European Journal of Obstetrics & Gynecology and Reproductive Biology 175 (2014) 87–91
Contents lists available at ScienceDirect
European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Is nerve-sparing surgery suitable for deeply infiltrating endometriosis? Xuan Che 2, Xiufeng Huang 1, Jing Zhang 1, Hong Xu 1, Xinmei Zhang 1,* 1 2
Women’s Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310006, PR China Jiaxing Maternity and Child Health Care Hospital, Jiaxing, Zhejiang 314050, PR China
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 September 2013 Received in revised form 10 January 2014 Accepted 24 January 2014
Objective: To investigate the efficacy of nerve-sparing surgery for deeply infiltrating endometriosis (DIE) and the bladder and sexual dysfunction that follow this procedure. Study design: A total of 108 women with DIE underwent conventional surgery (group A, n = 63) and nerve-sparing surgery (group B, n = 45). Three validated interview-based questionnaires – the visual analogue scale (VAS), the international prostate score symptom (IPSS), and the female sexual function index (FSFI) – were used to evaluate the efficacy and associated complications. Results: The VAS scores significantly decreased in both groups A and B after surgery, although two patients (4.4%) in group B had no improvement in their pain symptoms. The total FSFI and each domain scores significantly increased in the two groups after surgery except for satisfaction at the 24-month follow up in group A. Nine patients (15.9%) in group A required self-catheterization postoperatively. Based on the IPSS scores, a significant alteration in voiding symptoms in group A was observed at 6 months but not at 12 months or 24 months after surgery. In group B, however, no significant difference or self-catheterization requirement was observed after surgery. Conclusions: Reduced bladder and sexual dysfunction, but with a risk of absence of pain relief, suggests that the pros and cons of nerve-sparing surgery for DIE should carefully be evaluated before operation. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Deeply infiltrating endometriosis Visual analogue scale Nerve-sparing surgery International prostate score symptom Female sexual function index
1. Introduction Deeply infiltrating endometriosis (DIE) is a specific condition characterized by the infiltration of endometriotic lesions extending more than 5 mm beneath the peritoneal surface [1,2]. DIE lesions mostly involve the uterosacral ligaments, cul-de-sac, rectovaginal septum, rectum and sigmoid colon, and these lesions are directly related to painful symptoms [3,4]. Laparoscopic surgery is the primary option for DIE. Complete DIE lesion resection, however, can cause postoperative dysfunction of the genitals, bladder, and bowel, although pain symptoms are greatly alleviated [5–9]. These findings suggest that an appropriate surgical approach for DIE is needed. Recently, studies have shown that nerve-sparing surgery for DIE can reduce bowel and bladder dysfunction without decreasing surgical efficacy [6,10–15]. During this surgical procedure, the branches of the inferior hypogastric nerves that supply the bladder,
* Corresponding author at: The Department of Gynecology, Women’s Hospital, School of Medicine, Zhejiang University, 1 Xueshi Road, Hangzhou, Zhejiang 310006, PR China. Tel.: +86 571 87061501x2131; fax: +86 571 87061878. E-mail address: [email protected] (X. Zhang). 0301-2115/$ – see front matter ß 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejogrb.2014.01.027
colon, cervix, and vagina are identified and preserved, whereas DIE lesions are excised [6,10–15]. Identifying the inferior hypogastric nerve branches that pass through the uterosacral ligaments is not easy, however, because of the pelvic extensive adhesions caused by endometriosis [6,15]. Moreover, available data on the long-term efficacy that follows nerve-sparing surgery for DIE are very rare. Therefore, the objective of this study is to evaluate the longterm efficacy of nerve-sparing surgery for DIE compared with that of conventional surgery. The bladder and sexual dysfunction following nerve-sparing and conventional surgery were comparatively analyzed. Finally, we illustrate the pros and cons of nervesparing surgery for DIE. 2. Materials and methods 2.1. Patients Informed consent was obtained from each patient before the surgical procedure. The Ethics Committee of the Women’s Hospital, Zhejiang University School of Medicine, approved this study (No. 20100011). Between September 2010 and July 2012, 139 patients, who were referred to our tertiary endometriosis unit and underwent
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X. Che et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 175 (2014) 87–91
laparoscopy or open surgery for DIE, were recruited in this study. The inclusion criteria were as follows: fertile women more than 25 years old who were diagnosed with DIE by symptoms, clinical examination, and imaging techniques (including transvaginal sonography and magnetic resonance imaging (MRI)). The exclusion criteria were as follows: patients with a contraindication to laparoscopy because of severe medical illness. Thirty-one among 139 patients who were invited to participate refused treatment; therefore, only 108 patients were included in this study. The remaining 108 patients with DIE were assigned to undergo conventional surgery (group A, n = 63 (open = 30, laparoscopy = 33)) and nerve sparing surgery (group B, n = 45 (open = 21, laparoscopy = 24)) based on patient requirements. Among 24 patients with DIE who underwent laparoscopic nerve sparing surgery, two patients required conversion to open surgery because of multiple endometriotic lesions infiltrating the bowel (Fig. 1). None of the study patients revoked consent or was lost to follow up. During the surgical procedure, complete resection of all detectable endometriotic lesions was required for each patient. These procedures include ovarian cystectomy or salpingo-oophorectomy, uterosacral ligament resection, hysterectomy, ureterolysis or ureteral reimplantation, partial cystectomy, and multiple bowel resections. All operations were performed using classic open surgery or accepted operative laparoscopy [3]. Nerve-sparing surgery was performed using the technique described by Volpi et al. [10,11,14]. Three of the authors (XC, XFH, and XMZ) performed all operations. The endometriosis was confirmed by histopathological examination and was graded based on the revised American Fertility Society scoring (rAFS) system [15]. In addition, none of the study patients had received sex hormone drugs before surgery. 2.2. Follow up Before and after surgery, pain symptoms, including dysmenorrhoea, pelvic pain, dyspareunia, and dyschezia, were rated using an interview-based questionnaire (10-point visual analogue scale (VAS): 0 = absent, 10 = unbearable) [16]. Moreover, each patient was asked to complete two validated interview-based questionnaires: the international prostate score symptom (IPSS) [17,18] and the female sexual function index (FSFI) [19,20]. The IPSS consists of seven questions in three parts: voiding symptoms (four questions scored from 0 to 5 points), storage symptoms (three questions scored from 0 to 5 points), and one quality-of-life question with a sub-question about symptom severity. The FSFI includes 19 items that evaluate sexual function in six aspects (i.e.,
