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Multi-shot echo-planar Flair imaging of brain tumors: comparison of spin-echo T1-weighted, fast spin-echo T2-weighted, and fast spin-echo Flair imaging
Computerized Medical Imaging and Graphics PERGAMON
Computerized Medical Imaging and Graphics 26 (2002) 65±72
www.elsevier.com/locate/compmedimag
Multi-shot echo-planar Flair imaging of brain tumors: comparison of spin-echo T1-weighted, fast spin-echo T2-weighted, and fast spin-echo Flair imaging Noriaki Tomura*, Koki Kato, Satoshi Takahashi, Ryuji Sashi, Jun-ichi Izumi, Komei Narita, Jiro Watarai Department of Radiology, Akita University School of Medicine, 1-1-1 Hondo, Akita City, Akita, 010-8543, Japan Received 19 July 2001; revised 11 October 2001; accepted 11 October 2001
Abstract Multi-shot echo-planar ¯uid-attenuated inversion-recovery (EPI-Flair) was compared with spin-echo T1-weighted (SE-T1W), fast SE T2weighted (FSE-T2W), and fast Flair (F-Flair) in imaging brain tumors. In 32 patients with various different brain tumors, three reviewers independently evaluated image quality. Two reviewers evaluated the image quality of precontrast EPI-Flair to be signi®cantly better than that of precontrast SE-T1W. Two reviewers evaluated the image quality of postcontrast EPI-Flair as superior to that of postcontrast SE-T1W. Artifacts on postcontrast EPI-Flair were signi®cantly more prominent than those on postcontrast F-Flair. Multi-shot EPI-Flair appeared to be superior to SE-T1W, and almost equivalent to FSE-T2W in terms of image quality. q 2002 Elsevier Science Ltd. All rights reserved. Keywords: MR imaging; Echo-planar imaging; Fluid-attenuated inversion-recovery imaging; Brain; Neoplasms
Fluid-attenuated inversion-recovery (Flair) sequences provide good contrast between the white matter and cerebrospinal ¯uid (CSF) due to CSF nulling with heavily T2-weighted imaging (T2W) [1±4]. The usefulness of Flair sequences has been demonstrated in various different diseases of the brain, including infarct [2,3,5] subarachnoid hemorrhage [2,6], demyelinating diseases [1±5,7±9] in¯ammatory diseases [4,5], and neoplasms [2,5,10]. Most of these reports suggested the superiority of Flair for detecting cortical lesions and lesions located in the peripheral subcortical or periventricular regions [1,7,11,12]. Although the major disadvantage of Flair sequences is its prolonged acquisition time, a fast Flair sequence [1,3] imaging modality by combining Flair with fast spin-echo sequence imaging was developed. Echo-planar imaging (EPI) is a rapid imaging technique, which is capable of further shortening of the acquisition time. The EPI technique is currently used for functional MRI [13], perfusion studies, and diffusion studies [14]. Single-shot EPI is capable of producing more than 10 images a second [15], but has a major disadvantage of marked susceptibility artifacts near the skull base. EPI with a multi-shot technique [4] is also a fast imaging * Corresponding author. Tel.: 181-188-34-1111; fax: 181-188-36-2623. E-mail address: [email protected] (N. Tomura).
technique, and it is more promising for higher resolution imaging than single-shot EPI. The purpose of this investigation was to determine whether EPI-Flair with a multi-shot technique could replace T1-weighted images with conventional SE sequence (SET1W), T2-weighted images with fast SE sequence (FSET2W), and fast Flair (F-Flair) images. 1. Materials and methods The brains of 32 consecutive patients with brain tumors were prospectively imaged on a clinical 1.5-T imager. All patients underwent EPI-Flair before and/or after contrast administration to compare EPI-Flair with other sequences. All tumors were diagnosed by removal of the tumor or biopsy after MR examinations. The tumors analyzed were ®ve glioblastomas, six malignant astrocytomas, one malignant oligodendroglioma, one oligodendroglioma, one pilocytic astrocytoma, three medulloblastomas, three germinomas, two central neurocytomas, three malignant lymphomas, two leukemic masses and ®ve metastatic tumors. All MR examinations were performed with the use of a standard head coil. Axial images were obtained parallel to the plane including both the anterior commissure and posterior commissure. Twenty-two slices with 4 mm in thickness
0895-6111/02/$ - see front matter q 2002 Elsevier Science Ltd. All rights reserved. PII: S 0895-611 1(01)00039-8
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Table 1 Parameters of each sequence (EPI-Flair, multishot echo-planar ¯uid attenuated inversion recovery; SE-T1W, spin-echo T1-weighted imaging; FSE-T2W, fast spin-echo T2-weighted imaging; TI, inversion time; TR, time of repetition; TEeff, effective echo time; FOV, ®eld of view)
EPI-Flair SE-T1W FSE-T2W
TI (ms)
TR/TEeff (ms)
FOV (mm)
Matrix
Acquisition
Number of shots
Imaging time
2000
8000/100 300±540/8±14 4000±5000/90±110
180±220 180±220 180±220
256 £ 192 256 £ 224/256 £ 256 256 £ 256
1 2 2
8
1 min 8 s 2 min 14 s±4 min 2 s 2 min 8 s±3 min 34 s
were obtained. Table 1 summarizes several parameters in each sequence. Prior to administration of contrast material, axial EPI-Flair n 11; SE-T1W n 11; FSE-T2W n 11; and F-Flair n 9 were performed. After administration of gadopentetate dimeglumine (0.1 mmol/kg of body weight), axial EPI-Flair n 21; SE-T1W n 19; and F-Flair n 21 were performed in random order. Three neuroradiologists who were aware of only the clinical diagnosis independently assessed the image quality of each sequence. Image quality was assessed by lesion conspicuity, margin de®nition, and delineation of edema [16,17]. A fourpoint grading system (0, insuf®cient; 1, suf®cient; 2, good; 3, excellent) was employed. Moreover, for evaluating the presence of artifacts, a similar score (0, marked; 1, moderate; 2, mild; 3, none) was used [17]. The statistical signi®cance of differences with image quality and the presence of artifacts were determined with the Wilcoxon signed-ranks test. A p-value of 0.01 or less was considered signi®cant.
