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Outcome after traumatic frontal intracerebral haemorrhage: a comparison of unilateral and bilateral haematomas
Journal of Clinical Neuroscience (2004) 11(8), 849–853 0967-5868/$ - see front matter ª 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2003.06.009
Clinical study
Outcome after traumatic frontal intracerebral haemorrhage: a comparison of unilateral and bilateral haematomas Kuo-Sheng Hung1 MD PHD, Chung-Ling Liang2,6 MD, Cheng-Haung Wang3 MD, Hsueh-Wen Chang4 PHD, Naeun Park5 MS, Suh-Hang Hank Juo5,7 MD PHD 1 Department of Trauma and Neurosurgery, Chang Gung Memorial Hospital, Kaohsiung Medical Center, Kaohsiung, Taiwan, 2Department of Ophthalmology, Kaohsiung Municipal Ta Tung Hospital, Kaohsiung, Taiwan, 3Department of Anaesthesiology, Chang Gung Memorial Hospital, Kaohsiung Medical Center, Kaohsiung, Taiwan, 4Department of Biological Sciences, National Sun Yat-Sen University, Kaohsiung, Taiwan, , 5Columbia Genome Center, College of Physicians and Surgeons, Columbia University, NY, USA, 6Graduate Institute of Clinical Medical Sciences, Chang Gung University, Kaohsiung, Taiwan, 7Department of Medical Research, Mackay Memorial Hospital, Taipei, Taiwan
Summary Frontal intracerebral haemorrhage (ICH) is a common result of cranial trauma. Outcome differences between bilateral and unilateral frontal ICH are not well studied but would be valuable to predict prognosis in clinical practice. Two aims are proposed in this study: first to compare the risk of developing delayed ICH after bilateral or unilateral frontal ICH, and second to determine the variables helpful to predict outcome according to the Glasgow Outcome Scale (GOS). Between January 1993 and December 1997, 694 consecutive patients with traumatic ICH were admitted to the Chang Gung Medical Center within 24 h of the trauma. Patients with ICH in sites other than the frontal lobes were excluded. A total of 161 cases (mean age 46.3 ± 20.3 years), including 57 bilateral (mean age 52.5 ± 18.7 years) and 104 unilateral (mean age 42.9 ± 20.5 years) traumatic frontal ICH were studied. Twenty-eight of 57 patients (49%) with bifrontal ICH versus 17 of 104 patients (16%) with unilateral frontal ICH had a further, delayed ICH. In 42 of 45 patients (93%) with delayed ICH, this occurred within 5 days of the initial trauma. Multivariate logistic regression was used to select significant predictors of outcome. We found that delayed ICH (p < 0.001), age (p = 0.004) and mechanism of injury (p = 0.001) explained the worse outcome in patients with bifrontal ICH. The best-fitting logistic regression model included three variables: delayed ICH (p = 0.011), initial GCS (p = 0.023), and a sum score of clinical and radiological variables (p = 0.003). Bifrontal ICH tended to occur in older patients after a fall and was associated with a higher risk of developing delayed ICH or brain stem compression compared to unilateral ICH damage. Using these three variables – delayed ICH, initial GCS, and the sum score – in a logistical regression model is useful to predict outcome in patients with traumatic frontal ICH and may aid patient management. ª 2004 Elsevier Ltd. All rights reserved. Keywords: intracerebral haemorrhage, frontal lobe, head injury, Glasgow coma score, outcome
INTRODUCTION
CLINICAL MATERIAL AND METHODS
Traumatic intracerebral haemorrhage (ICH) or contusion, occurs in up to 15% of patients following head injury.1 Frontal ICH is common after trauma, but the study of traumatic frontal ICH is limited apart from some case reports. Although it seems logical to assume that bilateral ICH has a worse outcome than unilateral ICH, this has not been systematically studied. There is no simple model to predict outcome in traumatic frontal ICH. We retrospectively reviewed 161 consecutive cases of traumatic frontal ICH at the Chang Gung Medical Center in Taiwan. We had two aims. The first was to compare the risk of developing a delayed ICH between bilateral and unilateral frontal ICH. The second was to determine the variables useful to predict outcome after frontal ICH according to the Glasgow Outcome Scale (GOS).2
Inclusion and exclusion criteria
Received 18 February 2003 Accepted 6 June 2003 Correspondence to: Suh-Hang Hank Juo MD PhD, Columbia Genome Center, College of Physicians and Surgeons, Columbia University, 1150 St. Nicholas Ave. Room 531, New York, NY 10032, USA. Tel.: +1-212-851-5182; Fax: +1-212-851-5176; E-mail: [email protected]
Between January 1993 and December 1997, 694 consecutive patients with traumatic ICH were admitted to the Chang Gung Medical Center in Taiwan within 24 h of injury. Among them, patients with ICH in sites other than the frontal lobes were excluded, as were non-traumatic frontal ICH. A total of 161 cases, including 57 bilateral and 104 unilateral traumatic frontal ICH, were included. All patients had undergone at least two computerised tomography (CT) scans. This study was approved by the Institutional Review Committee of Chang Gung Memorial Hospital. Defining delayed ICH All patients had an initial brain CT scan within 24 h of trauma and at least two CT scans in total. CT scans were reviewed by two of the authors (K.H. and C.L.). Reasons for repeat CT were as follows: clinical deterioration (decreased consciousness or development of new neurological deficits), follow-up before discharge, on transfer from another institution and for postoperative follow-up. Therefore, the timing of the second brain CT was variable. By comparison of sequential brain CT scans, we defined delayed ICH as either ICH at a site where the initial CT showed no haemorrhagic lesion or increase in size of a known ICH (25% or more increase in one or more dimensions of one or more lesions seen on the initial CT). In ambiguous cases, a neuroradiologist’s report was used to determine the presence or absence of 849
850 Hung et al.
Fig. 1 This 24-year-old woman had a motorcycle accident while not wearing a helmet 6 h prior to admission. Her initial GCS was 5. The CT scan at admission (A) showed a small subdural haematoma and bilateral frontal lobe contusions. Twelve hours after admission she deteriorated to a GCS of 3 and both her pupils were fully dilated. A repeat CT scan (B) revealed delayed bifrontal contusional ICH with compression of both lateral ventricles. She died 9 days after admission.
haemorrhagic progression. Fig. 1 shows sequential CT scans obtained in one patient to illustrate the definition of delayed ICH in this study. Midline shift of the septum pellucidum was measured between the anterior horns of the lateral ventricles on the CT slice containing the third ventricle and pineal using the scale provided on the image. Measurements for multiple scans from the same patient were made on the slice that provided a similar image of the midline structures. The basal cisterns were also examined for obliteration. Clinical data The following information was obtained from the hospital records: age, gender, mechanism of injury, admission GCS, GCS during hospitalization, discharge GCS, GOS 6 months after admission, pupillary reactions, eye movement examination, focal neurological signs, seizures, delayed ICH, basal cistern obliteration, and midline shift. Reasons for repeat CT scans were obtained from the physician’s written orders, the hospital progress notes, and the nurses’ bihourly clinical assessments, which include GCS, pupil size and reactivity and the development of new neurological deficits. ICH volume was calculated using the formula A · B · C/2, where A, B, and C are dimensions of CT hyperdensity in three perpendicular axes.3 Surgical evacuation was performed for ICH exceeding 30 ml or for those with a focal neurological deficit, abnormal pupils, deteriorating neurological signs, or failure to improve. Unilateral or bilateral frontal craniotomy was performed in 63 cases to evacuate the haematoma. Intracranial pressure (ICP) monitoring was not always performed, and there was no consensus of indications for ICP monitoring in our series, so this data was not analysed.
