Abstract
Ureteral endometriosis is characterized by the develop-
ment of deep infiltrating islets of endometrial tissue
affecting the ureter, the optimal management in such
cases being still poorly defined. Once the techniques
of laparoscopic surgery improved, this minimally in-
vasive approach has been proposed with encouraging
Results
in treating such cases. When it comes to the
types of surgical procedure which are needed in such
cases, they are chosen accordingly to the degree, extent
and localization of the endometrial tissue. This is a
literature review of the largest studies which were con-
ducted on the theme of the laparoscopic management
of ureteral endometriosis; the main analyzed param-
eters refer to the efficacy and safety of the procedure.
Keywords
ureteral endometriosis, resection, laparos-
copy.
MINIREVIEW
LAPAROSCOPIC MANAGEMENT OF URETERAL
ENDOMETRIOSIS
Nicolae BACALBASA1,2 , Irina BALESCU3, Mihaela VILCU1,2, Iulian BREZEAN1,2
1 „Carol Davila“ University of Medicine and Pharmacy, Bucharest, Romania
2 „Ion Cantacuzino“ Clinical Hospital, Bucharest, Romania
3 Ponderas Academic Hospital, Bucharest, Romania
Received 26 Aug 2019, Accepted 07 Oct 2019
https:/ /doi.org/10.31688/ABMU.2019.54.4. 17
Address for correspondence: Nicolae BACALBASA
„Carol Davila“ University of Medicine and Pharmacy, Bucharest, Romania
Email:
[email protected], Phone +40 723 540 426
Laparoscopic management of ureteral endometriosis – BACALBASA et al
732 / vol. 54, no. 4
Introduction
Defined by the presence of ectopic islands of en-
dometrial cells and stroma outside the uterine body,
endometriosis can be classified according to its depth
in superficial – invading the peritoneum, and the
ovary or deep infiltrating – invading the viscera such
as rectum, colon, urinary tract or the enteral loops
by at least 5 mm in depth. According to the depth of
invasion, the clinical signs and symptoms may range
between diffuse pelvic pain, constipation, hematuria
and complete bowel or urinary tract obstruction
1-3.
Urinary tract involvement in patients with endo-
metriosis
When it comes to the urinary tract involvement,
the most commonly affected organs are represented
by the urinary bladder, followed by ureter and kidney,
accounting for 0.3-12% of all cases diagnosed with this
pathology
4,5. Depending on the degree of invasion, ure-
teral endometriosis can be classified as extrinsic – if
the periureteral tissues or the serosa are involved – and
intrinsic, if the muscularis propria or the mucosa is
damaged
6. In cases presenting extrinsic endometriosis,
the lesions originate from the peritoneum, ovaries or
uterosacral ligaments and produce an extrinsic com-
pression of the ureter, while in intrinsic lesions, inva-
sion of the muscularis or mucosa occurs. However, it
seems that extrinsic lesions are up to four times more
frequent when compared to intrinsic lesions
7,8.
In order to rule out which are the predictive
preoperative factors regarding the depth of ureteral
invasion, Gennaro et al. conducted a study on 82
women in whom ureteral involvement due to endo-
metriosis was encountered
9. Among these cases the
authors identified 15 cases in which deep infiltrat-
ing endometriosis was present and in which ureteral
resections were needed, and 67 cases in which the
urological procedure was limited to ureterolysis. The
authors underlined the fact that the most commonly
encountered symptom was represented by the ab-
dominal pain, equally encountered between the two
groups, while other signs or symptoms, such as uri-
nary urgency, hematuria, dysuria or hydronephrosis
were significantly more common among patients pre-
senting deep infiltrating lesions
9.
As for the preoperative investigations which
might predict the presence of ureteral involvement, it
has been widely accepted that pelvic MRI, cystoscopy
and urography might give important information in re-
gard to the extent of the disease. More recently, a study
conducted by Lima et al. demonstrated that the pres-
ence of endometrial nodules at the level of the utero-
sacral ligament represents a strong predictive factor
for the association of ureteral involvement. Therefore,
they concluded that the presence of uterosacral nod-
ules measuring at least 1.75 cm on the right side and
1.95 cm on the left side represents a strong predictive
factor for the concomitance of ureteral involvement
10.
