J Clin Pathol 1983;36:1335-1341

Subarachnoid haemorrhage due to upper cervicaltrauma

W ARTHUR HARLAND, JOHN F PITTS, ALAN A WATSON

From the Department of Forensic Medicine and Science, University of Glasgow, 8 Uniiversity Gardents,Glasgow G12 8QQ

SUMMARY Seventeen cases are reported in which fatal subarachnoid haemorrhage was associatedwith injury to the upper cervical region. Most of these cases were alcohol-intoxicated, most hadsustained their injuries in an altercation, and death was usually but not invariably rapid.

It is proposed that trauma to the upper cervical region can cause subarachnoid haemorrhage,by a mechanism involving tracking of blood into the subarachnoid space from a damaged ver-tebral artery or one of its branches.

Although the condition of spontaneous subarach-noid haemorrhage is well known, little attention haspreviousl-y been given in the literature to the distinctcondition of massive subarachnoid haemorrhagedue to trauma.The forensic implication of this condition is obvi-

ous: for example it can be difficult to state with cer-tainty whether subarachnoid haemorrhage found atnecropsy was the result of trauma, or coincidentalwith it. Moreover, a clinical application is suggestedby the fact that three of the cases survived longenough to be admitted to hospital for treatment.

Material and methods

A retrospective study was conducted on seventeencases of death due to subarachnoid haemorrhage,following immediately on trauma, seen between1972 and 1983. Post-mortem examination was car-ried out on these cases for legal purposes, andinvolved the staff of the Department of ForensicMedicine and Science at The University of Glasgow.Case histories were obtained from police reports.

In addition to routine post-mortem examinationprocedures, the upper cervical region was investi-gated in the following manner: the skin on the backof the neck was reflected from the level of the upperpart of the scapulae to the occipital region. This skinflap revealed the muscles on the posterior and lat-eral aspects of the neck, and these were examinedfor bruising. The muscle layers were then reflectedto reveal the deep muscles of the neck, such that

Accepted for publication 22 August 1983

contusional injury could be followed through thecervical structures, and a line of force inferred. Dis-section proceeded to reveal the upper cervical ver-tebrae and the extracranial portion of the vertebralarteries. The atlas vertebra was removed, fixed informalin and x-rayed. The vertebral arteries weretraced as far as the foramen magnum, and examinedfor surrounding haemorrhage. The vertebral andbasilar arteries were then removed for histologicalexamination. The site of maximal subarachnoidhaemorrhage was noted and the arteries constitutingthe Circle of Willis were carefully examined forlesions including aneurysms.

Case reports

CASE 4 (died 5.4.75)This 38-year-old man had been drinking since theearly evening. At 2315 h he became involved in afight outside the public house. He was punched andfell to the ground face down, when he was kickedtwice on the head, and lost consciousness. He wasmoribund on arrival at hospital at 2325 h butresponded to resuscitation and commenced regularspontaneous breathing at 0005 h. He remainedstable until 0130 h when seizures developed and hewas transferred to a neurosurgical unit. He showedfrequent left-sided seizures. The left pupil was largerthan the right, and did not react to light. Cheyne-Stokes respiration was present. An EMI scan wasnegative. Life was pronounced extinct at 1035 h.Post-mortem examination showed bruising on theleft eyelid, abrasions and lacerations on the leftupper lip, three dislodged teeth and a bruise behind

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the left ear. There was bruising of the scalp behindthe left ear, extending down 7 cm into the musclesbehind the angle of the left lower jaw. There washaemorrhage into the adventitia of the left vertebralartery, where it crossed the posterior arch of theatlas, which was not fractured. Extensive subarach-noid haemorrhage was found at the base of thebrain, extending over the vault bilaterally. Thearteries at the base of the brain showed no lesions.Blood was present in the ventricular system. Bloodand urine were negative for alcohol, but some ele-ven hours had elapsed since alcohol consumptionceased.

CASE 10 (died 14.8.78)This 45-year-old woman had been drinkingthroughout the day and she returned home verydrunk. At 2330 h her husband struck her once withhis right hand, and she hit her head as she fell. Thepolice arrived at 2340 h, noted a shallow pulse andheard the victim make gurgling sounds. She waspronounced dead at 2350 h. Post-mortem examina-tion showed a bruise on the forehead, an abrasionon the left side of the chin and an area of reddeningon the right side of the neck, measuring2.5 cm x 0-5 cm. There was bruising on theocciput and left upper neck, measuring2-5 cm x 2*0 cm. There was recent haemorrhagearound the intact left transverse process of the atlasand around the left vertebral artery. There was alarge subarachnoid haemorrhage at the base of thebrain with thin staining over the rest of the brain.The vessels of the Circle of Willis were thin-walledand healthy, and search revealed no lesions. Therewas blood in the ventricular system. Alcohol waspresent in a concentration of 290 mg per 100 ml ofblood, and 287 mg per 100 ml of urine.

