Histopathology 1989, 15,49-59

Diffuse axonal injury in head injury:

definition, diagnosis and grading

J.HUME ADAMS*, D.DOYLE*, I.FORDt,

T.A.GENNARELLI$., D.I.GRAHAM* & D.R.MCLELLAN*
*Department of Neuropathology and ?Department of Statistics,
University of Glasgow, Glasgow, Scotland and $.Department of
Neurosurgery, University of Pennsylvania, Philadelphia, USA

Accepted for publication 7 November 1988

HUMEADAMSJ., DOYLED., FORDI., GENNARELLI T.A., GRAHAM

D.I. &
MCLELLAN
D.R. (1989) Histopathology 15,49-59

Diffuse axonal injury in head injury: definition, diagnosis and grading

Diffuse axonal injury is one of the most important types of brain damage that can
occur as a result of non-missile head injury, and it may be very difficult to diagnose
postmortem unless the pathologist knows precisely what he is looking for. Increasing
experience with fatal non-missile head injury in man has allowed the identification or
three grades of diffuse axonal injury. In grade 1 there is histological evidence of
axonal injury in the white matter of the cerebral hemispheres, the corpus callosum,
the brain stem and, less commonly, the cerebellum; in grade 2 there is also a focal
lesion in the corpus callosum; and in grade 3 there is in addition a focal lesion in the
dorsolateral quadrant or quadrants of the rostra1 brain stem. The focal lesions can
often only be identified microscopically. Diffuse axonal injury was identified in 122 of
a series of 434 fatal non-missile head injuries-I 0 grade I , 29 grade 2 and 83 grade 3.
In 24 of these cases the diagnosis could not have been made without microscopical
examination, while in a further 31 microscopical examination was required to
establish its severity.

Keywords: head injury, axonal injury

Introduction

Diffuse axonal injury is an important factor contributing to a patient’s clinical state

and governing the outcome in anyone who sustains a non-missile head injury, and it
is also the commonest cause of the vegetative state and severe disability after injury
(McLellan et al. 1986). Yet not much more than a decade ago, there was still
considerable controversy as to the nature of the brain damage and its pathogenesis.
It had been referred to by several names, viz. shearing injury (Strich 1970, Peerless &
Address for correspondence: Professor J.H.Adams, Department of Neuropathology, Institute of
Neurological Sciences, Southern General Hospital, Glasgow G5 1 4TF, Scotland.

49
50 J.Hume Adams et al.

Rewcastle 1967), diffuse damage to white matter of immediate impact type (Adams
et al. 1977), diffuse white matter shearing injury (Zimmerman, Bilaniuk &
Gennarelli 1978) and inner cerebral trauma (Grcevic 1982). These authors took the
view that the damage to white matter occurred at the moment of injury, but other
experienced neuropathologists were of the opinion that it was secondary to hypoxic
brain damage, to cerebral oedema or to secondary damage in the brain stem
resulting from an intracranial expanding lesion (Jellinger & Seitelberger 1970,
Jellinger 1977, Peters & Rothemund 1977).
In our earlier studies we questioned whether focal damage could occur in the
brain stem as a result of a head injury as an isolated event (Mitchell & Adams 1973)
and we suggested at that time that the structural basis of the clinical syndrome of
‘primary brain stem injury’ was the type of brain damage now referred to widely as
diffuse axonal injury. In our initial attempts to identify diffuse axonal injury as a
distinctive clinicopathological entity (Mitchell & Adams 1973, Adams et al. 1977,
1982), it is now clear that we concentrated on the severe end of a spectrum. With
increasing experience of fatal head injuries in man, it has become clear that there are
less severe forms of diffuse axonal injury, and in this paper we wish to define three
grades. As a result of studies in man and of experimental work (Gennarelli et al.
1982, 1987), there is now no reasonable doubt that this type of brain damage is a
primary event that occurs at the moment of injury.
Attention has also been drawn to milder degrees of diffuse axonal injury by
Oppenheimer (1968) and Pilz (1983). Since the focal lesions in the corpus callosum
and in the brain stem can often only be identified microscopically, it is of the utmost
importance that pathologists dealing with fatal head injury should be acutely aware
of this type of brain damage lest they fail to interpret the type of brain damage that
has led to the patient’s clinical state. This is particularly so if there is no evidence of
an intracranial haematoma, severe cerebral contusions, or increased intracranial
pressure.

