Download PDF

Hindbrain Stroke in Children Caused by
Extracranial Vertebral Artery Trauma
BY RICHARD A. R. FRASER, M.D., F.R.C.S.(C),* AND SEYMOUR M. ZIMBLER, M.D., F.A.C.S.t
Abstract:
Hindbrain
Stroke in
Children
Caused by
Extracranial
Vertebral
Artery
Trauma
• Hindbrain transient ischemic attacks (TIAs) culminating in posterior circulation stroke are
described in five children. Atlanto-axial subluxation and angiographical documentation of Cl
to C2 level arterial pathology are documented in one patient. Four additional patients with
nearly identical clinical presentations, posterior fossa TIAs, stroke and basilar angiographical
pathology are reviewed. A mechanical traumatic etiology is suggested.
Unexplained transient repeated brain stem and/or cerebellar symptomatology may be due
to extracranial vertebral artery stenosis or occlusion by atlanto-axial instability. After appropriate documentation, stabilization may prevent further TIAs or strokes.
Additional Key Words
vertebrobasilar occlusion
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
DFor many years, neurosurgeons and neurologists,
when evaluating patients with cervical spine trauma or
congenital anomalies of the cervical spine, have
emphasized the direct compressive effects of such
lesions on the cervical spinal cord. Occasional patients
with cervical spine trauma and injury to the vertebral
arteries with subsequent brain stem and cerebellar
dysfunction have been reported. 16 All of these patients
have been adults. Additional patients have had
posterior fossa stroke symptoms following chiropractic cervical spine manipulation. 716
Occlusive cerebrovascular disease in children is
uncommon. The overwhelming majority of such
patients display lesions in the carotid circulation.17
Only seven children have been reported previously
with disease in the posterior cerebral circulation. 1821
Septic emboli occurred in two, while no clearly defined
etiology could be identified in the remaining five (table
1).
We wish to describe an additional patient, a sixyear-old boy with a history of vertebrobasilar TIAs,
which culminated in a major posterior circulation
stroke. Cervical spine x-rays and angiographical data
lead us to suggest that the cerebrovascular accident in
this patient was the result of atlanto-axial subluxation,
traumatic deformation of the vertebral arteries and
distal embolization to the basilar artery. Clinical and
angiographical similarities in other patients suggest a
common syndrome.
From the * Department of Neurological Surgery, the New York
Hospital-Cornell Medical Center, 525 East 68th Street, New York,
New York 10021.
tDepartment of Orthopedics, Tufts-New England Medical
Center Hospital, 171 Harrison Avenue, Boston, Massachusetts
02111.
Stroke, Vol. 6, March-April 1975
transient ischemic attack
atlanto-axial subluxation
extracranial cerebrovascular disease
cervical fusion
Case Report
A six-year-old right-handed boy was first admitted to the
Boston Floating Hospital because of gait ataxia and clumsiness of the right upper extremity. During the previous
month, he had experienced intermittent nausea, headache,
frequent vomiting, dysarthric speech, and clumsiness of the
right upper extremity. These symptoms would appear for a
day, improve spontaneously, and reappear two to three days
later. Because of these symptoms, he had been admitted to
another hospital where neurological examination, EEG,
brain scan, skull x-rays, and CSF formula were reported as
normal.
At the time of admission to the Boston Floating
Hospital, examination revealed a mild deficit with minor
clumsiness of the right hand, bradykinesia, and slow speech.
The diagnoses suggested included cerebellar ataxia of infectious or postinfectious etiology. A brain scan (technetium
99) was normal. Skull x-rays on this admission were
reported as normal, but closer examination revealed nonfusion of the odontoid and anterior displacement of Cl on C2.
While this finding was noted and confirmed on cervical spine
tomograms (fig. 1) and flexion and extension films (figs. 2
and 3), its significance and relationship to the current illness
were not appreciated and the patient was discharged without
cervical stabilization.
One day following discharge, the patient awoke with a
mild right hemiparesis which, over the ensuing six hours,
evolved into a flaccid hemiplegia and prompted his readmission to the Boston Floating Hospital. His parents stated that
he had fallen from bed the night before. Examination on the
second admission confirmed severely dysarthric speech, inability to gaze to the left of the midline, nystagmus on right
lateral gaze, lower motor neuron weakness of the left face,
and a virtually complete right hemiplegia. Deep tendon
reflexes were absent in the right extremities and a right-sided
extensor plantar response was elicited. Dysmetria was apparent in the left upper extremity. Laboratory studies, including hemogram, white blood count, serum electrolytes,
and urinalysis, were normal.
