Surgical Treatment of Deep Endometriosis

  • Rodrigo Fernandes
  • Karolina Afors
  • Arnaud Wattiez


  • Endometriosis is a complex gynecological disease, which presents a challenge for researchers and surgeons alike. Ectopic deposits of endometrial tissue typically found in the pelvis contribute to disease progression. Associated symptoms of pain and infertility are often attributed to adhesion formation and anatomical distortion frequently responsible for the clinical consequences of the disease [1]. Endometrial tissue within the uterine cavity is responsible for preparing the embryo implantation and nourishing the developing fetus. In the absence of a pregnancy, the corpus luteum degenerates, and hormone levels drop, the effect of which results in shedding of the endometrial lining. This continuous cycle exposes women to constant fluctuations in hormones levels, which in turn regulates the endometrium.

  • Endometriosis most commonly affects the ovaries, posterior cul-de-sac, and uterosacral ligaments [2]. Less frequently affected sites including the diaphragm, lungs, and even endometriotic implants involving the brain have been described [3].


Endometriosis Laparoscopy Surgical technique 


  1. 1.
    Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J. Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril. 2012;98(3):564–71.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Studio dell’Endometriosi lo GIP. Prevalence and anatomical distribution of endometriosis in women with selected gynaecological conditions: results from a multicentric Italian study. Gruppo italiano per lo studio dell’endometriosi. Hum Reprod. 1994;9(6):1158–62.Google Scholar
  3. 3.
    Sherif AM, Musa ER, Kedar R, Fu L. Subcapsular hepatic endometriosis: case report and review of the literature. Radiol Case Rep. 2016;11(4):303–8.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol. 1927;3(2):93–110.43.PubMedPubMedCentralGoogle Scholar
  5. 5.
    Batt RE, Smith RA, Buck Louis GM, Martin DC, Chapron C, Koninckx PR, et al. Müllerianosis. Histol Histopathol. 2007;22(10):1161–6.PubMedGoogle Scholar
  6. 6.
    Abrao MS, Muzii L, Marana R. Anatomical causes of female infertility and their management. Int J Gynaecol Obstet. 2013;123(S2):S18–24.PubMedCrossRefGoogle Scholar
  7. 7.
    Yu J-J, Sun H-T, Zhang Z-F, Shi R-X, Liu L-B, Shang W-Q, et al. IL15 promotes growth and invasion of endometrial stromal cells and inhibits killing activity of NK cells in endometriosis. Reproduction. 2016;152(2):151–60.PubMedCrossRefGoogle Scholar
  8. 8.
    Trippia CH, Zomer MT, Terazaki CRT, Martin RLS, Ribeiro R, Kondo W. Relevance of imaging examinations in the surgical planning of patients with bowel endometriosis. Clin Med Insights Reprod Health. 2016;10:1–8.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    ASRM. Revised American Society for Reproductive Medicine classification of endometriosis: 1996. Fertil Steril. 1997;67(5):817–21.Google Scholar
  10. 10.
    Dunselman GAJ, Vermeulen N, Becker C, Calhaz-Jorge C, D’Hooghe T, De Bie B, et al. ESHRE guideline: management of women with endometriosis. Hum Reprod. 2014;29:400–12.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Akladios C, Faller E, Afors K, Puga M, Albornoz J, Redondo C, et al. Totally laparoscopic intracorporeal anastomosis with Natural Orifice Specimen Extraction (NOSE) techniques, particularly suitable for bowel endometriosis. J Minim Invasive Gynecol. 2014;21(6):1–24.CrossRefGoogle Scholar
  12. 12.
    Simoens S, Dunselman G, Dirksen C, Hummelshoj L, Bokor A, Brandes I, et al. The burden of endometriosis: costs and quality of life of women with endometriosis and treated in referral centres. Hum Reprod. 2012;27(5):1292–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Soliman AM, Yang H, EX D, Kelley C, Winkel C. The direct and indirect costs associated with endometriosis: a systematic literature review. Hum Reprod. 2016;31(4):712–22.PubMedCrossRefGoogle Scholar
  14. 14.
    De Graaff AA, Van Lankveld J, Smits LJ, Van Beek JJ, Dunselman GAJ. Dyspareunia and depressive symptoms are associated with impaired sexual functioning in women with endometriosis, whereas sexual functioning in their male partners is not affected. Hum Reprod. 2016;31(11):2577–86.PubMedCrossRefGoogle Scholar
  15. 15.