Surgical goals in patients diagnosed with uret-
eral endometriosis
Once the diagnosis of ureteral endometriosis is
established, surgery is needed in order to relieve the
ureteral obstruction, to preserve the renal function
and to prevent the development of any recurrent dis-
ease
4. In order to achieve these goals certain authors
proposed initially performing a limited procedure
such as ureterolysis; however, in a significant number
of cases, recurrent disease might be encountered after
a relatively short period of time; therefore, in such
cases resection and urinary tract reconstruction is fi-
nally the option of choice. For example, in Ghezzi’s
study which included 33 patients who were submit-
ted to laparoscopic ureterolysis, the rate of early re-
currence imposing reoperation reached 12% during
the first three months postoperatively
11. In the last
decades, once the techniques of minimally invasive
surgical approach improved, the number of cases sub-
mitted to this approach increased as well; therefore,
a higher number of such cases have benefited lately
from the advantages of the laparoscopic approach.
Studies investigating the role of laparoscopic
ureteral resection for deep infiltrating endome-
triosis
The utility of the laparoscopic approach in such
cases has been established in the last decades once
the minimally invasive approach started replacing
the conventional approach; therefore, it has been
widely accepted that the minimally invasive approach
might offer certain advantages, such as a magnifica-
tion of the view and better individualization of the
structures. In the study conducted by Chudzinski
et al and published in 2017 the authors included 17
patients presenting ureteral involvement in which
ureteral resection and reimplantation were needed
12.
Among these cases, the ureteral involvement was
known preoperatively in 82% of cases, in 23% of
them bilateral ureteral involvement being reported;
moreover 35% of cases also associated renal atrophy,
while renal function impairment was found in 23%
of cases. When it comes to the preferred approach,
the authors underlined the fact that laparotomy was
the option of choice in 41% of cases, being followed
by laparoscopy in 35% of cases and robotics in 23%
of cases; however, the rate of laparotomies decreased
from 63% before the year of 2010 to 23% after the
year of 2010. Among cases submitted to a minimally
invasive approach, there were three cases in which
Archives of the Balkan Medical Union
December 2019 / 733
conversion to open surgery was needed due to the
presence of bowel injury – in one case and due to
the presence of iatrogenic ureteral lesions – in two
cases
12. In a similar study conducted by Sconman et
al in Tel-Aviv, Israel, and which included seven pa-
tients, the authors reported the necessity to convert
from laparoscopy to laparotomy in two cases, while
in other four cases laparotomy was the option of
choice
13; interestingly, in all cases a previous history
of at least one surgical intervention for endometrio-
sis was reported. In all cases resection with ureteral
reimplantation by using a psoas hitch technique was
the preferred technique. After a mean follow-up pe-
riod of 42 +/-20 months, a single patient reported no
improvement of the symptoms
13.
The benefits of the laparoscopic approach in
patients with ureteral endometriosis were also dem-
onstrated by Miranda-Mendoza in 2012
14. The study
included 13 patients submitted to surgery in a mini-
mally invasive manner, six cases being submitted to
ureteral resections, while the remaining seven cases
being submitted to ureterolysis. The histopathologi-
cal studies of the resected specimens demonstrated
the presence of ureteral invasion in all cases in
which segmental ureteral resections were performed.
However, at that moment the rates of postoperative
complications remained high, three of the 13 cases
developing vesical-vaginal leaks. However, after a me-
dian follow-up period of 24 months all but one cases
reported a significant improvement of the symptoms,
as well as the absence of recurrent disease. In the 13
th
case the patient developed an obstructive uropathy
and an ureteroneocystostomy was performed
14.
One of the largest studies which investigated
the feasibility and safety of laparoscopic management
of ureteral endometriosis was the one conducted by
Cavaco-Gomes et al and published in 2017
2. The
study, a review which included 18 articles published
since 1997 and 700 patients demonstrated the effi-
cacy of the method and underlined the fact that ure-
teral endometriosis is a more common finding at the
level of the left ureter (being encountered in 53.6%),
followed by the right ureter (in 35.8% of cases) and
bilateral lesions in only 10.6% of cases). As for the
type of surgical procedure which was performed, it
consisted of ureterolysis alone in 579 cases and ure-
teral resection in the remaining ones; moreover, in
two cases nephrectomy was imposed by the secondary
renal atrophy, while in other 19.8% of cases concomi-
tant urinary bladder resection was also needed. Other
common resections were represented by rectovaginal
or uterosacral ones. When it comes to the short-term
outcomes, the most frequently reported complica-
tions were represented by ureteral leaks or stenosis
(in 14 cases), hemorrhagic events (in three cases),
anastomotic digestive leaks (in two cases), bowel per-
foration (in one case), bladder atony (in one case) and
vesicovaginal leak (in one case). As for the long-term
outcomes, 90.5% of cases reported the resolution or
improvement of the symptoms. The authors also un-
derlined the recurrent pattern of this pathology as
well as the fact that most often this disease is a mul-
ticentric one
2.
