ORIGINAL ARTICLE

Non-Traumatic Acute Subdural Hemorrhage Due To Cranial Venous

Hypertension
Matthew M. Orde

ABSTRACT
Acute subdural hemorrhage is typically associated with a history of head trauma, and as such it is a finding with significant potential
medicolegal consequences. In this article, 37 adult and post-infantile pediatric sudden death autopsy cases with small volume (“thin film”
or “smear”) acute subdural hemorrhage are presented—in which there is either no further evidence of head trauma or only features of
minor head injury. The possible underlying pathophysiological mechanisms are explored, and it is concluded that a common thread in
many of these cases is likely to have been cranial venous hypertension at around the time of death. These findings may have implications
in instances where small volume subdural hemorrhage is identified in the absence of other evidence of significant head injury. Acad
Forensic Pathol. 2019 9(1-2): 33-43

AUTHOR
Matthew M. Orde MBChB FRCPath FRCPA DMJ (Path) Dip For Med (SA) MFFLM LLDip PgDLS, Forensic Pathology, Vancouver
General Hospital
Roles: Project conception and/or design, data acquisition, analysis and/or interpretation, manuscript creation and/or revision, approved final version for publication,
accountable for all aspects of the work, principal investigator of the current study.

CORRESPONDENCE
Matthew M. Orde MBChB FRCPath FRCPA, 855 West 12th Avenue, Vancouver BC, [email protected]
ETHICAL APPROVAL
As per Journal Policies, ethical approval was not required for this manuscript
STATEMENT OF HUMAN AND ANIMAL RIGHTS
This article does not contain any studies conducted with animals or on living human subjects
STATEMENT OF INFORMED CONSENT
No identifiable personal data were presented in this manuscript
DISCLOSURES & DECLARATION OF CONFLICTS OF INTEREST
The author, reviewers, editors, and publication staff do not report any relevant conflicts of interest
FINANCIAL DISCLOSURE
The author has indicated that he does not have financial relationships to disclose that are relevant to this manuscript
KEYWORDS
Forensic pathology, Neuropathology, Subdural hemorrhage, Etiology, Nontraumatic
INFORMATION
ACADEMIC FORENSIC PATHOLOGY: THE PUBLICATION OF THE NATIONAL ASSOCIATION OF MEDICAL EXAMINERS FOUNDATION
©2019 The Author • (ISSN: 1925-3621) • https://doi.org/10.1177/1925362119851114
Submitted for consideration on 1 Oct 2018. Accepted for publication on 24 Nov 2018

