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Employing laparoscopic surgery for endometriosis

Endometriosis is a chronic, multifactorial disease, which can impact significantly on a women’s quality of life. It is associated with pelvic pain, dyspareunia and intestinal disorders, and can lead to infertility. The use of laparoscopic surgery in the management of endometriosis is well documented; however, the optimal management of women with deep infiltrating disease remains controversial. This review describes the different surgical strategies for the treatment of endometriosis. Keywords:  bowel resection • economical surgery • endometriomas • endometriosis • laparoscopy • pelvic surgeon • surgery • young patient

Background Endometriosis is characterized by the presence of endometrial glands and stromal tissue outside the uterine cavity. The disease is more commonly found in the pelvis, inducing an inflammatory-type reaction leading to adhesions and distortion of pelvic anatomy. Symptoms vary greatly and often do not correlate well with disease severity [1] . Symptoms include pelvic pain, infertility, dyspareunia, dyschezia and painful micturition, which can range from mild to severe. In severe cases the disease can be physically debilitating, impacting significantly on a women’s quality of life, with both psychological and social implications. Laparoscopy remains the gold standard for the diagnosis and treatment of endometriosis; however, the standardization of specific surgical techniques is controversial and remains an intensely debated subject. One of the key hurdles in the management of this disease is that the etiology remains unclear. Treatment is therefore often targeted towards symptomatic management either by means of surgical excision of disease, or ablative techniques with or without the use of concurrent medical management. One must be mindful that endometriosis is a benign chronic disease affecting predominantly healthy young

10.2217/WHE.14.28 © 2014 Future Medicine Ltd

Karolina Afors*,1, Rouba Murtada1, Gabriele Centini1, Rodrigo Fernandes1, Carolina Meza1, Jesus Castellano1 & Arnaud Wattiez1 IRCAD, Hopitaux Universitaires, 1 Place  de l’Hopital, 67091 Strasbourg, France *Author for correspondence: drkafors@ gmail.com 1

women who wish to preserve their fertility. Laparoscopic management of endometriosis should be individualized, maintaining a radical approach towards the disease while preserving and safeguarding function of pelvic structures. This review will serve to appraise the evidence for different strategies of surgical management of endometriosis, in addition to addressing both the benefits and limitations of these procedures. Ablation & excision techniques Laparoscopy is the gold-standard investigation for diagnosis of endometriosis, with a sensitivity of 69% and a specificity of 83% where visual findings are correlated with histological diagnosis of endometriosis [2] . Although diagnosis is complicated by the need for an invasive procedure it enables simultaneous treatment of the disease. Surgical treatment can generally be divided into ablation or surgical techniques. Various modalities for ablation exist including carbon dioxide (CO2) laser ablation, bipolar diathermy and monopolar electrosurgery. The effectiveness of ablative surgery in the treatment of peritoneal disease has been demonstrated in randomized controlled trials. Sutton et al. randomized women with stage 1–2 disease to either laparoscopic

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Review  Afors, Murtada, Centini et al. ablation or diagnostic laparoscopy alone. At 6-months follow-up, 62% in the laser group reported improved pelvic pain compared with only 22% in the control group [2] . Benefits of ablative treatment were poorest in those patients with minimal disease. In patients with mild and moderate disease only, up to 73% of patients achieved adequate pain relief [2] . Further studies have confirmed these findings and a recent meta-analysis demonstrated laparoscopic surgery to be of significant benefit in the treatment of pain secondary to endometriosis when compared with diagnostic laparoscopy alone [3] . Presently, however, no randomized controlled evidence exists demonstrating the most effective surgical technique for the treatment of peritoneal disease [4] . A randomized controlled trial comparing excisional and ablative treatment modalities for mild endometriosis demonstrated good symptomatic relief for both treatment modalities [5] . There was no statistically significant difference between the two treatment options and excisional treatment was not associated with a higher morbidity [5] . A high pretreatment score level was a predictor for greater improvement following treatment [5] . The incidence of women who fail to improve following ablative surgery may occur as a result of incomplete treatment. In cases of deep infiltrative endometriosis the energy source used for ablation may only treat the superficial portion, being unable to penetrate deeper owing to the risk of thermal damage to underlying structures. These patients may benefit from excisional surgery. Abbott et al. conducted a randomized, blinded, crossover study examining the effectiveness of laparoscopic excision for all stages of endometriosis [3] . Significant symptomatic improvement was found in 80% of women following excisional surgery compared with a 30% placebo response rate irrespective of the severity of disease. However, 20% of women in this study reported no improvement in symptoms after excisional surgery [3,6] . These women typically had stage 1 disease, whereas women with more extensive disease had a greater response to laparoscopic excision [3,6] . Treatment of ovarian endometriomas Endometriotic deposits within the ovary, referred to as endometriomas, have been the subject of much debate with regard to appropriate surgical management, namely excision or drainage and ablation of the cyst. A Cochrane review found that laparoscopic excision of the endometriotic cyst wall was associated with reduced recurrence of dysmenorrhea, dyspareunia and nonmenstrual pelvic pain [7] . Based on the current evidence, laparoscopic ovarian cystectomy seems to be the preferred method of treatment with a significantly decreased risk of recurrence [6] .

