HAEMORRHAGES FROM HEAD INJURIES

Hunterian Lecture delivered at the Royal College of Surgeons of England on 9th June 1955 by Milroy Paul, F.R.C.S. Professor of Surgery, University of Ceylon MY COUNTRYMEN HAVE been enrolled as members of this College for over seventy years now, and our long connection with the College greatly increases our appreciation of the privilege accorded me of delivering this Hunterian Lecture. INTRODUCTION My interest in head injuries dates from the time when, as a medical student, I read and re-read Wilfred Trotter's chapter on " The Scalp, Skull and Brain" in Choyce's System of Surgery (1923). The clarity of Trotter's descriptions and the brilliance of his conceptions of the genesis of head injuries made a deep impression on me. The haemorrhages of head injuries are easy to observe, and I became aware that there were some discrepancies between the features of these haemorrhages as I observed them, and as they are described in standard works on surgery. This stimulated me to observe these haemorrhages more closely, and to extend the observations which I could make in the wards and on the operating table, to the more complete examinations which are possible at autopsy. The many distinctive features characterising the haemorrhages from head injuries should have led to recognition of the factors controlling their onset and progress, but this expectation has not been realised, and there is still much that is not known in regard to the mechanics of these haemor- rhages. This study of the haemorrhages from head injuries is an inquiry into their origins, and of their modes of progress and of arrest. It is based on observations made of these haemorrhages in the course of a practice as a general surgeon over a period of 28 years. Questions which were deemed to be worthy of fuller inquiry, were investigated during the last four years by experimental work on the cadaver, and by detailed observa- tions of every case of head injury at the Colombo Hospitals to which I could get access during this period. THE SCALP HAEMORRHAGES The subcutaneous haematoma The subcutaneous haematoma is described in textbooks on surgery as the lesion which establishes that blood will not extravasate into the thick- ness of the scalp, but the significance of the lesion as an accurate mark of 69 MILROY PAUL the site of a violent impact on the head is not given the attention it ought to have. A violent impact on the head usually leaves no external mark, or causes a lacerated wound of the scalp at the site of the impact, but when it occasionally results in a subcutaneous haematoma, the lesion is likely to be missed if it is not looked for in a good light after the scalp has been shaved. The small circle of slightly raised, plum coloured skin is only seen in these conditions. The shape of the lesion proves that it was caused by violent compression of the scalp between the skull and the surface of impact, and the circular lesion is the result of extravasation of blood into the area of imprisoned scalp after its release from compression. Blood cannot extravasate beyond this area into the uninjured thickness of the scalp bordering the lesion. The lesion is consequently an accurate mark of the site of an impact, and its detection is particularly valuable in cases of extra dural haemorrhage where the clot is always below the site of the impact. It is also of some service for assessing the sites of contre coup injuries, and it may be important in medico-legal investigations.

Sub-epicranial haemorrhage A sub-epicranial haemorrhage is described as a pool of blood on which the scalp floats. When fully developed it extends from the superior curved line on the occipital bone over the whole of the vault down into the interstitial tissues of the upper eyelids in front. This is the description given in every textbook on surgery (Rose and Carless (1952), Romanis and Mitchiner (1952)), although it relates to a lesion so rarely encountered in this form, that there would be many surgeons like myself, who have yet to see a fully developed case of this kind. The sub-epicranial haemorrhage is, however, a very common lesion in cases of head injury, but it differs markedly in characteristics from the haemorrhage as it is described in textbooks. In cases coming to autopsy I have found a sub-epicranial haemorrhage in everycase in which there were gross intracranial lesions. This sub-epicranial haemorrhage of every- day experience has not been described by writers on head injuries (Rose and Carless (1952), Romanis and Mitchiner (1952)), and the surgical and medico-legal implications of this haemorrhage have consequently not been appreciated. The lesion is to be observed in almost every severe head injury case. When the scalp is reflected off the skull at an autopsy, the sub-epicranial haemorrhage is displayed as two extensive sheets of extravasated blood, one coating the inner surface of the epicranial layer of the scalp, and the other coating the outer surface of the pericranium. There is no pool of liquid blood. Replacement of the scalp on the skull will demonstrate that the two coats of extravasated blood cover identical areas, and that they have been created by bisection of a single sheet of blood extravasated 70 HAEMORRHAGES FROM HEAD INJURIES in the sub-epicranial space. In any individual case there is in essence only one sheet of blood, and in cases in which the site of impact is marked by a lacerated scalp wound or by a subcutaneous haematoma, this mark will be at the centre of the sub-epicranial sheet of blood. The sub-epicranial sheet of blood gives no external evidence of its presence, and it is not seen till the scalp has been reflected off the skull. It gives evidence not only of a violent impact, but also of the site of the impact. The epicranial aponeurosis is connected by very numerous strands of connective tissue uniting it with the pericranium over the vault of the skull and with the temporal fascia on the sides of the skull. Extravasation of blood into the sub-epicranial space would be resisted by this forest of close set, short, connective tissue bands, and the collection of a pool of blood in the sub-epicranial space would not be possible if these bands were unbroken. The only blood vessels traversing the sub-epicranial space are a few emissary veins, and the invariable centering of the sub-epicranial sheet of blood on the site of impact, and not on the sites of these emissary veins, is evidence that the blood had extravasated from other sources. The blood vessels of the scalp lie in immediate contact with the epicranial aponeurosis, and violent bruising of the scalp at the point of impact can cause oozing of blood through the epicranial aponeurosis into the sub- epicranial space, although it cannot cause extravasation of blood into the thickness of the scalp, and blood from this source can then spread widely in the looser tissue spaces of the sub-aponeurotic space. Sub-epicranial haemorrhage is as constant in the head injuries of the new born infant as it is in the older age groups. In a series of autopsies on new born infants I found this extensive sheet of blood in the sub-epicranial space in every case in which there were gross intracranial lesions (Fig. 1). In most of these cases labour had been easy and without intravaginal manipulation. There could have been no violent impact on the skull in such cases and the mechanism must have been different. The squeezing of the head through the birth canal would have congested the vessels within the circle of scalp presenting in the lumen of the birth canal, and this congestion could have determined an oozing of blood through the epicranial sheet into the sub-epicranial space. As in adults there was no extravasation of blood into the thickness of the scalp. In most of the cases it was the sole herald of gross intracranial lesions. The haemorrhage into the interstitial tissues of the upper eyelids which would be the only visible manifestation of the commonly encountered sub-epicranial sheet of blood was found to be an independent lesion in many of the cases, as the " black eye," more often than not, involved the lower eyelids as well. The sub-epicranial sheet of blood can extend down on the side of the head over the temporal fascia and over the zygomatic arch on to the face, and when this occurs there is a swelling of the face extending from the zygomatic arch right down to and even below the mandible. 71 MILROY PAUL

Fig. 1. The scalp haemorrhages of the new born. A sub-pericranial haematoma on the right side, and on the left side the two slices of a sub-epicranial haemorrhage as they would be viewed at a post mortem examination.

The sub-pericranial haematomas The sub-pericranial haematoma is a common birth injury. The blood lies between the pericranium and the bone and it cannot extend beyond the margins of the bone on account of the firm blending of the pericranium with the intersutural fibrous tissue. In birth injury cases the haematoma is nearly always on one of the parietal bones. The details of the disposition of the haematoma on a parietal bone have not been previously described, although they are easy to observe (Fig. 1). The haematoma overlies that part of the parietal bone forming the roof of the vault, as distinct from the part of the parietal bone forming the side of the vault, and if it does extend on to the side of the vault, it should reach downwards as far as the superior curved line of the temporal fossa only, but as the temporal muscle in infants is an inconspicuous sheet on the parietal bone, the sub-pericranial haematoma in new born infants extends right down to the inferior margin of the parietal bone. Sub-pericranial haematomas do not occur in adults or older children, but they are not uncommon in very young children. The age incidence of the sub-pericranial haematoma cases has been attributed to the increased vascularity of the pericranium in the earlier age groups, but it is more likely that the cause of the haemorrhage lies in the elasticity of the largely cartilaginous vault of this age group, which permits 72 HAEMORRHAGES FROM HEAD INJURIES distortions and restorations of contour which could detach the peri- cranium off the bone. This birth injury is the result of squeezing of the head during its passage down the birth canal. The usual bone presenting within the lumen of the birth canal is the parietal bone and this bone would be distorted to curve more convexly outwards. Although this distortion would tighten the pericranium on to the bone, the sudden restoration of the contour of the bone occurring when the head has been born, will detach the pericranium from the bone. Only that part of the parietal bone forming the roof of the vault would present in the birth canal, and the detachment of the pericranium resulting from distortion of the vault would concern this part of the bone only. Apart from birth injuries, sub-pericranial haematomas occur usually on the frontal bones in very young children. There is always a history of a violent impact on the frontal region, and in such cases it is likely that the inbending of the bone at the point of impact had detached the pericranium off the frontal bone. The sub-pericranial haematomas of the new born and of very young children usually get absorbed ; they could ossify and they could suppurate; and in some cases, if the bone is broken, blood and cerebrospinal fluid could escape through a torn dura mater to mix with the sub-pericranial blood giving a safety valve haematoma, or a traumatic meningocele.