Harland, Pitts, Watson

left vertebral artery close to the origin of the basilarartery.

In seven of the other cases death followed anassault by kicking. In case 6, bruising suggested thatthe victim was kicked in the frontal region, and noneck bruising was evident. Haemorrhage was seenaroutnd both vertebral arteries in conjunction withbasal subarachnoid haemorrhage. Cases 3, 4, 9, 11and 17 were punched to the ground, whereuponthey were kicked several times about the head andneck. All five showed bruising to the upper neckand/or parotid region, and in one case this was in theform of a rectangular patterned bruise suggestive ofa shoe sole. Four showed haemorrhage around theipsilateral vertebral artery, but case 3 was found tohave a 2 mm transverse tear of the basilar artery,just beyond the origin of the right superior cerebel-lar artery. Fig. 1 shows the surface injuries sustainedin case 12 who was kicked once in the upper neck,was found to have an abrasion behind the left ear,and was found on histology to have haemorrhagearound a moderately atheromatous left vertebralartery. This is the only one of our cases to showpre-existing pathology in the cerebral arteries onhistology.Two cases had been struck with blunt instruments

in the parotid region (cases 1 and 8). A 1-22 mlength of wood of section 2-5 cm x 2*5 cm and apoker had been used.

Finally, one of our cases, number 13, was knockedover a fence after being struck by a motorvehicle. This was the only one of our cases to havesustained a fracture to the transverse process of theatlas. A post-mortem radiograph (Fig. 2) demons-trated a bilateral congenital absence of the anteriorarch of the foramen transversarium and a fracture ofthe posterior arch of the foramen on the right.

Results

The 17 cases have been tabulated with regard toage, sex, trauma, estimated maximum survival time,relevant necropsy findings, and toxicology (Table 1).There was a male to female preponderance of 14:3.The mean age was 34 yr, with a range of 19-58 yr.The type of violence is shown in Table 2.

Seven of the cases were struck by hand. In case 15the husband of the deceased was witnessed slappingher about the head several times and in case 16 thevictim was punched twice. However, in the otherfive cases there was a clear account of a single blowbeing struck, ranging in severity from the punch ofan ex-boxer to the blow of a drunken woman. Case14 had injuries about the left ear suggestive of a

blow from a fist, and a skin mark consistent with herhusband's ring; she was found to have a tear of the

SURVIVAL TIME

All estimates of the time elapsing between theassault and death in the series are maxima. Forexample, in case 5 the victim was left overnight andwas found to be dead the following morning, somenine hours later. In only one of our cases (No 8) hasno attempt been made to estimate the survival time,as the body of the deceased was only found 7 daysafter her death. The results for the remaining 16cases are given in Table I and summarised in Table3.The longest survivor was case 9, who lost con-

sciousness six hours after the assault and was main-tained on artificial ventilation for 39 h thereafter.However, the patient showed signs of brain deathshortly after losing consciousness.

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Subarachnoid haemorrhage due to upper cervical trauma

Table I Trauma, survival time, necropsy findings and toxicological results in 17 cases of subarachnoidhaemorrhage due to upper cervical trauma

Case Age Sex Traumatic history Survival Necropsy findings Blood alcohol(yr) time [urine alcohol]

(mgOl00 ml)

1 38 M Four kicks to head. Blow 40 min Abrasions and bruising around R ear. Haem around 280to neck with length of wood R TP of Cl and R VA Basal SAH

2 43 M Punched on side of chin 40 min Swelling angle of R jaw and neck. Haem around 200R TP of Cl and R VA Basal SAH [255]

3 23 M Kicked and punched on 15 min Bruise of helix L ear. Laceration to mouth. 250face and head 2 mm tear in basilar artery at R superior cerebellar [315]

artery. Basal SAH4 38 M Punched to ground. Two 11 h 20 min Bruise behind L ear. Haem into and around L VA Negative

kicks to head over Cl Basal SAH5 36 M Struck on face by hand <9 h Abrasions L ear. Bruising muscles of L posterolateral 238

neck. Haem around L TP of Cl and L VA Basal SAH [417]6 23 M Struck above left ear 40 min Bruise L forehead. No neck bruising. Blood around 142

both VA's Basal SAH [194]7 20 M Single punch to right side 12 min Bruising R neck. Haem around R TP of Cl and Negative

of neck R VA Basal SAH8 50 F Struck with poker ? Bruising behind L ear. Haem in soft tissues of left Negative

side of neck up to foramen magnum Basal SAH9 19 XI Punched to ground. 45 h Bruise behind L ear. Haem around L TP Cl and Negative

