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Pediatric Imaging |
1 From the Department of Pediatric Radiology, University Hospital La Paz, Paseo de la Castellana 246, 28046 Madrid, Spain. Received September 30, 2003; revision requested December 10; final revision received March 16, 2004; accepted April 15. Address correspondence to T.B. (e-mail: tberrocal.hulp@salud.madrid.org).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: This study was approved by the ethics committee on human research. Written informed consent was obtained for all patients. A total of 146 pediatric patients suspected of having vesicoureteral reflux underwent US with a galactose-based contrast agent. The bladder was instilled with contrast agent and then filled with saline. US images of the urethra were videotaped before catheterization and during voiding. VCUG was subsequently performed in all patients. In female patients, the probe (a 3.5- or 5-MHz sector array or a 7.5-MHz linear transducer) was positioned longitudinally between the labia. In male patients, the transducer was placed longitudinally on the scrotum and then displaced distally toward the penile urethra. During voiding, attention was focused on the distention of the urethral walls and on the caliber of both the posterior and anterior urethra, which were measured with calipers. Sensitivity and specificity were estimated by using a confidence interval (CI) of 95%.
RESULTS: All female patients and 75 male patients showed a normal urethra at both US and VCUG. Posterior urethral valves (PUV) were diagnosed in three patients at voiding US and were confirmed with findings from VCUG. Urethral stenosis was diagnosed in two male patients at voiding US and was confirmed with findings from VCUG. Seven male patients who had undergone surgery for PUV were adequately evaluated with both modalities. Sensitivity of voiding US was 100% (CI 95%: 96.5%, 100%); specificity was 100% (CI 95%: 69.9%, 100%).
CONCLUSION: Voiding US is a reliable imaging modality for studying the urethra.
© RSNA, 2005
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Findings from earlier studies have shown that ultrasonography (US) is not a sensitive method for the depiction of VUR (10–14). Because of the low sensitivity and specificity of both B-mode and Doppler US for the depiction of VUR, researchers have considered US contrast agents that, when instilled into the bladder as at VCUG, would improve depiction of VUR. After a few unsuccessful attempts with several substances (15–17), US contrast agents made from galactose suspension, such as galactose-palmitic acid (SH U 508A, Levovist; Schering, Berlin, Germany), proved to be useful in helping to diagnose and grade reflux (18,19). Compared with VCUG, contrast material–enhanced cystosonography has a sensitivity of 100% and a specificity of 86%–100% in demonstrating VUR (20–22). The main limitation that has been reported with cytosonography is that the urethra is difficult to assess adequately (18–23). Until now, the role of cystosonography has been limited to screening for VUR in female patients and for follow-up in both sexes.
The use of transperineal US for imaging of the urethra has been previously reported in pediatric patients with and pediatric patients without urethral obstruction (24,25). The appearance and width of the entire urethra before and during voiding in male infants and newborns with posterior and anterior urethral valves have also been described (26–28). In adult women, this imaging modality has been used to evaluate the bladder neck and urethra in cases of incontinence (29). In all these studies, saline or urine was used as a contrast medium.
In a study by Bosio and Manzoni (30), 100 boys who were suspected of having VUR underwent contrast-enhanced voiding US of the urethra by using a technique that was slightly different from the technique used in our current study. In this series by Bosio and Manzoni (30), the male urethra was adequately assessed in patients with a normal urethra, as well as in patients with an obstructed urethra. No results on the female urethra were reported.
The purpose of our study was to prospectively evaluate contrast-enhanced voiding US for the assessment of the urethra by using VCUG as the reference standard.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Voiding US of the Urethra and Analysis
All examinations were performed in the fluoroscopic suite with a US device (Sonolayer SSH-140; Toshiba Medical Systems, Tokyo, Japan). The US examinations were performed in fundamental frequency mode only, by using a 3.5- or 5-MHz sector array or a 7.5-MHz linear transducer. The entire procedure was videotaped to allow review of the complete examination in real time. No cyclic filling was performed.
