Article

Relationship Between Red Cell DistributionWidth and Stroke in Patients With StableChronic Heart Failure: A Propensity ScoreMatching Analysis

AhmAQ1 et Kaya1, Turgay Isik2, Yasemin Kaya3, Ozgur Enginyurt4,

Zeki Yuksel Gunaydin1, Murat Dogan Iscanli5, Mustafa Kurt2, and

Ibrahim Halil Tanboga2

Abstract

Aim:We aimed to investigate the association between baseline red cell distribution width (RDW) level and the risk of stroke in

patients with heart failure (HF). Methods: A total of 153 consecutive patients with HF (New York Heart Association [NYHA]

I-III and left ventricular ejection fraction of <40%) were included in this prospective study. All the patients were followed up for 1

year, and during this period the cerebrovascular disease was questioned. Results: In matched population, using propensity score

matching comparing patients with HF having stroke with patients without stroke, we found significantly increased basal RDW andserum uric acid. The receiver–operating characteristic curves of RDW for predicting stroke are shown in Figure 2.AQ2 An RDW

�15.2% measured on admission had 87% sensitivity and 74% specificity in predicting stroke in patients with HF (area under the

curve: 0.923, 95% confidence interval: 0.852-0.994, P < .001).Conclusion: In conclusion, this study demonstrated that RDWmay

be important hematological indices for stroke in patients with HF using propensity score analysis.

Keywords

stroke, heart failure, red cell distribution width

Introduction

Heart failure (HF) is a complex clinical syndrome caused by

structural or functional changes in the ventricles, which affect

the ventricular filling and/or ejection.1 The HF is associated

with an increased risk of stroke even if in sinus rhythm,2 and

the identification of new eligible indices of stroke could pro-

vide new knowledge about the pathogenesis and prevent this

complication in patients with HF.

Red cell distribution width (RDW) indicates the presence of

erythrocytes with different sizes (anisocytosis).3 The RDW

increases in many cases such as ineffective erythropoiesis

caused by hemolysis and iron deficiency anemia. Also, preg-

nancy and some hematological disorders (such as thrombotic

thrombocytopenic purpura [TTP]) and inflammatory bowel

disease (IBD) may cause increase in RDW.4-6 Previously,

RDW is an indicator that is used for the differential diagnosis

of the anemia, later, it was shown that it has a prognostic value

in acute and chronic cardiac events in healthy population,.7-9

Although it was shown that increased basal RDW level is an

index of hospitalization and mortality of patient with HF, the

relationship between RDW and risk of stroke has not been

investigated comprehensively.10,11 Therefore, in this particular

study, we aimed to investigate the association between the

baseline RDW level and the risk of stroke in patients with HF.

Methods

Patient Selection

A total of 153 consecutive patients with HF (New York Heart

Association [NYHA] I-III and left ventricular ejection fraction

1Department of Cardiology, Ordu University Medical School, Ordu, Turkey2Department of Cardiology, Erzurum Education and Research Hospital,

Erzurum, Turkey3Department of Internal Medicine, Ordu University Medical School, Ordu,

Turkey4Department of Family Medicine, Ordu University Medical School, Ordu,

Turkey5Department of Emergency Medicine, Ministry of Health-Ordu University

Education and Research Hospital, Ordu, Turkey

Corresponding Author:

Ahmet Kaya, Department of Cardiology, Ordu University Medical School,

Ordu 52000, Turkey.

Email: doktorahmetkaya@yahoo.com

Clinical and Applied

Thrombosis/Hemostasis

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ª The Author(s) 2013

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[LVEF] of <40%) who were admitted to outpatients clinics of

our hospital were included in this prospective study between

June and September 2011. Patients with anemia (n: 10), history

of stroke (n: 3), end-stage renal disease (ESRD; n: 3), inflam-

matory disease (n: 2), menorrhagia (n: 1), and malignancy

(n: 1) were excluded. Finally, 133 nonanemic patients with sta-

ble chronic HF were included in the study. All patients were

followed up for 1 year and during this period it was questioned

prospectively whether they have cerebrovascular disease. The

local ethics committee approved this study.

Patients’ laboratory and clinical characteristics, such as age,

sex, diabetes mellitus (DM), hypertension (HTN), hypercholes-

terolemia, smoking, family history of cardiovascular disease,

height, and weight, were questioned. By dividing weight in

kilograms by height in meters squared (kg/m2), the body mass

index (BMI) was calculated. The rhythm status was determined

in all the patients on admission using electrocardiogram. The

reason for HF (ischemic or nonischemic) and drug use was

questioned in all the patients. Hemoglobin (Hb), RDW, white

blood cell count, and other hematological indices were mea-

sured as part of the automated complete blood count using a

Coulter LH 780 Hematology Analyzer (Beckman Coulter

Ireland Inc, Mervue, Galway, Ireland). The glomerular filtra-

tion rate (GFR) was estimated by the simplified Modification

of Diet in Renal Disease Equation.

