Abstract
Purpose
We aimed to examine the clinical characteristics of patients with ovarian endometriosis (OMA) who were diagnosed with recurrent pain after laparoscopic surgery in an 8- to 12- year postoperative follow-up.
Methods
We retrospectively analyzed data of 45 OMA patients with recurrent pain, including a minimum 8 years of post-laparoscopic follow-up reports. All laparoscopic cystectomy procedures were performed by the same surgeon at Peking Union Medical College Hospital between January 2009 and April 2013. Clinical data were retrieved to analyze patients' preoperative characteristics, relevant surgical findings, and postoperative outcomes at follow-up.
Results
A total of 45 patients with OMA were included, with a mean age of 31.8 ± 4.92 years. The mean recurrence period was 45.78 ± 24.89 months. Before surgery, 60 % (27/45) of patients had severe dysmenorrhea. During surgery, 93.3 % (42/45) of patients were in stage III/IV, 51.1 % (23/45) had coexisting adenomyosis, and 66.7 % (30/45) had deep infiltrating endometriosis (DIE). For the whole study group, mean follow-up time was 121.96 ± 15.55 months. All patients underwent postoperative medical treatment. The mean recurrence period was 45.78 ± 24.89 months. Cyst recurrence was presented in 24.4 % (11/45) of patients, while 75.6 % (34/45) only complained of pain recurrence. At the end of follow-up, spontaneous pregnancy was seen in 24.4 % (11/45) of patients and 6.7 % (3/45) received in vitro fertilization and embryo transfer (IVF-ET).
Conclusions
Patients with symptomatic recurrence after surgery had more severe dysmenorrhea, larger proportion of coexisting adenomyosis and DIE, and a higher revised American Fertility Society (rAFS) stage. Recurrence of endometrial cysts was not related to pain recurrence. Long-term postoperative pharmacological therapy is recommended to reduce recurrence.
Keywords: Endometriosis, Pain, Laparoscopic cystectomy, Recurrence, Postoperative outcomes
Highlights
-
•
Patients with symptomatic recurrence frequently had coexisting adenomyosis and deep infiltrating endometriosis as well as a higher revised American Fertility Society stage.
-
•
There was no relationship to recurrence of endometrioma cyst.
-
•
Long-term postoperative pharmacological therapy is recommended to reduce recurrence.
1. Introduction
Endometriosis (EM), defined as the ectopic growth of stroma and endometrial glands outside the uterus [1], has an estimated prevalence of 10–15 % in women of reproductive age [2]. EM lesions can be classified into three subtypes based on their location and histological characteristics, including deep infiltrating endometriosis (DIE), cystic ovarian endometriosis/endometrioma (OMA), and superficial peritoneal endometriosis [3]. Among EM lesion types, OMA is the most frequently observed phenotype, accounting for 17–44 % of EM cases. Laparoscopic cystectomy, the gold standard for OMA diagnosis, is also recommended as the first-line therapy [4], [5], [6].
The recurrence rate of OMA following surgical intervention remains high, even for those who receive postoperative medical therapy. Therefore, recurrence of pain is one of the most important unresolved problems in the management of endometriosis. Previous research shows that the cumulative 5-year rate of pain recurrence is 33.4 % [7]. Surprisingly, few studies have analyzed the clinical features of patients who experience pain recurrence after surgery. Therefore, the aim of this study was to analyze the clinical data of recurrent endometriosis-related pain after long-term follow up among OMA patients.
2. Materials and methods
This study was performed in the Department of Obstetrics and Gynecology of the Peking Union Medical College Hospital (PUMCH), with prior approval from the Medical College Ethics Committee (I-22PJ661).
We retrieved data of OMA patients who received laparoscopic cystectomy at PUMCH between January 2009 and April 2013. All operations were performed by the same EM-specialized surgery team and patients were histopathologically diagnosed as having OMA. Patients were excluded if they were menopausal, pregnant, had complicated malignant gynecological diseases, or received any hormonal therapy within 3 months before the surgery.
During surgery, OMA cysts were carefully stripped and all identifiable peritoneal implants were cleared. The revised American Fertility Society (rAFS) scoring system was applied to score patients along with EM staging. DIE was diagnosed histologically if the lesion infiltrated > 5 mm under the peritoneal surface. Pain recurrence was defined as symptoms recurring at least 3 months after surgery.
