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Significance of minor traumatic lesions in focal head injuries
Journal of Clinical Neuroscience 18 (2011) 520–523
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Significance of minor traumatic lesions in focal head injuries Youichi Yanagawa ⇑, Toshihisa Sakamoto Department of Traumatology and Critical Care Medicine, National Defense Medical College (NDMC), 3-2 Namiki, Tokorozawa, Saitama 359-8513, Japan
a r t i c l e
i n f o
Article history: Received 24 May 2010 Accepted 30 July 2010
Keywords: Acute epidural hematoma Acute subdural hematoma Axonal injury Contusion Outcome T2⁄-weighted MRI
a b s t r a c t We investigated the significance of minor traumatic lesions associated with focal head injuries. Patients included in the study were admitted between January 2003 and December 2007 and had sustained a head injury with focal injury and undergone MRI examination including T2⁄-weighted imaging. Patients were divided into two groups: (i) a T2⁄-positive group – those who had hypointense lesions at sites other than the original injury site as shown by T2⁄-weighted MRI (n = 12); and (ii) a control group without hypointense lesions at sites other than the original injury (n = 25). The median Glasgow Outcome Scale score was significantly lower in the T2⁄-positive group (median = 4; range = 4–5) than in the control group (median = 5; range = 4–5; p = 0.003). We conclude that patients with a focal head injury and minor traumatic lesions are likely to have a poorer prognosis than patients without additional minor traumatic lesions. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Prognostic factors associated with focal head injuries, including cerebral contusion and acute subdural and epidural hematoma, are: level of unconsciousness, pupil abnormality, age, abnormal vital signs (hypotension and/or hypoxia), CT scan appearance and/or intracranial pressure.1–5 In contrast, prognostic factors associated with diffuse axonal injuries include level of consciousness and MRI scan appearance, particularly in diffusion tensor tractography, diffusion-weighted imaging, fluid-attenuated inversion recovery, susceptibility-weighted imaging and T2⁄-weighted imaging.6–10 We investigated focal head injuries using T2⁄-weighted MRI and determined that some focal head injuries, such as cerebral contusion, acute subdural hematoma and/or epidural hematoma, occur in association with minor traumatic lesions at sites distinct from the original injured area.11,12 No previous study has investigated the significance of minor traumatic lesions in patients with focal head injuries. We retrospectively investigated whether minor traumatic lesions in focal head injuries are clinically significant.
2. Materials and methods The study protocol was approved by our institutional review board, and examinations were conducted according to the standards of good clinical practice and the Declaration of Helsinki. We reviewed the medical records of patients admitted between January 2003 and December 2007. Patients with a head injury with ⇑ Corresponding author. Tel.: +81 04 2995 1888; fax: +81 04 2996 5221. E-mail address: [email protected] (Y. Yanagawa). 0967-5868/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2010.07.133
cerebral contusion, subdural hematoma and/or epidural hematoma, who had undergone MRI examination including T2⁄weighted imaging during hospitalization, were included in the series. Cerebral contusion was defined as a high- or mixed-density area >1 cm2 on a CT scan, which included the cerebral cortex or cerebellum. Patients aged >60 years were excluded from the present series, as elderly individuals may have asymptomatic microhemorrhages.13 Patients who died from their head injuries were also excluded. Patients were divided into two groups: (i) a T2⁄-positive group with hypointense lesions detected by T2⁄-weighted gradient echoweighted imaging (T2⁄-WI) in locations other than the original injury site; and (ii) a control group who did not show hypointense lesions other than at the original injury site. Indications for obtaining MRI at our institution included prolonged unconsciousness for >24 hours without the need for life-saving equipment, such as mechanical ventilation. Axial T2⁄-WI was performed using the following parameters: repetition time, 900 ms; echo time, 30 ms; excitations, 2; flip angle, 200°; matrix, 256 192; section thickness, 5 mm with a 2.5 mm gap; and imaging time, 2 min 56 s. All foci >1 mm in size with hypointensities on T2⁄-WI were defined as lesions, excluding lesions in the globus pallidus, which contained physiologically calcified deposits, and visible calcification on CT scans. In our department, indications for surgery depend heavily on the patient’s eye score on the Glasgow Coma Scale (GCS) score. Similar to the ‘‘alert verbal painful unresponsive’’ scale, eye response to stimulation is important in determining indications.14 Indications for acute epidural hematoma included patients who demonstrated both a GCS score of E3 or lower, and a hematoma with a width >2 cm or one that had caused a midline shift. Surgical
Y. Yanagawa, T. Sakamoto / Journal of Clinical Neuroscience 18 (2011) 520–523 Table 1 Details of 469 patients with head injuries who were admitted to our department, including all ages and deaths No. patients
Aged over 60 years Brain death due to head injury Intracranial hematoma or cerebral contusion (Patients who underwent MRI examination: subjects in this study 37) Cerebral concussion, simple head injury with other organ injuries Traumatic subarachnoid hemorrhage Isolated skull fracture Isolated diffuse axonal injury Chronic subdural hematoma
138 53 98
97 44 24 13 2
Total
469
521
others for daily support due to mental or physical disability or both; 4 = moderate disability, with the patient independent as far as daily life is concerned; and 5 = good recovery, with resumption of normal activities even though minor neurological or psychological deficits may be present. Investigators evaluating MRI were blinded to patient outcomes, including GOS score. Arousal was defined as the time from admission until the patient could follow simple commands. In addition, the distribution and total number of complicated traumatic lesions were analyzed for patients in the complicated traumatic lesion group. Statistical analysis was performed using the Student’s unpaired t-test, the Mann–Whitney U-test and the chi-squared test. Differences with values of p < 0.05 were considered statistically significant.
