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DOI: 10.1148/radiol.2321030824
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(Radiology 2004;232:211-220.)
© RSNA, 2004

Emergency Radiology

Admission Perfusion CT: Prognostic Value in Patients with Severe Head Trauma1

Max Wintermark, MD, Guy van Melle, PhD, Pierre Schnyder, MD, Jean-Pierre Revelly, MD, François Porchet, MD, Luca Regli, MD, Reto Meuli, MD, PhD, Philippe Maeder, MD and René Chioléro, MD

1 From the Department of Diagnostic and Interventional Radiology (M.W., P.S., R.M., P.M.), Surgical Intensive Care Unit (J.P.R., R.C.), and Department of Neurosurgery (F.P., L.R.), University Hospital, 1011 Lausanne, Switzerland; and Biostatistics Unit, University Institute of Social and Preventive Medicine, Lausanne, Switzerland (G.v.M.). Received May 27, 2003; revision requested August 6; final revision received December 3; accepted December 15. Address correspondence to M.W. (e-mail: max_wintermark@hotmail.com).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To assess the prognostic value of admission perfusion computed tomography (CT) in patients with severe head trauma.

MATERIALS AND METHODS: This prospective study included 130 patients with severe trauma, aged 19–86 years, admitted with a Glasgow Coma Scale score of 8 or less. They underwent perfusion CT as part of their admission CT survey. Clinical data, unenhanced cerebral CT findings, and perfusion CT scans were evaluated with respect to the Glasgow Outcome Scale (GOS) score at 3 months. Perfusion CT features were evaluated in patients with intracranial hypertension, cerebral contusions, and juxtadural hematomas. Ordered logistic regression was used to determine risk factors for an unfavorable GOS score at 3 months.

RESULTS: Perfusion CT was more sensitive than conventional unenhanced CT in the detection of cerebral contusions. Perfusion CT featured specific patterns with respect to patient outcome, with normal brain perfusion or hyperemia in patients with favorable outcome, and oligemia in patients with unfavorable outcome. The number of arterial territories with low regional cerebral blood volume at perfusion CT was an independent prognostic factor (P = .008), as were mean arterial pressure at the scene of accident (P = .083), base excess at admission (P = .002), presence of skull fractures (P = .041), and signs of herniation (P = .013) at admission unenhanced cerebral CT. Perfusion CT also showed a range of brain perfusion alterations in patients with juxtadural collections, cerebral edema, or intracranial hypertension.

CONCLUSION: Perfusion CT in patients with severe head trauma provides independent prognostic information regarding functional outcome.

© RSNA, 2004

Index terms: Brain, CT, 10.12119 • Brain, edema, 10.436 • Brain, injuries, 10.436 • Computed tomography (CT), perfusion study, 10.12119


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Severe brain injury is a major predictor of unfavorable outcome in patients with multiple injuries, independent of the presence and severity of extracranial lesions (1). It is associated with a specific mortality rate of 20%–30% and a disability rate of 5%–10% among the 500,000–750,000 head trauma cases recorded annually in the United States (2). Predicting outcome in patients with severe head trauma remains a challenging task and generates abundant controversy. Several clinical parameters, such as old age (3,4), low Glasgow Coma Scale (GCS) score (4,5), abnormal pupillary reaction (4,5), arterial hypotension (6,7), and hypoxia with subsequent metabolic acidosis (6,7), are evaluated prior to and/or at admission and are considered independent predictors of mortality in patients with traumatic brain injury.

Many authors have investigated the prognostic value of conventional computed tomography (CT). Indeed, CT is a sensitive primary diagnostic tool in the evaluation of patients with acute head injury and plays a critical role in the early detection of intracranial lesions that may require neurosurgical intervention. Several methods for classifying CT features have been proposed (8–11), including the trauma coma databank classification (12–14).

Unfortunately, the prognostic value of such classifications based on the results of admission CT has shown limited value. On one hand, early CT examinations (those performed within 3 hours of injury) lead to underestimation of the ultimate size of parenchymal lesions (15). On the other hand, conventional CT does not afford insight into secondary ischemic injuries related to traumatic cerebral edema and intracranial hypertension, which are responsible for about half of all deaths after admission (16).

