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(Radiology. 1999;213:423-428.)
© RSNA, 1999

Ultrasonography

Pulsed Doppler US Findings of Renal Interlobar Arteries in Pregnancy-induced Hypertension1

Akihito Nakai, MD, Hirobumi Asakura, MD, Atsuko Oya, MD, Akishige Yokota, MD, Tatsuo Koshino, MD and Tsutomu Araki, MD

1 From the Department of Obstetrics and Gynecology, Tama Nagayama Hospital, Nippon Medical School, 1-7-1 Nagayama, Tama-shi, Tokyo, 206-8512 Japan. Received May 1, 1998; revision requested July 6; final revision received February 11, 1999; accepted June 8. Address reprint requests to A.N. (e-mail: Nakai_Akihito/obgy@nms.ac.jp).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate whether Doppler ultrasonographic (US) velocimetry in renal interlobar arteries is altered in women with pregnancy-induced hypertension (PIH) compared with that in healthy pregnant and nonpregnant women.

MATERIALS AND METHODS: Flow waveform measurements in renal interlobar arteries were obtained in 39 nonpregnant women, 77 healthy pregnant women at 16–40 weeks gestation, and 15 women with PIH at 28–39 weeks gestation by using color and pulsed Doppler US.

RESULTS: In the nonpregnant group, the mean (± SD) peak systolic velocity, end-diastolic blood flow velocity, resistive index, and acceleration time were 0.34 m/sec ± 0.08, 0.14 m/sec ± 0.03, 0.62 m/sec ± 0.07, and 52.3 m/sec ± 13.7, respectively. In the healthy pregnant group, the peak systolic and end-diastolic blood flow velocities at 16 weeks gestation had decreased greatly by 40 weeks gestation. However, the values of other indexes in this group did not change with gestational age. In the PIH group, the acceleration time values were greatly prolonged compared with those in the other groups.

CONCLUSION: Acceleration time is one of the hemodynamic parameters of substantial upstream stenosis. These findings suggest that severe stenosis or continuous vasospasm in the proximal arteries, such as the main renal artery and segmental artery, might be implicated in the pathogenesis of PIH.

Index terms: Hypertension, 961.723 • Pregnancy, complications, 961.723 • Renal arteries, US, 961.12981, 961.12983, 961.12984 • Ultrasound (US), Doppler studies, 961.12981, 961.12983, 961.12984


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
In a normal pregnancy, a large increase in the renal plasma flow and glomerular filtration rate occurs as a result of renal vasodilatation, which decreases slightly in the third trimester. In addition, an increase in plasma volume occurs with arteriolar vasodilatation and with late decreases in arterial blood pressure (1). These renal and cardiovascular changes are important for the successful outcome of pregnancy. In contrast, pregnancy-induced hypertension (PIH) is associated with increased peripheral vascular resistance in the maternal circulation (2). Furthermore, the vascular pathologic condition in the kidneys of patients with preeclampsia has been amply demonstrated as being glomeruloendotheliosis (3). The physiologic consequence of the constricted vascular bed in the kidneys in preeclampsia is a diminished renal plasma flow and glomerular filtration rate (3). Therefore, considerable changes in the renal circulation can be anticipated in PIH compared with those in a normal pregnancy.

The development of color Doppler ultrasonography (US) has led to the possibility of evaluating kidney function in relation to changes in renal circulation. The possible use of this tool as a replacement for angiography was initially assessed in native renovascular disease (4–7) and in renal transplantation (8,9). In addition, several Doppler US studies (10–12) have been performed in healthy pregnant women and in women with PIH (13–16), although to date, the differences in renal arterial and intrarenal arterial Doppler indexes between normotensive and hypertensive pregnant women are ambiguous. However, authors (10–16) previously used only the most common parameters of distal vascular resistance, such as the systolic-diastolic ratio, resistive index, and pulsatility index.

