A Narrative Review Regarding Implication of Ovarian Endometriomas in Infertility
Abstract
:1. Introduction
2. Epidemiology
3. Etiology
- 1.
- Retrograde menstruation is the most widely accepted explanation [19]. Sampson hypothesizes that viable cells from the peritoneal fluid derived from retrograde menstruation can engraft, proliferate, and invade the peritoneal cavity [20]. Cells released from the endometrium during menstruation include epithelial cells, stromal fibroblasts/decidual cells, vascular cells, and various immune cells [21,22].
- 2.
- Embryonic Müllerian remnants. This concept states that residual embryonic Müllerian migration cells retain the ability to grow into endometriotic lesions under the influence of estrogen, beginning around puberty or possibly in response to estrogen mimetics [12]. Epidemiologic studies indicate a twofold increased risk of endometriosis in women exposed to diethylstilbestrol in utero [23].
- 3.
- Genetic and epigenetic theory. Changes in the genetic regulatory networks have been found in the stromal cells of the endometrium [24]. Epigenetic alterations found in endometriosis include genomic DNA methylation [25]. In addition, aberrant DNA methylation in endometriosis induces the expression of many genes, including homeobox A10 (HOXA10), an estrogen beta receptor gene, a progesterone receptor, aromatase, HOXC6, and ALDH1A2 [26]. HOXA-10 is an important regulator of two essential processes during implantation: stromal cell proliferation and local immunosuppression [27].
- 4.
- Hematogenous and lymphatic spread. Another idea is that the menstrual tissue diffuses from the uterine cavity to distant areas via lymphatic vessels and veins, which explains the presence of implants outside the pelvis [28]. The blood contains endometrial cells derived from the endometrium. Microvascular studies revealed lymphatic movements from the uterine body to the ovary, indicating a possible involvement of the lymphatic system in the etiology of OEs [29].
- 5.
- Celomic metaplasia. Ferguson hypothesized that celomic metaplasia may play a role in the etiology of endometriosis. It is based on the hypothesis that the peritoneum harbors undifferentiated cells that can differentiate into endometriosis cells [5].
- 6.
- Neuroangiogenesis. Recent studies suggest that ectopic endometriotic implants attract a distinct neuronal and vascular supply via neuroangiogenesis. Endometriotic implants are complex multicellular structures characterized by vascularization that include the development of new blood vessels. It is postulated that the developing nerve fibers in the endometriotic implants influence dorsal root neurons in the central nervous system, thereby enhancing patients’ perception of pain [29,30].
- 7.
- Stem cell theory. Progenitor cells within the endometrium and multipotent cells from the osseous sinus contribute to the composition of the eutopic endometrium [32].
- 8.
- Induction theory. Experts believe that hormones or immunologic factors may promote the transformation of peritoneal cells lining the internal abdominal cavity into cells resembling those of the endometrium [33].
4. Infertility Related to OEs
5. Symptomatology
6. Diagnosis
6.1. Examination of the Pelvis
6.1.1. Physical Examination
6.1.2. Laboratory Tests
6.1.3. Imaging
6.1.4. Laparoscoy
6.1.5. Pathology
6.2. Differential Diagnosis
7. Complications
7.1. Risk to Fertility
7.2. Risk of Infection or Contamination During IVF Cycles
7.3. Risk of Egg Retrieval
7.4. Risk for Pregnancy
7.5. Risk of Disease Development During IVF Cycles
7.6. Other Complications
8. Treatment
8.1. Surgical Treatment
8.2. Medical Treatment
8.2.1. Suppression of Ovarian Function
8.2.2. Symptomatic Therapy
8.2.3. Other Medical Therapies
8.3. Other Alternative Treatments
8.3.1. Sclerotherapy Is a Non-Surgical Approach to the Treatment of OEs
8.3.2. Drainage of Cysts
9. Prognosis
10. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Audebert, A.; Petousis, S.; Margioula-Siarkou, C.; Ravanos, K.; Prapas, N.; Prapas, Y. Anatomic distribution of endometriosis: A reappraisal based on series of 1101 patients. Eur. J. Obstet. Gynecol. Reprod. Biol. 2018, 230, 36–40. [Google Scholar] [CrossRef]
- Vercellini, P.; Fedele, L.; Aimi, G.; Pietropaolo, G.; Consonni, D.; Crosignani, P.G. Association between endometriosis stage, lesion type, patient characteristics and severity of pelvic pain symptoms: A multivariate analysis of over 1000 patients. Hum. Reprod. 2007, 22, 266–271. [Google Scholar] [CrossRef] [PubMed]