Variable and outcome measurements Patient outcome at 6 months after admission were recorded using the GOS.2 Outcomes were combined into two categories: favourable (good recovery and moderate disability) and unfavourable (severe disability, vegetative state and dead). The predictor variables used included age, sex, initial GCS, delayed ICH, bilateral or unilateral ICH, surgical evacuation, pupillary abnormalities, focal neurological signs, basal cistern obliteration, and midline shift. Initial GCS was considered the first GCS taken in the emergency room within 24 h of injury. We dichotomised the patients into good (GCS 8–15) and poor (GCS 3–7) initial GCS in the regression analysis. The number of patients who had abnormal pupils, focal neurological signs, basal cistern obliteration and midline shift was small (see Table 1). Thus, the statistical power was too low to distinguish them as useful outcome predictors. To avoid falsely rejecting these four potential variables, we defined a new variable called the “sum score” to include these four variables representing neurological examination and brain CT findings. The total “sum score” is the sum of the scores for four variables – pupillary abnormalities, focal neurological signs, basal cistern obliteration, and midline shift (Table 2). The scores for pupillary abnormalities were: 0 – normal, 1 – unilateral fixed, dilated pupil and 2 – bilateral fixed, dilated pupils. The scores for focal neurological signs were: 0 – normal, 1 – hemiplegia, and 2 – quadriplegia. The scores for basal cistern obliteration were: 0 – normal and 1 – obliteration. The scores for midline shift were: 0 – no shift, 1 – shift up to 10 mm, and 2 – shift greater than 10 mm. Therefore, the total score may range from 0 to 7.
RESULTS Descriptive analysis
Statistical analysis The predictor variables were first checked for skew. Skewed data were transformed to approximate a normal distribution before further statistical analysis. Chi-squared analysis was used to test for a significant difference between the risks of developing delayed ICH after bilateral and unilateral frontal ICH. Correlations between initial and delayed ICH in the ipsilateral frontal lobe were also calculated. To identify significant variables for outcome prediction, potential predictor variables were included in a multivariate logistic regression model using the backward stepwise method. The best-fit model was determined according to goodness-of-fit. Journal of Clinical Neuroscience (2004) 11(8), 849–853
A total of 161 cases (mean age 46.3 € 20.3 years), including 57 bilateral (mean age 52.5 € 18.7 years) and 104 unilateral (mean age 42.9 € 20.5 years) traumatic frontal ICH were included in this study. Demographic features are listed in Table 1. The age distribution was bimodal with peaks at age 20 and 60 (Fig. 2). This indicates the age groups most at risk. The most common causes of head injury were also related to age; motorcycle accidents (43.1%) for the younger group, and falls (38.1%) for the older group. Twenty-eight of 57 (49%) patients with bifrontal ICH versus 17 of 104 (16%) patients with unilateral frontal ICH had delayed ICH. Twenty-six of 45 (57.8%) patients with delayed ICH underwent craniotomy, but only 37 of 116 ª 2004 Elsevier Ltd. All rights reserved.
Outcome after traumatic frontal intracerebral haemorrhage 851
Table 1 Demographic characteristics of patients with traumatic frontal ICH
Age (years) Sex Mechanism
Good initial GCS (8 or more) Delayed ICH Surgery Sum score Pupillary abnormality
Focal neurological signs
Basal cistern obliteration Midline shift
Favourable outcome (%) GOS = 4 or 5
Total (n = 161)
Bifrontal (n = 57)
Unifrontal (n = 104)
p-value
46.3 (±20.3) M = 124 (77%) F = 37 (23%) Fall = 47 (29.2%) Motorcycle = 65 (40.4%) Others = 49 (30.4%) 137 (85.1%)
52.5 (±18.7) M = 45 (78.9%) F = 12 (21.1%) Fall = 24 (42.1%) Motorcycle = 26 (45.6%) Others = 7 (12.3%) 46 (80.7%)
42.9 (±20.5) M = 79 (76%) F = 25 (24%) Fall = 24 (22.1%) Motorcycle = 39 (37.5%) Others = 42 (40.4%) 91 (87.5%)
0.004 0.667
45 (28.3%) 63 (39.4%) 1.31 (±1.37) Normal = 139 (86.3%) Abnormal, 1 = 14 (8.7%) Abnormal, 2 = 8 (5%) Normal = 135 (83.9%) Hemiplegia = 17 (10.6%) Quadriplegia = 9 (5.6%) Normal = 115 (72.8%) Obliteration = 43 (27.2%) No shift = 66 (41.8%) Shift up to 10 mm = 85 (53.8%) Shift greater than 10 mm = 7 (4.4%) 131 (82.9%)
28 (49.1%) 24 (42.1%) 1.54 (±1.58) Normal = 49 (86%) Abnormal, 1 = 5 (8.8%) Abnormal, 2 = 3 (5.3%) Normal = 43 (75.4%) Hemiplegia = 8 (14%) Quadriplegia = 6 (10.5%) Normal = 37 (64.9%) Obliteration = 20 (35.1%) No shift = 22 (38.6%) Shift up to 10 mm = 33 (57.9%) Shift greater than 10 mm = 2 (3.5%) 43 (75.4%)
17 (16.7%) 39 (37.9%) 1.18 (±1.22) Normal = 90 (86.5%) Abnormal, 1 = 9 (8.7%) Abnormal, 2 = 5 (4.8%) Normal = 92 (88.5%) Hemiplegia = 9 (8.7%) Quadriplegia = 3 (2.9%) Normal = 78 (77.2%) Obliteration = 23 (22.8%) No shift = 44 (43.6%) Shift up to 10 mm = 52 (51.5%) Shift greater than 10 mm = 5 (5.0%) 88 (87.1%)
<0.001 0.599 0.107 0.991
0.001
0.247
0.061
0.095 0.717
0.061
Table 2 Calculation of the “sum score” using the sum of the scores for pupillary abnormalities, focal neurological signs, basal cistern obliteration and midline shift
Pupillary abnormalities Focal neurological signs Basal cistern obliteration Midline shift
0
1
2
Normal Normal Normal Normal
Unilateral pupillary dilatation Hemiplegia Obliteration Shift up to 10 mm
Bilateral pupillary dilatation Quadriplegia Shift greater than 10 mm
trauma), and “late” delayed ICH (occurring more than 2 days after trauma). Sixty-three of 161 (39.4%) patients underwent frontal craniotomy for evacuation of ICH. In the bifrontal ICH group, 24 of 57 (42.1%) patients had surgery: six with bifrontal craniotomy and 18 with unilateral craniotomy on the side of most mass effect. Three of the six (50%) patients having bifrontal craniotomy, and 12 of the 18 (67%) patients having unilateral frontal craniotomy had a favourable outcome. There was no significant difference in outcome between bilateral and unilateral frontal craniotomy in patients with bilateral frontal ICH. In the unilateral frontal ICH group, 39 of 104 (37.9%) patients underwent craniotomy for evacuation of ICH. Among these 39 operated patients, 27 (69%) had a favourable outcome. The selection of cases for surgery was non-randomised and therefore, no conclusions can be drawn about the efficacy of surgery from these observations. Furthermore, there was no statistically significant difference in outcome between surgically and nonsurgically treated patients in either the bilateral or unilateral frontal ICH groups. Fig. 2 Age distribution of traumatic frontal ICH. There were two peaks at ages 20 and 60 years.
