Clinical characteristics difference between early and late recurrence of ovarian endometriosis after laparoscopic cystectomy

Background Ovarian endometriosis is the most frequent type of endometriosis. Despite the use of surgery and medication, many patients suffer from recurrence within near future. Currently, there are no effective clinical characteristics available to predict the time to recurrence in ovarian endometriosis patients. Purpose To identify the effective clinical indicators for early and late endometrioma recurrence, we compared the clinical characteristics of early and late recurrence after treatment.

We collected 358 patients with ovarian endometriosis who had a minimum of 5 years of postoperative follow-up after undergoing a laparoscopic excision of ovarian endometrioma performed at Peking Union Medical College Hospital from January 2009 to April 2013.

A total of 358 patients were recruited in the validation set, with a median follow-up time of 83 months (60–120 months). Till the last follow-up, 68 patients exhibited recurrence. Three-year and 5-year recurrence rates were 9.2% and 15.4%, respectively. Univariate analysis in our study showed that patient with endometrioma surgery history had higher incidence of recurrence in 3 years after re-surgery (OR: 5.594, P = 0.029). Univariate and multivariate analyses using the logistic regression showed that the presence of tenesmus before surgery affected the incidence of early recurrence with a ratio of 57.9% (11/19) and 89.5% (17/19) in 3 years and 5 years after surgery, respectively.

Presence of tenesmus before surgery may be linked to the early recurrence of endometrioma. Similar content being viewed by others Availability of data and materials The dataset supporting the conclusions of this article is included within the article and its additional files. Abbreviations - ART: - Artificial reproduction technology - ASRM: - American Society for Reproductive Medicine - BMI: - Body mass index - CA-125: - Carbohydrate antigen 125 - CI: - Confidence interval - DIE: - Deep invasive endometriosis - GnRHa: - Gonadotropin-releasing hormone agonist - OR: - Odds ratio - QoL: - Quality of life - TTR: - Time to recurrence - VAS: - Visual analog scale

Chapron C, Boucher E, Fauconnier A, Vieira M, Dubuisson JB, Vacher-Lavenu MC (2002) Anatomopathological lesions of bladder endometriosis are heterogeneous. Fertil Steril 78(4):740–742. https://doi.org/10.1016/s0015-0282(02)03321-6 Gambadauro P, Carli V, Hadlaczky G (2019) Depressive symptoms among women with endometriosis: a systematic review and meta-analysis. Am J Obstet Gynecol 220(3):230–241. https://doi.org/10.1016/j.ajog.2018.11.123 Alio L, Angioni S, Arena S, Bartiromo L, Bergamini V, Berlanda N, Bonanni V, Bonin C, Buggio L, Candiani M, Centini G, D’Alterio MN, De Stefano F, Di Cello A, Exacoustos C, Fedele L, Frattaruolo MP, Geraci E, Lavarini E, Lazzeri L, Luisi S, Maiorana A, Makieva S, Maneschi F, Martire F, Massarotti C, Mattei A, Muzii L, Ottolina J, Pagliardini L, Perandini A, Perelli F, Pino I, Porpora MG, Remorgida V, Scagnelli G, Seracchioli R, Solima E, Somigliana E, Sorrenti G, Ticino A, Venturella R, Viganò P, Vignali M, Zullo F, Zupi E (2019) Endometriosis: seeking optimal management in women approaching menopause. Climacteric 22(4):329–338. https://doi.org/10.1080/13697137.2018.1549213 Chapron C, Tosti C, Marcellin L, Bourdon M, Lafay-Pillet MC, Millischer AE, Streuli I, Borghese B, Petraglia F, Santulli P (2017) Relationship between the magnetic resonance imaging