The Neurological Exam of a Comatose Patient: An Essential Practical Guide

A thorough examination of a comatose patient is essential given the spectrum of clinical diagnoses. The most immediate threat to patients is airway, breathing and circulation. All attending physician should employ a structured and focused approach in dealing with a comatose patient. It is important to recognise the urgent steps needed at the time to prevent further deterioration, followed by the final diagnosis of patient’s neurologic status. Here we provide the essential practical guide to the neurological exam of a comatose patient that would assist to determine the aetiology, location and nature of the neurological lesion.


Introduction
The evaluations of the comatose patients require a stepwise approach starting with a history, physical examination and laboratory evaluation. The causes of coma may be reversible when detected early. It therefore seems pertinent that once we confirmed an unobstructed airway, that the patient is breathing, and that there is normal circulatory function, a structured and focused examination must be undertaken (1). The examiner should determine where is the lesion responsible for coma, the nature and what is the urgent steps that are needed at the time to prevent further neurological damage. In the neurological exam of a comatose patient, the outline includes: i) general examination; ii) level of consciousness; iii) cranial nerves; and iv) motor assessment.

General Examination
The examiner must have a systematic and thorough examination. The general examination starts with observing the stationary position of the patient on the bed and attitude of the limb. It should be documented if there is any spontaneous motor behaviour or semi-purposive movements of all four extremities, breathing pattern and oropharyngeal reflexes such as coughing, swallowing, hiccupping or yawning. Inspection for clues for trauma such as bleeding, scars, track marks and post-operative drainage catheters may indicate the site of injury. In intensive care environment, all connected intravenous infusion is checked for sedative agents and or vasopressors. This is important if there is a question as to whether a drug or intervention has an effect to patient's conscious level. When the patient is on a mechanical ventilator, the settings give a clue if any spontaneous breaths are taken by the patient.

Level of Consciousness
The current recommendation by the European Academy of Neurology (EAN) (2) is that the Full Outline of UnResponsiveness (FOUR) score (Table 1) (3) is to be used for a comatose patient in intensive care unit (ICU) setting, instead of the Glasgow coma scale (GCS) score (Table 2) (4). The examiner must document what the patient did in response to particular stimuli. The stimuli are either peripheral or central.

Peripheral Painful Stimuli (as described by Teasdale and Jennett (4))
This technique is used to elicit an eyeopening response.
Interphalangeal joint pressure (IJP) i) Apply pressure with a pencil or pen to the lateral outer aspect of the proximal or distal interphalangeal joint for 10 s-15 s to elicit a response.
ii) A peripheral painful stimulus may elicit a spinal reflex, causing flexion of the tested limb; a spinal reflex is not an indication of intact brain function.

Central Painful Stimuli (as described by Teasdale and Jennett (4))
This technique is used to elicit a motor response. It is done by stimulating a cranial nerve, thus avoiding the possibility of eliciting a spinal reflex. iii) The pressure is applied for a maximum of 30 s and caution should be taken in patients with previous cardiac surgery or signs of injury to the sternum

Meningismus
In neurological condition that causes irritation to meninges, such as meningitis and subarachnoid haemorrhage, bedside diagnostic signs can be used for evaluation. The presence of meningeal irritation, however, is not pathognomonic for meningitis (6). The signs that can be elicited include: Neck stiffness/nuchal rigidity (7) i) With the patient lying on his or her back and both legs fully extended at the knee, an attempt is made to flex the patient's neck towards the chest ii) Due to spasm of the extensor muscles of the neck, there will be resistance to passive flexion of the head (stiffness) iii) The inability to either touch the chin to the chest or lift the head 8 cm off the bed when supine is used for definition iv) The lateral neck movements are preserved (versus neck rigidity from musculoskeletal pain) Kernig's sign (8)(9)(10)(11) i) With the patient lying on his or her back and both legs fully extended at the knee, a two-stage attempts is performed with flexing of lower limb simultaneously at the hip and knee, then extending the knee ii) Positive test is when there is resistance to the test and or involuntary flexion of the opposite hip Brudzinski's sign (8,12) i) With the patient lying on his or her back and both legs fully extended at the knee, keep one hand behind the patient's head and the other on the chest in order to prevent the patient from rising ii) An attempt is made to flex the patient's neck towards the chest; a positive test is when the patient involuntarily flexes his or her hips and knees in an attempt to minimise the meningeal irritation Blink-to-threat (14) i) The test is done by passively opening the eyes of the patient, then move your fingers rapidly towards the patient's eyes to see if a blink occurs ii) This test is done in all four direction

