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Journal of Ultrasound (2009) xx, 1e11

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7 journal homepage: www.elsevier.com/locate/jus 69
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12 Doppler ultrasound and renal artery stenosis: 74

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An overview 76
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A. Granata a,*, F. Fiorini b, S. Andrulli c, F. Logias d, M. Gallieni e,

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19 G. Romano a, E. Sicurezza a, C.E. Fiore a 81
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22 Q2 a 84
Department of Nephrology, Dialysis and Internal Medicine, Vittorio Emanuele Hospital, Catania, Italy
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Department of Nephrology and Dialysis, ASUL 1 San Remo (IM), Italy
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Department of Nephrology and Dialysis, A. Manzoni Hospital, Lecco, Italy
Department of Nephrology and Dialysis, S. Camillo Hospital, Sorgono (Nuoro), Italy
Department of Nephrology and Dialysis, San Paolo Hospital and DMCO, University of Milano, Italy
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KEYWORDS Abstract Renovascular disease is a complex disorder, most commonly caused by fibromuscu-
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Doppler ultrasound; lar dysplasia and atherosclerotic diseases. It can be found in one of three forms: asymptomatic
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Ischemic nephropathy; renal artery stenosis (RAS), renovascular hypertension, and ischemic nephropathy. Particu-
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Renal artery stenosis; larly, the atherosclerotic form is a progressive disease that may lead to gradual and silent loss
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Renovascular disease. of renal function. Thus, early diagnosis of RAS is an important clinical objective since interven-
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tional therapy may improve or cure hypertension and preserve renal function. Screening for
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RAS is indicated in suspected renovascular hypertension or ischemic nephropathy, in order
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to identify patients in whom an endoluminal or surgical revascularization is advisable.
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Screening tests for RAS have improved considerably over the last decade. While captopril
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renography was widely used in the past, Doppler ultrasound (US) of the renal arteries (RAs),
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angio-CT, or magnetic resonance angiography (MRA) have replaced other modalities and they
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are now considered the screening tests of choice. An arteriogram is rarely needed for diag-
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nostic purposes only. Color-Doppler US (CDUS) is a noninvasive, repeatable, relatively inexpen-


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sive diagnostic procedure which can accurately screen for renovascular diseases if performed
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by an expert. Moreover, the evaluation of the resistive index (RI) at Doppler US may be very
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useful in RAS affected patients for predicting the response to revascularization. However,
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when a discrepancy exists between clinical data and the results of Doppler US, additional tests
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are mandatory.
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50 Sommario La malattia nefrovascolare e un disordine complesso e le cause piu comuni sono la 112
51 malattia aterosclerotica e la displasia fibromuscolare. Classicamente si presenta in una delle 113
52 seguenti tre forme: stenosi dellarteria renale (SAR) asintomatica, associata ad ipertensione 114
53 nefrovascolare e/o con nefropatia ischemica. La SAR su base aterosclerotica e una malattia 115
54 progressiva che puo determinare in maniera asintomatica o paucisintomatica perdita graduale 116
55 della funzione renale. Per tale motivo, la diagnosi precoce di SAR e un obiettivo clinico impor- 117
56 tante poiche la terapia interventistica puo migliorare o curare lipertensione e preservare la 118
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58 * Corresponding author. Dipartimento di Nefrologia, Dialisi e Medicina Interna, ospedale Vittorio Emanuele, 95010 Catania, Italy. 120
59 E-mail address: antonio.granata4@tin.it (A. Granata). 121
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61 1971-3495/$ - see front matter 2009 Published by Elsevier Srl. 123
62 doi:10.1016/j.jus.2009.09.006 124

Please cite this article in press as: Granata A et al., Doppler ultrasound and renal artery stenosis: An overview, Journal of Ultrasound
(2009), doi:10.1016/j.jus.2009.09.006
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125 funzione renale. Lo screening per SAR e indicato nel sospetto di ipertensione nefrovascolare o 187
126 di nefropatia ischemica al fine di identificare i pazienti in cui e indicato un intervento di 188
127 rivascolarizzazione. I tests di screening per SAR sono migliorati considerevolmente durante 189
128 lultimo decennio. Mentre la scintigrafia con test al captopril e stata utilizzata quasi esclusiva- 190
129 mente nel passato, lecocolorDoppler delle arterie renali, langioTC e/o langioRM hanno sos- 191
130 tituito le altre modalita di screening in molti centri. Per tale motivo larteriografia riveste 192
131 sempre piu un ruolo interventistico e solo di rado diagnostico. LecocolorDoppler e una proce- 193
132 dura diagnostica non invasiva, ripetibile e relativamente economica che negli ultimi anni, in 194
133 mani esperte, si e accreditata sempre piu come ottimo strumento di screening di malattia 195
134 nefrovascolare. Inoltre, la determinazione dellindice di resistenza sembra essere utile nei 196
135 pazienti con SAR per la capacita di predire la risposta alla rivascolarizzazione. Tuttavia, quan- 197
136 do esiste una discrepanza fra i dati clinici ed i risultati dellecocolorDoppler e indicato il ricor- 198

