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Renal vein Doppler ultrasound of maternal

kidneys in normal second and third trimester
pregnancy
Article in British Journal of Radiology August 2003
DOI: 10.1259/bjr/81976752 Source: PubMed

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The British Journal of Radiology, 76 (2003), 444447

DOI: 10.1259/bjr/81976752

2003 The British Institute of Radiology

Renal vein Doppler ultrasound of maternal kidneys in normal

second and third trimester pregnancy
CI, MD and 2A KARABULUT, MD
N KARABULUT, MD, A BAKI YAG

1
1

Department of Radiology, Pamukkale University Hospital, 20010, Denizli and 2Clinic of Obstetrics and Gynaecology,
Denizli State Hospital, 20010, Denizli, Turkey

Abstract. 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,
0.300.10 versus 0.440.06 in the right (p,0.001), and 0.360.11 versus 0.410.07 in the left kidney
(p50.03). There was an inverse correlation between the grade of pelvicalyceal dilatation and the venous
impedance indexes in both kidneys in pregnant women (r520.62, p,0.001 for the right kidney, and r520.38,
p50.05 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.

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 [36].
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.

Subjects and methods

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, 1938 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 nonpregnant healthy women with a mean age of 25 years (age
range, 1932 years) were also studied with the same
technique. Informed consent was obtained from each
participant after a detailed explanation of the procedure.

Received 12 September 2002 and in revised form 3 January 2003,

accepted 9 April 2003.
Address correspondence to Nevzat Karabulut, MD, Hastane Cad.
Umut Apt. No: 5/3, 20010 Denizli, Turkey.
This study was presented at ECR-2003, March 711 2003, Vienna,
Austria.

444

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
The British Journal of Radiology, July 2003

Renal vein Doppler ultrasound of maternal kidneys

(Logiq 500 Pro, General Electric, Milwaukee, WI) with

2.05.0 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
(610 mm), moderate (1115 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 (AB/A) was
calculated (Figure 1).

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 meanstandard 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 MannWhitney
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 KruskalWallis one way analysis of variance, and
those from left kidney with two different grade of
pyelocaliectasis was compared using MannWhitney 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.

Results
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 p50.03 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 (p50.01), but not in nonpregnant subjects (p50.13). In pregnant women, the
venous impedance indexes between second and third
trimester were slightly different in the right kidney
(p50.04), but no statistical difference was found in the
left kidney (p50.09).
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 (r520.62, p,0.001 for the right kidney, and
r520.38, p50.05 for the left kidney). The venous
impedance indexes were significantly different among the
pregnant women with different degree of pyelocaliectasis
Table 1. The mean venous impedance indexes in right and left
kidneys in pregnant and non-pregnant women
Group

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.
The British Journal of Radiology, July 2003

Pregnant women (n535)

Second trimester
(1426 week) (n513)
Third trimester
(2740 week) (n522)
Non-pregnant women (n524)

Impedance index
Right

Left

0.300.10
0.340.10

0.360.11
0.390.10

0.280.09

0.330.10

0.440.06

0.410.07

445

N Karabulut, A Baki Yagci and A Karabulut

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.

Table 2. The mean venous impedance indexes in pregnant

women with different degree of pyelocaliectasis
Pyelocaliectasis grade Right

0
1
2
Total

Left

Impedance index n

Impedance index

19
9
7
35

0.350.08
0.290.07
0.190.09
0.300.10

0.370.10
0.230.08

0.360.11

31
4

35

(p50.001 for the right, and p50.03 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).

Discussion
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 [36]. The
Doppler ultrasound of kidneys has been directed mostly
toward the main and intrarenal arteries for the evaluation
of ureteral obstruction [1013], and the mean intrarenal
arterial resistivity indexes have been shown to remain
unaffected by physiological pyelocaliectasis or altered
renal haemodynamics in pregnancy [35]. 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.
446

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 [35]. 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
The British Journal of Radiology, July 2003

Renal vein Doppler ultrasound of maternal kidneys

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 nonpregnant 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

The British Journal of Radiology, July 2003

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.

References
1. Horowitz E, Schmidt JD. Renal calculi in pregnancy. Clin
Obstet Gynecol 1985;28:2348.
2. Swanson SK, Heilman RL, Eversman WG. Urinary tract
stones in pregnancy. Surg Clin North Am 1995;75:12342.
3. Hertzberg BS, Carroll BA, Bowie JD, et al. Doppler US
assessment of maternal kidneys: analysis of intrarenal
resistivity indexes in normal pregnancy and physiologic
pyelocaliectasis. Radiology 1993;186:68992.
4. Kara SA, Toppare MF, Sarac E. Pyelocaliectasis and
intrarenal artery Doppler indices in uncomplicated pregnancies. Gynecol Obstet Invest 1999;48:1821.
5. Nazarian GK, Platt JF, Rubin JM, Ellis JH. Renal duplex
Doppler sonography in asymptomatic women during pregnancy. J Ultrasound Med 1993;12:4414.
6. Karabulut N, Karabulut A. Colour Doppler evaluation of
ureteral jets in normal second and third trimester pregnancy:
effect of patient position. Br J Radiol 2002;75:3515.
7. Bateman GA, Cuganesan R. Renal vein Doppler sonography
of obstructive uropathy. AJR Am J Roentgenol 2002;
178:9215.
8. Wichman K, Ryden G. Blood pressure and renal function
during normal pregnancy. Acta Obstet Gynecol Scand
1986;65:5616.
9. Peake S, Roxburgh H, Langlois SLP. Ultrasonic assessment
of hydronephrosis of pregnancy. Radiology 1983;146:16770.
10. Platt JF, Rubin JM, Ellis JH. Acute renal obstruction:
evaluation with intrarenal duplex Doppler and conventional
US. Radiology 1993;186:6858.
11. Platt JF, Rubin JM, Ellis JH. Distinction between obstructive
and nonobstructive pyelocaliectasis with duplex Doppler
sonography. AJR Am J Roentgenol 1989;153:9971000.
12. Rodgers PM, Bates JA, Irving HC. Intrarenal Doppler
ultrasound studies in normal and acutely obstructed kidneys.
Br J Radiol 1992;65:20712.
13. Platt JF, Rubin JM, Ellis JH, DiPietro MA. Duplex Doppler
US of the kidney: differentiation of obstructive from
nonobstructive dilatation. Radiology 1989;171:5157.
14. Rasmussen PE, Nielsen FR. Hydronephrosis during pregnancy: a literature survey. Eur J Obstet Gynecol Reprod Biol
1988;27:24959.
15. Beydoun SN. Morphologic changes in the renal tract in
pregnancy. Clin Obstet Gynecol 1985;28:24956.
16. Appleton CP, Hatle LK, Popp RL. Superior vena cava and
hepatic vein Doppler echocardiography in healthy adults. J
Am Coll Cardiol 1987;10:10329.
17. Platt JF. Duplex Doppler evaluation of native kidney
dysfunction: obstructive and nonobstructive disease. AJR
Am J Roentgenol 1992;158:103542.
18. Roobottom CA, Hunter JD, Weston MJ, Dubbins PA.
Hepatic venous Doppler waveforms: changes in pregnancy. J
Clin Ultrasound 1995;23:47782.

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