Research

Anemia on admission predicts short- and long-term outcomes in patients with

acute ischemic stroke
Haralampos Milionis1,2, Vasileios Papavasileiou1,3, Ashraf Eskandari1,
Suzette DAmbrogio-Remillard1, George Ntaios1,3, and Patrik Michel1*
Background It is still debatable whether anemia predicts
stroke outcome.
Aim To describe the characteristics of patients with acute ischemic stroke (AIS) and anemia and identify whether hemoglobin status on admission is a prognostic factor of AIS outcome.
Methods All 2439 patients of the Acute Stroke Registry and
Analysis of Lausanne (ASTRAL) between January 2003 and
June 2011 were selected. Demographics, risk factors, prestroke
treatment, clinical, radiological and metabolic variables in
patients with and without anemia according to the definition
of the World Health Organization were compared. Functional
disability and mortality were recorded up to 12 months from
admission.
Results Anemic patients (175%) were older, had lower body
mass index, higher rates of coronary artery disease (CAD),
atrial fibrillation, diabetes mellitus and peripheral artery
disease. Anemia was associated with more severe stroke manifestations, lower systolic and diastolic blood pressure measurements, worse estimated glomerular filtration rate and
elevated C-reactive protein concentrations upon admission
and with increased modified Rankin scores during the followup. Anemic patients had higher 7-day, 3-month and 12-month
mortality, which was associated with hemoglobin status and
other factors, including age, CAD, stroke severity, and baseline
C-reactive levels. Hemoglobin levels were inversely associated
with recurrent stroke and mortality throughout the 12-month
follow-up.
Conclusion Anemia is common among AIS patients and is
associated with cardiovascular comorbidities. Low hemoglobin
status independently predicts short and long-term mortality.
Key words: anemia, disability, hemoglobin, ischemic stroke, mortality,
outcome

Introduction
Anemia is associated with increased mortality, decreased physical
performance and disability regardless of the underlying cause
(1,2). It is associated with adverse outcomes in patients with acute
myocardial infarction, congestive heart failure and chronic kidney
disease (36).
Correspondence: Patrik Michel*, Neurology Service, Centre Hospitalier
Universitaire Vaudois and University of Lausanne, Lausanne CH-1011,
Switzerland.
E-mail: patrik.michel@chuv.ch
1
Neurology Service, Centre Hospitalier Universitaire Vaudois, University
of Lausanne, Lausanne, Switzerland
2
Department of Internal Medicine, School of Medicine, University of
Ioannina, Ioannina, Greece
3
Department of Medicine, Medical School, University of Thessaly, Larissa,
Greece
Received: 5 March 2014; Accepted: 5 August 2014
Conflict of interest: None declared.
DOI: 10.1111/ijs.12397
2014 World Stroke Organization

Anemia represents a risk factor for ischemic stroke, and is

associated with a higher mortality following hospitalization (7,8).
Low hemoglobin levels are associated with decreased oxygencarrying, inflammatory response, alterations in blood viscosity
and impairment of cerebral autoregulation (9,10). Nonetheless,
data with regard to the relationship between anemia status upon
admission and short- and long-term outcome post-stroke are
scarce (1113). There are no specific recommendations as to the
management of acute stroke patients with anemia other than
sickle cell disease (14). It would be therefore useful to know the
range of hemoglobin or the severity of anemia on presentation to
identify patients at higher risk of adverse outcomes and to further
design potential intervention.

Aim
In this study, we examined the characteristics of patients with
anemia in a consecutive series of patients with acute ischemic
stroke and assessed the relationship between anemia and stroke
outcome.

