Eur Radiol (2002) 12:796–803 DOI 10.1007/s003300101121

V. Napoli S. Pinto I. Bargellini C. Vignali R. Cioni P. Petruzzi A. Salvetti C. Bartolozzi

Received: 13 April 2001 Revised: 26 June 2001 Accepted: 31 July 2001 Published online: 18 December 2001 © Springer-Verlag 2001

V. Napoli (✉) · I. Bargellini · C. Vignali R. Cioni · P. Petruzzi · C. Bartolozzi Division of Diagnostic and Interventional Radiology, Department of Oncology, Transplants and Advanced Technologies in Medicine, University of Pisa, Via Paradisa 2, Pisa 56124, Italy e-mail: [email protected] Tel.: +39-050-996961/995424 Fax: +39-050-996960 S. Pinto · A. Salvetti Department of Internal Medicine, University of Pisa, Via Paradisa 2, Pisa 56124, Italy

U R O G E N I TA L

Duplex ultrasonographic study of the renal arteries before and after renal artery stenting

Abstract The aim of our study was to evaluate feasibility and accuracy of colour-coded duplex US in the detection of renal artery stenosis before and after stenting. Eighty-four patients (23 women, 61 men; mean age 64 years) with significant renal artery stenosis were studied with Doppler US, before and after stenting. A combined anterior and translumbar approach was used to visualise the renal arteries. Renal artery stenosis and in-stent restenosis were proved by the increase of renal peak systolic velocity (PSV) and renoaortic ratio (RAR). Laboratory-specific threshold values of PSV and RAR were used to assess sensitivity and specificity of Doppler US. The renal arteries were visualised in all patients (feasibility 100%). A statistically significant difference of PSV and RAR was demonstrated be-

Introduction Atherosclerotic renal artery stenosis (ARAS) represents the most common cause of renovascular disease (ca. 70%), often associated with hypertension and progressive renal failure. When not treated, stenoses can progress to arterial occlusion [1, 2, 3]. This event is more frequent in high-grade stenoses [1, 2, 3, 4]. Renal artery stenting has become an important alternative to surgery in the treatment of renovascular disease, being associated with a high technical success rate (96–100%), low periprocedural mortality rate (0.5%) and an incidence of in-stent restenosis of approximately 16% [5].

tween patent and stenotic renal arteries, before stenting, and between stenotic and stented renal arteries. No difference was demonstrated in cases of in-stent restenosis (n=21). Before stenting, sensitivity of PSV and RAR was 93%, whereas specificity rates were 92 and 96%, respectively. After stenting sensitivity and specificity rates were, respectively, 90 and 93% for PSV, and 95 and 95% for RAR. Doppler US represents a feasible and reliable technique in the detection of renal artery stenosis and in-stent restenosis, although laboratory-specific threshold values are required to improve its accuracy. Keywords Duplex sonography · Ultrasound · Renal artery · Stent and prosthesis

Considering the increasing number of patients with renovascular disease treated percutaneously, a precise definition becomes necessary for the role of different clinical and radiological criteria in the follow-up of these patients. A discrepancy has been demonstrated between clinical data (blood pressure measurements and renal function evaluation) and angiographic findings. In fact, in up to 15% of patients with apparently cured renovascular hypertension after angioplasty a restenosis of the renal artery can be angiographically demonstrated [6]; therefore, clinical evaluation alone is inadequate, and accurate direct monitoring of renal artery patency is required. Duplex US represents a non-invasive, easily available, repeatable and well-tolerated technique that is able

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to detect renal artery stenosis before and after percutaneous treatment [4, 7, 8, 9]. Its sensitivity and specificity can improve by means of laboratory-specific threshold values of direct velocimetric indexes [10], whereas feasibility can increase combining the anterior approach with an alternative approach, such as the translumbar one. The purpose of our study was to evaluate feasibility and accuracy of duplex US in the follow up of patients with renovascular disease after renal artery stenting. We verified whether combining the anterior and the translumbar approaches might increase the feasibility of duplex US, and we calculated sensitivity and specificity of duplex US in the diagnosis of in-stent significant stenosis (>60%), using threshold values of the peak systolic velocity (PSV) and the reno-aortic ratio (RAR) obtained from published data and from our own series.