Haemorrhage in the temporal fossa The pericranium in the temporal fossa gives attachment of the temporal muscle to the bones, and this connection of muscle and fascia with the bone is so intimate that blood does not collect between the pericranium and the bone in the temporal fossa except in the new born. Blood in the temporal fossa extravasates into the muscles, and could cause a visible swelling outlying the temporal fossa. Blood at this site is the result of local violence. That it is not a safety valve haematoma working outwards through a fracture in the temporal fossa is shown by the demonstration that blood does not exude from such fractures when they are exposed at surgical operations. These haematomas can occur in the temporal muscle when there are no fractures in the temporal fossa. Local violence over the temporal fossa can detach the dura mater off the bone at a site very likely to result in an extra dural haematoma from the middle meningeal veins, and a haematoma ballooning the temporal fossa in a head injury case is therefore often associated with a middle meningeal haemorrhage.

The orbital haemorrhages The " black eye" of head injuries is differentiated from the ordinary "black eye " resulting from direct external violence by its being limited within the orbital margins, by the purple tint of its more deeply placed 73 MILROY PAUL

Fig. 2. Orbital haemorrhage between the orbital fascia and the bone near the apex of the orbital cavity. blood as contrasted with the beefy redness of the ordinary " black eye ", and by the associated sub-conjunctival haemorrhage which extends so far backwards that its posterior limit cannot be seen. This description taken from Trotter's account in Choyce's System of Surgery (1923) is coloured by the concept that the haemorrhages have tracked forwards from the orbit. This concept is still widely held although it was not based on the evidence of dissections made at autopsies. If blood had tracked forwards from the orbit into both upper and lower eyelids as well as on to the sub-conjunctival surface of the eyeball, there should be some interference with the movements of the eyeball, some chemosis and some degree of proptosis. That none of these sequels is found in the large numbers of head injury cases with " black eyes " is good evidence that neither the blood in the " black eye " nor the sub- conjunctival haemorrhage have tracked forwards from the orbit. The attachment of the orbital septum to the rim of the orbit and continuance of the orbital septum with the tarsal plates would carry blood tracking from the orbit into the eyelids, deep to these structures into the sub- conjunctival layer of the eyelids. The blood in the " black eye " in the head injury cases lies, however, between the skin and the orbital septum and tarsal plate. The " black eye " and the sub-conjunctival ecchymosis take some hours or even a day or two to appear, and there is then a period of several hours or days during which the haemorrhage spreads. The haemorrhage in the eyelids does not spread beyond the margins of the orbit probably because of resistance at the rim of bone. 74 HAEMORRHAGES FROM HEAD INJURIES On the eyeball the haemorrhage appears at the corneo-scleral junction at either the lateral or medial sides or at both these sites, and spreads peripherally from here to the conjunctival fornices, forming flame-shaped raised, red areas. Although the haemorrhage might on occasion spread till it covers the whole sub-conjunctival surface of the eyeball, it is usually limited to the flame-shaped areas. These areas are between the eyelids, and this suggests that further spread had been prevented by the pressure of the eyelids against the eyeball, and that the site of the haemorrhage was determined by the lack of support at this place by the eyelids. Both the subcutaneous haemorrhage on the eyelids and the sub- conjunctival haemorrhage on the eyeball show the same characteristic of late onset of the bleeding and limitation of spread by resistance at anatomical boundaries. The bleeding must have been caused by injuries to vessel walls at the time of a violent impact on the head, the delayed haemorrhage being due to slow oozing. The limitation of the site of bleeding to loosely supported tissues suggests that the injury had caused bleeding by jarring blood vessels in loosely supported tissues. On the other hand, the appearance of a " black eye" after operations in which the scalp was reflected down on to the face suggests that in these cases, the cause was the severe relaxation of the loose tissue of the eyelids by

Fig. 3. Apparatus used for introducing fluid at known pressures on to the outer surface of the dura mater. 75 MILROY PAUL displacement of the scalp down towards the eyelids. The " black eye in both instances is the result of violence in the neighbourhood of the eye and to that extent it is of localising value. Dissections made of the orbit in cases of head injuries showed that haemorrhage did not occur within the sheath of the orbital fascia, even in cases with fractures of the orbital plates of the frontal bone. Haemorrhage in the orbit between the bone and the orbital fascia is, however, not uncommon, but such haemorrhage is found only below the orbital plate of the frontal bone usually near the apex of the orbit (Fig. 2). Dissection of the orbital fascia showed that although it was like the dura mater in being a continuous sheet uninterrupted at suture lines, it was so firmly adherent to the bones on the floor and side walls of the orbit that extra-fascial haemorrhages could not occur at these places. The fascia is, however, easily separated from the roof of the orbit, and the blood vessels of the nasal cavity adjoining the roof of the orbit at its apex are the source of the haemorrhage so commonly found at this place in head injuries at autopsy. This extra-fascial haemorrhage caused no disturbance to the contents of the orbit. The structures within the orbital fascia are supplied by the ophthalmic artery and its branches and this artery was never found to have been injured in my series of head injury cases.

EXTRA DURAL HAEMORRHAGE An unexplored extra dural haemorrhage will go on bleeding till death supervenes. In 1886, W. H. A. Jacobson documented and reviewed a series of cases of extra dural haemorrhage in which simple evacuation of the massive blood clot had sufficed to determine the complete recovery of these patients. These successes have been repeated so often since then, that they are now the normal results of such surgical interventions. Success in this field has dulled curiosity in regard to two intriguing questions: Why does an unexplored extra dural haemorrhage continue relentlessly till death supervenes ? and why does simple evacuation of the massive blood clot arrest such haemorrhage ? It is remarkable that no new experimental work has been published on this and other related questions since the pioneer work of Sir Charles Bell (1816).

Is detachment of the dura mater from the bone a necessary prelude to the formation of an extra dural clot ? The following quotation is from Surgical Obser-vations by Sir Charles Bell (1816):- " It is extraordinary that anyone who has ever raised the skull cap in dissection, and felt the strength of the universal adhesions of the dura mater to the bone, could for an instant believe that the arteria meningea 76 HAEMORRHAGES FROM HEAD INJURIES media had power of throwing out its blood to the extent of tearing up these adhesions from the entire half of the cranium." I put this proposition to the test of experiment by submitting the dura mater exposed through a half-inch trephine hole in the vault of the skull to a hydrostatic force of 200 mm. of mercury for half an hour. This pressure proved inadequate to detach the dura mater off the bone (Fig. 3). Bell devised two experiments to show how the dura mater did get detached from the bone in head injury cases. He wrote, " Strike the skull of the subject with a heavy mallet. On dissecting you find the dura mater to be shaken from the point struck. Repeat the experiment in another subject, and inject the head minutely with size injection and you will find a clot of the injection lying between the skull and the dura mater at the point struck, and having an exact resemblance to the coagulum found after violent blows on the head. I imagine this is conclusive." To familiarise myself with these phenomena, I repeated Bell's experi- ments. The results were interesting. In a series of experiments, single severe blows were delivered on the vertex of the head of subjects, who were supported in the sitting position. Blows with a heavy wooden plank, a wooden mallet, and a small metal hammer failed either to fracture the vault of the skull or to detach the dura mater off the bone. Blows on the side of the head with a wooden mallet fractured the skull and detached the dura mater off the bone, but, in these experiments, the head rested on a hard surface and the blow was resisted by the support of this surface. A blow on the midline frontal region with the head resting on its occiput fractured the vault and detached the dura mater over an area three inches in diameter. The detachment in this instance was on one side of the middle line from the superior longitudinal sinus outwards (Fig. 4). These experiments proved that severe grades of blunt force are needed either to fracture the skull or to detach the dura mater off the bone. In head injuries caused by rapidly moving vehicles, the head is usually projected on to a hard stationary surface or is struck by the vehicle. Such conditions are difficult to reproduce on the cadaver, but it is easy to appreciate that the degree of violence in such circumstances would be much greater than that in the experiments cited. Bell's contention that extra dural bleeding could not occur without prior detachment of the dura mater off the bone, carries several corollaries. The detachment of the dura mater off the bone by the violence of an impact, occurs only at the site of the impact, and if this is to result in an extra dural haemorrhage, it should occur at the site of a blood vessel, which should be torn during the detachment of the dura mater off the bone. 77 7 MILROY PAUL