Methods
We used data derived between January 2003 and June 2011 from
the Acute STroke Registry and Analysis of Lausanne (ASTRAL).
Design, methods of data collection and definitions of recorded
variables have been described elsewhere (15). All patients receive
a basic blood chemistry profile on admission that includes full
blood count, INR, apTT, glucose, creatinine, sodium, potassium,
total cholesterol and mostly CRP. These values are often
repeated in the subacute phase but were not used for this
analysis.
Acute stroke management and secondary prevention of
ASTRAL patients followed current European Stroke Organization
(ESO) guidelines (16).
The World Health Organization guidelines that define anemia
as a blood hemoglobin level on admission of <12 g/dl for women
and <13 g/dl for men were used (17). Estimated glomerular filtration rate (eGFR) was calculated by Modification of Diet in
Renal Disease (MDRD) formula (18). Stroke severity was assessed
with the National Institute of Health Stroke Scale Score (NIHSS).
Functional outcome was assessed with the modified Rankin Scale
score (mRS); favorable functional outcome was defined as
mRS = 02.
The scientific use of the ASTRAL data was approved by the
ethics commission for research on humans of the Canton of Vaud,
Subcommission III.
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H. Milionis et al.

Statistical analysis
Statistical analysis was performed to compare stroke patients with
anemia vs. nonanemic patients in terms of demographics, preexisting conditions (comorbidities), medications prior to stroke
event, clinical and laboratory characteristics on admission and
subacutely, treatment modalities, favorable outcome (defined as
mRS = 02) at 3 and 12 months and mortality at seven-days,
three-months and one-year after stroke onset.
After testing for statistical normality, dichotomous or categorical variables were compared with the 2-test and continuous variables were compared with the unpaired t-test or MannWhitney
U-test, as indicated. Furthermore, univariate and multivariate
logistic regression analyses were performed to identify factors
associated with anemia in stroke patients. Associations are presented as odds ratios (OR) with their corresponding 95% confidence intervals (95%CI). The KaplanMeier product limit
method was used to estimate the probability of survival at 12
months after the index event according to the presence of anemia.
To evaluate the contribution of anemia (dichotomous variable)
and the levels of hemoglobin (continuous variable) on outcomes,
a univariate Coxs proportional hazards model was initially used.
Multivariate analyses were performed including demographics,
preexisting conditions, medications prior to stroke, clinical and
laboratory features on admission. Associations are presented as
hazard ratios (HR) with their corresponding 95% confidence
intervals (CIs). To confirm the robustness of the multivariable
models, we performed all analyses using a forward selection procedure. HosmerLemeshow statistic was used to evaluate models
goodness-of-fit. Significance levels were set at P < 005 in all cases.
Analyses were performed utilizing stata 111 (College Station,
Texas) and spss version 150 (SPSS Inc., Chicago, IL).

Results
All 2439 patients registered during the observation period were
included in the analysis; 427 (175%) were diagnosed with
anemia.
There was a strong correlation between hemoglobin levels and
hematocrit (Spearmans rho, 096, P < 0001). Demographic data,
comorbidities, treatment, medication prior and post stroke and
metabolic parameters between anemic and nonanemic patients
are summarized in Table 1. Anemic patients were older than
nonanemic ones which could explain most of the differences
observed in other parameters in Table 1. In multivariate linear
regression analysis, increasing age, decreasing BMI, CAD, hypertension and diabetes were independent predictors of anemia in
patients with stroke (Table 2). There was an inverse relationship
between anemia and the presence of dyslipidemia, diastolic blood
pressure measurements and serum glucose levels; on the contrary,
there was a positive association with CRP levels on admission
(Table 2).
Functional independence at 3 and 12 months was less frequent
in anemic patients. Ordinal shift analysis showed an increase in
mRS scores in anemic patients (Fig. 1). There was a tendency for
higher stroke recurrence rates in anemic patients (Table 3). Risk

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Fig. 1 Modified Rankin Scale (mRS) at 3 months (a) and 12 months (b)
according to the presence of anemia. Unadjusted odds ratios for patients
with anemia vs. nonanemic patients have been calculated with mRS = 02
(i.e. favorable outcome) as the reference category.

of early (up to three-months) and late (up to 12 months) recurrent stroke was higher in patients presenting with anemia (log
rank test, 4860, P = 0027 and 6391, P = 0011, respectively;
Fig. 2a). However, in multivariate cox-regression analysis,
anemia was not a significant predictor of stroke recurrence during
follow-up.
Mortality rates at 7 days, 3 months and 12 months were higher
among patients with low hemoglobin (Table 3). Survival was
better in patients with nonanemic patients (log rank test: 75487,
P < 0001; Fig. 2b).
Anemia either as a dichotomous variable or as continuous
variable was found to be a significant predictor of mortality
throughout the follow-up period on univariate cox-regression
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H. Milionis et al.

