Neurology Asia 2017; 22(3) : 185 – 191

REVIEW ARTICLE

The pathogenic mechanisms of motor weakness

following aneurysmal subarachnoid hemorrhage:
A review
Sung Ho Jang MD, Han Do Lee MS
Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University,
Taegu, Korea

Abstract

Motor weakness is one of the neurological complication that can occur after aneurysmal subarachnoid
hemorrhage (SAH); incidence of motor weakness of 14~29% has been reported. Detailed information
on the pathogenic mechanism of motor weakness is essential for brain rehabilitation because it enables
estimation of the severity of injury, establishment of scientific rehabilitative strategies, and prediction
of motor outcomes by clinicians. However, the exact pathogenic mechanisms of motor weakness
following aneurysmal SAH have not been clearly elucidated. In this article, 14 previous studies on
pathogenic mechanisms in patients with aneurysmal SAH were reviewed according to the location of
the lesion (cerebral cortex, brainstem, spinal cord, and peripheral nerve). The following pathogenic
mechanisms have been suggested: vasospasm, cerebral ischemia, hydrocephalus, compression of
cerebral cortex, neural injury, spinal cord infarction, and radiculo-neuropathy. Considering the high
incidence of aneurysmal SAH and motor weakness following aneurysmal SAH, we believe that the
pathogenic mechanisms of motor weakness have been relatively understudied. More effort should be
taken to investigate this important topic.

Keywords: Subarachnoid hemorrhage, aneurysm, motor weakness, hemiplegia, paraplegia, quadriparesis.

INTRODUCTION weakness in patients with aneurysmal SAH have

been suggested: vasospasm, cerebral ischemia,
Aneurysmal subarachnoid hemorrhage (SAH)
hydrocephalus, compression of neural structure,
involves bleeding into the subarachnoid space
neural injury, spinal cord infarction, and peripheral
between the arachnoid membrane and the pia
neuropathy.3,7-19
mater covering the brain following rupture of
an aneurysm. Motor weakness is one of the
In this article, previous studies on the
pathogenic mechanisms of motor weakness in
neurological complications that can occur after
patients with SAH following aneurysmal rupture
aneurysmal SAH, along with somatosensory
were reviewed. Relevant studies were identified
deficit, cranial nerve dysfunction, visual
using two electronic databases (Pubmed and
dysfunction, and consciousness disturbance.1-3
MEDLINE) from 1966 to 2014. The following
Incidence of motor weakness in aneurysmal
key words were used: SAH, aneurysm, motor
SAH of 14~29% has been reported.1,3-6 Detailed
weakness, hemiplegia, paraplegia, paraparesis,
information on the pathogenic mechanism of
and quadriparesis. This review was limited to
motor weakness is essential for brain rehabilitation
studies that included convincing evidence on the
because it enables estimation of the severity of
pathogenic mechanisms of motor weakness in
injury, establishment of scientific rehabilitative
patients with SAH, therefore, studies that did not
strategies, and prediction of motor outcomes
show definite evidence of motor weakness were
by clinicians.7 However, the exact pathogenic
excluded.20,21 Finally, 14 studies were selected
mechanisms of motor weakness following
and classified according to the location of the
aneurysmal SAH have not been clearly elucidated.
lesion and pathogenic mechanisms, as follows:
The following pathogenic mechanisms of motor

Address correspondence to: Dr Han Do Lee, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University. 317-1,
Daemyungdong, Namku, Taegu, 705-717, Republic of Korea. Tel: 82-53-620-4098, e-mail: [email protected]

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1) cerebral cortex (8 papers); vasospasm and weakness of both legs as the first symptom of a
cerebral ischemia - 6 papers, hydrocephalus - one ruptured anterior communicating artery (ACoA)
paper, and compression of the cerebral cortex- one aneurysm. 9 The patient became paraplegic
paper, 2) brainstem (3 papers); neural injury - 3 within 12-36 hours after onset and the brain
papers, and 3) spinal cord and peripheral nerve CT showed small lacunar ischemic hypodense
(three papers); spinal cord infarction - 2 papers lesions in both high frontoparietal parasagittal
and peripheral neuropathy - one paper.3,7-19 A flow regions. The authors concluded that insufficient
diagram of the study selection process is shown blood perfusion of both paracentral areas was
in Figure 1. the cause of paraplegia. In 1995, in a study by
Greene et al. for clinicopathologic evaluation
CEREBRAL CORTEX of patients with paraparesis following rupture
of ACoA aneurysms11, 7 of 101 patients with
Eight papers on lesions in the cerebral cortex
SAH from ruptured ACoA aneurysms were
were classified as follows: three pathogenic
recruited. Angiographic evidence of vasospasm
mechanisms: vasospasm and cerebral ischemia
in the anterior cerebral artery (ACA) distribution
(6 papers), hydrocephalus (one paper), and
was documented in all cases, and paraparesis
compression of the cerebral cortex (one
persisted beyond the angiographic resolution of
paper).8,9,11-15,17
vasospasm: motor weaknesses developed within
7 days of aneurysm rupture and persisted for a
Vasospasm and cerebral ischemia
mean duration of 39 days. Pathologic analysis
Vasospasm and cerebral ischemia are the most of autopsy material from one patient showed
commonly reported pathogenic mechanisms of laminar necrosis in the parasagittal distribution
motor weakness in patients with aneurysmal of the ACA, indicating microvascular ischemia
SAH (6 of 14 papers).8,9,11-15,17 In 1986, Maiuri and infarction. All patients showed cognitive
et al. reported on a patient who showed (memory impairment) and affective (affect