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137 so ad altre procedure diagnostiche. 199
138 2009 Published by Elsevier Srl. 200
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142 Introduction vessels, localize the site of stenosis or disease, provide 204
143 evidence for the hemodynamic significance of the lesion 205
144 Renal artery stenosis (RAS) is most commonly caused by and identify associated pathologies (e.g., abdominal aortic 206
145 either fibromuscular dysplasia or atherosclerosis, and it aneurysm, renal mass, etc.) that may have an impact on 207
146 may occur alone (isolated anatomical RAS) or associated the treatment of RAS. Angiography, once considered the 208
gold standard for arterial imaging, is invasive, expensive

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147 with hypertension, renal insufficiency (ischemic nephrop- 209
148 athy) or both. and carries a small but not negligible risk of severe 210
149 RAS due to atherosclerotic changes of the RAs has complications such as adverse contrast media reactions, 211
150 become a serious concern as a cause of hypertension and cholesterol embolization or arterial dissection. Owing to its 212
151 renal ischemia, resulting frequently in end-stage renal invasive character and the substantial costs involved, 213
152 failure [1]. Several epidemiologic studies [1,2] have shown angiography is not used as a screening method but as 214
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153 the elevated prevalence of ischemic nephropathy in elderly a guide for therapeutic transluminal angioplasty. Further- 215
154 patients mainly due to atherosclerotic RAS. Over the past more, angiography provides no information on the func- 216
155 decade, data have accumulated implicating atherosclerotic tional significance of the stenosis. Thus, in recent years 217
156 RAS as an increasingly significant cause of end-stage renal many less invasive or noninvasive diagnostic methods, such 218
157 disease (ESRD) ranging anywhere from 5% to 22% of incident as captopril renal scintigraphy, color-Doppler ultrasonog- 219
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158 ESRD patients [3,4]. RAS is the most common potentially raphy (CDUS), computed tomography angiography (CTA) 220
159 reversible and curable cause of secondary hypertension and and magnetic resonance angiography (MRA) have been 221
160 renal failure. Thus, early diagnosis of RAS is an important tested and compared to arteriography. Among these 222
161 clinical objective since interventional treatment may different methods, CDUS has been selected by many insti- 223
tutions as the principal screening tool used to detect RAS.
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162 improve or cure hypertension and preserve renal function 224


163 [5]. Prevalence of RAS is estimated to range from 1% to 5% 225
164 of all hypertensives in the general population up to 30% of Examination technique and normal findings 226
165 a highly selected referral population (i.e. malignant 227
166 hypertension, young patients with hypertension, the pres- RAS scanning is very difficult, and it requires a great 228
167 ence of an abdominal bruit, decreased serum potassium, amount of skill due to the depth of the arteries, the 229
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168 unexplained azotemia, recurrent congestive heart failure motion imposed by respiration, and intraabdominal gas. 230
169 or flash pulmonary edema) [6,7]. Clinical screening of The patients should therefore be examined early in the 231
170 hypertensive patients is therefore recommended before morning if at all possible after a 12-h overnight fast. This 232
171 extensive investigation for renovascular disease is started. will diminish the amount of bowel gas and also ensure that 233
172 The pathologic causes of RAS include atherosclerosis, the stomach is empty. 234
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173 fibromuscular dysplasia (FMD), arteritis, dissection and 235


174 neurofibromatosis. From a practical point of view, there are Examination technique and normal anatomy 236
175 only two major diseases that affect the RAs: (a) athero- 237
176 sclerotic disease, the most common pathologic condition, The procedure begins with the patient in the supine posi- 238
177 which mainly affects the orifice and proximal portion of the tion and the head of the bed elevated about 30 degrees. 239
178 RA; (b) FMD, much less common, which involves mid to A low-frequency scanhead (2.5e5.0 MHz) is used to depict 240
179 distal portion of the RAs. Intimal and periarterial FMD is the abdominal aorta and renal arteries (RAs). The two main 241
180 commonly associated with progressive dissection and approaches for imaging the RAs are through the anterior 242
181 thrombosis, whereas medial FMD progresses only in 30% of abdominal wall and the flank. Which approach is used 243
182 patients and is rarely associated with dissection and depends on the specific portion of the renal vasculature 244
183 thrombosis. Atherosclerotic RAS is a progressive disease, being investigated. In most cases the anterior approach is 245
184 particularly in patients with diabetes or other manifesta- used to evaluate the main RAs. The flank approach (Fig. 1) 246
185 tions of atherosclerosis [5]. The ideal imaging procedure for may be used to image both the intrarenal vasculature and 247
186 RAS should identify the main RAs as well as the accessory the main RAs. Each of these windows has limitations, which 248

