Recovery Process of Immediate Prolonged Posttraumatic Coma Following Severe Head Injury Without Mass Lesions

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1 Neurol Med Chir (Tokyo) 45, , 2005 Recovery Process of Immediate Prolonged Posttraumatic Coma Following Severe Head Injury Without Mass Lesions Tsukasa WADA, KiyoshiKURODA*, YukiYOSHIDA*, Akira OGAWA, and Shigeatsu ENDO* Departments of Neurosurgery and *Critical Care Medicine, Iwate Medical University, Morioka, Iwate Abstract The recovery process of immediate posttraumatic coma was investigated in 24 patients with severe head injury. The correlation between poor outcome in the recovery process and magnetic resonance (MR) imaging findings was analyzed. MR imaging was performed within the first 7 days for all patients. The recovery process was classified into phase 1 for recovery to moderately disabled and phase 2 to good recovery (GR) according to the Glasgow Outcome Scale. The median of phase 1 was 21.0 days. Four patients did not recover to GR and had poor outcome. Twenty patients recovered to GR. Thirteen patients had short phase 2 of under 10 days and seven patients had long phase 2 of over 60 days. All patients had abnormal lesions on MR imaging considered to be diffuse axonal injury. The number of lesions ranged from two to 10, with a mean of five. Lesions in the dorsal upper brainstem were significantly associated with poor outcome (p º 0.05). The combination of focal lesions in the callosal splenium and dorsal upper brainstem was most common in patients with poor outcome. Patients with long phase 2 had significantly more lesions than patients with short phase 2. Key words: diffuse axonal injury, posttraumatic coma, magnetic resonance imaging Introduction Patients frequently present with immediate posttraumatic coma associated with neither intracranial mass lesions (cerebral contusion and acute subdural hematoma, etc.) nor elevated intracranial pressure (ICP). Such cases are categorized as diffuse injury type I or II in the Traumatic Coma Data Bank (TCDB) computed tomography (CT) pathological classification. 4) Some of these patients fall into prolonged traumatic coma. 7) Magnetic resonance (MR) imaging reveals multiple small lesions in many of these patients. 8,15,19) In general, the coma in these patients is probably caused by diffuse axonal injury (DAI) and/or primary brainstem injury. Patients with severe head injury caused by DAI are likely to recover from the immediate posttraumatic coma as well as the DAI sooner or later. 7,21) However, the clinical recovery process of posttraumatic coma caused by DAI without primary Received December 3, 2004; Accepted June 13, 2005 brainstem injury is not well characterized. The present study investigated the recovery process from immediate posttraumatic coma following severe head injury without mass lesions. Materials and Methods This retrospective study included 24 patients aged 3 to 67 years (mean 29.6 years) admitted with closed head injury and immediate prolonged posttraumatic coma (Glasgow Coma Scale [GCS] scores of 4 8 at initial neurological examination and persisting for more than 6 hours) to our hospital from 1994 to 1999 (Table 1). Patients with lower brainstem damage detected by MR imaging were excluded because severe damage to the lower brainstem is probably associated with high mortality. 3) ICP was recorded epidurally in 18 patients, but not in the others becauseoftheabsenceoflesionsontheinitialct. Continuous ICP monitoring was performed for at least 7 days. Patients with ICP exceeding 20 mmhg over 24 hours were also excluded. All 24 patients were admitted to our hospital 614

