Archives of Gynecology and Obstetrics

, Volume 298, Issue 3, pp 639–647 | Cite as

Functional outcomes of nerve-sparing laparoscopic eradication of deep infiltrating endometriosis: a prospective analysis using validated questionnaires

  • Stefano UccellaEmail author
  • Baldo Gisone
  • Maurizio Serati
  • Sara Biasoli
  • Nicola Marconi
  • Gloria Angeretti
  • Valerio Gallotta
  • Silvia Cardinale
  • Stefano Rausei
  • Gianlorenzo Dionigi
  • Giovanni Scambia
  • Fabio Ghezzi
General Gynecology



Radical eradication of deep infiltrating endometriosis (DIE) is associated with a high risk of iatrogenic autonomic denervation and pelvic dysfunction. Our aim was to prospectively analyze peri-operative details and post-operative functional outcomes (in terms of pain relief and bladder, rectal, and sexual function) among women operated for DIE of the posterior compartment with nerve-sparing technique, using the visual analogue scale and validated questionnaires.


All women undergoing laparoscopic nerve-sparing eradicative surgery for DIE nodules of the posterior compartment ≥ 4 cm ± bowel resection were included. Pain scores [using Visual Analogue Scale (VAS) scores] were collected before surgery and 6 and 12 months after surgery. Functional outcomes in terms of bladder, rectal, and sexual function, were evaluated using validated questionnaires (i.e., ICIQ-UISF, NBD score, and FSFI) administered pre-operatively and 6 months after surgery.

Main results

A total of 34 patients were included. Twenty-eight (82.4%) of them had already undergone a previous abdominal surgery for endometriosis. Bowel resection was performed in 16 (47.1%) patients. Median VAS score levels of pelvic pain were significantly decreased after surgery both at 6 (median 3, range 0–7 and 2, 0–7, respectively) and at 12 months (3, 0–8 and 2, 0–7), compared to pre-operative levels (9, 1–10 and 3, 0–7, respectively) (p < 0.0001). No differences were found in terms of urinary function between pre- and post-operative ICIQ-SF questionnaires. In no cases, bladder self-catheterization was needed at the 6-and 12-month follow-up. Median NBD score was 3.5 (0–21) pre-operatively and 2 (0–18) after 6 months (p = 0.72). The pre-operative total FSFI score was 19.1 (1.2–28.9) vs. 22.7 (12.2–31) post-operatively (p = 0.004).


The nerve-sparing approach is effective in eradicating DIE of the posterior compartment, with satisfactory pain control, significant improvement of sexual function, and preservation of bladder and rectal function.


Laparoscopy Deep infiltrating endometriosis Nerve sparing Bladder function Rectal function Sexual function 


Author contributions

SU: project development, data collection and management, data analysis, and manuscript writing. BG: data collection and management, and data analysis. MS: project development. SB: data collection and management, and data analysis. NM: data collection and management, data analysis, and manuscript editing. GA: project development. VG: project development and manuscript writing. SC: data collection and management, and data analysis. SR: project development. GD: project development. GS: project development and manuscript editing. FG: project developmentand manuscript editing.


No funding was obtained for the present study.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interests to disclose.

