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  <front>
    <journal-meta>
      <journal-id journal-id-type="publisher-id">abc</journal-id>
      <journal-title-group>
        <journal-title>Arquivos Brasileiros de Cardiologia</journal-title>
        <abbrev-journal-title abbrev-type="publisher">Arq. Bras. Cardiol.</abbrev-journal-title>
      </journal-title-group>
      <issn pub-type="ppub">0066-782X</issn>
      <issn pub-type="epub">1678-4170</issn>
      <publisher>
        <publisher-name>Sociedade Brasileira de Cardiologia - SBC</publisher-name>
        <publisher-loc>S&#227;o Paulo, SP, Brazil</publisher-loc>
      </publisher>
    </journal-meta>
    <article-meta>
      <article-id pub-id-type="publisher-id" specific-use="scielo-v3">RZxDKVGDRBwXTktDctFVSRy</article-id>
      <article-id pub-id-type="other">00013</article-id>
      <article-id pub-id-type="publisher-id" specific-use="scielo-v2">S0066-782X2010000600013</article-id>
      <article-id pub-id-type="publisher-id" specific-use="scielo-v1">S0066-782X(10)09400613</article-id>
      <article-id pub-id-type="doi">10.1590/S0066-782X2010005000048</article-id>
      <article-categories>
        <subj-group subj-group-type="heading">
          <subject>Artigos Originais</subject>
        </subj-group>
      </article-categories>
      <title-group>
        <article-title>Anemia, disfun&#231;&#227;o renal e desnutri&#231;&#227;o associadas &#224; insufici&#234;ncia card&#237;aca em pacientes valvopatas</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="author">
          <name>
            <surname>Souza</surname>
            <given-names>Wysllenny Nascimento de</given-names>
          </name>
          <xref ref-type="aff" rid="aff01"/>
          <xref ref-type="aff" rid="aff02"/>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Ara&#250;jo</surname>
            <given-names>Cristiane Maria S&#225; de</given-names>
          </name>
          <xref ref-type="aff" rid="aff01"/>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Silva</surname>
            <given-names>Silvia Alves da</given-names>
          </name>
          <xref ref-type="aff" rid="aff03"/>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Petrib&#250;</surname>
            <given-names>Marina de Moraes Vasconcelos</given-names>
          </name>
          <xref ref-type="aff" rid="aff02"/>
        </contrib>
      </contrib-group>
      <aff id="aff02">
        <addr-line>
          <named-content content-type="city">Recife</named-content>
          <named-content content-type="state"/>
        </addr-line>
        <institution content-type="orgname">Faculdade Maur&#237;cio de Nassau</institution>
        <country country="BR">Brazil</country>
      </aff>
      <aff id="aff03">
        <addr-line>
          <named-content content-type="city">Recife</named-content>
          <named-content content-type="state"/>
        </addr-line>
        <institution content-type="orgname">Funda&#231;&#227;o Osvaldo Cruz</institution>
        <country country="BR">Brazil</country>
      </aff>
      <aff id="aff01">
        <addr-line>
          <named-content content-type="city">Recife</named-content>
          <named-content content-type="state">Pernambuco</named-content>
        </addr-line>
        <institution content-type="orgname">Pronto Socorro Cardiol&#243;gico de Pernambuco</institution>
        <country country="BR">Brazil</country>
      </aff>
      <pub-date date-type="collection" publication-format="electronic">
        <month>06</month>
        <year>2010</year>
      </pub-date>
      <volume>94</volume>
      <issue>6</issue>
      <fpage>794</fpage>
      <lpage>798</lpage>
      <history>
        <date date-type="received">
          <day>26</day>
          <month>03</month>
          <year>2009</year>
        </date>
        <date date-type="rev-recd">
          <day>19</day>
          <month>11</month>
          <year>2009</year>
        </date>
        <date date-type="accepted">
          <day>25</day>
          <month>11</month>
          <year>2009</year>
        </date>
      </history>
      <permissions>
        <license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/" xml:lang="en">
          <license-p>This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.</license-p>
        </license>
      </permissions>
      <abstract>
        <p>FUNDAMENTO: A doen&#231;a valvar pode cursar com insufici&#234;ncia card&#237;aca (IC), anemia e disfun&#231;&#227;o renal (DR), aumentando o risco nutricional e piorando o progn&#243;stico dos pacientes. OBJETIVO: Avaliar a preval&#234;ncia de anemia e DR em pacientes portadores de valvopatias com ou sem IC, bem como estabelecer correla&#231;&#227;o com o estado nutricional. M&#201;TODOS: Foram avaliados 104 pacientes internados na enfermaria de valvopatias do PROCAPE/UPE, no per&#237;odo de ago-out/2008. Os dados foram obtidos das fichas de acompanhamento nutricional e dos prontu&#225;rios. As vari&#225;veis coletadas foram: sexo, idade, estado nutricional segundo o &#237;ndice de massa corp&#243;rea (IMC), presen&#231;a de IC, anemia, DR. Considerou-se como anemia valores de hemoglobina &lt; 13 g/dl nos homens e &lt; 12 g/dl nas mulheres. A DR foi estabelecida de acordo com a taxa de filtra&#231;&#227;o glomerular (TGF), sendo calculada pela f&#243;rmula proposta por Cockcroft e Gault. RESULTADOS: A preval&#234;ncia de anemia e DR em pacientes com IC foi de 71,1% e de 68,8%, e nos pacientes sem IC foi de 48,1% e de 60,0%, respectivamente, com diferen&#231;a estatisticamente significativa para anemia (p = 0,022). Dos pacientes, 48,1% estavam eutr&#243;ficos, 26,9% com excesso de peso e 25,0% com algum grau de desnutri&#231;&#227;o. Os pacientes com IC apresentaram uma frequ&#234;ncia maior de baixo peso (p = 0,020). O estado nutricional n&#227;o apresentou associa&#231;&#227;o com anemia (p = 0,117), mas apresentou associa&#231;&#227;o com DR, sendo a fun&#231;&#227;o renal diminu&#237;da mais frequente nos pacientes com baixo peso (p = 0,000). CONCLUS&#195;O: Houve signific&#226;ncia estat&#237;stica quando comparamos as preval&#234;ncias de desnutri&#231;&#227;o, anemia e DR entre pacientes com e sem IC.</p>