Transthoracic echocardiography was performed on patients

before they were discharged using a system V (Vingmed, GE)

with a 2.5 MHz phased-array transducer.AQ3 Recordings were taken

on patients positioned in the left lateral decubitus position. The

LVEF was measured using the modified Simpson rule.12

Definitions

Anemia on admissionwas defined as a baseline Hb concentration

less than 13 mg/dL in men and less than 12 mg/dL in women, in

accordance with the World Health Organization criteria.13 The

diagnosis of DM was based on the previous history of diabetes

with or without drug therapies. Hypercholesterolemia was

defined as total cholesterol of�200 mg/dL. Obesity was defined

as a BMI of �30 kg/m2. Current smokers were defined as those

who had smoked for some period during the past year. Patients

were considered as having ESRD, if they were dependent on

chronic dialysis. Renal insufficiency was defined as a GFR of

<60 mL/min/1.732 m2.14

Statistics

Continuous variables are expressed as mean+ standard devia-

tion. Categorical variables are expressed as percentages. To

compare parametric continuous variables, the Student t test was

used; the Mann-Whitney U was used to compare nonpara-

metric continuous variables. To compare categorical variables,

the chi-square test was used. The receiver–operating character-

istics (ROC) curve was used to demonstrate the sensitivity and

specificity of RDW and its respective optimal cutoff value for

predicting stroke in patients with NYHA I to III HF.

As the study was nonrandomized, a propensity score was

created with variables frequently used by the clinician when

deciding the prediction of stroke for each patient (age, sex, dia-

betes, HTN, triglyceride [TG], high-density lipoprotein [HDL],

low-density lipoprotein [LDL], LVEF, systolic pulmonary

artery pressure (sPAP), glucose, and creatinine) to balance

patient characteristics and to generate propensity-matched

analysis for the 2 groups. The propensity score was developed

using SPSS, version 20.0 for Windows and the R statistical

package, version 2.12.1. Two-tailed P values <.05 were consid-

ered to indicate statistical significance.

Results

The RDW values of 133 patients enrolled in the study (mean

age 65.9+10.9, %71.4 male) ranged from 11% to 24%

(median 14.8%, mean 15.4%+ 2.2%). The baseline character-

istics of the patients with and without stroke are summarized in

Table 1. Patients with HF with and without stroke were compa-

rable for age, sex, HF etiology, atrial fibrillation, LVEF, sPAP,

Table 1. The Baseline Characteristics of the Patients With and With-out Stroke Before Propensity Matching.

VariablesStroke

(ÿ; n ¼ 119)Stroke

(þ; n ¼ 14) P Value

Age, years 66 + 10 65 + 8 .786Sex, male 75.3 64 .433Etiology, ischemic, % 67 78 .445Diabetes mellitus, % 34.3 50 .383Hypertension, % 81.5 78 .668Hyperlipidemia, % 34.9 64 .133Smoking,% 55.8 62 .719Atrial fibrillation, % 34 50 .396Hemoglobin, g/dL 14.7 + 1.6 14.7 + 1.8 .966RDW 14.6 + 1.4 16.9 + 1.14 <.001Glucose, mg/dL 122 + 53 157 + 69 .092Creatinine, mg/dL 1.0 + 0.32 1.3 + 1.0 .033HDL-cholesterol, mg/dL 41 + 10 36 + 9 .321hs-CRP, mg/dL 1.1 + 0.9 2.1 + 1.0 .004Serum uric acid, mg/dL 6.7 + 1.3 8.8 + 1.7 .010LDL-cholesterol, mg/dL 115 + 33 155 + 37 .012Triglyceride, mg/dL 134 + 75 168 + 43 .342Sodium, mmol/L 139 + 38 139 + 3.1 .804Potassium, mmol/L 4.5 + 0.56 3.9 + 0.5 .008LVEF, % 29 + 6.5 30 + 6 .747Systolic PAP, mm Hg 43 + 15 35 + 7 .457Medications, %

ACE-i 72.7 64 .553ARB 16.4 14 .782b-Blocker 76 78 .404Diuretic 83.6 87 .796Aspirin 80 75 .746Digoksin 18 36 .211Warfarine 12 14 .887

Abbreviations: RDW, red cell distribution width; HDL, high-density lipopro-tein; LDL, low-density lipoprotein; LVEF, left ventricular ejection fraction; PAP,pulmonary artery pressure; ACE-i, angiotensin converting enzyme inhibitors;ARB, angiotensin receptor blocker; hs-CRP, high-sensitive C-reactive protein.

