Here is a wonderful historical description of apparently the first experimental attempts to model the physical forces inside the brain during a concussion impact. The fact that they were done with such simple devices, two hundred years ago, reveals a remarkable descriptive elegance of the elastic spread within these observations is still pertinent to-day.
Neurosurgery, Vol 50, no. 2, February 2002 by Moshe Feinsod M.D.
The Center for Applied Research in Head Injuries, Department of Neurosurgery, Rambam (Maimonides)Medical Center, Faculty of Medicine, The Technion-Israel Institute with of Technology, Haifa, Israel
Nearly 3 centuries ago, in 1705, the French surgeon Alexis Littré (1658–1726) (21) reported to the Royal Academy of Surgery the case of a criminal sentenced
to be broken on the wheel; to escape the torture, the man had killed himself by rushing across the dungeon, a distance of 15 feet, and striking his head against the wall. Examination of the head revealed no external mark of violence. When the skullcap was removed, Littré was astonished to find that the cranium was not fractured and the brain and its membranes seemed very sound. Despite serious criticism that the craniocervical junction was not examined, and death as a result of high cervical fracture-dislocation was not considered as a possibility (16), Littré’s report was quoted repeatedly. During the centuries to come, it was recognized by a large number of observers and students of head injuries as the stimulus for their investigations. They attempted to fathom how immediate
death could result from a blow to the head, without any visible brain injury, in an event that very few of them had observed. They further attempted to understand how a temporary cessation of nervous function might result from even minor or moderate head injuries, which is an occurrence that they all had witnessed. These deliberations of the 18th and early 19th centuries were based on a very few original clinical and postmortem observations and on case reports, many times retold, by celebrated observers of previous decades or centuries; they did not result in any evidence-basedconclusions.
Concomitantly, another concept was evolving. During autopsies, surgeons observed that hematomas, contusions, and lacerations of the brain occasionally could occur at sites remote from the point of impact. Some claimed that the cranium could even be fractured at areas remote from the primary injury. These cerebral and bony lesions were assembled under the general term contrecoup lesions, and they were considered an important phenomenon that was not yet understood.
During the 18th and 19th centuries, surgery was transformed from a mere craft into a discipline that attempted to incorporate the scientific method, based on experimental evidence, into the traditional concepts (1). The French Royal Academy of Surgery sponsored research and even set prizes for the elucidation of problems concerning head injuries (3). Contrecoup injuries were declared a subject of interest to the Academy, and a prize was set (April 10, 1766) for the establishment of a theory to explain and indicate their practical consequences in the treatment of head injuries. This theory was expected to help resolve the extensive debate on the indications for surgery in closed-head injuries. It should be appreciated that when the surgeon’s only localizing guides were external wounds and cranial fractures, the new contrecoup concept was a source of bewilderment unless properly understood. According to the British surgeon Sir B.C. Brodie (4), the endeavor continued in England and Germany also,
and some crude experiments were performed on various animals and human cadavers.
The recognition of contrecoup injury and concussion as physical events occurring in the brain and the concept of spread of forces within the cranium were beginning to be vaguely recognized. In a historical review, Verneuil (28) pointed out that Littré was referring to a movement (ébranlement) communicated to an organ by a blow or a thrust from a somewhat distant part. This concept was shared by J.L. Petit, the 18th century surgeon, as well as by J.M. Delpeche at the eve of the 19th century. Concerning concussion, Brodie (4) mused, “If we consider that the ultimate structure of the brain is on so minute a scale that our senses are incapable of detecting it, it is evident that there may be changes and alterations of structure which our senses are incapable of detecting also. The speedy subsiding of the symptoms of concussion does not contradict this opinion” (4, p 337). Verneuil (28) emphasized that, according to this line of reasoning, although concussion was a clinical phenomenon, it should be regarded henceforth as a physical event of a transmission of movement. The notion of impact-induced brain movement was generally accepted, but no research was conducted to elucidate the exact physical events happening within the cranial cavity during concussive injury, and it was regarded as a phenomenon beyond comprehension.
In an attempt to reveal these enigmatic brain movements and render the hypothesized minute structural alterations perceivable and explainable in physical terms, the French surgeon Jean-Pierre Gama sought a then-entirely-novel approach:in vitro physical modeling of the brain.
Jean-Pierre Gama had some battlefield experience but spent most of his career as a senior surgeon and professor of surgery in Val-de-Grâce military hospital in Paris. His main clinical interest was head injuries, and his book Treatise of Head Injuries and of Encephalitis in which Many Questions Concerning the Functions of the Nervous System are Discussed was first published in 1830. The additional editions published in 1835 and 1837 (13) and the frequent quotations
by later authors are evidence of its significance to clinicians and researchers
involved with head injuries during the 19th century as well as the beginning of the 20th century. The later editions served as the source for the present study.