appearance of adenomyosis and endometriosis phenotypes. Hum Reprod 32(7):1393–1401. https://doi.org/10.1093/humrep/dex088 Deckers P, Ribeiro SC, Simoes RDS, Miyahara C, Baracat EC (2018) Systematic review and meta-analysis of the effect of bipolar electrocoagulation during laparoscopic ovarian endometrioma stripping on ovarian reserve. Int J Gynaecol Obstet 140(1):11–17. https://doi.org/10.1002/ijgo.12338 Bey E, Marchais-Oberwinkler S, Werth R, Negri M, Al-Soud YA, Kruchten P, Oster A, Frotscher M, Birk B, Hartmann RW (2008) Design, synthesis, biological evaluation and pharmacokinetics of bis (hydroxyphenyl) substituted azoles, thiophenes, benzenes, and aza-benzenes as potent and selective nonsteroidal inhibitors of 17beta-hydroxysteroid dehydrogenase type 1 (17beta-HSD1). J Med Chem 51(21):6725–6739. https://doi.org/10.1021/jm8006917 Mehdizadeh Kashi A, Chaichian S, Ariana S, Fazaeli M, Moradi Y, Rashidi M, Najmi Z (2017) The impact of laparoscopic cystectomy on ovarian reserve in patients with unilateral and bilateral endometrioma. Int J Gynaecol Obstet 136(2):200–204. https://doi.org/10.1002/ijgo.12046 Ozaki R, Kumakiri J, Tinelli A, Grimbizis GF, Kitade M, Takeda S (2016) Evaluation of factors predicting diminished ovarian reserve before and after laparoscopic cystectomy for ovarian endometriomas: a prospective cohort study. J Ovarian Res 9(1):37. https://doi.org/10.1186/s13048-016-0241-z Alabiso G, Alio L, Arena S, Barbasetti di Prun A, Bergamini V, Berlanda N, Busacca M, Candiani M, Centini G, Di Cello A, Exacoustos C, Fedele L, Fuggetta E, Gabbi L, Geraci E, Imperiale L, Lavarini E, Incandela D, Lazzeri L, Luisi S, Maiorana A, Maneschi F, Mannini L, Mattei A, Muzii L, Pagliardini L, Perandini A, Perelli F, Pinzauti S, Porpora MG, Remorgida V, Leone Roberti Maggiore U, Seracchioli R, Solima E, Somigliana E, Tosti C, Venturella R, Vercellini P, Vigano P, Vignali M, Zannoni L, Zullo F, Zupi E (2016) Adenomyosis: what the patient needs. J Minim Invasive Gynecol 23(4):476–488. https://doi.org/10.1016/j.jmig.2015.12.017 Chang HJ, Han SH, Lee JR, Jee BC, Lee BI, Suh CS, Kim SH (2010) Impact of laparoscopic cystectomy on ovarian reserve: serial changes of serum anti-Mullerian hormone levels. Fertil Steril 94(1):343–349. https://doi.org/10.1016/j.fertnstert.2009.02.022 Mabrouk M, Ferrini G, Montanari G, Di Donato N, Raimondo D, Stanghellini V, Corinaldesi R, Seracchioli R (2012) Does colorectal endometriosis alter intestinal functions? A prospective manometric and questionnaire-based study. Fertil Steril 97(3):652–656. https://doi.org/10.1016/j.fertnstert.2011.12.019 Takamura M, Koga K, Osuga Y, Takemura Y, Hamasaki K, Hirota Y, Yoshino O, Taketani Y (2009) Post-operative oral contraceptive use reduces the risk of ovarian endometrioma recurrence after laparoscopic excision. Hum Reprod 24(12):3042–3048. https://doi.org/10.1093/humrep/dep297 Benaglia L, Somigliana E, Vighi V, Ragni G, Vercellini P, Fedele L (2010) Rate of severe ovarian damage following surgery for endometriomas. Hum Reprod 25(3):678–682. https://doi.org/10.1093/humrep/dep464 Camara O, Herrmann J, Egbe A, Kavallaris A, Diebolder H, Gajda M, Runnebaum IB (2009) Treatment of endometriosis of uterosacral ligament and rectum through the vagina: description of a modified technique. Hum Reprod 24(6):1407–1413. https://doi.org/10.1093/humrep/dep016 Cunningham RK, Horrow MM, Smith RJ, Springer J (2018) Adenomyosis: a sonographic diagnosis. Radiographics 38(5):1576–1589. https://doi.org/10.1148/rg.2018180080 Bazot M, Daraï E (2018) Role of transvaginal sonography and magnetic resonance imaging in the diagnosis of uterine adenomyosis. Fertil Steril 109(3):389–397. https://doi.org/10.1016/j.fertnstert.2018.01.024 Naftalin J, Hoo W, Pateman K, Mavrelos D, Holland T, Jurkovic D (2012) How common is adenomyosis? A prospective study of prevalence using transvaginal ultrasound in a gynaecology clinic. Human reproduction (Oxford, England) 27(12):3432–3439. https://doi.org/10.1093/humrep/des332 Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J (2012) Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril 98(3):564–571. https://doi.org/10.1016/j.fertnstert.2012.07.1061 Keckstein J, Becker CM, Canis M, Feki A, Grimbizis GF, Hummelshoj L, Nisolle M, Roman H, Saridogan E, Tanos V, Tomassetti C, Ulrich UA, Vermeulen N, De Wilde RL (2020) Recommendations for the surgical treatment of endometriosis Part 2: deep endometriosis. Hum Reprod Open 2020:2. https://doi.org/10.1093/hropen/hoaa002 Tobiume T, Kotani Y, Takaya H, Nakai H, Tsuji I, Suzuki A, Mandai M (2016) Determinant factors of postoperative recurrence of endometriosis: difference between endometrioma and pain. Eur J Obstet Gynecol Reprod Biol 205:54–59. https://doi.org/10.1016/j.ejogrb.2016.07.516 Chon SJ, Lee SH, Choi JH, Lee JS (2016) Preoperative risk factors in recurrent endometrioma after primary conservative surgery. Obstetr Gynecol Sci 59(4):286–294. https://doi.org/10.5468/ogs.2016.59.4.286 Selcuk S, Cam C, Koc N, Kucukbas M, Ozkaya E, Eser A, Karateke A (2016) Evaluation of risk factors for the recurrence of ovarian endometriomas. Eur J Obstet Gynecol Reprod Biol 203:56–60. https://doi.org/10.1016/j.ejogrb.2016.05.008 Meuleman C, Tomassetti C, Wolthuis A, Van Cleynenbreugel B, Laenen A, D’Hoore A, D’Hooghe T (2015) Increasing the quality of surgery for deep endometriosis should be based on homogenous clinical patient phenotype, surgical experience, and standardized outcome reporting in multicenter multisurgeon prospective trials. Ann Surg 262(1):e26–28. https://doi.org/10.1097/sla.0000000000000573 Campagnacci R, Perretta S, Guerrieri M, Paganini AM, De Sanctis A, Ciavattini A, Lezoche E (2005) Laparoscopic colorectal resection for endometriosis. Surg Endosc 19(5):662–664. https://doi.org/10.1007/s00464-004-8710-7 Ní Laoire Á, Fettes L, Murtagh FE (2017) A systematic review of the effectiveness of palliative interventions to treat rectal tenesmus in cancer. Palliat Med 31(10):975–981. https://doi.org/10.1177/0269216317697897 Bertocchi E, Barugola G, Benini M, Bocus P, Rossini R, Ceccaroni M, Ruffo G (2019) Colorectal anastomotic stenosis: lessons learned after 1643 colorectal resections for deep infiltrating endometriosis. J Minim Invasive Gynecol 26(1):100–104. https://doi.org/10.1016/j.jmig.2018.03.033 Archer DF, Ng J, Chwalisz K, Chiu YL, Feinberg EC, Miller CE, Feldman RA, Klein CE (2020) Elagolix suppresses ovulation in a dose-dependent manner: results from a 3-month, randomized study in ovulatory women. J Clin Endocrinol Metab 105:3. https://doi.org/10.1210/clinem/dgz086 Lagana AS, Vitale SG, Salmeri FM, Triolo O, Ban Frangez H, Vrtacnik-Bokal E, Stojanovska L, Apostolopoulos V, Granese R, Sofo V (2017) Unus pro omnibus, omnes pro uno: a novel, evidence-based, unifying theory for the pathogenesis of endometriosis. Med Hypotheses 103:10–20. https://doi.org/10.1016/j.mehy.2017.03.032 Vitale SG, Capriglione S, Peterlunger I, La Rosa VL, Vitagliano A, Noventa M, Valenti G, Sapia F, Angioli R, Lopez S, Sarpietro G, Rossetti D, Zito G (2018) The role of