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. 2018 Feb 16;20(3):582–588. doi: 10.1111/jch.13212

Difference between renal and splenic resistive index as a novel criterion in Doppler evaluation of renal artery stenosis

Clemens Grupp 1,✉, Michael J Koziolek 1, Manuel Wallbach 1, Kerstin Hoxhold 1, Gerhard A Müller 1, Carsten Bramlage 1
PMCID: PMC8031111  PMID: 29450973

Abstract

Detection of renal artery stenosis (RAS) using Doppler is difficult to evaluate, particularly under conditions such as bilateral RAS or difficultly accessible renal arteries (RA). The objective of the present study was to assess the utility of splenic arterial compared to renal flow as an additional parameter in the Doppler evaluation of RAS. The difference between the resistive indices (RI) determined in renal and splenic parenchymal arteries (ΔRIK−S) was evaluated in 181 hypertensive subjects without any evidence of RAS. Subsequently 47 RA in 24 patients with suspected RAS were angiographically assessed. A ΔRIK−S of 0.055 (median) was determined in the population without any evidence of RAS similar to RA with angiographically excluded stenosis (ΔRIK−S 0.068). In contrast, in angiographic proven RAS, ΔRIK−S was significantly lower (−0.050; P < .005). The assessment of the ΔRIK−S, proved to be an easily feasible parameter, which improves the diagnostic accuracy in the detection of RAS.

Keywords: bilateral renal artery stenosis, duplex, flow profiles, renovascular hypertension, single kidney, ultrasound diagnostic

1. INTRODUCTION

Renal artery stenosis (RAS) is regarded as one of the most common secondary causes of arterial hypertension. Although several trials demonstrated similar outcomes for revascularization and conservative treatment,1, 2, 3, 4 the detection of this entity of hypertension is still particularly therapy‐relevant. At least in patients who present with “flash” pulmonary edema, congestive heart failure with preserved left ventricular function, or acute oligoanuric renal failure with global kidney ischemia, especially when they have severe bilateral RAS5, 6, 7, 8, 9, 10, 11, 12 as well as in patients with fibromuscular dysplasia.13 The presence of a renal artery stenosis is also of importance in determining appropriate antihypertensive medical treatment, for instance the application of ACE‐inhibitors or AT1‐blockers in certain cases.14 Screening for RAS is therefore still an integral component of the evaluation of secondary hypertension. Duplex scanning is principally used as a screening technique to detect RAS. This is probably due to the fact that compared to other screening techniques for RAS, Doppler is non‐invasive and cost‐effective with a high diagnostic power.15, 16, 17

Doppler diagnosis of RAS is usually based on several criteria, comprising the evaluation of flow profiles both in the stenotic area of the renal artery (direct criteria) and renal parenchyma (indirect criteria). Each of these criteria has some restrictions. Direct assessment of renal artery stenosis can be hampered by the difficulty in detecting the stenotic section.17, 18, 19 This may be due to impaired examination conditions, for example meteorism or obesity. Poststenotic flow profiles in the kidney are assessed by indirect criteria, which are usually more easily detectable. Both absolute and relative changes of renal intra‐parenchymatous resistive index (RI) are regarded as important indirect Doppler‐criteria for RAS, however both have limitations. The validity of the absolute value of the RI is restricted by its dependence (eg, from physiologic factors such as age or heart rate but also pathologic conditions like renal disease).20 The relative RI‐difference between the right and left kidneys cannot be assessed in bilateral RAS, where it might be overlooked because of the absence of RI‐difference between the 2 kidneys or after nephrectomy of the contralateral kidney. To overcome at least some of these pitfalls in evaluating renal RI in RAS‐diagnosis, we examined the value of an additional criterion. We hypothesized that diagnostic reliability of the renal RI could be improved by comparing it to an appropriate vascular system of another organ as additional reference besides the contralateral kidney. The spleen is closely localized to the left kidney and its perihilar arteries are easily accessible by a duplex ultrasound and therefore might be especially useful for this purpose.

