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1
Discipline of Medicine, University of Newcastle, Callaghan Campus, Callaghan,
New South Wales, 2308 Australia.
2
Department of Medical Imaging, John Hunter Hospital, Locked Bag 1, Newcastle
Region Mail Center, 2310 Australia.
Received March 20, 2001;
accepted after revision October 16, 2001.
Address correspondence to G. A. Bateman.
Abstract
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SUBJECTS AND METHODS. Twelve patients with clinical evidence of acute obstructive uropathy were referred for helical CT to confirm the diagnosis and to provide a gold standard by which we could evaluate the sonographic findings in the 12 test patients. Twelve patients without renal disease served as a control group. Doppler sonography of the interlobar arteries and veins of both kidneys then was performed, with the sonographer unaware of which kidney had an obstruction. Peak venous flow measurements and arterial resistive and venous impedance indexes were obtained. The impedance indexes of the obstructed and unobstructed kidney were compared for each patient.
RESULTS. The mean arterial resistive indexes of the obstructed kidneys were larger than those of the unobstructed kidneys, 0.67 ± 0.08 and 0.62 ± 0.05, respectively (p = 0.05). The venous impedance indexes comparing obstructed and unobstructed sides were 0.38 ± 0.25 and 0.80 ± 0.25, respectively, a statistically significant result (p = 0.0002). On average, the peak venous flow signal in the obstructed kidney was 69% higher than that of the unobstructed kidney (p = 0.04) and 86% higher than that of the peak venous flow signal in the control group (p = 0.005).
CONCLUSION. Renal obstruction alters the venous flow to a greater extent than the arterial flow, and a comparison between the venous flow in the obstructed and unobstructed kidneys may improve diagnostic accuracy.
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Dampening of the hepatic vein signal has been observed in patients with acute and chronic liver disease and has been attributed to reduced hepatic compliance [4]. In acute renal obstruction, pressure within the collecting system increases substantially, and a reduction in renal parenchymal compliance would be expected to rapidly ensue. We believed that the mechanism of dampening of hepatic venous pulsatility would be directly applicable to the kidney. Thus, we tested the hypothesis that acute obstruction of the renal collecting system reduces the intraparenchymal renal compliance and thereby affects the intraparenchymal venous blood flow to a greater degree than the arterial flow.
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Control Group
No significant difference between the right or left kidneys was found in
either the arterial resistive or venous impedance indexes or peak flows. The
peak venous flow rate was always significantly lower than the arterial flow
rate, and on average, the arterial rate was twice the venous rate.
Figure 1 shows the interlobar
arterial and venous blood flow in 54-year-old man who had no evidence of renal
disease. Because the interlobar arterial blood flow was toward the transducer,
we depicted it as positive and the venous flow, which was moving away from the
transducer, as negative. The venous signal showed a pronounced reduction in
flow in the presystolic portion of the cardiac cycle corresponding to the
atria ejection pressure wave that causes a momentary reduction in flow out of
the kidney.
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Unobstructed Kidneys
The unobstructed kidneys showed an 81% higher venous impedance index than
the combined right and left kidneys of the control group (p <
0.0001). All other findings showed no significant differences.
Obstructed Kidneys
In the obstructed side, the mean size of the obstructing stone was 3.5
± 1.0 mm. The mean arterial resistive index on the obstructed side was
0.67 ± 0.08, which was, on average, 0.05 larger than the index on the
unobstructed side and therefore statistically significant (p = 0.05).
The corresponding obstructed mean venous impedance index was 0.38 ±
0.25, which was, on average, 0.42 less than the mean unobstructed impedance
index; this result was also statistically significant (p = 0.0002).
The venous signal in the obstructed kidney of the 54-year-old man depicted in
Figure
2A,2B
showed an elevated peak flow and a minor reduction in presystolic flow. The
Doppler sonogram of the corresponding unobstructed kidney showed a reduced
presystolic flow and a normal peak flow.
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When we took the size of the stone into account, we found that the venous impedance index was always significantly less on the obstructed side than on the unobstructed side in patients with stones of 3 mm or larger. We found no significant difference in venous impedance index between the sides in two patients with stones of 2 mm. In reviewing the CT scans, we saw little evidence of collecting system dilatation. Furthermore, in one patient, we saw a normal ureteric jet on the same side as the stone, confirming that there was no significant obstruction.
The comparison between the peak arterial and venous flows and stone size is summarized in Table 3. Overall, a larger venous flow signal, 86% higher than in that in the control patients (p = 0.005), was noted, with a 69% higher flow than that in the unobstructed kidneys (p = 0.04). The actual difference in peak flows only became apparent for patients with stones of 4 mm or larger; for patients with stones smaller than 4 mm, the peak flows were not significantly different. No difference in the peak arterial flow signal was found among the groups, irrespective of the variables.