      </abstract>
      <kwd-group xml:lang="pt" kwd-group-type="author-generated">
        <kwd>Insufici&#234;ncia card&#237;aca</kwd>
        <kwd>anemia</kwd>
        <kwd>desnutri&#231;&#227;o</kwd>
        <kwd>doen&#231;a das valvas card&#237;acas</kwd>
      </kwd-group>
      <pub-date publication-format="electronic" date-type="pub">
        <day>07</day>
        <month>05</month>
        <year>2010</year>
      </pub-date>
    </article-meta>
  </front>
  <body>
    <p>
      <bold>ARTIGO ORIGINAL</bold>
    </p>
    <p> INSUFICI&#202;NCIA CARD&#205;ACA</p>
    <p>
      <bold>Anemia, disfun&#231;&#227;o renal e desnutri&#231;&#227;o associadas &#224; insufici&#234;ncia card&#237;aca em pacientes valvopatas</bold>
    </p>
    <p>
      <bold>Wysllenny Nascimento de Souza<sup>I, II</sup>; Cristiane Maria S&#225; de Ara&#250;jo<sup>I</sup>; Silvia Alves da Silva<sup>III</sup>; Marina de Moraes Vasconcelos Petrib&#250;<sup>II</sup></bold>
    </p>
    <p><sup>I</sup>Pronto Socorro Cardiol&#243;gico de Pernambuco, Recife, PE - Brasil </p>
    <p><sup>II</sup>Ensino Superior Bureau Jur&#237;dico (Faculdade Mauricio de Nassau), Recife, PE - Brasil </p>
    <p><sup>III</sup>Hospital Universit&#225;rio Osvaldo Cruz (HUOC), Recife, PE - Brasil</p>
    <p>
      <xref ref-type="corresp" rid="back">Correspond&#234;ncia</xref>
    </p>
    <p>
      <bold>RESUMO</bold>
    </p>
    <p><bold>FUNDAMENTO:</bold> A doen&#231;a valvar pode cursar com insufici&#234;ncia card&#237;aca (IC), anemia e disfun&#231;&#227;o renal (DR), aumentando o risco nutricional e piorando o progn&#243;stico dos pacientes. </p>
    <p><bold>OBJETIVO:</bold> Avaliar a preval&#234;ncia de anemia e DR em pacientes portadores de valvopatias com ou sem IC, bem como estabelecer correla&#231;&#227;o com o estado nutricional. </p>
    <p><bold>M&#201;TODOS:</bold> Foram avaliados 104 pacientes internados na enfermaria de valvopatias do PROCAPE/UPE, no per&#237;odo de ago-out/2008. Os dados foram obtidos das fichas de acompanhamento nutricional e dos prontu&#225;rios. As vari&#225;veis coletadas foram: sexo, idade, estado nutricional segundo o &#237;ndice de massa corp&#243;rea (IMC), presen&#231;a de IC, anemia, DR. Considerou-se como anemia valores de hemoglobina &lt; 13 g/dl nos homens e &lt; 12 g/dl nas mulheres. A DR foi estabelecida de acordo com a taxa de filtra&#231;&#227;o glomerular (TGF), sendo calculada pela f&#243;rmula proposta por Cockcroft e Gault. </p>
    <p><bold>RESULTADOS:</bold> A preval&#234;ncia de anemia e DR em pacientes com IC foi de 71,1% e de 68,8%, e nos pacientes sem IC foi de 48,1% e de 60,0%, respectivamente, com diferen&#231;a estatisticamente significativa para anemia (p = 0,022). Dos pacientes, 48,1% estavam eutr&#243;ficos, 26,9% com excesso de peso e 25,0% com algum grau de desnutri&#231;&#227;o. Os pacientes com IC apresentaram uma frequ&#234;ncia maior de baixo peso (p = 0,020). O estado nutricional n&#227;o apresentou associa&#231;&#227;o com anemia (p = 0,117), mas apresentou associa&#231;&#227;o com DR, sendo a fun&#231;&#227;o renal diminu&#237;da mais frequente nos pacientes com baixo peso (p = 0,000). </p>
    <p><bold>CONCLUS&#195;O:</bold> Houve signific&#226;ncia estat&#237;stica quando comparamos as preval&#234;ncias de desnutri&#231;&#227;o, anemia e DR entre pacientes com e sem IC. </p>
    <p><bold>Palavras-chave: </bold> Insufici&#234;ncia card&#237;aca, anemia, desnutri&#231;&#227;o, doen&#231;a das valvas card&#237;acas.</p>
    <p>
      <bold>Introdu&#231;&#227;o</bold>
    </p>
    <p>A doen&#231;a valvar &#233; uma doen&#231;a em evolu&#231;&#227;o nos &#250;ltimos anos, como resultado de diversos fatores, incluindo o aumento ineg&#225;vel das valvopatias de origem degenerativa pelo envelhecimento da popula&#231;&#227;o<sup>1</sup>.</p>
    <p>A preval&#234;ncia da doen&#231;a card&#237;aca valvar, embora seja menor do que outras doen&#231;as cardiovasculares, como insufici&#234;ncia card&#237;aca ou cardiopatia isqu&#234;mica, persiste como uma das principais fontes de assist&#234;ncia m&#233;dica e consumo de recursos. Apesar da preval&#234;ncia de valvopatia no Brasil ser elevada, dados sobre sua real preval&#234;ncia e perfil cl&#237;nico ainda s&#227;o muito escassos<sup>1,2</sup>.</p>
    <p>A insufici&#234;ncia card&#237;aca (IC), comum em pacientes valvopatas, &#233; uma s&#237;ndrome cl&#237;nica resultante da deteriora&#231;&#227;o da fun&#231;&#227;o card&#237;aca, a qual gera uma s&#233;rie de altera&#231;&#245;es hemodin&#226;micas e neuro-humorais, manifestando-se por dispneia, fadiga, redu&#231;&#227;o da capacidade funcional, reten&#231;&#227;o de l&#237;quidos, com consequente congest&#227;o pulmonar e edema perif&#233;rico<sup>3</sup>.</p>
    <p>Pacientes com IC, principalmente ap&#243;s uma interna&#231;&#227;o hospitalar, apresentam progn&#243;stico ruim<sup>4</sup>. Recentemente, demonstrou-se que esses pacientes, com frequ&#234;ncia, manisfestam anemia, tendo preval&#234;ncia aumentada com a gravidade da doen&#231;a, apresentando rela&#231;&#227;o com a mortalidade<sup>5-7</sup>.</p>
    <p>A disfun&#231;&#227;o renal (DR) tamb&#233;m &#233; comum nesses indiv&#237;duos, podendo interferir na intensidade dos sintomas, mudar o curso cl&#237;nico e alterar a resposta ao tratamento, influenciando no progn&#243;stico<sup>8</sup>.</p>
    <p>A desnutri&#231;&#227;o resulta em expressiva perda muscular esquel&#233;tica, sendo comum em valvopatas com IC, contribuindo para o aumento da preval&#234;ncia de comorbidades, mortalidade e tempo de interna&#231;&#227;o no p&#243;s-operat&#243;rio<sup>9</sup>.</p>