Patients and methods Eighty-four patients with haemodynamically significant renal artery stenosis proved by angiography were studied by means of colour duplex Doppler US, before and after stenting. Table 1 shows demographic, clinical and radiological baseline characteristics. Renal arteriography showed 165 main renal arteries (3 patients with single-functioning kidney) and 21 accessory renal arteries (19 patients, 22.6%), with a total number of 130 stenotic arteries. The degree of arterial stenosis was calculated by means of a built-in automatic angiographic software device as 1 minus the ratio between the diameter of the narrowest lumen of the artery and the diameter of the nearest distal normal lumen unaffected by post-stenotic dilatation [11]. Ninety-eight stenotic arteries underwent stent deployment, 16 were treated with percutaneous transluminal renal angioplasty (PTRA) and 2 renal occlusions required surgical nephrectomy. Fourteen significant stenoses (7 occlusions and 7>60%), in patients with a contralateral stented stenosis, entered follow-up without treatment. Blood pressure and serum creatinine levels were recorded preprocedurally and after stenting at 1, 3, 6 and 12 months follow-up, and every 6 months thereafter. Duplex US technique and protocol Patients underwent duplex US evaluation with multifunctioning echographic state-of-the-art equipment (AU5 Colour Imaging, Esaote Biomedica, Genova, Italy) using a convex-array 3.5-MHz probe. The Doppler frequency generally applied was 2.5 MHz. At least three velocimetric measurements were performed at the level of main renal artery and of the renal parenchyma, bilaterally, with a combined anterior and translumbar approach and multiple longitudinal, transversal and oblique scans. All US studies were performed by one sonographer who was blinded to the results of preinterventional angiography. Patients, fasting for at least 6–8 h, were first studied in a supine position with the anterior approach and transversal epigastric scans, to visualise the ostium and the proximal tract of the main renal artery. Then, in the lateral decubitus with translumbar approach, the ostium, the entire renal artery, the renal parenchyma and the intrarenal arteries were studied. The visualisation of the main renal arteries, as well as of accessory and aberrant renal arteries, was obtained with the colour function. The sampler volume

Table 1 Demographic, clinical and radiological baseline characteristics of patient population RAS renal artery stenosis; ARAS atherosclerotic renal artery stenosis; FMD fibromuscular-dysplastic renal artery stenosis Characteristics Demographic No. of patients Gender (M/F) Mean±SD age (years) Range age (years) Clinical Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Serum creatinine (mg/ml)

84 23 of 61 64±9.9 38–79 Mean±SD 166±20 93±10 1.51±0.61

Radiological (arteriographic) No. of RAS Type of stenosis (ARAS/FMD) Ostial site of stenosis (n) Single kidney (n) Bilateral stenosis (n/%) Unilateral stenosis (n/%) Mean±SD grade of stenosis (%) Range grade of stenosis (%) Occlusion (n)

130 128/2 67 3 46/35.7 84/64.6 70.6±11.8 60–100 11

was then positioned where a coloured mosaic pattern was shown. In case of absence of abnormalities in the colour patterns, the sampler volume was randomly positioned. The velocimetric Doppler spectral analysis was performed with a Doppler-to-vessel angle of 30–60° and a sampler volume size of 3 mm. In some cases wall filters (50–100 KHz) were required to reduce the pulsatility artefacts at the level of the ostium. The samplings of the main renal artery and of the abdominal aorta were performed with a pulsed repetition frequency (PRF) of 3 MHz. The US criteria for the diagnosis of renal artery stenosis and in-stent restenosis were represented by the increase of the renal peak systolic velocity (PSV), expressed in centimetres per second, after correction of the insonating angle, and of the reno-aortic ratio (RAR), calculated as the ratio between renal and aortic PSV (peak systolic velocity of the abdominal aorta at the level of the renal artery or above its ostium) [12]. The US examination was considered technically successful only when three velocimetric measurements were obtained at three different levels of the renal artery bilaterally. In case of no visualisation of the renal artery, renal artery occlusion was demonstrated by the absence of blood flow in the segmental arteries. After stenting, the structure of the stent yielded its direct visualisation by means of B-mode imaging, since stents create a double line and/or a typical hyperechoic aspect on B-mode. The coefficients of variation, evaluated in a selected group of five consecutive hypertensive patients, were 5.5 and 2.2% for RAR and PSV, respectively. Follow-up In all patients after stenting, duplex US was performed at discharge, at 1, 3, 6 and 12 months, and every 6 months thereafter; computed tomographic angiography (CTA) or magnetic resonance angiography (MRA) were performed within 12 months after treatment and annually thereafter. Restenosis was clinically suspected

