Risk factors for recurrent endometriosis after conservative surgery in a quaternary care center in southern Thailand

Ngernprom P, Pongpan Ngernprom, Satit Klangsin, Chitkasaem Suwanrath, Krantarat Peeyananjarassri, Peeyananjarassri K
PloS one · 2023 · vol. 18(8) , pp. e0289832 · doi:10.1371/journal.pone.0289832 · PMID:37561776 · PMC10414623 · W4385732654
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⚙ AI-generated summary by claude@2026-06, 2026-06-08 ⓘ

This study identified preoperative pain, specific surgical procedures, and less than 24 months of postoperative hormonal treatment as risk factors for recurrent endometriosis after conservative surgery.

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This retrospective quaternary-center study evaluated 362 women aged 18–45 who underwent first-time conservative surgery for endometriosis (2000–2019) with at least 2 years of follow-up, using record review of clinical features, rAFS stage, surgical approach/procedures, and postoperative hormonal therapy, and defining recurrence by return of pain or a new endometrioma. The 2-year recurrence rate was 23.2%, while the overall recurrence rate was 56.4% (median time to recurrence 49 months), with recurrence accelerating over the first 5 years before slowing; only 11 women were followed beyond 9 years. In multivariable analysis, independent associations with recurrence were preoperative moderate to severe pelvic pain, undergoing surgical procedures other than unilateral oophorectomy, and shorter duration of postoperative hormonal treatment (<24 months), with longer hormonal treatment associated with lower recurrence. This paper is centrally about endometriosis — it identifies risk factors for recurrent disease after conservative endometriosis surgery, with explicit use of recurrence definitions and rAFS staging.

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Abstract

OBJECTIVES: To determine the 2-year recurrence rate of endometriosis after conservative surgery and the risk factors for recurrence. METHODS: This study retrospectively analyzed women with endometriosis who underwent conservative surgery and had at least a 2-year follow-up at a quaternary care hospital in southern Thailand from January 2000 to December 2019. Recurrent endometriosis was defined as either presence of endometrioma with a diameter ≥ 2 cm for more than three consecutive menstrual cycles or relapse of pelvic pain with the same or higher visual analog scale (VAS) score as before surgery. Multivariate logistic regression analysis was used to identify the risk factors for recurrence. RESULTS: The median (interquartile range [IQR]) age was 34 (29, 38) years in 362 cases and nearly three-quarters (74.2%) were nulliparous. Cyclic pain was the most common clinical presentation (48.9%) and the median (IQR) VAS score of pelvic pain was 6 (5, 9). Ovarian cystectomy was the most common procedure (68.1%). The 2-year recurrent endometriosis rate after conservative surgery was 23.2%, and the overall recurrence rate was 56.4%. The risk factors of recurrence were preoperative moderate to severe pelvic pain (adjusted odds ratio [aOR] 1.93; 95% confidence interval [CI], 1.12-3.34; p = 0.017), adhesiolysis/ablation/ovarian cystectomy without unilateral oophorectomy (aOR 2.71; 95% CI, 1.40-5.23; p = 0.002), and duration of postoperative hormonal treatment < 24 months (aOR 10.58; 95% CI, 5.47-20.47; p < 0.001). CONCLUSION: The 2-year recurrence rate after conservative surgery for endometriosis was 23.2%. Preoperative moderate to severe pelvic pain, procedures except unilateral oophorectomy, and postoperative hormonal treatment < 24 months were risk factors for recurrence.
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Intro

Endometriosis, which is defined as the appearance of an endometrial glands with stroma outside the endometrium, is a common benign gynecological disease that affects 10% of reproductive women [ 1 , 2 ]. Uncommonly, it was found to vary between 2% and 5% in menopausal women [ 3 ]. Similar to malignancy, it is characterized as a progressive and invasive growth that is estrogen-dependent and recurs with a tendency to metastasize. It is definitively diagnosed by histologic confirmation or by a clinically acceptable diagnosis from laparoscopic observation of the typical lesions as superficial “power-burn” or black, dark-brown, or blue “gunshot” lesions [ 1 ]. The American Society for Reproductive Medicine classifies the severity of endometriosis as minimal (I), mild (II), moderated (III), and severe (IV) using the revised American Fertility Society (rAFS) score based on intraoperative findings [ 4 ]. Treatment options of endometriosis are medical therapy with analgesic or hormonal therapy and surgery. Conservative surgery is usually performed in fertile or young women, which includes adhesiolysis, ablation or excision of the lesion, ovarian cystectomy, and unilateral oophorectomy [ 5 – 7 ]. The recurrence rates of endometriosis after conservative surgery varied according to the definition of recurrence and were reported as 9–29% and 13–30% at 2-year and overall recurrence rates, respectively [ 8 – 11 ]. Recurrent endometriosis can interfere with the quality of life and lead to repetitive surgery, difficult surgery, and finally radical surgery. The various factors reported to predict the recurrence of endometriosis after surgery included younger age, nulliparity, overweight, sexual intercourse, abnormal menstruation, presence and duration of secondary dysmenorrhea, previous hormonal use, presence of nodularity, cervical displacement on pelvic examination, and high rAFS score [ 1 , 8 , 9 , 12 – 18 ]. The recurrence rate and associated risk factors were different among studies due to the definition of recurrence, sample size, duration of follow-up, types of surgery, experience of the surgeon, and postoperative medical therapy [ 1 , 8 , 9 , 12 – 19 ]. Songklanagarind Hospital is a quaternary care referral center for 14 provinces in southern Thailand with experience in treating endometriosis for more than 20 years and our previous study showed that the cumulative recurrence rates of pain after depot medroxyprogesterone acetate (DMPA) treatment at months 12, 24, 36, 48, and 60 were 18%, 28%, 41%, 46%, and 50%, respectively [ 20 ]. Long-term follow-up for the recurrence of endometriosis in women who undergo conservative surgery has not been evaluated. Therefore, we aimed to determine the 2-year recurrence rate of endometriosis after conservative surgery and the predictive factors for recurrence.

