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16 Detection of Renal Perfusion Defects

Emilio Quaia and Salvatore Siracusano

E. Quaia, MD

Assistant Professor of Radiology, Department of Radiology, Cattinara Hospital, University of Trieste, Strada di Fiume 447, 34149 Trieste, Italy

S. Siracusano, MD

Department of Urology, Cattinara Hospital, University of Tri- este, Strada di Fiume 447, 34149 Trieste, Italy

partial renal infarction of 20%. Contrast-enhanced color and power Doppler US are limited by bloom- ing and flash artifacts, which may be attenuated by reducing the instrument gain settings and also diminishing the detection of focal abnormalities in renal blood flow (Taylor et al. 1996).

Contrast-material-enhanced CT represents a ref- erence standard imaging technique to detect renal perfusion defects, which appear as focal wedge- shaped hypovascular lesions in normally perfused renal parenchyma.

Recent advances in microbubble-based contrast agents, and dedicated contrast-specific modes, have determined the achievement of increased image con- trast in tissues. By transmitting at the fundamental frequency and receiving selectively harmonic frequen- cies, the background signal from stationary tissues is markedly suppressed resulting in a greater signal-to- noise ratio (Mattrey et al. 1998) and a better visibil- ity of renal infarcts (Coley et al. 1991; Munzing et al.

1990; Girard et al. 2000). Blooming and flash artifacts are eliminated, shadowing artifacts are lessened, both spatial and temporal resolution are improved, and the brightness of gray-scale pixel does not depend on angle-dependent frequency shift estimates (Taylor et al. 1999). In contrast to iodinated contrast agent employed in CT, microbubbles are pure intravascular agents which are not excreted in renal tubules. Renal cortex rapidly enhances from 20 to 25 s after micro- bubble injection (Fig. 16.1a), while the vessels of renal medulla, which are less vascularized, are progressively filled from 30 to 35 s (Fig. 16.1b) and completely filled from 45 to 55 s (Fig. 16.1c) after microbubble injection.

16.2

Results in Animal Experimental Models

Animal models were firstly employed to assess the capabilities of contrast-enhanced US in detection of renal perfusion abnormalities (Taylor et al. 1998;

Claudon et al. 1999; Quaia et al. 2004). We pro-

CONTENTS

16.1 Introduction 245

16.2 Results in Animal Experimental Models 245 16.3 Results in Humans 246

16.3.1 Renal Perfusion Defects: Infarcts 246 16.3.2 Acute Renal Cortical Necrosis 249

16.3.3 Focal Acute Pyelonephritis and Renal Abscess 249 References 252

16.1

Introduction

Renal perfusion defects, often resulting in renal infarction, occur in a variety of clinical settings, such as thromboembolism, atherosclerosis, aneu- rysm of the aorta or renal artery, renal artery ste- nosis or occlusion, acute venous occlusion, subacute bacterial endocarditis (septic emboli), and vasculitis (Kawashima et al. 2000). Focal pyelonephritis man- ifests also as a perfusion defect. The most common cause is thromboembolism from cardiovascular dis- ease which may determine also multifocal infarcts (Wong et al. 1984), while the most common clinical manifestation is sudden onset of flank or back pain with or without hematuria, proteinuria, fever, and leukocytosis.

Color and power Doppler US is a first-line imag-

ing procedure to detect renal perfusion defect but

presents clear limitations due to the relative insensi-

tivity to low-velocity and low-amplitude flow states

(Taylor et al. 1996). Coley et al. (1991) found a

global accuracy of color Doppler US for detection of

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Fig. 16.1a–c. Animal model: New Zealand White rabbits. Con- trast-enhanced US after microbubble-based agent injection (contrast-specifi c mode: contrast-tuned imaging; Esaote, Genoa, Italy). Cortico-medullary phase after microbubble- based agent injection. Normal renal perfusion at the early (a) arterial phase (15–20 s from injection) when only the cortical portion of the kidney is enhancing while the renal medulla is not yet fi lled by microbubbles. Normal renal perfusion at the late (b) arterial phase (25–40 s from injection) when both cortical and medullary portion of the kidney are enhancing.

Normal renal perfusion at the late (c) phase (50–100 s from injection) when renal enhancement is homogeneous c

posed an animal model) in which bilateral diffuse renal parenchymal embolization was performed in five adult New Zealand White rabbits (Quaia et al.