Ethical approval

All procedures performed were in accordance with the ethical standards of the institutional and/or national research committee, and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Buck Louis GM, Hediger ML, Peterson CM, Croughan M, Sundaram R, Stanford J et al (2011) Incidence of endometriosis by study population and diagnostic method: the ENDO study. Fertil Steril 96:360–365CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Giudice LC (2010) Clinical practice. Endometriosis. N Engl J Med 362(25):2389–2398CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Uccella S, Cromi A, Casarin J, Bogani G, Pinelli C, Serati M et al (2014) Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes. Fertil Steril 102(160–166):e2. CrossRefGoogle Scholar
  4. 4.
    Koninckx PR, Ussia A, Adamyan L, Wattiez A, Donnez J (2012) Deep endometriosis: definition, diagnosis, and treatment. Fertil Steril 98:564–571. CrossRefPubMedGoogle Scholar
  5. 5.
    Vercellini P, Somigliana E, Consonni D, Frattaruolo MP, De Giorgi O, Fedele L (2012) Surgical versus medical treatment for endometriosis-associated severe deep dyspareunia: I. Effect on pain during intercourse and patient satisfaction. Hum Reprod 27:3450–3459. CrossRefPubMedGoogle Scholar
  6. 6.
    Vercellini P, Frattaruolo MP, Rosati R, Dridi D, Roberto A, Mosconi P et al (2017) Medical treatment or surgery for colorectal endometriosis? Results of a shared decision-making approach. Hum Reprod. CrossRefPubMedGoogle Scholar
  7. 7.
    Vercellini P, Buggio L, Somigliana E (2017) Role of medical therapy in the management of deep rectovaginal endometriosis. Fertil Steril 108:913–930. CrossRefPubMedGoogle Scholar
  8. 8.
    De Cicco C, Corona R, Schonman R, Mailova K, Ussia A, Koninckx P (2011) Bowel resection for deep endometriosis: a systematic review. BJOG 118:285–291. CrossRefPubMedGoogle Scholar
  9. 9.
    Berlanda N, Somigliana E, Frattaruolo MP, Buggio L, Dridi D, Vercellini P (2017) Surgery versus hormonal therapy for deep endometriosis: is it a choice of the physician? Eur J Obstet Gynecol Reprod Biol 209:67–71. CrossRefPubMedGoogle Scholar
  10. 10.
    Darai E, Thomassin I, Barranger E, Detchev R, Cortez A, Houry S, Bazot M (2005) Feasibility and clinical outcome of laparoscopic colorectal resection for endometriosis. Am J Obstet Gynecol 192:394–400CrossRefPubMedGoogle Scholar
  11. 11.
    Ceccaroni M, Clarizia R, Tebache L (2016) Role and technique of nerve-sparing surgery in deep endometriosis. J Endometr Pelvic Pain Disord 8:141–151Google Scholar
  12. 12.
    Ceccaroni M, Clarizia R, Bruni F et al (2012) Nerve-sparing laparoscopic eradication of deep endometriosis with segmental rectal and parametrial resection: the Negrar method. A single-center, prospective, clinical trial. Surg Endosc 26:2029–2045. CrossRefPubMedGoogle Scholar
  13. 13.
    Rob L, Halaska M, Robova H (2010) Nerve-sparing and individually tailored surgery for cervical cancer. Lancet Oncol 11:292–301CrossRefPubMedGoogle Scholar
  14. 14.
    Trimbos JB, Maas CP, Deruiter MC, Peters AA, Kenter GG (2001) A nerve-sparing radical hysterectomy: guidelines and feasibility in Western patients. Int J Gynecol Cancer 11:180–186CrossRefPubMedGoogle Scholar
  15. 15.
    Yabuki Y, Asamoto A, Hoshiba T, Nishimoto H, Nishikawa Y, Nakajima T (2000) Radical hysterectomy: an anatomic evaluation of parametrial dissection. Gynecol Oncol 77:155–163CrossRefPubMedGoogle Scholar
  16. 16.
    Ceccaroni M, Pontrelli G, Spagnolo E et al (2010) Parametrial dissection during laparoscopic nerve-sparing radical hysterectomy: a new approach aims to improve patients’ post-operative quality of life. Am J Obstet Gynecol 202:320.e1–320.e2CrossRefGoogle Scholar
  17. 17.
    Volpi E, Ferrero A, Sismondi P (2004) Laparoscopic identification of pelvic nerves in patients with deep infiltrating endometriosis. Surg Endosc 18:1109–1112CrossRefPubMedGoogle Scholar