Baseline US of the urinary tract included transverse and longitudinal scanning of both the bladder and kidneys. The urethra was studied by using a transperineal approach. For this approach, the patient was placed in the supine decubitus position with the thighs abducted and the heels opposed (25), and warm US gel was applied to the perineum. In female patients, the probe was positioned longitudinally between the labia to evaluate the bladder neck and urethra. In male patients, the transducer was initially placed longitudinally on the scrotum and ventral root of the penis to assess the bladder neck and proximal bulbar urethra; the transducer was then slightly displaced distally toward the penile urethra.
At baseline US, we identified the hyperechoic pubic bones on either side of the transducer and scanned the midline between the pubic bones. In this plane, we identified the bladder base, the bladder neck, and the entire urethra in female patients. At rest, the normal female urethra demonstrates a collapsed anechoic lumen and an echogenic mucosa (29). In male patients, we identified the bladder base, the bladder neck, and the posterior urethra. The posterior urethra is seen as a hypoechoic structure that is located posterior to the symphysis pubis and in continuity with the anterior urethra, which has hyperechoic walls (25,27). Behind the posterior urethra, the rectum is easily identified because of its air content. The urethral mucosa and lumen were identified and measured during distention.
All baseline US examinations were performed and images interpreted by a senior pediatric radiologist (T.B.) who has been out of training for 14 years and has 4 years of experience in contrast-enhanced cytosonography.
After baseline US was performed, the patients were catheterized transurethrally. The catheter, a 5- or 8-F infant feeding tube (vesical catheter; Vigon, Ecolien, France), was connected by means of a three-way stopcock to an intravenous tubing set, which was attached to a saline bottle placed 70 cm above the patient’s head. A 10-mL syringe of galactose-palmitic acid (concentration, 300 mg/mL) was also attached to the three-way stopcock. The catheter was secured to the perineum. Bladder capacity was estimated according to the following nomogram, which is based on the patient’s age: volume = (age + 2) x 30, where volume is measured in milliliters, age is measured in years, and 30 converts ounces to milliliters (31,32).
The bladder was filled with saline to half the estimated volume. The saline was infused by gravity. The contrast material was then instilled very slowly and was monitored by using continuous US surveillance. After the galactose-palmitic acid was injected, saline was instilled until the bladder was full. During bladder filling, the kidneys and distal ureters were studied for VUR according to the technique previously described by Berrocal et al (21).
After the bladder was filled, the transurethral catheter was removed from the bladder to allow study of the urethra. As at baseline US, the urethra was assessed by using a transperineal approach during voiding. Both the patients and the probe were positioned the same as for baseline US.
Patients older than 4 years were asked to void with the probe in place. Because the bladder was filled, it was not difficult to prompt patients, especially newborns and infants, to void. Some patients were reluctant to void while in the supine position with the probe in place. The parents’ cooperation was of great value in these cases. Patients who found it impossible to void in the supine position were examined voiding in the oblique position for their comfort. The probe was maintained directly against the perineum until the bladder and the entire urethra had been adequately assessed and videotaped.
During voiding, attention was focused on the elasticity and distention of urethral walls, as well as on the caliber of both the posterior and anterior portions of the urethra in male patients. The behavior of the contrast material during its progression along the urethra was evaluated to document the presence of any obstruction or voiding dysfunction. To evaluate the normal aspect of the female urethra, the anteroposterior diameter of the urethra was measured in the middle of the urethra during distention. In male patients, the transverse diameter of the urethra was measured at the posterior and at the bulbar urethra during distention. The transverse diameter of the lumen was measured at the beginning of voiding, when the distention is maximal. All measurements were made with calipers. A postvoiding study of the kidneys, distal ureter, and bladder was performed in all patients by using the technique previously described by Berrocal et al (21).
