Skip to main content

Ureteral endometriosis in patients with deep infiltrating endometriosis: characteristics and management from a single-center retrospective study

Archives of Gynecology and Obstetrics volume 300, pages 967–973 (2019)Cite this article

Abstract

Purpose

As a serious type of deep infiltrating endometriosis (DIE), ureteral endometriosis (UE) can result in decreased kidney function. The aims of this study are to investigate risk factors and surgical treatments for UE.

Methods

The study enrolled 329 patients with deep infiltrating endometriosis, who were treated with laparoscopic surgery between January 2014 to September 2018. All patients were divided into one of two groups: UE or non-UE. Clinical information and other surgery variables of the two groups were examined.

Result

Out of 329 patients with DIE, 68 (20.67%) cases of UE were diagnosed. Among them, 37 patients also had hydroureteronephrosis. In a multivariate analysis, the variables revised American Fertility Society (rAFS) stage IV, uterosacral ligament (USL) DIE lesion ≥ 3 cm in diameter and previous surgery for endometriosis significantly increased the risk of UE. A total of 27.03% (10/37) of patients with UE and hydroureteronephrosis showed decreased kidney function. Ureterolysis was performed in 59 patients, and an ureteroneocystostomy was performed in 9 patients. A double-J stent was placed in 37 patients with UE. Only 1 patient developed acute pyelonephritis postoperatively. During more than 2 years of follow-up, no patient experienced recurrence.

Conclusions

The variables of rAFS stage IV, USL DIE lesion ≥ 3 cm in diameter and previous surgery for endometriosis significantly increased the risk of UE. Laparoscopic ureterolysis and ureteroneocystostomy are feasible and safe procedures with low complication and recurrence rates.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

References

  1. Vercellini P, Vigano P, Somigliana E, Fedele L (2014) Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol 10(5):261–275. https://doi.org/10.1038/nrendo.2013.255

    CAS  Article  PubMed  Google Scholar 

  2. Cornillie FJ, Oosterlynck DJ, Lauweryns JM, Koninckx PR (1990) Deeply infiltrating pelvic endometriosis: histology and clinical significance. Fertil Steril 53(6):978–983. https://doi.org/10.1016/S0015-0282(16)53570-5

    CAS  Article  PubMed  Google Scholar 

  3. Koninckx PR, Martin DC (1992) Deep endometriosis: a consequence of infiltration or retraction or possibly adenomyosis externa? Fertil Steril 58(5):924–928. https://doi.org/10.1016/S0015-0282(16)55436-3

    CAS  Article  PubMed  Google Scholar 

  4. Lee HJ, Lee YS (2017) Deep infiltrating ureteral endometriosis with catamenial hydroureteronephrosis: a case report. J Med Case Rep 11(1):346. https://doi.org/10.1186/s13256-017-1518-6

    Article  PubMed  PubMed Central  Google Scholar 

  5. Campagnacci R, Perretta S, Guerrieri M, Paganini AM, De Sanctis A, Ciavattini A, Lezoche E (2005) Laparoscopic colorectal resection for endometriosis. Surg Endosc Other Interv Tech 19(5):662–664. https://doi.org/10.1007/s00464-004-8710-7

    CAS  Article  Google Scholar 

  6. Ruffo G, Scopelliti F, Manzoni A et al (2014) Long-term outcome after laparoscopic bowel resections for deep infiltrating endometriosis: a single-center experience after 900 cases. BioMed Res Int 2014:463058. https://doi.org/10.1155/2014/463058

    Article  PubMed  PubMed Central  Google Scholar 

  7. Comiter CV (2002) Endometriosis of the urinary tract. Urol Clin N Am 29(3):625–635. https://doi.org/10.1016/S0094-0143(02)00065-4

    Article  Google Scholar 

  8. Berlanda N, Vercellini P, Carmignani L, Aimi G, Amicarelli F, Fedele L (2009) Ureteral and vesical endometriosis. Two different clinical entities sharing the same pathogenesis. Obstet Gynecol Surv 64(12):830–842. https://doi.org/10.1097/OGX.0b013e3181c4bc3a

    Article  PubMed  Google Scholar 

  9. Antonelli A, Simeone C, Zani D, Sacconi T, Minini G, Canossi E, Cunico SC (2006) Clinical aspects and surgical treatment of urinary tract endometriosis: our experience with 31 cases. Eur Urol 49(6):1093–1098. https://doi.org/10.1016/j.eururo.2006.03.037

    Article  PubMed  Google Scholar 

  10. Abrao MS, Dias JA, Bellelis P, Podgaec S, Bautzer CR, Gromatsky C (2009) Endometriosis of the ureter and bladder are not associated diseases. Fertil Steril 91(5):1662–1667. https://doi.org/10.1016/j.fertnstert.2008.02.143

    Article  PubMed  Google Scholar 

  11. Frego E, Antonelli A, Tralce L, Micheli E, Cunico SC (2002) Ureteral endometriosis: urological features. Arch Ital Urol Androl 74(1):3–5

    PubMed  Google Scholar 

  12. Patel A, Thorpe P, Ramsay JW et al (1992) Endometriosis of the ureter BJUI 69(5):495–498. https://doi.org/10.1111/j.1464-410X.1992.tb15595.x