2 Clinical and Applied Thrombosis/Hemostasis 00(0)

cardiovascular risk factors, and medication. When patients with

HF having stroke were compared with patients without stroke,

we found significantly increased basal RDW creatinine, LDL,

and decreased potassium levels in unmatched analysis. A propen-

sity score was created with variables frequently used by the clin-

icianwhen deciding the prediction of stroke for each patient (age,

sex, diabetes, HTN, TG, HDL, LDL, LVEF, sPAP, glucose, and

creatinine) to balance patient characteristics and to generate

propensity-matched analysis for the 2 groups (Figure 1). In

matched population, when comparing patients with HF having

strokewith patients without stroke, we found significantly

increased basal RDW (16.9+ 1.14 vs 14.8+ 1.6, P < .001) and

serum uric acid (8.8+ 1.7 vs 7.5+ 1.1, P ¼ .027).

The ROC curves of RDW for predicting stroke is shown in

Figure 2. A RDW �15.2% measured on admission had 87%

sensitivity and 74% specificity in predicting stroke in patients

with HF (area under the curve: 0.923, 95% confidence interval:

0.852-0.994, P < .001). In addition, the analyses made in the

whole study population showed that there is a significant

correlation between RDW, high-sensitive C-reactive protein

(r: .312, P: .006), and uric acid levels (r: .299, P: .010; Figure 3).

Throughout the study, all strokes (n ¼ 14) were analyzed.

Transient ischemic attack (2 cardioembolic and 1 significant car-

otid artery disease), cardioembolic stroke, significant carotid

Figure 1. A propensity score histogram before and after matching.

Figure 2. Receiver–operating characteristic curve analysis for red celldistribution width (RDW) value in prediction of stroke.

Kaya et al 3

artery disease, and thromboembolic events of vertebra-basillary

arterial system were detected in 3, 5, 3, and 2 patients, respec-

tively. However, we could not find the exact etiology in 1

patient.

Discussion

In this study, for the first time in the literature, we evaluated the

relationship between baseline RDW levels and the risk of

stroke in patients with HF. The study results revealed that

elevated basal levels of RDW in stable patients with HF are

significantly associated with stroke, according to the propen-

sity score analysis. The risk of stroke increased in the patients

with HF regardless of atrial fibrillation.2 Hospitalization in

patients with chronic HF, stroke, and mortality risk is closely

associated with increased oxidative stress, and these are shown

in the previous studies.15 Increased vascular oxidative stress

and vascular endothelial dysfunction trigger the atherosclero-

sis responsible for the stroke.16,17

The clinical usage of RDW is rare outside of differential

diagnosis of anemia. Studies showed that RDW is predictive

for HF development in healthy population and in patient that

had MI, and it is also predictive for mortality in patients with

HF.10,11 The following studies showed that increased RDW

levels are related to poor prognosis in acute myocardial infarc-

tion8 and stable angina pectoris.7 The relationship between

RDW and stroke is controversial. Malandrino et al reported that

higher RDW values are related to increased risk of stroke in

diabetes.18 Tonelli et al demonstrated that increased RDW

levels were related to increased risk of stroke in patients with

coronary artery disease whowere free of HF.7Ani and Ovbiagele

showed that elevated RDWwas a predictor of cardiovascular and

all-causemortality in patientswithhistory of stroke.Additionally,

they reported RDWwas higher in patients with stroke compared

to patients without stroke.19 In contrast, Ntaios et al revealed that

RDW does not predict severity or functional outcome in patients

with acute ischemic stroke. Additionally, they found that RDW

was related to low ejection fraction.20 Indeed, increased RAAS

activation system was shown to be caused by increased erythro-

poiesis.21 Height of RDW is thought to be closely related to the

mortality in patients with HF and stroke, but there is no enough

information about predictive value for stroke in patients with

HF.With this study,we showed that increasedRDWlevels in sta-

ble patients with HF can be indices of stroke in 1-year follow-up.