EPI-Flair (2) more clearly revealed lesion conspicuity, delineation of edema, and margin de®nition (Fig. 1) than SE-T1W (2). There were no signi®cant differences between FSE-T2W and EPI-Flair (2). Precontrast F-Flair (F-Flair (2)) was graded as being signi®cantly superior to EPIFlair (2) by radiologist 1. After administration, radiologists 2 and 3 evaluated postcontrast EPI-Flair (EPI-Flair (1)) as being signi®cantly superior to postcontrast SE-T1W (SET1W (1)) (Figs. 2 and 3). With regard to the presence of artifacts, a signi®cant difference was observed between postcontrast F-Flair (F-Flair (1)) and EPI-Flair (1) by all radiologists (Table 3). The presence of artifacts of SE-T1W (2), FSE-T2W, F-Flair (2), or SE-T1W (1) did not show a signi®cant difference compared with that of EPI-Flair (2) or EPI-Flair (1) (Table 3). In a patient with residual tumor after surgery, parenchymal hemorrhage was seen more clearly in EPI-Flair than in the other sequences, however, its remarkable hypointensity was not distinguishable from the intensity of CSF.
2. Results
3. Discussion
The results for image quality are shown in Table 2. Prior to administration of contrast material, precontrast EPI-Flair (EPI-Flair (2)) was evaluated to be signi®cantly better than precontrast SE-T1W (SE-T1W (2)) by radiologists 2 and 3.
In the present study, EPI-Flair produced better images than SE-T1W (2) or SE-T1W (1) according to the evaluation of lesion conspicuity, margin de®nition, and delineation of edema for all radiologists. The presence of artifacts seen
Table 2 Mean score of image quality (SE-T1W (2), precontrast SE-T1W; F-Flair (2), precontrast Flair; EPI-Flair (2), precontrast EPI-Flair; SE-T1W (1), postcontrast SE-T1W; F-Flair (1), postcontast fast Flair; EPI-Flair (1), postcontrast EPI-Flair) n
Mean ^ SD
SE-T1W (2) vs EPI-Flair (2)
11
SE-T1W (2) EPI-Flair (2)
FSE-T2W vs EPI-Flair (2)
11
FSE-T2W EPI-Flair (2)
F-Flair (2) vs EPI-Flair (2)
9
F-Flair (2) EPI-Flair (2)
SE-T1W (1) vs EPI-Flair (1)
19
SE-T1W (1) EPI-Flair (1)
F-Flair (1) vs EPI-Flair (1)
21
F-Flair (1) EPI-Flair (1)
Radiologist 1
Radiologist 2
Radiologist 3
1.5 ^ 0.8 2.1 ^ 0.6 p , 0.05 2.3 ^ 0.9 2.2 ^ 0.6 ns 3.0 ^ 0 2.2 ^ 0.4 p , 0.01 1.7 ^ 0.7 2.2 ^ 0.7 p , 0.05 2.8 ^ 0.4 2.2 ^ 0.7 p , 0.01
1.2 ^ 0.6 2.5 ^ 0.5 p , 0.01 1.9 ^ 0.5 2.5 ^ 0.5 ns 2.9 ^ 0.3 2.4 ^ 0.5 ns 1.2 ^ 0.6 2.3 ^ 0.5 p , 0.01 2.7 ^ 0.5 2.3 ^ 0.5 ns
1.5 ^ 0.7 2.7 ^ 0.5 p , 0.01 2.3 ^ 0.9 2.7 ^ 0.5 ns 3.0 ^ 0 2.7 ^ 0.5 ns 1.6 ^ 0.8 2.3 ^ 0.5 p , 0.01 2.9 ^ 0.4 2.3 ^ 0.5 p , 0.01
N. Tomura et al. / Computerized Medical Imaging and Graphics 26 (2002) 65±72
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Fig. 1. A 61-year old man with a neurocytoma involving the corpus callosum. FSE-T2W TR=TE=excitations 4000=107=2 (A), precontrast F-Flair (TR=TE=excitations 10 002=150=1; TI 2200) (B), and precontrast EPI-Flair (TE=excitations 100=1; TI 2000) (C) more clearly differentiate the tumor from the peritumoral edema than precontrast SE-T1W TR=TE=excitations 300=10=2 (D). Arrows indicate the tumor.
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N. Tomura et al. / Computerized Medical Imaging and Graphics 26 (2002) 65±72
Fig. 2. An 11-year old boy with a malignant astrocytoma involving the cerebellar vermis. Postcontrast F-Flair (TR=TE=excitations 10 002=147=1; TI 2200) (A), and postcontrast EPI-Flair (TE=excitations 100=1; TI 2000) (B) more clearly de®ned the margin of the tumor than postcontrast SE-T1W TR=TE=excitations 519=10=2 (C). Arrows indicate the tumor in the cerebellar vermis.
N. Tomura et al. / Computerized Medical Imaging and Graphics 26 (2002) 65±72
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Fig. 3. A 67-year old woman with a malignant astrocytoma involving the cerebellar vermis and hemisphere. Postcontrast F-Flair (TR=TE=excitations 8002=150=1; TI 2000) (A), and postcontrast EPI-Flair (TE=excitations 100=1; TI 2000) (B) more clearly de®ned the margin of the tumor than postcontrast SE-T1W TR=TE=excitations 300=10=2 (C). Arrows indicate the tumor in the cerebellum. Artifacts are more prominent in postcontrast T1W than in postcontrast F-Flair and EPI-Flair.
