The essential neurological examination of the unconscious patient in the emergency room

Abstract Objective To determine whether neurologists with long‐term experience in the emergency room are in general agreement about the essential components of the neurological examination (NE) used on unconscious patients in whom an obvious cause for coma is lacking. Methods We surveyed 31 board‐certified practicing neurologists who regularly examine unconscious patients in the emergency room and asked them to list the specific components of the NE that they would normally choose to apply in at least 80% of cases. Results Twenty‐seven neurologists rated 24 of 38 items as essential steps of the neurological examination of the unconscious patient, with a high level of agreement amongst survey participants. Conclusions There was a high degree of consensus amongst the neurologists surveyed about which steps are essential for the NE of the unconscious patient. These findings provide an important source of validation for teaching this particular NE to medical students, as well as nonneurologists working in an emergency setting.

patient as a complex procedure that includes a multitude of elaborate features. It should be noted, however, that these appraisals are based on the opinions of just a few experts, mostly tracing back to the approaches described either by Plum and Posner, which was first published in 1966 (Plum & Posner, 1966), or C. M. Fisher's work (Fisher, 1969) published in 1969.
The most commonly applied approach to the NE aims to differentiate between focal asymmetric clinical deficits, primarily located in the motor system, and nonfocal symmetric findings; this can then help determine the underlying cause of the symptoms as being a localized structural brain lesion/functional disturbance (e.g., ischemic or epileptic) vs. nonstructural events (e.g., toxicmetabolic), respectively (Stevens & Bhardwaj, 2006;Stevens et al., 2015). However, severe neurological diseases such as meningitis, subarachnoid hemorrhage, or basilar artery occlusion (including top of the basilar syndrome) often present with coma, either without focal asymmetric deficits, or with bilateral symmetric deficits (Caplan, 1980;Mattle, Arnold, Lindsberg, Schonewille, & Schroth, 2011;Schwarz, Egelhof, Schwab, & Hacke, 1997). Furthermore, they are often difficult to detect in native cerebral CT scans. As late recognition of these conditions is associated with a high mortality rate, the identification of clinical signs that can facilitate early clinical diagnosis and the implementation of additional diagnostic steps are essential for optimizing treatment and should ideally be completed within a few minutes.
In the emergency room (ER) of most secondary and tertiary German hospitals, either the consulting neurologist or neurologists as permanent members of the ER team routinely take over the NE of unconscious patients. Strikingly, despite the time pressure associated with such an emergency situation, there are no validated step-by-step protocols available for a purposeful and short but sufficient NE of a comatose patient in the ER. Such protocols are potentially even more important for physicians without a background in neurology, in cases where no neurologist is available. Indeed, without daily practice in this particular examination, some nonneurologists may feel uncertain about which examination steps to choose. As a result, they often rely on common coma scales such as the Glasgow Coma Scale (GCS) (Teasdale & Jennett, 1974) or more recently devised elaborate scoring methods such as the "Full Outline of UnResponsiveness Score" (FOUR Score) (Wijdicks, Bamlet, Maramattom, Manno, & McClelland, 2005). For teaching proposes, the "Guidelines for the Neurologic Examination in Patients with Altered Level of Consciousness" by the Neurology Clerkship Core However, external validation of these guidelines is lacking.
No studies to date have attempted to identify and validate the particular components of the NE that are actually applied by neurologists experienced in examining unconscious patients who present to the ER without an obvious cause for their condition.
The aim of this study was therefore to establish whether there is consensus among experienced ER neurologists about the essential elements of the NE in the unconscious patient, and how this consensus compares to the GCS, FOUR score, and published AAN Guidelines for medical students.

