- -
SPONTANEOUS INTRACEREBRAL HEMORRHAGE
DELAYED TRAUMATIC
INTRACEREBRAL HEMORRHAGE
In 1891, Bollinger2 reported four patients
who were apparently doing well after head
injury but developed the sudden onset of
symptoms leading to death days or weeks
after their initial trauma. At autopsy two of
the patients had hemorrhages into the fourth
ventricle and the others had parenchymal
hemorrhages. Bollinger named this phenom-
enon "traumatische Spat-Apoplexie" or trau-
matic late apoplexy. According to Bollinger,
patients with this diagnosis must have had a
history of head trauma, an asymptomatic in-
terval, no preexisting vascular disease, and
the apoplectic appearance of neurologic defi-
cit or disturbance of consciousness.
Because Bollinger's observations predated
the appearance of cerebral angiography and
computed tomography (CT) scanning by
many decades, it is not possible to know
whether the patients he reported sustained
hemorrhagic lesions or other abnormalities of
the cerebral parenchyma at the time of their
original trauma. It is similarly impossible to
ascertain what the relationship of any such
lesions might have been to the patient's sub-
sequent demise. Moreover, these patients dif-
fer from those with delayed traumatic intra-
cerebral hematoma (DTICH) because this
latter group of patients has generally sus-
tained severe head injury and is rarely asymp-
tomatic in the period before the onset of
DTICH.9
From the Department of Neurosurgery, New York University School of Medicine, New York, New York
NEUROSURGERY CLINICS OF NORTH AMERICA
VOLUME 3 NUMBER 3 JULY 1992
1042-3680192 $0.00 + .2O
Paul R. Cooper, MD
MODERN DEFINITIONS OF
DELAYED TRAUMATIC
INTRACEREBRAL HEMATOMA
Before the advent of CT the definition of
DTICH depended on clinical signs of delayed
neurologic deterioration and angiographic or
operative confirmation of an intracerebral he-
matoma (ICH). In 1970 Morin and PittsZ0de-
fined DTICH as the "sudden appearance of
signs or symptoms of serious intracerebral
hemorrhage related to recent head injury in a
previously asymptomatic individual."
Current concepts and definitions of DTICH
depend on the ability of the CT scanner to
image hemorrhagic lesions of the brain. Nev-
ertheless, there is no universally accepted def-
inition of DTICH. Lipper et all8 make the di-
agnosis of DTICH if "no lesion or a negligible
one (smaller than 1 cm) was present on the
initial scan and parenchymal high-density le-
sions developed on subsequent studies."
Most authorities include those patients whose
initial scans do not show frank ICHs, al-
though presumably a contusion that develops
into an ICH could be included. Others12,l4are
more stringent in their criteria and would re-
ject those cases in which ICHs developed
from cerebral contusions or other abnormali-
ties. They would also exclude those cases in
which the initial lesion had enlarged or devel-
oped at the site of previous surgery.14
659
660 COOPER
Classification of Delayed Traumatic
lntracerebral Hemorrhage
A number of authors have taken a more
inclusive approach recognizing that DTICH
may originate from areas that were normal or
even pathologic on the initial CT scan. Fuka-
machi et all3 have classified posttraumatic
ICHs into four types: type I hematomas were
already apparent on the initial CT and de-
creased in size with time; type I1 hematomas
were small or medium sized on the initial scan
and increased in size on subsequent scans;
type I11 hematomas developed in areas that
were normal on the initial CT scan; and type
IV hematomas developed from areas of con-
tusions that were of mixed high density and
isodensity. They regarded only type I11 and IV
as true DTICH. Diaz et a17 have reported a
similar classification.
INCIDENCE
The incidence of DTICH reported in the
literature varies considerably because of sev-
eral factors. Prior to the advent of CT scan-
ning, DTICH was infrequently reported and it
was recognized only in those patients who
deteriorated after a period of neurologic im-
provement. The reported incidence of DTICH
in the CT era depends on the performance of
routine follow-up scans in the early posttrau-
matic period. Even more important is the tim-
ing of the initial scan. Because DTICH tends
to occur early in the posttraumatic period,
failure to perform the initial scan in the first
hours after trauma results in misidentification
of many delayed hematomas.
The incidence of DTICH also depends to a
large extent on the types of patients included
in the series. For example, if all patients with
head injuries of any kind who undergo CT
scanning are included, then the incidence of
DTICH is artifically low. If only those patients
with severe head injuries are included, the
reported incidence is higher.
