Open Journal of Urology, 2013, 3, 179-184
http://dx.doi.org/10.4236/oju.2013.34033 Published Online August 2013 (http://www.scirp.org/journal/oju)
The Long Term Follow-Up Results of the Direct Nipple
Ureteroneocystostomy Technique: A Prospective Study*
Abdullah Demirtas#, Nurettin Sahin, Emre Can Akinsal, Mehmet Ali Ergul, Mehmet Caniklioglu,
Oguz Ekmekcioglu, Atila Tatlisen
Department of Urology, Erciyes University Medical Faculty, Kayseri, Turkey
Received May 26, 2013; revised June 27, 2013; accepted July 5, 2013
Copyright © 2013 Abdullah Demirtas et al. This is an open access article distributed under the Creative Commons Attribution Li-
cense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Objective: To evaluate the long term follow-up results of the direct nipple u reteroneocystostomy technique. Materials
and Methods: We studied a total of 16 patients (19 renal units) who underwent direct nipple ureteroneocystostomy.
The mean age was 43 years and 3 patients had bilateral disease. In five units the ureters had been ligated during
gynecological surgery, 11 renal units were obstructive and three units were reflexive megaureters. The ureters were
spatulated for about 2 cm and folded back. Nipples 2 to 2.5 cm long were prepared. In two cases the ureters were
thin-walled (2 mm or less) and they were not spatulated but folded back onto themselves. In one case the ureter could
not be everted since it had a thick and fibrotic wall. The distal 2 to 2.5 cm segment of this ureter was directly inserted in
to the bladder. Postoperative follow-up was at 3 month intervals for the first year at 6 month intervals for 2 - 3 years and
yearly thereafter. At the time of follow-up serum creatinine, urine culture, ultrasound, intravenous urography, voiding
cystoureterography, nuclear renal scintigraphy and cystometric evaluations were performed. The functions of 11 and 15
renal units were evaluated scintigraphically and stereo logically, respectively, in the both preoperative and postoperative
first year follow-up. The Wilcoxon Signed Ranks test was used for statistical evaluation and p < 0.05 was considered
statistically significant. Results: Mean follow-up was 49 months. Three renal units had Grade III reflux (two of them
during voiding) and one unit had Grade IV reflux. At follow-up this patient developed in the ureteral stricture. No
patients had urinary tract infection, pyelonephritis or ureteral stricture follow-up period. Between the preoperative and
postoperative first year, there was an increase in postoperative split renal function based on renal scintigraphy but this
difference was not statistically significant. The stereologically calculated decrease in pelvicaliceal dilatation was
statistically significant. Conclusion: Ease of application and no need to taper or plicate the ureter or prepare a sub-
mucosal tunnel may be the reasons to consider the direct nipple ureteroneocystostomy technique for megaureters of
Keywords: Megaureter; Nipple; Technique; Ureter; Vesicoureteral Reflux
Primary obstructed megaureter (POM) is a result of obs-
truction or an adynamic ureteral segment in the uret-
erovesical junction. Megaureter can be classified as 1) re-
flux megaureter obstructed megaureter; 2) nonreflux and
nonobstructed megaureter and 3) megaureter with ob-
struction and reflux .
POM is occurs 3/12 to 5 times more often in males .
Although it is generally unilateral, it may be seen bilater-
ally in 15% to 25% of cases. Besides excretory urogra-
phy (IVU), diuretic renography and antegrade pyelogra-
phy are valuable tools for its diagnosis. As treatment, the
adynamic ureteral segment is excised and ureteroneo-
cystostomy is performed with different surgical tech-
niques. However, the r esults may be far from ideal [3,4].
Ureteric injury is one of the most serious complica-
tions of gyenocologic operations in the pelvis . Uret-
eric damage has significant morbidity and can present as
ureteric stenosis or obstruction and cause variable de-
grees of impaired renal function in some cases . When
the diagnosis of injury is made postoperatively then ei-
ther open surgery or endourologic procedures can be
employed. Delayed repair has been suggested based on
*There is no financial disclosure of any of the authors.