Materials and methods

During the 15 year period 1968-1982, full autopsies were undertaken in the Institute
of Neurological Sciences, Glasgow, on 635 fatal non-missile head injuries. The
brains were suspended in 10% formol saline for 3-4 weeks prior to dissection in a
standard fashion (Adams & Murray 1982); the cerebral hemispheres were sliced in
the coronal plane at 1 cm intervals, the cerebellum at right angles to the folia, and the
brain stem horizontally. Comprehensive histological studies were undertaken in 434
of these brains. Representative blocks from all regions of the brain were embedded
in celloidin and 30 pm sections were stained by Nissl’s method with cresyl violet and
by Woelke’s modification of Heidenhain’s technique for myelin. In 382 of these
cases, representative blocks from the cerebral hemispheres, the cerebellum and the
brain stem were also embedded in paraffin wax and sections stained with
haematoxylin and eosin, the Luxol fast blue/cresyl violet technique and by the
Palmgren technique for axons. All macroscopic and histological abnormalities were
 Difluse axonal injury 51

recorded on a series of line diagrams. The abnormalities were then recorded on a

proforma and the data stored on the University of Glasgow’s mainframe computer.
The clinical records in each case were assessed to ascertain if the patients had
been able to talk immediately after their injury (Reilly et al. 1975) on the assumption
that if they had, they had not sustained catastrophic brain damage at the time of
injury. Patients who could talk rationally were said to have had a complete lucid
interval. If they were confused, the lucid interval was said to have been partial.
In the analysis of the results, evidence of a relationship between the presence of
diffuse axonal injury and the other variable studies is assessed using a chi-squared
test.

Results

There were 342 males and 92 females; the age range was from 3 months to 89 years,
and the duration of survival ranged from 2 h to 14 years.
Evidence of diffuse axonal injury was identified in 122 of the 434 cases, an
incidence of 29%).The true incidence must have been higher since axonal damage
would be difficult to identify in the 52 cases in which only celloidin sections were
available, and in patients where the less severe features of diffuse axonal injury might
have been obscured by other types of brain damage such as severe contusions and
intracerebral haematomas, brain damage secondary to high intracranial pressure
and herniation of the brain leading to haemorrhage and infarction in the brain stem,
or severe hypoxic damage. Furthermore, axonal damage would also not be very
obvious in patients who had survived for less than 12-18 h after their injury.
There were 10 cases of grade 1 diffuse axonal injury, there being evidence of
axonal damage in the white matter of the cerebral hemispheres including the corpus
callosum, in the brain stem and, occasionally, in the cerebellum: this damage can
only be identified microscopically. There were 29 cases with grade 2 diffuse axonal
injury, i.e. there was a focal lesion in the corpus callosum in addition to diffuse
axonal damage: the focal lesion was identifiable only microscopically in 11 of these
cases. The majority of the cases-83-had sustained grade 3 diffuse axonal injury
since there were focal lesions both in the corpus callosum and the dorso-lateral
quadrant of the rostra1 brain stem: in only 49 of these cases were both the focal
lesions apparent macroscopically even in a properly fixed and dissected brain. Thus,
of the 122 cases the severity of diffuse axonal injury could only be defined by
histological studies in 24, whilst its presence in 31 cases would have been missed
unless appropriate histological studies had been undertaken. Grades 2 and 3 can be
said to be severe if the focal lesions are apparent macroscopically.
It is now clear that in our early attempts to define the clinicopathological entity
of diffuse axonal injury, we concentrated on severe grade 3 cases. The focal lesion in
the corpus callosum is typically haemorrhagic and tends to lie to one side of the
midline (Figure l), although it may extend to the midline and involve the
interventricular septum and the pillars of the fornix. The lesions occur most
frequently in the inferior part of the corpus callosum and usually extend over an
52 J.Hume Adams et al.

Figure 1. There is a haemorrhagic lesion in the corpus callosum to the left of the midline. The
interventricular septum has been torn. There is a parasagittal haematoma (‘gliding’ contusion) and a
small haematoma in the right basal ganglia. (From Adams & Graham 1988.)

Figure 2. There is a shrunken scar in the narrowed corpus callosum (arrow). There is also enlargement
of the lateral ventricles. (From Adams & Graham 1988.)

