대 한 방 사 선 의 학 회 지 1992 ; 28 (6) : 823~830 Journal of Korean Rad iological Society, November, 1992

Comparison of MRI and CT of (DIA)*

Jong Deok, Kim, M.D., Dong Woo, Park, M.D., Tchoong Kie, Eun, M.D.

Deþartmeη t 01 Diαgnostic Radiology, J.ηie Unversity College 01 Mediciηe

- Abstract- A retrospective comparative study of MRI and CT in 24 patients with diffuse axonal injury (DIA) was undertaken ‘ Three-quaters of the lesions were non-hemorrhagic, and the sites of involvement were lobar white matter (96%), corpus call osum (70 %), and rostral (42%), in descending order. MRI was singnficantl y more sensitive than CT in detecting DAI lesions. The average number of DAI lesions was higher with in­ creasin g clinical stage of the injury MRI is more valu able than CT for staging the full magnitude of the injury and in predicting the neurologic prognosis of DAI le sions. Index Words: Brain, trauma, 10.439 Brain, computed tomography, 11. 1211 Brain, magnetic resonance, 11. 1214 Brain, axon

prevalent in DAI. INTRODUCTION The purpose of this study is to compare the capability of MRI and CT to detect and to stage Diffuse axonal injury (DAI) is a widespread the DAI lesions. dam age to axons in the white matter of the brain as 'a consequence of closed head trauma. The ma­ jority of the patients sHstain their injury in a road MATERIALS AND METHODS traffic accident, usually have severe impairment of consciousness from at the time of injury than A retrospective comparative study of MRI do patients with many other primary lesions and and CT in 24 patients with the clinical diagnosis have a lower inciden ce of fracture of the skull, of DAI was under'taken to evaluate the usefulness intracranial hematoma, cerebral contusion, and of both imaging modalities during the one-year raised than patients without period from J anuary 1991 through D ecember DAI. 1991 MRI has clear advantages over CT in evalua Non-enhanced CT scans were obtained in all ting closed head trauma. Although its sensitivity patients within the first 24 hours aft er trauma in detecting hemorrhagic lesions is similar to that by using either TCT-80A or TCT-300A scan­ of CT, it is much better than CT in detecting ner, Toshiba. A slice thickness of lOmm was used non-hemorrhagic lesions, which are more in all insta nces. MRI was performed with a O.5T

* 이 논문은 19 9 1 년도 인제대학교 장학재단의 연구비보조로 이루어졌음. 이 논문은 19 92 년 4 월 28일 접수하여 199 2 년 8월 21 일에 채택되었음 Received April 28, Accepted August 21 , 1992