desire, arousal, lubrication, orgasm, satisfaction, and pain). The questions are grouped in six domains: desire (items 1 and 2), arousal (items 3–6), lubrication (items 7–10), orgasm (items 11– 13), satisfaction (items 14–16), and pain (items 17–19). Each domain has a maximal score of 6, and the total score ranges from 2 points to 36 points. All patients were followed up at 1, 3, 6, and 12 months after surgery and then each year after operation. We focused on two endpoints for short- and long-term surgical treatment efficacy. In this regard, the results of the preoperative visit were compared with those of the 6-month follow up and those of the 24-month follow-up to observe the short- and long-term efficacy that follows nerve-sparing surgery for DIE. 2.3. Statistical analysis We used the Statistical Package for the Social Sciences version 11.0 to perform statistical analyses. Nonparametric data were described as mean (range) and parametric data as mean (standard deviations (SDs)). Unpaired t test and one-way ANOVA were performed for parametric data comparison, Mann–Whitney U test for nonparametric data comparison and chi-square test for the frequency between groups. Differences were considered significant at P < 0.05. 3. Results 3.1. Patients’ characteristics No significant differences were observed with respect to age, body mass index (BMI), serum CA125, VAS, IPSS and FSFI scores, and the number of previous operations and DIE lesions between groups A and B before surgery (P > 0.05, Table 1). The maximal diameter of DIE lesions at preoperative MRI was 6 cm and 7 cm in groups A and B, respectively. The size of DIE lesions showed no statistical significance with the study population (P > 0.05). In group A, the DIE lesions were located at the uterosacral ligaments in 56 cases (88.9%), posterior cul de sac in 35 cases (55.6%), parametrium in 25 cases (39.7%), vagina in 15 cases (23.8%), bowel in 13 cases (20.6%), ureter in 10 cases (15.9%), and bladder in five cases (7.9%). By contrast, in group B, the DIE lesions were located at uterosacral ligaments in 41 cases (91.1%), posterior cul de sac in 23 cases (51.1%), parametrium in 15 cases (33.3%), vagina in 11 cases (24.4%), bowel in eight cases (17.8%), ureter in six cases (13.3%), and bladder in two cases (4.4%). No significant differences were found in DIE lesion location with the study population (P > 0.05). The resections of the uterosacral ligament, vaginal, ureter, bladder, parametrial, cul de sac, and bowel lesions showed no significant differences between groups A and B (P > 0.05). Moreover, the concurrent surgical operations that include ovarian cystectomy (20 vs. 18), salpingo-oophorectomy (3 vs. 2), and hysterectomy (7 vs. 5) were also similar in both groups (P > 0.05).
Table 1 Patients’ characteristics. Variable a
Age (years) BMI (kg/m2) CA125 (U/L) Number of previous operations Number of DIE lesions Baseline VAS score Baseline IPSS score Baseline FSFI scoreb a
Fig. 1. Protocol of patients assignment.
b
Mean (range). Mean SD.
Group A (n = 63)
Group B (n = 45)
32.9 (26–46) 20.1 (17–25) 98.9 (29.7–318.8) 2.1 (0–4) 4.8 (2–7) 7.1 (4–10) 5.6 (0–21) 18.9 4.5
33.2 (27–45) 19.8 (16–24) 71.3 (33.9–256.9) 1.9 (0–4) 5.0 (2–8) 6.8 (3–10) 5.3 (0–20) 19.3 4.8
X. Che et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 175 (2014) 87–91
Furthermore, the severity of endometriosis in groups A (rAFS: I = 2, II = 8, III = 21, IV = 32) and B (rAFS: I = 1, II = 3, III = 15, IV = 26) was not significantly different (P > 0.05). In addition, the surgical route was also similar between groups A and B (P > 0.05).
Table 2 The VAS, IPSS and FSFI scores after surgery between groups A and B. Variable Group A (n = 63) 6-month visit (n = 63) 12-month visit (n = 63) 24-month visit (n = 28) Group B (n = 45) 6-month visit (n = 45) 12-month visit (n = 45) 24-month visit (n = 19)
3.2. Urinary symptoms after surgery The median follow-up period was 22 months (range 13 months to 35 months) in group A and 21 months (range 13 months to 34 months) in group B. After surgery, nine patients (15.9%) required self-catheterization (four after laparoscopy vs. five after open surgery) with a mean duration of 56 days (range: 25 days to eight months) in group A, but no patient required self-catheterization postoperatively in group B. These nine patients in group A all underwent resections of the bowel, vagina, and bilateral uterosacral ligaments. In addition, all patients recovered within 6 months after operation, except one patient who required selfcatheterization for 8 months. A total of 13 patients with large nodular DIE lesions (>4 cm) infiltrating the right uterosacral ligament, parametrium, and vagina and who underwent right uterosacral ligament excision with and without bowel resections in group A required no self-catheterization after operation. After surgery, the total IPSS mean score at 6-month follow up in group A was significantly higher compared with that at the preoperative visit (P < 0.05). However, the total IPSS mean scores at 12- or 24-month follow up in group A were not significantly different from baseline (P > 0.05, Tables 1 and 2). In group B, the total IPSS scores at 6-, 12-, and 24-month follow up were all similar to that at the preoperative visit (P > 0.05, Table 2). We further categorized and evaluated the significant difference between the total IPSS score at the 6-month follow up and the preoperative visit in group A. We found an alteration of the IPSS score between the 6month follow up and the preoperative visit only for voiding symptoms (1.2 (0–13) vs. 3.1 (0–15), P < 0.01), but such alteration was not found for storage symptoms (4.3 (0–14) vs. 4.1 (0–15), P > 0.05) or quality of life (1.2 (0–6) vs. 1.1 (0–6), P > 0.05). 3.3. Pain symptoms after surgery After surgery, pain symptoms in group A were significantly improved (Tables 1 and 2). Compared with the preoperative VAS score, the VAS scores at all three follow-up time-points were significantly different (P < 0.001). However, the VAS score at the 24-month follow up was higher than that at the 6-month follow up, although the VAS score was not significantly different (P > 0.05). Similar to group A, the pain symptoms in group B
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a
VAS score
IPSS score
FSFI score
1.7 (0–4)a 1.8 (0–3) 2.2 (0–5)
7.8 (0–30) 5.9 (0–26) 5.6 (0–25)
25.3 5.1 24.9 4.9 23.6 4.7
2.2 (0–9) 2.1 (0–6) 2.5 (0–6)
6.1 (0–24) 5.4 (0–22) 5.5 (0–23)
26.2 5.2 25.8 5.0 24.9 4.6
Mean (range).
