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Diagnosis & Therapy

Modern surgical techniques for gastrointestinal endometriosis

 

Modern surgical techniques for gastrointestinal endometriosis

Current operative techniques for extragenital endometriosis can provide excellent outcomes with less risk for postoperative complications

BY Megan Kennedy Burns, MD, MA; Michelle A. Wood, DO; Ceana Nezhat, MD; Camran Nezhat, MD


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Perspectives on Endometriosis Management


Approximately 10% of all reproductive-aged women and 35% to 50% of women with pelvic pain and infertility are affected by endometriosis.1,2 The disease typically involves the reproductive tract organs, anterior and posterior cul-de-sacs, and uterosacral ligaments. However, disease outside of the reproductive tract occurs frequently and has been found on all organs except the spleen.3

The bowel is the most common site for extragenital endometriosis and is estimated to be affected in 3.8% to 37% of patients with known endometriosis.4-7

Figure 1. Diffuse serosal disease across the bowel.

Figure 2. Severe rectovaginal adhesions.

Implants may be superficial, involving the bowel serosa and subserosa (FIGURE 1), or they can manifest as deeply infiltrating lesions involving the muscularis and mucosa (FIGURE 2). The rectosigmoid colon is the most common location for bowel endometriosis, followed by the rectum, ileum, appendix, and cecum4,8 (FIGURES 3, 4, and 5). Case reports also have described endometrial implants on the stomach and transverse colon.9 Although isolated bowel involvement has been recognized, most patients with bowel endometriosis have concurrent disease elsewhere.2,4

Figure 3. Appendiceal endometriosis.

Figure 4. Severe rectosigmoid adhesions.

Figure 5. Ileocecal endometriosis.

Surgery for bowel endometriosis has been described since the early 1900s.10 Historically, segmental resection was performed regardless of the anatomical location of the lesion. Even today, many surgeons continue to routinely perform segmental bowel resection as a first-line surgical approach.11 Unnecessary segmental resection, however, places patients at risk for short- and long-term postoperative morbidity, including the possibility of permanent ostomy.

Modern surgical techniques, such as shaving excision and disc resection, have been performed to successfully treat bowel endometriosis with excellent long-term outcomes and fewer complications when compared with traditional segmental resection.2,12-16

 In this article we focus on the clinical indications and surgical techniques for laparoscopic management, but first describe the pathophysiology, clinical presentation, and diagnosis of bowel endometriosis.

Pathophysiology of bowel endometriosis

The pathogenesis of endometriosis remains unknown. Although several theories have been proposed, no single mechanism explains all clinical cases of the disease. The most popular theory describes retrograde menstruation through the fallopian tubes.17 Once inside the peritoneal cavity, endometrial cells attach to and invade healthy peritoneum, establishing a blood supply necessary for growth and survival.

In the case of bowel endometriosis, deposition of effluxed endometrial cells may lead to an inflammatory response that increases the risk of adhesion formation, leading to potential cul-de-sac obliteration. Lesions may originate as Allen-Masters peritoneal defects, developing into deeply infiltrative rectovaginal septum lesions. The anatomical shelter theory contributes to lesions within the pelvis, with the rectosigmoid colon blocking the cephalad flow of effluxed menstrual blood from the pelvis, thus leading to a preponderance of lesions in the pelvis and along the rectosigmoid colon.2

Clinical presentation and diagnosis of bowel endometriosis

Women presenting with endometriosis of the bowel are typically of reproductive age and commonly report symptoms of dysmenorrhea, chronic pelvic pain, dyspareunia, and dyschezia. Some women also experience catamenial diarrhea, constipation, hematochezia, and bloating.2  The differential diagnosis of these symptoms is broad and includes irritable bowel disease, ischemic colitis, inflammatory bowel disease, diverticulitis, pelvic inflammatory disease, and malignancy.

Because of its nonspecific symptoms, bowel endometriosis is often misdiagnosed and the disease goes untreated for years.18  Therefore, it is imperative that clinicians maintain a high index of suspicion when evaluating reproductive-aged women with gastrointestinal symptoms and pelvic pain.

