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 Table of Contents  
Year : 2019  |  Volume : 3  |  Issue : 4  |  Page : 213-221

Analysis of the predictive factors for the recurrence of deep infiltrating endometriosis: A 2-year prospective study

1 Department of Gynecology, Obstetrics and Gynecology Hospital; Department of Obstetrics and Gynecology, Shanghai Medical School, Fudan University; Department of Gynecology, Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Shanghai 200011, China
2 Department of Gynecology, Obstetrics and Gynecology Hospital, Fudan University, Shanghai 200011, China

Date of Submission17-Apr-2019
Date of Web Publication2-Jan-2020

Correspondence Address:
Xiao-Fang Yi
Obstetrics and Gynecology Hospital, Fudan University, 419 Fangxie Road, Shanghai 200011
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2096-2924.274543

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Objective: To investigate factors that may be associated with the recurrence of deep infiltrating endometriosis (DIE) and DIE-related symptoms.
Methods: Starting in September 2014, women with a confirmed diagnosis of DIE based on surgical and histological findings were included in the prospective study with a 2-year follow-up in our hospital. A total of 84 consecutive patients were included, all of whom underwent laparoscopic surgery. The data were obtained from the medical records of the patients. Follow-up data, including presence of pain as assessed using the visual analog scale (VAS) score and ultrasonography/magnetic resonance imaging findings, were obtained at 3, 6, 9, 12, and 24 months postoperatively. Variables, such as age, body mass index, severity and duration of symptoms, size and location of the lesion, and pre- and postoperative medical treatment, were evaluated using univariate and multivariate analyses to identify factors correlated to recurrence.
Results: A total of 11 (13.1%) patients presented with recurrence, with a mean time to recurrence of 14.2 months. The univariate analysis showed that the longer duration of menstruation (7.4 vs. 6.0, P = 0.010), the more advanced revised American Fertility Society (rAFS) stage (Stages I and II vs. III and IV, χ2 = 9.964, P = 0.001), the higher VAS score for dysmenorrhea (9.4 vs. 5.2, P = 0.001), and the more severe pain during defecation (7.8 vs. 4.8, P = 0.016) were positively correlated to DIE recurrence. However, the multivariate analysis also revealed that a more severe dysmenorrhea and advanced rAFS stage were the independent factors associated with the recurrence of DIE, with an odds ratio of 1.895 (confidence interval [CI]: 1.061–3.385, P = 0.031) and 4.310 (CI: 1.091–17.028, P = 0.037), respectively.
Conclusions: More than 10% of patients presented with recurrence of DIE 2 years after surgery. Recurrence of DIE was more common in patients who complained of more severe dysmenorrhea and had an advanced rAFS stage.

Keywords: Deep Infiltrating Endometriosis; Laparoscopic Surgery; Recurrence; Revised American Fertility Society Stage; Visual Analog Scale

How to cite this article:
Zheng YX, Cheng Q, Chang KK, Ruan JY, Tian Q, Gu SX, Chen Y, Yi XF. Analysis of the predictive factors for the recurrence of deep infiltrating endometriosis: A 2-year prospective study. Reprod Dev Med 2019;3:213-21

How to cite this URL:
Zheng YX, Cheng Q, Chang KK, Ruan JY, Tian Q, Gu SX, Chen Y, Yi XF. Analysis of the predictive factors for the recurrence of deep infiltrating endometriosis: A 2-year prospective study. Reprod Dev Med [serial online] 2019 [cited 2021 Jan 17];3:213-21. Available from: https://www.repdevmed.org/text.asp?2019/3/4/213/274543

  Introduction Top

Deep infiltrating endometriosis (DIE) is a specific type of endometriosis, which affects approximately 10% of reproductive age women, and is defined as the lesions infiltrating ≥5 mm of the peritoneum.[1] Approximately 5.3%–12% of patients with DIE presented with DIE infiltrating the bowel.[2],[3] Although surgery is considered the gold standard and first-line treatment for endometriosis,[4],[5] 5%–25% of patients experience recurrence postoperatively.[6] A previous study has revealed a symptomatic recurrence rate of 43.5%, which is significantly higher than that of surgical findings of relapse.[7] Symptoms correlated to DIE infiltrating the bowel, which include severe dysmenorrhea, dyspareunia, and defecation pain, may significantly impair the patients' quality of life;[8] therefore, the recurrence of DIE poses a great clinical challenge for gynecologists as well as a burden for the patients.

