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ARTIGO ORIGINAL
http://www.dx.doi.org/10.5935/2359-4802.20160007

Prevalence of anemia in patients with heart failure

Prevalência de anemia em pacientes com insuficiência cardíaca

Worens Luiz Pereira Cavalini1; Nico Ceulemans1; Ramon Bedenko Correa1; Patrick Willian
Padoani1; Edson Felipe Grudinski Delfrate1; Eliane Mara Cesário Pereira Maluf2

1. Universidade Positivo - Curso de graduação em Medicina - Curitiba, PR - Brazil

2. Universidade Positivo - Faculdade de Medicina - Curitiba, PR - Brazil

Corresponding author

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Eliane Mara Cesário Pereira Maluf

Rua Pedro Viriato Parrigot de Souza, 5300 - Campo Comprido

81280-330 - Curitiba, PR - Brazil

E-mail: eliane.cesario@yahoo.com.br (mailto:eliane.cesario@yahoo.com.br)

Received in 9/27/2015

Accepted em 3/1/2016

Reviewed in 3/5/2016

ABSTRACT

BACKGROUND: The prevalence of anemia and the morphology of red blood cells in patients
hospitalized with heart failure (HF) are not totally known.

OBJECTIVE: To check the prevalence of anemia in patients diagnosed with HF, characterize
the morphology and check its association with NYHA functional class.

METHODS: Cross-sectional retrospective study with 144 patients from the Brazilian Public
Health System hospitalized for HF at Hospital da Cruz Vermelha, Curitiba, PR, January 2010
to July 2014. Sociodemographic data and admission blood count information were taken
from the patients' medical records. The blood count analysis included: hemoglobin levels,
mean corpuscular volume (MCV), mean corpuscular hemoglobin concentration (MCHC) and
anisocytosis index (RDW). The reference values to characterize anemia followed the World
Health Organization's guidelines.

RESULTS: Population studied with similar distribution of sex (52.8% men), mean age
67.8±13.8 years and nearly all of them (95.8%) self-reported white ethnicity. Anemia
prevalence in this population was 41.0%, the majority (38.2%) corresponding to mild to
moderate degrees. Functional class III (FC III) was the most prevalent one (63.2%),
followed by FC IV (31.3%). The main morphological characteristic found was normocytic and
hypochromic with 49.1%. Correlation of anemia with increasing age (>60 years) was found
with p=0.008.

CONCLUSIONS: Prevalence of anemia in patients with HF was higher in older age groups,
in FC III and IV, and the main morphological characteristic was normocytic and
hypochromic.

Keywords: Anemia; Heart failure; Epidemiology; Comorbidity

INTRODUCTION

Abbreviations and Cardiovascular diseases are the leading cause of death

Acronyms worldwide. Of these, heart failure (HF) is the final pathway
for most cardiac diseases.
• CDC - Centers for
Disease Control and Decompensated heart failure (DHF) is a syndrome caused
Prevention by structural or functional changes in the body, causing
difficulties in ejecting or accommodating blood, maintaining
• DHF - decompensated the physiological blood pressure levels1. The main factors
heart failure that cause decompensation are infections, renal failure,
• DM - diabetes mellitus systemic arterial hypertension (SAH), abandonment of
treatment and nutritional deficiencies, particularly anemia.
• FC - functional class
Anemia in patients with heart failure could be easily
• HB - hemoglobin considered anemia of chronic, normocytic and
• HF - heart failure normochromic disease, with low reticulocyte count2,3.
However, the pathophysiology of anemia in HF is not well

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• MCHC - mean explained. Several hypotheses are postulated, even

corpuscular hemoglobin suggesting different etiologies, especially iron deficiency.
concentration The main hypotheses are: nutritional - iron deficiency,
vitamin B12 and folate4,5; blood loss from the use of AAS5;
• MCV - mean corpuscular
comorbidities - hypertension, diabetes and chronic renal
volume
failure5; urinary loss of transferrin or erythropoietin (EPO)5;
• NYHA - New York Heart use of angiotensin-converting enzyme inhibitors (ACEI)5,6;
Association increased activity of cytokines5; hemodilution1,4,5.