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Fig. 1 Color-Doppler US image of the right kidney with the renal vessels. Good visualization of the entire renal vascular tree.
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are dependent on individual body habitus and several other
variables, such as the ability of the patients to hold their
DPapproach is better. From this view, RA flow is in a direction
that is parallel to the Doppler beam, optimizing signal
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275 breath. In selected cases the posterior approach can be reception. The patient usually needs to be placed in the 337
276 used [8,9]. opposite lateral decubitus position [8,10]. 338
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277 The RAs originate from the lateral sides of the aorta The left RA tends to originate from the posterolateral 339
278 (Fig. 2), typically at the level of the superior border of the surface of the aorta and courses posteriorly the surface of 340
279 second lumbar vertebra, directed slightly anteriorly, the aorta and over the psoas muscle. An aid to locating the 341
280 usually 1e2 cm below the superior mesenteric artery origin. left RA is to first identify the left renal vein, which is usually 342
281 343
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The right RA originates from the anterolateral aspect of the large and easy to find [9,10]. Once the vein is identified, the
282 aorta and immediately turns posteriorly to course beneath artery will often be apparent as a smaller vessel directly 344
283 the inferior vena cava (IVC). The proximal right RA is not behind it, coursing in the opposite direction. A pitfall that 345
284 only deep in the abdomen but it also lies perpendicular to should be avoided is mistaking the origin of the inferior 346
285 the Doppler beam in the usual transverse scan plane mesenteric artery (IMA) for that of the left RA. However, 347
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286 [8,9,10]. The right RA may also be difficult to separate from the IMA tends to have a high resistance spectral waveform, 348
287 the overlying IVC in this plane, and in this case flank which is quite different from the normal low-resistance 349
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310 Fig. 2 Axial section of the midepigastric region showing the origin of both RAs. 372

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373 pattern of the RA [8,10]. The IMA also originates much The right renal vein runs in a posteroanterior direction, 435
374 lower along the aorta than the left RA, unless the latter with a short course to reach the IVC. The left vein is more 436
375 arises from an atypical location. A second approach to horizontal and passes between the abdominal aorta and the 437
376 imaging the left RA is a variation of the flank approach superior mesenteric artery before entering the IVC [8,9]. 438
377 described for the right RA above. In this case, the patient is 439
378 placed in the right lateral decubitus position, and with Normal findings 440
379 scanning through the kidney, the main RA is followed back 441
380 towards the aorta. The decubitus position is essential, When the origins of the RAs are depicted with color Doppler 442
381 because the kidney often falls towards the midline and acts in the transverse position, the flow of the first segment of 443
382 as its own window [8,9]. Another method of identifying the the right RA is directed towards the transducer depicted in 444
383 main RAs, particularly the areas of the ostia (where most red color. Color change is seen shortly after the origin, 445
384 stenoses occur in elderly patients), has been termed the where the direction of the flow is directed posteriorly. Most 446

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385 banana peel view (Fig. 3). of the course of the vessels is then displayed in blue. If the 447
386 Also in this situation, the patient is turned to the origin of the RAs is imaged in the oblique longitudinal 448
387 opposite decubitus position from the vessel being exam- section, the right RA passes directly towards the transducer 449
388 ined. For the banana peel view, the transducer is from the aorta and is red, whereas the left RA is directed 450
389 oriented longitudinally [8]. The aorta is located, and the away from the transducer and is blue. The normal 451

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390 transducer is moved in an anterior-to-posterior direction waveform of the main renal artery demonstrates a low- 452
391 until the RA is identified arising from it, coursing towards resistance pattern similar to that found in all the paren- 453
392 the transducer. Looking at the RAs and the aorta as chymal organs of the body (Fig. 5). Although the main RAs 454
393 a whole, some have likened this appearance to a half- may be imaged from an anterior approach, the deep loca- 455
394 peeled banana with its skin curved alongside. On the right, tion in the abdomen often limits the resolution of the 456

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395 an additional aid in locating the RA is to image the IVC and transducer that may be applied. Lower frequency trans- 457
396 to look posterior to it until a vessel crossing perpendicularly ducers will have better sonographic penetration, but there 458
397 and of the opposite color is found [9]. This must be the right is a trade-off of decreased spatial resolution. The highest 459
398 RA, because no other large vessel lies posterior to the IVC. frequency transducer that allows good demonstration of 460
399 Approximately 20e30% of patients have one or more arterial waveforms is preferable. Doppler gain should be 461
400 accessory renal arteries (Fig. 4) [8e10]. The main RA optimized to detect flow by increasing the gain to a level 462
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401 divides at the hilum, either within or outside the kidney, just below color artifact visualization in adjacent struc- 463
402 into anterior and posterior branches that further divide into tures. The pulse repetition frequency, or velocity scale, is 464
403 segmental and then interlobar arteries. The interlobar the frequency of sampling; undersampling may underesti- 465
404 arteries further divide into a network of arcuate arteries mate peak velocities. For spectral Doppler, the Doppler 466
405 that run at the corticomedullary junction and give off the gate should be set to include the entire artery lumen and 467
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406 cortical (interlobular) branches, which run radially towards angled with the direction of flow. The angle of insonation 468
407 the periphery, and the medullary branches, which supply should be maintained at 60 degrees or less. Although the 469
408 the renal pyramids. The renal veins usually follow the exact angle should be reproduced for follow-up studies, 470
409 course of the arteries running in a more ventral position. this is not widely performed [8,11]. The frequency shift 471
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432 Fig. 3 Color image of the ostium (arrows) in both RAs arising from the aorta using the banana peel technique. The Doppler 494
433 beam angle is optimized and close to zero. The right RA is depicted in red, the left RA in blue. Abdominal aorta (AA), left RA (LRA), 495
434 right RA (RRA), inferior vena cava (IVC). 496