The figure above includes the 37 patients in the study.
3. Results indications for acute subdural hematoma included a GCS score of E3 or lower, and hematoma with a width >5 mm or that had caused a midline shift. Surgical indications for cerebral contusion included patients who demonstrated a GCS score of E3 or lower, and contusion with a diameter >3 cm, located in a non-eloquent area. A follow-up head CT scan was routinely performed at least 6 hours, 24 hours and 7 days after injury for any surviving patient with intracranial lesions. The basic Intensive Care Unit protocol for severe head injury care was as follows: the patient’s head was elevated 30° above the horizontal position; mean arterial pressure was maintained at >70 mmHg with systolic pressure between 100 and 170 mmHg; mechanical ventilation was used to maintain the partial pressure of oxygen (PaO2) at 100–150 mmHg and carbon dioxide (PaCO2) at 30–40 mmHg if the patient was intubated; and intravenous infusions of 10% glycerin (600–900 mL/day glycerol; Chugai Pharmaceutical, Tokyo, Japan) with 0.9% NaCl plus 5% fructose solution were administered. After mechanical ventilation was ceased and the patient was stabilized, T2⁄-WI MRI at 1.5 Tesla was performed. The following variables were analyzed between groups: gender; age; mechanism of injury; direction of impact to the head; GCS score at time of arrival; injury severity score (ISS);15 details of head injury pattern as determined by CT scan; number of skull fractures; volume of focal injury; frequency of craniotomy; hospital day on which MRI was performed; duration from admission until arousal; and Glasgow Outcome Scale (GOS) score at 3 months after admission.16 GOS score was scored as: 1 = death; 2 = persistent vegetative state, with the patient exhibiting no obvious cortical function; 3 = severe disability, with the patient dependent upon
During the investigation period, 469 patients with a head injury were admitted to our institution. Details of these patients are shown in Table 1. The T2⁄-positive group comprised 12 patients and there were 25 patients in the control group. The mean number of lesions in the T2⁄-positive group was 3.2 (range = 1–10). Representative imaging studies from a patient with T2⁄-positive lesions, distinct from the focal head injuries, are shown in Figs. 1 and 2. We compared patients with an intracranial hematoma or cerebral contusion who underwent MRI with those who did not (Table 2). No significant differences were apparent between the groups with regard to sex or age. However, the median GCS score was significantly lower in patients who underwent MRI than in patients who did not. The ISS and the total volume of contusion and hematoma were significantly higher in the MRI group than in the non-MRI group. The GOS score for all patients with an intracranial hematoma or cerebral contusion who did not undergo MRI examination was calculated as 5 within 3 months. Conversely, the GOS score of all patients who underwent MRI examination was calculated as 4 or 5 (GOS score = 4 in 10 of 35 patients). The median GOS score was significantly higher in patients who did not undergo MRI than in patients who underwent MRI. No significant differences were apparent between groups regarding sex, age, mechanism of injury, direction of impact to the head, GCS score, ISS, presence of focal head injuries, frequency of skull fracture, volume of focal head injury or frequency of neurosurgical procedure (Table 3). Patient outcomes are shown in Table 4. The time from loss of consciousness to arousal tended to be longer in the T2⁄-positive group than in the control group, but this difference was not
Fig. 1. Axial CT scans showing the time course of a head injury in a 17-year-old female patient: (left) a right acute subdural hematoma; (middle) a left frontal acute epidural hematoma; and (right) a right temporal contusion after evacuation of the hematomas.
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Y. Yanagawa, T. Sakamoto / Journal of Clinical Neuroscience 18 (2011) 520–523
Fig. 2. Day 17 axial T2⁄-weighted MRI of a 17-year-old female patient (same patient as Fig. 1) showing hypointense lesions in the left thalamus, caudate nuclei and corpus callosum. The final Glasgow Outcome Scale score, 3 months after the injury, was 4.
Table 2 Comparison of patients with intracranial hematoma or cerebral contusion who did (MRI+) or did not (MRI ) undergo MRI (n = 98)
Sex (male/female) Age (years) GCS score on arrival (median, range) Injury severity score Total volume of contusion and hematoma (mL) GOS after 3 months (median, range)
MRI+ n = 37
MRI n = 61
p value
23/14 35.4 ± 2.7 12 (3–15) 13.3 ± 0.8 20.2 ± 3.0
44/17 28.8 ± 2.5 14 (6–15) 10.3 ± 0.4 5.9 ± 1.5
NS 0.08 <0.01 0.0004 <0.0001
5 (4–5)
5 (5)
<0.0001
GCS = Glasgow Coma Scale score, GOS = Glasgow Outcome Scale score, NS = not significant. Values represent mean ± standard error of the mean.