• RDW - anisocytosis index It should be considered that anemia worsens the prognosis
in patients with HF due to reduced oxygen supply,
• SAH - systemic arterial
ventricular remodeling, neurohormonal profile and
hypertension
proinflammatory state, combined with several
• WHO - World Health comorbidities, including renal failure and cardiac cachexia.
Organization Therefore, anemia is both a mediator and a poor prognosis
marker in HF7.

Anemia is a common comorbidity in chronic heart failure and is associated with increased
cardiovascular outcome, reduced ability to exercise due to reduced ability to carry and store
oxygen, impaired quality of life and increased risk of hospitalization8,9. Patients affected by
HF usually have other associated comorbidities that expose them to a range of organ
dysfunctions which, interrelated, worsen the clinical picture and make treatment more
difficult. The presence of anemia would be a poor prognostic factor, regardless of ventricular
dysfunction10. Moreover, it is related to intolerance to physical activity, advanced clinical
stage and acceleration of heart failure1,4. Therefore, identifying the morphology of red blood
cells is critical to optimize appropriate treatment for patients with this condition11.

The prevalence of anemia in patients with heart failure varies depending on the type and its
severity9,12. Until then, there is no consensus on the most common morphological type of
red blood cells and it is not possible to compare anemia and functional class of the New York
Heart Association (NYHA)13. The NYHA classification is a dynamic assessment related to the
clinical state of the patient at the time of medical assessment; worse FC have a worse
degree of anemia5.

The purpose of this study was to determine the prevalence of anemia in hospitalized
patients with HF in a university hospital in Curitiba, PR, Brazil, to characterize its
morphology and check its association with the NYHA functional class.

METHODS

Cross-sectional study with collection of retrospective data from medical records of patients
admitted with a diagnosis of heart failure in a university hospital in Curitiba, PR, from
January 2010 to July 2014.

This study has been approved by the Research Ethics Committee of Universidade Positivo
under no. 742 883 (CAAE: 31510114.9.0000.0093), in accordance with the Declaration of
Helsinki. The Research Ethics Committee did not require Informed Consent Form.

The population sample was defined as all patients hospitalized for HF in the cardiology
service of Hospital Cruz Vermelha, Curitiba, PR. The selection of patients followed the
flowchart shown in Figure 1.

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Subsequently, demographic data were collected from electronic medical records: age, sex,
education and ethnicity and clinical information: length of hospital stay, death, need for
blood transfusion and/or iron supplementation.

Admission blood count was assessed and verified: hemoglobin count (HB), mean corpuscular
volume (MCV), anisocytosis index (RDW) and mean corpuscular hemoglobin concentration
(MCHC).

In this study, anemia was defined according to the reference values of the World Health
Organization (WHO): for men, hemoglobin <13.0 g/dL and for women, <12.0 g/dL. It is
further classified according to its severity:

• in men: mild (10.0 - 12.9 g/dL), moderate (8.0 - 10.9 g/dL) and severe (<8.0 g/dL)

• in women: mild (11.0 - 11.9 g/dL), moderate (8.0 - 10.9 g/dL) and severe (<8.0
g/dL)

All patients included in the study met the hospitalization criteria for decompensation of HF;
they were all older than 18. Patients with acute coronary syndrome, renal failure, end-stage
liver failure previously been diagnosed and registered in the medical records; and patients
with active bacterial infection14 diagnosed through antibiotics or alterations in blood count
(leukocytosis >12,000 or <4,000 or rod cells >10%) were excluded from the study. Patients
with comorbidities such as systemic arterial hypertension (SAH) and diabetes mellitus (DM)
were not excluded.
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Quantitative variables were expressed as mean and standard deviation and the categorical
variables were expressed as absolute and percentage frequencies. To investigate the
association between anemia and other variables (sex, FC, ICU, death and age group), the
chi-square test was used, considering a 0.05 significance level.