In a recent study conducted by Ceccaromi et al,
the authors included 160 patients submitted to total
laparoscopic ureteroneocystostomy between January
2009 and December 2016
15; in all cases surgery was
successfully ended in a minimally invasive manner,
while the histopathological studies confirmed the
presence of ureteral invasion in all cases (in 45.6%
the urinary tract involvement occurred in an extrin-
sic manner while in the remaining 54.4% of cases an
extrinsic manner being demonstrated); after resection
the authors reported the use of the psoas technique
of reconstruction in 58.7%. Moreover, concomitant
digestive tract invasion was seen in 75.6% and im-
posed performing a bowel resection. When it comes
to the short-term outcomes, the authors reported the
necessity of reoperation in 4.4% of cases; as for the
long-term outcomes, after a follow-up of six months,
15% of cases reported impaired bladder voiding. In
the meantime after a mean follow-up period of 20.5
months regression of the symptoms was seen in most
patients, only 1.2% of them requiring a ureteroneo-
cystostomy on the opposite side
15.
When it comes to the modalities of reconstruc-
tion after ureteral resections, while certain authors
prefer performing an uretero-ureteral anastomosis
whenever is possible, other authors consider that
a ureteral reimplantation in the urinary bladder
through an ureteroneocystostomy should be the op-
tion of choice due to a lower risk of complications,
such as anastomotic stenosis
14,16,17.
Moreover, in cases presenting deep infiltrating
lesions, a combined laparoscopic and cystoscopic ap-
proach might be tempted, encouraging results being
reported so far
18,19. This combined approach seems to
have the benefit of removing only the affected segment
of the detrusor muscle decreasing in this way the risk
of postoperative complications such as dysuria, polaki-
uria or bladder denervation. The procedure begins in
a laparoscopic manner by identifying and dissecting
the endometrial nodule followed by a cystoscopic step
which identifies the area of mucosal involvement
20,21.
Conclusions
Although urinary tract involvement is a com-
mon finding in patients diagnosed with endometrio-
sis, ureteral invasion is lower when compared to the
Laparoscopic management of ureteral endometriosis – BACALBASA et al
734 / vol. 54, no. 4
rates of urinary bladder invasion. Even though, when-
ever ureteral involvement is discovered, laparoscopy
seems to be a feasible method in order to achieve an
adequate alleviation of the symptoms. Depending on
the degree of invasion and on the site of invasion
multiple therapeutic strategies might be proposed,
ranging from ureterolysis to ureteral resection with
end to end anastomosis or ureteral resection followed
by ureteral reimplantation by ureteroneocystostomy.
Although initially the rates of postoperative com-
plications were considerable, once more experience
has been gained these rates of morbidity decreased.
In the meantime, the rates of recurrences seen after
a long-term follow-up seem to report a descendent
trend during the last decade.
Acknowledgements
This work was supported by the project enti-
tled „Multidisciplinary Consortium for Supporting
the Research Skills in Diagnosing, Treating
and Identifying Predictive Factors of Malignant
Gynecologic Disorders“, project number PN-III-P1-
1.2-PCCDI2017-0833.
Compliance with Ethics Requirements:
„The authors declare no conflict of interest regarding
this article“
“The authors declare that all the procedures and ex-
periments of this study respect the ethical standards in the
Helsinki Declaration of 1975, as revised in 2008(5), as
well as the national law.“
References
1. Koninckx PR, Martin DC. Deep endometriosis: a conse-
quence of infiltration or retraction or possibly adenomyosis
externa? Fertil Steril 1992; 58(5): 924-928.
