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Contrast-enhanced Voiding US for Grading of Reflux in Adult Patients Prior to Antireflux Ureteral Implantation¹

¹ From the Departments of Radiology (A.L.V., A.M.D.G., L.M.M., V.T.) and Surgery (G.N., F.C., A.M.V., C.D.), Università Cattolica del Sacro Cuore, Policlinico A. Gemelli, L.go A. Gemelli 8, 00168 Rome, Italy. Received November 12, 2003; revision requested January 21, 2004; revision received February 17; accepted March 26. Address correspondence to A.L.V. (e-mail: alvalentini@mclink.it).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To prospectively assess contrast material–enhanced voiding ultrasonography (US) for grading of vesicoureteral reflux (VUR) and to compare results with those of voiding cystourethrography (VCUG) in adult patients undergoing antireflux ureteral implantation.

MATERIALS AND METHODS: Thirty-seven consecutive adult patients who had undergone renal transplantation with Politano-Leadbetter (18 patients) or Lich-Gregoire (19 patients) technique were included on the basis of previous urinary tract infections (UTIs) and time elapsed after renal transplantation. Exclusion criterion was current UTI. US was performed by one of two sonologists with injection of saline and microbubble suspension and was recorded on videotape. Sonologists assigned VUR diagnosis in consensus after videotape review. VCUG was performed by one of two radiologists immediately after US. Radiologists were blinded to US findings and assigned VCUG diagnoses in consensus. Contingency table was used to compare US and VCUG. Agreement between US and VCUG was determined with statistics.

RESULTS: With VCUG, VUR was diagnosed in 15 patients and not diagnosed in 22 patients. US and VCUG results were in agreement in 14 patients with VUR and 21 patients without VUR. US sensitivity and specificity for detection of VUR were 93% (14 true-positive results in 15 abnormal cases) and 95% (21 true-negative results in 22 normal cases), respectively. Agreement between US and VCUG was 95% ( = 0.89, P < .001). In 11 of 14 patients, VUR grades were in agreement for US and VCUG. In three of 14 patients, US indicated a higher grade than did VCUG. VUR was diagnosed in seven of 18 Politano-Leadbetter cases and eight of 19 Lich-Gregoire cases.

CONCLUSION: A high rate of agreement was seen between voiding US and VCUG.

© RSNA, 2004

Index terms: Genitourinary system, US, 80.12983, 80.12988 • Ureter, reflux, 82.85 • Voiding cystourethrography, 80.1232, 80.1233

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Vesicoureteral reflux (VUR) is the most common urinary tract abnormality in children, with 1%–2% incidence in the general population and a higher incidence (30%–40%) in children who have repeat episodes of urinary tract infections (UTIs) (1). VUR is usually investigated by means of voiding cystourethrography (VCUG) or radionuclide cystography. Since VCUG and radionuclide cystography involve the use of radiation, contrast material–enhanced voiding ultrasonography (US) has been used in children to reduce the radiation dose (1–6). This new US technique involves the use of an echo-enhancing contrast agent that is introduced slowly into the bladder through a catheter. Diagnosis of VUR is assigned on the basis of echoes refluxing from the bladder to the ureter, renal pelvis, and calyces or when color signals are seen in the urinary tract. The associated morphologic signs (dilated or nondilated ureter, renal pelvis, and calyces) contribute to VUR assessment with the use of five grades assigned on the basis of voiding US findings (5), which makes this system comparable to the most frequently used radiographic system of VUR grading (7). In reports of studies in children, sensitivity and specificity of voiding US in the detection of VUR range from 69% to 100% and from 87% to 97%, respectively (8). In some of these studies, it is also stated that US sensitivity increases when color Doppler (5) or harmonic US (9) is used.

VUR can be found in adult patients who undergo renal transplantation. Among the several factors potentially involved in VUR development, such as graft rejection and damage to the ureteral blood supply, the surgical technique for the ureteral implantation could be included (10). The inefficiency of the ureteral implantation might be responsible for VUR. However, few investigators have studied the relationship between surgical approach (antireflux or non-antireflux techniques for ureteral implantation) and VUR incidence at VCUG (11–14). To our knowledge, only two studies to date (15,16) have involved the use of voiding US in the investigation of VUR in patients with renal transplants: One study (15) involves the simultaneous comparison of voiding US with radionuclide cystography, and the second study (16) involves the use of only cyclic voiding US. To the best of our knowledge, no study has been performed to investigate the use of voiding US versus VCUG, the latter of which has high spatial resolution and well-known assessment of VUR grade.