Previous studies have revealed that older age, advanced revised American Fertility Society (rAFS) stage, and a lack of continuous medical treatment postoperatively [6],[9],[10],[11] may be the factors associated with the recurrence of endometriosis. Moreover, continuous hormonal treatment was not effective in decreasing the recurrence rate.[1],[10] Our group has previously identified that the different surgical procedures for DIE may affect recurrence.[12] However, the risk factors for recurrence were not determined. Whether the severity and the preoperative status would be predictive factors for the recurrence of DIE patients? This was the motivation for conducting a prospective cohort study in a university-affiliated obstetrics and gynecology hospital in China.

  Methods Top

A prospective cohort study was performed, and all patients diagnosed with DIE at the Obstetrics and Gynecology Hospital of Fudan University, Shanghai, China, were included. This study was approved by the institutional review board of our hospital. Patients who met the following criteria were included:

  1. Patients diagnosed with DIE, with lesions infiltrating ≥5 mm of the peritoneum and were confirmed via histological examinations
  2. Those with lesion at the pouch of Douglas. Bowel involvement was observed on physical examination, magnetic resonance imaging (MRI), and/or colonoscopy before surgery
  3. Those aged >18 years and <45 years old
  4. Those with complaints of at least one DIE-related symptom
  5. Those who were mentally and physically healthy and could describe their symptoms and answer questions.

Medical records, including presurgery treatments and surgical information, were reviewed. Moreover, the demographic characteristics of the patients, including body mass index (BMI), rAFS stage, and ENZIAN classification, were also obtained.

Diagnosis of deep infiltrating endometriosis

Both the clinical findings and pathological examination findings were used for the diagnosis of DIE in terms of clinical symptoms. Moreover, at least one of the following four criteria was satisfied by the patient. The final diagnosis of endometriosis was confirmed by two independent gynecological pathologists (Dr. N.Y. and Z. XR.):

  1. Clinical symptoms: Dysmenorrhea, dyspareunia, cyclic rectorrhagia, pain during defecation, or pelvic pain
  2. Physical examination: Painful nodule was detected through vagino-recto-abdominal examination or bimanual examination
  3. Ultrasonic, radiological, and/or colonoscopic examination: Transvaginal/transanal ultrasonography was recommended to each patient before the surgery and during his/her postoperative follow-up. For patients with inconclusive ultrasonography and physical examination findings, MRI and/or colonoscopy was recommended. Solid pelvic mass, thickened uterosacral ligament or bowel wall, and constricted colon were considered positive findings
  4. Surgical findings: Typical lesions in the endometriosis were found during the surgery by two experienced gynecological surgeons, which infiltrated more than 5 mm under the peritoneum.

Visual analog scale score

Visual analog scale (VAS) score was used to evaluate the pain of the patients. The intensity of symptoms was classified as none (0), mild (1–4), moderate (5–7), or severe (8–10). The following items were assessed before the surgery and 3, 6, 9, and 12 months postoperatively.

  1. Dysmenorrhea
  2. Deep dyspareunia
  3. Chronic pelvic pain (CPP), defined as noncyclic pelvic pain
  4. Ovulation period pain (OPP), defined as pelvic pain during the mid-term of the menstrual cycle
  5. Defection pain, which has been considered after ruling out rectum diseases, such as hemorrhoids
  6. Dysuria, which has been considered after ruling out urinary tract infection.

Definition for recurrence

Recurrence was defined as the reappearance of symptoms and/or clinical evidence of the disease.[13],[14] Briefly, it can be classified as follows:

  1. Symptomatic recurrence: Based on a postoperative VAS pain score >5 in women with preoperative pain symptoms
  2. Clinical findings indicative of recurrence: Pelvic masses, pelvic tenderness, or nodulations via pelvic examination
  3. Ultrasonic/radiological diagnosis of recurrence: Newly found pelvic mass that matches the diagnosis of endometriosis via ultrasound/MRI.

Statistical analysis

SPSS software version 19.0 (Chicago, Illinois, USA) was used for statistical calculations. P < 0.05 was considered statistically significant. Univariate analysis was performed using Chi-square test (or Fisher's exact test when appropriate) for categorical variables, whereas Student's t-test was performed for continuous variables. Multivariate analysis was also performed for identifying the possible risk factors of recurrence.

  Results Top

Clinical characteristics of the participants

The clinical characteristics of this cohort are summarized in [Table 1]. The average age of the participants was 35 (range: 20–49) years, with an average BMI of 20.9 (ranged: 16.2–27.9) kg/m 2. Most patients complained about dysmenorrhea (57/84, 67.9%), followed by tenesmus (21/84, 25.0%) and dyspareunia (14/84, 16.7%). The average duration of DIE-related symptoms was 35.2 (range: 1–168) months. The duration of menstruation was 6.1 (3–13)/29.2 (20–80) days, with an average menarche age of 13.6 (range: 11–16) days.
Table 1: Clinical characteristics of patients with deep infiltrating endometriosis

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Before surgery, each patient underwent transvaginal/transanal ultrasonography. Considering disease history, physical examination results, and ultrasonography findings, a total of 26 patients underwent pelvic MRI examination to determine the characteristics of the lesions. In 20 cases, the patients underwent colonoscopy.

