Doron Kopelman, MD; Edited by Louise P. King MD, JD, Camran Nezhat MD
Endometriosis is a progressive medical condition in women in which endometrial glands and stroma are found outside the uterine cavity. These endometrial cells are influenced by hormonal changes. Symptoms of endometriosis often present cyclically or worsen with the menstrual cycle. Clinical manifestations of endometriosis include: pelvic pain, infertility and pelvic mass. Treatment is aimed at symptomatic relief and prevention of organ damage in severe cases.1
Endometriosis predominantly affects the pelvic organs. When found outside the pelvis, it is termed extragenital endometriosis and preferentially affects the intestinal tract.2 Diagnosis, treatment and long term management of bowel endometriosis is a difficult clinical challenge. A surgical approach, when clinically indicated, must be individualized, taking into account the severity of symtoms, extent and location of disease, age and desire for future fertility. This chapter will describe strategies for successful treatment of bowel endometriosis.
The true prevalence of endometriosis in the general population is not known. However, estimates range from 1-7% of reproductive age women undergoing surgery for tubal sterilization or for a gynecologic condition other than pain.3-6 In women of reproductive age undergoing surgery for pelvic pain or infertility, estimates range from 4-82% and 9-50% respectively.1, 3-5, 7 The age at time of diagnosis is usually between 25 and 29 years old. Diagnosis is frequently delayed in those who present solely for fertility as opposed to pain. A familial tendency has been identified.1, 7
The reported incidence of bowel endometriosis varies from 3-34% of women with pelvic endometriosis; the wide range results from differences in case selection between studies.7-13 A strong association with pelvic endometriosis exists; however, reports of bowel endometriosis independent from pelvic disease exist.8 Endometriosis may affect any portion of the gastrointestinal tract and can present with multiple sites of involvement in either a single lesion with small satellite lesions surrounding or as isolated nodules.12 True multifocal involvement has been observed in 15-35% of cases.8
The most frequent site of bowel involvement with endometriosis is the rectum including the rectosigmoid segment, accounting for 70-88% of cases, followed by the sigmoid colon, rectum, ileum, appendix and cecum.14-17 The small intestine is less frequently involved.18, 19 A review of cases presenting to the Mayo Clinic over 20 years found small intestinal endometriosis in 0.53% of 7200 cases.17, 20 Case reports of gastric endometriosis and transverse colonic disease have also been reported.13, 21-23 The incidence of appendeceal endometriosis has been estimated to be 0.054% of the general population according to autopsy studies.16 Almost 50% of appendices removed in one case series of patients with proven pelvic endometriosis had were involved in disease.24 Involvement of the bowel and rectovaginal septum usually occurs in conjunction with deep infiltrating endometriosis (DIE). This severe form of disease almost invariably involves the uterosacral ligaments and may also affect the ureters and bladder.
Endometriosis of the bowel varies in extent of involvement from microscopic foci of disease to large space-occupying lesions. These larger lesions can invade the bowel wall resulting in significant narrowing of its lumen although such extensive disease is fortunately rare. Endometriosis of the bowel typically involves the serosa and muscularis propria, rarely involving the submucosa or mucosa. Endometrial implants are usually found in the antimesenteric edge of the bowel.12 Less extensive disease appears macroscopically as pigmented nodules on the peritoneum. Microscopically, endometrial gland and stroma are seen to invade the bowel wall from the serosa inwards.12 When larger lesions invade the muscularis, endometriotic nodules become surrounded by smooth muscle hyperplasia and fibrosis which may produce mural thickening and stenosis.12, 25, 26 The enteric nervous system, including Auerbach’s plexus, Meisner’s Plexus and the interstitial cells of Cajal can all be damaged if in proximity to endometriotic nodules causing symptoms including pain discussed more fully below.27
Endometriosis has been described as a great masquerader.28 Symptoms can be generalized and lesions, especially if firm and obstructive, can be mistaken intra-operatively for gastrointestinal carcinoma. The differential diagnosis is wide and includes: inflammatory diseases (such as Crohn’s); diverticulitis; radiation colitis; ischemic colitis and stricture; malignancies of the gastrointestinal tract (including metastatic tumor felt on rectal examination or Blumer’s shelf); and other gynecologic pathologies including pelvic inflammatory disease.25 The existence of intestinal endometriosis may be suggested by anamnesis, physical exam or imaging studies; nevertheless, laparoscopy remains the gold standard of diagnosis.
The extent of bowel involvement by endometriosis varies widely; consequently, a wide range of presenting symptoms exists.12, 29, 30 Disease limited to the bowel serosa may be asymptomatic.12 The most commonly reported symptoms are catamenial and include pelvic pain, dyspareunia and low back pain. These symptoms are non-specific and do not necessarily indicate bowel involvement.14, 15, 31-33 Unfortunately, therefore, bowel endometriosis may be an unexpected finding or may simply be overlooked at surgery if the possibility of bowel endometriosis was not fully entertained during pre-operative planning.
Symptomatology more specific to bowel endometriosis includes: painful defecation and/or tenesmus; cyclic hematochezia; a change in bowel habits (diarrhea, constipation, hyperperistalsis, flatulence); and rectal bleeding.25, 34 Rectal pain and painful defecation are generally more prevalent when the rectum is involved with disease. Certainly, when such symptoms are present, pre-operative imaging and consultation with a surgeon or team experienced in the treatment of extensive endometriosis should be considered.
Physical findings associated with bowel endometriosis are variable and will depend upon the specific location and size of the implants. The most common finding is nodularity and localized tenderness in the cul-de-sac and along the uterosacral ligament. Adherence of the rectal wall to the cul-de-sac is possible and often more prominent on bi-digital examination.14, 15 A recent study has suggested that transvaginal ultrasound is more useful in detecting rectosigmoid endometriosis than vaginal examination; however this study did not employ a bi-digital examination.35
Endometriosis rarely involves the mucosa of the bowel, thus direct endoscopic visualization of colorectal endometriosis is uncommon.28, 36 The main utility of colonoscopy is to rule out alternative sources of pathology such as colorectal cancer or inflammatory bowel disease.37-39 Nevertheless, a finding at endoscopy of extrinsic compression or a fixed area of narrow lumen suggests involvement of the rectum or colon by endometriosis. In addition, secondary changes may be seen in the mucosa and include: edema; flattening or puckering of the mucosa; and loss mucosal mobility from the underlying muscularis. These findings are subtle and easily overlooked. We do not routinely request colonoscopy in the evaluation of our patients when we suspect bowel endometriosis.
Most imaging modalities have proven to be of limited value in the diagnosis and preoperative evaluation of intestinal endometriosis. Because they lack adequate resolution to detect smaller superficial implants or adhesions, preoperative imaging studies will, by definition, be primarily useful in the case of larger lesions with mass effect. Nevertheless, preoperative diagnosis of significant bowel involvement allows for planning and consultation with a surgeon or team competent to fully treat disease and is recommended.40 Research is ongoing to identify the best imaging modality available or develop new approaches. Currently, the most useful imaging techniques are transvaginal sonography (TVUS), transrectal sonography (TRUS), double contrast barium enema (DCBE) and magnetic resonance imaging (MRI).