The urethra was considered normal at voiding US when adequate distention and a homogeneous caliber of the whole urethra, as well as continuous progression of the contrast material, were observed (30). Posterior urethral valves (PUVs) were diagnosed at voiding US when a dilated (diameter of 7 mm or larger) posterior urethra was observed with poor distention of the valve area and a reduced caliber of the anterior urethra; the difficult progression of the contrast material through the valve area was also noted in these patients (25,30). A urethral stenosis was diagnosed when a difference in caliber of at least one-third was observed between the pre- and poststenotic areas (33). In patients who had undergone surgery for PUV and who had demonstrated a residual dilated posterior urethra, special attention was focused on the caliber of the anterior urethra and the distention and progression of contrast material through the valvular area. The approximate mean duration for voiding US, including baseline US, catheterization, and completion of voiding US, was 30 minutes.
Voiding US and Measurements
After voiding US, patients were catheterized again and VCUG was performed according to the guidelines suggested by the International Reflux Study in Children (34). Both studies were performed with the same liquid volume, rate of infusion, and temperature. VCUG was performed with a digital fluoroscopic unit (Fluorospot Compact; Siemens Medical Systems, Berlin, Germany). Intermittent fluoroscopy (300 mrad/min [0.003 Gy/min]) was performed, and several abdominal radiographs were obtained as follows: (a) half-filled and (b) completely filled bladder radiographs, (c) anteroposterior and oblique voiding radiographs, (d) postvoiding radiographs, and (e) voiding lateral radiographs, which were obtained in male patients only. VCUG findings were regarded as the standard of reference for the assessment of normal and abnormal urethra.
Voiding US studies were conducted and images interpreted by the same pediatric radiologist (T.B.) who performed the baseline US examination, and VCUG images were interpreted by a second pediatric radiologist (A.A.). Images from voiding US were interpreted before VCUG was performed. Neither radiologist knew the results that were obtained with the other technique or at any prior VCUG examination. All the images from voiding US were reinterpreted from videotape at the end of the investigation after all data were obtained by consensus of both radiologists (T.B., A.A.). Neither radiologist had knowledge of the original interpretation. Results of voiding US and the results of VCUG were compared.
Statistical Analysis
For statistical analysis, VCUG was considered the reference standard. Statistical analysis was performed by using a statistical software package (SPSS for Windows, release 9.0; SPSS, Chicago, Ill). Quantitative data are described as a mean ± standard deviation, and qualitative data are described as counts and percentages. The sensitivity and specificity of voiding US versus the sensitivity and specificity of VCUG were estimated by using a confidence interval (CI) of 95%.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The microbubbles persisted long enough to allow adequate urethral assessment, even in cases where the procedure was lengthened because patients were reluctant to void spontaneously. The additional administration of contrast material was not necessary in any patients.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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The prevalence of VUR ranges from 0.5% to 1.5% in the pediatric population (4,41). Screening programs in high-risk populations can enable early diagnosis and prophylaxis, thereby preventing renal damage (4,40,41). It is important that the chosen imaging modality is as safe as possible (4). The first-choice imaging modality for the diagnosis of VUR is VCUG. Another highly sensitive technique is radionuclide cystography; this technique has the advantage of low irradiation of the patient, but it lacks spatial resolution (42).
Cystosonography with galactose-palmitic acid has proved to be a reliable method for the identification and grading of VUR. The main advantage of cystosonography is the accurate and reliable depiction of VUR without the use of ionizing radiation (18–23). The absence of ionizing radiation is paramount in the pediatric population, especially considering the number of imaging evaluations for VUR that each child may undergo. On the other hand, cystosonography with US contrast material may be even more sensitive than VCUG and may improve the depiction of transient VUR through the use of continuous US instead of intermittent fluoroscopy imaging (21,23). The intermittent nature of VUR is well known, and the chance of demonstrating VUR increases with the time of visualization (1,5,7,43).
