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CONTRAST-ENHANCED PORTAL MAGNETIC RESONANCE ANGIOGRAPHY IN DOGS WITH SUSPECTED CONGENITAL PORTAL VASCULAR ANOMALIES WILFRIED MAI,CHICK WEISSE Contrast-enhanced multiphase magnetic resonance angiography (CE-MRA) was used in 17 dogs with a suspected congenital portal vascular anomaly. Portal vascular anomalies were identified in 16 of the 17 dogs. Eleven had a single intrahepatic portocaval shunt (two central divisional, three right divisional, and six left divisional), one dog had a double intrahepatic portocaval shunt, one dog had a hepatic arteriovenous malformation, one dog had a complex intrahepatic porto-caval shunt. Two dogs had an extrahepatic portosystemic shunt and no shunt was identified in one dog. Total imaging time was o10 min and image quality was good to excellent in all dogs. Portal CE-MRA is a feasible, fast and non invasive technique to diagnose portal vascular anomalies in dogs, with a large field-of-view and good anatomic depiction of the abnormal vessels. Based on these results, CE-MRA is an efficient imaging technique for the diagnosis of portal vascular anomalies in dogs. r 2010 Veterinary Radiology & Ultrasound, Vol. 52, No. 3, 2011, pp 284–288. Key words: arteriovenous fistula, dogs, gadolinium, magnetic resonance angiography, portosystemic shunts. P ORTAL VASCULAR ANOMALIES in the dog and cat include congenital or acquired porto-systemic shunts, portal venous hypoplasia (formerly called micro-vascular dyspla- sia), noncirrhotic portal hypertension with portal vein atresia and hepatic arteriovenous malformation. 1–9 Vascular opacification with contrast medium to identify abnormal anatomy can be replaced with computed tomography angiography or magnetic resonance angio- graphy (MRA), which are noninvasive. In addition, as interventional procedures are becoming more available to treat portosystemic shunts, minimally invasive imaging techniques that provide anatomic depiction and precise measurements of the abnormal vessels are needed. 10–16 Contrast-enhanced magnetic resonance angiography (CE-MRA) can provide excellent assessment of portal vascular anatomy in short acquisition times. 17,18 CE-MRA has surpassed noncontrast MRA techniques in many applications. 19–21 Although magnetic resonance imaging is used frequently in veterinary medicine, there is only limited information on the use of MRA. 17,18,22–30 Our objective was to evaluate CE-MRA for the diagnosis of congenital hepatic vascular diseases in dogs. Materials and Methods Seventeen dogs suspected of having congenital vascular liver disease were evaluated. Inclusion criteria were: clinical signs consistent with hepatic vascular disease and elevated circulating bile acids. There were eight males and nine females, with age ranging between 4 and 36 months (median 7 months). Breeds were: Brittany spaniel (n ¼ 2), Golden Retriever (n ¼ 2), Labradoodle (n ¼ 2), Bernese mountain dog (n ¼ 2), Labrador mixed dog (n ¼ 2), Ger- man shepherd (n ¼ 1), Pomeranian (n ¼ 1), Boxer (n ¼ 1), Labrador (n ¼ 1), Portuguese water dog (n ¼ 1), Maltese (n ¼ 1), Havanese (n ¼ 1). Whenever possible, MRA findings were confirmed at surgery or with invasive angiography during coil embolization. Anesthesia and imaging protocols were similar to those described previously. 18 Briefly, a three plane 2D T2 - weighted gradient echo localizer was used to plan the MRA acquisition. For CE-MRA, a 3D Fast Spoiled Gradient Recalled Echo (3D FSPGR) sequence with elliptic centric view ordering of k-space was used with parallel acquisition (array spatial sensitivity encoding technique). The 3D volume for MRA was prescribed in the dorsal plane, and positioned to cover as much of the liver as possible in the dorsal to ventral direction, and including at least the confluence of the left hepatic vein cranially and the splenoportal confluence caudally. In each dorsal plane, phase encoding was left to right and This study was funded by a grant from the American Kennel Club/ Canine Health Foundation (ACORN No. 1160-A). Partial results from this study were presented at the ACVR Annual Scientific Meeting, San Antonio, TX, August 2008. Address correspondence and reprint requests to Dr. Wilfried Mai, at the above address. E-mail: [email protected] Received July 23, 2010; accepted for publication October 26, 2010. doi: 10.1111/j.1740-8261.2010.01771.x From the Rosenthal Imaging and Treatment Center, University of Pennsylvania, School of Veterinary Medicine, Philadelphia, PA 19104 (Mai), and The Animal Medical Center, New York, NY 10065 (Weisse). 284