Recently, perfusion CT has been introduced as a simple imaging technique to be used in routine clinical practice. It has gained recognition in the early care of adult patients with acute stroke and other cerebrovascular disorders (17–20) because it affords direct insight into cerebral infarct and penumbra (19,20). Thus, the purpose of this study was to assess the prognostic value of admission perfusion CT in patients with severe head trauma.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Patients
During the period from July 2001 to October 2002, all adult patients with trauma were prospectively identified in the emergency room of our institution as candidates for enrollment in this study. Inclusion criteria involved all adult patients with trauma who underwent intubation and had a GCS score of 8 or less at admission. The GCS score at admission was not necessarily the same as the GCS score at the scene of the accident. At our institution, such patients undergo routine unenhanced cerebral and cervical multi–detector row CT and contrast material–enhanced thoracic-abdominal-pelvic multi–detector row CT. The study protocol was approved by the ethics committee for research of Lausanne University, and institutional informed consent guidelines were followed regarding consent of the patient or his or her legal representative. Declaration of Helsinki principles were followed.

One hundred thirty-seven patients were considered for inclusion in this study, and 130 were included. Seven patients did not undergo CT at admission but were instead taken directly to the operating room; thus, these patients were excluded from our study. Our series consisted of 101 men and 29 women with a median age of 56 years (age range, 19–86 years; interquartile age range, 27–51 years). The median age of men was 32 years (age range, 19–86 years; interquartile age range, 25–51 years). The median age of women was 36 years (age range, 22–77 years; interquartile age range, 28–53 years), and the age distribution in women was not significantly different from that in men (P = .965). Ninety patients were injured in traffic accidents (car accidents, n = 63 [70%]; motorcycle accidents, n = 16 [18%]; pedestrians, n = 11 [12%]), 34 in falls, and six in crushing accidents.

Imaging Protocol
Unenhanced cerebral CT was performed, and approximately 30 5-mm-thick transverse sections were acquired with 120 kVp and 200 mA.

Perfusion CT was performed immediately after unenhanced cerebral CT and before cervical CT. Perfusion CT consisted of a 40-second series, with 40 gantry rotations performed at a rate of 1 rotation per second in cine mode during intravenous administration of iodinated contrast material. The acquisition parameters for perfusion CT series were 80 kVp and 100 mA (21). Perfusion CT scanning was initiated 7 seconds after injection of 40 mL of iohexol (300 mg/mL of iodine; Accupaque 300, Nycomed, Oslo, Norway) at a rate of 5 mL/sec into an antecubital vein by using a power injector (CT9000; Libel-Flarsheim Company, Cincinnati, Ohio). The time delay before contrast material reached the brain parenchyma allowed baseline images to be acquired without contrast enhancement. Multi–detector row CT (Lightspeed; GE Medical Systems, Milwaukee, Wis) enabled the assessment of two adjacent 10-mm-thick sections. Two 10-mm-thick sections were preferred to four adjacent 5-mm-thick sections, which would have meant lower signal-to-noise ratio for the same acquisition parameters. The two cerebral sections were selected above the orbits to protect the lenses, at the level of the third ventricle and the basal nuclei, then toward the vertex. They were matched with two unenhanced cerebral CT sections.

All admission perfusion CT examinations were well tolerated, with no reported side effects, such as allergic reaction to the contrast material, contrast material extravasation, or nephrotoxicity. Perfusion CT did not interfere with screening for traumatic injuries with contrast-enhanced thoracic-abdominal-pelvic CT, which was performed immediately after perfusion CT.

Data Processing
Perfusion CT data were used to create time-enhancement curves registered in each pixel; these curves are linearly related to the time-concentration curves for iodinated contrast material. Perfusion CT data were analyzed by using perfusion CT software developed at our institution (22,23); the results obtained with this software have been validated by comparison with stable xenon CT data (24). This software relies on the central volume principle, which is the most accurate for low injection rates of iodinated contrast material (25). The central volume principle uses a mathematic operation called deconvolution (least mean square deconvolution for the used software) to calculate the mean transit time (MTT) (26–28). The deconvolution operation requires a reference arterial input function, which is automatically selected with the perfusion CT software in a region of interest that is drawn by the user around the anterior cerebral artery. The regional cerebral blood volume (rCBV) map is calculated from the areas under the time-enhancement curves. This map relies on a quantitative measurement of the partial size averaging effect and takes into account the fact that there is no partial averaging effect at the center of the large superior sagittal venous sinus (29–31). Finally, a simple equation that combines rCBV and MTT values leads to the regional cerebral blood flow (rCBF) value: rCBF = rCBV/MTT (26–28).