Early research with this contrast material focused on its usefulness to demonstrate VUR. To the best of our knowledge, the possibility of evaluating the urethra during voiding US was not taken into consideration (18,19). In later studies, the main limitation of contrast-enhanced cytosonography compared with VCUG was its difficulty in accurately imaging the urethra (20–23). According to the results of these studies, cystosonography should not replace VCUG for the initial evaluation of patients who are suspected of having VUR because a small, but clinically important, number of male patients with secondary VUR have urethral anomalies. Nevertheless, only a minority of patients who are affected with VUR have US abnormalities of the bladder or upper urinary tract that are suggestive of urethral obstruction (eg, bladder wall thickening, dilated and tortuous ureters, and hydronephrotic kidneys) (30,44). To identify these relatively few patients, however, many fluoroscopic VCUG procedures are required, thus exposing patients to ionizing radiation (8,45).
It is known that transperineal sonography in children can reveal the anatomy of the urethra, periurethral soft tissues, anterior portion of the rectum, and, in female patients, the distal gynecologic tract (24). In 1982, Gilsanz et al (46) suggested that transvesical US be performed to assess the bladder and identify the "dilated and elongated prostatic urethra" of PUV, allowing the differentiation of PUV from a neurogenic cause of outlet obstruction. In 1983, Cremin and Aaronson (47) reported the use of a perineal sagittal US view in obtaining images of the dilated posterior urethra for the diagnosis of PUV. Cohen et al (27), by using the transperineal approach, were able to visualize the PUV directly as a linear area of echogenicity within the dilated posterior urethra.
More recently, Good et al (25) described dynamic transperineal imaging of the posterior urethra before and during voiding. In their study, the authors were able to measure the diameter of the urethra in patients with a normal posterior urethra and patients with an obstructed posterior urethra. The authors were also able to identify the obstructing urethral valves in more than half of the patients. The anterior urethra was also depicted during voiding. Likewise, in 1997 Teele and Share (24) demonstrated the utility of transperineal sonography to demonstrate urethral obstruction (posterior and anterior valves); urethral diverticulum; urethral stricture; urethral insertion of ureter and ureterocele; and urethral polyp, tumor, granuloma, or stone.
Our transperineal (interscrotal or interlabial) approach is the same as that used in all these reports. Most of these previous studies were performed during voiding by using urine as a contrast medium. For our current study, we assessed the urethra during voiding and used the contrast material already instilled into the bladder for investigation of VUR.
Recently, Bosio and Manzoni (30) studied the urethra in 50 patients during retrograde instillation of the same contrast material that was used in our current study. During voiding, the researchers initially investigated the posterior urethra by using a transabdominal sagittal and transverse approach. Findings from further experience, however, demonstrated that a transperineal sagittal US approach was more accurate because the bladder neck and the critical parts of the urethra were better visualized with the probe located coaxial to the structures. Therefore, Bosio and Manzoni studied 50 more patients by using the transperineal approach, and the urethra of each of these patients was adequately assessed. Eight of these patients were suspected of having PUVs, which were confirmed with findings from VCUG and cystoscopy. Bosio and Manzoni did not compare the urethral imaging in the rest of the patients. None of the patients with normal findings at urethral US, however, showed clinical or US signs of urethral obstruction after a minimal follow-up of 12 months.
Our study differs from the study by Bosio and Manzoni in that every patient in our study was examined with both voiding US and VCUG. In our study, voiding US was performed first, and the radiologist was unaware of the results from VCUG. Furthermore, we included male patients and female patients in the study. To avoid selection bias, we included all patients who were suspected of having VUR, excluding only those patients who were unable to void spontaneously. At voiding US, the transurethral catheter was removed from the bladder before voiding to avoid catheter-related artifacts, and a second catheterization was performed for VCUG. Videotaping of the entire procedure allowed for review of the complete examination in real time, as well as for the measurement of urethral width in all patients.
Our results show that voiding US can adequately assess the female, as well as the male, urethra. Specific pitfalls and problems that have been described with the transperineal approach, such as insufficient US penetration in large children (24), have been currently solved with multifrequency microconvex probes, which allow good visualization of the entire lower urinary tract. The number of cases in which it was impossible to perform a voiding study were similar for both voiding US and VCUG.
