Does laparoscopic management of deep infiltrating endometriosis improve quality of life? A prospective study

Background: Deep infiltrating endometriosis (DIE) can affect importantly patients ’ quality of life (QOL). The aim of this study is to evaluate the impact of the laparoscopic management of DIE on QOL after six months from treatment.

It is a prospective cohort study. In a tertiary care university hospital, between April 2008 and December 2009, 100 patients underwent laparoscopic management of DIE and completed preoperatively and 6-months postoperatively a QOL questionnaire, the short form 36 (SF-36). Quality of life was measured through the SF-36 scores. Intra-operative details of disease site, number of lesions, type of intervention, period of hospital stay and peri-operative complications were noted.

Six months postoperatively all the women had a significant improvement in every scale of the SF-36 (p 0.05). There was no significant difference in the SF-36 scores at 6 months from surgery between patients who received postoperative medical treatment and patients who did not (p > 0.05).

Laparoscopic excision of DIE lesions significantly improves general health and psycho-emotional status at six months from surgery without differences between patients submitted to intestinal segmental resection or intestinal nodule shaving.

Deep infiltrating endometriosis (DIE) defined as the infiltration of anatomic structures, pelvic organs, or both, is a source of pelvic pain and altered quality of life [1-4]. The exact incidence of DIE in the general popula- tion is not known, but it is estimated to affect 20% of women with endometriosis [5]. Although many studies demonstrated that surgical resection of all endometriotic lesions is recommended to relieve pain, its effectiveness is still debated [5-16]. In addition, the risk of serious complications inherent to this type of surgery has been estimated between 4 and 6% of cases [17,18] with a high rate of de novo neurolo- gical disorders [19]. It has been demonstrated that the secondary effects of surgical treatment and the persis- tence of some symptoms can have an impact on the patient’s quality of life [20]. Furthermore, when we treat endometriosis we have to consider that it is a benign disease which affects young, professionally active women, who may plan to conceive. In our opinion, quality of life (QOL) evaluation is important to assess the overall effects of radical excision of DIE, taking in consideration that endometriosis is a pathology that has symptoms which may disrupt work- ing ability, social relationships and sexual functioning. * Correspondence: [email protected] † Contributed equally 1Minimally Invasive Gynaecological Surgery Unit, S.Orsola Hospital, University of Bologna, Italy Full list of author information is available at the end of the article Mabrouk et al . Health and Quality of Life Outcomes 2011, 9:98 http://www.hqlo.com/content/9/1/98 © 2011 Mabrouk et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Several general questionnaires have been recom- mended for QOL assessment ([2,3,20-23]). Between them, the short form 36 (SF-36) has been used to evalu- ate the improvement in QOL in patients submitted to laparoscopic surgery [4,24] for endometriosis and, in general, to evaluate the impact of endometriosis and its treatment on women ’s health-related quality of life [25]. Two surgical approaches are usually employed in management of deep endometriosis with intestinal mus- cularis involvement: segmental resection and nodule excision. This latter approach may be performed with- out opening the intestinal lumen (shaving) or by remov- ing the nodule along with the surrounding intestinal wall (full thickness or disc excision). A strong debate continues between advocates of the nodule excision techniques and supporters of segmental resection. To date, there is no consensus made about the surgical management of deep intestinal endometriosis [26]. Recently SF-36 has been proposed as a complementary tool to select and inform women who might benefit from laparoscopic segmental resection for endometriosis [27]. In the present study we sought to prospectively evalu- ate the impact of laparoscopic management of DIE on the patients ’ QOL. We also aimed to investigate whether or not a greater level of QOL improvement can be achieved by performing segmental resection rather than nodule excision in patients with deep intestinal endometriosis.