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in case of rapid deterioration of renal function and/or increase of blood pressure (n=38). In these cases, further US controls were required, associated with CTA (n=28), MRA (n=6) or both (n=4). All US studies were performed by one sonographer, blinded to clinical and MRA/CTA findings. Renal arteriography was performed in those cases in whom significant restenosis was demonstrated by means of duplex US and CTA or MRA (n=21). Mean follow-up time was 24 months (range 3–61 months).

Table 2 Duplex US results before stenting and at follow-up Doppler studies

Before

Follow-up study

Mean±SD study time (min) Approaches Feasibility rate (%)

22±7 A A plus TL 79 100

18±3 A A plus TL 87 100

Anterior (A) and translumbar (TL) approaches Statistical analysis Data series were processed with a JMP software package (Statistics Made Visual, SAS Institute Inc., Cary, N.C.). Continuous variables of PSV and RAR obtained at the Doppler spectral analysis were given as mean±SD. A paired Student’s t-test was used to compare mean±SD values. Chi-square testing was used for analysis of categorical data. A p-value <0.05 was considered as statistically significant. Sensitivity, specificity, positive predictive values and negative predictive values, in the diagnosis of significant renal artery stenosis (>60%), were calculated for a range of values of PSV and RAR, large enough to produce false-positive rates from 0 to 100%. From these data receiver operating characteristics (ROC) curves were obtained for each parameter, through a NCSS 97 software package. The chosen laboratory-specific threshold values were those associated with highest sensitivity and lowest number of false-positive results [13]. In order to avoid underestimation of true-positive results, renal artery occlusions were not considered to build ROC curves.

Results Combining the anterior and the translumbar approaches, renal arteries and stents could be visualised in all cases (Table 2). Mean US study time significantly decreased after stenting (due to the acquired knowledge of the vascular anatomy after DSA; Table 2). In the pre-procedural study, a statistically significant difference of mean values±SD and values of PSV and RAR was proved between patent and stenotic renal arteries. No significant differences of PSV and RAR were observed between ostial and non-ostial stenosis (Table 3). Renal artery stenting was performed monolaterally in 70 patients and bilaterally in 14. On follow-up, in-stent restenosis was angiographically demonstrated in 21 patients (restenosis rate of 21.4%, 21 of 98 lesions). After stenting, at discharge and at 1-month followup, no significant difference of PSV and RAR was demonstrated between non-stenotic and stented renal arteries. A significant difference of PSV and RAR before and after stenting was proved. It persisted over time in case of stent patency, whereas it was no longer demonstrated when in-stent restenosis occurred, because of the increase of mean values±SD of PSV and RAR (Table 4). Before stenting, sensitivity rates of PSV and RAR in the detection of renal artery stenosis calculated on the basis of published threshold values (PSV>180 cm/s and RAR>3.5 units) [12] were 87 and 79%, respectively,

Table 3 Comparison of duplex US results before stenting in patent vs stenotic arteries. n=number of renal arteries; PSV renal artery peak systolic velocity; RAR reno-aortic ratio Groups

N

PSV

RAR

Patent arteries Ostial stenosis Proximal stenosis

35 67 61

102±35 229±102a,b 203±77a

1.8±0.6 3.89±1.8a,b 3.52±1.4a

a p<0.05 b p>0.05

vs patent arteries vs proximal stenosis

Table 4 Doppler indexes before and after renal stenting US studies

Before 42–72 h 1 month 3 months 6 months 12 months a p<0.05 b p>0.05

Patent stents (n=77)

In-stent restenosis (n=21)