Figure 1: Flow diagram of study selection. SAH; subarachnoid hemorrhage.

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flattening) manifestations. The authors proposed required urgent ventriculostomy for hydrocephalus
that this combination of lower limb weakness (5 patients went on to require permanent shunt
with cognitive and affective dysfunctions be placement). Five of the 6 patients showed gradual
referred to as the ACoA aneurysm paraparesis resolution of their paraparesis over the course
syndrome. Subsequently, Kombos et al. reported of 3 to 6 months: one patient - walker gait at 6
on a patient who developed paraplegia one week months, one patient - wide based gait at 3 years,
after rupture of an ACoA aneurysm.12 Brain 2 patients - normal gait at 3 weeks and 6 months,
CT showed cerebral infarction in the bilateral respectively, one patient - abnormal tandem gait at
frontomedial areas, which are supplied by the 16 months, and one patient - minimal improvement
ACAs. In 2000, Warrenburg et al. reported on at 3 weeks. Based on these results, they suggested
a patient who showed symmetrical proximal that hydrocephalus was the cause of paraparesis
muscle weakness of the legs (Medical Research of these patients.
Council grade: 4).13 Brain MRI at nine days after
the initial headache showed residual blood in the Compression of cerebral cortex
anterior interhemispherical fissure. Brain MR
In 1984, Kudo and Uno reported on a patient who
angiography showed an aneurysm of the ACoA
presented with ipsilateral hemiparesis following
and extreme spasm of both ACAs. Consequently,
a ruptured middle cerebral artery aneurysm.8
they assumed that the proximal weakness of the
The patient had a moderate right hemiparesis
legs was the result of ischemia of the medial
with the upper extremity weaker than the lower
parts of the frontal lobes secondary to spasm of
extremity. Brain CT showed SAH in the basal
both ACAs. In 2005, Endo et al. reported on 9 of
cistern, ambient cistern, and the cistern of the
178 patients with ruptured aneurysms of ACoA
Sylvian fissure: the SAH was most severe in the
or ACA who presented with paraparesis.14 In 4
right cistern of the Sylvian fissure. Therefore, they
of the 9 patients, diffusion-weighted brain MRI
concluded that the ipsilateral hemiparesis was
performed within 48 hours of onset of SAH
most likely due to compression of the secondary
showed high-intensity lesions in the medial aspects
motor area in the island of Reil by SAH.
of the bilateral frontal lobes, which were supplied
by the ACAs. Normal to subnormal values
BRAINSTEM
of apparent diffusion coefficient (ADC) were
observed for these high-intensity lesions. Most
Neural injury
high-intensity lesions recovered and did not result
in final lesions, regardless of the ADC values, To the best of our knowledge, three studies on
but some lesions with subnormal ADC values neural injury at the brainstem level have been
resulted in cerebral infarction. Three patients reported.3,7,19 In 1992, Ferrante et al. reported on
showed complete recovery and the remaining a patient who showed contralateral leg weakness
one patient showed partial recovery. Teufack et following SAH from an aneurysm of the first
al. recently reported on a patient who presented PICA segment.3 The patient showed complete
with SAH with intraventricular extension.17 The recovery from the motor weakness at three months
patient was treated with coil embolization of an after onset. They assumed that the corticospinal
ACoA aneurysm. Postoperatively, the patient tract of the contralateral leg was affected by
was found to have weakness of both ankle and SAH and/or spasm of branches of the PICA. In
toe dorsiflexion, and brain MRI showed acute 2012, Yeo et al. investigated corticospinal tract
infarction in the parasagittal bifrontal gyriform injury in patients with spontaneous SAH using
areas. diffusion tensor imaging (DTI).7 Twenty two
patients who showed quadriparesis (19 patients)
Hydrocephalus and hemiparesis (3 patients) with no lesion in the
cerebral cortex were recruited and DTI parameters
In 2008, Johnston et al. reported on six of 695
of the corticospinal tract were measured. They
patients who presented with profound paraparesis
found partial injury of the whole corticospinal
after SAH following rupture of an aneurysm
tract in patients with SAH and the injury level
(ACoA: one patient, posterior communicating
appeared to be at the midbrain. They suggested
artery (PCoA): one patient, posteroinferior
that injury of the corticospinal tract occurred at the
cerebellar artery [PICA]: 2 patients, and ACoA
midbrain due to its close proximity to the cistern
and internal carotid artery: one patient).15 These
by mechanical (increased intracranial pressure or
patients showed hydrocephalus and all patients
direct mass effect by SAH) or chemical (blood clot

