AJR 2000; 174:433-439
© American Roentgen Ray Society
Comparing Contrast-Enhanced Breath-Hold MR Angiography and Conventional Angiography
Olivier Ernst1,2,
Vincent Asnar3,
Géraldine Sergent1,
Emmanuel Lederman3,
Lionel Nicol4,
Jean-Claude Paris3 and
Claude L'Herminé1
1
Department of Radiology, Hôpital Huriez, Centre
Hospitalier Universitaire de Lille, 1 rue Polonovski, F-59037 Lille,
France.
2
Department of Radiology, Hôpital Calmette,
Centre Hospitalier Universitaire de Lille, Blvd. du Professeur Leclerc,
F-59037 Lille, France.
3
Department of Gastroenterology, Hôpital Huriez,
Centre Hospitalier Universitaire de Lille, F-59037 Lille, France.
4
Siemens SAS, 39 Blvd. Ornano, F-93527 Saint-Denis, France.
Received January 13, 1999;
accepted after revision July 8, 1999.
Address correspondence to O. Ernst.
Abstract
OBJECTIVE. Our aim was to compare the results of gadolinium-enhanced
breath-hold
MRangiographywiththoseofconventionalangiographyforthestudyofmesentericcirculation.
SUBJECTS AND METHODS. MR angiography and digital subtraction
angiography were prospectively performed in 33 patients referred for hepatic,
pancreatic, or mesenteric disease. MR angiography was performed with four
three-dimensional acquisitions at 0, 30, 60, and 90 sec after injection of 0.1
mmol/kg of gadolinium. Selective conventional angiography was used as the
standard of reference.
RESULTS. A pure arterial angiogram (one on which veins could not be
visualized) was obtainedin 27 patients during the second or third acquisition.
By subtracting the arterial phase from an arteriovenous phase (third or fourth
acquisition) we obtained a pure venous angiogram (one on which arteries could
not be visualized) in 28 patients. Agreement was good or excellent for the
hepatic artery (
= 0.78), the superior mesenteric artery ( =
0.65), the splenic artery ( = 0.70), the portal vein ( = 1.0),
the superior mesenteric vein ( = 0.88), and the splenic vein ( =
0.75). Agreement was poor, and vessels were better shown by conventional
angiography, for the intrahepatic arteries ( = 0.006) and the branches
of the superior mesenteric artery ( = 0.14). MR angiography and
conventional angiography revealed 29 and 27 portosystemic collaterals,
respectively.
CONCLUSION. Dynamic breath-hold contrast-enhanced MR angiography
compared favorably with conventional angiography in preoperative assessment of
the proximal mesenteric arteries and in the evaluation of portal hypertension;
however, conventional angiography is still necessary to evaluate distal
arteries.
Introduction
In the past, MR angiography was seldom used for the evaluation of
the mesenteric vasculature. The first techniques of MR angiography,
time-of-flight and phase contrast, required an acquisition time up to several
minutes [1,
2]. This long acquisition time
makes the acquisition of MR angiography impossible during a single
breath-hold; therefore, MR angiography of the upper abdomen was limited by
blurring from extensive motion artifacts
[3]. Furthermore, it was
impossible to obtain a pure arterial phase (phase in which veins could not be
visualized) andapurevenousphase(phaseinwhicharteriescouldnotbevisualized).
Gadolinium-enhanced breath-hold MR angiography can now be achieved by using
fast imaging techniques
[4,5].
Breath-hold MR angiography limits motion artifacts
[3] and has proven reliable for
evaluation of the renal arteries
[6,7,8].
With fast MR angiography it is possible to obtain angiograms during the
arterial and venous phases of the contrast medium injection by using several
acquisitions repeated at short intervals
[9]. Gadolinium-enhanced
breath-hold MR angiography has recently been used to evaluate the mesenteric
circulation
[9,10,11,12,13,14,15,16],
but to our knowledge only a few studies have compared its results with those
of conventional angiography
[11,14].
The purpose of our study was to compare the results of gadolinium-enhanced
breath-hold MR
angiographywiththoseofconventionalangiographyintheevaluationofthemesentericcirculation.