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The stripping technique is often employed to excise the cyst wall; however, when utilizing this technique care should be taken to minimize damage and inadvertent removal of normal ovarian tissue. Even in the hands of experienced surgeons, significant reduction in ovarian volume following excision of endometriomas has been observed [8] . In our practice, we use a standardized approach starting with adequate exposure of the surgical field. Adhesiolysis is performed and the cyst ruptured. The cyst is intentionally emptied and removed through a single puncture point. Multiple openings and incisions are avoided to minimize potential damage to functional ovarian tissue. In order to identify the correct cleavage plane the cyst is everted and a central incision made. This divides the cyst in equal halves and gentle traction and counter-traction is used to strip the cyst capsule from the ovarian parenchyma. Correct identification of the cleavage plane minimizes bleeding, reducing the need for blind bipolar coagulation. Surgical experience is necessary to minimize damage to normal ovarian tissue while at the same time avoiding the risk of recurrence from residual disease. A combined technique using both excisional and ablative strategies has also been described [9] . Similarly the cyst is opened and drained followed by identification of the cleavage plane. Gentle traction is used to strip the cyst wall from the normal ovarian tissue. If, however, bleeding occurs, which is typically seen at the hilum where the cleavage plane is often fused and difficult to identify, then the tissue is removed and a partial cystectomy performed. CO2 laser or bipolar can then be applied to treat the remaining foci of the endometrioma. Suturing of the ovary may then be considered to restore its anatomical position. For large endometriomas, greater than 5 cm, a twostep procedure can be used. A small puncture site is made on the antimesenteric border of the ovary, the cyst wall is opened and emptied by means of irrigation and drainage, and a biopsy taken. Following this initial step, gonadotrophin-releasing hormone agonist therapy is administered for 3 months, over which time the thickness of the cyst wall significantly decreases, with atrophy and reduction in stromal vascularization of the cyst [10] . The surgery is completed with a secondlook laparoscopy allowing CO2 vaporization, bipolar diathermy or plasma ablation of the cyst wall lining. Although women are required to undergo two invasive procedures, results have shown a recurrence rate of 8% with a follow-up of 2–11 years and a smaller decrease in ovarian reserve rates confirmed by measuring anti-Müllerian hormone (AMH) levels [11–13] . Achieving hemostasis following cystectomy has not been shown to adversely effect ovarian reserve [14] .

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Employing laparoscopic surgery for endometriosis 

The effects of bipolar electrocoagulation compared with suturing following laparoscopic excision of endometriomas found no significant difference in AMH levels between the two groups [15] . There was also no difference in IVF outcomes between the two groups [15] . Fertility-preserving surgery in endometriosis The cause of infertility secondary to endometriosis is unclear, but it is probably multifactorial. The inflammatory response in even superficial endometriosis may affect oocyte quality and interfere with both fertilization and implantation. In cases of more severe infiltrative disease, the presence of adhesions distorting pelvic anatomy is sufficient to impact on fertility. Severe symptomatology in endometriosis may also indirectly affect fertility secondary to its negative impact on sexual relations, potentially compromising a couple’s relationship. Laparoscopic surgical treatment of mild (stage 1–2) endometriosis, whether by means of ablation or excision, has proven effective in improving fertility when compared with diagnostic laparoscopy alone [16] . No randomized controlled trial was able to determine the most effective surgical technique (excision vs ablation); however, in the presence of deep infiltrating endometriosis and pain, excisional treatment may be considered beneficial [17] . Laparoscopic excision of endometriomas increases spontaneous pregnancy rates in cases of subfertility when compared with ablative techniques alone [6] . A more favorable response to ovulation stimulation with clomiphene and gonadotrophins has also been noted [6] . The effect of endometriomas on fertility treatment remains controversial. A meta-analysis evaluating IVF outcomes found no significant difference in pregnancy and clinical pregnancy rates per cycle in patients who underwent surgery or conservative management of endometriomas [18] . Within the meta-analysis several studies were excluded from analysis as they did not have adequate control groups. In addition, it is difficult to confirm whether patients had co-existing peritoneal endometriosis, which may have further contributed to poor IVF outcomes. A Cochrane review published in 2010 confirmed similar findings with regard to IVF outcomes [16] . In women with bilateral endometriomas, IVF outcomes showed a reduction in ovarian responsiveness, although the overall pregnancy rate was not affected [19] . Despite this evidence, it is important to emphasize that endometriosis itself can impact significantly on fertility and can cause chronic pain. Women with ovaries containing endometriomas have been associated with a lower spontaneous ovulation rate, irrespective of the size of the cyst [20] . The benefit with surgical treatment is that it can both

