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2 Fig. 1. Measurement of the signal intensity of CSF in the rabbit. The area of ROI is 5 mm 2 (Magnified post-enhanced FLAIR image). 10 Fig. 2. Measurement of the signal intensities of CSF and parenchyma in the normal volunteer. The signal intensities of CSF are measured in the lateral ventricle (1) and subarachnoid space (2). The signal intensities of parenchyma are measured in the gray (3) and white matters (4). The areas of round ROI was 4 5 mm 2 (Pre-enhanced FLAIR mage).

The signal intensities of CSF are measured in the lateral ventricle (1) and subarachnoid space (2).

3 Fig. 3. Changes in the signal intensities of CSF and parenchyma in the rabbit study. The signal intensities of CSF increase after an hour of contrast infusion on FLAIR images. But those of parenchyma do not increase at all. Table 1. Clinical Features of the Patient Group Patient CSF FLAIR* Hosp No. WBC Diff Prot Glc ADA Diagnosis L viral L viral L tuberculous P bacterial L tuberculous * Interval between onset of symptom and FLAIR study (day) Duration of hospitalization (day) Differential count of WBC in the CSF; L=lymphocyte, P=polymorphonuclear leukocyte (mm 3 ) Protein concentration of CSF (mg/dl) Glucose concentration of CSF (mg/dl) Adenosine deaminase concentration of CSF (IU/L; normal value <8) 11

2 viral 2 7 12 0075 L 74 123 48 01.0 viral 3 7 19 0310 L 81 246 56 12.1 tuberculous 4 4 16 1120 P 74 172 67 04.2 bacterial 5 9 13 0270 L 46 281 11 77.

4 Fig. 5. Comparison of the signal intensities of CSF according to the location of ROI. In the patient group, the signal intensities of CSF in the subarachnoid spaces (SAS) are higher than those in the normal control group on post-enhanced FLAIR images. But the signal intensities of CSF in the lateral ventricles (LV) are not different on any FLAIR images in the both groups. A: pre B: 1 hour C: 2 hours D: 3 hours E: 4 hours Fig. 4. Serial FLAIR images of the rabbit. The signal intensities of CSF in the ambient cistern (arrows) increase on post-enhanced FLAIR images (B E) after infusing triple doses of contrast. 12

FLAIR images. But the signal intensities of CSF in the lateral ventricles (LV) are not different on any FLAIR images in the both groups.

5 Fig. 6. Comparison of the signal intensities of parenchyma according to the location of ROI. The signal intensities of parenchyma are not different irrespective of the location of ROI which is in the gray (GM) or white matter (WM) in the both groups. Fig. 7. Comparison of the slopes of the signal intensities of CSF and parenchyma in the both groups. In the patient group, the slope of signal intensities of CSF in the subarachnoid spaces (P- SAS) is higher compared with that in the normal control group (N-SAS). But the slopes of parenchyma are not different in the both groups. 13

both groups. Fig. 7. Comparison of the slopes of the signal intensities of CSF and parenchyma in the both groups.

6 이은혜 외: 연수막염의 진단에서 조영증강 후 지연획득 FLAIR 영상의 유용성 A: patient No. 1, pre B: early C: delayed D: normal, pre E: early F: delayed G: patient No. 2, pre H: early I: delayed Fig. 8. Pre- and post-enhanced FLAIR images: comparison of the patients and the normal volunteer. There is a markedly meningeal enhancement in the subarachnoid space on post-enhanced delayed FLAIR image (C) of one patient (patient No. 1) compared with pre- (A) and post-enhanced early FLAIR images (B). But, there is no evidence of meningeal enhancement on any post-enhanced FLAIR images (E, F) of the normal volunteer compared with pre-enhanced FLAIR image (D). There is another example showing the meningeal enhancement on post-enhanced delayed FLAIR image (I) of another patient (patient No. 2) compared with pre- (G) and post-enhanced early FLAIR images (H). The open ring (C) and arrow (I) show the representative areas. 14

There is a markedly meningeal enhancement in the subarachnoid space on post-enhanced delayed FLAIR image (C) of one patient (patient No.