- Working Group of ESGE, ESHRE and WES; Saridogan, E.; Becker, C.M.; Feki, A.; Grimbizis, G.F.; Hummelshoj, L.; Keckstein, J.; Nisolle, M.; Tanos, V.; Ulrich, U.A.; et al. Recommendations for the Surgical Treatment of Endometriosis. Part 1: Ovarian Endometrioma. Hum. Reprod. Open 2017, 2017, hox016. [Google Scholar] [CrossRef] [PubMed]
- Meggyesy, M.; Friese, M.; Gottschalk, J.; Kehler, U. Case Report of Cerebellar Endometriosis. J. Neurol. Surg. A Cent. Eur. Neurosurg. 2020, 81, 372–376. [Google Scholar] [CrossRef] [PubMed]
- Bulun, S.E. Endometriosis. N. Engl. J. Med. 2009, 360, 268–279. [Google Scholar] [CrossRef]
- International Working Group of AAGL, ESGE, ESHRE and WES; Tomassetti, C.; Johnson, N.P.; Petrozza, J.; Abrao, M.S.; Einarsson, J.I.; Horne, A.W.; Lee, T.T.M.; Missmer, S.; Vermeulen, N.; et al. An International Terminology for Endometriosis, 2021. Facts Views Vis. Obgyn 2021, 13, 295–304. [Google Scholar] [CrossRef]
- Exacoustos, C.; De Felice, G.; Pizzo, A.; Morosetti, G.; Lazzeri, L.; Centini, G.; Piccione, E.; Zupi, E. Isolated Ovarian Endometrioma: A History Between Myth and Reality. J. Minim. Invasive Gynecol. 2018, 25, 884–891. [Google Scholar] [CrossRef]
- Hwu, Y.M.; Wu, F.S.; Li, S.H.; Sun, F.J.; Lin, M.H.; Lee, R.K. The impact of endometrioma and laparoscopic cystectomy on serum anti-Müllerian hormone levels. Reprod. Biol. Endocrinol. 2011, 9, 80. [Google Scholar] [CrossRef]
- Vaduva, C.C.; Dira, L.; Carp-Veliscu, A.; Goganau, A.M.; Ofiteru, A.M.; Siminel, M.A. Ovarian reserve after treatment of ovarian endometrimas by ethanolic sclerotherapy compared to surgical treatment. Eur. Rev. Med. Pharmacol. Sci. 2023, 27, 5575–5582. [Google Scholar]
- Daniilidis, A.; Angioni, S.; Di Michele, S.; Dinas, K.; Gkrozou, F.; D’Alterio, M.N. Deep Endometriosis and Infertility: What Is the Impact of Surgery? J. Clin. Med. 2022, 11, 6727. [Google Scholar] [CrossRef]
- Barnhart, K.; Dunsmoor-Su, R.; Coutifaris, C. Effect of endometriosis on in vitro fertilization. Fertil. Steril. 2002, 77, 1148–1155. [Google Scholar] [CrossRef] [PubMed]
- Alborzi, S.; Zahiri Sorouri, Z.; Askari, E.; Poordast, T.; Chamanara, K. The success of various endometrioma treatments in infertility: A systematic review and meta-analysis of prospective studies. Reprod. Med. Biol. 2019, 18, 312–322. [Google Scholar] [CrossRef] [PubMed]
- Zondervan, K.T.; Becker, C.M.; Missmer, S.A. Endometriosis. N. Engl. J. Med. 2020, 382, 1244–1256. [Google Scholar] [CrossRef] [PubMed]
- Giudice, L.C.; Kao, L.C. Endometriosis. Lancet 2004, 364, 1789–1799. [Google Scholar] [CrossRef] [PubMed]
- Ballard, K.D.; Seaman, H.E.; de Vries, C.S.; Wright, J.T. Can symptomatology help in the diagnosis of endometriosis? Findings from a national case-control study—Part 1. BJOG 2008, 115, 1382–1391. [Google Scholar] [CrossRef]
- Missmer, S.A.; Hankinson, S.E.; Spiegelman, D.; Barbieri, R.L.; Malspeis, S.; Willett, W.C.; Hunter, D.J. Reproductive history and endometriosis among premenopausal women. Obstet. Gynecol. 2004, 104 Pt 1, 965–974. [Google Scholar] [CrossRef]
- Ozkan, S.; Murk, W.; Arici, A. Endometriosis and infertility: Epidemiology and evidence-based treatments. Ann. N. Y. Acad. Sci. 2008, 1127, 92–100. [Google Scholar] [CrossRef]
- Nouri, K.; Ott, J.; Krupitz, B.; Huber, J.C.; Wenzl, R. Family incidence of endometriosis in first-, second-, and third-degree relatives: Case-control study. Reprod. Biol. Endocrinol. 2010, 8, 85. [Google Scholar] [CrossRef]
- Bulun, S.E.; Yilmaz, B.D.; Sison, C.; Miyazaki, K.; Bernardi, L.; Liu, S.; Kohlmeier, A.; Yin, P.; Milad, M.; Wei, J. Endometriosis. Endocr. Rev. 2019, 40, 1048–1079. [Google Scholar] [CrossRef]
- Yovich, J.L.; Rowlands, P.K.; Lingham, S.; Sillender, M.; Srinivasan, S. Pathogenesis of endometriosis: Look no further than John Sampson. Reprod. Biomed. Online 2020, 40, 7–11. [Google Scholar] [CrossRef] [PubMed]
- Dorien, F.O.; Roskams, T.; Van den Eynde, K.; Vanhie, A.; Peterse, D.P.; Meuleman, C.; Tomassetti, C.; Peeraer, K.; D’Hooghe, T.M.; Fassbender, A. The Presence of Endometrial Cells in Peritoneal Fluid of Women with and Without Endometriosis. Reprod. Sci. 2017, 24, 242–251. [Google Scholar] [CrossRef] [PubMed]