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alleviate symptoms and also increase spontaneous pregnancy rates without the need for invasive fertility treatments. It begs to reason that although there is evidence of a deleterious effect on ovarian reserve in the case of removal of endometriomas, employing precise surgical strategies in experienced hands can minimize this risk while improving fecundity. In women undergoing laparoscopic surgical treatment of endometriomas particular care in evaluating ovarian reserve is important, as removal of ovarian tissue during cystectomy has been observed in several studies. Serum levels of AMH have been shown to correlate well with resting follicle count, thereby serving as a useful marker in measuring ovarian reserve [21] . In women, AMH levels remain stable throughout the menstrual cycle, decline with age and are undetectable after the menopause. Significant reductions in AMH have been documented following excisional surgery for endometriomas [22] . Busacca et al. demonstrated a 2.5% ovarian failure rate following bilateral endometrioma surgery and Muzi et al. showed removal of ovarian tissue in 54% of patients undergoing excisional treatment utilizing the stripping technique [23,24] . A meta-analysis in 2012 analyzing changes in serum AMH following surgical excision of endometriomas demonstrated a significant reduction in AMH levels [25] . These findings were confirmed by a second meta-analysis by Raffi et al. [22] . Whether the initial decrease in AMH following excision of an endometrioma persists is difficult to evaluate. Several studies have demonstrated a persistent decline in AMH levels up to 12 months following surgery [8,26] . Conversely, other studies have demonstrated an initial decrease in AMH levels followed by a subsequent recovery 1 month after surgery [27] . Differing surgical skill or study population, and changes in AMH secondary to storage processing may explain discrepancies in the available data [14] . The most appropriate surgical strategy in cases of infertility related to severe endometriosis is unclear. No randomized controlled trials have assessed whether fertility improves following radical surgery for stage 3 and 4 disease, although observational studies have demonstrated promising results [28,29] . A study by Stepniewska et al. compared three groups of infertile patients with severe endometriosis [30] . One group underwent segmental resection for bowel endometriosis, the second group underwent excision of endometriosis without bowel resection (despite disease being present), and the third underwent surgery for treatment of severe endometriosis but had no bowel involvement [30] . The spontaneous pregnancy rate was lower in patients found to have bowel endometriosis, and in these women improved reproductive outcome was noted if bowel resection was performed [30] . The place for segmental

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Review  Afors, Murtada, Centini et al. bowel resection in cases of deep infiltrating endometriosis in patients whose only symptom is infertility in the absence of pain has not been determined. Bowel resection is not without its risk and the extent to which rectovaginal endometriosis affects infertility is unclear. As such, patients should be carefully selected and counseled regarding the specific complication risk and uncertain benefit of surgery. Recurrent endometriosis may have a considerable negative impact on reproductive performance. A systematic review demonstrated a significant reduction in conception rate in women undergoing repeat surgery compared with those undergoing a primary procedure [31] . The chance of achieving a pregnancy was almost half that observed in primary surgery [31] . When comparing IVF and repeat surgery the conception rate was lower following only one cycle, but higher when two cycles of IVF were performed [32] . In women presenting with infertility, stage 3/4 endometriosis and who have previously undergone surgery, IVF may be considered beneficial over repeat surgical intervention [33] . However, there is insufficient data to assess the effect of surgical treatment in addition to IVF on pregnancy outcomes in endometriosis [33] . Urinary tract endometriosis Endometriosis of the urinary tract is generally reported as affecting approximately 1% of women with endometriosis; however, the incidence varies between centers and has been reported to be as high as 20% [34,35] . Of these cases, 85% involve the bladder, 10% ureter, 4% kidney and 2% urethra [36] . Bladder endometriosis is more commonly associated with other lesions of the pelvis such as nodules of the uterosacral ligaments and rectovaginal septum. Bladder endometriosis