According to these criteria, a total of 45 patients were included. Adenomyosis was confirmed by ultrasonic diagnostics criteria including globular-appearing uterus, asymmetrical thickness of the anteroposterior wall of the myometrium, heterogeneous myometrial echotexture, sub-endometrial echogenic linear striations, sub-endometrial myometrial cysts, and poor definition of the endometrial-myometrial junction[8], [9]. Patients who received biopsy or adenomyomectomy during the surgery were diagnosed via postoperative pathology.
The size of OMA cysts was defined as the largest diameter of cysts measured by ultrasound examinations. An elevated serum CA-125 level was defined as > 35 U/mL, according to the clinical laboratory references at PUMCH. The possibility of infertility in women was diagnosed when the patient was unable to conceive for more than 1 year despite having a normal sex life without using any contraceptives, after ruling out any male etiological factors of infertility.
Clinical indications before and after surgery including body mass index (BMI), age, parity, history of surgery, symptoms of dysmenorrhea, location of cysts, size of OMA cysts, serum CA-125 level, intraoperative blood loss, operating time, and rAFS stage were retrieved and analyzed. As postoperative management, patients with a fertility need received a short-term GnRHa course of 3–6 injections. Furthermore, for patients with no fertility requirements, long-term therapy was recommended using a combination of GnRHa and a levonorgestrel intrauterine system.
All patients were examined and followed up in our outpatient clinic. Ultrasound and standard gynecological examination were conducted at 3, 6, and 12 months after surgery, then yearly during follow-up. Menstrual fertility factors and pain symptoms were also evaluated. OMA was defined as the persistent presence of ovarian cysts with a thin wall, with a diameter of at least 2 cm, low echogenic fluid content with scattered internal echoes regular margins, and persisting after cycles of menstruation. Long-term postoperative follow-up data included postoperative medications, infertility and related symptoms, and recurrence time.
Statistical analyses were performed using IBM SPSS 25.0 software. The Kruskal-Wallis test was applied to analyze continuous variables, and categorical variables were analyzed using the t-test or Fisher's exact test. All statistical tests were two-sided, and P < 0.05 was set to identify the statistical significance of the results.
3. Results
Following the inclusion criteria, a total of 45 OMA patients with recurrent pain after surgery were included in this study, Clinical and demographic features are shown in Table 1. The mean age of the patients was 31.8 ± 4.92 years; mean gravidity and parity was 0.76 ± 1.07 and 0.18 ± 0.39 times, respectively. The recurrence period of pain ranged from 6 to 100 months, with a mean of 45.78 ± 24.89 months.
Table 1.
Baseline characteristics of patients.
| Characteristic | n (%) | Mean±SD | P value |
|---|---|---|---|
| Age (years) | 31.8 ± 4.92 | - | |
| Gravidity | 0.76 ± 1.07 | - | |
| Parity | 0.18 ± 0.39 | - | |
| BMI (kg/㎡) | 20.59 ± 2.31 | - | |
| Dysmenorrhea, VAS | 6.8 ± 1.90 | - | |
| Extent of dysmenorrhea (%) | < 0.001 | ||
| Mild | 4 (8.9 %) | ||
| Moderate | 14 (31.1 %) | ||
| Severe | 27 (60.0 %) | ||
| CPP (%) | 7 (15.6 %) | ||
| Dyspareunia (%) | 18 (40.0 %) | ||
| Tenesmus (%) | 13 (28.9 %) | ||
| Dyschizia (%) | 4 (8.9 %) | ||
| Ca125, U/mL | 107.86 ± 101.79 | ||
| Elevated Ca125 (%) | 33 (82.5 %) | ||
| Infertility (%) | |||
| No | 31 (68.9 %) | ||
| Primary | 9 (20.0 %) | ||
| Secondary | 5 (11.1 %) | ||
| Laterality | 0.031 | ||
| Left | 9 (20.0 %) | ||
| Right | 13 (28.9 %) | ||
| Bilateral | 23 (51.1 %) | ||
| Size (cm) | |||
| Left | 5.32 ± 1.75 | ||
| Right | 5.38 ± 1.91 | ||
| Leiomyoma (%) | 11 (24.4 %) | ||
| Adenomyoma (%) | 23 (51.1 %) |
As for symptoms, dysmenorrhea was presented in all patients. For degree of dysmenorrhea, the mean VAS score was 6.8 ± 1.90 %, and 60 % of patients had severe dysmenorrhea. Seven (15.6 %) patients presented CPP. Tenesmus during menstruation and dyspareunia was seen in 13 (28.9 %) and 18 (40.0 %) patients. Four (8.9 %) patients also presented with dyschizia. The average CA-125 level was 107.86 ± 101.79 U/mL, and 33 (82.5 %) patients had an abnormal CA-125 level. According to ultrasound, nine (20.0 %) patients had a left OMS cyst with mean size of 5.32 ± 1.75 cm. Thirteen (28.9 %) patients had right OMA cyst with average size 5.38 ± 1.91 cm. Twenty-three (51.1 %) patients complained of bilateral EM cysts. Eleven (24.4 %) patients were diagnosed with leiomyoma and 23 (51.1 %) had concurrent adenomyoma. Before surgery, infertility was present in 14 (31.1 %) patients. Among infertile patients, nine (20.0 %) patients had primary infertility and five (11.1 %) had secondary infertility.