TVUS and TRUS can be useful tools in the evaluation of suspected rectal endometriosis. Bowel endometriosis will appear on sonography as an irregular hypoechoic mass, with or without hypoechoic or hyperechoic foci, penetrating into the intestinal wall.12, 41 The hypoechoic lesion corresponds to a layer of hypertrophic muscularis propria and may be surrounded by a hyperechoic rim corresponding to the mucosa and submucosa.
A recent meta-analysis found that TVUS alone is 91% sensitive and 98% specific for the detection of deep infiltrating endometriosis of the rectosigmoid.42 Limitations of TVUS include an inability to determine the exact distance of rectal lesions from the anal margin or to determine the precise depth of rectal wall involvement.12 Lesions above the rectosigmoid junction are beyond the field of view. Advances continue to be made and studies have shown the utility of bowel preparation, water-contrast medium and 3-D imaging in TVUS when used to evaluate bowel endometriosis; however, further randomized trials are required.43-46
TRUS has the potential to evaluate the extent of involvement of the muscularis propria of the bowel, the largest diameter of smaller lesions within view, the distance of a lesion from the anus and the infiltration of adjacent pelvic organs.12, 41, 47, 48 Sensitivity and specificity for detection of intestinal lesions is similar to that of TVUS ranging in different studies from 88-96% and 80-100% respectively.43, 49, 50 However, as with TVUS, examination of the upper part of the colon is not possible. The technique is not as widely used and the quality and predictive value of the images is dependent on the experience of the sonographer.12
TVUS is cost-effective, familiar and does not require anesthesia. It should be considered as a first line modality for any patient suspected of endometriosis.51 If bowel involvement is suspected, the requesting physician should take care to inform the radiologist of the particular concern and thus direct imaging accordingly.
Characteristics but non-specific findings suggestive of bowel involvement on DCBE include extrinsic mass effect with fine mucosal crenulations or a serrated wavy outline of the colonic mucosa.12, 39, 52 Annular structures or polypoid masses may be seen in advanced cases. Major limitations exist not the least of which is an inability to evaluate the depth of infiltration of the lesion in the bowel wall. Additionally, DCBE suffers from low specificity in that it is difficult to distinguish bowel endometriosis from other pathologies with similar findings.39 A recent limited study of 65 patients found that DCBE was superior to unenhanced MRI in detection of bowel endometriosis; however, there was no comparison made to TVUS or TRUS.53
MRI of deeply infiltrating intestinal endometriosis affecting the rectosigmoid can be challenging. The anatomical area in question is relatively small and includes several thin fibromuscular anatomic structures such as the uterosacral ligaments, as well as the vaginal and rectal walls. The endometriotic lesions are themselves fibromuscular structures and thus have similar MRI signal intensity to the anatomy surrounding them.54 Various methods can be used to aid in delineation of lesions on MRI including an endoluminal coil positioned in the rectum or insertion of vaginal and rectal contrast medium.12, 55 Studies have shown MRI to be inferior to DCBE, TVUS and TRUS in evaluation of intestinal endometriosis, although all studies to date have been underpowered to truly assess the gold standard of imaging in this area.50, 53, 56
Multislice Computed Tomography Enteroclysis (MSCTe)
Newer imaging techniques are being explored including the use of multislice computed tomography (CT) combined with colon distension by water enteroclysis in determining the presence and depth of bowel endometriotic lesions. A prospective trial involving 98 women established a sensitivity of 98.7% and a specificity of 100% for this method in identifying women with bowel endometriosis.57 Subsequently, MSCTe was found to have similar accuracy in the diagnosis of rectosigmoid endometriosis when compared to rectal water contrast TVUS.58 MSCTe may be effective in determining the presence and depth of bowel endometriotic lesions; however, further study is warranted.
Endometriosis is likely to be a progressive disease. To date, however, the natural history of endometriosis and specifically bowel endometriosis is not fully understood. Expectant management may be an option for patients with superficial lesions in the absence of subocclusive symtoms.12 Yet, patients desiring expectant management should be carefully counseled about the possibility of larger lesions and organ damage in the future. Bowel obstruction and emergent presentation secondary to endometriosis is a rare event but has been reported.19, 59-62
Surgery Video 1
There is little support in the current literature for medical treatment of bowel endometriosis. When disease is advanced and presumably associated with fibrosis it is unlikely to respond to hormonal manipulation.12 Single case reports have been published of successful treatment using gonadotropin-releasing hormone agonists; however, further study is required.63, 64 Two recent pilot studies demonstrate a reduction in pain and gastrointestinal symptoms when patients are treated with either norethisterone acetate alone as well as in combination with letrozole in patients with colorectal endometriosis.65, 66 Further study of medical management of bowel endometriosis is warranted.
Surgical management of bowel endometriosis remains controversial.12 In the absence of bowel obstruction or other emergent presentation, the optimal timing of surgery and extent of intervention has not been determined. Recently, a group attempted to perform a meta-analysis of existing data concerning bowel resection for deep endometriosis.67 However, after a systematic review the group found that the indication to perform segmental resection was poorly documented in existing literature and the available data did not permit an analysis of indication and outcome according to the location or size of the lesions in questions. Nevertheless, the authors were able to determine that complication rate for bowel resection in cases of endometriosis is comparable to that for other indications.
Given comparable complication rates, in severely symptomatic patients with presumed fibrotic lesions of the bowel not amenable to hormonal manipulation, it seems clear that surgical removal is the best therapeutic alternative. Thus, indications for surgical intervention in cases of suspected bowel endometriosis should include severe, incapacitating symptoms not responsive to medical therapy or the presence of advanced disease indicated by anatomic distortion of pelvic organs or partial bowel obstruction.
When preparing for a surgery to evaluate potential endometriosis, the patient should be consented not only for a diagnostic procedure but also for synchronous ablation or excision of endometriotic implants and adhesions. Consent for treatment of intestinal endometriosis must include a full discussion of potential complications including the possibility of protective colostomy. However, the benefits of full surgical treatment of intestinal endometriosis should not be downplayed as multiple studies have shown a significant improvement in gastrointestinal symptoms and quality of life. 27, 48, 68
Open versus Minimally Invasive Techniques
Laparoscopy is the procedure of choice for the diagnosis and treatment of endometriosis including disease affecting the bowel. A recent randomized trial of laparoscopically assisted versus open colorectal resection for endometriosis found that laparoscopy was equally safe and offered a higher pregnancy rate with similar improvements in symptomotology and quality of life.69
Operative videolaparoscopy using high resolution techniques was first introduced by Nezhat in the late 1970s and early to mid-1980s70, 71 and offers several important benefits over open techniques. First and foremost, videolaparoscopy offers excellent visualization of pelvic and abdominal anatomy, far superior to that achieved with open procedures. Relevant anatomy is magnified by the video camera and laparoscope which facilitates not only full recognition of all evident pathology but also adequate treatment by microsurgical techniques when indicated. The pressure created by the pneumoperitoneum decreases bleeding and provides a clean operating field, further enhancing visualization. In addition, laparoscopic surgery results in fewer adhesions, fewer intra-operative and fewer post-operative complications than conventional open procedures.72
Accurate diagnosis is dependant not only upon visualization of lesions but also upon the experience of the surgeon in identification and treatment of endometriosis. Histological confirmation is advisable in all cases.73 Peritoneal endometriosis has a wide range of appearance on laparoscopy including raised erythematous patches, whitish opacifications, yellow-brown discoloration, translucent blebs, or reddish or reddish-blue irregularly shaped lesions. The peritoneal surface may be scarred, puckered or a window may be apparent. Similar lesions can be found on the serosal surface of the bowel. When disease is more advanced, firm infiltrating intestinal wall lesions can easily be mistaken for gastrointestinal carcinoma. When concern for malignancy exists, histopathological frozen section should be requested.