Physical examination can be helpful in making the diagnosis of endometriosis. During bimanual examination, findings such as a fixed, tender, or retroverted uterus, uterosacral ligament nodularity, or an enlarged adnexal mass representing an ovarian endometrioma may be appreciated. Rectovaginal exam can identify areas of tenderness and nodularity along the rectovaginal septum. Speculum exam may reveal a laterally displaced cervix or blue powder-burn lesions along the cervix or posterior fornix.19 Rarely, endometriosis is found on the perineum within an episiotomy scar.20

Imaging studies can be used in conjunction with physical examination findings to aid in the diagnosis of endometriosis. Images also guide preoperative planning by characterizing lesions based on their size, location, and depth of invasion. Hudelist and colleagues found transvaginal ultrasound (TVUS) to have an overall sensitivity of 71% to 98% and a specificity of 92% to 100%.21 However, it was noted that the accuracy of the diagnosis was directly related to the experience of the sonographer, and lesions above the sigmoid colon were generally unable to be diagnosed. Other imaging modalities that have been reported to have high sensitivity and specificity for diagnosing bowel endometriosis include rectal water contrast TVUS,22,23 rectal endoscopic sonography,22 magnetic resonance imaging,22 and barium enema.24

Medical management

Medical therapy for patients with endometriosis is utilized with the goal of suppressing ovulation, lowering circulating hormone levels, and inducing endometrial atrophy. Medications commonly employed include gonadotropin-releasing hormone agonists and antagonists, anabolic steriods such as danazol, combined oral contraceptive pills, progestins, and aromatase inhibitors.

To date, no optimal hormonal regimen has been established for the treatment of bowel endometriosis.

Vercellini and colleagues demonstrated progestins with and without low-dose estrogen–improved symptoms of dysmenorrhea and dyspareunia.25 Ferrero et al reported that 2.5 mg of norethindrone daily resulted in 53% of participants with colorectal endometriosis reporting an improvement in gastrointestinal symptoms.26 However, it was noted that by 12 months of follow-up, 33% of these patients had elected to undergo surgical management.

Gonadotropin-releasing hormone agonists, such as leuprolide acetate, also can be used to mitigate symptoms of bowel endometriosis or to decrease disease burden at the time of surgery, and they can be used with add-back norethindrone acetate. The use of these medications is limited by adverse effects, such as vasomotor symptoms and decreased bone mineral density when used for greater than 6 months.2

Medical therapy is commonly employed for patients with mild to moderate symptoms and in those who are poor surgical candidates or decline surgical intervention.

Medical therapy is especially useful when employed postoperatively to suppress the regrowth of microscopic ectopic endometrial tissue.

However, patients must be counseled that even with medical management, they may still require surgery in the future to control their symptoms and/or to preserve organ function.2

Surgical management

Surgical treatment for bowel endometriosis depends on the location of the disease, size and depth of the lesion, presence or absence of stricture, and the level of expertise of the surgeon.2,12,27-30 In our group, we advocate for laparoscopy, with or without robotic assistance. Minimally invasive surgery offers the advantages of reduced blood loss, shorter recovery time, and fewer postoperative complications over laparotomy.2,16,27,31-33 The conversion rate to laparotomy has been reported to be about 3% when performed by an experienced surgeon.12 Darai and colleagues performed a randomized trial of 52 patients undergoing surgery for colorectal endometriosis via either laparoscopic or open colon resection.33 Blood loss was significantly lower in the laparoscopic group (1.6 vs 2.7 mg/L, P <.05). No difference in long-term outcomes was noted. In a retrospective study of 436 cases, Ruffo et al showed that those who underwent laparoscopic colorectal resection had higher postoperative pregnancy rates compared with those undergoing laparotomy (57.6% vs 23.1%, P <.035).32

The goal of surgical management of bowel endometriosis is to remove as many of the endometriotic lesions as possible, while minimizing short- and long-term complications. Three surgical approaches have been described: shaving excision, disc resection, and segmental resection.2 Some surgeons prefer traditional segmental resection of the bowel regardless of the anatomical site, citing reduced disease recurrence with this approach; however, traditional segmental resection confers increased risk of complications.

Increasingly, in an effort to reduce morbidity, more surgeons are advocating for the less aggressive methods of shaving excision and disc resection.