Kicked on head. L VA. Basal SAH10 45 F Struck once by hand 20 min Reddening R side of neck. Haem around L TP of 290

Cl and L VA. Basal SAH [287]11 31 NI Punched to ground: kicked 1O min Bruising L neck, and muscles down to spine. Haem 256

at least twice around L TP of Cl and VA. Basal SAH [337]1 2 58 M Kicked on neck once 30 min Abrasion behind L ear. Haem around L TP of Cl 193

and L VA. VAs + BA atheromatous Basal SAH [294]13 26 M Struck by vehicle and 35 min Bruise and swelling below R ear. Haem into muscle Negative

knocked over fence on R side of neck. Fracture R TP of Cl Basal SAH.Fracture R sphenoid bone

14 53 M Struck once on face 30 min Bruising & abrasion around L ear. Torn R VA at 214BA Basal SAH [278]

15 29 F Struck by hand 15 min Three bruises L upper neck. Bruising in deep muscle 162over L TP of Cl. Haem around L VA. Basal SAH [197]

16 19 M Punched twice on head 4 h Bruising and abrasion of R ear. Haem around R TP 76of Cl and R VA. Basal SAH [1331

17 31 M Punched and kicked 1 h 15 min Multiple superficial injuries to face bruise anterior to 262repeatedly R ear. Haem around R TP of Cl and R VA. Basal SAH[300]

TP = transverse processCl = first cervical vertebraVA = vertebral arteryBA = basilar arteryHaem= haemorrhageSAH subarachnoid haemorrhage

Table 2 Type of violenice in 17 cases of subarachnoidhaetnorrhage due to upper cervical trauma

No of cases Trawna7 Kicked7 Struck by hand2 Struck by blunt instrument

I Struck by motor vehicle

Table 3 Survival time in 16 cases of subarachnoidhaemorrhage due to upper cervical trauma

Survival time No of cases

0-30 min 730-60 min 460 min-12 h 412-48 h 1

TOXICOLOGY

All 17 cases were assayed for alcohol in blood, and16 for alcohol in urine. These were negative in fivecases, two of whom were known to have been drink-ing, but survived long enough to metabolise largeamounts of alcohol. Three of our cases had not beendrinking. For the remaining cases the mean valueswere: blood alcohol = 213 mg/l00 ml (range =76-290 mg/100 ml) and urine alcohol = 275 mg/100 ml (range = 133-417 mg/100 ml).

DISCUSSION

The condition described in this paper has generallybeen referred to as "traumatic subarachnoidhaemorrhage". Although well established, we feelthat this term is somewhat misleading, as it is com-

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Fig. 1 Photograph of the left upper neck in case 12,showing the typical external injury seen in cases ofsubarachnoid haemorrhage due to upper cervical trauma.

Fig. 2 Post-mortem radiographofthe first cervical vertebra fromcase 13, demonstrating acongenital defect in each transverseprocess and a fracture in the righttransverse process.

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mon knowledge that subarachnoid haemorrhage isfrequently seen following head injuries such as aresustained in road traffic accidents. In these cases thehaemorrhage is diffuse and thin, arising fromsuperficial cortical vessels, and is often associatedwith cerebral contusions. There may also be associ-ated subdural haemorrhage or cerebral lacerations.'It is clear that we are discussing quite a differentcondition, in which fatal massive basal subarachnoidhaemorrhage results from a discrete injury and isfound in isolation from other meningealhaematomata and cerebral injuries. We suggest thatthe term "traumatic subarachnoid haemorrhage" berestricted to this entity, as opposed to the non-

specific condition.

DEGREE OF TRAUMA

From our results, it is clear that subarachnoidhaemorrhage can result from a relatively minordegree of trauma. In the present series, only one

showed a fracture of transverse process of the atlas(case 13). This victim was subjected to the severetrauma of collision with a motor vehicle, and waspredisposed to fracture by a congenital defect in thetransverse processes of his atlas. In the remainingcases fractures were not demonstrated, indicatingthat fracture of the transverse process of the firstcervical vertebra is by no means an essential featureof the syndrome. The degree of trauma in 14 of our17 cases was only moderate, in that it was the resultof the impulse generated by an unarmed person inan assault. In our view, it is the accuracy rather thanthe sheer magnitude of the traumatic force that iscritical. In short, subarachnoid haemorrhage may

result when a relatively minor force is "on target" atthe correct angle in the region of the transverse pro-cess of the atlas.

