Prevalence and Risk Factors Associated With Reversed
Robin Hood Syndrome in Acute Ischemic Stroke
Andrei V. Alexandrov, MD; Huy Thang Nguyen, MD; Marta Rubiera, MD;
Anne W. Alexandrov, PhD; Limin Zhao, MD; Ioannis Heliopoulos, MD; Alice Robinson, RVT;
Jennifer DeWolfe, DO; Georgios Tsivgoulis, MD, FESO
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Background and Purpose—Early deterioration can occur after acute stroke for a variety of reasons. We describe a
hemodynamic steal and associated neurological deterioration, the reversed Robin Hood syndrome (RRHS). We aimed
to investigate the frequency and factors associated with RRHS.
Methods—Consecutive patients with acute cerebral ischemia underwent serial National Institutes of Health Stroke Scale
and bilateral transcranial Doppler monitoring with breathholding. Steal magnitude (%) was calculated from transient
mean flow velocity reduction in the affected arteries at the time of velocity increase in normal vessels. Excessive
sleepiness and likelihood of sleep apnea were evaluated by the Epworth Sleepiness Scale and Berlin Questionnaire.
Results—Among 153 patients (age, 61⫾14 years; 48% women; 21% transient ischemic attack) admitted within 48 hours
from symptom onset, 21 (14%) had steal phenomenon (median steal magnitude, 20%; interquartile range, 11%; range,
6% to 45%), and 11 (7%) had RRHS. RRHS was most frequent in patients with proximal arterial occlusions (17% versus
1%; P⬍0.001). The following factors were independently (P⬍0.05) associated with RRHS (multivariate logistic
regression model): male gender, younger age, persisting arterial occlusions, and excessive sleepiness (P⬍0.001). A
1-point increase in the Epworth Sleepiness Scale was independently related to an increased likelihood of RRHS of 36%
(95% CI, 7% to 73%).
Conclusions—RRHS and hemodynamic steal can be found in 7% and 14%, respectively, of consecutive patients with
stroke without other known causes for deterioration. Patients with persisting arterial occlusions and excessive sleepiness
can be particularly vulnerable to the steal. (Stroke. 2009;40:2738-2742.)
Key Words: arterial occlusion 䡲 reversed Robin Hood syndrome 䡲 sleep apnea 䡲 stroke 䡲 transcranial Doppler
N
eurological deterioration can occur in approximately
15% of patients with acute stroke.1–3 Several mechanisms can lead to ischemic lesion extension and subsequent
neurological worsening, including reocclusion, edema progression, and cardiovascular instability.4 – 6 However, these
long-recognized mechanisms do not account for all cases of
neurological deterioration or symptom recurrence. Changes
in cerebral hemodynamics can be detected in real time using
transcranial Doppler (TCD), and several groups, including
ours, deployed this modality to determine predictors of
neurological deterioration.4,6 – 8
We observed paradoxical decreases in flow velocity during
episodes of hypercapnia in vessels supplying ischemic areas
of the brain at the time of expected velocity increase in
nonaffected vessels.8 Hypercapnia triggered vasodilation
more effectively in normal vessels, thus producing arterial
blood flow steal toward the path of least resistance. The steal
magnitude was linked to severity of neurological worsening
in patients with acute stroke.8,9 We termed this “reversed
Robin Hood” for an analogy with “rob the poor to feed the
rich.”8 In the first documented cases of reversed Robin Hood
syndrome (RRHS), neurological worsening was also more
pronounced in patients with sleep apnea,8 a condition that can
trigger a perfect storm in a patient with acute stroke, whereas
apnea correction can reduce the chances of new vascular
events.10 There is a growing interest in obstructive sleep
apnea and noninvasive ventilatory correction in acute
stroke,11,12 and RRHS may provide a missing link between
the respiratory status and neurological worsening.
However, it remains unknown how often the steal and
clinical syndrome can be detected. We therefore set out to
prospectively determine the prevalence and risk factors associated with intracranial hemodynamic steal phenomenon and
RRHS in patients with acute cerebral ischemia. We hypothesized that RRHS would be positively associated with the
likelihood of obstructive sleep apnea syndrome and with
Received January 16, 2009; final revision received February 15, 2009; accepted March 19, 2009.
