Skip to main content

Factors associated with recurrent endometriomas after surgical excision

Abstract

Background

Endometriosis affects women in reproductive age and causes a great impact on their lives. When affecting the ovary, excision represents the main management option. However, recurrence represents a challenging situation for patients and physicians. This study aimed to determine factors contributing to endometriomas recurrence after surgical excision.

Results

This was a quasi-experimental study recruiting 60 patients with ovarian endometrioma. The mean age was 30.33 ± 7.95 years. The mean parity was 1.27 ± 0.69. The recurrence rate after excision was 11/60 (18.3%) after a mean follow-up period of 22.62 ± 4.96 months. None of the patients’ characteristics or endometriosis-related characteristics were significant factors contributing to cyst recurrence (age, parity, history of infertility, preoperative endometrioma diameter, preoperative AFC, preoperative AMH, degree of pelvic pain, degree of dysmenorrhea, degree of dyspareunia, pelvic tenderness, and induration) (p value > 0.05).

Conclusion

The patient’s related factors and endometrioma characteristics did not predict its recurrence.

Background

Endometriosis is a gynecological condition which affects women of reproductive age, causing infertility, dysmenorrhea, and dyspareunia [1]. Surgical excision is the principal treatment, as medical options are of limited efficacy. Although effective, surgery is associated with multiple complications, with recurrence representing a challenging one reaching 40–45% after 5 years [2] and reoperation rates of 27% [3]. Additionally, fertility decline was noted to be more prominent after further interventions rather than after primary surgery [4]. This makes endometriosis a dreadful disease, and concerns about avoiding recurrence are paramount [5]. Several studies evaluated the role of adjuvant therapies in preventing recurrence as hormonal treatments [6]. Variable results were reported with a predilection toward the insignificant impact of hormonal treatment in preventing recurrence [7, 8]. Determining possible factors associated with recurrent endometriomas would influence treatment decisions and optimize treatment planes [9]. Accordingly, this study evaluated factors affecting endometrioma recurrence after laparoscopic excision.

Methods

This quasi-experimental study was conducted in the Obstetrics and Gynecology Department at Suez Canal University Hospital from November 1, 2020, to July 31, 2022. We recruited eligible patients during the study duration according to prespecified inclusion and exclusion criteria. Inclusion criteria: (a) unilateral endometrioma, (b) unilocular endometrioma 3–8 cm, (c) age 18–45 years, (d) regular cycles, (e) no previous history of ovarian operations, and (f) patients undergoing surgical excision of the endometrioma by laparoscopy. Exclusion criteria: (a) suspected or confirmed malignancy, (b) women within 2 years of menarche, (c) women on progesterone only or combined hormonal contraception, (d) women refusing to participate in the study, and (f) women preferring medication for the management of endometriomas.

Informed consent was obtained from all eligible study participants after adequately explaining the study procedures and aim. Eligible patients were subjected to the following:

  1. 1-

    Complete personal and medical history. Data about pelvic pain, dysmenorrhea, and dyspareunia were obtained and graded as mild, moderate, or severe.

  2. 2-

    The local gynecological examination, performed by the same researcher, focused on evaluating pelvic tenderness and induration and was graded into mild, moderate, or severe.

  3. 3-

    Ultrasound examination to diagnose ovarian endometrioma and measure its diameter [10]. The antral follicle count (AFC) of the affected ovary was evaluated on days 2–3 of the cycle by determining the number of follicles measuring 2–10 mm [11].

  4. 4-

    Routine preoperative laboratory investigations such as complete blood count, coagulation profile, liver function test, and anti-mullerian hormone (AMH) were withdrawn.

  5. 5-

    Patients were prepared for laparoscopic cystectomy. Any adhesions were lysed to free the ovary before excision. An incision in the endometrioma was done. Suction of the endometrioma contents was done. Stripping of the cyst wall from the ovarian tissue was done. Handling of the ovary was done using atraumatic grasping forceps. Bipolar cauterization was used to achieve hemostasis using pinpoint coagulations to avoid thermal damage to the ovary. Complete removal of the cyst wall was ensured [12]. No hormonal treatment was offered after the operation.

