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by the American Institute of Ultrasound in Medicine J Ultrasound Med 23:1607-1611 0278-4297 Renal Venous Doppler Sonography in PreeclampsiaDepartments of Medical Imaging (G.A.B.) and Reproductive Medicine (W.G.), John Hunter Hospital, Newcastle, New South Wales, Australia; Faculty of Health, University of Newcastle, Newcastle, New South Wales, Australia (G.A.B., W.G.); and Department of Medical Imaging, Belmont District Hospital, Belmont, New South Wales, Australia (S.L.E.). Address correspondence and reprint requests to Grant A. Bateman, MBBS, FRANZCR, Department of Medical Imaging, John Hunter Hospital, Locked Bag 1, Newcastle Region Mail Center, Newcastle NSW 2310, Australia. E-mail: grant.bateman{at}hunter.health.nsw.gov.au.
Objective. The elevation in blood pressure associated with preeclampsia appears to be associated with a shift in the renal pressure natriuresis curve. Pressure natriuresis is modulated by renal medullary pressure. In obstructive uropathy, Doppler sonography has been used to indicate changes in renal venous impedance, possibly measuring alterations in medullary pressure and compliance in this condition. The hypothesis tested in this study was that an elevation in renal venous pulsation may occur in preeclampsia compared with normal pregnancy. Methods. Seven patients with clinical evidence of preeclampsia were referred for fetal well-being confirmation by sonography in the third trimester. Seven pregnant patients without renal disease or hypertension reviewed in the third trimester served as a control group. Doppler studies of the interlobar arteries and veins of both kidneys were performed, with a total of 14 kidneys imaged per group. Arterial and venous impedance indices were obtained. The impedance indices for the patients were compared by the Student t test. Results. No significant difference was noted between the arterial resistive indices. The mean venous impedance index for the hypertensive patients was 0.50 ± 0.12, and that for the control patients was 0.37 ± 0.06 (P = .003). Conclusions. Preeclampsia in the third trimester appears to be associated with altered medullary venous pulsation, possibly indicating reduced medullary pressure.
Key Words: Doppler sonography impedance index preeclampsia venous compliance
Preeclampsia or pregnancy-induced hypertension is estimated to affect 7% to 10% of pregnancies in the United States. It is one of the leading causes of maternal death and maternal and perinatal morbidity.1 The kidneys perform long-term blood pressure regulation, with normal pregnancy associated with both a reduction in mean blood pressure and elevations in renal plasma flow and the glomerular filtration rate of approximately 30% to 40%.2 Preeclampsia, conversely, is associated with elevations in total peripheral resistance (and therefore pressure), possibly because of enhanced responsiveness to angiotensin II, marked reductions in renal blood flow and the glomerular filtration rate, and proteinuria.3 It has been suggested that there is an alteration in the way that the kidneys sense and respond to changes in systemic blood pressure in preeclampsia, indicating a change in the pressure natriuresis response of the renal parenchyma.3 The pressure natriuresis curve is a concept describing the way that elevations in blood pressure cause excretion of sodium and therefore a reduction in blood pressure back toward normal.4 In rats, papillary blood flow (medullary flow) is not autoregulated well compared with cortical flow; therefore, increases in renal perfusion pressure elevate vasa recta capillary pressure and renal interstitial fluid pressure. Increased interstitial fluid pressure is associated with decreased tubular reabsorption of sodium. Therefore, sodium and water excretion is very sensitive to small changes in renal perfusion pressure, providing a mechanism for pressure regulation.4 Thus, elevation of the systemic pressure increases medullary perfusion but not cortical perfusion. The increased medullary perfusion increases medullary pressure, which directly increases the elimination of sodium and water, which brings the systemic pressure back toward normal. The Doppler examination of the arterial tree includes measuring the resistive index, which is defined as the systolic velocity minus the diastolic velocity divided by the systolic velocity; that is, resistive index = (systolic diastolic)/systolic. This index actually measures impedance, which is a combination of both the downstream resistance and the vessel compliance.5 The downstream resistance on the venous side of the arterial tree is usually minimal because the veins act as capacitance vessels; therefore, the term resistive index is confusing, and the term impedance index is preferred on the venous side of the vascular tree. In acute renal ureteric obstruction, there is an elevation in interstitial pressure, and this has been associated with a reduction in the venous impedance index.6 If a shift in the renal pressure natriuresis curve is involved in the pathophysiologic mechanism of preeclampsia, then one may predict a reduction in renal medullary pressure for any given systemic blood pressure in preeclampsia compared with normal pregnancy. A change in medullary pressure should alter the medullary venous impedance in the opposite direction to that found in renal obstruction. Therefore, in this study, the hypothesis tested was that an elevation in renal venous pulsation may occur in preeclampsia compared with normal pregnancy.