From the Comprehensive Stroke Center (A.V.A., H.T.N., M.R., A.W.A., L.Z., A.R., J.D., G.T.), University of Alabama Hospital, Birmingham, Ala;
the Department of Neurology (I.H., G.T.), Democrition University of Thrace School of Medicine, Alexandroupolis, Greece; and Sleep Disorder Medicine
(J.D.), the Department of Neurology, University of Alabama at Birmingham, Birmingham, Ala.
Correspondence to Andrei V. Alexandrov, MD, Comprehensive Stroke Center/Neurology, The University of Alabama at Birmingham, RWUH M226,
619 19th Street South, Birmingham, AL 35249-3280. E-mail [email protected]
© 2009 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.109.547950
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Alexandrov et al
Reversed Robin Hood Syndrome Prevalence
2739
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Figure. Velocity changes indicating intracranial steal during breathholding in a patient with RRHS. SM was calculated at 20 seconds
after the initiation of breathholding. SM⫽[(43 cm/s⫺51 cm/s)/51 cm/s]⫻100⫽[⫺8/51]⫻100⫽⫺16%.
greater neurological deterioration in the setting of acute
cerebral ischemia.
Subjects and Methods
Consecutive patients with symptoms of both posterior and anterior
acute cerebral ischemia admitted within 48 hours from symptom
onset to our tertiary hospital stroke service were prospectively
evaluated. Patients who met inclusion criteria were adults ⱖ19 years
of age, had an ischemic stroke or transient ischemic attack (TIA), had
temporal windows for TCD examination, and consented to participation in the study. According to the Trial of Org 10172 in Acute
Stroke Treatment criteria, ischemic strokes were classified based on
etiopathogenetic mechanisms into the following groups: large artery
atherosclerotic stroke, cardioembolic stroke, small artery occlusion
or lacunar stroke, and infarct of undetermined cause.13 Because we
aimed to detect the prevalence of RRHS in consecutive patients with
acute cerebral ischemia, all ischemic stroke subtypes were included
in the present study. Patients with known causes of clinical or
neurological deterioration, including reocclusion, continuing embolization, edema with mass effect, cardiovascular instability, and
hemorrhagic transformation were excluded from the study. Consecutive TCD evaluations were performed on a daily basis during
hospitalization to document the presence of reocclusion as a cause of
deterioration. The project was approved by our Institutional Review
Board.
Neurological deficits were measured by serial National Institutes
of Health Stroke Scale (NIHSS) scores obtained by certified stroke
team members. Neurological deficits were assessed using NIHSS
evaluations on a daily basis during hospitalization. Standard diagnostic TCD and bilateral TCD monitoring with voluntary breathholding14 were performed by registered vascular technologists or
registered vascular technologist-eligible sonographers. TCD monitoring of the symptomatic and asymptomatic side was performed
simultaneously. As an indirect measure of the effectiveness of
breathholding in producing hypercapnia, we used the increase in
mean flow velocity (MFV) in the asymptomatic side, which was
quantified as a breathholding index (BHI) of ⬎0.69 at the end of
breathholding.15 If the BHI in the nonaffected vessel was ⱕ0.69, the
breathholding procedure was repeated. No case was excluded from
the present study on the basis of ineffective breathholding. We
measured the MFV changes during 15 to 30 seconds of breathholding (a technique modified from Markus and Harrison14).8 Persistence
of an arterial occlusion was documented from CT or MR angiography. The time elapsed between baseline TCD assessment and CT
angiography or MR angiography was ⬍48 hours in all cases.