2004). From 2 to 3 ml of polyvinyl alcohol particles (150–250 µm in diameter) were directly injected in the aorta 2 cm above the level of renal arteries. After embolization, both kidneys were surgically exposed at midline laparotomy. Each kidney was scanned at low acoustic power using a linear transducer before and after microbubble injection, 15 min after embo- lization, by placing the transducer on the surface of each kidney by interposing a gel pad to avoid rever- beration artifacts. Digital subtraction angiography and macroscopic/histologic analysis of each kidney were considered as the reference standards.

After microbubble injection, renal perfusion defects appeared as single or multiple focal wedge- shaped areas of absent or diminished contrast enhancement in comparison with the adjacent renal parenchyma (Figs. 16.2, 16.3). Contrast-enhanced US revealed from 4 of 6 (66%) to 8 of 10 (80%) of renal perfusion defects confirmed by reference stan- dards. The smallest renal perfusion defects identi- fied by contrast-enhanced US revealed a diameter of 6 mm, while reference standards allowed detection of renal perfusion defects up to 3 mm in diameter. A significant increase in diagnostic confidence about presence or absence of renal perfusion defects was obtained by contrast-enhanced US in comparison

with baseline US, even though it is limited in detec- tion of renal perfusion defects smaller than 6 mm by volume average artifacts determined by the thick- ness of the US beam (about 5 mm).

16.3

Results in Humans

16.3.1

Renal Perfusion Defects: Infarcts

A) Baseline US and color Doppler US. Even though

large renal perfusion defects or infarcts may be

hypoechoic in comparison with the viable renal

parenchyma, segmental renal infarcts are usually

isoechoic or rarely hyperechoic if hemorrhagic

component is present. Renal infarcts often reveal a

wedge shape with capsular base. Even though base-

line color Doppler US and power Doppler US present

overt limitations to detect renal perfusion defects

due to the low sensitivity to low-velocity and low-

amplitude flow states, they may increase diagnostic

capabilities of US in detecting renal infarcts, espe-

cially in elderly or obese patients and in patients

with renal diseases. In renal infarct, color Doppler

US and power Doppler US reveal absolute absence

of renal cortical flows, even though it is very dif-

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Fig. 16.2a,b Animal model: New Zealand White rabbits. Contrast-enhanced US after microbubble-based agent injection (con- trast-specifi c mode: contrast-tuned imaging; Esaote, Genoa, Italy). Single focal renal perfusion defect (arrows) determined by random bilateral renal embolization by polyvinyl alcohol particles.

a

b

Fig. 16.3a–c. Animal model: New Zealand White rabbits. Con- trast-enhanced US after microbubble-based agent injection (contrast-specifi c mode: contrast-tuned imaging; Esaote, Genoa, Italy). Different types for dimension and location of focal renal perfusion defects (arrows) determined by random bilateral renal embolization by polyvinyl alcohol particles.

Contrast-enhanced US (a,b) allows a reliable depiction of renal perfusion defects which are confi rmed at the gross specimen analysis (c).

a b

c

ficult to differentiate renal segmental infarct from areas which appear poorly perfused due to underly- ing parenchymal disease, deep renal position, and artifacts. Moreover, color Doppler US presents a low accuracy in detection of small renal infarcts in the subcapsular region for limited spatial resolution and in the superior renal pole for the high Doppler angle and for the depth position (Correas et al. 2003).

B) Contrast-material-enhanced CT. Both CT and

angiography are reference imaging techniques in

renal infarct detection (Kawashima et al. 2000). The

parenchymal appearance of renal perfusion defects

depends on the size of the embolus, the location

of the arterial occlusion, and its age (Kawashima

et al. 2000). Contrast-material-enhanced CT shows

the absence of enhancement in the affected renal

tissue. Acute renal infarctions typically appear as

wedge-shaped areas of decreased attenuation, while

after the acute phase of renal infarction, atrophy

begins and the infarcted tissue contracts, leaving a

cortical scar.

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Fig. 16.4a–e. Human: focal renal perfusion defects. Contrast-enhanced US after microbubble-based agent injection (contrast- specifi c mode: pulse-inversion mode; Philips–ATL, Bothell, Wash.). Contrast-enhanced US (a,b) allows a reliable depiction of renal perfusion defect (arrows). The same renal perfusion defect (arrow) is confi rmed at contrast-material-enhanced CT (c–e) after iodinated agent injection.

a b

c d e

enhancement of renal parenchyma sparing the renal collecting system. Both kidneys are scanned by low acoustic power in the longitudinal and axial plane during early and late corticomedullary phase.

