Prognostic Performance of Initial Clinical Examination in Predicting Good Neurological Outcome in Cardiac Arrest Patients Treated with Targeted Temperature Management

Abstract

Prognostication studies of cardiac arrest patients have mainly focused on poor neurological outcomes. However, an optimistic prognosis for good outcome could provide both justification to maintain and escalate treatment and evidence-based support to persuade family members or legal surrogates after cardiac arrest. The aim of the study was to evaluate the utility of clinical examinations performed after return of spontaneous circulation (ROSC) in predicting good neurological outcomes in out-of-hospital cardiac arrest (OHCA) patients treated with targeted temperature management (TTM). This retrospective study included OHCA patients treated with TTM from 2009 to 2021. Initial clinical examination findings related to the Glasgow coma scale (GCS) motor score, pupillary light reflex, corneal reflex (CR) and breathing above the set ventilator rate were assessed immediately after ROSC and before the initiation of TTM. The primary outcome was good neurological outcome at 6 months after cardiac arrest. Of 350 patients included in the analysis, 119 (34%) experienced a good neurological outcome at 6 months after cardiac arrest. Among the parameters of the initial clinical examinations, specificity was the highest for the GCS motor score, and sensitivity was the highest for breathing above the set ventilator rate. A GCS motor score of >2 had a sensitivity of 42.0% (95% confidence interval [CI] = 33.0–51.4) and a specificity of 96.5% (95% CI = 93.3–98.5). Breathing above the set ventilator rate had a sensitivity of 84.0% (95% CI = 76.2–90.1) and a specificity of 69.7% (95% CI = 63.3–75.6). As the number of positive responses increased, the proportion of patients with good outcomes increased. Consequently, 87.0% of patients for whom all four examinations were positive experienced good outcomes. As a result, the initial clinical examinations predicted good neurological outcomes with a sensitivity of 42.0–84.0% and a specificity of 69.7–96.5%. When more examinations with positive results are achieved, a good neurological outcome can be expected.

Introduction

After out-of-hospital cardiac arrest (OHCA), patient survival to hospital discharge is 9.1% (Tsao et al., 2022). Eighty percent of OHCA patients are comatose upon admission, and two-thirds of them die due to hypoxic-ischemic brain injury (HIBI) (Sandroni et al., 2018). Despite all odds, 7.2% of OHCA patients survive with good neurological outcome, defined as cerebral performance category (CPC) 1–2 (Tsao et al., 2022). Techniques and procedures in postcardiac arrest care, such as targeted temperature management (TTM) and critical care medicine, are constantly being developed. If physicians can quickly select patients predicted to have good outcomes and provide these intensive treatments properly, patient outcomes could be improved (Belohlavek et al., 2022; Nolan et al., 2021; Panchal et al., 2020; Pineton de Chambrun et al., 2016).

Prediction of poor neurological outcome in cardiac arrest patients has been a key focus of research, requiring high specificity as it provides the basis for withdrawal of life-sustaining treatment (WLST). A systematic review of poor neurological outcomes after cardiac arrest published in 2020 included 94 studies and provided the foundation for the 2021 European Resuscitation Council and European Society of Intensive Care Medicine guidelines (Nolan et al., 2021; Sandroni et al., 2020). In contrast, research on good neurological outcomes is lacking. A systematic review that included literature published as late as October 2021 included 37 studies, of which only 2 concerned clinical examinations (Sandroni et al., 2022).

As much is known about poor neurological prognosis, more research is still needed regarding assessment of a good prognosis for purposes of accurate stratification. An optimistic prognosis provides both justification to maintain and/or escalate treatment by attending physicians and evidence-based support to persuade family members or legal surrogates. Moreover, as no prognostic examination is perfect, a re-examination for good prognostic markers provides a safety brake—a double check before WLST. Among the neuroprognostication tests recommended in the guidelines, procedures involving neurophysiology, biomarkers, and imaging require considerable time for performance and evaluation. However, if an examination can be performed manually and quickly without special equipment, we can expect not only time savings but also cost savings. In particular, by performing tests that detect preserved brain function, the possibility of HIBI and good neurological outcome could be estimated.

Herein, the aim of this study was to evaluate clinical examination as a means of predicting good neurological outcomes in OHCA patients treated with TTM. In this study, four parameters were evaluated: (1) Glasgow coma scale (GCS) motor score, (2) pupillary light reflex (PLR), (3) corneal reflex (CR), and (4) breathing above the set ventilator rate. The predictive accuracy of each parameter was analyzed.