Surgical features are shown in Table 2. The mean operating time was 71.95 ± 20.97 min, and mean bleeding volume was 71.71 ± 104.35 mL. Most patients with adenomyosis (n = 16, 69.6 %) remained untreated intraoperatively; five (21.7 %) patients received adenomyoma lesion excision. During laparoscopy, 30 (66.7 %) patients were diagnosed with DIE. We separately recorded the site of DIE invasion. In 19 patients (63.3 %), DIE was located in the uterosacral (USL); in two patients (6.7 %), it was limited to the cul-de-sac. In two patients (6.7 %), DIE involved in the recto–vaginal septum, and in seven patients (23.3 %), both the USL and cul-de-sac were involved. According to the rAFS classification, the mean score was 54.74 ± 24.03.
Table 2.
Surgical characteristics.
| Characteristic | n (%) | Mean±SD | P value |
|---|---|---|---|
| Operating time (min) | 71.95 ± 20.97 | ||
| Mean bleeding volume (mL) | 71.71 ± 104.35 | ||
| DIE (%) | 30 (66.7 %) | < 0.001 | |
| USL | 19 (63.3 %) | ||
| Cul-de-sec | 2 (6.7 %) | ||
| Recto–vaginal septum | 2 (6.7 %) | ||
| USL+cul-de-sec | 7 (23.3 %) | ||
| Closed Douglas pouch (%) | 37 (82.2 %) | ||
| rAFS score | 54.74 ± 24.03 | ||
| Staging | < 0.001 | ||
| I | 0 (0 %) | ||
| II | 3 (6.7 %) | ||
| III | 11 (24.4 %) | ||
| IV | 31 (68.9 %) | ||
| AM surgery(%) | < 0.001 | ||
| No | 16 (69.6 %) | ||
| Lesion resection | 5 (21.7 %) | ||
| Biopsy | 2 (8.7 %) |
For the whole study group, mean follow-up time was 121.96 ± 15.55 months, and the median follow-up time was 120 months. Post-surgical characteristics are shown in Table 3. All patients underwent postoperative medical treatment; 42 patients (93.3 %) had short-term GnRHa injection and three patients (6.7 %) received GnRHa and LNG. The mean recurrence period was 45.78 ± 24.89 months. Cyst recurrence was present in 11 (24.4 %) patients, whereas 34 (75.6 %) patients only complained pain recurrence. At the end of follow-up, spontaneous pregnancy was seen in 11 (24.4 %) patients, and three (6.7 %) patients received in vitro fertilization and embryo transfer (IVF-ET). All pregnant patients had live births.
Table 3.
Postoperative outcomes.
| Characteristic | n (%) | Mean±SD | P value |
|---|---|---|---|
| Follow-up time (months) | 121.96 ± 15.55 | ||
| Recurrence period (months) | 45.78 ± 24.89 | ||
| Cysts recurrence (%) | 0.001 | ||
| No | 34(75.6 %) | ||
| OMA | 11(24.4 %) | ||
| Postoperative medication | |||
| GnRHa | 42(93.3 %) | ||
| GnRHa+LNG | 3(6.7 %) | ||
| Medication time(months) | 3.47 ± 1.1 | ||
| Pregnancy after surgery (%) | |||
| No | 31 (68.9 %) | ||
| Spontaneous pregnancy | 11 (24.4 %) | ||
| IVF-ET | 3 (6.7 %) |
4. Discussion
EM is considered an estrogen-dependent benign medical condition that affects 10–15 % of women of reproductive age. OMA lesions are the most common among all EM types. The recurrence rate following surgical treatment remains high. Previous studies have reported a recurrence rate of ovarian endometrioma after conservative laparoscopic surgery of 29–89.6 % at 2 years and 15.1–56 % at 5 years [10], [11], [12], [13]. The huge variability in the recurrence rate found in the literature may depend on different factors, including the definition of recurrence. In our previous study, the pain recurrence rate after laparoscopic cystectomy was 12.6 % (45/358) over 5-year follow up [14]. In this study, we initially investigated 45 patients with pain recurrence over a minimum 8-year follow-up, providing detailed information to better understand the clinical characteristics of this common condition.
