Subarachnoid Hemorrhage: Continuumaudio Interview Available Online

Subarachnoid REVIEW ARTICLE

Hemorrhage C O N T I N U UM AUDIO
INTERVIEW AVAILABLE
ONLINE
By Susanne Muehlschlegel, MD, MPH, FNCS, FCCM
CITE AS:
CONTINUUM (MINNEAP MINN)
2018;24(6, NEUROCRITICAL CARE):
ABSTRACT 1623–1657.
PURPOSE OF REVIEW: This article reviews the epidemiology, clinical
Address correspondence to
presentation, diagnosis, and management of patients with aneurysmal Dr Susanne Muehlschlegel,
subarachnoid hemorrhage (SAH). SAH is a type of hemorrhagic stroke and Departments of Neurology,
is a neurologic emergency with substantial morbidity and mortality. This Anesthesia/Critical Care &
Surgery, University of
article reviews the most common and potentially life-threatening Massachusetts Medical School,
Downloaded from http://journals.lww.com/continuum by BhDMf5ePHKbH4TTImqenVMtmbmyf2CDPUCCzc+eo5gXmRZwBf+0pucS1qla6hTrq on 12/06/2018
neurologic and medical complications to promote their early recognition University Campus, S-5, 55 Lake
and prevent secondary brain injury. Ave N, Worcester, MA 01655,
susanne.muehlschlegel@
umassmemorial.org.
RECENT FINDINGS: Over the past 30 years, the incidence of SAH has remained
RELATIONSHIP DISCLOSURE:
stable; yet, likely because of improved care in specialized neurocritical
Dr Muehlschlegel has received
care units, discharge mortality has considerably decreased. Two research/grant support from the
consensus guidelines by the American Heart Association/American Stroke National Institutes of Health/
National Institute of Child Health
Association and the Neurocritical Care Society have outlined best and Human Development and
practices for the management of patients with SAH. The most important the Prize for Academic
recommendations include admission of patients to high-volume centers Collaboration and Excellence
(PACE) from the University of
(defined as more than 35 SAH admissions per year) under the management Massachusetts Memorial
of a multidisciplinary, specialized team; expeditious identification and Medical Group. Dr Muehlschlegel
treatment of the bleeding source with evaluation by a multidisciplinary receives partial research salary
support as the site principal
team consisting of cerebrovascular neurosurgeons, neuroendovascular investigator for the INTREPID
specialists, and neurointensivists; management of patients in a (Impact of Fever Prevention
Continued on page 1657
neurocritical care unit with enteral nimodipine, blood pressure control,
euvolemia, and close monitoring for neurologic and medical
UNLABELED USE OF
complications; and treatment of symptomatic cerebral vasospasm/ PRODUCTS/INVESTIGATIONAL
delayed cerebral ischemia with induced hypertension and endovascular USE DISCLOSURE:
therapies. This article also highlights new insights of SAH pathophysiology Dr Muehlschlegel discusses
the unlabeled/investigational
and provides updates in the management approach. short-term use of
antifibrinolytics (ε-aminocaproic
SUMMARY: SAH remains a neurologic emergency. Management of patients acid and tranexamic acid) for
the treatment of early aneurysm
with SAH includes adherence to published guidelines, but some areas of bleeding, the use of
SAH management remain understudied. Clinical trials are required to fludrocortisone for the
treatment of cerebral salt
elucidate the role of these controversial management approaches in
wasting syndrome after
improving patient outcomes. subarachnoid hemorrhage, the
use of levetiracetam for seizure
prophylaxis, and the use of
INTRODUCTION milrinone, nicardipine, and
N
verapamil as endovascular
ontraumatic subarachnoid hemorrhage (SAH) is a type of therapy using intraarterial
hemorrhagic stroke most commonly due to the rupture of saccular vasodilators for the treatment
(berry) aneurysms and comprises 3% of all stroke types.1 While a of subarachnoid hemorrhage.
17% to 50% decrease in the worldwide case fatality rate has been © 2018 American Academy
reported in the last 2 to 3 decades, thought to be due to more rapid of Neurology.
CONTINUUMJOURNAL.COM 1623
Copyright © American Academy of Neurology. Unauthorized reproduction of this article is prohibited.

SUBARACHNOID HEMORRHAGE
recognition and improved treatment strategies, the prehospital and 30-day

mortality rates remain high (15% and 35%, respectively).2,3 The annual incidence
of aneurysmal SAH has not declined, affecting 9/100,000 people in the
United States and with approximately 600,000 cases worldwide.4
Despite a decline in the mortality, SAH remains a highly morbid disease.
Survivors are commonly left with permanent disability, cognitive deficits
(particularly executive functioning and short-term memory), and mental health
symptoms (eg, depression, anxiety), resulting in a significant reduction in
health-related quality of life, which has been reported to occur in 35% of patients
1 year after SAH.5–7 The average age at aneurysm rupture is 53 years; SAH onset
at this young age results in a high societal cost and a number of years of
lost productivity.8
The most common cause for SAH is a ruptured cerebral aneurysm (85%);
however, despite modern neuroimaging techniques, 10% of SAHs may not
reveal a bleeding source, while the minority of cases (5%) may be due to
other vascular causes (eg, arteriovenous malformation, arteriovenous fistula,
reversible cerebral vasoconstriction syndrome [RCVS]).9 Particularly in RCVS,
the presence of high-convexity SAH, rather than SAH in the basal cisterns, in
addition to the typical “sausage shape” areas of constriction/vasodilation on
vessel imaging has been described.10
TABLE 3-1 Risk Factors for Subarachnoid Hemorrhagea
Modifiable Risk Factors

◆ Hypertension
◆ Smoking
◆ Heavy alcohol use
◆ Sympathomimetic drug use (eg, cocaine)
Nonmodifiable Risk Factors
◆ Increasing age (peak in fifth and sixth decade)
◆ Female sex
◆ African American ethnicity
◆ Hispanic ethnicity
◆ Japanese or Finnish ethnicity
◆ Prior history of subarachnoid hemorrhage
◆ Family history of subarachnoid hemorrhage
◆ History of aneurysm in two or more first-degree relatives
◆ Autosomal dominant polycystic kidney disease
◆ Type IV Ehlers-Danlos syndrome
◆ Cerebral aneurysms of more than 7 mm in diameter
a
Modified with permission from Suarez JI, Continuum (Minneap Minn).12
© 2015 American Academy of Neurology.
1624 DECEMBER 2018

Several epidemiologic and genetic risk factors for SAH have been identified. KEY POINTS
Notably, SAH is predominant in women (female to male ratio of 1.6:1), African
● Despite a decline in the
Americans, and Hispanics.9 Hypertension, smoking, and excess alcohol intake mortality, subarachnoid
are modifiable risk factors that individually double the risk of SAH.9,11 Several hemorrhage remains a highly
other nonmodifiable and genetic risk factors have emerged (TABLE 3-1).1,9,12–14 morbid disease.
Patient counseling on the modifiable risk factors is recommended to reduce the
● In patients with
risk of SAH.
subarachnoid hemorrhage,
Current guidelines recommend screening for aneurysms if the patient has two aneurysm rupture occurs at
or more first-degree relatives with aneurysms or SAH.15–18 This is based on an average age of 53 years.
several long-term cohort screening studies from the Familial Intracranial This young age at onset
Aneurysm study and the International Study of Unruptured Intracranial results in a high societal cost
and number of years of
Aneurysms.15–18 Notably, siblings are more likely than children of patients productivity lost.
with SAH to have an unruptured intracranial aneurysm detected.
A plethora of genetic studies have emerged for unruptured and ruptured ● The most common cause
intracranial aneurysms using linkage and genome-wide association approaches. for subarachnoid
hemorrhage is a ruptured
The American Heart Association’s “Guidelines for the Management of Patients cerebral aneurysm (85%);
With Unruptured Intracranial Aneurysms” provides a brief overview of the however, 10% of
current state of genetics in intracranial aneurysms and SAH.19 While a subarachnoid hemorrhages
meta-analysis of both unruptured and ruptured intracranial aneurysms may not reveal a bleeding
source, while the minority of
identified the interleukin-6 (IL6) gene polymorphism G572C (chromosome 7)
cases (5%) may be due to
to have an elevated risk for aneurysm formation, no predominant genetic risk other vascular causes.
factor has been identified. Several other single-nucleotide polymorphisms
have been associated with aneurysm formation, with the strongest associations ● Subarachnoid
on chromosome 9 (near CDKN2B antisense inhibitor gene), chromosome 8 hemorrhage is predominant
in women, African
(near the SOX17 transcription regulator gene), and chromosome 4 (near the Americans, and Hispanics.
EDNRA gene).19 Hypertension, smoking, and
Controversy surrounds the heritability of aneurysms and SAH, and several excess alcohol intake are
studies, including a twin study, have suggested that environmental risk factors modifiable risk factors that
individually double the
(many of which are modifiable) are far more important than genetic or familial risk of subarachnoid
inheritance.20–22 A recent review suggests that familial does not equal genetic hemorrhage.
because of the familial aggregation of risk factors (such as smoking and
hypertension).20 Currently, routine genetic screening is not performed. ● Current guidelines
recommend screening for
SAH remains one of the top neurologic emergencies treated in a neurocritical
aneurysms if the patient has
care unit. Neurologists should familiarize themselves with this highly morbid two or more first-degree
disease, particularly in light of the emerging science on acute brain injury after relatives with aneurysms or
SAH and changes in the classic teaching of the etiology of cerebral vasospasm and subarachnoid hemorrhage.
delayed cerebral ischemia.
● Subarachnoid
The acute phase of SAH can be divided into two disease phases (TABLE 3-2): hemorrhage typically
(1) prompt evaluation, recognition, and diagnosis23; immediate transfer to presents with a sudden and
appropriate SAH centers13,24; and rapid treatment of the bleeding source25,26 and severe headache (“worst
(2) close monitoring in a neurocritical care unit with expertise in SAH and overall headache of life”), which is
distinctly different from
good neurocritical care that adheres to existing management guidelines to usual headaches.
prevent or ameliorate secondary neurologic and medical complications.13,24
CLINICAL PRESENTATION
SAH typically presents with a sudden and severe headache (often described as
the “worst headache of life”), which is distinctly different from usual headaches
and is often accompanied by loss of consciousness, nausea, vomiting,
photophobia, and neck pain (CASE 3-1). A small proportion of patients may
experience a headache without many or any of the associated symptoms