    CAS  Article  Google Scholar 

  13. Bosev D, Nicoll LM, Bhagan L, Lemyre M, Payne CK, Gill H, Nezhat C (2009) Laparoscopic management of ureteral endometriosis: the Stanford University Hospital experience with 96 consecutive cases. J Urol 182(6):2748–2752. https://doi.org/10.1016/j.juro.2009.08.019

    Article  PubMed  Google Scholar 

  14. Yohannes P (2003) Ureteral endometriosis. J Urol 170(1):20–25. https://doi.org/10.1097/01.ju.0000054836.32660.9e

    Article  PubMed  Google Scholar 

  15. Chapron C, Chiodo I, Leconte M, Amsellemouazana D, Chopin N, Borghese B, Dousset B (2010) Severe ureteral endometriosis: the intrinsic type is not so rare after complete surgical exeresis of deep endometriotic lesions. Fertil Steril 93(7):2115–2120. https://doi.org/10.1016/j.fertnstert.2009.01.102

    Article  PubMed  Google Scholar 

  16. Shook TE, Nyberg LM (1988) Endometriosis of the urinary tract. Urology 31(1):1–6. https://doi.org/10.1016/0090-4295(88)90560-2

    CAS  Article  PubMed  Google Scholar 

  17. Seracchioli R, Mabrouk M, Manuzzi L et al (2008) Importance of retroperitoneal ureteric evaluation in cases of deep infiltrating endometriosis. J Minim Invasive Gynecol 15(4):435–439. https://doi.org/10.1016/j.jmig.2008.03.005

    Article  PubMed  Google Scholar 

  18. Leonhartsberger N, Zelger B, Rehder P (2008) Intrinsic endometriosis of ureter and bladder in young women without gynecological symptoms. Urol Int 80(2):222–224. https://doi.org/10.1159/000112619

    Article  PubMed  Google Scholar 

  19. Alves J, Puga M, Fernandes R, Pinton A, Miranda I, Kovoor E, Wattiez A (2017) Laparoscopic management of ureteral endometriosis and hydronephrosis associated with endometriosis. J Minim Invasive Gynecol 24(3):466–472. https://doi.org/10.1016/j.jmig.2016.11.018

    Article  PubMed  Google Scholar 

  20. Andrews WC, Buttram VC, Behrman SJ et al (1985) Revised American Fertility Society classification of endometriosis: 1985. Fertil Steril 43(3):351–352

    Article  Google Scholar 

  21. Knabben LM, Imboden S, Fellmann B, Nirgianakis K, Kuhn A, Mueller MD (2015) Urinary tract endometriosis in patients with deep infiltrating endometriosis: prevalence, symptoms, management, and proposal for a new clinical classification. Fertil Steril 103(1):147–152. https://doi.org/10.1016/j.fertnstert.2014.09.028

    Article  PubMed  Google Scholar 

  22. Cavacogomes J, Martinho M, Gilabertaguilar J, Gilabertestelles J (2017) Laparoscopic management of ureteral endometriosis: a systematic review. Eur J Obstet Gynecol Reprod Biol 210:94–101. https://doi.org/10.1016/j.ejogrb.2016.12.011

    CAS  Article  Google Scholar 

  23. Huang J, Guo H, Li J, Chen S (2017) Management of ureteral endometriosis with hydronephrosis: Experience from a tertiary medical center. J Obstet Gynaecol Res 43(10):1555–1562. https://doi.org/10.1111/jog.13422

    Article  PubMed  Google Scholar 

  24. Stepniewska A, Grosso G, Molon A et al (2011) Ureteral endometriosis: clinical and radiological follow-up after laparoscopic ureterocystoneostomy. Hum Reprod 26(1):112–116. https://doi.org/10.1093/humrep/deq293

    Article  PubMed  Google Scholar 

  25. Husby GK, Haugen RS, Moen MH (2003) Diagnostic delay in women with pain and endometriosis. Acta Obstet Gynecol Scand 82(7):649–653. https://doi.org/10.1034/j.1600-0412.2003.00168.x

    Article  PubMed  Google Scholar 

  26. Hadfield RM, Mardon HJ, Barlow DH, Kennedy S (1996) Delay in the diagnosis of endometriosis: a survey of women from the USA and the UK. Hum Reprod 11(4):878–880. https://doi.org/10.1093/oxfordjournals.humrep.a019270

    CAS  Article  PubMed  Google Scholar 

  27. Kondo W, Branco AW, Trippia CH, Ribeiro R, Zomer MT (2013) Retrocervical deep infiltrating endometriotic lesions larger than thirty millimeters are associated with an increased rate of ureteral involvement. J Minim Invasive Gynecol 20(1):100–103. https://doi.org/10.1016/j.jmig.2012.09.012

    Article  PubMed  Google Scholar 

  28. Kinkel K, Chapron C, Balleyguier C, Fritel X, Dubuisson J, Moreau J (1999) Magnetic resonance imaging characteristics of deep endometriosis. Hum Reprod 14(4):1080–1086. https://doi.org/10.1093/humrep/14.4.1080