Fig. 4. Experiment on the cadaver. A blow on the front of the head caused a fissured fracture of the vault (thick lines), a depressed fracture of the inner table (area with transverse ruling), and detached the dura mater on the left of the superior longitudinal sinus (area with dots). Is progressive dissection of the dura mater off the bone an inevitable sequel to its detachment by blunt force ? Bell overlooked the fact that the detachment of the dura mater from the bone produced by the violence of an impact, was too localised to account for the extensive separations of the dura mater from the bone which occur with massive extra dural blood clots. Sir John Erichsen (1895) suggested that the dura mater became progressively detached off the bone by transmission of the hydrostatic pressures of blood emerging from a bleeding point, to the entire surface of the detached dura mater on the principle of the hydraulic press. I put this hypothesis to the test of experiment by subjecting dura mater detached from the bone over a circle two inches in diameter, to a hydro- static pressure of 200 mm. of mercury for five minutes. This force detached the dura mater off the bone over a wide area, four inches by three inches. There are, however, good reasons for rejecting Erichsen's hypothesis. Hydrostatic pressures cannot be transmitted through a mass of blood clot, and the blood clot of an extra dural haemorrhage is almost dry. Evidence will be adduced which establishes that the blood at the bleeding point of an extra dural haemorrhage escapes at pressures considerably below the venous pressures. Such pressures could not dissect the dura mater off the bone. As there is little doubt that the dura mater does separate off the bone, pani passu with increase in size of the clot, there must be a mechanical 78 HAEMORRHAGES FROM HEAD INJURIES factor which determines this. If the dura mater be exposed by removal by a trephine of a disc of bone one inch in diameter, direct inward pressure by a finger on this circle of dura mater will fail to detach the dura mater off the bone at the margins of the hole. Indeed, the dura mater will tear before this could occur. On the other hand, a finger inserted at the junction between the dura mater and the bone at the margins of the hole, will separate the dura mater off the bone with ease, and if the finger is then inserted through the hole in the bone into the angle between the detached dura mater and the bone, it will continue to separate the dura mater from the bone over a wide area. This separation leaves the bone bare, and does not tear the surface of the dura mater. It is evident that this separation is effected by shearing the connective tissue bands uniting the dura mater to the bone, from their attachments to the bone. The force required for this dissection is small. In an extra dural haematoma, the clot lies between the inelastic dura mater and the rigid bone. Expansion in volume of the blood clot will bulge the dura mater towards the brain, till the dura mater becomes taut. The blunt edge of the almost solid blood clot will then drive into the angle between the dura mater and the bone and shear the dura mater off the bone, with the same ease that a finger does, when it is inserted at this place (Fig. 5). The extent to which the dura mater can be separated from the bone by blunt dissection The extent to which the dura mater can be separated off the bone must affect the spread of extra dural blood clots. A very good estimate can be made of the varying degrees of fixation between the dura mater and the bone at different sites, by inserting a finger through a one-inch trephine hole into the angle between the dura mater and the bone. Working upwards from the side of the vault, the duratmater separates easily off the bone

Fig. 5. Diagram showing how the blunt edge of an extra dural blood clot shears the dLira mater off the bone. 79 7-2 MILROY PAUL till the superior longitudinal sinus is reached. The dura mater forming the outer wall of the superior longitudinal sinus is so adherent to the shallow gutter in the bone over the sinus, that considerably greater force must be exerted at this place to separate the dura mater off the bone. Finger dissection can however, separate the dura mater forming the outer wali of the superior longitudinal sinus cleanly off the bone, and the dura mater can then be separated easily on the other side of the middle line. Working from the side of the vault to the base of the skull the dura mater separates easily off the floor of the anterior fossa up to the cribriform plate, and off the floor of the middle fossa up to the lateral border of the cavernous sinus (Fig. 6). Separation of the dura mater off the posterior edge of the great wing of the sphenoid is easy and this allows blood in the extra dural space to dissect its way from the middle to the anterior fossa or vice versa.