Results

The records of 367 women who underwent conservative surgery for endometriosis were reviewed. After excluding 2 women due to chemotherapy and 3 women due to pregnancy, 362 women were included in the study. Table 1 and S1 Table show the demographic and clinical characteristics, surgical approaches, operative findings, and postoperative data of the recurrence and non-recurrence groups. BMI, body mass index; mm, millimeter; rAFS, revised American Fertility Society; VAS, visual analog scale. a Data are presented as median (interquartile range). b Some patients underwent surgery with more than one procedure. Data were compared using Wilcoxon Rank Sum test for continuous data and the chi-square test or Fisher’s exact test for categorical data. P values of 0.05 were significant and analyzed between the non-recurrence and recurrence groups. The most common clinical presentation was cyclic pain. Laparoscopy was the most common approach and 6.8% of cases were converted to laparotomy. The majority of conservative surgeries were adhesiolysis and/or ablation and/or ovarian cystectomy. Based on intraoperative findings, ovarian endometrioma was found in most cases. Post-operative hormonal treatment was administered in 237 women: DMPA (154), continuous combined oral contraceptives (COCs) (58), cyclic COCs (49), gonadotropin releasing hormone (GnRH) agonists (49), dienogest (39), levonorgestrel-releasing intrauterine system (LNG-IUS) (11), and monthly injectable contraceptives (9). Some patients had more than one hormonal treatment. Compared to the non-recurrence group, the recurrence group was younger, had a higher rate of infertility, longer duration of a second dysmenorrhea, higher rate of operations other than unilateral oophorectomy, absence of endometrioma, lower rate of severe stage by rAFS, and a lower rate of receiving post-operative hormonal treatment. The cumulative recurrence rates of endometriosis after conservative surgery are shown in Fig 1 . The two-year recurrence rate was 23.2% (84/362 cases), whereas the overall recurrence rate was 56.4% with a median (IQR) duration of recurrence of 49 months (42, 55). The earliest time of recurrence was 3 months after surgery. During the first 5 years, a rapidly increasing rate of recurrence was observed, then the rate of recurrence became slower and finally constant after 9 years. However, only 11 cases were followed up after 9 years. Univariate analysis and Cox’s multivariate proportional hazard analysis were performed ( Table 2 ). From the univariate analysis, we chose 11 factors with a p-value 35 years), (ii) duration of dysmenorrhea (< 12 vs. ≥ 12 months), (iii) severity of preoperative pelvic pain (none to mild vs. moderate to severe), (iv) dyspareunia (no/yes), (v) infertility (no/yes), (vi) palpation of pelvic mass (no/yes), (vii) surgical approach (laparotomy vs. laparoscopy), (viii) adenomyosis (no/yes), (ix) procedure (unilateral oophorectomy with or without adhesiolysis/ablation/ovarian cystectomy vs. adhesiolysis/ablation/ovarian cystectomy), (x) rAFS stage of endometriosis (minimal to mild vs. moderate to severe), and (xi) duration of postoperative hormonal treatment (< 24 vs. ≥ 24 months). We did not choose the factors following endometrioma and size of largest endometrioma for the univariate analysis because those factors are the components of rAFS score calculation. We found three factors that were independently associated with recurrence: preoperative moderate to severe pelvic pain, surgical procedures other than unilateral oophorectomy (adhesiolysis/ablation/ovarian cystectomy), and duration of postoperative hormonal treatment < 24 months. Fig 2 . compares the 3 groups of women who received no postoperative hormonal treatment (91/125 [72.8%]), postoperative hormonal treatment < 24 months (69/86 [80.2%]), and postoperative hormonal treatment ≥ 24 months (44/151 [29.1%]) in terms of recurrence of endometriosis after conservative surgery. Only postoperative hormonal treatment ≥ 24 months had a significantly lower recurrence rate. OR, odds ratio; 95% CI, 95% confidence interval. Significant risk factors using multivariate logistic regression at a p value of 0.05. In women with recurrent endometriosis, lesion and pain recurrences were the most common clinical presentations (42.6%) followed by recurrence of pain (30.9%) and recurrence of lesion (26.5%). The most common symptom presentation was dysmenorrhea (63.7%). Treatments in recurrent endometriosis were medication (61.3%), surgery (38.2%), and follow-up (0.5%).