were also significantly improved. The mean VAS scores at the three follow-up time-points were all significantly lower compared with that at the preoperative visit (P < 0.001, Tables 1 and 2). Two patients (4.4%) in group B, however, showed no improvement in their pain symptoms. The VAS scores for these two patients were 8 and 9, respectively. One patient had severe pelvic pain and dysmenorrhea, and another patient had severe dyspareunia and dysmenorrhea. Both underwent surgery (one laparoscopy and one open surgery) for the left uterosacral ligament lesions. In addition, their VAS scores dropped to 7 at 10 and 11 months after operation and remained unchanged until now. These techniques led to higher VAS score at each time-point follow up in group B compared with group A (Table 2). 3.4. Sexual function after surgery The total postoperative FSFI score at the three follow-up timepoints all showed statistically significant differences in groups A and B compared with that at the preoperative visit (P < 0.01, Tables 1 and 2). However, no significant difference in the total FSFI scores between groups A and B was found (P > 0.05), although the total FSFI mean score was higher at each time-point follow up after surgery in group B compared with that in group A. Moreover, the total FSFI score in both groups A and B tended to decrease over time after operation, although the differences did not reach statistical significance (P > 0.05, Table 2). When analyzed separately for each FSFI domain, both groups A and B showed a similar pattern for desire, arousal, and orgasm and had an elevated FSFI score after surgery (P < 0.01), which almost remained unchanged over time (Tables 3 and 4). The pain FSFI score in groups A and B significantly increased after operation (P < 0.01) and dropped over time, although significant differences were found between the pre- and post-operative FSFI scores (Tables 3 and 4, P < 0.05). The FSFI score for satisfaction in group A
Table 3 Each FSFI domain at baseline and at follow-up in group A (mean SD). FSFI domain
Baseline (n = 63)
6 months (n = 63)
12 months (n = 63)
24 months (n = 28)
Desire Arousal Lubrication Orgasm Satisfaction Pain
3.3 1.1 3.2 0.9 3.4 1.1 3.2 0.7 3.6 1.0 2.4 0.6
4.1 1.2 4.2 1.1 4.1 1.2 4.3 1.0 4.6 1.4 4.1 1.0
4.1 1.2 4.2 1.1 4.1 1.2 4.2 1.0 4.1 1.1 4.0 1.0
4.0 1.0 4.1 1.0 4.0 1.2 4.1 1.1 3.9 1.0 3.5 0.9
Table 4 Each FSFI domain at baseline and at follow-up in group B (mean SD). FSFI domain
Baseline (n = 45)
6 months (n = 45)
12 months (n = 45)
24 months (n = 19)
Desire Arousal Lubrication Orgasm Satisfaction Pain
3.3 0.9 3.4 1.0 3.4 0.8 3.2 0.8 3.6 1.0 2.5 0.6
4.2 1.1 4.4 1.3 4.6 1.3 4.4 1.1 4.6 1.3 4.0 1.1
4.2 1.1 4.3 1.2 4.5 1.2 4.4 1.1 4.4 1.2 3.9 0.9
4.1 1.0 4.3 1.2 4.5 1.2 4.2 1.0 4.3 1.1 3.3 0.9
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X. Che et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 175 (2014) 87–91
significantly increased at the 6-month follow up (P < 0.01) and then dropped at the 12-month follow up. In addition, the results showed no significant difference at the 24-month follow up compared with that at the preoperative visit (P > 0.05, Table 3). In addition, the FSFI score for satisfaction in group B also increased after surgery (P < 0.01) but slightly decreased over time (Table 4). 4. Comments Our results showed that the pain symptoms in all patients were greatly improved after surgery, which suggests that surgery can effectively treat women with DIE [5,6]. However, two patients (4.4%) who underwent nerve-sparing surgery had no improvement in their pain symptoms, although the pain symptoms were all improved after conventional surgery. DIE lesions from these two patients were located at the right uterosacral ligament and extended to the vagina, parametrium, and pelvic floor. In addition, these patients had dense extensive adhesions with the uterosacral ligament. Therefore, from the lesion, identifying and separating the inferior hypogastric nerves, which pass through the uterosacral ligaments, are difficult [10–12]. The reasons for persistent postoperative pain in these two cases may include incomplete laparoscopic excision of endometriosis and misidentification of the inferior hypogastric nerve anatomy. Our results also showed that nine patients (15.9%) required selfcatheterization after conventional surgery, but no patient required self-catheterization after nerve-sparing surgery. All patients who underwent self-catheterization recovered within 6 months after operation, except one who recovered 8 months after surgery. Nerve-sparing surgery can help the bladder function to recover after operation compared with non-nerve-sparing surgery [6,10– 15]. Based on the IPSS scores, the differences in the voiding symptoms reached statistical significance only at the 6-month follow up but not at the 12- or 24-month follow up. The storage symptoms or quality of life showed no significant difference between nerve-sparing surgery and non-nerve-sparing surgery. This finding suggests that bladder dysfunction following conventional surgery is temporary, and recovers after operation. Besides the IPSS scores, the Bristol female low urinary tract symptom (BFLUTS) scores are also useful in evaluating the urinary dysfunction following gynaecologic surgery [21,22]. However, the results that were evaluated using the IPSS scores and the BFLUTS scores are similar, and only the voiding symptoms had a significant difference after surgery [10]. Approximately 74% of patients who undergo unilateral resection of the uterosacral ligament are shown to have urine retention [8,11]. Resections of vagina and parametrium in women with DIE can also cause bladder voiding symptoms [10]. In the present study, self-catheterization only appeared in these patients with bilateral uterosacral ligament and bowel resections. The possible reasons for the differences of postoperative urinary complications between our study and other studies may be related to the location of the lesions and the extent of surgery. Sexual dysfunction is very common in women with endometriosis but is usually ignored [23,24]. In the present study, the total FSFI score and the sub-score for each of the six domains in all study patients were below the clinical cut-off scores before surgery [25], and these scores significantly increased after surgery. The only difference between the two methods is that satisfaction disappeared 24 months after non-nerve-sparing surgery but not after nerve-sparing surgery when the comparisons were made between the findings before and after surgery. These findings suggest that sexual dysfunction is reduced by surgery but not by the nervesparing technique. The tendency to increased pain symptoms and sexual dysfunction over time after operation may be caused by new DIE lesions or remaining DIE lesions which are caused by incomplete excision during the surgical procedure [26].