Role of Staging
The revised American Fertility staging system (rAFS) only indirectly considers intestinal endometriosis and thus is of limited clinical value. A new scoring system called ENZIAN was introduced in 2005 as a supplement to better classify deep infiltrating endometriosis.74 A recent study evaluated the use of ENZIAN as a supplement to rAFS and found it duplicative at times. The authors suggested simplifying the scoring system to encourage ease of use and reproducibility.75 Further investigation is needed to elucidate a useful and reproducible scoring system in deeply infiltrating and intestinal endometriosis.
Laparoscopic Colorectal Surgery
Laparoscopically assited colon resection was performed successfully by Nezhat as early as 1988.76-82 However, laparoscopic colectomy has not been adopted into general practice as readily as other minimally invasive procedures. Adoption was hindered by concerns for oncological outcomes, a lack of randomized controlled trials and initial reports of port-site recurrence after curative resection. In addition, a long learning curve exists given the relative complexity of the procedure. Laparoscopic colectomy requires operating in more than one abdominal quadrant, difficult mobilization and exposure because of the length of resected segments, the ligation of major vascular pedicles and the creation of a safe anastomosis.83, 84
Despite these hurdles, laparoscopic techniques are increasingly being adopted for treatment of a wide range of pathologies of the bowel including inflammatory disease, diverticular disease and endometriosis.80, 81, 85-90 A multi-institutional study reported in 2004 sought to address the major concerns surrounding adoption of laparoscopically assisted colon resection in the context of malignancy. In that study, the rates of recurrent cancer were similar after laparoscopically assisted colectomy and open colectomy, suggesting that the laparoscopic approach is an acceptable alternative to open surgery for colon cancer.83
Specific Techniques in Laparoscopic Management of Intestinal Endometriosis
Surgical treatment of intestinal endometriosis often requires the expertise of both gynecologists and general or colorectal surgeons. Cooperation and a multi-disciplinary approach are advised. The first reported laparoscopic colon resection for endometriosis was performed in 1989;76 since that time minimally invasive techniques to treat intestinal endometriosis have been increasingly utilized with favorable results.77, 80, 81, 91-97
Multiple minimally invasive surgical approaches and techniques are available for treatment of intestinal endometriosis. This is especially true with regard to treatment of disease affecting the rectum which is most commonly involved with endometriosis. Selection of the surgical approach and extent of needed excision will depend in part on the experience and skill of the surgical team. As a general rule, less invasive is better when treating rectal endometriosis assuming the lesion can be completely excised with adequate margins using shaving or disk excision techniques.98 Avoiding the morbidity of anterior rectal resection and preservation of normal rectal function can have significant benefits in terms of quality of life for young patients afflicted by this disease.
Use of the CO2 laser for treatment of deep rectosigmoid colon and rectovaginal septum endometriosis was reported as early as 1992 by Nezhat.91 A randomized trial of CO2 laser laparoscopic treatment of minimal, mild and moderate endometriosis, although not specific to intestinal endometriosis, established this modality as a safe, simple and effective treatment.99 A subsequent retrospective study of CO2 laser laparoscopic excision of deep endometriosis with colorectal extension demonstrated a reduction in pain while improving quality of life.100 Post operative complications and recurrence rates were relatively low. The cumulative pregnancy rate was 31 and 70% at 1 and 4 years after surgery respectively. Techniques such as hydrodissection and new technology including a super pulsed laser allow for removal of adherent endometriotic implants without damage to underlying normal tissue. Unfortunately, few gynecologists or general surgeons are trained in the use of CO2 laser despite its obvious benefits in the treatment of endometriosis. Diathermy excision should be used with caution as thermal damage to the bowel may result in a delayed postoperative fistula or other complication.12
Superficial rectovaginal endometriosis can be shaved off the rectal wall while leaving the mucosa intact.91 The most distal peritoneal attachments of the rectum on both the anterior and lateral aspects are incised to enable access to the extraperitoneal rectovaginal septum. The endometrial implant is then dissected free from the anterior rectal wall and the posterior vaginal wall. The extraperitoneal rectal wall lacks the outer serosal lining and is comprised of mucosa, submucosa, muscularis propria and peri-rectal fat. If the dissection is maintained as superficial then bowel integrity will not be compromised. By contrast, if the dissection requires resection of a portion of the muscularis propria, the surgeon should reinforce any defect with laparoscopically placed sutures to diminish the risk of postoperative bowel perforation. Mechanical or thermal damage to the mucosa should be avoided. Visual inspection with proctoscopy after completion of the excision and an air leak test can ensure that no inadvertent proctotomy exists.101
Anterior Disk Excision (open)
Deeper lesions of the intestinal wall may require full thickness excision yet not require a full segmental resection. For example, an infiltrating lesion located in the anterior aspect of the rectum may be treated by local full thickness excision.80, 102 The excision can be performed with the aid of electrocautery or CO2 laser after adequate laparoscopic mobilization of the rectum. The bowel is then repaired by laparoscopic suturing or with the aid of an endo linear stapling device.103 The repair should be made in the transverse axial plane so as to prevent narrowing and potential stricture of the bowel lumen.
Anterior Disk Excision (closed)
An alternative approach to disk excision allows for use of a circular stapler, introduced transanally, to remove a full thickness patch of the anterior rectal wall.104, 105 This procedure is appropriate for anterior rectal endometriosis that occupies less than one third of the circumference of the rectal wall and is less than 2 centimeters in diameter. After the rectum is adequately mobilized, the circular stapler is introduced and opened. The area to be excised is placed in the circular hollow chamber between the anvil and the main body of the stapler. Once excision is completed, the specimen should be inspected to confirm adequate margins of resection.
The main advantage of this technique is avoidance of an “open” bowel in the abdominal cavity. In theory, this would reduce the frequency of contamination and resulting postoperative infectious complications. In addition, use of the circular stapler in this fashion obviates the need for laparoscopic suturing of the anterior rectal wall which can be technically difficult. Nevertheless, further study is warranted to fully elucidate the benefits of this approach.
