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Pediatric Endosurgery & Innovative Techniques
Volume 7, Number 1, 2003
© Mary Ann Liebert, Inc.
Downloaded by Linkoping University Library from online.liebertpub.com at 10/26/17. For personal use only.
Long-Term Follow-Up of Endoscopic Treatment of
Vesicoureteral Reflux: Three-Center Experience
BORIS CHERTIN, MD,1 ALON FRIDMANS, MD,2 CLAUDIO GRANATA, MD,3
VINCENZO JASONNI, MD,3 AMICUR FARKAS, MD, FAAP,2 and
PREM PURI, MD, MS, FRCS, FACS1
ABSTRACT
Background: We reviewed our experience with subureteral polytetrafluoroethylene (Teflon)
injection (STING) in the treatment of vesicoureteral reflux (VUR), with special emphasis on
long-term effectiveness and morbidity.
Patients and Methods: From 1984 to 2001, 1916 patients, 488 male and 1428 female (3037
refluxing ureters) with a mean age of 3.7 years (range, 3 months–15 years), were treated endoscopically with STING. Reflux was grade I in 154 (5.1%), II in 509 (16.8%), III in 1450
(47.7%), IV in 743 (24.5%), and V in 181 (6%) ureters. Primary VUR, reflux in duplex systems, and reflux secondary to neuropathic bladder were present in 2778 (91.4%), 205 (6.8%),
and 54 (1.8%) ureters, respectively. All patients were followed up for periods ranging from
1 to 18 years, with a median follow-up of 11 years.
Results: Reflux resolved in 2032 (66.9%) ureters after one injection, in 776 (25.5%) after
two, and in 111 (3.7%) after three injections. VUR improved to grade I after one or two injections in 81 (2.7%) ureters, which required no further treatment. Subureteral injection
failed to correct reflux in 37 (1.2%), which then were treated with ureteral reimplantation.
At follow-up, reflux had recurred in 41 (1.4%) ureters, and 23 of these had only grade I or
II VUR.
Conclusion: The results of this study confirm that endoscopic STING is a simple and effective outpatient procedure in the treatment of VUR. No long-term morbidity was observed
in our patients with the use of polytetrafluoroethylene during 17 years of follow-up.
P
INTRODUCTION
(VUR) is the most common urologic anomaly in children and has been
reported in 30% to 50% of those who present with a urinary tract infection.1,2 The association of VUR,
urinary tract infection, and renal damage is well-known. Reflux nephropathy is the cause of end-stage renal failure in 3% to 25% of children and 10% to 15% of adults.2 Several antireflux procedures have been
RIMARY VESICOURETERAL REFLUX
1 Children’s
Research Centre, Our Lady’s Hospital for Sick Children, University College-Dublin, Dublin, Ireland.
Urology, Shaare Zedek Medical Centre, Faculty of Health Science, Ben-Gurion University, Jerusalem,
2 Department of
Israel.
3 Department of Paediatric Surgery, Giannina Gaslini Hospital for Sick Children, Genova, Italy.
39
CHERTIN ET AL.
Downloaded by Linkoping University Library from online.liebertpub.com at 10/26/17. For personal use only.
described for the surgical correction of VUR.3 Most entail opening the bladder and performing a variety of
procedures on the ureters. These operations are effective but not free of complications, even in the best
hands.4 The introduction of endoscopic correction was a radical departure from the standard surgical intervention and observational management of VUR in this large group of patients.5,6
In 1984, Puri and O’Donnell5 reported the correction of experimentally produced VUR in eight piglets
by means of subureteral Teflon (polytetrafluoroethylene) injection (STING). Since then, endoscopic STING
has been used successfully to treat primary and secondary VUR in children.7–14 Recently, a number of other
tissue-augmenting substances have been used endoscopically for subureteral injection to correct VUR.12–14
Some of these substances, such as cross-linked bovine collagen, have short-term durability. For others, longterm follow-up is required to assess long-term effectiveness. The aim of this study was to review the more
than 18 years of experience with STING in the treatment of VUR at three large institutions, with special
reference to long-term effectiveness and morbidity.
MATERIALS AND METHODS
From 1984 to 2001, 1916 patients, 488 male and 1428 female (3037 refluxing ureters), were treated endoscopically with STING in three institutions. Of those, 1368 patients (2130 refluxing ureters) underwent
endoscopic treatment in Dublin, 288 patients (504 ureters) in Jerusalem, and 260 patients (403 ureters) in
Genoa. The mean age of the patients was 3.7 years (range, 3 months–15 years). According to the International Classification, reflux was grade I in 154 (5.1%), grade II in 509 (16.8%), grade III in 1450 (47.7%),
grade II in 743 (24.5%), and grade V in 181 (6%) ureters (Table 1). Primary VUR, reflux in duplex systems, and reflux secondary to neuropathic bladder were present in 2778 (91.4%), 205 (6.8%), and 54 (1.8%)
ureters, respectively. In all patients, STING was performed on an outpatient basis. The technique of endoscopic treatment of VUR has been previously described in detail.15 Under direct vision through a cystoscope, a 9.5F to 14F needle of a 4F Puri disposable catheter (Storz, Tuttlingen, Germany) is introduced under the bladder mucosa, 2 to 3 mm below the affected ureteral orifice, at the 6-o’clock position (Fig. 1A).