The objective of the present study was to evaluate the utility of a comparison of arterial flows between the kidney and spleen as an additional parameter in the Doppler evaluation of renal artery stenosis. The present study analyzed the difference between the RI in the segment arteries of the kidney (RIK) and the spleen (RIS), and shows this to be an easily determinable parameter with high specificity and sensitivity for the detection of renal artery stenosis.

2. METHODS

2.1. Patients

The study population was selected from hypertensive patients in either ambulatory or inpatient care settings, who had been consecutively referred for Doppler assessment of RAS within their evaluation for secondary causes of hypertension.

Not considered in this examination were patients in whom not all of the below mentioned Doppler criteria for RAS were negative and/or in whom published clinical criteria for RAS15, 17, 21 were not completely negative, with the exception of those patients who underwent angiography for reasons as outlined below.

Furthermore, patients with chronic renal disease who were considered to suffer from reno‐parenchymatous hypertension and patients with suspected stenosis of a branched renal artery as assessed by the Doppler evaluation, as well as patients without sinus rhythm, were omitted from this analysis.

As shown in Figure 1, in this study by Doppler evaluation, a total of 213 patients were assessed both with respect to RAS and the flow in perihilar spleen arteries as outlined below. Subsequently patients were evaluated as follows:

Figure 1.

Figure 1

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Patient selection criteria for this study. To examine the physiological difference of Resistive Indices (RIs) between kidney and spleen in hypertensives, 181 patients without any evidence for renal artery stenosis (RAS) both by duplex and clinical evaluation and without any exclusion criteria were examined. The utility of this difference in the diagnostic RAS was assessed in 24 patients (47 renal arteries), who underwent angiography for suspected RAS. For further details see text

Eight of these patients had no evidence for RAS by Doppler, but were excluded from evaluation because they were suspected of having liver cirrhosis or splenomegaly, which was identified from their medical history by ultrasound examination of the abdomen or from laboratory findings (eg, elevated glutamic‐oxalacetic transaminase [GOT]). None of the patients were suspicious for angina mesenterialis or Dunbar syndrome by clinical symptoms (eg, typical abdominal pain).

The physiological difference between renal and spleen arterial RI (ΔRIK−S) was studied in those patients who had absolutely no evidence for RAS neither by Doppler evaluation (all of the criteria outlined in the following were negative) nor from their medical history. This group comprised 362 renal arteries of 181 patients (75 females and 106 males; age range 10‐79 years; mean age: 51.0 years).

Forty‐seven renal arteries in 24 patients were angiographically assessed (9 females and 15 males; age range 10‐77 years; mean age: 54.6 years). One of the kidneys of these patients proved to be an atrophic kidney, in which no significant blood flow could be detected. The attending physicians made the indications for these angiographic examinations independently. The reason for angiographic evaluation was mainly a suspect Doppler finding (in 18 patients at least 1 of the below outlined standard Doppler criteria were positive, and in 2 patients the right renal artery was not entirely accessible). In 3 patients primarily clinical tests were highly suggestive for RAS and in 1 patient renal angiography was combined with a coronary angiography performed for other reasons. All angiographic evaluations were performed within 14 days after Doppler assessment for RAS, including the evaluation of the difference between the RI‐values determined in renal and spleen parenchyma (ΔRIK−S). Renal arteries were angiographically evaluated by intra‐arterial digital subtraction angiography (i.a. DSA) or primarily by magnetic resonance angiography (MRA). DSA was omitted in 7 patients with completely negative MRA.

All analyses were conducted in accordance with the Helsinki Declaration.

2.2. Renal Doppler sonography

Patients were instructed to fast overnight before the morning of the Doppler examination. All Doppler examinations were conducted by 1 of 2 experienced investigators from our group who perform Doppler scanning on a regular basis. The patients were examined in supine and lateral positions using a 2.0‐4.0 MHz‐phased curved array transducer with a commercially available color Doppler unit. Following B‐scanning to determine kidney size and evaluation of parenchymal disorders, the color mode was added for vascular imaging.