(sentinel headache) and may either not seek medical attention or are
misdiagnosed, thereby remaining unrecognized, with a high risk for major
life-threatening rebleeding within a short period of time (hours to days).23,27,28
Other less typical presenting signs may be seizures, acute encephalopathy, and
concomitant subdural hematoma with or without associated head trauma (due to
the SAH-related syncope), which may make a diagnosis of aneurysmal SAH
more difficult.23
The physical examination should include determination of the level of
consciousness and the patient’s score on the Glasgow Coma Scale, evaluation for
meningeal signs, and presence of focal neurologic deficits. In cases with unusual
presentation or uncertainty, funduscopic evaluation may be helpful. Intraocular
hemorrhage associated with SAH (Terson syndrome) is associated with
increased mortality and may be seen in 40% of patients with SAH.29
Transient elevation in intracranial pressure (ICP) is the cause of nausea,
vomiting, and syncope and may be associated with additional cardiac and
pulmonary complications after SAH. The intraocular hemorrhages in Terson
syndrome are thought to be due to the sudden elevation in the ICP. When ICP
elevations are severe and sustained, coma and rapid deterioration to brain death
can result.
DIAGNOSIS
Several diagnostic modalities may be used for the diagnosis of SAH.
Head Computed Tomography

The most rapidly available and appropriate initial diagnostic test for patients with
suspected SAH is a noncontrast head CT (CASE 3-1). It is important to correlate
head CT findings to the time of headache onset, as the sensitivity of head CT
changes over the first 7 days from 93% (first 6 hours), to close to 100% (first
TABLE 3-2 Two Phases of Caring for a Patient With Subarachnoid Hemorrhage
Phase 1: Diagnosis and Aneurysm Treatment (Minutes to Hours)

◆ Recognize that subarachnoid hemorrhage may be present
◆ Aggressive blood pressure control (systolic blood pressure of less than 160 mm Hg)
◆ Rapid diagnostics
◆ Rapid initiation of aneurysm treatment (if not at a high-volume center, transfer to one)
◆ Secure aneurysm (clip or coil)
Phase 2: Vasospasm Period and Prevention of Delayed Cerebral Ischemia (Days to Weeks)
◆ Admit to neurocritical care unit specialized in subarachnoid hemorrhage care
◆ Hemodynamic and oxygenation monitoring
◆ Guideline-driven, protocolized neurocritical care
◆ Clinical examination and monitoring for vasospasm
◇ If available, daily transcranial Doppler trend evaluation
◇ If available, multimodality brain monitoring
◇ If symptomatic vasospasm, medical and interventional therapy
1626 DECEMBER 2018

12 hours), to 93% (first day), to less than 60% (at 7 days).30 The characteristic KEY POINTS
appearance of hyperdense blood in the basal cisterns or sylvian, interhemispheric,
● Physical examination of a
and interpeduncular fissures should immediately lead to the suspicion of an patient with subarachnoid
aneurysmal etiology. In fact, any SAH on head CT, especially in the absence of a hemorrhage should include
trauma history, should prompt further vessel imaging. In addition to the determination of the level of
presence of SAH, clinicians should also evaluate the head CT for presence of consciousness and the
patient’s score on the
hydrocephalus, intraventricular hemorrhage, and intracerebral hemorrhage.
Glasgow Coma Scale,
evaluation for meningeal
Lumbar Puncture signs, and the presence of
In cases of negative or equivocal head CT findings in which a high suspicion for focal neurologic deficits.
SAH still exists, a lumbar puncture is the immediate next recommended step
● Transient elevation in the
(FIGURE 3-2).31 Opening pressure should be measured routinely. To differentiate intracranial pressure is the
a traumatic tap from true SAH, CSF should be collected in four consecutive cause of nausea, vomiting,
tubes, with red blood cell count measured in tubes one and four. CSF should be and syncope and may be
spun down and evaluated for xanthochromia by visual inspection and, if associated with additional
cardiac and pulmonary
available, spectrophotometry, which is superior in diagnostic accuracy for complications after
xanthochromia than visual inspection alone.32 subarachnoid hemorrhage.
Xanthochromia takes approximately 12 hours to develop and may not be
present if a lumbar puncture is performed earlier after headache onset. Most ● The most rapidly available
and appropriate initial
hospitals do not offer spectrophotometry, and it is unknown what the false-
diagnostic test for patients
negative rate for xanthochromia is at various time intervals after SAH onset. with suspected
subarachnoid hemorrhage is
Magnetic Resonance Imaging a noncontrast head CT.
Head CT and MRI are considered to be equally sensitive in detecting SAH in the
● In cases of negative or
first 2 days, except in the hyperacute first 6 hours after SAH, during which head equivocal head CT findings
CT may miss a small proportion of SAHs and MRI may be slightly superior.30 in which a high suspicion still
Because of its rapid image acquisition, its widespread availability in the exists for subarachnoid
emergency department, and its very high sensitivity in the first 2 days after SAH, hemorrhage, a lumbar
puncture is the immediate
head CT remains the diagnostic modality of choice for early SAH. However, next recommended step.
hemosiderin-sensitive MRI sequences (gradient recalled echo [GRE] and
susceptibility-weighted imaging [SWI]) or fluid-attenuated inversion recovery ● CSF should be spun down
(FLAIR) sequences have superior sensitivity to detect subacute or chronic SAH and evaluated for
xanthochromia by visual
compared to head CT.33 Additionally, MRI may be helpful in differentiating
inspection and, if available,
alternative pathologies, such as arteriovenous malformations and inflammatory, spectrophotometry.
infectious, and neoplastic etiologies.30 Xanthochromia takes
approximately 12 hours to
develop and may not be
Identifying the Bleeding Source
present if a lumbar puncture
Vessel imaging should be the next step in all patients with a diagnostic head CT, is performed earlier after
lumbar puncture, or MRI. The gold standard of vessel imaging remains cerebral headache onset.
digital subtraction angiography (DSA) (CASE 3-1). CT angiography (CTA) has
become widely available and is now commonly performed as the first-line ● Head CT and MRI are
considered equally sensitive
vascular imaging in many institutions. Depending on the technique, slice in detecting subarachnoid
thickness, and postimaging data processing, the sensitivity and specificity of hemorrhage in the first
CTA can range from 90% to 97% and 93% to 100%, respectively, when compared 2 days, except in the
to DSA.34,35 However, CTA may miss aneurysms as small as 4 mm or less.34 hyperacute first 6 hours
after subarachnoid
In specialized stroke and aneurysm centers, DSA is readily available for hemorrhage, during which
diagnostic as well as treatment purposes. At the author’s institution, two- head CT may miss a small
dimensional and three-dimensional DSA is pursued as standard diagnostics for proportion of subarachnoid
aneurysm detection as soon as the diagnosis of SAH has been established; CTA is hemorrhages and MRI may
be slightly superior.
usually omitted at the author’s institution to prevent the additional exposure to

CASE 3-1 A 43-year-old woman with a past medical history of smoking and
depression presented to a community hospital with sudden onset of
severe headache, brief loss of consciousness, nausea, and vomiting while
using the bathroom. She reported a moderate, persistent, sudden-onset
headache that had continued for 36 hours.
In the emergency department, her blood pressure was 185/100 mm Hg,
pulse was 105 beats/min, arterial oxygen saturation was 95% on room air,
and temperature was 36.8°C (98.2°F).
On examination, she reported neck pain, was disoriented (Glasgow
Coma Scale score of 13), but had no focal deficits. Her World Federation
of Neurological Surgeons Scale (WFNSS) score was 2, Hunt and Hess
Scale score was 3, and modified Fisher Scale score was 4. Bolus
injections of 10 mg IV labetalol and 4 mg IV morphine resulted in a partial
blood pressure reduction to 170/90 mm Hg. She was started on a
nicardipine infusion to achieve and maintain a systolic blood pressure of
less than 160 mm Hg.
A noncontrast head CT revealed subarachnoid hemorrhage (SAH) in
multiple cisterns, intraventricular hemorrhage, and mild hydrocephalus
(FIGURE 3-1A). She received a loading dose of IV levetiracetam.
The patient was immediately transferred to a comprehensive stroke
center and was admitted to the neurocritical care unit. Since her Glasgow
Coma Scale had worsened to a score of 10 because of hydrocephalus, she
had an external ventricular drain (EVD) placed, which was kept clamped
prior to aneurysm coiling with intermittent opening to drain 5 mL to 10 mL
of CSF hourly.
After discussion among the interventional neuroradiologist,
cerebrovascular neurosurgeon, and neurointensivist, the patient
underwent digital subtraction angiography (DSA) and coiling of her
unsecured aneurysm (FIGURE 3-1B–D). Following the coiling, the patient was
transferred back to the neurocritical care unit, where she received
enteral nimodipine, pain control, IV normal saline to maintain euvolemia,
intermittent compression devices, and subcutaneous enoxaparin for
chemoprophylaxis for deep vein thrombosis, and IV dexamethasone
(for 2 days only) for refractory headaches. The levetiracetam was
discontinued based on guideline recommendations, as further discussed
in the section on seizures and seizure prophylaxis in this article.
Nicardipine was discontinued, and she maintained a systolic blood
pressure between 140 mm Hg and 165 mm Hg spontaneously, with a goal
systolic blood pressure of 100 mm Hg to 200 mm Hg with the secured
aneurysm. Her EVD was leveled at 10 mm Hg and open, and 5 mL to 12 mL
of CSF was drained hourly. Her neurologic examination improved to a
Glasgow Coma Scale score of 15 with no focal deficits, and she was
mobilized out of bed.
1628 DECEMBER 2018

FIGURE 3-1
Neuroimaging of the patient in CASE 3-1. Noncontrast head CT (A) showing acute
subarachnoid hemorrhage, and two-dimensional (B) and three-dimensional (C) four-vessel
angiogram showing a large top of the basilar artery aneurysm with an irregular shape
(B, C, arrows). Two-dimensional angiogram after coiling shows obliteration of the aneurysm
(D, arrow).
This case demonstrates the first phase of SAH management: rapid COMMENT
diagnosis of SAH and hydrocephalus and immediate emergency treatment
with blood pressure lowering, EVD placement, and obliteration of the
ruptured cerebral aneurysm.

