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AJR 2003; 180:885-892
© American Roentgen Ray Society

Review

The Resistive Index in Renal Doppler Sonography: Where Do We Stand?

Mitchell E. Tublin1, Ronald O. Bude2 and Joel F. Platt2

1 Department of Radiology, University of Pittsburgh School of Medicine, 200 Lothrop St., Pittsburgh, PA 15213.
2 Department of Radiology, University of Michigan Medical School, 130 Catherine Rd., M4101 MS1, Box 0624, Ann Arbor, MI 48109.

Received February 27, 2002; accepted after revision September 19, 2002.

 
Address correspondence to M. E. Tublin.


Introduction
Top
 Introduction
Technique
 Applications
 Doppler Sonography of Renal...
 Theory of RI
 Conclusion
 References
 
Gray-scale renal sonography is still routinely performed during the initial evaluation of both native and transplant renal dysfunction. The results of the sonography study, however, often do not impact the differential diagnosis or management of renal disease. Indeed, despite marked improvements in technology, gray-scale renal sonography has changed little since the 1970s. Only basic anatomic information is obtained with the modality: renal length, cortical thickness, and grade of collecting system dilatation are assessed. Although these findings may help in evaluating disease chronicity, often the findings of sonography are normal despite severe renal dysfunction. Moreover, clinicians and radiologists accept that even the increased renal echogenicity that may be seen with renal failure (medical renal disease) lacks the specificity and sensitivity to be clinically relevant. Finally, although collecting system dilatation is reliably detected, it is often not possible to differentiate obstructive and nonobstructive pelvicaliectasis on gray-scale sonography alone. We suspect that this purely anatomic approach to renal sonography, coupled with improved yet less expensive platforms, has resulted in significant incursions on radiology turf by nephrologists, internists, and urologists.

A series of articles published during the past decade indicated the potential of Doppler sonography for improving the sonographic assessment of renal dysfunction. Changes in intrarenal arterial waveforms were shown to be associated with urinary obstruction, several types of intrinsic renal disorders, and renal vascular disease [1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36]. The Doppler resistive index (RI) ([peak systolic velocity – end diastolic velocity] / peak systolic velocity) was advanced as a useful parameter for quantifying the alterations in renal blood flow that may occur with renal disease. Although the results of this work initially led many laboratories to attempt to incorporate Doppler sonography into the evaluation of renal dysfunction, discrepant findings in the literature and discouraging clinical experience prompted most radiologists to quickly abandon the RI.

In retrospect, the failure of the RI to live up to its promise as a parameter for measuring changes in renal status may be due to our often rudimentary understanding of the pathophysiology of renal disease and how it affects the Doppler arterial waveform. Nonetheless, we believe that current skepticism regarding the role of renal Doppler sonography may be unfortunate, given several recent studies that have provided a theoretic basis for understanding the abnormal arterial spectra that may be seen with renal disease. This article may explain why Doppler sonography may not be helpful in certain situations. Perhaps more important, it may provide a framework for future investigations of a more refined Doppler assessment of renal pathophysiology. A more sophisticated, clinically relevant approach to renal imaging, combining anatomy and function, may justify the continued sonographic assessment of renal dysfunction. The purpose of this article is to discuss the technical requirements of intrarenal Doppler sonography, proposed applications and controversies, recent research exploring the factors that influence the Doppler arterial waveform, and prospects for the future of renal Doppler sonography.


Technique
Top
 Introduction
 Technique
Applications
 Doppler Sonography of Renal...
 Theory of RI
 Conclusion
 References
 
Most studies describing the potential use of Doppler sonography for evaluating renal disease have stressed the need for meticulous technique [12, 15]. The highest frequency probe that gives measurable waveforms should be used, supplemented by color or power Doppler sonography as necessary for vessel localization. Arcuate arteries (at the corticomedullary junction) or interlobar arteries (adjacent to medullary pyramids) are then insonated using a 2- to 4-mm Doppler gate. Waveforms should be optimized for measurement using the lowest pulse repetition frequency without aliasing (to maximize waveform size), the highest gain without obscuring background noise, and the lowest wall filter (Fig. 1). Three to five reproducible waveforms from each kidney are obtained, and RIs from these waveforms are averaged to arrive at mean RI values for each kidney.



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  		Fig. 1. —Normal resistive index in 25-year-old healthy woman. Color Doppler sonogram is used to identify inter-lobar artery (arrow); waveform is maximized using lowest pulse repetition frequency possible.

