Published online August 1, 2006
PEDIATRICS Vol. 118 No. 2 August 2006, pp. 698-703 (doi:10.1542/peds.2006-0178)
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ARTICLE

Treatment of Vesicoureteral Reflux Using Endoscopic Injection of Nonanimal Stabilized Hyaluronic Acid/Dextranomer Gel: Initial Experience in Pediatric Patients by a Single Surgeon

Richard N. Yu, MD, PhDa and David R. Roth, MDa,b

a Scott Department of Urology, Baylor College of Medicine, Houston, Texas
b Department of Pediatric Urology, Texas Children’s Hospital, Houston, Texas


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. Endoscopic injection of nonanimal stabilized hyaluronic acid/dextranomer gel is an increasingly recognized treatment option for vesicoureteral reflux. The procedure is minor compared with open surgery and, when successful, avoids the need for long-term antibiotic prophylaxis. We present data from our first 18 months using nonanimal stabilized hyaluronic acid/dextranomer gel to treat children with vesicoureteral reflux.

PATIENTS AND METHODS. Pediatric patients aged ≤15 years with uncomplicated primary vesicoureteral reflux were recruited for endoscopic treatment with nonanimal stabilized hyaluronic acid/dextranomer gel. A follow-up voiding cystourethrogram was scheduled at ≥2 weeks after treatment, and vesicoureteral reflux resolution was defined as grade 0. Repeat nonanimal stabilized hyaluronic acid/dextranomer gel treatment was offered to patients with persistent vesicoureteral reflux.

RESULTS. Of 120 patients treated, 6 were lost to follow-up, and 7 were yet to undergo posttreatment voiding cystourethrogram. The 107 remaining patients (efficacy population) had a mean age of 4.1 years (range: 0.5–15.0), and the median reflux grade was 2 (range: 1–5). The mean time to follow-up voiding cystourethrogram was 9.7 weeks (range: 2–26). Vesicoureteral reflux was resolved in 82.2% of patients and 86.9% of ureters after initial endoscopic treatment with nonanimal stabilized hyaluronic acid/dextranomer gel. The overall reflux resolution rate for patients increased to 90.7% after a second treatment in 14 patients. Two patients reported postoperative flank pain, although this was mild and transient in nature. No other adverse events were reported. No patients underwent open surgery for vesicoureteral reflux.

CONCLUSIONS. Endoscopic treatment with nonanimal stabilized hyaluronic acid/dextranomer gel is effective in a high proportion of children with vesicoureteral reflux and, in our opinion, may be considered as a first-line treatment option.

Key Words: NASHA/Dx gel • vesicoureteral reflux • endoscopic injection • pediatric • ureter

Abbreviations: VUR—vesicoureteral reflux • UTI—urinary tract infection • FDA—U.S. Food and Drug Administration • NASHA/Dx—nonanimal stabilized hyaluronic acid/dextranomer • VCUG—voiding cystourethrogram • STING—subureteric transurethral injection • HIT—hydrodistention-implantation technique