The needle is advanced about 4 to 5 mm into the lamina propria in the submucosal portion of the ureter,
and the injection is started slowly (Fig. 1B). During the injection, the needle is slowly withdrawn until a
“volcanic bulge” of the paste is seen (Fig. 1C). A correctly placed injection creates the appearance of a nipple, on the top of which is a slitlike orifice (Fig. 2). The procedure was performed by the senior authors
(P.P., A.F., V.J.) or under their personal supervision with the same technique. The indications for endoscopic treatment of VUR were the same in all institutions as those for open antireflux operations (i.e., highgrade reflux of grades III–V). Low-grade reflux was treated only if a radionuclide scan showed the presence of renal scarring or if a patient had recurrent urinary tract infection while on chemoprophylaxis.
Antibiotic prophylaxis is prescribed for 12 weeks after the procedure. Voiding cystourethrography (VCUG)
and renal ultrasonography (US) were performed in all patients 3 months after discharge. If the result was
negative, VCUG or direct radionucleide cystography was performed in most of the patients at 1 year and
3 years after STING. In 247 patients treated in Dublin between 1984 and 1990, VCUG was performed 10
years after surgery to assess the long-term durability of the Teflon implant.16 Renal and bladder US was
TABLE 1. INTERNATIO NAL REFLUX CLASSIFICATION
Grade VUR
IN
2130 URETERS
No. ureters (%)
I
II
III
IV
V
154 (5.1)
509 (16.8)
1450 (47.7)
743 (24.5)
181 (6)
VUR, vesicoureteral reflux.
40
Downloaded by Linkoping University Library from online.liebertpub.com at 10/26/17. For personal use only.
LONG-TERM FOLLOW-UP OF ENDOSCOPIC TREATMENT OF VESICOURETERAL REFLUX
FIG. 1.
Technique of endoscopic subureteral injection.
performed annually to monitor the results of this procedure closely. The appearance of the upper urinary
tract and the site and size of the subureteral polytetrafluoroethylene (PTFE) implants were assessed on US.
All patients were followed up for periods ranging from 1 to 18 years, with a median follow-up of 11 years.
RESULTS
Reflux resolved in 2032 (66.9%) ureters after one injection, in 776 (25.5%) after two, and in 111 (3.7%)
after three injections. VUR improved to grade I after one or two injections in 81 (2.7%) ureters, which required no further treatment. Subureteral injection failed to correct the reflux in 37 (1.2%), which then were
FIG. 2.
Appearance of the ureteral orifice at the completion of the subureteral injection.
41
CHERTIN ET AL.
Downloaded by Linkoping University Library from online.liebertpub.com at 10/26/17. For personal use only.
treated with ureteral reimplantation (Table 2). At follow-up, reflux had reflux recurred in 41 (1.4%) ureters,
and 23 of these had only grade I or II VUR. The remaining 18 ureters required reinjection because of either high-grade VUR or breakthrough injections. No clinically untoward effects were reported in any patients from the use of PTFE as an injectable material.
We found a positive correlation between a correct position of the Teflon implant on US and the absence
of reflux during long-term follow-up. US failed to demonstrate a Teflon implant in 21 of the 379 ureters
10 years after surgery. Six of these 21 ureters showed recurrence of high-grade reflux on VCUG and required repeated STING to correct the VUR. Thirteen ureters had lower-grade VUR and did not require any
treatment. The remaining two ureters were free of reflux.
DISCUSSION
The management of VUR in children is still controversial.3 A number of studies have prospectively compared the medical and surgical treatment of VUR.17–19 The International Reflux Study in Children (IRSC)
clearly demonstrated a high rate of spontaneous resolution (80%) in medically managed patients with undilated ureters.17 However, 75% of grade IV ureters were still refluxing after 5 years of continuous antibiotic prophylaxis. In this study, new scars or parenchymal thinning developed in 16% of children on continuous prophylaxis, and these children had breakthrough infection while on prophylaxis. Most scars
developed in children under 5 years of age, although some were older. In the American Urological Association reflux guidelines report, original patient data from several large series were analyzed.19 The study
showed a 90% resolution rate and an 80% resolution rate for grades I and II, respectively, at 5 years regardless of the age at diagnosis or whether VUR was unilateral or bilateral. In contrast, in children with bilateral grade III VUR diagnosed at 6 years of age or later, the resolution rate was only 10% at 5 years, compared with 60% if the VUR was diagnosed before the age of 1 year. For those with grade IV VUR, the
resolution rate was 45% in cases of unilateral VUR, but less than 10% in cases of bilateral VUR. Questions often asked in relation to these patients include how long they should be followed, and whether they
should have antireflux surgery or embark on a lifetime of chemoprophylaxis.