The origin and course of the main renal arteries, as well as segmental and interlobar renal arteries in the upper pole, mid portion, and lower pole of each kidney were located and Doppler scans were taken. Each analyzed scan comprised at least 3 complete pulse cycles.

In each case, angle‐corrected (<60°) peak systolic and end diastolic velocity were determined from the Doppler spectra, and the resistive index (RI) was calculated according to the formula: RI = (peak systolic velocity − end diastolic velocity)/peak systolic velocity. RI values of at least 3 different segment artery spectral samples were arithmetically averaged to give a mean intrarenal RI of each kidney. Patients with a RI difference >0.03 within a kidney were suspected for stenosis of a branched renal artery and were excluded from the study.

To assess splenic flow parameters, the RI and the peak systolic velocity (V max) were also determined in the arteries of the spleen parenchyma, close to the hilus. At least 3 determinations at different locations were performed and the mean values were calculated.

Side‐to‐side differences between the right and left kidney (ΔRI) as well as the RI difference between the kidney and the spleen were calculated (ΔRIK−S). The difference of the resistive indices between the kidney and the spleen was individually calculated for each side and defined for the right and left side as ΔRIKr−S or ΔRIKl−S, respectively.

In accordance with our previous experience and with reports in the literature,22 significant RAS was considered if the angle‐corrected peak systolic velocity (PSV) in the main renal artery was greater than 1.8 m/s or the ΔRI between the 2 kidneys was >0.05 (lower RI on the stenotic side). In the 181 patients evaluated for the assessment of the physiological ΔRIK−S, all of the aforementioned Doppler criteria were determined and entirely negative and in 2 out of the 24 patients who underwent angiography, the right renal arteries were not completely accessible and therefore PSV not determinable.

2.3. Angiographic evaluation of the renal artery

Intraarterial digital subtraction angiography (i.a. DSA) was performed with a femoral artery approach and standard Seldinger techniques. Magnet resonance angiography (MRA) was applied in some patients. In 7 patients with a negative MRA examination i.a. DSA was omitted, whereas all patients with a positive MRA result were subjected to i.a. DSA. A stenosis of the renal artery of 50% or more in the i.a. DSA was considered as significant. The arterial diameters were measured with a hand‐held ruler.

2.4. Statistics

Results are given as median with the 25th and 75th percentiles (interquartile range [IQR]). Medians were compared applying the Mann‐Whitney U test. A covariance analysis was applied to examine potential interactions between ΔRIK−S and various parameters such as age, sex, or localization of the kidney. Intraobserver variability was assessed by the Levene‐test. For these statistical analysis software Statistica, version 12, from StatSoft, Tulsa, was used. Receiver operating characteristic (ROC) curve analysis was carried out to test the ability of the various ΔRIK−s values to discriminate between cases with and without significant renal artery stenosis. The ROC curve is considered by plotting diagnostic sensitivity (true positives) against 1‐specificity (true negatives) over all possible decision thresholds. The areas under the individual ROC curves were computed using the non‐parametric method of Hanley and McNeil.23 Receiver operating characteristic (ROC) curve analysis was performed using the software package Analyse‐IT version 1.44 (Analyse‐IT Software Ltd, UK). A P‐value <.05 was considered as statistically significant.

3. RESULTS

3.1. Comparison of resistive index (RI)‐values determined in splenic and renal arteries

Determination of the RI‐values in arteries close to the hilus in both the kidney and the spleen in 181 subjects without any evidence for renal artery stenosis, revealed an age‐dependent increase of the absolute values in both organs (Figure 2). For all age‐groups, the RI‐values determined in the spleen were always below those determined in the kidney and the slopes of both curves were rather parallel. Therefore, the difference between the RI values determined in the ΔRIK−S was constant over the whole age range. The median of ΔRIK−S as well as the IQR averaged for all ages were 0.055 (0.025‐0.095) (Figure 3, Group: Not suspected to have RAS). Variance of ΔRIK−S of the 2 operators was very low (0.056 ± 0.00045 and 0.054 ± 0.00034 respectively) and interobserver variability was not significantly different as assessed by the Levene‐test (P = .53).