Methods

Study design and population

The study is a retrospective analysis of data from a single center (The Catholic University of Korea Seoul St. Mary's Hospital) collected prospectively from February 2009 to December 2021. During the study period, investigators enrolled study participants into the Utstein-style registry.

This study included all adult OHCA patients (18 years and older) treated with TTM. Patients with active intracranial bleeding, acute stroke, known limitations in therapy and a do-not-attempt resuscitation order, known prearrest CPC score of 3 or 4, body temperature of 30°C on admission and unknown outcomes for 6 months after return of spontaneous circulation (ROSC) were excluded. The initial clinical examination was conducted immediately after ROSC and before starting TTM. For patients who arrived at the emergency room with ongoing cardiac arrest, intubation was performed during cardiopulmonary resuscitation (CPR) without any sedative or paralytics, and the patient's clinical status was evaluated immediately after ROSC.

For patients who arrived with ROSC during emergency medical services transportation, initial clinical examination was performed on arrival at the emergency room and, if necessary, sedatives (etomidate or midazolam) and paralytics (vecuronium) were administered for intubation. For patients transferred from other hospitals with ROSC, the medical records of the referring hospital were reviewed to analyze the results of the initial clinical examination immediately after ROSC. Patients with missing data for GCS motor score, PLR, CR, or breathing above the set ventilator rate after achieving ROSC were excluded. Implementation of TTM, including the target temperature setting, TTM duration, and TTM methods, was in accordance with a pre-established protocol (Rittenberger et al., 2011). Midazolam for sedation and rocuronium for neuromuscular block were continuously given during the induction and maintenance phases of TTM in this center.

At this center, all patients who are eligible for TTM after ROSC receive continuous intensive care without WLST because decisions regarding allowing WLST are still under debate in the Republic of Korea. However, when refractory shock or multiple organ failure persists during TTM or brain death is determined after completing TTM, some caregivers may request do-not-escalate or do-not-resuscitate.

Data collection and endpoint

The data extracted from the registry included the following: age, sex, comorbidities (hypertension and diabetes), witnessed arrest, bystander CPR, shockable rhythm, cause of arrest, time from collapse to ROSC, initial lactate level, initial glucose level, and results of clinical examination. The clinical examination included the following four parameters, procedures regarding which were performed immediately after ROSC and before initiation of TTM: GCS motor score, PLR, CR, and breathing above set ventilator rate (spontaneous respiration determined by physicians).

The primary outcome was good neurological outcome, defined as a CPC score of 1–2, at 6 months after cardiac arrest. The CPC scale ranges from 1 to 5 (1: good cerebral performance or slight cerebral disability; 2: moderate disability or independent activities of daily life; 3: severe disability or dependence on others for daily support; 4: a coma or vegetative state; 5: death or brain death). The researcher contacted surviving discharged patients or their relatives. For follow-up, face-to-face visits or telephone interviews were recommended.

Statistical analyses

All data are displayed as numbers and percentages for categorical variables and as medians with interquartile ranges for continuous variables. Comparisons of categorical variables between the groups were made using the chi-square test or Fisher's exact test. After testing for normal distribution, continuous variables were compared using Student's t-test or Wilcoxon's rank-sum tests. A prognostic accuracy study was evaluated by using receiver operating characteristic (ROC) curves, and sensitivity and specificity were calculated. Statistical analyses were performed using SPSS version 24.0 (SPSS, Chicago, IL, USA). A p-value <0.05 was considered statistically significant.

The study was approved by the Institutional Review Boards of Seoul St. Mary's Hospital (XC15OIMI0081K). In accordance with the Helsinki Declaration, all enrolled patients or their legal surrogates were required to provide written informed consent.

Results

Among 404 subjects considered for inclusion, a total of 350 subjects were ultimately included. Fifty-four patients were excluded because 37 had been treated with extracorporeal membrane oxygenation and 17 had missing data. The data most often missing were related to CR. Of the 350 analyzed patients, 119 (34%) experienced good neurological outcomes and 231 (68%) exhibited poor neurological outcomes at 6 months after ROSC (Fig. 1 and Supplementary Table S1).

FIG. 1.

Flowchart for study inclusion. CR, corneal reflex; ECMO, extracorporeal membrane oxygenation; GCS, Glasgow coma scale; PLR, pupillary light reflex.

The demographic characteristics of subjects according to neurological outcome are shown in Table 1. The median age was 50 years in the good neurological outcome group and 59 years in the poor neurological outcome group. Males comprised the majority in the good and poor neurological outcome groups at 76.5% and 70.1%, respectively. Among 119 patients with good neurological outcomes, 79.8% experienced witnessed cardiac arrests, 67.2% received bystander CPR, 75.6% had a shockable rhythm, 89.9% had a cardiac cause of arrest, and the median time from collapse to ROSC was 17 min.