Aggressive resection at the level of the low rectum requires extensive surgical dissection of the retrorectal space, with the potential for inadvertent injury to surrounding neurovascular structures, such as the pelvic splanchnic nerves and superior and inferior hypogastric plexus.29 Injury to these structures can lead to significant complications, including bowel stenosis, fistula formation, constipation, and urinary retention. Complete resection of other areas, such as the small bowel, do not carry the same risks and may have more significant benefit to the patient than less aggressive techniques.

Our group recommends carefully balancing the risks and benefits of aggressive surgical treatment for each individual and treating the patient with the appropriate technique.

Regardless of technique, surgical treatment of bowel endometriosis can lead to long-term improvements in pain and infertility.29,30,34,35

Shaving excision is the most conservative approach to resection of bowel endometriosis and involves removing endometriotic tissue layer-by-layer until healthy, underlying tissue is encountered.2 With bowel endometriosis, the goal of shaving excision is to remove as much of the diseased tissue as possible while leaving behind the mucosal layer and a portion of the muscularis.2,15,16,36-38 This technique is the most conservative of the 3 techniques and is associated with the lowest complication rate.2,14,15,36,39 Our group reported on 185 women who underwent shaving excision for bowel endometriosis. At the time of surgery, 80 women had complete obliteration of the cul-de-sac (FIGURE 6). Of these patients, 174 patients were available for follow-up, with 93% reporting moderate to complete pain relief.15 In a retrospective analysis of 3,298 surgeries for rectovaginal endometriosis in which shaving excision was used on all but 1% of patients, Donnez and colleagues reported a very low complication rate, with 1 case of rectal perforation, 1 case of fecal peritonitis, and 3 cases of ureteral injury.40 Roman et al described the use of shaving excision for rectal endometriosis using plasma energy (n = 54) and laparoscopic scissors (n = 68).41 Only 4% of patients reported experiencing symptom recurrence, and the pregnancy rate was 65.4%, with 59% of those patients spontaneously conceiving. Two cases of rectal fistula were noted.

Figure 6. Complete obliteration of the cul-de-sac.

Laparoscopic disc excision has been described in the literature since the 1980s and involves the full-thickness removal of the diseased portion of the bowel, followed by closure of the remaining defect.2,12-14,28,29,31,42-46 To be appropriate for this technique, a lesion should involve only a portion of the bowel wall and preferably less than one-half of the bowel circumference.2,43 Disc excision results in excellent outcomes with fewer postoperative complications than segmental resection, but with more complications when compared to shaving excision.2,12,13,29,46,47 We reported on a series of 141 women with bowel endometriosis who underwent disc excision. At 1-month follow-up, 87% of patients experienced an improvement in their symptoms. No cases required conversion to laparotomy or were complicated by rectovaginal fistula formation, ureteral injury, bowel perforation, or pelvic abscess.2

Segmental resection is the most aggressive surgical approach and involves complete removal of a diseased portion of bowel, followed by side-to-side or end-to-end reanastomosis of the adjacent segments.2 For this procedure, a multidisciplinary approach is recommended, with involvement of a colorectal surgeon or gynecologic oncologist who is trained in performing bowel resections. Segmental resection is indicated for lesions that are >3 cm, circumferential, obstructive, or multifocal.

Given the higher complication rate associated with this procedure and the good outcomes associated with less invasive techniques, we avoid segmental resection whenever possible, especially for lesions near the anal verge.2

In 2005, our group reported on a cohort of 178 women who underwent laparoscopic treatment of deeply infiltrative bowel endometriosis utilizing shaving excision (n = 93), disc excision (n = 38), and segmental resection (n = 47).34 The major complication rate was significantly higher for those undergoing segmental resection (12.5%, P <.001); only 7.7% of those who underwent disc resection experienced a major complication, and none were observed in the group treated with shaving excision. In 2011, De Cicco and colleagues performed a systematic review of 1,889 patients who underwent segmental bowel resection.35 The major complication rate was 11%, with a leakage rate of 2.7%, fistula rate of 1.8%, major obstruction rate of 2.7%, and hemorrhage rate of 2.5%. It was noted, however, that many of these complications occurred in patients undergoing low rectal resections.

