Genitourinary Steven S. Eilenberg, Scott A. Mirowitz,
MD MD
#{149} Joseph #{149} V.
Marie
Renal Masses: Gd-DTPA-enhanced
K. T. Lee, MD Tartar, MD
Evaluation
Index terms: Cadolinium #{149} Kidney, cysts, 81.3111 #{149} Kidney, MR studies, 81.1214 #{149} Kidney neoplasms, diagnosis, 81.3141, 81.32 #{149} Kidney neoplasms, MR studies, 81.1214 #{149} Magnetic resonance (MR), contrast enhancement
‘From From
ary
the the
masses
14, 1990; RSNA,
MD
(5-7), of renal
RSNA
revision 1990
PATIENTS
of renal the do-
main of computed tomography (CT) and ultrasound. The diagnostic accuracy of these imaging modalities in the characterization of renal lesions approaches 100% (1-4). Magnetic resonance (MR) imaging has met with some success in the detection and characterization of renal cysts and neoplasms staging
#{149}
Gradient-Echo MR Imaging’
as well as in the cell carcinoma (8,9).
Institute
of Radiology,
assembly.
received
March
Received
16; accepted
METHODS
Patients Fifteen
ther
patients
a simple
neoplasm
with
renal
were
CT
cyst
evidence
or a solid
prospectively
of ei-
renal
examined
with the use of MR imaging from April 1989 to September 1989. The 10 men and five women had a mean age of 59 years (range, 25-80 years). One 55-year-old man with no identifiable risk factors had three
renal
cytoma;
cell
carcinomas
an additional
and
an
onco-
six carcinomas
simple renal cysts were identified in six patients (a seventh patient also had a small renal cell carcinoma). The single angiomyolipoma was discovered during chest CT in a 35-year-old woman with ad-
solid
els
neoplasms
and
renal
parenchy-
techniques
during
undertaken
vanced
to evaluate
the
enhancement patterns of simple renal cysts and solid neoplasms and to investigate the usefulness of MR imaging in the differentiation of these lesions.
5105
Kingshighway
December
April
29,
23. Address
Blvd. 1989;
St Louis,
in six other
pulmonary
sis. All patients less
than
Seven
lymphangiomyomatohad
1.4
patients.
serum
mg/dL
creatinine
(120
1ev-
zmol/L).
suspend-
ed respiration (11). By adjusting the flip angle, the repetition time (TR), and the echo time (TE), variable degrees of Ti and T2 weighting can be achieved (12). Further improvement in lesion detection and characterization can be accomplished with the administration of gadolinium diethylenetniaminepentaacetic acid (DTPA) (13-15). This contrast material is handled by the kidney in much the same way that iodinated intravenous contrast agents are (16). This was
present
Eleven contralateral kidneys with normal morphologic features from this same patient population were also studied.
ma (10). A significant reduction in breathing artifacts can be achieved with the use of gradient-echo (GRE) imaging
were
Other
Imaging
All 15 patients dium-enhanced
MO
63110.
revision requested Februreprint requests to J.K.T.L.
