DOI:10.2214/AJR.07.2696
AJR 2008; 190:1318-1323
© American Roentgen Ray Society
Effect of T1 Shortening on T2-Weighted MRI Sequences: Comparison of Hepatic Mass Conspicuity on Images Acquired Before and After Gadolinium Enhancement
Silvia D. Chang1 and
Ruedi F. Thoeni2
1 Department of Radiology, University of British Columbia, Vancouver Hospital
and Health Sciences Centre, 899 W 12th Ave., Vancouver, BC, Canada V5Z
1M9.
2 Department of Radiology, University of California at San Francisco, San
Francisco, CA.
Received June 7, 2007;
accepted after revision November 9, 2007.
Address correspondence to S. D. Chang
(Silvia.Chang{at}vch.ca).
Abstract
OBJECTIVE. The purpose of this study was to compare the conspicuity
of hepatic lesions on T2-weighted fast-recovery fast spin-echo MR images
obtained before and after administration of gadolinium.
MATERIALS AND METHODS. We reviewed T2-weighted fast-recovery fast
spin-echo images before and after gadolinium enhancement for 84 patients with
118 focal liver lesions. Solid lesions (22 hepatomas, seven ablated hepatomas,
12 metastatic lesions, six cases of focal nodular hyperplasia, five dysplastic
nodules, one adenoma) were proved pathologically or with multiple follow-up
studies. Nonsolid lesions were diagnosed as hemangiomas (n = 33) or
cysts (n = 32) on the basis of imaging features. Two blinded
radiologists interpreted the images independently, reading unenhanced images
first and gadolinium-enhanced images at least 2 weeks later. Lesion
conspicuity was ranked as follows: 1, poor; 2, moderate; 3, good; 4,
excellent. The sign test was used for qualitative scoring of imaging pairs
(unenhanced and gadolinium enhanced). The Fisher's exact test was used for
subgroup analysis of solid and nonsolid lesions.
RESULTS. On gadolinium-enhanced T2-weighted images, 21 (17.8%) of
118 of the lesions had improved conspicuity, 86 (72.9%) had no difference in
conspicuity, and 11 (9.3%) appeared worse. No statistically significant
difference was found between unenhanced and enhanced images (p =
0.11), but a trend toward improved conspicuity with gadolinium enhancement was
observed. Subgroup analysis showed that on gadolinium-enhanced T2weighted
images, visualization of solid hepatic lesions (28.3%) was significantly
better than that of nonsolid lesions (9.2%) (p = 0.01).
CONCLUSION. Compared with unenhanced T2-weighted images,
gadolinium-enhanced T2-weighted images had a trend toward improved conspicuity
of focal liver lesions. Subgroup analysis showed that visualization of solid
lesions benefited significantly more from use of gadolinium-enhanced
T2-weighted sequences than did visualization of nonsolid lesions.
Keywords: gadolinium • liver lesions • liver neoplasms • MRI • T2-weighted sequences
Introduction
T2-weighted MRI is considered essential for detecting and characterizing
focal hepatic lesions [1,
2]. Conventional T2-weighted
spin-echo sequences were initially used for this purpose and yielded good
lesion conspicuity. However, the long imaging times often resulted in
deterioration of image quality due to motion artifacts. These conventional
sequences have essentially been replaced by faster imaging sequences, such as
fast spinecho (FSE), single-shot FSE, and fast-recovery FSE
[3–8].
However, the multiple rapidly repeated refocusing radiofrequency pulses used
in breath-hold FSE sequences decrease the contrast between solid lesions and
the hepatic parenchyma owing to magnetization transfer saturation effects
[5,
9–11].
This effect occurs largely because the longer T1 of hepatic lesions compared
with hepatic parenchyma results in slower recovery after magnetization
transfer saturation.
Recovery from magnetization transfer saturation is faster in tissues with a
substantial amount of paramagnetic ions, as after IV administration of
gadolinium. The result is a reduction of the loss of signal intensity induced
by magnetization transfer. It therefore can be expected that solid lesions
with their larger in terstitial spaces and greater enhancement compared with
surrounding hepatic parenchyma on delayed gadolinium-enhanced images may have
improved conspicuity on T2-weighted FSE images obtained after administration
of gadolinium. This finding was made in a study with 21 patients in whom this
effect was detected in a qualitative and quantitative manner
[12]. The purpose of our study
was to compare the conspicuity of hepatic lesions on T2-weighted fast-recovery
FSE MR images obtained before administration of gadolinium with that on imag
es obtained after gadolinium administration.