Bladder endometriosis is defined as the presence of endometrial glands infiltrating the detrusor muscle. It is associated with a myriad of nonspecific urinary symptoms such as urinary frequency, dysuria, urgency and, rarely, hematuria, which can delay diagnosis. Cyclical pain related to menses may confirm a clinical suspicion of endometriosis [34,37] . The gold standard for diagnosis of bladder endometriosis is direct visualization of lesions at cystoscopy or laparoscopy. Transvaginal ultrasonography and MRI may be useful in diagnosis; however, small lesions may be missed. Laparoscopic management of bladder endometriosis is dependent on the anatomical position and size of the infiltrative lesion. Careful dissection using a skinning technique removing superficial endometriosis of the bladder peritoneum can be performed, followed

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by closure of the defect with interrupted 3/0 monofilament suture. Infiltrative lesions with involvement of the bladder mucosa situated in the bladder dome can be managed with partial cystectomy. Closure of the bladder with a single or double layer monofilament is recommended and methylene blue test should be performed to ensure integrity of the suture line. In cases of more complex lesions involving the posterior wall of the bladder or the trigone, cystoscopy and insertion of double J stents may be considered. Adhesions between the anterior uterine wall and the vesicouterine fold should be divided prior to performing partial cystectomy. Removal of double J stents should be delayed by 6–8 weeks postoperatively and a urinary catheter left in situ for a minimum of 7 days. In our practice, a urinary catheter is more often left in place for a minimum of 10 days. Low-pressure cystography can also be performed prior to removal of the catheter to verify adequate repair and healing of the bladder. Ureteral endometriosis

Ureteric involvement can be categorized into intrinsic or extrinsic and although rare can cause significant morbidity with silent loss of renal function. Extrinsic disease accounts for 85% of cases and causes infiltration of the overlying peritoneum, which can cause compression of the ureter resulting in hydronephrosis and, if left untreated, renal impairment [36,38] . Intrinsic disease occurs in 15% of cases leading to fibrosis of the muscularis and, in some instances, the mucosa. Ureteric endometriosis is more prevalent on the left-hand side, which may be attributed to the menstrual reflux theory and anatomical differences of the right and left hemi pelvis [39] . The main aim of surgical treatment is to relieve obstruction, if present, while preserving renal function and preventing recurrence. Surgical treatment options include: ureterolysis, ureteral resection with end-to-end anastomosis or ureteroneocystostomy, and in cases of complete loss of kidney function, ureteronephrectomy can be considered [36,40] . Placement of a double J stent should be considered in cases of urinary obstruction and hydronephrosis or where significant ureteric stenosis has been diagnosed preoperatively. Due to the inflammatory nature of endometriosis the double J stent should be left in place for approximately 6 weeks. At laparoscopy the ureter should be identified above the level of disease. This is more easily done at the level of the pelvic brim where the retroperitoneal space can be opened and the course of the ureter followed. In ureteric endometriosis ureterolysis should be performed with care taken to avoid devascularization by preserving the adventitial layer and corresponding

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vascular branches. Fibrosis secondary to endometriosis often leads to medial displacement of the ureter and care should be taken during its dissection. In cases of critical stenosis of the ureter or intrinsic disease, a ureteral resection with end–end anastomosis can be performed. Studies have shown promising results with minimal complications and recurrence rates [38,41,42] . Ureteroneocystostomy is recommended when a long ureteric segment requires resection or if the disease is near the level of the ureterovesical junction. Reimplantation of the ureter allows the fibrotic area of disease to be bypassed, minimizing the risk of recurrence [36] . A tension-free anastomosis should always be observed and if more length is required a psoas hitch can be considered. Due to the rarity of this condition there is limited evidence regarding treatment of ureteral endometriosis. Most studies involve observational case series; however, the results are promising and in terms of patient morbidity, results are comparable to those treated by laparotomy. The overall incidence of complications has been reported as 12% with some studies illustrating no long-term consequences and low recurrence rates [43] . Similarly, recurrence rates have been reported ranging from 5–15% with some studies reporting no relapses [38] . Deep infiltrating endometriosis of the Pouch of Douglas Deep infiltrating endometriosis typically refers to endometriotic lesions involving the rectovaginal space and occurs in approximately 20% of women with endometriosis. It infiltrates the vagina, rectum, cervix and rectovaginal septum and in some cases can completely obliterate the Pouch of Douglas. A systematic surgical approach can be adopted for removal of rectovaginal nodules (Table 1) .

