British Journal of Radiology (2003) 76, 444-447
© 2003 British Institute of Radiology
doi: 10.1259/bjr/81976752
Renal vein Doppler ultrasound of maternal kidneys in normal second and third trimester pregnancy
N Karabulut, MD1,
A Baki Ya
ci, MD and
A Karabulut, MD2
1 Department of Radiology, Pamukkale University Hospital, 20010, Denizli and 2 Clinic of Obstetrics and Gynaecology, Denizli State Hospital, 20010, Denizli, Turkey
Correspondence: Nevzat Karabulut, MD, Hastane Cad. Umut Apt. No: 5/3, 20010 Denizli, Turkey
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Abstract
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The flow pattern in intrarenal veins depends on renal parenchymal histology and cardiac physiology. The intrarenal venous impedance index obtained by Doppler ultrasound is related to compliance in vein, and can be helpful in the assessment of renal parenchymal compliance. The purpose of this study was to determine whether normal pregnancy has a significant effect on intrarenal venous blood flow, and assess if the physiological pyelocaliectasis causes a measurable reduction in venous impedance indexes in pregnant women. Doppler ultrasound of intrarenal veins was performed in 35 asymptomatic pregnant women in the second and third trimester of gestation, and in 24 non-pregnant healthy women. After grading the degree of hydronephrosis, venous impedance index was obtained from the interlobar veins. The venous waveforms in pregnant women showed diminished phasic oscillations owing to elevated pre-systolic flow. The mean venous impedance indexes in pregnant women were significantly lower than the values in non-pregnant subjects, 0.30±0.10 versus 0.44±0.06 in the right (p<0.001), and 0.36±0.11 versus 0.41±0.07 in the left kidney (p=0.03). There was an inverse correlation between the grade of pelvicalyceal dilatation and the venous impedance indexes in both kidneys in pregnant women (r=-0.62, p<0.001 for the right kidney, and r=-0.38, p=0.05 for the left kidney). An abnormally reduced venous impedance index in pregnant women can at least in part be explained by reduced vascular compliance from increased interstitial pressure subsequent to partial obstruction of ureters by the gravid uterus, and caution should be exercised in interpreting it as a sign of pathological ureteral obstruction.
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Introduction
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Extensive alterations occur in renal haemodynamics during pregnancy, and maternal pyelocaliectasis is a frequent finding. The differentiation of true renal obstruction from physiological pyelocaliectasis is important since renal colic is the most common painful non-obstetric condition for which hospitalization is required during pregnancy [1, 2]. Although ultrasound is frequently performed as the initial imaging study for the evaluation of renal colic, its specificity is limited owing to the pregnancy-related calyceal dilatation [2]. Doppler investigation of maternal kidneys and ureteral jet flows has been shown to be useful adjunct to grey scale ultrasound [3–6]. However, the Doppler ultrasound of kidneys has been directed mostly toward the main and intrarenal arteries, and the Doppler analysis of intrarenal veins in various renal diseases has not been investigated widely. In a recent study by Bateman and Cuganesen [7], intrarenal venous flow has been shown to be affected to a greater extent than the arterial flow in case of ureteral obstruction exhibiting reduced venous impedance index values on the obstructed side. The impedance index, equivalent of resistivity index in an artery, is mainly determined by the compliance in veins since normal venous resistance is negligible. It is calculated by subtracting the least diastolic flow from the peak flow signal and dividing by the peak flow value [7]. However, normal values for venous impedance index cannot be assumed to be the same during pregnancy, as changes in renal blood flow, haemodynamics and function are well known to occur in pregnancy [8]. In this study, we investigated whether normal pregnancy has a significant effect in intrarenal venous blood flow, and assessed if the physiological maternal pyelocaliectasis causes a measurable reduction in venous impedance indexes in pregnant women.