Continuous medical treatment which included GnRH-analog (GnRH-a), oral contraceptive (OC), and Mirena ®, and long-term follow-up were performed in every patient. For patients over 40 years of age or those with other contraindications to GnRH-a injection, secondary medication was recommended. Therefore, 73 (86.9%) of 84 patients received 3–6 cycles of GnRH-a, and OC and Mirena ® were recommended in 24 (28.6%, 12 for each) of 84 patients. A total of 24 patients received combined medical treatment postoperatively.

Surgical assessment

As shown in [Table 2], the most common site involved was the uterorectal space. Lesions with an average size of 2.4 (range: 0.5–5.0) cm were found in 70.2% (59/84) of patients. Single lesion was found in most cases (65/84, 77%), and only a small proportion of the patients presented with multiple lesions. We performed the conservative surgical procedure (simple lesion cut or full-thickness disc excision) in 75 (89.3%) patients, and 40 (47.6%) patients in the multidisciplinary treatment (MDT) group underwent surgery performed by gynecological, gastrointestinal, and/or urological surgeons. The average surgical time was 155.1 (range: 23–440) min, and the average blood loss was 142.7 (range: 10–800) mL. During the surgery, we assessed the involvement of DIE lesion using the rAFS and ENZIAN system. The advanced stages (III and IV) accounted for 72.6% (61/84) of all the cases, with an average score of 47.74 (2–150). The most common ENZIAN classification was A3 (35/84, 42.9%), followed by B2 and A2 (17/84 and 15/84; 20.2% and 17.9%, respectively).
Table 2: Surgical findings during operation for patients with DIE

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Visual analog scale curve for deep infiltrating endometriosis-related painful symptoms

As shown in [Figure 1], the VAS score for DIE-related painful symptoms, including dysmenorrhea, OPP, dyspareunia, CPP, pain during defecation, and dysuria, significantly decreased postoperatively. At the end of the follow-up, the decreasing VAS scores were −5.8, −3.9, −3.4, −3.0, −2.5, and 3.0, respectively. All the results were statistically significant (all P < 0.01).
Figure 1: VAS score for DIE-related pain during 1-year follow-up. The VAS score of dysmenorrheal was 5.5, 0.4, 0.5, 0.8, and 1.0 at every evaluating time point, and other DIE-related painful symptoms shared the similar trends. At the endpoint of the study, the VAS scores were all statistically lower than preoperative evaluation (P < 0.01, all). DIE: Deep infiltrating endometriosis; VAS: Visual analog scale.

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Recurrence status

After a mean follow-up of 23.2 months, 11 (13.1%) patients presented with recurrence postoperatively [Table 3]. Only one (1.1%) patient presented with a recurrent 2-cm solid mass based on a vagino-recto-abdominal examination. Two (18.2%) of 11 patients presented with recurrent lesions in the pelvis based on ultrasonography and MRI, and 9 (81.2%) had DIE-related symptom recurrence, which included 4 cases of dysmenorrhea, 3 of CPP, 1 of OPP, 2 of dyspareunia, 2 of pain during defecation, and 2 of dysuria. The average time period for recurrence was 14.2 (range: 6–22) months postoperatively [Figure 2]. Patients with recurrence, which was mostly symptomatic recurrence, received medical treatment for pain relief, which includes OC pills, Mirena ®, or GnRH-a injection. Inpatients with recurrent lesions were detected on ultrasonography/MRI; one refused the second surgery. Meanwhile, one patient presented with frozen pelvis; thus, conservative treatment was recommended.
Table 3: Clinicopathological characteristics of recurrent DIE cases

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Figure 2: Recurrence analysis in patients with DIE. (a) All patients; (b) stratified according to rAFS stages. DIE: Deep infiltrating endometriosis; rAFS: Revised American Fertility Society.