  18. 18.
    Landi S, Ceccaroni M, Perutelli A et al (2006) Laparoscopic nerve-sparing complete excision of deep endometriosis: is it feasible? Hum Reprod 21:774–781CrossRefPubMedGoogle Scholar
  19. 19.
    Kavallaris A, Banz C, Chalvatzas N et al (2011) Laparoscopic nervesparing surgery of deep infiltrating endometriosis: description of the technique and patients’ outcome. Arch Gynecol Obstet 284:131–135CrossRefPubMedGoogle Scholar
  20. 20.
    von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, STROBE Initiative (2007) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. PLoS Med 4:e296CrossRefGoogle Scholar
  21. 21.
    Revised American Fertility Society classification of endometriosis (1985) Fertil Steril 43:351–352CrossRefGoogle Scholar
  22. 22.
    Haas D, Wurm P, Shamiyeh A, Shebl O, Chvatal R, Oppelt P (2013) Efficacy of the revised Enzian classification: a retrospective analysis. Does the revised Enzian classification solve the problem of duplicate classification in rASRM and Enzian? Arch Gynecol Obstet 287:941–945. CrossRefPubMedGoogle Scholar
  23. 23.
    Tuttlies F, Keckstein J, Ulrich U, Possover M, Schweppe KW, Wustlich M et al (2005) ENZIAN-score, a classification of deep infiltrating endometriosis. Zentralbl Gynakol 127:275–281CrossRefPubMedGoogle Scholar
  24. 24.
    Uccella S, Cromi A, Agosti M, Casarin J, Pinelli C, Marconi N et al (2016) Fertility rates, course of pregnancy and perinatal outcomes after laparoscopic ureterolysis for deep endometriosis: a long-term follow-up study. J Obstet Gynaecol 36:800–805CrossRefPubMedGoogle Scholar
  25. 25.
    Rausei S, Sambucci D, Spampatti S, Cassinotti E, Dionigi G, David G, Ghezzi F, Uccella S, Boni L (2015) Laparoscopic treatment of deep infiltrating endometriosis: results of the combined laparoscopic gynecologic and colorectal surgery. Surg Endosc 29:2904–2909. CrossRefPubMedGoogle Scholar
  26. 26.
    Uccella S, Marconi N, Casarin J, Ceccaroni M, Boni L, Sturla D et al (2016) Impact of endometriosis on surgical outcomes and complications of total laparoscopic hysterectomy. Arch Gynecol Obstet 294:771–778. CrossRefPubMedGoogle Scholar
  27. 27.
    Uccella S, Cromi A, Bogani G, Casarin J, Formenti G, Ghezzi F (2013) Systematic implementation of laparoscopic hysterectomy independent of uterus size: clinical effect. J Minim Invasive Gynecol 20:505–516. CrossRefPubMedGoogle Scholar
  28. 28.
    Uccella S, Cromi A, Bogani G, Casarin J, Serati M, Ghezzi F (2013) Transvaginal specimen extraction at laparoscopy without concomitant hysterectomy: our experience and systematic review of the literature. J Minim Invasive Gynecol 20(5):583–590CrossRefPubMedGoogle Scholar
  29. 29.
    Uccella S, Ceccaroni M, Cromi A, Malzoni M, Berretta R, De Iaco P et al (2012) Vaginal cuff dehiscence in a series of 12,398 hysterectomies: effect of different types of colpotomy and vaginal closure. Obstet Gynecol 120(3):516–523. CrossRefPubMedGoogle Scholar
  30. 30.
    Filocamo MT, Serati M, Li Marzi V, Costantini E, Milanesi M, Pietropaolo A et al (2014) The Female Sexual Function Index (FSFI): linguistic validation of the Italian version. J Sex Med 11:447–453. CrossRefPubMedGoogle Scholar
  31. 31.
    Rosen R, Brown C, Heiman J, Leiblum S, Meston C, Shabsigh R et al (2000) The Female Sexual Function Index (FSFI): a multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther 26:191–208CrossRefPubMedGoogle Scholar
  32. 32.
    Krogh K, Christensen P, Sabroe S, Laurberg S (2006) Neurogenic bowel dysfunction score. Spinal Cord 44:625–631CrossRefPubMedGoogle Scholar
  33. 33.
    Crabtree-Hartman E (2018) Advanced symptom management in multiple sclerosis. Neurol Clin 36:197–218. CrossRefPubMedGoogle Scholar
  34. 34.
    Avery K, Donovan J, Peters T, Shaw C, Gotoh M, Abrams P (2004) ICIQ: a brief and robust measure for evaluating the symptoms and impact of urinary incontinence. Neurourol Urodyn 23:322–330CrossRefPubMedGoogle Scholar