- Armstrong, G.M.; Maybin, J.A.; Murray, A.A.; Nicol, M.; Walker, C.; Saunders, P.T.K.; Rossi, A.G.; Critchley, H.O.D. Endometrial apoptosis and neutrophil infiltration during menstruation exhibits spatial and temporal dynamics that are recapitulated in a mouse model. Sci. Rep. 2017, 7, 17416. [Google Scholar] [CrossRef] [PubMed]
- Missmer, S.A.; Hankinson, S.E.; Spiegelman, D.; Barbieri, R.L.; Michels, K.B.; Hunter, D.J. In utero exposures and the incidence of endometriosis. Fertil. Steril. 2004, 82, 1501–1508. [Google Scholar] [CrossRef]
- Dyson, M.T.; Roqueiro, D.; Monsivais, D.; Ercan, C.M.; Pavone, M.E.; Brooks, D.C.; Kakinuma, T.; Ono, M.; Jafari, N.; Dai, Y.; et al. Genome-wide DNA methylation analysis predicts an epigenetic switch for GATA factor expression in endometriosis. PLoS Genet. 2014, 10, e1004158. [Google Scholar] [CrossRef] [PubMed]
- Izawa, M.; Taniguchi, F.; Harada, T. GATA6 expression promoted by an active enhancer may become a molecular marker in endometriosis lesions. Am. J. Reprod. Immunol. 2019, 81, e13078. [Google Scholar] [CrossRef]
- Naqvi, H.; Ilagan, Y.; Krikun, G.; Taylor, H.S. Altered genome-wide methylation in endometriosis. Reprod. Sci. 2014, 21, 1237–1243. [Google Scholar] [CrossRef]
- Celik, O.; Unlu, C.; Otlu, B.; Celik, N.; Caliskan, E. Laparoscopic endometrioma resection increases peri-implantation endometrial HOXA-10 and HOXA-11 mRNA expression. Fertil. Steril. 2015, 104, 356–365. [Google Scholar] [CrossRef]
- Macer, M.L.; Taylor, H.S. Endometriosis and infertility: A review of the pathogenesis and treatment of endometriosis-associated infertility. Obstet. Gynecol. Clin. N. Am. 2012, 39, 535–549. [Google Scholar] [CrossRef]
- Burney, R.O.; Giudice, L.C. Pathogenesis and pathophysiology of endometriosis. Fertil. Steril. 2012, 98, 511–519. [Google Scholar] [CrossRef]
- Yu, J.; Francisco, A.M.C.; Patel, B.G.; Cline, J.M.; Zou, E.; Berga, S.L.; Taylor, R.N. IL-1β Stimulates Brain-Derived Neurotrophic Factor Production in Eutopic Endometriosis Stromal Cell Cultures: A Model for Cytokine Regulation of Neuroangiogenesis. Am. J. Pathol. 2018, 188, 2281–2292. [Google Scholar] [CrossRef]
- Nishida, M.; Nasu, K.; Narahara, H. Role of chemokines in the pathogenesis of endometriosis. Front. Biosci. (Schol. Ed.) 2011, 3, 1196–1204. [Google Scholar] [CrossRef] [PubMed]
- Bonavina, G.; Taylor, H.S. Endometriosis-associated infertility: From pathophysiology to tailored treatment. Front. Endocrinol. 2022, 13, 1020827. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Istrate-Ofiţeru, A.-M.; Mogoantă, C.A.; Zorilă, G.-L.; Roşu, G.-C.; Drăguşin, R.C.; Berbecaru, E.-I.; Zorilă, M.V.; Comănescu, C.M.; Mogoantă, S.; Vaduva, C.-C.; et al. Clinical Characteristics and Local Histopathological Modulators of Endometriosis and Its Progression. Int. J. Mol. Sci. 2024, 25, 1789. [Google Scholar] [CrossRef]
- Bourdel, N.; Alves, J.; Pickering, G.; Ramilo, I.; Roman, H.; Canis, M. Systematic review of endometriosis pain assessment: How to choose a scale? Hum. Reprod. Update 2015, 21, 136–152. [Google Scholar] [CrossRef]
- Garzon, S.; Laganà, A.S.; Barra, F.; Casarin, J.; Cromi, A.; Raffaelli, R.; Uccella, S.; Franchi, M.; Ghezzi, F.; Ferrero, S. Novel drug delivery methods for improving efficacy of endometriosis treatments. Expert Opin. Drug Deliv. 2021, 18, 355–367. [Google Scholar] [CrossRef] [PubMed]
- Rafique, S.; Decherney, A.H. Medical Management of Endometriosis. Clin. Obstet. Gynecol. 2017, 60, 485–496. [Google Scholar] [CrossRef]
- Schliep, K.; Chen, Z.; Stanford, J.; Xie, Y.; Mumford, S.; Hammoud, A.; Johnstone, E.B.; Dorais, J.; Varner, M.; Louis, G.B.; et al. Endometriosis diagnosis and staging by operating surgeon and expert review using multiple diagnostic tools: An inter-rater agreement study. BJOG 2017, 124, 220–229. [Google Scholar] [CrossRef]
- Tanbo, T.; Fedorcsak, P. Endometriosis-associated infertility: Aspects of pathophysiological mechanisms and treatment options. Acta Obstet. Gynecol. Scand. 2017, 96, 659–667. [Google Scholar] [CrossRef] [PubMed]
- Trinchant, R.; García-Velasco, J.A. Oocyte Quality in Women with Endometriosis. Gynecol. Obstet. Investig. 2024, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Somigliana, E.; Benaglia, L.; Paffoni, A.; Busnelli, A.; Vigano, P.; Vercellini, P. Risks of conservative management in women with ovarian endometriomas undergoing IVF. Hum. Reprod. Update 2015, 21, 486–499. [Google Scholar] [CrossRef] [PubMed]