The renal poles are the most difficult regions to be assessed, since they are often hidden by interposing bowel gas. For this reason the position of the probe has to be dynamically modified during scanning

tion, since in this clinical situation the renal perfu-

sion defects are often too small to be detected by

contrast-enhanced US. If ≥5 mm, renal perfusions

defects can be identified after microbubble injec-

tion (Fig. 16.5). Microbubble-based agents should

be always employed to exclude renal infarcts in

every old patient presenting with a renal colic-like

pain in the flank region.

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Fig. 16.5a–d. Human: cholesterinic renal embolization. Cholesterinic embolization proved by cutaneous biopsy. Contrast- enhanced US after microbubble-based agent injection (contrast-specifi c mode: pulse-inversion mode; Philips–ATL, Bothell, Wash.). Baseline color Doppler US (a,b) does not allow identifi cation of renal perfusion defects. Contrast-enhanced US (c,d) allows a reliable depiction of renal perfusion defect (arrow).

a b

c d

16.3.2

Acute Renal Cortical Necrosis

Acute renal cortical necrosis is a rare form of acute failure and results from ischemic necrosis of the renal cortex with sparing of the renal medulla.

The process is either multifocal or diffuse; in most cases, it is bilateral. This condition is associated with complications of pregnancy, including abruptio pla- centae and septic abortion, sepsis, shock, or severe dehydration.

Contrast-material-enhanced CT scan shows enhancing interlobar and arcuate arteries adja- cent to the nonenhancing cortex, enhancement of the medulla but no enhancement of the cortex, and/or a rim of subcapsular cortical enhancement (Kawashima et al. 2000; Jeong et al. 2002).

Acute renal cortical necrosis may be effectively represented by contrast-enhanced US (Fig. 16.6).

The necrotic cortex appears as a hypoechoic zone circumscribing the kidneys at contrast-enhanced US (Correas et al. 2003). Microbubble-based agents have to be always employed to exclude diffuse renal cortical necrosis, if it is clinically suspected.

16.3.3

Focal Acute Pyelonephritis and Renal Abscess

The visibility of focal pyelonephritis may be

improved by color and power Doppler US in com-

parison with baseline gray-scale US (Quaia and

Bertolotto 2002). Focal infective areas in acute

pyelonephritis are prevalently less visible after

microbubble injection in comparison with baseline

gray-scale and color Doppler US (Fig. 16.7). This

is because microbubbles remain entirely intravas-

cular and renal vessels remain prevalently patent

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Fig. 16.6a–d. Human: renal acute cortical necrosis. An 80-year-old patient who was admitted to the emergency unit with acute renal failure. Baseline US (a) scan in the longitudinal plane did not demonstrate abnormalities as hydronephrosis. Absence of contrast enhancement in the superfi cial renal cortex identifi ed after microbubbles injection (b–d; arrows). Acute cortical necrosis was confi rmed at gross specimen and histologic analysis after patient death.

c b

d

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Fig. 16.7a–h. Human: acute focal pyelonephritis. A 32-year-old woman who was admitted to the emergency unit with fever and pain in the right fl ank. Two distinct areas of acute focal pyelonephritis in the right kidney are shown (arrows). The fi rst area is located in the mesorenal region (a–d), while the second area is located in the lower renal pole (e–h). Baseline US (a,e) scan in the longitudinal plane shows a wedge-shaped hypoechoic area in the renal parenchyma which appears as an hypovascular region at color Doppler US (b,f). From 20 to 35 s after microbubble injection (c,d,g,h), renal parenchyma reveals homogeneous contrast enhancement (arrows) without evidence of renal perfusion defects.

a b

c d

e f

g h

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in focal infective areas, while color Doppler US exclusively depicts large renal vessels which are prevalently displaced by inflammatory edema.

Focal acute pyelonephritis may improve in con- spicuity after microbubble injection if renal vessels are compressed by the adjacent edema revealing a triangular shape, similarly to the renal perfusion defects (Fig. 16.8). In fact, contrast-enhanced US was shown to improve the detection and conspi- cuity of renal parenchymal abnormalities in acute pyelonephritis in comparison with baseline US (Kim et al. 2001) and to improve the diagnosis of acute pyelonephritis (Duval et al. 2003).