In summary, our results showed that nerve-sparing surgery or conventional surgery for DIE can reduce pain symptoms and sexual dysfunction. However, non-nerve-sparing surgery caused bladder dysfunction after operation, whereas nerve-sparing surgery did not. On the other hand, all pain symptoms improved for nonnerve-sparing surgery, whereas, nerve-sparing surgery had a risk for absence of pain relief. Therefore, the advantages and disadvantages of nerve-sparing surgery for each patient with DIE should be carefully evaluated before and during the surgical procedure. Thus, further studies are needed. Conflict of interest We declare no conflicts of interest. Ethical approval This study was undertaken after obtaining approval from the Ethics Committee of the Women’s Hospital, Zhejiang University School of Medicine, Zhejiang, China. We obtained the approval in 2010, and the number was 20100011. The patients provided written informed consent before participating in this study. Acknowledgments We appreciate the financial support of the National Nature Science Foundation of China (81270672), the Nature Science Foundation of Zhejiang Province (Y2110181, Y2110128), the Science and Technology Fund of Zhejiang Province (2011C13028-1, 2013C33149) and the Key Medical Science (Innovation) Project of Zhejiang Province. References [1] Marcal L, Nothaft MA, Coelho F, Choi H. Deep pelvic endometriosis: MR imaging. Abdom Imaging 2010;35:708–15. [2] Coccia ME, Rizzello F. Ultrasonographic staging: a new staging system for deep endometriosis. Ann NY Acad Sci 2011;1221:61–9. [3] Chapron C, Fauconnier A, Vieira M, et al. Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod 2003;18:157–61. [4] Wang G, Tokushige N, Markham R, Fraser IS. Rich innervation of deep infiltrating endometriosis. Hum Reprod 2009;24:827–34. [5] Kondo W, Bourdel N, Tamburro S, et al. Complications after surgery for deeply infiltrating pelvic endometriosis. BJOG 2011;118:292–8. [6] Ballester M, Chereau E, Dubernard G, Coutant C, Bazot M, Daraı¨ E. Urinary dysfunction after colorectal resection for endometriosis: results of a prospective randomized trial comparing laparoscopy to open surgery. Am J Obstet Gynecol 2011;204. 303.e1–e6. [7] Dubernard G, Rouzier R, David-Montefiore E, Bazot M, Daraı¨ E. Urinary complications after surgery for posterior deep infiltrating endometriosis are related to the extent of dissection and to uterosacral ligaments resection. J Minim Invasive Gynecol 2008;15:235–40. [8] Kovoor E, Nassif J, Miranda-Mendoza I, Lang-Ave´rous G, Wattiez A. Long-term urinary retention after laparoscopic surgery for deep endometriosis. Fertil Steril 2011;95. 803.e9–e12. [9] Ceccaroni M, Clarizia R, Bruni F, et al. Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, prospective, clinical trial. Surg Endosc 2012;26:2029–45. [10] Volpi E, Ferrero A, Sismondi P. Laparoscopic identification of pelvic nerves in patients with deep infiltrating endometriosis. Surg Endosc 2004;18:1109–12. [11] Kavallaris A, Banz C, Chalvatzas N, et al. Laparoscopic nerve-sparing surgery of deep infiltrating endometriosis: description of the technique and patients’ outcome. Arch Gynecol Obstet 2011;284:131–5. [12] Ceccaroni M, Pontrelli G, Scioscia M, Ruffo G, Bruni F, Minelli L. Nerve-sparing laparoscopic radical excision of deep endometriosis with rectal and parametrial resection. J Minim Invasive Gynecol 2010;17:14–5. [13] Ceccaroni M, Clarizia R, Alboni C, et al. Laparoscopic nerve-sparing transperitoneal approach for endometriosis infiltrating the pelvic wall and somatic nerves: anatomical considerations and surgical technique. Surg Radiol Anat 2010;32:601–4. [14] Landi S, Ceccaroni M, Perutelli A, et al. Laparoscopic nerve-sparing complete excision of deep endometriosis: is it feasible? Hum Reprod 2006;21:774–81. [15] Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 1997;67:817–21.