- Matsuzaki, S.; Schubert, B. Oxidative stress status in normal ovarian cortex surrounding ovarian endometriosis. Fertil. Steril. 2010, 93, 2431–2432. [Google Scholar] [CrossRef] [PubMed]
- Sanchez, A.M.; 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, 217–230. [Google Scholar] [CrossRef]
- Takeuchi, A.; Koga, K.; Satake, E.; Makabe, T.; Taguchi, A.; Miyashita, M.; Takamura, M.; Harada, M.; Hirata, T.; Hirota, Y.; et al. Endometriosis Triggers Excessive Activation of Primordial Follicles via PI3K-PTEN-Akt-Foxo3 Pathway. J. Clin. Endocrinol. Metab. 2019, 104, 5547–5554. [Google Scholar] [CrossRef] [PubMed]
- Sanchez, A.M.; Somigliana, E.; Vercellini, P.; Pagliardini, L.; Candiani, M.; Vigano, P. Endometriosis as a detrimental condition for granulosa cell steroidogenesis and development: From molecular alterations to clinical impact. J. Steroid Biochem. Mol. Biol. 2016, 155 Pt A, 35–46. [Google Scholar] [CrossRef]
- Paffoni, A.; Bolis, V.; Ferrari, S.; Benaglia, L.; Vercellini, P.; Somigliana, E. The Gametotoxic Effects of the Endometrioma Content: Insights From a Parthenogenetic Human Model. Reprod. Sci. 2019, 26, 573–579. [Google Scholar] [CrossRef]
- Kitajima, M.; Defrère, S.; Dolmans, M.-M.; Colette, S.; Squifflet, J.; Van Langendonckt, A.; Donnez, J. Endometriomas as a possible cause of reduced ovarian reserve in women with endometriosis. Fertil. Steril. 2011, 96, 685–691. [Google Scholar] [CrossRef]
- Foti, P.V.; Farina, R.; Palmucci, S.; Vizzini, I.A.A.; Libertini, N.; Coronella, M.; Spadola, S.; Caltabiano, R.; Iraci, M.; Basile, A.; et al. Endometriosis: Clinical features, MR imaging findings and pathologic correlation. Insights Into Imaging 2018, 9, 149–172. [Google Scholar] [CrossRef]
- Hansen, K.E.; Kesmodel, U.S.; Baldursson, E.B.; Kold, M.; Forman, A. Visceral syndrome in endometriosis patients. Eur. J. Obstet. Gynecol. Reprod. Biol. 2014, 179, 198–203. [Google Scholar] [CrossRef]
- Koninckx, P.R.; Oosterlynck, D.; D’Hooghe, T.; Meuleman, C. Deeply infiltrating endometriosis is a disease whereas mild endometriosis could be considered a non-disease. Ann. N. Y. Acad. Sci. 1994, 734, 333–341. [Google Scholar] [CrossRef] [PubMed]
- Fauconnier, A.; Chapron, C. Endometriosis and pelvic pain: Epidemiological evidence of the relationship and implications. Hum. Reprod. Update 2005, 11, 595–606. [Google Scholar] [CrossRef]
- Anaf, V.; Simon, P.; El Nakadi, I.; Fayt, I.; Simonart, T.; Buxant, F.; Noel, J.C. Hyperalgesia, nerve infiltration and nerve growth factor expression in deep adenomyotic nodules, peritoneal and ovarian endometriosis. Hum. Reprod. 2002, 17, 1895–1900. [Google Scholar] [CrossRef] [PubMed]
- Al-Fozan, H.; Bakare, S.; Chen, M.F.; Tulandi, T. Nerve fibers in ovarian dermoid cysts and endometriomas. Fertil. Steril. 2004, 82, 230–231. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Jiang, Y.J. Rupture of ovarian endometriotic cyst complicated with endometriosis: A case report. World J. Clin. Cases 2021, 9, 8524–8530. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Sanada, T.; Park, J.; Hagiwara, M.; Ikeda, N.; Nagai, T.; Matsubayashi, J.; Saito, K. CT and MRI findings of bronchopulmonary endometriosis: A case presentation. Acta Radiol. Open 2018, 7, 2058460118801164. [Google Scholar] [CrossRef] [PubMed]
- Kingsberg, S.A.; Janata, J.W. Female sexual disorders: Assessment, diagnosis, and treatment. Urol. Clin. N. Am. 2007, 34, 497–506. [Google Scholar] [CrossRef]
- Kennedy, S.; Bergqvist, A.; Chapron, C.; D’Hooghe, T.; Dunselman, G.; Greb, R.; Hummelshoj, L.; Prentice, A.; Saridogan, E.; on behalf of the ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development Group. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum. Reprod. 2005, 20, 2698–2704. [Google Scholar] [CrossRef]
- Mounsey, A.L.; Wilgus, A.; Slawson, D.C. Diagnosis and management of endometriosis. Am. Fam. Physician 2006, 74, 594–600. [Google Scholar]
- Cranney, R.; Condous, G.; Reid, S. An update on the diagnosis, surgical management, and fertility outcomes for women with endometrioma. Acta Obstet. Gynecol. Scand. 2017, 96, 633–643. [Google Scholar] [CrossRef] [PubMed]
- Wieser, F.; Dogan, S.; Klingel, K.; Diedrich, K.; Taylor, R.N.; Hornung, D. Expression and regulation of CCR1 in peritoneal macrophages from women with and without endometriosis. Fertil. Steril. 2005, 83, 1878–1881. [Google Scholar] [CrossRef] [PubMed]