    <p>Portanto, a desnutri&#231;&#227;o, junto &#224; DR e &#224; anemia podem ser fatores de risco associados ao progn&#243;stico de IC e, tamb&#233;m, podem estar relacionadas entre si. A anemia promove a ativa&#231;&#227;o do sistema nervoso simp&#225;tico que, frente ao aumento da pr&#233;-carga, acentua o remodelamento card&#237;aco com posterior dilata&#231;&#227;o ventricular. Como o rim &#233; um &#243;rg&#227;o que est&#225; em rela&#231;&#227;o direta com o funcionamento cardiovascular, a ativa&#231;&#227;o neuro-humoral e inflamat&#243;ria, presente na IC, contribui para a progressiva perda da fun&#231;&#227;o renal. Forma-se, ent&#227;o, um ciclo conhecido como s&#237;ndrome anemia-cardiorrenal (SACR)<sup>10</sup>.</p>
    <p>Considerando-se a import&#226;ncia da SACR e que a desnutri&#231;&#227;o &#233; frequente em pacientes com IC, torna-se fundamental a avalia&#231;&#227;o nutricional para se diagnosticar e corrigir o quadro nutricional e diminuir a sobrecarga renal, reduzindo assim os custos hospitalares e a mortalidade.</p>
    <p>O objetivo deste estudo foi avaliar a preval&#234;ncia de anemia e DR em pacientes portadores de valvopatias, com ou sem IC, e investigar a associa&#231;&#227;o dessas vari&#225;veis com o estado nutricional.</p>
    <p>
      <bold>M&#233;todos</bold>
    </p>
    <p>Um estudo do tipo s&#233;rie de casos, de delineamento transversal, foi realizado com portadores de valvopatias internados no Pronto-Socorro Cardiol&#243;gico de Pernambuco (PROCAPE/UPE), durante o per&#237;odo de agosto a outubro de 2008. Os dados foram coletados em prontu&#225;rios e fichas de acompanhamento nutricional de 104 pacientes de ambos os sexos, com ou sem interven&#231;&#227;o cir&#250;rgica.</p>
    <p>Foram considerados crit&#233;rios de exclus&#227;o a presen&#231;a de patologias que pudessem exercer influ&#234;ncia negativa no trofismo muscular localizado ou geral e de patologias hipercatab&#243;licas, como AIDS, neoplasias, doen&#231;as disarbsortivas e doen&#231;as cr&#244;nicas degenerativas.</p>
    <p>As vari&#225;veis coletadas foram: sexo, idade, peso, altura, presen&#231;a de IC, hemoglobina e hemat&#243;crito.</p>
    <p>Os pacientes foram pesados, na posi&#231;&#227;o ereta, usando roupas leves e descal&#231;os, em balan&#231;a digital tipo plataforma da marca <italic>Filizola</italic><sup>&#174;</sup>, com capacidade m&#225;xima de 300 quilos e varia&#231;&#227;o de 100 gramas. A altura foi verificada com r&#233;gua antropom&#233;trica met&#225;lica de dois metros, com fra&#231;&#245;es de um cent&#237;metro, acoplada &#224; plataforma da balan&#231;a digital. Os pacientes foram mantidos em posi&#231;&#227;o ereta, descal&#231;os, no centro da plataforma, p&#233;s unidos, membros superiores pendentes ao longo do corpo e em apneia respirat&#243;ria.</p>
    <p>Valores de hemoglobina menores do que 13 g/dl nos homens e 12 g/dl nas mulheres foram considerados anemia, de acordo com a Organiza&#231;&#227;o Mundial da Sa&#250;de (OMS)<sup>11</sup>.</p>
    <p>A presen&#231;a de DR foi avaliada atrav&#233;s da taxa de filtra&#231;&#227;o glomerular (TGF) calculada por meio da f&#243;rmula proposta por Cockcroft e Gault<sup>12</sup>, sendo a fun&#231;&#227;o renal reclassificada em duas categorias: <underline>&gt;</underline> 60 ml/min/1,73 m<sup>2</sup>, normal; e &lt; 60 ml/min/1,73 m<sup>2</sup>, diminu&#237;da. O est&#225;gio de vida foi classificado em adultos e idosos segundo crit&#233;rios da OMS (1997) e as dosagens bioqu&#237;micas coletadas nos prontu&#225;rios foram classificadas segundo Waitzberg<sup>13</sup>. O diagn&#243;stico de IC foi obtido dos prontu&#225;rios dos pacientes.</p>
    <p>O diagn&#243;stico nutricional foi realizado atrav&#233;s do &#237;ndice de massa corp&#243;rea (IMC), utilizando-se os crit&#233;rios da OMS para adultos<sup>14</sup> e Lipschitz<sup>15</sup> para idosos.</p>
    <p>A constru&#231;&#227;o do banco de dados e a an&#225;lise estat&#237;stica foram realizadas no programa <italic>Statistical Package for Social Sciences</italic> (SPSS), vers&#227;o 13.0 (SPSS Inc., Chicago, IL, USA)<sup>16</sup>. As vari&#225;veis categ&#243;ricas foram apresentadas em propor&#231;&#245;es, onde a distribui&#231;&#227;o binomial foi aproximada &#224; distribui&#231;&#227;o normal pelo intervalo de confian&#231;a de 95,0%. A associa&#231;&#227;o entre as vari&#225;veis analisadas foi avaliada pelo teste de correla&#231;&#227;o de Pearson. O n&#237;vel de signific&#226;ncia estat&#237;stica adotado para todos os testes foi de 5,0%.</p>
    <p>O estudo foi pautado pelas normas &#233;ticas para pesquisa envolvendo seres humanos constantes da resolu&#231;&#227;o 196 do Conselho Nacional de Sa&#250;de e foi submetido e aprovado pelo Comit&#234; de &#201;tica em Pesquisa da Faculdade Maur&#237;cio de Nassau (parecer 004/2008). Os pacientes que concordaram em participar receberam todas as informa&#231;&#245;es sobre o estudo e assinaram o Termo de Consentimento Livre e Esclarecido.</p>
    <p>
      <bold>Resultados</bold>
    </p>
    <p>A casu&#237;stica foi constitu&#237;da por 104 pacientes, com distribui&#231;&#227;o similar entre os sexos e idade m&#233;dia de 49,4 &#177; 16,2 anos, sendo que, com rela&#231;&#227;o ao est&#225;gio de vida, houve maior preval&#234;ncia de pacientes com menos de 60 anos.</p>
    <p>A presen&#231;a de IC, anemia e fun&#231;&#227;o renal diminu&#237;da foram diagnosticadas em 47,1%, 58,8% e 64,1% dos pacientes, respectivamente (<xref ref-type="table" rid="t1">Tabela 1</xref>). A avalia&#231;&#227;o do estado nutricional revelou que 48,1% estavam eutr&#243;ficos, 26,9% dos pacientes apresentavam excesso de peso (sobrepeso e/ou obesidade) e 25,0% apresentavam algum grau de desnutri&#231;&#227;o.</p>
    <table-wrap id="t1">
      <graphic xlink:href="1678-4170-abc-94-06-0794-00048-gt01.jpg"/></table-wrap>
    <p>O diagn&#243;stico de IC n&#227;o foi associado a preju&#237;zo na fun&#231;&#227;o renal dos pacientes estudados, visto que a distribui&#231;&#227;o de pacientes com fun&#231;&#227;o renal normal e diminu&#237;da foi similar entre os pacientes com e sem IC. No entanto, observou-se que os pacientes com IC apresentaram uma frequ&#234;ncia maior de anemia, em compara&#231;&#227;o aos pacientes sem IC (p = 0,022). Da mesma forma, os pacientes com IC apresentaram uma frequ&#234;ncia maior de baixo peso, em compara&#231;&#227;o aos pacientes sem IC, os quais apresentaram maior frequ&#234;ncia de eutrofia e excesso de peso (p = 0,020) (<xref ref-type="table" rid="t2">Tabela 2</xref>).</p>