oxidative stress and membrane transport systems during endometriosis: a fresh look at a busy corner. Oxid Med Cell Longev 2018:7924021. https://doi.org/10.1155/2018/7924021 Borghese B, Gayet V, Chiche JD, Vernerey D, de Ziegler D, Bonaiti-Pellie C, Chapron C (2009) Absence of association between a functional polymorphism of ALOX15 gene and infertility in endometriosis. Fertil Steril 91(4 Suppl):1414–1416. https://doi.org/10.1016/j.fertnstert.2008.05.039 Lagana AS, Vitale SG (2016) Full-thickness excision versus shaving by laparoscopy for intestinal deep infiltrating endometriosis: rationale and potential treatment options. BioMed Res Int 2016:3617179. https://doi.org/10.1155/2016/3617179 Armengol-Debeir L, Savoye G, Leroi AM, Gourcerol G, Savoye-Collet C, Tuech JJ, Vassilieff M, Roman H (2011) Pathophysiological approach to bowel dysfunction after segmental colorectal resection for deep endometriosis infiltrating the rectum: a preliminary study. Hum Reprod 26(9):2330–2335. https://doi.org/10.1093/humrep/der190 Badescu A, Roman H, Aziz M, Puscasiu L, Molnar C, Huet E, Sabourin JC, Stolnicu S (2016) Mapping of bowel occult microscopic endometriosis implants surrounding deep endometriosis nodules infiltrating the bowel. Fertil Steril 105(2):430–434.e426. https://doi.org/10.1016/j.fertnstert.2015.11.006 Benbara A, Fortin A, Martin B, Palazzo L, Le Tohic A, Madelenat P, Yazbeck C (2008) Surgical and functional results of rectosigmoidal resection for severe endometriosis. Gynecol Obstet Fertil 36(12):1191–1201. https://doi.org/10.1016/j.gyobfe.2008.09.016 Augoulea A, Alexandrou A, Creatsa M, Vrachnis N, Lambrinoudaki I (2012) Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress. Arch Gynecol Obstet 286(1):99–103. https://doi.org/10.1007/s00404-012-2357-8 Asante A, Taylor RN (2011) Endometriosis: the role of neuroangiogenesis. Annu Rev Physiol 73:163–182. https://doi.org/10.1146/annurev-physiol-012110-142158 Ianieri MM, Mautone D, Ceccaroni M (2018) Recurrence in deep infiltrating endometriosis: a systematic review of the literature. J Minim Invasive Gynecol 25(5):786–793. https://doi.org/10.1016/j.jmig.2017.12.025 Acknowledgments None. Funding Our work was supported by the National Key R&D Program of China (No. 2017YFC1001200), National Natural Science Foundation of China (No. 81501237), and 2016 PUMCH Science Fund for Junior Faculty (No. PUMCH-2016-2.2). Author information Authors and Affiliations Contributions JL: study conception and design. XL: manuscript writing. WZ: data analysis. XC, YD, JS: data collection. SJ, SC, YW: pathological investigation. The manuscript has been read and approved by all the authors. The requirements for authorship have been met. Each author believes that the manuscript represents honest work. Corresponding author Ethics declarations Conflicts of interest The authors declare that they have no conflict of interests. Code availability Not applicable. Ethics approval and consent to participate This study was approved by the Ethics Committee of Peking Union Medical College Hospital. Additional information Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Rights and permissions About this article Cite this article Li, X., Zhang, W., Chao, X. et al. Clinical characteristics difference between early and late recurrence of ovarian endometriosis after laparoscopic cystectomy. Arch Gynecol Obstet 302, 905–913 (2020). https://doi.org/10.1007/s00404-020-05657-5 Received: Accepted: Published: Version of record: Issue date: DOI: https://doi.org/10.1007/s00404-020-05657-5