CASE REPORT

Hemorrhagic Transformation of Stroke
Secondary to Spontaneous Internal
Carotid Artery Dissection
Ju-Sing Fan1,4, Feng-Chi Chang2,4, Han-Hwa Hu3,4, Li-Chi Hsu3,4*
Departments of 1Emergency Medicine and 2Radiology, and the 3Neurological Institute,
Taipei Veterans General Hospital, and 4National Yang-Ming University School of Medicine,
Taipei, Taiwan, R.O.C.

The clinical course of patients with hemorrhagic transformation in stroke secondary to spontaneous cervical internal
carotid artery dissection (ICAD) has not been elucidated. We report a 36-year-old man with presentation of headache
and subsequent left hemiparesis. Magnetic resonance imaging disclosed right ICAD with nearly complete occlusion of
the right distal internal carotid artery and infarction over the right basal ganglion with hemorrhagic transformation in its
central area. Hemorrhagic transformation can develop early in ICAD patients without preceding treatment with antithrombotic agents. Clinicians are urged to use antithrombotic agents with caution in patients with spontaneous ICAD with
ischemic stroke because early hemorrhagic transformation may also be present. Possible pathomechanisms and treatment strategies are also discussed. [J Chin Med Assoc 2006;69(12):585–588]
Key Words: hemorrhagic transformation, internal carotid artery dissection

Introduction

promote further discussion of ICAD treatment and
prognosis, we report this case.

Recent studies investigating the effects of administering antithrombotic agents in internal carotid artery
dissection (ICAD) to prevent thromboembolic events
and to improve prognosis have found that not all
ICAD patients are suited to receive antithrombotic
agents.1,2 Antithrombotic agents can be detrimental
if the ICAD-induced stroke is accompanied by hemorrhagic transformation. This suggests that the influence
of hemorrhagic transformation should be considered
in the management of ICAD with ischemic stroke. If
they are misadministered because hemorrhagic transformation was not discovered earlier, antithrombotic
agents may cause adverse consequences. The clinical
course of hemorrhagic transformation has not been
comprehensively described, imaging studies of ICAD
in patients with hemorrhagic transformation have not
been reported, and the treatment and prognosis of
ICAD have not been amply discussed.1–4 Hence, to

Case Report
A 36-year-old man suffered from sudden onset of a
throbbing headache over his right parietal region while
walking on December 25, 2004. The man presented to
the emergency department (ED) within 1 hour. Initial
neurologic examination did not reveal any abnormality.
The patient was admitted to the ED observation room
with the tentative diagnosis of primary headache. No
medications except pain killers were prescribed at that
time. Ten hours later, the patient suffered from transient left hemiparesis and hemihypesthesia. Computed
tomography (CT) of the brain was performed within
30 minutes, and did not disclose any intracranial lesion.
His hemiparesis and hemihypesthesia relapsed on the
following morning. Early stroke was suspected and

*Correspondence to: Dr Li-Chi Hsu, Neurological Institute, Taipei Veterans General Hospital, 201, Section 2,
Shih-Pai Road, Taipei 112, Taiwan, R.O.C.
Received: April 18, 2006
Accepted: October 18, 2006
E-mail: lchsu@vghtpe.gov.tw
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© 2006 Elsevier. All rights reserved.

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J.S. Fan, et al

Figure 1. Axial T1-weighted magnetic resonance imaging of the
brain shows nearly total occlusion of the right petrous internal
carotid artery with soft tissue signal around the stagnant flow
(long arrow). The left distal internal carotid artery is normal (short
arrow).

Figure 2. Axial T2-weighted magnetic resonance imaging of the
brain shows infarction over the right basal ganglion with central
hemorrhagic transformation (arrow).

magnetic resonance imaging (MRI) was arranged.
The symptoms presented with undiminished sensation
over the right parietal and right retro-orbital areas.
MRI disclosed nearly complete occlusion of the right
distal internal carotid artery, with soft tissue signal
around the region of stagnant flow (Figure 1) and
infarction over the right basal ganglion with hemorrhagic transformation in its central area (Figure 2).
586

Figure 3. Right carotid angiography showed segmental narrowing
over the distal cervical and petrous portions of the right internal
carotid artery (arrows).

Conventional angiography showed a long segmental
narrowing over the distal cervical and petrous portions of the right internal carotid artery (Figure 3).
Hemorrhagic transformation of ICAD-induced stroke
was diagnosed. Upon providing informed consent, the
patient was enrolled as a case in our study. He was
then admitted to the neurologic ward for further
evaluation and intervention.
The patient denied having a history of head or
neck trauma, cervical manipulation, chronic migraine,
illicit drug use, or any other known systemic disease.
On admission, neurologic examination showed clear
consciousness, isocoric pupils with partially limited
eye movement, left hemiparesis and hemihypesthesia,
increased tendon reflex, and positive Babinski response
on the left. The National Institutes of Health Stroke
Scale (NIHSS) score was 13. Laboratory studies, including hemogram, biochemistry, α1-antitrypsin, VDRL
(venereal disease research laboratory slide test), coagulation, autoimmune and inflammation profiles, were
all within normal limits. Electrocardiogram and transthoracic echocardiography were normal. During the
admission period, the patient experienced progressive
hemiplegia and headache in the first 2 days. Follow-up
brain CT showed enlarged hematoma without midline
deviation. Symptomatic hemorrhagic transformation
was impressed. Without significant sign of increased
intracranial pressure, the patient received only conservative management such as maintaining adequate vital
signs and use of nonsteroidal anti-inflammatory drugs
for pain relief. After that, no other adverse event