CONTRAST-ENHANCED PORTAL MAGNETIC RESONANCE ANGIOGRAPHY IN DOGS WITH SUSPECTED CONGENITAL PORTAL VASCULAR ANOMALIES

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CONTRAST-ENHANCED PORTAL MAGNETIC RESONANCE

ANGIOGRAPHY IN DOGS WITH SUSPECTED CONGENITAL PORTAL

VASCULAR ANOMALIES

WILFRIED MAI, CHICK WEISSE

Contrast-enhanced multiphase magnetic resonance angiography (CE-MRA) was used in 17 dogs with a

suspected congenital portal vascular anomaly. Portal vascular anomalies were identified in 16 of the 17 dogs.

Eleven had a single intrahepatic portocaval shunt (two central divisional, three right divisional, and six left

divisional), one dog had a double intrahepatic portocaval shunt, one dog had a hepatic arteriovenous

malformation, one dog had a complex intrahepatic porto-caval shunt. Two dogs had an extrahepatic

portosystemic shunt and no shunt was identified in one dog. Total imaging time waso10min and image quality

was good to excellent in all dogs. Portal CE-MRA is a feasible, fast and non invasive technique to diagnose

portal vascular anomalies in dogs, with a large field-of-view and good anatomic depiction of the abnormal

vessels. Based on these results, CE-MRA is an efficient imaging technique for the diagnosis of portal vascular

anomalies in dogs. r 2010 Veterinary Radiology & Ultrasound, Vol. 52, No. 3, 2011, pp 284–288.

Key words: arteriovenous fistula, dogs, gadolinium, magnetic resonance angiography, portosystemic

shunts.

PORTAL VASCULAR ANOMALIES in the dog and cat include

congenital or acquired porto-systemic shunts, portal

venous hypoplasia (formerly called micro-vascular dyspla-

sia), noncirrhotic portal hypertension with portal vein

atresia and hepatic arteriovenous malformation.1–9

Vascular opacification with contrast medium to identify

abnormal anatomy can be replaced with computed

tomography angiography or magnetic resonance angio-

graphy (MRA), which are noninvasive. In addition, as

interventional procedures are becoming more available to

treat portosystemic shunts, minimally invasive imaging

techniques that provide anatomic depiction and precise

measurements of the abnormal vessels are needed.10–16

Contrast-enhanced magnetic resonance angiography

(CE-MRA) can provide excellent assessment of portal

vascular anatomy in short acquisition times.17,18 CE-MRA

has surpassed noncontrast MRA techniques in many

applications.19–21 Although magnetic resonance imaging

is used frequently in veterinary medicine, there is only

limited information on the use of MRA.17,18,22–30 Our

objective was to evaluate CE-MRA for the diagnosis of

congenital hepatic vascular diseases in dogs.

Materials and Methods

Seventeen dogs suspected of having congenital vascular

liver disease were evaluated. Inclusion criteria were: clinical

signs consistent with hepatic vascular disease and elevated

circulating bile acids. There were eight males and nine

females, with age ranging between 4 and 36 months

(median 7 months). Breeds were: Brittany spaniel (n¼ 2),

Golden Retriever (n¼ 2), Labradoodle (n¼ 2), Bernese

mountain dog (n¼ 2), Labrador mixed dog (n¼ 2), Ger-

man shepherd (n¼ 1), Pomeranian (n¼ 1), Boxer (n¼ 1),

Labrador (n¼ 1), Portuguese water dog (n¼ 1), Maltese

(n¼ 1), Havanese (n¼ 1). Whenever possible, MRA

findings were confirmed at surgery or with invasive

angiography during coil embolization.

Anesthesia and imaging protocols were similar to those

described previously.18 Briefly, a three plane 2D T2�-weighted gradient echo localizer was used to plan the

MRA acquisition. For CE-MRA, a 3D Fast Spoiled

Gradient Recalled Echo (3D FSPGR) sequence with

elliptic centric view ordering of k-space was used with

parallel acquisition (array spatial sensitivity encoding

technique). The 3D volume for MRA was prescribed in

the dorsal plane, and positioned to cover as much of the

liver as possible in the dorsal to ventral direction, and

including at least the confluence of the left hepatic vein

cranially and the splenoportal confluence caudally. In each

dorsal plane, phase encoding was left to right and

This study was funded by a grant from the American Kennel Club/Canine Health Foundation (ACORN No. 1160-A).Partial results from this study were presented at the ACVR AnnualScientific Meeting, San Antonio, TX, August 2008.Address correspondence and reprint requests to Dr. WilfriedMai, at the

above address. E-mail: [email protected] July 23, 2010; accepted for publication October 26, 2010.doi: 10.1111/j.1740-8261.2010.01771.x

From the Rosenthal Imaging and Treatment Center, University ofPennsylvania, School of Veterinary Medicine, Philadelphia, PA 19104(Mai), and The Animal Medical Center, New York, NY 10065 (Weisse).