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Toshiba MRT -50A scanner. The interval from Table 1. Age & Sex Distribution the lnJury to MRI evaluation was 1-17 days (mean, 5.6 days). All patients were examined 짧성 M F Total with both T 1-and T2 -weighted pulse sequences. 3 。 10 J Scans were obtained with a contiguous multislice ?-3 qJ 11 - 20 1i technique with a slice thickness of 5-8mm and 21 - 30 cJ oo interslice gap of 2mm. The T2-weighted scans q ’ 4 31 - 40 J i ‘ were obtained with a spin-echo sequences with ? nJ 41 - 50 J ? q4 . a repetiton time (TR) of 2500-3000 msec and 51 - 60 • echo time (TE) of 80 msec. T l-weighted scans 61 1i were obtained with a TR of 450-500 msec and Total 16 8 24 TE of 15-20 msec. Two or more imaging planes were used in all patients The MR and CT scans were analyzed in­ in stage III and 7 each were in stage 1 and stage dependently, and all abnormalities visualized II. Lobar white matter was the most common were classified by Adams’s staging of DAI (1) site of involvement (23/24;96%) (Fig. 1) , and according to increasing severity of the trauma: the next common sites were corpus collosum Stage 1, DAI lesions confined to the white mat­ (17/24; 70 % ) (Fig. 2) and rostral brainstem ter of the frontal and temporallobes, Stage II, (10/24; 42 % ) (Fig. 3) , in descending order. The lesions in lobar white matter as well as the white matter of frontallobe was most common­ posterior half of the corpus callosum, and Stage ly involved , and those of temporal and parietal III, additionallesions in the dorsolateral aspect lobes were the next. Posterior portion of the cor­ of the midbrain and upper pons. After initial in­ pus callosum (body and splenium) was more dividual analysis, the CT and MR scans were commonly involved than anterior portion. compared. Equivocal abnormalities seen on only Cerebellar white matter, internal capsule, and one study or one imaging plane were omitted were also involved. Associated le­ from the calculation. W e used the following sions.were as follows:cerebral contusion (n = 3), criteria to classify a lesion as hemorrhagic on (n = 2) , and intraventricular­ MRI. On T 1-weighted image (T 1WI) , the (n = 1) and su barachnoid hemorrhages (n = 1) shortening of the T 1 relaxation time by Skull fracture and maxilla with zygoma fractures methemoglobin within the hemorrhagic lesion were seen in one case each. Total number of the had to be of sufficient degree that the hemor­ lesions detected on MRI (T2WI) was 201 , 26 % rhagic fo cus was at least partially hyperintense (53/201) of which were detectable on CT. The relative to white matter. On T2-weighted image number of DAI lesions ranged from 2 to 28 in (T2WI), we required the evidence of centtal hy­ one patient. The shape of the lesions was ovoid, pointensity (relative to brain parenchyma) within elliptical, small patchy, or short linear. Of 531e­ the hemorrhagic lesion sions detected on CT, 45 lesions (85 % ) were hemorrhagic. The ratio ofhemorrhagic to non­ RESULTS hemorrhagic lesion on MR was 50: 151 , reveal­ ing 75 % of DAI lesions consisted of non­ The male-to-fem ale ratio was 2: 1 and the age hemorrhagic (Table 3,4). The average numbers ran ge was 6 to 68 years old. Twenty-one of 24 of DAI lesions were 8, which were higher with cases (87.5 % ) were below 50 years old (Table 1). increasing severity of trauma, i.e., 5, 7, and 11 An analysis of the stage and the site of DAI in stage 1, II, and III, respectively (Table 4). lesions are given in Table 2. T en of24 cases were Cases with comatous or semicomatous m en-

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Table 2. Sites of DAI Les ions on MRI (T2WI)

Stage 1 Stage II Stage III Total 씩과「냐현e (n = 7) (n = 7) (n = 10) (n = 24) Lobar WM (23 /24) Frontal 6 5 8 19 Temporal 7 5 13 Pa ri etal 4 3 3 10 Occipi tal 0 0 0 0

Corpus call osum (17/24) Genu 2 2 4 Body 3 9 12 Splenium 4 6 10

Rostral brainstem ( 10124) 10 10 Other Cbl. WM 4 4 Int. capsule 4 5 Basal gangli a 4 3 8

Note: DAI = diffu se axonal lnJury WM = white matter Cbl. = ce rebell ar Int. = internal

Fig. 1. Stage 1 DAI. 22 year-old­ female with drowsy mentality. Axial T2WI (TR/TE = 3000/ 120) obtained on the day ofhead injury (a) reveals multiple, small, focal high singal intensity lesions in the lobar white matter of the frontal and temporallobes. Brain CT (not shown) was normal. Five and a half months later (b), the number of the lesions decreased in accor­ dance with improvement of im­ paired consciousness.

a. Initial b. 5.5M Later tality from the time of the injury were in stage duced by closed head traurna with rotationally II or stage III (8 /2 4). Three of the 4 cases who accelerated shear-strain at the mornent of irnpact. died within 10 days after the injury were in stage Closed head trauma with a significant inertial 11 1. component may produce differential inertia at areas of differing d ensity of fixation with resul­ DISCUSSION tant shearing injury at these sites. Shear-stra in Diffuse axonal injury (DAI) is the most com­ will be greatest at the junction of the tissues of m on type of primary tra urnatic intracra nial le­ different rigidity (gray/white-matter interface, sion constituting a pproximately 48% of all brain/CSF interface, skull/brain interface, dura prima ry lesions of (1-3). It is pro- m ater/b rain interface). The gray-white m atter