Modalities
contrast me3 weeks of MR imaging. CT was performed with either a Somatom DRH or PLUS unit (Siemens Medical Systems, Iselin, NJ) with 8mm beam collimation and 10-mm table increments during the rapid infusion of 100-150 mL of Conray 60 (iothalamate meglumine, Mallinckrodt, St Louis) or a similar dose of Optiray 300 (ioversol; Mallinckrodt). All seven renal cysts met strict
underwent CT within
contrast-enhanced
CT criteria
for simple
cysts, including a sharp interface with nal parenchyma, an attenuation value near that of water, absence of a perceptible wall, and lack of contrast enhancement (2-4). The nine renal cell carcino-
re-
mas and the oncocytoma were prospectively diagnosed at contrast-enhanced CT as solid neoplasms, and the diagnosis was confirmed
scientific
AND
Despite reports to this effect, renal MR imaging remains largely a problem-solving tool. Limitations associated with standard spin-echo (SE) renab imaging include image degradation caused by breathing artifacts and suboptimal lesion conspicuity due to the similarity of Ti and T2 values of
176:333-338
Mallinckrodt
1989
assessment remains largely
ADIOLOGIC
study
1990;
with Dynamic
Dynamic contrast material-enhanced gradient-echo magnetic resonance (MR) imaging was performed on 15 patients with 18 renal masses (seven simple renal cysts, nine renal cell carcinomas, one angiomyolipoma, and one oncocytoma). Fifteen sequential images were obtained while the patients held their breath during a 2.5-3.5minute interval during and immediately after the intravenous administration of gadolinium diethylenetriaminepentaacetic acid (DTPA); delayed images were also obtained for 15 minutes. Time-intensity curves showed that renal cortical enhancement reached maximal intensity 80 seconds after the injection of Gd-DTPA. Medullary enhancement reached maximal intensity at 120 seconds. None of the simple renal cysts showed enhancement; each cyst displayed a signal intensity less than that of the renal cortex on precontrast images. All renal cell carcinomas were isointense with the renal cortex and demonstrated variable enhancement. Three patterns of enhancement were observed: predominantly peripheral, heterogeneous, and homogeneous. Both the angiomyolipoma and the oncocytoma showed brisk, homogeneous enhancement. This MR imaging technique appears to be useful in the detection and characterization of simple renal cysts and solid neoplasms.
Radiology
J. Brown,
#{149} Jeffrey
Radiology
at surgery.
Abbreviations:
DTPA
pentaacetic acid, GRE = gradient
FLASH echo, SE
echo
repetition
time,
TR
The
angiomyoli-
diethylenetriamine-
= = =
fast low-angle spin echo, TE
shot, =
time.
333
3.
2.
1.
11 normal kidneys studied with the dyof renal cortex and medulla were normalized to the signal intensity of retroperitoneal fat (SI tissue/SI fat). (2) Comparison of time-intensity curves for seven simple renal cysts, the enhancing portions of nine renal cell carcinomas, and normal renal cortex of 11 kidneys. All signal intensities were normalized to the signal intensity of retroperitoneal fat. (3) Comparison of time-intensity curves for angiomyolipoma, oncocytoma, simple renal cysts, and the enhancing portions of the Figures
1-3.
namic
(1) Time-intensity
curve
Gd-DTPA-enhanced
renal
FLASH
cell carcinomas.
All
signal
for
renal
technique.
intensities
Imaging
were
Protocol
MR imaging
was performed
commercially
available
with
1 .0-T
a
msec/TE
msec)
transaxial
x
256
sequence
in either
or the coronal
matrix,
section
plane
the
with
thickness
a 192
of 8 mm,
intersection gap of 2 mm, four signals averaged, and an imaging time of 6.5 mmutes.
In
all
15 cases,
the
kidneys
and
the
renal mass were localized during suspended respiration with use of a singlesection GRE (fast low-angle shot [FLASH]) imaging sequence (30/10; flip angle, 40#{176}; 128 X 256 matrix; section thickness, onds). This
8 mm; imaging sequence was
time, selected
from
signal
intensity
of retroperitoneal
Interpretation
from
5 to 80 mm.
sities
of retroperitoneal medulla,
geneous),
renal
The
entire and
mass
mean
inten-
cortex
renal
mass
were
(if homo-
portion
measured.
ty curves were generated ratio of the mean signal
the
signal
fat, renal
enhancing
tissue studied fat. On isolated
of the
Time-intensiwith intensity
use
of the of the
to that of retroperitoneal images acquired during
dynamic
phase
of various
examina-
tions, we observed an apparent increase in the signal intensity of the mass relative to the appearance on the preceding or subsequent image; in each case, this ap-
to be related was
protocol
more
to breathing
prevalent
1 than
FLASH
imaging
was
per-
formed in one of two ways: FLASH protocol i (10 cases) consisted of five cycles of three consecutive 6-second images ob-
with
artifact,
with
FLASH
FLASH
protocol
J.K.T.L.,
J.J.B.) subjectively
Ti-weighted
sequence
2.
postcontrast spicuity.