153
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
Not reported
Not reported
Sudden coma following severe
bums and septicemia
Two months' intermittent vertigo,
ataxia, sudden right
hemiparesis, left cerebellar
deficit
Three months' intermittent vertigo, Not reported
fall with occipital fracture
one month prior —diplopia,
bilateral cerebellar deficit
6 yr, M
7yr, M
18 mo, F
4yr, M
9 yr, M
14 yr, M
Dooley et al.19
Fowler20
Fowler20
Ouvrier and
Hopkins21
Ouvrier and
Hopkins21
Ouvrier and
Hopkins21
Coarctation aorta, septicemia,
endocarditis, sudden right
hemiparesis
Sudden coma, decerebrotion
without antecedent illness or
trauma
Not reported
Normal
Two months' intermittent ataxia,
Not reported
vertigo, vomiting, transient
left hemiparesis, left cerebellar
deficit, "jarred" in auto
accident eight months
previously
Eight months' intermittent
Normal
diplopia, vertigo, followed by
sudden right sensory motor
disturbance, ataxia, anisocoria
9yr, M
Cervical spine x-rays
C1-C2 subluxation
DeVivo and
Farrell18
Clinical presentation
One-month transient intermittent
vomiting, dysarthria, ataxia,
sudden right hemiplegia
6 yr, M
Age/<ex
Present
case
Reference
Childhood Vertebrobasilar Arfery Occlusion
TABLE 1
Terminal basilar
artery occlusion
Severe dementia,
hemiparesis
Septic
Mechanical?
Moderate
dysarthria and
cerebellar
deficit
C2 stenosis left
vertebral;
terminal basilar
artery
Septic
Unknown
Mechanical?
Died
Died
Mechanical?
Mechanical?
Mechanical deformation;
probable thrombotic
embolus to basilar
artery
Etiology
C1-C2 left vertebral; Severe left
C4 stenosis right
cerebellar
vertebral
deficit
Distal basilar
artery
Posterior cerebral
artery occlusion
C2 stenosis left
Horner's syndrome
vertebral; right
and cerebellar
vertebral occlusion deficit
of the foramen
magnum; basilar
and (eft posterior
cerebral
Right brachial
dysmefria
C1-C2 occlusion
left vertebral;
right vertebral
"kinked" at C2;
left posterior
cerebral artery
occlusion
Result
Right hemiparesis,
C1-C3 fused
Arteriography
C1-C2 occlusion
left vertebral
artery, partial
right basilar
artery
S
N
HINDBRAIN STROKE IN CHILDREN
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
FIOUII1
Tomogram Cl toC2. Un-united odontoid immediately posterior to
arch of Cl.
HOSPITAL COURSE
The following day, four-vessel angiography was performed,
prompted by a diagnostic impression of "arteritis." The
presence of atlanto-axial subluxation was not communicated
to the neuroradiologist so that the study was performed in
the usual hyperflexed position, causing maximum anterior
displacement of the atlas. The arteriogram revealed occlusion of the right vertebral artery at the level of C2.
Collateral vessels were seen at this level bypassing the
occluded portion of the vertebral artery and rejoining the
vessel at the rostral border of C2. The right vertebral artery
terminated in the posterior inferior cerebellar artery without
opacification of the basilar artery (fig. 4). The left vertebral
artery demonstrated aneurysmal dilatation at C2. This
vessel also terminated in the posterior inferior cerebellar
artery without filling of the basilar artery (fig. 5). Carotid injections opacified the rostral tip of the basilar artery and
both superior cerebellar arteries and posterior cerebral
arteries.
Neurosurgical consultation was again requested. It was
our impression that the arterial pathology revealed by
angiography was the result of mechanical trauma to each
vertebral artery as it crossed the transverse foramen of C2.
The occlusion of the right vertebral artery and the
aneurysmal dilatation of the left was thought to result from
chronic intermittent mechanical trauma and stretching of
each vessel by the anterior displacement of Cl upon C2. A
presumptive diagnosis of a posterior circulation stroke was
suggested.
It was decided to stabilize the patient externally in
halotraction and await maturation of his neurological
deficit. One week after admission, he was able to flex and extend the right leg against gravity and demonstrated a flicker
of movement in the right toes. Functional improvement occurred in conjunction with active physiotherapy.
Strok; Vol. 6. March-April 1975
FlOUtll
Cervical spine —flexion Anterior displacement of Cl and united
odontoid process.
Neurological improvement continued for another four
weeks, at which time the patient was ambulatory with a right
leg brace and demonstrated proximal movement against
gravity in the right upper extremity. The right hand,
however, remained plegic. Eye movements were normal.