FIGURE 3-2
Diagnostic algorithm for subarachnoid hemorrhage.
CT = computed tomography; CTA = computed tomography angiography; DSA = digital subtraction angiography.
Reprinted with permission from Suarez JI, et al, N Engl J Med.31 © 2006 Massachusetts Medical Society.
radiation, iodine contrast, and its potential for anaphylactic reaction and
nephrotoxicity. Patients with a negative initial DSA should have a repeat study
7 to 14 days after the initial one. In addition, in those with negative initial DSA,
MRI of the brain and, depending on the location of the SAH, MRI of the cervical
spine should be performed to search for a possible arteriovenous malformation
of the brain, brainstem, or spinal cord.9,30
Perimesencephalic Subarachnoid Hemorrhage

Approximately 15% of patients with SAH will have negative imaging studies for a
source of bleeding, of which approximately 38% have nonaneurysmal
perimesencephalic SAH,36 a special form of nontraumatic SAH with blood
isolated to the perimesencephalic cisterns (CASE 3-2).37 The clinical course has
been reported to be more benign,36 although case reports have been published
1630 DECEMBER 2018

demonstrating rare cases of small aneurysms in the posterior circulation,
fenestration of the vertebral or basilar arteries, or anterior spinal artery
abnormalities. Therefore, DSA should still be performed. At the author’s
institution, a brain and cervical spine MRI, as well as a repeat DSA approximately
7 days after the initial tests, are performed in all cases of perimesencephalic SAH.
Patients with perimesencephalic SAH are monitored in a step-down unit and,
if no bleeding source is discovered, discharged after 8 to 10 days at the author’s
institution, as long as their hospital course remains uncomplicated.
INITIAL EVALUATION
This section focuses on the emergency department evaluation and management
of a patient with SAH.
A 23-year-old man presented to the emergency department for CASE 3-2

evaluation after developing a sudden-onset headache posteriorly while
lifting weights in the gym. He described the headache as the “worst
headache of his life.”
A noncontrast head CT revealed blood around the perimesencephalic
and prepontine cisterns (FIGURE 3-3). Six-vessel angiography did not reveal
a bleeding cause. He underwent MRI of the brain and cervical spine,
which also did not reveal a cause for the bleeding. He was observed in the
step-down unit until 8 days posthemorrhage, when he received a repeat
six-vessel angiogram, which was again negative. The patient was
discharged home on day 10 post–subarachnoid hemorrhage in normal
condition.
FIGURE 3-3
Imaging of the patient in CASE 3-2. Noncontrast
head CT at two brainstem levels showing blood in
the perimesencephalic cisterns (arrows) consistent
with a perimesencephalic subarachnoid hemorrhage.
This case demonstrates a typical presentation and hospital course for a COMMENT
perimesencephalic subarachnoid hemorrhage, with the adequate workup
for a bleeding source. The patient’s course was benign, as commonly seen
in patients with perimesencephalic subarachnoid hemorrhage.

Airway, Breathing, and Circulation

The emergency evaluation and management of patients with SAH should focus
on the airway, breathing, and circulation (the ABCs).13,24,38 Those patients
unable to protect their airway should be intubated immediately, which includes
patients in coma, in stupor from hydrocephalus, with seizures, or patients in
need of sedation for agitation.
Rebleeding
The focus in the first few minutes to hours after SAH, until the patient can
undergo treatment of the ruptured aneurysm, should be directed toward the
prevention of rebleeding. This life-threatening complication, with a mortality rate
of 20% to 60%, has its highest rate (8% to 23%) within the first 72 hours after SAH,
with the majority of rebleeding (50% to 90%) occurring within the first 6 hours,
not including patients who die before hospital arrival.9 After the first month,
rebleeding rates are low, at 3% per year. Risk factors for rebleeding include
poor-grade SAH, hypertension, a large aneurysm, and, potentially, the use of
antiplatelet drugs.27 Particularly, blood pressure fluctuations and extreme blood
pressure peaks should be avoided because of the presumed propensity to
cause rebleeding.39
Current guideline recommendations for blood pressure goals are to keep
systolic blood pressure below 160 mm Hg.13,24 Continuous blood pressure
TABLE 3-3 Clinical and Radiologic Grading Scales for Subarachnoid Hemorrhagea
World Federation of Neurological

Surgeons Scale43 Hunt and Hess Scale44 Modified Fisher Scale45
Glasgow Neurologic Subarachnoid Intraventricular

Grade Coma Scale Examination Grade Neurologic Examination Scale Hemorrhage Hemorrhage
1 15 No motor 1 Awake, alert, no cranial 0 Absent Absent

deficit nerve or motor deficits,
mild headache, minimal or
no nuchal rigidity
2 13–14 No motor 2 Awake, alert, moderate to 1 Thin Absent

deficit severe headache, nuchal
rigidity, no motor deficits,
may have cranial nerve
deficit
3 13–14 Motor deficit 3 Confusion or lethargy, with 2 Thin Present

or without mild focal
neurologic deficits
4 7–12 With or without 4 Stuporous, more severe 3 Thickb Absent

motor deficit focal neurologic deficit
5 3–6 With or without 5 Comatose, motor 4 Thickb Present

motor deficit posturing or no motor
response
a
Modified with permission from Suarez JI, et al, N Engl J Med.31 © 2006 Massachusetts Medical Society.
b
Thick is defined as a subarachnoid hemorrhage filling one or more cisterns or fissures out of a total of 10 cisterns/fissures: interhemispheric
fissure, the quadrigeminal cistern, both suprasellar cisterns, both ambient cisterns, both basal sylvian fissures, and both lateral sylvian fissures.
1632 DECEMBER 2018

monitoring with an arterial line is highly recommended. IV medications KEY POINTS
to control blood pressure should preferably be continuous infusions of
● Hemosiderin-sensitive
antihypertensives (nicardipine 5 mg/h to 15 mg/h or labetalol 5 mg/h to 20 mg/h) MRI sequences (gradient
over bolus infusions (labetalol 5 mg bolus to 20 mg bolus, captopril) to prevent recalled echo and
wide fluctuations of blood pressure that may be as detrimental to aneurysm susceptibility-weighted
rebleeding as high blood pressure itself. imaging) or fluid-attenuated
inversion recovery
Therefore, at the author’s institution, hydralazine is avoided as it can cause
sequences have superior
rebound hypertension. Pain control is best achieved with short-acting opiates. sensitivity to detect
Meningeal chemical irritation from the SAH often responds to one or several subacute or chronic
single doses of dexamethasone (2 mg to 10 mg). subarachnoid hemorrhage
compared to head CT.
Antifibrinolytics ● The “gold standard”

While prolonged infusion of antifibrinolytics can result in deep vein thrombosis, vessel imaging remains
venous thromboembolism, stroke, and myocardial infarction, and should cerebral digital subtraction
angiography.
therefore not be applied, the short-term use (up to a maximum of 72 hours until
aneurysm securement) of antifibrinolytics (tranexamic acid or ε-aminocaproic ● Approximately 15% of
acid) is recommended by guidelines based on a randomized controlled trial patients with subarachnoid
and several small observational studies.24,40,41 Recently, however, a large hemorrhage will have
retrospective study including 341 patients over 12 years, of whom 146 patients negative imaging studies for
a source of bleeding, of
received ε-aminocaproic acid before their endovascular coiling, showed that which approximately 38%
short-term antifibrinolytic therapy was safe but did not reduce preprocedural have nonaneurysmal
rebleeding.42 Therefore, institutional variation may occur in the use of short- perimesencephalic
term antifibrinolytics to prevent rebleeding until a randomized controlled trial subarachnoid hemorrhage.
confirms or refutes the guideline recommendations.
● The focus in the first few
minutes to hours after
Disease Severity Scoring subarachnoid hemorrhage,
The importance of severity scoring lies in the observation that outcome and until the patient can undergo
treatment of the ruptured
delayed cerebral ischemia are associated with clinical and radiologic scales,
aneurysm, should be
respectively (TABLE 3-3).43–45 Disease severity scoring provides a common directed toward the
language between all providers caring for a patient with SAH.31 The two most prevention of rebleeding.
commonly used clinical scales, the World Federation of Neurological Surgeons
Scale (WFNSS) and the Hunt and Hess Scale, are strong predictors of outcome.43,44 ● Risk factors for
rebleeding include
Higher scores are associated with worse clinical outcome. The most reliable and poor-grade subarachnoid
validated radiologic scale is the modified Fisher Scale (TABLE 3-3), which is hemorrhage, hypertension,
nearly linearly associated with worse cerebral vasospasm and delayed cerebral a large aneurysm, and,
ischemia.46 potentially, the use of
antiplatelet drugs.
The classic Fisher Scale score holds several disadvantages and has largely been
replaced by the modified Fisher Scale.45 For example, it was developed on 1980s ● The short-term use (up to
head CTs and does not reflect modern multislice head CT imaging. Also, it is not a maximum of 72 hours until
linear (a Fisher Scale score of 3 has a higher vasospasm risk than a score of 4), aneurysm securement) of
antifibrinolytics (tranexamic
making it more difficult to apply in regression models in research and simply
acid or ε-aminocaproic
making it less intuitive to apply at the bedside. acid) is recommended by
guidelines, although there is
Admission to High-volume Centers institutional variation in
If the patient is not already at a high-volume SAH-specialized center (defined their use.
as more than 35 SAH cases per year with experienced cerebrovascular
surgeons, endovascular specialists, and neurocritical care services),12 transfer
to such a center should be initiated immediately (TABLE 3-4). Likely owing to
lack of protocolized care and expertise, admission of patients with SAH to
low-volume centers is associated with a higher 30-day mortality.47 Admission

TABLE 3-4 Summary of Key Recommendations for the Management of Patients With
Subarachnoid Hemorrhagea
American Heart Association/American

Treatment Decision Stroke Association13,b Neurocritical Care Society24,c
Hospital/system Low-volume hospitals (eg, fewer than 10 Patients with SAH should be treated at high-
characteristics subarachnoid hemorrhage [SAH] cases per year) volume centers (moderate quality of evidence,
should consider early transfer of patients with SAH strong recommendation).
to high-volume centers (eg, more than 35 SAH
High-volume centers should have appropriate
cases per year) with experienced cerebrovascular
specialty neurointensive care units,
surgeons, endovascular specialists, and
neurointensivists, vascular neurosurgeons, and
multidisciplinary neurointensive care services
interventional neuroradiologists to provide the
(Class I, Level B).
essential elements of care (moderate quality of
After discharge, it is reasonable to refer patients evidence, strong recommendation).
with SAH for a comprehensive evaluation, including
cognitive, behavioral, and psychosocial
assessments (Class IIa, Level B).
Aneurysm treatment Surgical clipping or endovascular coiling of the Early aneurysm repair should be undertaken,
ruptured aneurysm should be performed as early as when possible and reasonable to prevent
feasible in the majority of patients to reduce the rebleeding (high quality of evidence, strong
rate of rebleeding after SAH (Class I, Level B). recommendation).
For patients with ruptured aneurysms judged to be An early, short course of antifibrinolytic therapy
technically amenable to either endovascular coiling prior to early aneurysm repair (begun at
or neurosurgical clipping, endovascular coiling diagnosis and continued up to the point at which
should be considered (Class I, Level B). the aneurysm is secured or at 72 hours postictus,
whichever is shorter) should be considered (low
Complete obliteration of the aneurysm is
quality of evidence, weak recommendation).
recommended whenever possible (Class I, Level B).
Delayed (more than 48 hours after the ictus) or
Stenting of a ruptured aneurysm is associated with
prolonged (more than 3 days) antifibrinolytic
increased morbidity and mortality (Class III, Level C).
therapy exposes patients to side effects of
For patients with an unavoidable delay in therapy when the risk of rebleeding is sharply
obliteration of aneurysm, a significant risk of reduced and should be avoided (high quality of
rebleeding, and no compelling medical evidence, strong recommendation).
contraindications, short-term (less than 72 hours)
therapy with tranexamic acid or aminocaproic acid
is reasonable to reduce the risk of early aneurysm
rebleeding (Class IIa, Level B).
Blood pressure Between the time of SAH symptom onset and Treat extreme hypertension in patients with an
control aneurysm obliteration, blood pressure should be unsecured, recently ruptured aneurysm. Modest
controlled with a titratable agent to balance the elevations in blood pressure (mean blood
risk of stroke, hypertension-related rebleeding, pressure of less than 110 mm Hg) do not require
and maintenance of cerebral perfusion pressure therapy. Premorbid baseline blood pressures
(Class I, Level B). should be used to refine targets and
hypotension should be avoided (low quality of
The magnitude of blood pressure control to reduce
evidence, strong recommendation).
the risk of rebleeding has not been established, but
a decrease in systolic blood pressure to less than
160 mm Hg is reasonable (Class IIa, Level C).
Intravascular Maintenance of euvolemia and normal circulating Intravascular volume management should target
volume status blood volume is recommended to prevent delayed euvolemia and avoid prophylactic hypervolemic
cerebral ischemia (Class I, Level B). therapy. In contrast, there is evidence for harm
from aggressive administration of fluid aimed at
achieving hypervolemia (moderate quality of
CONTINUED ON PAGE 1635
1634 DECEMBER 2018