Fig. 6. Dura mater detached off the base of the skull by blunt dissection with a finger. Posteriorly the dura mater separates off the occipital bone right down to the foramen magnum. There is greater fixation between the outer walls of the lateral sinuses and the bone than over the rest of the dura mater, but finger dissection can separate the dura mater walling the lateral sinus cleanly off the bone (Fig. 6). The detachment can be continued from the occipital bone forwards across the sigmoid sinus on to the postero-medial surface of the petrous part of the temporal bone. Although the dura mater can be separated off the postero-superior border of the petrous part of the temporal bone, separation at this place does not occur in extra dural haemorrhages from middle meningeal vessels and extra dural clots do not extend over this edge between the middle fossa and the posterior fossa with haemorrhages from these vessels. 80 HAEMORRHAGES FROM HEAD INJURIES The dura mater cannot be separated by blunt dissection off the basi- occipital bone, the basi-sphenoid bone, the body of the sphenoid or the cribriform plate. These blunt finger dissections closely approximate to the dissections of the dura mater off the bone by extra dural blood clots. Middle meningeal haemorrhage W. H. A. Jacobson (1886) chose the title "On Middle Meningeal Haemorrhage " for his paper, because most of the extra dural clots in his series of cases were overlying the anterior branches of the middle meningeal vessels. In common with all writers of his period, Jacobson accepted this as evidence that the bleeding had come from the middle meningeal artery. Wood Jones (1912) made serial sections of the meningeal vessels from three cases coming to post mortem with massive extra dural blood clots overlying the anterior branches of the middle meningeal vessels. He demonstrated that the middle meningeal artery was intact in all three cases, and that there were no less than twelve tears in the walls of the middle meningeal veins of these three cases. He showed that the meningeal vessels are embedded in the outermost layers of the dura mater with the artery deepest and the veins overlying the artery. The veins lie in grooves on the inner surface of the bones of the cranial chamber, and the outer walls of the veins covered by a thin layer of the dura mater are attached to the bone in these grooves. Detachment of the dura mater off the bone will be liable to tear the walls of the veins, but cannot tear the walls of the arteries. These observations of Wood Jones are fundamental to an understanding of the mechanics of middle meningeal haemorrhage. I have made close observations on the bleeding from the meningeal vessels when the blood clot overlying these vessels is evacuated at a surgical operation. The bleeding comes from one or more points on the meningeal vessels as an ooze which usually soon ceases. If the ooze continues, light pressure with a gauze swab for a few minutes will stop the flow. In some of the cases the bleeding had ceased before the vessels could be inspected. These observations confirm Wood Jones's findings that there are two or three tears and that the tears are on the walls of the veins. Inspection of the meningeal vessels after the bleeding had ceased revealed the surprising feature that there was no break in the walls of the vessels visible to the naked eye. In three cases of massive extra dural clot overlying the meningeal vessels, coming to post mortem, I examined the meningeal vessels with a hand lens ( 10), and confirmed that there were no visible breaks in the walls of the vessels. These findings were investigated from a different angle by noting that when a disc of bone was outlined by a trephine over the branches of the meningeal vessels, elevation of the disc of bone often caused profuse bleeding. This bleeding could be slowed by packing gauze on to the dura mater exposed within the trephine hole. When the gauze is removed the bleeding is reduced to an ooze from one or more localised points on 81 MIILROY PAUL the meningeal vessels. Reapplication of the gauze pack for a little longer arrests the bleeding, and at this stage inspection shows that there is no tear in the dura mater and no visible break in the walls of the meningeal vessels. The observations established that separation of the dura mater from the bone may tear the walls of the meningeal veins at one or more points, and that when the bleeding stops the tears are not visible to the naked eye. These observations are not without significance for the management of cases of haemorrhage from the middle meningeal vessels. Ligature of the vessels is unnecessary as the bleeding is arrested so easily, and once it is arrested it will not recur. Blood leaking through a hole in a meningeal vein will emerge at a considerably reduced pressure, because of the frictional resistance to flow at the margins of the hole. The smaller the hole becomes with vasoconstriction the greater the frictional resistance, and this will reduce the flow to an ooze. The surprising feature is not that the haemorrhage ceases so easily when it is exposed at a surgical operation, but that so insignificant a trickle could have led to the formation of so massive an extra dural clot, and that the trickle would have continued till the time of death, if the clot had been undisturbed. The final arrest of the bleeding following exposure of the bleeding points must be from sealing of holes in the walls of the veins by the deposition of platelets. This would have been prevented before the operation by a continual flow of blood through the holes, carrying the blood into the serum bathing the walls of the veins and causing clotting at a little distance from the walls of the veins. Such clotting would not interfere with the flow. The flow would be arrested if the serum outside the vessel walls accumulated at a pressure higher than the pressure with which the blood emerged from the veins, and the continuance of the flow in the middle meningeal haemorrhage case is evidence that the serum in the extra dural compartment never accumulates under sufficient tension to exert even this small degree of pressure. The intracranial pressures in middle meningeal haemorrhage The very low pressures at which blood leaks from meningeal vessels in cases of middle meningeal haemorrhage, raises the question whether leaks at these low pressures would continue till so much blood accumulated in the cranial chamber that it interfered with the vital functions of the brain. The accumulation of a massive extra dural clot is regarded as the most typical cause of traumatic cerebral compression. But could compression ensue from the escape of blood at minimal pressures? In the first instance, when the dura mater has been detached from the bone by the violence of an impact, filling of the extra dural space so created necessitates pushing the flaccid dura mater against the surface of the brain. Although the brain is as incompressible as water, it is sheared 82 HAEMORRHAGES FROM HEAD INJURIES by negligible forces (Holbourn, 1943). The indentation of the surface of a cerebral hemisphere by an extra dural blood clot pressing the dura mater against it, would be a deformation of this kind requiring a negligible shearing force, provided that space is found for the extra dural blood clot by a reduction in the volume of the intracranial contents. The intracranial contents are as incompressible as water, and space can only be found for an encroachment on the intracranial space by the expulsion of some of the intracranial contents. A reduction in the volume of blood circulating in the intracranial chamber, and in the volume of the cerebrospinal fluid would be equivalent to the expulsion of some of the intracranial contents. It is the only way by which space could be made for an extra dural blood clot. Blood leaking into the extra dural space could fill the space till the dura mater became taut, without raising the pressures in this space, provided that the brain did not resist indentation from the bulge of the dura mater (Fig. 5). When the dura mater becomes taut the pressure in the extra dural space should rise, but if at this stage, more room is made in the extra dural space by dissection of the dura mater off the bone by the blunt edge of the clot there will be no rise of pressure in the extra dural space. The pressure will not rise so long as the dura mater continues to be dissected off the bone, and so long as the brain does not resist indentation. That the brain does not resist indentation, even when its surface has been greatly hollowed by a massive extra dural clot is evident from the observation that the clot does not extrude when a hole is made in the skull to expose it. The clot needs to be mechanically evacuated and when this is done the dura mater still remains depressed with wrinkles on its surface for several minutes, hours or even days till the brain re-expands sufficiently to push the dura mater back against the bone. The re-expansion of the brain after removal of an extra dural clot is the result of an inflow of blood and cerebrospinal fluid into the cranial chamber. If a mass of extra dural blood clot built up a pressure in the intra dural compartment as a result of its encroachment on the intracranial space, this pressure would be readily transmitted from the intra dural compart- ment to the extra dural space, and the extra dural space would be obliterated if there were no corresponding pressure in this space to resist the pressure in the intra dural compartment. The collection of blood in the extra dural space from blood leaking at a trickle, can go on till death occurs from interference with cerebral functions, only because there is no rise of pressure in the extra dural space. The gross encroachment on the intracranial space by the massive clot is compensated for by reduction in the volumes of cerebrospinal fluid and circulating blood in the intracranial chamber. These reductions in volumes must be from reflex physiological responses to the encroachment by the clot. Removal of the clot and withdrawal of the mild force deforming the cerebral hemispheres brings 83 MILROY PAUL more blood and cerebrospinal fluid to the cranial chamber probably from reversal of these reflex physiological responses. The gross indentation of the surfaces of the cerebral hemispheres by an extra dural blood clot is accompanied by displacement of the cerebral hemisphere down towards the base of the brain and by displacement of the other cerebral hemisphere against the side of the skull. The flattening of the convolutions of this hemisphere which results from this is taken as evidence of a grossly raised intracranial pressure, but it is no more than the effect of the mild force flattening the cerebral surface against the bone. The evidence presented shows that traumatic cerebral compression from a massive extra dural blood clot is accomplished without building up pressures in the intracranial chamber, and that the gross interference with the functions of the brain caused by the clot are the result of distortions and displacements of the brain and not the effects of compression of the brain. The effects on the brain of a middle meningeal haemorrhage The massive blood clot from a middle meningeal haemorrhage causes the dura mater to bulge, and indent the surface of the cerebral hemisphere, and the effects on the brain of the haemorrhage are largely the result of this indentation of the surface of the cerebral hemisphere and of the displacement of the hemisphere accompanying this indentation. The two principal consequences of the presence of the clot are loss of consciousness and motor paralysis, and the gradual onset and the pro- gressive march of these two consequences with increase in size of the extra dural blood clot, leaves little doubt that the clot is directly responsible for these symptoms. The complete recovery attending evacuation of the blood clot at a surgical operation, and the occasional return to the previous condition, if the bleeding should continue after a surgical operation for evacuation of the blood clot, are good evidence that not only is the clot responsible for interference with the functions of the brain, but that removal of the clot causes restoration of function, and that recurrence of the clot causes a return of interference with brain function of the same nature as before. The process is truly reversible. Loss of consciousness In middle meningeal haemorrhage, loss of consciousness is gradual, and the clot must attain a particular size before it is sufficiently large to interfere with consciousness. The gradual deepening of unconsciousness which occurs thereafter is related to the progressive increase in size of the clot. If there is no rise of intracranial pressure within or without the extra dural compartment in cases of middle meningeal haemorrhage, the loss of consciousness must be related to the slow distortion and displacement of the cerebral hemisphere which accommodates the clot. The return of consciousness with evacuation of the clot is slow, if the brain does not 84 HAEMORRHAGES FROM HEAD INJURIES re-expand at once to its original shape and position after the clot is removed. This evidence suggests that it is the distortion and displacement of the cerebral hemisphere which causes unconsciousness. The clot could not have disrupted neural tissues nor could it have appreciably impeded the circulation to the neural tissues. Either of these contingencies would cause irreversible changes. Motor paralysis The gradual onset of facial, followed by upper limb paralysis on the side opposite the clot of a middle meningeal haemorrhage is clearly the result of increasing height of the clot from the base of the brain. Cushing's conception based on animal experiment that hydrostatic pressures on the motor cortex produced first motor convulsive seizures and then motor paralysis, depending on an increasing pressure causing first venous obstruction, with engorgement of blood, and later arteriolar compression with anaemia, was elaborated in great detail by Trotter who postulated a zone of the brain with arteriolar compression surrounded by a zone of brain with venous compression, centred on the site of the extra dural blood clot. Motor convulsions would precede motor paralysis, and motor paralysis would be succeeded by compression of the mid-brain indicated by the Hutchinson pupil. There would finally be compression of the vital centres of the medulla with the " Vasomotor reaction of Cushing," the " Compression pulse," and the onset of Cheyne-Stokes respiration as clinical manifestations of a medulla combatting loss of function from cerebral compression. There are good reasons for reassessment of this picture of the cerebral compression caused by middle meningeal haemorrhage. If the motor paralysis were the result of compression obliterating the blood flow through the arterioles of the motor cortex, such compression would cause irreversible paralysis in the space of some minutes. The motor paralysis of a middle meningeal haemorrhage recovers completely with evacuation of the blood clot, even when it has been present for hours or even days. It is likely that the indentation of the cerebral hemisphere caused by the clot of a middle meningeal haemorrhage causes a paralysis by distortion of the motor cortex. The spread of the paralysis from face to upper limb would be related to the extension of the distortion from the face to the arm area of the motor cortex. As with the loss of consciousness, the paralysis recovers when the distortion corrects itself after removal of the blood clot. This correction of distortion and displacement is caused by re-expansion of the brain from increase in its intracranial blood and cerebrospinal fluid volumes following evacuation of the blood clot. The Hutchinson pupil Dilatation of the pupil on the same side as as extra dural clot was ascribed by Hutchinson (1897) to powerful pressure on the cavernous 85 MILROY PAUL sinus by a clot extending deeply in at the base of the brain. He described fullness of vessels and protusion of the eyeball as accompaniments of the pressure. If the dilatation of the pupil was the result of pressure on the cavernous sinus by an extra dural clot as postulated by Hutchinson, there should be paralysis of other muscles supplied by the oculomotor nerve, and also interference with the functions of other nerves in the wall of the cavernous sinus. Trotter (1923) believed that the Hutchinson pupil was the result of an increasing intracranial pressure affecting the third nerve nucleus in the mid-brain, first on one side and then on the other. Each nucleus reacted first by stimulation and then by paralysis. Rowbotham (1949) ascribed the Hutchinson pupil to a tentorial pressure cone compressing the brain stem and stretching the oculomotor nerve at its point of entrance into the wall of the cavernous sinus. Gillingham (1954) ascribed it to stretching of the third nerve by prolapse of the hippocampal gyrus through the tentorial notch. All these explanations of the genesis of the Hutchinson pupil put the lesion at the level of the oculomotor nerve or its nucleus where it ought to involve all muscles supplied by the third nerve. As this never occurs, the lesion must be supranuclear, and it is likely that the deformation of the surface of the cerebral hemisphere over the facial area of the motor cortex is the cause of the Hutchinson pupil. Dean (1896) pointed out that localised pressure on the cortex caused dilatation of the pupil on the same side. If the Hutchinson pupil is the result of deformation of the motor cortex by an extra dural blood clot, it is a valuable localising sign of the lesion. Although the Hutchinson pupil may be absent in cases where the motor cortex is indented by an extra dural clot, it is an accurate guide to the side of the lesion when it is present. The subsequent dilatation of the pupil on the opposite side in the later stages of a middle meningeal haemorrhage could be the effect of flattening of the opposite motor cortex against the side of the skull. Haemorrhage from the large venous sinuses The evacuation at a surgical operation of an extra dural blood clot which reaches up to or overlies either the superior longitudinal or the lateral sinuses, can cause a flow of blood which is so profuse that it will exsanguinate the patient in a short time, if it is not controlled. Such bleeding comes from the deep recess between the dura mater and the bone at the site of the venous sinus and it is clear that the blood clot had been sealing a large tear in the extra dural wall of the sinus. Although the pressures obtaining in the large venous sinuses are not appreciably different from those in other large veins of the body, the blood emerges forcibly from the vein, because of the negligible frictional resistance to flow at the margins of a large tear. If a gauze plug could be inserted between the dura mater and the bone at the site of the tear in the vein, 86 HAEMORRHAGES FROM HEAD INJURIES the bleeding would cease forthwith because of the low pressures in the veins. The technical difficulty in localising a tear at so remote a part as the deep recess between the dura mater and the bone is, however, quite appreciable. In cases of this kind where I was able to palpate a fissured fracture on the inner wall of the vault overlying the area of the clot, I followed this fissured fracture up to the point at which it crossed the line of the venous sinus, and packed gauze between the dura mater and the bone at this point. The bleeding ceased forthwith proving that the vein had been torn at this point. In other cases I have inserted gauze in the line of the probable direction of the blood flow and after one or two attempts, the bleeding is arrested, if the gauze plug is correctly positioned over the tear. The tear in the vein wall is the result of detachment of the dura mater off the bone from the violence of the impact. The dura mater usually separates only on one side up to the venous sinus, and the extra dural clot extends laterally from the wall of the sinus on this side (Fig. 7). In the case of the superior longitudinal sinus the blood clot will extend laterally from the vertex of the skull, and the motor paralysis which results will affect