Conclusions

The two-year recurrence rate of endometriosis after conservative surgery was 23.2%, while the overall recurrence rate was 56.4%. Preoperative moderate to severe pelvic pain, procedures that include adhesiolysis/ablation/ovarian cystectomy, except unilateral oophorectomy, and a postoperative hormonal treatment duration less than 24 months were risk factors for recurrence.

Materials|Methods

A retrospective study was conducted at Songklanagarind Hospital after protocol approval by the Human Research Ethics Committee of the Faculty of Medicine, Prince of Songkla University (REC.64-210-12-4). The study population included women with endometriosis who underwent conservative surgery between January 2000 and December 2019. Diagnosis was confirmed by either pathologic examination or intraoperative visualization of a typical endometriosis lesion. The inclusion criteria included age 18–45 years, received conservative surgery for the first time, and at least a 2-year follow-up after surgery. Patients who had emergency surgery for endometriosis, received radiotherapy, chemotherapy, or tamoxifen during follow-up, and pregnancy at the time of surgery were excluded. The medical records of all eligible women were reviewed. Data collection included age, body mass index (BMI), symptoms of dysmenorrhea, infertility, parity, vaginal bleeding patterns according to the FIGO recommendation of 2011 [ 21 ], previous hormonal treatment, size of endometrioma, location of cysts, presence of adenomyosis or leiomyoma, presence of deep endometriosis, type of conservative surgery, approach of surgery, operative time, intraoperative blood loss, rAFS score, postoperative hormonal treatment, postoperative pregnancy, and recurrence time. The size of an endometrioma was defined as the largest diameter of the cysts. Obliteration of the pouch of Douglas was defined as any adhesion in the pouch. Pain was rated on the basis of a 10-cm visual analog scale (VAS) score, and the intensity was divided into none (0), mild (1–4), moderate (5–7), and severe (8–10) [ 8 ]. The indications for conservative surgery in our routine practice are fertility desire, or the preservation of ovarian function and an ovarian endometrioma ≥ 4 cm, or pelvic pain with medical treatment failure. The surgical procedures depended on the endometriotic lesion, malignancy concern, and the operators’ preference. Conservative surgery was performed by fellows training in obstetrics and gynecology or gynecologic staff doctors. The surgical procedures were as follows: Adhesiolysis: a procedure used to separate or remove adhesions using scissors, cauterization, and blunting. Ablation: using an electrical current technique to destroy the endometriotic lesions. Excision of endometriotic lesion: removing the endometriotic lesions such as endometriotic spot, bleb or deep infiltrative lesion using scissors or cauterization. Ovarian cystectomy: a stripping technique used to remove the endometriotic cyst wall after the plane between the cyst wall and the ovarian tissue has been cleaved. Unilateral oophorectomy: a surgery that removes all ovarian pathology while leaving the contralateral ovary intact. After surgery, the patients were observed for recurrence every 3 months for 1–2 years, then every 6–12 months thereafter. Postoperative hormonal treatment was prescribed for some patients based on pregnancy desire and clinical judgement of the staff doctors. The recurrence of endometriosis was defined as either pain or endometrioma that recurred during follow-up. The pain recurrence was defined as relapse of pain with a VAS score of at least equal to the score before surgery for at least 3 months. Recurrent endometrioma was defined as the presence of a new ovarian cyst characterized by a thin wall with a diameter of at least 2 cm, regular margin, and homogenous low echogenic fluid content with scattered internal echoes that, persisted for 3 consecutive menstrual cycles [ 8 ]. The statistical analysis was performed using R 4.1.3 (R Foundation for Statistical Computing, Vienna, Austria). The data were presented as absolute numbers and percentages for categorical variables and as the median and interquartile range (IQR) for continuous variables. A univariate analysis was initially performed to identify any potential predictor variables. Variables with a p-value < 0.2 according to the univariate analysis and variables considered to be clinically relevant were included in a multivariate analysis to determine any independent predictors. A multivariate logistic regression analysis was used to determine the associations of the potential risk factors with the primary outcome variables and to estimate the adjusted odds ratios (aOR) and the 95% confidence intervals (CI). We used a variable inflation factor below 5 to avoid multicollinearity for a logistic regression model. A stepwise selection procedure was used to identify variables with a p-value < 0.05.

Supplementary Material

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Outcome instruments

VAS-pain

Condition tags

endometriosischronic_pelvic_painendometrioma

MeSH descriptors

Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis Endometriosis

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