 

Several studies have shown that a normal mean renal RI is approximately 0.60. The largest series to date (58 patients) reported a mean (±SD) RI of 0.60 ± 0.01 for subjects without preexisting renal disease [37]. Three prior studies also reported normal mean RI values of 0.64 ± 0.05 (21 patients) [38], 0.58 ± 0.05 (109 kidneys) [8], and 0.62 ± 0.04 (28 patients) [39]. In general, most sonographers now consider 0.70 to be the upper threshold of the normal RI in adults [12, 15]. Important exceptions to this threshold have been reported, however. In children, it is common for the mean RI to exceed 0.70 through the first year of life, and a mean RI greater than 0.70 can be seen through at least the first 4 years of life [40, 41]. In elderly patients without renal insufficiency, the normal RI can also exceed 0.70 [42]. It is uncertain whether this is a normal phenomenon, perhaps due to age-related changes in vascular compliance, or the consequence of small vessel changes in the kidney due to aging.


Applications
Top
 Introduction
 Technique
 Applications
Doppler Sonography of Renal...
 Theory of RI
 Conclusion
 References
 
Obstruction
Most literature on renal Doppler sonography has focused on the potential role of Doppler sonography in the evaluation of ureteral obstruction. The limitations of the gray-scale examination for potential acute and chronic obstruction have been recognized for the past quarter century. The purely anatomic information that is obtained on sonography may be incomplete or misleading: collecting system dilatation can be caused by conditions that are not obstructive (residual dilatation from prior obstruction that has been relieved, pyelonephritis, and reflux). Also, in the acute setting, obstruction may be present for several hours before collecting system dilatation occurs.

In the early 1990s, several groups postulated that the pathophysiology of urinary obstruction might be reliably manifested by changes in arterial Doppler spectra [2, 5, 8, 9, 15, 17, 25]. This application was based on exhaustive animal research that showed a unique biphasic hemodynamic response to complete ureteral obstruction. A short period (<2 hr) of likely prostaglandin-mediated vasodilatation occurs immediately after obstruction. After this period, renal blood flow decreases, and renal vascular resistance increases [43, 44, 45, 46, 47]. Initial studies suggested that this vasoconstriction response was primarily mechanical, due to increases in collecting system pressures. Recent research, however, suggests that complex interactions between several regulatory pathways (renin–angiotensin, kallikrein–kinin, and prostaglandin–thromboxane) are responsible for intense, postobstructive renal vasoconstriction [48, 49, 50, 51, 52, 53, 54, 55, 56].

This vasoconstriction response, however mediated, seemed to be an ideal phenomenon to be detected by changes in the RI. In an initial series from researchers at the University of Michigan, RIs from 21 hydronephrotic kidneys were obtained before nephrostomy. The mean RI in 14 kidneys with confirmed obstruction (0.77 ± 0.04) was significantly higher than the mean RI from seven kidneys with nonobstructive pelvicaliectasis (0.64 ± 0.04). Moreover, RI values returned to normal after nephrostomy [8]. These encouraging results were essentially duplicated in a larger study of 229 kidneys. In this study, a discriminatory RI threshold of 0.70 was used; the sensitivity and specificity of the Doppler diagnosis of obstruction were 92% and 88%, respectively. Moreover, the accuracy of the Doppler diagnosis of obstruction increased when the RI of the potentially obstructed kidney was compared with that of the unaffected contralateral kidney (Fig. 2A, 2B). An RI difference greater than 0.10 between kidneys was seen only with true obstructive pelvicaliectasis [9]. After these encouraging results, series were published indicating the potential of Doppler sonography to differentiate renal transplant obstructive and nonobstructive pelvicaliectasis [13] and to determine ureteral stent patency [16].



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  		Fig. 2A. —30-year-old man with acute left flank pain. Sonogram shows unobstructed right kidney and corresponding normal resistive index.

 


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  		Fig. 2B. —30-year-old man with acute left flank pain. Sonogram shows obstructed left kidney. Note mild collecting system dilatation, elevated left RI, and marked difference in RIs (0.12) between kidneys. (Reprinted with permission from [58])

 

Although these and several other encouraging reports [2, 5, 25, 33, 36, 57] have prompted many centers to add RI analysis to the sonographic evaluation of collecting system dilatation, anecdotal experience, follow-up clinical trials, and animal studies have dampened enthusiasm for the clinical impact of Doppler sonography [58, 59, 60, 61, 62, 63, 64, 65]. The utility of Doppler sonography in the evaluation of partial ureteral obstruction was found to be particularly limited. In a series published by Chen et al. [60], for example, the sensitivity of Doppler sonography for the diagnosis of obstruction was reported to be only 52%. Although the results of the examination were often positive with high-grade obstruction, most patients with partial obstruction had normal RIs. This failure of Doppler sonography to reliably detect low-grade obstruction was subsequently confirmed in pig and rabbit models [64, 65]. Several groups have shown that the sensitivity of Doppler sonography for the detection of partial obstruction may be improved by performing the study after forced diuresis (diuretic Doppler sonography) [66, 67, 68, 69, 70, 71, 72, 73, 74]. This technique has not yet been embraced by either the general radiology or the urology community, although recent experimental work has provided a theoretic justification for the use of diuretic Doppler sonography in the evaluation of obstructive uropathy.