  6. 6-

    Initial follow-up visit was after 3 months. However, longer duration of follow-up was recommended to evaluate recurrences properly. Accordingly, further follow-up was done after at least 1 year of the operation. Recurrence was defined as cyst diameter > 10 mm [5].

Statistical analysis

Data were statistically described as mean and standard deviation, frequencies (number of cases), and percentages when appropriate. P value of less than 0.05 were considered statistically significant. All statistical calculations were done using the computer program SPSS (Statistical Package for the Social Science; SPSS Inc., Chicago, IL, USA), release 23 for Microsoft Windows. Comparison between patients with recurrent endometriosis and those without was done by the student T test. Multivariate and univariate regression analysis was performed to determine possible factors associated with cyst recurrence.

Results

Sixty patients were recruited throughout the study duration. The mean age was 30.33 ± 7.95 years. The study population was either virgins or married/divorced/widowed equally. The mean parity of the married/divorced/widowed patients was 1.27 ± 0.69. The mean follow-up period was 22.62 ± 4.96 months (Table 1).

Table 1 Basic demographic data of the studied population (N = 60)

The recurrence rate after excision was 11/60 (18.3%). The mean endometrioma size after recurrence was 3.27 ± 0.17. There was no significant difference in the ovarian reserve either before or after surgery as represented by AMH and AFC levels between patients who had recurrent endometriosis and those who did not (P value > 0.05) (Table 2). There was no significant difference in the extend of dysmenorrhea between both groups (p value 0.575).

Table 2 Ovarian reserve and endometrioma size between patients with recurrent endometriomas and those without

None of the patients’ characteristics or endometriosis-related characteristics were significant factors contributing to cyst recurrence by multivariate analysis (age, parity, history of infertility, preoperative endometrioma diameter, preoperative AFC, preoperative AMH, degree of pelvic pain, degree of dysmenorrhea, degree of dyspareunia, pelvic tenderness, and induration) (p value > 0.05) (Table 3).

Table 3 Multivariate analysis for the factors affecting recurrent endometriomas after laparoscopic excision

Discussion

After surgical excision, recurrence was noted in 18.3% of the participants. The recurrence rate after endometrioma excision was reported to be high. It ranged from 29 to 56% after 2 years, while after 5 years, it was 43% [13] without postoperative medical treatment. Another study reported a recurrence rate of 6.4%. This study conducted follow-up visits every 3 months of surgery, and the results were reported after a mean follow-up period of 22.62 ± 4.96 months, while they reported their results after 5 years. A large number of their participants received postoperative hormonal treatment in the form of oral contraceptives, Mirena for at least 1 year, Gonadotropin releasing hormone analogs (GnRHa) for 3–6 months, or GnRHa followed by Mirena. Only 3.4% of their studied population did not receive any hormonal treatment which might impact the recurrence rates after surgery [14]. Hormonal treatment leads to apoptosis of the ectopic endometrial implants either in the pelvis or de novo implants leading to decreased recurrences [15]. The current study provided no medical treatment after surgery. Immune cells and extracellular matrix metalloproteinase lead to the proliferation and survival of endometriotic cells, explaining recurrent endometriosis [16].

Recurrent endometriosis differed in its rate between studies. This was rendered to the variable factors contributing to its recurrence as the definition of recurrence depended on subjective pain sensation or clinical and radiological evaluation. Also, the type of endometriosis, disease severity, method of excision, surgical skills, and time to recurrence was reported [5]. The evaluation of recurrence depending on symptoms was higher than the sonographic evaluation, with a poor correlation between pain and actual recurrence [17]—the current study evaluated recurrence using ultrasound after 3 months of excision.

There was no difference in the endometrioma size before surgery among women with recurrent endometriosis and those without. Also, there was no difference in age, parity, extend of dysmenorrhea, and the ovarian reserve before and after surgery among both groups. This was evident in an earlier study where there was no difference in patients’ age, parity, and BMI among those with recurrent endometriosis and those without. However, the extent of dysmenorrhea was increased significantly among those with recurrent endometriosis (p value 0.001) [14]. This difference would be related to the presence of concomitant conditions as adenomyosis which was not evaluated in our study population. it has been reported that dysmenorrhea was evident in women with adenomyosis due to associated deeply situated dense endometrial glands in the myometrium [18].