Table 1 Demographic and clinical characteristics for patients with first-ever ischemic stroke according to anemia status (as defined by WHO criteria)

Characteristic
Gender
Women
Age (years)
Smoking
Actively smoking (or stopped <2 years)
Insurance
Private/semiprivate
Mode of hospital arrival
Direct
Type of onset
Wake known
Intervention type
No intervention
IV-standard thrombolysis according to guidelines
Endovascular intervention (including bridging) < 6 h
Time to treatment (min)
Comorbidities
Hypertension
Atrial fibrillation (persistent or intermittent)
Diabetes mellitus
Documented coronary artery disease
Peripheral artery disease
Heart failure
Hyperlipidemia
Medication prior to stroke onset
Anticoagulants
Antiplatelets
Antihypertensives
Oral antidiabetics
Lipid lowering drugs
Clinical characteristics
Body mass index (BMI, kg/m2)
Heartrate (beats/min)
Systolic blood pressure (mmHg)
Diastolic blood pressure (mmHg)
TOAST classification
Atherosclerosis
Cardioembolism
Small-vessel occlusion
Other determined etiology
Undetermined etiology
Metabolic parameters
Serum creatinine (mol/l)
eGFR (ml/min/173 m2)
Serum glucose (mmol/l)
Serum total cholesterol (mmol/l)
White blood cell count (103/l)
Platelet count (103/l)
Hematocrit (%)
Hemoglobin (g/dl)
C-reactive protein (mg/l)

Anemia
N = 427

No-anemia
N = 2012

189 (443)
7345 1477*

876 (435)
6882 2568

168 (413)

817 (416)

67 (161)

393 (198)

317 (760)

1588 (811)

303 (713)

1383 (690)

334 (784)
76 (178)
9 (21)
155 (76)

1527 (764)
380 (192)
51 (26)
160 (90)

300 (711)
140 (335)*
92 (223)
99 (237)*
34 (80)
34 (168)
246 (589)*

1349 (677)
501 (252)
333 (168)
280 (141)
104 (52)
147 (156)
1399 (703)

58 (138)
189 (449)
277 (663)*
51 (122)
111 (266)

194 (98)
721 (363)
1090 (552)
162 (82)
441 (223)

2475 467*
8098 1787
15066 2857*
8132 1759*

2581 476
8055 1844
15851 2778
8866 1772

52 (124)
166 (396)
47 (112)
32 (76)*
122 (291)

270 (137)
650 (331)
287 (146)
66 (34)
691 (352)

92 (51)*
6834 (3867)*
704 249
47 (15)*
857 397
24928 9548
3441 452*
1124 123*
7 (11)*

87 (29)
7667 (3254)
728 305
54 (17)
862 311
22793 6311
4256 369
1443 299
3 (8)

*P < 0001; P < 001; P < 005.

Continuous data are presented as mean SD, noncontinuous data are presented as numbers and percentages and nonparametric variables, including
Time to treatment, serum creatinine, eGFR, serum total cholesterol, C-reactive protein as median (interquartile range). eGFR, estimated glomerular
filtration rate according to the MDRD method.

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Table 2 Logistic regression analysis for factors associated with anemia in patients with acute ischemic stroke
Multivariate analysis
Model A

Age (10 years)

Body mass index (kg/m2)
Coronary artery disease
Hypertension
Diabetes mellitus
Dyslipidemia
Diastolic blood pressure on admission (10 mmHg)
Serum glucose (mmol/l)
C-reactive protein (mg/l)

Model B

Odds ratio

95% CI

119

102141

169
194
296*
060

100297
111337
155566
039091

Odds ratio

95% CI

093

088099

296

140626

082
083
103*

066090
071097
102104

Adjustment for all variables described in Table 1 concerning demographics, comorbid conditions and medications prior to admission (model A) and,
in addition, clinical and laboratory characteristics as recorded on admission (model B).
*P < 0001; P < 001; P < 005.