Position
Upon lifting the patient's eyelids, the examiner should notice the shape and position of the pupils, whether it is central, deviated or dysconjugate gaze. Examples of findings include:

i)
A frontal lobe lesion, commonly a stroke: the eyes deviation is on the same side of the lesion ii) Todd's paralysis following a seizure: the eyes deviate in the opposite direction iii) A pontine lesion or thalamic haemorrhage: the eyes deviate in the opposite direction

Pupillary response
Pupillary light reflex (PLR) is simply the change in pupil size that occurs after a light stimulus. It provides information on the brainstem integrity in the comatose patients (15). A transient flash of light within 3 s-5 s will produce a decrease in pupil size. PLR is generated by smooth muscle and is unaffected by neuromuscular blocking drugs. However, the examiner has to ensure whether the patient is on sedative agent and the level of sedation, since the sympathetic contribution to pupil size may be absent due to anaesthetic-induced miosis (15,16). It is also useful to check whether the patient is on any pupil dilator medication or has an underlying optic nerve injury, such as traumatic optic neuropathy.
It has previously been recommended to use the NeurOptics portable pupillometer for bedside assessment. The device measures the Neurological Pupil index (NPi) to determine each pupil assessment (15); the NPi is scored from 0 (nonreactive) to 5 (brisk) with values < 3 considered to be sluggish or abnormal. The Lasègue's sign (as published by Wartenberg (9), and Maranhão-Filho and Vincent (13)) i) With the patient lying on his or her back and both legs fully extended at the knee, the examiner passively flexes each leg at the hip while keeping the knee joint extended ii) Normally the straight leg can be lifted to an angle (with horizontal) of 65°-90° position iii) Positive test is when the angle is reduced as well as pain and limitation of movements present earlier The sign of meningism may present bilaterally in patients with meningeal irritation and unilaterally in patients with unilateral sciatica. Whenever Kernig's sign is positive, Lasègue's sign is generally also found to be positive and vice versa.

Vision (Cranial Nerve II)
Assessment of vision includes voluntary eye movements, visual pursuit and blink-to-threat techniques.
Voluntary eye movements (2) i) The test is done by passively opening the eyes of the patient without stimulation to trigger the eye opening ii) Then, look for spontaneous eye movement, or eye movement on command. If there was no response, then proceed for visual pursuit Visual pursuit (2) i) The test is done using a bedside tool such as a mirror. Put the mirror in front of the patient's face to evoke a response and moves it horizontally and vertically  (17) The steps are as follows: i) While standing at the head of the patient's bed, elevates both lids and releases them simultaneously ii) The lid of the hemiplegic side closes slowly because of the flaccidity of its orbicularis oculi muscle, whereas the lid of the normal side closes briskly because of tonus in its orbicularis oculi muscle Oculocephalic Manoeuvre (Doll's Eye Test) (18,19) The steps are as follows: i) Ensure the C-spine is cleared ii) The patient's eyes are held open iii) The head is briskly turned from side to side with the head held briefly at the end of each turn iv) The degree of rotation must be more than The steps are as follows: i) Stimulus is applied from the side while the patient is looking in the opposite direction ii) Gently touching or stroking the cornea with a wisp of moistened cotton iii) Positive results will elicit bilateral blinking of eyes iv) Also observe for contralateral deviation of jaw (corneomandibular reflex) (21): tend to occur with firm stimulation of cornea iii) The afferent arc of the gag reflex is primarily innervated by the glossopharyngeal nerve; the efferent arc is innervated by the vagus nerve

Motor Assessment
The neurological assessment may be limited particularly when the patient is unable to follow steps command or respond to sensory examination (17,23,24). However, the examiner can still be able to perform certain manoeuvres and elicits signs. The motor assessment is divided into:

Motor Tone
The grading can be done using the 1964 Ashworth scale (25)

Motor Responses
For movements with elimination of gravity, the head end of the bed is placed in 10° position. The arm and legs are put in a neutral position and are observed for weakness. The flaccid arm will be in extension with semiflexed fingers, while the leg will be in extension and externally rotated. Each muscle strength is tested and graded using the Medical Research Council (MRC) grading (27). Some examinations require a conscious patient, such as Holmes tremor (28) and Mingazzinni test (29,30). Hence, in this scenario, we will show several tests that can be done to test muscle weakness.