Thus, the purpose of our study was to prospectively assess voiding US for grading of VUR and to compare results with those of VCUG in adult patients undergoing antireflux ureteral implantation.

	MATERIALS AND METHODS

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Patients
This prospective blinded study was approved by the institutional review board, and the tenets of the Declaration of Helsinki were followed. Written informed consent was obtained from all patients.

From January 2000 to June 2003, 37 consecutive patients aged 23–69 years (mean age, 46.5 years ± 12.1 [standard deviation]) who underwent renal transplantation according to Politano-Leadbetter technique (a transvesical approach for ureteral anastomosis) or Lich-Gregoire technique (an extravesical approach for ureteral anastomosis) were included. Eighteen patients were assigned to the Politano-Leadbetter group (12 men and six women; mean age, 48.4 years ± 11.2), while 19 patients were assigned to the Lich-Gregoire group (10 men and nine women; mean age, 44.7 years ± 12.9). There were no significant differences between the two groups with regard to age (t test, P value not significant) or sex distribution (Fisher exact test, P value not significant).

Fifteen kidneys were transplanted on the right side of the pelvis in 15 patients (Politano-Leadbetter technique, seven patients; Lich-Gregoire technique, eight patients), while 22 kidneys were transplanted on the left side of the pelvis in 22 patients (Politano-Leadbetter technique, 11 patients; Lich-Gregoire technique, 11 patients). Inclusion criteria were (a) one or more episodes of UTIs within the past year and (b) elapsed time of at least 2 years from renal transplantation to the time the present study was undertaken (median time after renal transplantation, 3 years; range, 2–6 years). To recruit patients for our study population, both criteria had to be satisfied. Patients whose graft had survived 2 years after renal transplantation were preferred to avoid acute rejection episodes, urologic complications and infective problems, and drug toxicity, which are more probable in the first months after renal transplantation and do not depend on VUR (11). The only exclusion criterion was a current UTI. The protocol for the present study required that both voiding US and VCUG be performed in the same examination session (one after the other) by using the same catheter to avoid repeat catheter placement.

Voiding US Procedure
US was performed with an SSA 270A unit (Toshiba, Tokyo, Japan) equipped with a 3.75-MHz convex-array transducer. For color Doppler examination, 4-kHz pulse repetition frequency was used, and color filters and color gains were adjusted to optimize imaging. One of two sonologists (A.L.V., A.M.D.G., with 15 and 25 years of experience in kidney and bladder US) performed the US examinations.

Preliminary evaluation of the transplanted kidney was conducted with conventional gray-scale US. A catheter was used to fill the bladder with room-temperature saline solution (250 mL), which was administered by means of drip infusion, with the top of the drip chamber 30–50 cm above the patient’s head. Preliminary US was then performed in the bladder. Afterward, microbubble suspension (Levovist; Schering, Berlin, Germany) was injected with a concentration of 300 mg/mL in a volume of 10% of the bladder volume. In this way, (echogenic) microbubbles were easily identified in the bladder, which was filled with (anechoic) saline. Microbubble suspension was introduced slowly. Because it has a high density, a fast injection would result in a massive settling of the suspension at the bottom of the bladder, which would hide the ureteral orifice and make it difficult to detect echoes in this region (4).

During microbubble injection, the bladder, ureter, renal pelvis, and calyces were reevaluated with gray-scale US. With the patient in the supine position, an oblique scan of the bladder-ureteral junction and a scan along the longitudinal axis of the transplanted kidney were obtained. Since it has been demonstrated (5) that color Doppler technique increases US sensitivity, color Doppler imaging was used to support gray-scale US findings. The same evaluation was repeated during the voiding phase, which was performed with the catheter inside the patient. The examination was recorded on videotape.

