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1 All authors: Department of Pediatric Radiology, Radiological Clinic, Ruprecht-Karls University Heidelberg, Im Neuenheimer Feld 153, 69120 Heidelberg, Germany.
Received April 25, 2001;
accepted after revision June 14, 2001.
Address correspondence to K. Darge.
Abstract
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SUBJECTS AND METHODS. Fifty-four children presenting for diagnostic examination of vesicoureteral reflux underwent standard sonography of the urinary tract in the fundamental mode, followed by intravesical administration of a galactose-based contrast medium containing microbubbles. The contrast-enhanced sonography was conducted by scanning the bladder and each kidney in transverse and longitudinal planes, from ventral and dorsal views, consecutively in B-mode using fundamental, contrast harmonic, and tissue harmonic imaging modalities. Soft-touch buttons on the console screen were used to alternate between the three imaging options, so that switching from one modality to the other could be done almost instantaneously. For comparison, in each patient, we selected one set of contrast-enhanced images of the bladder and two sets, one ventral and one dorsal, of the kidney. In a series, the images were compared and ranked from 1 to 3, with 1 being the best, with regard to sonomorphology (demarcation of the retrovesical space and renal pelvis as the potential sites to look for vesicoureteral reflux) and reflux detection and conspicuity, if present.
RESULTS. In all, 248 sets of images were available for comparison. The delineation of both the retrovesical space and the renal pelvis was found to be best with tissue harmonic imaging in 84% and 96% of the image sets, respectively (p < 0.01). Forty-one sets of images were compared from 27 kidney-ureter image units of 22 children (41%) with reflux. The refluxing microbubbles were much more conspicuous in the harmonic imaging mode (tissue harmonic, 100%; contrast harmonic, 93%) than in the fundamental mode (p < 0.01). In eight kidney-ureter units, the reflux was detected only by using the harmonic imaging modalities.
CONCLUSION. Visualization of the urinary tract and detection of ultrasound contrast media is significantly improved by the use of the harmonic imaging modalities. When both fundamental and harmonic imaging options are available, we recommend harmonic imaging for contrast-enhanced sonographic diagnosis of vesicoureteral reflux.
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Harmonic sonography is a novel imaging technique that is increasingly becoming available for routine clinical use, potentially providing images of higher spatial and contrast resolution than those of conventional sonographic techniques [7,8]. Conventional sonography is based upon transmission of echoes at a given center frequency (the fundamental) and subsequent image formation using echoes received at that same frequency, thus the term, fundamental imaging. Harmonic imaging uses echoes received at twice the fundamental frequency (commonly referred to as second or narrow band harmonic imaging) or at multiples of that frequency (known as wide-band harmonic imaging) as the source for the image data [8,9]. Harmonic formation results from the phenomenon of nonlinear sound propagation. In tissue, the compressive phase of the wave front travels faster than the rarefaction phase, leading to progressive distortion of the waveform and, therefore, formation of harmonics (tissue harmonic imaging) [8]. When acoustic waves strike contrast microbubbles, they oscillate in a nonlinear fashion, meaning the expansion of the bubble is stronger than the compression, and they scatter at second and higher multiples of the fundamental frequency. Therefore, tuning the sonography receiver to the harmonic frequency will preferentially display the contrast agent within the image (contrast harmonic imaging) [9]. Technically, the separation of the undesired fundamental frequency from the harmonic frequency is carried out using high-pass filters, the so-called phase or pulse inversion technique, or both [10]. Wide-band harmonic imaging uses phase or pulse inversion imaging and has been found to be superior in image quality to second harmonic imaging [9].
The objective of this study was to compare, in children, sonographic reflux studies using fundamental imaging with sonographic reflux examinations using phase or pulse inversion harmonic imaging comprising both tissue and contrast harmonic options. The evaluation of any potential improvement in diagnostic imaging incorporated two aspects: sonomorphology with regard to demarcation of the retrovesical space and renal pelvis as potential sites of vesicoureteral reflux; and reflux detection and conspicuity.
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Imaging Technique
Sonographic images were obtained using a Sonoline Elegra scanner, equipped
for the phase inversion technique and with both the tissue and contrast
harmonic options (Ensemble Tissue and Contrast Harmonic Imaging, Siemens
Medical Systems, Issaquah, WA). Multifrequency 3.5-MHz convex or 7.5-MHz
linear transducers were used, the former more for older children and the
latter in neonates. Standard sonographic scanning of the urinary tract in
fundamental B-mode was followed by transurethral bladder catheterization.