Fig. 7. An extra dural clot from blood leaking from the superior longitudinal sinus. the lower limb before it affects the upper limb. This feature enables such a clot to be differentiated from the clot from a middle meningeal vessel where the paralysis affects the face and the upper limb, and never affects the lower limb. Even if an extra dural clot from the middle meningeal veins reaches up to the superior longitudinal sinus from below, it is easily differentiated at a surgical operation from an extra dural haemorrhage which had extended downwards from the superior longitudinal sinus by the profuse bleeding following evacuation of the blood clot, if the blood had come from the superior longitudinal sinus. Although the violence of an impact does not usually detach the whole outer wall of a venous sinus off the bone, it may occasionally do so, and in such cases the extra dural haemorrhage will override the venous sinus. 87 N1ILROY PAUL Extra dural clots in the posterior fossa of the skull always originate from a tear in the wall of a lateral sinus, and plugging between the wall of the sinus and the bone at the site of the tear will arrest this bleeding, even though it becomes torrential when the clot is disturbed at a surgical operation. Although the violence of an impact tears the dura mater where it forms the outer wall of a venous sinus, these tears do not extend beyond the outer wall of the vein, and the tear never extends from the outer wall of the sinus into its intra dural walls. Sub-dural haemorrhages from tears of the large venous sinuses are unknown, except in new born infants where a tentorial tear could extend into the sub dural walls of the lateral sinus. The sources of extra dural haemorrhages and their arrest at a surgical operation The arrest of an extra dural haemorrhage is dependant on exposure of the source of the bleeding. If the blood clot overlies a meningeal vessel, evacuation of the blood clot will show that the bleeding comes from a mere trickle from one or more points on the walls of the meningeal vessels, and this bleeding is easily arrested by light gauze pressure maintained till the bleeding points are sealed. If evacuation of a blood clot is followed by a torrential haemorrhage, the haemorrhage will be either from the superior longitudinal sinus or from the lateral sinus. This haemorrhage must be immediately controlled if the life is to be saved, and plugging between the dura mater and the bone at the site of the tear in the sinus wall will do this. If necessary a fresh opening may be made in the skull near the line of the sinus to facilitate the insertion of the gauze plug, which will need to be kept in place for a few days. In a consecutive series of 33 cases of extra dural haemorrhage under my care the bleeding had occurred either from the meningeal veins or from the large venous sinuses. Haemorrbage from other sources has never been encountered by me. These findings permit a simple plan for the management of cases of extra dural haemorrhage; an extra dural blood clot must be evacuated. If the clot overlies the meningeal vessels evacuation will reveal a gentle ooze at one or more points on the meningeal vessels which will cease with light gauze pressure. There is no risk of recurrence of such haemor- rhage once the ooze has been arrested. If the clot reaches up to or overlies a large venous sinus, evacuation of the clot will unseal an opening in the vein wall and cause torrential bleeding which must be arrested forthwith. Plugging against the vein wall between the dura mater and the bone, will arrest this haemorrage if the plug is placed over the tear in the wall of the vein. SUB-DURAL HAEMORRHAGE A sub-dural haemorrhage is the collecting of blood between the outer surface of the dura mater and the arachnoid membrane. The definition 88 HAEMORRHAGES FROM HEAD INJURIES specifies the outer surface of the dura mater and not its inner surface, to include the contingency envisaged by Hannah (1936) and Kaump and Love (1938) that sub-dural haemorrhages are within the thickness of the dura mater. There is, however, little need to discuss this proposition on account of the improbability that the dura mater would split to enclose several hundred cubic centimetres of blood over an area overlying the greater part of a cerebral hemisphere (Leary, 1939). The blood in a sub- dural haemorrhage is truly sub-dural in position. The accommodation of blood in the sub-dural cavity The space between the inner surface of the dura mater, and the outer surface of the arachnoid membrane is as much a body cavity as are the peritoneal, pleural or pericardial cavities, and it would be more accurate to refer to it as the sub-dural cavity rather than as the sub-dural space. In many head injury cases, a considerable volume of blood is accom- modated in the sub-dural cavity despite its being a potential space for the greater part of its extent. The location of blood in this cavity has been inadequately appreciated by writers on head injuries. Surgeons have confined their attentions to collections of blood overlying the outer and the inferior surfaces of the cerebral hemispheres, and pathologists have not described or assessed the effects of the large volume of blood in the posterior fossa, which is found so often at autopsies on head injury cases. The blood vessels traversing the sub-dural cavity All the blood brought to the brain by the two internal carotid and the two vertebral arteries is returned to the large venous sinuses within the dura mater, by a literal forest of venules passing from the brain through the sub-arachnoid space and then across the sub-dural cavity. These venules are unsupported, thin-walled and fragile, running a straight course between the brain and the dura mater. They are the only blood vessels traversing the sub-dural cavity apart from the two internal carotid arteries and the two vertebral arteries. As the brain within the sub-dural cavity has no attachment equivalent to a mesentery, its anchors are these four main arteries, the forest of thin-walled venules and the cranial nerves. The descriptions of the venules crossing the sub-dural space which are given in textbooks on anatomy do not give an adequate picture of their dispositions. The literature on this subject is meagre. Trotter (1914) stated that " it is nearly certain that the cerebral veins passing from the brain to the tributaries of the superior longitudinal sinus are nearly always the source of the blood in a chronic sub-dural haemorrhage."' Hannah (1936) termed these venules " the bridging veins.' As long ago as 1889, Mittenzweig noted that rupture of a vein passing from the frontal lobe as far away as four centimetres from the superior longitudinal sinus had caused an acute sub-dural haemorrhage of fluid blood. From dissections of two hundred subjects, he found that 89 MILROY PAUL venules remote from the superior longitudinal sinus were present over the frontal lobe in 59 subjects and over the occipital lobe in nine subjects. Leary (1939) recognised that bridging venules opened either into the large venous sinuses or into their tributaries within the dura mater, at places remote from the main sinuses. He noted that bridging venules were present over the outer surface of the cerebral hemispheres, that there were aggregations of bridging venules on the under surfaces of the hemispheres at the frontal and temporal poles, with isolated bridging venules on the under surfaces of the temporal and occipital poles, and that there were bridging venules below the tentorium. These descriptions do not, however, give adequate recognition of the disposition of the venules. From obser- vations of these venules in 10 subjects, they were noted to be disposed in constant patterns, which influence the mechanics of the sub - dural haemorrhages. The whole of the arc of the superior border of each cerebral hemisphere is anchored by scores of bridging venules passing to the superior longi- tudinal sinus. The venules were so closely set that they constituted a mesentery suspending the cerebral hemispheres from the dura mater. The superior borders of the lobes of the cerebellum are connected by a similar set of close set venules passing to the lateral sinus immediately below the tentorium cerebelli. These venules were also so closely set that they formed a mesentery suspending the cerebellum from the under surface of the tentorium cerebelli. There were forests of veins passing from the frontal poles and the temporal poles to the dura mater. There were many solitary bridging venules over the outer surfaces of the cerebral hemispheres, the surfaces of the cerebellar lobes, and the under surface of the temporal and occipital lobes of the cerebral hemispheres, but on the medial surfaces of the cerebral hemispheres there were no bridging venules except in the depth just above the corpus callosum. These bridging venules passed from the brain to the falx cerebri near its free border. There were no bridging venules passing from the front of the brain stem to the dura mater over the basi-occipital and the basi-sphenoid bones. There were veins running from the brain stem with the cranial nerves on each side. Recognition of the pattern of the disposition of the bridging venules is necessary for assessment of the mechanics of ruptures of these vessels. They have been described at length because of the lack of adequate descriptions in the literature. Sub-dural haemorrhage overlying the outer surfaces of the cerebral hemi- spheres Blood in the sub-dural space overlying the convex surfaces ofthe cerebral hemispheres is visible through the dura mater as a blue discoloration. Although blood at this site could clot, more often than not it is fluid at the time it is exposed at a surgical operation or at an autopsy. Incision of the dura mater gives exit to this blood. It spurts through the opening at 90 HAEMORRHAGES FROM HEAD INJURIES first and then continues to flow gently till all the blood has been evacuated. The blood has remained fluid because it does not come into contact with rough surfaces, both the inner surface of the dura mater and the outer surface of the arachnoid membrane being smooth and lined by endothelial cells. The blood overlying the convex surface of a cerebral hemisphere lies in a hollow formed by an indentation of the surface of the cerebral hemi- sphere, and the blood is prevented from flowing out of this hollow, down the sides of the cerebral hemispheres, by the close contact of the surface of the brain with the dura mater beyond the margins of the hollow. Blood leaking into the sub-dural space overlying the convex surface of a cerebral hemisphere can indent the surface of the cerebral hemisphere as this requires but slight force, but it cannot separate the arachnoid mem- brane from the dura mater sufficiently to escape down the sides of the cerebral hemisphere as this requires greater force. With the ingress of more blood the pool widens but it does not increase in depth, and the indentation of the cerebral hemisphere is consequently not great. The only source for bleeding into the sub-dural space with an intact arachnoid membrane, would be from a " bridging vein" connecting the cerebral veins with the veins within the dura mater. The veins could rupture from violent displacements of the cerebral hemispheres within the cranial chamber. There are scores