The acceleration time is one of the hemodynamic parameters that is measured in several renal diseases. The usefulness of the acceleration time (or other related parameters such as the acceleration index) in the evaluation of possible substantial upstream stenosis (ie, proximal renal arterial stenosis) and possible acute allograft rejection has been suggested in many studies (17–19). In addition, in animal studies of preeclampsia, PIH (20–23), and HELLP (hemolysis, elevated liver enzymes, low platelets) syndrome (24), it has been suggested that the continuous vasospasm that occurs upstream in the renal artery is implicated in the pathogenesis of PIH. Therefore, we conducted a study to evaluate Doppler US renal circulation measurements in women with PIH to determine whether for upstream and downstream these measurements are altered in these women compared with those in healthy pregnant and nonpregnant women.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Between August 1991 and November 1996, at the First Hospital of Nippon Medical School, the flow velocity waveforms in the renal interlobar arteries were evaluated bilaterally in 39 nonpregnant women, 77 healthy pregnant women at 16–40 weeks gestation, and 15 patients with PIH at 28–39 weeks gestation. All of these subjects provided written informed consent for participation in this study, which was approved by the institutional review board. These women denied having a history of renal disease or essential hypertension. The nonpregnant women and healthy pregnant women were randomly chosen from the outpatients who visited our hospital.

The Doppler US velocimetric examination was performed within 1 week after PIH was diagnosed in each patient. None of the patients had begun antihypertensive treatment at the time of the Doppler US study. PIH was defined as a blood pressure elevation higher than 140/90 mm Hg in both systole and diastole or an increase in either the systolic (>30 mm Hg) or the diastolic (>15 mm Hg) values over the baseline blood pressure before 16 weeks gestation in at least two measurements obtained 6 hours apart.

All of the women were examined by means of color Doppler US with a 3.5-MHz convex transducer (Hitachi-Medico EUB-515A; Hitachi, Tokyo, Japan). We excluded several women because they had existing renal problems such as hydronephrosis and horseshoe kidney. However, we did not exclude women because of technical reasons. Each subject was placed in the left lateral decubitus position, and real-time imaging of the kidneys was performed bilaterally to rule out gross abnormalities in renal size, shape, and echogenicity. The kidneys were then insonated by using a longitudinal scanning plane from a posterior angle. The renal sinus was depicted by using color flow mapping in an attempt to identify the interlobar artery, which runs between the renal pyramids and extends into the renal cortex. The Doppler gate was then placed over the investigated vessel. Angle-corrected velocity waveform measurements were obtained in each kidney; the insonation angles were less than 30° during a period of suspended respiration. The sample volume on the Doppler system was set at 3 mm, and a 100-Hz pass filter was used to reduce the noise from the pulsating arterial wall. Pulsed Doppler US waveforms were displayed at sweep speeds of 40–80 mm/sec.

Doppler US spectral analysis included measurement of the peak systolic and end-diastolic velocities and of the acceleration time. These measurements were calculated with machine software (Hitachi-Medico EUB-515A) by placing electronic calipers on the Doppler tracing displayed on the image monitor. A series of three to five waveforms was sampled from one site on each kidney. The average value of each parameter was used for this study. The peak systolic and end-diastolic velocities were measured at the apex of the highest systolic peak and at the end of diastole, respectively.

The acceleration time was measured from the beginning of the systolic upstroke to the highest systolic peak in the waveform; any break in the systolic upstroke before it reached its peak was ignored. The systolic acceleration was calculated by dividing the peak systolic velocity during this same interval by the acceleration time. Because the durations of systole and diastole depend on the heart rate (25,26), a change in heart rate values will influence the acceleration time. Therefore, we normalized the acceleration time to be the duration of the cardiac cycle (measured from one systolic peak to the next), which was expressed as the acceleration time percentage (7). The resistive index was calculated as follows: (peak systolic flow velocity - end-diastolic flow velocity)/peak systolic flow velocity.

All data were expressed as the mean ± SD. One-way analysis of variance followed by the Scheffé F test also was used to compare the values within each study group. Regression analysis was used to correlate relationships between Doppler US indexes and gestational age. Differences with a P value of less than .05 were considered to be statistically significant.

Because all of the examinations were performed by one of four investigators (A.N., H.A., A.O., A.Y.), the interobserver and intraobserver reproducibilities of Doppler US waveform measurements were assessed in a separate series of studies. By using color Doppler US, the four investigators performed the measurements described above blindly in the right kidney of six healthy nonpregnant women aged 28–32 years. In each woman in this group, the Doppler waveform was measured three times in succession by each investigator, and the variability between the measurements was analyzed.