Seven patients with a clinical diagnosis of preeclampsia were referred from a district hospital obstetric clinic for fetal well-being confirmation sonography in the third trimester between October 2002 and December 2003. Preeclampsia was diagnosed by the obstetrician overseeing each patients care using standard criteria. Blood pressure measurements and evidence of proteinuria were obtained by review of the antenatal records, with the birth weight obtained from review of the delivery record. The mean age of the patients ± SD was 31 ± 4 years, with a mean gestational age of 33 ± 3 weeks at the time of sonography. The standard fetal sonographic examination was extended to include an examination of the maternal kidneys. The examination included a review of the renal parenchyma to exclude any significant abnormalities as well as a Doppler examination of the interlobar arteries and veins from both kidneys. The Doppler angle was kept to a minimum by selection of midpole vessels as parallel to the beam as possible. The impedance index, also commonly known as the resistive index, was recorded. The same sonographer (S.L.E.) performed all the examinations in this study to standardize the technique. The arterial and venous Doppler spectra were optimized with several arterial and venous measurements performed in various phases of suspended respiration. Three or 4 waveforms were then averaged for each arterial and venous measurement. Seven patients without evidence of renal disease or notable hydronephrosis and no evidence of blood pressure elevation or proteinuria served as control patients. This group was referred for third-trimester fetal well-being studies for indications such as "confirm placenta previa" or "? small for dates" in which the subsequent examination findings were entirely within normal limits. The mean age of the control patients was 31 ± 3, with a mean gestational age of 36 ± 1 weeks. Comparison between the hypertensive and control groups was tested with a nonpaired t test, and P = .05 was used to indicate significance. Informed consent was obtained from each patient in this study, and the protocol was reviewed by and conformed to the Ethics Committee guidelines of the hospital.
The results are summarized in Table 1
Control Group The mean blood pressure in the third trimester for the control group was 110 ± 8/65 ± 8 mm Hg (systolic/diastolic). There was no evidence of proteinuria at any stage during pregnancy for the control patients. The mean birth weight was 3300 ± 500 g. Renal sonography showed no evidence of renal disease or hydronephrosis in any of the patients studied. There was no significant difference between the right and left kidneys in the arterial resistive index. There was a minimal difference between the kidneys in the venous impedance (11% larger on the left compared with the right; P = .04). Figure 1
Preeclampsia Group Hypertension developed during pregnancy in all 7 patients, with the mean blood pressure in the third trimester for the preeclampsia group being 145 ± 16/86 ± 13 mm Hg. These values are significantly elevated compared with those of the control group (P = .0003 and .004, respectively). Five patients had proteinuria outside the reference range on formal 24-hour urine testing. (Proteinuria was measured at 190, 500, 710, 880, and 1320 mg/d, respectively.) The other 2 patients had no notable proteinuria. The mean birth weight was 2800 ± 500 g. Renal sonography showed no evidence of renal disease or hydronephrosis in any of the patients studied. No significant difference was noted between the right and left kidneys for the arterial resistive and venous impedance indices. There was no significant difference in the arterial resistive indices noted in the hypertensive patients compared with those in the control patients. The venous impedance indices for the hypertensive patients were greater than those for the control patients. The right kidney impedance index was 34% greater that that of the control patients, and the left index was 33% greater (P = .04 and .02, respectively). As a group, the 14 hypertensive kidneys had a mean venous impedance index of 0.50 ± 0.12; the control group has a mean index of 0.37 ± 0.06 (P = .003). Figure 2
