On the mechanism of brain injuries. By Alexander Miles, MD, FRCS. Edin. Syme Surgical Fellow (From the Laboratory of the Royal College of Physicians, Edinburgh) Brain 1892: 15; 153–189; Experimental cerebral concussion. By D. Denny Brown and W. Ritchie Russell (From the Laboratory of Physiology, Oxford) Brain 1941: 64; 93–164
Cambridge
That a bang on the head may prove fatal has been known since Biblical times. Despite the celebrated description by Alexis Littré in 1705 of a condemned criminal who anticipated his executioner by head-banging until dead but without breaking his skull, the nature of fracture-less head injury is not so clear. Although many doubt that this can happen, no less an authority than Mr Jonathan Hutchinson has argued that violence of the shake may itself lead to death. Do uncontrolled brain vibrations follow rapid alteration in shape of the skull (as proposed by Professor Miller of Edinburgh)? Perhaps not, since the brain has some freedom of manoeuvre in the cranium: it is a hollow structure, requiring I atmosphere pressure to cause compression by 1/25 000th of its volume; and the meninges or tentorium must tear in the face of such distortions. Is it due to diffuse petechial haemorrhage and cerebral contusions? Could the explanation lie in focal brain lesions caused by squeezing the intracranial vessels or congesting their venous drainage? Is it all due to reflex changes in brain perfusion dependent on cardiac output and peripheral nerve stimulation? Or is it merely a ‘fons et origo mali’? To answer these questions, Dr Miles has experimented on anaesthetized rabbits, struck variously on the head with a force insufficient to cause death, and observed the effects.
He notices profound irregularities and slowing of the heart beat, and a reduced respiratory rate. The altered reactivity of blood vessels and poor oxygenation, identical to ‘anaemia of the brain’ observed following ligation of the main extracerebral vessels, depend on efferent discharges in the restiform bodies. Studying anaesthetized experimental animals and pigs with swine fever being slaughtered, Dr Miles concludes that this reflex vasospasm leads to tetanus followed by paralysis and cardio-respiratory collapse. Next, the Syme Surgical Fellow considers the role of cerebrospinal fluid—normally a cushion that buffers otherwise abrupt movements of the brain within the cranium. The forcibly struck skull bends and absorbs part of any blow, and it has been argued that such denting is associated with an equal and opposite bulging that may even result in fracture remote from the site of injury without the abruptly displaced head having struck some other object in its path. This bulge is immediately filled with displaced cerebrospinal fluid but since the cranium distorts faster than the brain inside, a vacuum is created opposite the site of injury and local blood vessels may rupture as Henri Duret (1878) has shown. An obvious impression can be observed on a dollop of glazier's putty filling the head at the point contre-coup to the blow when the skull is struck by a wooden mallet. Although partially protecting brain substance otherwise threatened by denting and bulging of the skull, uncompensated changes in cerebrospinal fluid dynamics close to and opposite the point of impact send a shock wave through the ventricular system that also ruptures tissues at sites of natural narrowing—the aqueduct and floor of the 4th ventricle.
With rapid aspiration of cerebrospinal fluid, the negative pressure so created does indeed cause intraventricular haemorrhage. More gentle removal of cerebrospinal fluid followed by a blow to the front of the head allows, from the brain perspective, the animal to ‘escape serious harm’, even though the skull base may be fractured. Conversely, a head-injured rabbit with intact cerebrospinal fluid does show extensive peri-ventricular damage and contre-coup bleeding but no fracture. These observations support the shock wave hypothesis, to which Dr Miles adds details of another experiment designed to show that cerebrospinal fluid pressure waves also cause haemorrhage along the sleeves of cranial nerves. By opening the nerve sheath of one optic nerve, allowing fluid to escape at the moment of injury, no haemorrhage occurs, whereas extensive bleeding occurs in association with the shock-wave of cerebrospinal fluid on the intact side. So what has he learned? Concussion is due to ‘anaemia of the brain’ resulting from reflex vascular reactivity depending on stimulation of the restiform body. In turn, this is stimulated by the cerebrospinal fluid shock wave, its impulse and withdrawal tearing blood vessels and causing parenchymal damage due to the resulting haemorrhage.
Fifty-one years later Derek Denny Brown and (William) Ritchie Russell return to the ‘interest in states of coma, stupor and confusion following injury to the head . represented by the word "concussion" ’. Starting their historical account with Alexis Littré, they also consider that there is work still to be done in seeking to explain ‘death due to shock of the violence rather than to lesions’. They adopt a strict definition of concussion, and once more inflict experimental injuries on anaesthetized cats, dogs and monkeys. Physiological measurements of respiratory and cardiovascular functions and intracranial pressure are recorded, and manipulations to organs and peripheral nerves made in order to control these functions and responses (Fig. 1). Head injury is inflicted using a 400 g weight attached to a pendulum that—depending on the animal in question—achieves a striking velocity of 28.4 ft/s transmitting 17.83 foot lbs; excursion of the struck head is limited to 4 cm. The ‘ideal’ concussive blow is one that arrests respiration, following an inspiratory gasp, for around 10 s. This also results in an abrupt rise of arterial blood pressure and bradycardia. It causes a start reflex beginning with an extensor jerk as the blow falls, then flexor spasms of the limbs, primitive running or galloping movements, and subsequent loss of muscle tone or, with less severe injuries, decerebrate posturing: ‘following the start reflex postural tone is abolished . the motor centres in the pons suffer reflex paralysis and gradually recover . strong vagal stimulation . can evoke a passing muscular spasm .’. The pinna, swallowing and corneal reflexes are abolished for 1–2 min, and there are overactive twitchings of the vibrissae and other facial muscles. Through collaboration with Dr (Solly, later Lord) Zuckerman the same features have been observed in animals concussed whilst fully conscious.