The current study demonstrated no significant risk factor associated with cyst recurrence. Another study done by Koga et al. 2006 demonstrated that previous history of medical treatment and endometrioma size predicted recurrence significantly [19]. An earlier study reported that younger age at surgery was associated with recurrent endometriosis. This was rendered to the increased estrogen concentration in younger women leading to preoperative hormonal treatment which results in atrophy and reduced size of the endometriotic lesions leading to missed removal in surgery [20]. It has been reported that risk factors contributing to endometriosis recurrence were heterogeneous among studies. The stage of endometriosis, adhesions, and size and number of endometrioma did not influence recurrence while previous surgery was significantly associated with recurrence. This was explained by the progressive and aggressive nature of the disease [21]. Another study concluded that dysmenorrhea and ovarian cyst separations were associated with endometrioma recurrence [22]. Dysmenorrhea was rendered to the disease itself as a result of bleeding from focal endometriotic implants, release of inflammatory mediators, and direct irritation of the pelvic nerves and peritoneum [22]. While Selcuk et al. mentioned that deeply penetrating endometrial tissue in the ovary was significantly associated with recurrent endometrioma [23]. This was explained by decreased apoptosis and increased proliferation with deeply infiltrated endometriosis [22].

Other mechanical factors explaining recurrent endometriosis were regrowth of endometriotic lesions from residual loci [24], which was emphasized by the reappearance of endometriotic lesions at the same site after excision [25]. The use of laser ablation results in prevention of recurrence for at least 2 years, which elaborates the role of abnormal uterine contraction in the generation of ectopic endometrial implants [26, 27]. Lymph node involvement has also been reported as a possible cause of recurrence [28]. Immunological factors contribute to endometriotic spots’ de novo or in situ regeneration. It has been reported that CD-16 expressing natural killer cells are abundant in the peritoneal fluid and blood of women with endometriosis and are not affected by surgical excision or hormonal therapy [29].

Variable results were rendered to multiple factors, including different surgical procedures adopted, different surgical experiences, different outcome measures, different types and stages of endometriosis between studies, different target populations, and the evaluation duration. Also, a possible bias in selection and recruitment, recall and data reporting, and inaccurate statistical analysis would contribute to the contradictory results. Incomplete removal of endometriomas because of extensive pelvic adhesions contributed to endometrioma recurrence. Additionally, different methodologies and power between studies are paramount [5, 14]. The presence of associated conditions as adenomyosis was associated with increased recurrence rates; however, this was not evaluated in the current study [30].

Strengths of the study

The study used the same technique of the surgical excision performed by the same surgical team. The recurrence rate was evaluated depending on recurrence in the same ovary. Recurrence was evaluated depending on ultrasound visualization of the cyst rather than depending on symptoms.

Limitations of the study

The follow-up duration was relatively small from 12 to 30 months. The sample size was small. Pregnancy rates after the intervention was not evaluated. It was performed in a single hospital which limits data generalization. We recruited women with unilocular endometriomas, while the involvement of women with multilocular cysts would be more informative.

Conclusion

The patient’s related factors and endometrioma characteristics did not predict its recurrence.

Availability of data and materials

Not applicable.

Abbreviations

ANC:

Antral follicle count

AMH:

Anti-Mullerian hormone

rAFS:

Revised American Fertility Society

References

  1. Farquhar CM (2000) Endometriosis Extracts from the clinical evidence. BMJ 320:1449–1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Garry R (2004) The effectiveness of laparoscopic excision of endometriosis. Curr Opin Obstet Gynecol 16(4):299–303

    Article  PubMed  Google Scholar 

  3. Cheong Y, Tay P, Luk F, Gan HC, Li TC, Cooke I (2008) Laparoscopic surgery for endometriosis: how often do we need to re-operate? J Obstet Gynaecol 28(1):82–85