Clinical Data
All patients were treated according to the same written protocol that involved one or several of the following procedures in case of intracranial hypertension: controlled mechanical ventilation, continuous intracranial pressure monitoring (Camino; Integra NeuroSciences, Plainsboro, NJ) (R.C., J.P.R., F.P., L.R.), osmotherapy (mannitol 20%), and controlled sedation and analgesia. Intracranial hypertension was diagnosed either when invasive measurement revealed that intracranial pressure was more than 18 mm Hg or when CT patterns of herniation were present in patients without intracranial pressure monitoring.

The following clinical data were prospectively collected: GCS score at the scene of the accident, worst GCS score during the first 24 hours after admission, pupillary reactivity and mean arterial pressure at the scene of the accident, blood gas analysis at admission, and time delay until admission to the emergency room.

The functional outcome was evaluated 3 months after trauma, either during neurosurgic follow-up (F.P., L.R.) or by the family doctor, with the Glasgow Outcome Scale (GOS). A GOS score of 5 indicated good recovery (ie, good outcome with minimal to no dysfunction). A GOS score of 4 indicated moderate disability (ie, minimal functional abnormality and no interference with daily life activities). A GOS score of 3 indicated severe disability that required institutional care. A GOS score of 2 indicated a vegetative state (ie, no reaction to outside stimuli). A GOS score of 1 indicated death; a score of 1a indicated that death was due to a primary lesion, and a score of 1b indicated that death was due to a late complication.

Data Analysis
Unenhanced cerebral CT studies were reviewed for the following items by one of two neuroradiologists (R.M., 15 years of experience; P.M., 14 years of experience), both of whom were blinded to the following clinical findings: trauma coma databank classification, number of focal parenchymatous lesions, skull fractures, epidural hematoma, subdural hematoma, subarachnoid hemorrhage, ventricular blood, cerebral contusions, diffuse axonal injuries, cerebral edema, and herniation. CT features of cerebral edema included diffuse hypoattenuation, loss of distinction between gray and white matter, swollen gyri, and compressed or absent cisterns (12,13). The follow-up unenhanced CT studies obtained in the same patients between 12 hours and 5 days after admission were also reviewed for the same items by one of the neuroradiologists (R.M. or P.M.), with special attention to delayed cerebral contusions and CT features of cerebral ischemia consequent to intracranial hypertension.

For each of the maps extracted from perfusion CT data that describe rCBV, MTT, and rCBF values, the following systematic analysis scheme was applied: Regions of interest of approximately 500 mm2 were drawn to include the anterior, middle, and posterior cerebral artery territories of each hemisphere. Anterior, middle, and posterior cerebral artery territories were delineated by a radiologist (M.W., 5 years experience in perfusion CT reading). An average value was calculated for the entire cerebral parenchyma displayed on the two sections obtained with perfusion CT. The number of patients with a preexisting stroke at the time of the study was limited (5). In these five patients, the perfusion CT alterations associated with preexisting stroke were set apart and not taken into account in the calculation of the perfusion CT scores.

In a distinct survey of the rCBV, MTT, and rCBF maps extracted from perfusion CT data, the radiologist (M.W.) who assessed these maps drew regions of interest within abnormal areas (ie, cerebral contusions) or within their vicinity (ie, juxtadural collections) on the unenhanced CT scans (R.M., P.M.). These abnormal areas were delineated as they were demonstrated on the unenhanced cerebral CT scans at admission or on the unenhanced CT scans at follow-up.

A subgroup of control patients was defined as those who satisfied both the general inclusion criteria and the additional four criteria: (a) no abnormality was seen on the unenhanced cerebral CT scans at admission; (b) no diagnosis of intracranial hypertension was assigned; (c) normal clinical and/or radiologic follow-up, including additional investigations, was required; and (d) the patient had a GOS score of 5 at 3-month follow-up. Means and SDs of rCBV, MTT, and rCBF were calculated for this subgroup of control patients. The range in patients in the control group was defined as mean ± 2 SDs.

In the remaining patients who were not included in the control group, each of the six vascular territories (right and left anterior cerebral artery, right and left middle cerebral artery, and right and left posterior cerebral artery) were scored as follows: low (values that were two SDs less than the mean), normal (values that were within two SDs of the mean), or high (values that were two SDs greater than the mean). This procedure was performed separately for rCBV, MTT, and rCBF maps. The number of low-value territories and high-value territories (score of 0–6) was determined for each patient who was not included in the control group, and a global score was calculated (–6 to 6) to take into account the possible coexistence of low-value and high-value territories in the same patient (–6 corresponds to all territories with low values and 6 corresponds to all territories with high values). This global score describes the extent of the perfusion CT abnormalities.