Vesicoureteral reflux (VUR) is the most common abnormality of the urinary tract in children, affecting ~1% of all children.1,2 The condition is characterized by backflow of urine from the bladder toward the kidney, increasing the risk of infection of the upper urinary tract, renal scarring, and, in the long-term, kidney damage and hypertension.2–5 In the United States, in accordance with the 1997 American Urological Association guidelines, the majority of VUR patients are managed using either antibiotic prophylaxis or ureteral reimplantation. Although effective in the treatment of symptomatic urinary tract infection (UTI) and widely used as a prophylactic agent in children with VUR, antibiotics are not approved by the U.S. Food and Drug Administration (FDA) for that indication. Moreover, this approach requires compliance with long-term medication, potentially encourages antibiotic resistance, and does not cure the condition.6 Ureteral reimplantation offers a high chance of curing VUR, but it is an invasive surgical procedure that requires hospitalization and carries a risk of significant complications.7,8 A third treatment option, endoscopic injection, was pioneered >20 years ago.9,10 This option was not included in the American Urological Association guidelines, because no injectable agent was approved by the FDA in 1997. Four years later, nonanimal stabilized hyaluronic acid/dextranomer (NASHA/Dx) gel (Deflux, Q-Med AB, Uppsala, Sweden) became the first material approved by the FDA for endoscopic injection in children with VUR (grades II–IV). It is composed of cross-linked dextranomer microspheres (80–250 µm in diameter) suspended in a 1% carrier gel of nonanimal stabilized hyaluronic acid. NASHA/Dx gel is a biodegradable material that does not migrate from the injection site to distant organs.11,12 Furthermore, it does not have immunogenic properties or the potential to cause malignant transformation.13 Long-term experience has indicated a lack of any chronic ill effects from treating children with NASHA/Dx gel.14,15

Endoscopic injection is generally performed as an outpatient procedure, sparing young patients the trauma of major surgery and hospitalization. It is quick to perform (~15 minutes), and no incision is required. Moreover, cure rates approaching those with open surgery have been reported recently, particularly with a newly developed injection procedure.16,17

Few US urologists have reported their initial experience of endoscopically injecting NASHA/Dx gel for VUR. In this article, we report the efficacy and safety outcomes for all of the patients treated with NASHA/Dx gel during our first 18 months of administering this treatment.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Children aged ≥15 years with a diagnosis of uncomplicated, primary grade I–V VUR (unilateral or bilateral) were recruited for this open study. VUR was diagnosed by voiding cystourethrogram (VCUG), and all of the patients were presented with the after management options: (1) antibiotic prophylaxis, (2) ureteral reimplantation, or (3) subureteric injection of NASHA/Dx gel. Parental choice determined the subsequent treatment of the VUR. Exclusion criteria for subureteric injection included neurogenic bladder, Hutch diverticulum, bladder exstrophy, double ureters, previous history of surgical or endoscopic treatment of VUR, and concurrent serious illness. For patients with bilateral reflux or a history of reflux, both renal units were treated. Also, contralateral nonrefluxing ureters with anatomic abnormalities (cephalad ectopia) or a previous history of previous reflux were injected, which is consistent with our indications for contralateral reimplantation in nonrefluxing ureters.

The study was performed in accordance with the Declaration of Helsinki and was approved by the Institutional Review Board of Baylor College of Medicine for retrospective review of the patients’ charts. Signed informed consent was obtained from the parents or guardians of all of the patients.

Patients were treated between June 2, 2003, and January 18, 2005. Treatment was administered in accordance with either the subureteric transurethral injection (STING) procedure10 or the hydrodistention-implantation technique (HIT),17 depending on intraoperative findings. For the STING procedure, patients received general anesthesia and were placed in the lithotomy position. A 9.5 Fr Storz cystoscope (Richard Wolf GmbH, Knittlingen, Germany) was used to facilitate the injection of NASHA/Dx gel via a prefilled syringe (standard low-pressure type) and needle (3.7 Fr, 21 gauge, with a 23-gauge tip) as supplied by Q-Med AB. The needle was inserted tangentially to a depth of 4 to 5 mm, just below the ureteral orifice (6 o’clock position), for injection until creation of a prominent bulge. The distal ureter and the ureteral orifice were uplifted, increasing the submucosal length of the ureter. The HIT was performed similarly to the STING but with the following changes. NASHA/Dx gel was injected into the distal ureteral submucosa (6 o’clock position). Pressurized irrigation (hydrodistention) of the ureter was used to facilitate correct positioning of the needle. Hydrodistention was stopped and the needle inserted to a depth of 4 mm. NASHA/Dx gel was then injected until complete coaptation of the ureter was achieved (Fig 1) (in case of inadequate coaptation, a standard STING injection was performed additionally). Initially, for the first few cases, the STING injection procedure was used exclusively. Subsequently, a combination of STING and HIT injection techniques were used for the majority of patients, based on anatomic findings at the time of surgery and the process of the injection.