Subjects and Methods Patients
Between January and July 1998, 38 consecutive patients, referred by the
department of hepatogastroenterology for conventional angiography of the
mesenteric circulation, were requested to undergo MR angiography according to
a protocol approved by our institutional review board. Five patients were
excluded from this study either because of a contraindication to MR imaging or
a patient's refusal. Twenty-four men and nine women, 28-65 years old (mean, 51
years), were enrolled in our study and underwent conventional angiography and
MR angiography. Angiographic examinations were performed either before liver
transplantation for cirrhosis (n = 14); or before treatment of
hepatocellular carcinoma (n = 10), pancreatitis (n = 6),
pancreatic tumor (n = 1), mesenteric ischemia (n = 1), or
periarteritis nodosa (n = 1). The delay between both examinations was
1-60 days (mean, 18 days).
MR Angiography
All examinations were performed with a 1.5-T system (Magnetom Vision;
Siemens, Erlangen, Germany) with a 300-µsec rise time, 25 mT/m maximum
gradient strength, and a body phased array coil. We used a three-dimensional
fast low-angle shot sequence with the following imaging parameters: TR/TE,
3.2/1.1 msec; flip angle, 30-35°; section thickness, 2.3 mm; matrix, 256
x 160; field of view, 35 cm; excitation, 0.5; and acquisition time, 13
sec. The coronal plane was used with a 120-mm slab thickness. An IV bolus of
0.1 mmol/kg of gadopentetate dimeglumine (Magnevist; Schering, Lys lez Lannoy,
France) was injected at 0.01 ml·kg-1·sec-1
through an MR power injector (Spectris; MedRad, Pittsburgh, PA). Gadolinium
injection was immediately followed with a 20-ml saline flush at 2 ml/sec. Data
acquisition was initiated at the start of injection. Four acquisitions were
successively obtained at the start of injection and 30, 60, and 90 sec
afterward.
An image set was prepared for analysis. All post-processing was performed
by the same radiologist, without knowledge of the conventional angiography
results. Subvolume maximum-intensity-projection images were obtained in the
coronal and the sagittal planes to assess the celiac trunk; the hepatic,
superior mesenteric, and splenic arteries; the superior mesenteric, splenic,
and portal veins; and the portosystemic collateral vessels. The arterial phase
(second or third acquisition) was systematically subtracted from a delayed
phase (third or fourth acquisition).
Conventional Angiography
Digital subtraction angiography was performed in all patients with an
Advantx AFM 40 (General Electric Medical Systems, Milwaukee, WI), a 1024
x 1024 matrix, and a field of view of 30 or 40 cm as appropriate.
Selective studies were made using a 4- or 5-French catheter and selective
injection of 35 ml of iohexol (Omnipaque 300; Nycomed, Paris, France) in the
hepatic artery and the splenic artery and 60 ml in the superior mesenteric
artery, with a 6 ml/sec injection rate. All views were obtained in the frontal
plane. The left gastric artery and the inferior mesenteric artery were
catheterized only when necessary.
Image Analysis
The quality of all conventional angiograms and MR angiograms was graded at
a 1-month interval by two radiologists on a 1-4 scale (1 = no information, 2 =
bad, 3 = good, 4 = excellent). Separate analyses were performed for the common
and the proper hepatic arteries, the intrahepatic arteries, the splenic
artery, the superior mesenteric artery and its branches, the gastroduodenal
artery, the superior mesenteric vein, the splenic vein, and the portal vein.
For the maximum intensity projections obtained from the arterial phase, the
reviewers scored the projection of the vein on the arteries on a 1-4 scale (1
= nondiagnostic images because of venous projections, 2 = many venous
projections, 3 = a few venous projections, 4 = no vein visible). The
projection of the arteries on the veins was scored with the same scale on the
maximum intensity projections obtained from the delayed phases (portal phases)
and from the subtraction of the arterial phase from a portal phase. A
subjective diagnostic classification was made for all the vessels: diagnostic
value, none; diagnostic value, normal; diagnostic value, abnormal. The
reviewers also noted aberrant hepatic artery anatomy. These variations were
considered to be hepatic abnormalities. The number of collateral branches
arising from the superior mesenteric artery and the presence of portosystemic
collaterals such as gastroesophageal varices, umbilical vein, splenorenal
anastomoses, or other hepatofugal venous pathways were evaluated on MR and
conventional angiography. When discrepancies occurred between the two primary
observers, these images were reviewed with a third observer and a consensus
was reached.
Statistical Analysis
Agreement between MR angiography and conventional angiography, as well as
interobserver agreement, was assessed by weighted kappa analysis. Kappa index
values greater than 0.80 were considered excellent agreement; between 0.60 and
0.80, good; between 0.41 and 0.60, moderate; and less than 0.40, fair to poor
[17]. A nonparametric
Wilcoxon's rank sum test was used when appropriate.