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Table 1: Previous studies on motor weakness in patients with aneurysmal subarachnoid hemorrhage

Lesion Pathogenic
Authors Publication Patients Weakness Evaluation tool Results
location mechanism year

Cerabral Vasospasm &  

Cortex Cerebral Maiuri et al.8 1986 1 Paraplegia Brain CT Cerebral
ischemia ischemia

Cerebral
Greene et al. 9
1995 7 Paraparesis angiography Vasospasm
Microvascular
Pathology ischemia

Kombos Cerebral
et al. 10 1996 1 Paraplegia
infarction Brain CT

Symmetrical
Warrenburg
et al. 11 2000 1 proximal leg Brain MRA Vasospasm
weakness

Diffusion- High intensity

weighted brain lesion in
Endo et al. 12
2005 9 Paraparesis MRI bilateral medial
(4 Patients) frontal lobes

Teufack Bilateral foot Brain MRI Acute infarction
et al.13 2011 1 drop

Johnson 2008 6 Paraparesis Brain CT Hydrocephalus

Hydrocephalus et al.14

Compression Compression of
of cerebral Kudo & Uno15 1984 1 Ipsilateral Brain CT secondary motor
cortex hemiparesis area by SAH

Contralateral CST injury by

Brainstem Neural injury Ferrante et al. 2
1992 1 leg weakness Brain CT SAH

Quadriparesis CST injury at

Yeo et al. 7
2012 22 or hemiparesis DTI midbrain

Contralateral
Jang et al. 16 2014 12 proximal DTI CRP injury at
weakness midbrain

Spinal
cord & Spinal cord Kashiwagi Unilateral lesion
Peripheral infarction 1992
et al. 19 1 Paraplegia MRI in upper spinal
nerve cord

Spinal cord
Krishna et al. 17
2012 1 Paraplegia Spine MRI infarction

Radiculo- Leg Radiculo-

Kostov18 2010 2
neuropathy monoparesis Lumbar MRI neuropathy

CT: computed tomography, MRA: magnetic resonance angiography, MRI: magnetic resonance imaging, SAH: subarachnoid hemorrhage,
DTI: diffusion tensor imaging, CST: corticospinal tract, CRP: corticoreticular pathway.