CONTINUED FROM PAGE 1634

Cardiopulmonary No recommendations given Baseline cardiac assessment with serial

complications enzymes, ECG, and echocardiography is
recommended, especially in patients with
evidence of myocardial dysfunction (low quality
of evidence, strong recommendation).
Monitoring of cardiac output may be useful in
patients with evidence of hemodynamic
instability or myocardial dysfunction (low quality
Seizures The use of prophylactic anticonvulsants may be Routine use of anticonvulsant prophylaxis with
considered in the immediate posthemorrhagic phenytoin is not recommended after SAH (low
period (Class IIb, Level B). quality of evidence, strong recommendation).
The routine long-term use of anticonvulsants is not If anticonvulsant prophylaxis is used, a short
recommended (Class III, Level B). course (3–7 days) is recommended (low quality
of evidence, weak recommendation).
Continuous EEG monitoring should be
considered in patients with poor-grade SAH
who fail to improve or who have neurologic
deterioration of undetermined etiology (low
quality of evidence, strong recommendation).
Fever treatment Aggressive control of fever to a target of During the period of risk for delayed cerebral
normothermia by use of standard or advanced ischemia, control of fever is desirable; intensity
temperature modulating systems is reasonable in should reflect the individual patient’s relative
the acute phase of SAH (Class IIa, Level B). risk of ischemia (low quality of evidence, strong
recommendation).
Surface cooling or intravascular devices are
more effective and should be employed when
antipyretics fail in cases where fever control is
highly desirable (high quality of evidence, strong
recommendation).
Glucose control Careful glucose management with strict avoidance Hypoglycemia (serum glucose of less than
of hypoglycemia may be considered as part of the 80 mg/dL) should be avoided (high quality of
general critical care management of patients with evidence, strong recommendation).
SAH (Class IIb, Level B)
Serum glucose should be maintained below
200 mg/dL (moderate quality of evidence,
strong recommendation).
Deep vein Heparin-induced thrombocytopenia and deep vein Measures to prevent deep vein thrombosis
thrombosis thrombosis are relatively frequent complications should be employed in all patients with SAH
prophylaxis after SAH. Early identification and targeted (high quality of evidence, strong
treatment are recommended, but further research recommendation).
is needed to identify the ideal screening paradigms
The use of unfractionated heparin for
(Class I, Level B)
prophylaxis could be started 24 hours after
undergoing aneurysm obliteration (moderate
quality of evidence, strong recommendation).
CONTINUED ON PAGE 1636

CONTINUED FROM PAGE 1635

Delayed cerebral Oral nimodipine should be administered to all Oral nimodipine (60 mg every 4 hours) should be
ischemia patients with SAH (Class I, Level A). administered after SAH for a period of 21 days
(high quality of evidence, strong
Maintenance of euvolemia and normal circulating
recommendation).
blood volume is recommended to prevent delayed
cerebral ischemia (Class I, Level B). The goal should be maintaining euvolemia, rather
than attempting hypervolemia (moderate quality
Prophylactic hypervolemia or balloon angioplasty
before the development of angiographic spasm is
not recommended (Class III, Level B). Transcranial Doppler may be used for monitoring
and detection of large artery vasospasm with
Transcranial Doppler is reasonable to monitor for
variable sensitivity (moderate quality of
the development of arterial vasospasm (Class IIa,
Level B).
Digital subtraction angiography is the gold
Perfusion imaging with CT or MRI can be useful to
standard for detection of large artery
identify regions of potential brain ischemia (Class
vasospasm (high quality of evidence, strong
IIa, Level B).
recommendation).
Induction of hypertension is recommended for
Patients clinically suspected of delayed cerebral
patients with delayed cerebral ischemia unless
ischemia should undergo a trial of induced
blood pressure is elevated at baseline or cardiac
hypertension (moderate quality of evidence,
status precludes it (Class I, Level B).
strong recommendation).
Cerebral angioplasty and/or selective intraarterial
Endovascular treatment using intraarterial
vasodilator therapy is reasonable in patients with
vasodilators and/or angioplasty may be
symptomatic vasospasm, particularly those who
considered for vasospasm-related delayed
are not responding to hypertensive therapy (Class
cerebral ischemia (moderate quality of
IIa, Level B).
Anemia and The use of packed red blood cell transfusion to Patients should receive packed red blood cell
transfusion treat anemia might be reasonable in patients with transfusions to maintain hemoglobin
SAH who are at risk of cerebral ischemia. The concentration above 8–10 g/dL (moderate
optimal hemoglobin goal is still to be determined quality of evidence, strong recommendation).
(Class IIb, Level B).
Hyponatremia The use of fludrocortisone acetate and hypertonic Fluid restriction should not be used to treat
saline solution is reasonable for preventing and hyponatremia (weak quality of evidence, strong
correcting hyponatremia (Class IIa, Level B). recommendation).
Early treatment with hydrocortisone or
fludrocortisone may be used to limit natriuresis
and hyponatremia (moderate quality of
evidence, weak recommendation).
Mild hypertonic saline solutions can be used to
correct hyponatremia (very low quality of
CT = computed tomography; ECG = electrocardiogram; EEG = electroencephalogram; MRI = magnetic resonance imaging.
a
Reprinted with permission from Suarez JI, Continuum (Minneap Minn).12 © 2015 American Academy of Neurology.
b
American Heart Association/American Stroke Association recommendations follow the American Heart Association Stroke Council’s methods of
classifying the level of certainty of the treatment effect and the class of evidence.
c
For the Neurocritical Care Society’s guidelines, the quality of the data was assessed and recommendations developed using the Grading of
Recommendations, Assessment, Development, and Evaluation (GRADE) system.
1636 DECEMBER 2018

to a neurocritical care unit staffed by dedicated neurointensivists has been
associated with lower in-hospital mortality in patients with stroke,
including SAH.48
Aneurysm Treatment
With the publication of the ISAT (International Subarachnoid Aneurysm Trial),25,26
which compared endovascular coiling to surgical clipping after SAH, the treatment
of an unsecured aneurysm has shifted from surgical clipping to mostly
endovascular coiling.49 ISAT showed that patients in the endovascular coiling
group had significantly higher odds of survival free of disability 1 year after SAH
and a lower risk of epilepsy when compared to the surgical clipping group.
Even 10 years after SAH, patients who underwent endovascular coiling had
better outcomes.50 In contrast, the risk of rebleeding and incomplete occlusion of
the aneurysm was lower with surgical clipping. With the introduction of newer
techniques such as stent-assisted or balloon-assisted coiling, even broad-neck
aneurysms can now be treated with endovascular coiling.
Currently, endovascular coiling is preferred over surgical clipping whenever
possible. However, follow-up angiograms are necessary, as the recurrence rate of
aneurysms is higher when they are treated with endovascular coiling.50
At the author’s institution, approximately 95% of aneurysms are treated with
endovascular coiling (CASE 3-1). Many aneurysms are not equally suited for
endovascular coiling or surgical clipping (TABLE 3-5 and CASE 3-3A). The choice
of treatment depends on the patient’s age as well as the aneurysm location,
morphology, and relationship to adjacent vessels. A multidisciplinary approach
to the swift treatment decision with consensus between cerebrovascular
neurosurgeons, neuroendovascular specialists, and neurointensivists is
recommended given the complexity of the decision. Regardless of the treatment
modality, rebleeding must be prevented, and the unsecured aneurysm must be
treated as soon as possible (TABLE 3-4).
Critical Care Management of Subarachnoid Hemorrhage

SAH is a systemic disease and is not isolated to the brain. It is commonly
associated with systemic inflammatory response syndrome (SIRS) (75%), which
is related to elevated levels of inflammatory cytokines. SIRS has been associated
with long-term cognitive dysfunction and has been linked to nonconvulsive
seizures in SAH.51 SIRS has been found to precede nonconvulsive seizures, and
patients with in-hospital nonconvulsive seizures are almost twice as likely to
have SIRS as those without nonconvulsive seizures. Therefore, it has been
Preference for Treatment of Unsecured Aneurysmsa TABLE 3-5
Treatment Type Clinical or Aneurysm Factors Supporting Treatment Type

Endovascular coiling Older age, poor clinical grade, multiple comorbidities, top of the basilar aneurysm, high surgical risk,
aneurysm suitable for coiling or clipping
Surgical clipping Aneurysm with wide neck-to-body ratio, crucial arteries arising from aneurysm dome, middle cerebral
artery aneurysm, aneurysm with large parenchymal hematoma
a
Modified with permission from Suarez JI, Continuum (Minneap Minn).12 © 2015 American Academy of Neurology.

CASE 3-3A A 51-year-old man presented to the emergency department of a

comprehensive stroke center for evaluation of sudden-onset severe
headache with rapidly worsening left-sided hemiplegia that began while
shoveling snow. Upon arrival, his blood pressure was 205/110 mm Hg, his
heart rate was 98 beats/min, his oxygen saturation was 98% on room air,
and his temperature was 36.5°C (97.7°F). His Glasgow Coma Scale score
was 14, and he had left facial weakness and a dense left hemiplegia. His
World Federation of Neurological Surgeons Scale (WFNSS) score was 3,
his Hunt and Hess Scale score was 3, and his modified Fisher Scale score
was 4.
A noncontrast head CT revealed a subarachnoid hemorrhage with a
large right frontotemporal intraparenchymal clot and intraventricular
hemorrhage (FIGURE 3-4A). He received immediate blood pressure–
lowering agents. A CT angiogram confirmed a suspected right middle
cerebral artery aneurysm (FIGURE 3-4B). A three-dimensional digital
subtraction angiogram revealed the complicated anatomy of this middle
cerebral artery aneurysm with multiple vessels coming off the aneurysm
and areas of irregular outpouching (FIGURE 3-4C). The patient was taken to
the operating room immediately for craniotomy, clipping of the
aneurysm, and clot evacuation. He was admitted to the neurocritical care
unit for routine postclipping subarachnoid hemorrhage care.
COMMENT This case shows a patient with a clear indication for surgical clipping due to
the more superficial location of the aneurysm at the distal middle cerebral
artery and the aneurysm’s anatomy with multiple vessels coming off the
aneurysm. It also shows how patients with large temporal hematomas (with
or without subarachnoid hemorrhage) should always undergo vessel
imaging, as a middle cerebral artery aneurysm may be the culprit.
1638 DECEMBER 2018