Thrombolysis in Brain Ischemia flow grades16 were used to further
guide TCD assessment of hypercapnia-induced velocity changes in
the affected brain vessels. More specifically, if there was a decrease
in flow during the breathholding in the occluded vessel, this was also
quantified using Thrombolysis in Brain Ischemia flow grades in
addition to measuring MFV changes. Collaterals on TCD were
identified using previously validated criteria.17–20 The presence of a
proximal arterial occlusion was diagnosed when a Thrombolysis in
Brain Ischemia flow grade of 0 to 3 was identified in any of the
following vessels: M1 middle cerebral artery (MCA), M2 MCA,
terminal internal carotid artery, anterior cerebral artery, posterior
cerebral artery, vertebral artery, and basilar artery.17–20
Our TCD assessment of vasomotor reactivity differs from previously proposed techniques that focus on steady-state conditions
achieved either at the end of breathholding or a plateau response to
dose-controlled CO2 inhalation or Diamox injection. Instead, we
focused on the initial velocity changes at the time when breathholding just induced an initial rise in CO2. Our rationale for choosing this
methodology to quantify this steal phenomenon has been recently
described.8 Briefly, previous steady-state methodologies such as the
BHI assess velocity changes at the end of 30 seconds breathholding
and therefore do not take into account possible transient velocity
decreases. If steal occurs during breathholding, it may also manifest
as a velocity decrease at the time of initial normal vessel dilation
(that could be expected at 15 to 30 seconds) as pressure gradient
shifts toward vessels that can dilate more in response to hypercapnia.
Hypercapnia induces vasodilatation mainly at the arteriolar level.
This is accompanied by a decrease in resistance in feeding vessels. In
turn, blood flow moves faster into a dilated vascular bed, thus
increasing velocities in the proximal intracranial vessels. This is
consistently seen in normal vessels on the nonaffected side of the brain.
If a hemodynamic steal occurs during breathholding, it manifests as a
velocity decrease in the affected vessel at the time of normal vessel
dilation as pressure gradient shifts toward vessels that can dilate
more in response to hypercapnia.
Therefore, steal was defined as an MFV decrease in the affected
vessel at the time of hypercapnia-induced velocity increase in the
normal MCA. The vascular steal phenomenon had to occur in the
vascular territory considered responsible for the patient’s ischemic
stroke or TIA for the patient to be classified as having RRHS. The
steal magnitude (SM, %) was quantified as the maximum negative
percent velocity reduction during breathholding (Figure):
SM⫽[(MFVm⫺MFVb)/MFVb]⫻100, where m is minimum and b
is baseline MFV.8 Steal was considered present when SM was
negative, ie, SM ⬍0 in the affected vessel.
In patients with brainstem strokes referable to the basilar artery,
bilateral transtemporal insonation was performed. We monitored
2740
Stroke
August 2009
Table 1.
Baseline Characteristics
Variable
RRHS
(n⫽11)
Age, years
51⫾9
62⫾14
Gender, female
1 (9%)
72 (51%)
Race, white
8 (73%)
87 (61%)
0.737
Diabetes mellitus
1 (9%)
29 (20%)
0.324
Dyslipidemia
9 (82%)
103 (73%)
0.394
Atrial Fibrillation
1 (8%)
9 (6%)
0.537
CAD
4 (36%)
22 (16%)
0.093
LVA
10 (91%)
50 (35%)
⬍0.001*
2 (0–19; IQR, 3)
3 (0–13; IQR, 8)
0.321
24⫾10
1⫾4
⬍0.001*
Baseline NIHSS
SM, %
Non-RRHS
(n⫽142)
Table 2. Factors Independently Associated With RRHS on
Multivariate Logistic Regression Models
P
Variable
Coefficient (SE)
0.003*
Age (per 1-year increase)
⫺0.156 (0.059)
0.007*
Presence of proximal
arterial occlusion
3.141 (1.524)
ESS score (per 1-point
increase)
0.308 (0.122)
1.36 (1.07–1.73)
0.012
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ICA 50%–100% stenosis
4 (36%)
25 (18%)
0.131
Reversed OA
4 (36%)
17 (12%)
0.046*
Anterior crossfilling
5 (46%)
17 (12%)
0.010*
PcomA flow
3 (27%)
7 (5%)
0.026*
ESS score ⬎12
5 (50%)
18 (13%)
0.008*
Berlin Questionnaire 2⫹
3 (38%)
65 (51%)
0.359
CAD indicates coronary artery disease; LVA, large vessel atheromatous
stroke mechanism; ICA, internal carotid artery; OA, ophthalmic artery; PcomA,
posterior communicating artery; IQR, interquartile range; 2⫹, at least 2
components of the questionnaire were positive.