Statistical aims
(31.9%) patients without delayed ICH underwent craniotomy. In 42 of 45 (93%) patients with delayed ICH, this occurred within 5 days of trauma (Fig. 3). Outcome was not significantly different between “early” delayed ICH (occurring within 2 days of
The risk of delayed ICH after bilateral and unilateral frontal traumatic ICH The overall prognosis for traumatic frontal ICH was good (Table 1). The percentage of favourable outcomes (GOS 4 or 5) was 82.9% for all patients: 75.4% for bilateral frontal ICH and
ª 2004 Elsevier Ltd. All rights reserved.
Journal of Clinical Neuroscience (2004) 11(8), 849–853
852 Hung et al.
good initial GCS had 4.37-fold higher chance of a favourable outcome than patient with a poor initial GCS. Therefore, delayed ICH, the sum score, and initial GCS were powerful predictors of outcome after traumatic frontal ICH. DISCUSSION Clinical considerations after frontal ICH
Fig. 3 Time of occurrence of delayed ICH. Most (93%) occurred within 5 days of trauma.
87.1% for unilateral frontal ICH. This represented a borderline worse outcome for bilateral versus unilateral frontal ICH (p = 0.061). The risk of developing delayed ICH was significantly higher in bilateral versus unilateral ICH (p < 0.001), thus delayed ICH probably contributed to the worse outcome in the bifrontal cases. Correlation of the initial and the delayed ICH occurring on the same side was high: the correlation coefficients were 0.844 (p < 0.001) and 0.707 (p < 0.001), respectively, for right-right and left-left. There was no correlation between initial and delayed ICH on the opposite side. Other than delayed ICH, age (p = 0.004) and mechanism of injury (p = 0.001) may contribute to the worse outcome from bilateral frontal ICH (Table 1).
Variables which may be useful to predict outcome in traumatic frontal ICH To search for significant variables predicting outcome, several logistical regression models were fit. The best-fitting model, using both unilateral and bilateral frontal ICH cases, included the following variables: delayed ICH, initial GCS, and the “sum score”. The regression coefficients, the correspondent risk and p value of each variable are listed in Table 3. Despite inevitable random variations, measurement errors and unknown or unmeasured factors inherent in a retrospective study, this model explained 40% of all contributions to the final outcome. The interpretation of each variable was as follows: with other variables the same, a patient with delayed ICH had 26.2% (that is, e 1.34) the chance of a favourable outcome compared to a patient without delayed ICH. In other words, a patient without delayed ICH had 3.82-fold (1/0.262) greater chance of a favourable outcome. Similarly, when the sum score increased by one unit, the chance of a favourable outcome was reduced to 52.7% when other variables were the same, and a patient with a
Statham et al.4 analysed 18 traumatic frontal contusions and reported that unilateral traumatic frontal contusions had good outcome, while extensive bifrontal contusions had a significant risk of deterioration. Although it seems logical to assume that bilateral frontal ICH has a worse outcome than unilateral frontal ICH, the contributors to this phenomenon have not been well studied. In our series, bilateral frontal ICH had a borderline worse outcome than unilateral frontal ICH (p = 0.061). We also found that delayed ICH, age and mechanism of injury may explain this worse outcome in bilateral frontal ICH (Table 1). It is perhaps surprising that bifrontal ICH was associated with falling accidents, rather than motorcycle accidents. Considering age, we predicted that older age may be associated with both falls and delayed ICH. Recent studies5–7 have shown that hypertension, diabetes mellitus, and amyloidosis are associated with blood vessel fragility, are more common in older patients, and are important in the development of haemorrhagic stroke. Because of the limitations of this retrospective study, whether these factors are relevant in delayed ICH after head injury is unclear. In clinical practice, the elderly patient injured in a fall should be observed carefully. As the presentation of frontal lesions is nonspecific, we suggest liberal use of brain CT for these patients. If the CT shows bilateral frontal ICH, the risk of a delayed ICH is around 50%. Oertel et al.8 found that early progressive haemorrhage occurs in almost 50% of head-injured patients who undergo a CT scan within 2 h of injury, thus they also suggested repeated CT scanning for these patients.8 In our study, only 13.7% of patients with traumatic frontal ICH had abnormal pupillary reactions, and 16.2% had hemiplegia or quadriplegia. Therefore frontal lesions may not be evident by lateralising or focal neurological signs. A lesion in the frontal region is often silent compared to those in other lobes, which may have more obvious presentations, including motor and sensory abnormalities in parietal ICH, rapid disturbance of consciousness in temporal ICH, and visual field defects in occipital ICH. Although the prognosis after traumatic frontal ICH is generally good (82.9% of our cases had favourable outcome), a patient with a frontal lesion may deteriorate abruptly, as herniation occurs anteroposteriorly, obscuring the early symptoms and signs of brain stem compression (Fig. 1). The classic lateralising signs of focal limb weakness, hemianaesthesia and pupillary dilatation, develop in the late stages of anteroposterior herniation. Paucity of signs is especially relevant for patients with an initial GCS of less than 7, who are often intubated and sedated for airway control or agitation, and thus their neurological examination is obscured. With these difficulties in mind, it is important to develop a reliable protocol for treating traumatic frontal ICH. In Table 3, we show that three variables: delayed ICH, initial GCS, and the sum score significantly predict outcome at 6 months
Table 3 Variables in the best fitting regression model Variable Delayed ICH Initial GCS Sum score
Coefficient 1.34 1.48 0.64
Journal of Clinical Neuroscience (2004) 11(8), 849–853
Odds ratio
p-value
0.26 4.37 0.53
0.011 0.023 0.003
ª 2004 Elsevier Ltd. All rights reserved.