Figure 3. There is a recent haemorrhagic lesion in the dorsolateral quadrant of the rostral pons. (From
Adams & Graham 1988.)

Figure 4. There is a granular and slightly shrunken lesion in the dorsolaterdl quadrant of the rostral
pons. (From Adams & Graham 1988.)
54 J.Hume Adams et ul.

antero-posterior distance of several centimetres. Occasionally, abnormalities are

restricted to the splenium. If the patient survives for some weeks, the lesion becomes
rather granular and brown in colour, whilst with a survival of months it is
represented by a shrunken cystic scar (Figure 2). The lesions in the dorsolaterdl
quadrants of the rostra1 brain stem follow a similar time course (Figures 3 & 4), but
occasionally there is no haemorrhage into these focal lesions, there simply being
histological evidence of vacuolation and rarefaction of the affected tissue. The
diffuse injury to axons can only be seen microscopically and takes three forms
depending on the duration of survival. In patients of short survival (days) there are
large numbers of axonal bulbs throughout the white matter of the cerebral
hemispheres, the cerebellum and the brain stem, as well as adjacent to the focal
lesions. These can be seen in sections stained by haematoxylin and eosin (Figure 5a),
but they are more readily apparent in silver impregnations (Figure 5b). In patients of
intermediate survival (weeks), there are large numbers of small clusters of microglia
throughout the white matter of the cerebral hemispheres, the cerebellum and the
brain stem (Figure 6). There is also a diffuse non-specific astrocytosis. In patients
who survive vegetative for a longer period (months), there is Wallerian-type
degeneration of the white matter in the cerebral hemispheres, the brain stem and the
spinal cord (Figure 7). By this time the ventricles are usually enlarged as a result of a
reduction in volume of the white matter (Figure 2).
The relationship between diffuse axonal injury and fracture of the skull, type of
accident and lucid interval are given in Table 1 . As in our earlier study (Adams et ul.
1982), there is a significantly reduced incidence of fracture of the skull and a lucid
interval, and a significantly increased incidence of road traffic accidents and a
decreased incidence of falls in patients who sustain diffuse axonal injury, even when
less severe degrees of diffuse axonal injury are included. In our earlier studies on
patients with the most severe type of diffuse axonal injury, we established that it
occurred only as a result of a fall from greater than one’s own height (Adams et ul.
1984). Analysis of the 22 cases with all grades of diffuse axonal injury resulting from
a fall discloses that at least 19 fell from a height-six down stairs, three from a 2nd or
3rd storey window, three from a ladder, two from a lorry and one each into the hold
of a ship, down a lift shaft, from a railway bridge, from the top of a wall and down a
mountain! In the remaining three cases there was some doubt as to the nature of the
injury: two were found unconscious in the street under the influence of alcohol and
one was found unconscious in an office. One of the former had grade I diffuse axonal
injury, while the other two had microscopic grade 2 diffuse axonal injury. Thus, we
have still not encountered a case that could be classified as severe diffuse axonal
injury in someone who has sustained a simple fall from his or her own height.
In contrast to our previous studies on the most severe type of diffuse axonal
injury when all of the patients had been unconscious from the moment of injury, 17
of the 122 patients with diffuse axonal injury experienced a lucid interval. Only two
cases had a total lucid interval, i.e. they were able to talk clearly and rationally, and
both of these had grade I diffuse axonal injury. Of the 15 cases who had a partial
lucid interval, not one had the most severe type as shown by the presence of
macroscopic focal lesions in the corpus callosum and in the dorsolateral quadrant of
 Diffuse axonal injury 55

Table 1. The relationship between diffuse axonal injury (DAI) and

fracture of skull, type of injury and the occurrence of a lucid interval as
defined in the text
Cases with DAI Cases without DAI P
(n= 122) (n=312) value

Fracture of skull 70 (57%) 254 (8 I %) <O.OOl

Road traffic accident 84 (69%) 157 (50%) < 0.005
Fall 22 (18%) 122 (39'Xi) < 0.001
Lucid interval 17 (14%~) 119 (59"h) <O.OOl

Table 2. The relationship between diffuse axonal injury (DAI) and some
othcr types of brain damage resulting from a head injury
~