The interobserver variability of all the measurements was assessed by using one-way analysis of variance followed by the Scheffé F test. Statistical significance was established at P less than .05. The interobserver reproducibility and intraobserver reproducibility were quantified by using the intraclass correlation coefficient Ri (27, 28). The following criteria for clinically relevant agreement were used: poor, Ri less than 0.40; fair, Ri greater than or equal to 0.40 but less than or equal to 0.59; good, Ri greater than or equal to 0.60 but less than or equal to 0.74; and excellent, Ri greater than or equal to 0.75 (29). The Ri was derived from two-way analysis of variance in which the observers and subjects were factors. The formula used to calculate the Ri was (s2b - s2w)/[s2b + (n - 1)s2w], where s2b is the mean squared variation between subjects; s2w, the mean squared variation between observers (or repeated measurements); and n, the number of subjects.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
The characteristics of the subjects are reported in Table 1. There was no substantial difference in the mean age and parity of subjects among the three groups. Systemic arterial pressure values were recorded twice a day, with a 6-hour interval between measurements; there were significant differences in these values between the PIH group and the other two groups (P < .001). In all groups, there were no significant differences in any indexes of the interlobar arteries between the right and left kidneys.


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  		TABLE 1. Characteristics of Subjects
 
The mean peak systolic and end-diastolic blood flow velocities, resistive indexes, acceleration times, and systolic accelerations in the three groups of women are shown in Table 2. The individual peak systolic and end-diastolic blood flow velocities in the interlobar arteries of the healthy pregnant women are shown in Figure 1. Both the peak systolic velocity and the end-diastolic velocity decreased significantly with advancing gestational age. However, there were no significant differences in the other indexes, such as acceleration time, acceleration time percentage, systolic acceleration, and resistive index, associated with gestational age.


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  		TABLE 2. Values of Left and Right Interlobar Arterial Blood Flow Velocity Waveforms in Nonpregnant Women, Healthy Pregnant Women, and Women with PIH
 


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  		Figure 1. Scattergram illustrates the correlation of blood flow velocity and gestational age in healthy pregnant women. The circles indicate the peak systolic blood flow velocities in the right ({bigcirc}) and left (•) interlobar arteries. The squares indicate the end-diastolic blood flow velocities in the right ({square}) and left ({block}) interlobar arteries. A significant relationship was found between gestational age and both the peak systolic (r = -0.61, P < .05) and end-diastolic (r = -0.55, P < .05) blood flow velocities.

 
The Doppler waveform measurements in a healthy pregnant woman and in a woman with PIH are shown in Figure 2. To examine the change in blood flow with PIH, the maternal ages and gestational ages of the healthy pregnant women were compared with those of the women with PIH. The Doppler index measurements obtained in the three study groups are shown in Table 2. In the healthy pregnant and PIH groups, the peak systolic and end-diastolic blood flow velocities decreased significantly. In the women with PIH, the acceleration time and acceleration time percentage were significantly prolonged, and the systolic acceleration was significantly decreased compared with that in the other two groups. The graphs in Figure 3 illustrate the individual acceleration times with arterial blood pressure in the healthy pregnant women and in the women with PIH. In the women with PIH, the acceleration time tended to increase with the rise in diastolic blood pressure (not significant).



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  		Figure 2a. Typical Doppler US waveform measurements on longitudinal scans (posterior angle) obtained in (a) a healthy pregnant woman and (b) a woman with PIH, both of whom were at 32 weeks gestation. In a, R, ILA = right interlobar artery. (b) The Doppler US waveform measurement obtained in the woman with PIH demonstrates a delayed systolic upstroke (arrows). The acceleration time of this waveform is 132 msec, which is markedly prolonged compared with that in the healthy pregnant woman, 81 msec.

 


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  		Figure 2b. Typical Doppler US waveform measurements on longitudinal scans (posterior angle) obtained in (a) a healthy pregnant woman and (b) a woman with PIH, both of whom were at 32 weeks gestation. In a, R, ILA = right interlobar artery. (b) The Doppler US waveform measurement obtained in the woman with PIH demonstrates a delayed systolic upstroke (arrows). The acceleration time of this waveform is 132 msec, which is markedly prolonged compared with that in the healthy pregnant woman, 81 msec.

 


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  		Figure 3a. Scattergram illustrates the acceleration time plotted against (a) the diastolic blood pressure (DBP) and (b) the systolic blood pressure (SBP) in healthy pregnant women (circles) and in women with PIH (triangles). The open and closed shapes indicate the right and left interlobar arteries, respectively. The acceleration times are clearly divided into two groups. In the women with PIH, the acceleration time tended to increase as the DBP increased.