Outcome after traumatic frontal intracerebral haemorrhage 853
after injury using a regression model. The sum score, the combination of four neurological and radiological variables (pupillary abnormalities, focal neurological signs, basal cistern obliteration and midline shift) was one of the three significant predictors. However, each individual variable of the sum score was not statistically significant in the regression model due to the small number of patients with abnormal findings (Table 1). Our statistical strategy of combining them into a single variable avoids false rejection of these possibly important variables, although this combination may also create some statistical aberrations. As all the four variables indicated brain stem compression, our approach was justified from a biological standpoint. Thus, not only initial GCS and delayed ICH, but also the sum score can predict outcome. Combining the clinical presentation and CT findings, we suggest that using the data of delayed ICH, initial GCS, and the sum score (pupillary abnormalities, focal neurological signs, basal cistern obliteration and midline shift) may not only predict outcome, but also help to evaluate the patient in a more comprehensive way. Delayed ICH Delayed or evolving traumatic ICH has been previously reported in the literature.4,9–12 Recently, with the increasing availability of CT, sequential scans are frequently performed and the interval between scans has diminished. In recent studies, 23–47.5% of patients have demonstrated progressive enlargement of an ICH if two consecutive CT scans are performed within 24–72 h of injury.13–15 In our series, traumatic haemorrhagic cerebral contusions were prone to increase in size and evolve into intraparenchymal haematomas. Progressive haemorrhagic enlargement may develop in previously contused areas, but haematomas may also develop in areas of brain that appear normal on initial CT scans. In our study, five of the 45 patients with delayed ICH had near normal findings on their initial CT scans. We suggest that a patient with haemorrhagic contusions on initial CT scan should be considered at risk of developing an evolving ICH. Our data also show that traumatic intracerebral haematomas may increase in size any time up to the fifth day after injury, thus these patients need close observation until the lesion stabilises. Once delayed ICH occurred (in 49% of bilateral frontal and 16% of unilateral frontal ICH in this series), surgical intervention was considered. In our study, 26 of 45 (57.8%) patients with delayed ICH underwent craniotomy, but only 37 of 116 (31.9%) patients without delayed ICH underwent craniotomy. In Table 3, we show that patients without delayed ICH had 3.82-fold (1/0.262) greater chance of a favourable outcome than those with delayed ICH. Patients with delayed ICH had a higher incidence of surgery for evacuation of ICH, and also a worse outcome, thus delayed ICH is a major complication in patients with traumatic frontal ICH. Surgical evacuation of ICH In this study, data were collected retrospectively, and there was no consistent protocol for surgical evacuation. Therefore, no conclusions can be drawn regarding the indications for surgery. The following criteria are often used as indications for surgical removal of traumatic ICH: depressed level of consciousness or focal neurological deficit associated with a large haematoma in an anatomically appropriated location,16 deteriorating or unimproved neurological status,17 or significant midline shift on CT.18 These general principles are applied to reduce the risk of brain stem compression. In our study, we found that the sum score (which included the symptoms and signs of brain stem compression) (Table 2) was a significant outcome predictor (p = 0.003). This suggests ª 2004 Elsevier Ltd. All rights reserved.
that early treatment to relieve brain stem compression may increase the odds of a favourable outcome. CONCLUSIONS In conclusion, we have shown that bilateral frontal ICH tends to occur in older patients, often caused by falls and was associated with a higher chance of developing a delayed ICH or brain stem compression when compared to unilateral frontal traumatic ICH. Thus, patients with bilateral frontal ICH have a marginally worse outcome than those with a unilateral frontal injury. Using the three variables: delayed ICH, good initial GCS, and the “sum score” in a logistical regression model may aid the management of patients with traumatic frontal ICH by substantially predicting outcome.
ACKNOWLEDGEMENT We thank Ping-Chuan Chen for data collection. Dr. Hung is supported by the National Science Council, Taiwan (NSC89-2314-B182A-095). REFERENCES 1. McCormick WF. Pathology of closed head injury. In: Wilkins RH, Rengachary SS, editors. Neurosurgery, Vol. 2. second edn. New York: McGraw-Hill; 1996. p. 2639–2666. 2. Jennett B, Snoek J, Bond MR. Disability after severe head injury: observations on the use of the Glasgow Outcome Scale. J Neurol Neurosurg Psychiatry 1981; 44: 285–293. 3. Broderick JP, Brott TJ, Duldner JE, Tomsick T, Huster G. Volume of intracerebral hemorrhage: a powerful and easy-to-use predictor of 30-day mortality. Stroke 1993; 24: 987–993. 4. Statham PF, Johnston RA, Macpherson P. Delayed deterioration in patients with traumatic frontal contusions. J Neurol Neurosurg Psychiatry 1989; 52: 351–354. 5. Arboix A, Garca-Eroles L, Massons J, et al.. Hemorrhagic lacunar stroke. Cerebrovasc Dis 2000; 10: 229–234. 6. McCarron MO, Nicoll JA, Ironside JW, et al.. Cerebral amyloid angiopathyrelated hemorrhage. Interaction of APOE epsilon2 with putative clinical risk factors. Stroke 1999; 30: 1643–1646. 7. Roses AD, Saunders A. Head injury, amyloid beta and Alzheimer’s disease. Nat Med 1995; 1: 603–604 (Letter). 8. Oertel M, Kelly DF, Mcarthur D, Boscardin WJ, Glenn TC, Lee JH, et al.. Progressive hemorrhage after head trauma: predictors and consequences of the evolving injury. J Neurosurg 2002; 96: 109–116. 9. Brown FD, Mullan S, Duda EE. Delayed traumatic intracerebral hematomas: report of three cases. J Neurosurg 1978; 48: 1019–1022. 10. Daz FG, Yock Jr DH, Larson D, Rockswold GL. Early diagnosis of delayed posttraumatic intracerebral hematomas. J Neurosurg 1979; 50: 217–223. 11. Gudeman SK, Kishore PRS, Miller JD, Girevendulis A, Lipper MH, Becker DP. The genesis and significance of delayed traumatic intracerebral hematoma. Neurosurgery 1979; 5: 309–313. 12. Young HA, Gleave JRW, Schmidek HH, Gregory S. Delayed traumatic intracerebral hematoma: report of 15 cases operatively treated. Neurosurgery 1984; 14: 22–25. 13. McBride DQ, Patel AB, Caron M. Early repeat CT scan: importance in detecting surgical lesions after closed head injury. J Neurotrauma 1993; 10(Suppl 1): S227 (Abstract). 14. Servadei F, Nasi MT, Giuliani G, et al.. CT prognostic factors in acute subdural haematomas: the value of the `worst’ CT scan. Br J Neurosurg 2000; 14: 110–116. 15. Stein SC, Spettell C, Young G, et al.. Delayed and progressive brain injury in closed-head trauma: radiological demonstration. Neurosurgery 1993; 32: 25–31. 16. Cooper PR. Post-traumatic intracranial mass lesions. In: Cooper PR, editor. Head Injury. second edn. Baltimore: Williams & Wilkins; 1987. p. 238–284. 17. Soloniuk D, Pitts LH, Lovely M, Barkowski H. Traumatic intracerebral hematomas: timing of appearance and indications for operative removal. J Trauma 1986; 26: 787–794. 18. Tsementzis SA. Surgical management of intracerebral hematomas. Neurosurgery 1985; 16: 562–572.