2 . C a v a c o - G o m e s J , M a r t i n h o M , G i l a b e r t - A g u i l a r J ,
Gilabert-Estelles J. Laparoscopic management of ureteral en-
dometriosis: A systematic review. Eur J Obstet Gynecol Reprod
Biol 2017; 210: 94-101.
3. Fritz MA, Speroff L. Clinical Gynecologic Endocrinology
and Infertility. 8 ed. Philadelphia: Lippincott Williams &
Wilkins; 2011. p. 1221–1223.
4. Maccagnano C, Pellucchi F, Rocchini L et al. Ureteral en-
dometriosis: proposal for a diagnostic and therapeutic algo-
rithm with a review of the literature. Urol Int 2013; 91(1): 1-9.
5 . Sillou S, P oiree S, Millischer AE, Chapron C, Helenon
O. Urinary endometriosis: MR imaging appearance with
surgical and histological correlations. Diagn Interv Imaging
2015;96(4):373-381.
6. Yohannes P. Ureteral endometriosis. J Urol 2003;170(1):
20-25.
7. Bulkley GJ, Carrow LA, Estensen RD. Endometriosis of the
ureter. J Urol 1965;93: 139-143.
8. Fujita K. Endometriosis of the ureter. J Urol 1976;116(5):664.
9. Gennaro KH, Gordetsky J, Rais-Bahrami S, Selph JP.
Ureteral endometriosis: preoperative risk factors predicting
extensive urologic surgical intervention. Urology 2017;100:
228-233.
1 0 . Lima R, Abdalla-Ribeiro H, N icola AL, Eras A, Lobao
A, Ribeiro PA. Endometriosis on the uterosacral liga-
ment: a marker of ureteral involvement. Fertil Steril
2017;107(6):1348-1354.
11. Ghezzi F, Cromi A, Bergamini V, Serati M, Sacco A, Mueller
MD. Outcome of laparoscopic ureterolysis for ureteral endo-
metriosis. Fertil Steril 2006;86(2):418-422.
1 2 . C h u d z i n s k i A , C o l l i n e t P , F l a m a n d V , R u b o d C .
Ureterovesical reimplantation for ureteral deep infiltrating
endometriosis: A retrospective study . J Gynecol Obstet Hum
Reprod 2017;46(3):229-233.
13. Schonman R, Dotan Z, Weintraub AY, et al. Long-term fol-
low-up after ureteral reimplantation in patients with severe
deep infiltrating endometriosis. Eur J Obstet Gynecol Reprod
Biol 2013;171(1):146-149.
14. Miranda-Mendoza I, Kovoor E, Nassif J, Ferreira H, Wattiez
A. Laparoscopic surgery for severe ureteric endometriosis.
Eur J Obstet Gynecol Reprod Biol 2012;165(2):275-279.
15. Ceccaroni M, Ceccarello M, Caleffi G, et al. Total laparo-
scopic ureteroneocystostomy for ureteral endometriosis: a
single-center experience of 160 consecutive patients. J Minim
Invasive Gynecol 2019; 26(1): 78-86.
16. Bratu OG, Cherciu AI, Bumbu A, et al. Retroperitoneal tu-
mors – treatment and prognosis of tumor recurrence. Rev
Chim (Bucharest) 2019;70(1):191-194.
17. Bodean O, Bratu O, Munteanu O, et al. Iatrogenic injury of
the low urinary tract in women undergoing pelvic surgical
interventions. Arch Balk Med Union 2018;53(2):281-284.
18. Tiglis M, Neagu TP, Elfara M, et al. Nefopam and its role
in modulating acute and chronic pain. Rev Chim (Bucharest)
2018;69(10):2877-2880.
19. Diaconu CC, Arsene D, Balaceanu A, Bartos D. A rare
tumor revealed by abdominal trauma: case presenta-
tion. Romanian Journal of Morphology and Embryology
2014;55(3):973-976.
20. Millochau JC, Stochino-Loi E, Defortescu G, Darwish B,
Roman H. Combined laparoscopic and cystoscopic ap-
proach in large deep infiltrating endometriosis of the blad-
der. J Gynecol Obstet Hum Reprod 2017;46(9):691-692.
21. Bodean O, Bratu OG, Bohiltea R, et al. The efficacy of syn-
thetic oral progestin pills in patients with severe endome-
triosis. Rev Chim (Bucharest) 2018;69(6):1411-1415.
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