of these veins connecting the superior border of the cerebral hemisphere with the superior longitudinal sinus, but these veins are so thick set that they form a " mesentery " suspending the superior border of the cerebral hemisphere to the dura mater which is unbroken in most head injury cases. Sub-dural haemor- rhage overlying the outer surface of a cerebral hemisphere, comes from the rupture of one of the many solitary veins passing from the convex surface of the cerebral hemisphere to the dura mater. Although rupture of a " bridging vein ' could occur either in the sub- dural space or in the sub-arachnoid space, as the vein traverses both spaces, rupture occurs only in the sub-dural space because of the much greater length of the vein within this compartment. The blood leaks at low pressure with an increase of flow during straining efforts. The pool of blood will eventually cover the greater part of the cerebral hemisphere, but as the deformation of the surface is slight, there are usually no localising signs of this haemorrhage. If localising signs are present they would be the same localising signs that occur with the extra dural clots overlying the convex surface of a cerebral hemisphere, but there will not be the march of symptoms going on to death, which occurs with extra dural haemorrhages. In most cases the evacuation of an acute sub-dural haemorrhage is incidental to the finding of tense blue dura mater at a surgical operation. Sub-dural blood under the inferior surfaces of the cerebral hemispheres Sub-dural blood which is partly clotted is not uncommonly found below the frontal lobes of the brain and at the temporal poles. There is 91 MILROY PAUL also a coat of sub-arachnoid blood at these sites and often a superficial laceration of the cortex of the brain as well, giving evidence of violent impact of the brain on the base of the skull. Although such an impact would not directly distract the very numerous bridging veins at the temporal pole and on the under surface of the frontal lobe, distraction might have occurred during a shearing movement of the brain following its impact downwards on to the base of the skull. This sub-dural blood extends later- ally till it reaches the dura mater on the side of the cranial chamber immediately above the bases of the anterior and middle fossae and it may be seen at this place during a surgical operation. These lesions do not manifest themselves by localising signs and the blue dura mater overlying such a haemorrhage will be exposed only if an exploratory hole happens to be made low down on the side of the skull at this place. Sub-dural blood from rupture of any of the numerous solitary veins between the under surface of the temporo-occipital lobe and the dura mater will be free to flow along the floor of the supra-tentorial compartment of the brain case. This blood is seen at autopsy around the occipital poles of the brain, but blood at this site is a gravitational effect occurring after the body was laid out. It does not indicate local injury to the occipital poles of the brain. Sub-dural blood never collects between the falx cerebri and the medial surfaces of the cerebral hemispheres Collections of sub-dural blood between the medial surfaces of the cerebral hemispheres and the falx cerebri have never been encountered either at a surgical operation or at an autopsy. Blood leaking into the sub-dural space at this site would flow down the vertical walls of this ravine on to the upper surface of the corpus callosum from where it would flow off to the base of the brain. Sub-dural blood in the posterior fossa Leary (1939) describing autopsy findings of sub-dural blood stated that " Subtentorial veins are often aberrant, but are not important from the standpoint of sub-dural haemorrhages, which are almost exclusively above the tentorium." These are in essence the views of all writers on head injuries, who do not even refer to haemorrhages at this place. Observations made on autopsies of head injuries in subjects of all ages, show that a considerable volume of blood fills the posterior fossa in every case in which sub-dural blood is found above the tentorium cerebelli. How has this obvious haemorrhage come to be overlooked by surgeons and pathologists ? So large a volume of blood in so vital a place must affect the condition of the patients and this haemorrhage merits close investigation. The blood in the posterior fossa bathes the cerebellum and the brain stem and it also fills the wide extension of the sub-dural space which 92 HAEMORRHAGES FROM HEAD INJURIES passes down from in front of the brain stem into the spinal canal in front of the spinal cord. Sub-dural blood in the posterior fossa is always fluid, and this accounts for the absence of distortions of the brain which would be produced if the blood had clotted in a part of the posterior fossa. What is the effect of this large volume of blood in the posterior fossa ? Does it compress the cerebellum and the brain stem, causing an increasing abolition of its functions? If it did so, this would be the lesion " par excellence " to determine the onset of the gradual rise in blood pressure, the slowing of the pulse which becomes fuller and stronger as it slows, and the change to Cheyne-Stokes respiration which were envisaged by Trotter as the reactions of the medulla oblongata to the increasing compression of an intracranial haemorrhage. Observations of cases which were found at autopsy to have a large volume of blood in the posterior fossa showed that the sequence of events postulated by Trotter had not occurred. The patients had been deeply unconscious with the stertorous respirations and the failing pulse of the patient dying of a severe head injury. There were no localising signs of blood in the posteror fossa. Would evacuation of sub-dural blood from the posterior fossa relieve the patient and perhaps determine recovery of a patient who would otherwise have died ? I put this matter to the test in one case. The making of a trephine hole through a small incision on one side of the middle line well below the superior curved lines of the occipital bone did not present much difficulty. Incision of the dura mater gave direct access at a dependent point to the sub-dural space of the posterior fossa. The case in which I performed this operation had no blood in the posterior fossa. At the subsequent autopsy it was established that he had no sub-dural blood in the posterior fossa. The operation was, however, proved to be feasible, and it could have emptied the posterior fossa of sub-dural blood. It does, however, introduce the risk ofintroducing sepsis into the posterior fossa, and I have not persuaded myself it was needed in the head injury cases I have had since then. Wthat happens to the blood in the sub-dural space if the patient survives the immediate effects of the injury ? What happens to the appreciable volumes of blood found in the posterior fossa and at the base of the supra-tentorial compartment of the cranial chamber if the patient survives the immediate effects of an injury ? Neither blood nor serum has ever been found either in the posterior fossa or below the inferior surfaces of the cerebral hemispheres several weeks or months after a head injury. Is this blood completely absorbed ? The evidence, meagre though it is, suggests that this is what happens, although the inert fibrous dura mater and the transparent arachnoid membrane are barriers across which absorption of blood would not be expected. Blood could be absorbed from new formed granulations in the sub-dural space, and perhaps this is how this blood is absorbed. The 93 8 MILROY PAUL only lesion in the sub-dural space which could be the sequel of an acute sub-dural haemorrhage is the sub-dural blood cyst, but these cysts are found only over the convex surfaces of the cerebral hemispheres. At other sites sub-dural blood must have been absorbed leaving not a trace behind. The sub-dural blood cysts The sub-dural blood cyst is a lesion of considerable surgical importance. The cyst is thin-walled and contains serum mixed with a variable amount of blood. It is sited in the sub-dural space between the inner surface of the dura mater and the outer surface of the arachnoid membrane, and once formed it continues to increase in size, covering a wider and wider area, and causing a deeper and deeper indentation on the surface of a cerebral hemisphere. The cyst goes on growing till death results from interference with brain functions. This sombre march of events is arrested, and the cavity of the cyst becomes completely obliterated by the simple expedient of evacuation of fluid from the cyst. These are truly remarkable features for any cyst. What are the factors which determine these features ? These cysts are only to be found over the convex surface of the cerebral hemispheres and this must be related to the circumstance that this is the only site in the sub-dural space where blood is walled in by apposition of a hollow on the surface of the brain against the dura mater. Retention of blood at this site will eventually cause sufficient clotting to wall the blood within a thin-walled neomembrane of organising clot. The progressive increase in the size of the cyst has been attributed to indrawing of fluid across the arachnoid membrane. The theory supposes that the osmotic pressure of the proteins in the plasma and serum draws in this fluid. Munro (1934) suggested that this osmotic pressure could be increased by breaking down of proteins into more numerous simpler products. The theory takes no note of the fact that although the arachnoid membrane is a thin transparent membrane, fluid has not been known to transude through it into the sub-dural space in any other pathological condition. The opportunity to examine this theory in the light of observations made on the fluid from a sub-dural cyst was taken in two of my cases. In the first case there was a clear history of an injury (fall from a bicycle) three months prior to the operation. Dr. N. G. Baptist, Reader in Biochemistry, University of Ceylon, reported that the fluid was definitely not whole blood, but accumulated fluid mixed with blood. It contained no free amino acids. The protein content was at the upper limit for normal serum. There were 3,280,000 red blood cells per cubic millimetre and the red cells were biconvex discs with no evidence of crenation. The fluid had not clotted when it was inspected six hours after removal from the cyst. The findings in the second case were substantially the same.* * Biochemical examinations were made by Dr. T. W. Wickremanayake, Lecturer in Biochemistry. 94 HAEMORRHAGES FROM HEAD INJURIES The evidence from these examinations establishes that fresh blood must have contributed to the fluid in the cyst, as the fresh looking red blood cells could not have been in the cyst for some months. The normal contour of these red blood cells established the osmotic pressure of the fluid as being within the limits of the osmotic pressure of normal blood, and the slight clotting showed that the blood in the cysts had been defibrinated. The theory that the serum proteins in the cyst fluid would break down to simpler products was discounted by the finding that there were no amino acids in the fluid. The fluid in the cyst was serum and to this serum was added fresh blood which had become defibrinated.