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Univariate analysis of the indicative factors for recurrence

As shown in [Table 4], patients with longer days of menstruation (7.4 vs. 6.0 days, P = 0.010), more severe dysmenorrhea, and pain during defecation (VAS score of 9.4 vs. 5.2, P = 0.001; and 7.8 vs. 4.8, P = 0.016) presented with recurrence. In addition, all patients presented with advanced rAFS stage (III and IV) in the recurrent group, whereas only 49.3% (36/73) of patients had Stage III and IV disease (P = 0.001) in the other group (Stage I and II). Other clinicopathological factors, including demographic characteristics, size, location and number of lesions, or surgical procedures, did not significantly different between the two groups.
Table 4: Univariate analysis of clinical features of patients with DIE accompanied with or without recurrence

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Multivariate analysis of the indicative factors for recurrence

Factors that significantly differed in the univariate analysis were used in the multivariate analysis [Table 5]. Higher VAS scores for dysmenorrhea and advanced rAFS stage were considered an independent indicative factor for recurrence, with an odds ratio (OR) of 1.895 (95% confidence interval [CI]: 1.061–3.385, P = 0.031) and 4.310 (95% CI: 1.091–17.028, P = 0.037), respectively.
Table 5: Logistic regression analysis of factors related to the recurrence of DIE

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  Discussion Top

Previous studies have revealed that laparoscopic excision of DIE lesions could relieve DIE-related symptoms [15] and improve the quality of life [16] and reproductive outcomes.[17] Unfortunately, even in patients managed in specialized medical centers, recurrence is still commonly observed postoperatively.[13],[18] With the 4-year follow-up of 1,106 patients with endometriosis, Busacca et al. found that the recurrent rate was significantly higher in the DIE group than in the groups with other types of endometriosis (30.6%, 24.6%, 17.8%, and 23.7% for DIE, ovarian, pelvic, and ovarian plus pelvic types, respectively, P < 0.05).[13] In our study, the recurrence rate was 13.1% (11/84) during the 2-year follow-up, which is similar to that of other studies.[19] However, till today, the high-risk factors of the recurrence of DIE in China remained unsolved.

From 2004 to 2018, we searched for published papers in PubMed and Web of Knowledge using the following key words: “deep endometriosis” and “recurrence.” The literature review showed that the recurrence rate was approximately 6.6%–28%, which shows a minimal difference in terms of clinical recurrence, symptomatic recurrence, and reoccurrence of lesions as detected on ultrasonography/MRI [Table 6].[4],[13],[17],[19],[20],[21],[22],[23],[24],[25],[26] A published review has already revealed that age, weight, and type of surgery may be correlated to the recurrence of endometriosis infiltrating the bowel.[27] However, the relevant high-risk factors for the recurrence of DIE in China were not present in the published literature.
Table 6: Literature review of bowel endometriosis

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In our study, both univariate and multivariate analysis indicated rAFS stage as a predictive factor for recurrence of DIE (Stages III and IV vs. I and II, OR = 4.310, 95% CI: 1.091–17.028, P = 0.037). This result was consistent with previously retrospective study results, which revealed that the more advanced the rAFS stage, the easier it is for DIE to recur.[17] However, Busacca et al.[13] reported an nonrandomized prospective clinical study, which was performed in two tertiary care centers and the collective result of an 8-year follow-up showed that there was no difference in the recurrence rate of DIE between patients with Stage I–II and Stage III–IV (11/65 [16.9%] vs. 14/82 [17.0%], P > 0.05).

Although the usefulness of rAFS stage in the prediction of bowel DIE is limited, it still can reflect some features of this disease. Vignali et al.[19] have found that the obliteration of the pouch of Douglas was a significant factor for recurrence, which would account for up to 40 points in the rAFS scoring system, and result in an upgrading of the stage. As shown in the ENZIAN classification,[28] most DIE lesions were classified as A3, A2, and B2, which indicated that the lesions were located at the pouch of Douglas and uterosacral ligaments. Therefore, cul-de-sac blockage is common to be seen. With the more advanced stage, pelvic adhesion is more likely to be observed, which may increase the difficulty in exposing the lesion during the surgery. Cooperation between departments for MDT in a referral center recommended for DIE cases.

Whether surgical treatment is a risk factor for the recurrence of DIE remains a debate.[19],[29] In our prospective study, different procedures did not significantly affect recurrence (13.3% [10/75] vs. 11.1% [1/9], conservative vs. radical treatment, P = 1.00). Hidaka et al.[15] conducted a retrospective study that included 151 patients who received conservative treatment and 47 patients who underwent radical surgeries. After a 36-month follow-up, the conservative group experienced a significantly higher rate of recurrence than the radical group (80.7% vs. 51.1%, P = 0.015). Similarly, in Roman's study,[29] 46 patients underwent shaving surgery, and colorectal resection was performed in 25 patients. During the 5-year follow-up, four patients presented with recurrence of colorectal nodules, and all of these patients belonged to the Shaving group (P < 0.05). However, Fedele et al.[30] found that bowel resection could not reduce the symptom-related recurrence (22% [5/30] vs. 30% [16/53], P = 0.06). However, it could significantly reduce clinical recurrence (10% [3/30] vs. 38% [22/53], P = 0.02) during the 3-year follow-up. In addition to the uncertainty with regard to the benefits of decreasing the recurrence rate after radical surgery, patients are more likely to present with postoperative bowel dysfunction, such as incontinence and fecal urgency. Therefore, considering the tendency of function preservation, patients should be fully aware of these risks.