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itself can cause extensive damage or release of ACoA.18 Nine days after aneurysmal rupture, the
potentially damaging substances, such as free iron, patient was found to be paraplegic. Spine MRI
which may generate free radicals or inflammatory showed subarachnoid blood in the lumbo-sacral
cytokines) factors by SAH.22-25 Jang et al. recently subarachnoid space along with signal abnormality
reported injury of the corticoreticular pathway within the spinal cord at the level of the conus
(CRP) in 17 patients who showed contralateral extending from T11-L1 and multiplanar spin echo
proximal weakness with no lesion in the cerebral diffusion weighted imaging confirmed spinal cord
cortex among 137 patients with aneurysmal SAH stroke in this region.
(ACoA-14 patients, PCoA: one patient, ACA: one
patient, and internal carotid artery: one patient. Radiculo-neuropathy
Twelve (70.6%) of 17 patients and 18 (52.9%)
of 34 hemispheres showed a discontinuation of In 2010, Kostov et al. reported on two
the CRP at the midbrain level. Therefore, they patients who presented with acute SAH from
concluded that either mechanical or chemical a ruptured intracranial aneurysm (PCoA and
injury of the corticoreticular pathway by SAH had ophthalmic artery).16 Both patients were treated
occurred at the midbrain, although the location of by endovascular coil embolization, and both
the corticoreticular pathway is deeper than that developed delayed unilateral lower extremity
of the corticospinal tract in the midbrain.22,26,27 weakness without associated symptoms, which
resolved over the ensuing months. Lumbar MRI
showed significant layering of bold products in
SPINAL CORD AND PERIPHERAL NERVE
the dependent portion of the thecal sac from L3
down to the S2 level. Based on this finding, they
Spinal cord infarction
concluded that the painless neuropathy likely
Two studies on spinal cord infarction following resulted from nerve root irritation from abundant
aneurysmal SAH have been reported.10,18 In 1992, subarachnoid blood in the lumbar cistern.
Kashiwagi et al. reported on a patient who showed
paraplegia following a ruptured aneurysm of the CONCLUSION
distal PICA.10 The patient regained walking ability
at 3 months after onset and returned to walking In this mini-review article, 14 previous studies
at 6 months after onset. MRI showed a vascular on pathogenic mechanisms of motor weakness
lesion in the subarachnoid space adjacent to the in patients with aneurysmal SAH were reviewed
spinal cord at the level of C1. Based on this finding, according to the location of the lesion (cerebral
the authors concluded that the patient’s paraplegia cortex, brainstem, spinal cord, and peripheral
was caused by a unilateral lesion located between nerve). The pathogenic mechanisms of motor
the cervicomedullary junction and the C2 level, weakness were summarized as follows: vasospasm,
involving both crossed and uncrossed CST fibers cerebral ischemia, hydrocephalus, compression
projecting to the lower extremities. Krishna et al. of the cerebral cortex, neural injury, spinal
recently reported on a patient who showed sudden cord infarction, and peripheral neuropathy.3,7-19
onset of SAH by the rupture of an aneurysm of Figure 2 and Table 2 showed a pie chart and

Figure 2: A pie chart about the number of studies and patients.

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Table 2: A cross-table about the number of studies and patients in each pathogenic mechanism

Number of
Syndrome Mechanism Remarks
patients
Paraparesis/paraplegia Vasospasm and cerebral ischemia 18
Hydrocephalus 6
Spinal cord infarction 2
Symmetrical proximal leg
Vasospasm and cerebral ischemia 1
weakness

Bilateral foot drop Vasospasm and cerebral ischemia 1

Quadriparesis or hemiparesis Brainstem neural injury 22

Compression of cerebral cortex by

Ipsilateral hemiparesis 1
SAH

Contralateral proximal
Brainstem neural injury 12
weakness

Contralateral leg weakness Brainstem neural injury 1

Leg monoparesis Radiculo- neuropathy 2

table about the number of studies and patients REFERENCES

in each pathogenic mechanism. Considering the 1. Sarner M, Rose F. Clinical presentation of ruptured
high incidence of aneurysmal SAH and motor intracranial aneurysm. J Neurol Neurosurg Psychiatry
weakness following aneurysmal SAH, we believe 1967; 30:67-70.
that there is inadequate study on the pathogenic 2. van Gijn J, van Dongen KJ, Vermeulen M, et al.
mechanisms of the motor weakness.1-6 In addition, Perimesencephalic hemorrhage: a nonaneurysmal and
some studies did not show clear association with benign form of subarachnoid hemorrhage. Neurology
motor weakness and evidence for a pathogenic 1985; 35:493-7.
3. Ferrante L, Acqui M, Mastronardi L, et al. Posterior
mechanism.8,13,15 Therefore, further studies on inferior cerebellar artery (PICA) aneurysm presenting
this topic should be encouraged. In particular, with SAH and contralateral crural monoparesis: a
studies using DTI, which has a unique advantage case report. Surg Neurol 1992; 38:43-5.
in finding lesions at the subcortical level, would 4. Hudgins RJ, Day AL, Quisling RG, et al. Aneurysms
be helpful. In addition, further studies on the of the posterior inferior cerebellar artery. A clinical
non-corticospinal tract neural pathways for and anatomical analysis. J Neurosurg 1983; 58:381-7.
5. Lee KS, Gower DJ, Branch CL, Jr., et al. Surgical
motor function, such as the corticoreticulospinal
repair of aneurysms of the posterior inferior cerebellar
tract and corticorubrospinal tract should also be artery--a clinical series. Surg Neurol 1989; 31:85-91.
encouraged. 6. Salcman M, Rigamonti D, Numaguchi Y, et al.
Aneurysms of the posterior inferior cerebellar artery-
ACKNOWLEDGEMENT vertebral artery complex: variations on a theme.
Neurosurgery 1990; 27:12-20; discussion 20-1.
This work was supported by the National 7. Yeo SS, Choi BY, Chang CH, et al. Evidence of
Research Foundation (NRF) of Korea Grant Corticospinal Tract Injury at Midbrain in Patients
funded by the Korean Government (MSIP) With Subarachnoid Hemorrhage. Stroke 2012;
(2015R1A2A2A01004073). 43:2239-41.
8. Kudo T, Uno T. Ipsilateral hemiparesis caused by
subarachnoid hemorrhage in a patient with a ruptured
middle cerebral artery aneurysm: a case report.
Neurosurgery 1984; 15:727-9.