Regardless of surgical approach, the complication rate is related to the surgeon’s ability to preserve the superior and inferior hypogastric plexuses and the sympathetic and parasympathetic nerve bundles. Nerve-sparing techniques should be used to decrease the incidence of postoperative bowel, bladder, and sexual function complications (FIGURE 7).2

Figure 7. Innervation of the pelvic organs.

Copyright Joe Gorman

Conclusion

The clinical presentation of bowel endometriosis is often nonspecific and the differential diagnosis is broad. Affected patients often are misdiagnosed and may not receive adequate treatment for many years. Clinicians should maintain a high index of suspicion when reproductive- age women present for evaluation of dysmenorrhea, chronic pelvic pain, dyspareunia, bloating, dyschezia, or hematochezia. Symptomatic patients not desiring fertility, poor surgical candidates, and those declining surgical intervention may benefit from medical management. Patients who failed medical therapy, have severe symptoms, or experience infertility are candidates for surgical intervention.

Surgical management involves 3 approaches: shaving excision, disc resection, and segmental resection. Some surgeons advocate for aggressive segmental resection regardless of the location of the endometriotic lesion.

Based on our extensive experience, we prefer shaving excision for lesions below the sigmoid colon to avoid dissection into the retrorectal space and inadvertent injury to nerve tissue controlling bowel and bladder function.

Following shaving excision, patients experience low complication rates29,40,41 and favorable long-term outcomes.15,41,57 For lesions above the sigmoid colon, including the small bowel, segmental resection or disc resection for smaller lesions are reasonable surgical approaches.

Dr. Burns is Fellow, Camran Nezhat Institute, Palo Alto, California.

Dr. Wood is Fellow, Camran Nezhat Institute.

Dr. Ceana Nezhat is Director, Nezhat Medical Center, Atlanta, Georgia.
Dr. Camran Nezhat is Director of the Camran Nezhat Institute and Founder of Worldwide Endometriosis March.

The authors report no financial relationships relevant to this article.