opyright © 2013 SciRes. OJU
A. DEMIRTAS ET AL.
the view that this will reduce inflammation and tissue
The treatment of vesicoureteral reflux (VUR) is indivi-
dualized. Before recommending surgery, consideration is
given to the severity of the reflux, possible underlying
risk factors including bladder dysfunction, age at prese
closentation, and duration of the disorder. A variety of
techniques have been described for the correction of
VUR. These are anatomically categorized as extravesical,
intravesical, or combined, depending on the approach to
the ureter . In this study we evaluated the long term
follow-up results of the direct nipple ureteroneocysto-
2. Materials and Methods
A total of 16 patients (19 renal units), seven males and
nine females, with a median age of 43 years (21 - 73)
who underwent nipple ureteroneocystostomy operation
were enrolled in this study. Three cases underwent bilat-
eral repair. Eight of the 19 renal units were on the right
side and 11 were on the left side. Three of the repaired
renal units were reflux megaureter, 11 were obstructed
megaureter, and 5 were units at the lower end of the
ureter which were ligated at previous gynecologic opera-
tions. Neurogenic bladder cases and cases with surgical
wound infection were excluded. Preoperative evaluation
consisted of urine culture, serum creatinine, urinary sys-
tem ultrasonography, renal Technetium-99 m-Dimercap-
tosuccinic Acid (DMSA) scintigraphy, cystoscopy, voi-
ding cystourethrography (VCU), intravenous urography
(except for two cases), antegrade pyelograpy and Whi-
taker test (Life-Tech, Stafford, Texas) in 4 cases with
percutaneous nephrostomy, and cystometric assessment
(Life-Tech, Stafford, Texas) in 5 cases with vo iding dys-
function. Cases with proliferation in urine culture were
not operated on until after their urine became sterile and
other cases were operated on after a course of antibio-
therapy with intravenous 3rd generation cephalosporins.
In the Whitaker test, a pressure gradient above 22 cm
H2O between the renal pelvis and bladder during ad-
ministration of 10 ml isotonic saline is considered diag-
nostic for obstru ction while 15 - 22 cm H2O suggests ob-
struction, and below 15 cmH2O indicates no obstruction
. All cases were operated on under general anesthesia.
A direct nipple ureteroneocystostomy (DNU) operation
was carried out with a lower middle incision in cases
where bilateral repair was undertaken and with a Gibson
incision for the rest of the cases .
A follow-up was planned at every three months in the
first year, at every 6 months between the 1st and 3rd
years and yearly thereafter. Follow-up tests included
urine culture, serum creatinine, ultrasonography (USG),
VCU, IVU (if creatinine was normal), DMSA scintigra-
phy, endoscopy (at postoperative 3rd month), and uro-
dynamic examination in cases with dysfunctional mic-
turition. A sample of the lower ureteral end of 9 renal
units was evaluated pathologically. In cases attending
regular follow-ups, preoperative and postoperative 1st
year DMSA results and amount of pelvicaliceal dilatation
in the IVU of the unit that underwent surg ery were com-
pared statistically (by counting the dots falling on the
pelvis and calices using stereologic methods which use
transparent acetates with 3 mm inter-grid distances [10-
Inter-IVU image differences between IVUs taken at
different centers were resolved by using the value found
by counting the dots falling on the 4th lumbar vertebra in
both films and proportioning the results with each other
as the multiplier. Measurable values were expressed as
means + standard deviation. Preoperative and postopera-
tive values were compared using the Wilcoxon signed
rank test. A p value less than 0.05 was accepted as statis-
The results of a median 49 months follow-up of the 19
renal units that underwent DNU operation were assessed.
One reflexive and two obs tructive cases underwent bilat-
eral repair. While two cases with an excessively dilated
and thin-walled (2 mm or less) ureter were anastomosed
by folding back without spatulation, one case with a
ureter with an excessively thick and fibrotic wall was
directly anastomosed without being everted and spatu-
lated, with a 2 to 2.5 cm part being free in the bladder. In
one obstructive case there was a 6 cm stone at the lower
end of the ureter. As the ureter of this case undergoing
ureterolithotomy and DNU operations was so thick and
fibrotic, excessive ureter dissection was avoided to pre-
serve circulation and the bladder was attached to the
tendon of the ipsilateral psoas minor muscle by using the
Psoas hitch method. Urine cultur es of the cases were free
of proliferation. All cases underwent preoperative VCU
and no reflux was observed except for 3 units. Two cases
did not undergo IVU (one of these cases had a serum
creatinine level of 1.9 mg/dl and the other was at the
early postpartum period). The Whitaker test was applied
to 4 cases with percutaneous nephrostomy and the test
results of these 4 cases were consistent with obstruction.