Journal of Clinical Neuroscience (2004) 11(8), 849–853
Clinical study
Outcome after traumatic frontal intracerebral haemorrhage: a comparison of unilateral and bilateral haematomas Kuo-Sheng Hung1 MD PHD, Chung-Ling Liang2,6 MD, Cheng-Haung Wang3 MD, Hsueh-Wen Chang4 PHD, Naeun Park5 MS, Suh-Hang Hank Juo5,7 MD PHD 1 Department of Trauma and Neurosurgery, Chang Gung Memorial Hospital, Kaohsiung Medical Center, Kaohsiung, Taiwan, 2Department of Ophthalmology, Kaohsiung Municipal Ta Tung Hospital, Kaohsiung, Taiwan, 3Department of Anaesthesiology, Chang Gung Memorial Hospital, Kaohsiung Medical Center, Kaohsiung, Taiwan, 4Department of Biological Sciences, National Sun Yat-Sen University, Kaohsiung, Taiwan, , 5Columbia Genome Center, College of Physicians and Surgeons, Columbia University, NY, USA, 6Graduate Institute of Clinical Medical Sciences, Chang Gung University, Kaohsiung, Taiwan, 7Department of Medical Research, Mackay Memorial Hospital, Taipei, Taiwan
Summary Frontal intracerebral haemorrhage (ICH) is a common result of cranial trauma. Outcome differences between bilateral and unilateral frontal ICH are not well studied but would be valuable to predict prognosis in clinical practice. Two aims are proposed in this study: first to compare the risk of developing delayed ICH after bilateral or unilateral frontal ICH, and second to determine the variables helpful to predict outcome according to the Glasgow Outcome Scale (GOS). Between January 1993 and December 1997, 694 consecutive patients with traumatic ICH were admitted to the Chang Gung Medical Center within 24 h of the trauma. Patients with ICH in sites other than the frontal lobes were excluded. A total of 161 cases (mean age 46.3 ± 20.3 years), including 57 bilateral (mean age 52.5 ± 18.7 years) and 104 unilateral (mean age 42.9 ± 20.5 years) traumatic frontal ICH were studied. Twenty-eight of 57 patients (49%) with bifrontal ICH versus 17 of 104 patients (16%) with unilateral frontal ICH had a further, delayed ICH. In 42 of 45 patients (93%) with delayed ICH, this occurred within 5 days of the initial trauma. Multivariate logistic regression was used to select significant predictors of outcome. We found that delayed ICH (p < 0.001), age (p = 0.004) and mechanism of injury (p = 0.001) explained the worse outcome in patients with bifrontal ICH. The best-fitting logistic regression model included three variables: delayed ICH (p = 0.011), initial GCS (p = 0.023), and a sum score of clinical and radiological variables (p = 0.003). Bifrontal ICH tended to occur in older patients after a fall and was associated with a higher risk of developing delayed ICH or brain stem compression compared to unilateral ICH damage. Using these three variables – delayed ICH, initial GCS, and the sum score – in a logistical regression model is useful to predict outcome in patients with traumatic frontal ICH and may aid patient management. ª 2004 Elsevier Ltd. All rights reserved. Keywords: intracerebral haemorrhage, frontal lobe, head injury, Glasgow coma score, outcome
INTRODUCTION
CLINICAL MATERIAL AND METHODS
Traumatic intracerebral haemorrhage (ICH) or contusion, occurs in up to 15% of patients following head injury.1 Frontal ICH is common after trauma, but the study of traumatic frontal ICH is limited apart from some case reports. Although it seems logical to assume that bilateral ICH has a worse outcome than unilateral ICH, this has not been systematically studied. There is no simple model to predict outcome in traumatic frontal ICH. We retrospectively reviewed 161 consecutive cases of traumatic frontal ICH at the Chang Gung Medical Center in Taiwan. We had two aims. The first was to compare the risk of developing a delayed ICH between bilateral and unilateral frontal ICH. The second was to determine the variables useful to predict outcome after frontal ICH according to the Glasgow Outcome Scale (GOS).2
Inclusion and exclusion criteria
Received 18 February 2003 Accepted 6 June 2003 Correspondence to: Suh-Hang Hank Juo MD PhD, Columbia Genome Center, College of Physicians and Surgeons, Columbia University, 1150 St. Nicholas Ave. Room 531, New York, NY 10032, USA. Tel.: +1-212-851-5182; Fax: +1-212-851-5176; E-mail: [email protected]
Between January 1993 and December 1997, 694 consecutive patients with traumatic ICH were admitted to the Chang Gung Medical Center in Taiwan within 24 h of injury. Among them, patients with ICH in sites other than the frontal lobes were excluded, as were non-traumatic frontal ICH. A total of 161 cases, including 57 bilateral and 104 unilateral traumatic frontal ICH, were included. All patients had undergone at least two computerised tomography (CT) scans. This study was approved by the Institutional Review Committee of Chang Gung Memorial Hospital. Defining delayed ICH All patients had an initial brain CT scan within 24 h of trauma and at least two CT scans in total. CT scans were reviewed by two of the authors (K.H. and C.L.). Reasons for repeat CT were as follows: clinical deterioration (decreased consciousness or development of new neurological deficits), follow-up before discharge, on transfer from another institution and for postoperative follow-up. Therefore, the timing of the second brain CT was variable. By comparison of sequential brain CT scans, we defined delayed ICH as either ICH at a site where the initial CT showed no haemorrhagic lesion or increase in size of a known ICH (25% or more increase in one or more dimensions of one or more lesions seen on the initial CT). In ambiguous cases, a neuroradiologist’s report was used to determine the presence or absence of 849
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Fig. 1 This 24-year-old woman had a motorcycle accident while not wearing a helmet 6 h prior to admission. Her initial GCS was 5. The CT scan at admission (A) showed a small subdural haematoma and bilateral frontal lobe contusions. Twelve hours after admission she deteriorated to a GCS of 3 and both her pupils were fully dilated. A repeat CT scan (B) revealed delayed bifrontal contusional ICH with compression of both lateral ventricles. She died 9 days after admission.
haemorrhagic progression. Fig. 1 shows sequential CT scans obtained in one patient to illustrate the definition of delayed ICH in this study. Midline shift of the septum pellucidum was measured between the anterior horns of the lateral ventricles on the CT slice containing the third ventricle and pineal using the scale provided on the image. Measurements for multiple scans from the same patient were made on the slice that provided a similar image of the midline structures. The basal cisterns were also examined for obliteration. Clinical data The following information was obtained from the hospital records: age, gender, mechanism of injury, admission GCS, GCS during hospitalization, discharge GCS, GOS 6 months after admission, pupillary reactions, eye movement examination, focal neurological signs, seizures, delayed ICH, basal cistern obliteration, and midline shift. Reasons for repeat CT scans were obtained from the physician’s written orders, the hospital progress notes, and the nurses’ bihourly clinical assessments, which include GCS, pupil size and reactivity and the development of new neurological deficits. ICH volume was calculated using the formula A · B · C/2, where A, B, and C are dimensions of CT hyperdensity in three perpendicular axes.3 Surgical evacuation was performed for ICH exceeding 30 ml or for those with a focal neurological deficit, abnormal pupils, deteriorating neurological signs, or failure to improve. Unilateral or bilateral frontal craniotomy was performed in 63 cases to evacuate the haematoma. Intracranial pressure (ICP) monitoring was not always performed, and there was no consensus of indications for ICP monitoring in our series, so this data was not analysed.