Baseline characteristics of pain recurrence showed that patients with recurrent pain had more severe dysmenorrhea. As the most commonly observed symptom, dysmenorrhea affects 70–80 % of OMA patients [15]. The mechanisms of dysmenorrhea are complicated and remain undetermined; however, direct and indirect effects of cyclic focal bleeding from endometrial implants, consequent actions of inflammatory cytokines in the peritoneal cavity, and infiltration of nerves in the pelvic floor may be the cause of severe dysmenorrhea among women with endometriosis [16], [17]. These changes not only enhance dysmenorrhea but also provide a more suitable environment for implantation and development of endometriosis. Patients with severe dysmenorrhea are more likely to be complicated by multiple pelvic endometriosis; these small satellite lesions may lead to the recurrence of disease and symptoms.
Patients with pain recurrence manifested a higher rate of concurrent adenomyosis and DIE. These patients also had a higher rAFS stage and a higher proportion of closed Douglas pouch. Previous studies have reported that in patients with pain recurrence, 76.7 % have a moderate-to-severe rAFS stage [18]. Other studies have also indicated that rAFS staging is significantly correlated with pain recurrence.[19]. A higher rAFS stage points to heavier pelvic adhesions, multiple pelvic endometriosis lesions, and deeper invasive depth. These indicates enormous difficulty in completely removing all lesions during surgery. Extensive adhesions and inflammation may lead to incomplete resection, leaving small or invisible lesions remaining in the pelvis, and thereby causing recurrence.
Among all patients with recurrent pain, only 24.4 % had cyst recurrence. This suggested that ovarian cysts are not closely related to pain symptoms. Previous studies have revealed a strong connection between DIE, adenomyosis, and pain. DIE and adenomyosis are also considered risk factors for endometriosis-related pain recurrence [14]. Pain is the most evident clinical manifestation of DIE [20]. Wu et al. [21] found that OMA patients with DIE showed higher recurrence rates, with most having symptomatic recurrence. This suggests that patients with DIE are more likely to experience pain recurrence. Our study of the population with pain recurrence also showed that most patients with pain recurrence had DIE, which was consistent with previous findings. In our study, all visible pelvic endometrial lesions were excised or fulgurated during surgery. Anatomical restoration was then carried out. However, surgery does not address invisible pelvic lesions and underlying mechanisms that are active and driving disease in the pelvic cavity. DIE and a closed Douglas pouch may be indirect signs of more aggressive disease and adhesion formation, causing small endometrial lesions to be overlooked and leading to incomplete surgery, which naturally leads to recurrence of endometriosis in various forms after a certain period.
Adenomyosis is considered another risk factor of symptomatic recurrence. Previous studies observed a significant correlation between pelvic pain and the presence of adenomyosis [14]. We initially analyzed the surgical procedure of adenomyosis. We noted that adenomyosis lesion was not surgically removed in 69.6 % patients concurrent with adenomyosis. Unresolved adenomyosis may lead to symptomatic recurrence. For patients who have ovarian endometriosis coexisting with DIE or adenomyosis, it is important to identify the lesion and formulate appropriate surgical protocols.
All patients received postoperative medication, and 93.3 % had short-term GnRHa injection. The average time to relapse for patients was 45.78 months, much longer than the postoperative treatment time, which was 3.47 months. Previous studies have shown that to reduce recurrence, apart from thorough surgery, continuous consolidation of drugs also plays an important role [22]. Therefore, in addition to careful exploration of the pelvic cavity during surgery, long-term drug management should also be considered after the operation to improve the quality of life of the patient and reduce recurrence.