The potential role of Doppler sonography in the evaluation of renal colic has been particularly controversial. In two initial series, either an RI greater than 0.70 or a difference of greater than 0.06–0.10 in mean RI values between kidneys was found to be highly specific and sensitive for acute obstruction [17, 25]. Perhaps more important, several cases of obstruction were identified before the development of collecting system dilatation. Unfortunately, to our knowledge, these results were not duplicated in later series. In a study performed at the University of Pittsburgh of 32 patients with suspected ureteral obstruction, for example, the sensitivity and specificity of the Doppler assessment of obstruction were only 44% and 82%, respectively [58]. Deyoe et al. [59] published nearly identical results. Several reasons for these discrepant findings were suggested in a spirited commentary published in Radiology [75, 76]. These reasons included the absence of patients with partial obstruction in initial promising studies, the potential vasodilatory effects of nonsteroidal medications typically used for the treatment of pain associated with urinary calculi, the uncertain effect of hydration on renal blood flow (and the RI), and the potential of the iodinated contrast material used for excretory urography (the gold standard in all studies) to induce intense vasoconstriction. Many of these confounding factors were subsequently addressed in follow-up studies [66, 77, 78].

Unfortunately, instead of fostering investigation into the role of Doppler sonography in the acute setting, this debate contributed to skepticism over the utility of the RI. Moreover, the recent almost universal acceptance of unenhanced CT as a gold standard for the identification of ureteral calculi has markedly decreased any incentive to perform sonography in the acute setting, except perhaps in the evaluation of the pregnant patient [79, 80].

Nonobstructive Renal Disease
The lack of specificity of the gray-scale examination in evaluating intrinsic renal disease has been frustrating to nephrologists and radiologists for decades. Although renal size, cortical thickness, and echogenicity may be helpful in assessing disease chronicity, these findings typically do not aid in the differential diagnosis or management of renal disease.

The potential of Doppler sonography to serve as a useful adjunct for the gray-scale assessment of renal disease was advanced in a series of articles published by the group from the University of Michigan. In the initial work performed by Platt et al. [10], renal biopsy results of 41 patients were correlated with RI analysis. Those patients with isolated glomerular disease had normal RI values (mean, 0.58), whereas subjects with vascular or interstitial disease had markedly elevated RI values (means, 0.87 and 0.75, respectively). Unfortunately, these encouraging results were not reproduced in similarly designed studies performed by Mostbeck et al. [81] and more recently by McDermott et al. [82]. Moreover, there was little correlation between the degree of renal dysfunction (assessed by serum creatinine values) and the RI.

Although Doppler sonography clearly does not substitute for renal biopsy, several studies have suggested that Doppler sonography might aid in the management of established renal disease. In a series published by Patriquin et al. [7], for the example, Doppler sonography could predict renal recovery from hemolytic uremic syndrome before clinical improvement. Similarly, the RI was thought to correlate well with renal involvement in patients with progressive systemic sclerosis [28]. The ability of Doppler sonography to identify latent hepatorenal syndrome before liver transplantation was shown by the University of Michigan group [14]. Those same researchers reported that Doppler sonography was useful in predicting the outcome of patients with lupus nephritis: in a prospective series of 34 patients with various degrees of nephritis, an elevated RI value was shown to be a predictor of poor renal outcome, even in patients with normal baseline renal function [20]. Doppler sonography was also suggested as a useful tool for evaluating nonobstructive acute renal failure; an RI greater than 0.07 was found to be a reliable discriminator between acute tubular necrosis and prerenal failure, although a theoretic framework (and supporting histologic findings) to explain this finding was lacking [11]. Finally, the RI has been advocated as a useful marker of diabetic nephropathy [83, 84], although other studies have suggested that Doppler sonography offers little beyond serum creatinine levels and creatinine clearance rates in patients with early diabetic nephropathy and normal renal function [19, 31, 35, 85].