FIGURE 3-4
Ruptured right middle cerebral artery aneurysm requiring clipping, and subsequent cerebral
vasospasm and delayed cerebral ischemia, in the patient in CASE 3-3A. A, Noncontrast head CT
shows a large intraparenchymal component (thick arrows), small subarachnoid hemorrhage
(arrowheads), and intraventricular hemorrhage with hydrocephalus (thin arrows). B, Cerebral
angiogram reveals a right middle cerebral artery aneurysm (yellow arrow) as the culprit of
the hemorrhage. C, Three-dimensional cerebral angiogram shows the complicated anatomy
of this middle cerebral artery aneurysm with multiple vessels coming off the aneurysm and
areas of irregular outpouching (blue arrows).

postulated that the negative impact of SIRS on functional outcome is mediated in

part by nonconvulsive seizures.51
Additionally, patients with SAH are at risk for several additional neurologic
complications, including hydrocephalus, brain edema, delayed cerebral ischemia,
rebleeding, seizures, and neuroendocrine disorders, the latter of which can lead
to impaired regulation of sodium, volume, and glucose. Furthermore, mediated
through the hypothalamus, sympathetic release can result in cardiac and pulmonary
complications, including neurogenic ECG changes, arrhythmias, diminished
cardiac contractility (stress Takotsubo cardiomyopathy), troponin leaks, and
myocardial contraction band necrosis. The early recognition and treatment of these
complications is key to achieve the best possible outcome of the patient with SAH.
NEUROLOGIC COMPLICATIONS
Several serious neurologic complications may occur after SAH.
Rebleeding
Rebleeding is the most immediately life-threatening neurologic complication
after SAH. The best measure to reduce the risk of rebleeding is the early and rapid
treatment of the unsecured, ruptured aneurysm. The prevention of rebleeding
via aggressive blood pressure control should begin during the prehospital
transport and in the emergency department.
Hydrocephalus
Acute symptomatic hydrocephalus occurs in 20% of patients with SAH, usually
within minutes to days after SAH onset (FIGURE 3-1A and FIGURE 3-4A). Clinical
signs of hydrocephalus are decreased levels of consciousness, impaired upgaze,
hypertension, and delirium. The diagnosis is made by repeat head CT and
clinical symptoms.
Hydrocephalus can resolve spontaneously in 30% of patients but can also
rapidly worsen. Insertion of an external ventricular drain (EVD) can be
lifesaving. Some centers insert a lumbar drain instead of an EVD in cases of
communicating hydrocephalus, while some centers insert both. Reluctance to
place an EVD includes the risks of infection, bleeding (intracerebral or
intraventricular), and changes in the transmural pressure precipitating the
rebleeding of an unsecured aneurysm. The bleeding and infection risk for EVD
insertions are close to 8% for each.9
A rapid weaning of the EVD is recommended after aneurysm obliteration or
within 48 hours of insertion if the patient is neurologically stable. In those for
whom weaning is unsuccessful (approximately 40%), placement of a chronic
ventriculoperitoneal shunt may be required. A small retrospective study from
Germany has suggested that dexamethasone dosed 12 mg/d for at least 5 days
may lower the risk of hydrocephalus after SAH.52 Given the lack of randomized
controlled studies, the routine use of corticosteroids outside its application for
headache control from meningeal chemical irritation after SAH cannot
be recommended.
Seizures and Seizure Prophylaxis

Determining the true incidence of seizures in patients with SAH is difficult as
many patients (up to 26%) present with seizurelike episodes, but these episodes
are not easy to characterize as they occur at the onset of symptoms.13,24 If seizures
1640 DECEMBER 2018

occur prior to aneurysm securement, they are usually a sign of early rebleeding. KEY POINTS
Long-term epilepsy develops in 2% of patients with SAH and is correlated to
● The two most commonly
a higher severity of SAH.9 The occurrence of nonconvulsive seizures (7% to used clinical scales, the
18%) and nonconvulsive status epilepticus (3% to 13%) is more common in World Federation of
patients with SAH who are comatose and has been associated with delayed Neurological Surgeons Scale
cerebral ischemia and worse outcomes.51,53,54 It is not completely understood and the Hunt and Hess
Scale, are strong predictors
whether nonconvulsive seizures are the cause of delayed cerebral ischemia
of outcome in patients with
and worse outcomes or are an epiphenomenon of poor-grade SAH with subarachnoid hemorrhage.
outcomes due to the severity of SAH. Because nonconvulsive seizures are The most reliable and
treatable, continuous EEG monitoring should be considered in patients with validated radiologic scale is
the modified Fisher Scale.
high-grade SAH.54 A 2015 review summarized nonconvulsive seizures and
status epilepticus in SAH.54 However, at some institutions, the limitations lie ● For the treatment of
in the capacity of performing and interpreting prolonged continuous EEG aneurysm, endovascular
monitoring. Furthermore, recent discoveries show that surface EEG may detect coiling is preferred over
nonconvulsive seizures in only 8% of patients with SAH, while they were seen in surgical clipping whenever
possible, but the choice
38% of patients when intracortical depth electrodes were placed via a burr hole.53 of treatment depends on
Such depth electrode recording, however, is more invasive, is limited to very the patient’s age as well as
few centers, and is currently not considered standard of care. The suspicion the aneurysm’s location,
of nonconvulsive status epilepticus should be high in patients with SAH who morphology, and
relationship to adjacent
are comatose. vessels.
Currently, in the absence of randomized controlled trials of antiepileptic drug
treatment in patients with SAH, treatment with antiepileptic drugs should be ● Patients with
limited to the preaneurysm treatment time frame only, considering the known subarachnoid hemorrhage
are at risk for several
negative effects of anticonvulsants, particularly phenytoin, on neurocognitive
additional neurologic
recovery after SAH.55,56 complications, including
Guidelines and experts recommend stopping antiepileptics in patients in hydrocephalus, brain
whom a clinical examination can be followed reliably as soon as the aneurysm has edema, delayed cerebral
been secured and not to extend prophylaxis beyond 3 to 7 days unless the patient ischemia, rebleeding,
seizures, and
presented with a seizure at the onset of SAH.9,24 At the author’s institution, only neuroendocrine disorders,
patients who are comatose and patients with poor-grade SAH are continued on the latter of which can lead
antiepileptics after the aneurysm has been secured given the high risk for to impaired regulation
nonconvulsive seizures in these patients. of sodium, volume,
and glucose.
Levetiracetam has become a popular antiepileptic because of its high
bioavailability, favorable side effect profile, and lack of drug-drug interactions. ● Acute symptomatic
However, it should be noted that no studies have shown an advantage of hydrocephalus occurs in
levetiracetam over other antiepileptic drugs. In addition, levetiracetam has 20% of patients with
subarachnoid hemorrhage,
not been approved by the US Food and Drug Administration (FDA) for
usually within minutes to
monotherapy in epilepsy; therefore, no specific antiepileptic drugs can be days after subarachnoid
recommended for seizure prophylaxis in patients with SAH. hemorrhage onset. In cases
of hydrocephalus, insertion
of an external ventricular
Delayed Cerebral Ischemia
drain can be lifesaving.
Delayed cerebral ischemia is one of the most feared neurologic complications
after SAH, as cerebral infarction from delayed cerebral ischemia is the leading ● If seizures occur prior to
cause for morbidity in patients who survive the initial SAH. Monitoring for aneurysm securement, they
delayed cerebral ischemia is the main reason for the recommended prolonged are usually a sign of early
rebleeding.
ICU stay for patients with SAH. Delayed cerebral ischemia is defined as any
neurologic deterioration that persists for more than 1 hour and cannot be
explained by any other neurologic or systemic condition, such as fever, seizures,
hydrocephalus, sepsis, hypoxemia, sedation, and other metabolic causes
(CASE 3-3B).57 Delayed cerebral ischemia is diagnosed when other causes of

CASE 3-3B The patient in CASE 3-3A was admitted to the neurocritical care unit. He
was monitored with daily transcranial Doppler (TCD). On day 5 post–
subarachnoid hemorrhage (SAH), he had an uptrend in the daily TCD mean
velocities from 50 cm/s to 153 cm/s in the right middle cerebral artery
(FIGURE 3-5A–B).
On day 6 post-SAH, he developed worse headaches, disorientation,
neglect, dysarthria, and worse left-sided weakness. He was afebrile, had
a normal glucose level, and was euvolemic. He was given a fluid bolus,
and his systolic blood pressure goal was elevated to greater than
180 mm Hg with phenylephrine infusion.
An emergent EEG did not reveal nonconvulsive seizures. The blood
pressure augmentation improved the disorientation and neglect but not
the weakness and dysarthria. Four-vessel angiography was performed,
which revealed cerebral vasospasm in the right middle cerebral artery
and right anterior cerebral artery (FIGURE 3-5C–D). He was treated with
intraarterial nicardipine. Postprocedure he had resolution of symptoms
to his immediate post-SAH baseline, but they returned by the next
morning. Repeat four-vessel angiography was performed, and he was
treated with intraarterial nicardipine and angioplasty (FIGURE 3-5E).
He experienced complete resolution of his symptoms. He was
maintained on hypertensive and mild hypervolemic therapy until day 15
post-SAH. His TCD velocities were downtrending, and he was slowly
weaned off induced hypertension. He was eventually discharged to
rehabilitation.
COMMENT This case demonstrates how asymptomatic cerebral vasospasm on TCD

was initially appropriately treated with just euvolemia without induced
hypertension. However, given the elevated alert level of the providers,
when the patient worsened and developed symptomatic cerebral
vasospasm, treatment with induced hypertension and endovascular
treatment was swiftly initiated.
1642 DECEMBER 2018

FIGURE 3-5
Ruptured right middle cerebral artery aneurysm requiring clipping, and subsequent cerebral
vasospasm and delayed cerebral ischemia, in the patient in CASE 3-3B. Transcranial Doppler
reveals the baseline (on day 1 post–subarachnoid hemorrhage) waveform of the right middle
cerebral artery with a normal mean velocity of 50 cm/s (A). Transcranial Doppler reveals
the change in the waveform and increase in the mean velocity to 153 cm/s on day 5
post–subarachnoid hemorrhage (B). Note the change in the y axis between the two images
required to record the severe velocity elevation. Together with an elevated Lindegaard ratio of
5 (not shown), this indicates cerebral vasospasm. Cerebral angiogram performed on day 6
post–subarachnoid hemorrhage shows severe vasospasm of the middle cerebral artery and
anterior cerebral arteries (C, arrowheads), as compared to FIGURE 3-4B, and also reveals the delay
in distal perfusion (D, arrows) in the middle cerebral artery territory as a result of the vasospasm.
Cerebral angiogram after intraarterial vasodilator infusion and angioplasty shows the
posttreatment improvement of the middle cerebral artery vasospasm (E, arrowheads).