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Neither the force nor energy transmitted are key factors. Rather, it is acceleration or deceleration that matter. Concussion depends on a change from 0 to 28 ft/s occurring in minimal time and equivalent to a rate of change of velocity of 48 000 feet per second. This results in a flinging movement of the brain within the skull, to which the brain stem is especially vulnerable. Concussion does not occur if the head does not move when struck, although the direct injuries—skull fracture and penetrating wounds—may nevertheless be terrible. Now, Denny Brown and Ritchie Russell apply the rigours of experimental physiology to characterize the mechanisms of concussion. Cardiovascular elements are critical. By manipulating each component, and comparing intermediate blows that recover with those proving fatal, they show that the initial abrupt rise in blood pressure depends on medullary stimulation and vago-glossopharyngeal reflexes. Brain perfusion increases since there is no associated intracranial vascular spasm. Conversely, there is concomitant peripheral vasoconstriction. These can be considered responses to shock. Indeed, it is the integrity of this vasomotor-vagal reflex circuit, first described by Friedrich Goltz in 1863, that determines survival. Reflex hypertension protects from the collapse of blood pressure accompanying injuries eventually proving fatal or those resulting from repeated concussive blows. These vasomotor responses are not the result of increased intracranial pressure—for none is measurable—and the classical relationship between intracranial and systemic blood pressure, described by Harvey Cushing in 1901, is only seen when the former rises slowly. Increased intracranial pressure only causes concussion if it also inflicts velocity-related changes on the brain. Whilst there are some differences of detail between ‘acceleration/deceleration’ and ‘compression’ concussion, in both—by comparison with the brief stunning that a boxer may enjoy at the hands of his assailant, the ‘knock-out blow’—concussion is ‘an immediate traumatic paralysis of reflex function, which occurs in the absence of visible lesions in the nervous system . and in association with the hypertensive cardiovascular vagal reflex that protects from acute traumatic shock’ (Fig. 2).
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For Denny Brown and Ritchie Russell, morphological lesions resulting in contre-coup damage and petechial haemorrhage (described by Richard Bright in 1831)—usually in the brainstem, medulla and upper cervical cord—are changes that go beyond, but not infrequently accompany, mere concussion. It takes a very hefty blow to cause brain contusions. Because these vascular effects of injury occur at sites remote from those implicated in the genesis of concussion, and follow a much slower time course, they can be considered merely as coincidental complications of the violent movements experienced by the brain and not causative. By softening the blow, depressed skull fracture may, paradoxically, protect from concussion even though contusion and fracture each may be associated with fatal damage to the cervico-medullary junction. Contre-coup petechial haemorrhages and remote contusions arising from suction that separates the cortex and the pia mater are probable explanations for death from blows to a head, held stationary through being fixed against a hard object and not experiencing the brief but high-velocity acceleration–deceleration forces.
Taken together, Denny Brown and Ritchie Russell consider concussion to be a ‘molecular reaction’ of neurons to physical stress applied at a critical speed. It is the subsequent rate of change in velocity not the absolute excursion that creates the sequence of ‘excitation, excitation with reflex paralysis, excitation followed by complete paralysis and complete paralysis alone’—most obviously affecting respiratory rhythms but also seen with other brain functions. Vestibular dysfunction, respiratory failure, forebrain injury, fat embolism, toxic factors, raised intracranial pressure and vascular mechanisms are not relevant. Everything depends on movement and inertia arising from the lag between excursions of the skull and the brain within. Although the physiological sequelae are transient, in man stupor followed by intellectual impairment may be prolonged. Self evidently, everything changes with the use of a helmet (and protection from hair and the scalp) that cushions the head, absorbs energy and—more importantly—offsets accelerated head and brain movement. Experimentally, Dr Zuckerman has shown that a makeshift crash-helmet made from a disused tobacco tin partially protects monkeys from concussion. Therefore it makes sense to encase the at-risk head in a helmet that is close fitting but yielding and protects the neck from violent movements; or the boxing glove to be padded so as to slow the critical period of altered brain velocity. For the avoidance of concussion, a restricted point of impact is preferable to a diffuse blow—exchanging depressed fracture that absorbs energy for commotio cerebri: ‘we recently observed an airman, a large slice of whose skull was sliced off by a fast-moving aircraft propeller . the injury did not even cause a momentary impairment of consciousness . acting simply as a knife without imparting acceleration to the head’.
Thus compression, contusion and concussion each may complicate closed head injury, alone or in combination. Denny Brown and Ritchie Russell refer only to the work of Alexander Miles in connection with his views on nerve sheath haemorrhages. Each set of authors describes in detail, and with remarkable agreement, the brainstem-mediated reflexes that accompany concussion. It is their interpretation of the mechanisms that differ—Miles favouring the pulse pressure of cerebrospinal fluid as the insulting force, and the Oxonian physiologists preferring molecular reactions of neurones. As papers in the present issue remind us, the circumstances leading to concussive head injury and the physiological effects are short and sharp; but the consequences of such injuries may blight the lives of affected individuals for a very long time.
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