Statistical Analysis
The ordered logistic regression model was used to describe the data. This is an extension of the classic logistic regression to the situation where three ordered outcomes are considered. This generalization takes advantage of the ordinal scale of the outcome, of which the GOS score is a typical example. The estimation procedure determines not only the coefficients of the regression equation but also the k-1 cut-points, which separate the k categories of the outcome (ie, a GOS score of 5). Thus, patients were predicted to belong in category 1 if their computed score was less than the first cut-point and in category 2 if their computed score was less than the second cut-point but greater than the first. Finally, patients were predicted to be in category k if their score was higher than the k-1 cut-point. The entire estimation procedure is based on the maximum likelihood approach, and testing of successive (sub)models is based on the likelihood ratio test statistic, which approximately follows a {chi}2 distribution on degrees of freedom equal to the difference in the number of estimated parameters. The statistical package used was Stata version 7.0 (StataCorp LP, College Station, Tex). In this package, the variant of the ordered logistic regression is the proportional odds logit model.

In the analysis of data, a univariate screening of the available clinical items and of the CT findings was first performed to reduce the large number of those factors (24) compared with the relatively small number of patients (n = 130) enrolled in this study. This screening was performed with the ordered logistic model, with the significance level set at .10. We selected .10 rather than .001 as a significance threshold because our goal was to screen for relevant prognostic factors rather than to verify a specific hypothesis of perfusion CT as a prognostic factor. All variables were tested one at a time to decide which were capable of distinguishing between the various outcome categories.

Next, by allowing all factors accepted in the screening process to participate in a stepwise (step down) multivariate-ordered logistic regression model, those factors that were no longer significant in the presence of the other selected items were removed. The likelihood ratio test was applied to perform stepwise eliminations; for example, when the likelihood of the data did not become significantly worse after removal of a given factor, this factor was considered nonsignificant. Again, the significance level was set at .10.

The aim of this study was to evaluate whether CT findings were useful predictors of outcome in the presence of all usual clinical information. Consequently, we proceeded in the following manner. Having used the stepwise procedure described previously to find the best subset of clinical items to predict the outcome of the patients, we tried to improve this model by using the items obtained with the perfusion CT examination. Again, the likelihood ratio test was applied for this step of the analysis with a significance level of .10.

For the assessment of perfusion CT modifications in case of intracranial hypertension, within cerebral contusions or in the vicinity of juxtadural contusions, values obtained in these subgroups of patients were compared with those obtained in the subgroup of control patients by using the Wilcoxon (Mann-Whitney) rank sum test, with a significance level of .001 to account for the multiple tests. The Bonferroni correction was used.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Patients
The patients were categorized as follows with respect to the 3-month GOS score: 39 patients had a score of 5, 21 had a score of 4, 18 had a score of 3, eight had a score of 2, 38 had a score of 1a (early mortality from intracranial hypertension in 29 patients, hypovolemic shock in five, respiratory failure due to cervical spine fracture in two, and extensive burns in two), and six had a score of 1b (late mortality from bacteremia in five patients and respiratory failure due to cervical spine fracture in one).

Sixty-one patients required invasive monitoring of intracranial pressure. Among these patients, 34 had intracranial hypertension (intracranial pressure > 18 mm Hg); all 34 had CT signs of cerebral edema, and 18 had CT signs of herniation. Among the 69 patients without invasive measurement of intracranial pressure, 10 had CT features of herniation. Thus, a total of 44 patients were considered with a diagnosis of intracranial hypertension.

Clinical Findings and Outcome
Evaluated clinical variables and their results are summarized in Table 1. Pupillary reaction was normal in 88 patients and abnormal in 42. The variables with a significant association with the GOS score at 3 months were mean arterial pressure at the scene of the accident and base excess in the admission blood gas analysis. Neither age nor sex were significant risk factors for an unfavorable GOS score at 3-month follow-up.


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  		TABLE 1. Value of Clinical Outcome Variables in Our Series of Patients

 
Conventional Unenhanced Cerebral CT Findings and Outcome
The occurrences of the items evaluated on the conventional unenhanced cerebral CT scan obtained at admission are listed in Table 2. The CT findings deemed statistically significant with respect to the GOS score at 3-month follow-up were presence of skull fractures and CT features of cerebral edema and herniation, as shown in Figure 1.