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on the EPI-Flair (2) was more prominent that on the SET1W (2), while more prominent artifacts were observed on SE-T1W (1) compared with EPI-Flair (1). EPI-Flair appears to represent an alternative to SE-T1W for the depiction of brain tumors. Although artifacts on the EPI-Flair were more prominent than those on FSE-T2W, the mean scores for image quality did not differ signi®cantly between FSE-T2W and EPI-Flair. This indicates that FSE-T2W can be replaced by EPI-Flair to reduce the imaging time in unstable or uncooperative patients. F-Flair (1) was better than EPI-Flair (1) according to the evaluation of image quality of two of the three radiologists, and artifacts were signi®cantly more prominent on EPI-Flair (1) than on FFlair (1) according to every radiologist. This result showed that EPI-Flair could not replace F-Flair on the basis of its ability to depict the tumor. However, F-Flair sequences require approximately 4 min of acquisition time, which is more than three times the acquisition time of EPI-Flair. EPIFlair is also useful in unstable or uncooperative patients because of its short acquisition time. Single-shot EPI is a much faster imaging modality than the multi-shot EPI used in the present study. The acquisition time of single shot EPI is several seconds for the entire brain. However, susceptibility artifacts, which is much more prominent than those on the multi-shot EPI, disturbs the imaging of lesions near the skull base. Korogi et al. [15] compared single-shot EPI-Flair with F-Flair in the detection of various brain lesions. Their results showed that single-shot EPI-Flair provided almost equivalent tissue contrast and CSF suppression as F-Flair, but a susceptibility to artifacts at the skull base and posterior to the frontal sinus degrades its quality. Single-shot EPIFlair, used in their study, has a shortened imaging time as fast as 4 s, and can reduce motion artifacts. Single-shot EPIFlair is also useful in screening for supratentorial lesions. Bruning et al. [10] compared echo-planar T2W (EPI-T2W)
with SE-T2W for the depiction of intra-axial brain tumors, and reported that EPI-T2W produce images of a suf®cient quality to depict intra-axial brain tumors. They used doubleshot EPI, of which the acquisition time was within 25 s. However, their study did not include patients with an infratentorial tumor. On the double-shot EPI, severe susceptibility artifacts were found in the posterior fossa and in the sections of the brain adjacent to the skull base. Susceptibility artifacts on the multi-shot EPI could be further reduced compared with those on single shot EPI. Simonson et al. [4] reported that multi-shot EPI-Flair was a practical and ef®cient means of screening the entire brain. They mentioned that increased sensitivity to susceptibility effects could be clinically useful in detecting minute areas of hemorrhage, cavernous angioma, shear injury, and contusion. In particular, hemorrhage may go undetected on fast spin-echo SE-T1W or Flair images, because susceptibility effects are decreased in fast spin-echo sequences. EPI sequences are useful in detecting subtle calci®cation. This increased sensitivity to susceptibility effects of EPI-Flair may provide more information than other sequences, which should prove useful in the differential diagnosis of a tumor. Eight-shot EPI, used in the present study, reduces artifacts near the skull base, and at the bone and air interfaces. Multi-shot EPI-Flair used in the present study suffers less image degradation due to susceptibility artifacts, although the acquisition time to cover the entire brain was 68 s. There are some limitations to the present study. Firstly, three independent reviewers evaluated lesion conspicuity and the degree of artifacts qualitatively. However, each reviewer was able to identify which image was a Flair sequence. This likely somewhat biased the study. Calculation of sensitivity and speci®city was not performed due to an absence of controls. A quantitative analysis is necessary
Table 3 Overall assessment of artifacts (SE-T1W (2)), FSE-T2W, F-Flair (2), EPI-Flair (2), SE-T1W (1), F-Flair (1), and EPI-Flair (1), the same as those in the Table 2) n
Mean ^ SD
SE-T1W (2) vs EPI-Flair (2)
11
SE-T1W (2) EPI-Flair (2)
FSE-T2W vs EPI-Flair (2)
11
FSE-T2W EPI-Flair (2)
F-Flair (2) vs EPI-Flair (2)
9
F-Flair (2) EPI-Flair (2)
SE-T1W (1) vs EPI-Flair (1)
19
SE-T1W (1) EPI-Flair (1)
F-Flair (1) vs EPI-Flair (1)
21
F-Flair (1) EPI-Flair (1)
Radiologist 1
Radiologist 2
Radiologist 3
2.8 ^ 0.4 2.5 ^ 0.7 ns 3^0 2.5 ^ 0.7 p , 0.05 3^0 2.7 ^ 0.5 p , 0.05 2.4 ^ 1.1 2.1 ^ 0.9 ns 2.8 ^ 0.4 2.1 ^ 0.8 p , 0.01
2.9 ^ 0.3 2.4 ^ 0.5 p , 0.05 3^0 2.5 ^ 0.8 p , 0.05 3^0 2.6 ^ 0.7 ns 2.6 ^ 0.8 1.9 ^ 0.8 p , 0.05 2.8 ^ 0.4 2.0 ^ 0.8 p , 0.01
2.8 ^ 0.4 2.4 ^ 0.8 p , 0.05 2.9 ^ 0.3 2.4 ^ 0.5 ns 2.9 ^ 0.3 2.3 ^ 0.5 p , 0.05 2.6 ^ 0.8 2.2 ^ 0.8 p , 0.05 2.9 ^ 0.3 2.1 ^ 0.8 p , 0.01
N. Tomura et al. / Computerized Medical Imaging and Graphics 26 (2002) 65±72
for further studies. Comparison of multi-shot EPI-Flair with single-shot EPI-Flair should be performed in future research. The relationship between the number of shots and the image quality should also be evaluated. There have been a few reports concerning contrast enhancement on Flair images after the administration of contrast medium [18,19]. Contrast enhancement is seen because the signal intensity of Flair is partially dependent of T1 [19]. The inversion pulse in Flair sequences might introduce T1 weighting. A preliminary report by Tsuchiya et al. [19] showed that contrast enhancement on postcontrast Flair images was comparable to that seen on SE-T1W (1) in patients with intracranial tumors. In the present study, EPIFlair was performed before and after the administration of contrast medium only in two patients. EPI-Flair showed almost an equivalent degree of contrast enhancement as SE-T1W. Flair images have the advantages of both T2W and T1W for tissue contrast. The usefulness of Flair sequences has also been reported in other diseases of the central nervous system, such as infarction [2,3,5], subarachnoid hemorrhage [2,6], and multiple sclerosis [1,4,9,16]. Simonson et al. [4] showed the superiority of EPI-Flair in several cases with demyelinating disease or infection. Lesions