As previously reported by Bosio and Manzoni (30), voiding US was as useful as VCUG in depicting PUVs. In our study, the three patients with PUV demonstrated a dilated posterior urethra; a considerable difficulty in the progression of contrast medium through the valvular area toward the anterior urethra was also noted. In these three patients, the contrast material pooled behind the valvular area for a length of time that was not observed in healthy subjects. Moreover, when the US contrast material did reach the anterior urethra, the lumen was filiform and the urine jet always intermittent. In two patients with stenosis of the anterior urethra, the portion of the urethra behind the stenosis appeared slightly dilated, and an abrupt width change was observed between the prestenotic and the poststenotic segments. In patients with PUV, the contrast medium progressed without delay through the narrowed segment; the reduction in lumen size, however, increased the urination time.
The dynamic information obtained at voiding US was especially useful in evaluating patients who had previously undergone PUV surgery. Despite a common finding of a dilated posterior urethra, the progression of contrast material, as well as the distention of the anterior urethra, was normal in all cases.
Our study has some limitations. The number of patients who exhibited urethral abnormalities in our series is very small. Some rare but substantial causes of urethral obstruction, such as anterior urethral valves, have not been studied. No patients with abnormalities, such as diverticulitis or syringocele, have been evaluated, and further research is necessary to establish the true usefulness of voiding US in depicting these entities. The limitations of this technique that were noted during our study of the urethra are similar to the limitations that have been noted in the assessment of VUR. As was discussed by other authors (21,48), compared with the sensitivity of VCUG the sensitivity of cytosonography is dependent on the experience of the operator. We believe that correct procedures can help avoid mistakes and thereby exploit the diagnostic outcome of voiding US. Also, the assistance and cooperation of the children’s parents and careful attention in setting the US equipment are advisable.
A possible pitfall of this procedure is the amount of contrast material that is used. Some authors have reported that the microbubbles persisted for only 10–15 minutes before becoming excessively diluted, resulting in a voiding delay that can cause difficulties in image interpretation (20,48). These authors, however, used the minimum available amount of contrast material. As was noted by one of the authors, if more contrast material had been used then this pitfall could have possibly been avoided.
Another disadvantage is that patients must void with the probe in place, which may be awkward, especially for older children. Additionally, voiding US may prove more expensive than fluoroscopic VCUG, depending on the cost of galactose-palmitic acid and the additional US equipment used.
The biggest advantage of voiding US over VCUG is the absence of radiation exposure. The absence of ionizing radiation during the examination allows the patient to be accompanied by parents or a caregiver, even a pregnant caregiver, which is important in the pediatric population. An added advantage is that dynamic, real-time information is obtained during urination.
Our study was designed to analyze the reliability of transperineal voiding US as part of the routine work-up for adequate assessment of the urethra in patients suspected of having VUR. In our opinion, the current role of VCUG can be questioned. In this study, we have shown that voiding US depicts the anatomic regions of the female urethra and male urethra in all cases. Despite the small number of patients with urethral abnormalities that were included in the study, we consider that PUVs, which are the most relevant urethral anomaly, and urethral stenosis can be reproducibly diagnosed without VCUG. We therefore believe that cystosonography with US contrast material, complemented by voiding US, could be used as the initial diagnostic step in male patients and female patients suspected of having VUR. VCUG should still be recommended to confirm findings and to plan surgery, if required, whenever an abnormal urethra is demonstrated with contrast-enhanced US.
In conclusion, voiding US is a reliable imaging modality that is sufficiently sensitive and specific to adequately study the urethra and thus can be used as a complement to cystosonography in patients suspected of having VUR.
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FOOTNOTES |
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Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, T.B.; study concepts, T.B., A.A.; study design, T.B., F.G.; literature research, T.B., F.G.; clinical studies, T.B., A.A.; data acquisition, T.B., A.A.; data analysis/interpretation, all authors; statistical analysis, F.G.; manuscript preparation, definition of intellectual content, and editing, T.B.; manuscript revision/review, all authors; manuscript final version approval, T.B.
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