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Fig. 4 Color image of the ostium (arrows) in both RAs arising from the aorta using the banana peel technique. The Doppler
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beam angle is optimized and close to zero. The right RA is depicted in red, the left RA in blue. Abdominal aorta (AA), left RA (LRA),
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right RA (RRA), inferior vena cava (IVC), accessory right RA (aRRA).
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depends on the angle between the vessel and the ultra-
sound (US) beam, and on the frequency of the transducer
used. If the course of the main RAs is well recognized,
DPdiseases (i.e. nephroangiosclerosis, hypertension, tubular-
interstitial disease, diabetes mellitus, and severe brady-
cardia) can cause an increase of RI, even in the presence of
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523 angle-corrected velocity estimates can be made. The peak normal serum creatinine levels [12]. In clinical practice the 585
524 systolic velocity (PSV) in the main RA and its branches value of RI 0.7 is used to discriminate between normal and 586
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525 should be less then 120 cm/s [11]. The velocity slowly pathologic resistance to flow. Various authors [8,9,11] 587
526 decreases in the intrarenal arteries as they branch into the currently think that the best signals for evaluation come 588
527 kidney. The resistive index (RI) measures the degree of from the large segmental or interlobar arteries as they 589
528 intrarenal arterial impedance and is calculated using the course directly towards the transducer. In this location, 590
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following formula: ([PSV e end-diastolic velocity]/PSV). signals are the strongest and most reproducible. Weak
530 RI values measured in healthy subjects show a significant signals from peripheral (arcuate arteries) should be avoided 592
531 dependence on age and the area sampled. The values in the [12,13]. Modern sonographic equipment has practically 593
532 main RA are higher in the hilar region (0.65  0.17) than in overcome problems due to obesity and bowel gas, so it is 594
533 the more distal small arteries, and they are lowest in the possible to study about 90% of the patients who are 595
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534 interlobar arteries (0.54  0.20) [8,10,11]. Intrinsic renal referred for investigation [14]. In one study, direct 596
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557 Fig. 5 Spectral Doppler US image of the right RA in a normal subject. Note the small spike occurring at the end of the systolic 619
558 rise. This feature is seen only in a normal main RA. 620

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621 visualization of both main RAs was possible in 84% of analysis, PSV was the best predictor of RAS, with a sensi- 683
622 patients, right renal artery in 91% and left renal artery in tivity and specificity of 85% and 92%, respectively [20]. 684
623 85%. In 5% non-visualization was due to total occlusion of The second criterion is the comparison of PSV values 685
624 the renal artery, as suspected by absent intrarenal color- obtained in the prerenal abdominal aorta with those 686
625 Doppler signals and as confirmed by angiography [15]. measured in the RAs, the so-called renal/aortic ratio (RAR) 687
626 [21]. The use of the RAR instead of the absolute PSV value is 688
627 preferable since hypertension itself can cause increased 689
Doppler criteria for diagnosis of RAS
628 PSV velocities in all the vessels in hypertensive patients [8]. 690
629 In normal conditions, RAR is lower than 3.5. If PSV obtained 691
Doppler US criteria of RAS can be divided into two groups in the prerenal abdominal aorta is abnormally low (less than
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based on direct findings obtained at the level of the 40 cm/s), RAR cannot be used. In one study, a RAR of 3.5 or
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stenosis (proximal criteria), or on flow changes observed in greater identified hemodynamically significant lesions with
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the renal vasculature distal to the site of stenosis (distal

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633 a sensitivity and specificity of 91e92% and 75e95%, 695
criteria). respectively [21,22]. In another study by Chain et al. [23],
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635 a diagnosis of severe RAS based on RAR >3 yielded a sensi- 697
636 Proximal criteria (direct evaluation of the stenosis) tivity of 77%, specificity of 90%, PPV of 90% and NPV of 76%. 698
637 In a recent study, RAR > 3.5 yielded a sensitivity and 699

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638 Proximal criteria are direct signs obtained at the site of the specificity of 91% and 91%, respectively [24]. Technical 700
639 stenosis. Four criteria are used to diagnose significant failure is reported to be due to severe obesity, the use of 701
640 proximal stenosis or occlusion of the RA. The first and most older US devices, excessive bowel gas or poor flow in the 702
641 important sign is the increase in PSV. Velocities higher than main RA due to severe renal impairment. For the identifi- 703
642 180 cm/s suggest the presence of a stenosis of more cation of RAS  50%, Soares et al. [25] reported that renal- 704

