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Doppler Velocimetry of Maternal Renal

Circulation in Pregnancy-Induced
Hypertension

Hidehiko Miyake, MD, Akihito Nakai, MD, Tatsuo Koshino, MD, Tsutomu Araki, MD

Department of Obstetrics and Gynecology, Tama Nagayama Hospital, Nippon Medical School, 1-7-1 Nagayama,
Tama-shi, Tokyo 206-8512, Japan

Received 20 February 2001; accepted 22 May 2001

ABSTRACT: Purpose. The purpose of this study was


to evaluate whether the Doppler waveforms of the
maternal main renal, segmental, and interlobar ar-
H ypertension develops during pregnancy in
about 4 8% of nulliparous women. The hy-
pertensive disorders complicating pregnancy are
teries are altered in women with pregnancy-induced associated with substantial morbidity and mor-
hypertension (PIH) compared with healthy pregnant
tality rates. Despite improvements in obstetric
women.
care, these disorders are the second leading cause
Methods. Flow waveforms of the maternal main
renal, segmental, and interlobar arteries were ob- of maternal death.1 The perinatal mortality rate
tained from 42 healthy pregnant women between 24 is also increased as a consequence of placental
and 41 weeks of gestation and 21 women with PIH insufficiency, preterm delivery, and placental
between 28 and 40 weeks of gestation using pulsed separation.
Doppler sonography. We used spectral analysis to The renal vascular pathologic condition of
measure the peak systolic and end-diastolic velocities pregnancy-induced hypertension (PIH) is associ-
and the acceleration time. The presence or absence of ated with glomerular capillary endotheliosis.2
the normal early systolic compliance peak-reflective- The constricted vascular bed in the kidney in PIH
wave complex (ESP) was assessed in only the main diminishes the renal plasma flow and glomerular
renal artery.
filtration rate.2 Several Doppler sonographic
Results. The acceleration times of the segmental
studies of renal circulation in healthy pregnant
and interlobar arteries were significantly prolonged in
the PIH group compared with those in the healthy women3 5 and women with PIH6 9 have been
pregnant women. Of the 21 women with PIH, 3 performed, but the differences in Doppler indices
showed loss of the ESP in the renal artery, but these between the 2 groups have been inconsistent.
changes were not significant. Hemodynamically significant arterial stenoses
Conclusions. Decreased systolic acceleration and cause changes in velocity waveforms that can be
the absence of ESP, the hemodynamic indicators for detected with Doppler sonography in distal con-
significant proximal stenosis, suggest that severe tiguous arteries. Kotval10 reported such changes
stenosis or continuous vasospasm in the proximal in peripheral arteries and called them tardus-
arteries, such as the main renal or segmental artery, parvus Doppler waveforms. In the poststenotic
may be implicated in the pathogenesis of PIH. ã 2001
region, these phenomena are observed on Dopp-
John Wiley & Sons, Inc. J Clin Ultrasound 29:
ler sonography as a prolonged acceleration time,
449 455, 2001.
diminished systolic acceleration, and loss of the
Keywords: acceleration time; Doppler ultrasonogra-
normal early systolic compliance peak-reflective-
phy; pregnancy-induced hypertension; renal circula-
wave complex (ESP).10 The usefulness of these
tion
indices in the evaluation for significant proximal
stenosis in the renal circulation and acute renal
allograft rejection has been suggested.11,12 Nakai
Correspondence to : H. Miyake
et al,13 who used Doppler sonography to evaluate
ã 2001 John Wiley & Sons, Inc. the maternal renal arterial circulation, demon-