immediately adjacent to ventricles or cortical sulci could be overlooked or mistaken for partial volume effects on SE- or FSE-T2W. They presented a case of septic emboli of which multiple lesions at the gray±white matter junction could not be demonstrated by T2W, but could be by EPI-Flair. The superiority of EPI-Flair over conventional SE images in the depiction of herpes simplex encephalitis has also been established. In the present study, EPI-Flair was superior to T1W sequences in our criteria. However, T1W images are used to produce high quality anatomic images and to provide information concerning the presence of substances that shorten T1. To replace a T1W sequence with EPI-Flair may limit information available from MR. Further studies on various other diseases should be done to compare EPI-Flair with SE or FSE sequences. In conclusion, this study showed that multi-shot EPI-Flair appeared to be superior to SE-T1W, and almost equivalent to FSE-T2W in terms of its ability to depict tumors. This sequence could be valid not only for tumors in the supratentorial region but also for those in the infratentorial region. Compared with F-Flair, multi-shot EPI-Flair cannot replace F-Flair, but it can reduce acquisition time. This sequence is also useful for uncooperative patients due to its short imaging time. 4. Summary EPI with a multi-shot technique is also a fast imaging technique, and it is more promising for higher resolution imaging than single-shot EPI. The purpose of this investigation was to determine whether EPI-Flair with a multi-shot technique could replace T1-weighted images with conventional SE
71
sequence (SE-T1W), T2-weighted images with fast SE sequence (FSE-T2W), and fast Flair (F-Flair) images. The brains of 32 consecutive patients with brain tumors were prospectively imaged on a clinical 1.5-T imager. All patients underwent EPI-Flair before and/or after contrast administration to compare EPI-Flair with other sequences. All tumors were diagnosed by removal of the tumor or biopsy after MR examinations. The tumors analyzed were ®ve glioblastomas, six malignant astrocytomas, one malignant oligodendroglioma, one oligodendroglioma, one pilocytic astrocytoma, three medulloblastomas, three germinomas, two central neurocytomas, three malignant lymphomas, two leukemic masses and ®ve metastatic tumors. Prior to administration of contrast material, axial EPI-Flair n 11; SET1W n 11; FSE-T2W n 11; and F-Flair n 9 were performed. After administration of contrast material, axial EPI-Flair n 21; SE-T1W n 19; and F-Flair n 21 were performed in random order. Three neuroradiologists who were aware of only the clinical diagnosis independently assessed the image quality of each sequence. Image quality was assessed by lesion conspicuity, margin de®nition, and delineation of edema. A four-point grading system (0, insuf®cient; 1, suf®cient; 2, good; 3, excellent) was employed. Moreover, for evaluating the presence of artifacts, a similar score (0, marked; 1, moderate; 2, mild; 3, none) was used. Prior to administration of contrast material, precontrast EPI-Flair (EPI-Flair (2)) was evaluated to be signi®cantly better than precontrast SE-T1W (SE-T1W (2)) by two radiologists. EPI-Flair (2) more clearly revealed lesion conspicuity, delineation of edema, and margin de®nition than SE-T1W (2). There were no signi®cant differences between FSE-T2W and EPI-Flair (2). Precontrast F-Flair (F-Flair (2)) was graded as being superior to EPI-Flair (2) by one radiologist. After administration, two radiologists evaluated postcontrast EPI-Flair (EPI-Flair (1)) as being superior to postcontrast SE-T1W (SE-T1W (1)). With regard to the presence of artifacts, a signi®cant difference was observed between postcontrast F-Flair (F-Flair (1)) and EPI-Flair (1) by all radiologists. The presence of artifacts of SE-T1W (2), FSE-T2W, F-Flair (2), or SE-T1W (1) did not show a signi®cant difference compared with that of EPIFlair (2) or EPI-Flair (1). This study showed that multi-shot EPI-Flair appeared to be superior to SE-T1W, and almost equivalent to FSE-T2W in terms of its ability to depict tumors. This sequence could be valid not only for tumors in the supratentorial region but also for those in the infratentorial region. Compared with FFlair, multi-shot EPI-Flair cannot replace F-Flair, but it can reduce acquisition time. This sequence is also useful for uncooperative patients due to its short imaging time.
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Noriaki Tomura, M.D. is an associate professor at Akita University and chief of neuroradiology. He received Japanese board certi®cation in radiology in 1986, Japanese board certi®cation in nuclear medicine in 1992, and his M.D. degree in 1989 from Akita University. His research interests are primarily in diagnostic neuro-, head and neck radiology, and nuclear medicine of the brain.
Jun-ichi Izumi, M.D. is a staff radiologist at Akita University. He received Japanese board certi®cation in nuclear medicine in 2000, and Japanese board certi®cation in radiology in 2001. His research interests are primaily in radiation therapy.
Koki Kato, M.D. is a staff radiologist at Akita University. He received Japanese board certi®cation in nuclear medicine in 1997, Japanese board certi®cation in radiology in 1998, and his M.D. degree in 2000 from Akita University. His research interests are primarily in diagnostic neuroradiology.
Komei Narita, R.T. is a supervisor of radiological technicians at Akita University. He is an expert of technology of MR imaging, especially in the ®eld of the central nervous system.
Satoshi Takahashi, M.D. is a staff radiologist at Akita University and chief of interventional radiology. He received Japanese board certi®cation in radiology in 1990, and his M.D. degree in 2001 from Akita University. His research interests are primarily in neuroradiology and interventional neuroangiography.
Jiro Watarai, M.D. is a professor and chairman of radiology at Akita University. He received his M.D. degree in 1982 from Tohoku University. Japanese board certi®cation in radiology in 1986, and Japanese board certi®cation in nuclear medicine in 1997. He has worked over 30 years on developing radiation therapy and diagnostic radiology. His research interests are primarily in radiation therapy for head and neck tumors.