- Nisenblat, V.; Bossuyt, P.M.; Shaikh, R.; Farquhar, C.; Jordan, V.; Scheffers, C.S.; Mol, B.W.J.; Johnson, N.; Hull, M.L. Blood Biomarkers for the Non-Invasive Diagnosis of Endometriosis. Cochrane Database Syst. Rev. 2016, 2016, CD012179. [Google Scholar] [CrossRef]
- Surrey, E.; Carter, C.M.; Soliman, A.M.; Khan, S.; DiBenedetti, D.B.; Snabes, M.C. Patient-Completed or Symptom-Based Screening Tools for Endometriosis: A Scoping Review. Arch. Gynecol. Obstet. 2017, 296, 153–165. [Google Scholar] [CrossRef] [PubMed]
- Akter, S.; Xu, D.; Nagel, S.C.; Bromfield, J.J.; Pelch, K.E.; Wilshire, G.B.; Joshi, T. GenomeForest: An Ensemble Machine Learning Classifier for Endometriosis. AMIA Summits Transl. Sci. Proc. 2020, 2020, 33–42. [Google Scholar] [PubMed]
- Bendifallah, S.; Suisse, S.; Puchar, A.; Delbos, L.; Poilblanc, M.; Descamps, P.; Golfier, F.; Jornea, L.; Bouteiller, D.; Touboul, C.; et al. Salivary MicroRNA Signature for Diagnosis of Endometriosis. J. Clin. Med. 2022, 11, 612. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Melinte-Popescu, A.S.; Popa, R.F.; Harabor, V.; Nechita, A.; Harabor, A.; Adam, A.M.; Vasilache, I.A.; Melinte-Popescu, M.; Vaduva, C.; Socolov, D. Managing Fetal Ovarian Cysts: Clinical Experience with a Rare Disorder. Medicina 2023, 59, 715. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Albu, D.F.; Albu, C.C.; Gogănău, A.M.; Albu, S.D.; Mogoantă, L.; Edu, A.; DiŢescu, D.; Văduva, C.C. Borderline Brenner tumors associated with ovarian cyst—Case presentation. Rom. J. Morphol. Embryol. 2016, 57, 893–898. [Google Scholar]
- Noventa, M.; Scioscia, M.; Schincariol, M.; Cavallin, F.; Pontrelli, G.; Virgilio, B.; Vitale, S.G.; Laganà, A.S.; Dessole, F.; Cosmi, E.; et al. Imaging Modalities for Diagnosis of Deep Pelvic Endometriosis: Comparison between Trans-Vaginal Sonography, Rectal Endoscopy Sonography and Magnetic Resonance Imaging. A Head-to-Head Meta-Analysis. Diagnostics 2019, 9, 225. [Google Scholar] [CrossRef]
- Young, S.W.; Groszmann, Y.; Dahiya, N.; Caserta, M.; Yi, J.; Wasson, M.; Patel, M.D. Sonographer-acquired ultrasound protocol for deep endometriosis. Abdom. Radiol. 2020, 45, 1659–1669. [Google Scholar] [CrossRef]
- Cohen Ben-Meir, L.; Mashiach, R.; Eisenberg, V.H. External Validation of the IOTA Classification in Women with Ovarian Masses Suspected to Be Endometrioma. J. Clin. Med. 2021, 10, 2971. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Abrao, M.S.; Goncalves, M.O.D.C.; Dias, J.A., Jr.; Podgaec, S.; Chamie, L.P.B.R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis. Hum. Reprod. 2007, 22, 3092–3097. [Google Scholar] [CrossRef]
- Guerriero, S.; Ajossa, S.; Gerada, M.; Virgilio, B.; Angioni, S.; Melis, G.B. Diagnostic value of transvaginal ’tenderness-guided’ ultrasonography for the prediction of location of deep endometriosis. Hum. Reprod. 2008, 23, 2452–2457. [Google Scholar] [CrossRef]
- Martin, D.C.; Batt, R.E. Retrocervical, retrovaginal pouch, and rectovaginal septum endometriosis. J. Am. Assoc. Gynecol. Laparosc. 2001, 8, 12–17. [Google Scholar] [CrossRef] [PubMed]
- Leon, M.; Alcazar, J.L. High sliding sign: A new soft marker of uterine fundus compromise in deep infiltrating endometriosis. Ultrasound Obstet. Gynecol. 2015, 45, 624. [Google Scholar] [CrossRef] [PubMed]
- Guerriero, S.; Alcazar, J.L.; Ajossa, S.; Pilloni, M.; Melis, G.B. Three-dimensional sonographic characteristics of deep endometriosis. J. Ultrasound Med. 2009, 28, 1061–1066. [Google Scholar] [CrossRef] [PubMed]
- Rolla, E. Endometriosis: Advances and controversies in classification, pathogenesis, diagnosis, and treatment. F1000Research 2019, 8, F1000 Faculty Rev-529. [Google Scholar] [CrossRef]
- Vercellini, P.; Frontino, G.; Pietropaolo, G.; Gattei, U.; Daguati, R.; Crosignani, P.G. Deep endometriosis: Definition, pathogenesis, and clinical management. J. Am. Assoc. Gynecol. Laparosc. 2004, 11, 153–161. [Google Scholar] [CrossRef] [PubMed]
- Duffy, J.M.; Arambage, K.; Correa, F.J.; Olive, D.; Farquhar, C.; Garry, R.; Barlow, D.H.; Jacobson, T.Z. Laparoscopic surgery for endometriosis. Cochrane Database Syst. Rev. 2014, 4, CD011031. [Google Scholar]
- Mobeen, S.; Apostol, R. Ovarian Cyst. In StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2025. [Google Scholar] [PubMed]