VOL. 29, NO. 8, OCTOBER 2001 449


MIYAKE ET AL

strated a prolonged acceleration time and de- placed over the investigated vessel. Angle-cor-
creased systolic acceleration in the interlobar rected velocity waveforms were obtained in each
arteries of women with PIH. The results sug- kidney; the insonation angles were less than 30°
gested that severe stenosis or permanent vaso- during a period of suspended respiration. The
spasm in proximal arteries might be implicated sample volume of the Doppler system was set at 3
in the pathogenesis of PIH. The measurements in mm, and a 100-Hz high-pass filter was used to
that study, however, were restricted to the in- reduce the noise from the pulsating arterial wall.
terlobar arteries. Pulsed Doppler waveforms were displayed at
In the present study, we evaluated whether the sweep speeds of 40 80 mm/second. All scans were
Doppler waveforms of the maternal main renal, performed by the same operator.
segmental, and interlobar arteries are altered in Spectral analysis in the main renal artery, in
women with PIH. an isolated segmental artery, and in an isolated
interlobar artery included measurements of the
peak systolic and end-diastolic velocities and the
PATIENTS AND METHODS acceleration time. The presence or absence of the
normal ESP was assessed in only the main renal
Between August 1999 and March 2000, we eval- artery because in the segmental and the interlo-
uated the Doppler velocity waveforms in the renal bar arteries, the ESP is commonly absent in
arteries bilaterally in 47 pregnant women without pregnant women.7,13 Values were calculated with
PIH between 24 and 41 weeks of gestation and 21 the built-in software of the scanner by placing
patients with PIH between 28 and 40 weeks of electronic calipers on the Doppler tracing dis-
gestation who were seen at our hospital. The preg- played on the image monitor. At least 3 Doppler
nant women without PIH were randomly chosen waveforms were recorded in sequence, and the
from outpatients who visited our hospital. We ex- best tracing obtained in each artery was selected
cluded from the study 5 pregnant women without for analysis. The peak systolic and end-diastolic
PIH because they had existing renal problems such velocities were measured at the apex of the
as significant hydronephrosis or horseshoe kid- highest systolic peak and at the end of diastole,
ney. However, we did not exclude women because respectively. The acceleration time was measured
of technical reasons such as an inability to iden- from the beginning of the systolic upstroke to the
tify the renal vessels. Patients were included in highest systolic peak in the waveform; any break
the study only if PIH had been diagnosed less in the systolic upstroke before it reached its peak
than 1 week previously and the patient had not was ignored. The systolic acceleration was cal-
begun antihypertensive treatment at the time of culated by dividing the peak systolic velocity
the Doppler sonographic study. None of the during this same interval by the acceleration
women in the study had a history of renal disease time. Resistance index (RI) was calculated as
or essential hypertension. All participants pro- follows: (peak systolic flow velocity) end-diastolic
vided written informed consent, and the study velocity)/peak systolic velocity.
was approved by the institutional review board. All data except for the presence or absence of
PIH was defined as a blood pressure elevation ESP were expressed as mean ‹ standard devia-
to higher than 140/90 mm Hg or a rise in either tion. The unpaired t-test was used to compare the
the systolic (by >30 mm Hg) or diastolic (by >15 values within each study group. The significance
mm Hg) values over the baseline blood pressure of the presence or absence of ESP was analyzed
before 16 weeks of gestation in at least 2 mea- by the chi-squared test. Regression analysis was
surements obtained 6 hours apart. used to evaluate relationships between Doppler
Sonography was performed using an EUB-555 indices and diastolic arterial blood pressure. A p
ultrasound scanner (Hitachi, Tokyo, Japan and a value of less than 0.05 was considered to be sta-
3.5-MHz convex-array transducer). Each subject tistically significant. The selection of an appro-
was placed in the left lateral decubitus position, priate cut-off value for acceleration time in the
and real-time imaging of the kidneys was per- interlobar artery was determined using a re-
formed bilaterally to rule out gross abnormalities ceiver operating characteristic curve.
in renal size, shape, and echogenicity. The kid-
neys were then scanned in the longitudinal plane
from a posterior approach. The course of the main RESULTS
renal artery and its branches, the segmental and
interlobar arteries, was determined with color The characteristics of the healthy subjects and
Doppler flow mapping. The Doppler gate was then the patients are given in Table 1. Gestational age
450 JOURNAL OF CLINICAL ULTRASOUND
MATERNAL RENAL CIRCULATION IN PREGNANCY-INDUCED HYPERTENSION

FIGURE 1. Spectral analyses show waveforms obtained in the renal artery (A), a segmental artery (B), and an interlobar artery (C) in healthy
pregnant women compared with those in the renal artery (D), a segmental artery (E), and an interlobar artery (F) in women with pregnancy-
induced hypertension (PIH). In healthy pregnant women, the waveform of the renal artery demonstrates early systolic compliance peak-reflective-
wave complex (ESP), and the angle of the early systolic phase is acute in all 3 vessels. In women with PIH, however, ESP of the renal artery is
absent, the angle of the early systolic phase in the renal, segmental, and interlobar arteries is more rounded, and the acceleration time is
prolonged in waveforms from both the segmental and interlobar arteries.