With DAI Without DAI P

(n = 122) (n = 312) value

Gliding contusions 71 (58%) 65 (2 1 ' X , ) < 0.001

Raised intracranial pressure 85 (70%) 253 (8 I Y") <O.Ol
Modcrate/severe hypoxic 60 (49%) 171 (55%) NS
brain damage
Large intracranial haematoma 32 (26%) 182 (58%) < 0.001
Basal ganglia haematoma 23 (19%) 24 (8%) <0.001
Swelling 49 (40%) I69 (54%) <0.01

the brain stem. Five had grade 2 diffuse axonal injury and six had grade 3 diffuse
axonal injury as identified microscopically.
The relationship between diffuse axonal injury and several other types of brain
damage is given in Table 2. As with the most severe types of diffuse axonal injury
that we have previously analysed, there is a significantly increased incidence of
gliding contusions (Adams et al. 1986a) and deeply seated ('basal ganglia')
haematomas (Adams et al. 1986b). The importance of this observation is that
gliding contusions and basal ganglia haematomas are readily identifiable in CT and
MRI scans. As in our previous studies on severe diffuse axonal injury, there is a
reduced incidence of a high intracranial pressure, intracranial haematoma and brain
swelling, and there is no difference in the incidence of moderate or severe hypoxic
brain damage.

Discussion

Diffuse axonal injury can now therefore be defined as the occurrence of diffuse
damage to axons in the cerebral hemispheres, in the corpus callosum, in the brain
stem and sometimes also in the cerebellum resulting from a head injury. Three
grades in increasing severity can be identified on the basis of the presence of
additional focal lesions in the corpus callosum (grade 2), or in the corpus callosum
and in the brain stem (grade 3).
56 J.Hume Adams et al.

There is no doubt that at least the most severe grades of diffuse axonal injury are
a cause of clinical evidence of severe brain damage in head injury, and that it is the
commonest cause of the vegetative state and severe disability after a non-missile
head injury (McLellan et al. 1986). Whether or not, in the absence of other
complications of head injury, it is a cause of death remains unclear. Even in the
present series there was evidence of a high intracranial pressure in 70% of the cases.
It is our impression, therefore, that in patients with diffuse axonal injury and no
other complications leading to a high intracranial pressure, they either die as a result
of other factors such as multiple injuries, hypoxic brain damage or cerebral fat
embolism, or exist in coma, vegetative or severely disabled until they die as a result
of a respiratory infection. Axonal bulbs are brought about by the extrusion of
axoplasm resulting from anterograde axoplasmic flow, and classic swellings take
about 12-18 h to develop. Hence the difficulty in diagnosing beyond reasonable
doubt the occurrence of diffuse axonal injury in patients who survive for a shorter
time than this after their injury.
Thus, since most patients who sustain diffuse axonal injury die within a week or
so of their injury, rather than weeks or months, the diagnosis is based on the
presence of axonal bulbs rather than the occurrence of clusters of microglia and long
tract degeneration in longer survivors. Axonal bulbs, although they can be seen in
sections stained by haematoxylin and eosin (Figure 5a), are best seen by the silver
impregnation techniques (Figure 5b), or by immunocytological techniques for
neurofilaments. According to Vowles et al. (1987) the Nauomenko-Feigin technique
is required to demonstrate these swellings in early infancy. A major problem in this
field is the interpretation of sinusoidally enlarged axons which, when present on
their own, may be indistinguishable from post-mortem artifact. It has been
suggested, however, that when associated with an astrocytic response, such
sinusoidal changes are likely to represent the earliest stage in the time course of the
development of axonal bulbs and therefore should correlate with the depth of coma
(Vanezis et al. 1987). However, in our experience such axons are often seen in
control specimens and we are therefore reluctant to diagnose diffuse axonal injury
unless we can identify at least occasional classic axonal bulbs in a patient surviving
some 15- 18 h after head injury. There is no doubt that genuine axonal injury can be
identified earlier in perfusion-fixed experimental material (Graham et al. 1985, Erb
& Povlishock 1988, Maxwell et al. 1988), but it is difficult to identify these changes in
the brains of head-injured individuals who live for only a short time. The
immunohistochemical identification of an astrocytic response, while helpful, is by
no means conclusive because of pre-existing disease and the vagaries of immunohis-
tochemical staining in post-mortem material.
The identification and definition of the less severe grades of diffuse axonal injury
have considerable implications for pathologists, particularly those involved in
forensic work. Since the diffuse injury to axons can only be identified microscopi-
cally, appropriate histological screening therefore has to be undertaken in any fatal
head injury to ascertain whether or not diffuse axonal injury is present. This is most
readily seen in the parasagittal white matter, in the corpus callosum, in the midbrain
and in the pons. Of particular medicolegal significance is the fact that we have still to
 Difluse uxonal injury 57