    Article  CAS  PubMed  Google Scholar 

  4. Vercellini P, Somigliana E, Viganò P, De Matteis S, Barbara G, Fedele L (2009) The effect of second-line surgery on reproductive performance of women with recurrent endometriosis: a systematic review. Acta Obstet Gynecol Scand 88(10):1074–1082

    Article  PubMed  Google Scholar 

  5. Guo SW (2009) Recurrence of endometriosis and its control. Hum Reprod Update 15(4):441–461

    Article  PubMed  Google Scholar 

  6. Prentice A (2001) Regular review-endometriosis. BMJ 323(7304):93–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Muzii L, Marana R, Caruana P, Catalano GF, Margutti F, Panici PB (2000) Postoperative administration of monophasic combined oral contraceptives after laparoscopic treatment of ovarian endometriomas: a prospective, randomized trial. Am J Obstet Gynecol 183(3):588–592

    Article  CAS  PubMed  Google Scholar 

  8. Furness S, Yap C, Farquhar C, Cheong YC. Pre and postoperative medical therapy for endometriosis surgery. Cochrane Database Syst Rev 2004;3:CD003678. https://doi.org/10.1002/14651858.CD003678.pub2. Accessed 11 Aug 2023.

  9. Koga K, Osuga Y, Takemura Y, Takamura M, Taketani Y (2013) Recurrence of endometrioma after laparoscopic excision and its prevention by medical management. Front Bioscience-Elite 5(2):676–683

    Article  Google Scholar 

  10. Van Holsbeke C, Van Calster B, Guerriero S, Savelli L, Paladini D, Lissoni AA, ..., Timmerman D (2010) Endometriomas: their ultrasound characteristics. Ultrasound Obstetrics Gynecol 35(6):730–740

  11. Broekmans FJ, de Ziegler D, Howles CM, Gougeon A, Trew G, Olivennes F (2010) The antral follicle count: practical recommendations for better standardization. Fertil Steril 94(3):1044–1051

    Article  PubMed  Google Scholar 

  12. Saeki A, Matsumoto T, Ikuma K, Tanase Y, Inaba F, Oku H, Kuno A (2010) The vasopressin injection technique for laparoscopic excision of ovarian endometrioma: a technique to reduce the use of coagulation. J Minim Invasive Gynecol 17(2):176–179

    Article  PubMed  Google Scholar 

  13. Lee DY, Bae DS, Yoon BK, Choi D (2010) Post-operative cyclic oral contraceptive use after gonadotrophin-releasing hormone agonist treatment effectively prevents endometrioma recurrence. Hum Reprod 25(12):3050–3054

    Article  CAS  PubMed  Google Scholar 

  14. Li X Y, Chao XP, Leng JH, Zhang W, Zhang JJ, Dai Y, ..., Wu YS (2019) Risk factors for postoperative recurrence of ovarian endometriosis: long-term follow-up of 358 women. J Ovarian Res 12(1):1–10

  15. Vercellini P, Somigliana E, Daguati R, Vigano P, Meroni F, Crosignani PG (2008) Postoperative oral contraceptive exposure and risk of endometrioma recurrence. Am J Obstet Gynecol 198(5):504 e1–5

  16. Salvatore GV, 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. The Role of Oxidative Stress and Membrane Transport Systems during Endometriosis: A Fresh Look at a Busy Corner. Oxid Med Cell Longev. 2018;2018(7924021):14. https://doi.org/10.1155/2018/7924021.

  17. Exacoustos C, Zupi E, Amadio A, Amoroso C, Szabolcs B, Romanini ME, Arduini D (2006) Recurrence of endometriomas after laparoscopic removal: sonographic and clinical follow-up and indication for second surgery. J Minim Invasive Gynecol 13(4):281–288

    Article  PubMed  Google Scholar 

  18. Mehasseb MK, Bell SC, Pringle JH, Habiba MA (2010) Uterine adenomyosis is associated with ultrastructural features of altered contractility in the inner myometrium. Fertil Steril 93(7):2130–2136

    Article  PubMed  Google Scholar 

  19. Koga K, Takemura Y, Osuga Y, Yoshino O, Hirota Y, Hirata T, ..., Taketani Y (2006) Recurrence of ovarian endometrioma after laparoscopic excision. Hum Reprod 21(8):2171–2174