at the time of examination, maternal age, and the are shown in Figure 1. In both groups, there were
percentage of nulliparous women did not differ no significant differences in any of the Doppler
significantly between the healthy women and the indices between the right and left kidneys.
patients with PIH. The systemic arterial blood The peak systolic and end-diastolic velocities,
pressure differed significantly between the 2 RI, acceleration time, systolic acceleration, and
groups (p < 0.001). the presence or absence of ESP in the main renal
Typical Doppler waveform measurements in artery and the segmental and interlobar arteries
healthy pregnant women and in women with PIH in both groups are shown in Table 2.
VOL. 29, NO. 8, OCTOBER 2001 451
MIYAKE ET AL

TABLE 1
Characteristics of Healthy Pregnant Subjects and

p Value

<0.001
<0.001
0.66
0.10
0.05
Patients with PIH

Analysis of Doppler Waveforms of the Renal Artery, the Segmental Arteries, and the Interlobar Arteries in Healthy Pregnant Subjects and Patients with PIH
Healthy Patients
Subjects with PIH p

0.05
0.02
0.06

0.86
Patients with

43.5
PIH (n = 21)
Interlobar Artery
Patient Characteristic (n = 42) (n = 21) Value

‹
‹
‹

‹
‹
0.24
0.09
0.62

1.89
Age, years* 30.8 ‹ 3.5 31.7 ‹ 3.4 0.57

135.4

NA
Nulliparity, no. 28 (67) 15 (71) 0.92
patients (%) 
Gestational age 33.5 ‹ 4.1 35.2 ‹ 3.3 0.09
at examination, weeks*

Healthy Subjects

0.23 ‹ 0.05
0.08 ‹ 0.03
0.65 ‹ 0.07

5.02 ‹ 2.55
Arterial blood pressure,

55.5 ‹ 24.2
mm Hg*

(n = 42)
Systole 113.2 ‹ 20.5 154.2 ‹ 19.1 <0.001
Diastole 69.9 ‹ 7.9 98.7 ‹ 10.8 <0.001

NA
Abbreviation: PIH, pregnancy-induced hypertension.
*
Values are given as mean ‹ standard deviation. Statistical analysis
by unpaired t-test.

p Value

<0.001
<0.001
Three of the 21 patients with PIH showed loss

0.87
0.27
0.24
of the normal ESP in the renal arterial Doppler
waveforms compared with none of the healthy

0.10
0.03
0.06

2.17
47.8
Patients with
pregnant women; but these changes did not reach

PIH (n = 21)
Segmental Artery
significance (p = 0.06). In the women with PIH,

‹
‹
‹
‹
‹
0.38
0.14
0.64

3.58
128.2
the peak systolic velocity of the renal artery was

NA
significantly decreased (p = 0.01) and the accel-
eration time was significantly prolonged (p =
0.02) compared with those in the healthy preg-

Healthy Subjects

0.38 ‹ 0.08
0.13 ‹ 0.03
0.65 ‹ 0.06

7.10 ‹ 2.51
59.5 ‹ 23.6
nant women. However, these changes might be

(n = 42)
TABLE 2

due to the absence of ESP in 3 patients with PIH.


In the segmental and interlobar arteries of the

NA
patients with PIH, the acceleration times were
significantly prolonged (p < 0.001) and the sys-
tolic acceleration values were significantly de-

Values are given as mean ‹ standard deviation. Statistical analysis by unpaired t-test.
creased (p < 0.001) compared with those in the
p Value

0.01
0.08
0.21
0.02
0.06

0.06
healthy pregnant women. The other indices (ie,
peak systolic velocity, end-diastolic velocity, and
RI) in the segmental and interlobar arteries did
Abbreviation: PIH, pregnancy-induced hypertension; NA, not applicable.
11.92 ‹ 7.30
0.57 ‹ 0.10
0.17 ‹ 0.04
0.67 ‹ 0.11
Patients with
PIH (n = 21)

77.2 ‹ 63.4

not differ significantly between the 2 groups


Renal Artery

(Table 2).
Figure 2 illustrates the correlation between the
18
3

acceleration time in the interlobar artery and the


diastolic arterial blood pressure. The acceleration
Healthy Subjects

time increased significantly with the increase in


15.46 ‹ 5.21
0.67 ‹ 0.14
0.20 ‹ 0.05
0.70 ‹ 0.06
46.0 ‹ 12.2

diastolic arterial blood pressure. The receiver


(n = 42)

operating characteristic curve indicated that in


42

the interlobar artery, an acceleration time of


0

Statistical analysis by chi-squared test.