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643 than 60% (Fig. 6), while an end-diastolic velocity greater segmental ratio (RSR), i.e. a ratio of PSV measured in the 705
644 than 150 cm/s suggests a degree of stenosis greater than renal artery to that obtained in the segmental artery, was 706
645 80%. Using a cut-off value of 180 cm/s and RA diameter the best parameter (sensitivity 93.33%; specificity 89.47%). 707
646 reduction of more than 50%, Radermacher et al. [15] Other authors [26] found that renal-interlobar ratio (RIR), 708
647 evaluated 226 patients using CDUS and arteriography i.e. a ratio of PSV measured in the renal artery to that 709
648 reaching a sensitivity of 96.7% and a specificity of 98%. In obtained in the interlobar artery, was more accurate 710
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649 another study, Hua et al. [16] used a cut-off value of (sensitivity 88%; specificity 88%). Chain et al. [23] proposed 711
650 200 cm/s and RA diameter reduction of more than 60% in a new direct-method Doppler parameter, the renal renal 712
651 a series of 107 patients reaching a sensitivity of 91% and ratio (RRR), which was defined as the rate between renal 713
652 a specificity of 75%. A PSV greater than 200 cm/s has been artery peak systolic velocity (RPSV) at the proximal or mid 714
653 suggested as the threshold for Doppler diagnosis of 60% segment of the RA and RPSV measured at the distal segment 715
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654 reduction of the RA diameter [17,18]. This criterion yielded of the renal artery (RRR Z RPSV (proximal or mid RA)/RPSV 716
655 a positive predictive value (PPV) of 60%, a negative (distal RA). It is based on the fact that increased blood flow 717
656 predictive value (NPV) of 95%, and an overall accuracy of velocity through the stenosis and the immediate post- 718
657 79%. In a recent study [19], PSV >200 cm/s resulted in stenotic segments and the observed decrease in blood flow 719
a sensitivity of 97%, specificity of 72%, PPV of 81% and NPV velocity distal to the stenosis is proportional to the degree
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659 of 95% in terms of diagnostic accuracy for RAS. In a meta- of stenosis. The intra-examiner variability was good 721
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681 Fig. 6 Spectral Doppler waveform of the stenotic area in the right RA. Increased peak systolic velocities are seen (PSV 286 cm/s); 743
682 Mosaic flow is seen within the stenotic area. 744

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745 (correlation 0.86, coefficient of variation 8.9%). The best 807


Table 1 Criteria for the classification of RA stenosis by
746 estimated cut-off value for the new RRR was 2.7. The RRR 808
color-Doppler US from Zieler and Strandness (Am J Hyper-
747 values, when compared to the other direct-method 809
tens, 1996).
748 parameters (PSV > 200 cm/s and RAR > 3) showed a sensi- 810
749 tivity and specificity of 97% and 96%, respectively. The main Renal artery Renal artery PSV RAR 811
750 limitation of this study was that Chain et al. [23] evaluated diameter reduction 812
751 only the main RAs because these vessels have a more Normala <180 cm/s <3.5 813
752 important role in renovascular diseases and could be <60% >180 cm/s <3.5 814
753 submitted to endovascular treatment, while results 60% >180 cm/s 3.5 815
754 obtained by other authors [10] using the parameters PSV Occlusion No signal Indeterminable 816
755 and RAR included accessory RAs detected at arteriography. a 817
PSV Z 100  20 cm/s.
756 Recently, Li et al. [27] found that receiver operating 818

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757 characteristic (ROC) curve analysis for RAS  50% showed 819
758 that the areas under the curve (AUCs) for RPSV, RAR, RRR, 820
759 RSR, and RIR were 0.92, 0.87, 0.90, 0.93, and 0.94, A stenosis is important when it is more than 60%. In this 821
760 respectively, and the optimal threshold values of the five case, the stenosis produces a significant decrease in renal 822
761 parameters were 170 cm/s, 2.3, 2.0, 4.0, and 5.5, respec- blood flow. 823

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762 tively. The authors [27] state that in RAS diagnosis it was 824
763 possible and necessary to measure 3 representative Distal criteria (indirect evaluation of the stenosis) 825
764 hemodynamic parameters (RAR, RPSV and RIR or RSR) in the 826
765 diagnosis of 50% RAS. PSVs in the abdominal aorta and RA The difficulties related to the direct evaluation of the 827
766 can be affected by factors other than RAS, which may stenosis (the mean examination time was 69 min for the 828
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decrease the accuracy of RAR. However, post-PSV ratios are
little affected by PSV in the abdominal aorta or by an equal
proportional change in PSVs in the RA trunk and its intra-
renal RAs; therefore, the use of post-PSV ratios overcomes
some limitations of RAR. In the detection of RAS, it is
DPcomplete examination and 14 min for the distal evaluation)
have led several investigators [28] to search for and to
identify waveform alterations, other than increased
velocity, distal to the stenosis in arterial segments more
accessible with Doppler US (i.e. hilar or interlobar arteries).
829
830
831
832
771 833
772 helpful to notice the degree and location of stenosis, Many distal quantitative criteria have been proposed in the 834
TE
773 arterial tortuosity and factors that influence PSVs in the literature [27,29] (loss of early systolic peak; acceleration 835
774 abdominal aorta and RA. Accessory RAs are quite common, index (AI) lower than 3 m/s2; acceleration time 836
775 seen in approximately 25e30% of cases [23]. Two or more (AT) < 0.07 s; a difference between the kidneys in RI > 5% 837
776 RAs are common, although typically one is dominant. It may or in pulsatility index >0.12). Correlative studies using 838
777 be difficult or impossible to see accessory RAs, leading angiography are confusing because of the variability in 839
EC

