The association of findings on brain computed tomography with neurologic outcomes following extracorporeal cardiopulmonary resuscitation
© The Author(s). 2017
Received: 8 September 2016
Accepted: 4 January 2017
Published: 25 January 2017
Limited data are available on imaging predictors of neurological outcomes after extracorporeal cardiopulmonary resuscitation (ECPR). We investigated the association of initial brain computed tomography (CT) findings with neurological outcomes following ECPR.
Between February 2005 and December 2015, a total of 42 patients who underwent brain CT scans within 48 h after ECPR were analyzed. Loss of the boundary between gray matter and white matter (LOB) or cortical sulcal effacement (SE), gray-to-white matter ratio (GWR), and optic nerve sheath diameter (ONSD) were measured on initial brain CT. The primary outcome was the Cerebral Performance Categories (CPC) scale at discharge.
Of the 42 adult ECPR patients, 23 (54.8%) patients survived to discharge and 19 (45.2%) patients had good neurological outcomes (CPC 1 and 2). The area under the curve (AUC) of GWR in the basal ganglia (GWR-BG) was 0.792 (95% confidence interval (CI), 0.639–0.901, p = 0.001). ONSD (AUC 0.745; 95% CI, 0.587 – 0.867, p = 0.007) was 5.57 (interquartile range (IQR) 5.14 – 5.98) mm in the good neurological outcome group versus 6.07 (IQR 5.71 – 6.64) mm in the poor outcome group. LOB or SE were more often detected in the poor neurological outcome group (AUC 0.817; 95% CI, 0.682–0.952, p <0.001). The predictive performance of poor neurological outcomes of a composite of GWR-BG, ONSD, and LOB/SE was significantly improved (AUC 0.904; 95% CI, 0.773–0.973) compared to when each brain CT marker was considered separately (GWR-BG, p = 0.048; ONSD, p = 0.026; LOB/SE, p = 0.028).
GWR, ONSD, and LOB/SE on initial brain CT scans are associated with neurological prognosis in patients who underwent ECPR. The new risk prediction model, which uses a composite of GWR, ONCD, and LOB/SE, could provide better information on neurologic outcomes in patients underwent ECPR.
KeywordsBrain computed tomography Cardiopulmonary resuscitation Extracorporeal membrane oxygenation
Unconscious patients admitted to intensive care units (ICUs) after cardiac arrest are at a high risk of death, and development of neurologic deficits is common among those who survive . In particular, neurological outcomes have been investigated more in patients with stable vital signs and reversible causes of arrest after a return of spontaneous circulation (ROSC). In the setting of conventional cardiopulmonary resuscitation (CPR), several predictors of neurological outcome have been reported such as physical examination of brainstem reflexes, various serum markers, and electrophysiologic study results [2–4]. Additionally, brain imaging may be helpful for predicting neurological outcomes after cardiac arrest [5–11]. Recently, extracorporeal cardiopulmonary resuscitation (ECPR) has been increasingly utilized to supply oxygenated blood and hemodynamic support in the absence of spontaneous cardiac circulation. Similar to studies on conventional CPR, there have been several studies on neurological prognosis in patients receiving ECPR [12–17]. However, there are limited data available on prognostic imaging markers of neurological outcomes after ECPR . Brain computed tomography (CT) is simple, cost-effective, and easily implemented after ECPR . Therefore, we investigated the association of initial brain CT findings with neurological outcomes following ECPR.
This was a retrospective, single-center, observational study of adult patients who underwent ECPR during hospitalization at the Samsung Medical Center between February 2005 and December 2015. This study was approved by the Institutional Review Board of the Samsung Medical Center. The requirement for informed consent was waived due to the retrospective nature of the study.
Definitions and outcomes
CPR was led by the CPR team of the hospital, and all facts related to the CPR scene were recorded by bedside nurses according to Utstein-style guidelines . When CPR was performed for more than 10 min or in the event of unstable vital signs or recurrent cardiac arrest, the institutional rapid response team contacted the on-call ECMO team leader who, along with the CPR leader, assessed the patient and made a decision about whether to institute ECPR. ECPR was performed when a witnessed arrest was confirmed, the arrest persisted despite conventional CPR lasting for more than 10 min, and the event that caused the arrest was considered reversible . Cases in which ECPR was deferred included a short life expectancy (<6 months), terminal malignancy, an unwitnessed collapse, limited physical activity, an unprotected airway, or CPR undertaken for more than 60 min at the time of initial contact. Age alone did not constitute a contraindication to ECPR .