100 msec was considered the best cut-off point for


distinguishing the 2 groups, showing a sensitivity
Systolic acceleration, m/second2*
*

End-diastolic velocity m/second*


Peak systolic velocity, m/second

of 83% and a specificity of 92%.


Acceleration time, msec*
Patient Characteristic

Present, no. patients

DISCUSSION
Absent, no. patients
Early systolic peak 
Resistance index*

In a normal pregnancy, large increases in renal


plasma flow and glomerular filtration rate result
from renal vasodilatation in the second trimester,
*
 

followed by slight decreases in the third trimes-


452 JOURNAL OF CLINICAL ULTRASOUND
MATERNAL RENAL CIRCULATION IN PREGNANCY-INDUCED HYPERTENSION

FIGURE 2. Graph shows correlation between the acceleration time of the interlobar artery and the diastolic
arterial blood pressure. Open circles, healthy pregnant women; closed circles, women with pregnancy-in-
duced hypertension. These give the linear regression: AT = 2.2DBP)95; r2 = 0.52, where AT is acceleration
time (msec) and DBP is diastolic arterial blood pressure (mm Hg).

ter. In addition, plasma volume expansion occurs differ from those in healthy pregnant women,
with arteriolar vasodilatation followed by a de- even in the interlobar arteries that might be more
crease in arterial blood pressure.14 These renal likely than the proximal arteries to demonstrate
and cardiovascular adjustments are important increased resistance to blood flow.
for the successful outcome of the pregnancy. In In the present study, we examined the accel-
contrast, PIH is associated with increased eration time, the systolic acceleration, and the
peripheral vascular resistance in the maternal ESP, which are the hemodynamic parameters for
circulation.15 The increased peripheral vascular substantial upstream stenosis. Severe stenosis of
resistance in the kidneys decreases the renal an artery causes a pressure drop in the immedi-
plasma flow and glomerular filtration rate.2 ate poststenotic region, which results in a weak-
Therefore, considerable changes in the renal cir- ened pulse in the downstream arterial network
culation can be anticipated in patients with PIH that is clinically described as pulsus tardus (pulse
compared with women with a normal pregnancy. wave slow to rise) and pulsus parvus (small am-
Several investigators have attempted to eval- plitude pulse).18 In the poststenotic region, these
uate renal circulation by performing Doppler so- phenomena are observed with Doppler sonogra-
nography in healthy pregnant women3 5 and in phy as prolonged acceleration time, diminished
women with pre-eclampsia or PIH.6 9,16,17 Al- systolic acceleration, and loss of the normal
though these studies evaluated the renal vessels ESP.10 This principle is easily applied to the re-
that can be detected with Doppler sonography, nal arterial circulation. The evaluation of the
such as the main renal artery, the segmental tardus-parvus waveform for the diagnosis of re-
arteries, and the interlobar arteries, the results nal arterial stenosis was initiated, to our knowl-
have been inconsistent. The diagnostic strategies edge, with the work of Handa et al.11 These
found to be promising in some studies were not investigators found substantial decreases in sys-
uniformly successful in other laboratories. How- tolic acceleration distal to the renal arterial
ever, the parameters analyzed in these studies3 9 stenosis. The results of our study, which demon-
were restricted to the most common parameters strate prolonged acceleration time and dimin-
of distal vascular resistance, such as systolic-di- ished systolic acceleration in the segmental and
astolic ratio, RI, and pulsatility index. In our the interlobar arteries of women with PIH, are in
study, the waveform indices for downstream agreement with former observations of renal ar-
vascular resistance in patients with PIH did not terial stenosis in nonpregnant women.11,12 The
VOL. 29, NO. 8, OCTOBER 2001 453
MIYAKE ET AL

prolonged acceleration time and decreased sys- with PIH. This was because we selected only pa-
tolic acceleration in these arteries suggest the tients who were diagnosed with hypertension less
possibility that vasospasm is a pathogenic event than 1 week previously and who had not begun
for PIH and causes changes in the distal seg- antihypertensive treatment at the time of the
mental and interlobar arteries. In addition, be- Doppler study. However, we believe that our re-
cause the acceleration time of the interlobar sults provide new insight into the pathogenesis of
artery showed a positive correlation with the di- PIH and suggest the need for further study.
astolic arterial blood pressure, we speculated that
acceleration time could be effective as a routine
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