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Deep infiltrating endometriosis commonly affects the posterior compartment, with involvement of the uterosacral ligaments most frequently found. Isolated uterosacral lesions occur in up to 83% of cases [44] . Lateral extension of lesions from the uterosacral ligament can result in infiltration of the cardinal ligament and may lead to ureteric involvement by means of extrinsic compression [45] . In 16.8% of cases, uterosacral disease was associated with additional lesions, most commonly of the vagina, followed by intestinal and lastly bladder lesions [44] . Surgical excision of uterosacral endometriosis has been demonstrated to be effective in the management of pelvic pain symptoms with a 0.8% risk of major intraoperative complications [44] . Surgical strategy for the management of isolated uterosacral lesions typically involves ureterolysis, with dissection medial to the ureter so it can be lateralized. The dissection is continued caudally until the level of insertion of the uterosacral ligaments (instead of uterine torus). In cases of additional infiltrative disease of the vagina, excision of the posterior upper component may need to be performed. During dissection, care should be taken to avoid damage to the hypogastric nerve, which is closely related to the uterosacral ligaments at it attaches to the posterolateral aspect of the uterus [46] . If possible, dissection should be limited and not pass beyond the deep uterine vein, the location at which the hypogastric nerve joins the inferior hypogastric plexus. Damage of this nerve complex during radical excision of uterosacral endometriosis can result in functional postoperative complications, namely bladder voiding problems requiring intermittent self-catheterization [47] . In cases of bilateral uterosacral disease there is a higher risk of nerve damage and subsequent functional bowel and bladder disorders. In these instances a more conservative approach may be adopted to preserve organ function [48] .

Table 1. Systematic surgical approach for resection of rectovaginal endometriosis. Surgical steps

Explanation

Identification of ureters

Consider ureterolysis if course of ureter is obscured

Dissection of the pararectal fossa

Avascular space that can be dissected lateral to the rectum and medial to the hypogastric nerve

Rectovaginal dissection

Start cranially and end caudally. Identification and dissection of nodule until healthy tissue is reached on posterior vaginal wall

Dissection of endometriosis from anterior rectal wall

Enables nodule to be freed from the rectum

Removal of nodule from posterior vaginal wall

Depending on the depth of involvement and size of nodule the vagina may be opened and specimen extracted

Closure of colpotomy

Closure with interrupted monocryl 2/0. Use a vertical incision so as not to shorten the vagina

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Review  Afors, Murtada, Centini et al. Bowel endometriosis Endometriosis involving the bowel occurs in 3–37% of cases, commonly affecting the rectum, rectosigmoid junction or sigmoid colon in up to 90% of cases [49] . This type of deep infiltrating disease is complex, able to distort pelvic anatomy and often requires a multidisciplinary team approach with involvement of colorectal surgeons. Different surgical techniques exist, ranging from less radical excision by means of ‘shaving’ or discoid resection to more aggressive surgical treatment, namely bowel resection (Figure 1) . Perioperative imaging remains an important tool in assessing depth of disease, location and the occurrence of multiple lesions if present. Appropriate preoperative investigations can aid in treatment planning, preparing both the patient and surgeon alike. Several imaging modalities have been recommended such as transrectal/transvaginal ultrasonography, MRI, computed tomography and colonoscopy. Studies have demonstrated a sensitivity and specificity of 98 and 100%, respectively, with the use of transrectal/transvaginal ultrasonography. Similarly, MRI was shown to have a sensitivity of 83% and specificity of 98% [50,51] . Transvaginal sonography with water contrast in the rectum has also been demonstrated as effective in detecting endometriotic lesions of the bowel, with a sensitivity of 96% and specificity of 90% [52] . Moreover, studies have shown this technique to be effective in detecting stenotic endometriotic lesions with successful evaluation of the degree of lumen narrowing [52] . Double-contrast barium enema has demonstrated good correlation with pathological

findings of bowel endometriosis. It is cost effective, and enables assessment of the complete large bowel, with a sensitivity of 84.7% and a specificity of 93.7% [53] . Despite this evidence, location of endometriotic lesions can be underestimated where depth of infiltration is often overestimated due to the extent of surrounding fibrosis [54] . In cases where bowel resections were performed based on imaging findings alone, no rectal involvement was found in up to 29% of cases based on histological findings. Digestive symptoms are not pathognomonic for rectal involvement; instead, pelvic pain radiating to the rectum has been reported as the most common presenting complaint of patients with colorectal endometriosis [55] . This makes pre­ operative planning and predicting the need for extensive excisional bowel surgery difficult. Patients recognized as having severe, deep infiltrating endometriosis should be operated on by an experienced specialist with sufficient skill and ability in an appropriate center with multidisciplinary team input. Conservative laparoscopic excision: ‘shaving’ & discoid resection Shaving, or mucosal skinning, involves careful dissection of the endometriotic nodule freeing it from the bowel wall without breaching the bowel lumen (Figure 1) . Areas of exposed mucosa are then sutured to maintain integrity and avoid postoperative perforation. This shaving technique has had promising results with low complication rates. Donnez and Squifflet reported a 1.4% rate of rectal perforation in a series