Table 3 Stroke severity and outcomes according to the admission hemoglobin status
Characteristic
NIHSS at admission
NIHSS 24 h after admission
NIHSS at 7 days
Hemorrhagic transformation 07 days according to ECASS-II
Length of hospital stay (days)
Orientation at discharge
Home/short recovery
Any institution/hospital (including palliative care)
Recurrent cerebrovascular events (within first 12 months):
None
1 ischemic event (stroke, TIA, retinal event)
1 intracranial hemorrhage(s)
Favorable outcome (mRS 02)
3 months
12 months
Mortality
7 days
3 months
12 months
Cause of death
Stroke-related
Nonstroke-related
Unknown

Anemia

No-anemia

Odds ratio (95% CI)

8 (13)
5 (12)
3 (13)
8 (21)
10 (8)

6 (11)
4 (9)
3 (8)
33 (18)
9 (8)

103* (102105)
103* (101104)
102* (101103)
119 (055260)
101(101102)

135 (379)
221 (621)

772 (417)
1078 (583)

100a
135*(108169)

288 (862)
42 (126)
4 (12)

1475 (893)
167 (101)
10 (06)

100a
129 (090185)
205 (064658)

181 (485)
160 (448)

1118 (640)
1083 (640)

053* (042066)
046* (036057)

65 (152)
103 (241)
133 (311)

134 (67)
216 (107)
289 (144)

251* (183345)
264* (203344)
270* (212343)

66 (537)
52 (423)
5 (40)

169 (612)
85 (308)
22 (80)

100a
157 (100245)
058 (021160)

*P < 0001; P < 001; P < 005.

a
Reference group.
Non-normally distributed variables, including NIHSS and length of stay are presented as median (interquartile range), and noncontinuous data as
numbers (percentages). ECASS, European Cooperative Acute Stroke Study.

analysis (Table 4). Decreasing levels of hemoglobin remained a

significant predictor of short- and long-term mortality in the
multivariate analysis. Other significant independent predictors
were increasing age, documented CAD, CRP levels on admission,
the severity of stroke reflected on NIHSS score. (Table 4).

Discussion
In this study of a large number of consecutive acute ischemic
strokes, patients with anemia had higher 7-day, 3-month and

Vol , 2014,

12-month death rates and disability compared with nonanemic

patients.
The prevalence of anemia in acute stroke patients has been
reported to range between 17% and 29% (19,20). Accordingly,
anemia defined according to an admission hemoglobin status was
present in 27% of our study population. There is long-standing
evidence that a high hematocrit may increase the risk of cerebral
infarction (21). The few studies investigating a low hematocrit or
hemoglobin value as a risk factor for ischemic stroke have produced conflicting findings and anemia is not considered a definite
2014 World Stroke Organization

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H. Milionis et al.

Fig. 2 KaplanMeier estimates of recurrent stroke risk and survival of patients with anemia and without anemia.

risk factor for stoke (22,23). It has been suggested that low hematocrit levels lead to low blood oxygen content, which may subsequently cause cerebral ischemia (24). Anemia might also induce a
hyperkinetic circulatory state and upregulate the endothelial
adhesion molecule genes, which could lead to thrombus generation (25). Furthermore, blood flow augmentation and turbulence
may result in the migration of an already existing thrombus
leading to artery-to-artery embolism (25).
As yet, there is a paucity of studies that clarify the relationship
between anemia and stroke recurrence. In line with Huang et al.,
we found that the rate of stroke recurrence was similar in anemia
2014 World Stroke Organization

and anemia-free groups, which may indicate that anemia does not
influence stroke recurrence (20).
Few studies have looked into the relationship between the
hemoglobin or hematocrit level and stroke outcome. Indeed,
some (4,8,12,13,2628) but not all (28,29) studies indicated low
hemoglobin as a predictor of poor outcome after ischemic stroke.
Moreover decreasing hemoglobin and hematocrit levels as well as
their nadir during the first 5 days after admission have been
associated with either three-month poor outcome or mortality
(30). Also hemoglobin levels that decrease after admission independently predict infarct growth in thrombolyzed stroke patients
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Table 4 Cox regression analyses determining the effect of hemoglobin status and various factors on mortality in patients with acute ischemic stroke
Univariate analysis