Diagnosis of VUR was assigned when echoes refluxing from the bladder to the urinary tract were identified (5) or when echoes were scarcely detected but color signals were seen clearly. The technical difficulty of obtaining images during the voiding phase in women in the supine position was overcome by equipping the patient with a diaper. VUR grading with voiding US was assessed in five grades (5): grade I, echoes or color signals in the ureter above the ureteral orifice; grade II, echoes or color signals extending up to the renal pelvis without ureteral dilatation; grade III, echoes or color signals extending up to the renal pelvis and calyces (nondilated) with mild dilatation of the ureter; grade IV, echoes or color signals in dilated ureter, renal pelvis, and calyces; and grade V, echoes or color signals in markedly dilated ureter, renal pelvis, and calyces. The two sonologists assessed US findings in consensus by reviewing the videotape. No adverse events due to the intravesical administration of the echogenic contrast agent were observed.

VCUG Procedure
VCUG was conventionally performed with a standardized technique. One of two radiologists (L.M.M., V.T., with 10 and 5 years of experience in VCUG) performed VCUG immediately after US by using the same catheter. The fact that VCUG was performed immediately after US with the same catheter could raise the hypothesis that the first examination (US) might affect the second (VCUG)—for example, by increasing the likelihood of obtaining similar findings. Actually, the second procedure was always started after restoration of the basal study condition.

An ionic water-soluble contrast agent with 36% iodamide (Uromiro; Bracco, Milan, Italy) was introduced slowly through the catheter with fluoroscopic guidance by keeping the bladder volume comparable to that at US (250 mL). Radiographs were obtained during filling and during the voiding phase. VUR at VCUG was assessed with five grades, according to the international system of radiographic grading of VUR: grade I, contrast material in the ureter only; grade II, contrast medium extending up to the renal pelvis and calyces, with no dilatation; grade III, ureter, renal pelvis, and calyces contain contrast material, with mildly dilated ureter; grade IV, moderate dilatation of the ureter, renal pelvis, and calyces with obliteration of the sharp angle of the fornices but maintenance of the papillary impression in most calyces; and grade V, marked dilatation and tortuosity of the ureter and gross dilatation of the renal pelvis and calyces, with papillary impression no longer visible in most calyces (7). The two radiologists assessed VCUG findings in consensus while blinded to US results.

Statistical Analysis
The results of US and VCUG were compared by using a 2 x 2 table. US sensitivity, specificity, and positive and negative predictive values for the diagnosis of VUR were calculated. For the analysis of diagnostic accuracy, 95% confidence intervals (CIs) were given, as described by Harper and Reeves (17). Agreement between the results of US and VCUG was determined with statistics. A P value of less than .05 was considered to indicate a statistically significant difference.

The statistic is an index of agreement, with 1.0 indicating perfect reproducibility or concordance. The statistic is estimated to be the difference between the observed agreement and the expected agreement, divided by the remainder of 1 minus the expected agreement. Expected agreement is defined as the agreement with the assumption of independence of the two measurement tools, or no concordance. A value of 0–0.40 indicates marginal agreement; 0.41–0.75, good agreement; and 0.76–1.00, excellent agreement (18). Rate of VUR in Politano-Leadbetter and Lich-Gregoire groups was evaluated on the basis of the reference standard—the VCUG results.

	RESULTS

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On the basis of VCUG results, VUR was diagnosed by the two radiologists (L.M.M., V.T.) in 15 patients and was not diagnosed in 22 patients. Consensus was reached in all cases. US results were assessed by the two sonologists (A.L.V., A.M.D.G.). Consensus was reached in all cases. US findings were in agreement with VCUG findings in 14 patients with VUR and in 21 patients without VUR (Table 1; Figs 1, 2). One false-positive case was identified at US (grade II VUR). In one case, VUR was depicted with only VCUG (grade I VUR).

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Concordance between US and VCUG for grade II VUR. (a) Oblique voiding US image of transplanted kidney obtained during filling phase demonstrates echoes in the renal pelvis (arrow) due to microbbubbles refluxing up from the bladder. (b) Oblique voiding US image of transplanted kidney obtained only a few seconds after a during the same filling phase demonstrates microbubble movement into the renal pelvis. Calyces are not dilated (grade II VUR). (c) Anteroposterior VCUG image obtained during the filling phase confirms grade II VUR in the transplanted kidney.