284

frequency encoding cranial to caudal. Scan parameters

varied slightly depending on patient size and were as

follows: field of view 24� 24–34 � 34 cm; in-plane matrix

256 � 160; 2mm section thickness; 301 flip angle; band-

width 31.25–62.5 kHz; TR 4.1–6.6ms; TE 1.02–1.77ms;

NEX of 0.5–1. Zero filling was performed to obtain an

interpolated matrix of 512 pixels in the frequency encode

direction with additional overlapping interpolated slices

along the z-axis. The number of locations per 3D volume

varied from 34 to 60 depending on the size of the dog.

For image acquisition, apnea was induced by a constant

infusion of cisatracurium and turning the ventilator off

during acquisition.� In some patients, this was later

reversed using atropinew and neostigmine.z A precontrast

mask was acquired for all dogs just before gadolinium

injection. Four consecutive 3D-volumes were acquired

starting immediately after the injection of gadolinium

(0.3mmol/kg, followed by a flush of 5–10ml of saline).y As

reported previously, the contrast medium was injected

manually as rapidly as possible.17,18 A single injection was

used in all dogs.

Images were reviewed on a dedicated work station by a

board-certified radiologist (W.M.).z The phase with overall

best portal vascular enhancement was identified subjec-

tively and the mask was subtracted from this series before

reconstruction. Images were examined using full and

subvolume maximum intensity projections (MIP) in

various planes as well as volume rendering. Single voxel-

thick images in the dorsal, transverse, and sagittal planes

were also reviewed to assess specific vessels.

Results

Acquisition time ranged between 60 and 70 s. Including

the 3-plane localizer, 3D volume planning, mask acquisi-

tion and CE-MRA multiphase acquisition, total imaging

time was o10min. An additional 10–15min was required

for inspection, subtraction, reformatting, and generation of

MIPs and volume rendering.

In all dogs arterial enhancement occurred during the first

phase and the best enhancement of the portal venous

system occurred during the second or third phase after

contrast medium injection. No motion artifact was present,

and adequate suppression of background signal from soft

tissues was observed. At the portal phase, the enhanced

liver parenchyma and kidneys provided useful landmarks

for identification of specific vessels.

Three dogs had a single intrahepatic right divisional

shunt (Fig. 1), two dogs had a single intrahepatic central

divisional shunt (Fig. 2), six dogs had a single intrahepatic

left divisional shunts (Fig. 3), one dog had a combination

of two intrahepatic shunt (right divisional and central

divisional) (Fig. 4), one dog had a complex intrahepatic

shunt with multiple intrahepatic tortuous vessels which

were believed to be secondary intrahepatic communica-

tions, two dogs had an extrahepatic shunt (splenocaval and

splenophrenic), and one dog had a hepatic arteriovenous

Fig. 1. Left panel: 3D volume rendering of a right divisional intrahepaticshunt in a dog. The U shaped shunting vessel can be seen entering the rightside of the caudal vena cava (CVC). Right panel: Corresponding selectiveportal angiography. The shunting vessel (S) is visible.

Fig. 2. Dorsal oblique thick subvolume maximum intensity projectionat the portal phase in a dog with a typical bulbous intrahepatic cen-tral divisional portocaval shunt (CVC, caudal vena cava; LK, left kidney;LGV, left gastric vein, PDV, pancreatico-duodenal vein, GDV, gastro-duodenal vein; SV, splenic vein).

�Nimbex, cisatracurium bensylate 2mg/ml, Abbott Laboratories,North Chicago, IL.wAtroject, atropine 5mg/ml, Butler American Health Supply, St.

Joseph, MO.zReversal Neostigmine, 1mg/ml, American Regent, Shirley, NY.yMagnevist, Berlex Imaging, Wayne, NJ.zGE Signa, 1.5T, 9.1 Software M4, Milwaukee, WI.

285PORTAL MRAVol. 52, No. 3

malformation (Figs. 5 and 6). One dog (Havanese) did not

have a macroscopic shunt.