The elevation in systemic pressure found in preeclampsia suggests a change in the set point for blood pressure regulation within the kidney.3 The pressure natriuresis response of the kidney has been found to be regulated within the medulla of the kidney.4 Unlike the renal cortex, where blood flow is constant over a large range of perfusion pressures, within the medulla, blood flow and therefore interstitial pressure vary with perfusion pressure.4 It has been shown in rats that changes in renal parenchymal pressure directly alter renal reabsorption of salt and water, and this provides a mechanism for blood pressure regulation.4 There is the suggestion of abnormal endothelial function with decreased production of endothelial-derived relaxing factors, such as nitric oxide and prostacyclin, increased production of endothelin and thromboxane, and enhanced vascular reactivity to angiotensin II in women with preeclampsia.3 A reduction in nitric oxide synthesis results in a hypertensive shift in the pressure natriuresis relationship and is also associated with reductions in renal plasma flow and the glomerular filtration rate and an inability to transmit renal perfusion pressure into the renal interstitium,7 with these latter findings being hallmarks of preeclampsia.4 If there is a change in the pressure natriuresis effect in preeclampsia, then a reduced medullary interstitial pressure for any given systemic pressure should occur. An association between an elevation in interstitial pressure (caused by acute renal ureteric obstruction) and a reduced renal venous impedance index has been shown.6 In a similar way, measuring the pulsatility of the venous signal in the hepatic veins has been put forward as a method of identifying disease in the liver because of the changes in venous pulsation that are produced.8 Liver disease has been noted to be associated with dampening of the hepatic venous signal.8 Britton et al8 speculated that the pulsatility of the hepatic venous Doppler flow reflects the compliance of the liver tissue because most diseases expand the liver parenchyma within its confining capsule. Using a technique that was the same as that used in this study, Karabulut et al9 found renal vein impedance indices of nonpregnant women to be 0.44 ± 0.06 for the right kidney and 0.41 ± 0.07 for the left. In pregnant patients in whom there was no evidence of renal collecting system dilatation or hypertension, the impedance indices were 0.35 ± 0.08 on the right and 0.37 ± 0.10 on the left, indicating a substantially reduced renal venous impedance index even in the absence of maternal pyelocaliectasis.9 A further reduction in the impedance index was noted when there was evidence of pyelocaliectasis.9 The venous impedance indices for the control patients in this study closely match those in the study by Karabulut et al.9 The venous impedance indices for the preeclampsia group were significantly elevated compared with those for the control group (overall, a 35% increase; P = .003). The effect noted is a reduction in venous velocities in the last 200 milliseconds of diastole, which is accentuated in preeclampsia. The Doppler arterial data indicate that the inflow into the kidney is continuous during this period of diastole; therefore, the reduced venous velocities seen are not due to an abrupt reduction in inflow velocity in end diastole. If the inflow into the veins is continuous, then possible causes for the altered pulsation found may be a selective increase in downstream resistance, a reduction in the pressure gradient between the renal veins and the right atrium, and an increase in venous compliance. It may be that a shift in the pressure natriuresis curve caused by a reduction in interstitial pressure may be a cause of the effect found by allowing a greater fluctuation in venous size during the cardiac cycle in these patients compared with those without preeclampsia. However, this is speculative, and further study to correlate the inferior vena cava and renal vein pulse pressure would be required to prove this hypothesis. The numbers of patients in this study were not large, but the measurement of both right and left kidneys in the control and preeclampsia groups doubled the available data, and we think that the high degree of significance found in the test group warrants a preliminary report. There is a limitation in this study in that the inferior vena cava Doppler signal was not correlated with the renal venous findings. Potentially, an elevation in the inferior vena cava pulsation could elevate the renal venous pulsatility. In conclusion, preeclampsia in the third trimester appears to be associated with elevated medullary venous pulsatility. The cause of this observation has not been proved but may be associated with a shift in the pressure natriuresis curve.
Received March 15, 2004, from the Departments of Medical Imaging (G.A.B.) and Reproductive Medicine (W.G.), John Hunter Hospital, Newcastle, New South Wales, Australia; Faculty of Health, University of Newcastle, Newcastle, New South Wales, Australia (G.A.B., W.G.); and Department of Medical Imaging, Belmont District Hospital, Belmont, New South Wales, Australia (S.L.E.). Revision requested May 10, 2004. Revised manuscript accepted for publication August 25, 2004.
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