Four-vessel angiography was repeated at this time and
revealed no change in the vertebral artery anomalies. These
films did demonstrate, however, that the basilar artery had
recanalized with filling of the superior cerebellar and
posterior cerebral arteries from the posterior circulation.
Slight narrowing of the distal basilar artery just proximal to
the origin of the superior cerebellar arteries remained (figs. 6
and 7).
At this time, a cervical spine fusion of Cl to C3 using
wire and iliac bone was performed. The patient was discharged on the tenth postoperative day after an uneventful
convalescence. Follow-up at three months revealed little improvement with persistent severe right hemiparesis, most
marked in the right upper extremity.
Discussion
Only seven children have been previously reported
with occlusive or stenotic pathology of the
vertebrobasilar system.18"21 Review of the case
material (table 1) reveals that in five of these patients
15S
FRASER, ZIMBLER
t
f
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
FIOUII4
noun 3
Right vertebral angiogram — lateral view. Occlusion of vertebral
artery at C2. collateral supply to Cl segment with distal vertebral
filling but termination in the posterior inferior cerebellar artery
(PICA).
Cervical spine — extension Normal allanlo-axial relationships
restored. Distal un-united odontoid has undergone counterclockwise rotation
no apparent cause for the vascular pathology could be
assigned and all were designated as either a congenital
or idiopathic disorder. The remaining two patients
had septicemia and obvious septic emboli to many
vessels, including the intracranial circulation. Closer
attention to this table reveals that four of the remaining five presented with syndromes strikingly similar to
the present case. All were male. Intermittent attacks
of vertigo, ataxia, and sensory motor disturbances,
presumably posterior circulation TIAs, were followed
after weeks or months by a sudden stroke-like syndrome of hemiparesis and ataxia. In case 4, a severe
fall and a documented occipital fracture preceded the
permanent stroke-like syndrome by a month. There
was no antecedent trauma in case 3 or 5, but the
patient described in case 7 experienced the onset of
sudden hemiparesis while walking home from baseball
practice where cervical trauma might have occurred.
In each of these patients, arteriography revealed
stenosis or occlusion of the vertebral arteries of one or
both sides at the level of the second cervical vertebra.
In addition, incomplete filling of the basilar artery was
156
Left vertebral angiogram — lateral view. Dilatation of vertebral
artery at C2. Vessel terminates in left PICA. No filling of basilar
artery.
S l r o t ; Vol. 6, March-April 1975
HINDBRAIN STROKE IN CHILDREN
"V \
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
i
FIOURI 7
Right vertebral angwgram four weeks later — lateral view.
Vertebral artery unchanged Basilar artery now opacified, but
narrow. Marked stenosis ofbasilar artery just proximal to origin of
superior cerebellar artery.
present in three. Cervical spine films were normal in
one case and not described in the remaining three.
These patients all survived with minor to moderate
cerebellar and brain stem deficits.
It seems apparent that our case is a clear example
of a posterior circulation stroke. Serial angiograms
revealed an occluded basilar artery which later
recanalized concomitant with minor improvement in
the patient's neurological deficit. (Anticoagulants
were not administered at any time.) We believe that
the most reasonable explanation for this
vertebrobasilar arterial lesion is traumatic and that
repeated anterior subluxation of Cl on C2 caused
mechanical deformation and occlusion of both
vertebral arteries. Thrombus formation in the
deformed vertebral arteries with distal embolization
into the basilar artery presumably caused the stroke in
our patient. Though no mention was made of cervical
spine anomalies in four previously reported patients
with almost identical findings, we wonder whether a
similar mechanism was playing an etiological role.
It is possible, even in the absence of bony
anomalies, that mechanical distortion of the vertebral
arteries may result from subluxation secondary to laxity of the ligaments connecting the atlas and axis. In
Slrok: Vol. 6, March-April 1975
Left vertebral angiogram four weeks later — lateral view. Vertebral
dilatation at C2 unchanged Basilar artery now fills tortuously with
right vertebral injection.
this instance, no radiographical changes would be apparent except on flexion and extension films.
Atlanto-axial subluxation with non-union of the
odontoid is a frequent congenital anomaly of the
spinal column. Previous series of patients with
atlanto-axial anomalies do not contain a single example of angiographically documented vertebrobasilar
pathology." 2 * Ford2 has described a 17-year-old boy
similar to the case reported here. Recurrent posterior
circulation TIAs were eventually diagnosed after
atlanto-axial instability was discovered and treated by
cervical fusion. Unfortunately, this case lacks
angiographical documentation. The patient's symptoms were recurrent, transient, and closely resembling
those reviewed above; they seem a convincing, if not
proved, example of this syndrome.