RESULTS

144 medical records of patients with HF were included. The average age found was
67.8±13.8 years. The median was 67, ranging from 26-97 years (Table 1).

The prevalence of anemia in this population was 40.97% (n=59), occurring in varying
degrees of intensity (Table 2).

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There was predominance of functional classes III and IV (Table 3). The anemia prevalence
distribution according to CF is shown in Table 4.

 
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The morphological pattern of anemia, the need for hospitalization at the Intensive Care Unit
(ICU) and the outcome of death in 59 patients with anemia are shown in Table 5.

There were 2 deaths in the non-anemic group. Of the 5 deaths among anemic patients, 3
(60.0%) were in the NYHA FC IV and all patients presented HF as the underlying cause or
mentioned in any line of the death certificate. In 3 anemic patients, it was necessary to
perform blood transfusion and 2 were prescribed iron supplementation.

Several analyzes were performed to identify possible associations between variables. The
frequency of the elderly (>60 years) was 84.7% among patients with HF and anemia. The
frequency of the elderly in the population with HF without anemia was 60.0% with statistical
significance (Table 6).

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DISCUSSION

The prevalence of anemia in hospitalized patients with HF found in this study was 40.97%.
In the literature, there is a huge variation15. Such heterogeneity is due to the lack of
consensus on the definition of anemia16-18 and the different exclusion criteria9 applied in the
studies.

Silverberg et. al.19 in a retrospective study held in Tel Aviv, Israel, found a prevalence of
55.0% of anemia among 142 patients. Sales et al.10 in a multicenter retrospective study
conducted in São Paulo, Brazil in 2001 with 204 patients found a prevalence of 62.6%. This
study also found that the prevalence of anemia was higher with increasing age (p=0.008),
which may be explained by the high prevalence of chronic diseases such as SAH and DM,
favoring the onset of anemia. Another important cause that should be highlighted are the
nutritional deficiencies caused by inadequate nutrition with iron deficiency.

The difficulty presented to determine the presence of anemia meets the criteria used for this
purpose. The two main criteria are: those of the World Health Organization (WHO) and those
of the Center for Disease Control and Prevention - CDC20. The WHO criteria (men
hemoglobin <13.0 g/dL and women hemoglobin <12.0 g/dL) was chosen in this study to be
the most used in the literature. The CDC defines anemia for men: hemoglobin <13.5 g/dL
and women: hemoglobin <12 g/dL20. As a direct consequence, there is inclusion of more
patients when the CDC criteria are used. This divergence of the diagnostic criteria can be an
explanation for the wide variation in the prevalence of anemia found in the literature.

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The exclusion criteria applied in different studies also interfere directly in the prevalence of
anemia. The idea of excluding, in this study, acute coronary syndrome, renal failure, end-
stage liver failure and active bacterial infection aims to produce a scenario that is closer to
the actual relationship between HF and anemia21. This helps limiting the causes of anemia of
chronic disease.

From a pathophysiological point of view, anemia of chronic disease is mediated by

inflammatory cytokines22. Therefore, the expected morphological characteristic for anemia
in patients with HF would be anemia of chronic (normocytic/normochromic) disease. This
morphological characteristic was the second most frequent form, with 30.5%, surpassed by
normocytic/hypochromic characteristic - 49.1%. This, in turn, may be differential diagnosis
of anemia of chronic disease or iron deficiency anemia; in this case, it is essential to
determine the serum ferritin. Note that this protein, responsible for iron reserve, was not
determined in any of the hospitalized patients. Rangel et al.21 point out the presence of a
greater number of cases of mortality outcomes and nonfatal cardiovascular events in
patients with iron deficiency and anemia (p=0.006), confirming the importance of knowing
the red blood cell morphology.