Differing Approaches to Laparoscopic Segmental Bowel Resection
There is more than one potentially successful strategy to perform laparoscopic resection of any gastrointestinal tract segment. The following descriptions reflect the accepted personal preference of the main author; however other approaches may be equally efficient and efficacious. As these procedures are clean-contaminated they require intravenous administration of prophylactic antibiotics thirty to sixty minutes before incision. The need for mechanical bowel preparation is controversial. Studies have shown that mechanical bowel preparation may actually increase the likelihood of spillage of bowel contents because of the large volume of liquid colonic contents that results from mechanical bowel preps.106 Meta-analysis has shown no advantage to bowel preparation and consequently we do not routinely use mechanical bowel preparation in our patients.107, 108 We do recommend a clear liquid diet the day before surgery. We also ask that patients perform up to three enemas the night before surgery to decompress the rectum and allow for better visualization of the posterior cul-de-sac.
The following paragraphs will address what are considered basic principles of the procedures in question. Different instruments and energy sources may be used at the preference of the surgeon taking into account availability and cost.
Distal Small Bowel, Ileo-Colic and Right Hemicolon Resection
Resection of endometriotic implants involving the distal ileum, cecum, or ascending colon will require mobilization of the small bowel mesentery as well as of the peritoneal attachments of the right colon. Primary anastomosis will consist of either ileo-ileostomy or ileo-colostomy. Tredenlenburg positioning, tilt to the left and cephalad medial traction of the cecum may facilitate mobilization of the small bowel away from the pelvis and the operative field. The ileal and right colon mesentery is mobilized from the retroperitoneum in a medial to lateral fashion using both blunt and sharp dissection. The surgeon should take care to avoid mechanical or thermal injury to the right gonadal vessels, the right ureter and kidney, as well as the second and third parts of the duodenum. The lateral attachements of the ascending colon and hepatic flexure can then be divided. Dissection of the high and long hepatic flexure may be made easier by early transaction of the right gastro-colic ligament from medial to lateral. The bowel is transected using linear endo staplers with subsequent construction of a side-to-side functional end-to-end stapled anastomosis. The bowel anastomosis may be constructed either intra or extracorporally. Because a small four to five centimeter incision must be made to extract the specimen, most surgeons prefer extracorporeal anastomosis.
Sigmoid Colon Resection
The sigmoid colon is the intestinal segment most commonly affected by endometriosis and thus most likely to require resection. Laparoscopically assisted resection of the involved segment with primary colorectal anastomosis is the procedure of choice. First, mobilization of the sigmoid mesentery is required. Steep trendelenburg positioning and right tilt may facilitate mobilization of small bowel loops exposing the pelvis and the operative field so as to expose the base and posterior attachments of the meso-sigmoid colon to the retroperitoneum. The medial aspect of the peritoneum covering the meso-sigmoid is then cut open from the sacral promontory up to the origin of the left colic artery. The superior rectal artery is divided proximal to the sigmoidal artery and secured using hemostatic clips, thermal energy device or vascular stapler. The surgeon should take care when mobilizing the sigmoid to avoid mechanical or thermal injury to the left ureter and left gonadal vessels. Leaving the lateral attachments of the sigmoid and descending colon intact can provide passive lateral traction so as to facilitate dissection. The descending colon should be mobilized up to and in most cases including the splenic flexure so as to achieve a tension free colorectal anastomosis. The mesorectum is divided at the desired level and the rectosigmoid junction is also transected using a laparoscopic linear stapling device through a 12 millimeter right lower quadrant port. If the patient is undergoing a simultaneous laparoscopic hysterectomy, the proximal transected bowel end may be delivered through the open vaginal cuff in a natural orifice procedure. The anvil of the circular stapling device is secured with a purse-string suture extracorporeally at the proximal open end of the bowel which is then retracted back intraperitoneally. A trans-anal circular stapling device is then used to perform anastomosis. The use of the vagina as a natural orifice avoids the need for the four to five centimeter incision described previously and required when hysterectomy is not indicated. Intact anastamosis should be confirmed using an “air leak test” and sigmoidoscopy. Any air leak should lead the surgeon to consider re-anastomosis or in selected cases may reinforce the anastomosis with laparoscopically placed sutures. The surgeon must ensure that both ends of the anastomosed bowel are adequately vascularized and that the anastomosis is under no tension so as to minimize the risk of anastomotic leak.
Anterior and Low Anterior Resection of the Rectum
The term “low” anterior resection usually refers to a procedure in which the pelvic peritoneum is opened, the lateral ligaments are ligated and divided and construction of a colorectal anastomosis occurs below the pelvic peritoneal reflection or even below the lateral ligaments. The operative principles at work are similar to those encountered in laparoscopic sigmoidectomy; however, rather than perform the anastomosis at the level of the promontory, the extraperitoneal rectum is mobilized far inferior so as to fully resect low endometriotic implants.
The fatty mesorectum encircles the rectum from the posterior and lateral aspects of the bowel. The arterial blood to the proximal third of the rectum is supplied by the superior rectal artery, a branch of the inferior mesenteric artery. The distal two thirds of the rectum derive their blood supply from the middle and inferior rectal arteries, branches of the internal iliac artery. Mobilization of the rectum distal to the levator ani is best done by dissecting the avascular planes around the rectum and mesorectum: posteriorly the pre-sacral fascia; laterally the fascia propria containing the mesorectum; and anteriorly the rectovaginal fascia of Denonvillier. Once sufficiently mobilized, the rectum is transected transversely with an articulating linear stapler device. Extraction and anastomosis is performed as described previously.
Endometriosis of the appendix can mimic or be the obstructive etiology of acute appendicitis resulting in the need for emergent surgery. Elective appendectomy is indicated when performing surgery for intestinal endometriosis as the appendix frequently may be involved by disease.24, 31, 109 Laparoscopic appendectomy is readily performed using three ports, a single port or even a natural orifice approach.24, 110, 111
Two recent meta-analyses have been attempted to analyze the clinical outcome of surgical treatment of deeply infiltrating endometriosis and specifically of bowel endometriosis.67, 112 Unfortunately in both instances, full meta-analysis was not possible as the indications to perform aggressive surgical resection were poorly documented in studies reported and the available data did not permit an analysis of the indication and outcome according to location and size of endometriotic implants. No such meta-analysis has been attempted to date concerning more conservative approaches to treatment including shaving. Overall, studies have reported favorable outcomes with both approaches;113-119 however, further study is warranted to truly determine the optimal timing and approach to treatment of bowel endometriosis. It has been our experience that opting for the least aggressive approach so as to achieve adequate margins of resection while preserving normal anatomy results in favorable outcomes with acceptable resulting morbidity and complication rates.