Fig. 8. Upper Diagram. Bleeding from a torn " bridging vein " into a sub-dural blood cyst. Lower Diagram. A " bridging vein " leading from a cerebral vein to a large venous sinus. The long course of the vein in the sub-dural space is shown. The increase in size of the cyst must have been from the flow of fresh blood into the cyst. The persistance of bleeding over a period of three months would be possible ifblood issuing from bleeding points flowed into the cyst fluid and clotted away from the orifices through which it had leaked (Fig. 8). The dramatic break in this cycle by the simple act of emptying the cyst of its fluid content would be due to the sealing of bleeding points by clotting and platelet deposition within the orifices of the blood vessels. 95 8-2 MILROY PAUL The causation of the clinical signs of a sub-dural blood cyst In most cases the sub-dural blood cyst declares itself by severe head- aches and vomiting, and examination often reveals papilloedema of the optic discs, usually more marked on the side of the cyst. These are the classical triad of symptoms and signs of a relatively slowly growing space occupying intracranial lesion, and this triad is accepted as evidence of a generalised raising of the intracranial pressures. In two of my cases of large sub-dural blood cysts, I recorded the pressure of the fluid in the unopened cysts at a surgical operation. The pressures were seven and eight centimetres of fluid respectively which would correspond to a pressure of only six millimetres of mercury. Here was a quite unexpected finding. In both cases, opening of the cyst wall and emptying it of fluid left the cavity as large as it was before, with the deeply indented cerebral hemisphere forming a bed for the now air-filled cyst. This air was shown by X-rays to have remained in the cyst for several days after the operation. The slow re-expansion of the brain was evidence that it had not been resisting the encroachment on the space by the cyst. Could a cyst containing fluid at only six millimetres of mercury pressure have caused a generalised raising of the intracranial pressures, and would not such a raised intracranial pressure have been communicated to the fluid in the cyst through its thin walls? The low intracystic pressure suggests that the time honoured triad of symptoms and signs of raised intracranial pressure might not be indicative of a generalised rise of intracranial pressure. The headache could be the result of stretching of the dura mater by the fluid within the cyst, and the vomiting could be a reflex set up by distortion and displacement of the cerebral hemisphere, but what of papilloedema? A raised intracranial pressure could not be transmitted through the optic nerve, and such pressures could not, therefore, affect the retinal vein within the optic nerve, as the trunk of this vein emerges from the optic nerve in the orbit. Papilloedema must, in the first instance, be determined by a seeping of cerebrospinal fluid along the interstices of the optic nerve. This fluid could secondarily compress the retinal veins within the optic nerve and cause an additional transudation of fluid into the optic discs. Is the seepage of cerebrospinal fluid indicative of a generalised raising of intracranial pressures? Might the seepage not be the result of localised damming of cerebrospinal fluid in the interpeduncular cistern from down- ward displacement of the cerebral hemisphere? The evidence of the sub- dural cyst cases suggest that this is likely. The blood exudes into a sub-dural blood cyst at negligible pressures, and raising of intracranial pressures would arrest such an ooze of blood altogether. Although sub-dural blood cysts manifest themselves by headache, vomiting and papilloedema of the optic discs, the deformation of the cerebral hemisphere that takes place is accomplished over such a long period of time that physiological adjustments often prevent the 96 HAEMORRHAGES FROM HEAD INJURIES development of those localising signs which are produced by an extra dural blood clot of the same bulk. When localising signs are present they would be similar to those of an extra dural blood clot, but in many cases such signs are conspicuous by their absence. Sub-arachnoid haemorrhage Sub-arachnoid haemorrhage is a common lesion in head injury cases. Blood leaking into the sub-arachnoid space clots in spite of its dilution with the cerebrospinal fluid, and the sulci of the brain are filled and the convolutions are thinly coated with red jelly clot. The clot covers wide areas of the brain, but it never accumulates to form a massive clot. Clots so thick as to conceal both sulci and convolutions are formed on the under surfaces of the frontal lobes and at the temporal poles, and there is often a superficial laceration of the cortex under these clots. The lesion at the site of these thick clots constitutes a bruise of the surface of the brain, which could only have resulted from a " contre coup " impact of the brain on the base of the skull. The blood must have come from bruising of the cerebral veins. What is the cause of the sub-arachnoid clot covering wide areas of the surface of the brain ? If the sites of sub-arachnoid bleeding are examined in the light of the hypothesis that the brain is driven away from the point of impact until it collides against the walls of the cranial chamber or against the dural septa within it, the surfaces showing sub-arachnoid bleeding are noted to be just those surfaces which would have been expected to have collided with the parietes. Working backwards, the surfaces showing sub-arachnoid bleeding indicate the direction in which the brain had been propelled within the cranial cavity by the impact. Could the sub-arachnoid haemorrhage be the result of the rupture of a vein, with carrying away of blood widely from the bleeding point by the cerebrospinal fluid before the blood clotted ? The uniformity of the films of sub-arachnoid blood over wide areas discounts this. The sub- arachnoid haemorrhage could result either from distraction of a cerebral surface from the dura mater or from collision of a cerebral surface against the dura mater. If a cerebral surface were distracted from the dura mater the only vessels which could rupture would be the " bridging veins.", The sub-arachnoid course of a " bridging vein " is less than a thirtieth part of its sub-dural course, and this gives dual fixation of the vein at its sub-arachnoid end which will prevent it from rupturing within the sub-arachnoid space. On the other hand, although collision of a cerebral surface against the dura mater would not rupture the cerebral veins, by stretching it could bruise them, and bruises would be more likely to affect all the veins of a surface rather than a single vein. The sub-arachnoid coat of blood is therefore a collision bruise. The coagulated films of sub-arachnoid blood give rise to no localising symptoms or signs, and it would be impossible to map these films from a 97 MILROY PAUL clinical examination of a patient. Although lumbar punctures can with- draw much blood mixed with cerebrospinal fluid from the sub-arachnoid space, it is evident that even repeated lumbar punctures could not remove the sheets of clotted blood coating the brain in the sub-arachnoid space. Blood in serous cavities causes pain and reflex muscle rigidity. It is remarkable that even when almost pure blood is withdrawn by lumbar puncture. there are none of the signs of meningeal irritation which are so evident when pus is found in the cerebrospinal fluid. Only one of my cases manifested such signs. A young boy who had fallen on to the back of his head had neck rigidity, abdominal rigidity, rigidity of the back and a positive Kernig's sign which persisted for several weeks during which time the blood withdrawn by repeated lumbar punctures changed from almost pure blood to clear cerebrospinal fluid. Intracranial haemorrhages in the new born The intracranial haemorrhages in the new born were examined at autopsies on infants who had died soon after birth. The earlier autopsies were made on infants who had manifested signs of cerebral disturbance before death, but later autopsies were on unselected cases as it was realised that severe intracranial haemorrhages could be present in infants who had not been noted to have signs of cerebral disturbance. An unexpected feature of the investigations was the finding of severe intracranial haemorrhages in infants who had had uneventful and un- assisted births from multiparous mothers. External examinations of the infants showed no injuries in cases with severe intracranial haemorrhages. A constant indication of the presence of intracranial haemorrhages was an extensive sheet of blood in the sub-epicranial space of the scalp. Cases with no blood in the sub-epicranial space proved to have no intracranial haemorrhages. If the sub-epicranial sheet of blood lay more on one side of the middle line the intracranial haemorrhages were more marked on this side.