778 some to conclude that US evaluation for RAS is not suffi- criteria and in the corresponding degree of stenosis. 840
779 ciently sensitive. However, the occurrence of hemody- Interobserver and intraobserver variability using these 841
780 namically significant stenosis isolated to an accessory RA criteria is high [29,30]. The rationale is that the flow at the 842
781 was 1e1.5% in a retrospective review of renal angiograms renal hilum downstream to a hemodynamically significant 843
obtained in patients who underwent workup for renovas-
RR

782 stenosis should become damped and show a slow rise to the 844
783 cular hypertension [21], thus decreasing the significance of peak systole [26]. This phenomenon has been called the 845
784 non-visualized accessory RAs [22]. tarduseparvus effect. Tardus means slow and late and 846
785 However, when is investigation of accessory RAs parvus means small and little. Tardus refers to the fact that 847
786 required? In angiographic investigations, the caliber of the systolic acceleration of the waveform is slow with conse- 848
787 single renal artery originating from the abdominal aorta quent increase in time to reach the systolic peak. Parvus 849
CO

788 was found to measure between 5 and 10 mm in adults, with refers to the fact that the systolic peak is of low height, 850
789 values for women in the lower part of the range [23]. Aytac indicating a slow velocity (Fig. 7). However, although the 851
790 et al. [24] showed that if the diameter of a RA measured by presence of this finding is helpful in forming the diagnosis, 852
791 US is 4.65 mm or less, the presence of an accessory renal its absence does not exclude RAS. In patients with athero- 853
792 artery can be established with 80% sensitivity and 80.5% sclerosis, vessel compliance may be reduced, making the 854
UN

793 specificity. If the diameter of the renal artery is 4.15 mm or parvusetardus waveform morphology less obvious [31,32]. 855
794 smaller, the presence of an accessory renal artery is Several articles have shown excellent results with this 856
795 extremely probable, with 98.8% specificity. It was also indirect technique [9,10,11,14,17] and a slow systolic 857
796 interesting that in kidneys with a main RA diameter of upstroke or AI (the upstroke of the systolic peak adjusted to 858
797 5.5 mm, no accessory RAs were encountered. the transmitted frequency), an increase in AT (the interval 859
798 The third criterion is identification of RAs with no measured in seconds between the onset of the wave and 860
799 detectable Doppler signal, a finding than indicates occlu- the initial systolic peak) and loss of the early systolic peak 861
800 sion. The fourth criterion is the visualization of color arti- (ESP) appear to be the most useful parameters [27]. 862
801 facts such as aliasing at the site of the stenosis and the Hausberg et al. and Rabbia et al. [32,33] confirm the 863
802 presence of turbulence at Doppler evaluation indicating the usefulness of AI and AT but report that a simple pattern 864
803 presence of a significant stenosis upstream. Usually, these recognition of the Doppler waveform from the segmental 865
804 two patterns are the first and immediate signs of a stenosis arteries (persistence of the ESP) may be more valuable than 866
805 [25]. These criteria permit classification of RA narrowing calculating AI and AT with 95% sensitivity, 97% specificity, 867
806 into the four categories listed in Table 1. and 96% accuracy for stenosis greater than 60%. On the 868

Please cite this article in press as: Granata A et al., Doppler ultrasound and renal artery stenosis: An overview, Journal of Ultrasound
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+ MODEL
8 A. Granata et al.

869 931
870 932
871 933
872 934
873 935
874 936
875 937
876 938
877 939
878 940
879 941
880 942

OF
881 943
882 944
883 945
884 946
885 947

RO
886 948
887 949
888 950
889 951
890 952

DP
891 953
892 954
893 Fig. 7 Tarduseparvus waveform in a patient with RA stenosis. Note the delayed and dampened upstroke yielding a rounded 955
894 appearance to the waveform. 956
895 957
896 other hand, in a comprehensive review, the authors [19,34] post-stenotic flow in the RA beyond the region of stenosis 958
TE
897 found for AT and AI a sensitivity of 80% and 74% and will often have low-resistance waveforms [37e39]. 959
898 a specificity of 88% and 85%, respectively. Many factors However, this criterion is not commonly used in our practice. 960
899 influence systolic acceleration and may make the test non- Unlike obstructive uropathy [40,41], the abnormal kidney 961
900 specific. Extrarenal factors such as aortic and mitral will show reduced RIs beyond the point of stenosis [42]. 962
901 valvular diseases, left ventricular dysfunction or even Another advantage of US over other modalities is its 963
EC