The Israeli19 study showed 79.1% patients in FC IV and 52.6% in FC III. It is noticed that
this upward distribution according to functional class would be expected and found in other
studies11,19, which was not found in this study, where 31.3% were in FC IV and 63.2% in FC
III. This may be due, among other causes, to a different population profile in the service
concerned or to the subjectivity of the NYHA classification, which depends on the views and
interpretation of the physician to determine it.

On the other hand, the high prevalence of FC III patients raises important questions. The
first is in relation to hospitalization of patients with milder symptoms in FC III. Thinking of a
public health system, this implies expenses with hospitalizations in patients that could be
managed on an outpatient basis or patients seeking tertiary care as a gateway. A second
reasonable question would be the existence of a parallel between FC and severity of the
disease.

Most cases of anemia (38.2%) were classified as mild or moderate degree of intensity, which
is similar to the 30% of mild to moderate anemia found in other studies16,23. Though these
patients are classified as mild or moderate degree, the possibility of treatment should
always be a clinical issue.

Treatment of anemia is related to improvement in the patient's hemodynamic status.

Studies indicate that a correction of 10 g/dL to 12 g/dL (correction of mild/moderate
severity) is associated with the optimization of cardiac function, with improvement in left
ventricular ejection fraction18-20. Besides this, patients present improvement in NYHA
functional class, drop in the number of hospitalizations, reduced doses of oral and
intravenous diuretic (furosemide) and considerable improvement in the symptoms of
fatigue5. Silverberg et al.4 also suggest that the treatment of anemia is an alternative to
avoid the cardio-renal-anemia syndrome (CRA)4. This association between renal failure,
anemia and HF generates a vicious cycle and self-feedable14. It is worth noting that there is
no consensus in the literature regarding the management of cardiac patients who develop
anemia, but major studies point out the relevance of this issue24.

The importance of treatment of anemia is related to the mortality of patients. In this study,
there was no significant association of anemia with deaths (p=0.093). A study conducted in
São Paulo indicated lethality of 16.8% of anemic patients vs. 8% non-anemic patients, but
that was not significant (p=0.11)10.

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Larger studies consider the higher mortality rate for patients developing anemia to be
significant. Ezekowitz et al.24, in a cohort study with 12,065 Canadian patients, showed
higher survival of non-anemic patients on anemic patients (p<0.0001). Horwich et al.11, in a
cohort study conducted in the United States with 1 733 patients, found an increase of 16%
risk of death for every 1 g/dL of hemoglobin decrease. In the multivariate analysis, the risk
of death was 13% for each decrease of 1 g/dL hemoglobin (RR=1.131 and IC95=1.045-
1.224). In 2006, Consuegra Sánchez et al.14, in Spain, also pointed anemia as an outcome
with an independent association for mortality (RR=1.15, 95% CI=1.04-1.25, p=0.003).
Similar results can be seen in the systematic review by Groenveld et al.25. Mortality
parameters are also associated with sex, with a predominance of the male sex10,11. In this
study, sex showed no statistical difference (p=0.528).

The study limitations are due mainly to the fact that the data collection was retrospective,
which only allowed the analysis of information from medical records. Besides, using data
from a single service may not have represented the sample population in the region.

Larger multicenter studies are of great importance to define more accurately the prevalence
of anemia found in patients hospitalized with HF. Furthermore, randomized clinical trials
defining the actual validity of pharmacological intervention in this group turns out to be a
focal point for new therapies to prevent the progression of the condition and negative
outcome for the patient.

CONCLUSIONS

The prevalence of anemia in patients with HF was higher in older age groups, in FC III and
IV, and the main morphological characteristic was normocytic and hypochromic.

Potential Conflicts of Interest

This study has no relevant conflicts of interest.

Sources of Funding

This study had no external funding sources.

Academic Association

This study is not associated with any graduate programs.

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