X. Che et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 175 (2014) 87–91 [16] Zhang X, Yao H, Huang X, Lu B, Xu H, Zhou C. Nerve fibres in ovarian endometriotic lesions in women with ovarian endometriosis. Hum Reprod 2010;25:392–7. [17] Pocard M, Zinzindohoue F, Haab F, Caplin S, Parc R, Tiret E. A prospective study of sexual and urinary function before and after total mesorectal excision with autonomic nerve preservation for rectal cancer. Surgery 2002;131: 368–72. [18] Ko YH, Moon du G, Moon KH. Testosterone replacement alone for testosterone deficiency syndrome improves moderate lower urinary tract symptoms: one year follow-up. World J Men’s Health 2013;31:47–52. [19] Souza Fde O, Dias LA, Franco Mde M, et al. Assessment of female sexual function in pregnant women with gestational diabetes mellitus. J Sex Med 2013;10:1350–4. [20] Ghanbarzadeh N, Nadjafi-Semnani M, Ghanbarzadeh MR, Nadjfai-Semnani A, Nadjfai-Semnani F. Female sexual dysfunction in Iran: study of prevalence and risk factors. Arch Gynecol Obstet 2013;287:533–9. [21] Brookes ST, Donovan JL, Wright M, Jackson S, Abrams P. A scored form of the Bristol Female Lower Urinary Tract Symptoms questionnaire: data from a
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Contents lists available at ScienceDirect
European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Is nerve-sparing surgery suitable for deeply infiltrating endometriosis? Xuan Che 2, Xiufeng Huang 1, Jing Zhang 1, Hong Xu 1, Xinmei Zhang 1,* 1 2
Women’s Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang 310006, PR China Jiaxing Maternity and Child Health Care Hospital, Jiaxing, Zhejiang 314050, PR China
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 September 2013 Received in revised form 10 January 2014 Accepted 24 January 2014
Objective: To investigate the efficacy of nerve-sparing surgery for deeply infiltrating endometriosis (DIE) and the bladder and sexual dysfunction that follow this procedure. Study design: A total of 108 women with DIE underwent conventional surgery (group A, n = 63) and nerve-sparing surgery (group B, n = 45). Three validated interview-based questionnaires – the visual analogue scale (VAS), the international prostate score symptom (IPSS), and the female sexual function index (FSFI) – were used to evaluate the efficacy and associated complications. Results: The VAS scores significantly decreased in both groups A and B after surgery, although two patients (4.4%) in group B had no improvement in their pain symptoms. The total FSFI and each domain scores significantly increased in the two groups after surgery except for satisfaction at the 24-month follow up in group A. Nine patients (15.9%) in group A required self-catheterization postoperatively. Based on the IPSS scores, a significant alteration in voiding symptoms in group A was observed at 6 months but not at 12 months or 24 months after surgery. In group B, however, no significant difference or self-catheterization requirement was observed after surgery. Conclusions: Reduced bladder and sexual dysfunction, but with a risk of absence of pain relief, suggests that the pros and cons of nerve-sparing surgery for DIE should carefully be evaluated before operation. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Deeply infiltrating endometriosis Visual analogue scale Nerve-sparing surgery International prostate score symptom Female sexual function index
1. Introduction Deeply infiltrating endometriosis (DIE) is a specific condition characterized by the infiltration of endometriotic lesions extending more than 5 mm beneath the peritoneal surface [1,2]. DIE lesions mostly involve the uterosacral ligaments, cul-de-sac, rectovaginal septum, rectum and sigmoid colon, and these lesions are directly related to painful symptoms [3,4]. Laparoscopic surgery is the primary option for DIE. Complete DIE lesion resection, however, can cause postoperative dysfunction of the genitals, bladder, and bowel, although pain symptoms are greatly alleviated [5–9]. These findings suggest that an appropriate surgical approach for DIE is needed. Recently, studies have shown that nerve-sparing surgery for DIE can reduce bowel and bladder dysfunction without decreasing surgical efficacy [6,10–15]. During this surgical procedure, the branches of the inferior hypogastric nerves that supply the bladder,
* Corresponding author at: The Department of Gynecology, Women’s Hospital, School of Medicine, Zhejiang University, 1 Xueshi Road, Hangzhou, Zhejiang 310006, PR China. Tel.: +86 571 87061501x2131; fax: +86 571 87061878. E-mail address: [email protected] (X. Zhang). 0301-2115/$ – see front matter ß 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejogrb.2014.01.027
colon, cervix, and vagina are identified and preserved, whereas DIE lesions are excised [6,10–15]. Identifying the inferior hypogastric nerve branches that pass through the uterosacral ligaments is not easy, however, because of the pelvic extensive adhesions caused by endometriosis [6,15]. Moreover, available data on the long-term efficacy that follows nerve-sparing surgery for DIE are very rare. Therefore, the objective of this study is to evaluate the longterm efficacy of nerve-sparing surgery for DIE compared with that of conventional surgery. The bladder and sexual dysfunction following nerve-sparing and conventional surgery were comparatively analyzed. Finally, we illustrate the pros and cons of nervesparing surgery for DIE. 2. Materials and methods 2.1. Patients Informed consent was obtained from each patient before the surgical procedure. The Ethics Committee of the Women’s Hospital, Zhejiang University School of Medicine, approved this study (No. 20100011). Between September 2010 and July 2012, 139 patients, who were referred to our tertiary endometriosis unit and underwent