J-P. GAMA’S DESCRIPTION OF HIS EXPERIMENT
The original description (13) is quite lengthy with many repetitions. An attempt was made to preserve its spirit, despite the use of some abbreviations.
The direct or indirect commotion that stir the brain and mold its movements follow always lines that are difficult to be predicted a priori. But an experiment
enabled us to unveil the precise direction, which they affect. For this purpose we prepared in a Matras [in old chemistry, a round-bottom glass flask having a long
neck] of white glass several strands of wire in different directions and filled it with a solution of ichthyocelle [isinglass] strong enough to have, after being cooled,
the consistency of the cerebral substance. We then corked the neck of the Matras and percussed this vase, with the hand or various objects, with a measured force.
The percussions of the circumference of the sphere demonstrate that the gelatinous mass is shaken on all the points in proportion to the force that was communicated to it; but it occurs from the various movements that the vibrations of the wires were dispersed in this transparent mass are logical. A slight percussion is always transmittable to the region correspondent location between the glass and the gelatin and the effect extends to some distance. One observes, by what occurs, that the shock is conveyed in the direction of the impulse, but that it decreases little by little until it is lost in the more distant points without being able to follow it. In stronger strikes the gelatinous mass is temporarily detached from the vase under the percussion and at the same time as a similar effect is observed at the opposite pointof the diameter; it tightens up to close instantaneously the gap we have just spoken about and that one may distinguish in the two sides of the vase; then it assumes again its primary position, without being able to ascertain then if this separation and retightening repeats itself in a weaker way. This kind of double impulse directs, consequently, the jolt into the center of the gelatin in two opposite directions: from there, according to the laws of repulsion, it is returned towards the circumference. The wires which had obeyed the two impulses, i.e., which had gone towards the inside from the two planes, vibrate then in opposite direction; they then have irregular movements, which still last some time, but the direction is not appreciable any more. One cannot distinguish the vibrations elicited by any percussion from the sphere, neither has the eye, nor has the hand, despite everything the attention that one brings there.
These experiments not only light the mechanism of the concussion, but also make it possible to give a plausible and a useful explanation of some of its effects. The uniform distribution in the brain of an indirect commotion, as in the case of percussion at the top of the head, can never cause the separation of the dura at an
opposite point. It is consequently more frequently free from complication and reduced to the strict meaning of the word [commotion].
But if the Matras is held reversed, i.e., its neck at bottom and the sphere on top, and if one strikes with the hand or with a padded object while holding fast the corked end as if for enforcing a cork, one observes the strands of wire to vibrate from inside outwards, which is the opposite of the first test; even more, in the higher part of the sphere opposed to the insertion of the collar there is no separation between the sphere and the jelly.
The movement is not marked more in this place than on all other points of the circumference; it appears to uniformly spread from the center to the periphery of the gelatinous substance, though the percussion is as strong as possible. The vibrations of wire indicate, nevertheless, that this movement is then returned from the circumference towards the center, but in a way far from significant, and it is necessary to take a very close look to recognize this type of oscillation. These effects clearly demonstrate that, in the indirect commotion, at least when it is made by the spinal column as an intermediary, represented here by the neck of the Matras, the movement is distributed from the inside to the outside of the brain.
These experiments not only light the mechanism of the concussion, but make it possible to give a plausible and a useful explanation of some of its effects. (13)
Gama’s description of his experiment was not illustrated graphically, the described vibratory movements of the wires within the jelly were not recorded, the materials of which the wires were made was not specified, and the percussive forces were not measured or calibrated. There is no information as to whether the flask was stabilized or whether it was handheld and thus unsteady. The cranium was regarded as a nonelastic structure, and its fractures were not taken into consideration because of the momentary separations that occurred between the gelatin and the sphere. Gama thought that these separations acted as protection for the brain from any local effect of the percussion. The cerebrospinal fluid and the ventricular system were not included in the model, and the acceleration and deceleration of the head that were soon to be recognized as a crucial component of head injuries, in the clinical setup, were not even considered. It took more than a century to make use of modern techniques such as rapid cinematography
(26) to demonstrate the rapid movements of the brain caused by a blow to the head. This method, as well as the use of strain gauges to measure the spread of forces, was not even dreamed of in 1830. Still, by conceiving and constructing an in vitro physical model of the brain, Gama was the first to use an entirely novel approach that was referenced in nearly all studies of head injuries that followed. On reading the sentence: “This kind of double impulse directs, consequently, the
jolt into the center of the gelatin in two opposite directions: from there, according to the laws of repulsion, it is returned towards the circumference,” we may regard Gama as having a creative mind to foresee the concepts and studies of strains and shearing forces occurring in the brain at the time of injury.
Gama was satisfied with the correspondence that, in his opinion, could have been derived from his model to known clinical observations. For example, blows delivered to the circumference of the cranium produced more pronounced concussive effects than when the vault was hit from above with approximately the same force. Separation of the brain from the cranium, as evidenced by intracranial “extravasations” (the term used then for hematomas), followed the same pattern.