Table 4 Between-group statistical comparison of outcome in patients who had hypointense lesions at sites other than the original injury site (T2⁄-weighted MRI-positive group) compared to those who did not (control group)
No. days to arousal after admission GOS over 3 months (median, range) No. days hospitalization in our institution Discharged
T2⁄positive n = 12
Control
3.5 ± 1.3 4 (4–5) 33.9 ± 5.4
1.4 ± 0.5 5 (4–5) 36.9 ± 10.0
0.08 0.003 NS
6 (50%)
21 (84%)
<0.05
p value
n = 25
GOS = Glasgow Outcome Scale score, NS = not significant.
Table 5 Distribution and total number of T2⁄-positive lesions Table 3 Between-group statistical comparison of patients who had hypointense lesions at sites other than the original injury site (T2⁄-weighted MRI-positive group) compared to those who did not (control group)
Sex (male/female) Age, years Cause of injury (%) Traffic accident Fall Direction of impact to head (%) Anterior-posterior Lateral Unknown GCS on arrival (median, range) Injury severity score Head injury pattern on CT scan (%) Isolated cerebral contusion Isolated epidural hematoma Isolated subdural hematoma Combined type Skull fracture Total volume of contusion and hematoma (mL) Craniotomy (%) Hospital day of MRI
T2⁄-positive n = 12
Control n = 25
p value
8/4 38.4 ± 4.8
15/10 33.9 ± 3.2
NS NS NS
10 (83) 2 (17)
17 (68) 8 (32)
6 (50) 5 (42) 1 (8) 10 (3–15) 14.2 ± 1.4
12 (48) 10 (40) 3 (12) 12 (7–15) 12.8 ± 0.9
6 (50) 1 (8) 0 5 (42) 4 (33) 24 ± 5.8
10 (40) 3 (12) 0 12 (48) 8 (32) 18.1 ± 3.6
NS NS
4 (33) 29.5 ± 6.7
4 (16) 19.4 ± 3.6
NS NS
Enlarge to full column width
Total
Frontal white matter Temporal white matter Parietal white matter Thalamus and hypothalamus Occipital white matter Corpus callosum Putamen Caudate nuclei
12 9 4 3 2 2 1 1
NS
NS NS NS
ian GOS score was significantly lower in the T2⁄-positive group (GOS score = 4) than in the control group (GOS score = 5, p = 0.003). The duration of hospitalization did not differ significantly between groups; however, fewer patients were discharged home in the T2⁄-positive group than in the control group (50% v. 84%, p < 0.05). The remaining patients who were not discharged were transferred to another hospital for rehabilitation. Table 5 shows the distribution and total number of T2⁄-positive lesions. T2⁄-positive lesions were predominantly located in either the frontal or temporal white matter. 4. Discussion
Values represent mean ± standard error of the mean. GCS = Glasgow Coma Scale score, NS = not significant.
significant (3.5 days versus [v.] 1.4 days; p = 0.08). All patients achieved a GOS score of 4 or 5 within 3 months. However, the med-
Focal head injuries, such as cerebral contusion or acute epidural and/or subdural hematoma with concomitant minor traumatic lesions, tend to be associated with a poorer prognosis compared to injuries in which other minor traumatic lesions are absent.