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Because of difficulties associated with using the arterial resistive index as a measure of acute obstruction, our study focused on the venous side of the vascular tree. Measuring the pulsatility of the venous signal in the hepatic veins has been suggested as a method of identifying disease in the liver because of the changes in compliance that are produced. The pulsatility of the hepatic venous signal reflects the compliance of the liver tissue because most pathologies expand the liver parenchyma within its confining capsule, reducing compliance and resulting in dampening of the hepatic venous signal [11].
A similar mechanism is believed to occur in the kidney. Changes in right-sided atrial pressure produce a triphasic waveform with the atrial and occasionally the ventricular components of the venous pulse producing a reversed flow in the inferior vena cava [12]. The reversal of flow at the end of diastole (from atrial contraction) is propagated into the renal vessels (Fig. 1). From the arterial data, it is known that there is a high flow of blood into the kidney throughout diastole and that a temporary reduction in outflow must be accommodated by enlargement of the veins (i.e., compliance). If the veins are rendered incompliant because of an increase in interstitial pressure, this end diastolic flow reduction is reduced. As a corollary, if compliance is increased, venous pulsatility also increases.
In our study, a reduction in venous pulsation did occur in the obstructed kidneys compared with the venous pulsation in the kidneys of the control group. This finding lacked statistical significance, suggesting that the isolated venous impedance measurement may not be useful. However, a significant difference in venous impedance between the unobstructed kidney and the obstructed kidney of the same patient was observed. A mean difference of 0.42 (p = 0.0002) was seen, indicating that direct comparison between the two kidneys may be useful. The unobstructed kidneys appear to be substantially altered in their venous pulsatility by the disease in the contralateral kidney. Using an acutely obstructed unilateral lamb model, Kim et al. [13] showed that the total blood flow in the obstructed side decreased by 29% and that the total blood flow increased by 22% in the unobstructed kidney. This finding suggests increased resistance on the obstructed side and reduced resistance on the unobstructed side and indicates that there is a considerable effect produced by contralateral obstruction on the unobstructed kidney.
The findings raise the question, What is the impedance index measuring on the venous side? On the arterial side, it is noted that the impedance or resistive index is not only a measure of resistance [14]. Doppler sonographic indexes are hemodynamic measurements that primarily depend on the patient's vascular compliance and thus correlate with the patient's age and arterial pulse pressure [15]. Therefore, the impedance index measures both resistance and compliance of a vessel simultaneously. Difficulties arise if both variables are altered by the same pathologic process. This situation occurs in the case of renal obstruction on the obstructed side because increased interstitial pressure raises the resistance and reduces the vascular compliance. The lower the compliance, the lower the resistive index for the same degree of vascular resistance [16]. In fact, when there is no vascular compliance, the renal arterial resistive index has been found to be independent of vascular resistance [16].
The unimpressive results obtained when arterial resistive indexes are used to predict obstruction may be explained by the fact that the reduced vascular compliance reduces the sensitivity of the test. On the venous side, the normal resistance is negligible, and the pulsatility directly relates to compliance. As we noted, there is a reduction in resistance in the unobstructed kidney, but in our study, the arterial resistive index was not sensitive to this change. In comparing the reduction in arterial impedance in patients with obstructions with the arterial impedance in the control group, we found no significant difference. The solution to the lack of sensitivity of the arterial resistive index to the reduction in resistance in the unobstructed kidneys appears to be the same as that for the poor sensitivity to the increased resistance (i.e., the reduced resistance is matched by an equal increase in compliance).
Although venous resistance is thought to be minimal, it may not be in patients with highgrade obstruction. The classic teaching is that the first phase of ureteral obstruction lasts from 1 hr to 1 hr 30 min and is characterized by a rise in both ureteral pressure and renal blood flow mediated by afferent arteriole dilatation. In the second phase, renal blood flow declines and ureteral pressure continues to rise; this phase lasts up to 5 hr and is mediated by efferent arteriole vasoconstriction. After 5 hr, the third phase begins with a further decline in renal blood flow, a progressive decrease in ureteral pressure, and in both afferent and efferent vasoconstriction [5]. At the stage measured in our study (mean, 11 hr), all patients should have had reduced total renal blood flow (phase 3). Counterintuitively, we discovered that the peak arterial flow in the obstructed kidneys was similar to that in the unobstructed side despite the presumed reduction in the total blood flow volume in the obstruction. The total blood flow is equal to the average flow rate (approximately one half the peak flow) multiplied by the cross-sectional area of the vessel, and both variables may change in obstruction.