902 cardiovascular medication might affect systolic accelera- ability to predict which patients will benefit from thera- 964
903 tion. Numerous factors, such as age, hypertension and peutic correction of RAS. Radermacher et al. [43] showed in 965
904 diabetes affect vessel compliance. Such variables may a large prospective study that symptoms and urinary values 966
905 explain why some authors have not been able to reproduce do not improve after stenting in patients with elevated 967
these results [30,35]. Therefore, these criteria are used RI > 0.80. The authors [43] therefore suggested that repair
RR

906 968
907 only when obvious on spectral traces, when quantifying the of the stenosis is not warranted in these patients. However, 969
908 stenosis as severe (> 75%), or when identifying a down- a subsequent study showed that 29% of patients with renal 970
909 stream pattern of a stenosis on a segmental or an accessory insufficiency and RI > 0.80 showed improved renal function 971
910 artery that has been missed [28,36]. Most accrediting after revascularization, and 50% had improvement of 972
911 organizations recommend the use of a combination of intra- hypertension [28]. 973
CO

912 and extrarenal parameters, as it results in an overall 974


913 sensitivity of 89% and specificity of 92% [11,37]. 975
914 Bardelli et al. [38] recently introduced new intrarenal Evaluation in assessing restenosis of renal 976
915 echo-Doppler velocimetric indices for the diagnosis of RAS. artery stents 977
916 The maximal acceleration index (AImax s 1, defined as the 978
UN

917 maximal slope of the systolic acceleration corrected for the Several studies [44,45] have shown good technical success 979
918 relative district flow regimen, as stated by the PSV). rates immediately after the procedure, but restenosis rates 980
919 The sensitivity and specificity of AImax at the best cut-off approximately from 2% to 36% at 6e12 months follow-up. 981
920 value of 9.0 s 1 was found to be 88% and 89%, respectively, Assessment of restenosis of RA stents is important in the 982
921 for stenoses 50%, 93% and 84% for stenoses 60% and 92%, clinical management of individual patients to determine 983
922 and 82% for stenoses 70%. However, the study design did the long-term benefits of the procedure. MRA and spiral 984
923 not provide comparative analyses of the new intrarenal CTA are less suitable for assessing restenosis because of 985
924 indices and of the proximal ones. Thus, it cannot be artifacts caused by the stent material. CDUS follow-up to 986
925 established from the present data which of the two assess for restenosis may be warranted in patients after 987
926 approaches is better. Furthermore, the accuracy of this stent placement for RAS, even in the absence of clinical 988
927 new index for the diagnosis of RAS has not been evaluated signs of restenosis (Fig. 8a,b). Girndt et al. [44] reported 989
928 in other studies. a sensitivity and specificity of 100% and 74%, respectively, 990
929 A great difference in RI values obtained on the 2 kidneys using the published threshold value of in-stent PSV 991
930 (>0.05e0.07) is another criterion for diagnosis of RAS as the >180 cm/s. If the published threshold value of RAR >3.5 992

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Doppler ultrasound and renal artery stenosis 9

993 1055
994 1056
995 1057
996 1058
997 1059
998 1060
999 1061
1000 1062
1001 1063
1002 1064
1003 1065
1004 1066

OF
1005 1067
1006 Fig. 8 (a) Gray-scale US examination showed a stent in the left RA (arrow); (b) Color US examination showed restenosis in the left 1068
1007 RA (arrow). 1069
1008 1070
1009 was used, sensitivity and specificity were 50% and 89%, where Doppler trace is difficult to obtain in basal conditions 1071

RO
1010 respectively. In another study, Bakker et al. [46] used an because of the overlying tissues, calcifications or weakness 1072
1011 optimal threshold value of 226 cm/s rather than 180 cm/for of the signal. 1073
1012 in-stent PSV and an optimal threshold value for the RAR of Missouris et al. [47] showed that renal duplex scanning 1074
1013 2.7 rather than 3.5, and reported a sensitivity of 100% for using contrast enhancement produces more reproducible 1075
1014 both parameters and a specificity of 90% for in-stent PSV spectral waveforms, improves accuracy and reduces the 1076
1015
1016
1017
1018
and 84% for RAR.
Finally, the number of technically inadequate US
examinations may be reduced by searching for alterations
in Doppler waveforms in areas of renal vasculature distal to
DPtime needed for the examination. They demonstrated
a sensitivity of 85% and a specificity of 79% without contrast
enhancement, and a sensitivity of 94% and a specificity of
88% with contrast enhancement, besides an important
1077
1078
1079
1080
1019 a stenosis, instead of directly insonating the RA. However, reduction in the duration of the procedure. In another 1081
1020 the results of these indirect methods are controversial and study, Claudon et al. [48] showed that the number of 1082
TE
1021 several investigators question their usefulness [44,46]. examinations with successful results was increased by CEUS 1083
1022 examination compared to non-enhanced Doppler US, also in 1084
1023 patients affected by obesity or renal dysfunction. However, 1085
1024 Contrast-enhanced ultrasound and renal artery the sensitivity and specificity of Doppler US examination did 1086
1025 stenosis 1087
EC

not substantially increase. Teixeira et al. [49] showed that


1026 CEUS does not improve the accuracy despite a reduced 1088
1027 Contrast-enhanced ultrasound (CEUS) has recently added duration of the procedure and an increase in specificity 1089
1028 new possibilities to CDUS in the detection or RAS as it based on one Doppler criterion. CEUS imaging of the RAs is 1090
1029 improves visualization of the main RAs and accessory safe but not routinely required when Doppler US is per- 1091
RR