References

  1. Giudice LC. Clinical practice. Endometriosis. N Engl J Med. 2010;362(25):2389-2398.
  2. Nezhat C, Li A, Falik R, et al. Bowel endometriosis: diagnosis and management. Am J Obstet Gynecol. 2018;218(6):549-562.
  3. Markham SM, Carpenter SE, Rock JA. Extrapelvic endometriosis. Obstet Gynecol Clin North Am. 1989;16(1):193-219.
  4. Veeraswamy A, Lewis M, Mann A, Kotikela S, Hajhosseini B, Nezhat C. Extragenital endometriosis. Clin Obstet Gynecol. 2010;53(2):449-466.
  5. Redwine DB. Ovarian endometriosis: a marker for more extensive pelvic and intestinal disease. Fertil Steril. 1999;72(2):310-315.
  6. Weed JC, Ray JE. Endometriosis of the bowel. Obstet Gynecol. 1987;69(5):727-730.
  7. Wheeler JM. Epidemiology of endometriosis-associated infertility. J Reprod Med. 1989; 34(1):41-46.
  8. Redwine DB. Intestinal endometriosis. In: Surgical Management of Endometriosis. New York, NY: Informa Healthcare; XXX-XXX.
  9. Hartmann D, Schilling D, Roth SU, Bohrer MH, Riemann JF. [Endometriosis of the transverse colon—a rare localization]. Dtsch Med Wochenschr. 2002;127(44):2317-2320.
  10. Nezhat C, Nezhat F, Nezhat C. Endometriosis: ancient disease, ancient treatments. Fertil Steril. 2012;98(6 suppl):S1-62.
  11. Macafee CH Greer HL. Intestinal endometriosis. A report of 29 cases and a survey of the literature. J Obstet Gynaecol Br Emp. 1960;67:539-555.
  12. Nezhat C, Nezhat F, Ambroze W, Pennington E. Laparoscopic repair of small bowel and colon. A report of 26 cases. Surg Endosc. 1993;7(2):88-89.
  13. 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. 1994;8(6):682-685.
  14. Nezhat C, Nezhat F. Evaluation of safety of videolaseroscopic treatment of bowel endometriosis. Presented at: 44th Annual Meeting of the American Fertility Society; October, 1988; Atlanta, GA.
  15. 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. 1992;99(8):664-667.
  16. Nezhat C, Crowgey SR, Garrison CP. Surgical treatment of endometriosis via laser laparoscopy. Fertil Steril. 1986;45(6):778-783.
  17. Sourial S, Tempest N, Hapangama DK. Theories on the pathogenesis of endometriosis. Int J Reprod Med. 2014;2014:179515.
  18. Heller DS, Lespinasse P, Mirani N. Endometriosis of the perineum: a rare diagnosis usually associated with episiotomy. J Low Genit Tract Dis. 2016;20(3): e48-e49.
  19. Skoog SM, Foxx-Orenstein AE, Levy MJ, Rajan E, Session DR. Intestinal endometriosis: the great masquerader. Curr Gastroenterol Rep. 2004;6(5):405-409.
  20. Alabiso G, Alio L, Arena S, et al. How to manage bowel endometriosis: the ETIC approach. J Minim Invasive Gynecol. 2015;22(4):517-529.
  21. 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. 2011;37(3):257-263.
  22. Nisenblat V, Bossuyt PM, Farquhar C, Johnson N, Hull ML. Imaging modalities for the non-invasive diagnosis of endometriosis. Cochrane Database Syst Rev. 2016;2:CD009591.
  23. Menada MV, Remorgida V, Abbamonte LH, Fulcheri E, Ragni N, Ferrero S. Transvaginal ultrasonography combined with water-contrast in the rectum in the diagnosis of rectovaginal endometriosis infiltrating the bowel. Fertil Steril. 2008;89(3):699-700.
  24. Gordon RL, Evers K, Kressel HY, Laufer I, Herlinger H, Thompson JJ. Double-contrast enema in pelvic endometriosis. AJR Am J Roentgenol. 1982;138(3):549-552.
  25. Vercellini P, Pietropaolo G, De Giorgi O, Pasin R, Chiodini A, Crosignani PG. Treatment of symptomatic rectovaginal endometriosis with an estrogen-progestogen combination versus low-dose norethindrone acetate. Fertil Steril. 2005;84(5):1375-13787.
  26. 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. 2010;25(1):94-100.
  27. Nezhat C, Hajhosseini B, King LP. Robotic-assisted laparoscopic treatment of bowel, bladder, and ureteral endometriosis. JSLS. 2011;15(3):387-392.
  28. Nezhat C, Hajhosseini B, King LP. Laparoscopic management of bowel endometriosis: predictors of severe disease and recurrence. JSLS. 2011;15(4):431-438.
  29. Roman H, Milles M, Vassilieff M, et al. Long-term functional outcomes following colorectal resection versus shaving for rectal endometriosis. Am J Obstet Gynecol. 2016;215(6): 762.e1-762.e9.
  30. Kent A, Shakir F, Rockall T, et al. Laparoscopic surgery for severe rectovaginal endometriosis compromising the bowel: a prospective cohort study. J Minim Invasive Gynecol. 2016;23(4):526-534.
  31. Nezhat F, Nezhat C, Pennington E. Laparoscopic proctectomy for infiltrating endometriosis of the rectum. Fertil Steril. 1992;57(5):1129-1132.