    Renner SP, Boosz AS, Burghaus S, Maihöfner C, Beckmann MW, Fasching PA, et al. Visual pain mapping in endometriosis. Arch Gynecol Obstet. 2012;286(3):687–93.PubMedCrossRefGoogle Scholar
  16. 16.
    Rozsnyai F, Roman H, Resch B, Dugardin F, Berrocal J, Descargues G, et al. Outcomes of surgical management of deep infiltrating endometriosis of the ureter and urinary bladder. JSLS. 2011;15(4):439–47.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Roman H, Loisel C, Resch B, Tuech JJ, Hochain P, Leroi AM, et al. Delayed functional outcomes associated with surgical management of deep rectovaginal endometriosis with rectal involvement: giving patients an informed choice. Hum Reprod. 2010;25(4):890–9.PubMedCrossRefGoogle Scholar
  18. 18.
    Bispo Dos APS, Ploger C, Loureiro AF, Sato H, Kolpeman A, Girão MJBC, et al. Assessment of pelvic floor muscles in women with deep endometriosis. Arch Gynecol Obstet. 2016;294(3):519–23.CrossRefGoogle Scholar
  19. 19.
    Somigliana E, Paffoni A, Busnelli A, Filippi F, Pagliardini L, Vigano P, et al. Age-related infertility and unexplained infertility: an intricate clinical dilemma. Hum Reprod. 2016;31(7):1390–6.PubMedCrossRefGoogle Scholar
  20. 20.
    Prescott J, Farland LV, Tobias DK, Gaskins AJ, Spiegelman D, Chavarro JE, et al. A prospective cohort study of endometriosis and subsequent risk of infertility. Hum Reprod. 2016;31(7):1475–82.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Roustan A, Perrin J, Debals-Gonthier M, Paulmyer-Lacroix O, Agostini A, Courbiere B. Surgical diminished ovarian reserve after endometrioma cystectomy versus idiopathic DOR: comparison of in vitro fertilization outcome. Hum Reprod. 2015;30(4):840–7.PubMedCrossRefGoogle Scholar
  22. 22.
    Witz CA, Burns WN. Endometriosis and infertility: is there a cause and effect relationship? Gynecol Obstet Investig. 2002;53(Suppl 1):2–11.CrossRefGoogle Scholar
  23. 23.
    Witz CA, Allsup KT, Montoya-Rodriguez IA, Vaughan SL, Centonze VE, Schenken RS. Pathogenesis of endometriosis--current research. Hum Fertil (Camb). 2003;6(1):34–40.CrossRefGoogle Scholar
  24. 24.
    Santulli P, Lamau MC, Marcellin L, Gayet V, Marzouk P, Borghese B, et al. Endometriosis-related infertility: ovarian endometrioma per se is not associated with presentation for infertility. Hum Reprod. 2016;31(8):1765–75.PubMedCrossRefGoogle Scholar
  25. 25.
    Muzii L, Achilli C, Bergamini V, Candiani M, Garavaglia E, Lazzeri L, et al. Comparison between the stripping technique and the combined excisional/ablative technique for the treatment of bilateral ovarian endometriomas: a multicentre RCT. Hum Reprod. 2015;31(2):339–44.PubMedGoogle Scholar
  26. 26.
    Ata B, Urman B. Endometrioma excision and ovarian reserve; do assessments by antral follicle count and anti-Müllerian hormone yield contradictory results? Hum Reprod. 2014;29(12):2852–4.PubMedCrossRefGoogle Scholar
  27. 27.
    Centini G, Afors K, Murtada R, Argay IM, Lazzeri L, Akladios CY, et al. Impact of laparoscopic surgical management of deep endometriosis on pregnancy rate. J Minim Invasive Gynecol. 2016;23(1):113–9.PubMedCrossRefGoogle Scholar
  28. 28.
    Santos TMV, Pereira AMG, Lopes RGC, Depes DDB. Lag time between onset of symptoms and diagnosis of endometriosis. Einstein (São Paulo). 2012;10(1):39–43.CrossRefGoogle Scholar
  29. 29.
    Abrao MS, Goncalves MODC, Dias JA, Podgaec S, Chamie LP, Blasbalg R. Comparison between clinical examination, transvaginal sonography and magnetic resonance imaging for the diagnosis of deep endometriosis. Hum Reprod. 2007;22(12):3092–7.PubMedCrossRefGoogle Scholar
  30. 30.