2 Recovery Process of Posttraumatic Coma by DAI 615 Table 1 Clinical features of the 24 patients Case No. Age (yrs) Sex CT classification by TCDB Initial GCS Follow-up period (days) Final GOS 1 33 M DI I 7 87 GR 2 23 M DI II 6 99 MD 3 26 M DI I GR 4 18 M DI II GR 5 67 M DI II GR 6 44 M DI II GR 7 18 M DI I MD 8 47 M DI II GR 9 7 M DI II GR 10 7 M DI I GR 11 3 M DI II GR F DI II VS M DI II GR M DI I GR M DI II GR M DI II GR M DI II GR M DI II MD M DI II GR 20 6 F DI I GR F DI II GR M DI II GR M DI II GR M DI II GR CT: computed tomography, DI I: diffuse injury type I, DI II: diffuse injury type II, GCS: Glasgow Coma Scale, GOS: Glasgow Outcome Scale, GR: good recovery, MD: moderately disabled, TCDB: Traumatic Coma Data Bank, VS: vegetative state. within 2 hours of head injury. Traffic accident was the cause in all patients. Ten patients presented with multi-system trauma. No patient had documented respiratory or cardiac arrest, and none had documented hypoxia (O 2 saturation less than 90% for over 5 minutes). No patient needed intubation. The mean initial GCS was 7.0. No patient had a documented lucid interval. Initial CT was performed immediately after admission. Follow-up CT was performed 2 hours after initial CT. Six patients had diffuse injury type I and 18 patients had type II, based on the CT classification of the TCDB. 4) T 2 -weighted spin-echo MR imaging (1.5 T) was performed within the first 7 days (mean interval 2.3 days) after admission for all patients. The midline and brainstem were investigated with 5 mm sagittal plane slices. Finally, a coronal section was obtained. Two neuroradiologists unaware of the patient details independently evaluated the MR images and noted all foci of abnormal hyper- and hypointensity in the brain, which were recorded as DAI signals. VerycloseDAIsignalswerecountedasonesignal. The number and location (gray matter, white matter, corpus callosum [genu, body, and splenium], basal ganglia or thalamus, dorsal upper brainstem, cerebellum) of each DAI signal were recorded. The recovery process was evaluated using the Glasgow Outcome Scale (GOS) by two neurologists during hospitalization. After discharge, evaluations were obtained through telephone interviews with the guardians or parents of the patients. To minimize errors in the estimates of patient status, the interviews with guardians and parents were structured to obtain yes or no answers to specific questions as well as to provide descriptions of the patient's behavior and progress within a given category. The period of recovery from the head trauma to moderately disabled (MD) of the GOS was defined as phase 1. The period of recovery from MD to good recovery (GR) of the GOS was defined as phase 2 (Fig. 1). The follow-up period of this study was 87 to 1,845 days (mean days) (Table 1). Results Twenty of the 24 patients recovered to GR in the follow-up period. Three only recovered to MD. One patient remained in the vegetative state (VS) during

3 616 T. Wada et al. Fig. 1 Criteria for phase 1 and phase 2 in the recovery process of posttraumatic coma. Phase 1 was the period from the head trauma to moderately disabled (MD) of the Glasgow Outcome Scale (GOS). Phase 2 was the period from MD to good recovery (GR) of the GOS. Fig. 3 Phase 2 of each case according to length. Cases could be divided into short phase 2 (Cases 1, 3 5, 10, 11, 16, and 19 24) and long phase 2 (Cases 6, 8, 9, 13 15, and 17). **Phase 2 of Cases 2, 7, 12, and 18 were not recorded because these patients did not recover to good recovery. Fig. 2 Phase 1 of each case according to length. *Phase 1 of Case 12 was not recorded because she remained in vegetative state. the follow-up period (Table 1). Poor outcome was defined as comparatively severe problems with higher functions such as memory and/or intellectual deficits, which resulted in final evaluation as MD or VS. Phase 1 of recovery ranged from 1 to 750 days, with a median 21.0 and mean 50.0 days (Fig. 2). Phase 1 of Case 12 was not recorded because she remained in VS. Phase 2 ranged from 1 to 450 days, with mean 52.0 days (Fig. 3). Phase 2 of Cases 2, 7, 12, and 18 were not recorded because these patients did not recover to GR. Figure 3 reveals that the 20 patients recovering to GR could be classified into two subgroups, 13 patients with phase 2 of under 10 days and seven with phase 2 of over 60 days. All patients in phase 2 had mild disturbance of consciousness, so were judged to be MD. Table 2 shows the locations of the abnormal lesions detected by MR imaging. The number of lesions ranged from two to 10, with a mean of five. DAI lesions were most common in the frontal lobe and only one patient had lesions in the cerebral area other than the frontal lobe. Eight patients had lesions in only white matter and two had lesions in only gray matter. Two patients had lesions in the putamen, and two in the thalamus. Six patients had lesions in the cerebral peduncle associated with lesions of the dorsal upper brainstem. Three patients had lesions of the cerebellum, all in white matter. The poor outcome group had a significantly higher frequency of lesions in the dorsal upper brainstem than did patients with GR (p º 0.05, Fisher's exact test). There was no significant difference in the frequency of lesions in other areas (Table 3). The most common combination of injury in the poor outcome group was callosal splenium and dorsal upper brainstem injury (p º 0.01, Fisher's exact test; odds ratio 66.6, 95% confidence interval ). Patients in the GR group with phase 2 of over 60 days had more DAI lesions significantly than patients with phase 2 of under 10 days (p º 0.05, Mann-Whitney-U rank sum test). No significant correlation was found between phase 2 of over 60 days and location of DAI lesions (Table 4).