The test was repeated on the 14th day after the operation
and the test results were negative. These cases also un-
derwent postoperative antegrade pyelography which re-
vealed that the contrast material readily passed to the
bladder and no obstruction existed, and their nephrosto-
mies were removed. Drains were removed on the 3rd -
5th days. Cases underwent VCU on the postoperative 14t h
day, which revealed extravasation in no patients. In most
of the cases the filling defect caused by to the nipp le was
evident in the bladder in the VCU taken postoperatively
Copyright © 2013 SciRes. OJU
A. DEMIRTAS ET AL. 181
(Figure 1(A)). Filling defects seen on the left and right
sides of the bladder belong to the nipple while that on the
base is of the balloon of the urethral catheter. Five cases
whose ureteral lower ends were bound due to previous
gynecologic operations were followed up for 8 weeks
after the operation for inflammation, edema, and suture
reabsorption if they were sutured with an absorbable su-
ture; however, these cases were taken to nipple uretero-
neocystostomy as no recovery took place. Urethral cathe-
ters of the cases were removed 14 days after VCU.
The flank pain of the patients being followed up
abated. One case attended the first month follow-up but
quit thereafter. Another case, on the other hand, was ad-
mitted for the first appointment on the postoperative 54th
day. The high preoperative creatinine level of one case
persisted during the postoperative period. Other cases
had normal creatinine levels (Normal: 0.6 - 1.3 mg/dl).
Five cases in which had a preoperative cystometry had
normal control cystometric examination and this test was
not repeated at follow-up. Four out of 19 units (21%)
were diagno sed with reflux. Wh ile 3 cases had Grade III
reflux occurring only during voiding, another case had
Grade IV reflux. While one case with voiding-associated
Grade III reflux had a preoperative Grade V reflux, other
cases had obstructive megaureters.
Two of 3 units operated on for obstructive MGU were
diagnosed with Grade III reflux during voiding whereas
one case had Grade IV reflux. The latter had a severe
stenosis in the bulbous urethra in control endsocopy and
an optic urethrotomy was perf o r med.
No case attending follow-ups had a retracted nipple in
endoscopic examinations. A 2 to 2.5 cm nipple ureter
was found to be moving freely inside the bladder and the
endoscope could easily pass to the lower end of the
ureter (Figure 1(B)).
Comparison of the preoperative and postoperative
USGs revealed that dilatations decreased in size and thus
the cases benefited from surgery but residual dilatations
persisted. Radiologists were informed that the nipple
occupies space in the bladder and resembles a soft tissue
mass and could easily be misdiagnosed as a solid mass
Among those patients who underwent preoperative
renal scintigraphy and attended regular follow-up ap-
pointments in the postoperative period, preoperative and
postoperative first year the Tc99m-DMSA renal scinti-
graphic results of 11 renal units were statistically com-
There was a postoperative increase in renal functions,
albeit statistically insignificant (Table 1). IVU showed
that the dilatations decreased, no obstructions were pre-
sent, and the pelvicaliceal structures of the units that
were observable only at the nephrogram phase of the late
films in preoperative IVU became visible. Dilatations of
the pelvis and calices of 15 renal units in the preoperative
Figure 1. (A) Fourteenth day cystographic image of the case
that underwent bilateral DNU. (B) Endoscopic appearance
of the bladder at postoperative 6th month of a case that
underwent DNU operation. (C) USG appearance of the
bladder at postoperative 6th month of a case that under-
went DNU operation. The nipple appears inside the bladder
lumen as if it were a soft tissue mass.
and postoperative 1st year IVUs were compared statisti-
cally by counting the dots on these regions. Postopera-
tively the dilatations significantly diminished (Table 2).
Samples of the lower end of the ureter of 9 units which
were excised at operation and sent for pathology were
examined and only two were diagnosed with an agangli-
onic segment. The lower end pathologies of the remain-
ing 7 units were reported as chronic inflammatory proc-
ess and fibroadipose tissue.
Many methods have been defined in megaureter surgery.
The main principle is to practice an ureteroneocysto-
stomy suitable for the antireflux technique. Absence of
reflux and obstruction, resolution of upper urinary sys-
tem dilatations, recovery or stabilization of renal func-
tions, regression or elimination of preoperative symp-
toms, a sterile urinary culture, regression or normaliza-
tion of serum urea and creatinine levels are all considered
as evidence of treatment success. It is not necessary to
fulfill all criteria for treatment success. For instance,
treatment success may be accepted to exist when the pa-
tient is asymptomatic postoperatively and the urinary
system is seen to have recovered radiologically .