Ryuji Sashi, M.D. is an instructor at Akita University. He received Japanese board certi®cation in radiology in 1987, and his M.D. degree in 1990 from Akita University. His research interests are primarily in diagnostic radiology of the bone and soft tissues.
Computerized Medical Imaging and Graphics 26 (2002) 65±72
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Multi-shot echo-planar Flair imaging of brain tumors: comparison of spin-echo T1-weighted, fast spin-echo T2-weighted, and fast spin-echo Flair imaging Noriaki Tomura*, Koki Kato, Satoshi Takahashi, Ryuji Sashi, Jun-ichi Izumi, Komei Narita, Jiro Watarai Department of Radiology, Akita University School of Medicine, 1-1-1 Hondo, Akita City, Akita, 010-8543, Japan Received 19 July 2001; revised 11 October 2001; accepted 11 October 2001
Abstract Multi-shot echo-planar ¯uid-attenuated inversion-recovery (EPI-Flair) was compared with spin-echo T1-weighted (SE-T1W), fast SE T2weighted (FSE-T2W), and fast Flair (F-Flair) in imaging brain tumors. In 32 patients with various different brain tumors, three reviewers independently evaluated image quality. Two reviewers evaluated the image quality of precontrast EPI-Flair to be signi®cantly better than that of precontrast SE-T1W. Two reviewers evaluated the image quality of postcontrast EPI-Flair as superior to that of postcontrast SE-T1W. Artifacts on postcontrast EPI-Flair were signi®cantly more prominent than those on postcontrast F-Flair. Multi-shot EPI-Flair appeared to be superior to SE-T1W, and almost equivalent to FSE-T2W in terms of image quality. q 2002 Elsevier Science Ltd. All rights reserved. Keywords: MR imaging; Echo-planar imaging; Fluid-attenuated inversion-recovery imaging; Brain; Neoplasms
Fluid-attenuated inversion-recovery (Flair) sequences provide good contrast between the white matter and cerebrospinal ¯uid (CSF) due to CSF nulling with heavily T2-weighted imaging (T2W) [1±4]. The usefulness of Flair sequences has been demonstrated in various different diseases of the brain, including infarct [2,3,5] subarachnoid hemorrhage [2,6], demyelinating diseases [1±5,7±9] in¯ammatory diseases [4,5], and neoplasms [2,5,10]. Most of these reports suggested the superiority of Flair for detecting cortical lesions and lesions located in the peripheral subcortical or periventricular regions [1,7,11,12]. Although the major disadvantage of Flair sequences is its prolonged acquisition time, a fast Flair sequence [1,3] imaging modality by combining Flair with fast spin-echo sequence imaging was developed. Echo-planar imaging (EPI) is a rapid imaging technique, which is capable of further shortening of the acquisition time. The EPI technique is currently used for functional MRI [13], perfusion studies, and diffusion studies [14]. Single-shot EPI is capable of producing more than 10 images a second [15], but has a major disadvantage of marked susceptibility artifacts near the skull base. EPI with a multi-shot technique [4] is also a fast imaging * Corresponding author. Tel.: 181-188-34-1111; fax: 181-188-36-2623. E-mail address: [email protected] (N. Tomura).
technique, and it is more promising for higher resolution imaging than single-shot EPI. The purpose of this investigation was to determine whether EPI-Flair with a multi-shot technique could replace T1-weighted images with conventional SE sequence (SET1W), T2-weighted images with fast SE sequence (FSET2W), and fast Flair (F-Flair) images. 1. Materials and methods The brains of 32 consecutive patients with brain tumors were prospectively imaged on a clinical 1.5-T imager. All patients underwent EPI-Flair before and/or after contrast administration to compare EPI-Flair with other sequences. All tumors were diagnosed by removal of the tumor or biopsy after MR examinations. The tumors analyzed were ®ve glioblastomas, six malignant astrocytomas, one malignant oligodendroglioma, one oligodendroglioma, one pilocytic astrocytoma, three medulloblastomas, three germinomas, two central neurocytomas, three malignant lymphomas, two leukemic masses and ®ve metastatic tumors. All MR examinations were performed with the use of a standard head coil. Axial images were obtained parallel to the plane including both the anterior commissure and posterior commissure. Twenty-two slices with 4 mm in thickness
0895-6111/02/$ - see front matter q 2002 Elsevier Science Ltd. All rights reserved. PII: S 0895-611 1(01)00039-8
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Table 1 Parameters of each sequence (EPI-Flair, multishot echo-planar ¯uid attenuated inversion recovery; SE-T1W, spin-echo T1-weighted imaging; FSE-T2W, fast spin-echo T2-weighted imaging; TI, inversion time; TR, time of repetition; TEeff, effective echo time; FOV, ®eld of view)
EPI-Flair SE-T1W FSE-T2W
TI (ms)
TR/TEeff (ms)
FOV (mm)
Matrix
Acquisition
Number of shots
Imaging time
2000
8000/100 300±540/8±14 4000±5000/90±110
180±220 180±220 180±220
256 £ 192 256 £ 224/256 £ 256 256 £ 256
1 2 2
8
1 min 8 s 2 min 14 s±4 min 2 s 2 min 8 s±3 min 34 s
were obtained. Table 1 summarizes several parameters in each sequence. Prior to administration of contrast material, axial EPI-Flair n 11; SE-T1W n 11; FSE-T2W n 11; and F-Flair n 9 were performed. After administration of gadopentetate dimeglumine (0.1 mmol/kg of body weight), axial EPI-Flair n 21; SE-T1W n 19; and F-Flair n 21 were performed in random order. Three neuroradiologists who were aware of only the clinical diagnosis independently assessed the image quality of each sequence. Image quality was assessed by lesion conspicuity, margin de®nition, and delineation of edema [16,17]. A fourpoint grading system (0, insuf®cient; 1, suf®cient; 2, good; 3, excellent) was employed. Moreover, for evaluating the presence of artifacts, a similar score (0, marked; 1, moderate; 2, mild; 3, none) was used [17]. The statistical signi®cance of differences with image quality and the presence of artifacts were determined with the Wilcoxon signed-ranks test. A p-value of 0.01 or less was considered signi®cant.