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 ORIGINAL ARTICLE
INTRODUCTION curred during or after pregnancy in circumstances
that might reasonably be attributable to pregnancy; or
Intracranial acute subdural hemorrhage is typically when the death occurred while the deceased was in
associated with trauma (1-3). Indeed, the association custody (10). Approximately 500 to 600 autopsies are
is considered to be so strong that when subdural hem- conducted annually at this institution.
orrhage is encountered at autopsy, many practitioners
will readily attribute the bleeding to trauma when they Electronic autopsy report files in the Vancouver Gen-
fail to identify another potential cause—even in the eral Hospital Pathology Department database were
absence of other positive markers of head injury. searched using standard Microsoft Word (2003) tools
for “subdural hemorrhage/haemorrhage” and “subdu-
In cases with a documented history of trauma, the sub- ral hematoma/haematoma.” Cases were included in
dural hemorrhage will typically be of large volume the study if the hemorrhage was described as being
and pose a risk of mass effect with elevation of intra- acute and of small volume—typically described as ei-
cranial pressure, particularly when paired with brain ther a “film,” “thin film,” or “smear.” Cases were ex-
swelling. However, in other instances, the subdural cluded if one or more of the following criteria applied:
hemorrhage encountered is of much smaller volume (a) the deceased was younger than five years (primar-
and is often described as forming only a “thin film” or ily due to the paucity of infant autopsy cases at this
a “smear” of blood over the surface of the brain. The institution; but also because the mechanism of hem-
smaller volume in such cases might of course be ex- orrhage in this age-group is notoriously contentious
plained by there having been only a short time interval and potentially different from that operative in older
between injury and death, insufficient to permit the age groups), (b) there were changes of more than early
accumulation of a significant volume of blood, but on decomposition, (c) there were features of more than
occasion, it may be that different mechanisms come minor recent head trauma (not including the subdu-
into play—a somewhat contentious area in pediatric ral hemorrhage) (minor head trauma in this context
(infant) neuropathology in particular (4-9). is defined to include localized facial/scalp abrasions,
contusions, or superficial lacerations, but to exclude
In this article, the potential pathophysiological mech- cases with deep facial/scalp lacerations or fracturing
anisms of thin film acute subdural hemorrhage in 37 of the skull or facial skeleton), (d) there was a his-
sudden death autopsy cases performed on adults and tory of sizeable acceleration/deceleration forces, such
children older than five years—in which there is either as road traffic incidents and falls from height, or (e)
no further evidence of head trauma or only features of there was evidence of a hemorrhagic diathesis, either
minor head injury—are explored. congenital or acquired, or the presence of a risk factor
for a bleeding disorder—such as hepatic cirrhosis.
MATERIALS AND METHODS
The following gross postmortem data were obtained
A retrospective study examining coronial (medicole- from the autopsy report in each case: age, sex, circum-
gal) and noncoronial consented (“hospital”) autopsy stances surrounding death, other significant medical
cases performed at the Vancouver General Hospital, history, whether or not chest compressions were per-
British Columbia, Canada from January 1, 2011, to formed as part of attempted resuscitation, the postmor-
July 1, 2018. Autopsies performed under the auspices tem interval prior to autopsy, documented features of
of the British Columbian coronial legislation include decomposition, laterality of the subdural hemorrhage,
deaths which were sudden and unexpected, and where whether or not there were features of established brain
the cause of death was hitherto unknown; where the swelling, toxicology results, the cause of death as pro-
cause of death was the result of violence, accident, vided by the autopsy pathologist, and other significant
negligence, misconduct, or malpractice; the result of postmortem findings, with particular emphasis on
a self-inflicted illness or injury; when the death oc- craniocervical hemorrhage and features of injury.

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Ethical clearance for the study was granted by the subdural hemorrhage was bilateral in 19 cases and
Clinical Research Ethics Board of the University of unilateral in 18. In almost every instance, the brain
British Columbia (ref: H17-02323). Each case was in- and/or cerebral vessels were noted to appear congest-
dexed with reference to the institutional case number ed—either as described in the written report or evi-
only in order to ensure anonymity. dent in postmortem images. Features of brain swelling
were identified in four cases, though in no cases did
RESULTS this appear pronounced. None of the cases included in
this study showed either gross or microscopic features
Thirty-seven autopsy cases of thin film/smear subdu- of chronic subdural hemorrhage. Microscopic assess-
ral hemorrhage were identified during the period Jan- ment of the brain revealed scattered petechial hemor-
uary 2011 to July 2018 (Table 1). The age range was rhages within the brain parenchyma in two instances,
seven to 70 years, with a mean of 36.6 years (stan- and focal microscopic cortical hemorrhages in anoth-
dard deviation [SD]: 2.2). The sex distribution was er, but—other than congestive features—no further
25 male/12 female. All were cases of sudden death, significant cerebral pathology was identified. In the
without a protracted prodrome or hospitalization pri- two cases in which sections of dura were sampled
or to death. As per the study inclusion criteria set out for histological assessment, the dura also appeared
previously, all cases were without evidence—either as congested and adjacent hemorrhage was confirmed,
suggested by the history or postmortem findings—of but no further dural pathology was noted. In none of
more than minor recent head trauma (not including the cases was the source of subdural blood positively
the subdural hemorrhage). None showed features of identified. See Images 1 and 2 which show typical
disseminated intravascular coagulation or other hem- examples.
orrhagic diathesis. The known or estimated postmor-
tem interval prior to autopsy ranged from one to 13 In addition to these 37 cases, it is of potential rele-
days, with a mean of 5.7 days (SD: 0.5). vance that a further case with unilateral thin film acute
subdural hemorrhage was also identified—a 33-year-
All of the autopsies included in this study had been old male who died during forcible restraint by law
undertaken by accredited forensic pathologists, and enforcement personnel, it seems being held down in
the large majority had photographs taken at the time of a prone position at the time of his death. Autopsy find-
examination. The brain was retained for formal neu- ings in this case included fracturing of the laryngeal
ropathologic assessment after fixation in 16 of these skeleton, with adjacent hemorrhage, and there were
37 cases. Histological examination of all the major also features of significant head injuries—including a
organs—including the brain—was undertaken in each fairly deep scalp laceration, multifocal facial bruising,
and every case, but sections of dura were examined and a “blowout” type orbital fracture. Primarily as a
in only two instances. Toxicological analyses were result of ongoing uncertainty regarding the precise se-
performed on all 37 cases. In no cases were radiolog- quence of events leading up to his death, the cause of
ical studies undertaken either shortly prior to death or death in this individual was considered unascertained
postmortem prior to autopsy. but likely multifactorial, with possible contributory
factors including chest compression, compression of
In every case which had been photographed, the hem- the neck structures, and excited delirium. As a result
orrhage was evident while the brain was still in-situ, of the head injuries, the case was deemed to fall out-
with the hemispheric dura incised laterally and re- side the study inclusion criteria.
flected upwards, and appeared as a thin film of blood
over the cerebrum, most likely with a volume of a few DISCUSSION
milliliters at most. The subdural hemorrhage typical-
ly involved the mid to posterior parasagittal regions Intracranial acute subdural hemorrhage—that is,
overlying the cerebral hemispheric convexities. The bleeding into the potential space between the dura ma-

