The Long Term Follow-Up Results of the Direct Nipple Ureteroneocystostomy Technique: A Prospective Study

doi:10.4236/oju.2013.34033

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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

Email: #[email protected]

Received May 26, 2013; revised June 27, 2013; accepted July 5, 2013

cense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

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

different etiologies.

Keywords: Megaureter; Nipple; Technique; Ureter; Vesicoureteral Reflux

1. Introduction

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 [1].

POM is occurs 3/12 to 5 times more often in males [2].

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 [5]. 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 [6]. 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.

#Corresponding author.

A. DEMIRTAS ET AL.

180

the view that this will reduce inflammation and tissue

edema [7].

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 [2]. In this study we evaluated the long term

follow-up results of the direct nipple ureteroneocysto-

stomy technique.

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

[8]. 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 [9].

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-

12].

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-

tically significant.

3. Results

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

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

(Figure 1(C)).

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-

pared.

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.

4. Discussion

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 [13].

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% [14]. Stenosis and obstruction in this study were

attributed to intraoperative damage to branches of the

inferior vesical artery and hypogastric artery supplying

A. DEMIRTAS ET AL.

182

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 [4].

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% [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 [15].

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 [16].

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

[17]. 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 [18].

Al-Shukri and Alwan repaired 1 14 of 560 ureters with

bilharziasis-induced stenosis with the nipple ureterıo-

neocystostomy technique [13]. 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

[15].

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 [14]. 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 [2].

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 [19]. 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

[20].

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 [21]. 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-

tively [22].

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 [23]. 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 [24].

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 [1]. 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 [8]. 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 [25].

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

preoperative period.

5. Conclusion

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

may be cause to prefer the direct nipple ureteroneo-

cystostomy technique.

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