Results
In one patient, catheterization of the celiac trunk was not possible during
conventional angiography. In another patient, on MR angiography the arteries
were faintly visible because the arterial phase occurred between the second
and the third acquisitions. In the other patients, an arterial phase was
always obtained, corresponding either to the second phase (n = 28) or
the third phase (n = 4). A portal phase was obtained for all
patients.
On conventional angiography, the average image quality for each vessel was
good or excellent. On MR angiography, the average image quality was also good
or excellent except for intrahepatic arteries and collaterals of the superior
mesenteric artery (Table 1).
The agreement between the two observers was moderate ( = 0.57). During
the arterial phase, the venous system was visible in six patients (18%) but it
hindered visualization of the arteries in only one. In five patients the
presence of veins did not worsen the image quality, and the arteries were
clearly depicted. Arteries were visualized on the portal phase in 31 patients
(94%). After subtraction of the arterial phase from the portal phase, arteries
were no longer visible in 28 patients (85%). The number of mesenteric branches
depicted on MR angiography (mean, 5.07; SD, 1.95) and conventional angiography
(mean, 9.37; SD, 2.3) was significantly different (p = 0.001).
The overall agreement between MR angiography and conventional angiography
for depicting vascular normality or abnormality was moderate ( = 0.53).
The agreement was good or excellent for the hepatic artery ( = 0.78),
the superior mesenteric artery ( = 0.65), the splenic artery ( =
0.70), the gastroduodenal artery ( = 0.74), the portal vein ( =
1), the superior mesenteric vein ( = 0.88), and the splenic vein
( = 0.75). There was poor agreement for the distal arteries such as the
intrahepatic arteries ( = 0.01) and the branches of the superior
mesenteric artery ( = 0.14). The distal arteries were better visualized
on conventional angiography. The agreement between the two primary observers
was good ( = 0.76). No vessel was considered normal by one observer and
abnormal by the other observer. However, in eight cases discrepancies occurred
between the two observers; one observer concluded that MR angiograms had no
diagnostic value for a given vessel, whereas this vessel was considered normal
by the other observer. Conventional angiography confirmed a normal pattern of
these vessels.
MR angiography depicted a left hepatic artery arising from the left gastric
artery in four patients, whereas conventional angiography depicted this
variant in two patients. MR angiography and conventional angiography showed a
right hepatic artery arising from the
superiormesentericarteryinfivepatients(Fig.
1A,1B,1C),
ananeurysmofthehepaticarteryinonepatient, a stenosis of the gastroduodenal
artery in threepatients,astenosisofthesplenicarteryin two patients (Fig.
2A,2B),
and a segmental thrombosis of the superior mesenteric artery in one patient
(Fig.
3A,3B,3C,3D).
Nine venous thromboses involvingeithertheportalvein (n = 2), the
superior mesenteric vein (n = 2) (Fig.
4A,4B),
or the splenic vein (n = 5) were depicted on MR angiography and
conventional angiography. In one patient the splenic vein was not depicted on
MR angiography but was visible on conventional angiography.
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Fig. 1A. —Hepatic cirrhosis in 48-year-old man. Contrast-enhanced breath-hold
MR angiogram shows left hepatic artery (arrow) arising from left
gastric artery and right hepatic artery (arrowhead) arising from
superior mesenteric artery.
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Fig. 1B .—Hepatic cirrhosis in 48-year-old man. Conventional angiography with
selective catheterization of left gastric artery reveals pattern in left
gastric artery (arrow) similar to that seen in A.
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Fig. 3A .—Mesenteric ischemia in 26-year-old woman.
A and B, Gadolinium-enhanced breath-hold MR angiograms show
segmental occlusion of superior mesenteric artery (large arrow,
A). Distal part of the superior mesenteric artery (small
arrow, A) is revascularized by arc of Riolan (arrowheads,
A and B).
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Fig. 3B .—Mesenteric ischemia in 26-year-old woman.
A and B, Gadolinium-enhanced breath-hold MR angiograms show
segmental occlusion of superior mesenteric artery (large arrow,
A). Distal part of the superior mesenteric artery (small
arrow, A) is revascularized by arc of Riolan (arrowheads,
A and B).
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Fig. 3C .—Mesenteric ischemia in 26-year-old woman.
C and D, Conventional angiograms with selective
catheterization of superior mesenteric artery (arrow, D) and
inferior mesenteric artery (arrowhead, C) reveal pattern
similar to that seen in A and B.