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Table 1: Study Data
Circumstances surrounding death and scene Quantity Notes
findings (n = 37)

Found dead in ‘benign’ circumstances, without 21

obvious cause prior to autopsy
Witnessed or suspected seizure event 5

Suspicious for assault 2

Witnessed collapse 1
Found in open water, possibly drowned 2

Ligature strangulation 1
Found submerged in bathtub 2

Pinned under heavy load 1

Found wedged in open window 1

Found dead in house fire 1

Resuscitative chest compressions performed 13

Changes of early decomposition 3

Features of minor recent head injury 13 Two of whom also had signs of significant recent trauma elsewhere to the body
Primary underlying cause of death, as determined after autopsy, microscopy, and following consideration of the results of ancillary studies as applicable
(n = 37)
Acute drug/alcohol toxicity 12 Three opioids and alcohol
Two cocaine and opioids
Two alcohol and benzodiazepines
One cocaine
One methamphetamine
One opioid, cocaine, and methamphetamine
One opioids
One clozapine

Natural extracranial cardiovascular disease 5 One with acute toxic effects of methamphetamine considered contributory to death

Seizure disorder 5 One suspected stemming from drug/alcohol withdrawal

Neck compression 4

Drowning 3

Smoke inhalation 1
Alcohol-withdrawal syndrome 1

Drug (likely cocaine)-related acute-on-chronic heart 1 This case in addition to the other cases in which cocaine was detected
disease, contributed to by acute cocaine toxicity
Positional asphyxia 1
Traumatic (crush) asphyxia 1

Undetermined 3 One queried due to either

(a) acute mixed drug toxicity [including opioids and amphetamine],
(b) ‘asphyxia’ by way of smothering or neck compression, or
(c) drowning;
One queried due to asphyxia, with a band-like mark noted around the lower chest/
upper bdomen;
One queried due to seizure disorder
Other relevant observations
Petechiae identified within brain parenchyma, 3 Two cases with evidence of neck compression, and 1 case of acute clozapine
thought not due to direct trauma toxicity