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  		TABLE 2. Items Evaluated on Admission Unenhanced Cerebral CT Scans and Their Occurrence

 


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  		Figure 1. Chart shows findings at admission conventional unenhanced CT that showed a statistically significant association with the GOS at 3-month follow-up. This chart summarizes the regression coefficients (ß) and the corresponding P values of the approximative Wald test. The sign of the ß coefficients indicates the dirrection of the associations. For example, a positive ß coefficient indicates that an increase of the factor would lead to a better GOS score, and vice versa. This chart shows that perfusion CT data, specifically the number of arterial territories with low rCBV values, yielded a significant prognostic contribution, in addition to clinical and conventional unenhanced cerebral CT prognostic factors.

 
Perfusion CT Results and Outcome
Average values measured in the subgroup of 32 control patients are reported in Table 3. The median age in the control group was 37 years (range, 19–78 years; interquartile range, 26–49 years), which was not significantly different (P = .686) from the median age in the other patients (median age, 32 years; range, 22–86 years; interquartile range, 27–55 years). The sex ratio was similar in the control (25 men, seven women) and noncontrol (76 men, 22 women) patients. The normal ranges for the three parameters that were used as references for the scoring of arterial territories in the noncontrol patients, as described in the Materials and Methods section, were as follows: (a) 2.1–4.5 mL · 100 g–1 for the rCBV, (b) 2.7–5.9 seconds for the MTT, and (c) 28.6–69.0 mL · 100 g–1 · min–1 for the rCBF.


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  		TABLE 3. MTT, rCBF, and rCBV Values

 
As demonstrated in Figure 2, patients with a GOS score of 5, 4, or 3 at 3-month follow-up had one or more arterial territories with high rCBV values, whereas patients with a GOS score of 2 or 1a had one or more arterial territories with low rCBV values. Patients from all the GOS categories demonstrated more or less extensive prolongation of MTT values, with a trend for higher MTT values when the GOS score decreased. Finally, patients with a GOS score of 5, 4, or 3 had one or more arterial territories with high rCBF values, whereas patients with a GOS score of 2 or 1a showed one or more arterial territories with low rCBF values. The distribution of perfusion CT results with respect to the GCS score at the scene of the accident was similar, as shown in Figure 3.



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  		Figure 2. Graphs show brain perfusion alterations with respect to GOS score at 3-month follow-up. X axis designates the GOS score. Y axis relates to the number of arterial territories characterized by low and high rCBV, MTT, and rCBF values, expressed on a scale ranging from –6 to +6, to take into account the possible coexistence of low-value and high-value territories in the same patient. For each category of GOS score at 3-month follow-up, the dot indicates median score, whereas the line represents interquartile range. These graphs show that favorable outcome is associated with normal brain perfusion or hyperemia (high rCBV and rCBF values, low MTT values), whereas unfavorable outcome is associated with oligemia (low rCBV and rCBF values, high MTT values).

 


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  		Figure 3. Graphs show brain perfusion alterations with respect to GCS score at the scene of the accident. X axis designates the GCS score at the scene of the accident. Y axis relates to the number of arterial territories characterized by low and high rCBV, MTT, and rCBF values, expressed on a scale ranging from –6 to +6, to take into account the possible coexistence of low-value and high-value territories in the same patient. For each category of GCS score at the scene of the accident, the dot indicates median score, whereas the line represents interquartile range. This graph shows that normal or moderately altered GCS score at the scene of the accident is associated with normal brain perfusion or hyperemia (high rCBV and rCBF values, low MTT values), whereas low GCS score at the scene of the accident is associated with oligemia (low rCBV and rCBF values, high MTT values).

 
Perfusion CT findings, especially the number of arterial territories with low regional cerebral blood volume, were demonstrated to be an additional independent prognostic factor, with significant likelihood ratio test results (Figure 1).

Figure 4 shows the prognosis with respect to the GOS category provided by the final ordered logistic regression, as well as the observed GOS score.



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  		Figure 4. Graph shows predicted GOS categories provided by the final ordered logistic regression analysis and involving the five statistically independent prognostic factors demonstrated in the present study: mean arterial pressure at the scene of the accident (ß = 0.060, P = .083), base excess at admission (ß = 0.243, P = .002), presence or absence of skull fractures (ß = –1.464, P = .041), CT features of cerebral herniation (ß = –2.001, P = .013), and the number of arterial territories with low rCBV values at perfusion CT (ß = –1.194, P = .008). This graph shows that the prognosis with respect to GOS category provided by the final ordered logistic regression model fits pretty well with the observed GOS score, which is featured as numbers superimposed on the prognostic curve.