EPI-Flair (2) more clearly revealed lesion conspicuity, delineation of edema, and margin de®nition (Fig. 1) than SE-T1W (2). There were no signi®cant differences between FSE-T2W and EPI-Flair (2). Precontrast F-Flair (F-Flair (2)) was graded as being signi®cantly superior to EPIFlair (2) by radiologist 1. After administration, radiologists 2 and 3 evaluated postcontrast EPI-Flair (EPI-Flair (1)) as being signi®cantly superior to postcontrast SE-T1W (SET1W (1)) (Figs. 2 and 3). With regard to the presence of artifacts, a signi®cant difference was observed between postcontrast F-Flair (F-Flair (1)) and EPI-Flair (1) by all radiologists (Table 3). The presence of artifacts of SE-T1W (2), FSE-T2W, F-Flair (2), or SE-T1W (1) did not show a signi®cant difference compared with that of EPI-Flair (2) or EPI-Flair (1) (Table 3). In a patient with residual tumor after surgery, parenchymal hemorrhage was seen more clearly in EPI-Flair than in the other sequences, however, its remarkable hypointensity was not distinguishable from the intensity of CSF.
2. Results
3. Discussion
The results for image quality are shown in Table 2. Prior to administration of contrast material, precontrast EPI-Flair (EPI-Flair (2)) was evaluated to be signi®cantly better than precontrast SE-T1W (SE-T1W (2)) by radiologists 2 and 3.
In the present study, EPI-Flair produced better images than SE-T1W (2) or SE-T1W (1) according to the evaluation of lesion conspicuity, margin de®nition, and delineation of edema for all radiologists. The presence of artifacts seen
Table 2 Mean score of image quality (SE-T1W (2), precontrast SE-T1W; F-Flair (2), precontrast Flair; EPI-Flair (2), precontrast EPI-Flair; SE-T1W (1), postcontrast SE-T1W; F-Flair (1), postcontast fast Flair; EPI-Flair (1), postcontrast EPI-Flair) n
Mean ^ SD
SE-T1W (2) vs EPI-Flair (2)
11
SE-T1W (2) EPI-Flair (2)
FSE-T2W vs EPI-Flair (2)
11
FSE-T2W EPI-Flair (2)
F-Flair (2) vs EPI-Flair (2)
9
F-Flair (2) EPI-Flair (2)
SE-T1W (1) vs EPI-Flair (1)
19
SE-T1W (1) EPI-Flair (1)
F-Flair (1) vs EPI-Flair (1)
21
F-Flair (1) EPI-Flair (1)
Radiologist 1
Radiologist 2
Radiologist 3
1.5 ^ 0.8 2.1 ^ 0.6 p , 0.05 2.3 ^ 0.9 2.2 ^ 0.6 ns 3.0 ^ 0 2.2 ^ 0.4 p , 0.01 1.7 ^ 0.7 2.2 ^ 0.7 p , 0.05 2.8 ^ 0.4 2.2 ^ 0.7 p , 0.01
1.2 ^ 0.6 2.5 ^ 0.5 p , 0.01 1.9 ^ 0.5 2.5 ^ 0.5 ns 2.9 ^ 0.3 2.4 ^ 0.5 ns 1.2 ^ 0.6 2.3 ^ 0.5 p , 0.01 2.7 ^ 0.5 2.3 ^ 0.5 ns
1.5 ^ 0.7 2.7 ^ 0.5 p , 0.01 2.3 ^ 0.9 2.7 ^ 0.5 ns 3.0 ^ 0 2.7 ^ 0.5 ns 1.6 ^ 0.8 2.3 ^ 0.5 p , 0.01 2.9 ^ 0.4 2.3 ^ 0.5 p , 0.01
N. Tomura et al. / Computerized Medical Imaging and Graphics 26 (2002) 65±72
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Fig. 1. A 61-year old man with a neurocytoma involving the corpus callosum. FSE-T2W TR=TE=excitations 4000=107=2 (A), precontrast F-Flair (TR=TE=excitations 10 002=150=1; TI 2200) (B), and precontrast EPI-Flair (TE=excitations 100=1; TI 2000) (C) more clearly differentiate the tumor from the peritumoral edema than precontrast SE-T1W TR=TE=excitations 300=10=2 (D). Arrows indicate the tumor.
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Fig. 2. An 11-year old boy with a malignant astrocytoma involving the cerebellar vermis. Postcontrast F-Flair (TR=TE=excitations 10 002=147=1; TI 2200) (A), and postcontrast EPI-Flair (TE=excitations 100=1; TI 2000) (B) more clearly de®ned the margin of the tumor than postcontrast SE-T1W TR=TE=excitations 519=10=2 (C). Arrows indicate the tumor in the cerebellar vermis.
N. Tomura et al. / Computerized Medical Imaging and Graphics 26 (2002) 65±72
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Fig. 3. A 67-year old woman with a malignant astrocytoma involving the cerebellar vermis and hemisphere. Postcontrast F-Flair (TR=TE=excitations 8002=150=1; TI 2000) (A), and postcontrast EPI-Flair (TE=excitations 100=1; TI 2000) (B) more clearly de®ned the margin of the tumor than postcontrast SE-T1W TR=TE=excitations 300=10=2 (C). Arrows indicate the tumor in the cerebellum. Artifacts are more prominent in postcontrast T1W than in postcontrast F-Flair and EPI-Flair.