Materials and Methods
This retrospective study was performed at two institutions. It was approved
by the institutional human ethics boards at both institutions and was HIPAA
compliant. Informed consent for review of the patients' records and images was
not required.
Subjects
Patients with focal hepatic lesions found on routine MRI of the liver that
included T2-weighted sequences before and after gadolinium enhancement were
entered into this study. Imaging was performed from July 14, 2003, to February
3, 2006. Only lesions that measured 1 cm or greater in diameter were analyzed.
Eighty-four patients (35 from one institution, 49 from the other institution)
fulfilled these criteria. Two patients had been excluded because they could
not tolerate completion of the examination. No patient was excluded because of
poor image quality. The mean age of the patients was 54 years (range,
18–78 years). There were 48 men and 36 women in the study.
There were a total of 132 lesions in the 84 patients. One hundred eighteen
(89.4%) of the 132 lesions were visible on T2-weighted images. The other 14
(10.6%) lesions were seen only on the dynamic gadolinium-enhanced images and
not on the T2-weighted images and therefore were excluded from the study.
Comparison between the unenhanced and gadolinium-en hanced T2-weighted images
was made for the 118 lesions. Proof of the lesions was determined by review of
the medical records in each case. Pathologic proof of the hepatic lesions was
based on findings at biopsy, examination of the surgical specimen, or autopsy.
Patients who had no patho logic proof of a hepatic lesion but underwent at
least two follow-up MRI or CT studies at intervals of approximately 6 months
also were included in the study.
The diagnoses of the 118 lesions are shown in
Table 1. Thirty-four of the
solid lesions were pathologically proven (14 hepatocellular carcinomas [HCCs],
12 metastatic lesions, five dysplastic nodules, two ablated HCCs, and one
hepatic adenoma). The diagnoses of the other 19 solid lesions were based on
clinical presentation and imaging features. Eight of these lesions were
presumed to be HCC on the basis of a positive serologic result for hepatitis
with or without an elevated 
-fetoprotein level. These eight lesions
were subsequently managed as HCC with radio frequency ablation, percutaneous
ethanol in jection, or chemoembolization. At the time of the study, five of
the 19 lesions had been ablated lesions because they were presumed HCC. Six
lesions were pre sumed focal nodular hyperplasia because of typical imaging
features and stability on follow-up imaging. All of the nonsolid lesions were
diagnosed on the basis of typical imaging features. One hemangioma was
confirmed at biopsy performed because the pa tient had hepatitis C and an
elevated -fetoprotein level.
For image analysis, HCC, metastatic lesions, focal nodular hyperplasias,
dysplastic nodules, and adenomas were classified as solid lesions. Heman
giomas and cysts were classified as nonsolid lesions. Heman giomas were
diagnosed on the basis of their typical imaging features of nodular
progressive enhance ment with IV contrast enhancement on MRI or CT and uniform
hyperechogenicity and increased through-transmission on sonography. Lesions
were considered cystic if there was no enhancement on MRI or CT and they had a
thin, smooth wall and exhibited posterior en hancement on sonography. These
cystic lesions were regarded as simple cysts if they also had homogeneously
high signal intensity on T2-weighted MR images and low signal intensity on
T1-weighted MR images and lacked internal echoes on sono graphic images. The
cystic lesions were dia gnosed as hemorrhagic if they had high signal
intensity on unenhanced T1-weighted MR images and had internal echoes on
sonographic images (n = 2).