Y. Yanagawa, T. Sakamoto / Journal of Clinical Neuroscience 18 (2011) 520–523
Most minor T2⁄-positive lesions associated with focal head injuries are thought to involve axonal injury, as these lesions appeared hypointense on T2⁄-WI and the distribution of minor traumatic lesions is similar to that of diffuse axonal injuries.17,18 Few studies have examined the effects of focal head injuries in combination with axonal injury. Honda et al. previously reported that of five patients with diffuse axonal injuries with lesions in the corpus callosum, deep white matter, periventricular gray matter, pons, midbrain and cerebellum visible on MRI, two also demonstrated a subdural hematoma and cortical contusional hemorrhage.19 In addition, Dixon et al., using a controlled cortical impact model of traumatic brain injury in rats, demonstrated that high injury levels produced cortical contusions and intraparenchymal hemorrhaging in combination with axonal injury.20 Thus, while the combination of focal brain injury and axonal injury may be rare, it does exist. In this study, patients with a focal head injury and an axonal injury tended to have a poorer prognosis than patients without axonal injury. Wallesch et al. reported a comparison of the effects of focal and diffuse axonal injury in mild-to-moderate traumatic brain injuries using neuropsychological assessments 8–31 days after trauma and subsequent assessments 18–45 weeks later.21 Their results indicated that traumatic diffuse axonal injuries largely resulted in transient neuropsychological deficits, and focal contusions resulted in more permanent deficits that affected behaviour at outcome. Accordingly, adding neuropsychological deficits to these behavioural dysfunctions in patients with a focal head injury and axonal injury may result in a worse prognosis compared to patients without axonal injury. However, as the duration of evaluation in this study was shorter than that in the study by Wallesch et al., our long-term follow-up may show decreased differences between patients with focal head injuries with axonal injury and those without. A limitation of the current study was that MRI was not performed for all patients with focal head injuries during the investigation period; therefore, these results may show some bias. In particular, the GOS of all patients who did not undergo the MRI examination was 5 (good recovery), so bias may have affected recovery outcomes. One indication for obtaining MRI in our institution was prolonged unconsciousness (P24 hours) as we have previously found that MRI, including T2⁄-WI, has a low probability of identifying traumatic lesions that have not been found by CT scan.12 The duration of unconsciousness generally correlates with neurological outcomes among patients with head injuries.12 Accordingly, the possibility of finding new lesions using MRI was low in the excluded patients. In addition, if the same frequency of T2⁄-positive findings in patients with a GOS of 5 was applicable to excluded patients who did not undergo MRI, the same statistical tendencies would remain. Accordingly, the bias for patients with good recovery in this study was minimized. The retrospective
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nature and relatively low number of patients in the series are further limitations of this study. Larger prospective studies are warranted to determine whether patients with focal head injuries and minor traumatic lesions show a poorer prognosis than patients without such lesions. References 1. Tasaki O, Shiozaki T, Hamasaki T, et al. Prognostic indicators and outcome prediction model for severe traumatic brain injury. J Trauma 2009;66:304–8. 2. Hukkelhoven CW, Steyerberg EW, Habbema JD, et al. Predicting outcome after traumatic brain injury: development and validation of a prognostic score based on admission characteristics. J Neurotrauma 2005;22:1025–39. 3. Steyerberg EW, Mushkudiani N, Perel P, et al. PLoS Med 2008;5:e165. 4. Immonen RJ, Kharatishvili I, Gröhn H, et al. Quantitative MRI predicts long-term structural and functional outcome after experimental traumatic brain injury. Neuroimage 2009;45:1–9. 5. Servadei F, Piazza GC, Padovani R, et al. ‘‘Pure’’ traumatic cerebral lacerations. A review of 129 cases with long-term follow-up. Neurochirurgia (Stuttg) 1985;28:170–3. 6. Schaefer PW, Huisman TA, Sorensen AG, et al. Diffusion-weighted MR imaging in closed head injury: high correlation with initial glasgow coma scale score and score on modified Rankin scale at discharge. Radiology 2004;233:58–66. 7. Tong KA, Ashwal S, Holshouser BA, et al. Diffuse axonal injury in children: clinical correlation with hemorrhagic lesions. Ann Neurol 2004;56:36–50. 8. Huisman TA, Sorensen AG, Hergan K, et al. Diffusion-weighted imaging for the evaluation of diffuse axonal injury in closed head injury. J Comput Assist Tomogr 2003;27:5–11. 9. Sugiyama K, Kondo T, Oouchida Y, et al. Clinical utility of diffusion tensor imaging for evaluating patients with diffuse axonal injury and cognitive disorders in the chronic stage. J Neurotrauma 2009;26:1879–90. 10. Tong KA, Ashwal S, Holshouser BA, et al. Hemorrhagic shearing lesions in children and adolescents with posttraumatic diffuse axonal injury: improved detection and initial results. Radiology 2003;227:332–9. 11. Yanagawa Y, Sakamoto T, Takasu A, et al. Relationship between maximum intracranial pressure and traumatic lesions detected by T2⁄-weighted imaging in diffuse axonal injury. J Trauma 2009;66:162–5. 12. Yanagawa Y, Tsushima Y, Tokumaru A, et al. A quantitative analysis of head injury using T2⁄-weighted gradient-echo imaging. J Trauma 2000;49:272–7. 13. Blitstein MK, Tung GA. MRI of cerebral microhemorrhages. AJR Am J Roentgenol 2007;189:720–5. 14. Kelly CA, Upex A, Bateman DN. Comparison of consciousness level assessment in the poisoned patient using the alert/verbal/painful/unresponsive scale and the Glasgow Coma Scale. Ann Emerg Med 2004;44:108–13. 15. The abbreviated injury scale: 1990 revision. Des Plaines, IL, USA: Association for the Advancement of Automotive Medicine; 1990. 16. Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975;1:480–4. 17. 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 1988;150:663–72. 18. Blitstein MK, Tung GA. MRI of cerebral microhemorrhages. AJR Am J Roentgenol 2007;189:720–5. 19. Honda E, Tokunaga T, Oshima Y, et al. MRI findings of closed head injury in children; with special reference to the effect of central shearing force. No Shinkei Geka 1992;20:235–42 [In Japanese]. 20. Dixon CE, Clifton GL, Lighthall JW, et al. A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods 1991;39:253–62. 21. Wallesch CW, Curio N, Kutz S, et al. Outcome after mild-to-moderate blunt head injury: effects of focal lesions and diffuse axonal injury. Brain Inj 2001;15:401–12.