GRE
images
Statistical
Analysis
compared with
the
the
pre-
for lesion
tamed
during
a 20-second
and
con-
10-second
images,
pause.
each
The
second
followed
by
flushing
with
protocol
re-
40 mL of normal
saline. Delayed FLASH images were obtained at 5, 7, 10, 12, and 15 minutes, followed by an incremental examination of the entire kidney with use of the singlesection FLASH sequence. The total examination time was 35-45 minutes. Radiology
#{149}
analyses
were
performed
independent
RESULTS
a
placed the first to shorten the apneic period and to improve patient cooperation. Imaging was begun during the 50-60-second intravenous infusion of Gd-DTPA (0.1 mmol/kg of body weight) (Schering, Berlin). This was immediately followed by rapid
statistical
use of a two-sample
test.
breath-holding
period, with each cycle followed by a 10second pause. FLASH protocol 2 (five cases) consisted of i5 individual 6-second single-breath
All
ty data
All patients completed the dynamic portion of the examination. Evaluation of the mean signal intensity of the retropenitoneal fat on the preand post-Gd-DTPA FLASH images (n = 15) demonstrated no change throughout the 15-minute study period. Detailed time-intensity curves showing the ratios of the mean signal intensities of the various tissues studied relative to the signal intensity of fat were generated without standard deviations (Figs 1-3). The Table pro-
a summary along
of the with
time-intensi-
the
standard
devi-
ations. Subjective assessment of the Tiweighted and pre- and postcontrast GRE images for lesion conspicuity demonstrated that contrast-enhanced GRE imaging was superior in 100% of cases. Comparison of the noncontrast GRE sequence with the Ti-weighted sequence showed it to be of equivalent value in 50% of cases, superior in 17% of cases, and inferior in 33% of cases. Parenchymal Patterns
Enhancement
Precontrast kidneys
Signal intensities were not measured from these isolated frames; excluded data constituted only 5% of the total measurements. In addition, three of us (S.S.E.,
with
fat.
vides
Objective assessment of the precontrast, dynamic, and delayed FLASH images was performed with use of operator-defined circular regions of interest that ranged
which
6 secbecause
obtained
in four.
Dynamic
334
MR
were
intensities
to the
peared
of its short imaging time and moderate Ti weighting. It produces images free of breathing artifact that optimally demonstrate contrast medium enhancement. The optimal imaging plane was then selected: coronal in six cases, transaxial in five, and sagittal
signal
normalized
and
Magnetom
SP unit (Siemens). The kidneys of 11 patients were first localized and examined with use of a Ti-weighted SE 500/15 (TR
Measurements
The mean
poma was diagnosed at CT on the basis of identification of a small amount of intratumoral fat.
MR
parenchyma.
without
FLASH
images
malignant
from neo-
plasms demonstrated the mean cortical signal intensity to be approximately 12% greaten than that of the medulla (P .057) (Fig 1). Cortical enhancement was brisk in all cases and peaked approximately 80 seconds after contrast material administration; peak cortical signal intensity was 190% greater than that of retropenitoneal fat. Cortical enhancement then gradually decreased throughout the remaining 15 minutes to 70% of its peak
value.
Medullany
enhance-
ment lagged behind that of the contex, becoming maximal and isointense at 120 seconds (P .56). For the remaining 1 1 minutes, the signal intensity of the medulla remained nearly constant, becoming slightly hypenintense relative to the cortex at 4 minutes (P = .18-.026) and demonstrating maximal contrast difference relative to cortex at 12 minutes (19%, P = .026). Renal
Cysts
Precontrast seven simple ed homogeneous
FLASH images of the renal cysts demonstratand relatively low August
1990
a.
Figure precontrast
4.
Selected
sagittal
image
shows
images
relative
from
a dynamic
hypointensity
ity of the cyst, which has no perceptible 190 seconds, the cortex and medulla are
wall nearly
b.
a.
ci-
C.
b. contrast-enhanced
of the cyst relative and does isointense.
not
display (d) At
MR
study
to the cortex. enhancement. 15 minutes,
the
of a patient
with
(b) Image
obtained
Peak cortical nonenhancing
a small
simple
renal
at 90 seconds
signal cyst
intensity remains
cyst
shows
occurred unchanged
(arrow).
increased
(a) The
conspicu-
at this time. (c) At and well defined.
d.