Recent advances in technology have introduced enabling devices such a robotic assisted laparoscopy which may broaden the availability and accessibility of laparoscopic procedures. Initial reports of robotic assistance in the treatment of endometriosis and specifically bowel endometriosis are promising.120-124 Robotic-assisted laparoscopic surgery provides several advantages in the management of women with severe endometriosis including 3-D visualization, a decrease in hand tremors, a decrease in surgeon fatigue and increased degrees of freedom in wrist movement with resultant improved dexterity and surgical precision. The disadvantages include high cost, added operative time and bulky equipment. Further experience is necessary to fully appreciate what benefits robotic assistance will afford to laparoscopic treatment of intestinal endometriosis.
Intestinal endometriosis occurs in a relatively small number of women but may be a significant source of pain and cause of infertility. A number of surgical techniques are available for treatment of endometriosis affecting the bowel. The optimal surgical method has not yet been determined; however, laparoscopy should be preferred over open techniques whenever feasible. A multi-disciplinary team is usually required; certainly, both a gynecologist and a general or colorectal surgeon with experience in endometriosis should be involved in cases of severe endometriosis affecting the bowel.
1. Eskenazi B, Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am. Jun 1997;24(2):235-258.
2. Veeraswamy A, Lewis M, Mann A, Kotikela S, Hajhosseini B, Nezhat C. Extragenital endometriosis. Clin Obstet Gynecol. Jun 2010;53(2):449-466.
3. Sangi-Haghpeykar H, Poindexter AN, 3rd. Epidemiology of endometriosis among parous women. Obstet Gynecol. Jun 1995;85(6):983-992.
4. Chatman DL, Ward AB. Endometriosis in adolescents. J Reprod Med. Mar 1982;27(3):156-160.
5. Missmer SA, Hankinson SE, Spiegelman D, Barbieri RL, Marshall LM, Hunter DJ. Incidence of laparoscopically confirmed endometriosis by demographic, anthropometric, and lifestyle factors. Am J Epidemiol. Oct 15 2004;160(8):784-796.
6. Ballard KD, Seaman HE, de Vries CS, Wright JT. Can symptomatology help in the diagnosis of endometriosis? Findings from a national case-control study--Part 1. BJOG. Oct 2008;115(11):1382-1391.
7. Wellbery C. Diagnosis and treatment of endometriosis. Am Fam Physician. Oct 15 1999;60(6):1753-1762, 1767-1758.
8. Redwine DB. Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril. Aug 1999;72(2):310-315.
9. Sakamoto K, Maeda T, Yamamoto T, et al. Simultaneous laparoscopic treatment for rectosigmoid and ileal endometriosis. J Laparoendosc Adv Surg Tech A. Jun 2006;16(3):251-255.
10. Kratzer GL, Salvati EP. Collective review of endometriosis of the colon. Am J Surg. Nov 1955;90(5):866-869.
11. Macafee CH, Greer HL. Intestinal endometriosis. A report of 29 cases and a survey of the literature. J Obstet Gynaecol Br Emp. Aug 1960;67:539-555.
12. Remorgida V, Ferrero S, Fulcheri E, Ragni N, Martin DC. Bowel endometriosis: presentation, diagnosis, and treatment. Obstet Gynecol Surv. Jul 2007;62(7):461-470.
13. Weed JC, Ray JE. Endometriosis of the bowel. Obstet Gynecol. May 1987;69(5):727-730.
14. Williams TJ, Pratt JH. Endometriosis in 1,000 consecutive celiotomies: incidence and management. Am J Obstet Gynecol. Oct 1 1977;129(3):245-250.
15. Bailey HR, Ott MT, Hartendorp P. Aggressive surgical management for advanced colorectal endometriosis. Dis Colon Rectum. Aug 1994;37(8):747-753.
16. Collins DC. A study of 50,000 specimens of the human vermiform appendix. Surg Gynecol Obstet. Oct 1955;101(4):437-445.
17. Jerby BL, Kessler H, Falcone T, Milsom JW. Laparoscopic management of colorectal endometriosis. Surg Endosc. Nov 1999;13(11):1125-1128.
18. Decker D, Konig J, Wardelmann E, et al. Terminal ileitis with sealed perforation--a rare complication of intestinal endometriosis: case report and short review of the literature. Arch Gynecol Obstet. May 2004;269(4):294-298.
19. De Ceglie A, Bilardi C, Blanchi S, et al. Acute small bowel obstruction caused by endometriosis: a case report and review of the literature. World J Gastroenterol. Jun 7 2008;14(21):3430-3434.
20. Martimbeau PW, Pratt JH, Gaffey TA. Small-bowel obstruction secondary to endometriosis. Mayo Clin Proc. May 1975;50(5):239-243.
21. Iaroshenko VI, Salokhina MB. [Endometriosis of the stomach]. Vestn Khir Im I I Grek. Aug 1979;123(8):82-83.
22. Collier HA, Gonzales LL, Bossert LJ. Cyclic ascites as a manifestation of endometriosis. Report of a case. Obstet Gynecol. May 1962;19:681-683.
23. Meyers WC, Kelvin FM, Jones RS. Diagnosis and surgical treatment of colonic endometriosis. Arch Surg. Feb 1979;114(2):169-175.
24. Berker B, Lashay N, Davarpanah R, Marziali M, Nezhat CH, Nezhat C. Laparoscopic appendectomy in patients with endometriosis. J Minim Invasive Gynecol. May-Jun 2005;12(3):206-209.
25. Yantiss RK, Clement PB, Young RH. Endometriosis of the intestinal tract: a study of 44 cases of a disease that may cause diverse challenges in clinical and pathologic evaluation. Am J Surg Pathol. Apr 2001;25(4):445-454.
26. Remorgida V, Ragni N, Ferrero S, Anserini P, Torelli P, Fulcheri E. How complete is full thickness disc resection of bowel endometriotic lesions? A prospective surgical and histological study. Hum Reprod. Aug 2005;20(8):2317-2320.
27. Remorgida V, Ragni N, Ferrero S, Anserini P, Torelli P, Fulcheri E. The involvement of the interstitial Cajal cells and the enteric nervous system in bowel endometriosis. Hum Reprod. Jan 2005;20(1):264-271.
28. Shah M, Tager D, Feller E. Intestinal endometriosis masquerading as common digestive disorders. Arch Intern Med. May 8 1995;155(9):977-980.
29. Ballard K, Lane H, Hudelist G, Banerjee S, Wright J. Can specific pain symptoms help in the diagnosis of endometriosis? A cohort study of women with chronic pelvic pain. Fertil Steril. Jun 2010;94(1):20-27.
30. Seaman HE, Ballard KD, Wright JT, de Vries CS. Endometriosis and its coexistence with irritable bowel syndrome and pelvic inflammatory disease: findings from a national case-control study--Part 2. BJOG. Oct 2008;115(11):1392-1396.
31. Gustofson RL, Kim N, Liu S, Stratton P. Endometriosis and the appendix: a case series and comprehensive review of the literature. Fertil Steril. Aug 2006;86(2):298-303.