MRI Technique
The MRI examinations were performed with a 1.5-T unit (Signa Horizon, GE
Healthcare) with a phased-array torso coil. A routine clinical MRI liver
protocol was used that was identical at the two institutions. Axial
T2-weighted fast-recovery FSE sequences (TR range/TE, 2,500–3,000/100;
echo-train length, 17; bandwidth, 32 kHz; field of view, 32–40
cm2; slice thickness, 5–6 mm with 1-mm gap; matrix size, 256
x 160; number of signals averaged, 1; average number of slices, 30) were
performed before and immediately after the gado linium-enhanced sequences. The
severity of flow-related artifacts was reduced by gradient-moment nulling in
the section-select axis and saturation bands superior and inferior to the
imaging volume. Fat signal intensity was suppressed by the addition of
frequency-selective fat-saturation pulses. The contrast agent gado diamide
(Omniscan, GE Healthcare) in a dose of 0.1 mmol/kg was ad ministered between
dynamic T1-weighted 3D vascular time-of-flight fast spoiled gradient-echo
(SPGR) sequences. Images were acquired before administration of gadolinium and
20 seconds and 1, 2, 3, and 5 minutes after administration (mini mum TR/TE,
195/4.2; flip angle, 20°; bandwidth, 31 kHz; field of view, 32–40
cm2; slice thickness, 6–8 mm with 50% overlap; matrix size,
320 x 160; number of signals averaged, 0.5). Additional sequences not
used in the analysis included axial SPGR T1-weighted in- and out-of phase
sequences (90–150/4.2 and 2.1; flip angle, 70°; bandwidth, 16 kHz;
field of view, 32–40 cm2; slice thickness, 8 mm with 1-mm
gap; matrix size, 256 x 128–192; number of signals averaged, 1)
and coronal T2-weighted single-shot FSE sequences (infinite/100; echo-train
length, 100+; bandwidth, 62.5 kHz; field of view, 32–40 cm2;
slice thickness, 6 mm with 1-mm gap; matrix size, 256 x 160–192;
number of signals averaged, 0.5; no fat suppres sion). Axial T2-weighted
single-shot FSE se quences (infinite/100; echo-train length, 100+; bandwidth,
62.5 kHz; field of view, 32–40 cm2; slice thickness, 6 mm
with 1-mm gap; matrix size, 256 x 160–192; number of signals
averaged, 0.5; no fat suppression) also were performed before and after
gadolinium enhancement.
Image Analysis
Two blinded radiologists, both unaware of the patient's history, analyzed
the MR images. To avoid bias, each radiologist read only images from the other
institution. For the first reading, only T2-weighted images obtained before
gadolinium administration were analyzed for each patient. Then all images
except the T2-weighted images obtained after gadolinium enhancement were
interpreted to further characterize the lesion and to detect any lesions seen
only on the gadolinium-enhanced images and not on the unenhanced T2-weighted
images. In the second set of interpretations, which was separated by at least
2 weeks from the initial reading, the T2-weighted images obtained after
gadolinium enhancement were interpreted alone and then compared with the
T2-weighted images obtained before gadolinium administration. Finally, all
images were interpreted together. Lesion conspicuity was ranked on the
following scale: 1, poor; 2, moderate; 3, good; 4, excellent. When a rank of 1
on unenhanced T2-weighted images changed to 2 or 3 on gadolinium-enhanced
images or if the rank on unenhanced images changed from 2 to 3, diagnostic
confidence was considered increased and thus was recorded. Size and location
of the lesion also were recorded. We did not analyze the T2-weighted
single-shot FSE images for lesion conspicuity because the sequence is not
ideal for detecting hepatic lesions and is used mainly to assess anatomic
features in the clinical setting.
Statistical Analysis
Statistical analysis was performed with Stata statistical software (version
9.0, StataCorp). The alpha level was set at p = 0.05 for all tests.
The qualitative scoring of imaging pairs (T2-weighted images alone before gado
linium administration and T2-weighted images alone after gadolinium
administration) was evaluated with the sign test. Subgroup analysis of solid
and nonsolid lesions was performed with Fisher's exact test. Lesion
conspicuity rank and size of the lesions were assessed with the Kruskal-Wallis
test.
Results
The results of the qualitative analysis of lesion conspicuity on the
T2-weighted unenhanced images compared with the gadolinium-enhanced
T2-weighted images are shown in Table
2. There was no statistically significant difference between
unenhanced and gadolinium-enhanced images (p = 0.11, sign test), but
there was a trend toward improved visualization on gadolinium-enhanced images.
Examples are shown in Figures
1A,
1B,
2A,
2B,
3A,
3B,
4A,
4B.
Table 3 shows the lesion
conspicuity results with the lesions organized into the subgroups, solid and
nonsolid lesions. The subgroup of solid lesions had better conspicuity on
gadolinium-enhanced than on unenhanced T2-weighted images. This finding was
statistically significant for both readers (p = 0.01, Fisher's exact
test). In evaluation of five of 15 solid lesions, the readers considered their
diagnostic confidence increased with the gadolinium-enhanced T2-weighted
images. Table 4 shows the
conspicuity of the subtypes of solid lesions. There was no statistically
significant correlation between lesion conspicuity and lesion size
(Fig. 5). Although there
appeared to be a trend toward smaller lesions in the worse conspicuity group,
the Kruskal-Wallis test showed the difference was not significant (p
= 0.22).