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Hemorrhagic transformation of stroke caused by ICAD

Figure 4. Brain magnetic resonance angiography shows no flow
in the distal cervical carotid artery (long arrow) and normal flow in
the intracranial carotid artery (short arrow).

occurred during the admission period. He was discharged 1 month later in a stable condition with satisfying neurologic recovery. His NIHSS score was
7 on discharge.
Follow-up brain magnetic resonance angiography
(MRA) 4 months later showed no flow in the distal
cervical internal carotid artery but relatively normal
blood flow in the intracranial carotid artery (Figure 4).
The patient’s neurologic deficits improved gradually
despite the unresolved internal carotid artery occlusion. He did not receive any antithrombotic agent
during the admission period. His NIHSS score was 2
and modified Rankin Scale score was 1 (minor sequelae) 1 year later, representing a satisfactory neurologic
outcome.

Discussion
Hemorrhagic transformation develops in about 1-third
of all stroke patients within the first week of symptom
onset, but its incidence is much lower in patients with
stroke secondary to cervical ICAD.3–5 This difference
may be due to younger age at onset and fewer predisposing factors of intracranial hemorrhage (such as
hypertension, diabetes, and atherosclerotic vessels) in
patients with cervical ICAD.3,4 In ICAD patients with
or without cerebral ischemic events, the long-term
neurologic prognosis is good.1,2,6,7
Most authors agree that ICAD is probably the endpoint of a complex and possibly heterogeneous group
of vasculopathies developing under the influence of
various genetic and environmental factors.1,2,6–8 The
subsequent hemorrhagic transformation is considered
to be related to ischemia and reperfusion injury to vessel
walls and capillaries.5 Like most patients with ICAD,
the stroke pattern of our patient was thromboembolic
type because the infarcted area on MRI was territorial
rather than border-zoned.1,2,9,10 Although controlled

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studies of the treatment of cervical artery dissections
have not been performed, most clinicians agree that
antithrombotic therapy is a reasonable choice.1,2,7 More
invasive treatments like surgical or catheter-based revascularization are allowed in selective cases.1,2 However,
the standard treatments of hemorrhagic transformation
of stroke caused by ICAD have not been documented.
Most authors agree that anticoagulants should not be
used in patients with hemorrhagic transformation or
those at high risk for hemorrhagic transformation.1,2
In our patient, antithrombotic therapy was not done
because the intracranial hemorrhage and ICAD were
noted concurrently. Due to the symptomatic enlarging
cerebral hematoma, we also withheld antiplatelet agent,
although there was no evidence that antiplatelet agents
worsen the hemorrhagic transformation.
In addition to young age, our patient exhibited 2
features of the carotid artery dissection triad (i.e. pain
on 1 side of the head, face, or neck, partial Horner’s
syndrome, and oculosympathetic palsy, which was then
followed by cerebral or retinal ischemia hours or days
later).1,2,7 Some authors describe symptoms resembling
migraine attack with aura.11 Although differentiating
between migraine with aura and ICAD in the early
stage can be difficult, unusual headaches in patients
with or without previous history of migraine need
further investigation.11 The treating physician should
maintain a high level of suspicion even if the warning
signals are subtle or subclinical.5 In our patient, the
follow-up brain CT was not done because MRI could
be performed quickly (within 10 minutes after it was
arranged). Although it was incidental, the finding of
hemorrhagic transformation on MRI shows that hemorrhagic transformation can develop in the early stage
of spontaneous ICAD even before administration of
antithrombotic agents.
MRI techniques are replacing conventional angiography as the best imaging modality for diagnosing
ICAD.12 MRI can also identify patients who are at
increased risk of secondary hemorrhagic transformation
following acute ischemic stroke.13,14 To find the best
treatment plan in a timely fashion, we recommend
that MRI be arranged as soon as possible to diagnose
carotid artery dissection in all young stroke patients
and patients with migraine-like unusual headache with
aura, and that before administering antithrombotic
agents, the treating physician should carefully look for
signs of hemorrhagic transformation. Once the signs
of hemorrhagic transformation arise, immediate brain
CT is needed. Our patient’s condition improved gradually during his month-long admission and the ensuing
1 year. The neurologic outcome indicated that the brain
tissue supplied by the occluded internal carotid artery
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J.S. Fan, et al

remained viable. Most authors believe that the ischemic
territory is rescued by collateralization from the part
of the Circle of Willis,15 and the follow-up MRA
(Figure 4) in our patient showing the normal flow of
the right intracranial internal carotid artery supports
this belief. These results challenge the need for surgical
or catheter revascularization in ICAD patients with
persistent deficits. However, studies comparing the
outcomes of different management strategies might
be useful.
In conclusion, hemorrhagic transformation can
occur in young stroke patients secondary to spontaneous cervical ICAD even in the early stage before
administration of antithrombotic agents. Physicians
should be more cautious in the routine use of anticoagulants in patients with ICAD. Early MRI study
facilitates early diagnosis of spontaneous ICAD, and
follow-up brain CT in patients with clinical suspicion
of hemorrhagic transformation can help in its early
recognition. Conservative management may be an
alternative approach for ICAD patients with proven
stroke with hemorrhagic transformation.

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