Lastly, if strict CT criteria are applied and
only those hematomas arising from com-
pletely normal areas of brain are classified as
DTICH, the incidence is relatively low. In
those series in which delayed hemorrhages
originating from areas of contusion, edema,
or small hemorrhagic lesions are classified as
DTICH, the incidence is much higher. The
incidence of DTICH reported by a number of
authors is shown in Table 1. The highest inci-
dence occurred in those series that included
patients with severe head injuries who were
scanned at fixed time intervals after injury
regardless of clinical findings. In a study of 58
patients with a Glasgow Coma Scale (GCS)
score of 8 or less, Cooper et a14 reported the
development of new hemorrhagic lesions in
43%. In 33% of patients the delayed or recur-
rent hematomas were located within the cere-
bral parenchyma. The lowest incidence seen
in Table 1 occurred in series accumulated
prior to the advent of CT scanning1and in the
early days of CT scanning,'' when only a sin-
gle scan was obtained unless there was evi-
dence of deterioration.
Although there are considerable data on the
incidence of DTICH in series of patients with
head injury, there is little information on the
percentage of all traumatic ICHs that form on
a delayed basis. Fukamachi et all3 reported
that 42 of 84 traumatically-induced ICHs were
delayed in onset and developed from areas
that were either normal or of heterogeneous
density consistent with small contusions. At
first glance this figure seems high. If Fuka-
machi et a1 are correct, then doubling the fig-
ures given for the incidence of DTICH in the
series reported in the CT era in Table 1should
give one a rough approximation of the inci-
dence of all posttraumatic hematomas. Thus,
in the series of patients with severe head in-
jury of Lipper et al,18 by extrapolating one
could calculate a 16% incidence of ICHs (de-
layed or immediate in onset). This figure does
not seem unreasonable.
Table 1. REPORTED INCIDENCE OF
DELAYED TRAUMATIC
INTRACEREBRAL HEMORRHAGE
Series Patients with DTlCH (%)
Baratham' 0.26
Cooper4
Diaz7
French"
Gentlemani4
Gudemani5
Kaufman17
Lipperi8
Merino-de Villasanteig
Ninchoji2'
Sprick26
 DELAYED TRAUMATIC INTRACEREBRAL HEMORRHAGE 661

COMPUTED tion of DTICH may be predicted by abnormal

TOMOGRAPHIC APPEARANCE
Imaging Characteristics
The location of DTICH is identical to ICHs
or contusions that are visualized immediately
after trauma (Fig. 1).Like contusions and he-
matomas of immediate onset, they are found
predominantly in the subcortical regions of
the frontal and temporal lobes.7,17, 20, 26 Their
shape is irregular and the CT density is heter-
ogeneous. In one series the mean volume of
hematomas requiring operative treatment
was 24 mL; the volume of those that were not
evacuated because they were not believed to
be contributing to cliiical deterioration was
7 mL.14
DTICH is almost always associated with
ICHs or contusions at other locations or extra-
cerebral hematomas (Fig. 2).7, 14, ''
In one
series15only 2 of 12patients had an initial scan
that was completely normal. Others14believe
that a patient "whose admission CT is normal
will not develop a delayed haematoma." In
some patients with an apparently normal ap-
pearance of the cerebral parenchyma the loca-
enhancement after the intravenous adminis-
tration of contrast agents.21
Skull fracture is a frequent accompaniment
of DTICH and was seen in five of nine pa-
tients in one series7and in 21 of 25 in another
series." In this latter series, 44% of patients
sustained basal skull fractures.
Time Course of Appearance
Despite reports of many days or weeks be-
tween the initial traumatic event and the ap-
pearance of the hematoma made before
the advent of CT,', 9, 20 most DTICHs visual-
ized on CT scans occur within 48 hours of in-
jUIy.14,15, 18, 26 1, four series14. 15. 18. 29 with a
total of 93 patients only a single patient devel-
oped a hematoma more than 48 hours after
injury. Of 48 patients reported by Yamaki et
al,29no hematoma larger than 3 cm developed
more than 24 hours after head injury and 84%
reached their maximum size within 12 hours
of injury. In another series7 four of nine pa-
tients had CT identification of DTICH more
than 48 hours after trauma. These patients

Figure 1. A, Medium-sized right frontal contusion or hemorrhage is seen in a scan taken within 2 hours of head
injury. Although confused, the patient was awake and had no focal defic~t.5, Three hours later the patient became
less alert and developed focal deficit. Repeat CT scan shows the development of a large right frontal hematoma at
the site of the contusion. Dilatation of the temporal horns and obliteration of the basal cisterns are consistent with
early tentorial herniation.