Variable and outcome measurements Patient outcome at 6 months after admission were recorded using the GOS.2 Outcomes were combined into two categories: favourable (good recovery and moderate disability) and unfavourable (severe disability, vegetative state and dead). The predictor variables used included age, sex, initial GCS, delayed ICH, bilateral or unilateral ICH, surgical evacuation, pupillary abnormalities, focal neurological signs, basal cistern obliteration, and midline shift. Initial GCS was considered the first GCS taken in the emergency room within 24 h of injury. We dichotomised the patients into good (GCS 8–15) and poor (GCS 3–7) initial GCS in the regression analysis. The number of patients who had abnormal pupils, focal neurological signs, basal cistern obliteration and midline shift was small (see Table 1). Thus, the statistical power was too low to distinguish them as useful outcome predictors. To avoid falsely rejecting these four potential variables, we defined a new variable called the “sum score” to include these four variables representing neurological examination and brain CT findings. The total “sum score” is the sum of the scores for four variables – pupillary abnormalities, focal neurological signs, basal cistern obliteration, and midline shift (Table 2). The scores for pupillary abnormalities were: 0 – normal, 1 – unilateral fixed, dilated pupil and 2 – bilateral fixed, dilated pupils. The scores for focal neurological signs were: 0 – normal, 1 – hemiplegia, and 2 – quadriplegia. The scores for basal cistern obliteration were: 0 – normal and 1 – obliteration. The scores for midline shift were: 0 – no shift, 1 – shift up to 10 mm, and 2 – shift greater than 10 mm. Therefore, the total score may range from 0 to 7.
RESULTS Descriptive analysis
Statistical analysis The predictor variables were first checked for skew. Skewed data were transformed to approximate a normal distribution before further statistical analysis. Chi-squared analysis was used to test for a significant difference between the risks of developing delayed ICH after bilateral and unilateral frontal ICH. Correlations between initial and delayed ICH in the ipsilateral frontal lobe were also calculated. To identify significant variables for outcome prediction, potential predictor variables were included in a multivariate logistic regression model using the backward stepwise method. The best-fit model was determined according to goodness-of-fit. Journal of Clinical Neuroscience (2004) 11(8), 849–853
A total of 161 cases (mean age 46.3 € 20.3 years), including 57 bilateral (mean age 52.5 € 18.7 years) and 104 unilateral (mean age 42.9 € 20.5 years) traumatic frontal ICH were included in this study. Demographic features are listed in Table 1. The age distribution was bimodal with peaks at age 20 and 60 (Fig. 2). This indicates the age groups most at risk. The most common causes of head injury were also related to age; motorcycle accidents (43.1%) for the younger group, and falls (38.1%) for the older group. Twenty-eight of 57 (49%) patients with bifrontal ICH versus 17 of 104 (16%) patients with unilateral frontal ICH had delayed ICH. Twenty-six of 45 (57.8%) patients with delayed ICH underwent craniotomy, but only 37 of 116 ª 2004 Elsevier Ltd. All rights reserved.
Outcome after traumatic frontal intracerebral haemorrhage 851
Table 1 Demographic characteristics of patients with traumatic frontal ICH
Age (years) Sex Mechanism
Good initial GCS (8 or more) Delayed ICH Surgery Sum score Pupillary abnormality
Focal neurological signs
Basal cistern obliteration Midline shift
Favourable outcome (%) GOS = 4 or 5
Total (n = 161)
Bifrontal (n = 57)
Unifrontal (n = 104)
p-value
46.3 (±20.3) M = 124 (77%) F = 37 (23%) Fall = 47 (29.2%) Motorcycle = 65 (40.4%) Others = 49 (30.4%) 137 (85.1%)
52.5 (±18.7) M = 45 (78.9%) F = 12 (21.1%) Fall = 24 (42.1%) Motorcycle = 26 (45.6%) Others = 7 (12.3%) 46 (80.7%)
42.9 (±20.5) M = 79 (76%) F = 25 (24%) Fall = 24 (22.1%) Motorcycle = 39 (37.5%) Others = 42 (40.4%) 91 (87.5%)
0.004 0.667
45 (28.3%) 63 (39.4%) 1.31 (±1.37) Normal = 139 (86.3%) Abnormal, 1 = 14 (8.7%) Abnormal, 2 = 8 (5%) Normal = 135 (83.9%) Hemiplegia = 17 (10.6%) Quadriplegia = 9 (5.6%) Normal = 115 (72.8%) Obliteration = 43 (27.2%) No shift = 66 (41.8%) Shift up to 10 mm = 85 (53.8%) Shift greater than 10 mm = 7 (4.4%) 131 (82.9%)
28 (49.1%) 24 (42.1%) 1.54 (±1.58) Normal = 49 (86%) Abnormal, 1 = 5 (8.8%) Abnormal, 2 = 3 (5.3%) Normal = 43 (75.4%) Hemiplegia = 8 (14%) Quadriplegia = 6 (10.5%) Normal = 37 (64.9%) Obliteration = 20 (35.1%) No shift = 22 (38.6%) Shift up to 10 mm = 33 (57.9%) Shift greater than 10 mm = 2 (3.5%) 43 (75.4%)
17 (16.7%) 39 (37.9%) 1.18 (±1.22) Normal = 90 (86.5%) Abnormal, 1 = 9 (8.7%) Abnormal, 2 = 5 (4.8%) Normal = 92 (88.5%) Hemiplegia = 9 (8.7%) Quadriplegia = 3 (2.9%) Normal = 78 (77.2%) Obliteration = 23 (22.8%) No shift = 44 (43.6%) Shift up to 10 mm = 52 (51.5%) Shift greater than 10 mm = 5 (5.0%) 88 (87.1%)
<0.001 0.599 0.107 0.991
0.001
0.247
0.061
0.095 0.717
0.061
Table 2 Calculation of the “sum score” using the sum of the scores for pupillary abnormalities, focal neurological signs, basal cistern obliteration and midline shift
Pupillary abnormalities Focal neurological signs Basal cistern obliteration Midline shift
0
1
2
Normal Normal Normal Normal
Unilateral pupillary dilatation Hemiplegia Obliteration Shift up to 10 mm
Bilateral pupillary dilatation Quadriplegia Shift greater than 10 mm
trauma), and “late” delayed ICH (occurring more than 2 days after trauma). Sixty-three of 161 (39.4%) patients underwent frontal craniotomy for evacuation of ICH. In the bifrontal ICH group, 24 of 57 (42.1%) patients had surgery: six with bifrontal craniotomy and 18 with unilateral craniotomy on the side of most mass effect. Three of the six (50%) patients having bifrontal craniotomy, and 12 of the 18 (67%) patients having unilateral frontal craniotomy had a favourable outcome. There was no significant difference in outcome between bilateral and unilateral frontal craniotomy in patients with bilateral frontal ICH. In the unilateral frontal ICH group, 39 of 104 (37.9%) patients underwent craniotomy for evacuation of ICH. Among these 39 operated patients, 27 (69%) had a favourable outcome. The selection of cases for surgery was non-randomised and therefore, no conclusions can be drawn about the efficacy of surgery from these observations. Furthermore, there was no statistically significant difference in outcome between surgically and nonsurgically treated patients in either the bilateral or unilateral frontal ICH groups. Fig. 2 Age distribution of traumatic frontal ICH. There were two peaks at ages 20 and 60 years.