  35. 35.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D'Hooghe T, De Bie B et al (2013) Management of women with endometriosis. Guideline of the European Society of Human Reproduction and Embryology. ESHRE Endometriosis Guideline Development Group.
  37. 37.
    Possover M, Quakernack J, Chiantera V (2005) The LANN technique to reduce post-operative functional morbidity in laparoscopic radical pelvic surgery. J Am Coll Surg 201:913–917CrossRefPubMedGoogle Scholar
  38. 38.
    Mangler M, Herbstleb J, Mechsner S, Bartley J, Schneider A, Köhler C (2014) Long-term follow-up and recurrence rate after mesorectum-sparing bowel resection among women with rectovaginal endometriosis. Int J Gynaecol Obstet 125:266–269CrossRefPubMedGoogle Scholar
  39. 39.
    Morelli L, Perutelli A, Palmeri M et al (2016) Robot-assisted surgery for the radical treatment of deep infiltrating endometriosis with colorectal involvement: short- and mid-term surgical and functional outcomes. Int J Colorectal Dis 31:643–652CrossRefPubMedGoogle Scholar
  40. 40.
    Ballester M, Chereau E, Dubernard G, Coutant C, Bazot M, Daraï E (2011) Urinary dysfunction after colorectal resection for endometriosis: results of a prospective randomized trial comparing laparoscopy to open surgery. Am J Obstet Gynecol 204:303.e1–303.e6CrossRefGoogle Scholar
  41. 41.
    Che X, Huang X, Zhang J, Xu H, Zhang X (2014) Is nerve-sparing surgery suitable for deeply infiltrating endometriosis? Eur J Obstet Gynecol Reprod Biol 175:87–91CrossRefPubMedGoogle Scholar
  42. 42.
    Spagnolo E, Zannoni L, Raimondo D et al (2014) 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 21:1080–1085CrossRefPubMedGoogle Scholar
  43. 43.
    Ercoli A, Bassi E, Ferrari S, Surico D, Fagotti A, Fanfani F, De Cicco F, Surico N, Scambia G (2017) Robotic-assisted conservative excision of retrocervical-rectal deep infiltrating endometriosis: a case series. J Minim Invasive Gynecol 24:863–868. CrossRefPubMedGoogle Scholar
  44. 44.
    Lemos N, Souza C, Marques RM, Kamergorodsky G, Schor E, Girão MJ (2015) Laparoscopic anatomy of the autonomic nerves of the pelvis and the concept of nerve-sparing surgery by direct visualization of autonomic nerve bundles. Fertil Steril 104:e11–e12. CrossRefPubMedGoogle Scholar
  45. 45.
    Serati M, Cattoni E, Braga A, Uccella S, Cromi A, Ghezzi F (2013) Deep endometriosis and bladder and detrusor functions in women without urinary symptoms: a pilot study through an unexplored world. Fertil Steril 100:1332–1336. CrossRefPubMedGoogle Scholar
  46. 46.
    Donnez O, Roman H (2017) Choosing the right surgical technique for deep endometriosis: shaving, disc excision, or bowel resection? Fertil Steril 108:931–942. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Stefano Uccella
    • 1
    • 2
    Email author
  • Baldo Gisone
    • 2
  • Maurizio Serati
    • 2
  • Sara Biasoli
    • 2
  • Nicola Marconi
    • 3
  • Gloria Angeretti
    • 4
  • Valerio Gallotta
    • 1
  • Silvia Cardinale
    • 2
  • Stefano Rausei
    • 5
  • Gianlorenzo Dionigi
    • 6
  • Giovanni Scambia
    • 1
    • 7
  • Fabio Ghezzi
    • 2
  1. 1.Department of Woman and Child HealthFondazione Policlinico Universitario A. Gemelli I.R.C.C.S.RomaItaly
  2. 2.Department of Obstetrics and GynecologyUniversity of Insubria, F. Del Ponte HospitalVareseItaly
  3. 3.Institute of Applied Health SciencesUniversity of AberdeenAberdeenUK
  4. 4.Radiology Unit, Department of Surgical and Morphological SciencesUniversity of InsubriaVareseItaly
  5. 5.Department of SurgeryGallarate HospitalGallarateItaly
  6. 6.Division for Endocrine and Minimally Invasive Surgery, Department of Human Pathology in Adulthood and Childhood “G. Barresi”University Hospital “G. Martino”, University of MessinaMessinaItaly
  7. 7.Università Cattolica del Sacro CuoreRomaItaly

Personalised recommendations