jog.13826.

Iwase, Akira, Wakana Hirokawa, Maki Goto, Sachiko Takikawa, Yoshinari Nagatomo, Tatsuo Nakahara, Shuichi Manabe, and Fumitaka Kikkawa. 2010. “Serum Anti-Müllerian Hormone Level Is a Useful Marker for Evaluating the Impact of Laparoscopic Cystectomy on Ovarian Reserve.” Fertility and Sterility 94(7):2846–49. doi: https://doi.org/10.1016/j.fertnstert.2010.06.010.

Keyhan, Sanaz, Claude Hughes, Thomas Price, and Suheil Muasher. 2015. “An Update on Surgical versus Expectant Management of Ovarian Endometriomas in Infertile Women.” 2015. doi: 10.1155/2015/204792.

Khan, Khaleque Newaz, Michio Kitajima, Akira Fujishita, Koichi Hiraki, Ayumi Matsumoto, Masahiro Nakashima, and Hideaki Masuzaki. 2013. “Pelvic Pain in Women with Ovarian Endometrioma Is Mostly Associated with Coexisting Peritoneal Lesions.” Human Reproduction 28(1):109–18. doi: 10.1093/humrep/des364.

Kitajima, Michio, Sylvie Defrère, Marie-Madeleine Dolmans, Sebastien Colette, Jean Squifflet, Anne Van Langendonckt, and Jacques Donnez. 2011. “Endometriomas as a Possible Cause of Reduced Ovarian Reserve in Women with Endometriosis.” Fertility and Sterility 96(3):685–91. doi: https://doi.org/10.1016/j.fertnstert.2011.06.064.

Kitajima, Michio, D. Ph, Marie-madeleine Dolmans, D. Ph, Olivier Donnez, and D. Ph. 2014. “Enhanced Follicular Recruitment and Atresia in Cortex Derived from Ovaries with Endometriomas.” Fertility and Sterility 101(4):1031–37. doi: 10.1016/j.fertnstert.2013.12.049.

Koninckx, Philippe R., Rodrigo Fernandes, Anastasia Ussia, Larissa Schindler, Arnaud Wattiez, Shaima Al-Suwaidi, Bedayah Amro, Basma Al-Maamari, Zeinab Hakim, and Muna Tahlak. 2021. “Pathogenesis Based Diagnosis and Treatment of Endometriosis.” Frontiers in Endocrinology 12(November):1–13. doi: 10.3389/fendo.2021.745548.

Korkmaz, D., E. Bastu, O. Dural, C. Yasa, E. Yavuz, and F. Buyru. 2013. “Apoptosis through Regulation of Bcl-2, Bax and Mcl-1 Expressions in Endometriotic Cyst Lesions and the Endometrium of Women with Moderate to Severe Endometriosis.” Journal of Obstetrics and Gynaecology 33(7):725–28. doi: 10.3109/01443615.2013.824416.

Lew, Raelia. 2019. “Natural History of Ovarian Function Including Assessment of Ovarian Reserve and Premature Ovarian Failure.” Best Practice and Research: Clinical Obstetrics and Gynaecology 55:2–13. doi: 10.1016/j.bpobgyn.2018.05.005.

Margarida. 2017. “Endometrioma Em Contexto de Infertilidade.” Angewandte Chemie International Edition, 6(11), 951–952. 5–24.

Matsuzaki, Sachiko. 2010. “Oxidative Stress Status in Normal Ovarian Cortex Surrounding Ovarian Endometriosis.” Fertility and Sterility 93(7):2431–32. doi: 10.1016/j.fertnstert.2009.08.068.

Miller, Emily M., Timothy M. Samec, and Angela A. Alexander-Bryant. 2021. “Nanoparticle Delivery Systems to Combat Drug Resistance in Ovarian Cancer.” Nanomedicine: Nanotechnology, Biology and Medicine 31:102309. doi: https://doi.org/10.1016/j.nano.2020.102309.

Molvig. 1988. “Endotoxin-Stimulated Human Monocyte Secretion of Interleukin 1, Tumour Necrosis Factor Alpha, and Prostaglandin E2 Shows Stable Interindividual Differences.” Scandinavian Journal of Immunology 27(6):705–16. doi: https://doi.org/10.1111/j.1365-3083.1988.tb02404.x.