Statistical aims
(31.9%) patients without delayed ICH underwent craniotomy. In 42 of 45 (93%) patients with delayed ICH, this occurred within 5 days of trauma (Fig. 3). Outcome was not significantly different between “early” delayed ICH (occurring within 2 days of
The risk of delayed ICH after bilateral and unilateral frontal traumatic ICH The overall prognosis for traumatic frontal ICH was good (Table 1). The percentage of favourable outcomes (GOS 4 or 5) was 82.9% for all patients: 75.4% for bilateral frontal ICH and
ª 2004 Elsevier Ltd. All rights reserved.
Journal of Clinical Neuroscience (2004) 11(8), 849–853
852 Hung et al.
good initial GCS had 4.37-fold higher chance of a favourable outcome than patient with a poor initial GCS. Therefore, delayed ICH, the sum score, and initial GCS were powerful predictors of outcome after traumatic frontal ICH. DISCUSSION Clinical considerations after frontal ICH
Fig. 3 Time of occurrence of delayed ICH. Most (93%) occurred within 5 days of trauma.
87.1% for unilateral frontal ICH. This represented a borderline worse outcome for bilateral versus unilateral frontal ICH (p = 0.061). The risk of developing delayed ICH was significantly higher in bilateral versus unilateral ICH (p < 0.001), thus delayed ICH probably contributed to the worse outcome in the bifrontal cases. Correlation of the initial and the delayed ICH occurring on the same side was high: the correlation coefficients were 0.844 (p < 0.001) and 0.707 (p < 0.001), respectively, for right-right and left-left. There was no correlation between initial and delayed ICH on the opposite side. Other than delayed ICH, age (p = 0.004) and mechanism of injury (p = 0.001) may contribute to the worse outcome from bilateral frontal ICH (Table 1).
Variables which may be useful to predict outcome in traumatic frontal ICH To search for significant variables predicting outcome, several logistical regression models were fit. The best-fitting model, using both unilateral and bilateral frontal ICH cases, included the following variables: delayed ICH, initial GCS, and the “sum score”. The regression coefficients, the correspondent risk and p value of each variable are listed in Table 3. Despite inevitable random variations, measurement errors and unknown or unmeasured factors inherent in a retrospective study, this model explained 40% of all contributions to the final outcome. The interpretation of each variable was as follows: with other variables the same, a patient with delayed ICH had 26.2% (that is, e 1.34) the chance of a favourable outcome compared to a patient without delayed ICH. In other words, a patient without delayed ICH had 3.82-fold (1/0.262) greater chance of a favourable outcome. Similarly, when the sum score increased by one unit, the chance of a favourable outcome was reduced to 52.7% when other variables were the same, and a patient with a
Statham et al.4 analysed 18 traumatic frontal contusions and reported that unilateral traumatic frontal contusions had good outcome, while extensive bifrontal contusions had a significant risk of deterioration. Although it seems logical to assume that bilateral frontal ICH has a worse outcome than unilateral frontal ICH, the contributors to this phenomenon have not been well studied. In our series, bilateral frontal ICH had a borderline worse outcome than unilateral frontal ICH (p = 0.061). We also found that delayed ICH, age and mechanism of injury may explain this worse outcome in bilateral frontal ICH (Table 1). It is perhaps surprising that bifrontal ICH was associated with falling accidents, rather than motorcycle accidents. Considering age, we predicted that older age may be associated with both falls and delayed ICH. Recent studies5–7 have shown that hypertension, diabetes mellitus, and amyloidosis are associated with blood vessel fragility, are more common in older patients, and are important in the development of haemorrhagic stroke. Because of the limitations of this retrospective study, whether these factors are relevant in delayed ICH after head injury is unclear. In clinical practice, the elderly patient injured in a fall should be observed carefully. As the presentation of frontal lesions is nonspecific, we suggest liberal use of brain CT for these patients. If the CT shows bilateral frontal ICH, the risk of a delayed ICH is around 50%. Oertel et al.8 found that early progressive haemorrhage occurs in almost 50% of head-injured patients who undergo a CT scan within 2 h of injury, thus they also suggested repeated CT scanning for these patients.8 In our study, only 13.7% of patients with traumatic frontal ICH had abnormal pupillary reactions, and 16.2% had hemiplegia or quadriplegia. Therefore frontal lesions may not be evident by lateralising or focal neurological signs. A lesion in the frontal region is often silent compared to those in other lobes, which may have more obvious presentations, including motor and sensory abnormalities in parietal ICH, rapid disturbance of consciousness in temporal ICH, and visual field defects in occipital ICH. Although the prognosis after traumatic frontal ICH is generally good (82.9% of our cases had favourable outcome), a patient with a frontal lesion may deteriorate abruptly, as herniation occurs anteroposteriorly, obscuring the early symptoms and signs of brain stem compression (Fig. 1). The classic lateralising signs of focal limb weakness, hemianaesthesia and pupillary dilatation, develop in the late stages of anteroposterior herniation. Paucity of signs is especially relevant for patients with an initial GCS of less than 7, who are often intubated and sedated for airway control or agitation, and thus their neurological examination is obscured. With these difficulties in mind, it is important to develop a reliable protocol for treating traumatic frontal ICH. In Table 3, we show that three variables: delayed ICH, initial GCS, and the sum score significantly predict outcome at 6 months
Table 3 Variables in the best fitting regression model Variable Delayed ICH Initial GCS Sum score
Coefficient 1.34 1.48 0.64
Journal of Clinical Neuroscience (2004) 11(8), 849–853
Odds ratio
p-value
0.26 4.37 0.53
0.011 0.023 0.003
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Outcome after traumatic frontal intracerebral haemorrhage 853