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ter and the arachnoid mater surrounding the brain or, as ruptured aneurysms, vascular malformations, and
to be more anatomically precise, within the plane of intracerebral bleeds. Some researchers, notably in the
weakness within the inner dural border layer (11)—is field of infantile neuropathology, have also suggest-
typically associated with traumatic head injury (1-3). ed that blood may ooze directly from the dura in the
In the majority of instances of traumatic acute subdu- setting of the combination of hypoxic brain damage,
ral hemorrhage, the forces involved are sizeable, at brain swelling, and elevated central venous pressure
least in the young and physically robust, with typi- (5-7, 9, 18)—though this is not without controversy.
cal scenarios including motor vehicle accidents, falls,
assaults, sporting events, and industrial accidents The source of the blood in most instances of traumat-
(12). However, other nontraumatic causes have been ic, or presumed traumatic, subdural hemorrhage has
described, including neoplasia (13), sepsis (14), co- traditionally been attributed to torn bridging veins
agulation disorders (15, 16), high altitude (17), intra- traversing from cerebral cortex to dural sinus, or on
cranial hypotension (13), and of course extension of occasion direct injury to the brain substance—but a
hemorrhage from another intracranial source—such definitive site of bleeding is frequently not identified

Image 1: A typical case showing a thin film of subdural blood over the cerebral hemispheric convexity and prominent cerebral vascular
congestion.

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 ORIGINAL ARTICLE
(2). In these traumatic cases, the subdural hemorrhage type acute subdural hemorrhage encountered in in-
will typically be of large volume, unilateral, and pose stances of traumatic head injury.
a risk of mass effect with associated elevation of the
intracranial pressure, particularly when coupled with One common theme that emerges in many of these
brain swelling. cases is the possibility of venous hypertension in ves-
sels draining the head and neck region, which could
These 37 adult and post-infantile children sudden have developed by way of a variety of mechanisms—
death cases—none of whom had further evidence either stemming from direct pressure gradients or
of significant recent injury to the head region, ei- consequent upon impaired venous return to the heart.
ther from the history or postmortem findings—were Those cases involving compression of the neck or tor-
found at autopsy to have small volume (“thin film” or so can of course be readily seen to have the potential
“smear”) acute subdural hemorrhage. These findings for direct impairment of cranial venous outflow or ve-
are thought to be suggestive of a nontraumatic causal nous return to the heart. A Valsalva-type mechanism
mechanism of accumulation of the blood in the sub- may be operative in seizure-associated apnea or breath
dural space, distinct from the usual space-occupying holding in instances of drowning and smoke inhala-

Image 2: A case of quite localized and minor subdural hemorrhage. Note the characteristic distribution over the mid-posterior parasagit-
tal cerebral hemispheric convexity. Vascular congestion again evident.