  32. Ruffo G, Scopelliti F, Scioscia M, Ceccaroni M, Mainardi P, Minelli L. Laparoscopic colorectal resection for deep infiltrating endometriosis: analysis of 436 cases. Surg Endosc. 2010;24(1):63-67.
  33. 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. 2010;251(6):1018-1023.
  34. Mohr C, Nezhat FR, Nezhat CH, Seidman DS, Nezhat CR. Fertility considerations in laparoscopic treatment of infiltrative bowel endometriosis. JSLS. 2005;9(1):16-24.
  35. De Cicco C, Corona R, Schonman R, Mailova K, Ussia A, Koninckx P. Bowel resection for deep endometriosis: a systematic review. BJOG. 2011;118(3):285-291.
  36. Nezhat C, Nezhat FR. Safe laser endoscopic excision or vaporization of peritoneal endometriosis. Fertil Steril. 1989;52(1):149-151.
  37. 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. 2010;25(8):1949-1958.
  38. Nezhat C, Crowgey SR, Garrison CP. Surgical treatment of endometriosis via laser laparoscopy and videolaseroscopy. Contrib Gynecol Obstet. 1987;16:303-312.
  39. 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. 2010;25(8):1949-1958.
  40. Donnez J, Jadoul P, Colette S, et al. Deep rectovaginal endometriotic nodules: perioperative complications from a series of 3,298 patients operated on by the shaving technique. Gynecol Surg. 2013;10(1):31-40.
  41. Roman H, Moatassim-Drissa S, Marty N, et al. Rectal shaving for deep endometriosis infiltrating the rectum: a 5-year continuous retrospective series. Fertil Steril. 2016;106(6):1438-1445.e2.
  42. Mohr C, Nezhat FR, Nezhat CH, Seidman DS, Nezhat CR. Fertility considerations in laparoscopic treatment of infiltrative bowel endometriosis. JSLS. 2005;9(1):16-24.
  43. Jerby BL, Kessler H, Falcone T, Milsom JW. Laparoscopic management of colorectal endometriosis. Surg Endosc. 1999;13(11):1125-1128.
  44. Coronado C, Franklin RR, Lotze EC, Bailey HR, Valdés CT. Surgical treatment of symptomatic colorectal endometriosis. Fertil Steril. 1990;53(3):411-416.
  45. Fanfani F, Fagotti A, Gagliardi ML, et al. Discoid or segmental rectosigmoid resection for deep infiltrating endometriosis: a case-control study. Fertil Steril. 2010;94(2):444-449.
  46. 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. 2008;207(2):205-209.
  47. Slack A, Child T, Lindsey I, et al. Urological and colorectal complications following surgery for rectovaginal endometriosis. BJOG. 2007;114(10):1278-1282.
  48. Ceccaroni M, Clarizia R, Bruni F, et al. Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: The negrar method. A single-center, prospective, clinical trial. Surg Endosc. 2012;26(7):2029-2045.
  49. Roman H, Abo C, Huet E, Tuech JJ. Deep shaving and transanal disc excision in large endometriosis of mid and lower rectum: the Rouen technique. Surg Endosc. 2016;30(6):2626-2627.
  50. Gustofson RL, Kim N, Liu S, Stratton P. Endometriosis and the appendix: a case series and comprehensive review of the literature. Fertil Steril. 2006;86(2):298-303.
  51. Berker B, Lashay N, Davarpanah R, Marziali M, Nezhat CH, Nezhat C. et al. Laparoscopic appendectomy in patients with endometriosis. J Minim Invasive Gynecol. 2005;12(3):206-209.
  52. Ret Dávalos ML, De Cicco C, D’Hoore A, De Decker B, Koninckx PR. Outcome after rectum or sigmoid resection: a review for gynecologists. J Minim Invasive Gynecol. 2007;14(1):33-38.
  53. Alves A, Panis Y, Mathieu P, Kwiatkowski F, Slim K, Mantion G; Association Française de Chirurgie (AFC). Mortality and morbidity after surgery of mid and low rectal cancer. Results of a French prospective multicentric study. Gastroenterol Clin Biol. 2005;29(5):509-514.
  54. Camilleri-Brennan J, Steele RJ. Objective assessment of morbidity and quality of life after surgery for low rectal cancer. Colorectal Dis. 2002;4(1):61-66.
  55. Acien P, Núñez C, Quereda F, Velasco I, Valiente M, Vidal V. Is a bowel resection necessary for deep endometriosis with rectovaginal or colorectal involvement? Int J Womens Health. 2013;5:449-455.
  56. Abrão MS, Petraglia F, Falcone T, Keckstein J, Osuga Y, Chapron C. Deep endometriosis infiltrating the recto-sigmoid: critical factors to consider before management. Hum Reprod Update. 2015;21(3):329-339.
  57. 57. Donnez J, Nisolle M, Gillerot S, Smets M, Bassil S, Casanas-Roux F. Rectovaginal septum adenomyotic nodules: a series of 500 cases. Br J Obstet Gynaecol. 1997;104(9):1014-1018.