after injury using a regression model. The sum score, the combination of four neurological and radiological variables (pupillary abnormalities, focal neurological signs, basal cistern obliteration and midline shift) was one of the three significant predictors. However, each individual variable of the sum score was not statistically significant in the regression model due to the small number of patients with abnormal findings (Table 1). Our statistical strategy of combining them into a single variable avoids false rejection of these possibly important variables, although this combination may also create some statistical aberrations. As all the four variables indicated brain stem compression, our approach was justified from a biological standpoint. Thus, not only initial GCS and delayed ICH, but also the sum score can predict outcome. Combining the clinical presentation and CT findings, we suggest that using the data of delayed ICH, initial GCS, and the sum score (pupillary abnormalities, focal neurological signs, basal cistern obliteration and midline shift) may not only predict outcome, but also help to evaluate the patient in a more comprehensive way. Delayed ICH Delayed or evolving traumatic ICH has been previously reported in the literature.4,9–12 Recently, with the increasing availability of CT, sequential scans are frequently performed and the interval between scans has diminished. In recent studies, 23–47.5% of patients have demonstrated progressive enlargement of an ICH if two consecutive CT scans are performed within 24–72 h of injury.13–15 In our series, traumatic haemorrhagic cerebral contusions were prone to increase in size and evolve into intraparenchymal haematomas. Progressive haemorrhagic enlargement may develop in previously contused areas, but haematomas may also develop in areas of brain that appear normal on initial CT scans. In our study, five of the 45 patients with delayed ICH had near normal findings on their initial CT scans. We suggest that a patient with haemorrhagic contusions on initial CT scan should be considered at risk of developing an evolving ICH. Our data also show that traumatic intracerebral haematomas may increase in size any time up to the fifth day after injury, thus these patients need close observation until the lesion stabilises. Once delayed ICH occurred (in 49% of bilateral frontal and 16% of unilateral frontal ICH in this series), surgical intervention was considered. In our study, 26 of 45 (57.8%) patients with delayed ICH underwent craniotomy, but only 37 of 116 (31.9%) patients without delayed ICH underwent craniotomy. In Table 3, we show that patients without delayed ICH had 3.82-fold (1/0.262) greater chance of a favourable outcome than those with delayed ICH. Patients with delayed ICH had a higher incidence of surgery for evacuation of ICH, and also a worse outcome, thus delayed ICH is a major complication in patients with traumatic frontal ICH. Surgical evacuation of ICH In this study, data were collected retrospectively, and there was no consistent protocol for surgical evacuation. Therefore, no conclusions can be drawn regarding the indications for surgery. The following criteria are often used as indications for surgical removal of traumatic ICH: depressed level of consciousness or focal neurological deficit associated with a large haematoma in an anatomically appropriated location,16 deteriorating or unimproved neurological status,17 or significant midline shift on CT.18 These general principles are applied to reduce the risk of brain stem compression. In our study, we found that the sum score (which included the symptoms and signs of brain stem compression) (Table 2) was a significant outcome predictor (p = 0.003). This suggests ª 2004 Elsevier Ltd. All rights reserved.
that early treatment to relieve brain stem compression may increase the odds of a favourable outcome. CONCLUSIONS In conclusion, we have shown that bilateral frontal ICH tends to occur in older patients, often caused by falls and was associated with a higher chance of developing a delayed ICH or brain stem compression when compared to unilateral frontal traumatic ICH. Thus, patients with bilateral frontal ICH have a marginally worse outcome than those with a unilateral frontal injury. Using the three variables: delayed ICH, good initial GCS, and the “sum score” in a logistical regression model may aid the management of patients with traumatic frontal ICH by substantially predicting outcome.
ACKNOWLEDGEMENT We thank Ping-Chuan Chen for data collection. Dr. Hung is supported by the National Science Council, Taiwan (NSC89-2314-B182A-095). REFERENCES 1. McCormick WF. Pathology of closed head injury. In: Wilkins RH, Rengachary SS, editors. Neurosurgery, Vol. 2. second edn. New York: McGraw-Hill; 1996. p. 2639–2666. 2. Jennett B, Snoek J, Bond MR. Disability after severe head injury: observations on the use of the Glasgow Outcome Scale. J Neurol Neurosurg Psychiatry 1981; 44: 285–293. 3. Broderick JP, Brott TJ, Duldner JE, Tomsick T, Huster G. Volume of intracerebral hemorrhage: a powerful and easy-to-use predictor of 30-day mortality. Stroke 1993; 24: 987–993. 4. Statham PF, Johnston RA, Macpherson P. Delayed deterioration in patients with traumatic frontal contusions. J Neurol Neurosurg Psychiatry 1989; 52: 351–354. 5. Arboix A, Garca-Eroles L, Massons J, et al.. Hemorrhagic lacunar stroke. Cerebrovasc Dis 2000; 10: 229–234. 6. McCarron MO, Nicoll JA, Ironside JW, et al.. Cerebral amyloid angiopathyrelated hemorrhage. Interaction of APOE epsilon2 with putative clinical risk factors. Stroke 1999; 30: 1643–1646. 7. Roses AD, Saunders A. Head injury, amyloid beta and Alzheimer’s disease. Nat Med 1995; 1: 603–604 (Letter). 8. Oertel M, Kelly DF, Mcarthur D, Boscardin WJ, Glenn TC, Lee JH, et al.. Progressive hemorrhage after head trauma: predictors and consequences of the evolving injury. J Neurosurg 2002; 96: 109–116. 9. Brown FD, Mullan S, Duda EE. Delayed traumatic intracerebral hematomas: report of three cases. J Neurosurg 1978; 48: 1019–1022. 10. Daz FG, Yock Jr DH, Larson D, Rockswold GL. Early diagnosis of delayed posttraumatic intracerebral hematomas. J Neurosurg 1979; 50: 217–223. 11. Gudeman SK, Kishore PRS, Miller JD, Girevendulis A, Lipper MH, Becker DP. The genesis and significance of delayed traumatic intracerebral hematoma. Neurosurgery 1979; 5: 309–313. 12. Young HA, Gleave JRW, Schmidek HH, Gregory S. Delayed traumatic intracerebral hematoma: report of 15 cases operatively treated. Neurosurgery 1984; 14: 22–25. 13. McBride DQ, Patel AB, Caron M. Early repeat CT scan: importance in detecting surgical lesions after closed head injury. J Neurotrauma 1993; 10(Suppl 1): S227 (Abstract). 14. Servadei F, Nasi MT, Giuliani G, et al.. CT prognostic factors in acute subdural haematomas: the value of the `worst’ CT scan. Br J Neurosurg 2000; 14: 110–116. 15. Stein SC, Spettell C, Young G, et al.. Delayed and progressive brain injury in closed-head trauma: radiological demonstration. Neurosurgery 1993; 32: 25–31. 16. Cooper PR. Post-traumatic intracranial mass lesions. In: Cooper PR, editor. Head Injury. second edn. Baltimore: Williams & Wilkins; 1987. p. 238–284. 17. Soloniuk D, Pitts LH, Lovely M, Barkowski H. Traumatic intracerebral hematomas: timing of appearance and indications for operative removal. J Trauma 1986; 26: 787–794. 18. Tsementzis SA. Surgical management of intracerebral hematomas. Neurosurgery 1985; 16: 562–572.
Journal of Clinical Neuroscience (2004) 11(8), 849–853