    <table-wrap id="t2">
      <graphic xlink:href="1678-4170-abc-94-06-0794-00048-gt02.jpg"/></table-wrap>
    <p>A presen&#231;a de anemia n&#227;o obteve diferen&#231;a estat&#237;stica em rela&#231;&#227;o aos pacientes com baixo peso, eutrofia ou excesso de peso. Por outro lado, a fun&#231;&#227;o renal apresentou diferen&#231;a altamente significativa em rela&#231;&#227;o ao estado nutricional dos pacientes avaliados, sendo a fun&#231;&#227;o renal diminu&#237;da mais frequente nos pacientes com baixo peso e a fun&#231;&#227;o renal normal mais frequente nos pacientes com excesso de peso (<xref ref-type="table" rid="t3">Tabela 3</xref>).</p>
    <table-wrap id="t3">
      <graphic xlink:href="1678-4170-abc-94-06-0794-00048-gt03.jpg"/></table-wrap>
    <p>
      <bold>Discuss&#227;o</bold>
    </p>
    <p>A anemia &#233; comum em pacientes com IC e sua etiologia &#233; multifatorial, estando associada &#224; alta mortalidade<sup>7,17</sup>. Sua preval&#234;ncia oscila entre 5,0% e 55,0%, dependendo dos crit&#233;rios utilizados e da popula&#231;&#227;o estudada<sup>18</sup>.</p>
    <p>Na presente pesquisa, a preval&#234;ncia de anemia em pacientes com IC foi similar aos achados de Silverbeg e cols.<sup>19</sup>, onde 55,0% de pacientes com IC apresentavam hemoglobina inferior a 12 g/dl. No estudo desenvolvido por Sales e cols.<sup>20</sup>, com pacientes com IC, tamb&#233;m foi encontrada uma alta incid&#234;ncia de anemia (63,0%), enquanto que Ezekowitz e cols.<sup>7</sup>, analisando pacientes n&#227;o selecionados com IC, encontraram apenas 17,0% de anemia. Ressalta-se que nesses estudos a insufici&#234;ncia card&#237;aca n&#227;o foi por valvopatias.</p>
    <p>A anemia em pacientes com IC pode ocorrer por diversos fatores, tais como: a redu&#231;&#227;o da absor&#231;&#227;o intestinal de ferro, ocasionada ou por ingest&#227;o insuficiente ou por edema nas al&#231;as intestinais, e a perda g&#225;strica cr&#244;nica de sangue em usu&#225;rios de &#225;cido acetilsalic&#237;lico.</p>
    <p>O aumento de citocinas, como o fator de necrose tumoral alfa, que produzem depress&#227;o da medula &#243;ssea &#233; outro fator que causa anemia em pacientes com IC. Pode-se citar ainda fatores como a ativa&#231;&#227;o do sistema renina-angiotensina-aldosterona (SRAA), que causa reten&#231;&#227;o de s&#243;dio e &#225;gua ocasionando uma anemia por hemodilui&#231;&#227;o, e a disfun&#231;&#227;o renal que afeta com frequ&#234;ncia os pacientes com IC, em parte por vasoconstri&#231;&#227;o e isquemia renal, levando a uma diminui&#231;&#227;o na produ&#231;&#227;o de eritropoetina e a pr&#243;pria perda da eritropoetina e transferrina por coexist&#234;ncia de protein&#250;ria. Al&#233;m do tratamento com inibidores da enzima conversora de angiotensina (ECA), que podem alterar a produ&#231;&#227;o de eritropoetina no rim, sobretudo em doses elevadas, o tratamento com anticoagulantes pode contribuir para a presen&#231;a de anemia, produzindo perdas hem&#225;ticas<sup>21</sup>.</p>
    <p>Por outro lado, a pr&#243;pria anemia contribui para a IC, j&#225; que ocorre um gasto card&#237;aco mais elevado para suprir o aporte necess&#225;rio de oxig&#234;nio aos tecidos, o que produz a estimula&#231;&#227;o do sistema nervoso simp&#225;tico com vasoconstri&#231;&#227;o e taquicardia. A vasoconstri&#231;&#227;o renal ativa o SRAA, com redu&#231;&#227;o do fluxo renal e reten&#231;&#227;o h&#237;drica, causando insufici&#234;ncia renal secund&#225;ria que agrava a anemia e causa, em longo prazo, hipertrofia e remodelamento ventricular, piorando a IC<sup>22</sup>. Esse ciclo de anemia e IC foi observado em nosso estudo, onde a preval&#234;ncia de anemia foi bastante alta em pacientes com IC, demonstrando assim a contribui&#231;&#227;o destas duas comorbidades para um pior progn&#243;stico.</p>
    <p>Anemia e DR s&#227;o comorbidades comuns reconhecidas atualmente como fatores de risco que modificam o curso da IC<sup>8</sup>.</p>
    <p>A DR &#233; um achado cada vez mais frequente em pacientes com IC e sua detec&#231;&#227;o precoce, com correto estadiamento e controle, representa um desafio cl&#237;nico. A maioria dos estudos cl&#237;nicos em IC exclui pacientes com DR; portanto, at&#233; mesmo o emprego de medicamentos usados no tratamento de IC apresenta potenciais riscos &#224; fun&#231;&#227;o renal. A DR desequilibra o sistema cardiorrenal, podendo instabilizar a IC em curto prazo<sup>23</sup>.</p>
    <p>Atualmente, a DR &#233; considerada um fator de risco independente para o progn&#243;stico em pacientes hospitalizados com IC descompensada<sup>10,24</sup>. V&#225;rios estudos avaliaram a presen&#231;a de anemia em pacientes com taxa de filtra&#231;&#227;o glomerular abaixo de 60 ml/min/1,73 m<sup>2</sup><sup>5</sup>, demonstrando grande impacto sobre a mortalidade na associa&#231;&#227;o de DR, IC e anemia, em pacientes hospitalizados<sup>26</sup>. Na nossa casu&#237;stica, apenas 1/3 dos pacientes apresentavam TGF maior do que 60 ml/min/1,73 m<sup>2</sup>.</p>
    <p>Na popula&#231;&#227;o estudada, n&#227;o foi encontrada correla&#231;&#227;o positiva entre a DR e a presen&#231;a de IC, o que pode ser atribu&#237;do a uma poss&#237;vel preval&#234;ncia maior de pacientes com IC n&#227;o grave, o que n&#227;o p&#244;de ser mensurado em nosso estudo, j&#225; que a gravidade da IC n&#227;o foi avaliada, nem classificada.</p>
    <p>A desnutri&#231;&#227;o, assim como a DR e a anemia, &#233; frequente em valvopatas, em especial em portadores de IC. Em nossa casu&#237;stica, a correla&#231;&#227;o entre a anemia e desnutri&#231;&#227;o n&#227;o foi encontrada. Por outro lado, o estudo de Horwich e cols.<sup>6</sup> apontou para a poss&#237;vel rela&#231;&#227;o entre anemia e desnutri&#231;&#227;o, considerando a rela&#231;&#227;o entre os n&#237;veis s&#233;ricos de albumina e IMC.</p>