Our previous study has revealed that incomplete surgery could increase the recurrence rate postoperatively (3.9% [2/55] vs. 35.3% [13/38], P = 0.000).[12] Currently, we divided the patients with recurrence according to three subtypes and confirmed that the symptom-related recurrence rate was significantly higher in the group of patients with residual lesions during the surgery (20.4% [19/93] vs. 37.5% [9/24], P = 0.03), and in terms of clinical recurrence, the result was similar (10.7% [10/93] vs. 22.7% [5/22], P = 0.03). However, the multivariate analysis did not show a significant difference in terms of OR (0.24; 95% CI: 0.05–1.24, P = 0.07).

In our prospective cohort, symptomatic recurrence was noted in four patients with dysmenorrhea, three with CPP, one with OPP, two with dyspareunia, two with pain during defecation, and two with dysuria. Our multivariate analysis showed that the severity of dysmenorrhea was an independent factor of recurrence (OR = 1.895, 95% CI: 1.061–3.385, P = 0.031), which was consistent with the results in the report of Coccia et al.[31] Based on the Cox model analysis, a more severe CPP and dysmenorrhea led to a higher risk of recurrence, with an hazard ratio (HR) of 1.128 (95% CI: 1.024–1.242, P = 0.014) and 1.236 (95% CI: 1.035–1.476, P = 0.019), respectively. A previous study has shown that DIE lesions may infiltrate the hypogastric plexus and splanchnic nerves;[32] we proposed that the pain due to recurrence may likely be attributed to the regrowth of nerves.

One of the compelling questions concerns the characteristics of menstruation correlated to the recurrence of DIE. Coccia et al.[31] have shown that menarche is an independent factor for pain recurrence in individuals with ovarian endometrioma, with an HR of 0.645 (95% CI: 0.496–0.838, P = 0.001). Our univariate analysis showed that duration of menstruation was correlated to recurrence (7.4 vs. 6.0, P = 0.01). However, no significant difference was found in terms of menarche (13.6 vs. 13.6, P = 0.807). However, the multivariate analysis did not confirm any significant difference.

The relationship between the use of postoperative hormonal treatment and recurrence rate remains controversial. Donnez and Squifflet [17] had reported that during the 3.1-year follow-up (range: 2–6 years), a 2% (2/107) recurrence rate was observed in patients who received continuous progestogen treatment until the time they wanted to conceive. Meanwhile, in patients receiving free hormonal treatment, the recurrence rate was up to 20% (12/60). Busacca et al.[9] did not find any significant differences between the two groups when stratified based on hormonal treatment (7.1% in the recurrence group and 11.1% in the other group [P > 0.05]). Endometriosis is an estrogen-driven disease; thus, the blockage of ovarian function can reduce postoperative recurrence. Therefore, GnRH-a injection was considered the first-line treatment for endometriosis. However, in our cohort, such treatment was only recommended for patients aged <40 years or those without other contraindications to GnRH-a injection and secondary medications, such as OC and Mirena ®. The statistical result showed no difference between the two groups with or without GnRH-a treatment for 3–6 months (90.9% [10/11] vs. 80.8% [59/73], P = 0.682). Moreover, after the withdrawal of drugs as well as the fibrotic changes and scar tissue, medical therapy would be refractory;[33] therefore, symptomatic and clinical recurrence could possibly occur.

In conclusion, patients with DIE who present with severe dysmenorrhea or more advanced rAFS stage were more likely to develop recurrence. Thus, patients with DIE infiltrating the bowel must be treated in referral centers by skilled and experienced surgeons, and each patient should be informed about the risk of recurrence. Overall, as this was a 2-year prospective cohort study, the follow-up period was not long enough. To obtain a more definitive conclusion, studies with longer follow-up duration and much more patients must be conducted in the future.

Financial support and sponsorship

This study was supported in part by the following foundations: Promotion project of advanced and appropriate technology, Shanghai municipal health commission (2019SY064); Cultivation project for clinical research, Shanghai hospital development center (SHDC12019X27).

Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


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