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Significance of minor traumatic lesions in focal head injuries Youichi Yanagawa ⇑, Toshihisa Sakamoto Department of Traumatology and Critical Care Medicine, National Defense Medical College (NDMC), 3-2 Namiki, Tokorozawa, Saitama 359-8513, Japan
a r t i c l e
i n f o
Article history: Received 24 May 2010 Accepted 30 July 2010
Keywords: Acute epidural hematoma Acute subdural hematoma Axonal injury Contusion Outcome T2⁄-weighted MRI
a b s t r a c t We investigated the significance of minor traumatic lesions associated with focal head injuries. Patients included in the study were admitted between January 2003 and December 2007 and had sustained a head injury with focal injury and undergone MRI examination including T2⁄-weighted imaging. Patients were divided into two groups: (i) a T2⁄-positive group – those who had hypointense lesions at sites other than the original injury site as shown by T2⁄-weighted MRI (n = 12); and (ii) a control group without hypointense lesions at sites other than the original injury (n = 25). The median Glasgow Outcome Scale score was significantly lower in the T2⁄-positive group (median = 4; range = 4–5) than in the control group (median = 5; range = 4–5; p = 0.003). We conclude that patients with a focal head injury and minor traumatic lesions are likely to have a poorer prognosis than patients without additional minor traumatic lesions. Ó 2010 Elsevier Ltd. All rights reserved.
1. Introduction Prognostic factors associated with focal head injuries, including cerebral contusion and acute subdural and epidural hematoma, are: level of unconsciousness, pupil abnormality, age, abnormal vital signs (hypotension and/or hypoxia), CT scan appearance and/or intracranial pressure.1–5 In contrast, prognostic factors associated with diffuse axonal injuries include level of consciousness and MRI scan appearance, particularly in diffusion tensor tractography, diffusion-weighted imaging, fluid-attenuated inversion recovery, susceptibility-weighted imaging and T2⁄-weighted imaging.6–10 We investigated focal head injuries using T2⁄-weighted MRI and determined that some focal head injuries, such as cerebral contusion, acute subdural hematoma and/or epidural hematoma, occur in association with minor traumatic lesions at sites distinct from the original injured area.11,12 No previous study has investigated the significance of minor traumatic lesions in patients with focal head injuries. We retrospectively investigated whether minor traumatic lesions in focal head injuries are clinically significant.
2. Materials and methods The study protocol was approved by our institutional review board, and examinations were conducted according to the standards of good clinical practice and the Declaration of Helsinki. We reviewed the medical records of patients admitted between January 2003 and December 2007. Patients with a head injury with ⇑ Corresponding author. Tel.: +81 04 2995 1888; fax: +81 04 2996 5221. E-mail address: [email protected] (Y. Yanagawa). 0967-5868/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2010.07.133
cerebral contusion, subdural hematoma and/or epidural hematoma, who had undergone MRI examination including T2⁄weighted imaging during hospitalization, were included in the series. Cerebral contusion was defined as a high- or mixed-density area >1 cm2 on a CT scan, which included the cerebral cortex or cerebellum. Patients aged >60 years were excluded from the present series, as elderly individuals may have asymptomatic microhemorrhages.13 Patients who died from their head injuries were also excluded. Patients were divided into two groups: (i) a T2⁄-positive group with hypointense lesions detected by T2⁄-weighted gradient echoweighted imaging (T2⁄-WI) in locations other than the original injury site; and (ii) a control group who did not show hypointense lesions other than at the original injury site. Indications for obtaining MRI at our institution included prolonged unconsciousness for >24 hours without the need for life-saving equipment, such as mechanical ventilation. Axial T2⁄-WI was performed using the following parameters: repetition time, 900 ms; echo time, 30 ms; excitations, 2; flip angle, 200°; matrix, 256 192; section thickness, 5 mm with a 2.5 mm gap; and imaging time, 2 min 56 s. All foci >1 mm in size with hypointensities on T2⁄-WI were defined as lesions, excluding lesions in the globus pallidus, which contained physiologically calcified deposits, and visible calcification on CT scans. In our department, indications for surgery depend heavily on the patient’s eye score on the Glasgow Coma Scale (GCS) score. Similar to the ‘‘alert verbal painful unresponsive’’ scale, eye response to stimulation is important in determining indications.14 Indications for acute epidural hematoma included patients who demonstrated both a GCS score of E3 or lower, and a hematoma with a width >2 cm or one that had caused a midline shift. Surgical
Y. Yanagawa, T. Sakamoto / Journal of Clinical Neuroscience 18 (2011) 520–523 Table 1 Details of 469 patients with head injuries who were admitted to our department, including all ages and deaths No. patients
Aged over 60 years Brain death due to head injury Intracranial hematoma or cerebral contusion (Patients who underwent MRI examination: subjects in this study 37) Cerebral concussion, simple head injury with other organ injuries Traumatic subarachnoid hemorrhage Isolated skull fracture Isolated diffuse axonal injury Chronic subdural hematoma
138 53 98
97 44 24 13 2
Total
469
521
others for daily support due to mental or physical disability or both; 4 = moderate disability, with the patient independent as far as daily life is concerned; and 5 = good recovery, with resumption of normal activities even though minor neurological or psychological deficits may be present. Investigators evaluating MRI were blinded to patient outcomes, including GOS score. Arousal was defined as the time from admission until the patient could follow simple commands. In addition, the distribution and total number of complicated traumatic lesions were analyzed for patients in the complicated traumatic lesion group. Statistical analysis was performed using the Student’s unpaired t-test, the Mann–Whitney U-test and the chi-squared test. Differences with values of p < 0.05 were considered statistically significant.