190
 9. Maiuri F, Gangemi M, Corriero G, et al. Anterior diffusion coefficient in normal-appearing brain tissue
communicating artery aneurysm presenting with after treatment. Radiology 2007; 242:518-25.
sudden paraplegia. Surg Neurol 1986; 25:397-8. 27. Yeo SS, Chang MC, Kwon YH, et al. Corticoreticular
10. Kashiwagi S, Tsuchida E, Shiroyama Y, et al. pathway in the human brain: diffusion tensor
Paraplegia due to a ruptured aneurysm of the tractography study. Neurosci Lett 2012; 508:9-12.
distal posterior inferior cerebellar artery. J Neurol
Neurosurg Psychiatry 1992; 55:836-7.
11. Greene KA, Marciano FF, Dickman CA, et al.
Anterior communicating artery aneurysm paraparesis
syndrome: clinical manifestations and pathologic
correlates. Neurology 1995; 45:45-50.
12. Kombos T, Meisel HJ, Janz C, et al. Paraplegia
due to rupture of an anterior communicating artery
aneurysm. Consequence of a rare anatomic variant
of the A2 segment. Interv Neuroradiol 1996; 2:53-7.
13. van de Warrenburg B, Vos P, Merx H, et al. Paroxysmal
leg weakness and hearing loss in a patient with
subarachnoid hemorrhage. Eur Neurol 2000; 44:186-7.
14. Endo H, Shimizu H, Tominaga T. Paraparesis
associated with ruptured anterior cerebral artery
territory aneurysms. Surg Neurol 2005; 64:135-9;
discussion 39.
15. Johnston JM, Chicoine MR, Dacey RG, Jr.,
et al. Aneurysmal subarachnoid hemorrhage,
hydrocephalus, and acute paraparesis. Neurosurgery
2008; 63:1119-24; discussion 24.
16. Kostov D, Jankowitz B, Kanaan H, et al. Lower
extremity monoparesis after aneurysmal subarachnoid
hemorrhage. Clin Neurol Neurosurg 2010; 112:710-2.
17. Teufack S, Gonzalez F, Rosenwasser R, et al. Bilateral
footdrop after treatment of an anterior communicating
artery aneurysm: a case report and review of the
literature. Neurosurgery 2011; 68:373-6;discussion
76.
18. Krishna V, Lazaridis C, Ellegala D, et al. Spinal cord
infarction associated with subarachnoid hemorrhage.
Clin Neurol Neurosurg 2012; 114:1030-2.
19. Jang SH, Choi BY, Kim SH, et al. Injury of
the corticoreticular pathway in subarachnoid
haemorrhage after rupture of a cerebral artery
aneurysm. J Rehabil Med 2015; 47:133-7.
20. Logue V. Surgery in spontaneous subarachnoid
haemorrhage; operative treatment of aneurysms on
the anterior cerebral and anterior communicating
artery. Br Med J 1956; 1:473-9.
21. Paulson G. Subarachnoid Hemorrhage Associated
with Paraplegia. Dis Nerv Syst 1963; 24:419-22.
22. Chua CO, Chahboune H, Braun A, et al. Consequences
of intraventricular hemorrhage in a rabbit pup model.
Stroke 2009; 40:3369-77.
23. Jang SH. Somatotopic arrangement and location of
the corticospinal tract in the brainstem of the human
brain. Yonsei Med J 2011; 52:553-7.
24. Kwon HG, Hong JH, Jang SH. Anatomic location
and somatotopic arrangement of the corticospinal
tract at the cerebral peduncle in the human brain.
AJNR Am J Neuroradiol 2011; 32:2116-9.
25. Yeo SS, Choi BY, Chang CH, et al. Periventricular
white matter injury by primary intraventricular
hemorrhage: a diffusion tensor imaging study. Eur
Neurol 2011; 66:235-41.
26. Liu Y, Soppi V, Mustonen T, et al. Subarachnoid
hemorrhage in the subacute stage: elevated apparent

191