Full ethical approval was obt ained from the local ethics committee to the study protocol (155/2008U/Oss). Protocol and surgical treatment From April 2008 through December 2009, in the Mini- mally Invasive Gynaecological Surgery Unit, S. Orsola- Malpighi Hospital, University of Bologna, a consecutive series of 120 patients with preoperative diagnosis of deep infiltrating endometriosis agreed to take part to the study protocol. Exclusion criteria were as follows: major medical con- ditions, psychiatric disorders, current or past (within 6 months from study enrolment) use of drugs affecting cognition, vigilance and/or mood. For each patient, general data were assessed together with history of surgical treatment for endometriosis and the scoring of pelvic pain symptoms using a 10-point visual analogue scale (VAS). All women underwent gynaecological examination, pelvic trans-vaginal and abdominal ultra-sonography in order to evaluate the presen ce of pelvic endometriosis before surgery. Other diagnostic tests were performed when indicated, as previously described [28,29]. All women were scheduled for laparoscopic manage- ment of deep infiltrating endometriosis and they gave informed written consent to surgical treatment and the possible use of their anonymous data for research pur- poses. The surgical strategy was complete laparoscopic excision of all visually suspected endometriotic lesions and the laparoscopic procedures were performed by the same surgeon (R.S.). The surgical team had a consistent

in laparoscopic treatment of patients with DIE. Laparoscopic resectio n of endometriosis was per- formed as previously described [28-32]. In particular, women were scheduled for segmental recto-sigmoid resection when bowel function was greatly impaired and when radiological diagnosis o f intestinal endometriosis confirmed the presence of intestinal lesions associated with marked restriction of the bowel lumen. Moreover, deciding the necessity of intestinal resection or intestinal nodule shaving, we took into account endometriosis and intestinal symptoms, impairment of quality of life due to intestinal symptoms, desire of pregnancy and finally the intra-operative evaluation performed by the gynaecologi- cal surgeon and the general surgeon. Only after histolo- gical confirmation of diagnosis, the patients were asked to continue the postoperative phase of the study. Deep infiltrating endometriosis ( DIE) was considered histolo- gically confirmed when the lesion penetrates >5 mm under the peritoneal surface [33]. We considered intest- inal DIE when the lesion infiltrated the muscularis [34]. After surgical treatment patients were recommended to use medical therapy to prevent anatomical lesion recurrences and symptoms relapse. All patients were asked to undergo a follow-up visit six months after sur- gery. During the follow-up visit, patients underwent physical examination and trans-vaginal ultrasonography to evaluate symptoms and/or anatomical relapse of endometriotic nodules. Women were asked to complete the SF-36 Questionnaire and to rank their symptom i n t e n s i t yu s i n gt h es a m en u m e r i c a l l yr a t e dV A Su s e d preoperatively. QOL assessment The SF-36 is a multi-purpose health survey with 36 questions. It yields an eight-scale profile of functional health and well-being scores, as well as psychometrically based physical and mental health summary measures (standardized). The eight scales are hypothesized to form two distinct higher-ordered clusters due to the physical and mental health variance that they have in common. Among the eight scales, three [physical func- tioning (PF), role physical (RP), bodily pain (BP)] corre- late most strongly with the physical component and contribute most to the Physical Component Summary (PCS) score. The mental component correlates best with the mental health (MH), role emotional (RE) and social Mabrouk et al . Health and Quality of Life Outcomes 2011, 9:98 http://www.hqlo.com/content/9/1/98 Page 2 of 7 functioning (SF) scores, which also contribute most to the Mental Component Summary (MCS) score. Two of the scales [vitality (VT) and general health (GH)] have noteworthy correlations with both components. All the women completed preoperatively and 6-months post- operatively the SF- 36 questionnaire, Italian version, release 1.6 [35]. Statistical Analysis All continuous variables were expressed in terms of mean ± standard deviation of the mean. The Kolmo- gorov Smirnov test was performed to assess the normal distribution. The Paired t test was performed to assess the difference between score means when the data were normally distributed; otherwise the Wilcoxon Test was used to check T test results. One Way ANOVA was performed to assess the difference of the score means between patients with and without the studied charac- teristic. When the Levene test for homogeneity of var- iances was significant (p < 0.05) the Mann Whitney test was used to check ANOVA results. Pearson ’s Chi square test, calculated by Exact Method, was performed to investigate the relationships between grouping variables. Pearson’s correlation analysis was used to test relationship between continuous variables. For all tests p < 0.05 was considered significant. Statistical Analysis was performed by means of the Statistical Package for the Social Sciences (SPSS) software version 15.0 (SPSS Inc., Chicago, USA).