 
Perfusion CT and Intracranial Hypertension
Average values measured in the subgroup of 44 patients with a diagnosis of intracranial hypertension are reported in Table 3. No statistically significant difference could be identified between these values and the corresponding ones in the subgroup of control patients, except for the MTT (P < .001), which was higher in patients with intracranial hypertension. Variability was substantial; the SDs for the three parameters were two and three times higher in the patients with intracranial hypertension than in the control patients.

When considering the number of arterial territories with low or high perfusion CT values, there was a trend for patients with intracranial hypertension to have more arterial territories with low rCBV values (median score, –1.00; interquartile range, –3.00 to 1.75; P = .004) and rCBF values (median score, –1.00; interquartile range, –2.75 to 2.00; P = .017) and to demonstrate more territories with MTT prolongation (median score, 2.00; interquartile range, 0.25–3.00; P = .018) when compared with the subgroup of patients without intracranial hypertension (rCBV: median score of 1.00 and interquartile range of 0.00–3.25; MTT: median score of 1.00 and interquartile range of 0.00–1.00; rCBF: median score of 1.00 and interquartile range of 0.00–3.00).

Perfusion CT and Cerebral Contusions
Cerebral contusions were diagnosed in 48 patients (Fig 5). In 19 patients, the contusions were detected on the admission unenhanced cerebral CT scans (hypodensities at admission, n = 11; hemorrhagic foci and hypodensities at admission, n = 8); thus, the sensitivity was 39.6%. The contusions in the remaining 29 patients (60.4%) were detected only on the delayed follow-up unenhanced CT scans (delayed hypodensities, n = 17; delayed hemorrhagic foci and hypoattenuation, n = 12).



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  		Figure 5. Perfusion CT depicts the full extent of cerebral contusions earlier and more accurately than conventional unenhanced cerebral CT. Scans were obtained in a 20-year-old man involved in a high-speed traffic accident. At admission, unenhanced cerebral CT depicts only a small hemorrhagic focus in the right frontal operculum (arrow); however, admission perfusion CT shows a more extensive brain perfusion abnormality, involving most of the right frontal lobe (white contour). This area is characterized by low rCBV, high MTT, and low rCBF values. Unenhanced cerebral CT scan obtained 24 hours after admission shows a hemorrhagic contusion in the exact zone that appeared to be abnormal on the admission perfusion CT scan. This zone progressed into a sequellar lesion, as evidenced by the unenhanced CT scan obtained at day 15.

 
In 42 of the 48 patients mentioned previously, admission perfusion CT demonstrated abnormalities in the same locations as the contusions demonstrated with conventional CT, conferring to admission perfusion CT a significantly (P < .001) higher sensitivity of 87.5%. Perfusion CT abnormalities in patients with contusions were focal corticosubcortical perfusion deficits and outlying boundaries between arterial territories. Brain perfusion showed diffuse oligemia in one of the six patients with false-negative perfusion CT results. In the five remaining patients with false-negative perfusion CT results, cerebral contusions were located outside of the two evaluated perfusion CT sections. Finally, five additional patients who had similar corticosubcortical focal perfusion deficits on the admission perfusion CT scan did not show cerebral contusions on the admission unenhanced cerebral CT scan or even on follow-up unenhanced CT scans. Overall, specificity of perfusion CT for cerebral contusions was 93.9%.

Perfusion CT values within cerebral contusions are reported in Table 3. The rCBV and rCBF values were significantly (P < .001) less than the corresponding values in control patients, while MTT was significantly (P < .001) greater. The rCBV values within the cerebral contusions were 2.7 mL · 100 g–1 ± 0.5 (mean±SD) and 2.9 mL · 100 g–1 ± 0.7 (P = .274), respectively, for the contusions that were demonstrated with both admission unenhanced cerebral CT and perfusion CT and those demonstrated only with perfusion CT. MTT values were 9.6 seconds ± 3.7 and 7.2 seconds ± 2.1, respectively (P = .139). The rCBF values were 20.7 mL · 100 g–1 · min–1 ± 10.9 and 43.0 mL · 100 g–1 · min–1 ± 25.5, respectively (P = .054).

Perfusion CT and Juxtadural Collections
Twelve epidural hematomas were diagnosed in our series. Perfusion CT values in the immediate vicinity of the epidural hematomas are reported in Table 3. They were significantly (P < .001) less than the corresponding values in control patients.