The figure above includes the 37 patients in the study.
3. Results indications for acute subdural hematoma included a GCS score of E3 or lower, and hematoma with a width >5 mm or that had caused a midline shift. Surgical indications for cerebral contusion included patients who demonstrated a GCS score of E3 or lower, and contusion with a diameter >3 cm, located in a non-eloquent area. A follow-up head CT scan was routinely performed at least 6 hours, 24 hours and 7 days after injury for any surviving patient with intracranial lesions. The basic Intensive Care Unit protocol for severe head injury care was as follows: the patient’s head was elevated 30° above the horizontal position; mean arterial pressure was maintained at >70 mmHg with systolic pressure between 100 and 170 mmHg; mechanical ventilation was used to maintain the partial pressure of oxygen (PaO2) at 100–150 mmHg and carbon dioxide (PaCO2) at 30–40 mmHg if the patient was intubated; and intravenous infusions of 10% glycerin (600–900 mL/day glycerol; Chugai Pharmaceutical, Tokyo, Japan) with 0.9% NaCl plus 5% fructose solution were administered. After mechanical ventilation was ceased and the patient was stabilized, T2⁄-WI MRI at 1.5 Tesla was performed. The following variables were analyzed between groups: gender; age; mechanism of injury; direction of impact to the head; GCS score at time of arrival; injury severity score (ISS);15 details of head injury pattern as determined by CT scan; number of skull fractures; volume of focal injury; frequency of craniotomy; hospital day on which MRI was performed; duration from admission until arousal; and Glasgow Outcome Scale (GOS) score at 3 months after admission.16 GOS score was scored as: 1 = death; 2 = persistent vegetative state, with the patient exhibiting no obvious cortical function; 3 = severe disability, with the patient dependent upon
During the investigation period, 469 patients with a head injury were admitted to our institution. Details of these patients are shown in Table 1. The T2⁄-positive group comprised 12 patients and there were 25 patients in the control group. The mean number of lesions in the T2⁄-positive group was 3.2 (range = 1–10). Representative imaging studies from a patient with T2⁄-positive lesions, distinct from the focal head injuries, are shown in Figs. 1 and 2. We compared patients with an intracranial hematoma or cerebral contusion who underwent MRI with those who did not (Table 2). No significant differences were apparent between the groups with regard to sex or age. However, the median GCS score was significantly lower in patients who underwent MRI than in patients who did not. The ISS and the total volume of contusion and hematoma were significantly higher in the MRI group than in the non-MRI group. The GOS score for all patients with an intracranial hematoma or cerebral contusion who did not undergo MRI examination was calculated as 5 within 3 months. Conversely, the GOS score of all patients who underwent MRI examination was calculated as 4 or 5 (GOS score = 4 in 10 of 35 patients). The median GOS score was significantly higher in patients who did not undergo MRI than in patients who underwent MRI. No significant differences were apparent between groups regarding sex, age, mechanism of injury, direction of impact to the head, GCS score, ISS, presence of focal head injuries, frequency of skull fracture, volume of focal head injury or frequency of neurosurgical procedure (Table 3). Patient outcomes are shown in Table 4. The time from loss of consciousness to arousal tended to be longer in the T2⁄-positive group than in the control group, but this difference was not
Fig. 1. Axial CT scans showing the time course of a head injury in a 17-year-old female patient: (left) a right acute subdural hematoma; (middle) a left frontal acute epidural hematoma; and (right) a right temporal contusion after evacuation of the hematomas.
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Y. Yanagawa, T. Sakamoto / Journal of Clinical Neuroscience 18 (2011) 520–523
Fig. 2. Day 17 axial T2⁄-weighted MRI of a 17-year-old female patient (same patient as Fig. 1) showing hypointense lesions in the left thalamus, caudate nuclei and corpus callosum. The final Glasgow Outcome Scale score, 3 months after the injury, was 4.
Table 2 Comparison of patients with intracranial hematoma or cerebral contusion who did (MRI+) or did not (MRI ) undergo MRI (n = 98)
Sex (male/female) Age (years) GCS score on arrival (median, range) Injury severity score Total volume of contusion and hematoma (mL) GOS after 3 months (median, range)
MRI+ n = 37
MRI n = 61
p value
23/14 35.4 ± 2.7 12 (3–15) 13.3 ± 0.8 20.2 ± 3.0
44/17 28.8 ± 2.5 14 (6–15) 10.3 ± 0.4 5.9 ± 1.5
NS 0.08 <0.01 0.0004 <0.0001
5 (4–5)
5 (5)
<0.0001
GCS = Glasgow Coma Scale score, GOS = Glasgow Outcome Scale score, NS = not significant. Values represent mean ± standard error of the mean.