Several mechanisms may be suggested for increased stroke

risk in patients with HF with elevated RDW levels. But the

most probable mechanism is oxidative stress. There is a rela-

tionship between uric acid levels and stroke risk as an indicator

of increased oxidative stress.22 AQ4Increased oxidative stress, by

causing injury to the vessel wall (which is responsible for many

strokes triggering atherosclerosis), is thought to have the

tendency to develop stroke.16,17 In our study, we found that uric

acid was an independent predictor of stroke. There is a close

relationship between elevated levels of RDW and reduced

oxidative stress in the previous studies.23 Similarly, we found

that RDWwas significantly correlated with uric acid level. The

possible mechanism is increased RDW levels after increased

oxidative stress.24,25 Red blood cells have a strong antioxidant

capacity so that they are exposed to oxidative stress and dam-

age commonly. Therefore, it is more possible to be damaged by

oxidative stress and immature blood cell participation to the

circulation. More studies are needed to fully understand the

pathophysiological mechanistic relationship between RDW

and stroke. However, we thought that the oxidative stress,

which is closely related to stroke development risk, affects the

erythropoiesis, by increasing the level of RDW.

Figure 3. Relation of red cell distribution width (RDW) with uric acid and high-sensitive C-reactive protein (hs-CRP) in a scatter figures.

4 Clinical and Applied Thrombosis/Hemostasis 00(0)

In conclusion, this study demonstrated that RDW may be an

important hematological index for stroke in patients with HF.

The use of anticoagulant therapy in patients with HF regardless

of rhythm remains controversial.2,26 This large-scale prospec-

tive, randomized studies in patients with HF and with a high

RDW show the need for closer follow-up and/or preventive

treatment against the risk of stroke development (such as the

anticoagulants).

Limitations

First,being a single-center study and containing a relatively low

number of patients may be a limitation. Second, we did not make

distinction between hemorrhagic and ischemic stroke. Third, the

RDW may increase in many clinical situations such as hemoly-

sis, transfusion, and iron, vitamin B12, and folate deficiency,

which cause ineffective erythropoiesis. In addition, clinical

situations such as pregnancy, TTP, and IBD can result in

increased RDW levels. In this study, only the Hb level was

checked, and those of iron, vitamin B12, and folic acid were not.

However, none of the patients in the study had the diagnosis of

IBD or TTP, and also they were not pregnant or in malnutrition.

Only stable patients were taken into the study, and they were

followed up in terms of stroke prospectively. In our study, non-

analysis of oxidative stress indicators is seen to be a limitation,

but in the previous studies those markers have been shown to be

correlated with RDW.

Acknowledgment

The authors thank Dr Tanboga for performing Propensity score match-

ing analysis.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to

the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, author-

ship, and/or publication of this article AQ5.

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VariablesStroke

(ÿ; n ¼ 14)Stroke

(þ; n ¼ 14) P Value

Age, years 63.1 + 5.1 65 + 8 .393Sex, male 64 64 1.000Etiology, ischemic, % 64 78 .411Diabetes mellitus, % 57 50 .705Hypertension, % 78 78 1.000Hyperlipidemia, % 43 64 .256Smoking,% 35 62 .131Atrial fibrillation, % 28 50 .246Hemoglobin, g/dL 14.3 + 1.2 14.7 + 1.8 .431RDW 14.8 + 1.6 16.9 + 1.14 <.001Glucose, mg/dL 145 + 85 157 + 69 .682Creatinine, mg/dL 1.25 + 0.4 1.3 + 1.0 .672HDL-cholesterol, mg/dL 40 + 6 36 + 9 .218hs-CRP, mg/dL 2.1 + 1.1 2.1 + 1.0 .892Serum uric acid, mg/dL 7.5 + 1.1 8.8 + 1.7 .027LDL-cholesterol, mg/dL 146 + 48 155 + 37 .583Triglyceride, mg/dL 163 + 111 168 + 43 .877Sodium, mmol/L 139 + 4.9 139 + 3.1 .964Potassium, mmol/L 4.1 + 0.4 3.9 + 0.5 .365LVEF, % 32 + 7.8 30 + 6 .670Systolic PAP, mm Hg 36 + 12 35 + 7 .925Medications, %ACE-i 85 64 .190ARB 14 14 1.000b-Blocker 85 78 .622Diuretic 78 85 .622Aspirin 85 75 .622Digoksin 7 36 .065Warfarine 14 14 1.000

Abbreviations: RDW, red cell distribution width; HDL, high-density lipopro-tein; LDL, low-density lipoprotein; LVEF, left ventricular ejection fraction; PAP,pulmonary artery pressure; ACE-i, angiotensin converting enzyme inhibitors;ARB, angiotensin receptor blocker; hs-CRP, high-sensitive C-reactive protein.

Kaya et al 5

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SCIENCE CITATION INDEX EXPANDED JOURNAL LIST

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1. CLINICAL AND APPLIED THROMBOSIS-HEMOSTASISBimonthly ISSN: 1076-0296

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1. Science Citation Index Expanded2. Current Contents - Clinical Medicine

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