Several patients presenting with brain stem
and/or cerebellar deficits due to stroke have been
reported following cervical spine trauma1"*' w and an
even larger number following chiropractic neck
manipulation. 719 In two patients of the latter group,
angiography confirmed vertebral artery lesions at the
level of the axis,11 similar to those described above.
Schneider and Crosby3 have suggested that the
vertebral arteries are especially vulnerable to compression at three sites: (1) at any fracture dislocation
above C6, (2) at the atlanto-axial level with Cl to C2
compression, and (3) at Cl because of atlanto-axial
1975
FRASER, ZIMBLER
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
dislocation resulting from the occipital condyles
sliding forward over the articular facets of Cl.
Arteriograms in the present case, in two post-neck
manipulation cases,12 and in four children without
antecedent trauma18'19'21 revealed similar Cl to C2
arterial pathology, and confirm the potential
vulnerability of the vertebral artery at this level.
Our patient was treated by fusion of the first three
cervical vertebrae when his neurological condition
stabilized. This procedure seemed warranted to prevent future additional mechanical trauma to the
vertebral arteries and further posterior circulation
strokes. Potential cervical cord compression was also
prevented.
A recent report attempts to define angiographically prognostic indicators in patients with
basilar artery occlusion.30 These authors point out that
such patients present in two ways: (1) with abrupt
onset of coma, often leading to death, or (2) with transient symptoms of brain stem ischemia. The latter
patients are a diagnostic problem. These authors also
suggest, not surprisingly, that small or absent
collaterals from the anterior circulation carry a poor
prognosis. Basilar artery occlusion has been regarded
in the past as nearly always fatal.31 More recent
reports,30'32 however, suggest that survival is the rule.
Increased awareness of the syndrome described in
this report might lead to documentation of similar
pathology in patients with otherwise unexplained
repeated transient brain stem and cerebellar symptomatology. Appropriate x-ray studies, including flexion and extension cervical spine films and vertebral
angiography, are urged in such cases. These patients
represent an additional syndrome of extracranial
occlusive cerebrovascular disease, one in which surgical stabilization provides appropriate therapy and
removes further risk of stroke.
Summary
A patient is described with bilateral vertebral artery
anomalies at Cl to C2, with occlusion of the basilar
artery occurring in conjunction with a posterior circulation stroke. The anomalies are believed to be the
result of chronic and repeated atlanto-axial subluxation.
Review of the literature provides four previous
patients with strikingly similar clinical presentations.
All were male and all presented with intermittent
symptoms suggestive of brain stem and/or cerebellar
dysfunction. All were retrospectively diagnosed as experiencing posterior cerebral circulation transient
ischemic attacks, which culminated in a stroke with
varying degrees of static neurological deficit. Patients
with severe atlanto-axial instability are at risk for
posterior circulation injury and possible brain stem
stroke. Vertebral artery angiography should be considered in such patients.
158
References
1. Carpenter S: Injury of neck as cause of vertebral artery
thrombosis. J Neurosurg 18:849-853, 1961
2. Ford FR: Syncope, vertigo, and disturbances of vision
resulting from intermittent obstruction of the vertebral
arteries due to defect in the odontoid process and excessive
mobility of the second cervical vertebra. Bull Johns Hopkins
Hosp 91:168-173, 1952
3. Schneider RC, Crosby EC: Vascular insufficiency of brain
stem and spinal cord in spinal trauma. Neurology 9:643656, 1959
4. Schneider RC, Schemm GW: Vertebral artery insufficiency in
acute and chronic spinal trauma. J Neurosurg 1 8:348-360,
1961
5. Simeone FW, Goldberg HI: Thrombosis of vertebral artery
from hyperextension injury to the neck. J Neurosurg 29:540554, 1968
6. Svechting Rt, French LA: Posterior inferior cerebellar artery
syndrome following fracture of cervical vertebra. J
Neurosurg 12:187-189, 1955
7. Blaine ES-. Manipulative (chiropractic) dislocations of atlas.
JAMA 85:1356-1359, 1925
8. Ford FR, Clark D: Thrombosis of the basilar artery with
softenings in the cerebellum and brain stem due to manipulation of the neck. A report of two cases with one post-mortem
examination. Reasons are given to prove that damage to the
vertebral arteries is responsible. Bull Johns Hopkins Hosp
98:37-42, 1956
9. Green D, Joynt RJ: Vascular accidents to brain stem
associated with neck manipulation. JAMA 170:522-524,
1959
10. Kunkle EC, Muller JC, Odom PL: Traumatic brain stem thrombosis: Report of a case and analysis of mechanism of injury.