32. Jatan AK, Solomon MJ, Young J, Cooper M, Pathma-Nathan N. Laparoscopic management of rectal endometriosis. Dis Colon Rectum. Feb 2006;49(2):169-174.
33. Maroun P, Cooper MJ, Reid GD, Keirse MJ. Relevance of gastrointestinal symptoms in endometriosis. Aust N Z J Obstet Gynaecol. Aug 2009;49(4):411-414.
34. Marcoux S, Maheux R, Berube S. Laparoscopic surgery in infertile women with minimal or mild endometriosis. Canadian Collaborative Group on Endometriosis. N Engl J Med. Jul 24 1997;337(4):217-222.
35. Hudelist G, Ballard K, English J, et al. Transvaginal sonography vs. clinical examination in the preoperative diagnosis of deep infiltrating endometriosis. Ultrasound Obstet Gynecol. Apr 2011;37(4):480-487.
36. Rowland R, Langman JM. Endometriosis of the large bowel: a report of 11 cases. Pathology. Oct 1989;21(4):259-265.
37. Lewis LA, Nezhat C. Laparoscopic treatment of bowel endometriosis. Surg Technol Int. 2007;16:137-141.
38. Farinon AM, Vadora E. Endometriosis of the colon and rectum: an indication for peroperative coloscopy. Endoscopy. May 1980;12(3):136-139.
39. Gordon RL, Evers K, Kressel HY, Laufer I, Herlinger H, Thompson JJ. Double-contrast enema in pelvic endometriosis. AJR Am J Roentgenol. Mar 1982;138(3):549-552.
40. Kaufman LC, Smyrk TC, Levy MJ, Enders FT, Oxentenko AS. Symptomatic Intestinal Endometriosis Requiring Surgical Resection: Clinical Presentation and Preoperative Diagnosis. Am J Gastroenterol. Apr 19 2011.
41. Bazot M, Darai E. Sonography and MR imaging for the assessment of deep pelvic endometriosis. J Minim Invasive Gynecol. Mar-Apr 2005;12(2):178-185; quiz 177, 186.
42. Hudelist G, English J, Thomas AE, Tinelli A, Singer CF, Keckstein J. Diagnostic accuracy of transvaginal ultrasound for non-invasive diagnosis of bowel endometriosis: systematic review and meta-analysis. Ultrasound Obstet Gynecol. Mar 2011;37(3):257-263.
43. Bergamini V, Ghezzi F, Scarperi S, Raffaelli R, Cromi A, Franchi M. Preoperative assessment of intestinal endometriosis: A comparison of transvaginal sonography with water-contrast in the rectum, transrectal sonography, and barium enema. Abdom Imaging. Dec 2010;35(6):732-736.
44. Goncalves MO, Podgaec S, Dias JA, Jr., Gonzalez M, Abrao MS. Transvaginal ultrasonography with bowel preparation is able to predict the number of lesions and rectosigmoid layers affected in cases of deep endometriosis, defining surgical strategy. Hum Reprod. Mar 2010;25(3):665-671.
45. Pascual MA, Guerriero S, Hereter L, et al. Diagnosis of endometriosis of the rectovaginal septum using introital three-dimensional ultrasonography. Fertil Steril. Dec 2010;94(7):2761-2765.
46. Morotti M, Ferrero S, Bogliolo S, Venturini PL, Remorgida V, Valenzano Menada M. Transvaginal ultrasonography with water-contrast in the rectum in the diagnosis of bowel endometriosis. Minerva Ginecol. Jun 2010;62(3):179-185.
47. Bazot M, Bornier C, Dubernard G, Roseau G, Cortez A, Darai E. Accuracy of magnetic resonance imaging and rectal endoscopic sonography for the prediction of location of deep pelvic endometriosis. Hum Reprod. May 2007;22(5):1457-1463.
48. Thomassin I, Bazot M, Detchev R, Barranger E, Cortez A, Darai E. Symptoms before and after surgical removal of colorectal endometriosis that are assessed by magnetic resonance imaging and rectal endoscopic sonography. Am J Obstet Gynecol. May 2004;190(5):1264-1271.
49. Ribeiro HS, Ribeiro PA, Rossini L, Rodrigues FC, Donadio N, Aoki T. Double-contrast barium enema and transrectal endoscopic ultrasonography in the diagnosis of intestinal deeply infiltrating endometriosis. J Minim Invasive Gynecol. May-Jun 2008;15(3):315-320.
50. Bazot M, Lafont C, Rouzier R, Roseau G, Thomassin-Naggara I, Darai E. Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril. Dec 2009;92(6):1825-1833.
51. Piketty M, Chopin N, Dousset B, et al. Preoperative work-up for patients with deeply infiltrating endometriosis: transvaginal ultrasonography must definitely be the first-line imaging examination. Hum Reprod. Mar 2009;24(3):602-607.
52. Landi S, Barbieri F, Fiaccavento A, et al. Preoperative double-contrast barium enema in patients with suspected intestinal endometriosis. J Am Assoc Gynecol Laparosc. May 2004;11(2):223-228.
53. Faccioli N, Foti G, Manfredi R, et al. Evaluation of colonic involvement in endometriosis: double-contrast barium enema vs. magnetic resonance imaging. Abdom Imaging. Aug 2010;35(4):414-421.
54. Loubeyre P, Petignat P, Jacob S, Egger JF, Dubuisson JB, Wenger JM. Anatomic distribution of posterior deeply infiltrating endometriosis on MRI after vaginal and rectal gel opacification. AJR Am J Roentgenol. Jun 2009;192(6):1625-1631.
55. Chassang M, Novellas S, Bloch-Marcotte C, et al. Utility of vaginal and rectal contrast medium in MRI for the detection of deep pelvic endometriosis. Eur Radiol. Apr 2010;20(4):1003-1010.
56. Chapron C, Vieira M, Chopin N, et al. Accuracy of rectal endoscopic ultrasonography and magnetic resonance imaging in the diagnosis of rectal involvement for patients presenting with deeply infiltrating endometriosis. Ultrasound Obstet Gynecol. Aug 2004;24(2):175-179.
57. Biscaldi E, Ferrero S, Fulcheri E, Ragni N, Remorgida V, Rollandi GA. Multislice CT enteroclysis in the diagnosis of bowel endometriosis. Eur Radiol. Jan 2007;17(1):211-219.
58. Ferrero S, Biscaldi E, Morotti M, et al. Multidetector computerized tomography enteroclysis vs. rectal water contrast transvaginal ultrasonography in determining the presence and extent of bowel endometriosis. Ultrasound Obstet Gynecol. May 2011;37(5):603-613.
59. Liang HH, Huang MT, Wei PL, et al. Endometriosis-induced appendiceal intussusception. Am J Surg. Jun 2009;197(6):e66-68.
60. Pramateftakis MG, Psomas S, Kanellos D, et al. Large bowel obstruction due to endometriosis. Tech Coloproctol. Nov 2010;14 Suppl 1:S87-89.