- 825 Journal of Korean Radi 이 ogical Society 1992; 28 (6) : 823""'830 junction is a prime example of just such an in­ Rotatory acceleration of the head is much terface, where differing density and differential more likely to occur during road traffic accident fixation among axons, cell bodies, and blood and in this situation the acceleration of the head vessels result in differential inertia causing distor­ is relatively of long duration. Subdural tion of the brain with tearing of the axons and hematom a and intracranial hematoma occur vessels. In DAI, widespread tearing ofaxons in significantly less frequently with increasing ac­ the cerebrum leads to disconnection of the cor­ celeration pulse duration , which are related to tex from lower center and hence to the state of the much lower incidence of raised intracranial , so the clinical hallmark of DAI is loss of pressure in DAI. Therefore, m ajority of the pa­ consciousness and DAI is a frequent cause of the tients with DAI sustain injury in a road traffic persistent vegetable state following head injury accident, never experience a lucid interval, and Because of their inherently low rigidity, neurons have a longer duration of survival than the pa­ are extremely susceptible to shear-strain defor­ tients in whom DAI has not occurred. In addi­ mation. Pure shearing injuries generally produce tion, they have a lower incidence of fracture of non-localized , diffuse neuronal deficits. The the skull, intracranial hematoma and cerebral degree of injury is in large part related to the contusion (1 ,7) magnitude of force , and patient presentation It is characterized by multiple, small. focal varies accordingly, from mild confusion with lit­ traumatic lesions scattered throughout the white tle or no retrograde amnesia and complete matter. They are typically found near the cor­ recovery to irreversible brain injury, persistent ticomedullary interface of the lobar white mat­ vegetable state, and death (1-2 , 4-6) ter or in the large white-matter fiber bundles

Fig. 2. Stage II DAI. 6 year-old­ male with stuporous mentality. Brain CT scans (a, b) obtained on the day of trauma show a small round low density in the midline of splenium (a) and a smaller high density in the right sided body (b) of corpus callosum . Axial T 1WIs (TR/TE = 400/15) (c,d) obtained 3 days after the head lnJury reveal multiple, ovoid and small patchy high signal intensity lesions in the white matter of the frontal and a b parietal lobes, and splenium and body of corpus callosum bilateral­ ly. The lesions appear more exten­ sive on MR than on CT

c d

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Fig. 3. Stage III DAI. 6 year-old male with coma. Multiple, ovoid and elliptical high densities with surrounding in both frontal white matters and corticomedullary junctional regions, body of corpus callosum, dors이 ateral rostral brainstem are demonstrated on CT of the day of head injury (a,b). On axial T2WI (c) , the lesions are more extensive than those of CT, and multiple hemorrhagic foci are contained within them. Coronal T1WI (d) a shows a hemorrhagic contusion and a in the left posterior temporal and posterior parietal region, respec tively, in addition to the lesion in lobar white matter, corpus callosum and brainstem. Most of the lesions are hemorrhagic

c d

Table 3. Total Numbers ofDAI Lesions Detected on to be multiple with as many as 15-20 lesions MRI and CT found in some severely injured patients (2-5, 8). 1n our cases, 75% of DA1 lesions were non­ 펴파꽉an MRI( %) CT(%) hemorrhagic and the number of DA1 lesions ranged from 2 to 28 per patient Hemorrhagic 50(25) 45(85) The pathologic hallmark of DA1 is axonal Non-hemorrhagic 151(75) 8(15) disruption. Microscopic manitestations are time Total 201 53 dependent. Early changes in short survivors