1030 vessels and reduces the number of equivocal examinations formed by an experienced sonographer. However, CEUS 1092
1031 (Fig. 9). US contrast agent increases the intensity of the may increase visualization and accuracy in patients 1093
1032 Doppler signals, thus producing a more rapid and complete affected by stenosis and in patients whose vessels are not 1094
1033 visualization of the RAs. Main indications include cases initially visualized. Although increased velocities are seen 1095
1034 1096
1035 1097
CO

1036 1098
1037 1099
1038 1100
1039 1101
1040 1102
UN

1041 1103
1042 1104
1043 1105
1044 1106
1045 1107
1046 1108
1047 1109
1048 1110
1049 1111
1050 1112
1051 1113
1052 1114
1053 1115
1054 Fig. 9 Contrast-enhanced US examination showed proximal stenosis in the left renal artery (arrow). 1116

Please cite this article in press as: Granata A et al., Doppler ultrasound and renal artery stenosis: An overview, Journal of Ultrasound
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10 A. Granata et al.

1117 when contrast agent is used, this does not appear to [15] Radermacher J, Chavan A, Schaffer J, et al. Detection of 1179
1118 necessitate different Doppler criteria [50]. significant renal artery stenosis with color Doppler sonog- 1180
1119 The feasibility of US examination depends on the quality raphy: combining extrarenal and intrarenal approaches to 1181
of the equipment, and the injection of contrast agent does minimize technical failure. Clin Nephrol 2000;53(5):333e43.
1120 1182
[16] Hua HT, Hood DB, Jensen CC, Hanks SE, Weaver FA. The use of
1121 not add advantages if the performance of the US equipment 1183
colorflow duplex scanning to detect significant renal artery
1122 is excellent. Contrast agents (microbubbles) do not undergo stenosis. Ann Vasc Surg 2000;14:118e24. 1184
1123 renal filtration or tubular excretion and, on the whole, they [17] Olin JW, Piedmonte MR, Young JR, DeAnna S, Grubb M, 1185
1124 can be considered as purely vascular tracers. Childs MB. The utility of duplex ultrasound scanning of the 1186
1125 Following recent improvements in CEUS techniques, renal arteries for diagnosing significant renal artery stenosis. 1187
1126 a quantitative time-intensity analysis of the wash-in wash- Ann Intern Med 1995;122:833e8. 1188
1127 out enhancement curve of tissues is currently feasible [51]. [18] Bokhari SW, Faxon DP. Current advances in the diagnosis and 1189
1128 Time-intensity enhancement curves show the variation of treatment of renal artery stenosis. Rev Cardiovasc Med 2004; 1190

OF
1129 the average pixel power over time within a box that is sized 5:204e15. 1191
and shaped to match the target organ and enables direct [19] Williams GJ, Macaskill P, Chan SF, et al. Comparative accuracy
1130 1192
of renal duplex sonographic parameters in the diagnosis of
1131 and immediate quantitative evaluation of curve-related 1193
renal artery stenosis: paired and unpaired analysis. Am J
1132 parameters such as time to peak, maximum peak concen- Roentgenol 2007;188:798e811. 1194
1133 tration and the area under the curve [8,31,52]. CEUS is [20] Hoffmann U, Edwards JM, Carter S, Goldman ML, Harley JD, 1195

RO
1134 a new promising method of screening, and a renewal of Zaccardi MJ, et al. Role of duplex scanning for the detection 1196
1135 interest in Doppler techniques is therefore to be expected. of atherosclerotic renal artery disease. Kidney Int 1991;39(6): 1197
1136 At present, however, only preliminary results have been 1232e9. 1198
1137 presented in the literature, and further studies are needed [21] Bude RO, Forauer AR, Caoili EM, Nghiem HV. Is it necessary to 1199
1138 before the introduction of this technique in clinical study accessory arteries when screening the renal arteries for 1200
renovascular hypertension? Radiology 2003;226:411e6.

DP
1139 practice. 1201
[22] Labropoulos N, Ayuste B, Leon Jr LR. Renovascular disease
1140 1202
among patients referred for renal duplex ultrasonography.
1141 References J Vasc Surg 2007;46:731e7.
1203
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TE
1145 [2] Coen G, Calabria S, Lai S, et al. Atherosclerotic ischemic renal 25(4):4. 1207
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RR

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UN

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Doppler ultrasound and renal artery stenosis 11

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