Eighteen subdural hematomas were diagnosed in our patients. Perfusion CT values in the immediate vicinity of the subdural hematomas are reported in Table 3. They were significantly (P < .001) different from the corresponding values in control patients.

Perfusion CT values of rCBV tended to be lower in the vicinity of epidural hematomas than in the vicinity of subdural hematomas, but this trend was not statistically significant (P = .154).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
We report a series of 130 patients with severe head trauma who underwent perfusion CT at admission as part of the initial CT survey. These patients were then categorized according to their GOS score at 3-month follow-up; GOS score was selected as an indicator of functional outcome. To our knowledge, this is the first study in which the use of perfusion CT in patients with head trauma has been assessed.

Perfusion CT can easily be performed as a complement to conventional unenhanced and contrast-enhanced cerebral CT and does not interfere with the contrast-enhanced thoracic-abdominal CT survey performed in patients with severe trauma (32). In our institution, as in most trauma centers, we routinely perform contrast-enhanced chest, abdominal, and pelvic CT in patients with severe trauma to rule out aortic injuries. Contrast material is administered, even to obtunded patients who are unable to report previous reactions to contrast material and patients whose renal function is uncertain, because the risk associated with an allergic reaction or renal malfunction is substantially outweighed by the risk of a missed traumatic aortic injury. The 40-mL dose of contrast material that is added for perfusion CT is minor compared with the 100–120-mL dose that is used for imaging the chest, abdomen, and pelvis. In our series of 130 patients, we observed no side effects related to contrast material administration, such as extravasation, nephrotoxicity, or an allergic reaction.

Perfusion CT involves dynamic acquisition of sequential CT sections with cine mode during intravenous administration of nonionic iodinated contrast material. We believe that perfusion CT can be implemented in all hospitals and institutions equipped with CT units that are usually available 24 hours a day and 7 days a week. Perfusion CT necessitates neither specialized technologists nor extra contrast material and requires only dedicated postprocessing software. This modality affords real-time postprocessing, with a complete set of parametric maps that are typically generated within 5 minutes of the completion of data acquisition. Perfusion CT provides quantitatively accurate assessment of brain perfusion; in fact, results have been validated by comparison with results obtained with stable xenon CT (24,33) and positron emission tomography (PET) (34).

Conventional Prognostic Factors
Among clinical findings and conventional unenhanced cerebral CT findings, the mean arterial pressure at the scene of accident, the base excess at admission, the presence or absence of skull fractures, and the CT features of cerebral herniation could be identified as independent prognostic factors. On the other hand, older age and abnormal pupillary reaction were not significantly associated with the GOS score, although they have been reported to be outcome predictors (3–5,16,35,36). This is likely related to the rather small number of old patients in the present study. Indeed, old age and abnormal pupillary reaction were correlated with clinical outcome in the simple regression analysis but not in the multiple regression analysis.

Perfusion CT and Outcome
Perfusion CT data, specifically the number of arterial territories with low rCBV values, yielded a significant prognostic contribution, in addition to clinical and conventional unenhanced cerebral CT prognostic factors.

Specific patterns of admission perfusion CT results could be identified with respect to patient outcome. Normal brain perfusion or hyperemia (high rCBV and rCBF values) was associated with a favorable outcome, whereas oligemia (low rCBV and rCBF values) was associated with an unfavorable outcome. The distribution of perfusion CT results with respect to the GCS score at the scene of the accident was similar. This is in agreement with the findings of previous studies, in which different imaging techniques were used (37–44). This pattern of brain perfusion with respect to the functional outcome can probably be attributed to the preservation or loss of cerebral vascular autoregulation (45). In patients with benign head trauma, autoregulation is preserved or very temporarily stunned. Thus, regional brain perfusion is either maintained or shows a phasic increase, and outcome is favorable (37,39,41–43,46). The phasic rise in brain perfusion observed shortly after head injury has also been attributed to an increase in brain metabolic demands in the setting of intact vasoreactivity (37–39,42,47).

In patients with more severe head trauma, autoregulation is more severely altered. Brain perfusion becomes completely dependent on systemic hemodynamics, which often results in oligemia. Luxury perfusion is uncommon in adults with such a condition (40–42,46,48).

Beside the severity of the initial injury, intracranial hypertension is the principal factor that determines outcome in patients with head injuries and is often fatal in patients with sustained values of more than 30–40 mm Hg (16). This is confirmed in the present study by the demonstration of CT signs of herniation as an independent prognostic factor in our patients.