Doppler Sonography of Renal Transplant Dysfunction
Top
 Introduction
 Technique
 Applications
 Doppler Sonography of Renal...
Theory of RI
 Conclusion
 References
 
A swing from initial enthusiasm to skepticism also occurred over a series of articles exploring the role of Doppler sonography in the evaluation of transplant dysfunction [1, 3, 4, 22, 23, 24, 86, 87, 88, 89, 90]. An elevated RI was initially considered a finding specific for rejection [1, 3, 22, 23]. Multiple researchers have since documented the lack of specificity of an elevated RI [86, 87, 88, 89, 90]. In a series published by Perrella et al. [87], for example, the sensitivity and specificity of Doppler sonography for the diagnosis of rejection were 43% and 67%, respectively, when a threshold RI of 0.90 was applied. Because of these discouraging results, most physicians consider an elevated RI to be a nonspecific marker of transplant dysfunction. Although RI analysis is not helpful in differentiating the typical causes of transplant dysfunction (acute tubular necrosis, rejection, and immunosuppression toxicity), it is still useful for potentially identifying vascular complications associated with transplantation. Although intrarenal Doppler sonography has failed as a reliable screening examination for transplant renal artery stenosis, identification of a tardus–parvus waveform from an intrarenal artery should prompt even more diligent color and duplex Doppler evaluation of the renal artery anastomosis to exclude arterial stenosis [6]. Focal high-velocity, low-impedance intrarenal arterial flow might suggest an arteriovenous fistula. Finally, renal vein thrombosis may be present when diastolic flow is reversed and no renal venous flow is detected [91].


Theory of RI
Top
 Introduction
 Technique
 Applications
 Doppler Sonography of Renal...
 Theory of RI
Conclusion
 References
 
As suggested previously, the failure of the RI to become a meaningful parameter for evaluating kidney physiology and function may be due to our often rudimentary understanding of renal disease. Furthermore, Doppler sonographic analysis of renal artery waveforms was empirically applied to disease characterization before a full understanding of the factors that affect the arterial waveform (e.g., vascular compliance, vascular resistance, and heart rate) was obtained. Thus, this empiric use of Doppler sonography gave less than satisfactory results. For example, it was almost universally accepted in the early Doppler literature that the RI varied directly with changes in renal vascular resistance. In many reports, the terms "resistive index" and "renal vascular resistance" are used interchangeably, although the relationship between these factors and other potentially confounding variables has, generally, not been considered.

A series of in vitro experiments recently performed at the University of Michigan has convincingly shown the importance of vascular compliance in RI analysis [92]. (Compliance is the rate of change of volume of a vessel as a function of pressure. Anyone who has observed a pulsating artery whose diameter expands in systole and contracts in diastole has seen the visual manifestation of the effect of compliance.) In vitro experiments were performed to assess the impact of changes in vascular resistance and compliance on the RI. The RI was dependent on vascular compliance and resistance, becoming less and less dependent on resistance as compliance decreased, and being completely independent of vascular resistance when compliance was zero. In another in vitro study performed by the same group, the RI was shown to decrease with increases in the cross-sectional area of the distal arterial bed; this effect was independent of compliance and vascular resistance.

Ex vivo results, similar to in vitro results, were obtained in a series of experiments performed at Albany Medical College [93]. Rabbit kidneys were perfused ex vivo using a pulsatile perfusion system (Fig. 3). Renal vascular resistance, systole, diastole, pulse pressure, and pulse rate were controlled and monitored while the RI was simultaneously measured. A linear relationship was seen between the RI and pharmacologically induced changes in renal vascular resistance. However, the RI increased only with marked, likely nonphysiologic increases in renal vascular resistance. Those changes in the RI that were seen with intense vasoconstriction were only marginally greater than RI measurement variability. The RI was markedly affected by changes in driving pulse pressures, however. A linear relationship was shown between the pulse pressure index (systolic pressure – diastolic pressure / systolic pressure) and the RI.



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  		Fig. 3. —Diagram of ex vivo pulsatile perfusion system. Perfusion pressures (systole and diastole) are adjusted by changing heights of reservoirs, and pulse rate is controlled by function generator. Flow (F) and pressure (P) are measured instantaneously upstream from renal artery using in-line probes. Doppler spectra are simultaneously obtained from perfused kidney using commercially available ultrasound platform. Temp = temperature. (Reprinted with permission from [94])

 