61. Pisanu A, Deplano D, Angioni S, Ambu R, Uccheddu A. Rectal perforation from endometriosis in pregnancy: case report and literature review. World J Gastroenterol. Feb 7 2010;16(5):648-651.
62. Chaabouni S, Makni SK, Kallel RI, et al. Unusual cause of intestinal obstruction: ileal endometriosis. Pathologica. Jun 2009;101(3):130-132.
63. Porpora MG, Pallante D, Ferro A, Crobu M, Cerenzia P, Panici PL. Intestinal endometriosis without evident pelvic foci treated with gonadotropin-releasing hormone agonist. Eur J Obstet Gynecol Reprod Biol. Apr 1 2006;125(2):265-266.
64. Markham SM, Welling DR, Larsen KS, Snell MJ. Endometriosis of the rectum treated with a long term GnRH agonist and surgery. N Y State J Med. Feb 1991;91(2):69-71.
65. Ferrero S, Camerini G, Ragni N, Venturini PL, Biscaldi E, Remorgida V. Norethisterone acetate in the treatment of colorectal endometriosis: a pilot study. Hum Reprod. Jan 2010;25(1):94-100.
66. Ferrero S, Camerini G, Ragni N, et al. Letrozole and norethisterone acetate in colorectal endometriosis. Eur J Obstet Gynecol Reprod Biol. Jun 2010;150(2):199-202.
67. De Cicco C, Corona R, Schonman R, Mailova K, Ussia A, Koninckx P. Bowel resection for deep endometriosis: a systematic review. BJOG. Feb 2011;118(3):285-291.
68. Ribeiro PA, Rodrigues FC, Kehdi IP, et al. Laparoscopic resection of intestinal endometriosis: a 5-year experience. J Minim Invasive Gynecol. Sep-Oct 2006;13(5):442-446.
69. Darai E, Dubernard G, Coutant C, Frey C, Rouzier R, Ballester M. Randomized trial of laparoscopically assisted versus open colorectal resection for endometriosis: morbidity, symptoms, quality of life, and fertility. Ann Surg. Jun 2010;251(6):1018-1023.
70. Nezhat C, Crowgey SR, Garrison CP. Surgical treatment of endometriosis via laser laparoscopy. Fertil Steril. Jun 1986;45(6):778-783.
71. Nezhat C, Crowgey SR, Garrison CP. Surgical treatment of endometriosis via laser laparoscopy and videolaseroscopy. Contrib Gynecol Obstet. 1987;16:303-312.
72. Nezhat C, Nezhat F. Operative laparoscopy (minimally invasive surgery): state of the art. J Gynecol Surg. Fall 1992;8(3):111-141.
73. Wykes CB, Clark TJ, Khan KS. Accuracy of laparoscopy in the diagnosis of endometriosis: a systematic quantitative review. BJOG. Nov 2004;111(11):1204-1212.
74. Tuttlies F, Keckstein J, Ulrich U, et al. [ENZIAN-score, a classification of deep infiltrating endometriosis]. Zentralbl Gynakol. Oct 2005;127(5):275-281.
75. Haas D, Chvatal R, Habelsberger A, Wurm P, Schimetta W, Oppelt P. Comparison of revised American Fertility Society and ENZIAN staging: a critical evaluation of classifications of endometriosis on the basis of our patient population. Fertil Steril. Apr 2011;95(5):1574-1578.
76. Nezhat C, Nezhat FR. Safe laser endoscopic excision or vaporization of peritoneal endometriosis. Fertil Steril. Jul 1989;52(1):149-151.
77. Nezhat F, Nezhat C, Pennington E. Laparoscopic proctectomy for infiltrating endometriosis of the rectum. Fertil Steril. May 1992;57(5):1129-1132.
78. Jacobs M, Verdeja JC, Goldstein HS. Minimally invasive colon resection (laparoscopic colectomy). Surg Laparosc Endosc. Sep 1991;1(3):144-150.
79. Wexner SD, Johansen OB. Laparoscopic bowel resection: advantages and limitations. Ann Med. Apr 1992;24(2):105-110.
80. Nezhat C, Pennington E, Nezhat F, Silfen SL. Laparoscopically assisted anterior rectal wall resection and reanastomosis for deeply infiltrating endometriosis. Surg Laparosc Endosc. Jun 1991;1(2):106-108.
81. Nezhat F, Nezhat C, Pennington E, Ambroze W, Jr. Laparoscopic segmental resection for infiltrating endometriosis of the rectosigmoid colon: a preliminary report. Surg Laparosc Endosc. Sep 1992;2(3):212-216.
82. Nezhat CN, F. Evaluation of safety of videolaparoscopic treatment of bowel endometriosis. Scientific Paper and Poster Sessions, 44th Annual Meeting of the American Fertility Society. October 8-13, 1988. Atlanta, Georgia.
83. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. May 13 2004;350(20):2050-2059.
84. Pappas TN, Jacobs DO. Laparoscopic resection for colon cancer--the end of the beginning? N Engl J Med. May 13 2004;350(20):2091-2092.
85. Milsom JW, Hammerhofer KA, Bohm B, Marcello P, Elson P, Fazio VW. Prospective, randomized trial comparing laparoscopic vs. conventional surgery for refractory ileocolic Crohn's disease. Dis Colon Rectum. Jan 2001;44(1):1-8; discussion 8-9.
86. Aleali M, Milsom JW. Laparoscopic surgery in Crohn's disease. Surg Clin North Am. Feb 2001;81(1):217-230, x.
87. Marcello PW, Milsom JW, Wong SK, et al. Laparoscopic restorative proctocolectomy: case-matched comparative study with open restorative proctocolectomy. Dis Colon Rectum. May 2000;43(5):604-608.
88. Alves A, Panis Y, Slim K, Heyd B, Kwiatkowski F, Mantion G. French multicentre prospective observational study of laparoscopic versus open colectomy for sigmoid diverticular disease. Br J Surg. Dec 2005;92(12):1520-1525.
89. Aly EH. Laparoscopic colorectal surgery: summary of the current evidence. Ann R Coll Surg Engl. Oct 2009;91(7):541-544.
90. Langebrekke A, Istre O, Busund B, Johannessen HO, Qvigstad E. Endoscopic treatment of deep infiltrating endometriosis (DIE) involving the bladder and rectosigmoid colon. Acta Obstet Gynecol Scand. 2006;85(6):712-715.
91. Nezhat C, Nezhat F, Pennington E. Laparoscopic treatment of infiltrative rectosigmoid colon and rectovaginal septum endometriosis by the technique of videolaparoscopy and the CO2 laser. Br J Obstet Gynaecol. Aug 1992;99(8):664-667.
92. Dubernard G, Piketty M, Rouzier R, Houry S, Bazot M, Darai E. Quality of life after laparoscopic colorectal resection for endometriosis. Hum Reprod. May 2006;21(5):1243-1247.
93. Ford J, English J, Miles WF, Giannopoulos T. A new technique for laparoscopic anterior resection for rectal endometriosis. JSLS. Jan-Mar 2005;9(1):73-77.