Subsequently, SH U 508 A (Levovist; Schering, Berlin, Germany), a
galactose-based contrast agent containing microbubbles, was administered at a
concentration of 300 mg/mL and a volume of 10% of that of the bladder filling.
A detailed description of this procedure has been presented elsewhere
[2].
The contrast-enhanced scanning was also carried out in B-mode, this time using consecutively the three imaging modalities: fundamental, contrast harmonic, and tissue harmonic. The same transducer was used for the all scans during one examination session. Soft-touch buttons on the console screen were used to alternate among the three imaging options, switching from one modality to the other almost instantaneously. The transmit frequency ranges for the 3.5-MHz transducer were 2.8-5.1 MHz for fundamental imaging, 1.9-2.7 MHz for tissue harmonic imaging, and 2.0-3.6 MHz for contrast harmonic imaging. For the 7.5-MHz transducer, the transmit frequency ranges were 5.1-9.0 MHz for fundamental imaging, 3.0-4.5 MHz for tissue harmonic imaging, and 3.3-7.2 MHz for contrast harmonic imaging. The imaging parameter settings were those standardized according to the manufacturer's recommendation. Only the frequency and gain compensation were varied to optimize the image for each imaging modality. A single focal zone was applied and kept at the same point during all three imaging procedures. The focus was set at the level of the terminal ureters for scanning the bladder and at the level of the renal pelvis for scanning a kidney.
For each modality, standard planes in both the longitudinal and transverse axes of the respective organ were documented sequentially on laser films (Scopix LR 5200; Agfa-Gevaret, Mortsel, Belgium). When reflux was detected in one imaging modality, additional scans were obtained in the same plane using the other two modalities. At least two sets of images of a bladder and four sets of images of a kidney (ventral and dorsal) were available. The voiding urosonography with the sequential application and documentation of all three imaging modalities lasted on average 30-45 min.
Image Analysis
One set of contrast-enhanced images was selected for a bladder and two
sets, one from ventral and one from dorsal, were selected for a kidney. For
purposes of comparison, either the longitudinal or transverse scans were
selected, depending on which plane was most similar in all three imaging
modalities. If comparable images could not be obtained, for example, in a
restless child, the particular image site was excluded from further
evaluation. When reflux was revealed, the respective series depicting the
refluxing microbubbles was chosen. Over the course of our study, only contrast
harmonic imaging was available for scanning initially; shortly afterward,
tissue harmonic imaging was added. Consequently, all patients had examinations
with fundamental and contrast harmonic modalities, but only a subset of
patients underwent imaging that included the tissue harmonic option.
In a series, the images were compared and ranked from 1 to 3, with 1 being the best, with regard to depiction of the retrovesical space or the renal pelvis, and with regard to how conspicuous reflux was, if present. The depiction of the retrovesical space refers to the ability to clearly visualize the area behind the bladder where the terminal ureter is seen or is expected to be, having in mind the ease of identification of refluxing microbubbles. In a similar manner, the depiction of the renal pelvis refers to the ease of delineating the renal pelvis or the degree of contrast between the renal parenchyma and the renal pelvis. In addition, in the case of vesicoureteral reflux, the microbubble density was assigned a score from 1 (lowest) to 3 (highest), and the renal pelvic dilatation was measured in the transverse plane. Each set of images was evaluated by two reviewers unaware of the type of imaging modality used. The results of the two evaluations were reviewed; in cases with a mismatch, the two reviewers reevaluated the images together and assigned the rank or score in consensus.
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Sonomorphology
The delineation of the retrovesical space was found to be best with tissue
harmonic imaging in 27 (84%) of 32 cases (p < 0.01)
(Table 1). Fundamental imaging
ranked second, being superior to contrast harmonic imaging in 39 (75%) of 52
image sets. For evaluation of the retrovesical space, contrast harmonic was
the least suitable. In the renal pelvis, again, tissue harmonic imaging ranked
first in 116 (96%) of 121 image sets (p < 0.01). Contrast harmonic
imaging was found to generate better images of the renal pelvis than
fundamental mode in 140 (71%) of 196 cases
(Table 2). Thus, visualization
of the renal pelvis was least optimal using fundamental imaging as compared
with the tissue and contrast harmonic modalities. No significant difference
(p > 0.05) with regard to the ranking was found when kidney image
sets from ventral and dorsal views were compared. Overall, tissue harmonic
imaging was found to be the best imaging modality for producing the highest
quality of images of both the retrovesical space and renal pelvis.