The main problem is the anastomosis of excessively
dilated ureters. Hendren applied an anastomosis by
forming a submucosal tunnel after constricting and then
excising the ureter from the antimesenteric side in 169
patients and reported a reflux rate of 5% and stenosis rate
of 7% . Stenosis and obstruction in this study were
attributed to intraoperative damage to branches of the
inferior vesical artery and hypogastric artery supplying
Copyright © 2013 SciRes. OJU
A. DEMIRTAS ET AL.
Copyright © 2013 SciRes. OJU
Table 1. Comparison of preoperative and postoperative 1st year renal DMSA scintigraphies of the cases.
Preoperative (n:11) Mean + standard deviation Postoperative first year (n:11) Mean ± standard deviation P
Scintigraphy (%) 55.2 ± 26.1 55.8 ± 29.7 0.721
Table 2. Comparison of dilatations of pelvis and calices of the cases in preoperative and postoperative 1st year IVU by
stereologic grid counting method.
Preoperative (n:15) Mean ± standard dev i ation Postoperative first year (n:15) Mean ± standard deviation P
Area 353.0 ± 367.4 246.4 ± 261.1 0.003
the ureter .
An alternative option to relieve dilatation is to scale
down the distal ureteric diameter by plication. Ehrlic
applied submucosal ureteroneocystostomy after ureteric
plication in 74 ureters and repor ted an obstruction rate of
1.4% and a reflux rate of 4% . Perovic applied ureter-
oneocystostomy to 167 megaureters and performed an
anastomosis with the extravesical submucosal tunnel
technique without plicating and excising the ureter. He
reported stenosis in 2 cases and reflux in 3 patients after
a median follow-up of 2.5 years. In addition he reported
that a ratio of submucosal tunnel length/ureter diameter
of 3/1, or even 2/1 can prevent reflux. He argued that
even this ratio is high and the dilated ureteric lu men fold s
back onto itself inside the tunnel and is easily placed
between the detrusor and the mucosa .
Hill et al. formed a new cuff by folding on approxima-
tely 1 cm distal part of the ureter back onto itself and
anastomosed it to the new hiatus in 16 renal un its in dogs.
No nipple could be seen in 2 units at 3-month follow-up
while hydronephrosis developed in 4 units with no reflux.
They held that retraction and atrophy of the muscles of
cuff wall were responsible for not being able to see the
nipple. The advantages of this technique have been re-
ported as being easy and rapid use and its forming a
permanent intraluminal papilla .
Sagalowsky performed anastomosis in 46 ureters with
the split-cuff nipple technique and observed a reflux rate
of 2.4% at the early period and 5% in the postoperative
second year; however, they observed no obstruction at all
. Turner-Warvick et al. reported that the nipple they
formed can cause ischemic necrosis due to co nstriction if
not spatulated and it also leads to outside shifting of the
inner wall of the nipple since the everted part would not
fully adhere to the ureter .
Al-Shukri and Alwan repaired 1 14 of 560 ureters with
bilharziasis-induced stenosis with the nipple ureterıo-
neocystostomy technique . They reported a success
rate of 94.7% at 6 months, % at 3 years and argued that a
6-month follow-up is sufficient in the postoperative pe-
riod. The main difference between that study and our
study was the anastomosis site of the ureter. While it was
suggested in that technique that the ureter must be anas-
tomosed to a region as close to the original hiatus as pos-
sible, our technique involves an anastomosis performed
in the upper posterolateral region, as in psoas hitch tech-
nique. In our opinion, an anastomosis to this region is
more easily performed [9,13]. It has been reported that it
is very challenging to form a tunnel to the ureter without
performing constriction or excision in adult megaureters
The two main complications following megaureter re-
pair are reflux or obstruction. In some cases, on the other
hand, a temporary obstruction may be observed in the
early postoperative period. A short tunnel and excessive
lateral anastomosis of the ureter have been held respon-
sible for postoperative reflux formation . Persistent
VUR results from inability to form an insufficient tunnel
length or to provide the ureter with sufficient muscle
support. Fibrotic ureters may not be completely closed
due to intravesical pressure and cause persistent reflux.
Also, inability to identify and treat secondary causes of
reflux results in recurrences .