Figure 1
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  		FIGURE 2 Ureteral outcomes after the first NASHA/Dx gel treatment procedure, stratified according to baseline reflux grade. Resolved indicates VUR grade 0 at the last VCUG; worsened, VUR grade at the last VCUG worse than baseline.

 
Preoperative prophylactic cefazolin (30 mg/kg per dose) was administered within 30 minutes of procedure initiation. Sulfamethoxazole (200 mg) and trimethoprim (40 mg per 5 mL), at 2 mg of trimethoprim per kilogram per dose daily, or nitrofurantoin 1 to 2 mg/kg per day, as a single daily dose, were used for postoperative antibiotic prophylaxis until a postoperative cystogram confirmed reflux resolution.

To monitor treatment efficacy, children returned for a single VCUG assessment ≥2 weeks after treatment. VCUGs were conducted using a standard protocol, and resolution of reflux was defined as grade 0. In addition, patients and their parents were asked whether any adverse events had become apparent after treatment. Renal ultrasounds were performed posttreatment with no specific abnormalities noted. If patients had resolution of their reflux and no further issues with UTIs, no additional VCUG studies were performed. A follow-up renal ultrasound study was planned at 1 year postprocedure.

Repeat treatment with NASHA/Dx gel injection was offered to patients with continuing reflux (grade ≥II). This second implantation was again followed by a VCUG scheduled at any time ≥2 weeks posttreatment. Patients with reflux grade 0–I according to their last VCUG did not routinely undergo any further treatment or assessment, unless presenting with subsequent UTIs.

Data were analyzed for all of the children undergoing NASHA/Dx gel treatment. Children without VCUG results after their last NASHA/Dx gel implantation were excluded from the efficacy population. Furthermore, ureters with grade 0 reflux at baseline were excluded from the efficacy analysis. Efficacy data were stratified according to reflux grade and according to when patients presented to the operating room (the latter to assess the effect of the authors’ experience with the technique on treatment efficacy). No analysis was performed to measure the statistical significance of between-group differences.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patients and Procedures
A total of 120 children with VUR were endoscopically treated between June 2, 2003, and January 18, 2005. The female/male ratio of these patients was 4.5:1, and their mean age was 4.1 years (range: 0.5–15). Seventy-six patients had either bilateral reflux or indications in the contralateral ureter warranting NASHA/Dx gel injection, so a total of 196 ureters were initially treated. Of these, 14 were nonrefluxing ureters meeting the criteria for contralateral treatment. The mean volume of NASHA/Dx gel injected was 1 mL per ureter. After the initial treatment, 6 patients were lost to follow-up, and 7 had not yet undergone a postoperative VCUG and could not be included in the subsequent analysis. Therefore, the efficacy population consisted of 107 patients, in whom 162 refluxing ureters were treated. The baseline reflux grade of these ureters is shown in Table 1; the median reflux grade was 2.


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  		TABLE 1 Baseline Grade of Ureters Included in the Efficacy Analysis

 
Fifteen patients (14%) underwent a second endoscopic injection, because reflux did not resolve after the first treatment; 14 of these patients were included in the efficacy population, with 1 patient awaiting a repeat VCUG. At the time of repeat cystoscopy, there was either medial migration of the NASHA/DX mound or no evidence of a previous injection. During the study period, 8 patients (9.3%) who had unilateral injection of Deflux developed new contralateral reflux after endoscopic treatment. No patients underwent a third treatment, and none underwent ureteral reimplantation during the 18-month study period. Follow-up VCUGs were performed 2–26 weeks posttreatment (mean: 9.7 weeks).