neurologic deterioration have been excluded or deemed insufficient to cause the

neurologic deterioration and is therefore a diagnosis of exclusion.
Historically, delayed cerebral ischemia was thought to be caused by cerebral
vasospasm. However, evidence now indicates that the pathophysiology of
delayed cerebral ischemia includes an interaction of early brain injury,
microthrombosis, cortical spreading depolarizations, related ischemia, and
cerebral vasospasm (FIGURE 3-6).58,59 Increasingly, some experts believe that
cerebral vasospasm is only an epiphenomenon and that the underlying biochemical
and biophysical changes that lead to delayed cerebral ischemia occur as early as at
SAH onset.58,59 This fundamental change in the approach to delayed cerebral
ischemia is supported by the negative endothelin 1 antagonist trials in patients
with SAH undergoing clipping or coiling.60,61
Endothelin 1 has been implicated to be the strongest vasoconstriction mediator
in SAH. However, the administration of clazosentan, a potent inhibitor of the
endothelin 1 receptor, resulted in less angiographic cerebral vasospasm yet did
not ameliorate delayed cerebral ischemia and did not lead to improvement in
outcomes 3 months after SAH.
Delayed cerebral ischemia occurs on average 3 to 14 days after SAH. The risk
for delayed cerebral ischemia increases with SAH thickness and intraventricular
hemorrhage, as demonstrated by the modified Fisher Scale. Additional risk
factors include poor clinical grade, loss of consciousness at ictus, cigarette
FIGURE 3-6
The pathophysiology of delayed cerebral ischemia.
Reprinted with permission from Macdonald RL, Nat Rev Neurol.59 © 2013 Springer Nature Limited.
1644 DECEMBER 2018

smoking, cocaine use, SIRS, hyperglycemia, hydrocephalus, and nonconvulsive KEY POINTS
seizures.59 Predicting who will develop delayed cerebral ischemia has proven
● The occurrence of
very difficult but is of great importance. Not only does such prediction have an nonconvulsive seizures (7%
impact on ICU monitoring, early recognition, and treatment, but also on resource to 18%) and nonconvulsive
allocation and early ICU discharge for low-grade, lower-risk patients with SAH. status epilepticus (3% to 13%)
The best predictors for patients requiring less frequent monitoring include older is more common in patients
with subarachnoid
age (older than 65 years of age), a low WFNSS score of 1 to 3, and a modified
hemorrhage who are
Fisher Scale score of less than 3 (TABLE 3-4).59 comatose and has been
associated with delayed
cerebral ischemia and
Delayed Cerebral Ischemia Prophylaxis worse outcomes.
Calcium channel blockers (nimodipine) and maintenance of normal intravascular
volume status have the strongest evidence of prophylactic interventions for the ● Continuous EEG
monitoring should be
prevention of delayed cerebral ischemia. Nimodipine (60 mg every 4 hours for
considered in patients with
21 days) is neuroprotective and has Class I evidence for decreasing the risk of high-grade subarachnoid
poor functional outcome.13,24,59 Notably, however, it does not decrease the hemorrhage.
frequency of angiographic vasospasm. A common side effect of nimodipine
is hypotension, which may lead to hypoperfusion and decreased cerebral ● In the absence of
randomized controlled trials
perfusion pressure. Therefore, to prevent hypotension, a dose reduction with of antiepileptic drug
an increase in frequency to 30 mg every 2 hours may be necessary. treatment in subarachnoid
In all cases, adequate maintenance of intravascular euvolemia is hemorrhage, but with known
recommended.13,24 Decreased intravascular volume and a negative fluid balance negative effects of
anticonvulsants, particularly
have been associated with a higher incidence of delayed cerebral ischemia and phenytoin, on
poor neurologic outcomes.59 neurocognitive recovery
How to monitor for euvolemia has not been defined. Trending the central after subarachnoid
venous pressure has fallen out of favor as it has been shown to be a poor predictor hemorrhage, treatment
with antiepileptic drugs
of fluid responsiveness and intravascular volume.62 Measurements of pulse should be limited to the
pressure variation or respiratory variability of the inferior vena cava diameter preaneurysm treatment
using point-of-care bedside ultrasound are easy to perform and are much more time frame only.
reliable monitoring techniques for fluid responsiveness of patients who are
● Delayed cerebral
critically ill, including those with SAH.62 Prophylactic hypervolemia must be
ischemia after subarachnoid
avoided, as this strategy has not been shown to improve cerebral blood flow or hemorrhage is defined as
decrease the frequency of cerebral vasospasm or delayed cerebral ischemia but any neurologic deterioration
increases adverse cardiopulmonary complications. that persists for more than
Maintenance of a euvolemic state may be difficult in the presence of cerebral 1 hour and cannot be
explained by any other
salt wasting, a common neuroendocrine disorder in SAH (see the following neurologic or systemic
section on hyponatremia). In patients with SAH and significant diuresis and condition.
natriuresis, additional administration of fludrocortisone can be helpful in
maintaining intravascular volume and normal sodium values (fludrocortisone ● Delayed cerebral ischemia
occurs on average 3 to
0.2 mg to 0.4 mg enterally every 12 hours) (TABLE 3-4). 14 days after subarachnoid
hemorrhage. The risk for
delayed cerebral ischemia
Delayed Cerebral Ischemia Diagnosis and Monitoring increases with subarachnoid
Diagnosing delayed cerebral ischemia is not easy. The combination of neurologic hemorrhage thickness and
examination and imaging studies can enhance the early detection and proper intraventricular hemorrhage,
management. Admission to the neurocritical care unit with frequent neurologic as demonstrated by the
modified Fisher Scale.
examination by experienced nurses and providers every 1 to 2 hours is necessary.
Delayed cerebral ischemia should be suspected if patients with SAH develop a
focal or global neurologic deficit or have a decrease of 2 or more points on the
Glasgow Coma Scale that lasts for at least 1 hour and cannot be explained by
another cause.

Experts have recommended that all patients with SAH undergo a head
CT at 24 to 48 hours after aneurysm treatment to establish any treatment-
related infarctions.57 Any subsequent new hypodensities not attributable to
EVD insertion or intraparenchymal hematoma should be regarded as cerebral
infarctions from delayed cerebral ischemia regardless of the clinical signs.
Patients with SAH should undergo physiologic or imaging monitoring
routinely during the risk period for delayed cerebral ischemia.13,24 Such
monitoring is usually multimodal and includes ICP, cerebral perfusion pressure,
continuous EEG, and transcranial Doppler (TCD) monitoring; DSA, CTA, and
CT perfusion (CTP) imaging are also used when indicated as well as brain tissue
oxygenation and microdialysis monitoring, when available.
TCD has been the longest used and best studied of all the monitoring
modalities. In the large vessels of the circle of Willis, TCD has adequate
sensitivity and specificity to detect increased cerebral blood flow velocities
secondary to cerebral vasospasm but is highly dependent on the operator and
cranial bone window (CASE 3-3B).63
Practitioners need to be aware that the sensitivity/specificity of TCD is good
for the middle cerebral and internal carotid arteries but is much lower for the
anterior cerebral arteries and posterior circulation arteries. Thresholds for the
diagnosis of cerebral vasospasm have been summarized.63
In addition, cerebral blood flow velocities can be elevated for other reasons
(hyperemia due to fever, induced hypertension, anemia), and therefore a
diagnosis of cerebral vasospasm should only be made when the ratio of mean
cerebral blood flow velocity of the intracranial vessel to mean cerebral blood flow
velocity of the extracranial internal carotid artery is elevated. Therefore, for the
diagnosis of middle cerebral artery vasospasm, routine measurement of the
Lindegaard ratio (mean velocity in the middle cerebral artery/mean velocity in
ipsilateral extracranial internal carotid artery) is prudent. A Lindegaard ratio
of >3 indicates cerebral vasospasm. Similar ratios exist for the other main
intracranial vessels.
DSA remains the gold standard for the detection of large- and middle-sized
artery vasospasm. CTA is now widely available and is often applied for
vasospasm screening before DSA given its high degree of specificity and lack of
invasiveness. CTA, however, can overestimate cerebral vasospasm. CTP imaging
with elevated mean transit time may be of additional value to CTA to assess for
decreased cerebral perfusion, but further investigations on the application of
CTP in SAH are needed.
Brain tissue oxygenation, cerebral blood flow, and microdialysis monitoring
can provide additional information when used in the context of multimodality
monitoring and may be able to detect early cerebral vasospasm before it becomes
symptomatic and before delayed cerebral ischemia occurs. Clinicians must
bear in mind the limitations of such monitoring, including the restriction to
monitoring local rather than global brain areas.
Continuous scalp EEG offers the advantage of monitoring broader regions of
the brain. Quantitative continuous EEG, if available, may offer easier
interpretation of bedside data even by providers not trained or certified to
interpret EEG. The cost, and thereby lack of widespread availability, is currently
limiting quantitative continuous EEG from becoming standard of care.
It is very important to differentiate between angiographic/TCD vasospasm
and clinical symptomatic vasospasm (CASE 3-3B).64 The former occurs in the
1646 DECEMBER 2018