    <p>Os dados cl&#237;nicos e experimentais dispon&#237;veis indicam uma rela&#231;&#227;o entre a IC e a desnutri&#231;&#227;o<sup>27</sup>. H&#225; d&#250;vidas sobre quais mecanismos levam &#224; desnutri&#231;&#227;o e qual a import&#226;ncia de cada mecanismo na manuten&#231;&#227;o e agravamento do quadro<sup>28</sup>. Krummel<sup>29</sup> ratifica o que foi achado em nosso trabalho, quando afirma que de 35,0% a 53,0% dos pacientes com IC apresentaram-se desnutridos. A preval&#234;ncia de desnutri&#231;&#227;o em nosso trabalho foi de 69,2% em pacientes com IC. Em um estudo retrospectivo realizado por Herreros e cols.<sup>30</sup>, foi observada a preval&#234;ncia de 28,0% de desnutri&#231;&#227;o em pacientes valvopatas, confirmando mais uma vez o nosso achado.</p>
    <p>Veloso e cols.<sup>27</sup> sugerem que a repercuss&#227;o do estado nutricional na insufici&#234;ncia card&#237;aca avan&#231;ada, embora resulte da disfun&#231;&#227;o contr&#225;til do ventr&#237;culo esquerdo como fator etiol&#243;gico comum, tenha como determinantes principais, em cada indiv&#237;duo, fatores outros que transcendem o simples comprometimento da bomba card&#237;aca. O comprometimento nutricional poderia ser mais bem compreendido no &#226;mbito da complexa adapta&#231;&#227;o perif&#233;rica e da resposta neuro-hormonal &#224; fal&#234;ncia mioc&#225;rdica<sup>27</sup>.</p>
    <p>A desnutri&#231;&#227;o nesses pacientes tamb&#233;m poderia ser explicada pela eleva&#231;&#227;o dos n&#237;veis de citocinas, como o fator de necrose tumoral-alfa e a interleucina-6. As citocinas est&#227;o bastante elevadas nas formas avan&#231;adas da doen&#231;a e estudos mostraram haver rela&#231;&#227;o entre a eleva&#231;&#227;o de seus n&#237;veis e a perda de peso<sup>31</sup>.</p>
    <p>
      <bold>Conclus&#227;o</bold>
    </p>
    <p>A preval&#234;ncia de anemia, DR e desnutri&#231;&#227;o foram elevadas na popula&#231;&#227;o em estudo, especialmente nos pacientes portadores de IC, o que pode contribuir para um pior progn&#243;stico, sendo necess&#225;rio o diagn&#243;stico e tratamento precoce de tais comorbidades.</p>
    <p>
      <bold>Potencial Conflito de Interesses</bold>
    </p>
    <p>Declaro n&#227;o haver conflito de interesses pertinentes.</p>
    <p>
      <bold>Fontes de Financiamento</bold>
    </p>
    <p>O presente estudo n&#227;o teve fontes de financiamento externas.</p>
    <p>
      <bold>Vincula&#231;&#227;o Acad&#234;mica</bold>
    </p>
    <p>Este artigo &#233; parte de tese de conclus&#227;o de curso de Wysllenny Nascimento de Souza pelo Ensino superior Bureau jur&#237;dico (Faculdade Mauricio de Nassau).</p>
    <p>16. Statistical Package for the Social Sciences for Windows Student version. Release 7.5. Marketing Department. Chicago, 1996</p>
    <p>
      <fn id="back" fn-type="corresp">
        <p>Correspond&#234;ncia:</p>
        <p> Wysllenny Nascimento de Souza </p>
        <p> Av. Prof. Lineu Prestes, 580 </p>
        <p> Departamento de Alimentos e Nutri&#231;&#227;o Experimental FCF-USP </p>
        <p> Bloco 14 - 05508-900 - S&#227;o Paulo, SP - Brasil </p>
        <p> E-mail: </p>
        <p>
          <email xlink:href="lenny.souzaa@gmail.com">lenny.souzaa@gmail.com</email>
        </p>
      </fn>
    </p>
    <p>Artigo recebido em 26/03/09; revisado recebido em 19/11/09; aceito em 25/11/09.</p>
  </body>
  <back>
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  <sub-article article-type="translation" id="TRen" xml:lang="en">
    <front-stub>
      <article-categories>
        <subj-group subj-group-type="heading">
          <subject>Original Articles</subject>
        </subj-group>
      </article-categories>
      <title-group>
        <article-title xml:lang="en">Anemia, renal dysfunction and malnutrition associated with heart failure in patients with valvulopathy</article-title>
      </title-group>
      <abstract xml:lang="en">
        <p>BACKGROUND: Valvular disease can course with heart failure (HF), anemia and renal dysfunction (RD), increasing the nutritional risk and worsening patient prognosis. OBJECTIVE: To evaluate the prevalence of anemia and RD in patients with valvulopathy with or without HF, as well as establish a correlation with the nutritional status. METHODS: A total of 104 patients admitted at the Clinic of Valvulopathy of PROCAPE/UPE, during the period of Aug-Oct/2008. The data were obtained from the nutritional and medical follow-up files. The collected variables were: sex, age, nutritional status according to the body mass index (BMI), presence of HF, anemia and RD. Anemia was considered when hemoglobin values were &lt; 13 g/dl in men and &lt; 12 g/dl in women. RD was established according to the glomerular filtration rate (GFR) and it was calculated through the formula proposed by Cockcroft and Gault. RESULTS: The prevalence of anemia and RD was 71.1% and 68.8%, and 48.1% and 60.0%, in patients with and without HF, respectively, with a statistically significant difference for anemia (p = 0.022). Of the patients, 48.1% were eutrophic, 26.9% had excess weight and 25.0% presented some degree of malnutrition. The patients with HF presented a higher frequency of low weight (p = 0.020). The nutritional status was not associated with anemia (p = 0.117), but it was associated with RD, with renal function being decreased more often in patients with low weight (p = 0.000). CONCLUSION: When the prevalence of malnutrition, anemia and RD was compared between patients with and without HF, it showed statistical significance.</p>
      </abstract>
      <kwd-group xml:lang="en">
        <kwd>Heart failure</kwd>
        <kwd>anemia</kwd>
        <kwd>malnutrition</kwd>
        <kwd>heart valve diseases</kwd>
      </kwd-group>
    </front-stub>
    <body>
      <p>
        <bold>ORIGINAL ARTICLE</bold>
      </p>
      <p>
        <fn id="top-body2">
          <label>