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Fig. 3D .—Mesenteric ischemia in 26-year-old woman.
C and D, Conventional angiograms with selective
catheterization of superior mesenteric artery (arrow, D) and
inferior mesenteric artery (arrowhead, C) reveal pattern
similar to that seen in A and B.
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Fig. 4A .—Pancreatitis in 61-year-old man. Venous contrast-enhanced MR
angiogram shows occlusion of upper part of superior mesenteric vein
(arrow) with collateral circulation through first jejunal vein
(arrowhead) feeding the portal vein.
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In most cases, it was not possible to make a diagnosis for the intrahepatic
arteries and the branches of the superior mesenteric artery on MR angiography,
but this was possible on conventional angiography. For the other vessels, MR
angiography allowed a diagnosis in more than 88% of the cases and conventional
angiography allowed a diagnosis in more than 94% of the cases
(Table 2). All vascular
abnormalities evidenced on conventional angiography were also depicted on MR
angiography. All vessels considered normal on MR angiography were also
considered normal on conventional angiography
(Table 2).
MR angiography depicted the left gastric (coronary) vein in 19 patients and
other portosystemic collaterals in 10 patients (Fig.
5A,5B).
Conventional angiography depicted the left gastric vein in 18 patients
( = 0.93) and other portosystemic collaterals in 9 patients ( =
0.92).
Discussion
MR angiography was seldom used in the past for the evaluation of the
mesenteric circulation [1,
2,
18,19,20,21,22,23,24].
With time-of-flight and phase contrast MR angiography, respiration-induced
motion of abdominal vessels caused a blurring that precluded a high image
quality for the abdominal vessels
[3]. Then the use of
time-of-flight or phase contrast MR angiography was mainly limited to the
portal venous system [1,
18,19,20,21,22,23].
The development of breath-hold MR angiography with gadolinium enhancement has
increased the quality of abdominal MR angiography
[3]. The first abdominal
applications of breath-hold gadolinium-enhanced MR angiography were the aorta
and the renal arteries [3,
7,
25]. The results of this
method in the study of the mesenteric, hepatic, and portal vessels have rarely
been evaluated
[9,10,11,12,
14].
In our study, the image quality was good for all vessels except small
arteries such as the intrahepatic arteries and branches of the superior
mesenteric artery, which are better depicted on conventional angiography. This
image quality can probably be explained by the use of a power injector
[26] and a short acquisition
time (13 sec) that allowed a breath-hold acquisition and a decrease in motion
artifacts [3]. Another
advantage of fast abdominal MR angiography is the possibility of having
several consecutive acquisitions repeated at short intervals, thus obtaining
an arterial phase without any venous overlap in most cases (82%). During the
subsequent phases, overlapping of the arteries on the veins occurred in 94% of
our patients. The phases during which overlapping occurs are actually not pure
portal phases but mixed arterioportal phases
[9]; however, arterial images
can easily be eliminated by subtracting an arterial phase from a mixed
arterioportal phase. We obtained a pure portal phase in 85% of the patients.
This postprocessing was useful for differentiating venous images from arterial
images, and particularly for evaluating portocaval anastomoses.
In our study, MR angiography depicted all arterial abnormalities and
variations diagnosed with conventional angiography. These results suggest that
MR angiography is as sensitive as conventional angiography for evaluating the
main mesenteric arteries. The advantage of gadolinium-enhanced breath-hold MR
angiography for mesenteric, hepatic, and splenic arteries was previously
described in only a few studies
[9,
11,
14] with few comparisons
between the results of MR angiography and those of conventional angiography
[11,
14]. Stafford-Johnson et al.
[11] showed that
gadolinium-enhanced MR angiography can depict vascular complications of liver
transplantation, and Meaney et al.
[14] showed that this
technique is useful in the evaluation of patients with suspected mesenteric
ischemia. The relatively low number of arterial lesions and stenoses in our
study is probably a limitation of the study. Additional studies will help to
further evaluate the accuracy of MR angiography in quantifying mesenteric
artery stenosis, as has been done for the renal arteries
[27]. In our study, arteries
were hidden by veins in one patient because the arterial phase occurred
between the second and the third acquisitions. To decrease the effects caused
by the variations of the blood circulation, the time interval between two
acquisitions can be reduced from 17 to 6 sec
[9]. In our study, MR
angiography showed two more left hepatic arteries arising from the left
gastric artery than did conventional angiography. This is because the left
gastric artery was not selectively catheterized in all patients during
conventional arteriography, and all aberrant arteries included in the volume
of interest can be depicted through MR angiography.