The abnormal vessels could be identified in all animals

and the origin and termination were clearly visible in all

but one dog, in which there was a complex network of

enlarged tortuous intrahepatic vessels; some communicated

with the portal vein or its intrahepatic branches while

others communicated with the caudal vena cava. During

transjugular retrograde portography, it was apparent that

the primary shunt was central divisional and there had

been development of a complex network of large intra-

hepatic venous collaterals.31

In one dog a complex double intrahepatic shunt was

observed (Fig. 4): there was a combination of a right-

divisional-like vessel that appeared as a U-shaped loop in

the right dorsal liver blending cranially with an aneurismal

dilation of the portal vein, which was communicating

dorsally with the caudal vena cava, suggestive of a central-

divisional anatomy.

Fig. 3. 3D reconstructions in a dog with a left divisional intrahepaticshunt. Left lateral view is on the left and ventral view on the right. Theshunting vessel (S) can be seen merging with a dilated portion of the lefthepatic vein (CVC, caudal vena cava; LK, left kidney; PDV, pancreatico-duodenal vein; GDV, gastro-duodenal vein; SV, splenic vein, Ao, aorta).

Fig. 4. Dorsal subvolume MIPs at six different levels in a dog with a double intrahepatic shunt. The U-shaped right divisional shunt is indicated by the blackarrow and the bulbous central divisional shunt is indicated by � (PDV, pancreaticoduodenal vein; GDV, gastroduodenal vein; SV, splenic vein).

Fig. 5. Volume rendering of the arterial phase of the multiphase magneticresonance angiography study in a dog with a hepatic arteriovenousmalformation. Cranial is to the top. (A) Oblique view from the left side.(B) ventral view. Note the large size of the celiac artery compared with thecranial mesenteric artery. The celiac artery feeds a network of tortuousvessels in the liver around the gallbladder and early filling of dilatedintrahepatic portal vessels is seen. In (B) early retrograde filling of the mainportal vein (�) indicative of hepatofugal flow is seen, due to the high pressuretransmitted through the fistula. Also note the dramatic reduction in size ofthe aorta just caudal to the origin of the celiac artery, also typical of thisanomaly.

286 MAI ANDWEISSE 2011

In the Boxer, a hepatic arteriovenous malformation was

diagnosed and confirmed with selective arteriography. At

the arterial phase of the study (Phase 1) the celiac artery fed

a fine network of tortuous vessels near the gallbladder that

communicated with a large dilated portal venous branch,

in the cranioventral aspect of the liver. There was early

retrograde filling of the portal vein during the arterial

phase consistent with hepatofugal portal flow (Fig. 5). The

aorta decreased in size abruptly caudal to the origin of the

celiac artery, and the celiac artery was dilated compared

with the cranial mesenteric artery (Fig. 5). At the portal

venous phase, a complex network of intrahepatic dilated

vascular structures was seen. Multiple extrahepatic tortu-

ous small vessels were observed in the region of the left

kidney, draining into an enlarged left phrenicoabdominal

vein consistent with gastrophrenic varices (Fig. 6).32

Results of CE-MRA were confirmed with invasive

selective angiography in 13 dogs (Fig. 1) and surgery in

one dog. In the other three dogs, no additional procedures

were performed.

Discussion

CE-MRA allowed accurate characterization of porto-

systemic shunts in 16 dogs. The single intrahepatic and

extrahepatic shunts had the typical expected appear-

ance.33,34 For the complex double intrahepatic shunt, the

anatomy was similar to that described previously.35 Others

have also found excellent depiction of portosystemic shunts

with CE-MRA.17

In one Havanese dog, a portosystemic communication

was not identified. This dog was 2.5 years old and referred

because of mildly elevated ALT values found incidentally.

Post-prandial bile acids were increased moderately. A

biopsy was not obtained but based on the absence of

macroscopic shunt a tentative diagnosis of portal venous

hypoplasia was made.

In other work using CE-MRA for portosystemic shunt

characterization, the majority of the shunts were of the

single extrahepatic type.17 Our population, on the other

hand, contained a majority of dogs with a single in-

trahepatic shunts. This was expected as the majority of

dogs in our study were large breed dogs, whereas in the

other work the population was mostly small and toy-breed

dogs.

In the context of assessing a patient for portal vascular

anomalies, MRA has some limitations. It does not allow

accurate identification of renoliths or cystoliths that are

commonly associated with portosystemic shunts in dogs.

Such lesions are usually readily identified with CT due to

their high attenuation. If a portal anomaly is identified

with MRA, it is warranted to perform an ultrasound to

identify calculi.

Our study complements other recently published in-

formation and illustrates the use of CE-MRA in the

diagnosis of portosystemic communications of various

types. Altogether, these data indicate that CE-MRA is an

efficient tool for the diagnosis of all types of macroscopic

portal vascular anomalies in the dog.

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