Figure 2.

Figure 2

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Age‐dependence of the Resistive Indices (RI) determined in the kidney and the spleen. With increasing age an almost parallel increase of the absolute values of RI‐indices determined in the kidney and spleen was observed. The difference between the 2 curves was constant for nearly all ages. Only subjects without any evidence for renal artery stenosis were considered. The median of each group is given (n = number of renal arteries per age group, in total 362 renal arteries)

Figure 3.

Figure 3

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Difference of the Resistive Indices (RIs) determined in the kidney and the spleen (ΔRIK−S) in patients with and without renal artery stenosis (RAS). ΔRIK−S was significantly reduced in case of angiographically proven RAS (“RAS”; n = 15) compared to subjects in whom RAS had been excluded by angiography (“no RAS”; n = 32). ΔRIK−S in patients without any evidence for RAS both by Doppler examination and medical history (“Not suspect for RAS”; n = 181) did not differ significantly from those, in whom RAS had been angiographically excluded (“no RAS”). Values are given as median and 25%‐ and 75%‐quantiles, respectively

Covariance analyses including all classes of ages showed that the ΔRIK−S measurements were in particular independent of age (P = .70). Furthermore it was also independent of the localization of the kidney (left/right side) and sex (P = .94, P = .57 respectively), and that there was no interaction between these parameters.

3.2. Difference in RI between kidney and spleen in patients with renal artery stenosis (RAS)

Forty‐seven renal arteries in 24 patients were evaluated by angiography. A significant stenosis was detected in 15 renal arteries (13 of atherosclerotic, 2 of fibromusclar genesis): in 6 patients on the right side, in 3 patients on the left side, and in 3 patients bilaterally. No multiple renal arteries in these patients were detected.

As shown in Figure 3, a significantly lower ΔRIK−S was observed in stenosed renal arteries (median −0.050, [IQR −0.11 to 0.00]; P < .002) compared to cases with angiographically excluded renal artery stenosis (median 0.068, [IQR 0.05 to 0.11]). The latter value was not significantly different from the above reported value for kidneys without any evidence for RAS (median 0.055, [IQR 0.04 to 0.09]). In most cases of renal artery stenosis, the RI value determined in the renal parenchyma fell below that determined in the spleen. Determination of the ΔRIK−S proved especially useful in patients with bilateral renal artery stenosis. An example, in which no significant difference between RI values of the right and left kidney was observed, is shown in Figure 4. However, a reduced ΔRIK−S for both kidneys was suggestive of bilateral RAS, which was confirmed by i.a. DSA.

Figure 4.

Figure 4

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Flow profiles in parenchyma of the spleen and kidney in a patient with bilateral renal artery stenosis (RAS). The Resistive Index (RI) values determined in the right and left kidney were 0.56 (A) and 0.53 (B), respectively. In splenic parenchyma RI value of 0.61 (C) was determined. Difference between the RI values determined in the kidney and the spleen (ΔRIK−S) calculated both for the right and left sides were −0.05 and −0.08 respectively, suggesting bilateral RAS, which could be confirmed by angiography. The RI values in the figures are marked by green arrows

To estimate the threshold of the ΔRIK−S value, which exhibits the best discriminatory power in the evaluation of renal artery stenosis, ROC curve analysis was performed (Figure 5). Based on this analysis, optimal discrimination was obtained for a ΔRIK−S value ≤0.03 as indicative for RAS. Taking this threshold, sensitivity and specificity were 93.3% and 81.2%, respectively. The positive predictive value was 70.0%, and the negative predictive value was 96.2%. The corresponding data of the diagnostic accuracy for PSV as a direct Doppler criterion (2 right renal arteries were not completely accessible) were 77.7%, 89.5%, 82.3%, and 86.6%, for ΔRI between both kidneys as an indirect criterion were 63.6%, 88.0%, 82.3%, and 73.3%, respectively. Therefore the determination of ΔRIK−S proved a valuable additional parameter in the evaluation of RAS by Doppler.