View larger version (159K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Concordance between US and VCUG for grade II VUR. (a) Oblique voiding US image of transplanted kidney obtained during filling phase demonstrates echoes in the renal pelvis (arrow) due to microbbubbles refluxing up from the bladder. (b) Oblique voiding US image of transplanted kidney obtained only a few seconds after a during the same filling phase demonstrates microbubble movement into the renal pelvis. Calyces are not dilated (grade II VUR). (c) Anteroposterior VCUG image obtained during the filling phase confirms grade II VUR in the transplanted kidney.

View larger version (136K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Concordance between US and VCUG for grade II VUR. (a) Oblique voiding US image of transplanted kidney obtained during filling phase demonstrates echoes in the renal pelvis (arrow) due to microbbubbles refluxing up from the bladder. (b) Oblique voiding US image of transplanted kidney obtained only a few seconds after a during the same filling phase demonstrates microbubble movement into the renal pelvis. Calyces are not dilated (grade II VUR). (c) Anteroposterior VCUG image obtained during the filling phase confirms grade II VUR in the transplanted kidney.

View larger version (120K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Concordance between color Doppler voiding US and VCUG for grade III VUR. (a) Oblique color Doppler voiding US image obtained in the bladder-ureteral anastomosis shows color signals in a mildly dilated ureter (arrow). K = kidney, B = bladder. (b) Oblique color Doppler voiding US image obtained in the transplanted kidney shows color signals up to the pelvis of the kidney (arrow). (c) Left oblique VCUG image obtained during the voiding phase shows grade III VUR in a right transplanted kidney.

View larger version (120K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Concordance between color Doppler voiding US and VCUG for grade III VUR. (a) Oblique color Doppler voiding US image obtained in the bladder-ureteral anastomosis shows color signals in a mildly dilated ureter (arrow). K = kidney, B = bladder. (b) Oblique color Doppler voiding US image obtained in the transplanted kidney shows color signals up to the pelvis of the kidney (arrow). (c) Left oblique VCUG image obtained during the voiding phase shows grade III VUR in a right transplanted kidney.

View larger version (92K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. Concordance between color Doppler voiding US and VCUG for grade III VUR. (a) Oblique color Doppler voiding US image obtained in the bladder-ureteral anastomosis shows color signals in a mildly dilated ureter (arrow). K = kidney, B = bladder. (b) Oblique color Doppler voiding US image obtained in the transplanted kidney shows color signals up to the pelvis of the kidney (arrow). (c) Left oblique VCUG image obtained during the voiding phase shows grade III VUR in a right transplanted kidney.

US and VCUG findings were in agreement with VUR grades in 11 of 14 cases (four grade III cases, six grade II cases, and one grade I case), while in three cases, US indicated a higher grade than that with VCUG (two grade II cases instead of grade I and one grade III case instead of grade II) (Table 2).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
For years, the technique of choice in the detection of VUR has been VCUG, especially at the first examination in VUR investigation. Radionuclide cystography is usually used for follow-up. In studies of voiding US in children (1–6,8,9), US shows high sensitivity and specificity in the prediction of VUR at VCUG (91.7%–100% and 86–97%, respectively) and radionuclide cystography (79% and 92%, respectively). This is why some authors prefer voiding US to VCUG and radionuclide cystography in women and in the follow-up of children with reflux documented previously (1–3). Other authors also recommend use of voiding US in the screening of children at risk for VUR because of its high negative predictive value, especially when supported by color Doppler or harmonic US findings (5).

The only limitation of the voiding US technique seems to be the evaluation of the urethra. In kidney transplantation, adult patients with UTIs do not usually undergo urethral evaluation, but an accurate investigation for VUR detection might be needed. The results of our study, which are in agreement with those in previous studies in children, show high sensitivity and specificity of US in the detection of VUR (93% and 95%, respectively). The high rate of agreement between US and VCUG (95%), as well as its high negative predictive value (95%), confirms that US is a credible technique in VUR investigation and justifies more extensive use.