The ECMO team consisted of cardiologists, cardiovascular surgeons, intensivists, special nurses, and perfusionists. Either the Capiox Emergency Bypass System (Terumo, Tokyo, Japan) or the Prolonged Life Support System (Maquet Cardiopulmonary, Hirrlingen, Germany) was used in all cases. A crystalloid solution such as normal saline or balanced solution was used for priming; no patient had blood-primed ECMO. A percutaneous vascular approach was tried initially in all cases using the Seldinger technique, but when percutaneous cannulation failed surgical cut-down exposure was performed . The femoral vessels were the most common sites of vascular access, with the use of 14 to 17 French arterial cannulas and 20 to 24 French venous cannulas . Cardiac compression was stopped once ECMO pump-on was successful during CPR. Anticoagulation was accomplished by a bolus injection of unfractionated heparin, followed by continuous intravenous heparin infusion to maintain an activated clotting time between 150 and 180 s. The initial number of revolutions per minute of the ECMO device was adjusted to achieve an ideal cardiac index greater than 2.2 L/min/m2 of body surface area, central mixed venous oxygen saturation above 70%, and a mean arterial pressure above 65 mm Hg . Blood pressure was monitored continuously through an arterial catheter, and an artery in the right arm was used for arterial blood gas analysis to estimate cerebral oxygenation. After ECMO, the necessary steps were taken to treat the cause of the arrest, such as percutaneous coronary intervention, coronary artery bypass grafting, heart transplantation, non-coronary cardiopulmonary surgery, or non-cardiopulmonary surgery .
All data are presented as medians and interquartile ranges (IQRs) for continuous variables and as numbers (percentages) for categorical variables. Data were compared using the Mann-Whitney U test for continuous variables, and the Chi-square test or Fisher’s exact test for categorical variables. The predictive performance of each brain CT marker was assessed using the area under the curve (AUC) of the receiver operating characteristic (ROC) curves of the sensitivity over 1 – specificity. AUCs were compared using the nonparametric approach published by DeLong et al.  for two correlated AUCs. The optimal cut-off values of each brain CT marker for predicting poor neurological outcome were obtained by ROC curve and Youden index [28, 29]. All tests were two-sided, and p values <0.05 were considered to indicate statistical significance. Data were analyzed using IBM SPSS statistics version 20 (IBM, Armonk, NY, USA).
Baseline characteristics of comatose patients who underwent brain CT scans after ECPR
Good neurological outcome (n = 19)
Poor neurological outcome (n = 23)
Total (n = 42)
Age, years (median (IQR))
Gender, male (n (%))
Body mass index (kg/m2)
Medical history (n (%))
Previous myocardial infarction
Initial Glasgow Coma Scale (median (IQR))
Target temperature manage by surface cooling device (n (%))
Interval between ECPR and CT scan (n (%))
Laboratory data on admission (median (IQR))
Initial lactate (mg/dl)
Hemoglobin before ECPR (g/dl)
Hemoglobin after ECPR (g/dl)
Total bilirubin (mg/dl)
Blood urea nitrogen (mg/dl)
Characteristics of cardiac arrest in comatose patients who underwent brain CT scans after ECPR
Good neurological outcome (n = 19)
Poor neurological outcome (n = 23)
Total (n = 42)
Type of cardiac arrest (n (%))
Out-of-hospital cardiac arrest
In-hospital cardiac arrest
Bystander-witnessed cardiac arrest (n (%))
Bystander-performed CPR (n (%))
First monitored rhythm (n (%))
Pulseless electrical activity
Shockable rhythm (VT or VF)
Defibrillation (n (%))
ROSC before ECMO insertion (n (%))
CPR to ECMO pump-on time, min (median (IQR))
Location of ECMO insertion (n (%))
Intensive care unit
Cardiac cause of arrest (n (%))
Acute coronary syndrome
Acute aortic syndrome
Left ventricular wall rupture
Clinical and neurological outcomes
Among 42 adult cardiac arrest patients who underwent ECPR, successful ECMO weaning was achieved in 29 patients (69.0%) and survival to discharge was identified in 23 patients (54.8%). Of these 23 survivors, 19 patients (45.2%) had good neurological outcomes (CPC 1 and 2). The ICU mortality rate was 40.5% (17 patients). Of the 42 patients, target temperature management was performed in 16 patients (38.1%) using surface cooling devices.