 


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  		Figure 3b. Scattergram illustrates the acceleration time plotted against (a) the diastolic blood pressure (DBP) and (b) the systolic blood pressure (SBP) in healthy pregnant women (circles) and in women with PIH (triangles). The open and closed shapes indicate the right and left interlobar arteries, respectively. The acceleration times are clearly divided into two groups. In the women with PIH, the acceleration time tended to increase as the DBP increased.

 
In the separate studies of interobserver variability, there was no significant difference in the peak systolic (P = .47) and end-diastolic (P = .46) blood flow velocities, acceleration times (P = .50), and systolic accelerations (P = .29) obtained by the four observers. Interobserver reproducibility was fair for measurements of peak systolic blood flow velocity, end-diastolic blood flow velocity, and systolic acceleration measurements and excellent for acceleration time measurements (Table 3). There was no poor level of intraobserver reproducibility, as shown in Table 3. Thus, both the interobserver reproducibility and the intraobserver reproducibility of Doppler waveform measurements were clinically acceptable in this study.


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  		TABLE 3. Intraclass Correlation Coefficients for Doppler Measurements
 

   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
The results of the present study give important information on how blood flow velocimetry in the intrarenal vessels is affected by pregnancy and how PIH influences renal blood circulation.

Theoretically, the increase in blood volume and cardiac output during pregnancy is accommodated by a pronounced decrease in peripheral vascular resistance due to vasodilatation. Usually, the vascular resistance decreases more than is required to maintain pressure, so the arterial blood pressure tends to decrease (30). However, in our study, there was no correlation between the resistive index of the interlobar arteries and the gestational age. These findings are similar to those obtained by Hata et al (10) in their study involving the renal artery.

The results of the present study demonstrated that the peak systolic and end-diastolic blood flow velocities in healthy pregnant women are significantly decreased during the third trimester compared with those during the first trimester. Because the plasma volume increases during early pregnancy, we speculate that intrarenal vasculature compliance might increase to result in decreased blood flow velocities. We also speculate that these physiologic changes may be due to decreased renal plasma flow, because it has been reported that renal plasma flow increases during early pregnancy but decreases during the third trimester (31,32). The final decrease in renal plasma flow is probably due to interference caused by weight on the renal veins from the uterus that contains a near-term fetus.

Several investigators have attempted to evaluate the renal circulation by performing Doppler US in healthy pregnant women (10–12) and in women with preeclampsia or PIH (13–16,33,34). The literature on renal blood flow velocimetry in PIH, however, is sharply divided: The diagnostic strategies that were found to be promising in some reports have not been uniformly successful when used in other laboratories. Sohn and Fendel (13) and Boemi et al (16) claimed that the Doppler indexes of the renal arteries in women with PIH are different from those in healthy pregnant women; this finding is suggestive of increased downstream vascular resistance. Contrary to this, others (14,33,34) have found no differences in the Doppler indexes of the renal arteries between normotensive and hypertensive pregnant women. Such differences have prompted the recent shift of attention from analysis of the proximal main renal artery to that of the distal intrarenal vessels.

In this study, to examine the changes in renal vascular resistance by using Doppler US parameters, we measured the flow velocity waveforms of the interlobar arteries, which run between the pyramids and extend into the renal cortex, because these vessels are "resistance vessels" of the renal vasculature (15). Our measurements of waveform indexes of downstream vascular resistance, such as the resistive index in PIH, were not different from those in healthy pregnant women. Liberati et al (15) also evaluated the Doppler velocimetry in the renal interlobar arteries of patients with hypertensive disorders of pregnancy. Although they hypothesized that the Doppler velocimetry in the interlobar arteries might be more sensitive than that in the main renal artery for the detection of increased resistance to blood flow, no differences in the Doppler indexes of the interlobar arteries were found between healthy pregnant women and women with PIH. However, the parameter that they analyzed was restricted to the resistive index, which is a known index of distal vascular resistance.

Herein, we examined acceleration time, which is one of the hemodynamic parameters of substantial upstream stenosis. Severe stenosis of an artery causes a pressure drop in the immediate poststenotic region, which results in a weakened pulse in the downstream arterial network that is clinically described as pulsus tardus (ie, pulse wave slow to rise) and pulsus parvus (small pulse) (35). In the poststenotic region, these phenomena are observed at Doppler US as a prolonged acceleration time, diminished acceleration index, and loss of the normal early systolic compliance peak–reflective-wave complex (36). This principle is easily applied to the renal arterial circulation.