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Subjects and methods
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Study population
Study population was drawn from the patients undergoing routine obstetric ultrasound examination during a 2 month period. A total of 35 women with a mean age of 27 years (age range, 19–38 years) who denied a prior or current history of urinary obstruction or previous urological surgery and in whom renal ultrasound excluded evidence for nephrolithiasis, and solitary kidney were prospectively enrolled in this study. All women had singleton pregnancies between 14 weeks' and 40 weeks' (mean, 28.1 weeks') gestation. A control group of 24 non-pregnant healthy women with a mean age of 25 years (age range, 19–32 years) were also studied with the same technique. Informed consent was obtained from each participant after a detailed explanation of the procedure.
Doppler ultrasound
All pregnant women and healthy control subjects were examined by B-mode and duplex Doppler ultrasound using a commercially available colour Doppler scanner (Logiq 500 Pro, General Electric, Milwaukee, WI) with 2.0–5.0 MHz convex probe. Both kidneys were scanned in all women in the lateral decubitus position without hydrating the subjects or asking to empty bladder. Degree of hydronephrosis was graded on a scale from 0 to 3, indicating no pelvicalyceal dilatation (
5 mm), mild (6–10 mm), moderate (11–15 mm) and severe (>15 mm) sinus echo separation, respectively [9]. Apart from pyelocaliectasis, all kidneys were otherwise normal on ultrasound in both pregnant women and control subjects. Colour flow mapping was used to identify the renal interlobar or arcuate veins. During a brief period in which the subject held her breath the pulsed Doppler sample volume was positioned over the vessel of interest and at least three similar, sequential Doppler waveforms were obtained from the middle portion (middle one-third) of the kidney. This was done to keep the angle of incidence of the Doppler ultrasound beam as parallel to the investigated vessel as possible. Colour scale was adjusted as needed, and venous flow away from the transducer was assigned a blue colour, and depicted as negative. The pulse repetition frequency of the Doppler ultrasound beam was set according to the peak flow velocity avoiding aliasing. After measuring peak venous flow signal (A) and least flow signal (B), venous impedance index (A–B/A) was calculated (Figure 1
).
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Figure 1. Doppler ultrasound of the right kidney in a 28-year-old non-pregnant woman shows normal phasic oscillations in the intrarenal veins with reduced pre-systolic component (small arrow). The intrarenal venous impedance index was 0.43. Large arrow indicates peak venous flow signal.
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Statistical analysis
The statistical analysis was performed with the Statistical Package for Social Sciences computer program version 9.0 (SPSS, Inc., Chicago, IL). The results were expressed as mean±standard deviation. Student t-test was used to determine if the venous impedance indexes were different between pregnant and non-pregnant women, and whether there were any differences between kidneys of pregnant women without pyelocalyceal dilatation and the kidneys of control group. Paired Student t-test was performed to investigate whether the impedance indexes were significantly different between right and left kidneys in pregnant women. The non-parametric Mann–Whitney U test was used to compare the venous impedance indexes in right and left kidneys in the control group, and to determine if the impedance indexes were significantly different between second and third trimester of gestation in pregnant women. In the pregnant women, the impedance indexes obtained from the right kidney with three different degree of pyelocaliectasis were compared using Kruskal–Wallis one way analysis of variance, and those from left kidney with two different grade of pyelocaliectasis was compared using Mann–Whitney U test. Correlation between the grade of hydronephrosis and impedance indexes was investigated by Pearson correlation test. p values less than or equal to 0.05 indicated a statistically significant difference.
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Results
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The mean intrarenal venous impedance indexes in pregnant and non-pregnant women are summarized in Table 1. The venous impedance indexes were significantly lower in pregnant women than the values in non-pregnant subjects (p<0.001 for the right and p=0.03 for the left kidney). The venous waveforms in pregnant women showed diminished phasic oscillations due to elevated pre-systolic flow (Figure 2). The difference in venous impedance indexes between right and left kidneys was significant in pregnant women (p=0.01), but not in non-pregnant subjects (p=0.13). In pregnant women, the venous impedance indexes between second and third trimester were slightly different in the right kidney (p=0.04), but no statistical difference was found in the left kidney (p=0.09).
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Figure 2. 24-year-old asymptomatic woman with 32 weeks' singleton gestation. Doppler ultrasound of the right kidney with grade 2 pyelocaliectasis shows flattened venous waveform and a reduced intrarenal venous impedance index (0.12) owing to elevated pre-systolic flow (small arrow). Large arrow indicates peak venous flow signal.