Efficacy
Reflux was resolved in 88 patients (82.2%) after a single NASHA/Dx gel treatment (ie, bilaterally, reflux grade 0). After the second implantation, the number of patients free from reflux increased to 97 (90.7%). No patients required a third implantation.

When outcomes were examined by ureter instead of by patient, similar results were found, with a total of 86.9% successfully treated after the first implantation, increasing to 92.6% after the second implantation. The positive response rates for ureters, stratified according to baseline reflux grade, are shown in Fig 2 according to data from the first follow-up. A small decrease in the resolution rate is apparent as the baseline reflux grade increases from II to IV, although this trend is reversed by the 100% success rate with grade V. The ureteral resolution rate for the second NASHA/Dx gel injection was 64.3%, moderately lower than for the first treatment (Fig 3). All of the treated ureters that had an initial reflux grade of 0 remained free from reflux throughout. For the first 50 patients that we treated, the resolution rate after the first endoscopic treatment was 85.0%, a figure that changed little (83.9%) for the second 50 patients.


Figure 2
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  		FIGURE 3 Comparison of total patients and ureters successfully treated after the first and second NASHA/Dx gel implantations.

 

Figure 3
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  		FIGURE 1 (Used with permission of Q-med Scandinavia Inc and Q-med AB). A, Initial placement of injection needle into the ureter for the HIT injection. B, Location of Deflux after HIT injection.

 
Safety and Tolerability
There were no complications associated with endoscopic injection of NASHA/Dx gel in this study. Postoperative flank pain was reported in 2 patients, but this was short lived (<4 hours immediately postprocedure) and did not require any intervention. No additional adverse events were reported.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
This study has demonstrated that endoscopic injection of NASHA/Dx gel can be successfully administered to children with VUR without previous experience of the technique. Reflux was resolved in >90% of patients (reflux grade 0) at their last VCUG, after 1 to 2 treatments. Similarly, reflux was resolved in 92.6% of ureters after 1 to 2 treatments. It is notable that in 82.2% of children, a single endoscopic injection was sufficient, and none of the patients underwent open surgery during the study period. In patients not responding to the first endoscopic injection, repeat treatment proved viable, with a resolution rate of the second injection approaching two thirds.

This study provided some evidence of a reduced chance of reflux resolution among children with high-grade reflux treated with Deflux. Although a 100% resolution rate was observed in grade V reflux, it must be borne in mind that only 2 ureters of this grade were treated, so the outcome must be treated with caution. Nevertheless, the lowest grade-specific resolution rate (grade IV) was 68%, meaning the majority of patients can expect a positive outcome. The injection technique may influence the sensitivity of resolution rate to the baseline grade. Administering NASHA/Dx gel using the STING technique, the likelihood of failure has been reported previously to increase with increasing baseline reflux severity.15 However, a recent study of NASHA/Dx gel administered using the HIT indicated a lack of correlation between success rate and baseline grade.17

The results from the present study are consistent with the favorable outcomes seen in previous studies of endoscopic injection of NASHA/Dx gel. A study by Lackgren et al,15 with a mean follow-up duration of 5 years, demonstrated that 68% of patients receiving 1 to 3 endoscopic treatments were positive responders (ie, reflux grade 0–I) at their last VCUG. These data were obtained with the STING procedure. A more recent study of NASHA/Dx gel compared outcomes after a single treatment, administered using either the HIT or STING. Similarly to the present study, ureters with reflux grade I–IV were treated.17 Among patients treated with the STING procedure, 71% had reflux grade 0 ≥3 months posttreatment, compared with 89% for the HIT. A relatively short learning curve has been noted previously with subureteric injection, with lower cure rates in the first few cases.18 However, we report no such learning curve, with consistently high cure rates in all of our patients. It is unclear why in our hands there was no learning curve, but it may be related to a long history of treating children with urologic problems.