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laparoscopy or open surgery for DIE, were recruited in this study. The inclusion criteria were as follows: fertile women more than 25 years old who were diagnosed with DIE by symptoms, clinical examination, and imaging techniques (including transvaginal sonography and magnetic resonance imaging (MRI)). The exclusion criteria were as follows: patients with a contraindication to laparoscopy because of severe medical illness. Thirty-one among 139 patients who were invited to participate refused treatment; therefore, only 108 patients were included in this study. The remaining 108 patients with DIE were assigned to undergo conventional surgery (group A, n = 63 (open = 30, laparoscopy = 33)) and nerve sparing surgery (group B, n = 45 (open = 21, laparoscopy = 24)) based on patient requirements. Among 24 patients with DIE who underwent laparoscopic nerve sparing surgery, two patients required conversion to open surgery because of multiple endometriotic lesions infiltrating the bowel (Fig. 1). None of the study patients revoked consent or was lost to follow up. During the surgical procedure, complete resection of all detectable endometriotic lesions was required for each patient. These procedures include ovarian cystectomy or salpingo-oophorectomy, uterosacral ligament resection, hysterectomy, ureterolysis or ureteral reimplantation, partial cystectomy, and multiple bowel resections. All operations were performed using classic open surgery or accepted operative laparoscopy [3]. Nerve-sparing surgery was performed using the technique described by Volpi et al. [10,11,14]. Three of the authors (XC, XFH, and XMZ) performed all operations. The endometriosis was confirmed by histopathological examination and was graded based on the revised American Fertility Society scoring (rAFS) system [15]. In addition, none of the study patients had received sex hormone drugs before surgery. 2.2. Follow up Before and after surgery, pain symptoms, including dysmenorrhoea, pelvic pain, dyspareunia, and dyschezia, were rated using an interview-based questionnaire (10-point visual analogue scale (VAS): 0 = absent, 10 = unbearable) [16]. Moreover, each patient was asked to complete two validated interview-based questionnaires: the international prostate score symptom (IPSS) [17,18] and the female sexual function index (FSFI) [19,20]. The IPSS consists of seven questions in three parts: voiding symptoms (four questions scored from 0 to 5 points), storage symptoms (three questions scored from 0 to 5 points), and one quality-of-life question with a sub-question about symptom severity. The FSFI includes 19 items that evaluate sexual function in six aspects (i.e.,
desire, arousal, lubrication, orgasm, satisfaction, and pain). The questions are grouped in six domains: desire (items 1 and 2), arousal (items 3–6), lubrication (items 7–10), orgasm (items 11– 13), satisfaction (items 14–16), and pain (items 17–19). Each domain has a maximal score of 6, and the total score ranges from 2 points to 36 points. All patients were followed up at 1, 3, 6, and 12 months after surgery and then each year after operation. We focused on two endpoints for short- and long-term surgical treatment efficacy. In this regard, the results of the preoperative visit were compared with those of the 6-month follow up and those of the 24-month follow-up to observe the short- and long-term efficacy that follows nerve-sparing surgery for DIE. 2.3. Statistical analysis We used the Statistical Package for the Social Sciences version 11.0 to perform statistical analyses. Nonparametric data were described as mean (range) and parametric data as mean (standard deviations (SDs)). Unpaired t test and one-way ANOVA were performed for parametric data comparison, Mann–Whitney U test for nonparametric data comparison and chi-square test for the frequency between groups. Differences were considered significant at P < 0.05. 3. Results 3.1. Patients’ characteristics No significant differences were observed with respect to age, body mass index (BMI), serum CA125, VAS, IPSS and FSFI scores, and the number of previous operations and DIE lesions between groups A and B before surgery (P > 0.05, Table 1). The maximal diameter of DIE lesions at preoperative MRI was 6 cm and 7 cm in groups A and B, respectively. The size of DIE lesions showed no statistical significance with the study population (P > 0.05). In group A, the DIE lesions were located at the uterosacral ligaments in 56 cases (88.9%), posterior cul de sac in 35 cases (55.6%), parametrium in 25 cases (39.7%), vagina in 15 cases (23.8%), bowel in 13 cases (20.6%), ureter in 10 cases (15.9%), and bladder in five cases (7.9%). By contrast, in group B, the DIE lesions were located at uterosacral ligaments in 41 cases (91.1%), posterior cul de sac in 23 cases (51.1%), parametrium in 15 cases (33.3%), vagina in 11 cases (24.4%), bowel in eight cases (17.8%), ureter in six cases (13.3%), and bladder in two cases (4.4%). No significant differences were found in DIE lesion location with the study population (P > 0.05). The resections of the uterosacral ligament, vaginal, ureter, bladder, parametrial, cul de sac, and bowel lesions showed no significant differences between groups A and B (P > 0.05). Moreover, the concurrent surgical operations that include ovarian cystectomy (20 vs. 18), salpingo-oophorectomy (3 vs. 2), and hysterectomy (7 vs. 5) were also similar in both groups (P > 0.05).
Table 1 Patients’ characteristics. Variable a
Age (years) BMI (kg/m2) CA125 (U/L) Number of previous operations Number of DIE lesions Baseline VAS score Baseline IPSS score Baseline FSFI scoreb a
Fig. 1. Protocol of patients assignment.
b
Mean (range). Mean SD.
Group A (n = 63)
Group B (n = 45)
32.9 (26–46) 20.1 (17–25) 98.9 (29.7–318.8) 2.1 (0–4) 4.8 (2–7) 7.1 (4–10) 5.6 (0–21) 18.9 4.5
33.2 (27–45) 19.8 (16–24) 71.3 (33.9–256.9) 1.9 (0–4) 5.0 (2–8) 6.8 (3–10) 5.3 (0–20) 19.3 4.8
X. Che et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 175 (2014) 87–91
Furthermore, the severity of endometriosis in groups A (rAFS: I = 2, II = 8, III = 21, IV = 32) and B (rAFS: I = 1, II = 3, III = 15, IV = 26) was not significantly different (P > 0.05). In addition, the surgical route was also similar between groups A and B (P > 0.05).