Of the 120 patients assessed for eligibility, 20 were excluded. Seven did not have a histologically confirmed DIE following laparoscopic excision of their disease. Nine did not complete the questionnaire. Four did not come to the 6 months follow-up visit. Consequently, 100 patients were enrolled in our study. Average age at the time of surgery was 34.2 ± 4 years (range [23-39]) and mean body mass index was 21.6 ± 2.7 Kg/m² (range [19-32]). Regarding previou ss u r g i c a lt r e a t m e n t sf o r endometriosis, 27% (27/100) had one previous proce- dure, 4% (4/100) had two and one patient had three pre- vious interventions. Operative findings, surgical procedures, additional procedures performed and com- plications are summarized in Table 1. SF 36 Scores After laparoscopic surgery for DIE, at 6-months follow up, a significant improvement was observed in the SF- 36 total score, in the SF-36 component summaries and in every scale of the SF-36 (p < 0.0005) (Table 2). Among patients with intestinal DIE, significant differ- ences in postoperative scores of SF-36 were not detected between patients submitted to intestinal nodule shaving and segmental intestinal resection (p > 0.05) (Table 3). Pain scores were significantly improved after six months from surgical treatment (p < 0.05). Preopera- tively 99% of women had dysmenorrhea (mean VAS Table 1 Surgical procedures, additional surgical procedures, intra-operative and postoperative complications of the laparoscopic management of DIE Number Surgical procedures: - Recto-vaginal septum nodule resection 62 - Intestinal nodule shaving 50 - Segmental intestinal resection 16 - Vagina nodule resection 32 - Utero-sacral ligaments nodule resection 44 - Bladder nodule resection 41 - Ureteral nodule resection: 18 - Ureterolyisis 15 - Segmental ureteral resection with end to end anastomosis 3 Additional surgical procedures performed: - Appendectomy 4 - Nephrectomy 1 - Temporary colostomy 1 Intra-operative complications - Bowel injury 0 - Bladder injury 0 - Ureteral injury 0 - Vascular injury 1 - Blood loss exceeding 500 ml - Conversion to laparotomy 1 0 Postoperative complications - Transient fever > 38 °C 8 - Transient urinary retention 3 - Urinary incontinence 1 - Uretero-vaginal fistula 1 - Recto-vaginal fistula 1 Table 2 Mean (± Standard deviation) preoperative and postoperative scores of the scale of SF-36 BEFORE AT 6 MONTHS FOLLOW-UP P value SF-36 total score 49 ± 20 71 ± 17 < 0.0005 Physical Component Summary 49 ± 19 70 ± 17 < 0.0005 Physical Function 77 ± 23 90 ± 14 < 0.0005 Role - Physical 40 ± 39 77 ± 35 < 0.0005 Body pain 38 ± 20 68 ± 24 < 0.0005 Mental Component Summary 47 ± 20 66 ± 17 < 0.0005 Social Functioning 50 ± 22 72 ± 22 < 0.0005 Role Emotional 40 ± 40 76 ± 33 < 0.0005 Mental Health 54 ± 18 65 ± 16 < 0.0005 General Health 47 ± 21 59 ± 19 < 0.0005 Vitality 46 ± 19 57 ± 17 < 0.0005 Mabrouk et al . Health and Quality of Life Outcomes 2011, 9:98 http://www.hqlo.com/content/9/1/98 Page 3 of 7 score of 7 ± 3), 76% dyspareunia (mean VAS score of 5 ± 3), 63% chronic pelvic pain (mean VAS score of 4 ± 3), 67% dyschezia (mean VAS score 5 ± 4) and 34% had dysuria (mean VAS score of 2 ± 3). Postoperatively, at 6 months follow up, 23% of women reported dysmenor- rhea (mean VAS score 1 ± 3), 23% dyspareunia (mean VAS score of 1 ± 2), 18% chronic pelvic pain (mean VAS score of 1 ± 2), 17% dyschezia (mean VAS score of 1 ± 2) and 6% dysuria (mean VAS score of 0 ± 1). On pelvic examination and through ultrasound exam, there were no cases of anatomical recurrence at 6- months follow-up. Seventy-one percent of patients (71/100) assumed postoperative hormonal treatment (33 with cyclic, 27 with continous oral estro-p rogestogenic; 4 with cyclic estro-progestogenic, 2 with continous vaginal ring; 3 with oral progestins and 2 with estro-progestogenic cyc- l i cp a t c h ) .T h e r ew e r en os i g n i f i c a n td i f f e r e n c ei nt h e SF-36 postoperative scores between patients who received postoperative medical treatment and patients who did not (p > 0.05). outcomes after surgical treat- ment of DIE.