  20. Blumenfeld Z (2004) Hormonal suppressive therapy for endometriosis may not improve patient health. Fertil Steril 81(3):487–492

    Article  CAS  PubMed  Google Scholar 

  21. Busacca M, Marana R, Caruana P, Candiani M, Muzii L, Calia C, Bianchi S (1999) Recurrence of ovarian endometrioma after laparoscopic excision. Am J Obstet Gynecol 180(3):519–523

    Article  CAS  PubMed  Google Scholar 

  22. Chon SJ, Lee SH, Choi JH, Lee JS (2016) Preoperative risk factors in recurrent endometrioma after primary conservative surgery. Obstet Gynecol Sci 59(4):286–294

    Article  PubMed  PubMed Central  Google Scholar 

  23. Selcuk S, Cam C, Koc N, Kucukbas M, Ozkaya E, Eser A et al (2016) Evaluation of risk factors for the recurrence of ovarian endometriomas. Eur J Obstet Gynecol Reprod Biol 203:56–60

    Article  PubMed  Google Scholar 

  24. Nisolle-Pochet M, Casanas-Roux F, Donnez J (1988) Histologic study of ovarian endometriosis after hormonal therapy. Fertil Steril 49(3):423–426

    Article  CAS  PubMed  Google Scholar 

  25. Vignali M, Bianchi S, Candiani M, Spadaccini G, Oggioni G, Busacca M (2005) Surgical treatment of deep endometriosis and risk of recurrence. J Minim Invasive Gynecol 12(6):508–513

    Article  PubMed  Google Scholar 

  26. Bulletti C, DeZiegler D, Stefanetti M, Cincinelli E, Pelosi E, Flamigni C (2001) Endometriosis: absence of recurrence in patients after endometrial ablation. Hum Reprod 16(12):2676–2679

    Article  CAS  PubMed  Google Scholar 

  27. Kunz G, Beil D, Huppert P, Leyendecker G (2000) Structural abnormalities of the uterine wall in women with endometriosis and infertility visualized by vaginal sonography and magnetic resonance imaging. Hum Reprod 15(1):76–82

    Article  CAS  PubMed  Google Scholar 

  28. Thomakos N, Rodolakis A, Vlachos G, Papaspirou I, Markaki S, Antsaklis A (2006) A rare case of rectovaginal endometriosis with lymph node involvement. Gynecol Obstet Invest 62(1):45–47

    Article  PubMed  Google Scholar 

  29. Maeda N, Izumiya C, Kusum T, Masumoto T, Yamashita C, Yamamoto Y, ..., Fukaya T (2004) Killer inhibitory receptor CD158a overexpression among natural killer cells in women with endometriosis is undiminished by laparoscopic surgery and gonadotropin releasing hormone agonist treatment. Am J Reprod Immunol 51(5):364–372

  30. Fauconnier A, Chapron C (2005) Endometriosis and pelvic pain: epidemiological evidence of the relationship and implications. Hum Reprod Update 11(6):595–606

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Not applicable. The authors are compliant to respond to any post-publication queries regarding this study. Contact would be through the corresponding author.

Funding

Self-funded.

Author information

Authors and Affiliations

Authors

Contributions

KH Atwa: protocol/project development and manuscript writing/editing. OT Taha: data collection and analysis. EM El Bassuony: data collection and management and manuscript writing/editing. ZM Ibrahim: protocol/project development, manuscript writing/editing, data analysis, and manuscript writing/editing.

Corresponding author

Correspondence to Omima T. Taha.

Ethics declarations

Ethics approval and consent to participate

All procedures performed in in the study were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was conducted after the approval of our research ethics committee. Informed consent was obtained from all participants before recruitment.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Atwa, K.A., Ibrahim, Z.M., Bassuony, E.M.E. et al. Factors associated with recurrent endometriomas after surgical excision. Middle East Fertil Soc J 28, 21 (2023). https://doi.org/10.1186/s43043-023-00146-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s43043-023-00146-6

Keywords