Simonsen2 states that the trauma need not be par-ticularly great, and he considers injuries at the levelof the base of the skull particularly apt to producethis condition-such a site was found in 725% of hiscases. All of the cases described by Contostavlos3had been involved in physical encounters with anunarmed person, which were severe enough to frac-ture the tips of their transverse processes by directinjury; in addition, two of them had suffered man-

dibular fractures. Cameron and Mant4 are in accordthat trauma need only be minor: of their four cases,two were punched in the neck, one was struck withthe open hand, and one kicked. In Simonsen's twolater cases blows were struck with the fist and, afterdefleshing the atlas, fissures were found in onetransverse process.5

MECHANISM OF HAEMORRHAGE

It can be seen from our data (Table 3) that deathfrom subarachnoid haemorrhage due to trauma isusually very rapid. 69% of our cases died within onehour of injury, and not one case survived longerthan 48 h. The range of survival times was 10 min to45 h. Death was almost immediate in most reportedcases,34 with the longest survival time being 18 day-s.s

Nevertheless, the mechanism whereby trauma tothe upper neck produces subarachnoid haemorrhageis unclear. There are several hypotheses that mayexplain this condition:(a) The blunt force incident on the neck may be

transmitted to the vertebral artery where it isfirmly fixed by the foramen transversarium ofthe atlas, resulting in a shearing force causingrupture of the vessel wall, either within or out-side the skull.

(b) Alternatively, the same effect may result fromcompression of the vertebral artery against thecrescentic lower border of the posterioratlanto-occipital membrane, with tearing ofthe artery or one or more of its small branches.

When the tear is extracranial, there are two routesby which blood may then reach the subarachnoidspace:(i) By dissecting upwards in and around the arter-

ial wall to reach the subarachnoid space wherethe vertebral artery passes through the foramenmagnum. In 15 of our 17 cases (88%) there washaemorrhage around the vertebral artery,which clearly extended upwards from the trans-verse process of the atlas to the foramen mag-num. These necropsy findings tend to stronglysupport Contostavlos' view that blunt trauma tothe vertebral artery causes disruption of thetunica, with consequent dissection into the sub-arachnoid space.3

(ii) By tracking from the site of injury through theintervertebral foramina into the subarachnoidspace of the upper cervical spine. The extrac-ranial portion of the vertebral artery does infact give off some small branches which passthrough the intervertebral foramina to anas-tomose with the anterior spinal arteries in thespinal canal. In the longer surviving cases thehaemorrhage may have occurred from one ofthese spinal branches rather than the mainarterial trunk. Another possible explanation isthat in these cases the site of haemorrhage isthe vertebral venous plexus, which runs withthe artery throughout the formina transver-saria of the upper six cervical vertebrae.

(c) The trauma applied to the upper neck may

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1340somehow cause rupture of the intracranial partof the vertebrobasilar arterial system. In two ofour 17 cases (12%) there was no haemorrhagearound the extracranial part of the vertebralartery, but the sites of rupture were positivelyidentified within the subarachnoid space. Thesewere a tear in the basilar artery in case 3, and a

tear in the intracranial portion of the vertebralartery in case 14. Simonsen concentrated atten-tion on the basilar artery. In 75 cases oftraumatic subarachnoid haemorrhage he found28% associated with pathological changes inthe artery, compared with 73% in the compari-son group of 341 cases of spontaneous sub-arachnoid haemorrhage.2 Only one of our casesshowed pre-existing arterial pathology, in theform of moderate atheroma, despite a carefulsearch for lesions such as aneurysms by bothgross examination and histology.

In summary, the evidence in our series favours theview that, in the majority of cases, haemorrhageoriginates from the extracranial portion of the ver-

tebral artery. However, the actual site of rupture isdifficult to demonstrate. It is likely that in a minorityof cases the site of rupture is intracranial. The avail-able evidence indicates that such haemorrhage can

occur in previously healthy arteries.

TOXICOLOGY

In our series, the deceased was not intoxicated inonly three cases. The remaining 14 were known tohave been drinking, and the mean blood alcohol inthose cases where this is applicable was 213 mg per100 ml.Simonsen2 found that 87% of his 75 cases of

traumatic subarachnoid haemorrhage were underthe influence of alcohol, compared with only 9.7%of 145 cases of spontaneous haemorrhage whereblood alcohol was measured. He considers alcoholto have a dual role: primarily the local dilating effecton the cerebral vessels, rendering them more likelyto rupture, and also "as alcohol-intoxicated persons

fall more heavily and have less appropriate avoidingreactions than have sober persons. This increasesthe possibility of head injuries during fights". Allthree of Contostavlos' cases were heavily intoxi-cated,3 but the author makes no comment on therole of alcohol. Cameron and Mant4 found highblood alcohol concentrations in two of their fourcases, and stated that alcohol is an important con-tributory factor. They do not comment on the factthat two of their cases were not drinking at the timeof their haemorrhages.