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tion (19-22); a similar mechanism has been invoked bral hemorrhages in two of the cases involving com-
by others in instances of subdural hemorrhage asso- pression of the neck structures—an observation that
ciated with paroxysmal coughing (23,24). Indepen- has previously been reported by others in instances of
dent autonomic effects may additionally be a factor traumatic (crush) asphyxia (27).
in cases where terminal seizures are suspected (25).
It is also conceivable that acute drug toxicity might The lack of a protracted survival period in any of these
play a part in the development of acute cranial venous cases would likely weigh against the possibility that
engorgement in the period leading up to death, par- hypoxic damage to the tissues might have been a sig-
ticularly in instances involving stimulant drug usage nificant factor in the origin of hemorrhage, in these
with associated excitatory cardiovascular effects. The cases at least—a mechanism that has previously been
mechanisms that may be at play in deaths attributed to put forward by others (5, 9, 28).
the acute toxic effects of opioids and other nonstimula-
tory drugs remain obscure, but in the author’s personal This venous hypertension hypothesis in the formation
experience profound congestion of the head and upper of acute subdural hemorrhage would of course also
torso in such instances is a common finding, perhaps provide a ready explanation for the hemorrhage being
reflecting a terminal Valsalva-type mechanism and/or of only small volume—namely, developing as an ooze
agonal and postmortem positioning, and it is speculat- from engorged venous channels, in contrast to flow of
ed whether such a mechanism may be a factor in these blood from a frank vascular tear as is thought to be
cases. While there is no obvious causal mechanism for the case in most instances of typical space-occupying,
the subdural hemorrhage in the deaths attributed to trauma-related subdural hemorrhage.
natural cardiovascular causes captured by this study,
similar mechanisms may well be operative. There is scarce prior mention of this proposed mech-
anism of subdural hemorrhage in the published litera-
It is proposed that cranial venous hypertension, when ture. However, it is notable that, shortly after the turn
pronounced, can result in seepage of blood from en- of the twentieth century, Cushing observed that sub-
gorged intracranial, possibly peridural or dural-based, dural hemorrhage “may occur when too great strain
vascular channels—perhaps too small to be appreci- has been put upon the vessels by the profound ve-
ated with the naked eye or upon routine histological nous stasis of postpartum asphyxiation; just as in later
assessment (though interestingly, in a recent study months they may rupture under the passive conges-
involving a small number of infantile “triad” cases, tion brought about by a paroxysm of whooping-cough
three of which had no further features of head trau- or a severe convulsion” (29). In addition, Spitz and
ma, it is reported that “torn/ruptured small and medi- Fisher make reference to small amounts of subarach-
um-sized veins” were identified histologically in sec- noid bleeding in some instances of asphyxial death
tions from deep to the subdural blood in a paramedian (30). As noted previously, some workers in the field
distribution (26)). After all, it is very well recognized of infantile neuropathology have also suggested that
that petechiae can develop within the skin and mucous subdural hemorrhage may develop consequent upon
membranes of the head and neck in association with a combination of hypoxic tissue damage and elevated
venous hypertension in instances of compression of intravascular pressure (5-7, 9, 18).
the neck and/or torso—indeed, petechial hemorrhag-
es are frequently used as a supportive diagnostic sign Notwithstanding the preceding commentary, consid-
in cases such as these. It would seem logical that the eration must also be given to the possibility that the
same processes may well apply to the cranial vascu- subdural bleeding identified in at least some of these
lature in instances of venous hypertension. Such an cases might be explained by postmortem phenomena.
explanation for the origin of the subdural hemorrhage The so-called hypostatic hemorrhage has been de-
in the cases identified in this study would appear to scribed in the soft tissues in gravitationally dependent
be supported by the finding of perivascular intracere- parts of the body after death (31), and animal models