The evaluation of the tardus-parvus waveform for the diagnosis of renal arterial stenosis was initiated, to our knowledge, with the work of Handa et al (17). By using the acceleration index, they found substantial decreases in the systolic acceleration distal to the renal arterial stenosis. In recent studies, this same conceptual approach has been applied to renal arterial stenosis in different contexts. Lafortune et al (18) created acute stenosis in the renal arteries of 10 dogs and found that the acceleration index decreased with a stenosis of 75%–90% but not with a more moderate stenosis of 60%. A similar result was reported by Patriquin et al (19) in a study involving 20 children suspected of having renal arterial stenosis. Conflicting results were reported by Kliewer et al (7), who examined the utility of Doppler US parameters for the diagnosis of renal arterial stenosis and concluded that Doppler US–based characterization of the tardus-parvus phenomenon in the distal renal artery is not an adequate screening method for the detection of renal arterial stenosis.

The results of our study, which demonstrated a prolonged acceleration time and decreased systolic acceleration in the interlobar arteries of women with PIH, are in agreement with former observations of renal arterial stenosis in nonpregnant women (17–19). This suggests the possibility that the pathogenesis of PIH is what causes the disturbance that occurs upstream in the renal interlobar arteries, such as the main renal artery or segmental artery. In addition, it has been reported that the acceleration index decreases with increasing compliance of the poststenotic segment (37). Therefore, one might also postulate that elevated compliance in the vessels distal to the interlobar arteries may occur in women with PIH.

The results of some studies showed that vasoconstriction is involved in the pathophysiology of preeclampsia (38). One of the consequences is the development of endothelial damage in the maternal circulation, which is responsible for the involvement of various organ systems (eg, the kidneys, liver, brain, and coagulation system) (39). Levels of the vasospastic peptide endothelin are increased in patients with preeclampsia (40). In addition, the results of experimental studies (23,41) in rats and primates have shown that the inhibition of nitric oxide synthesis during a normal pregnancy results in a clinical picture that is similar to that of preeclampsia. Podjarny et al (42) showed that rats with doxorubicin-induced nephropathy develop a preeclampsia-like syndrome during late pregnancy. In another model, they demonstrated that PIH is associated with an inadequate production of nitric oxide (23). Furthermore, in a case report (43), the beneficial effect of a nitric oxide donor in the treatment of HELLP syndrome was documented. It was therefore suggested that nitric oxide contributes to the development of hypertension in pregnancy as an endothelial derived relaxing factor. Kanayama et al (24) showed that an animal model of HELLP syndrome can be developed by stimulating the celiac ganglion in rats. They speculated that repeated transient vasospasms of the renal artery induced by catecholamines cause endothelial injury that results in continuous vasospasms and hypertension. These pathologic and neurologic findings suggest that the prolonged acceleration time in the interlobar artery and the severe stenosis or continuous vasospasms that occur in the proximal arteries, such as the main renal artery or the segmental artery, may be implicated in the pathogenesis of PIH.

The hypertensive disorders that complicate pregnancy are associated with substantial morbidity and mortality. Despite improvements in obstetric care, these disorders are the second leading cause of maternal mortality (44). The perinatal mortality rate is increasing also as a consequence of placental insufficiency, preterm delivery, and placental separation. We acknowledge that because of the relatively small number of patients with PIH in our study, our series was probably too limited to determine the pathogenesis of PIH. This is because we selected only those patients who had hypertension for less than 1 week and had not started antihypertensive treatment at the time of the Doppler US study. However, we believe that the results of this study have the potential to provide new insight into the pathogenesis of PIH and suggest the need for further study.


   Acknowledgments
 
We greatly appreciate the advice of Tsunehito Mukai, MD, throughout this project.


   Footnotes
 
Abbreviation: PIH = pregnancy-induced hypertension

Author contributions: Guarantor of integrity of entire study, A.N.; study concepts and design, A.N., H.A.; definition of intellectual content, A.N.; literature research, A.N.; clinical studies, A.N., H.A., A.O., A.Y.; data acquisition, A.N., H.A., A.O., A.Y.; data and statistical analyses, A.N.; manuscript preparation, A.N.; manuscript editing, A.N., H.A., A.O.; manuscript review, A.N., H.A., T.K., T.A.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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K. Williams and C. Kocer
Vascular Reactivity in Preeclampsia Assessed Noninvasively Using Maternal Brachial Artery Hyperemic Response
Obstet. Gynecol., November 1, 2004; 104(5): 1025 - 1029.
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