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Overall the collecting system dilatation was present in 20 (28.6%) of 70 kidneys in pregnant women, and it was more frequent and severe on the right side than on the left. There were no cases of severe or high-grade physiological hydronephrosis. There were 7 (20%) grade 2, and 9 (25.7%) grade 1 pyelocaliectasis in right kidneys, and there were only 4 (11.4%) grade 1 pyelocaliectasis in left kidneys. No collecting system dilatation was seen in control subjects and in 19 (54.3%) right and 31 (88.6%) left kidneys in pregnant women. Table 2 reveals the mean venous impedance indexes for kidneys of pregnant subjects, grouped according to presence and degree of pyelocaliectasis. There was an inverse correlation between the grade of pelvicalyceal dilatation and the venous impedance indexes in both kidneys in 35 pregnant women (r=-0.62, p<0.001 for the right kidney, and r=-0.38, p=0.05 for the left kidney). The venous impedance indexes were significantly different among the pregnant women with different degree of pyelocaliectasis (p=0.001 for the right, and p=0.03 for the left kidney). The venous impedance indexes were also reduced in the kidneys of pregnant women without pyelocalyceal dilatation compared with the kidneys of control group (p<0.001).
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Discussion
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Maternal pyelocaliectasis is a frequent finding during pregnancy, and differentiation from pathological renal obstruction can be difficult. Doppler investigation of maternal kidneys and ureteral jet flows has been shown to be useful adjunct to grey scale ultrasound [3–6]. The Doppler ultrasound of kidneys has been directed mostly toward the main and intrarenal arteries for the evaluation of ureteral obstruction [10–13], and the mean intrarenal arterial resistivity indexes have been shown to remain unaffected by physiological pyelocaliectasis or altered renal haemodynamics in pregnancy [3–5]. On the other hand, the Doppler analysis of intrarenal veins in various renal diseases has not been investigated widely. Only recently has the venous Doppler ultrasound technique been usefully applied to evaluation of ureteral obstruction, in which intrarenal venous flow has been shown to be affected to a greater extent than the arterial flow showing elevated peak flow and minor reduction in pre-systolic flows [7]. However, to date no studies have addressed the use of venous Doppler ultrasound in pregnancy. This study is the first investigating the changes in intrarenal venous impedance in pregnant women.
In this study, the occurrence of more frequent maternal pyelocaliectasis in the right kidney is in agreement with previous studies reporting that gestational hydronephrosis was seen early on pregnancy and more prominent on the right possibly due to the dextrarotation of the uterus [9]. Although the venous impedance index values were significantly reduced in both kidneys in pregnant women, the reduction was more prominent in the right kidney (Table 1
) suggesting a reduced parenchymal compliance owing to pyelocaliectasis. The venous impedance indexes in control subjects (0.44 for the right kidney, 0.41 for the left kidney) were similar to the values in a previous study by Bateman and Cuganesen [7] who found the mean impedance indexes of 0.45 and 0.43 for the right and left kidneys, respectively.