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on the EPI-Flair (2) was more prominent that on the SET1W (2), while more prominent artifacts were observed on SE-T1W (1) compared with EPI-Flair (1). EPI-Flair appears to represent an alternative to SE-T1W for the depiction of brain tumors. Although artifacts on the EPI-Flair were more prominent than those on FSE-T2W, the mean scores for image quality did not differ signi®cantly between FSE-T2W and EPI-Flair. This indicates that FSE-T2W can be replaced by EPI-Flair to reduce the imaging time in unstable or uncooperative patients. F-Flair (1) was better than EPI-Flair (1) according to the evaluation of image quality of two of the three radiologists, and artifacts were signi®cantly more prominent on EPI-Flair (1) than on FFlair (1) according to every radiologist. This result showed that EPI-Flair could not replace F-Flair on the basis of its ability to depict the tumor. However, F-Flair sequences require approximately 4 min of acquisition time, which is more than three times the acquisition time of EPI-Flair. EPIFlair is also useful in unstable or uncooperative patients because of its short acquisition time. Single-shot EPI is a much faster imaging modality than the multi-shot EPI used in the present study. The acquisition time of single shot EPI is several seconds for the entire brain. However, susceptibility artifacts, which is much more prominent than those on the multi-shot EPI, disturbs the imaging of lesions near the skull base. Korogi et al. [15] compared single-shot EPI-Flair with F-Flair in the detection of various brain lesions. Their results showed that single-shot EPI-Flair provided almost equivalent tissue contrast and CSF suppression as F-Flair, but a susceptibility to artifacts at the skull base and posterior to the frontal sinus degrades its quality. Single-shot EPIFlair, used in their study, has a shortened imaging time as fast as 4 s, and can reduce motion artifacts. Single-shot EPIFlair is also useful in screening for supratentorial lesions. Bruning et al. [10] compared echo-planar T2W (EPI-T2W)
with SE-T2W for the depiction of intra-axial brain tumors, and reported that EPI-T2W produce images of a suf®cient quality to depict intra-axial brain tumors. They used doubleshot EPI, of which the acquisition time was within 25 s. However, their study did not include patients with an infratentorial tumor. On the double-shot EPI, severe susceptibility artifacts were found in the posterior fossa and in the sections of the brain adjacent to the skull base. Susceptibility artifacts on the multi-shot EPI could be further reduced compared with those on single shot EPI. Simonson et al. [4] reported that multi-shot EPI-Flair was a practical and ef®cient means of screening the entire brain. They mentioned that increased sensitivity to susceptibility effects could be clinically useful in detecting minute areas of hemorrhage, cavernous angioma, shear injury, and contusion. In particular, hemorrhage may go undetected on fast spin-echo SE-T1W or Flair images, because susceptibility effects are decreased in fast spin-echo sequences. EPI sequences are useful in detecting subtle calci®cation. This increased sensitivity to susceptibility effects of EPI-Flair may provide more information than other sequences, which should prove useful in the differential diagnosis of a tumor. Eight-shot EPI, used in the present study, reduces artifacts near the skull base, and at the bone and air interfaces. Multi-shot EPI-Flair used in the present study suffers less image degradation due to susceptibility artifacts, although the acquisition time to cover the entire brain was 68 s. There are some limitations to the present study. Firstly, three independent reviewers evaluated lesion conspicuity and the degree of artifacts qualitatively. However, each reviewer was able to identify which image was a Flair sequence. This likely somewhat biased the study. Calculation of sensitivity and speci®city was not performed due to an absence of controls. A quantitative analysis is necessary
Table 3 Overall assessment of artifacts (SE-T1W (2)), FSE-T2W, F-Flair (2), EPI-Flair (2), SE-T1W (1), F-Flair (1), and EPI-Flair (1), the same as those in the Table 2) n
Mean ^ SD
SE-T1W (2) vs EPI-Flair (2)
11
SE-T1W (2) EPI-Flair (2)
FSE-T2W vs EPI-Flair (2)
11
FSE-T2W EPI-Flair (2)
F-Flair (2) vs EPI-Flair (2)
9
F-Flair (2) EPI-Flair (2)
SE-T1W (1) vs EPI-Flair (1)
19
SE-T1W (1) EPI-Flair (1)
F-Flair (1) vs EPI-Flair (1)
21
F-Flair (1) EPI-Flair (1)
Radiologist 1
Radiologist 2
Radiologist 3
2.8 ^ 0.4 2.5 ^ 0.7 ns 3^0 2.5 ^ 0.7 p , 0.05 3^0 2.7 ^ 0.5 p , 0.05 2.4 ^ 1.1 2.1 ^ 0.9 ns 2.8 ^ 0.4 2.1 ^ 0.8 p , 0.01
2.9 ^ 0.3 2.4 ^ 0.5 p , 0.05 3^0 2.5 ^ 0.8 p , 0.05 3^0 2.6 ^ 0.7 ns 2.6 ^ 0.8 1.9 ^ 0.8 p , 0.05 2.8 ^ 0.4 2.0 ^ 0.8 p , 0.01
2.8 ^ 0.4 2.4 ^ 0.8 p , 0.05 2.9 ^ 0.3 2.4 ^ 0.5 ns 2.9 ^ 0.3 2.3 ^ 0.5 p , 0.05 2.6 ^ 0.8 2.2 ^ 0.8 p , 0.05 2.9 ^ 0.3 2.1 ^ 0.8 p , 0.01
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for further studies. Comparison of multi-shot EPI-Flair with single-shot EPI-Flair should be performed in future research. The relationship between the number of shots and the image quality should also be evaluated. There have been a few reports concerning contrast enhancement on Flair images after the administration of contrast medium [18,19]. Contrast enhancement is seen because the signal intensity of Flair is partially dependent of T1 [19]. The inversion pulse in Flair sequences might introduce T1 weighting. A preliminary report by Tsuchiya et al. [19] showed that contrast enhancement on postcontrast Flair images was comparable to that seen on SE-T1W (1) in patients with intracranial tumors. In the present study, EPIFlair was performed before and after the administration of contrast medium only in two patients. EPI-Flair showed almost an equivalent degree of contrast enhancement as SE-T1W. Flair images have the advantages of both T2W and T1W for tissue contrast. The usefulness of Flair sequences has also been reported in other diseases of the central nervous system, such as infarction [2,3,5], subarachnoid hemorrhage [2,6], and multiple sclerosis [1,4,9,16]. Simonson et al. [4] showed the superiority of EPI-Flair in several cases with demyelinating disease or infection. Lesions immediately adjacent to ventricles or cortical sulci could be overlooked or mistaken for partial volume effects on SE- or FSE-T2W. They presented