- Patel, M.D.; Feldstein, V.A.; Filly, R.A. The likelihood ratio of sonographic findings for the diagnosis of hemorrhagic ovarian cysts. J. Ultrasound Med. 2005, 24, 607–614, quiz 15. [Google Scholar] [CrossRef]
- Costea, D.; Serbanescu, L.; Badiu, D.; Ardeleanu, V.; Branescu, C.; Zgura, A.; Costea, A. Pain Managemnent in the Right Iliac Fossa During the COVID-19 Pandemic. J. Mind Med. Sci. 2022, 9, 162–167. [Google Scholar] [CrossRef]
- Benaglia, L.; Somigliana, E.; Vercellini, P.; Abbiati, A.; Ragni, G.; Fedele, L. The rate of spontaneous ovulation is negatively affected by endometriotic ovarian cysts. Hum. Reprod. 2009, 24, 2183–2186. [Google Scholar] [CrossRef]
- Kim, S.K.; Lee, J.R.; Lee, D.; Jee, B.C. Treatment options and considerations for infertility due to endometriosis. Clin. Exp. Reprod. Med. 2020, 47, 1–11. [Google Scholar]
- Benaglia, L.; Cardellicchio, L.; Guarneri, C.; Paffoni, A.; Restelli, L.; Somigliana, E.; Fedele, L. IVF outcomes in women with accidental contamination of follicular fluid with endometrioma contents. Eur. J. Obstet. Gynecol. Reprod. Biol. 2014, 181, 130–134. [Google Scholar] [CrossRef] [PubMed]
- Huang, Y.H.; Liou, J.D.; Hsieh, C.L.; Shiau, C.S.; Lo, L.M.; Chang, M.Y. Long-term follow-up of patients surgically treated for ruptured ovarian endometriotic cysts. Taiwan. J. Obstet. Gynecol. 2011, 50, 306–311. [Google Scholar] [CrossRef] [PubMed]
- Leone Roberti Maggiore, U.; Ferrero, S.; Mangili, G.; Bergamini, A.; Inversetti, A.; Giorgione, V.; Viganò, P.; Candiani, M. A systematic review on endometriosis during pregnancy: Diagnosis, misdiagnosis, complications and outcomes. Hum. Reprod. Update 2016, 22, 70–103. [Google Scholar] [CrossRef] [PubMed]
- Coccia, M.E.; Rizzello, F.; Gianfranco, S. Does controlled ovarian hyperstimulation in women with a history of endometriosis influence recurrence rate? J Womens Health 2010, 19, 2063–2069. [Google Scholar] [CrossRef] [PubMed]
- Ueda, Y.; Enomoto, T.; Miyatake, T.; Fujita, M.; Yamamoto, R.; Kanagawa, T.; Shimizu, H.; Kimura, T. A retrospective analysis of ovarian endometriosis during pregnancy. Fertil. Steril. 2010, 94, 78–84. [Google Scholar] [CrossRef] [PubMed]
- Benaglia, L.; Somigliana, E.; Calzolari, L.; Busnelli, A.; Cardellicchio, L.; Ragni, G.; Fedele, L. The disappearing endometrioma: The intriguing effect of pregnancy on small endometriotic ovarian cysts. Gynecol. Endocrinol. 2013, 29, 863–866. [Google Scholar] [CrossRef]
- Sasaki, K.J.; Miller, C.E. Adnexal torsion: Review of the literature. J. Minim. Invasive Gynecol. 2014, 21, 196–202. [Google Scholar] [CrossRef] [PubMed]
- Centini, G.; Schettini, G.; Pieri, E.; Giorgi, M.; Lazzeri, L.; Martire, F.G.; Mancini, V.; Raimondo, D.; Seracchioli, R.; Habib, N.; et al. Endometriosis-Related Ovarian Cancer: Where Are We Now? A Narrative Review towards a Pragmatic Approach. J. Clin. Med. 2024, 13, 1933. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Pearce, C.L.; Templeman, C.; Rossing, M.A.; Lee, A.; Near, A.M.; Webb, P.M.; Nagle, C.M.; Doherty, J.A.; Cushing-Haugen, K.L.; Wicklund, K.G.; et al. Association between endometriosis and risk of histological subtypes of ovarian cancer: A pooled analysis of case-control studies. Lancet Oncol. 2012, 13, 385–394. [Google Scholar] [CrossRef]
- Saavalainen, L.; Lassus, H.; But, A.M.; Tiitinen, A.; Härkki, P.; Gissler, M.; Pukkala, E.; Heikinheimo, O. Risk of Gynecologic Cancer According to the Type of Endometriosis. Obstet. Gynecol. 2018, 131, 1095–1102. [Google Scholar] [CrossRef]
- Samartzis, E.P.; Noske, A.; Dedes, K.J.; Fink, D.; Imesch, P. ARID1A mutations and PI3K/AKT pathway alterations in endometriosis and endometriosis-associated ovarian carcinOEs. Int. J. Mol. Sci. 2013, 14, 18824–18849. [Google Scholar] [CrossRef]
- Dunselman, G.A.; Vermeulen, N.; Becker, C.; Calhaz-Jorge, C.; D’Hooghe, T.; De Bie, B.; Heikinheimo, O.; Horne, A.W.; Kiesel, L.; Nap, A.; et al. ESHRE guideline: Management of women with endometriosis. Hum. Reprod. 2014, 29, 400–412. [Google Scholar] [CrossRef] [PubMed]
- Mansouri, G.; Safinataj, M.; Shahesmaeili, A.; Allahqoli, L.; Salehiniya, H.; Alkatout, I. Effect of laparoscopic cystectomy on ovarian reserve in patients with ovarian cyst. Front. Endocrinol. 2022, 13, 964229. [Google Scholar] [CrossRef] [PubMed]