Ann Int Med 36:1329-1335, 1952
11. Lyness SS, Wogman AD: Neurological deficit following surgical manipulation. Surg Neurol 2:121-124, 1974
12. Mahalic T, Farhat SM: Vertebral artery injury after
chiropractic manipulation of the neck. Surg Neurol 2:125129, 1974
13. Pratt-Thomas HR, Berger KE: Cerebellar and spinal injuries
after chiropractic manipulation. JAMA 133:600-603, 1945
14. Pubek RA: Brain stem vascular accident following neck
manipulation. Wis Med J 62:141-143, 1963
15. Schwarz GA, Geiger JK, Spano AV: Posterior inferior
cerebellar artery syndrome of Wallenberg after chiropractic
manipulation. Arch Int Med 97:352-354, 1956
16. Smith RA, Estridge MN: Neurologic complications of head
and neck manipulations: Report of two cases. JAMA
182:528-531, 1962
17. Banker BQ: Cerebral vascular disease in infancy and
childhood. J Neuropath Exp Neurol 20:127-140, 1961
18. DeVivo DC, Farrell FW Jr: Vertebrobasilar occlusive disease
in children: A recognizable clinical entity. Arch Neurol
26:278-281, 1972
19. Dooley JM, Smith KR: Occlusion of the basilar artery in a 6year-old boy. Neurology 18:1034-1036, 1968
20. Fowler M: Two cases of basilar artery occlusion in childhood.
Arch Dis Child 37:78-81, 1962
21. Ouvrier RA, Hopkins IJ: Occlusive disease of the vertebral
basilar arterial system in childhood. Dev Med Child Neurol
12:186-192, 1970
22. Bull JM: The syndrome of atlanto-axial dislocation. Clin Proc
1:336-345, 1942
23. Dunbar HS, Ray BS: Chronic atlanto-axial dislocations with
Stroke, Vol. 6, March-April 1975
HINDBRAIN STROKE IN CHILDREN
24.
25.
26.
27.
late neurological manifestations. Surg Gynec Obstet
113:757-762, 1961
Garber JN: Abnormalities of the atlas and axis vertebrae —
congenital and traumatic. J Bone Joint Surg 4 6 A : 17821791, 1964
MacCrae DL: Bony abnormalities in the region of the
foramen magnum: Correlations of the anatomic and
neurological findings. Acta Radiol 40:335-354, 1953
Paradis GR, Janes JM: Post traumatic atlanto-axial instability: The fate of the odontoid process fracture in 46
cases. J Trauma 13:359-367, 1973
Roberts A, Wickstrom J: Prognosis of odontoid fractures.
Acta Orthop Scand 44:21-30, 1973
28. Shatzker J, Rorabeck CH, Daddell JP: Fractures of the dens
(odontoid process). An analysis of 37 cases. J Bone Joint
Surg 53B:392-404, 1971
29. Nagler W: Vertebral artery obstruction by hyperextension of
the neck: Report of 3 cases. Arch Phys Med Rehab 54:237240, 1973
30. Moscow NP, Newton TH: Angiographic implications in
diagnosis and prognosis of basilar artery occlusion. Amer J
Roentgen 119:597-604, 1973
31. Kubik CS, Adams RD: Occlusion of the basilar artery: A
clinical study. Brain 69:6-15, 1946
32. Fields WS, Ratinor G, Weibel J, et al: Survival following
basilar artery occlusion. Arch Neurol 15:463-471, 1966
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
Stroke, Vol. 6, March-April 1975
159
Hindbrain Stroke in Children Caused by Extracranial Vertebral Artery Trauma
RICHARD A. R. FRASER and SEYMOUR M. ZIMBLER
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
Stroke. 1975;6:153-159
doi: 10.1161/01.STR.6.2.153
Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
Copyright © 1975 American Heart Association, Inc. All rights reserved.
Print ISSN: 0039-2499. Online ISSN: 1524-4628
The online version of this article, along with updated information and services, is located on
the World Wide Web at:
http://stroke.ahajournals.org/content/6/2/153
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally
published in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the
Editorial Office. Once the online version of the published article for which permission is being requested is
located, click Request Permissions in the middle column of the Web page under Services. Further
information about this process is available in the Permissions and Rights Question and Answer document.
Reprints: Information about reprints can be found online at:
http://www.lww.com/reprints
Subscriptions: Information about subscribing to Stroke is online at:
http://stroke.ahajournals.org//subscriptions/