4 Recovery Process of Posttraumatic Coma by DAI 617 Table 2 Distribution of abnormal signals on T 2 -weighted magnetic resonance images Case No. Corpus callosum Genu Body Splenium Basal ganglia or thalamus Cerebral gray and white matter Dorsal upper brainstem Cerebellum Total Table 3 Magnetic resonance imaging lesions in patients with good recovery and poor outcome* Good recovery (n=20) No. of lesions Poor outcome (n=4) Odds ratio (95% CI) Probability Corpus callosum ( ) 1 Genu ( ) 1 Body ( ) 0.58 Splenium ( ) 0.09 Basal ganglia or thalamus ( ) 1 Cerebral gray and white matter ( ) 1 Dorsal upper brainstem ( ) º0.05 Cerebellum ( ) 0.54 Mean±SD 5.0± ± *No recovery to good recovery of Glasgow Outcome Scale in the follow-up period. Whitney-U rank sum test. CI: confidence interval, SD: standard deviation. Fisher's exact test, Mann- Discussion DAI has been recognized since ) DAI is caused by shearing or tensile strains at the time of injury, when different structures move relative to one another. 1,6,7) MR imaging has clearly demonstrated evidence of DAI in patients with severe head injury. Coma caused by DAI is described as immediate posttraumatic coma and prolonged traumatic coma. 5) The TCDB group found that the mortality of

5 618 T. Wada et al. Table 4 Magnetic resonance imaging lesions in patients with phase 2 of under 10 days and over 60 days Groupwithphase2 under 10 days (n=13) No. of lesions Groupwithphase2 over 60 days (n=7) Odds ratio (95% CI) Probability Corpus callosum ( ) 1 Genu ( ) 0.52 Body ( ) 0.35 Splenium ( ) 0.36 Basal ganglia or thalamus ( ) 0.10 Cerebral gray and white matter ( ) 0.37 Dorsal upper brainstem ( ) 1 Cerebellum ( ) 0.52 Mean±SD 3.6± ±3.2 º0.05 Fisher's exact test, Mann-Whitney-U rank sum test. CI: confidence interval, SD: standard deviation. diffuse injury type I and II is 9.6% and 13.5%, not 0%. 18) Consequently, better understanding of the recovery process of posttraumatic coma can affect the early management for patients with DAI. Patients with no abnormal CT findings have a better outcome than patients with diffuse brain swelling. 17,23) Patients with traumatic hyperextension of the head may have both DAI and lesions of lower brainstem caused by direct impact and not shearing. 2,9,16) Mortality is significantly higher in patients with lower brainstem lesions than in patients with DAI of the upper brainstem. 3) Therefore, investigation of the recovery process of traumatic coma due to DAI must exclude patients with either elevated ICP or lower brainstem injury. In this study, the recovery process was separated into phase 1 and phase 2. Neuropsychological dysfunctions are often caused by head injury. Our patients in phase 2 had mild disturbance of consciousness and, therefore, were judged to be MD. The present study suggests that prolonged traumatic coma caused by DAI will recover in about 3weeks. Four patients including one patient in VS had persistent disturbance of consciousness in this study. These patients had a significantly higher number of lesions in the brainstem and callosal splenium compared with patients with good outcome. The combination of focal lesions in the corpus callosum and the dorsolateral brainstem is the most common pattern associated with persistent VS after head injury. 8,10 12) However, whether specific combinations of cerebral lesions contribute to persistent VS remains unknown. In this study, a phase 2 of over 60 days corresponded to extended transient disturbance of consciousness. Patients with long phase 2 had more DAI lesions than patients with short phase 2. We suppose that the finding of many DAI lesions may indicate widespread injuries to the brain and, therefore, disturbance of consciousness continues for a long period. However, disturbance of consciousness might recover if there is no lesion of the corpus callosum or dorsolateral brainstem. Persistent neuropsychological dysfunction have been reported following severe head injury. 13,14,20,24) In this study, neuropsychological examinations were not performed, so some patients who were judged as GR may have had neuropsychological dysfunctions. Focal lesions in the corpus callosum and dorsolateral brainstem may be associated with persistent conscious dysfunction, and widespread lesions in the brain with prolonged conscious dysfunction. Acknowledgment This work was supported by grants (No ) from The General Insurance Association of Japan. References 1) Adams JH, Graham DI, Murray LS, Scott G: Diffuse axonal injury due to nonmissile head injury in humans: An analysis of 45 cases. Ann Neurol 12: , ) Bhatoe HS: Primary brain injury: Benign course and improved survival. Acta Neurochir (Wien) 141: , ) Firsching R, Woischneck D, Diedrich M, Klein S, Räuckert A, Wittig H, Däohring W: Early magnetic resonance imaging of brainstem lesions after severe head injury. JNeurosurg89: , ) Foulkes MA, Eisenberg HM, Jane JA, Marmarou A, Marshall LF, and the Traumatic Coma Data Bank Research Group: The Traumatic Coma Data Bank:

6 Recovery Process of Posttraumatic Coma by DAI 619 design, methods, and baseline characteristics. J Neurosurg 75 (Suppl): S8 S13, ) Gennarelli TA: Emergency department management of head injuries. Emerg Med Clin North Am 2: , ) Gennarelli TA: Mechanisms of brain injury. JEmerg Med 11 (Suppl 1): 5 11, ) Gennarelli TA, Thibault LE, Adams JH, Graham DI, Thompson CJ, Marcincin RP: Diffuse axonal injury and traumatic coma in the primate. Ann Neurol 12: , ) Gentry LR, Godersky JC, Thompson B: MR imaging of head trauma: review of the distribution and radiopathologic features of traumatic lesions. AJR Am J Roentgenol 150: , ) Hardman JM: The pathology of traumatic brain injuries. Adv Neurol 22: 15 50, ) Hoelper BM, Soldner F, Chone L, Wallenfang T: Effect of intracerebral lesions detected in early MRI on outcome after acute brain injury. Acta Neurochir Suppl 76: , ) Kampehl A, Franz G, Aichner F, Pfausler B, Haring HP, Felber S, Luz G, Schocke M, Schmutzhard E: The persistent vegetative state after closed head injury: clinical and magnetic resonance imaging findings in 42 patients. J Neurosurg 88: , ) Kampfl A, Schmutzhard E, Franz G, Pfausler B, Haring HP, Ulmer H, Felber S, Golaszewski S, Aichner F: Prediction of recovery from post-traumatic vegetative state with cerebral magnetic-resonance imaging. Lancet 351: , ) Keren O, Ben-Dror S, Stern MJ, Goldberg G, Groswasser Z: Event-related potentials as an index of cognitive function during recovery from severe closed head injury. JHeadTraumaRehabil13: 15 30, ) Lannoo E, Van Rietvelde F, Colardyn F, Lemmerling M, Vandekerckhove T, Jannes C, De Soete G: Early predictors of mortality and morbidity after severe closed head injury. JNeurotrauma17: , ) Levi L, Guilburd JN, Lemberger A, Soustiel JF, Feinsod M: Diffuse axonal injury: analysis of 100 patients with radiological signs. Neurosurgery 27: , ) Lindenberg R, Freytag E: Brainstem lesions characteristic of traumatic hyperextension of the head. Arch Pathol 90: , ) Marshall LF, Gautille T, Mlauber MR, Eisenberg HM, Jane JA, Luerssen TG, Marmarou A, Foulkes MA: The outcome of severe closed head injury. J Neurosurg 75 (Suppl): S28 S36, ) Marshall LF, Marhsall SB, Klauber MR, van Berkum Clark M, Eisenberg HM, Jane JA, Luerssen TG, Marmarou A, Foulkes MA: A new classification of head injury based on computerized tomography. J Neurosurg 75 (Suppl): S14 S20, ) Mittl RL, Grossman RI, Hiehle RW, Kauder HDR, Gennarelli TA, Alburger GW: Prevalence of MR evidence of diffuse axonal injury in patients with mild head injury and normal head CT findings. AJNR Am J Neuroradiol 15: , ) Schoenhuber R, Gentilini M: Auditory brain stem responses in the prognosis of late postconcussional symptoms and neuropsychological dysfunction after minor head injury. Neurosurgery 19: , ) Smith DH, Nonaka M, Miller R, Leoni M, Chen XH, Alsop D, Meaney DF: Immediate coma following inertial brain injury dependent on axonal damage in the brainstem. J Neurosurg 93: , ) Strich SJ: Diffuse degeneration of the cerebral white matter in severe dementia following head injury. J Neurol Neurosurg Psychiatry 19: , ) Tomei G, Sganzerla E, Spagnoli D, Guerra P, Lucarini C, Gaini SM, Villani R: Posttraumatic diffuse cerebral lesions. Relationship between clinical course, CT findings and ICP. J Neurosurg Sci 35: 61 75, ) Uzzell BP, Obrist WD, Dolinskas CA, Langfitt TW: Relationship of acute CBF and ICP findings to neuropsychological outcome in severe head injury. J Neurosurg 65: , 1986 Address reprint requests to: T.Wada,M.D.,Departmentof Neurosurgery, Iwate Medical University, 19 1 Uchimaru, Morioka, Iwate , Japan. twada@iwate-med.ac.jp Commentary The authors report on an extremely interesting investigation of 24 patients after head injury. Magnetic resonance imaging (MRI) proved to be of high predictive value. Four out of 24 patients with lesions of the corpus callosum and the dorsal upper brain stem turned out to have a poor outcome. The authors are to be congratulated on this careful study. The idea of a diffuse axonal injury had been coined in 1956 by Strich. 4) In the 1980s Adams and coworkers 1) attached much clinical significance to this histological phenomenon, but he insisted in 1982 that diffuse axonal injury could only be diagnosed by someone who can look at axons, the neuropathologist. Disregarding this reasonable claim, Gennarelli 3) in 1982 suggested to call any head injury with a minimum of 6 hours of coma a ``diffuse brain injury,'' when the corresponding computerized tomography (CT) scan did not show a mass lesion. The authors of this paper now claim ``MR imaging has clearly demonstrated evidence of diffuse axonal injury in patients with severe head injury,'' on the other hand the hallmark of a poor outcome in this series was reported to be ``focal lesions of the brain stem and the corpus callosum.'' We must humbly and in a matter-of-fact-manner acknowledge that neither CT nor MRI can identify