There have been two main mechanisms postulated to explain maternal pyelocaliectasis in pregnancy: an obstructive theory that attributes dilatation to compression by the enlarging gravid uterus and a hormonal theory that relates dilatation to smooth muscle relaxation in the ureteral wall, subsequent to high progesterone levels [9, 14, 15]. Our data in this study at least in part support the mechanical obstruction theory. The impedance index is determined by both resistance and compliance of a vessel. Because normal venous resistance is negligible, the impedance index is mainly related to compliance in veins [7]. The decrease in venous impedance during pregnancy can be explained by reduced vascular compliance from increased interstitial pressure subsequent to partial obstruction of ureters by the gravid uterus. However, the flow pattern in intrarenal veins is affected not only by renal parenchymal histology, but also by the extensive alterations in cardiac physiology. Because our study was directed only to intrarenal veins, the effect of cardiac and haemodynamic changes altering the venous flow in the inferior vena cava cannot be excluded completely. In pregnant women the increase in blood volume and cardiac output is accommodated by a pronounced decrease in peripheral vascular resistance. Because there is a reversed flow in the inferior vena cava during right atrial contraction [16], high arterial flow into the kidneys throughout diastole must be accommodated by compliance of the veins, manifesting as end diastolic flow reduction in the venous waveform. If the veins become less compliant due to increased interstitial pressure, the end diastolic flow reduction is diminished, producing a nearly flat waveform. This observation contradicts the previous studies in pregnant women, which showed no significant change in arterial resistivity indexes with varying degree of pyelocaliectasis, the kidney (right versus left) investigated, or the stage of pregnancy, discounting the possibility of complete obstruction as a cause of pyelocaliectasis [3–5]. However, it was shown that partial mild obstruction might not elevate the arterial resistivity indexes [17]. Furthermore, the intrarenal venous flow has been shown to be affected to a greater extent than the arterial flow in case of ureteral obstruction [7]. Similar to our findings, Roobottom et al [18] reported decreased hepatic venous pulsatility during pregnancy, which became completely flat with increasing gestational age. They attributed this alteration to increased cardiac output coupled with the increase in portal velocity and the pressure effect of the enlarged gravid uterus. Therefore, on the basis of our findings, we can postulate that partial obstruction of ureters by the gravid uterus increases the interstitial pressure that exerts a possible compression over the intrarenal veins owing to the low stretching of the renal capsule. This mechanism also explains the lower impedance value in the right kidney that showed more frequent and severe pelvicalyceal dilatation, and the negative correlation between the degree of pelvicalyceal dilatation and venous impedance index. However, the observation that the impedance indexes in kidneys without collecting system dilatation were also significantly reduced compared with normal control subjects indicates that alteration in venous flow occurs even in the absence of maternal pyelocaliectasis. The modified blood flow in inferior vena cava either from cardiovascular alterations during pregnancy or pressure effect of the enlarged gravid uterus might also contribute to flattened waveform pattern in intrarenal veins, and explain reduced impedance indexes in the absence of maternal pyelocaliectasis. Whatever the underlying mechanism is, the arterial resistivity remains the same during pregnancy, but intrarenal venous flow is affected regardless of collecting system dilatation and venous waveform becomes almost flat similar to that of hepatic veins in pregnant women.
In our study, the venous impedance indexes (0.30 for the right kidney, 0.36 for the left kidney) in pregnant women were lower than the mean value of 0.38 reported in obstructed kidneys [7]. Although the difference of 0.06 between right and left kidneys was statistically significant, it is much lower than the average difference of 0.42 between obstructed and unobstructed kidneys in non-pregnant population [7]. This can be explained by partial obstruction and the bilaterality of the process to some extent. This explanation is also supported by the recent study in which the reduction in venous impedance index on the obstructed side compared with unobstructed side was significant in patients with stones of 3 mm or larger, but no significant difference was found between two sides in patients with smaller stones [7].
A relative limitation of our study is the lack of definitive proof of the absence of other causes of ureteral obstruction that may cause pyelocaliectasis in pregnant women. However, we limited our study to asymptomatic pregnant women who denied a prior or current history of urinary obstruction. Another limitation is that we did not investigate the waveform in the inferior vena cava and main renal veins which might likely be altered in pregnant women and affect the intrarenal venous waveform.
In conclusion, the venous waveforms in pregnant women showed diminished phasic oscillations due to elevated pre-systolic flow causing a significant reduction in intrarenal venous impedance indexes. The reduction was evident even in the absence of maternal pyelocaliectasis, but the degree of reduction correlated with the grade of pelvicalyceal dilatation. Caution should be exercised in interpretating an abnormally reduced venous impedance index as a sign of pathological ureteral obstruction in pregnant women. Further studies in larger series are warranted to test the accuracy and reproducibility of this observation in pregnant women with and without pathological obstruction and to evaluate when the pregnancy related alteration in venous flow returns to normal.
Received for publication September 12, 2002.
Revision received January 3, 2003.
Accepted for publication April 9, 2003.
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Abstract
Introduction