Arm dropping test (Reeve and Bullen test) (31) i)
With patient lying supine, put patient's arm over the head and drops the weak arm ii) The hemiplegic arm drops limply, whereas the normal arm glides or floats down iii) This is also useful to test for psychogenic neurologic deficits, whereby in organic paresis the arm hits the face. However, in functional paresis a voluntary movement allows avoiding the face   Jaw jerk (first described by Morris J Lewis (38), and reiterated by Lanska (39) ii) The response is a brisk, partial, upward jerk of the mandible caused by contraction of the temporalis, masseter and medial pterygoid muscles (40)

Upper limbs
Biceps reflex (41,42) i) Place a slight tension on the patient's biceps tendon and strike with the reflex hammer.
Brachioradialis reflex (41,42) i) Cradle the patient's forearm in one hand ii) Tap just above the styloid process of the radius with the forearm in semiflexion and semipronation Triceps reflex (41,42) i) The patient's wrist has to be across the chest with the elbow about 90° flexion ii) Tap the triceps brachial tendon directly above the olecranon process Finger flexor reflex (Wartenberg sign) (42,43) i) The patient's hand is in supination, resting on a solid surface, with the fingers slightly flexed i) The ability of the patient to maintain a fixed posture of a lower limb for a few (3-5) seconds is regarded as power 3/5.
ii) E.g. the patient's thigh is flexed with knee flexed at 90° and observe the ability of the patient to maintain the position.

Barré test (manoeuvre de la jambe)
i) Known as 'leg drift test' (30,35). In a prone position, the patient's legs are bent at 90° angle from the bed. The extremity on the paretic side will lower earlier.
ii) This is also useful to test for psychogenic neurologic deficits, whereby in organic paresis, the leg falls but contraction of hamstring muscle is seen. However, in functional paresis, leg falls without contraction of the hamstrings or no fall at all.

Motor Reflexes
Reflexes are divided into deep tendon reflex (DTR), clonus, cutaneous reflex and frontal lobe release phenomena.

DTR
The standardise measurement of DTR is based on the National Institute of Neurological Disorders and Stroke (NINDS) (36, 37) ( Table 4). The assessments include jaw jerk, upper limbs and lower limbs. The examiner places his or her fingers against the patient's fingers, and taps the back of the examiner's own fingers lightly Hoffman sign (23,44) i) The patient's hand is held with the wrist dorsiflexed and fingers dorsiflexed ii) With another hand, the examiner holds the partially extended middle finger of the patient between his or her index finger and thumb. Then, snaps the nail of patient's middle finger

iii)
Observe for flexion of all fingers, including the thumb in a pathological response Trömner sign (23,45) i i) The examiner holds the patient's hand in supination with the fingers fully extended.
Then with the other hand, the examiner moves a sharp object over the palm from the wrist across the hypothenar eminence in a direction below the fingers and above the metacarpal heads ii) Observe for adduction and opposition of an extended thumb in a pathological response Lower limbs (first described by Erb (47) and Westphal (48)) Patellar (quadriceps, knee jerk) reflex (reiterated by Gower (49, 50)) i) If the patient is supine, this reflex is easier to elicit with the patient's knee in slight flexion. A knee jerk can be enhanced by slipping the examiner's hand under the patient's knee and resting it on the patient's opposite thigh ii) The examiner then strikes the patella tendon just below the patella of the patient's relaxed leg iii) Observe for contraction of the quadriceps femoris muscle

Achilles (ankle jerk) reflex
i) The patient is either in a supine or seated position, the thigh should be held in moderate abduction and at external rotation, and the knee is flexed ii) Strike the Achilles tendon just above its insertion on the calcaneus Clonus (first described by Erb (47) and Westphal (48)) Clonus is series of rhythmic involuntary muscular contractions induced by the sudden passive stretching of a muscle or tendon (23). The most commonly elicited are at the ankle, patellar and wrist. Cutaneous reflex (first described by Rosenbach (52), and reiterated by Wartenberg (42,53)) Cutaneous reflexes response to stimulation of either the skin or mucous membrane. This is a polysynaptic reflex that is performed by a superficial skin stimulus, causing pulling of the umbilicus to the stimulated quadrant. The response is slower and is not consistently present. Dissociation of the abdominal reflexes, with the absence of superficial reflex and exaggerated deep reflexes may suggest a corticospinal tract lesion (23). Absent response may occur in previous abdominal operations, old age, obesity and those who have multiple pregnancies. The most often obtained are superficial abdominal reflex, cutaneous anal reflex and cremasteric reflex.

Superficial abdominal reflex
The stimulus is best directed toward the umbilicus. The response is a quick, flicking contraction of the abdominal muscles (rectus abdominis and external oblique) followed by immediate relaxation.