Muzii, Ludovico, Antonella Bianchi, Filippo Bellati, Emanuela Cristi, Milena Pernice, Marzio A. Zullo, Roberto Angioli, and Pierluigi Benedetti Panici. 2007. “Histologic Analysis of Endometriomas: What the Surgeon Needs to Know.” Fertility and Sterility 87(2):362–66. doi: 10.1016/j.fertnstert.2006.06.055.

Nisolle, Michelle, and Jacques Donnez. 2019. “Reprint of: Peritoneal Endometriosis, Ovarian Endometriosis, and Adenomyotic Nodules of the Rectovaginal Septum Are Three Different Entities.” Fertility and Sterility 112(4):e125–36. doi: 10.1016/j.fertnstert.2019.08.081.

Obstet, Arch Gynecol, Francesca Maria Salmeri, Vaclav Vetvicka, and Antonio Simone. 2016. “Regulation of Apoptotic Pathways during Endometriosis?: From the Molecular Basis to the Future Perspectives.” doi: 10.1007/s00404-016-4195-6.

Parameswaran, Narayanan, and Sonika Patial. 2010. “Tumor Necrosis Factor-α Signaling in Macrophages.” Critical Reviews in Eukaryotic Gene Expression 20(2):87–103. doi: 10.1615/critreveukargeneexpr.v20.i2.10.

Parsa, Sepideh, Ian Roper, Michael Muller-Camen, and Eva Szigetvari. 2018. “Have Labour Practices and Human Rights Disclosures Enhanced Corporate Accountability? The Case of the GRI Framework.” Accounting Forum 42(1):47–64. doi: 10.1016/j.accfor.2018.01.001.

Pejovic, Tanja, Sarah Thisted, Michael White, and Farr R. Nezhat. 2020. “Endometriosis and Endometriosis-Associated Ovarian Cancer (EAOC) BT  - Hormonal Pathology of the Uterus.” Pp. 73–87 in, edited by L. Deligdisch-Schor and A. Mares Miceli. Cham: Springer International Publishing.

Porpora, M. G., P. R. Koninckx, J. Piazze, M. Natili, S. Colagrande, and E. V Cosmi. 1999. “Correlation between Endometriosis and Pelvic Pain.” The Journal of the American Association of Gynecologic Laparoscopists 6(4):429–34. doi: https://doi.org/10.1016/S1074-3804(99)80006-1.

Raffi, F., R. W. Shaw, and S. A. Amer. 2012. “National Survey of the Current Management of Endometriomas in Women Undergoing Assisted Reproductive Treatment.” Human Reproduction 27(9):2712–19. doi: 10.1093/humrep/des195.

Rosen, Mitchell P., Erica Johnstone, Charles E. McCulloch, Sonya M. Schuh-Huerta, Barbara Sternfeld, Renee A. Reijo-Pera, and Marcelle I. Cedars. 2012. “A Characterization of the Relationship of Ovarian Reserve Markers with Age.” Fertility and Sterility 97(1):238–43. doi: https://doi.org/10.1016/j.fertnstert.2011.10.031.

Rumph, Jelonia T., Victoria R. Stephens, Anthony E. Archibong, Kevin G. Osteen, and Kaylon L. Bruner-Tran. 2020. “Environmental Endocrine Disruptors and Endometriosis.” Advances in Anatomy, Embryology, and Cell Biology 232:57–78. doi: 10.1007/978-3-030-51856-1_4.

Salmeri, Francesca M., Vincenza Sofo, Antonio S. Lagana, Onofrio Triolo, Emanuele Sturlese, Giovanni Retto, Alfonsa Pizzo, Angela D. Ascola, and Salvatore Campo. 2015. “Behavior of Tumor Necrosis Factor- α and Tumor Necrosis Factor Receptor 1 / Tumor Necrosis Factor Receptor 2 System in Mononuclear Cells Recovered From Peritoneal Fluid of Women With Endometriosis at Different Stages.” Reproductive Sciences 22(2):165–72. doi: 10.1177/1933719114536472.

Sanchez, A. M., P. Viganò, E. Somigliana, P. Panina-Bordignon, P. Vercellini, and M. Candiani. 2014. “The Distinguishing Cellular and Molecular Features of the Endometriotic Ovarian Cyst: From Pathophysiology to the Potential Endometrioma-Mediated Damage to the Ovary.” Human Reproduction Update 20(2):217–30. doi: 10.1093/humupd/dmt053.