Lee et al. reported that increased Type III collagen in
megaureters with reflux decreases surgical success and
forms an intrinsic solid structure in the ureter . Re-
sidual ectasia in the upper urinary system may cause an
apparently high reflux grade. Scintigraphically, no new
scar formation was evident in kidneys at the side of the
operated ureters; no pyelonephritis attack developed and
the urine remained sterile during follow-up. Except for
case with a high creatinine level in the preoperative pe-
riod (preoperative: 1.9 mg/dl, postoperative: 1.9 - 2.2
mg/dl), no case developed an increase in biochemical
parameters in the postoperative period.
The phenomenon rendering vesicoureteral reflux im-
portant is that it causes parenchymal damage. Reflux can
damage the kidneys only when it is intrarenal. Hydro-
static pressure of the intrarenal reflux, the age of the pa-
tient, and whether or not the urine is infected are decisive
on the severity of the scarring in kidney parenchyma
In one study conducted by the Birmingham Reflux
Working Group both groups randomized to surgical and
conservative treatment approaches had the same kidney
scarring rate at study entry whereas subsequent follow-up
revealed that the new scarring rate was 20% in the con-
servative group and 24.1% in the surgical group and
A. DEMIRTAS ET AL. 183
while the progressive scarring rate was 10.5 % in the sur-
gical group and 11.6% in the conservative group. No
significant difference was noted between the two groups
in terms of infection rates . In the “International Re-
flux Study Group” study in which centers from America
and Europe collaborated 60% of cases had scarring at the
beginning, with subsequent new scarring rates of 14.6%
and 14.5% in surgical and conservative groups, respec-
It has been reported, and many authors agree, that
modest refluxes following megaureter surgery may re-
cover by themselves in a period of 2 - 3 months, and thus
require no therapy . As further surgery in patients
with residual reflux carries the risk of ischemia and is
technically demanding, endoscopic substance infusion is
recommended. A success rate of 80% has been reported
following a single endoscopic in jection to 20 u reters with
ongoing reflux (Grade III or above in 13 ureters) follow-
ing ureteroneocystostomy .
Obstruction, the other common co mplication, is the re-
sult of fibrosis due to deranged ureter blood supply par-
ticularly following excisional constriction or plication.
Entry of the ureteric hiatus into the bladder from an ex-
cessive cranial and lateral aspect also causes obstruction.
In such a situation a second operation is needed. Tempo-
rary obstruction seen postoperatively, on the other hand,
is the result of edema at the lower end of the ureter and
nephrostomy usually suffices. Although our sample size
was small, we did not observe obstruction or stricture
development, suggesting that a minimal trauma to the
ureter ensues. No infection or worsening of renal func-
tion due to residual urine in the pelvicaliceal system was
observed after surgery. King reported that there is no
need for constriction to repair ureter peristaltism . In
Whitaker test, a pressure gradient above 22 cm H2O be-
tween the renal pelvis an d the bladder during administra-
tion of 10 ml isotonic saline is considered diagnostic for
obstruction while 15 - 22 cm H2O suggests obstruction,
and below 15 cm H2O indicates no obstruction . In
one study it has been suggested that administration of
isotonic saline at a rate of 10 ml/min may not suffice to
show obstruction in dilated urinary systems and a rate of
12 - 20 ml/min may be more appropriate .
The nipple appears as a smooth-bordered filling defect
in the bladder in postoperative cystograms and IVUs
while it is observed as a soft tissue mass in the bladder in
USG. Endoscopically, the nipple prolapsing into the lu-
men is easily seen on the lateral superior wall of the
bladder and it is easy to advance through the ureter with
a cystoscope in the postoperative period. It has been cli-
nically and cystometrically shown that the nipple inside
the bladder does not produce symptoms of bladder irrita-
tion. None of the patients had irritative symptoms in the
As the technique is an easy-to-perform one, the learning
curve is substantially short. Unlike the previously men-
tioned techniques, this method does not need a submu-
cosal tunnel, ureteric plication, or tapering, thus shorten-
ing surgical time and anesthetic complications, and lim-
iting the frequency of major surgical complications such
as ureteral stenosis. Lack of the need for a ureteral stent
protects the patient from stent-induced irritation and an
additional endosco pic pro cedu re. A read ily seen nipple in
the bladder and easily performed endoscopy in the post-
operative period facilitates intervention. Its potential to
be performed in obstructive and reflexive megaureter
cases including ureter dilatations caused by a variety of
etiologies such as iatrog enic ureteric lower end dilatation
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