C-
Figure 5. Selected axial images from a dynamic contrast-enhanced MR study of a patient with a renal cell carcinoma with an enhancing rim. (a) The precontrast image shows the carcinoma as a centrally hypointense, largely exophytic cortical mass (arrow). (b) At 90 seconds, portions of the tumor rim (arrow) display enhancement similar to that of the adjacent renal cortex. (c) This pattern is maintained at 220 seconds with only minimal central enhancement. The renal medulla is isointense with the cortex. (d) At 15 minutes, the overall intensity (parenchyma and tumor) has decreased modestly. The central portion of the tumor (*), representing an area of coagulation necrosis, demonstrates only minimal interval enhancement.
Renal
signal intensity (approximately 75% of that of renal cortex [P = .008]). Examination of the time-intensity curves revealed no enhancement during the 15-minute imaging period (Figs 2, 4). Comparison with CT scans demonstrated agreement in size (average, 4.7 cm; range, 1.5-8.0 cm) and appearance of the cysts. In each case, Volume
176
Number
#{149}
2
the cyst was round; had smooth, imperceptible, nonenhancing walls; maintained a low signal intensity; and had a sharp interface with the surrounding renal panenchyma on postcontnast images. In every case, the conspicuity of the renal cyst became much greater after administration of Gd-DTPA.
Cell
Carcinomas
Precontrast FLASH imaging of the nine renal cell carcinomas demonstrated signal intensities similar to the intensity of renal cortex (P 1.0) (Table, Fig 2). Visual inspection of the renal cell carcinomas demonstrated three distinct enhancement patterns: (a) irregular peripheral enhancement with only minimal, heterogeneous central enhancement; (b) heterogeneous enhancement; and (c) mild homogeneous enhancement. Five cases demonstrated the first pattern, with some degree of enhancement of an irregular rim on periphery and with minimal heterogeneous enhancement of the more central portion (Fig 5). The average tumor size in this group was 5 cm (range, 3-8 cm). In each case, tumors that demonstrated regions of little to no contrast enhancement contained foci of pathologically proved coaguRadiology
335
#{149}
lation and/or liquefaction necrosis. Two cases demonstrated the second pattern of enhancement. Both were large tumors, measuring 8.0 and 8.5 cm in diameter, that lacked a clear margin with adjacent parenchyma and demonstrated patchy, hetenogeneous areas of brisk contrast enhancement intermixed with areas of minimal to no enhancement (Fig 6). In both cases enhancing tumor thrombus extended from the renal vein into the inferior vena cava. In the remaining two cases, mild homogeneous enhancement was depicted throughout the mass (Fig 7). The two tumors in this group were the smallest in the series, measuring 1 .5 and 2.5 cm in diameter. Both had irregulan margins with the surrounding panenchyma.
Oncocytoma
to that
throughout study period.
the
of renal
cortex
remainder
of the
The precontrast GRE images of the angiomyolipoma demonstrated fairly homogeneous signal intensity that was nearly isointense with surrounding cortex. The small amount of intratumoral fat cleanly identified at CT and SE MR imaging was almost mapparent. After administration of conmaterial, the enhancement and homogeneous and
was approxi-
mated that of renal cortex; however, the fat was completely obscured. The time to peak enhancement was 80 seconds, at which time the tumor was isointense with renal cortex. A decline in signal intensity followed this peak and closely paralleled that of renab cortex. Delayed images were not 336
Radiology
d.
Figure
6.
Selected
images
large, infiltrating, age demonstrates nephnic struction. less
collateral
(b) At
110
enhancement but
hypointense
nical
seconds,
still
areas
obtained
a dynamic
in this
(arrowheads) heterogeneous
than
in
the
heterogeneous
within
normal
due
have
MR
cell carcinoma.
to a tech-
problem.
involved
left
kidney.