Mortality at 7 days
Anemia
Age (10 years)
Coronary arterydisease
Serum glucose (mmol/l)
C-reactive protein (10 mg/l)
NIHSS on admission
Hemoglobin (g/dl)
Mortality at 3 months
Anemia
Age (10 years)
Coronary artery disease
C-reactive protein (10 mg/l)
NIHSS on admission
Hemoglobin (g/dl)
Mortality at 12 months
Anemia
Age (10 years)
Coronary artery disease
C-reactive protein (mg/l)
NIHSS on admission
Hemoglobin (g/dl)

Multivariate analysis

Hazard ratio

95% CI

Hazard ratio

95% CI

236*

175317

079*

073085

145
142*
172
112
106
115*
089

087189
122168
111267
104121
102110
112117
080099

242*

192306

077*

073081

149
152*
167
108*
114*
088

089166
134174
117238
105117
112113
082097

241*

196296

078*

074082

135
155*
183*
108*
112*
089

101183
137174
134249
105111
110114
083097

*P < 0001; P < 001; P < 005.

Multivariate analysis included demographics, preexisting conditions, medications prior to stroke, clinical and laboratory features on admission. NIHSS,
National Institutes of Health Stroke Scale.

(31). It has been reported that midrange hematocrit levels were

associated with a better outcome after discharge (32). Our study
shows that hemoglobin levels at admission constitute an independent predictor of short- and long-term mortality. A J-shaped
relationship between hematocrit level and adverse outcomes in
patients with severe stroke has also been described (13). Nevertheless, in our cohort, survival in patients with hemoglobin values
>16, 17 or 18 g/dl was similar to nonanemic patients (data not
shown).
The results of our study must be interpreted in view of several
limitations. This is a retrospective observational single-center
study of prospectively collected, consecutive, acute ischemic
stroke patients. Despite a potential selection bias in the analysis,
ASTRAL is a solid hospital-based registry with well-characterized
variables, meticulous monitoring and prospective follow-up for
12 months for disability, mortality and recurrences. Additional
strengths of our study include analysis of hemoglobin status both
as a dichotomous and continuous variable, while the large database permitted additional multivariate modeling. However,
unmeasured confounding variables or complex interactions
between covariates on the observed associations cannot be ruled
out. Furthermore, we cannot comment on the etiology of anemia
(acute blood loss anemia, anemia due to chronic disease, etc),
and/or on the relationship between etiology of anemia and poststroke outcomes. Moreover, subsequent measurements of hemoglobin are not systematically performed and therefore not used
for analysis. Finally, we cannot comment on the role of direct
interventions for anemic patients with stroke (e.g. blood transfu-

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sions). Although patients with moderate to severe anemia had a

higher mortality rate, anemia was rarely in the range to require
blood transfusion.
Despite the study limitation our data suggest that patients
with moderate anemia on admission should be monitored
closely. Our observational, retrospective study of prospectively
collected data cannot answer the question whether anemia itself
causes poor outcome after stroke or whether anemia is just a
surrogate marker for general poor health of the patient; this can
only be addressed by well-designed, prospective studies. We
cannot generate a hypothesis about specific interventions like
blood transfusion or synthetic erythropoietin administration,
since we could not identify a cutoff value toward the category of
severe anemia and the benefits of these measures have not been
proven in stroke patients, while potential harm should be
avoided. For example, in the context of nonstroke diabetic
patients, anemia was found to be a risk factor for cardiovascular
events and death, but the use of darbepoetin alfa in patients with
diabetes, chronic kidney disease, and moderate anemia (hemoglobin < 110 g/dl) was associated with an increased risk of fatal
or nonfatal stroke (hazard ratio, 192; 95% CI, 138268) (33).
What seems to be a reasonable recommendation for stroke
patients with anemia is to avoid excess blood sampling. First
things first, anemia has to be recognized in stroke patients upon
admission and a diagnostic work-up toward reversible causes
should be implemented.
In conclusion, anemia is common among patients with acute
ischemic stroke and is associated with cardiovascular comorbidi 2014 World Stroke Organization

H. Milionis et al.
ties. Low hemoglobin status, especially in the range of moderate/
severe anemia predicts short- and long-term mortality.

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