Brain CT findings
Comparisons of the attenuation in regions of interest and of the gray-to-white matter ratio (GWR), optic nerve sheath diameter, and early computed tomography signs between groups
Good neurological outcome (n = 19)
Poor neurological outcome (n = 23)
Density of regions of interest, HU (median (IQR))
Centrum semiovale (cortical)
High convexity area (cortical)
GWR (median (IQR))
GWR-BG (basal ganglia)
Optic nerve sheath diameter, mm (median (IQR))
LOB at level of basal ganglia (n (%))
SE at level of centrum semiovale (n (%))
ECPR has been increasingly utilized to supply oxygenated blood and hemodynamic support in the absence of spontaneous cardiac circulation. Therefore, ECPR may be considered in settings where it can be rapidly implemented among selected cardiac arrest patients who have not responded to initial conventional CPR . In addition, ECPR had a short-term and long-term survival benefit over conventional CPR in patients with in-hospital cardiac arrest of cardiac origin [14, 31]. Similar to studies on conventional CPR, there have been several studies on neurological prognosis in patients receiving ECPR [12–17]. However, limited data are available on prognostic imaging markers of neurological outcomes after ECPR .
In the present study, we evaluated whether GWR, ONSD, and LOB/SE as measurable variables on initial brain CT scans were associated with neurological outcome in patients who underwent ECPR. Although there were no significant differences between the average attenuation in Hounsfield units of each ROI, GWRs (except GWR-CO) on initial brain CT were higher in the good neurological outcome group than in the poor outcome group. ONSD on initial brain CT was correlated closely with neurologic outcome and was greater in the poor neurological outcome group. LOB sign and SE sign were more likely to be detected in the poor neurological outcome group than in the good neurological outcome group. GWR, ONSD, and LOB/SE were associated with neurological outcome after ECPR, and these three CT markers had statistically similar predictive power on poor neurological outcome. Furthermore, a composite of GWR-BG, ONSD, and LOB/SE was a significantly greater predictor of poor neurological outcomes than were each brain CT marker alone.
There have been reports on several predictors of neurological outcome after conventional CPR . Absence of brainstem reflex and motor response other than extensor posturing over a period of 72 h and myoclonic status epilepticus are markers of poor outcomes after cardiac arrest [2, 3]. Elevated serum S-100B and neuron-specific enolase levels and bilaterally absent somatosensory evoked potentials appear to have prognostic value in predicting a poor outcome [2, 3]. In addition, there have been reports of neuroimaging studies such as brain CT, brain magnetic resonance imaging, and magnetic resonance spectroscopy after conventional CPR . In particular, brain CT scans may be helpful for predicting neurological outcomes after ECPR because brain magnetic resonance imaging is an expensive and time-consuming procedure and cannot be immediately performed because of ECMO equipment in patients receiving ECPR . Sedation may confound outcome prediction in survivors of cardiac arrest . Sedative medications are commonly used in comatose CPR survivors for 72 h and are an important confounder . Some clinical signs and examinations such as a motor response to noxious stimuli, corneal reflex, caloric testing, and electroencephalography may also be confounded by sedation [2, 32]. Therefore, brain CT may be more helpful for predicting neurological outcome in ECPR patients under sedation. However, there are limited data on prognostic markers of brain CT for neurological outcomes after ECPR [13, 18].
Some signs on brain CT have been associated with ischemic cerebral insult and poor neurological outcome [5, 7–11]. The LOB and SE signs are associated with ischemic brain damage and poor outcome after cardiac arrest . These signs were also associated with poor neurological outcomes after ECPR in this study. However, identification of these signs may be subject to the abilities of each investigator, and these signs are not quantifiable. GWR was associated with neurological outcome in patients receiving both conventional CPR and ECPR [5, 7–11]. GWR may be explained by the quantitative association of cerebral edema following hypoxic injury with increased intracranial pressure. Similar to other studies, GWRs were significantly different and the attenuation in Hounsfield units in the ROIs were not statistically different between the two groups in this study [5, 9, 10]. In previous studies, average GWR was a better predictor of neurologic outcome than the GWRs of single regions such as BG or the cerebellum alone [5, 9–11]. However, GWR-BG had the largest AUC for prediction of poor neurological outcome among the GWRs in this study. The predictive power of GWR-AV may have been decreased because GWR-CO had little association with poor neurological outcomes in this study. GWRs may be a useful predictor of neurological outcome after ECPR, although the GWR cut-off values were different in different studies [5, 9, 10].