Table 4 Between-group statistical comparison of outcome in patients who had hypointense lesions at sites other than the original injury site (T2⁄-weighted MRI-positive group) compared to those who did not (control group)
No. days to arousal after admission GOS over 3 months (median, range) No. days hospitalization in our institution Discharged
T2⁄positive n = 12
Control
3.5 ± 1.3 4 (4–5) 33.9 ± 5.4
1.4 ± 0.5 5 (4–5) 36.9 ± 10.0
0.08 0.003 NS
6 (50%)
21 (84%)
<0.05
p value
n = 25
GOS = Glasgow Outcome Scale score, NS = not significant.
Table 5 Distribution and total number of T2⁄-positive lesions Table 3 Between-group statistical comparison of patients who had hypointense lesions at sites other than the original injury site (T2⁄-weighted MRI-positive group) compared to those who did not (control group)
Sex (male/female) Age, years Cause of injury (%) Traffic accident Fall Direction of impact to head (%) Anterior-posterior Lateral Unknown GCS on arrival (median, range) Injury severity score Head injury pattern on CT scan (%) Isolated cerebral contusion Isolated epidural hematoma Isolated subdural hematoma Combined type Skull fracture Total volume of contusion and hematoma (mL) Craniotomy (%) Hospital day of MRI
T2⁄-positive n = 12
Control n = 25
p value
8/4 38.4 ± 4.8
15/10 33.9 ± 3.2
NS NS NS
10 (83) 2 (17)
17 (68) 8 (32)
6 (50) 5 (42) 1 (8) 10 (3–15) 14.2 ± 1.4
12 (48) 10 (40) 3 (12) 12 (7–15) 12.8 ± 0.9
6 (50) 1 (8) 0 5 (42) 4 (33) 24 ± 5.8
10 (40) 3 (12) 0 12 (48) 8 (32) 18.1 ± 3.6
NS NS
4 (33) 29.5 ± 6.7
4 (16) 19.4 ± 3.6
NS NS
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Total
Frontal white matter Temporal white matter Parietal white matter Thalamus and hypothalamus Occipital white matter Corpus callosum Putamen Caudate nuclei
12 9 4 3 2 2 1 1
NS
NS NS NS
ian GOS score was significantly lower in the T2⁄-positive group (GOS score = 4) than in the control group (GOS score = 5, p = 0.003). The duration of hospitalization did not differ significantly between groups; however, fewer patients were discharged home in the T2⁄-positive group than in the control group (50% v. 84%, p < 0.05). The remaining patients who were not discharged were transferred to another hospital for rehabilitation. Table 5 shows the distribution and total number of T2⁄-positive lesions. T2⁄-positive lesions were predominantly located in either the frontal or temporal white matter. 4. Discussion
Values represent mean ± standard error of the mean. GCS = Glasgow Coma Scale score, NS = not significant.
significant (3.5 days versus [v.] 1.4 days; p = 0.08). All patients achieved a GOS score of 4 or 5 within 3 months. However, the med-
Focal head injuries, such as cerebral contusion or acute epidural and/or subdural hematoma with concomitant minor traumatic lesions, tend to be associated with a poorer prognosis compared to injuries in which other minor traumatic lesions are absent.
Y. Yanagawa, T. Sakamoto / Journal of Clinical Neuroscience 18 (2011) 520–523
Most minor T2⁄-positive lesions associated with focal head injuries are thought to involve axonal injury, as these lesions appeared hypointense on T2⁄-WI and the distribution of minor traumatic lesions is similar to that of diffuse axonal injuries.17,18 Few studies have examined the effects of focal head injuries in combination with axonal injury. Honda et al. previously reported that of five patients with diffuse axonal injuries with lesions in the corpus callosum, deep white matter, periventricular gray matter, pons, midbrain and cerebellum visible on MRI, two also demonstrated a subdural hematoma and cortical contusional hemorrhage.19 In addition, Dixon et al., using a controlled cortical impact model of traumatic brain injury in rats, demonstrated that high injury levels produced cortical contusions and intraparenchymal hemorrhaging in combination with axonal injury.20 Thus, while the combination of focal brain injury and axonal injury may be rare, it does exist. In this study, patients with a focal head injury and an axonal injury tended to have a poorer prognosis than patients without axonal injury. Wallesch et al. reported a comparison of the effects of focal and diffuse axonal injury in mild-to-moderate traumatic brain injuries using neuropsychological assessments 8–31 days after trauma and subsequent assessments 18–45 weeks later.21 Their results indicated that traumatic diffuse axonal injuries largely resulted in transient neuropsychological deficits, and focal contusions resulted in more permanent deficits that affected behaviour at outcome. Accordingly, adding neuropsychological deficits to these behavioural dysfunctions in patients with a focal head injury and axonal injury may result in a worse prognosis compared to patients without axonal injury. However, as the duration of evaluation in this study was shorter than that in the study by Wallesch et