majority of patients with SAH (70%) but has not been associated with outcome KEY POINTS
after SAH. Only symptomatic vasospasm, occurring in 30% of patients with
● Delayed cerebral
SAH, has been associated with delayed cerebral ischemia and poor outcome after ischemia should be
SAH.64 Given the risks of endovascular cerebral vasospasm treatment, experts suspected if patients with
recommend such treatment only for patients with symptomatic vasospasm, subarachnoid hemorrhage
while angiographic/TCD vasospasm should be managed with a careful watch develop a focal or global
neurologic deficit or have a
and wait approach with a very low threshold to trigger DSA and endovascular
decrease of 2 or more points
treatment.13,24 on the Glasgow Coma Scale
Some variability exists regarding the timing and frequency of the application that lasts for at least 1 hour
of the various monitoring modalities. At a minimum, the care for patients with and cannot be explained by
any other cause.
SAH should be protocolized using a written protocol and an algorithm. Patients
with SAH should be admitted to a neurocritical care unit and have their ● Patients with
aneurysm secured as quickly as possible, preferably within the first 6 to 12 hours subarachnoid hemorrhage
after presentation. should undergo physiologic
Monitoring in the neurocritical care unit includes daily TCD monitoring, or imaging monitoring
routinely during the risk
although in low-risk patients it may be sufficient to monitor every other day as period for delayed cerebral
long as neurologic monitoring can be performed every 1 to 2 hours. Some centers ischemia.
perform CTA/CTP or DSA routinely for all patients 5 to 7 days after admission to
screen for cerebral vasospasm. Most centers, however, perform these tests only if ● Transcranial Doppler has
adequate sensitivity and
concern arises for symptomatic vasospasm.
specificity to detect
In patients who are comatose or obtunded, it may be difficult to obtain a increased cerebral blood
reliable examination, and therefore TCD examination and, in addition, flow velocities secondary to
CTA/CTP or DSA for vasospasm screening may be required. Particularly in cerebral vasospasm in the
middle cerebral and basilar
patients with high-grade SAH with poor examination findings, diagnosis and
arteries but is highly
treatment initiation of delayed cerebral ischemia may be difficult, somewhat dependent on the operator
subjective, and mostly based on neuromonitoring findings. and cranial bone window.
At the author’s institution, the SAH treatment protocol dictates induced
hypertension, CT/CTA, and DSA when these patients have elevated TCD mean ● Digital subtraction
angiography remains the
velocities and elevated Lindegaard (or other) ratios (CASE 3-3B). Other centers gold standard for detection
use information from multimodality monitoring (continuous EEG or even of large- and middle-sized
intracortical depth EEG, brain tissue oxygenation, microdialysis, cerebral blood flow artery vasospasm.
monitoring) to decide if hypoperfusion or vasospasm may be occurring and when
● Only symptomatic
to send the patient for DSA. While randomized controlled data are lacking on the
vasospasm, occurring in
value of multimodality monitoring on short-term and long-term outcomes in the 30% of patients with
treatment of patients with SAH, resources at the various institutions may dictate, subarachnoid hemorrhage,
at least in part, how much advanced multimodality monitoring can be employed. has been associated with
delayed cerebral ischemia
and poor outcome after
Management subarachnoid hemorrhage.
At the author’s institution, all patients are treated with nimodipine and euvolemia.
Low-risk patients whose neurologic examination, TCD, and, if performed, CTA ● Hypervolemic,
remain unchanged are transferred to the neuro step-down unit under the care of hypertensive, and
hemodilutional (Triple H)
neurointensivists between days 8 and 10 and receive neurologic examinations less therapy is no longer
frequently (every 2 hours instead of hourly) than in the ICU. Patients are then supported by guidelines
discharged to the floor or home by day 14. High-risk patients whose neurologic because of the existing
examination, TCD, and, if performed, CTA remain unchanged will transfer to the evidence of adverse
associations with outcomes
floor or other lower level of care 14 days after SAH. If at any time the patient after the use of
develops elevated TCD mean cerebral blood flow velocities and abnormal CTA hemodilution. Standard
findings, the intensity of neurologic monitoring is escalated (CASE 3-3B). treatment is now
If patients experience a neurologic deterioration suggestive of delayed cerebral hypertensive and mild
hypervolemic therapy (HHT).
ischemia, certain rescue therapies are initiated. In the case of symptomatic

cerebral vasospasm and delayed cerebral ischemia, induced hypertension is

indicated per current guidelines (TABLE 3-4 and FIGURE 3-6). Hypervolemic,
hypertensive, and hemodilutional (Triple H) therapy is no longer supported
by guidelines because of the existing evidence of adverse associations with
outcomes after the use of hemodilution,13,24,65 and the standard treatment is now
hypertensive and mild hypervolemic therapy (HHT). Many institutions initiate
an IV fluid bolus (1 L to 2 L of 0.9% saline) and maintain fluids for euvolemia
or mild hypervolemia. Hypertension is preferably induced using α1 receptor
agonists by a continuous infusion (norepinephrine or phenylephrine). This
group of drugs are the vasopressors of choice in SAH, as the brain vessels lack α1
receptors, and therefore only systemic but not brain vasoconstriction is achieved.
Blood pressure augmentation should progress in a stepwise fashion with frequent
neurologic assessments at each step.
At the author’s institution, a mean arterial pressure (MAP) about 20 mm Hg
above the baseline MAP is set as the first goal (often MAP >90 mm Hg). Some
institutions use systolic blood pressure goals instead of MAP goals, and no evidence
exists to guide clinicians regarding whether one parameter is better than the other.
In institutions where systolic blood pressure goals are set for induced hypertension,
the initial goal for induced hypertension should be approximately 20 mm Hg to
40 mm Hg above the baseline systolic blood pressure. This commonly results in a
systolic blood pressure goal of >180 mm Hg or >200 mm Hg.
If the clinical examination has returned to the prior baseline examination, no
further blood pressure elevations are necessary, unless the clinical examination
deteriorates further at this blood pressure goal. In the latter case, further
increases in the blood pressure goal should be attempted. While no optimal or
maximum blood pressure goal is known, adverse effects on the cardiac and
pulmonary systems and the brain (for example, autoregulatory side effects with
elevated ICP with increasing MAP or posterior reversible encephalopathy
syndrome [PRES]) should be considered for each patient.
At the author’s institution, inotropic agents (milrinone, dobutamine) are
reserved for those patients with known poor cardiac output from acute or
chronic cardiomyopathy. If neurologic deficits persist despite induced
hypertension, the patient is sent for CT/CTA followed by DSA with endovascular
therapy if cerebral vasospasm is confirmed. A noncontrast head CT prior to DSA
is useful in ruling out hydrocephalus and determining preexisting stroke prior to
endovascular treatment. If other causes for the neurologic deterioration have
already been ruled out, and TCDs suggest cerebral vasospasm, the CTA may be
skipped to spare the patient radiation, iodine contrast, and to save time and allow
the patient to go to DSA immediately for treatment. Endovascular therapy using
intraarterial vasodilators (nicardipine, milrinone, verapamil) or angioplasty is
supported by prospective and retrospective observational data and is
recommended by guidelines (TABLE 3-4 and CASE 3-3B).13,24 At the author’s
institution, prophylactic angioplasty is not performed if cerebral vasospasm is
detected during TCD or CTA without neurologic deterioration because this
practice is associated with higher complication rates.13,24
MEDICAL COMPLICATIONS
SAH is a systemic disease, and patients commonly experience additional medical
complications. Anticipation of these complications leads to rapid recognition
and treatment.
1648 DECEMBER 2018

Cardiopulmonary KEY POINTS
Cardiopulmonary dysfunction is a well-known complication of SAH and can
● In the management of
range from minor ECG changes to severe stress cardiomyopathy and neurogenic patients with symptomatic
pulmonary edema. The incidence of left ventricular dysfunction in the first week vasospasm, hypertension is
after SAH ranges from 9% to 30%66,67 and can include regional wall motion preferably induced using α1
abnormalities not correlating with coronary artery territories or severe systolic receptor agonists by a
continuous infusion
left ventricular dysfunction with an ejection fraction of less than 30%. ECG
(norepinephrine or
changes can include T-wave inversions and prolonged QTc intervals and may be phenylephrine).
the culprit for arrhythmias such as bradycardia, atrial fibrillation, ventricular
tachycardia, and ventricular fibrillation. The severity of SAH is an independent ● Cardiopulmonary
predictor of cardiopulmonary injury, suggesting that the cardiopulmonary injury dysfunction is a well-
known complication of
is neurally mediated.68 Troponin elevation can be seen in up to 30% of patients, subarachnoid hemorrhage
but its significance is unclear. Certain ECG changes, such as prolonged QTc and can range from minor
intervals, have been reported to predict death.69 ECG changes to severe
Similarities have been observed between pheochromocytoma crisis and SAH, stress cardiomyopathy
and neurogenic
linking the observed cardiac changes to a catecholamine surge. Patients with SAH pulmonary edema.
can have a threefold increase in norepinephrine levels for 10 days or longer after
ictus, which normalize after this time period.70 Myocardial cell necrosis, also known ● The severity of
as contraction band necrosis, is the hallmark of a catecholamine surge and can be subarachnoid hemorrhage is
an independent predictor of
found in patients with pheochromocytoma and SAH.71 The central catecholamine
cardiopulmonary injury,
release has been localized to the posterior hypothalamus based on postmortem suggesting that the
pathologic studies,72 which found microscopic hypothalamic lesions including cardiopulmonary injury is
small hemorrhages and infarctions in patients with contraction band necrosis. neurally mediated.
Clinically, the catecholamine surge during aneurysm rupture results in direct
● Takotsubo
myocardial injury, leading to decreased inotropy and an increase in cardiac cardiomyopathy in
preload due to venous constriction, as well as increased cardiac afterload due to subarachnoid hemorrhage is
peripheral arterial constriction (FIGURE 3-7).73 Consequently, stroke volume associated with higher
diminishes, which cannot be compensated by reflex tachycardia, resulting in mortality and worse
long-term outcomes.
decreased cardiac output and neurocardiogenic shock. Because of loss of
myocardial compliance (“stunning” of the heart), the cardiac silhouette on a
ventriculogram and on chest radiograph has the characteristic shape of a
Japanese octopus fishing pot (tako-tsubo), which is why this disease has also been
named Takotsubo cardiomyopathy. Neurogenic cardiomyopathy in SAH is
associated with higher mortality and worse long-term outcomes.74
Pulmonary edema leading to hypoxia is also frequently encountered and
may occur either as a result from the acute left ventricular dysfunction or
independently as neurogenic pulmonary edema from substantial increases in
pulmonary capillary pressures from the sympathetic surge. FIGURE 3-7
summarizes the pathophysiology of cardiopulmonary complications mediated by
alpha and beta receptors. Cardiopulmonary complications after SAH are usually
transient and resolve within several days to 2 weeks. However, during this
period, the patient must be maximally supported to prevent secondary brain
injury from hypoxia and decreased cerebral perfusion. In extreme cases, the
insertion of an intraaortic balloon pump may be required to support the patient
until resolution of the transient symptoms.
At the author’s institution, every patient with SAH receives a baseline ECG,
echocardiogram, and chest x-ray on admission. Excessive fluid intake is avoided
with a goal of euvolemia and not hypervolemia. Lung-protective mechanical
ventilation with tidal volumes of less than 7 cc/kg of ideal body weight without
permissive hypercarbia is performed routinely. If delayed cerebral ischemia is

FIGURE 3-7
The pathophysiology of cardiopulmonary complications in subarachnoid hemorrhage (SAH).
SAH leads to a sudden catecholamine surge, which activates alpha, alpha + beta, and beta
receptors, leading to pulmonary and myocardial dysfunction as well as platelet aggregation.
Consequently, patients can develop neurogenic pulmonary edema, left ventricular
dysfunction (Takotsubo cardiomyopathy), and shock.
LVEF = left ventricular ejection fraction.
Modified with permission from Bassil R, et al.73 © 2017 Wolters Kluwer.
present and induced hypertension is initiated, inotropic agents may be used in

addition to vasopressors to increase cardiac contractility. Hypervolemia is
restricted to avoid or prevent worsening of pulmonary edema. A repeat
follow-up echocardiogram is performed 10 to 14 days after ictus to evaluate for
resolution of Takotsubo cardiomyopathy.
Fever
Fever is the most common medical complication after SAH, occurring in up to
70% of patients.13,24 Fever is more likely to occur in patients with high-grade
SAH and poor neurologic status. Fever has been associated with delayed cerebral
ischemia and worse clinical outcomes and is likely related to SIRS and chemical
meningitis rather than an infectious process. While fever is commonly treated
with therapeutic temperature modulation and induced normothermia, no clear
evidence currently indicates that such treatment is beneficial. Current
recommendations are to monitor body temperature and to rule out or treat
infectious etiologies. If fever is suppressed with induced normothermia,
shivering should be strictly avoided and aggressively treated if it occurs.
1650 DECEMBER 2018