By performing this trial and re viewing the available lit- erature, we tried to answer some questions related to this particular pathology, DIE: 1) Is it important to consider objective QOL evaluation in patients with DIE? In 2000, Garry et al. affirmed that endometriosis exerts a profoundly adverse effect on the personal life and rela- tionships of patients [2]. The intensity and frequency of symptoms, their association and concomitant infertility, the secondary effects of medical and surgical manage- ment, symptoms persistence after treatment, disease relapse and the need of continuing a therapy for a long term affect negatively quality of life [20]. We believe that one of the primary goals of the management of endometriosis is not only symptom reduction, but also improvement of the overall patient ’s quality of life. In this perspective, the evaluation of the efficacy of surgical management of endometriosis only in terms of pain and symptoms improvement seems insufficient. Recently Dubernard et al. proposed SF-36 questionnaire as a tool that can predict the degree of change in QOL after laparoscopic management of posterior DIE [27], deli- neating a new approach of DIE in which QOL evalua- tion can guide the management of the disease. 2) Does laparoscopic management of DIE improve QOL? After laparoscopic surgery for DIE, at six-month follow up, we observed a significant improvement in all scales of the SF-36. Many studies confirmed that laparoscopic treatment of endometriosis is effective in relieving dysmenorrhoea, dyspareunia, non-menstrual pelvic pain and dyschezia ([2,33,34,36]). In a randomized placebo-controlled trial of 39 women, Abbott et al. demonstrated that laparoscopic excision of endometriosis is more effective than placebo on pain reduction and quality of life improvement at 12 months from surgery [21]. However, in this trial, authors evalu- ated all rAFS stages of endometriosis and not DIE. Jones et al. included in their study on laparoscopic ablative surgery for endometriosis, the evaluation not only of pain scores, but also of patient satisfaction scores. They showed that women with rAFS stage III-IV of endometriosis who underwent treatment presented a high rate (87.7%) of satisfaction [36]. In 2000, Garry et al showed that radical laparoscopic excision of endometriosis stage III and IV of rAFS sig- nificantly improved the physical component score of the QOL questionnaire, return ing the score value to a Table 3 Mean improvement (± Standard deviation) of SF-36 scores six months after surgery. INTESTINAL RESECTION (16 patients) NODULE EXCISION (50 patients) P value ΔSF-36 total score 37 ± 36 35 ± 42 0.08 ΔPhysical Component Summary 36 ± 35 35 ± 41 0.23 ΔPhysical Function 14 ± 25 13 ± 24 0.30 ΔRole - Physical 41 ± 46 43 ± 40 0.06 ΔBody pain 32 ± 31 30 ± 26 0.41 ΔMental Component Summary 24 ± 42 26 ± 36 0.09 ΔSocial Functioning 21 ± 32 21 ± 26 0.08 ΔRole Emotional 35 ± 51 38 ± 41 0.07 ΔMental Health 8 ± 24 10 ± 19 0.09 ΔGeneral Health 10 ± 22 11 ± 20 0.06 ΔVitality 10 ± 22 11 ± 18 0.07 Comparison between patients submitted to segmental intestinal resection and patients submitted to intestinal nodule excision. Mabrouk et al . Health and Quality of Life Outcomes 2011, 9:98 http://www.hqlo.com/content/9/1/98 Page 4 of 7 normal range. The mental component score improved too, but this was not statistically significant and failed to reach a normal range four months after treatment [2]. This study analyzed prospectively 57 patients and was performed using Short Form 12 (SF12) and Euro QOL (EQ-5D) questionnaire preoperatively and 4 months after surgery. However, SF-12 questionnaire reproduces the eight scale profile with fewer levels than SF-36 scales and yields less precise scores [27]. In 2003, Abbott et al. studied 176 women who under- went laparoscopic excision of endometriosis, evaluating long term outcome through the use of QOL question- naire [3]. The results evidenced that women with endo- metriosis have an impaired QOL which improve after treatment in a significant manner. The increase in the physical component appeared greater than the mental component of the score. However the results of this prospective study with an evaluation of the QOL in the long-term may be affected by the high rate of women who did not respond to the follow-up questionnaire (26%). 