662 COOPER
Figure 2. A, CT scan taken shortly after head injury shows bifrontal contusions. B, CT scan of the same patient
performed 48 hours later shows a right posterior temporoparietal hematoma not seen on the initial scan.
were not scanned routinely after the first scan
and had follow-up scans only after they expe-
rienced neurologic deterioration, however.
CLINICAL FEATURES
The cardinal signs of DTICH are a progres-
sive decrease in the GCS score, the onset of
focal neurologic deficit, and focal seizures."
One or more of these was present in almost
90% of ~atients." Gudeman et all5 analyzed
the clinical course in 12 patients at the time
that they developed DTICH. Only 2 showed
evidence of clinical deterioration. The remain-
der were either unchanged or were improv-
ing. DTICH is a relatively uncommon cause of
neurologic deterioration in patients with head
injury. In an analysis of 33 patients who
"talked and deteriorated,'lZ3only 4 of 33 pa-
tients had DTICH as a cause of their deterio-
ration.
The severity of the head injury in patients
who develop DTICH varies and appears to
depend on the demographics of the particular
series more than anything else. In one se-
ries," 14 of 25 patients had an admission GCS
score of 9 or more. Six hours after admission,
10 patients still had a GCS score of 9 or more.
In two other reports17, 26 more than three
fourths of the patients had an admission GCS
score of 7 or less. Eight of the nine patients
reported by Diaz et a17 were comatose at the
time of their first examination. The frequent
occurrence of extra-axial hematomas, other
parenchymal hematomas, and poor outcome
in a high percentage of patients with DTICH
strongly suggests that patients with this en-
tity have sustained a severe head injury.
PATHOGENESIS
The pathogenesis of DTICH has not been
established with certainty. It is likely that
hemorrhage occurs into brain that has been
injured by the initial traumatic event. The ini-
tial CT scans obtained on patients who later
develop DTICH frequently show no abnor-
malities in the region where hemorrhage later
develops, however. Whether abnormalities
exist that predispose the patient to later hem-
orrhage but are beyond the imaging capabili-
ties of CT is not clear at this time. Although
there is now little experience with the use of
magnetic resonance (MR) imaging in patients
with acute head injury, this imaging modality
may resolve the issue in the future. Even
 DELAYED TRAUMATIC INTRACEREBRAL HEMORRHAGE
when there are anatomic abnormalities in the
brain after head injury, relatively few patients
develop DTICH. It is thus likely that the mul-
tiple factors discussed next must interact to
produce DTICH.
Necrotic Softening of the Brain
In 1891, ~ o l l i n g e was
r ~ the first to describe
the clinical entity of delayed apoplexy or
"traumatische Spat-Apoplexie." His diagno-
sis was based on purely clinical criteria and
referred to sudden neurologic deterioration
many days or even weeks after injury. Hem-
orrhage was confirmed at autopsy in all pa-
tients. He postulated that the original injury
caused areas of necrosis in the cerebral paren-
chyma and walls of small arterial vessels with
subsequent rupture and hemorrhage. It is not
clear why the patients who Bollinger and oth-
ers8, reported deteriorated so long after their
trauma, whereas most patients in CT era se-
ries usually deteriorate within 48 hours of
injury.
Dysautoregulation
Evans and Scheinker", 24 and Gudeman et
all5 proposed the concept of dysautore-
gulation to explain DTICH. They hypothe-
sized that in the damaged brain there was
failure of the mechanisms that regulate blood
flow. Vessels are subjected to increased intra-
vascular pressure that eventually results in
rupture of the vessel and hematoma forma-
tion. Evidence in experimental contusions
suggests that vasodilation occurs at the
capillary-venule junction with extravasation
of blood and formation of microhematomas,
which eventually enlarge.25
Systemic Insults
Some authorities believe that hypoxia and
hypercarbia exacerbate the phenomenon of
dysautoregulation and provoke delayed hem-
orrhage.'' Ninchoji et al2' found that hypo-
tension, hypoxia, or disseminated intravascu-
lar coagulation was present in 72% of their
patients. Others14 have found a similar inci-
dence of hypoxia, hypercarbia, and systemic
hypotension in patients with DTICH and
663
those with severe head injury who did not
have DTICH, however.