*P⬍0.05.
posterior circulation (top of the basilar artery: ipsilateral P1
posterior cerebral artery and contralateral P1 posterior cerebral
artery)18 with one probe, whereas with the other one, anterior
circulation was monitored (ipsilateral MCA). Steal phenomenon
was documented when there was reduction in P1 posterior
cerebral artery (ipsilateral to the probe monitoring posterior
circulation) MFV during breathholding with simultaneous increase in MCA MFV (ipsilateral to the probe monitoring anterior
circulation) during breathholding.
After the steal was documented on TCD, reversed Robin Hood
syndrome was suspected if new or recurrent neurological worsening
by ⱖ2 NIHSS points were observed without concurrent changes in
blood pressure or arterial patency.8 Given the current American
Heart Association recommendations that advocate against profound reductions of blood pressure (exceeding ⬎20%) in the setting of
acute cerebral ischemia,21 a range of blood pressure oscillations of
ⱕ20% was used for considering blood pressure as stable. Changes of
arterial patency were evaluated using consecutive TCD evaluations
on a daily basis during hospitalization. For the definition of neurological deterioration in patients with TIA, we used a cutoff of ⱖ2 points in
NIHSS score in the serial NIHSS assessments, because all patients with TIA
had a baseline NIHSS score of 0 on hospital admission.
Demographics and common risk factors were documented from
routine stroke workup. Patients or family members answered the
Epworth Sleepiness Scale (ESS) at the baseline assessment within
the first 24 hours from hospital admission, a subjective measure of
sleep propensity with scores ⬎10 defined as excessive sleepiness.22
The likelihood of obstructive sleep apnea was evaluated with the
Berlin Questionnaire at the baseline assessment within the first 24
hours from hospital admission. Both the ESS and Berlin Questionnaire referred to the patient’s condition before the stroke. Positive
scores in 2 or 3 of 3 categories were defined as high risk for
obstructive sleep apnea.23,24
Statistical analyses were performed with the SPSS 15.0 software
(SPSS Inc). The 2-tailed Fisher exact test or Pearson ␹2 test for
categorical variables and Student t test or Mann–Whitney U test for
continuous variables were used to assess intergroup differences.
Correlations between continuous variables were assessed by the
OR (95% CI)
P
0.86 (0.76 – 0.96)
0.008
23.14 (1.17–458.63)
0.039
Spearman correlation coefficient. We evaluated the interrater reliability for detection of RRHS using our newly developed dynamic
criteria8 and the more traditional steady-state criteria such as the
BHI15 using Cohen’s ␬ statistic. Initially, univariable analyses of
potential predictors (demographic characteristics, stroke risk factors,
admission NIHSS score, systolic blood pressure and serum glucose
levels, presence of proximal arterial obstruction on baseline TCD
assessment, excessive sleepiness, and likelihood of sleep apnea
syndrome on the basis of the ESS and Berlin Questionnaire,
respectively) were performed. To maximize sensitivity, those variables with a univariable association of P⬍0.1 were included as
candidates into a multivariable logistic regression model and then
removed by the backward stepwise selection procedure. To confirm
the robustness of multivariable models, we repeated all multivariable
analyses using a forward selection procedure. Predictor variables that
were significant at P⬍0.05 were retained in the multivariable model.
A level of P⬍0.05 was accepted as statistically significant.
Results
We studied 153 patients who met inclusion criteria: age 61⫾14
years, women 48%, and 21% with TIA. We found 21 (14%)
patients who had steal phenomenon (median SM, 20%; interquartile range, 11%; range, 6% to 45%) on TCD. The median
elapsed time between the beginning of breathholding and documentation of the SM was 23 seconds (range, 17 to 29 seconds).