While recognising the role of alcohol at an anec-

dotal level, we regard this as the most controversial

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area in the syndrome. Firstly, Simonsen2 omits topoint out that alcohol is significantly associated withhomicide in general. Persons intoxicated withalcohol are far more readily involved in fights, and itmay well be that the "less appropriate avoiding reac-tions" are relevant not only to the fact that drunkenpersons do not avoid the fight in the first place. Wehave seen cases in the literature and in our ownexperience where subarachnoid haemorrhage as aresult of upper cervical trauma occurred entirely inthe absence of alcohol. This is not to say that alcoholdoes not predispose, only to suggest that the predis-position is largely due to its effect in evoking aggres-sive tendencies in human behaviour. Nevertheless, itmay well be that alcohol does have a pharmacologi-cal role in the production of the subarachnoidhaemorrhage. Hillborne and Kaste6 carried out astudy on 75 cases of aneurysmal subarachnoidhaemorrhage in patients aged 15-55 yr, and foundthat the bleeding was preceded within 24 h by a boutof alcohol drinking in 25% of cases. They concludedthat occasional alcohol intoxication carries anincreased risk of aneurysmal subarachnoid haemor-rhage. Unfortunately for our purpose, patients whodied within the first 24 h without regaining con-sciousness were excluded from that study. A poss-ible mechanism is suggested by the work of Barryand Scott,7 who found that vasospasm in the cat basi-lar artery, produced by administration of the ani-mal's fresh blood to the artery, was of markedlyreduced intensity and duration after intravenousinfusion of 5% ethanol. These effects were unre-lated to changes in blood pressure. This suggeststhat the rapidity ofdeath in our cases may have beencontributed to by alcoholic inhibition of the spasmafter damage to the artery.

Conclusion

Fatal subarachnoid haemorrhage should be sus-pected to be traumatic in aetiology when injuries areseen on the ear, in the parotid region or on theupper neck. However, we have seen cases in whichthe external signs of injury are atypical; in such casesthe true cause of the subarachnoid haemorrhage willonly become apparent if the pathologist has a highindex of suspicion and dissects the upper extracra-nial portion of the vertebral arteries. Such dissectionusually reveals bruising in the deep muscles of theneck, with haemorrhage around the vertebral arteryand the transverse process of the first cervical ver-tebra. In our experience, fracture of the process is anunusual finding, indicating a particularly severedegree of trauma. Alcoholic intoxication is a fre-quent, but not an essential part of the syndrome.The mechanism of haemorrhage is still obscure, and

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in our opinion there may well be more than onemechanism involved. It is obviously important toestablish the exact source of haemorrhage in futurecases, and vertebral artery angiography probablyholds the greatest promise for research.

We wish to thank Dr MM Butt of the Department ofAnatomy, The University of Glasgow, for usefuldiscussion on the regional anatomy of the vertebralarteries.

References

'Bakay L, Glasauer F. Intracranial haemorrhage. In: Head injuryBoston: Little, Brown & Co, 1980.

2 Simonsen J. Fatal subarachnoid haemorrhage in relation tominor head injuries. J Forensic Med 1967;14: 146-55.

Contostavlos DL. Massive subarachnoid haemorrhage due tolaceration of the vertebral artery associated with fracture ofthe transverse process of the atlas. J Forensic Sci1971;16:40-56.

4 Cameron J, Mant K. Fatal subarachnoid haemorrhage associatedwith cervical trauma Med Sci Law 1982;12:66-70.

Simonsen J. Massive subarachnoid haemorrhage and fracture ofthe transverse process of the atlas. Med Sci Law 1976;16:13-16.

6 Hillborne M, Kaste M. Does alcohol precipitate aneurysmal sub-arachnoid haemorrhage? J Neurol Neurosurg Psychiatry1981;44:523-6.

7 Barry K, Scott M. Effect of intravenous ethanol on cerebral vas-ospasm produced by subarachnoid blood. Stroke1980;10:535-7.

Requests for reprints to: Professor WA Harland, Depart-ment of Forensic Medicine and Science, University ofGlasgow, 8 University Gardens, Glasgow G12 8QQ, Scot-land

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