Our long-term follow-up clearly demonstrates that STING is a simple outpatient procedure that is effective in correcting all grades of VUR. Children return to full activity on the day of the operation, and the
procedure is well tolerated. No clinically untoward effects were reported in any patients as a result of the
use of Teflon as an injectable material during long-term follow-up. The only significant complication of
this procedure was the failure to abolish reflux with the initial injection. In the present series, 67% of ureters
were cured of VUR with a single injection of Teflon, and 33% required more than one injection. In most
of the ureters, 0.03 to 0.1 mL of Teflon paste was required to correct VUR. No discrepancy in results was
found between the three institutions. However, the success rate in patients with high-grade VUR (grade IV
or V) was higher in the Dublin group than in patients in the other two institutions (99% vs. 80%2 and 71%3 ,
respectively). The success or failure of the procedure depends on the accuracy of the injection technique.
When proper attention is paid to the technical details and the lamina propria is injected with pinpoint accuracy, less Teflon paste is needed to correct the reflux. In cases of high-grade reflux, the injection is car-
TABLE 2. RESULTS
OF
SUBURETERAL TEFLON (POLYTETRA FLUOROETHYLENE )
INJECTION IN 3037 U RETERS
Results
No. ureters (%)
Cessation of VUR after single injection
Cessation of VUR after two injections
Cessation of VUR after three injections
Reflux converted to grades I and II
Failure to correct VUR
VUR, vesicoureteral reflux.
42
2032
776
111
81
37
(66.9)
(25.5)
(3.7)
(2.7)
(1.2)
LONG-TERM FOLLOW-UP OF ENDOSCOPIC TREATMENT OF VESICOURETERAL REFLUX
Downloaded by Linkoping University Library from online.liebertpub.com at 10/26/17. For personal use only.
ried out by inserting the needle into the orifice of the affected ureter to increase the length of the intravesical ureter and create a slitlike orifice.
The preceding data clearly show the long-term effectiveness of STING in the management of VUR. The
data support the long-term results published by other investigators.20,21 At follow-up, reflux had recurred
in only 41 (1.4%) of the treated ureters. Most ureters (23) had only grade I or II VUR. Only 18 ureters required reinjection because of either high-grade VUR or breakthrough injections. The remaining patients
with lower-grade reflux are free of urinary tract infection and do not require any treatment.
PTFE is a widely used surgical biomaterial.22,23 PTFE paste is a suspension of biologically inert PTFE
particles in glycerine. The glycerine is 50% of the paste by weight. Following injection, the glycerine is
absorbed into the tissues, and the PTFE implant achieves a firm consistency, retaining its shape and position at the injection site, and is encapsulated by thin fibrous tissue. PTFE paste has been used in clinical
medicine for nearly 40 years with little morbidity.22,23 It has been used to treat dysphonia since 1962, in
the periurethral region to treat urinary incontinence since 1964, and in the subureteral region to treat VUR
since 1984. No significant complications of the endoscopic treatment of VUR with PTFE paste have been
reported during the past 18 years.16,20,21
Most urologists acknowledge the success of STING, a 15-minute outpatient endoscopic procedure performed to correct reflux. However, some have been concerned about the use of PTFE paste as the implanted
substance because the distant migration of PTFE particles after periurethral, periureteral, and intravenous
injection has been reported in animal studies.24,25 Distant particle migration has been reported more often
with solid plastic implants, such as breast prostheses, artificial sphincters, hemodialysis tubing, and even
intravenous line tubing, than with injectable biomaterials.22,23 Miyakita and Puri26 performed a detailed experimental study in two animal species to determine whether PTFE particles migrate to the lungs and brain
after subureteral injections of PTFE paste.26 They showed that the subureteral injection of PTFE paste in
minimal doses that are accurately placed in the subureteral region is not associated with the distant migration of particles. In another study, Miyakita and colleagues27 injected PTFE paste intravascularly in dogs
to investigate its effects on brain parenchyma. After intravenous injection, they found no evidence of the
migration of PTFE to the brain. Small quantities of PTFE injected into the carotid arteries were associated
with a local foreign body reaction, but no brain parenchymal damage was found.