Table 1.

Demographic Characteristics of Subjects According to Neurological Outcome

	Good	Poor	p-Value
	n = 119	n = 231	p-Value
Age, median (IQR)	50 (39–61)	59 (46–72)	<0.001
Male, n (%)	91 (76.5)	162 (70.1)	0.257
Comorbidities
HTN, n (%)	30 (25.2)	88 (38.1)	0.017
DM, n (%)	12 (10.1)	69 (29.9)	<0.001
Witnessed arrest, n (%)	95 (79.8)	139 (60.4)	<0.001
Bystander CPR, n (%)	80 (67.2)	128 (55.7)	0.039
Shockable rhythm, n (%)	90 (75.6)	41 (17.7)	<0.001
Cardiac cause of arrest, n (%)	107 (89.9)	101 (43.7)	<0.001
Time from collapse to ROSC, median (IQR)	17.0 (10.0–28.5)	36.0 (26.0–46.5)	<0.001
Initial lactate, mmol/L	9.6 (6.4–13.3)	13.1 (10.2–17.0)	<0.001
Initial glucose, mg/dL	252.0 (197.5–288.8)	288.0 (229.5–363.5)	0.001
GCS motor score >1, n (%)	60 (50.4)	15 (6.5)	<0.001
GCS motor score >2, n (%)	50 (42.0)	8 (3.5)	<0.001
Reactive PLR, n (%)	86 (72.3)	38 (16.5)	<0.001
Reactive CR, n (%)	66 (55.5)	15 (6.5)	<0.001
Reactive in both PLR and CR, n (%)	100 (84.0)	70 (30.3)	<0.001
Reactive PLR or CR, n (%)	66 (55.5)	15 (6.5)	<0.001
Breathing above set ventilator rate, n (%)	86 (72.3)	38 (16.5)	<0.001
33°C as a target temperature,^a n (%)	106 (89.1)	211 (91.3)	0.492

Data presented as n (%) for categorical variables and as means ± standard deviations for continuous variables.

The remaining of patients had a target temperature set at 36°C during target temperature management.

CPR, cardiopulmonary resuscitation; CR, corneal reflex; DM, diabetes mellitus; GCS, Glasgow coma scale; HTN, hypertension; IQR, interquartile range; PLR, pupillary light reflex; ROSC, return of spontaneous circulation.

Ninety percent of the patients received TTM at 33°C, whereas the remaining 10% received TTM at 36°C. Age, presence of comorbidities (hypertension and diabetes mellitus), time from collapse to ROSC, lactate level, and glucose level were significantly higher in the poor neurological outcome group. The parameters of witnessed arrest, bystander CPR, shockable rhythm, and cardiac cause of arrest were observed in significantly higher percentages of patients in the good neurological outcome group.

Table 2 shows the prognostic performance of clinical examinations. Each area under the ROC curve showed fair discrimination (>0.7) except that of GCS motor score >2. The sensitivity was highest for breathing above the set ventilator rate (84%), and the specificity was highest for the GCS motor score (96.5%). A GCS motor score >2 had a sensitivity of 42.0% (95% confidence interval [CI] = 33.0–51.4) and a specificity of 96.5% (95% CI = 93.3–98.5). Breathing above the set ventilator rate had a sensitivity of 84.0% (95% CI = 76.2–90.1) and a specificity of 69.7% (95% CI = 63.3–75.6). The initial clinical examinations predicted good neurological outcomes with sensitivity ranging from 42.0% to 84.0% and specificity ranging from 69.7% to 96.5%.

Table 2.

Prognostic Performance of Single Prognostic Methods for Predicting Good Neurological Outcomes

	AUC (95% CI)	Sensitivity % (95% CI)	Specificity % (95% CI)	TP	TN	FP	FN
GCS motor score >1	0.720	50.4	93.5	60	216	15	59
GCS motor score >1	(0.658–0.781)	(41.1–59.7)	(89.5–96.3)	60	216	15	59
GCS motor score >2	0.693	42	96.5	50	223	8	69
GCS motor score >2	(0.629–0.756)	(33.0–51.4)	(93.3–98.5)	50	223	8	69
Reactive PLR	0.779	72.3	83.6	86	193	38	33
Reactive PLR	(0.725–0.834)	(63.3–80.1)	(78.1–88.1)	86	193	38	33
Reactive CR	0.745	55.5	93.5	66	216	15	33
Reactive CR	(0.685–0.805)	(46.1–64.6)	(89.5–96.3)	66	216	15	33
Reactive in both PLR and CR	0.745	55.5	93.5	66	216	15	53
Reactive in both PLR and CR	(0.685–0.805)	(46.1–64.6)	(89.5–96.3)	66	216	15	53
Reactive PLR or CR	0.779	72.3	83.6	86	193	38	33
Reactive PLR or CR	(0.725–0.834)	(63.3–80.1)	(78.1–88.1)	86	193	38	33
Breathing above set ventilator rate	0.769	84.0	69.7	100	161	70	19
Breathing above set ventilator rate	(0.717–0.821)	(76.2–90.1)	(63.3–75.6)	100	161	70	19

Data presented as n for TP, TN, FP, and FN.