In a follow-up series of experiments, the Albany group attempted to indirectly explore the effect of changes in vascular distensibility on the RI ex vivo [94]. Isolated rabbit kidneys were subjected to pulsatile perfusion while the renal pelvis was pressurized via the ureter. The authors hypothesized that resultant increases in renal interstitial pressure would decrease arterial distensibility and that these effects would be most marked during diastole. Arterial distensibility was indirectly assessed by analyzing changes in vascular conductance (flow / pressure). Graded increases in renal pelvic pressures resulted in increased renal vascular resistance, decreased mean conductance, an increased conductance index (systolic conductance – diastolic conductance / systolic conductance) and an increased RI. The results indicated the importance of the interaction among vascular distensibility, resistance, and pulsatile flow in RI analysis (Figs. 4 and 5). Many of these findings were replicated in a study performed by Claudon et al. [95], in which changes in pig renal blood flow during acute urinary obstruction were assessed using contrast-enhanced harmonic sonography. Overall, these trials have convincingly shown that disease phenomena that affect vascular distensibility, such as renal artery interstitial fibrosis and vascular stiffening, might substantially affect the RI.



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  		Fig. 4. —Diagram shows how ureteral pressure affects mean, systolic, and diastolic cross-sectional areas of renal arterioles. Area of compliant vessels is determined by transmural pressure (intraarterial pressure – interstitial pressure). Interstitial pressure is almost zero in absence of ureteral pressure (left half of diagram). During diastole, cross-sectional area of vessel is relatively large (B), and some additional distention occurs during systole (A). High ureteral pressures increase interstitial pressure (right half of diagram). In this setting, arteriole is almost occluded during diastole because transmural pressure is so low (D), but significant distention still occurs during systole (C). Although mean cross-sectional area is markedly smaller with high ureteral pressures (mean conductance of C and D, A and B), relative distention that occurs during systole is greater (conductance of A > B, but C >>D). These cyclic changes in cross-sectional area are underlying cause for parallel changes in total renal conductance (flow / pressure). (Reprinted with permission from [94])

 


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  		Fig. 5. —Diagram shows how ureteral pressure affects systolic and diastolic blood flow in larger renal arteries typically insonated during clinical renal Doppler studies. Each section of figure shows Doppler gate in conduit (segmental or arcuate) artery, which branches into smaller compliant vessels downstream. Length of arrow in Doppler gate represents velocity of blood flow. As shown in Figure 4, changes in ureteral pressure (0 mm Hg in A and B; 60 mm Hg in C and D) significantly affect arteriolar cross-sectional areas and thus total blood flow volume. In less compliant, larger conduit arteries, these changes in blood flow are manifested as cyclic changes in blood velocity. Thus, relative increase in velocity that occurs at systole (measured using resistive index) is greater when ureteral pressure is elevated (velocity in A > B, but C >> D). (Reprinted with permission from [94])

 

This body of experimental work may help explain the disappointing results obtained using the RI to evaluate ureteral obstruction. The high false-negative rate of the technique may, in some cases, be due to low-grade, extremely early obstruction or forniceal rupture. In these settings and with severe long-standing obstruction, arterial distensibility would be marginally affected because interstitial pressures are relatively normal. The increased reliability of Doppler sonography when a furosemide challenge is used might also suggest the impact of acutely elevated interstitial pressures on renal blood flow and the RI.

The complex interaction between renal vascular resistance and compliance might also help explain the failure of Doppler sonography to consistently differentiate types of intrinsic renal disease. One might speculate that early reports of elevated RIs with vascular–interstitial disease (and not glomerulopathies) were primarily due to the decreased tissue and vascular compliance associated with these types of renal diseases (and not only associated with increased renal vascular resistance). Later discouraging reports might be due to differing patient populations and mixed renal diseases; a single isolated RI may not be useful in the differential diagnosis of intrinsic renal disease because of mixed histology and differing effects on vascular compliance and resistance. On the other hand, the impact of vascular compliance on the RI may help to explain recent encouraging studies exploring the utility of Doppler sonography in the assessment of end-organ damage in patients with hypertension and arteriosclerosis. In several recent studies, an elevated RI was found to correlate with left ventricular hypertrophy and carotid intimal thickening [96, 97, 98].


Conclusion
Top
 Introduction
 Technique
 Applications
 Doppler Sonography of Renal...
 Theory of RI
 Conclusion
References
 
We do not mean to imply that Doppler sonography currently has no role in the evaluation of renal disorders. The Doppler arterial waveform is the product of the interaction of a number of factors, sometimes in a complicated way. Once these factors are better understood, and if they can be taken into account, correctly understood Doppler sonography may be a useful clinical tool to evaluate renal dysfunction. A more sophisticated functional approach may allow radiologists to maintain a preeminent role in the imaging assessment of renal disease. Further studies into this topic are suggested and strongly encouraged.


References
Top
 Introduction
 Technique
 Applications
 Doppler Sonography of Renal...
 Theory of RI
 Conclusion
 References
 

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