Note
developed
in
response
to
(c)
kidney. of
the
left
Our
data
show
that
The
slower
have
aging
and
guished
can on
the
from
be reliably basis
renal neoGRE im-
distin-
of their
appear-
ance and enhancement pattern. Renal cortex follows a predictable pattern of brisk early enhancement, with a gradual decrease in intensity the
remainder
of the
15-mm-
ute imaging period. Early medullany enhancement lags behind that of the cortex but becomes isointense within the first few minutes. The medulla maintains its enhancement to a greater degree than does the cortex and becomes
slightly
hypenmntense
rela-
tive
to cortex after about 4 minutes. Contrary to other reports, we did not observe a period of early decreasing medullary signal intensity in normal kidneys, which has been thought
medullary
to be
related
to transient
superconcentration
of the
Gd-DTPA (13,17,18). This phenomenon may depend somewhat on technical factors, such as the imaging sequence (18), as well as the rapidity of
the
contrast
material
infusion
(17).
At
220
penvein
there
At
15
a
im-
is noted,
seconds, (d)
rate
material
obwith
has
been
minutes,
of infusion
used
may
document
simple
the renal
left kidney
kidney.
with
precontrast
the
in partially.
10 sec)
cysts behave differently plasms at contrast-enhanced
(a) The
of the
trast
DISCUSSION
of a patient
that right
filled
study
renal of the
enhancement
enhancement
the tumor
patient
contrast-enhanced
enhancing distortion
and
vessels
overall
progressive
from
heterogeneously enlargement
venous
during
Angiomyolipoma
trast brisk
b.
C.
The precontrast FLASH images of the oncocytoma demonstrated homogeneous signal intensity that was isointense with renal parenchyma (Figs 3, 8). Focal cortical expansion from this 5.5-cm mass was apparent. In addition, several small, high-signal-intensity foci that were isointense with renal hilar vessels were noted at the periphery; these foci represented enlarged capsular yessels. Enhancement with Gd-DTPA was brisk and homogeneous. In the 1st minute, the time-intensity curve fell between the curves of renal contex and medulla. The peak enhancement of the tumor occurred at 80 seconds after contrast administration, when the tumor was isointense with renal cortex. The signal intensity was similar
a.
explain this
shown
of con-
in our
our
event.
a loss
study
(60
inability
Several
of this
vs
to groups
medullany
phenomenon in the presence of significant renal disease, including hydronephrosis in humans (17,18) and chemically induced acute tubular nephrosis in the rabbit (19); this loss is thought to be due to a loss of medullary concentrating ability. To the best
of our neys
knowledge, we
the
studied
1 1 normal
were
free
kid-
of medical
and surgical renal disease: They were of normal size, were not obstructed, had distinct tions seen
corticomedullary at MR imaging,
and
juncwere
from patients with normal serum creatinine values. The seven simple renal cysts studied had several common features, including a precontrast signal intensities less than that of the surrounding parenchyma, sharp margins, or oval shape, imperceptible and lack of contrast material hancement. These criteria,
round wall, enwhich
have proved trast-enhanced
to be reliable CT, should
at conbe equally
reliable hanced
applied to contrast-enMR imaging.
The
when GRE
nine
demonstrated
renal
cell
several
carcinomas common
August
fea-
1990
a.
b.
d.
C.
Figure
7. Selected sagittal images from a dynamic contrast-enhanced MR examination of a patient with a small, homogeneously enhancing renal cell carcinoma (arrow) and a cyst (arrowhead). (a) The precontnast image demonstrates the hypointense cyst; however, the carcinoma is not apparent. (b) At 100 seconds, the carcinoma is clearly seen as an irregular, mildly enhancing cortical mass. The cyst increased in conspicuity but did not enhance. (C) At 200 seconds, the carcinoma continues to enhance minimally while the signal intensity of the medulla ap-
proaches
that
of the cortex.