AUC, area under the curve; CI, confidence interval; FN, false negative; FP, false positive; TN, true negative; TP, true positive.

A greater number of positive clinical examination findings (GCS motor score >1, presence of PR, presence of CR, breathing above set ventilator rate) correlated with a greater percentage of good neurological outcome (Fig. 2). Even with no positive findings, 6.1% of patients experienced good neurological outcomes. Among the patients with one positive finding (n = 60), breathing above the set ventilator rate was observed in the highest proportion (n = 49). Patients with two positive findings (n = 34) mainly had a combination of reactive PLR and breathing above the set ventilator rate (n = 24, 70.6%). Both reactive PLR and CR with breathing above the set ventilator rate were the most common in the group of patients with three positive findings.

FIG. 2.

Association between clinical examinations and neurological outcomes at 6 months after cardiac arrest. Positive findings mean GCS motor score >1, reactive PLR, reactive CR, and breathing above the set ventilator rate.

Discussion

This study showed that GCS motor score, PLR, CR, and breathing above the set ventilator rate immediately after ROSC can predict good neurological outcome with sensitivity as high as 84.0% and specificity as high as 96.5%. The more of these positive clinical examination findings there were, the more the association with good neurological outcomes at 6 months after cardiac arrest.

Until recently, prognostication studies of cardiac arrest patients have mainly focused on poor neurological outcomes (CPC scores of 3–5). In previous studies predicting poor outcomes, the results of neurological examinations such as GCS motor score or the absence of PLR and CR were studied as predictors (Sandroni et al., 2020). The absence of PLR immediately after ROSC had high sensitivity, ranging from 65.5% to 77.1% in previous studies (Choi et al., 2017; Ryoo et al., 2015). These studies also showed that the absence of CR at ROSC had high sensitivities of 96.4% and 93.2%, respectively. The GCS motor score was also evaluated by Kim et al., and a motor score of 1 on admission provided 100% sensitivity but a false positive rate of 75.1% (Kim et al., 2013).

However, predicting a poor outcome necessitates 100% specificity because it is related to discontinuation of treatment such as WLST. Therefore, most guidelines recommended a multimodal neuroprognostication strategy involving clinical examination, neurophysiology, biomarkers, and imaging (Nolan et al., 2021; Panchal et al., 2020). Furthermore, delaying this assessment by at least 72 h is recommended to avoid making a premature decision. In contrast to poor neurological prognostication, good outcome prediction can identify the likelihood of favorable neurological recovery and aid in determining whether to increase the level of organ support. In this study, we tried to predict good outcome with GCS motor score, PLR, CR, and breathing above the ventilator setting immediately after ROSC.

Although only a few studies were found regarding the prediction of good outcomes, a recent systematic review showed that a withdrawal or localization motor response to pain after ROSC is a predictor of good neurological outcome (Sandroni et al., 2022). With a GCS motor score of >3 after TTM completion, a similar result was confirmed at a rate of 100% (Schefold et al., 2009). In a post hoc analysis of the TTM trial, the same parameters evaluated at 72–96 h predicted good outcome with 84% specificity (Moseby-Knappe et al., 2020).

However, since the results of clinical examination performed after TTM can be affected by the presence of sedative and paralytic agents, assessment ahead of TTM is relatively reliable for predicting outcome (Nolan et al., 2021). Hifumi et al. showed that a GCS motor score of 4–5 on admission without sedatives and paralytics had 98% specificity for good outcome (Hifumi et al., 2015). Consistent with this result, the highest specificity (96.5%) was found in our study when the patients' GCS motor score was >2 at ROSC.

Although there are many studies in which the absence of PLR or CR has been used as a predictor of poor neurological outcome, there have been few studies in which performance as a predictor of good outcome is evaluated. Among poor outcome studies, a study by Dhakal et al. mentioned a significant association between the reactive PLR before hypothermia and good outcomes (CPC score of 1–2) (Dhakal et al., 2016). In a study comparing the neurological pupil index (NPi) and standard PLR, 31% of patients with good outcomes had significantly higher initial NPi than patients with poor outcomes (59%) (Riker et al., 2020). However, since the primary indicator of a result in these studies was a poor neurological outcome, we evaluated the performance of PLR or CR as a parameter for predicting a good outcome.