Their baseline characteristics are summarized in Table 1.
RRHS was documented in 11 cases (7% of the study
population) using our recently developed criteria.8 The RRHS
prevalence using a more steady-state methodology such as
the BHI15 was 6% (n⫽9). The measure of agreement between
the 2 sets of criteria was satisfactory (Cohen’s ␬⫽0.89,
P⬍0.0001). The magnitude of steal was directly related with
the NIHSS score increase (range, 0 to 13 points; Spearman’s
correlation coefficient 0.453; P⫽0.039). RRHS was most
frequent in patients with proximal arterial occlusions (17%
versus 1%; P⬍0.001) and those with both arterial
occlusions⫹excessive sleepiness (40% versus rest 5%;
P⫽0.003). Among the patients with proximal arterial occlusions, a steal phenomenon was identified in the following
vessels: M1 MCA, M2 MCA, and terminal internal carotid
artery. In all of these cases, the steal phenomenon was
identified in the vessels with acute occlusions. No steal
phenomenon was identified in patients with basilar artery
occlusions (n⫽2). Half of patients with RRHS had high ESS
scores of ⬎12 points (50% versus rest 13%; P⫽0.008).
The following factors were independently (P⬍0.05)
associated with RRHS on multivariate logistic regression
model (Table 2): younger age (P⫽0.008), presence of
proximal arterial occlusions (P⫽0.039) and higher ESS
scores (P⫽0.012). A 1-point increase in the ESS score was
independently related to an increased likelihood of RRHS
of 36% (95% CI, 7% to 73%). Greater likelihood of
Alexandrov et al
obstructive sleep apnea (Berlin Questionnaire 2 or more
positive parts) was more common among patients with
excessive sleepiness (85%) versus rest (44%; P⫽0.01).
Neurological improvement at discharge was lower if
RRHS was present (median NIHSS decrease 4%; interquartile range, 100%) versus rest (5%; interquartile range,
100%; P⫽0.039).
Discussion
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Our study showed that intracranial steal and an associated
clinical syndrome leading to neurological worsening can
be found in a substantial number of consecutive patients
with stroke or TIA. Our findings indicate that RRHS was
associated with a trend toward less neurological improvement at hospital discharge, although it should be noted that
the present report was not designed to investigate a
temporal and potentially causative association among hypercapnia, vascular steal phenomenon, and neurological
deterioration.
Our study confirms our previous observations8 and
provides data on the syndrome prevalence and associated
risk factors. Our data highlight the need to pay more
attention to patients with persisting arterial occlusions and
excessive sleepiness because these 2 conditions may lead
to hemodynamic compromise and subsequent neurological
worsening. Although we did not measure arterial blood
gases, we suspect that sleep can lead to decreased cardiac
output, hypoventilation, and at least transient hypercarbia,
factors that can compromise cerebral perfusion. Patients
with symptomatic steal had a greater need for collateral
flow recruitment, because the underlying pathogenic
mechanism of cerebral ischemia in the vast majority of
patients with RRHS was large artery atherosclerotic stroke
(91%; Table 1). We hypothesize that these collaterals
appeared insufficient to fully compensate during sleep and
transient hypercapnia.
Although the likelihood of obstructive sleep apnea
syndrome did not appear as a factor independently associated with the steal, the majority of patients with excessive
sleepiness had Berlin scores predictive of obstructive sleep
apnea syndrome. Perhaps the next step could be to evaluate
an association between hypoventilation during sleep and
the hemodynamic sleep phenomenon. The question is
whether a confirmation of sleep apnea with a formal sleep
study is necessary to initiate ventilatory correction or,
because these hemodynamic changes are so “front-loaded”
and common with sleepiness, there is little time, if any, to
do a formal study. Perhaps a prospective documentation of
sleep apnea using unattended stroke unit-based polysomnography or even simple nocturnal oximetry25 (as valid
proxies for full-scale sleep laboratory polysomnography)
would be sufficient to better understand the association
between hypercapnia during sleep apnea and neurological
deterioration caused by RRHS.