94. Darai E, Thomassin I, Barranger E, et al. Feasibility and clinical outcome of laparoscopic colorectal resection for endometriosis. Am J Obstet Gynecol. Feb 2005;192(2):394-400.
95. Darai E, Marpeau O, Thomassin I, Dubernard G, Barranger E, Bazot M. Fertility after laparoscopic colorectal resection for endometriosis: preliminary results. Fertil Steril. Oct 2005;84(4):945-950.
96. Campagnacci R, Perretta S, Guerrieri M, et al. Laparoscopic colorectal resection for endometriosis. Surg Endosc. May 2005;19(5):662-664.
97. Abrao MS, Sagae UE, Gonzales M, Podgaec S, Dias JA, Jr. Treatment of rectosigmoid endometriosis by laparoscopically assisted vaginal rectosigmoidectomy. Int J Gynaecol Obstet. Oct 2005;91(1):27-31.
98. Mohr C, Nezhat FR, Nezhat CH, Seidman DS, Nezhat CR. Fertility considerations in laparoscopic treatment of infiltrative bowel endometriosis. JSLS. Jan-Mar 2005;9(1):16-24.
99. Sutton CJ, Ewen SP, Whitelaw N, Haines P. Prospective, randomized, double-blind, controlled trial of laser laparoscopy in the treatment of pelvic pain associated with minimal, mild, and moderate endometriosis. Fertil Steril. Oct 1994;62(4):696-700.
100. Meuleman C, D'Hoore A, Van Cleynenbreugel B, Beks N, D'Hooghe T. Outcome after multidisciplinary CO2 laser laparoscopic excision of deep infiltrating colorectal endometriosis. Reprod Biomed Online. Feb 2009;18(2):282-289.
101. Nezhat C, de Fazio A, Nicholson T. Intraoperative sigmoidoscopy in gynecologic surgery. J Minim Invasive Gynecol. Sep-Oct 2005;12(5):391-395.
102. Nezhat C, Nezhat F, Pennington E, Nezhat CH, Ambroze W. Laparoscopic disk excision and primary repair of the anterior rectal wall for the treatment of full-thickness bowel endometriosis. Surg Endosc. Jun 1994;8(6):682-685.
103. Landi S, Pontrelli G, Surico D, et al. Laparoscopic disk resection for bowel endometriosis using a circular stapler and a new endoscopic method to control postoperative bleeding from the stapler line. J Am Coll Surg. Aug 2008;207(2):205-209.
104. Gordon SJ, Maher PJ, Woods R. Use of the CEEA stapler to avoid ultra-low segmental resection of a full-thickness rectal endometriotic nodule. J Am Assoc Gynecol Laparosc. May 2001;8(2):312-316.
105. Woods RJ, Heriot AG, Chen FC. Anterior rectal wall excision for endometriosis using the circular stapler. ANZ J Surg. Aug 2003;73(8):647-648.
106. Mahajna A, Krausz M, Rosin D, et al. Bowel preparation is associated with spillage of bowel contents in colorectal surgery. Dis Colon Rectum. Aug 2005;48(8):1626-1631.
107. Wille-Jorgensen P, Guenaga KF, Matos D, Castro AA. Pre-operative mechanical bowel cleansing or not? an updated meta-analysis. Colorectal Dis. Jul 2005;7(4):304-310.
108. Rovera F, Dionigi G, Boni L, et al. Mechanical bowel preparation for colorectal surgery. Surg Infect (Larchmt). 2006;7 Suppl 2:S61-63.
109. Pittaway DE. Appendectomy in the surgical treatment of endometriosis. Obstet Gynecol. Apr 1983;61(4):421-424.
110. Song JY, Yordan E, Rotman C. Incidental appendectomy during endoscopic surgery. JSLS. Jul-Sep 2009;13(3):376-383.
111. Nezhat C, Datta MS, Defazio A, Nezhat F. Natural orifice-assisted laparoscopic appendectomy. JSLS. Jan-Mar 2009;13(1):14-18.
112. Meuleman C, Tomassetti C, D'Hoore A, et al. Surgical treatment of deeply infiltrating endometriosis with colorectal involvement. Hum Reprod Update. May-Jun 2011;17(3):311-326.
113. Darai E, Ackerman G, Bazot M, Rouzier R, Dubernard G. Laparoscopic segmental colorectal resection for endometriosis: limits and complications. Surg Endosc. Sep 2007;21(9):1572-1577.
114. Fedele L, Bianchi S, Zanconato G, Bettoni G, Gotsch F. Long-term follow-up after conservative surgery for rectovaginal endometriosis. Am J Obstet Gynecol. Apr 2004;190(4):1020-1024.
115. Busacca M, Chiaffarino F, Candiani M, et al. Determinants of long-term clinically detected recurrence rates of deep, ovarian, and pelvic endometriosis. Am J Obstet Gynecol. Aug 2006;195(2):426-432.
116. Darai E, Bazot M, Rouzier R, Houry S, Dubernard G. Outcome of laparoscopic colorectal resection for endometriosis. Curr Opin Obstet Gynecol. Aug 2007;19(4):308-313.
117. Dubernard G, Rouzier R, David-Montefiore E, Bazot M, Darai 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. Mar-Apr 2008;15(2):235-240.
118. Donnez J, Squifflet J. Complications, pregnancy and recurrence in a prospective series of 500 patients operated on by the shaving technique for deep rectovaginal endometriotic nodules. Hum Reprod. Aug 2010;25(8):1949-1958.
119. Ballester M, Chereau E, Dubernard G, Coutant C, Bazot M, Darai E. Urinary dysfunction after colorectal resection for endometriosis: results of a prospective randomized trial comparing laparoscopy to open surgery. Am J Obstet Gynecol. Apr 2011;204(4):303 e301-306.
120. Ragupathi M, Ramos-Valadez DI, Patel CB, Haas EM. Robotic-assisted laparoscopic surgery for recurrent diverticulitis: experience in consecutive cases and a review of the literature. Surg Endosc. Jan 2011;25(1):199-206.
121. Nezhat C, Lewis M, Kotikela S, Veeraswamy A, Saadat L, Hajhosseini B. Robotic versus standard laparoscopy for the treatment of endometriosis. Fertil Steril. May 25 2010.
122. Zimmern A, Prasad L, Desouza A, Marecik S, Park J, Abcarian H. Robotic colon and rectal surgery: a series of 131 cases. World J Surg. Aug 2010;34(8):1954-1958.
123. Averbach M, Popoutchi P, Marques Jr OW, Abdalla RZ, Podgaec S, Abrao MS. Robotic rectosigmoidectomy - pioneer case report in Brazil. Current scene in colorectal robotic surgery. Arq Gastroenterol. Mar 2010;47(1):116-118.
124. Nezhat C, King LP. Robotic Assisted Laparoscopic Treatment of Bowel, Bladder and Ureter Endometriosis. JSLS; Accepted for publication. 2011.