Note: DAI = diffuse axonal injury (days) include “ retraction balls" representing ex- truded axoplasm from the tom axon cylinders. (corona radiata, corpus callosum, internal cap­ “ Microglial stars" appear subacutely in in­ sule). Most lesions spare the overlying cortex but termediate survivals (several days to weeks) and occasionally, larger lesions may secondarily in­ consist of reactive microglial cells around the tom volve the cortex. About 80% ofDA1 lesions are axon cylinders. Chronically, in patients who sur­ non-hemorrhagic in nature and range in size vive for many weeks or months, cell death and form 5 to 15mm with peripherallesions tending gliosis are identified (4,9-10) to be smaller than more central ones, and are DA1 tends to occur in three fundamental usually ovoid to elliptical in shape with the long anatomical areas: 1) lobar white matter, 2) cor­ axis paralel to the direction ofaxonal tracts that pus callosum, and 3) dorsolateral aspect of the are involved. When present, DA1 lesions tend upper brainstem. Adams et 외 (1) classified three

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Table 4. Relationship between Clinical Stages and Brainstem DAI lesions are characteristically Numbers of DAI Lesions located in the dorsolateral quadrants of the rostral No. of Total Lesions brainstem (midbrain and upper pons). There Îs Stage No. of Pts strong predilection for lllJury to specific fiber MRI CT tracts such as the superior cerebellar peduncles 7 6 38 and medial lemnisci. Less commonly, lesions 7 9 II 51 may involve the lateral aspect of the mibdrain m %ω III 112 -% -E and cerebral peduncle. Brainstem DAI rarely oc­ Total 201 curs without the presence ofhistologically similar lesÎons in the corpus callosum and deep cerebral Note: DAI = diffuse axonal injury withe matter (stage III) (2-6,12-13). In our study, Pts. = patients lobar white matter was also the most common stages of DAI with the involvement becoming site of involvement (85 %) and the next were cor­ sequentially deeper with increasing severity of pus callosum (70 % ) and rostral brainstem trauma. In patients with mild trauma, DAI le­ (42 %), in descending order. The white matter sions may be confined to the white matterof the of frontallobe was more frequently involved than frontal and temporallobes (stage 1) (Fig. 1). Pa­ the remaining lobar white matter as were the tients with more severe rotational acceleration body and splenium of the corpus callosum than may develop lesions in the lobar white matter the anterior portion (Table 2) as well as the posterior half of the corpus callosum MRI has clear advantages over CT in (stage II) (Fig. 2) . If trauma is of even greater evaluating closed head trauma (3). Although its severity, DAI lesions will additionally be found sensitivity in detecting hemorrhagic lesions is in the dorsolateral aspect of the midbrain and similar to that of CT in acute stage, it is much upper pons (stage III) (Fig. 3). DAI lesions in better than CT in detecting non-hemorrhagic le­ these three locations form a frequently associated sions, which are more prevalent in DAI. MRI triad (1-3, 5-6, 8-9,11). will be more valuable than CT in staging the full The lobar white matter is the most common magnitude of lllJury in extensive traumatic area involved with DAI (67 %). Stage 1 DAI neuronal lesions and in predicting the final typically involves the parasagittal regions of the neurologic recovery. It is always desirable to per­ frontal lobes and the periventricular regions of form the MRI scan within the first 2 weeks of the temporallobes. Occasionally DAI lesions oc­ lllJury. During this period of time ed ema and cur in the parietal and occipitallobes. About 8 % axoplasmic leakage around the areas of neuronal of DAI lesions involve the internal and external disruption will be maximal, and traumatic lesions capsules, while only 4% of lesions are found in will be more conspicuous. After 2 weeks, as the the cerebellum. The second most common area edema gradually resolves, sm aller lesions will be involved with DAI is the corpus callosum (21 % ), more difficult to detect. Long TR/short TE and which invariably occurs in conjunction with DAI long TR/TE scans are more sensitive for detec­ of the lobar whi te matter (stage II). The vast ma­ tion of traumatic lesions over the whole time jority of callosal lesions (72 %) occur in the courses of injury (acute and subacute phases) posterior body and splenium, and more rostral (2-3, 5, 14) lesions are usually found in conjunction with le­ In Gentry’ s study (3), long TR/TE scans were sions of the splenium. Collosal lesions may in­ most sensitive, detecting 92 .4% ofDAI lesions. volve the entire corpus callosum and are usually CT was very insensitive, detecting only 19 % of unilateral and slightly eccentric to the midline lesions. DAI lesions were typically seen by CT but may also be bilateral and symmetric. only if larger than 1.5cm or located in the cor-