Serosa

Muscular Shaving Mucosal skinning Discoid resection

Mucosa

Submucosa

Figure 1. Illustrative diagram outlining differences in surgical techniques for treatment of endometriotic bowel lesions.

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of 500 patients and a recurrence rate of approximately 7% [28] . The overall pregnancy rate was 84%, with a natural conception rate of 78% [28] . Similar studies have reported low complication rates and recurrence rates of approximately 19%. This conservative approach allows preservation of nerves and blood supply, minimizing the risk of postoperative functional bowel and bladder complications. Discoid excision involves removal of disease with full-thickness resection of the anterior rectal wall and subsequent laparoscopic repair in 1–2 layers or by using a transanal circular stapler [56] . An initial shaving of the nodule may be necessary for debulking purposes. A guide suture is then placed at the level of the nodule and a circular stapler is inserted transanally. Once inserted, the device is opened and the bowel segment containing the nodule is placed within the groove between the anvil and the stapler. The stapler is angled upwards while gentle traction is placed on the guide suture downwards, ensuring only the anterior section of the rectal wall is included in the stapler. The device is then closed, fired and carefully removed. The remnant tissue on the anvil should consist of two semicircular segments, which should be verified to ensure an adequate anastomosis. This technique is suitable for bowel lesions up to 2–3 cm in size. For larger lesions up to 5 cm a double discoid technique can be used. Two circular stapling lines are formed the first above the lesion and the second more distal including the initial suture line from the first firing [57] . Limitations of this technique is that high lesions, >15 cm from the anal verge, are inaccessible due to the fixed length of the stapler. With concurrent stenotic lesions it may be impossible to pass the stapling device beyond the lesion, and as such it should not be used in instances where there is greater than a third obstruction of the bowel lumen. Anterior discoid resection has been shown as effective in reducing a patient’s symptoms with low complication rates ranging from 0 to 12.5% [56,58,59] . Retrospective studies have demonstrated a high patient satisfaction with significant improvement in dyspareunia and low postoperative complication rates [54,58] . In a case–control study comparing discoid and segmental bowel resections, segmental resection was associated with longer operative time, increased rate of temporary ileostomy, postoperative fever and long-term bladder dysfunction [56] . A total of 10.4% of the discoid resection group showed severe anemia secondary to bleeding at the level of the bowel anastomosis requiring blood transfusion [56] . A similar incidence of rectal bleeding requiring transfusion was noted in a study by Landi et al.; however, there were no complications of sepsis or fistulas [60] .

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Questions have been raised regarding the completeness of endometriosis excision when using the discoid resection technique. Remorgida et al. demonstrated positive margins with residual disease in 43.8% of patients undergoing discoid resection [61] . The impact of these findings is unclear and it is unknown whether risk of recurrence and reoperation rate is higher in the presence of residual disease. In cases of segmental resection, positive disease margins have been recorded in up to 20% of cases [62] . Furthermore, no significant difference was noted in terms of disease recurrence or pain symptoms when comparing patients with and without positive margins [63] . Radical excision There has been much debate regarding the treatment of bowel endometriosis, with two main approaches. On the one hand, there is a symptom-guided approach with emphasis on conservative techniques notably shaving or disc excision. On the other hand, there is a more radical approach advocating segmental resection in a bid to resect the disease in its entirety. In our practice, segmental resection is reserved for symptomatic patients following careful evaluation of the endometriotic lesion, in whom a less-invasive procedure would be considered inadequate. This is particularly evident in cases of large nodules with critical bowel stenosis, where shaving is considered subtherapeutic. In some instances radical excision is unavoidable, specifically in cases where the nodule is greater than 3 cm, where there is sigmoid involvement, more than 50% circumferential disease or concurrent bowel stenosis, and in multicentric disease [17,47] . Studies have demonstrated that complete excision of bowel lesions, including segmental resection, are associated with significant improvement in pain symptoms and subsequent quality of life [64,65] . Surgical excision of bowel and rectovaginal endometriosis can be associated with major complications such as bowel perforation and peritonitis. Segmental bowel resection may be indicated where endometriosis is found to be infiltrating both serosal and mucosal layers. In these instances we advocate segmental bowel resection to be as economic as possible. The bowel is dissected at the edge of the mesentery respecting all the vascular branches. Once the diseased segment has been adequately dissected, the bowel is divided caudal to the lesion using a linear stapler device. An endoscopic linear stapler is used to resect the bowel above the nodule. A mini-laparotomy incision can be used to resect the rectum and place the anvil in the proximal bowel; alternatively, a transvaginal or transanal approach can be used [47] . A circular stapler is inserted through the caudal portion of the rectum and an end-to-end anastomosis performed (Figure 2) [66] .