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have pointed to the same occurrence in brain tissue The possibility of subdural bleeding developing in
(32). Despite fairly lengthy postmortem intervals pri- association with cranial venous hypertension adds
or to autopsy in many of these cases, the exclusion another dimension to the ongoing vigorous debate re-
of cases from this study showing significant changes garding infantile subdural hemorrhage, particularly in
in decomposition would likely minimize the risk of instances where there is no, or only limited additional
such artefact. Nonetheless, it is perhaps of relevance evidence of trauma (4-6, 8, 9, 18, 35)—an issue of
that in several of these cases, the body of the deceased critical relevance given the widely accepted strong
was described as being prone or slumped over at the association between subdural hemorrhage and nonac-
scene, and of course the two bodies recovered from cidental head injury (36-38). Is it possible that it is
open water are likely to have adopted a backup/head cranial venous hypertension may be a factor, at least
down position prior to recovery of the remains. It is in some cases—rather than head trauma by way of
also possible that the subdural blood may have col- impact injury or forcible and repetitive shaking? This
lected as an artefact during the autopsy process—most cranial venous hypertension theory may go some way
likely stemming from incisions through, or by way of in explaining the apparent discrepancy between forc-
traction upon, vascular structures at the time of brain es required experimentally to rupture dural bridging
removal, perhaps exacerbated by a reduction in pres- veins and the quantification of forces actually gener-
sure inside the head during removal of the calvarium. ated in models of abusive infantile shaking (39-42), as
However, the fact that the observations were made by well as the limited radiological and pathological data
experienced forensic pathologists and neuropathol- suggestive of neck injury in cases of infant deaths tra-
ogists who are well-versed in postmortem artefact ditionally attributed to shaking (27, 43). However, it
would likely weigh against such an explanation. is acknowledged that different mechanistic processes
may be operative in infant cases from the post-infan-
Although the observations described in this study are tile pediatric and adult cases described in this study.
of interest, it is acknowledged that it would be desir-
able to collect a larger number of cases for assessment The fact that subdural hemorrhage has been docu-
in future studies, ideally with histological examina- mented to develop in association with otherwise “be-
tion of the dura in every case. Shorter postmortem in- nign” birthing processes—including instances of not
tervals and radiological imaging prior to instrumenta- only vaginal delivery, with and without instrumen-
tion at autopsy may assist further with the assessment tation, but also in association with cesarean delivery
of the possibility of artefactual origin of the subdural (44, 45)—would tend to suggest that subdural hem-
blood. Cases with evidence of head trauma, however orrhage occurs more readily in infants than adults.
minimal, should ideally also be excluded from subse- Spontaneous infantile subdural hemorrhage has also
quent projects. been described in association with a variety of natural
conditions (2), most notably in the presence of benign
It is of interest that cardiopulmonary resuscitation enlargement of the subarachnoid space (46, 47)—
had been attempted in 14 of the 37 cases described in though it has been stressed that spontaneous infantile
this study. This observation raises the possibility that, subdural hemorrhage ought not be definitively diag-
in at least some of the cases described, the subdural nosed simply because of the absence of markers of in-
hemorrhage may have been in part or wholly related jury, but only with positive evidence of predisposing
to an elevation of intracranial intravascular pressure conditions such as macrocrania, arachnoidomegaly, or
stemming from chest compressions—a mechanism severe dehydration (48).
that data from other published studies would perhaps
support (33), and which has previously been proposed Those used to handling young infants will no doubt
by others (34). However, the data set out herein are be familiar with the quite profound vascular engorge-
not thought to provide meaningful further assistance ment of the face that can occur in association with
in assessment of this theory. bouts of heavy and protracted crying, possibly at least

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in part reflecting a Valsalva-like physiological mech- rhagic retinopathy may have some parallels here too
anism. It may be the case that this congestion primes (54). Cerebral sinovenous thrombosis has also been
the infantile head to hemorrhage with additional me- proposed as a possible cause of subdural hemorrhage
chanically activated venous hypertension, perhaps in infancy (55), and such a possibility would appear
by way of compression of the infant torso. Similarly, to be supported by the findings in this study and the
compression of the infantile frame may also be a fac- proposed role of cranial venous hypertension in the
tor in the development of subdural hemorrhage during origin of subdural hemorrhage.
passage through the birth canal.
CONCLUSION
Infantile rib fractures, especially posteriorly sited
fractures, are traditionally frequently thought to be The autopsy cases described in this study highlight
caused by way of forcible gripping of the chest and the fact that acute subdural hemorrhage is not always
are typically described as having high specificity for traumatic in nature and reinforce the need to consid-
nonaccidental injury (49-51). Forcible compression of er other etiologies in the differential diagnosis. One
the infant chest can of course be readily seen to have possible explanation for these observations, at least
much in common with the cases of compression of in some instances, is that cranial venous hypertension
the torso identified in this adult study. Similarly, and results in oozing of blood from engorged, possibly
as touched upon previously, parallels could arguably dural-based, venous channels. Although this study
also be drawn with instances of resuscitative compres- focused on adults and post-infantile children, the hy-
sion of the infant chest. This observation, combined pothesis proposed may be of relevance to the ongoing
with the frequent combination of rib fractures and debate regarding subdural hemorrhage in infants.
acute subdural hemorrhage in many cases of appar-
ent abusive infantile head trauma, raises the possibil- ACKNOWLEDGEMENT
ity that in at least some of these cases the subdural
bleeding may be consequent upon compression of The author is grateful to Dr. Michael Rodriguez for
the infant chest, perhaps by way of forcible gripping his kind review of the manuscript prior to submission,
(maybe “squeezed infant syndrome” would be an ap- and his useful and constructive comments.
propriate moniker)—rather than head injury caused
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