Our study has limitations. First and most important,
because we aimed to document the prevalence of RRHS in
consecutive patients with symptoms of acute cerebral
ischemia, we included in the present study both patients
with posterior and anterior circulation symptoms. There-
Reversed Robin Hood Syndrome Prevalence
2741
fore, it may be argued that is unclear whether the effect of
hypercapnia is exerted directly through the arterial vessels
or else through the response of brainstem chemoceptors.
Also, the simultaneous TCD monitoring of posterior (top
of the basilar) and anterior circulation (MCA) is technically challenging and this may be related to the fact that we
did not document any steal phenomenon in strokes referable to the basilar artery. Second, we performed no
monitoring of respiratory function and subsequently we are
unable to evaluate a potential relationship between hypercapnia and neurological worsening. Our group plans to
address this question in a future study. Third, we used only
one Doppler test that provides only a snapshot and does not
answer the question what happens to the steal over time.
Fourth, because only proximal vessels were studied, we
cannot state how often the steal can affect more distal
vessels (ie, if an occlusion is more distal than M2). Of
note, however, our inability to detect this phenomenon in
distal MCA branches would result only in underestimating
the prevalence of RRHS. Fifth, our study did not show an
independent association between greater likelihood of
obstructive sleep apnea syndrome and RRHS/steal likely
due to the sample size of the patient population studied.
However, an alternative explanation could be given. Sleepiness is more common with larger strokes likely leading to
hypoventilation and hypercapnia that can have a more
profound effect producing symptomatic steal with or
without sleep apnea. Because the volume of ischemic
strokes was not documented in the present report, the
potential relationship between ischemic stroke size and
excessive sleepiness as well as occurrence of RRHS
remains to be determined in a future study. Furthermore,
we plan to further investigate the trend toward less
neurological improvement during hospitalization in patients with proximal arterial occlusions and RRHS compared with cases with proximal arterial occlusions and
absent vascular steal phenomenon, because the documented 1% difference in neurological improvement is
hardly strong evidence for a meaningful clinical impact.
Sixth, the introduction of novel dynamic ultrasonographic
criteria for the detection of RRHS may constitute another
study limitation. Interestingly, the interrater agreement
between our newly developed and more traditional steadystate criteria such as the BHI for detecting RRHS was
satisfactory (␬⫽0.89). Nevertheless, we consider that our
results regarding RRHS prevalence should be cautiously
interpreted and replicated in a larger series of patients by
other independent investigators using both recent dynamic
and more traditional steady-state ultrasonographic criteria.
Finally, it should be acknowledged that ESS and the Berlin
Questionnaire are designed for outpatient ambulatory use
and may not be applicable in patients with acute stroke.
This is the reason why, in cases of noncooperative patients
(sustaining a severe stroke), we asked the relatives to
answer the questionnaires. Also, the ESS and Belin Questionnaire have been previously used in studies evaluating
sleep apnea in the setting of acute ischemic stroke.26,27
In summary, RRHS and hemodynamic steal can be found
in a substantial number of consecutive patients without other
2742
Stroke
August 2009
known causes for deterioration. Patients with persisting
arterial occlusions and excessive sleepiness may be particularly vulnerable to the steal because both excessive sleepiness
and proximal arterial occlusions were independently associated with a higher likelihood of RRHS in our multivariate
analyses. With or without subsequent confirmation of sleep
apnea, these patients may represent a target group for early
noninvasive ventilatory correction after acute ischemic
stroke.
Disclosures
None.
14.
15.
16.
17.
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Prevalence and Risk Factors Associated With Reversed Robin Hood Syndrome in Acute
Ischemic Stroke
Andrei V. Alexandrov, Huy Thang Nguyen, Marta Rubiera, Anne W. Alexandrov, Limin Zhao,
Ioannis Heliopoulos, Alice Robinson, Jennifer DeWolfe and Georgios Tsivgoulis
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Stroke. 2009;40:2738-2742; originally published online May 21, 2009;
doi: 10.1161/STROKEAHA.109.547950
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