PSV

RAR

PSV

RAR

245±69 89±44a 85±35a 76±45a 105±47a 111±33a

4.2±1.3 1.58±0.7a 1.55±0.6a 1.29±0.7a 2.11±1.1a 2.09±1.0a

227±17 115±16a 107±95a 122±28a 138±80a 184±74°

3.93±1.5a 2.03±1.0a 1.80±1.4a 2.13±0.7a 2.41±1.5a 3.48±1.7°

vs before vs before

with specificity rates of 92 and 96%. With our own threshold values, obtained from ROC curves (PSV> 159 cm/s, RAR>3.26 units) the sensitivity rates of PSV and RAR were 93 and 93%, positive predictive values 79 and 77%, specificity rates 92 and 96%, and negative predictive values 98 and 99%, respectively (see Tables 5, 7). After stenting, with the use of published threshold values (PSV>180 cm/s and RAR>3.5 units) [12], sensitivity of PSV and RAR in the detection of in-stent restenosis was 57%, with specificity rates of 96 and 98%, respectively. Using our own threshold values (PSV> 144 cm/s and RAR >2.53 units), a higher sensitivity and a slightly lower specificity was demonstrated (Figs. 1, 2; Tables 6, 7). On the basis of Bayes theorem, the positive and negative predictive values of PSV, adjusted for the prevalence of in-stent restenosis, were 97 and 79%, respectively, and the positive and negative predictive values of RAR were 98 and 83%, respectively (Fig. 3).

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Fig. 1a–d Case of 47-year-old man with hypertension and normal renal function. Digital subtraction angiography (DSA) shows a significant >60% atherosclerotic renal artery stenosis in the proximal tract of the left renal artery, b treated by stenting. c Post-pro-

Table 5 Doppler US results using PSV>159 cm/s (a) and RAR>3.26 unit (b) in the diagnosis of RAS>60% before stenting, compared with digital subtraction angiography (DSA) findings

(a) DSA

cedural US examination allows visualisation of the stent using B-mode imaging and of its patency using d power Doppler. The arrows indicate the stent as visualised at DSA (b) and US (c, d)

Duplex US

Total

PSV<159 cm/s

PSV>159 cm/s

Renal artery occlusion

<60% RAS >60% RAS Total

23 (true negative) 6 (false negative) 29

2 (false positive) 88 (true positive) 90

0 11 11

(b) DSA

Duplex US

<60% RAS >60% RAS Total

25 105 130 Total

RAR<3.26 unit

RAR>3.26 unit

Renal artery occlusion

24 (true negative) 7 (false negative) 31

1 (false positive) 87 (true positive) 88

0 11 11

25 105 130

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Fig. 2a–e Same case as Fig. 1, 6 months after stenting. In-stent miointimal hyperplasia at a power Doppler associated with an increase of peak systolic velocity (PSV), detected by b the anterior approach. c The translumbar approach allows visualisation of the renal stent in B-mode and with the colour function. d The increase of PSV indicates the presence of significant in-stent restenosis >60%, confirmed at e DSA. The arrows indicate the stent with the typical hyperechoic pattern. A abdominal aorta; K kidney

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Table 6 Sensitivity and specificity for PSV>144 cm/s (a) and RAR>2.53 unit (b) in the diagnosis of significant in-stent restenosis (>60%). There are no stent occlusions

(a) DSA

Total

PSV<144 cm/s

PSV>144 cm/s

Renal artery occlusion

<60% RAS >60% RAS Total

72 (true negative) 2 (false negative) 74

5 (false positive) 19 (true positive) 24

0 0 0

(b) DSA

Duplex US

<60% RAS >60% RAS Total

Table 7 Sensitivity and specificity on ROC curves of PSV and RAR in the diagnosis of significant RAS (>60%) before stenting, and significant instent restenosis (>60%)

Duplex US

77 21 98 Total

RAR<2.53 unit

RAR>2.53 unit

Renal artery occlusion

73 (true negative) 1 (false negative) 74

4 (false positive) 20 (true positive) 24

0 0 0

Area under the curve

Standard errors

77 21 98

Optimal threshold value

Sensitivity (%)

Specificity (%)