Figure 5.

Figure 5

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Receiver operating characteristic (ROC) curve analysis of the utility of the difference of the Resistive Indices (RI) determined in the kidney and the spleen (ΔRIK−S) to detect renal artery stenosis (RAS). Sensitivity vs 1‐specificity of a renal artery stenosis ≥50% for different ΔRI k−s cut‐off values are shown. Best discriminatory efficiency was obtained for a threshold of ≤0.03 as indicative for RAS. The area under the ROC curve was 0.894 (95% confidence interval 0.770‐1.000; P < .0001). The broken line represents the line of identity (ie, no discrimination)

4. DISCUSSION

The present study evaluates ΔRIK−S as an additional parameter in the Doppler diagnosis of RAS. Determination of the intrarenal RI plays a crucial part in the diagnosis of RAS, in particular a side‐to‐side difference of >0.05 is highly suggestive for hemodynamic relevant unilateral RAS.16, 17, 19, 24, 25 However, absolute renal RI values formerly postulated as a diagnostic criterion are largely dependent on various factors, in particular on age,20, 24, 26 as shown also in this study. Evaluation using the difference of the renal RIs between the left and right kidneys is hampered in the case of a single kidney where the contralateral kidney is not available for comparison, and (in particular) in bilateral RAS where RAS might be not considered, since examiners are focused on a RI‐difference between the 2 kidneys. Several angiographic studies suggest that RAS occurs bilaterally in about 20%‐25% of the cases.25, 27, 28, 29 In an examination on pediatric patients, bilateral RAS has been observed even in 47%.30 In this study, we found bilateral RAS in 25%, which is well in the range reported by others.

The aim of the present study was to evaluate the utility of an additional arterial flow system as a reference point, particularly in those cases in which the contralateral kidney is not suitable for comparison. For this purpose, perihilar arteries of the spleen, which are easily accessible for Doppler sonographic assessment, were investigated.

An absolute prerequisite for the applicability of splenic flow parameters as a reference to evaluate poststenotic flows in the kidney is a constant interrelationship between the respective parameters determined in the spleen and the kidney. In a pivotal step, we therefore evaluated RI difference between the ΔRIK−S in hypertensive subjects without any evidence for RAS. Since the absolute value of RI determined in the renal parenchyma kidney varies with age,20, 24, 26 the question whether the RI difference between the kidney and the spleen is age‐dependent was of particular importance. In agreement with others, we found the lowest renal RI at the age of about 30 years with higher values for younger and (in particular) older subjects, reflecting a J‐curve.20, 24, 26 The slope of the age‐dependency of the RI determined in the spleen was absolutely parallel to the one determined in the kidney parenchyma. Therefore, ΔRIK−S proved to be in subjects without any evidence for RAS, a very constant parameter, independent of patients’ age, which is a precondition for its applicability as reference in the evaluation of renal flows. Covariance analysis showed that in addition to age, ΔRIK−S was independent of gender or localization of the kidney (right/left side), consistent with findings of Grun and colleagues.20

ΔRIK−S measured in patients in whom RAS has been excluded by angiography, was entirely in the same range of that in hypertensive patients without any evidence for RAS, excluded both by other Doppler and clinical criteria. This ΔRIK−S of about 0.06 in subjects without any evidence for RAS is very well in agreement with the ΔRIK−S reported for the “normal” patient collective in various others studies.20, 31, 32

We assumed that a hemodynamic relevant RAS decreases poststenotic intrarenal systolic flow resulting in a reduced intrarenal RI and thereby diminished ΔRIK−S. We confirmed this in the angiographic‐proven RAS.