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TABLE 2: Results of Qualitative Analysis of Lesion Conspicuity on T2-Weighted
Fast-Recovery Fast Spin-Echo Images Before and After Gadolinium
Enhancement
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Fig. 1A —55-year-old woman with hepatocellular carcinoma
(arrow). Fast-recovery fast spin-echo T2-weighted MR images before
(A) and after (B) administration of gadolinium. B was
rated as having better lesion conspicuity.
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Fig. 1B —55-year-old woman with hepatocellular carcinoma
(arrow). Fast-recovery fast spin-echo T2-weighted MR images before
(A) and after (B) administration of gadolinium. B was
rated as having better lesion conspicuity.
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Fig. 2A —39-year-old man with hemangioma of liver (arrow).
Fast-recovery fast spin-echo T2-weighted images before (A) and after
(B) administration of gadolinium. B was rated as having better
lesion conspicuity.
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Fig. 2B —39-year-old man with hemangioma of liver (arrow).
Fast-recovery fast spin-echo T2-weighted images before (A) and after
(B) administration of gadolinium. B was rated as having better
lesion conspicuity.
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Fig. 3A —56-year-old man with hepatocellular carcinoma
(arrow). Fast-recovery fast spin-echo T2-weighted images before
(A) and after (B) administration of gadolinium. Images were
rated as having same lesion conspicuity.
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Fig. 3B —56-year-old man with hepatocellular carcinoma
(arrow). Fast-recovery fast spin-echo T2-weighted images before
(A) and after (B) administration of gadolinium. Images were
rated as having same lesion conspicuity.
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Fig. 4A —59-year-old man with hepatocellular carcinoma
(arrow). Fast-recovery fast spin-echo T2-weighted images before
(A) and after (B) administration of gadolinium. A was
rated as having better lesion conspicuity.
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Fig. 4B —59-year-old man with hepatocellular carcinoma
(arrow). Fast-recovery fast spin-echo T2-weighted images before
(A) and after (B) administration of gadolinium. A was
rated as having better lesion conspicuity.
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View this table:
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TABLE 3: Conspicuity of Solid and Nonsolid Lesions on T2-Weighted Fast-Recovery
Fast Spin-Echo Images Before and After Gadolinium Enhancement
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TABLE 4: Conspicuity of Solid Lesions on T2-Weighted Fast-Recovery Fast Spin-Echo
Images Before and After Gadolinium Enhancement
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Fig. 5 —Distribution of lesion size and conspicuity of lesions on
gadolinium-enhanced T2-weighted fast-recovery fast spin-echo MR images. Graph
shows no correlation between lesion conspicuity and lesion size (p =
0.22, Kruskal-Wallis test). Each dot represents lesion.
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Discussion
Our overall results show no significant difference between the conspicuity
of lesions on T2-weighted fast-recovery FSE images obtained before gadolinium
enhancement and the conspicuity on images obtained with the same sequence
after enhancement. In a subgroup analysis, however, we did find a significant
difference in the conspicuity of solid lesions but not of hemangiomas and
cysts. These results are similar to those of a smaller study by Jeong et al.
[12] that involved 21 patients
with 58 lesions. In that study, 48 of the lesions were solid and 10 were
hemangiomas or cysts. We analyzed 53 solid and 65 nonsolid lesions. Although
the number of solid lesions was similar, we included more nonsolid lesions
(cavernous hemangiomas and cysts). Unlike solid lesions and the hepatic
parenchyma, nonsolid lesions do not lose signal intensity because of
magnetization transfer effects in T2-weighted fast-recovery FSE sequences
[13]. This fact likely
explains the lack of increased conspicuity of nonsolid lesions in the subgroup
analysis. It is difficult to compare our results directly with those of Jeong
et al. because the scoring systems were different in the two studies. We
qualified the conspicuity of each lesion as better, the same, or worse in
comparisons of unenhanced and gadolinium-enhanced images, whereas Jeong et al.
used a 4-point scoring system and reported only the mean score.