- Somigliana, E.; Berlanda, N.; Benaglia, L.; Viganò, P.; Vercellini, P.; Fedele, L. Surgical excision of endometriomas and ovarian reserve: A systematic review on serum antimüllerian hormone level modifications. Fertil. Steril. 2012, 98, 1531–1538. [Google Scholar] [CrossRef]
- Pais, A.S.; Flagothier, C.; Tebache, L.; Almeida Santos, T.; Nisolle, M. Impact of Surgical Management of Endometrioma on AMH Levels and Pregnancy Rates: A Review of Recent Literature. J. Clin. Med. 2021, 10, 414. [Google Scholar] [CrossRef] [PubMed]
- Tsolakidis, D.; Pados, G.; Vavilis, D.; Athanatos, D.; Tsalikis, T.; Giannakou, A.; Tarlatzis, B.C. 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. [Google Scholar] [CrossRef] [PubMed]
- Donnez, J.; Lousse, J.C.; Jadoul, P.; Donnez, O.; Squifflet, J. Laparoscopic management of endometrioms using a combined technique of excisional (cystectomy) and ablative surgery. Fertil. Steril. 2010, 94, 28–32. [Google Scholar] [CrossRef]
- Daniilidis, A.; Grigoriadis, G.; Kalaitzopoulos, D.R.; Angioni, S.; Kalkan, Ü.; Crestani, A.; Merlot, B.; Roman, H. Surgical Management of Ovarian Endometrioma: Impact on Ovarian Reserve Parameters and Reproductive Outcomes. J. Clin. Med. 2023, 12, 5324. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Zhang, Y.; Zhang, S.; Zhao, Z.; Wang, C.; Xu, S.; Wang, F. Impact of cystectomy versus ablation for endometrioma on ovarian reserve: A systematic review and meta-analysis. Fertil. Steril. 2022, 118, 1172–1182. [Google Scholar] [CrossRef] [PubMed]
- Muzii, L.; Achilli, C.; Bergamini, V.; Candiani, M.; Garavaglia, E.; Lazzeri, L.; Lecce, F.; Maiorana, A.; Maneschi, F.; Marana, R.; et al. Comparison between the stripping technique and the combined excisional/ablative technique for the treatment of bilateral ovarian endometriomas: A multicentre RCT. Hum. Reprod. 2016, 31, 339–344. [Google Scholar] [CrossRef]
- Alammari, R.; Lightfoot, M.; Hur, H.C. Impact of Cystectomy on Ovarian Reserve: Review of the Literature. J. Minim. Invasive Gynecol. 2017, 24, 247–257. [Google Scholar] [CrossRef] [PubMed]
- Lam, K.; Lang, E. Endometriosis as a rare cause of small bowel obstruction. ANZ J. Surg. 2020, 90, E137–E138. [Google Scholar] [CrossRef]
- Endo, Y.; Akatsuka, J.; Obayashi, K.; Takeda, H.; Hayashi, T.; Nakayama, S.; Suzuki, Y.; Hamasaki, T.; Kondo, Y. Efficacy of Laparoscopic Partial Cystectomy with a Transurethral Resectoscope in Patients with Bladder Endometriosis: See-Through Technique. Urol. Int. 2020, 104, 546–550. [Google Scholar] [CrossRef] [PubMed]
- Hoffman, B.L.; Schorge, J.O.; Halvorson, L.M.; Hamid, C.A.; Corton, M.M.; Schaffer, J.I. (Eds.) Williams Gynecology, 4th ed.; McGraw-Hill Education: Berkshire, UK, 2020. [Google Scholar]
- Kalaitzopoulos, D.R.; Samartzis, N.; Kolovos, G.N.; Mareti, E.; Samartzis, E.P.; Eberhard, M.; Dinas, K.; Daniilidis, A. Treatment of endometriosis: A review with comparison of 8 guidelines. BMC Women’s Health 2021, 21, 397. [Google Scholar] [CrossRef]
- Chen, I.; Veth, V.B.; Choudhry, A.J.; Murji, A.; Zakhari, A.; Black, A.Y.; Agarpao, C.; Maas, J.W. Pre- and postsurgical medical therapy for endometriosis surgery. Cochrane Database Syst. Rev. 2020, 11, CD003678. [Google Scholar] [CrossRef] [PubMed]
- Seracchioli, R.; Mabrouk, M.; Manuzzi, L.; Vicenzi, C.; Frasca, C.; Elmakky, A.; Venturoli, S. Post-operative use of oral contraceptive pills for prevention of anatomical relapse or symptom-recurrence after conservative surgery for endometriosis. Hum. Reprod. 2009, 24, 2729–2735. [Google Scholar] [CrossRef] [PubMed]
- Armour, M.; Sinclair, J.; Cheng, J.; Davis, P.; Hameed, A.; Meegahapola, H.; Rajashekar, K.; Suresh, S.; Proudfoot, A.; Leonardi, M. Endometriosis and Cannabis Consumption During the COVID-19 Pandemic: An International Cross-Sectional Survey. Cannabis Cannabinoid Res. 2022, 7, 473–481. [Google Scholar] [CrossRef]
- Alonso, A.; Gunther, K.; Maheux-Lacroix, S.; Abbott, J. Medical management of endometriosis. Curr. Opin. Obstet. Gynecol. 2024, 36, 353–361. [Google Scholar] [CrossRef]
- Cohen, A.; Almog, B.; Tulandi, T. Sclerotherapy in the management of ovarian endometrioma: Systematic review and meta-analysis. Fertil. Steril. 2017, 108, 117–124.e5. [Google Scholar] [CrossRef]
- Noma, J.; Yoshida, N. Efficacy of ethanol sclerotherapy for ovarian endometriomas. Int. J. Gynaecol. Obstet. 2001, 72, 35–39. [Google Scholar] [CrossRef]