7 대한영상의학회지 2006;55:9-19 독하였다(Fig. 10). 고 찰 연수막질환의 진단에서 조영증강 T1 강조영상을 주로 사용 하고 있으나 감염성 또는 종양성 연수막질환에 대한 민감도는 36-71%에 불과하며 특이도 역시 높지 않다(6-10). 연수막 질환의 진단은 주로 뇌척수액 분석에 의존하고 있는데 임상적 으로 흔한 바이러스성 수막염은 뇌척수액 소견이 비특이적이 고 배양도 어렵기 때문에 진단이 애매한 경우가 많다(6-10). 그러므로 조영증강 T1 강조영상보다 효과적으로 연수막질환 을 진단할 수 있는 영상기법이 필요하다. Fig. 9. Changes of signal intensities of the subarachnoid space in the patient group. Patients having tuberculous meningitis (patient No. 3,5) show the most increase of signal intensities in the subarachnoid space on post-enhanced delayed FLAIR images compared with post-enhanced early FLAIR images. A patient having bacterial meningitis (patient No. 4) shows the least increase of signal intensities in the subarachnoid space on post-enhanced delayed FLAIR image compared with post-enhanced early FLAIR image. A: pre-flair B: early-t1wi Hajnal 등(11)이 1992년에 최초로 소개한 FLAIR 영상은 긴 에코시간(echo time)을 이용한 강한 T2 강조영상이면서 동시에 반전회복 (inversion-recovery) 펄스연쇄 (pulse sequence)를 이용하여 뇌척수액의 고신호 강도를 효과적으로 상쇄(nulling)시키므로 T2 강조영상과 달리 뇌척수액이 저신 호 강도로 보인다. 따라서 뇌실질병변과 주변 뇌척수액의 대 조도가 증가하므로 뇌척수액이나 인접 뇌실질의 병변을 진단 하는데 효과적이다(11-20). 또한, FLAIR 영상은 다른 MR 펄 스연쇄들과 달리 지주막하 출혈에 의한 뇌척수액의 신호강도 변화도 나타낼 수 있는데(30-32) 이는 뇌척수액의 단백질 농 도가 역치(threshold) 이상 높아지면 뇌척수액의 T1 이완시 간(relaxation time)이 감소하여 무효역전시간(null inversion time)을 상쇄시키므로 뇌척수액이 고신호 강도로 나타나기 때 문이다(1). 정상 뇌척수액은 FLAIR 영상에서 저신호 강도로 보이지만 뇌혈관장벽이 파괴되어 조영제가 뇌척수액강으로 유출되면 뇌 척수액 고유의 T1, T2 반복시간이 짧아져서 더는 반전회복 연 쇄에 의해 상쇄되지 않는다. 따라서 원래의 고신호 강도를 유 지하게 되므로 조영증강 현상으로 나타난다(14-21). FLAIR 영상은 T1 강조영상이 인지할 수 있는 조영제 농도보다 4배 이상 낮은 농도의 조영제를 인지할 수 있으므로 근본적으로 T1 강조영상보다 T1 단축효과에 더 민감하다(1, 2, 21-23, 33, 34). 또한, T1 강조영상에서는 피질 정맥의 느린 혈류가 고신호 강도로 나타나므로 수막의 조영증강과 구분하기가 어 려운데 비해, FLAIR영상에서는 반복시간과 에코시간이 길어 서 느린 혈류가 유동공백(flow void)으로 나타나기 때문에 연 수막의 조영증강과 피질 정맥의 조영증강을 쉽게 구분할 수 있다(21, 24). 그러므로 조영증강 FLAIR 영상은 뇌혈관장벽 이 파괴되어 뇌척수액의 단백질 농도나 조영제 농도가 증가할 수 있는 연수막 질환의 진단에 유용하다(1, 21, 22, 24-28). 조영증강후 지연획득 MR영상에 대한 기존의 연구를 살펴보 면, Elster 등(35)은 조영제 주입 2-6일 후 T1 강조영상에서 C: early-flair D: delayed-flair Fig. 10. A patient having a tuberculous meningoencephalitis (patient No. 5): comparison of T1WI and FLAIR images. Pre-enhanced FLAIR (A) and post-enhanced early T1WI (B) do not show meningeal enhancement. The diffuse meningeal enhancement (arrows) is more conspicuous on post- enhanced delayed FLAIR (D) than post-enhanced early FLAIR image (C). Among all images (A-D), multiple enhancing nodules in brain parenchyma are most conspicuous on post-enhanced delayed FLAIR image (D). 15

Changes of signal intensities of the subarachnoid space in the patient group. Patients having tuberculous meningitis (patient No.