Thromboembolism and Prophylaxis KEY POINTS
Deep vein thrombosis after SAH is common, with rates between 2% and 20%
● Fever is the most common
depending on the screening method. Patients with high-grade SAH are at medical complication after
greatest risk, presumably because of limited mobility. To prevent the potential subarachnoid hemorrhage,
life-threatening consequences of pulmonary embolism, mechanical venous occurring in up to 70%
thromboembolism prophylaxis should be initiated immediately on admission of patients.
with the use of pneumatic compression devices. At the author’s institution,
● Fever has been
chemoprophylaxis with subcutaneous fractionated or unfractionated heparin is associated with delayed
usually initiated immediately after endovascular aneurysm repair and within cerebral ischemia and worse
24 hours after craniotomy for clipping.13,24 Heparin-induced thrombocytopenia clinical outcomes and is
type II affects 6% of patients with SAH.75 The exact mechanism for this likely related to systemic
inflammatory response
observation is not clear. However, a clinical suspicion of this syndrome should syndrome and chemical
immediately be raised and diagnostic measures and treatment should be initiated meningitis, rather than an
when the platelet counts are decreasing rapidly and the patient has been exposed infectious process.
to fractionated or unfractionated heparin.
● Deep vein thrombosis
after subarachnoid
Glycemic Dysfunction hemorrhage is common,
with rates between 2%
Glycemic dysfunction is very common after SAH because of stress and has and 20%.
been associated with delayed cerebral ischemia and poor clinical outcome.
However, it remains unclear whether this is merely an association or causative. ● Mechanical venous
Hypoglycemia can lead to brain metabolic crisis and must be vigilantly avoided. thromboembolism
prophylaxis should be
In the absence of clinical trials of glucose control in patients with SAH, current initiated immediately on
recommendations are to maintain a blood glucose level between 80 mg/dL and admission with the use of
200 mg/dL (TABLE 3-4).13,24 pneumatic compression
devices. At the
author’s institution,
Hyponatremia chemoprophylaxis with
Hyponatremia is the most common electrolyte disorder in SAH and can occur in subcutaneous fractionated
or unfractionated heparin is
up to 30% of patients. Its cause is presumed to be hypothalamic dysfunction, usually initiated immediately
most commonly from cerebral salt wasting due to an increase in circulating brain after endovascular
natriuretic peptide levels. The syndrome of inappropriate secretion of aneurysm repair and within
antidiuretic hormone (SIADH) should always be considered but is generally 24 hours after craniotomy
for clipping.
uncommon in patients with SAH. Knowledge about how to differentiate cerebral
salt wasting and SIADH is a basic and very important skill of any clinician caring ● In the absence of clinical
for patients with SAH. Reviews of the diagnoses of both syndromes have been trials of glucose control in
published (FIGURE 3-8).76,77 patients with subarachnoid
hemorrhage, current
It is important to note that in both cerebral salt wasting and SIADH, the
recommendations are to
laboratory findings are similar: low serum sodium (<134 mEq/mL), low serum maintain a blood glucose
osmolality (<274 mmol/L), high urine sodium (>20 mmol/L), and high urine level between 80 mg/dL and
osmolality (>100 mmol/L). The only differentiating finding is the patient’s 200 mg/dL.
intravascular volume status; cerebral salt wasting is a hypovolemic state, while
● Hyponatremia is the most
patients with SIADH are euvolemic or even hypervolemic. It is of utmost common electrolyte
importance to correctly differentiate these two syndromes because treatment is disorder in patients with
opposite and an incorrect diagnosis with improper treatment can lead to subarachnoid hemorrhage
detrimental effects in patients with SAH. and can occur in up to 30%
of patients.
Cerebral salt wasting is treated with fluid administration and sometimes a
continuous infusion of hypertonic saline (1.5% to 3%) and fludrocortisone if
diuresis and natriuresis impede maintenance of adequate volume status. However,
patients with SIADH are treated with fluid restriction and sometimes diuresis with
loop diuretics. Serum sodium as well as the volume status must be followed closely.

FIGURE 3-8
Differentiating different types of hyponatremia. The optimal way to differentiate different
etiologies for hyponatremia is to follow this flow chart as follows: serum sodium followed by
serum osmolality followed by urine sodium followed by urine osmolality (bottom to top).
There is no difference in the laboratory findings between cerebral salt wasting syndrome
(CSWS) and syndrome of inappropriate secretion of antidiuretic hormone (SIADH), and the
only difference between both common hyponatremia syndromes in subarachnoid
hemorrhage is volume status. Cerebral salt wasting is a hypovolemic state, and SIADH is a
euvolemic or hypervolemic state. Hence, treatment strategies are opposite: Cerebral salt
wasting is treated with fluids with or without fludrocortisone, and SIADH is treated with fluid
restriction with or without diuresis.
Modified with permission from Stiefel D, et al, Neurocrit Care.76 © 2007 Humana Press.
As shown in FIGURE 3-8, it is also important to test thyroid and adrenal functions
as well as serum glucose (>500 mg/dL can result in pseudohyponatremia) and
triglyceride levels to adequately address other causes of hyponatremia.
Pseudohyponatremia (not due to true hyponatremia but from laboratory test
interference from extreme triglyceridemia) should be considered in patients
on propofol.
Anemia
Most patients with SAH will experience anemia during their hospitalization, which
is presumably due to excessive blood draws, blood loss from other reasons, or
systemic inflammation.23 Anemia and hemoglobin concentrations of less than
9 g/dL have been associated with delayed cerebral ischemia and poor clinical
1652 DECEMBER 2018

outcomes; however, optimal hemoglobin goal levels and transfusion thresholds are KEY POINTS
not known.78,79 A recent small, randomized controlled trial comparing the safety
● The laboratory findings
and efficacy of transfusion to higher hemoglobin levels (goal hemoglobin are similar in both cerebral
concentration of at least 10 g/dL or 11.5 g/dL) in patients with SAH demonstrated salt wasting and syndrome
safety of transfusing to these high hemoglobin levels, but no differences were seen of inappropriate secretion
in delayed cerebral ischemia and short-term (14 days) functional outcomes.79 of antidiuretic hormone. The
only differentiating finding is
the patient’s intravascular
PROGNOSTICATION AFTER SUBARACHNOID HEMORRHAGE volume status; cerebral salt
While established clinical scales such as the WFNSS and the Hunt and Hess Scale wasting is a hypovolemic
may be helpful in discriminating high-risk from low-risk patients, just like any state, while patients with
syndrome of inappropriate
prognostic scale, they were established for populations and must not be applied
secretion of antidiuretic
to individual patients. hormone are euvolemic or
Outcome is also influenced by many other factors, which are generally not even hypervolemic. It is of
included in prognostic scales, such as patient values and preferences, utmost importance to
comorbidities, social networks, resilience, and time for recovery. Unless the correctly differentiate these
two syndromes because
patient presents with bilaterally dilated pupils and a head CT or DSA inconsistent treatment is opposite.
with brain perfusion and life, all efforts should be made initially to salvage even
patients with very high-grade SAH with treatment of high ICP and ● Cerebral salt wasting is
hydrocephalus, followed by securing the aneurysm. Adequate protocolized treated with fluid
administration and
neurocritical care should be provided for the first 2 weeks or longer, at which sometimes a continuous
time, after establishing preexisting patient wishes and preferences with the infusion of hypertonic saline
family, further goals of care may need to be discussed. and fludrocortisone if
The Functional Recovery Expected After Subarachnoid Hemorrhage (FRESH) diuresis and natriuresis
impede maintenance of
scale is a recently published prognostic scale for expected 12-month cognitive
adequate volume status.
outcome and quality of life after SAH, and the same caution should be used with Patients with syndrome of
this scale as should be used with any prognostic scale.80 This score has excellent inappropriate secretion of
discrimination and calibration, has been externally validated, and may be antidiuretic hormone are
treated with fluid restriction
calculated at the bedside using a free smartphone app.81
and sometimes diuresis with
loop diuretics.
CONCLUSION ● Anemia and hemoglobin

SAH is a life-threatening type of hemorrhagic stroke and a neurologic emergency concentrations of less than
9 g/dL have been associated
that carries a high risk of morbidity and mortality. This female-predominant with delayed cerebral
disease should be approached in two phases: (1) expeditious and accurate ischemia and poor clinical
recognition of SAH, transfer to an appropriate high-volume center, and outcomes; however, optimal
identification and securement of the aneurysm and (2) observation, prevention, hemoglobin goal levels and
transfusion thresholds are
or swift treatment of medical and neurologic complications in a neurocritical care not known.
unit with state of the art neurocritical care adhering to established guidelines.
The main neurologic complications include hydrocephalus, seizures, brain
edema, and delayed cerebral ischemia. Common medical complications
encompass cardiopulmonary complications, neuroendocrine disorders, and
fever, which require expert care.
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DISCLOSURE
Continued from page 1623
in Brain Injured Patients) trial sponsored by C. R.
Bard Inc. Dr Muehlschlegel has received
compensation for serving as a course director for
the American Academy of Neurology.

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Subarachnoid REVIEW ARTICLE

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recognition and improved treatment strategies, the prehospital and 30-day

TABLE 3-1 Risk Factors for Subarachnoid Hemorrhagea

Modifiable Risk Factors

1624 DECEMBER 2018

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Head Computed Tomography

Phase 1: Diagnosis and Aneurysm Treatment (Minutes to Hours)

1626 DECEMBER 2018

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1628 DECEMBER 2018

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Perimesencephalic Subarachnoid Hemorrhage

1630 DECEMBER 2018

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A 23-year-old man presented to the emergency department for CASE 3-2

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Airway, Breathing, and Circulation

World Federation of Neurological

Glasgow Neurologic Subarachnoid Intraventricular

1 15 No motor 1 Awake, alert, no cranial 0 Absent Absent

2 13–14 No motor 2 Awake, alert, moderate to 1 Thin Absent

3 13–14 Motor deficit 3 Confusion or lethargy, with 2 Thin Present

4 7–12 With or without 4 Stuporous, more severe 3 Thickb Absent

5 3–6 With or without 5 Comatose, motor 4 Thickb Present

1632 DECEMBER 2018

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Antifibrinolytics ● The “gold standard”

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American Heart Association/American

CONTINUED ON PAGE 1635

1634 DECEMBER 2018

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American Heart Association/American

Cardiopulmonary No recommendations given Baseline cardiac assessment with serial

CONTINUED ON PAGE 1636

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CONTINUED FROM PAGE 1635

American Heart Association/American

1636 DECEMBER 2018

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Critical Care Management of Subarachnoid Hemorrhage

Preference for Treatment of Unsecured Aneurysmsa TABLE 3-5

Treatment Type Clinical or Aneurysm Factors Supporting Treatment Type

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CASE 3-3A A 51-year-old man presented to the emergency department of a

1638 DECEMBER 2018

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postulated that the negative impact of SIRS on functional outcome is mediated in

Seizures and Seizure Prophylaxis

1640 DECEMBER 2018

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COMMENT This case demonstrates how asymptomatic cerebral vasospasm on TCD