The theory of oscillatory and vibratory movements of the brain produced by the percussive impact introduced an element not yet considered in the study of head injuries: the spread of forces into the depth of the brain and their impact on the function of the deep structures. At the eve of the 20th century, Kocher (20) demonstrated in an experiment performed by Ferrari that small glass threads buried in brain tissue could be fractured by the flinging movement of the
brain after a severe blow to the head, thus corroborating Gama’s concept of the spread of forces.
More than 30 years after the report in the first edition of his book, Gama’s findings and theory were critically challenged by Alexis Alquié (2), professor of surgery at the Faculty of Medicine in Montpellier. In a series of well-planned experiments, Alquié also used transparent glass containers that were filled by various fluids of different consistencies. In the gelatinous materials he embedded “strands of wire, filaments of tobacco, small fragments of wax, and bubbles of air, all examined with the favor of the sharp light and the magnifying glass which enlarged much even least displacements” (2). Alquié claimed that in every experimental setup, as long as the glass container was full of fluid, jelly as well as water, no oscillatory or vibratory movement could be perceived. The gelatinous mass moved, under the percussive impact, only once to the opposite point. In a further series of experiments performed on animals and human cadavers, he claimed to be able to reproduce the same movements. Alquié’s experiments were subject to all the shortcomings of the endeavors of his predecessor. They were conducted in the presence of many students, assistants, and university staff. The large number of witnesses seemed to have been arranged in an attempt to overcome the lack of any objective recording. Alquié continued his experiments on both cadavers and experimental animals.
Despite the different impressions of the two investigators, the concept of percussion-induced movement of the brain, either vibratory (as Gama visualized) or simple dislocation (according to Alquié), was largely accepted. David Ferrier (12), the great experimental neurologist, wrote in 1878, “It is commonly supposed that contrecoup occurs by actual concussionn of the cerebral mass against the skull” (12, p 102). Opinions differed as to whether the theory of Gama and Alquié, that the mere movement of the brain could cause concussion, should be acknowledged, as accepted by Hutchinson (18) Miller (24), and von Bergmann (29), or whether concussion, even in the momentary form, should be ascribed to structural changes such as petechiae caused by the transmission of forces, as stated by other 19th century authorities, such as Fano (9), Duret (8), Hewett (16), or Bryant (5).
Experimental investigations in animals and cadavers to clarify various aspects of concussive head injuries were conductedthroughout the 19th and 20th centuries. Some were briefly reviewed, several decades ago, by Denny-Brown and Russell (7). It is interesting to follow their development from
crude uncontrolled, noncalibrated, subjectively evaluated experiments that did not even consider the control of parameters such as respiration or blood pressure to the current elaborate setups. The impact of Gama’s concepts and experimental approach can be appreciated by their citation in nearly every major study of head injuries, whether purely clinical or experimental, beginning immediately after his time and continuing to the present.
For a long time, lack of the proper technologies precluded the development of the physical modeling approach. At the end of the 19th century, Chipault and Braquehaye (6) attempted to record the spread of forces in the cranium, but it
was only in 1941 that Goggio (14) tried to formulate his clinical observations into a series of mathematical equations to demonstrate the evolution of pressure gradients. Gama (13) may have sensed these momentary negative pressures in his
descriptions of “separations” of the isinglass from the percussed Matras but could not record the event. Two years later, A.H.S. Holbourn (17), an Oxford physicist, hypothesized in a series of articles that the theory of trauma should be regarded as a theory of elasticity, and he constructed in vitro physical models of gelatin and interfacing materials of different elastic properties to study the shear strains within the percussed brain. In 1948, Ward et al. (30) used a high-speed camera in percussed test tubes filled by fluids of various densities to record vibratory movements, the development of areas of negative pressure, and the formation of cavitations in the brain tissues corresponding to these areas. In 1958, Gross (15) investigated the effects of percussion of a model along various
axes in solutions representing the brain; with a high-speed camera, he was able to demonstrate the presence of a radial oscillatory mode, which Gama presumably observed. In addition, his experiment documented the formation of momentary cavitations as well as the vibratory movements of the percussed gelatin.
A brief review of the literature of the last decade reveals that physical modeling for the study of concussive head injury continues to be a suitable approach (22, 25). Combined with the mathematical tools of numerical finite element model and
numerical analysis (19, 23, 27) it enables recognition, isolation, characterization, and study of the various components of the biomechanics of concussive head injury, which continue to pose many unanswered questions after more than 2 centuries of research. Gama may be regarded as a researcher who, far ahead of
his technological time, recognized the importance of modeling as a means to study particular elements in a complex biological system. Once the proper technologies became available, his ideas were a constant stimulus for further research in the modeling of head injuries. His work represents an early example of the quest for collaboration among basic scientists, which can provide the tools to answer questions raised by clinicians.
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