al., our long-term follow-up may show decreased differences between patients with focal head injuries with axonal injury and those without. A limitation of the current study was that MRI was not performed for all patients with focal head injuries during the investigation period; therefore, these results may show some bias. In particular, the GOS of all patients who did not undergo the MRI examination was 5 (good recovery), so bias may have affected recovery outcomes. One indication for obtaining MRI in our institution was prolonged unconsciousness (P24 hours) as we have previously found that MRI, including T2⁄-WI, has a low probability of identifying traumatic lesions that have not been found by CT scan.12 The duration of unconsciousness generally correlates with neurological outcomes among patients with head injuries.12 Accordingly, the possibility of finding new lesions using MRI was low in the excluded patients. In addition, if the same frequency of T2⁄-positive findings in patients with a GOS of 5 was applicable to excluded patients who did not undergo MRI, the same statistical tendencies would remain. Accordingly, the bias for patients with good recovery in this study was minimized. The retrospective
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nature and relatively low number of patients in the series are further limitations of this study. Larger prospective studies are warranted to determine whether patients with focal head injuries and minor traumatic lesions show a poorer prognosis than patients without such lesions. References 1. Tasaki O, Shiozaki T, Hamasaki T, et al. Prognostic indicators and outcome prediction model for severe traumatic brain injury. J Trauma 2009;66:304–8. 2. Hukkelhoven CW, Steyerberg EW, Habbema JD, et al. Predicting outcome after traumatic brain injury: development and validation of a prognostic score based on admission characteristics. J Neurotrauma 2005;22:1025–39. 3. Steyerberg EW, Mushkudiani N, Perel P, et al. PLoS Med 2008;5:e165. 4. Immonen RJ, Kharatishvili I, Gröhn H, et al. Quantitative MRI predicts long-term structural and functional outcome after experimental traumatic brain injury. Neuroimage 2009;45:1–9. 5. Servadei F, Piazza GC, Padovani R, et al. ‘‘Pure’’ traumatic cerebral lacerations. A review of 129 cases with long-term follow-up. Neurochirurgia (Stuttg) 1985;28:170–3. 6. Schaefer PW, Huisman TA, Sorensen AG, et al. Diffusion-weighted MR imaging in closed head injury: high correlation with initial glasgow coma scale score and score on modified Rankin scale at discharge. Radiology 2004;233:58–66. 7. Tong KA, Ashwal S, Holshouser BA, et al. Diffuse axonal injury in children: clinical correlation with hemorrhagic lesions. Ann Neurol 2004;56:36–50. 8. Huisman TA, Sorensen AG, Hergan K, et al. Diffusion-weighted imaging for the evaluation of diffuse axonal injury in closed head injury. J Comput Assist Tomogr 2003;27:5–11. 9. Sugiyama K, Kondo T, Oouchida Y, et al. Clinical utility of diffusion tensor imaging for evaluating patients with diffuse axonal injury and cognitive disorders in the chronic stage. J Neurotrauma 2009;26:1879–90. 10. Tong KA, Ashwal S, Holshouser BA, et al. Hemorrhagic shearing lesions in children and adolescents with posttraumatic diffuse axonal injury: improved detection and initial results. Radiology 2003;227:332–9. 11. Yanagawa Y, Sakamoto T, Takasu A, et al. Relationship between maximum intracranial pressure and traumatic lesions detected by T2⁄-weighted imaging in diffuse axonal injury. J Trauma 2009;66:162–5. 12. Yanagawa Y, Tsushima Y, Tokumaru A, et al. A quantitative analysis of head injury using T2⁄-weighted gradient-echo imaging. J Trauma 2000;49:272–7. 13. Blitstein MK, Tung GA. MRI of cerebral microhemorrhages. AJR Am J Roentgenol 2007;189:720–5. 14. Kelly CA, Upex A, Bateman DN. Comparison of consciousness level assessment in the poisoned patient using the alert/verbal/painful/unresponsive scale and the Glasgow Coma Scale. Ann Emerg Med 2004;44:108–13. 15. The abbreviated injury scale: 1990 revision. Des Plaines, IL, USA: Association for the Advancement of Automotive Medicine; 1990. 16. Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975;1:480–4. 17. 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 1988;150:663–72. 18. Blitstein MK, Tung GA. MRI of cerebral microhemorrhages. AJR Am J Roentgenol 2007;189:720–5. 19. Honda E, Tokunaga T, Oshima Y, et al. MRI findings of closed head injury in children; with special reference to the effect of central shearing force. No Shinkei Geka 1992;20:235–42 [In Japanese]. 20. Dixon CE, Clifton GL, Lighthall JW, et al. A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Methods 1991;39:253–62. 21. Wallesch CW, Curio N, Kutz S, et al. Outcome after mild-to-moderate blunt head injury: effects of focal lesions and diffuse axonal injury. Brain Inj 2001;15:401–12.