Measurement of ONSD has been proposed as an alternative method for the detection of increased intracranial pressure . The optic nerve is surrounded by cerebrospinal fluid because it is a part of the central nervous system. Therefore, increased intracranial pressure will be transmitted through the subarachnoid space surrounding the optic nerve within the nerve sheath, especially the retrobulbar segment, unless circulation of cerebrospinal fluid is not blocked . ONSD on initial brain CT may be correlated with neurologic outcomes after cardiac arrest [11, 24, 25]. Simultaneous measurement of ONSD on initial CT and intracranial pressure were correlated, and ONSD was indicative of intracranial hypertension in patients with severe traumatic brain injury. ONSD may be a good predictive marker associated with intracranial pressure . Although ONSD is easy to measure on a brain CT scan, it may sometimes be difficult to measure ONSD precisely because of an inappropriate thickness of a CT section or artifacts on brain CT. In addition, similar to GWR, the cut-off values of ONSD differ between studies [11, 24, 25]. We developed a new predictive model for neurological outcomes to overcome a weakness caused by the variation in cut-off values of GWR and ONSD, and a composite of GWR, LOB/SE, and ONSD was a powerful predictor of neurological outcomes compared with each parameter alone. In real-world practice, combined CT parameters could provide improved information on early neurological prognosis in patients undergoing ECPR.
This study had several limitations. First, it was a retrospective review of medical records. Thus, the CPC scale was also retrospectively determined based on medical records. Second, we used a small heterogeneous group of subjects over a large period of time from a single institution. Over this time frame there has also been a significant change in post-arrest management which may affect patients’ outcomes over the study period. Third, the nonrandomized nature of the registry data could have resulted in selection bias. Although brain CT scans were performed within 48 h following ECPR, a major limitation of the study might be that the CT scans are performed in different time settings. However, in this study, AUC of a composite of three markers (GWR-BG + ONSD + LOB/SE) on brain CT within 15.2 h (median time) was not significantly different from that after 15.2 h (0.886 (95% CI, 0.749–0.963) vs. 0.943 (95% CI, 0.825–0.991); p = 0.448). One-third of patients received targeted temperature management. Hypothermia can cause coagulopathy, so therapeutic hypothermia was not attempted if patients had substantial bleeding after ECMO insertion. Therefore, surface cooling devices such as Arctic Sun were used on a limited number of patients in our study. Lastly, our study was conducted at a single institution and involved a small number of subjects. Thus, future studies with larger cohorts are needed to confirm these findings.
GWR, ONSD, and LOB/SE on initial brain CT scans are associated with neurological outcome in patients who underwent ECPR. The new risk prediction model, which uses a composite of GWR, ONCD, and LOB/SE, could provide better information on neurologic outcomes in patients who underwent ECPR.
Brain CT may be more helpful for predicting neurological outcome in ECPR patients under sedation because some clinical signs and examinations may also be confounded by sedation.
GWR, ONSD, and LOB/SE on initial brain CT scans are associated with neurological outcome in patients who underwent ECPR.
A composite of GWR, LOB/SE, and ONSD was a powerful predictor of neurological outcomes compared with each parameter alone. In real-world practice, combined CT parameters could provide improved information on early neurological prognosis in patients who underwent ECPR.
Area under the curve
Cerebral Performance Categories
Extracorporeal membrane oxygenation
Extracorporeal cardiopulmonary resuscitation
Gray-to-white matter ratio
Average of gray-to-white matter ratios
Gray-to-white matter ratio in the basal ganglia
Gray-to-white matter ratio in the cortex
Simplified gray-to-white matter ratio
Intensive care unit
Loss of the boundary between gray matter and white matter
Medial white matter
Optic nerve sheath diameter
Posterior limb of the internal capsule
Receiver operating characteristic
Regions of interest
Return of spontaneous circulation
Cortical sulcal effacement
We appreciate the excellent statistical support of Keumhee C. Carriere, PhD, and Joonghyun Ahn, MS, at the Samsung Biomedical Research Institute.
Availability of data and materials
Our data are available on the Harvard Dataverse Network (http://dx.doi.org/10.7910/DVN/FS7TVU) as recommended repositories of Critical Care.
JAR participated in study design, data collection, drafting of the manuscript, and the statistical analysis. CRC participated in the statistical analysis and helped draft the manuscript. YHC participated in study design, performed the statistical analysis, and drafted the manuscript. KS participated in the statistical analysis and helped draft the manuscript. GYS participated in study design and coordination and helped draft the manuscript. TKP participated in study design and drafting of the manuscript. YBS participated in study conception and design, data collection, and drafting of the manuscript. JYH participated in study design and coordination. JHC participated in the statistical analysis and helped draft the manuscript. HCG participated in the statistical analysis and helped draft the manuscript. SHC participated in the statistical analysis and helped draft the manuscript. JHY participated in study conception and design, data collection, and drafting of the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
Not applicable. This study did not contain any individual person’s data in any form (including individual details, images, or videos).
Ethics approval and consent to participate
This study was approved by the Institutional Review Board of the Samsung Medical Center (SMC 2016-05-086) according to the Declaration of Helsinki on reviewing and publishing information from patient’s records. Informed consent was waived because of the retrospective nature of the study.
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