Cutaneous anal reflex (anal wink) (S2-S4)
The reflex will cause a contraction of the external sphincter in response to stroking the skin around the anus.
Cremasteric reflex (L1-L2) (discovered by Jastrowitz (54)) i) The reflex is elicited by gently stroking the skin on the superior and medial aspect of the thigh. This will stimulate the femoral nerve ii) The response consists of contraction of the cremasteric muscle with ipsilateral elevation of testicle toward the inguinal canal iii) Abnormal response may indicate a spine injury or L1-L2 or testicular torsion Frontal Lobe Release Phenomena (55) These phenomena are generally demonstrable in patients with diffuse dementing illness due to widespread nonlocalised bilateral hemispheric lesions, especially in the frontal lobes. Some causes include extensive infiltrating neoplasm, normal pressure hydrocephalus, closed head injury and toxic-metabolic encephalopathy. Certain test, such as Glabellar tap or Myerson's sign (56) is only performed on a conscious patient.

Snout (orbicularis oris) reflex
Briskly tapping the upper or lower lip with a finger or percussion hammer. A pursing response is obtained if abnormal.

Sucking reflex
Elicited by stroking the lip with a finger or a tongue blade. An abnormal response will show a lip pout, sucking, chewing, or swallowing movements.

Grasp reflex i)
This reflex is normally seen in infants up to 4 months of age, after which this reflex is inhibited by the frontal lobes ii) The technique is by stroking the palm of the patient's hand (between the thumb and index finger) with the examiner's fingers iii) Abnormal response is when the patient grasps the examiner's hand and is unable to release the grasp. If it is unilateral, it is indicative of involvement of the contralateral frontal lobe, especially in the premotor cortex; bilateral grasp reflexes indicate a more diffuse bifrontal disorder Palmomental reflex (57) i) Stimulation of the thenar eminence in a proximal to distal direction using a sharp object such as the pointed end of a reflex hammer, key, paper clip, or fingernail ii) Abnormal response will cause an involuntary contraction of the mentalis muscle of the chin, that is liken to a grimace Groping reflex i) A rhythmic, oscillating groping movements are seen after the withdrawal of the examiner's fingers from the patient's grasp

ii)
In a marked response, the examiner's hand was grasp tightly (forced grasping reflex) due to the inability to relax the muscle in response to contact

Plantar Response
In the normal individual, stimulation of the skin of the plantar surface of the foot is followed by plantar flexion of the toes. Where there is disease of corticospinal system, there may be dorsiflexion of the toes, with ± fanning of the lateral four toes. The best position is supine, with hips and knees in extension and heels resting on the bed. The response may be reinforced by rotating the patient's head to the opposite side (23); the result is interpreted as flexor plantar response, extensor plantar response or Babinski sign, or equivocal plantar response. Different methods can be used to elicit extensor plantar response, including Babinski (23,58,59), Bing (60), Chaddock (23,61), Oppenheim (62), Gordon (63,64), Gonda (65,66), Schaefer (67) and Marie-Foix retraction sign (68)(69)(70).
Another pathological response is called flexion spastic response. In normal individuals, there is a slight dorsiflexion of the toes or no movement at all. However, the pathological response in patients with pyramidal tract disorder causes a quick plantar flexion of the toes at the metatarsophalangeal joints with fanlike positioning (71). The interphalangeal joint is typically in extension. Different methods can be used including the Rossolimo sign (72,73), Žukovskij-Kornilov sign (as published by Kolář et al. (46)) and Mendel-Bechterew or dorsocubital sign (71,74) (Table 5). Move a blunt object over the lateral aspect of the foot, drawing from heel towards the small toe 4. Oppenheim (62) Press your knuckles down anteromedial surface of tibia from the infrapatellar region to the ankle 5. Gordon (63,64) Squeeze the calf muscles momentarily 6. Gonda (65,66) Pull the fourth toe outward and downward for a brief time and release suddenly 7. Schaefer (67) Squeeze hard on the Achilles tendon 8. Marie-Foix retraction (68)(69)(70) In patient with pyramidal lesion, pressure on the toes or vigorous plantar flexion at the ankle leads to flexion at the hip and knee and to attempt to dorsiflex the ankle (triple reflex) Maneuver to elicit flexion spastic response 9. Rossolimo (72,73) Using the tendon hammer, tap the ball of the foot or metatarsal head of the toes. Another way is by giving a quick, lifting snap to the tips of the toes 10. Žukovskij-Kornilov (as published by Kolář et al. (46)) Using the tendon hammer, tap at the center of the sole of the foot 11. Mendel-Bechterew or dorsocubital (71,74) Using the tendon hammer, tap the outer aspect of the dorsum of the foot in the region of the cuboid bone (os cuboideum) or over the fourth or fifth metatarsal

Conclusion
It is crucial to identify the focal neurological finding during the examination of a comatose patient. This can help narrow the involved structural lesion and to determine the urgent steps that are needed at the time, in order to prevent further deterioration. Here, we provide a video (https://youtu.be/2PbquY7XIFg) of the essential practical guide to the neurological exam of a comatose patient that would assist to determine the aetiology, location and nature of the neurological lesion.