            <bold>Anemia, renal dysfunction and malnutrition associated with heart failure in patients with valvulopathy</bold>
          </label>
          <p>
            <bold>Wysllenny Nascimento de Souza<sup>I, II</sup>; Cristiane Maria S&#225; de Ara&#250;jo<sup>I</sup>; Silvia Alves da Silva<sup>III</sup>; Marina de Moraes Vasconcelos Petrib&#250;<sup>II</sup></bold>
          </p>
        </fn>
      </p>
      <p><sup>I</sup>Pronto Socorro Cardiol&#243;gico de Pernambuco, Recife, PE - Brazil</p>
      <p><sup>II</sup>Ensino Superior Bureau Jur&#237;dico (Faculdade Mauricio de Nassau), Recife, PE - Brazil</p>
      <p><sup>III</sup>Hospital Universit&#225;rio Osvaldo Cruz (HUOC), Recife, PE - Brazil</p>
      <p>Mailing address</p>
      <p>
        <bold>ABSTRACT</bold>
      </p>
      <p><bold>BACKGROUND: </bold> Valvular disease can course with heart failure (HF), anemia and renal dysfunction (RD), increasing the nutritional risk and worsening patient prognosis.</p>
      <p><bold>OBJECTIVE:</bold> To evaluate the prevalence of anemia and RD in patients with valvulopathy with or without HF, as well as establish a correlation with the nutritional status.</p>
      <p><bold>METHODS:</bold> A total of 104 patients admitted at the Clinic of Valvulopathy of PROCAPE/UPE, during the period of Aug-Oct/2008. The data were obtained from the nutritional and medical follow-up files. The collected variables were: sex, age, nutritional status according to the body mass index (BMI), presence of HF, anemia and RD. Anemia was considered when hemoglobin values were &lt; 13 g/dl in men and &lt; 12 g/dl in women. RD was established according to the glomerular filtration rate (GFR) and it was calculated through the formula proposed by Cockcroft and Gault.</p>
      <p><bold>RESULTS:</bold> The prevalence of anemia and RD was 71.1% and 68.8%, and 48.1% and 60.0%, in patients with and without HF, respectively, with a statistically significant difference for anemia (p = 0.022). Of the patients, 48.1% were eutrophic, 26.9% had excess weight and 25.0% presented some degree of malnutrition. The patients with HF presented a higher frequency of low weight (p = 0.020). The nutritional status was not associated with anemia (p = 0.117), but it was associated with RD, with renal function being decreased more often in patients with low weight (p = 0.000).</p>
      <p><bold>CONCLUSION: </bold> When the prevalence of malnutrition, anemia and RD was compared between patients with and without HF, it showed statistical significance. </p>
      <p><bold>Key words:</bold> Heart failure; anemia; malnutrition; heart valve diseases.</p>
      <p>
        <bold>Introduction</bold>
      </p>
      <p>Valvular disease has increased in the last years, as a result of several factors, including the undeniable increase in age-related degenerative valvulopathies due to the increase in life expectancy<sup>1</sup>.</p>
      <p>The prevalence of valvular heart disease, although lower than other cardiovascular diseases such as heart failure or ischemic cardiopathy, persists as one of the main sources of medical assistance and use of healthcare resources. Although the prevalence of valvulopathy is high in Brazil, data on its actual prevalence and clinical profile are still scarce<sup>1,2</sup>.</p>
      <p>Heart failure (HF), common in patients with valvular disease, is a clinical syndrome that results from the deterioration of the cardiac function, which generates a series of hemodynamic and neurohumoral alterations, manifesting as dyspnea, fatigue, reduced functional capacity, fluid retention, with consequent pulmonary congestion and peripheral edema<sup>3</sup>. Patients with HF, mainly after a hospital admission, present a poor prognosis<sup>4</sup>. Recently, it was demonstrated that these patients often present anemia, with increased prevalence with the disease severity and an association with mortality<sup>5-7</sup>.</p>
      <p>The renal dysfunction (RD) is also common in these individuals and can interfere in symptom intensity, change the clinical course and alter the response to treatment, influencing the prognosis<sup>8</sup>.</p>
      <p>Malnutrition results in significant loss of skeletal muscle mass, and it is common in patients with valvulopathies and HF, contributing to the increased prevalence of comorbidities, mortality and postoperative hospital stay duration<sup>9</sup>.</p>
      <p>Therefore, malnutrition, together with RD and anemia, can be risk factors associated with the HF prognosis, and can also be related among them. Anemia promotes the activation of the sympathetic nervous system, which, in the presence of an increase in preload, increases cardiac remodeling, with posterior ventricular dilatation. As the kidney is an organ that is directly related with the cardiovascular function, the neurohumoral and inflammatory activation, present in HF, contributes to the progressive loss of renal function. A cycle, known as the cardio-renal-anemia syndrome (CRAS) is thus created<sup>10</sup>.</p>
      <p>Considering the importance of CRAS and the fact that malnutrition is frequent in patients with HF, it becomes crucial to carry out a nutritional assessment to diagnose and correct the nutritional status and decrease the renal overload, thus decreasing hospital costs and mortality.</p>
      <p>The objective of the present study was to evaluate the prevalence of anemia and RD in patients with valvulopathies, with and without HF, and investigate the association of these variables with the nutritional status.</p>
      <p>
        <bold>Methods</bold>
      </p>
      <p>The present cross-sectional case-series study was carried out in patients with valvulopathies admitted at the Cardiology Emergency Room of Pernambuco (PROCAPE/UPE), deform August to October 2008. The data were collected from medical and nutritional follow-up files of 104 patients of both sexes, with or without surgical intervention.</p>