In all enrolled patients, 14 had successful pregnancies after surgery, and three received IVF-ET. All pregnant patients had live births. Although a lower proportion of pregnancy was shown in patients with pain recurrence, the recurrence of pain did not appear to have a significant effect on the live birth rates. The recurrence of pain may not be the cause of the lower pregnancy rate but may be the result of failed pregnancy attempts. Most patients with recurrent symptoms only received short-term postoperative pharmacological therapy, and their pain symptoms reappeared during a period after treatment was stopped. This further indicates that long-term postoperative management should be standardized for patients who have no fertility need so as to reduce the recurrence of symptoms. For patients with fertility requirements, long-term management plans should also be formulated after the completion of childbirth to reduce the recurrence of symptoms and improve patients' quality of life after surgery.
5. Conclusions
In this study, patients with symptomatic recurrence after surgery had more severe dysmenorrhea, more frequent coexisting adenomyosis and DIE, and higher rAFS staging. Recurrence of endometrial cysts was not related to pain recurrence. Long-term postoperative pharmacological therapy is recommended to reduce recurrence and improve patients' quality of life after surgery.
Ethics approval
This study was performed in the Department of Obstetrics and Gynecology of the Peking Union Medical College Hospital (PUMCH). Approval was granted by the Medical College Ethics Committee (I-22PJ661).
Author Contribution
YS Wu: Data collection, data analysis, and manuscript writing. Y Dai: Project development. JH Shi: Data collection. SQ Lyu: Data collection. ZY Gu: Data collection. CY Zhang: Data collection. HL Yan: Data collection. JH Leng: Project development and manuscript editing. XY Li: Project development and manuscript editing.
Consent to participate
Not applicable.
Consent to publish
Not applicable.
Funding
This work was supported by the National Key R&D Program (grant number: 2022YFC2704000) and National High Level Hospital Clinical Research Funding (2022-PUMCH-B-085).
CRediT authorship contribution statement
Jinghua Shi: Data curation. Yi Dai: Supervision, Conceptualization. Yushi Wu: Writing – original draft, Formal analysis, Data curation. Xiaoyan Li: Writing – review & editing, Supervision, Conceptualization. Jinhua Leng: Writing – review & editing, Funding acquisition, Conceptualization. Zhiyue Gu: Data curation. Shiqing Lyu: Data curation. Hailan Yan: Data curation. Chenyu Zhang: Data curation.
Declaration of Competing Interest
The authors have no relevant financial or non-financial interests to disclose.
References
- 1.Berveiller P., Ropert S., Mir O. Endometriosis. N Engl J Med. 2020;383(2):193–194. doi: 10.1056/NEJMc2013221. [DOI] [PubMed] [Google Scholar]
- 2.Zondervan K.T., Becker C.M., Missmer S.A. Endometriosis. N Engl J Med. 2020;382(13):1244–1256. doi: 10.1056/NEJMra1810764. [DOI] [PubMed] [Google Scholar]
- 3.Chapron C., Marcellin L., Borghese B., Santulli P. Rethinking mechanisms, diagnosis and management of endometriosis. Nat Rev Endocrinol. 2019;15(11):666–682. doi: 10.1038/s41574-019-0245-z. [DOI] [PubMed] [Google Scholar]
- 4.Giudice L.C. Clinical practice. Endometriosis. N Engl J Med. 2010;362(25):2389–2398. doi: 10.1056/NEJMcp1000274. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Falcone T., Flyckt R. Clinical Management of Endometriosis. Obstet Gynecol. 2018;131(3):557–571. doi: 10.1097/AOG.0000000000002469. [DOI] [PubMed] [Google Scholar]
- 6.Peiris A.N., Chaljub E., Medlock D. Endometriosis. JAMA. 2018;320(24):2608. doi: 10.1001/jama.2018.17953. [DOI] [PubMed] [Google Scholar]