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Vesicoureteral Reflux
Reflux was detected by at least one of the imaging modalities in 22 (41%)
of 54 patients in 27 kidney-ureter image units: 17 unilaterally and five
bilaterally. A total of 41 sets of images (bladder, n = 9; kidney,
n = 32), including 31 (bladder, n = 5; kidney, n =
26) obtained using tissue harmonic imaging, were available for reflux
comparison. The refluxing microbubbles were much more conspicuous in tissue
harmonic imaging in all 31 cases (100%) compared with fundamental mode
(p < 0.01) (Fig.
1A,1B,1C,1D).
The refluxing microbubbles were also more conspicuous in contrast harmonic
imaging than in fundamental mode in 38 (93%) of 41 image sets (p <
0.01) (Fig.
2A,2B).
When contrast and tissue harmonic modalities were compared, no significant
difference (p > 0.05) was seen in the evidence of reflux, the
former having the first rank in 15 of 31 image sets and the latter in 16 of 31
image sets (Fig.
3A,3B,3C,3D).
The mean microbubble density score of these two groups of images was 1.9 for
contrast harmonic imaging and 2.4 for tissue harmonic imaging; the median
score for both was 2. Although no statistical difference (p >
0.05) was found between the two groups with regard to the density of
microbubbles, we believe that in the presence of only very few microbubbles in
the renal pelvis, contrast harmonic imaging may be more suitable. A
significant difference between the two groups based on the extent of renal
pelvic dilatation, the right or left kidney, and the scan
position—ventral or dorsal—could not be observed (p >
0.05).
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In the kidney—ureter image units from eight (15%) of 54 patients, reflux was detected on one or both of the harmonic imaging modalities but not on fundamental imaging. Two instances of reflux were only into terminal ureters, but in six patients, microbubbles were detected in the renal pelvis. None of these refluxes were visualized in the fundamental mode even when the fundamental mode was switched on after reflux was seen with harmonic imaging. In seven of eight refluxes, the density of microbubbles was very low (score = 1), and in five of six, the renal pelvis was not dilated, suggesting that discrete reflux into a nondilated renal pelvis can be better detected with harmonic imaging. Reflux diagnosed with one or more of the imaging modalities was treated according to the local protocol by the referring pediatrician or urologist.
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The high sensitivity and specificity of voiding urosonography, using the same contrast medium as in this study, as compared with radiological reflux diagnosis has been shown in several other studies [1,2,3,4,5]. In these studies, of the total number of kidney—ureter units found to have reflux, the reflux was detected only by the sonographic reflux examination in 18% (32/175). This rate is higher than the 10% (17/175) of kidney—ureter image units that were found to have reflux only in the radiological reflux examination [11]. Thus, using the fundamental imaging modality for the purpose of comparison can be justified.
In our study, more cases of reflux were diagnosed by using harmonic imaging than were identified in the fundamental imaging mode. This high diagnostic yield can be attributed to the higher sensitivity of this new sonographic technology. However, it is necessary to note that the contrast-enhanced scanning time in the fundamental imaging mode was reduced by half to one third when tissue and contrast harmonic imaging were also being used, so that the examination time would not be inadvertently prolonged. To use the same transducer for all modalities, we had to refrain from using a 5-MHz transducer that had proved to be optimal for scanning children in the fundamental mode [2] because it had no harmonic option at the time of the study. These two factors may also have played some role in the lower reflux detection rate in the fundamental imaging than in the harmonic modalities.
In conclusion, tissue harmonic imaging was found to be superior in the evaluation of both the retrovesical space and the renal pelvis, at the same time producing striking images of the microbubbles. It is crucial to know that substantial diagnostic improvement of voiding urosonography can be achieved even without the contrast harmonic option, because each option represents an additional cost factor. The potential consequences of the application of harmonic imaging in the diagnosis of vesicoureteral reflux could be increased sensitivity combined with a reduction in contrast media dose and in cost, duration of learning curve, and examination time [12]. When both fundamental and harmonic imaging options are available, we recommend harmonic imaging for the contrastenhanced sonographic diagnosis of reflux.
Acknowledgments
We thank T. Friede, Department of Medical Biometry, University of
Heidelberg, for his assistance in the statistical analysis.
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