When considering the long-term efficacy of NASHA/Dx gel, the biodegradability of the substance would seem to be a major consideration. It might be expected that the volume of the implant would decrease over time, potentially affecting efficacy. When NASHA/Dx gel is injected into the submucosa, NASHA is degraded over a period of weeks. At the same time, in-growth of collagen between the dextranomer microspheres is stimulated, and a clinical study has shown that this limits volume reduction to 19% over the first 3 months posttreatment.11,18 Moreover, the volume reduction over 12 months has been shown in an animal study to be only 23%.13 As a result, injected NASHA/Dx gel is able to cure reflux for an extended period. In a long-term study, >95% of ureters that were free from reflux 3 to 12 months after treatment remained free from dilating reflux at 2 to 5 years.15 Further long-term data are needed to confirm the permanence of cure achieved with NASHA/Dx gel, but current evidence indicates that children with VCUG-demonstrated cure soon after treatment do not need routine follow-up VCUG assessment, at least in the absence of recurrent UTIs.

There were 10 ureters with grade 1 reflux injected. The indications for this treatment were presence of contralateral reflux of higher grade or the traditional clinical scenario of UTIs despite prophylactic antibiotics. Interestingly, 7.4% of the ureters with grade 1 reflux worsened after treatment. This may be because of the inherent variability of VUR that is graded by cystography.

In our study, 14 patients were injected bilaterally although they were diagnosed with grade 0 reflux unilaterally by VCUG. These injections were performed because of either the abnormal anatomic appearance of the ureteral orifice or a previous history of reflux. These ureters were not included in the efficacy analysis. Furthermore, contemporary studies demonstrate a 5% to 8% false-negative rate with VCUG,19,20 lending support to the idea of injecting abnormally appearing contralateral ureteral orifices.

Patients treated with NASHA/Dx gel in the present study experienced few complications, with only 2 patients experiencing postoperative flank pain, which was mild and transient in nature. This finding is in agreement with previous studies demonstrating that NASHA/Dx gel implantation is well tolerated.15,17,18 Such a lack of adverse events is attributable to the fundamental properties of NASHA/Dx gel: lack of potential for immunologic or autoimmune reactions, granuloma formation, DNA mutation, or migration from the injection site.11–13 Indeed, a histopathological study of NASHA/Dx gel, performed in VUR patients a mean of 3 years after NASHA/Dx gel treatment, demonstrated evidence of a minor inflammatory reaction only.14 The authors concluded that NASHA/Dx gel "remains safe and effective for VUR in children."

Endoscopic injection of NASHA/Dx gel has been proposed as first-line treatment for the majority of children with persistent VUR.21–23 Open surgery is then reserved for high-grade cases, and children not responding to ≤3 endoscopic treatment procedures. An important advantage of this approach to treatment is that many children are spared the trauma and risk of complications associated with open surgery. Indeed, 2 surveys of informed parental preference have indicated that endoscopic injection is preferred by patients over either open surgery or long-term antibiotic prophylaxis.22,24 These considerations, together with the results obtained during our first 18 months of experience, mean that we would recommend general adoption of NASHA/Dx gel as first-line treatment for children with grade II–IV VUR.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
The present study has shown that VUR may be cured by endoscopic injection of NASHA/Dx gel in a high proportion of patients. Therefore, endoscopic treatment with NASHA/Dx gel is a valuable treatment option for children with VUR and should be considered as a first-line treatment in place of antibiotic prophylaxis.


   FOOTNOTES
 
Accepted Mar 3, 2006.

Address correspondence to David R. Roth, MD, Scott Department of Urology, Baylor College of Medicine, Houston, TX 77030. E-mail: davidrr{at}bcm.tmc.edu

Financial Disclosure: Dr Roth is paid by Q-Med for services rendered for instructing urologists in Deflux injections.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics

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G. Lackgren and A. Stenberg
Endoscopic treatment of vesicoureteral reflux: current practice and the need for multifactorial assessment
Therapeutic Advances in Urology, August 1, 2009; 1(3): 131 - 141.
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