    CAS  Article  PubMed  Google Scholar 

  29. Bazot M, Lafont C, Rouzier R, Roseau G, Thomassinnaggara I, Darai E (2009) Diagnostic accuracy of physical examination, transvaginal sonography, rectal endoscopic sonography, and magnetic resonance imaging to diagnose deep infiltrating endometriosis. Fertil Steril 92(6):1825–1833. https://doi.org/10.1016/j.fertnstert.2008.09.005

    Article  PubMed  Google Scholar 

  30. Chamie L, Blasbalg R, Goncalves MO, Carvalho FM, Abrao MS, De Oliveira IR (2009) Accuracy of magnetic resonance imaging for diagnosis and preoperative assessment of deeply infiltrating endometriosis. Int J Gynecol Obstet 106(3):198–201. https://doi.org/10.1016/j.ijgo.2009.04.013

    Article  Google Scholar 

  31. Rozsnyai F, Roman H, Resch B et al (2011) Outcomes of surgical management of deep infiltrating endometriosis of the ureter and urinary bladder. J Soc Laparoendosc Surg 15(4):439–447. https://doi.org/10.4293/108680811X13176785203798

    Article  Google Scholar 

  32. Maccagnano C, Pellucchi F, Rocchini L et al (2013) Ureteral endometriosis: proposal for a diagnostic and therapeutic algorithm with a review of the literature. Urol Int 91(1):1–9. https://doi.org/10.1159/000345140

    Article  PubMed  Google Scholar 

  33. Uccella S, Cromi A, Casarin J, Bogani G, Pinelli C, Serati M, Ghezzi F (2014) Laparoscopy for ureteral endometriosis: surgical details, long-term follow-up, and fertility outcomes. Fertil Steril 102(1):160–166. https://doi.org/10.1016/j.fertnstert.2014.03.055

    Article  PubMed  Google Scholar 

  34. Buttice S, Lagana AS, Mucciardi G et al (2016) Different patterns of pelvic ureteral endometriosis What is the best treatment? Results of a retrospective analysis. Arch Ital Urol Androl 88(4):266–269. https://doi.org/10.4081/aiua.2016.4.266

    Article  PubMed  Google Scholar 

  35. Seracchioli R, Mabrouk M, Montanari G, Manuzzi L, Concetti S, Venturoli S (2010) Conservative laparoscopic management of urinary tract endometriosis (UTE): surgical outcome and long-term follow-up. Fertil Steril 94(3):856–861. https://doi.org/10.1016/j.fertnstert.2009.04.019

    Article  PubMed  Google Scholar 

  36. Saavalainen L, Heikinheimo O, Tiitinen A, Harkki P (2016) Deep infiltrating endometriosis affecting the urinary tract-surgical treatment and fertility outcomes in 2004–2013. Gynecol Surg 13(4):435–444. https://doi.org/10.1007/s10397-016-0958-0

    Article  PubMed  PubMed Central  Google Scholar 

  37. Yucel C, Ulker V, Kisa E, Koc G, Ilbey YO (2018) Laparoscopic transperitoneal nephrectomy in non-functioning severe hydronephrotic kidneys with or without renal stone. Cureus 10(12):e3729. https://doi.org/10.7759/cureus.3729

    Article  PubMed  PubMed Central  Google Scholar 

  38. Gulpinar MT, Akcay M, Sancak EB et al (2015) Comparison of transperitoneal laparoscopic nephrectomy outcomes in atrophic and hydronephrotic kidneys. Turk J Urol 41(4):181–184. https://doi.org/10.5152/tud.2015.97523

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Author notes

  1. Zhijun Hu and Peiquan Li are co-first authors and contributed equally to this work.

Authors and Affiliations

  1. Department of Gynecologic Oncology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, No. 145 Shandong Middle Road, Shanghai, 200000, China

    Zhijun Hu, Peiquan Li, Qing Liu, Hong Zhu, Yuxin Sun, Xuanxuan Zhao, Lei Xie & Kaijiang Liu

Authors
  1. Zhijun Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peiquan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuxin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xuanxuan Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lei Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kaijiang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZJH: protocol development, data collection and management, data analysis, manuscript writing, responsible surgeon. PQL: protocol development, data collection and management, data analysis, manuscript writing, responsible surgeon. QL: data collection, data analysis, responsible surgeon. HZ: data collection, data analysis, responsible surgeon, YXS: data collection, responsible surgeon, XXZ: data collection, responsible surgeon, LX: data collection, responsible surgeon, KJL: protocol development, data management, data analysis, manuscript editing, responsible surgeon.

Corresponding author

Correspondence to Kaijiang Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hu, Z., Li, P., Liu, Q. et al. Ureteral endometriosis in patients with deep infiltrating endometriosis: characteristics and management from a single-center retrospective study. Arch Gynecol Obstet 300, 967–973 (2019). https://doi.org/10.1007/s00404-019-05268-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-019-05268-9

Keywords

  • Ureteral endometriosis
  • Ureterolysis
  • Ureteroneocystostomy
  • Hydroureteronephrosis
  • Kidney function