| ME THODS
An analysis of eight widely used neurology textbooks (Bender et al., 2012;Biller et al., 2011;Delank & Gehlen, 2015;Fuller, 2013;Hacke, 2016;Mattle & Mumenthaler, 2015;Posner et al., 2007;Urban, 2012), as well as two emergency textbooks, (Marx et al., 2013;Tintinalli et al., 2010) collectively revealed 38 different steps for the NE of the unconscious patient. We asked 31 practicing board-certified neurologists with >2 years of experience in the examination of unconscious patients (23 neurologists from the Department of Neurology and Neuroscience, Medical Center, University of Freiburg, Germany; eight neurologists from other German clinics with an ED) to list which of these 38 steps they would use (prior to cerebral imaging) to examine an ER patient with acute unconsciousness that is not due to a known cause such as cardiac arrest or TBI. Participants were asked to use a four-point scale to assess the level of importance of each step (adapted from [19]): 4 = should always be included; 3 = included at least 80% of the time; 2 = sometimes included, but <80%; 1 = almost never included. In accordance with reference (Moore & Chalk, 2009), ratings with an average >3 were ranked as "essential." This process was facilitated by the Webbased questionnaire system (www.umfrageonline.com).

and (c) "Guidelines for the Neurologic Examination in Patients with
Altered Level of Consciousness" by the Neurology Clerkship Core Curriculum of the American Academy of Neurology (Gelb et al., 2002).
The study was approved by the local Ethics Committee (EK-Freiburg No. 10003/18).

| RE SULTS
Twenty-seven of 31 neurologists completed the survey. The results (mean ± standard deviation, SD) of the survey are shown for all 38 steps in Table 1. A total of 24 steps had a mean rating of 3.0 or higher. Notably, more examination steps were rated by the survey as essential when compared to the GCS and the FOUR score (Table 1). In contrast, almost all the recommended steps included in the "Guidelines for the Neurologic Examination in Patients with Altered Level of Consciousness" were rated by our experienced neurologists as essential steps of the NE; the exception here was caloric testing, which is sometimes used in intensive care units but is

| D ISCUSS I ON
The experienced neurologists who completed our survey identified 24 essential steps for the NE of the acutely-unconscious patient.
Five of these steps pertain to the inspection of the patient (Steps Despite being recommended in reviews about the approach to the comatose patient (e.g., Stevens & Bhardwaj, 2006;Stevens, Cadena, & Pineda, 2015), fundoscopy was rated lowest by our neurologists.
Reasons are speculative only: As fundoscopy may be a useful examination step in the approach to the awake patient with acute headache in the ED to stratify further diagnostic steps (Sachdeva et al., 2018), It is interesting to note that experienced neurologists apply considerably more examination steps in comparison with the "Glasgow TA B L E 1 (Continued) Coma Scale" (GCS) (Teasdale & Jennett, 1974), or the "Full Outline of UnResponsiveness Score" (FOUR Score) (Wijdicks et al., 2005), which are often used by emergency physicians. However, both these coma scoring methods were designed to predict the outcome of comatose patients rather than to help diagnose the underlying condition of the coma. Although it is not clear whether the extra steps rated by our experienced neurologists further benefit the diagnostic process -and hence improve patient outcome -the results of this survey may serve as a useful basis for future studies comparing the use of short scales by emergency physicians to the essential neurological examination recommended (and performed) by neurologists.
In contrast, the "Guidelines for the Neurologic Examination in Patients with Altered Level of Consciousness" by the Neurology Clerkship Core Curriculum of the American Academy of Neurology (Gelb et al., 2002) matched noticeably well with the practical approach of our experienced neurologists: Almost all the recommended steps in the guidelines were included in the items rated as essential in our survey. As the voting process for these guidelines is  (Moore & Chalk, 2009). All of these limitations could be overcome by repeating this study at other clinical locations, as conducted for the "essential neurological examination" (Lima & Maranhão-Filho, 2012;Moore & Chalk, 2009). Another limitation relates to the method of selecting the steps from a given list, which might result in a higher number of essential steps compared to actively listing the steps used. Moreover, depending on the individual scenario, adjustments to the number of applied steps might also occur.
In summary, we present the first data on the essential components of the NE in the unconscious patient, as generated by neurologists with long-term experience in the ER. These results could serve to validate the particular components of the NE of unconscious patients that expert neurologists consider important and may help to focus on teaching the most important examination steps to medical students and non-neurologists working in emergency departments.

ACK N OWLED G M ENT
The authors have no acknowledgments to declare.

CO N FLI C T O F I NTE R E S T
None of the authors declare conflict of interests.