Scutiero, Gennaro, Piergiorgio Iannone, Giulia Bernardi, Gloria Bonaccorsi, Savino Spadaro, Carlo Alberto Volta, Pantaleo Greco, and Luigi Nappi. 2017. “Oxidative Stress and Endometriosis: A Systematic Review of the Literature” edited by V. M. Victor. Oxidative Medicine and Cellular Longevity 2017:7265238. doi: 10.1155/2017/7265238.

Seifer, David B., Valerie L. Baker, and Benjamin Leader. 2011. “Age-Specific Serum Anti-Müllerian Hormone Values for 17,120 Women Presenting to Fertility Centers within the United States.” Fertility and Sterility 95(2):747–50. doi: https://doi.org/10.1016/j.fertnstert.2010.10.011.

Shi, Jinghua, Jinhua Leng, Quancai Cui, and Jinghe Lang. 2011. “Follicle Loss after Laparoscopic Treatment of Ovarian Endometriotic Cysts.” International Journal of Gynecology & Obstetrics 115(3):277–81. doi: https://doi.org/10.1016/j.ijgo.2011.07.026.

Sipak-Szmigiel, Olimpia, Piotr Wlodarski, Elzbieta Ronin-Walknowska, Andrzej Niedzielski, Beata Karakiewicz, Sylwia Sluczanowska-Glabowska, Maria Laszczynska, and Witold Malinowski. 2017. “Serum and Peritoneal Fluid Concentrations of Soluble Human Leukocyte Antigen, Tumor Necrosis Factor Alpha and Interleukin 10 in Patients with Selected Ovarian Pathologies.” Journal of Ovarian Research 10(1):1–14. doi: 10.1186/s13048-017-0320-9.

Somigliana, Edgardo, Nicola Berlanda, Laura Benaglia, Paola Viganò, Paolo Vercellini, and Luigi Fedele. 2012. “Surgical Excision of Endometriomas and Ovarian Reserve: A Systematic Review on Serum Antimüllerian Hormone Level Modifications.” Fertility and Sterility 98(6):1531–38. doi: https://doi.org/10.1016/j.fertnstert.2012.08.009.

Sugita, Atsuko, Akira Iwase, Maki Goto, Tatsuo Nakahara, Tomoko Nakamura, Mika Kondo, Satoko Osuka, Masahiko Mori, Ai Saito, and Fumitaka Kikkawa. 2013. “One-Year Follow-up of Serum Antimüllerian Hormone Levels in Patients with Cystectomy: Are Different Sequential Changes Due to Different Mechanisms Causing Damage to the Ovarian Reserve?” Fertility and Sterility 100(2):516-522.e3. doi: https://doi.org/10.1016/j.fertnstert.2013.03.032.

Uncu, Gurkan, Isil Kasapoglu, Kemal Ozerkan, Ayse Seyhan, Arzu Oral Yilmaztepe, and Baris Ata. 2013. “Prospective Assessment of the Impact of Endometriomas and Their Removal on Ovarian Reserve and Determinants of the Rate of Decline in Ovarian Reserve†.” Human Reproduction 28(8):2140–45. doi: 10.1093/humrep/det123.

Vercellini, Paolo, Paola Viganò, Laura Buggio, Sofia Makieva, Giovanna Scarfone, Fulvia Milena Cribiù, Fabio Parazzini, and Edgardo Somigliana. 2018. “Perimenopausal Management of Ovarian Endometriosis and Associated Cancer Risk: When Is Medical or Surgical Treatment Indicated?” Best Practice & Research Clinical Obstetrics & Gynaecology 51:151–68. doi: https://doi.org/10.1016/j.bpobgyn.2018.01.017.

Vercellini, Paolo, Paola Viganò, Edgardo Somigliana, and Luigi Fedele. 2014. “Endometriosis?: Pathogenesis and Treatment.” 10(May). doi: 10.1038/nrendo.2013.255.

WHO. 2023. “Endometriosis.” WHO. Retrieved (https://www.who.int/news-room/fact-sheets/detail/endometriosis).

Yeung, Patrick, Ken Sinervo, Wendy Winer, and Robert B. Albee. 2011. “Complete Laparoscopic Excision of Endometriosis in Teenagers: Is Postoperative Hormonal Suppression Necessary?” Fertility and Sterility 95(6):1909-1912.e1. doi: https://doi.org/10.1016/j.fertnstert.2011.02.037.

Zikargae, Mekonnen Hailemariam. 2018. “Analysis of Environmental Communication and Its Implication for Sustainable Development in Ethiopia.” Science of the Total Environment 634:1593–1600. doi: 10.1016/j.scitotenv.2018.04.050.

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