ΔRIK−S might also depend on changes of splenic RI. Whereas splenomegaly has been reported to have no significant impact on splenic flow parameters,33 an increase of splenic RI, but surprisingly also of renal RI, has been reported in liver cirrhosis.31, 32 For this reason we excluded all patients with even slight evidence for liver or splenic diseases from this study, although alterations of splenic RI should have been expected only in a minority of these patients. These subjects comprised only a very small portion of the patients who were referred to us for Doppler sonographic examination of the renal artery. Furthermore, a stenosis of the celiac trunk or the arteria lienalis as well as a Dunbar‐syndrome might reduce the splenic RI. Therefore, in cases in which these diseases are suspected, especially in generalized atherosclerosis, but also in patients with a single kidney, such a stenosis should be excluded by duplex. Nonetheless, Grun and colleagues20 observed that renal and splenic RIs are influenced to a similar degree by cardiovascular risk factors and by markers of systemic atherosclerotic disease.

On the other hand, the renal RI could be enhanced in chronic renal disease.16, 20, 24 In these cases however, “renalisation” of hypertension in the sense of reno‐parenchymatous hypertension has to be considered. A dilatation of RAS is probably without significant effect.16 Since these potential pitfalls occur rarely in the population typically referred to for evaluation of RAS and could easily be excluded in most cases, evaluation of ΔRIK−S is widely applicable in the screening for RAS.

So far, no optimal criteria for the identification of RAS by Doppler have been identified, although various alternatives have been suggested.17, 19, 34, 35, 36 Substantially different results have been reported for the diagnostic power of the respective Doppler criteria, mostly dependent on the experience of the examiner and the technical equipment used.22 There might be a publication bias where centers with expertise in this technique are more likely to publish their results.21 In this study, we observed for the direct Doppler criterium PSV and the indirect criterium side‐to‐side difference of the renal RI similar diagnostic accuracies, as reported by others.17, 25 (Eg, the widely used side‐to‐site difference of the renal RI ≥0.05 has a high specificity but low sensitivity, presumably also due to the problem of bilateral RAS, where it has no diagnostic validity.)15, 24, 25, 27 In particular, in cases where the contralateral RI is inconclusive, determination of splenic RI is a very significant additional reference in the assessment of renal RI. We found that the diagnostic power of ΔRIK−S in detecting RAS is at least well in the range of those reported for other Doppler criteria.15, 17, 19, 25, 36 Sensitivity and specificity as well as PPV and NPV for ΔRIK−S were comparable to, for example, the recently reported new criteria of maximal systolic acceleration (ACCMax) and maximal acceleration index (AImax), which are said to have a particularly high diagnostic power.19 However, whereas these parameters are relatively cumbersome to determine, ΔRIK−S is a very simple index that can be easily calculated by physicians at the bedside. In particular, we observed a high NPV (96.2%) for ΔRIK−S. Since the primary goal of RAS‐diagnostic by Doppler in clinical practice is the exclusion of a significant stenosis, a high NPV is of special importance.17, 19, 25 As shown by the present study, ΔRIK−S is an additional criterion for diagnosis of RAS. It is easily and rapidly measurable in virtually all patients, in contrast to the direct Doppler criteria. Its application should further enhance the diagnostic power of the Doppler sonographic diagnosis of renal artery stenosis, in particular in patients with bilateral renal artery stenosis, with a single kidney, or with proximal renal arteries difficult to access.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

ACKNOWLEDGMENTS

None.

Grupp C, Koziolek MJ, Wallbach M, Hoxhold K, Müller GA, Bramlage C. Difference between renal and splenic resistive index as a novel criterion in Doppler evaluation of renal artery stenosis. J Clin Hypertens. 2018;20:582–588. 10.1111/jch.13212

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