828 - Jong Deok Kim , et al : Comparison of Brain MRI and CT of Diffuse Axo nal Injury ona radiata or internal capsule. Small non­ was not proved statistically. In addition to these hemorrhagic lesions in outer locations were rare­ three fundamental anatomical regions, internal Iy seen by CT. T1-weighted image was also more capsule and cerebellar white matter were also in­ sensitive (7 1. 3%) than CT (19.0%), but less sen­ volved in 4 and 5 cases, respectively, and cerebral sitive than T2-weighted image. For hemorrhagic contusion, epidural hematoma, and subset, the sensitivities of all three imaging intraventricular- and subarachnoid hemorrhages methods were quite high and very similar were also associated in the present study, but (T2WI , 9 1. 3%; T1WI, 86.2%; CT, 85.7 % ) these appeared not directly proportional to the (3). In our study, only 26% ofDAI lesions were stage of DAI lesions. detectable on CT and, moreover, most ofthem In conclusion, 75 % of DAI lesions were non­ (85 % ) were hemorrhagic ones. hemorrhagic, and the average number of DAI Gentry (5) found a strong inverse relationship lesions was higher with increasing stage of the between mean initial Glasgow Coma Scale injury. MRI was 4 times more sensitive than CT (GCS) and the number of DAI lesions detected in detecting DAI lesions, and is more valuable by MRI (p

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Computed tomography of shearing lnjury of 196 1;Aug 26 ’ 443-448

cerebral white m atter. R adiology 1979; 127: 11 ‘ Lindell RG, Brad T , J ohn CG. Trauma to cor- 393-396 pus callosum . MR features. AJNR 8. Lindell RG, John CG, Brad T. MR Imaging 1988;9:1129-1138 of head trauma. R eview of the distribution and 12. 주양구， 우영훈， 서수지 . 미만성축색손상의 자기공명영 radiographic features of traumatic lesion.AJNR 상. 대한방사선의학회지. 1992: 28 (1) : 61 - 64 1988;9: 101-110 13. Adams JH. H ead lnjury. In: Greenfield’ s 9. Gennarelli TA, Thibault LE, ScD . et al. Diffuse neuropathology. Adams JH, Corsellis JAN , axonal lnjury and traumatic coma in the Duchen L\시 . 4th ed. New York: John Wiley & primate. Ann Neurol 1982;12:564-574 Sons, 1984;85-124 10. Strich SJ , Oxon DM. Shearing of nerve fibers 14. Gentry LR, Godersky JC, Thompson BH. as a cause of brian damage due to head injury. Traumatic brain stem lnjury; MR imaging. A patholgical study of twenty cases. Lancet R adiology 1989; 171: 177 -187

〈국문 요약〉 미만성 축색손상의 뇌자기공명영상과 뇌전산화단층촬영의 비교

인제대학교 의과대학 진단방사선과학교실

김 종 닥·박 동 우·은 충 기

1991년 한해동안에 발생한 24명의 미만성 축색손상 환자의 뇌자기공영영상과 뇌전산화단충촬영상을 비교하였다. 전체 병소의 75%가 비출혈성이었고， 발생장소는 뇌엽백질 ( 96% ) ， 뇌량 ( 70% ) ， 상부뇌간 ( 4 2% ) 의 순이었 다. 병소의 발견융은 자기공명영상이 전산화단충촬영보다 4배 높았으며， 병소의 평균수는 병기가 높아짐에 따라 증가하였다. 뇌 외상으로 인하여 뇌백질의 축색 을 따라 미만성으로 광범위하게 손상을 일으키며 대부분의 병소가 비출혈성인 미만성 축색손상에서 병소의 발견뿐만아니라 손상범위 에 따른 병기 결정과 예 후측정을 위하여는 자기공명영상촬영이 전산화 단충촬영보다 훨씬 좋음을 알 수 있었다.

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