a case of septic emboli of which multiple lesions at the gray±white matter junction could not be demonstrated by T2W, but could be by EPI-Flair. The superiority of EPI-Flair over conventional SE images in the depiction of herpes simplex encephalitis has also been established. In the present study, EPI-Flair was superior to T1W sequences in our criteria. However, T1W images are used to produce high quality anatomic images and to provide information concerning the presence of substances that shorten T1. To replace a T1W sequence with EPI-Flair may limit information available from MR. Further studies on various other diseases should be done to compare EPI-Flair with SE or FSE sequences. In conclusion, this study showed that multi-shot EPI-Flair appeared to be superior to SE-T1W, and almost equivalent to FSE-T2W in terms of its ability to depict tumors. This sequence could be valid not only for tumors in the supratentorial region but also for those in the infratentorial region. Compared with F-Flair, multi-shot EPI-Flair cannot replace F-Flair, but it can reduce acquisition time. This sequence is also useful for uncooperative patients due to its short imaging time. 4. Summary EPI with a multi-shot technique is also a fast imaging technique, and it is more promising for higher resolution imaging than single-shot EPI. The purpose of this investigation was to determine whether EPI-Flair with a multi-shot technique could replace T1-weighted images with conventional SE
71
sequence (SE-T1W), T2-weighted images with fast SE sequence (FSE-T2W), and fast Flair (F-Flair) images. The brains of 32 consecutive patients with brain tumors were prospectively imaged on a clinical 1.5-T imager. All patients underwent EPI-Flair before and/or after contrast administration to compare EPI-Flair with other sequences. All tumors were diagnosed by removal of the tumor or biopsy after MR examinations. The tumors analyzed were ®ve glioblastomas, six malignant astrocytomas, one malignant oligodendroglioma, one oligodendroglioma, one pilocytic astrocytoma, three medulloblastomas, three germinomas, two central neurocytomas, three malignant lymphomas, two leukemic masses and ®ve metastatic tumors. Prior to administration of contrast material, axial EPI-Flair n 11; SET1W n 11; FSE-T2W n 11; and F-Flair n 9 were performed. After administration of contrast material, axial EPI-Flair n 21; SE-T1W n 19; and F-Flair n 21 were performed in random order. Three neuroradiologists who were aware of only the clinical diagnosis independently assessed the image quality of each sequence. Image quality was assessed by lesion conspicuity, margin de®nition, and delineation of edema. A four-point grading system (0, insuf®cient; 1, suf®cient; 2, good; 3, excellent) was employed. Moreover, for evaluating the presence of artifacts, a similar score (0, marked; 1, moderate; 2, mild; 3, none) was used. Prior to administration of contrast material, precontrast EPI-Flair (EPI-Flair (2)) was evaluated to be signi®cantly better than precontrast SE-T1W (SE-T1W (2)) by two radiologists. EPI-Flair (2) more clearly revealed lesion conspicuity, delineation of edema, and margin de®nition than SE-T1W (2). There were no signi®cant differences between FSE-T2W and EPI-Flair (2). Precontrast F-Flair (F-Flair (2)) was graded as being superior to EPI-Flair (2) by one radiologist. After administration, two radiologists evaluated postcontrast EPI-Flair (EPI-Flair (1)) as being superior to postcontrast SE-T1W (SE-T1W (1)). With regard to the presence of artifacts, a signi®cant difference was observed between postcontrast F-Flair (F-Flair (1)) and EPI-Flair (1) by all radiologists. The presence of artifacts of SE-T1W (2), FSE-T2W, F-Flair (2), or SE-T1W (1) did not show a signi®cant difference compared with that of EPIFlair (2) or EPI-Flair (1). This study showed that multi-shot EPI-Flair appeared to be superior to SE-T1W, and almost equivalent to FSE-T2W in terms of its ability to depict tumors. This sequence could be valid not only for tumors in the supratentorial region but also for those in the infratentorial region. Compared with FFlair, multi-shot EPI-Flair cannot replace F-Flair, but it can reduce acquisition time. This sequence is also useful for uncooperative patients due to its short imaging time.
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Noriaki Tomura, M.D. is an associate professor at Akita University and chief of neuroradiology. He received Japanese board certi®cation in radiology in 1986, Japanese board certi®cation in nuclear medicine in 1992, and his M.D. degree in 1989 from Akita University. His research interests are primarily in diagnostic neuro-, head and neck radiology, and nuclear medicine of the brain.
Jun-ichi Izumi, M.D. is a staff radiologist at Akita University. He received Japanese board certi®cation in nuclear medicine in 2000, and Japanese board certi®cation in radiology in 2001. His research interests are primaily in radiation therapy.
Koki Kato, M.D. is a staff radiologist at Akita University. He received Japanese board certi®cation in nuclear medicine in 1997, Japanese board certi®cation in radiology in 1998, and his M.D. degree in 2000 from Akita University. His research interests are primarily in diagnostic neuroradiology.
Komei Narita, R.T. is a supervisor of radiological technicians at Akita University. He is an expert of technology of MR imaging, especially in the ®eld of the central nervous system.
Satoshi Takahashi, M.D. is a staff radiologist at Akita University and chief of interventional radiology. He received Japanese board certi®cation in radiology in 1990, and his M.D. degree in 2001 from Akita University. His research interests are primarily in neuroradiology and interventional neuroangiography.
Jiro Watarai, M.D. is a professor and chairman of radiology at Akita University. He received his M.D. degree in 1982 from Tohoku University. Japanese board certi®cation in radiology in 1986, and Japanese board certi®cation in nuclear medicine in 1997. He has worked over 30 years on developing radiation therapy and diagnostic radiology. His research interests are primarily in radiation therapy for head and neck tumors.
Ryuji Sashi, M.D. is an instructor at Akita University. He received Japanese board certi®cation in radiology in 1987, and his M.D. degree in 1990 from Akita University. His research interests are primarily in diagnostic radiology of the bone and soft tissues.