    Hottat N, Larrousse C, Anaf V, Noel J-C, Matos C, Absil J, et al. Endometriosis: contribution of 3.0-T pelvic MR imaging in preoperative assessment--initial results. Radiology. 2009;253(1):126–34.PubMedCrossRefGoogle Scholar
  31. 31.
    Manganaro L, Vittori G, Vinci V, Fierro F, Tomei A, Lodise P, et al. Beyond laparoscopy: 3-T magnetic resonance imaging in the evaluation of posterior cul-de-sac obliteration. Magnetic Resonance Imaging. 2012;30(10):1432–8.PubMedCrossRefGoogle Scholar
  32. 32.
    Bazot M, Bharwani N, Huchon C, Kinkel K, Cunha TM, Guerra A, et al. European society of urogenital radiology (ESUR) guidelines: MR imaging of pelvic endometriosis. Eur Radiol. 27(7):2765–75.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Spagnolo E, Zannoni L, Raimondo D, Ferrini G, Mabrouk M, Benfenati A, et al. Urodynamic evaluation and anorectal manometry pre- and post-operative bowel shaving surgical procedure for posterior deep infiltrating endometriosis: a pilot study. J Minim Invasive Gynecol. 2014;21(6):1080–5.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Centini G, Afors K, Murtada R, Argay IM, Lazzeri L, Akladios CY, et al. The impact of laparoscopic surgical management of deep endometriosis on pregnancy rate. J Minim Invasive Gynecol. 2015;23(1):1–26.Google Scholar
  35. 35.
    Wattiez A, Puga M, Albornoz J, Faller E. Surgical strategy in endometriosis. Best Pract Res Clin Obstet Gynaecol. 2013;27(3):381–92.PubMedCrossRefGoogle Scholar
  36. 36.
    Koninckx PR, Gomel V. Introduction: quality of pelvic surgery and postoperative adhesions. Fertil Steril. 2016;106(5):991–3.PubMedCrossRefGoogle Scholar
  37. 37.
    Koninckx PR, Donnez J, Brosens I. Microscopic endometriosis: impact on our understanding of the disease and its surgery. Fertil Steril. 2016;105(2):305–6.PubMedCrossRefGoogle Scholar
  38. 38.
    Anaf V, Nakadi El I, De Moor V, Chapron C, Pistofidis G, Nöel JC. Increased nerve density in deep infiltrating endometriotic nodules. Gynecol Obstet Investig. 2011;71(2):112–7.CrossRefGoogle Scholar
  39. 39.
    Arnold J, de Arellano MLB, Rüster C, Vercellino GF, Chiantera V, Schneider A, et al. Imbalance between sympathetic and sensory innervation in peritoneal endometriosis. Brain Behav Immun. 2012;26(1):132–41.PubMedCrossRefGoogle Scholar
  40. 40.
    Hart RJ HMMPBW. Excisional surgery versus ablative surgery for ovarian endometriomata (Review). 2013 Jan 1;:1–33.Google Scholar
  41. 41.
    Mei Zhang X, Feng Huang X, Xu H, Quinn M. Endometriosis: a consequence of varying injuries to pelvic autonomic nerves. Fertil Steril. American Society for Reproductive Medicine. 2012;98(6):e29.PubMedCrossRefGoogle Scholar
  42. 42.
    CHAPRON C, Bourret A, CHOPIN N, Dousset B, Leconte M, Amsellem-Ouazana D, et al. Surgery for bladder endometriosis: long-term results and concomitant management of associated posterior deep lesions. Hum Reprod. 2010;25(4):884–9.PubMedCrossRefGoogle Scholar
  43. 43.
    Anaf V, Nakadi El I, Simon P, Van de Stadt J, Fayt I, Simonart T, et al. Preferential infiltration of large bowel endometriosis along the nerves of the colon. Hum Reprod. 2004;19(4):996–1002.PubMedCrossRefGoogle Scholar
  44. 44.
    Donnez J. Endometriosis: enigmatic in the pathogenesis and controversial in its therapy. Fertil Steril. 2012;98(3):509–10.PubMedCrossRefGoogle Scholar
  45. 45.
    William Kondo, Reitan Ribeiro, Carlos Trippia, Monica Tessmann Zomer. Laparoscopic treatment of deep infiltrating endometriosis affecting the rectosigmoid colon: nodulectomy or segmental resection? Gynecol Obstet. 2013;03(01).Google Scholar
  46. 46.