      <p>The exclusion criteria were the presence of pathologies that could have a negative influence on localized or general muscle trophism or hypercatabolic pathologies, such as acquired immunodeficiency syndrome (AIDS), neoplasias, disabsorptive diseases and chronic degenerative diseases.</p>
      <p>The collected variables were: sex, age, weight, height, presence of HF, hemoglobin and hematocrit levels. The patients were weighed in the standing position, wearing light clothes and barefoot, on a <italic>Filizola<sup>TM</sup></italic> digital scale, with a maximum capacity of 300 kilograms and 100-gram increments. Height was verified sing a 2-meter metallic anthropometric measuring tape, with 1-cm increments, coupled to the digital scale platform. The patients remained standing, barefoot, on the center of the platform, with the feet side by side in parallel position and upper limbs hanging along the trunk, in respiratory apnea.</p>
      <p>Hemoglobin values &lt; 13 g/dl in men and 12 g/dl in women were considered anemia, according to the World health Organization (WHO)<sup>11</sup>.</p>
      <p>The presence of RD was assessed through the glomerular filtration rate (GFR), calculated through the formula proposed by tfgpor meio Cockcroft and Gault<sup>12</sup>, after which the renal function was reclassified in two categories: <underline>&gt;</underline> 60 ml/min/1.73 m&#178;, normal; and &lt; 60 ml/min/1.73 m&#178;, decreased. The stage of life was classified in adults and elderly according to the criteria of the WHO (1997) and the biochemical measurements collected from the files were classified according to Waitzberg<sup>13</sup>. The diagnosis of HF was obtained from the patients' files.</p>
      <p>The nutritional assessment was carried out through the body mass index (BMI), using the criteria of the WHO for adults<sup>14</sup> and of &#237;mcLipschitz<sup>15</sup> for the elderly.</p>
      <p>The creation of the database and the statistical analysis were carried out using the program Statistical Package for Social Sciences (SPSS), release 13.0 (SPSS Inc., Chicago, IL, USA)<sup>16</sup>. The categorical variables were presented in proportions, where the binomial distribution was close to the normal distribution through the 95% confidence interval.</p>
      <p>The association between the analyzed variables was evaluated through Pearson's correlation. The level of significance for all tests was set at 5.0%.</p>
      <p>The study followed the ethical rules for research involving human beings, as described in the Resolution #196 of the National Council of Health and was submitted to and approved by the Ethics Research Committee of Faculdade Mauricio de Nassau (resolution# 004/2008). The patients who agreed to participate in the study received all the information on the study and signed the Free and Informed Consent Form.</p>
      <p>
        <bold>Results</bold>
      </p>
      <p>The series consisted of 104 patients, with a similar distribution between the sexes and a mean age of 49.4 &#177; 16.2 years, with a higher prevalence of patients younger than 60 years.</p>
      <p>The presence of HF, anemia and decreased renal function were diagnosed in 47.1%, 58.8% and 64.1% of the patients, respectively (<xref ref-type="table" rid="t1-body2">Table 1</xref>). The assessment of the nutritional status showed that 48.1% of the patients were eutrophic, 26.9% had excess weight (overweight and/or obesity) and 25.0% presented some degree of malnutrition.</p>
      <table-wrap id="t1-body2">
        <graphic xlink:href="1678-4170-abc-94-06-0794-00048-gt01-en.jpg"/></table-wrap>
      <p>The diagnosis of HF was not associated with renal function impairment in the studied patients, considering that the distribution of patients with normal and decreased renal function was similar between patients with and without HF. However, it was observed that patients with HF presented a higher incidence of anemia, in comparison with patients without HF (p = 0.022). Similarly, patients with HF presented a higher frequency of low weight, in comparison with patients without HF, who presented a higher frequency of eutrophia and excess weight (p = 0.020) (<xref ref-type="table" rid="t2-body2">Table 2</xref>).</p>
      <table-wrap id="t2-body2">
        <graphic xlink:href="1678-4170-abc-94-06-0794-00048-gt02-en.jpg"/></table-wrap>
      <p>The presence of anemia showed no statistical difference regarding the patients with low weight, eutrophia or excess weight. On the other hand, the renal function showed a highly significant difference regarding the nutritional status of the assessed patients, with the decreased renal function being more frequent among patients with low weight and normal renal function more frequent in patients with excess weight (<xref ref-type="table" rid="t03e-body2">Table 3</xref>).</p>
      <p content-type="asset">
        <table-wrap id="t03e-body2">
          <graphic xlink:href="1678-4170-abc-94-06-0794-00048-gt03-en.jpg"/></table-wrap>
      </p>
      <p>
        <bold>Discussion</bold>
      </p>
      <p>Anemia is common in patients with HF and its etiology is multifactorial, being associated with high mortality<sup>7,17</sup>. Its prevalence ranges from 5.0% to 55%, depending on the criteria used and the studied population<sup>18</sup>.</p>
      <p>In the present study, the prevalence of anemia in patients with HF was similar to that demonstrated by the study of Silverbeg et al<sup>19</sup>, where 55.0% of the patients with HF presented hemoglobin levels &lt; 12 g/dl. The study developed by Sales et al<sup>20</sup> showed a high incidence of anemia (63.0%) in patients with HF, whereas Ezekowitz et al<sup>87</sup>, when analyzing non-selected patients with HF, found that only 17% of them presented anemia. It is noteworthy the fact that the heart failure in the two aforementioned studies was not due to valvulopathies.</p>
      <p>The anemia in patients with HF can occur due to several factors, such as decreased intestinal absorption of iron, caused by either insufficient ingestion of iron or intestinal loop edema and the chronic gastric loss of blood among patients who use acetylsalicylic acid.</p>