Disseminated lntravascular Clotting
and Fibrinolysis
The brain is rich in thromboplastic sub-
stances; brain injury results in the release of
these substances into the circulation, which
produces intravascular coagulation.17 Kauf-
man et all7 measured the presence of fibrin
split products, platelets, fibrinogen, and
other hemostatic indices in 12 patients with
DTICH. Eleven of these patients had clotting
abnormalities. They speculated that local in-
travascular coagulation and fibrinolysis
"could result in local vascular occlusion and
infarction and then hemorrhage after lysis of
intravascular clots." Bullock et a13 reported
that 12 of 13 patients had a frank coagulopa-
thy or were acutely intoxicated with alcohol.
Although it is known that alcohol ingestion
can induce quantitative changes in platelets
and clotting factors, it is likely that some of the
patients with acute alcoholism had qualitative
defects in their clotting mechanism that were
not d e t e ~ t e dDiaz
. ~ et a17 also found clotting
abnormalities in four of eight patients with
DTICH.
Removal of Tamponade Effect
Several authors3, 13' 16' 22 have noted the
appearance of DTICH after the evacuation of
extra-axial lesions or parenchymal hemato-
mas at noncontiguous sites. In one ~ e r i e s , 13
~'
of 25 patients who developed DTICH had
prior craniotomy for evacuation of extracere-
bra1 hematomas. In another series3 mannitol
administration was more frequent in patients
who developed DTICH than in those who did
not. It seems likely, as some of these authors
hypothesize, that DTICH develops as a result
of release of tamponade on injured areas of
the brain.
Taneda and ~ r i n o have
~ ~ suggested that a
compressive extra-axial lesion causes in-
creased venous pressure and thrombi within
small venules. Removal of the hematomas
and release of compression cause an increase
in the difference between tissue pressure and
intravascular pressure, with resultant dis-
lodging of thrombi and delayed bleeding.
664 COOPER
Czernicki and Koznieska6 produced cerebral
compression by inflating an epidural balloon.
ICHs formed after balloon deflation. They hy-
pothesized that the hematomas occurred as a
result of cerebral ischemia and disruption of
the blood-brain barrier.
MANAGEMENT OF PATIENTS WITH
DELAYED TRAUMATIC
INTRACEREBRAL HEMORRHAGE
In theory, the management of patients with
DTICH does not differ significantly from pa-
tients whose hematomas are visualized on
imaging studies shortly after trauma. In prac-
tice, however, patients with DTICH have fre-
quently undergone prior operation to evacu-
ate extra-axial or noncontiguous hematomas,
they often have abnormalities of coagulation,
and they have a generally poor prognosis.
There is thus an understandable tendency to
avoid operation if at all possible. Factors
that mitigate against hematoma removal are
(1) uncorrected disorders of coagulation,
(2) normal intracranial pressure or intracranial
pressure that is controlled with medical ther-
apy, (3) hematoma location other than the
temporal lobe, (4) stable neurologic deficit,
and (5) little mass effect. Obviously patients
who are deteriorating neurologically or who
do not meet one or more of the criteria listed
above require operation and hematoma re-
moval.
Patients who have DTICH are at risk for yet
additional hematomas and must be managed
postoperatively with intracranial pressure
monitoring. CT scan must be performed fre-
quently and on a regular basis regardless of
the patient's clinical status.
OUTCOME
The outcome of patients with DTICH re-
ported in the literature has been generally un-
satisfa~tor~ . ~17*
14, , 29 Interestingly the out-
come in the pre-CT and post-CT era is similar.
In 1970 Morin and PittsZ0reviewed the out-
come reported in the pre-CT literature and
recorded 11deaths in 24 cases. Baratham and
Dennysonl reported a mortality of almost
75%. In the CT era Diaz et a17 reported five
deaths in nine patients. Ninchoji et alZ1 re-
ported 11deaths in 25 patients. An additional
eight patients were severely disabled or vege-
tative. Others17, Is have reported similar re-
sults. There is only one series with a mortality
rate of less than 50%.I4
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Address reprint requests to
Paul R. Cooper, MD
Department of Neurosurgery
550 First Avenue
New York, NY 10016