7 620 T. Wada et al. singular axons. To infer diffuse axonal injury from CT or MRI is therefore clearly an act of speculation. In a similar study on comatose patients after head injury we 2) found lesions of the corpus callosum in survivors as often as in non-survivors. Thus lesions of the corpus callosum cannot be of high significance in terms of mortality. The brain stem lesions, however, were highly significantly correlated with morbidity and mortality. It is very reassuring to realize this scrupulous paper confirms the importance of the brain stem. References 1) Adams JH, Graham DI, Murray LS, Scott G: Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann Neurol 12: , ) Firsching R, Woischneck D, Klein S, Reissberg S, Dohring W, Peters B: Classification of severe head injury based on magnetic resonance imaging. Acta Neurochir (Wien) 143: , ) Gennarelli T: Cerebral concussion and diffuse brain injuries, in Cooper P (ed): Head Injury. Baltimore, London, Williams & Wilkins, 1982, pp ) Strich SJ: Diffuse degeneration of the cerebral white matter in severe dementia following head injury. J Neurol Neurosurg Psychiatry 19: , 1956 Raimund FIRSCHING, M.D., L.R.C.P., M.R.C.S. Klinik f äur Neurochirurgie Otto-von-Guericke-Universit äat Magdeburg, Germany The paper by Wada and colleagues addresses the problem of relatively ``pure'' diffuse axonal injury (DAI) following traumatic brain injury. To examine this particular type of head-injured patients, the authors excluded comatose patients who had intracranial hypertension, intracranial hemorrhage or lower brainstem injury on MR imaging. By excluding these factors, which predict poorer outcomes, they had a group of patients whose predominant or only injury was DAI. Interestingly this particular subgroup had quite good outcomes. Only one of their twentyfour patients remained in a vegetative state for longer than two years, and sixteen had achieved a good outcome within about three weeks. Given that only 2 of the 24 patients had motor posturing on their initial Glasgow Coma Scale, these good outcomes would be expected. MR images done within a week of injury showed all four of the patients who never achieved a good outcome (3 remained moderately disabled and 1 was vegetative) had lesions in the dorsal upper brainstem. However, five of the 20 with good outcomes also had MRI changes there and so the dorsal midbrain lesion alone does not produce poor outcome. All of the poor outcome patients also had MRI abnormalities in the splenium of the corpus callosum, whereas only one of the 20 good outcome patients had this combination. Why this combination is important prognostically is not obvious. One other interesting group emerged from this study, i.e. those who remained in a moderately disabled state for two months or longer before achieving a good outcome. The authors carefully analyzed their data looking for an explanation and found only that prolonged moderate disability was accompanied by a greaternumberofmrilesionsbutdistributionwas not clearly important. It is reassuring that DAI patients with no other radiographic indication of brain injury almost always achieve a good outcome, albeit with considerable delay in many. Evaluation of T2-weighted MRIs in these patients suggests that some particular areas of brain injury may be important, but a number of questions remain. Perhaps additional MRI sequences such as diffusion studies or injury to specific fiber tracts will shed new light on the pathophysiology of this interesting traumatic brain injury diagnosis. Lawrence H. PITTS, M.D. Neurosurgery University of California San Francisco San Francisco, California, U.S.A.

The significance of traumatic haematoma in the

Journal of Neurology, Neurosurgery, and Psychiatry 1986;49:29-34 The significance of traumatic haematoma in the region of the basal ganglia P MACPHERSON, E TEASDALE, S DHAKER, G ALLERDYCE, S GALBRAITH