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9 17 1. Dechambre SD, Duprez T, Grandin CB, Lecouvet FE, Peeters A, Cosnard G. High signal in cerebrospinal fluid mimicking subarachnoid hemorrhage on FLAIR following acute stroke and intravenous contrast medium. Neuroradiology 2000;42: Jackson EF, Hayman LA. Meningeal enhancement on fast FLAIR images. Radiology 2000;215: Naul LG, Finkenstaedt M. Extensive cerebrospinal fluid enhancement with gadopentate dimeglumine in a primitive neuroectodermal tumor. AJNR Am J Neuroradiol 1997;18: Sakamoto S, Kitagaki H, Ishii K, Yamaji S, Ikejiri Y, Mori E. Gadolinium enhancement of the cerebrospinal fluid in a patient with meningeal fibrosis and cryptococcal infection. Neuroradiology 1997;39: Pui MH, Langston JW, Arai Y. Gd-DTPA enhancement of CSF in meningeal carcinomatosis. J Comput Assist Tomogr 1993;17: Sze G, Soletsky S, Bronen R, Krol G. MR imaging of the cranial meninges with emphasis on contrast enhancement and meningeal carcinomatosis. 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Meningeal enhancement on fast FLAIR images. Radiology 2000;215:922-924 3. Naul LG, Finkenstaedt M.

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11 Usefulness of Post-enhanced Delayed FLAIR Imaging for Making the Diagnosis of Leptomeningitis 1 Eun Hye Lee, M.D., Deok Hee Lee, M.D. 2, Kwang Deog Jo, M.D. 3, Jae Seok Song, M.D. 4, Man Soo Park, M.D., Kyoung Sik Cho, M.D. 2 1 Department of Radiology, Gangneung Asan Hospital, University of Ulsan College of Medicine 2 Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine 3 Department of Neurology, Gangneung Asan Hospital, University of Ulsan College of Medicine 4 Department of Preventive Medicine & Public Health, College of Medicine Kwandong University Purpose: To evaluate the usefulness of post-enhanced delayed FLAIR (fluid-attenuated inversion-recovery) images in the diagnosis of leptomeningitis. Materials and Methods: We obtained the pre- and post-enhanced FLAIR images of 7 rabbits every hour after infusing triple doses of contrast, and we measured the signal intensities of the CSF (cerebrospinal fluid) and the brain parenchyma. Five leptomeningitis patients and 5 volunteers were enrolled to obtain the pre-enhanced FLAIR images, the early post-enhanced FLAIR images and the delayed post-enhanced FLAIR images, with using a standard dose of contrast, and to measure the signal intensities of the CSF and brain parenchyma. The statistical significances were determined by a mixed procedure and the Wilcoxon rank-sum test (p<0.05). Results: In the rabbits, the signal intensities of the CSF began to increase after an hour of contrast infusion, but those of the parenchyma did not increase. The time of maximum CSF enhancement was 2 hours after contrast infusion (p<0.001; standard estimate=750.43) and we obtained the post-enhanced delayed FLAIR images for clinical studies according to this result. The signal intensities of the CSF in the subarachnoid space were higher in the patient group compared with those of the normal control group on both the early post-enhanced FLAIR images and the delayed post-enhanced FLAIR images (p=0.0096) (p=0.0391). In the patient group, changes of signal intensities of the CSF in the subarachnoid space were more conspicuous on the delayed post-enhanced FLAIR images than on the early post-enhanced FLAIR images (p=0.0042). However, those of the parenchyma were not different in either group. Conclusion: The post-enhanced delayed FLAIR images obtained at 2 hours after contrast infusion are more useful for making the the diagnosis of leptomeningitis than are the post-enhanced early FLAIR images. Index words : Brain, MR Magnetic resonance (MR), pulse sequence Magnetic resonance (MR), contrast enhancement Meningitis Cerebrospinal fluid, MR Brain, diseases Address reprint requests to : Deok Hee Lee, M.D., Department of Radiology, Asan Medical Center, University of Ulsan College of Medicine 388-1, Poongnap-dong, Songpa-gu, Seoul , Korea. Tel Fax dhlee@amc.seoul.kr 19

Medicine 3 Department of Neurology, Gangneung Asan Hospital, University of Ulsan College of Medicine 4 Department of Preventive Medicine & Public Health, College of Medicine Kwandong University

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