      <p>The increase in cytokines, such as the tumor necrosis factor alpha (TNF-&#945;), which produce bone marrow depression, is another reported factor. The activation of the renin-angiotensin-aldosterone system (RAAS) causes sodium and water retention, resulting in anemia due to hemodilution.</p>
      <p>Similarly, the renal dysfunction, which affects patients with HF, partly due to vasoconstriction and renal ischemia, causes a decrease in the production of erythropoietin and loss of erythropoietin and transferrin due to the coexistence of proteinuria.</p>
      <p>In addition to the treatment with angiotensin-converting enzyme (ACE) inhibitors, which can alter the production of erythropoietin in the kidney, especially at high doses, the anticoagulant treatment can contribute to the presence of anemia, producing blood loss<sup>21</sup>.</p>
      <p>On the other hand, the anemia contributes to the HF, as there is higher cardiac expense to provide the necessary oxygen supply to the tissues, which produces the stimulation of the sympathetic nervous system with vasoconstriction and tachycardia. The renal vasoconstriction activates the RAAS, with decrease in the renal flow and water retention, causing secondary renal failure that aggravates anemia and causes, in the long term, ventricular hypertrophy and remodeling, worsening the HF<sup>22</sup>. This anemia and HF cycle was observed in our study, where the prevalence of anemia was quite high in patients with HF, thus demonstrating the contribution of these two comorbidities to a worse prognosis.</p>
      <p>Anemia and RD are common comorbidities currently recognized as risk factors that modify the course of HF<sup>8</sup>. RD is an increasingly more frequent finding in patients with HF and its early detection, correct staging and control represents a clinical challenge. Most of the clinical studies in HF exclude patients with RD; therefore, even the use of medications employed in the treatment of HF presents potential risks to renal function. The RD causes imbalance in the cardio-renal system and can cause HF instability in the short-term<sup>23</sup>.</p>
      <p>Currently, the RD is considered an independent risk factor for the prognosis in hospitalized patients with decompensated HF<sup>25,10,24</sup>. Several studies have assessed the presence of anemia in patients with a GFR &lt; 60 ml/min/1.73 m<sup>2</sup><sup>5</sup>, demonstrating a great impact, in hospitalized patients, of the association of RD, HF and anemia on mortality<sup>26</sup>. In our series, only 1/3 of the patients presented a GFR &gt; 60 ml/min/1.73 m<sup>2</sup>.</p>
      <p>No positive correlation was found between RD and the presence of HF in the studied population, which can be attributed to a possible higher prevalence of patients with non-severe HF; that could not be measured in our study, as the HF severity was not assessed, neither classified.</p>
      <p>Malnutrition, as well as RD and anemia, is frequently observed among patients with valvulopathies, especially those with HF. In our series, the correlation between anemia and malnutrition was not observed. On the other hand, the study by Horwich et al<sup>6</sup> oushowed a possible association between anemia and malnutrition, considering the association between the serum levels of albumin and BMI.</p>
      <p>The available clinical and experimental data indicate an association between HF and malnutrition<sup>27</sup>. There are some doubts on which mechanisms lead to malnutrition and what the importance of each mechanism is in the maintenance and aggravation of the condition<sup>28</sup>. Krummel<sup>29</sup> ratifies what was observed in the present study, when affirming that de 35.0% to 53.0% of the patients with HF presented malnutrition. The prevalence of malnutrition in our series was 69.2% in patients with HF. In a retrospective study carried out by Herreros et aland<sup>30</sup>, a prevalence of 28% of malnutrition was observed in patients with valvulopathies, confirming our findings once again.</p>
      <p>Veloso et al<sup>27</sup> suggest that the impact of the nutritional status on advanced heart failure, although it results from the left ventricular contractile dysfunction as a common etiological factor, have as its main determinant factors, in each individual, other factors that go beyond the involvement of the cardiac pump. The nutritional involvement could be better understood within the scope of the complex peripheral adaptation and the neurohumoral response to myocardial failure<sup>27</sup>.</p>
      <p>The malnutrition in these patients can also be explained by the increase in levels of cytokines such as TNF-&#945; and interleukin-6. The cytokines are also quite increased at the advanced stages of the disease and studies have demonstrated an association between the increase in their levels and weight loss<sup>31</sup>.</p>
      <p>
        <bold>Conclusion</bold>
      </p>
      <p>The prevalence of anemia, RD and malnutrition was high in the study population, especially in patients with HF, which can contribute to a worse prognosis; thus, it is necessary to establish the early diagnosis and treatment of such comorbidities.</p>
      <p>
        <bold>Potential Conflict of Interest</bold>
      </p>
      <p>No potential conflict of interest relevant to this article was reported.</p>
      <p>
        <bold>Sources of Funding</bold>
      </p>
      <p>There were no external funding sources for this study.</p>
      <p>
        <bold>Study Association</bold>
      </p>
      <p>This article is part of Wysllenny Nascimento de Souza's Senior Research Project submitted at <italic>Ensino superior Bureau jur&#237;dico</italic> (<italic>Faculdade Mauricio de Nassau</italic>).</p>
      <p>
        <bold>References</bold>
      </p>
      <p>16. Statistical Package for the Social Sciences for Windows Student version. Release 7.5. Marketing Department. Chicago, 1996</p>
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