Renal abscesses may be effectively represented after microbubble injection (Fig. 16.8), since they do not present intralesional vessels which are destroyed or displaced by the colliquative process (Correas et al. 2003).

References

Claudon M, Barnewolt C, Taylor GA et al (1999) Renal blood flow in pigs: changes depicted with contrast-enhanced harmonic US imaging during acute urinary obstruction.

Radiology 212:725–731

Coley BD, Mattrey RF, Roberts A, Keane S (1991) Potential role of PFOB enhanced sonography of the kidney. II. Detection of partial infarction. Kidney Int 39:740–745

Correas JM, Helenon O, Moreau JF (1999) Contrast enhanced ultrasonography of native and transplant kidney diseases.

Eur Radiol 9 (Suppl 3):394–400

Correas JM, Claudon M, Tranquart F, Hélenon O (2003) Con- trast-enhanced ultrasonography: renal applications. J Radiol 84:2041–2054

Duval A, Correas JM, Morelon E (2003) The diagnosis of acute pyelonephritis in renal transplants using contrast- enhanced US (abstract). RSNA 2003

Girard MS, Mattrey RF, Baker KG et al (2000) Comparison of standard and second harmonic B-mode sonography in the detection of renal infarction with ultrasound contrast in a rabbit model. J Ultrasound Med 19:185–192

Fig. 16.8a–d. Human: renal abscess. A 38-year-old woman who was admitted to the emergency unit with fever, shivers, and pain in the left fl ank. Baseline US (a) scan in the longitudinal plane shows increased thickness and heterogeneous appearance (arrows) of the left renal parenchyma. After 25 s from microbubble injection (b), renal parenchyma revealed homogeneous contrast enhancement in the longitudinal plane except for a hypovascular lesion (arrow) corresponding to a small renal abscess.

In the axial plane (c) a wedge-shaped renal perfusion defect (arrows) is identifi ed corresponding to focal pyelonephritis, and the renal abscess (arrow) is confi rmed (d).

a b

c d

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Jeong JY, Kim SH, Lee HJ (2002) Atypical low-signal-intensity renal parenchyma: causes and patterns. Radiographics 22:833–846

Kawashima A, Sandler CM, Ernst RD et al (2000) CT evaluation of renovascular disease. Radiographics 20:1321–1340 Kim B, Lim HK, Choi MH et al (2001) Detection of parenchymal

abnormalities in acute pyelonephritis by pulse inversion harmonic imaging with or without microbubble ultraso- nographic contrast agent. J Ultrasound Med 20:5–14 Mattrey RF, Steinbach G, Lee Y et al (1998) High-resolution

harmonic gray-scale imaging of normal and abnormal vessels and tissues in animals. Acad Radiol 5 (Suppl):

S63–S65

Munzing D, Mattrey RF, Reznik VM et al (1990) The potential role of PFOB enhanced sonography of the kidney, part I.

Detection of renal function and acute tubular necrosis.

Kidney Int 39:733–739

Quaia E, Bertolotto M (2002) Renal parenchymal diseases:

Is characterization feasible with ultrasound? Eur Radiol 12:2006–2020

Quaia E, Siracusano S, Ciciliato S et al (2004) Detection of renal perfusion defects in rabbits using non-linear con-

trast specific modes with low transmit power imaging and SonoVue (abstract). ECR 2004

Schmiedl UP, Carter S, Martin RW et al (1999) Sonographic detection of acute parenchymal injury in an experimen- tal porcine model of renal hemorrhage: gray-scale imag- ing using sonographic contrast agent. Am J Roentgenol 173:1289–1294

Taylor GA, Ecklund K, Dunning PS (1996) Renal cortical perfu- sion in rabbits: visualization with color amplitude imag- ing and an experimental mircobubble-based US contrast agent. Radiology 201:125–129

Taylor GA, Barnewolt CE, Adler BH, Dunning PS (1998) Renal cortical ischemia in rabbits revealed by contrast- enhanced power Doppler sonography. Am J Roentgenol 170:417–422

Taylor GA, Barnewolt CE, Claudon M, Dunning P (1999) Depic- tion of renal perfusion defects with contrast-enhanced harmonic sonography in a porcine model. Am J Roent- genol 173:757–760

Wong WS, Moss AA, Federle MP (1984) Renal infarction: CT diagnosis and correlation between CT findings and eti- ologies. Radiology 150:201–205

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