3) Is there a difference in QOL improvement between patients who undergo nodule shaving or segmental intestinal resection? We found that there was no significant difference in the six-month postoperative im provement of SF-36 scores among women with intestinal DIE who underwent nodule shaving or segmental intestinal resection. In the literature the debate regarding the surgical management of intestinal DIE is current [37]. While some studies evidenced a significant QOL improvement in women treated with colorectal segmental resection [38-41], others suggested nodule excision or shaving, as a first choice procedure. These authors retrieved an increased risk of postoperative complications together with de novo intestinal and urological symptoms appearance in patients submitted to segmental intestinal resection [37,40,42-44]). Recently Roman et al. in a ret- rospective study evidenced that women undergoing col- orectal resection when compared with women managed by nodule excision, were more likely to present several unpleasant functional digestive outcomes and urinary dysfunctions [37]. However, the choice of colorectal resection is supported by th ef a c tt h a tt h ea b s e n c eo f bowel resection in women with DIE and intestinal endo- metriosis is the factor most strongly associated with recurrence rate [8]. Moreover, there are studies which showed that microscopic end ometriotic lesions usually exist around the main rectal nodule [15,45]. In our opi- nion, important issues to be considered, when deciding the need and the type of surgery in women with intest- inal endometriosis, are the actual status and the expected improvement of the patient ’s QOL, as well as the potential functional ou tcomes of surgery. Finally, further prospective randomized studies are necessary to assess which surgical management is more indicated in patients with intestinal DIE. 4) Does postoperative hormonal treatment influence QOL at six-month follow up? We did not find any significant difference in all SF-36 scores between patients submitted to the surgical treat- ment alone and patients who received six-month post- operative hormonal treatment. Considering DIE, it has been shown that continuous post-operative hormonal treatment might prevent pain recurrences after surgical removal of deep infiltrating nodules [46] Regarding the elective postoperative management of endometriosis, data from the randomized trials are con- troversial in terms of pain recurrence and anatomical relapse. A Cochrane review of 2004 showed that post- surgical hormonal suppression of endometriosis com- pared to surgery alone (either no medical therapy or placebo) showed no benefit for the outcomes of pain [47]. Muzii et al [48] found no significantly difference in the recurrence rates of pain at follow-up between patients receiving oral contraceptives pills (9.1%) and untreated patients (17.1%). Furthermore, Koga et al. found in their retrospective study that a mean post- operative treatment of 9.5 months did not influence recurrence [49]. Recently, different studies evidenced an important role of long term postoperative use of oral contraceptive on symptoms and disease recurrence [50-52].It seems that the length of the treatment is, therefore, an important factor in the long-term efficacy of therapy. However, all these trials considered only pain recurrence and anatomical relapse, ignoring QOL evaluation. Further trials are necessary to assess whether postoperative medical therapy impact on the QOL. Recently, some authors adopted the concept that in the treatment of DIE, it is most likely that medical and sur- gical treatments should be associated [26,53]. Certain limitations of this study must be underlined. Our results may be influenced by the fact that one third of the women (31%) involved in the study had pre- viously been surgically treated for endometriosis. In these women, the previous failed surgery may bias the QOL perception with lower preoperative SF-36 scores. Second, more than an half of patients (56%) were taking hormonal therapy before surgical treatment and a large proportion (71%) of women was given postoperative hormonal treatment. This may potentially have a signifi- cant bias on the symptoms and QOL perception of these women. However, as it has been stated by recent studies, long term outcomes of the surgical treatment of endometriosis are positively correlated with the Mabrouk et al . Health and Quality of Life Outcomes 2011, 9:98 http://www.hqlo.com/content/9/1/98 Page 5 of 7 assumption of postoperativ e medical therapy leading to the conclusion that only the combination of surgery plus medical therapy may guarantee long term effect [ 5 3 ] .T h i r d ,o u rs t u d ye v aluated QOL after only six months postoperatively, which seems to be a short time to complete the recovery from this complex surgery. However, there is an ongoing study in our centre aiming to assess long term QOL outcomes after surgical treat- ment of DIE.