- 7.Tobiume T., Kotani Y., Takaya H., Nakai H., Tsuji I., Suzuki A., et al. Determinant factors of postoperative recurrence of endometriosis: difference between endometrioma and pain. Eur J Obstet Gynecol Reprod Biol. 2016;205:54–59. doi: 10.1016/j.ejogrb.2016.07.516. [DOI] [PubMed] [Google Scholar]
- 8.Dueholm M. Transvaginal ultrasound for diagnosis of adenomyosis: a review. Best Pract Res Clin Obstet Gynaecol. 2006;20:569–582. doi: 10.1016/j.bpobgyn.2006.01.005. [DOI] [PubMed] [Google Scholar]
- 9.Bazot M., Darai E. Role of transvaginal sonography and magnetic resonance imaging in the diagnosis of uterine adenomyosis. Fertil Steril. 2018;109:389–397. doi: 10.1016/j.fertnstert.2018.01.024. [DOI] [PubMed] [Google Scholar]
- 10.Guo S.W. Recurrence of endometriosis and its control. Hum Reprod Update. 2009;15:441–461. doi: 10.1093/humupd/dmp007. [DOI] [PubMed] [Google Scholar]
- 11.Fedele F., Bianchi S., Zanconato G., et al. Laparoscopic excision of recurrent endometriomas: long-term outcome and comparison with primary surgery. Fertil Steril. 2006;85:694–699. doi: 10.1016/j.fertnstert.2005.08.028. [DOI] [PubMed] [Google Scholar]
- 12.Tandoi I., Somigliana E., Riparini J., et al. High rate of endometriosis recurrence in young women. J Pedia Adolesc Gynecol. 2011;24:376–379. doi: 10.1016/j.jpag.2011.06.012. [DOI] [PubMed] [Google Scholar]
- 13.Soysal S., Soysal M.E., Ozer S., et al. The effects of post-surgical administration of goserelin plus anastrozole compared to goserelin alone in patients with severe endometriosis: a prospective randomized trial. Hum Reprod. 2004;19:160–167. doi: 10.1093/humrep/deh035. [DOI] [PubMed] [Google Scholar]
- 14.Li X.Y., Chao X.P., Leng J.H., Zhang W., Zhang J.J., Dai Y., et al. Risk factors for postoperative recurrence of ovarian endometriosis: long-term follow-up of 358 women. J Ovarian Res. 2019;12(1):79. doi: 10.1186/s13048-019-0552-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Ye M., Guo H., Han J., He H., Zhang K., Xiong G., et al. Relationship between endometriosis stage, characteristics of enodmetriotic lesions and severity of dysmenorrhoea. Zhonghua Yi Xue Za Zhi. 2015;95(9):685–688. [PubMed] [Google Scholar]
- 16.Lee D.Y., Kim H.J., Yoon B.K., Choi D. Factors associated with the laterality of recurrent endometriomas after conservative surgery. Gynecol Endocrinol. 2013;29(11):978–981. doi: 10.3109/09513590.2013.824959. [DOI] [PubMed] [Google Scholar]
- 17.Fauconnier A., Chapron C. Endometriosis and pelvic pain: epidemiological evidence of the relationship and implications. Hum Reprod Update. 2005;11(6):595–606. doi: 10.1093/humupd/dmi029. [DOI] [PubMed] [Google Scholar]
- 18.Coccia M.E., Rizzello F., Palagiano A., Scarselli G. Long-term follow-up after laparoscopic treatment for endometriosis: multivariate analysis of predictive factors for recurrence of endometriotic lesions and pain. Eur J Obstet Gynecol Reprod Biol. 2011;157(1):78–83. doi: 10.1016/j.ejogrb.2011.02.008. [DOI] [PubMed] [Google Scholar]
- 19.Tobiume T., Kotani Y., Takaya H., Nakai H., Tsuji I., Suzuki A., et al. Determinant factors of postoperative recurrence of endometriosis: difference between endometrioma and pain. Eur J Obstet Gynecol Reprod Biol. 2016;205:54–59. doi: 10.1016/j.ejogrb.2016.07.516. [DOI] [PubMed] [Google Scholar]
- 20.Ferrero S., Alessandri F., Racca A., Leone Roberti Maggiore U. Treatment of pain associated with deep endometriosis: alternatives and evidence. Fertil Steril. 2015;104(4):771–792. doi: 10.1016/j.fertnstert.2015.08.031. [DOI] [PubMed] [Google Scholar]
- 21.Wu Y.S., Li X.Y., Leng J.H., et al. Clinical features and long-term outcomes after laparoscopic surgery in patients co-existing with ovarian endometrioma and deep infiltrating endometriosis. Zhonghua Fu Chan Ke Za Zhi. 2021;56(12):842–848. doi: 10.3760/cma.j.cn112141-20211009-00576. [DOI] [PubMed] [Google Scholar]
- 22.Leng J.H., Shi J.H. Risk factors and prevention strategies for recurrence of endometriosis. Zhonghua Fu Chan Ke Za Zhi. 2018;53(9):640–643. [Google Scholar]