Fig. 9. A tear at the junction of the falx cerebri with the tentorium cerebelli tearing the great cerebral vein of Galen. 98 HAEMORRHAGES FROM HEAD INJURIES

Fig. 10. Birth injuries. A tear in the tentorium cerebelli. None of the infants had blood in the extra dural space. The dura mater in the new born fuses with the fibrous tissue at the intersutural lines. Both dura mater and pericranium are welded together by fusion with the fibrous tissue of the intersutural lines. The dura mater cannot be stripped off the bone beyond the suture lines and an extra dural haemorrhage is not possible because of this. The meningeal c vessels lie on the outer layers of the dura mater as in the adult, but at the suture lines these vessels penetrate the fibrous tissue between the bones and then emerge on the dura mater which is below the next bone. Sub-dural blood showed through the dura mater as a blue discoloration. It was fluid blood and it overlay the greater part of a cerebral hemisphere, but did not depress the surface of the brain very much. The underlying convolutions and sulci of the brain were thinly covered by a film of sub- arachnoid coagulated blood. Blood was found bathing the occipital poles of the brain, but there was no sub-arachnoid film of blood at the occipital poles. This blood was proved to have gravitated here after the infant had been laid out, as infants laid out face downwards had blood bathing the frontal poles of the brain instead of the occipital poles. Sub-dural blood in the posterior fossa bathed the cerebellum and the brain stem without distorting their surfaces, and the blood usually almost filled the fossa. There were also sub-arachnoid films of blood on the vermis and the lobes of the cerebellum. Special care in dissection is needed to demonstrate tears in the dural septa. The tears were found at one of two sites. One site was at the origin of the free border of the falx cerebri from the tentorium cerebelli and this was usually associated with a rupture of the great cerebral vein of Galen (Fig. 9). The other site was a tear in the tentorial notch where the tentorium cerebelli passed on to the superior surface of the petrous part of the temporal bone (Fig. 10). Although a tear at this place did not open into a venous sinus the injury was associated with much sub-dural bleeding. 99 MILROY PAUL A review of these findings permits the mode of production of the intracranial haemorrhages of the new born to be worked out. The many cases in which the head was subjected to no force other than that incidental to its passage down the birth canal proved that the haemorrhages were the result of moulding of the head. Moulding causes elongation of the head in the long axis of the birth canal and the distortion of the vault consequent on this would distract the vault from the surface of the brain, and rupture the bridging veins, giving a sub-dural haemorrhage over the surface of a cerebral hemisphere. The distortion of the vault would pull the falx cerebri upwards and the falx cerebri would in turn pull the tentorium cerebelli upwards off the upper surface of the cerebellum disrupting the bridging veins beneath it and causing a sub-dural haemorrhage in the posterior fossa. The tears of the falx cerebri or of the tentorium cerebelli at their attachments is clearly the result of upward pull during moulding of the vault. The great cerebral vein of Galen is the largest bridging vein and its rupture causesa profuse sub-dural haemorrhage in the posterior fossa. The sub-arachnoid films of blood in the birth injury cases could not have resulted from collisions of the brain with the walls of the cranial chamber. The slow distortions of moulding would, however, have been corrected by rebound of the elastic brain case to its original contour, and this would have driven the vault and the raised tentorium cerebelli down on to underlying brain surfaces sufficiently forcibly to cause sub-arachnoid bruising. Could evacuation of blood save the lives of infants with severe intra- cranial haemorrhages '? The sub-dural blood in the superior compartment of the cranial chamber has been aspirated through the lateral angle of the anterior fontanelle by Ingraham and Heyl (1939) with restoration of altered brain functions to normal. Sub-dural blood in the posterior fossa has hitherto received no treatment. It could be evacuated by an opening through the occipital bone below the superior curved line which would give access to the sub-dural space of the posterior fossa. The thin films of coagulated sub-arachnoid blood could not be removed, and the films of blood are so thin they would probably not require removal. The infants investigated in this series had died too soon after birth to permit the planning of surgical operations for evacuation of blood. What would happen if an infant survived rupture of the great cerebral vein of Galen ? The infants should develop internal non-obstructive hydrocephalus. This question could be decided by examining the great cerebral vein of Galen at autopsies on children dying of non-obstructive internal hydrocephalus. The suggestion has been made that the intracranial haemorrhages of the new born are attributable to vitamin C deficiency (Ingalls, 1936). 100 HAEMORRHAGES FROM HEAD INJURIES The distribution of the haemorrhages found in the series of cases investi- gated in this paper, establishes that the intracranial haemorrhages of the new born are consequences of the moulding of the head during birth, and not the fortuitous oozing of blood from deficiency of vitamin C. ACKNOWLEDGMENTS ` It is a pleasure to acknowledge the constant help of my Clinical Research Assistant, Dr. B. N. D. Fernando, M.B., B.S., who designed the apparatus for transmitting hydrostatic pressures to the cranial cavity, to Dr. R. Kanagasuntheram, Ph.D., Lecturer in Anatomy for his dissections of the pericranium and dura mater of infants and for the histological slides of the meningeal vessels and of a " bridging vein," to Mr. G. Webster for the colour photographs illustrating my lecture and to Dr. George Ratnavale, Neurologist, General Hospital, Colombo, for two cases of sub-dural blood cysts which he referred for operation and for his skilled investigations of several of the cases of head injuries treated in my department. I am grateful to my teacher and former chief, Sir Cecil Wakeley, for arranging for my lecture to be published in the Annals in greater detail than was possible at its delivery and for his help and encouragement in the preparation and presentation of this paper. REFERENCES BELL, C. (1816) Surgical Observations, London, 1, 466. CUSHING, H. (1903) Amer. J. med. Sci., 125, 1017-1044. DEAN, H. P. (1896) in Treves System of Surgery, 2, 92. ERICHSEN, J. E. (1895) The Science and Art ofSurgery, 10th edition, London, Longmans. GILLINGHAM, J. (1954) Proc. Royi. Soc. Med., 47, 869-872. HANNAH, J. J. (1936) J. neri'. menit. Dis., 84, 169. HOLBOURN, A. H. S. (1943) Lancet, 2, 438. HOOPER, R. S. (1954) Brit. J. Surg., 42, 19-25. HUTCHINSON, J. (1897) Lond. Hosp. Rep., 4, 28. INGALLS, T. H. (1936) New Eng. J. Med., 215, 1279. INGRAHAM, F. D., and HEYL, H. L. (1939) J. Amer. med. Ass., 112, 198-204. JACOBSON, W. H. A. (1886) Hosp. Rep., 43, 147. JONES, F. W. (I1912) Lancet, Guy's2, 7. KAUMP, D. H., and LOVE, J. G. (1938) Surg. Gvn1ec. Obstet., 67, 87. LEARY, T. (1939) Arch. Path. (Chicago), 28, 808-820. MITTENZWEIG, H. (1889) Neurol. Zbl., 8, 193. MUNRO, D. (1934) New Eng. J. Med., 210, 1145. ROMANIS, W. H. C., and MITCHINER, P. H. (1952) The Scientce anid Practice of Surgery, 9th edition, London, Churchill. ROSE and CARLESS, see Wakeley. ROWBOTHAM, G. F. (1949) Acute inljluries of the head, 3rd edition, Edinburgh, Livingstone, p. 135. TROTTER, W. (1914) Brit. J. Surg., 2, 271-291. WAKELEY, SIR C. (1952) Rose and Carless Manlal of Surgery, 18th edition. London, Bailliere, Tindall and Cox.

SOCIETY OF APOTHECARIES OF LONDON ON TUESDAY, JULY 19th, at a Soir6e of the Society of Apothecaries, the Gold Medal for Medical Therapeutics was presented by the Master, Sir Cecil Wakeley, to Sir Russell Brock for his distinguished work on the surgery of the heart. 101