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Figure 2. Technique for laparoscopic sigmoid resection. (A & B) Anvil of circular endoscopic stapler with detachable end. (C) The proximal bowel is opened using a vessel sealing device and the anvil introduced. (D) Laparoscopic view of transrectal position of of anvil of a circular endoscopic stapler. (E) Connection of the circular endoscopic anvils. (F) Circular end-to-end anastomosis is visible. (G) Two complete circular doughnuts should be identified to ensure adequate anastomosis.

Unlike radical surgery used for the treatment of cancer in colorectal surgery, safety margins are not necessary for adequate treatment of endometriosis. This more conservative approach to segmental bowel resection allows preservation of vasculature, lymphatics and nerve supply; thereby minimizing functional complications. Recent evidence has demonstrated that laparoscopic excision of deeply infiltrating pelvic endometriosis within a multidisciplinary set-up in a tertiary referral center appears to be safe, with a low rate of significant short-term complications. Pandis et al. performed a study of 177 women with rectovaginal endometriosis, demonstrating an overall complication rate of 10.2%; after excluding women with uncomplicated pyrexia the rate decreased to 3.2% [67] . No ureteric, unintentional bowel or vessel injury occurred [67] . In a large retrospective study of 750 patients undergoing laparoscopic resection of the mid-to-low rectum for bowel endometriosis the rate of complications were low. Rate of anastomotic fistula, rectovaginal fistula and intra-

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abdominal bleeding was 3, 2 and 1.2%, respectively [68] . A retrospective study of 568 patients conducted by Kondo et al. confirmed an intraoperative complication rate of 8% in cases of excision of rectovaginal nodules associated with bowel resection and anastomosis [45] . This was considerably higher when compared with excision of uterosacral ligaments (0.8%) and rectovaginal nodules (1%). The postoperative complication rate in those patients undergoing segmental resection was 24% [45] . This was significantly higher then the cases of rectal shaving observed to be 6.7%. Postoperative rectovaginal fistulas occurred in nine women; three occurred following colorectal resection and anastomosis, a further three following excision of a rectal nodule and the final three after rectal shaving [45] . In all but one of these cases of fistula, both the rectum and the vagina were opened during the procedure, suggesting this to be a risk factor. Adopting a more conservative approach may, therefore, avoid the risk of fistula formation. Alternatively, in cases of deep involvement of the bowel wall, a second step

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procedure for colorectal resection may be considered at a later date. In cases where two suture lines are unavoidable rectovaginal fistulas may be avoided by transposing omentum between the two anastomoses [69] . The omentoplasty serves as a physical barrier and may improve vascularization and subsequent healing, perhaps serving as a preventative measure against anastomotic leakage. In a recent meta-analysis, however, there were insufficient data to confirm whether omentoplasty reduced the rate of anastomotic leakage following colorectal surgery [70] . A recent systematic review of outcomes associated with different surgical treatment of bowel endometriosis described an overall complication rate of 13.9% [71] . This varied from 2.8% in the shaving group to 29.6% in the resection group [71] . Conservative surgery (i.e., shaving) may carry a lower risk of major complications, although in some studies additional surgery such as ureterolysis, uterosacral ligament resection and hysterectomy may have had an impact [71] . Despite a significant improvement in pelvic pain following segmental bowel resection for endometriosis, postoperative digestive symptoms may persist or de novo symptoms may develop. In a study by Roman et al., functional digestive complications, namely constipation, were found to occur more frequently following colorectal resection [72] . During segmental resection the mesocolon is dissected free from the bowel and despite attempts to preserve nerve supply pelvic denervation can still occur. Adopting a nerve-sparing resection technique has been shown to minimize the occurrence of abnormal bowel movements [73] . Care should be taken to preserve pelvic autonomic nerve function and maintain rectal, bladder and sexual function. The shaving technique may avoid deep lateral dissection allowing preservation of nerve function; however, bowel endometriosis often coexists with disease of the rectovaginal septum and uterosacral ligaments. Radical resection of disease in these areas can impair functionality and in a retrospective cohort of laparoscopic surgery for treatment of severe endometriosis urinary retention occurred in 4.6% of patients [48] .