In our study, there was good agreement between conventional angiography and
MR angiography in the depiction of venous abnormalities. Patency or thrombosis
of the superior mesenteric vein, the portal vein, and the splenic vein was
accurately depicted in all but one patient. In one patient, the patent splenic
vein was not visualized on maximum-intensity-projection or source images
because an aliasing artifact redisplayed the subcutaneous fat of the anterior
abdominal wall on the splenic vein. This artifact can be avoided by increasing
the slab thickness to 150 mm. Similar results were obtained in other studies
by using either time-of-flight MR angiography
[20,
22], phase contrast MR
angiography [18,
21], or contrast-enhanced MR
angiography [11,
12,
28]. Portosystemic collaterals
were also clearly depicted on MR angiography in our study, as in previous
studies [19,
22,
23]. The main advantage of
dynamic breath-hold MR angiography over other MR angiography techniques is the
possibility of eliminating the signal of the arteries by subtracting the
arterial phase from the arterioportal phase. The images obtained with this
postprocessing are similar to those obtained by conventional angiography with
catheterization of the splenic and superior mesenteric arteries.
The efficacy of gadolinium-enhanced MR angiography in our study is shown by
the good agreement between the results of MR angiography and those of
selective digital subtraction angiography with a 1024 x 1024 matrix for
the proximal arteries and the main veins. However, conventional angiography
was more diagnostic than MR angiography for the intrahepatic arteries and the
branches of the superior mesenteric artery (Fig.
6A,6B,6C).
Therefore, the results of MR angiography are still insufficient for the distal
arteries. This can be explained by the difference in spatial resolution
between both techniques; the pixel size is 1.4 x 2.2 mm for MR
angiography and less than 0.5 x 0.5 mm for digital subtraction
angiography.
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Fig. 6A .—Hepatic cirrhosis in 55-year-old man. Contrast-enhanced breath-hold
MR angiogram shows superior mesenteric artery (arrowhead), proper
hepatic artery (long arrow), and left hepatic artery (short
arrow) arising from left gastric artery.
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Fig. 6C .—Hepatic cirrhosis in 55-year-old man. Conventional angiography with
selective catheterization of superior mesenteric artery reveals several
arterial branches not shown on MR angiogram.
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In conclusion, our data indicate that MR angiography correctly predicted
all arterial abnormalities and anatomic variants identified with conventional
angiography in our study. Though proximal arterial pathology was limited in
our study, we have concluded that breath-hold abdominal MR angiography appears
to be sufficient for preoperative evaluation of the main mesenteric arteries
and veins. This will need to be confirmed in a larger study. Moreover,
breath-hold abdominal angiography can supplement standard MR examination or MR
cholangiopancreatography when performed in patients with hepatic, pancreatic,
or biliary disease with suspected vascular involvement. This procedure might
be particularly useful after liver transplantation because it enables an
examination for vascular anastomoses and biliary anastomosis. Dynamic MR
angiography can also be used to evaluate the portal venous system and the
portocaval anastomoses in cases of portal hypertension. However, conventional
angiography is still necessary to evaluate distal arteries such as
intrahepatic arteries and superior mesenteric branches.
Acknowledgments
We thank John Hall for manuscript preparation and editorial assistance.
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K. Ito, S. Koike, A. Shimizu, M. Tanabe, C. Jo, M. Miyazaki, and N. Matsunaga
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A. H. M. Caiado, R. Blasbalg, A. S. Z. Marcelino, M. da Cunha Pinho, M. C. Chammas, C. da Costa Leite, G. G. Cerri, A. C. de Oliveira, T. Bacchella, and M. C. C. Machado
Complications of Liver Transplantation: Multimodality Imaging Approach
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B. S. Kim, T. K. Kim, D. J. Jung, J. H. Kim, I. Y. Bae, K.-B. Sung, P. N. Kim, H. K. Ha, S. G. Lee, and M.-G. Lee
Vascular Complications After Living Related Liver Transplantation: Evaluation with Gadolinium-Enhanced Three-Dimensional MR Angiography
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F. Cognet, D. B. Salem, M. Dranssart, J.-P. Cercueil, M. Weiller, E. Tatou, L. Boyer, and D. Krause
Chronic Mesenteric Ischemia: Imaging and Percutaneous Treatment
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J. F. Glockner
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Top
Abstract
Introduction