Table 2 The VAS, IPSS and FSFI scores after surgery between groups A and B. Variable Group A (n = 63) 6-month visit (n = 63) 12-month visit (n = 63) 24-month visit (n = 28) Group B (n = 45) 6-month visit (n = 45) 12-month visit (n = 45) 24-month visit (n = 19)
3.2. Urinary symptoms after surgery The median follow-up period was 22 months (range 13 months to 35 months) in group A and 21 months (range 13 months to 34 months) in group B. After surgery, nine patients (15.9%) required self-catheterization (four after laparoscopy vs. five after open surgery) with a mean duration of 56 days (range: 25 days to eight months) in group A, but no patient required self-catheterization postoperatively in group B. These nine patients in group A all underwent resections of the bowel, vagina, and bilateral uterosacral ligaments. In addition, all patients recovered within 6 months after operation, except one patient who required selfcatheterization for 8 months. A total of 13 patients with large nodular DIE lesions (>4 cm) infiltrating the right uterosacral ligament, parametrium, and vagina and who underwent right uterosacral ligament excision with and without bowel resections in group A required no self-catheterization after operation. After surgery, the total IPSS mean score at 6-month follow up in group A was significantly higher compared with that at the preoperative visit (P < 0.05). However, the total IPSS mean scores at 12- or 24-month follow up in group A were not significantly different from baseline (P > 0.05, Tables 1 and 2). In group B, the total IPSS scores at 6-, 12-, and 24-month follow up were all similar to that at the preoperative visit (P > 0.05, Table 2). We further categorized and evaluated the significant difference between the total IPSS score at the 6-month follow up and the preoperative visit in group A. We found an alteration of the IPSS score between the 6month follow up and the preoperative visit only for voiding symptoms (1.2 (0–13) vs. 3.1 (0–15), P < 0.01), but such alteration was not found for storage symptoms (4.3 (0–14) vs. 4.1 (0–15), P > 0.05) or quality of life (1.2 (0–6) vs. 1.1 (0–6), P > 0.05). 3.3. Pain symptoms after surgery After surgery, pain symptoms in group A were significantly improved (Tables 1 and 2). Compared with the preoperative VAS score, the VAS scores at all three follow-up time-points were significantly different (P < 0.001). However, the VAS score at the 24-month follow up was higher than that at the 6-month follow up, although the VAS score was not significantly different (P > 0.05). Similar to group A, the pain symptoms in group B
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a
VAS score
IPSS score
FSFI score
1.7 (0–4)a 1.8 (0–3) 2.2 (0–5)
7.8 (0–30) 5.9 (0–26) 5.6 (0–25)
25.3 5.1 24.9 4.9 23.6 4.7
2.2 (0–9) 2.1 (0–6) 2.5 (0–6)
6.1 (0–24) 5.4 (0–22) 5.5 (0–23)
26.2 5.2 25.8 5.0 24.9 4.6
Mean (range).
were also significantly improved. The mean VAS scores at the three follow-up time-points were all significantly lower compared with that at the preoperative visit (P < 0.001, Tables 1 and 2). Two patients (4.4%) in group B, however, showed no improvement in their pain symptoms. The VAS scores for these two patients were 8 and 9, respectively. One patient had severe pelvic pain and dysmenorrhea, and another patient had severe dyspareunia and dysmenorrhea. Both underwent surgery (one laparoscopy and one open surgery) for the left uterosacral ligament lesions. In addition, their VAS scores dropped to 7 at 10 and 11 months after operation and remained unchanged until now. These techniques led to higher VAS score at each time-point follow up in group B compared with group A (Table 2). 3.4. Sexual function after surgery The total postoperative FSFI score at the three follow-up timepoints all showed statistically significant differences in groups A and B compared with that at the preoperative visit (P < 0.01, Tables 1 and 2). However, no significant difference in the total FSFI scores between groups A and B was found (P > 0.05), although the total FSFI mean score was higher at each time-point follow up after surgery in group B compared with that in group A. Moreover, the total FSFI score in both groups A and B tended to decrease over time after operation, although the differences did not reach statistical significance (P > 0.05, Table 2). When analyzed separately for each FSFI domain, both groups A and B showed a similar pattern for desire, arousal, and orgasm and had an elevated FSFI score after surgery (P < 0.01), which almost remained unchanged over time (Tables 3 and 4). The pain FSFI score in groups A and B significantly increased after operation (P < 0.01) and dropped over time, although significant differences were found between the pre- and post-operative FSFI scores (Tables 3 and 4, P < 0.05). The FSFI score for satisfaction in group A
Table 3 Each FSFI domain at baseline and at follow-up in group A (mean SD). FSFI domain
Baseline (n = 63)
6 months (n = 63)
12 months (n = 63)
24 months (n = 28)
Desire Arousal Lubrication Orgasm Satisfaction Pain
3.3 1.1 3.2 0.9 3.4 1.1 3.2 0.7 3.6 1.0 2.4 0.6
4.1 1.2 4.2 1.1 4.1 1.2 4.3 1.0 4.6 1.4 4.1 1.0
4.1 1.2 4.2 1.1 4.1 1.2 4.2 1.0 4.1 1.1 4.0 1.0
4.0 1.0 4.1 1.0 4.0 1.2 4.1 1.1 3.9 1.0 3.5 0.9
Table 4 Each FSFI domain at baseline and at follow-up in group B (mean SD). FSFI domain
Baseline (n = 45)
6 months (n = 45)
12 months (n = 45)
24 months (n = 19)
Desire Arousal Lubrication Orgasm Satisfaction Pain
3.3 0.9 3.4 1.0 3.4 0.8 3.2 0.8 3.6 1.0 2.5 0.6
4.2 1.1 4.4 1.3 4.6 1.3 4.4 1.1 4.6 1.3 4.0 1.1
4.2 1.1 4.3 1.2 4.5 1.2 4.4 1.1 4.4 1.2 3.9 0.9
4.1 1.0 4.3 1.2 4.5 1.2 4.2 1.0 4.3 1.1 3.3 0.9
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significantly increased at the 6-month follow up (P < 0.01) and then dropped at the 12-month follow up. In addition, the results showed no significant difference at the 24-month follow up compared with that at the preoperative visit (P > 0.05, Table 3). In addition, the FSFI score for satisfaction in group B also increased after surgery (P < 0.01) but slightly decreased over time (Table 4). 