encounter a case of diffuse axonal injury in anyone who has simply fallen from his or
her own height, the inference being that the change in velocity of the skull in a fall of
this type is insufficient to produce the severe shear and tensile strains in the brain
required to produce axonal disruption. Thus, if diffuse axonal injury is found in a
patient who appears to have died as a result of such a fall, the pathologist must be
alerted to the fact that the original injury must have been much more severe, e.g. as a
result of an assault when the head may have been forcibly propelled onto the ground
or a solid wall.
Throughout the long period that we have had an interest in brain damage
resulting from head injury, it has become increasingly apparent that there are certain
misconceptions about the interpretation of some of the lesions on which we have
placed particular importance, viz. focal lesions in the corpus callosum, axonal bulbs,
clusters of microglia and long tract degeneration. Thus, a lesion in the corpus
callosum is not diagnostic of diffuse axonal injury since focal infarcts (pale or
haemorrhagic) are frequently brought about by distortion and shift of the brain
caused by an intracranial haematoma leading to a compromised circulation through
the pericallosal arteries. Axonal bulbs are not restricted to head injury since they
occur in any situation where axons have been disrupted; they will inevitably occur
adjacent to focal lesions such as contusions, infarcts or haematomas. There are also
other causes of multiple microscopic collections of microglia in the white matter, the
most important of which are severe hypoxic brain damage, cerebral fat embolism
and any type of meningoencephalitis. Wallerian degeneration, too, is not restricted
to patients who have survived for several months after a head injury since this is
simply indicative of degeneration of a tract brought about by any type of brain
damage, particularly infarction.
In our earlier studies on severe diffuse axonal injury, not one of the patients was
able to talk after their injury (Adams et ul. 1982). It is of interest, therefore, that 17
(14%) of the 122 cases with diffuse axonal injury in the present series did experience a
complete or partial lucid interval as defined above. The two with a complete lucid
interval had grade I injury, while the remaining 15 had grade 2, in only one of whom
was the focal lesion identifiable macroscopically. Thus, even in this enlarged series,
none of the 17 patients who talked had the most severe type of diffuse axonal injury.
Furthermore, all died as a result of some other type of pathology-raised
intracranial pressure brought about by oedema related to contusions, diffuse brain
swelling or intracranial haematoma in 15, fat embolism in one, and massive gastro-
intestinal haemorrhage in one.
It is probably unfortunate that so much emphasis has to be placed on focal
lesions in defining the severity of a diffuse process. However, identical structural
changes have been produced in non-human primates subjected to angular
acceleration of the head, and there is a close correlation between the severity of the
brain damage and the grade of diffuse axonal injury (Gennarelli et ul. 1982, 1987,
Gennarelli, Adams & Graham 1986). In this model, all three grades of diffuse axonal
injury have been produced, the severity of the axonal injury depending principally
on the magnitude and duration of the acceleration and on the direction of head
motion. With sagittal acceleration, grade 1 but not grades 2 and 3 can be produced.
58 J.Hume Adams et al.

Acceleration of the same magnitude in the coronal plane produces more severe
diffuse axonal injury, usually grade 3, whilst rotation in the horizontal plane
produces diffuse axonal injury of intermediate grade similar to that seen in man. As
the grade of diffuse axonal injury increases, there is deeper and more prolonged
coma and the residual neurological deficits in survivors are more severe. Focal
axonal injury remote from the site of impact has been produced in other animal
models (Povlishock et al. 1983, Povlishock & Becker 1985, Lighthall 1988) but this
type of damage is not the same as that seen in diffuse axonal injury in man.

Acknowledgements

Figures 1, 2, 3 , 4 and 7 are reproduced from An Introduction to Neuropathology by

J.H.Adams and D.I.Graham by permission of Churchill Livingstone, Edinburgh.

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