Normal peak venous flow in the interlobar veins of the unobstructed kidneys and in the kidneys of the control patients is, on average, half as fast as the flow in the interlobar arteries. A larger cross-sectional area of the veins must exist; otherwise, equal blood flow volumes into and out of each kidney would not be maintained. In the obstructed kidneys with stones of 4 mm or larger, the peak venous flow mean was 34 ± 24 cm/sec compared with 14 ± 3 cm/sec for the peak venous flow mean on the unobstructed side (p = 0.02), suggesting considerable venous compression. If the arterial and venous peak flows are equal in obstructed kidneys and if the total inflow and outflow volumes are also equal, the vessel cross-sectional areas must be the same size (i.e., a reduction in normal venous cross-section). The highest venous flow that we found, 84 cm/sec in a 54-year-old man with renal obstruction, is seven times the flow in the veins of the unobstructed kidneys and two and one half times the peak arterial flow, suggesting the veins on the obstructed side in this patient were much smaller than the arteries; otherwise, total flow volumes would not have balanced.
The resistance in a vessel is dependent on the fourth power of the radius; the veins in patients with high-grade obstructions may begin to offer considerable resistance to flow. The resistance in a narrowed vessel is dependent not only on the radius but also on the length of the stenosis. In arteries, stenoses are often short, and the length can be ignored, but the entire length of a compressed vein would contribute to the elevated resistance, and thus a lower grade stenosis may become a resistor. The glomerular blood flow rate and hydraulic pressure in the glomerular capillary are governed by the resistances of the afferent and efferent arterioles [17], and as we previously described, the second and third phases of obstruction are characterized by increased resistance in the vessels after the glomerular capillary. Classically, this resistance is said to be completely attributable to efferent arteriolar constriction, but substantial venous compression may also account for some of the increased resistance. Similar findings, albeit in a different organ, have recently been reported [18]: Venous resistance was found to increase when the compliance was substantially reduced in the brains of patients with normal-pressure hydrocephalus. Further investigation is warranted to quantify the raised resistance in the venous outflow of obstructed kidneys to see if this phenomenon adds to the postglomerular resistance elevation found in obstructive uropathy.
We acknowledge that there are limitations in our study. CT is an excellent gold standard, and it is unlikely that our findings are compelling enough to supplant this more sensitive method of determining the primary diagnosis. For example, in our study, stones of less than 3 mm were not visualized. However, the data suggest that renal vein Doppler sonography may measure parenchymal pressure and the degree of obstruction, which may relate to the risk of parenchymal injury. Further, unobstructive 2-mm stones may pass unaided. In cases in which the stone is not visible on conventional radiography, sonographic follow-up may be useful. The number of patients in our study was not large, but the measurement of both right and left kidneys in the control group doubled the available control data and the high degree of significance found in the test group, we believe, warrants a preliminary report.
Formal Doppler sonographic angles were not attempted, and thus the velocities were not corrected to give absolute velocities. This omission has no effect on the calculated impedance index, but in the case of the arterial and venous velocities, the maximum velocities would be underestimated in proportion to the cosine of this angle. The Doppler sonographic angle was kept to a minimum by selecting mid pole vessels that were as parallel to the beam as possible. An estimated maximal angle of 15° would give an error of only 5% (cosine 20° = 0.94). We believed that this error was insignificant compared with other sources of error, such as different operators attempting to reproduce insonation of the same order of vessel in different patients. The practical difficulties of seeing such small compressed vessels in patients experiencing discomfort meant that a more accurate estimate of the direction of flow was often not possible.
It is unlikely that our findings will apply exclusively to renal obstruction; many diseases potentially will limit compliance in the kidney. However, the findings would appear to open a new field of research into the pathophysiology of renal diseases. As an example, the arterial resistive indexes of patients with preeclampsia of pregnancy are known to be significantly lower than those of nonhypertensive patients [19] despite the findings of substantially reduced total blood flow and thus elevated resistance in the hypertensive group [20]. The solution suggested for this apparent paradox is that a large reduction in renal parenchymal compliance could make the resistive index insensitive to the raised resistance. Severely compromised renal vein drainage could cause the hypertension (i.e., hypertension attributable to renal ischemia).
The compliance of the vessels in the kidney is reduced by ureteric obstruction. A corresponding increase in vascular resistance is seen. The arterial resistive index is relatively insensitive to the simultaneous increase in resistance and reduction in compliance, but the venous impedance index appears to be a more sensitive measure of the physiologic changes.
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