We found that laparoscopic excision of DIE lesions appreciably improves general health and psycho-emo- tional status at six-month follow up without differences between patients submitted to intestinal segmental resection or nodule shaving. We strongly believe that

QOL assessment should be considered as a complementary index to evaluate need and success of therapeutic interventions in DIE. List of abbreviations The abbreviations used in the manuscript are summarized: BP: bodily pain; DIE: deep infiltrating endometriosis; GH: general health; MCS: mental component summary; MH: mental health; PCS: physical component summary; PF: physical functioning; RE: role emotional; RP: role physical; QOL: quality of life; SF: social functioning; SF-36: short form 36; VAS: visual analogue scale; VT: vitality. Author details 1Minimally Invasive Gynaecological Surgery Unit, S.Orsola Hospital, University of Bologna, Italy. 2Department of Obstetrics and Gynecology, Alexandria University, Egypt. Authors’ contributions All authors read and approved the final manuscript. They contributed to the manuscript as follows: GM, MM and SR were involved in the conception and design of this study, in the analysis and interpretation of data, and in development and review of the manuscript for intellectual content. MG and GM were involved in the analysis and interpretation of data and in development and review of the manuscript for intellectual content. VG, MG and VC were involved in the interpretation of data and in review of the manuscript for intellectual content. FC, SA, DDN and FC were involved in the collection of data. FG, DFS, GE, SS and RD were involved in the statistical analysis. ZL was involved in the manuscript revision. Competing interests The authors declare that they have no competing interests. Received: 18 February 2011 Accepted: 6 November 2011 Published: 6 November 2011

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Gynecol Obstet Fertil 2009, 37(10):771-2. doi:10.1186/1477-7525-9-98 Cite this article as: Mabrouk et al .: Does laparoscopic management of deep infiltrating endometriosis improve quality of life? A prospective study. Health and Quality of Life Outcomes 2011 9:98. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit Mabrouk et al . Health and Quality of Life Outcomes 2011, 9:98 http://www.hqlo.com/content/9/1/98 Page 7 of 7