- Huang, L.; Chang, M.-Y.; Shiau, C.-S.; Hsieh, T.-T. Changes in anti-müllerian hormone after ultrasound guided aspiration and ethanol sclerotic therapy of ovarian cyst. Taiwan. J. Obstet. Gynecol. 2021, 60, 509–512. [Google Scholar] [CrossRef] [PubMed]
- Koo, J.H.; Lee, I.; Han, K.; Seo, S.K.; Kim, M.-D.; Lee, J.K.; Kwon, J.H.; Kim, G.M.; Lee, J.; Won, J.Y. Comparison of the therapeutic efficacy and ovarian reserve between catheter-directed sclerotherapy and surgical excision for ovarian endometrioma. Eur. Radiol. 2021, 31, 543–548. [Google Scholar] [CrossRef] [PubMed]
- Garcia-Tejedor, A.; Martinez-Garcia, J.M.; Candas, B.; Suarez, E.; Mañalich, L.; Gomez, M.; Merino, E.; Castellarnau, M.; Regueiro, P.; Carreras, M.; et al. Ethanol Sclerotherapy versus Laparoscopic Surgery for Endometrioma Treatment: A Prospective, Multicenter, Cohort Pilot Study. J. Minim. Invasive Gynecol. 2020, 27, 1133–1140. [Google Scholar] [CrossRef] [PubMed]
- Perrone, U.; Ferrero, S.; Gazzo, I.; Izzotti, A.; Leone Roberti Maggiore, U.; Gustavino, C.; Ceccaroni, M.; Bogliolo, S.; Barra, F. Endometrioma surgery: Hit with your best shot (But know when to stop). Best Pract. Res. Clin. Obstet. Gynaecol. 2024, 96, 102528. [Google Scholar] [CrossRef] [PubMed]
- Practice Committee of the American Society for Reproductive Medicine. Endometriosis and infertility: A committee opinion. Fertil. Steril. 2012, 98, 591–598. [Google Scholar] [CrossRef]
- Lee, D.; Kim, S.K.; Lee, J.R.; Jee, B.C. Management of endometriosis-related infertility: Considerations and treatment options. Clin. Exp. Reprod. Med. 2020, 47, 1–11, Erratum in: Clin. Exp. Reprod. Med. 2020, 47, 153. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Esinler, I.; Bozdag, G.; Arikan, I.; Demir, B.; Yarali, H. Endometrioma ≤3 cm in diameter per se does not affect ovarian reserve in intracytoplasmic sperm injection cycles. Gynecol. Obstet. Investig. 2012, 74, 261–264. [Google Scholar] [CrossRef]
- Hamdan, M.; Dunselman, G.; Li, T.C.; Cheong, Y. The impact of endometrioma on IVF/ICSI outcomes: A systematic review and metaanalysis. Hum. Reprod. Update 2015, 21, 809–825. [Google Scholar] [CrossRef]
- Rienzi, L.; Gracia, C.; Maggiulli, R.; LaBarbera, A.R.; Kaser, D.J.; Ubaldi, F.M.; Vanderpoel, S.; Racowsky, C. Oocyte, embryo and blastocyst cryopreservation in ART: Systematic review and meta-analysis comparing slow-freezing versus vitrification to produce evidence for the development of global guidance. Hum. Reprod. Update 2017, 23, 139–155. [Google Scholar] [CrossRef]
Stage | Classification | Description |
---|---|---|
I | Minimal | Few superficial implants |
II | Mild | More implants, deeper involvement |
III | Moderate | Many implants, small OEs, adhesions present |
IV | Severe | Many deep implants, large OEs, many adhesions |
Desire for natural conception | Indication: intact ovarian reserve, unilateral cyst, without surgical treatment Surgery—combined ablation and cystectomy |
Reproductive surgery to improve IVF results (pain or other symptoms, male or tubal infertility, women who do not want to wait for natural conception after surgery) | Indication: large cysts Surgery—three-stage techniques or aspiration with sclerotherapy followed by IVF with GnRH agonist’s long protocol |
Expectant management and IVF (no pain symptoms, male or tubal infertility) | Indications: low AMH, small cysts, bilateral OEs, previous surgical treatment IVF after 6 months of treatment with GnRH agonists |
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Văduva, C.-C.; Dîră, L.; Boldeanu, L.; Șerbănescu, M.-S.; Carp-Velișcu, A. A Narrative Review Regarding Implication of Ovarian Endometriomas in Infertility. Life 2025, 15, 161. https://doi.org/10.3390/life15020161
Văduva C-C, Dîră L, Boldeanu L, Șerbănescu M-S, Carp-Velișcu A. A Narrative Review Regarding Implication of Ovarian Endometriomas in Infertility. Life. 2025; 15(2):161. https://doi.org/10.3390/life15020161
Chicago/Turabian StyleVăduva, Constantin-Cristian, Laurențiu Dîră, Lidia Boldeanu, Mircea-Sebastian Șerbănescu, and Andreea Carp-Velișcu. 2025. "A Narrative Review Regarding Implication of Ovarian Endometriomas in Infertility" Life 15, no. 2: 161. https://doi.org/10.3390/life15020161
APA StyleVăduva, C.-C., Dîră, L., Boldeanu, L., Șerbănescu, M.-S., & Carp-Velișcu, A. (2025). A Narrative Review Regarding Implication of Ovarian Endometriomas in Infertility. Life, 15(2), 161. https://doi.org/10.3390/life15020161