4. Comments Our results showed that the pain symptoms in all patients were greatly improved after surgery, which suggests that surgery can effectively treat women with DIE [5,6]. However, two patients (4.4%) who underwent nerve-sparing surgery had no improvement in their pain symptoms, although the pain symptoms were all improved after conventional surgery. DIE lesions from these two patients were located at the right uterosacral ligament and extended to the vagina, parametrium, and pelvic floor. In addition, these patients had dense extensive adhesions with the uterosacral ligament. Therefore, from the lesion, identifying and separating the inferior hypogastric nerves, which pass through the uterosacral ligaments, are difficult [10–12]. The reasons for persistent postoperative pain in these two cases may include incomplete laparoscopic excision of endometriosis and misidentification of the inferior hypogastric nerve anatomy. Our results also showed that nine patients (15.9%) required selfcatheterization after conventional surgery, but no patient required self-catheterization after nerve-sparing surgery. All patients who underwent self-catheterization recovered within 6 months after operation, except one who recovered 8 months after surgery. Nerve-sparing surgery can help the bladder function to recover after operation compared with non-nerve-sparing surgery [6,10– 15]. Based on the IPSS scores, the differences in the voiding symptoms reached statistical significance only at the 6-month follow up but not at the 12- or 24-month follow up. The storage symptoms or quality of life showed no significant difference between nerve-sparing surgery and non-nerve-sparing surgery. This finding suggests that bladder dysfunction following conventional surgery is temporary, and recovers after operation. Besides the IPSS scores, the Bristol female low urinary tract symptom (BFLUTS) scores are also useful in evaluating the urinary dysfunction following gynaecologic surgery [21,22]. However, the results that were evaluated using the IPSS scores and the BFLUTS scores are similar, and only the voiding symptoms had a significant difference after surgery [10]. Approximately 74% of patients who undergo unilateral resection of the uterosacral ligament are shown to have urine retention [8,11]. Resections of vagina and parametrium in women with DIE can also cause bladder voiding symptoms [10]. In the present study, self-catheterization only appeared in these patients with bilateral uterosacral ligament and bowel resections. The possible reasons for the differences of postoperative urinary complications between our study and other studies may be related to the location of the lesions and the extent of surgery. Sexual dysfunction is very common in women with endometriosis but is usually ignored [23,24]. In the present study, the total FSFI score and the sub-score for each of the six domains in all study patients were below the clinical cut-off scores before surgery [25], and these scores significantly increased after surgery. The only difference between the two methods is that satisfaction disappeared 24 months after non-nerve-sparing surgery but not after nerve-sparing surgery when the comparisons were made between the findings before and after surgery. These findings suggest that sexual dysfunction is reduced by surgery but not by the nervesparing technique. The tendency to increased pain symptoms and sexual dysfunction over time after operation may be caused by new DIE lesions or remaining DIE lesions which are caused by incomplete excision during the surgical procedure [26].
In summary, our results showed that nerve-sparing surgery or conventional surgery for DIE can reduce pain symptoms and sexual dysfunction. However, non-nerve-sparing surgery caused bladder dysfunction after operation, whereas nerve-sparing surgery did not. On the other hand, all pain symptoms improved for nonnerve-sparing surgery, whereas, nerve-sparing surgery had a risk for absence of pain relief. Therefore, the advantages and disadvantages of nerve-sparing surgery for each patient with DIE should be carefully evaluated before and during the surgical procedure. Thus, further studies are needed. Conflict of interest We declare no conflicts of interest. Ethical approval This study was undertaken after obtaining approval from the Ethics Committee of the Women’s Hospital, Zhejiang University School of Medicine, Zhejiang, China. We obtained the approval in 2010, and the number was 20100011. The patients provided written informed consent before participating in this study. Acknowledgments We appreciate the financial support of the National Nature Science Foundation of China (81270672), the Nature Science Foundation of Zhejiang Province (Y2110181, Y2110128), the Science and Technology Fund of Zhejiang Province (2011C13028-1, 2013C33149) and the Key Medical Science (Innovation) Project of Zhejiang Province. References [1] Marcal L, Nothaft MA, Coelho F, Choi H. Deep pelvic endometriosis: MR imaging. Abdom Imaging 2010;35:708–15. [2] Coccia ME, Rizzello F. Ultrasonographic staging: a new staging system for deep endometriosis. Ann NY Acad Sci 2011;1221:61–9. [3] Chapron C, Fauconnier A, Vieira M, et al. Anatomical distribution of deeply infiltrating endometriosis: surgical implications and proposition for a classification. Hum Reprod 2003;18:157–61. [4] Wang G, Tokushige N, Markham R, Fraser IS. Rich innervation of deep infiltrating endometriosis. Hum Reprod 2009;24:827–34. [5] Kondo W, Bourdel N, Tamburro S, et al. Complications after surgery for deeply infiltrating pelvic endometriosis. BJOG 2011;118:292–8. [6] Ballester M, Chereau E, Dubernard G, Coutant C, Bazot M, Daraı¨ E. Urinary dysfunction after colorectal resection for endometriosis: results of a prospective randomized trial comparing laparoscopy to open surgery. Am J Obstet Gynecol 2011;204. 303.e1–e6. [7] Dubernard G, Rouzier R, David-Montefiore E, Bazot M, Daraı¨ E. Urinary complications after surgery for posterior deep infiltrating endometriosis are related to the extent of dissection and to uterosacral ligaments resection. J Minim Invasive Gynecol 2008;15:235–40. [8] Kovoor E, Nassif J, Miranda-Mendoza I, Lang-Ave´rous G, Wattiez A. Long-term urinary retention after laparoscopic surgery for deep endometriosis. Fertil Steril 2011;95. 803.e9–e12. [9] Ceccaroni M, Clarizia R, Bruni F, et al. Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, prospective, clinical trial. Surg Endosc 2012;26:2029–45. [10] Volpi E, Ferrero A, Sismondi P. Laparoscopic identification of pelvic nerves in patients with deep infiltrating endometriosis. Surg Endosc 2004;18:1109–12. [11] Kavallaris A, Banz C, Chalvatzas N, et al. Laparoscopic nerve-sparing surgery of deep infiltrating endometriosis: description of the technique and patients’ outcome. Arch Gynecol Obstet 2011;284:131–5. [12] Ceccaroni M, Pontrelli G, Scioscia M, Ruffo G, Bruni F, Minelli L. Nerve-sparing laparoscopic radical excision of deep endometriosis with rectal and parametrial resection. J Minim Invasive Gynecol 2010;17:14–5. [13] Ceccaroni M, Clarizia R, Alboni C, et al. Laparoscopic nerve-sparing transperitoneal approach for endometriosis infiltrating the pelvic wall and somatic nerves: anatomical considerations and surgical technique. Surg Radiol Anat 2010;32:601–4. [14] Landi S, Ceccaroni M, Perutelli A, et al. Laparoscopic nerve-sparing complete excision of deep endometriosis: is it feasible? Hum Reprod 2006;21:774–81. [15] Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril 1997;67:817–21.
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