Catheterization is needed with voiding US, as it is with VCUG. In comparison to VCUG, however, apart from the absence of radiation, voiding US has the great advantage of enabling continuous observation while not prolonging fluoroscopic time. Continuous observation might make voiding US better than VCUG in the observation of the intermittent nature of VUR. The authors stress that microbubbles refluxing from the bladder to the urinary tract were identified clearly in the patient with the false-positive US result and in patients with a higher VUR grade shown with US in comparison to that with VCUG. It could be said that gray-scale US might not demonstrate (echogenic) microbubbles in hydronephrosis cases with (echogenic) mucous debris, and grade I VUR is difficult to diagnose, since the ureter is not dilated.

Visualization in these cases can be improved by using color Doppler US, as it was demonstrated in a previous study on the comparison of gray-scale voiding US with color Doppler voiding US in VUR investigation (5). The authors attributed the superiority of color Doppler voiding US in the detection of VUR to the high-color effects that occur during VUR, which are seen immediately by the observer. In the present study, one case of grade I VUR was assessed correctly at voiding US by using color Doppler technique.

In the literature, the rate of VUR in renal transplants ranges from 2.9% to 50%, depending on the surgical technique used (12–14). Some of this discrepancy may be attributed to the timing of the study and the quality of the bladder wall. Recurrent UTI and renal graft pyelonephritis associated with VUR require antibiotic treatment, which does not always suffice. High-grade VUR in renal transplant recipients can also be treated with surgery (10). Therefore, for a surgical strategy, it would be useful to know whether an extravesical approach for ureteral anastomosis (which should be related to a lower incidence of leakage) also shows a lower incidence of VUR than does a transvesical approach, which involves use of a more extensive bladder opening. Nevertheless, the effect of VUR on the function of the renal transplant has not yet been determined. Controversy exists with regard to the relationship between VUR, UTI, and graft prognosis. Some investigators state that VUR is harmful to the renal transplant function in the long term. Others believe that the impairment of graft function is due to rejection and is not caused by VUR itself, and still others state that patients with VUR show a significantly worse graft survival rate (19,20). These controversies could be resolved by means of long-term follow-up. From these results, VUR rate was high for both surgical techniques.

In the Politano-Leadbetter group, a higher VUR grade was observed in some cases (Table 3). Because of the small size of this study, however, more investigations are needed to verify whether the surgical approach for renal transplantation has a correlation with VUR.

In conclusion, UTI can easily induce pyelonephritis and sepsis in individuals with compromised defense mechanisms, such as patients with renal transplants (10). Since VUR is one of the risk factors for UTI and the incidence of VUR in renal recipients seems to increase with time (15), follow-up of patients with VUR should always be performed to ensure that appropriate therapy is implemented. In the present study, as well as in previous reports, US was demonstrated to be a very promising technique and a credible alternative to VCUG in the investigation of VUR. US is easy to perform (a) in adults because of the great advantage of full patient cooperation and (b) in renal transplantation, since the attention of the examiner is focused on only one kidney. In addition, the favorable anatomic location of the transplanted kidney most often makes the complete urinary tract visible with the same oblique scan. The high cost of echogenic contrast agents remains the only limitation of this promising technique, which deserves, in our opinion, more extensive use.

	FOOTNOTES

 
Abbreviations: CI = confidence interval, VCUG = voiding cystourethrography, VUR = vesicoureteral reflux

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, A.L.V.; study concepts, A.L.V., A.M.D.G., C.D.; study design, A.L.V., C.D., A.M.D.G., G.N., F.C.; literature research, A.L.V., V.T., L.M.M., A.M.V.; clinical studies, G.N., F.C., C.D.; experimental studies, A.L.V., A.M.D.G.; data acquisition, A.L.V., C.D., A.M.V., V.T.; data analysis/interpretation, L.M.M., A.L.V., A.M.D.G.; statistical analysis, A.L.V., C.D.; manuscript preparation, A.L.V., C.D., A.M.V.; manuscript definition of intellectual content, A.L.V., A.M.D.G., G.N., F.C., L.M.M., V.T.; manuscript editing, A.L.V., C.D.; manuscript revision/review and final version approval, all authors

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