Significant RAS (>60%) before stenting PSV 0.976 0.021 RAR 0.974 0.022

159 cm/s 3.26 unit

93 93

92 96

Significant in-stent restenosis (>60%) PSV 0.948 0.020 RAR 0.980 0.012

144 cm/s 2.53 unit

90 95

93 95

Discussion Our findings indicate that Duplex colour Doppler study is a non-invasive, low-cost, effective tool in the assessment of renovascular disease that allows the detection of renal artery stenosis before and after treatment. It is able to directly visualise the stent and the distal tract of the renal artery. The use of colour/power Doppler US enables the evaluation of stent patency and the identification of instent restenosis, which can be better defined by the velocimetric Doppler spectral analysis. A high accuracy has been demonstrated in the diagnosis of haemodynamically significant renal arteries stenoses (>60%) using the direct velocimetric indices (PSV and RAR) obtained from the Doppler spectral analysis [12, 14, 15, 16, 17]. The evaluation of sensitivity and specificity of PSV and RAR must take into account the prevalence of renal artery stenosis in the studied population, by means of ROC curve statistical models [18]. In a recent European study, Bakker et al. underline the importance of stating laboratory-specific threshold Fig. 3a, b Receiver operating characteristic (ROC) curves statistical method used for the evaluation of sensitivity and specificity of PSV and reno-aortic ratio (RAR) in detecting significant renal artery stenosis (>60%), before and after stenting. The ROC plot sections are obtained for PSV–RAR criteria and response variable of DSA a before and b after stenting

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values of PSV and RAR to improve sensitivity and specificity of Doppler US [10]. In fact, using their own threshold values, the authors report a sensitivity rate for both PSV and RAR of 100%, with specificity rates of 90 and 84%, respectively. These data are confirmed by the results obtained in our series. In fact, comparing specificity and sensitivity rates obtained with our own threshold values with those obtained with published threshold values, a significant difference was observed, especially in terms of sensitivity (57 vs 90–95%). Bakker et al. showed a reduction of RAR threshold values from 3.5 to 2.7 units, associated with an increase of PSV threshold values from 180 to 226 cm/s, after treatment [10]. In our experience, instead, a progressive reduction of mean values ±SD of both PSV and RAR has been demonstrated after stenting, determining a reduction of the threshold values (from 159 to 144 cm/s and from 3.26 to 2.53 units, respectively). This phenomenon could be related to the reduction of the prevalence of renal artery stenosis in the studied population after stenting. Moreover, in-stent restenosis is usually due to intimal hyperplasia occurring at 3–12 months follow-up, which could be associated with lower values of PSV and RAR as compared with the chronic atherosclerotic or fibrodysplastic lesions that cause renal artery stenosis before stenting. Finally, there could be an overdilation of the renal arteries during stenting, which may contribute to the reduction of PSV and RAR absolute values [19]. Although associated with an increased sensitivity, the use of reduced threshold values on follow-up causes an increase in the number of false-positive results, from 1 (1.02%) to 5 (5.1%) for PSV, and from 1 (1.02%) to 4 (4.1%) for RAR. Further studies are required on the behaviour of the Doppler indices before and after treatment and on their role in the diagnosis of in-stent restenosis. The main limitation of Bakker et al.’s study is represented by the relatively low feasibility rate: 25% of patients could not be adequately studied because of bowel gas and/or obesity, which impeded the visualisation of

the stent [10]. In our study, combining the anterior and the translumbar approaches, correct sampling of in-stent velocity has been obtained in all patients. With the anterior approach alone, renal artery velocity can be adequately registered in 84–92% of patients [14, 20] and feasibility does not improve with the use of colour Doppler [21, 22]. The translumbar approach, introduced by Handa et al. to study the intrarenal arteries [23] and then used by Isikoff and Hill for the main renal artery [24], allows an optimal visualisation of the renal artery, avoiding the interposition of bowel gas or fat in obese patients [25]. With the translumbar approach, adjusting probe and patient positions, the US beam is almost parallel to the renal stent; therefore, during vessel sampling, noise and interference of stent material are reduced, and sampling can be performed at angles of incidence of approximately 45°, obtaining an optimal Doppler waveform. The main limitation of our study could be represented by the lack of angiographic follow-up; in fact, angiography was not performed routinely in all patients. However, all patients underwent accurate radiological follow-up by means of CTA and/or MRA, performed within 1 year from the procedure, in order to overcome the issue of clinically silent restenosis, avoiding more invasive techniques [26, 27].

Conclusion Colour duplex Doppler US represents a feasible, reliable and non-invasive technique for the study of renal arteries before and after stenting. A combined anterior and translumbar approach increases the feasibility, allowing an optimal visualisation of the renal artery and of the stent. The velocimetric Doppler spectral analysis of the renal arteries, with the evaluation of PSV and RAR, represents the best approach for the diagnosis of renal artery stenosis and in-stent significant restenosis, as long as appropriate laboratory-specific threshold values are chosen.

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