In recent years, a number of other tissue-augmenting substances have been used endoscopically for subureteral injection to correct VUR.12,13 Cross-linked bovine collagen has been used as an injectable material for the endoscopic treatment of VUR. Initially, collagen appeared promising for the correction of lowgrade reflux in short-term studies. However, long-term studies have shown that collagen is not an ideal
tissue-augmenting substance. It has a documented tendency to disappear with time, resulting in a recurrence
of reflux.28 Recently, polydimethylsiloxane and dextranomer in sodium hyaluronan (Deflux) was used in
the endoscopic correction of reflux. Long-term follow-up is required to confirm the long-term safety and
efficacy of polydimethylsiloxane for the treatment of VUR. The Uppsala group has reported the results of
long-term follow-up of children treated with dextranomer/hyaluronic acid copolymer (Deflux). A total of
228 patients (334 ureters) received endoscopic treatment.29 Two hundred twenty-one patients were followed
for 2 to 7.5 years (mean, 5 years). VCUG was performed at 3 and 12 months after the injections. The cure
rate was 75% in grades III and IV VUR, and 10% of the ureters showed grade I or II reflux after Deflux
injection. A recurrence rate of 10% was reported in 101 ureters at 1-year follow-up. In 45 ureters, late
VCUG was performed 2 to 5 years (median, 3 years) after treatment. Reflux developed in six (13%) of the
ureters. Four ureters showed grade II VUR, and the remaining two grade III and grade IV VUR, respectively. This material would seem to be a promising alternative to Teflon, showing a high cure rate and favorable safety profile. However, the long-term efficacy of this tissue-augmenting material should be demonstrated and supported by multiple clinical trials and long-term follow-up.
CONCLUSIONS
The long-term results of this series confirm that endoscopic STING is an effective procedure for all grades
of VUR. This procedure did not cause any clinically untoward effects during 18 years of follow-up.
43
CHERTIN ET AL.
REFERENCES
1. Report of the International Reflux Study in Children. Medical versus surgical treatment of primary vesicoureteral
reflux: Report of the International Reflux Study Committee. Pediatrics 1981;67:392–400.
2. Bailey RR, Maling TMJ, Swainson CP. Vesicoureteric reflux and reflux nephropathy. In: Schrier RW, Gottschalk
CW (eds). Diseases of the Kidney, 5th ed. Boston: Little, Brown and Company, 1993, pp 689–727.
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4. Mouriquand PDE. Surgical treatment of vesicoureteric reflux. In: Spitz L, Coran AG (eds). Rob & Smith’s Operative Surgery: Paediatric Surgery. London: Butterworth-Weinemann, 1995, pp 638–642.
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reflux. Urol Clin North Am 1999;26:81–94.
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Paediatric Surgery. London: Butterworth-Weinemann, 1995, pp 638–642.
16. Chertin B, Colhoun E, Murugesh V, Puri P. Endoscopic treatment of vesicoureteral reflux. An eleven- to seventeen-years follow-up. J Urol 2002;167:1443–1446.
17. Birmingham Reflux Study Group. Prospective trial of operative versus nonoperative treatment of severe vesicoureteric reflux in children: Five years’ observations. Br Med J 1987;295:237–241.
18. Tamminen-Mobius T, Burnier E, Ebel KD, et al. Cessation of vesicoureteral reflux for 5 years in infants and children allocated to medical treatment. J Urol 1992;148:1662–1666.
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21. Chaffange P, Dubois R, Bouhafas A, Valmalle AF, Dodat H. Endoscopic treatment of vesicorenal reflux in children: Short- and long-term results of polytetrafluoroethylene (Teflon) injections. Prog Urol 2001;11:546–551.
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LONG-TERM FOLLOW-UP OF ENDOSCOPIC TREATMENT OF VESICOURETERAL REFLUX
25. Aaronson IA, Rames RA, Greene WB, Walsh LG, Hasal UA, Garen PD. Endoscopic treatment of reflux: Migration of Teflon to the lungs and brain. Eur Urol 1993;23:394–396.
26. Miyakita H, Puri P. Particles found in lung and brain following subureteral injection of polytetrafluoroethylene
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28. Haferkamp A, Contractor H, Möhring K, Staehler G, Dörsam J. Failure of subureteral bovine collagen injection
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29. Läckgren G, Wählin N, Sköldenberg E, Stenberg A. Long-term follow-up of children treated with dextranomer/hyaluronic acid copolymer for vesicoureteral reflux. J Urol 2001;166:1887–1892.
Address reprint requests to:
Professor Prem Puri, MS, FRCS, FRCS(ed), FACS
Director of Research
Children’s Research Centre
Our Lady’s Hospital for Sick Children
Dublin
Ireland
E-mail: ppuri@crumlin.ucd.ie
45
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