    Afors K, Murtada R, Centini G, Fernandes RP, Meza C, Castellano J, et al. Employing laparoscopic surgery for endometriosis. Womens Health. 2014 Jul;10(4):431–43.Google Scholar
  47. 47.
    Afors K, Centini G, Fernandes RP, Murtada R, Zupi E, Akladios C, et al. Segmental and discoid resection are preferential to bowel shaving for medium-term symptomatic relief in patients with bowel endometriosis. J Minim Invasive Gynecol. 2016;23(7):1123–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Cherif Akladios MP, Emilie Faller MD, Karolina Afors MD, Marco Puga MD, Jaime Albornoz MD, Christina Redondo MD, et al. Totally laparoscopic intracorporeal anastomosis with Natural Orifice Specimen Extraction (NOSE) techniques, particularly suitable for bowel endometriosis. J Minim Invasive Gynecol. 2014;21(6):1–24.Google Scholar
  49. 49.
    Messori P, Faller E, Albornoz J, Leroy J, Wattiez A. Laparoscopic Sigmoidectomy for Endometriosis With Transanal Specimen Extraction. J Minim Invasive Gynecol. 2013;20(4):412.PubMedCrossRefGoogle Scholar
  50. 50.
    Costantino FA, Diana M, Wall J, Leroy J, Mutter D, Marescaux J. Prospective evaluation of peritoneal fluid contamination following transabdominal vs. transanal specimen extraction in laparoscopic left-sided colorectal resections. Surg Endosc. 2011;26(6):1495–500.PubMedCrossRefGoogle Scholar
  51. 51.
    Antonelli A. Urinary tract endometriosis. Urologia. 2012;79(3):167–70.PubMedCrossRefGoogle Scholar
  52. 52.
    Kovoor E, Nassif J, Miranda-Mendoza I, Wattiez A. Endometriosis of bladder: outcomes after laparoscopic surgery. J Minim Invasive Gynecol. 2010;17(5):600–4.PubMedCrossRefGoogle Scholar
  53. 53.
    Alves J, Puga M, Fernandes RP, Pinton A, Miranda I, Kovoor E, et al. Laparoscopic management of ureteral endometriosis and hydronephrosis associated with endometriosis. J Minim Invasive Gynecol. 2017;24(3):466–72.PubMedCrossRefGoogle Scholar
  54. 54.
    Bertrand MM, Alsaid B, Droupy S, Ripoche J, Benoit G, Adalian P, et al. Anatomical basis of the coordination between smooth and striated urethral and anal sphincters: loops of regulation between inferior hypogastric plexus and pudendal nerve. Immuno-histological study with 3D reconstruction. Surg Radiol Anat. Springer Paris; 2016:1–10.PubMedCrossRefGoogle Scholar
  55. 55.
    Ceccaroni M, Clarizia R, Alboni C, Ruffo G, Bruni F, Roviglione G, et al. Laparoscopic nerve-sparing transperitoneal approach for endometriosis infiltrating the pelvic wall and somatic nerves: anatomical considerations and surgical technique. Surg Radiol Anat. 2010;32(6):601–4.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Pandis GK, Saridogan E, Windsor ACJ, Gulumser C, Cohen CRG, Cutner AS. Short-term outcome of fertility-sparing laparoscopic excision of deeply infiltrating pelvic endometriosis performed in a tertiary referral center. Fertil Steril. 2010;93(1):39–45.PubMedCrossRefGoogle Scholar
  57. 57.
    Ruffo G, Sartori A, Crippa S, Partelli S, Barugola G, Manzoni A, et al. Laparoscopic rectal resection for severe endometriosis of the mid and low rectum: technique and operative results. Surg Endosc. 2012;26(4):1035–40.PubMedCrossRefGoogle Scholar
  58. 58.
    Kondo W, Bourdel N, Tamburro S, Cavoli D, Jardon K, Rabischong B, et al. Complications after surgery for deeply infiltrating pelvic endometriosis. BJOG Int J Obstet Gynaecol. 2011;118(3):292–8.CrossRefGoogle Scholar
  59. 59.
    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):1949–58.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Rodrigo Fernandes
    • 1
  • Karolina Afors
    • 1
  • Arnaud Wattiez
    • 2
    • 3
  1. 1.ICESP, University of São PauloSão PauloBrazil
  2. 2.Department of GynecologyLatifa HospitalDubaiUAE
  3. 3.University of StrasbourgStrasbourgFrance

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