postoperative complications, and have led to optimization of patient care. A recent review of data involving bowel resection in endometriosis was attempted. Unfortunately the data were insufficiently detailed to draw any clear conclusions, mainly as indications and outcomes according to localization and size of endometriotic lesions were not consistently documented [74] . Further research into the different surgical approaches for management of rectovaginal endometriosis is needed to determine whether complete resection with disease-free margins is necessary.

Conclusion The main shortcomings of surgical treatment of endometriosis include the lack of prospective randomized controlled trials, which compare different forms of surgical treatment (particularly in those patients with severe stage 4 disease). In addition, few long-term follow-up studies exist, thus making it difficult to draw clear conclusions. Advances in laparoscopic surgery and management of severe endometriosis by multidisciplinary tertiary centers have resulted in fewer

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Future perspective Rectal vaginal endometriosis remains a complex disease whose treatment has been debated between experts in the field. The approach adopted by Redwine and Wright in 2001, that successful surgery was dependent on aggressive excision of all disease in the majority of patients, has been superseded by a more individualized, patient-centered approach [75] . Radical excision to remove all macroscopic appearance of disease does not always translate into disease-free margins and can be associated with significant morbidity. Endometriosis is not a cancer and as such should not be treated as one. Maintaining a balance between high success rates of treatment, minimal risk of recurrence and low complication rate may necessitate the need for a more conservative surgical approach. Efficacy of surgical treatment should therefore be measured in terms of overall rate of improvement of symptoms. Future improvements in imaging modalities and their interpretation in the context of endometriosis may help in fine-tuning preoperative assessment and surgical planning. This would aid not only the surgeon, but also provide more accurate information for the patient with regard to the length, type of surgery, subsequent recovery and risk of complications. Finally, laparoscopic surgery is continuously evolving, and as gynecologists we too must evolve. Perhaps by assuming more the role of a pelvic surgeon with adequate transversal competencies of both the bowel and ureter, patients’ needs may be more appropriately addressed by a single surgeon.

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties. No writing assistance was utilized in the production of this manuscript.

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Executive summary Laparoscopy: diagnosis & treatment • Laparoscopy is the gold standard for the diagnosis and treatment of endometriosis. • There is a poor correlation between disease severity diagnosed at laparoscopy and symptoms. • The most effective laparoscopic surgical technique for the treatment of peritoneal disease has yet to be determined.

Laparoscopic management of endometriosis related to infertility • Laparoscopic treatment of mild endometriosis, whether by means of ablation or excision, significantly improves fertility. • Excisional treatment of endometriomas is associated with reduced rate of recurrence and increased spontaneous pregnancy rate compared with ablative techniques. • During excisional treatment of endometriomas care should be taken to avoid inadvertent damage to the underlying ovarian parenchyma. • Significant reduction in anti-Müllerian hormone has been documented following surgical treatment of endometriotic cysts. • There is, however, no significant difference in pregnancy rates for patients undergoing IVF whether they underwent surgical or conservative management of their endometriomas.

Urinary tract endometriosis • Ureteral endometriosis can be classified into intrinsic and extrinsic disease, with extrinsic accounting for 85% of cases. • Surgical treatment options for ureteric endometriosis include: ureterolysis, ureteral resection with end-to-end anastomosis or ureteroneocystotomy.

Surgical strategies in bowel endometriosis • Different surgical techniques exist for the management of bowel endometriosis; however, there is no consensus on the most effective method. • A more radical surgical approach for treatment of bowel endometriosis may be adopted if the nodule is large, involves the sigmoid and is associated with significant bowel stenosis. • In segmental bowel resection for the treatment of endometriosis, there are no safety margins; the bowel is dissected at the edge of the mesentery conserving vasculature and nerve supply. • Endometriosis is a benign condition and treatment should be individualized according to the woman’s needs and objectives. • The final decision on the extent of excisional surgery required is for the most part made intra-operatively. Patients recognized as having deep infiltrating endometriosis should therefore be operated on by an experienced surgeon in an appropriate specialized center.

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Endometriosis is a chronic, multifactorial disease, which can impact significantly on a women's quality of life. It is associated with pelvic pain, dy...
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