Most of the solid lesions in our study were HCC (n = 22) and
metastatic lesions (n = 12). A greater percentage of metastatic
lesions (6/12, 50%) than HCCs (6/22, 27.3%) had improved conspicuity on
enhanced images. One explanation for this result is that metastatic lesions
tend to have larger extracellular spaces and therefore take up more gadolinium
and remain enhanced on delayed images. In contrast, most HCCs tend to be
vascular in the arterial phase of MRI and exhibit washout on subsequent phases
[14,
15]. Among the cases of focal
nodular hyperplasia, dysplastic nodules, and adenoma, only three of 12 lesions
had greater conspicuity on gadolinium-enhanced images. This finding may
reflect gadolinium washout after 5 minutes in focal nodular hyperplasia and
adenoma and absence of substantial enhancement of dysplastic nodules with
subsequent absence of greater conspicuity on gadolinium-enhanced images.
None of the seven ablated HCC lesions had improved conspicuity on the
T2-weighted contrast-enhanced images. Six of these lesions had no difference,
and one lesion had worse lesion conspicuity on gadolinium-enhanced images. The
worse conspicuity may have been due to artifacts. The lack of improvement in
conspicuity of ablated lesions on gadolinium-enhanced images is to be expected
because these lesions consist of nonviable tissue or tissue affected by
liquefaction, which does not become enhanced with gadolinium and therefore
would not show a reduction in signal intensity loss induced by magnetization
transfer. If these ablated lesions are removed from the final analysis of
solid lesions, the conspicuity of solid lesions on gadolinium-enhanced
T2-weighted images improves from 28.3% to 32.6% (15/46).
We cannot explain why 11 (9%) of the 118 lesions appeared worse on
gadolinium-enhanced T2-weighted images than on unenhanced images. There is no
correlation with the type of lesion (solid vs nonsolid) because essentially
one half (six) of the lesions were solid (three HCC, one dysplastic nodule,
one ablated HCC, one case of focal nodular hyperplasia) and the other
approximately one half (five) were nonsolid (hemangiomas). One explanation may
be that the gadolinium-enhanced T2-weighted images were of inferior quality
because they were obtained at the end of the examination, when images are
prone to motion artifacts. Nine of these 11 cases, including the cases of
ablated HCC, had more motion artifacts on the contrast-enhanced images than on
the unenhanced images. There was no clear difference in motion artifacts
between the unenhanced and gadolinium-enhanced images in the other two cases.
Another explanation may be the qualitative subjective nature of the assessment
performed with two separate readings. One reason that hemangiomas might have
appeared worse on the gadolinium-enhanced T2-weighted images is the
possibility of pooling of contrast material within these lesions, leading to
T2 shortening compared with the unenhanced images. Even though it would be
expected that smaller lesions would be better seen on gadolinium-enhanced
T2-weighted images whereas larger lesions would be readily detected anyway, no
statistically significant correlation between lesion conspicuity and lesion
size was found in our study.
In our study, gadolinium-enhanced T2-weighted images did not depict new
lesions that were not visible on the unenhanced T2-weighted images. The
gadolinium-enhanced images, however, did have improved conspicuity for solid
lesions, which led to increased diagnostic confidence in 33.3% of these cases.
Because we had only a small number of cases, analysis of a larger series is
needed to confirm this point.
There were limitations to this study. To avoid bias the two radiologists
interpreted only cases from the other institution, thus interobserver
variability was not assessed. In addition, not all of the lesions had
pathologic proof, and we had to rely on follow-up CT or MRI and serologic
results. Finally, eliminating the T1-weighted SPGR images obtained at the
5-minute delay might have reduced washout of gadolinium and improved
conspicuity on the gadolinium-enhanced T2-weighted images.
Gadolinium-enhanced T2-weighted fast-recovery FSE images had a trend toward
improved conspicuity of focal hepatic lesions compared with unenhanced
T2-weighted fast-recovery FSE images. Subgroup analysis showed that this
finding was statistically significant for solid lesions. In the assessment of
focal hepatic lesions, we recommend acquisition of T2-weighted images after
gadolinium administration. Because 14 lesions seen on dynamic
gadolinium-enhanced images were not seen on T2-weighted images, use of
gadolinium-enhanced T2-weighted sequences may optimize diagnosis for patients
who cannot tolerate an entire MRI examination.
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Abstract
Introduction