(d) At
15
minutes,
the carcinoma
a.
remains
conspicuous,
with
irregular
margins.
hancement patterns of 16 renal carcinomas, little or no enhancement was found in seven cases (20). While our sample size is small, we believe that measurable enhancement is likely to be present in most renal carcinomas. Our increased sensitivity in the detection of enhancement may be due to higher field strength (1.0 vs 0.5 T), which increases the magnetic susceptibility artifact, as well as to shorter TE (iO vs 17 msec), which increases Ti weighting and, accordingly, the sensitivity to Gd-DTPA. Even in the absence of enhancement, the carcinomas in our series had sufficiently clear and identifiable features (eg, relatively high and often heterogeneous signal intensity and irregular margins) to place them in the indeterminate renal mass category. We did not specifically address the evaluation of indeterminate renal masses. Our anecdotal experience with the contrast-enhanced GRE MR technique in this category of renal masses has met with mixed success. In most cases, indeterminate renal
b.
masses
d.
C.
Figure
8.
patient
with
Selected
image
demonstrates
tense
oncocytoma
rowheads),
upper
ment
with
pole
images
renal two
in
the
pole
and
left lower
no
enhancement
mogeneously,
shows
similar
and right
enlarged
almost
tumor
from
cell carcinomas
left-sided
is seen
representing
right upper
coronal
multiple
to
mild the
a dynamic, (arrows) one right-sided
lower
feeder
pole
pole
vessels,
renal
(*).
contrast-enhanced MR examination of a and an oncocytoma. (a) The precontrast renal cell carcinoma. A nearly isoin-
Several
surround
high-signal-intensity this
cell carcinomas
of their
cortex.
(c)
At
(b)
mild while
The oncocytoma 210
seconds,
foci (an-
At 90 seconds,
centers,
enhancement.
surrounding
mass.
demonstrate
low-signal-intensity
heterogeneous
curvilinear
the
rim enhancethe
small
enhanced
left
ho-
enhance-
ment of the more central portions of the larger of the two renal cell carcinomas is depicted. The oncocytoma has become isointense with the renal parenchyma. (d) At 15 minutes, the renal cell carcinomas remain largely unchanged, while the oncocytoma has become mildly hypointense
relative
to
the
renal
parenchyma.
tunes:
(a) The precontrast signal intensity was similar to that of the surrounding parenchyma and was clearly greater than that of a simple cyst. (b) All lesions had irregular margins. (c) All
Volume
lesions
176
demonstrated
Number
#{149}
some
2
de-
The cyst did not enhance.
gree of contrast material enhancement. (d) All lesions became much more conspicuous after Gd-DTPA administration. In a previously published report, in which a similar technique was used to study the en-
had
enhanced wall, solid tenuation) firm
some
feature
at contrast-
CT (eg, thick on enhancing components, or high atthat we were able to con-
at contrast-enhanced
GRE
MR
imaging. These lesions still necessitate a biopsy or close follow-up. The precise role of the contrast-enhanced GRE MR imaging technique in this group of lesions remains to be determined. The MR imaging appearance of an oncocytoma has been described with use of SE techniques; one report descnibed a barge, encapsulation
necrotic (21), and
mass with another, a
smaller mass with a characteristic central scan (22). Our series includes what we believe to be the first oncocytoma
studied
trast-enhanced
with
GRE
the
use
of con-
MR imaging. Radiology
337
#{149}
The precontrast appearance was that of a homogeneous mass that was isointense with surrounding renal panenchyma. The enhancement pattern paralleled that of renal cortex, with the main difference being more rapid washout of the Gd-DTPA. The oncocytoma in our study was well defined and did not demonstrate central necrosis on scarring. Both CT and SE MR imaging are highly accurate in the diagnosis of angiomyolipoma (23,24). The contrast-enhanced GRE MR evaluation of the single angiomyolipoma included in our study highlighted the potential
shortcomings
of this
imag-
ing technique, including difficulty in the identification of small amounts of intratumoral fat and obscuration of fat after contrast material administration. The enhancement pattern demonstrated was nonspecific and did not provide additional information in this case; beyond that, the mass was solid and vascular. Although our study was not designed to compare the sensitivity of contrast-enhanced
GRE
MR
GRE
and
1.
HM,
Banner
Mulhern
CB,
differentiating nign
2.
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PH,
BC.
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ultrasonography
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RC,
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is cyst
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RJ, Melson
55.
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CL,
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and
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