As a result, PLR and CR showed fair discrimination ability with area under the curves (AUCs) of 0.779 and 0.745, respectively. We assumed that if both reflexes were present, the discrimination might be improved. However, the result was the same as the AUC of CR. All patients with reactive CR also had reactive PLR. One possible explanation may be that if the change in pupil size is too small to detect visually, the presence of PLR could be missed by the operator (Oddo et al., 2018). Another study showed that the specificity and sensitivity for poor outcome are significantly better when using a tool such as quantitative pupillary reflex (NPi) than when using standard PLR (Oddo et al., 2018). As inadequate agreement of manual pupillary assessment was also observed for each clinician (Olson et al., 2016), a more standardized approach to measuring PLR seems preferable.

To our knowledge, breathing above the set ventilator rate is a rarely used predictor in previous studies. Although spontaneous respiratory activity expressed as gasping in OHCA was associated with increased survival to discharge in a systematic review (Zhao et al., 2015), the association between neurological outcome and spontaneous respiration after ROSC was not evaluated. In a study by Abe et al., spontaneous respiration of cardiac arrest patients at emergency department arrival after ROSC was significantly related to good neurological outcome (CPC score of 1) at 30 days after cardiac arrest.

However, since the enrolled patients did not receive TTM, the impact of TTM on prognosis was not reflected (Abe et al., 2009). In our study, all patients were treated with TTM, and 90% of them were provided with a target temperature 33°C. Breathing above the set ventilator rate as a parameter showed a specificity of 69.7% and the highest sensitivity (84.0%) in predicting good neurological outcomes. Spontaneous respiration after ROSC also indicates that brainstem function remains, so we could utilize the parameter as a prognostic factor in the future.

This study has several strengths. We tried to predict cardiac arrest patient outcomes through clinical examinations that could be applied quickly, cost-effectively, and unlimitedly immediately after ROSC. Furthermore, the influence of sedatives and paralytics on results can be avoided because the examination is performed before TTM starts. The results of this early examination might also help patients proceed to receiving TTM or help determine subsequent treatment, providing caregivers with optimistic information. Furthermore, we discovered that the greater the number of positive findings observed in these examinations, the higher the proportion of patients with good outcomes. Early identification of these good outcomes with high sensitivity may be of value in making treatment strategy decisions and may facilitate future clinical research.

There were several limitations in this study. This retrospective analysis inevitably leads to selection bias, information bias, and the effects of other confounders. Because the study was limited to a single center, these results were difficult to generalize. Furthermore, the number of patients with a good outcome (34.0%) among the included patients in this study was lower than that in previous studies (53–66%) (Dankiewicz et al., 2021; Kirkegaard et al., 2017). This might be due to significantly fewer cases of witnessed arrests, bystander CPR, and shockable rhythms in our study, which were expected to have an impact on the outcome.

The data collection and processing were not blinded, and a self-fulfilling prophecy might have influenced the results. Since the examinations are performed manually, reliability might be lower than would have been provided by standardized methods (e.g., NPi). Finally, the study investigated clinical examinations solely, and there were patients who showed good outcomes even without any positive findings (6.1%). This might highlight the need for a multimodal approach in good outcome prediction, as is the case for poor outcome prediction. In the future, there is the promise of research that will combine clinical examination, neurophysiology, biomarkers, and imaging in predicting good outcomes.

Conclusions

This study showed that the parameters GCS motor score, PLR, CR, and breathing above set ventilator rate evaluated in initial clinical examinations predicted good neurological outcome at 6 months with sensitivity of 42.0–84.0% and specificity of 69.7–96.5%. Performing these examinations simultaneously might be helpful for predicting good neurological outcome after cardiac arrest.

Footnotes

Authors' Contributions

We confirm that authorship requirements have been met and the final article was approved by all authors. Data curation, formal analysis, investigation, and writing—original draft by J.-S.L. Methodology, formal analysis, investigation, data curation, and writing—review and editing by H.J.B. Conceptualization, methodology, validation, supervision, and project administration by C.S.Y. Conceptualization, resources, and visualization by S.H.K. Methodology, validation, and data curation by S.P. Resources, formal analysis, and project administration by H.J.K. Conceptualization and supervision by K.N.P. Methodology, validation, and visualization by S.H.O.

Author Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for the study.

Supplementary Material

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