With respect to perfusion CT results in cases of intracranial hypertension, a trend toward lower absolute rCBV and rCBF values with significantly higher MTT values and more extensive oligemia could be identified, possibly in relation to cerebral ischemia consecutive to intracranial hypertension. The absence of a clear statistically significant difference might result from the disparity of causes of intracranial hypertension, including juxtadural collections, focal parenchymatous injuries, and cerebral edema. Cerebral edema further divides into cytotoxic edema—where brain perfusion is reduced—and vasogenic edema—where brain perfusion can be increased or diminished.

Perfusion CT: Additional Information Compared with Conventional CT
The results of this study demonstrate that perfusion CT provides additional information with respect to focal brain traumatic injuries when compared with conventional cerebral CT.

Indeed, perfusion CT had a higher sensitivity for the diagnosis of cerebral contusions when compared with admission unenhanced cerebral CT, with a sensitivity of 87.5% versus a sensitivity of 39.6%, respectively. The selection of the evaluated perfusion CT sections immediately above the orbits, thus passing through the frontopolar and temporopolar regions, was ideal for the depiction of cerebral contusions, which were most often located within these areas. Similar results have been found with other functional imaging techniques, such as single photon emission CT or PET (49–53) or—more recently—MR imaging (54). Absolute perfusion values within cerebral contusions, as demonstrated with perfusion CT, are in global agreement with those measured with other imaging techniques, such as stable xenon CT (55). Perfusion was more altered within contusions that were visible on admission conventional CT scans than in those visible only on perfusion CT scans. Perfusion CT depicted focal corticosubcortical perfusion deficits in five patients who did not have cerebral contusions at admission or on follow-up unenhanced CT scans. These focal perfusion deficits were characterized by slight alterations in perfusion CT results. They may correspond to areas of traumatized brain parenchyma, with transitory cerebral edema, which recover rather than progress toward cerebral contusions, as suggested by findings of animal studies (56,57).

Finally, perfusion CT depicted brain perfusion alteration in the vicinity of juxtadural collections, as has been reported previously (58,59). This alteration tended to be more pronounced in epidural hematomas than in subdural hematomas; however, this difference was not statistically significant. It was beyond the scope of this study to determine how the thickness of the juxtadural collection and other factors influenced the perfusion CT results, and the number of observations (12 epidural hematomas and 18 subdural hematomas) was too limited to allow a definitive conclusion to be made about that topic.

We acknowledge limitations to our study. First, it included only patients with severe trauma who had a GCS score of 8 or less at admission. This may have induced some bias toward an apparent improvement in the sensitivity and specificity of perfusion CT.

There are also methodologic difficulties related to the multiple intricated variables that combine in the determination of outcome, which makes it difficult to assess the influence of each single parameter on its own. Finally, all patients were intubated and received continuous sedation. The possible repercussions of sedation on brain perfusion must be mentioned, although dedicated imaging studies have suggested that the effect of premedication on cerebral blood flow is limited (60).

In conclusion, perfusion CT can be performed in patients with severe head trauma, even in the emergency setting. Perfusion CT affords insight into regional brain perfusion alterations due to head trauma, with the major advantage of being able to depict regional heterogeneity. Its results show specific patterns that are linked to cerebral edema and intracranial hypertension. Perfusion CT offers prognostic information with respect to functional outcome, even as early as admission.

The potential repercussions of perfusion CT on the care of patients with severe head trauma remain to be evaluated. However, patients with altered brain perfusion CT results might be considered for more aggressive and early treatment to prevent intracranial hypertension, whereas patients with preserved brain perfusion might benefit from less invasive treatment.


   ACKNOWLEDGMENTS
 
The authors acknowledge the competence of L. de Palma as a research assistant in the Department of Diagnostic and Interventional Radiology. They thank M. Rousselle for her help in editing this manuscript.


   FOOTNOTES
 
Abbreviations: GCS = Glasgow Coma Scale, GOS = Glasgow Outcome Scale, MTT = mean transit time, rCBF = regional cerebral blood flow, rCBV = regional cerebral blood volume

Author contributions: Guarantor of integrity of entire study, M.W.; study concepts and design, M.W., G.v.M., P.S., R.C.; literature research, M.W.; clinical studies, all authors; data acquisition, all authors; data analysis/interpretation, M.W., P.S., J.P.R., F.P., L.R., R.M., P.M., R.C.; statistical analysis, M.W., G.v.M.; manuscript preparation and definition of intellectual content, M.W., P.S., R.C.; manuscript editing, M.W.; manuscript revision/review and final version approval, all authors


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
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