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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">rnfdv7gc7K9trKkzB5DqXwM</article-id>
      <article-id pub-id-type="other">00006</article-id>
      <article-id pub-id-type="publisher-id" specific-use="scielo-v2">S0066-782X2010001100006</article-id>
      <article-id pub-id-type="publisher-id" specific-use="scielo-v1">S0066-782X(10)09500106</article-id>
      <article-id pub-id-type="doi">10.1590/S0066-782X2010005000082</article-id>
      <article-categories>
        <subj-group subj-group-type="heading">
          <subject>Artigo Original</subject>
        </subj-group>
      </article-categories>
      <title-group>
        <article-title>&#205;ndices geom&#233;tricos de variabilidade da frequ&#234;ncia card&#237;aca em crian&#231;as obesas e eutr&#243;ficas</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="author">
          <name>
            <surname>Vanderlei</surname>
            <given-names>Luiz Carlos Marques</given-names>
          </name>
          <xref ref-type="aff" rid="aff01"/>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Pastre</surname>
            <given-names>Carlos Marcelo</given-names>
          </name>
          <xref ref-type="aff" rid="aff02"/>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Freitas J&#250;nior</surname>
            <given-names>Ismael Forte</given-names>
          </name>
          <xref ref-type="aff" rid="aff03"/>
        </contrib>
        <contrib contrib-type="author">
          <name>
            <surname>Godoy</surname>
            <given-names>Moacir Fernandes de</given-names>
          </name>
          <xref ref-type="aff" rid="aff03"/>
        </contrib>
      </contrib-group>
      <aff id="aff02">
        <addr-line>
          <named-content content-type="state">S&#227;o Paulo</named-content>
        </addr-line>
        <institution content-type="orgname">Universidade Estadual Paulista</institution>
        <institution content-type="orgdiv1">Faculdade de Ci&#234;ncias e Tecnologia </institution>
        <country country="BR">Brazil</country>
      </aff>
      <aff id="aff01">
        <addr-line>
          <named-content content-type="state">S&#227;o Paulo</named-content>
        </addr-line>
        <institution content-type="orgname">Universidade Estadual Paulista</institution>
        <institution content-type="orgdiv1">Faculdade de Ci&#234;ncias e Tecnologia </institution>
        <country country="BR">Brazil</country>
      </aff>
      <aff id="aff03">
        <addr-line>
          <named-content content-type="state">S&#227;o Paulo</named-content>
        </addr-line>
        <institution content-type="orgname">Faculdade de Medicina de S&#227;o Jos&#233; do Rio Preto</institution>
        <institution content-type="orgdiv1">Departamento de Cardiologia e Cirurgia Cardiovascular </institution>
        <country country="BR">Brazil</country>
      </aff>
      <pub-date date-type="collection" publication-format="electronic">
        <month>07</month>
        <year>2010</year>
      </pub-date>
      <volume>95</volume>
      <issue>1</issue>
      <fpage>35</fpage>
      <lpage>40</lpage>
      <history>
        <date date-type="accepted">
          <day>29</day>
          <month>12</month>
          <year>2009</year>
        </date>
        <date date-type="rev-recd">
          <day>12</day>
          <month>11</month>
          <year>2009</year>
        </date>
        <date date-type="received">
          <day>16</day>
          <month>09</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: Obesidade promove altera&#231;&#245;es na modula&#231;&#227;o auton&#244;mica card&#237;aca. OBJETIVO: Investigar a modula&#231;&#227;o auton&#244;mica de crian&#231;as obesas e eutr&#243;ficas por meio de &#237;ndices de variabilidade da frequ&#234;ncia card&#237;aca (VFC) obtidos por m&#233;todos geom&#233;tricos. M&#201;TODOS: Foram analisados dados de 133 crian&#231;as, com idade entre 8 e 13 anos, divididas em dois grupos: obeso (n = 61) e eutr&#243;fico (n = 72), segundo o &#237;ndice de massa corporal para sexo e idade. Para a an&#225;lise da VFC, a frequ&#234;ncia card&#237;aca foi captada batimento-a-batimento. Os intervalos RR obtidos foram convertidos em figuras geom&#233;tricas e, a partir delas, foram calculados o &#237;ndice triangular (RRtri), interpola&#231;&#227;o triangular dos intervalos RR (TINN), os &#237;ndices SD1, SD2 e rela&#231;&#227;o SD1/SD2, obtidos do plot de Poincar&#233;. An&#225;lise visual do plot foi tamb&#233;m realizada. Realizaram-se o teste t de Student para dados n&#227;o pareados e o teste de Mann-Whitney, com n&#237;vel de signific&#226;ncia de 5,0%, para an&#225;lise dos dados. RESULTADOS: Em crian&#231;as obesas, foram observadas redu&#231;&#245;es dos &#237;ndices RRtri (0,0730 vs 0,1084 [mediana]), TINN (171,80 &#177; 55,08 vs 218,26 &#177; 51,12), SD1 (19,93 &#177; 9,10 vs 24,10 &#177; 8,03) e SD2 (51,63 &#177; 16,53 vs 69,78 &#177; 17,19). A rela&#231;&#227;o SD1/SD2 n&#227;o apresentou diferen&#231;as significantes (0,3781 &#177; 0,12 vs 0,3467 &#177; 0,08). A an&#225;lise visual do plot, em crian&#231;as obesas, mostrou menor dispers&#227;o dos intervalos RR tanto batimento-a-batimento, como a longo prazo, indicando menor VFC. CONCLUS&#195;O: Crian&#231;as obesas apresentaram modifica&#231;&#245;es no sistema nervoso aut&#244;nomo, caracterizadas por redu&#231;&#245;es na atividade parassimp&#225;tica e na variabilidade global.</p>
      </abstract>
      <kwd-group xml:lang="pt" kwd-group-type="author-generated">
        <kwd>Frequ&#234;ncia card&#237;aca</kwd>
        <kwd>crian&#231;a</kwd>
        <kwd>obesidade</kwd>
        <kwd>&#237;ndice de massa corporal</kwd>
        <kwd>sistema nervoso aut&#244;nomo</kwd>
      </kwd-group>
      <pub-date publication-format="electronic" date-type="pub">
        <day>02</day>
        <month>07</month>
        <year>2010</year>
      </pub-date>
    </article-meta>
  </front>
  <body>
    <p>
      <bold>ARTIGO ORIGINAL</bold>
    </p>
    <p>
      <bold>CARDIOLOGIA PEDI&#193;TRICA</bold>
    </p>
    <p>&#205;ndices geom&#233;tricos de variabilidade da frequ&#234;ncia card&#237;aca em crian&#231;as obesas e eutr&#243;ficas</p>
    <p>
      <bold>Luiz Carlos Marques Vanderlei<sup>I</sup>; Carlos Marcelo Pastre<sup>II</sup>; Ismael Forte Freitas J&#250;nior<sup>III</sup>; Moacir Fernandes de Godoy<sup>III</sup></bold>
    </p>
    <p><sup>I</sup>Faculdade de Ci&#234;ncias e Tecnologia - UNESP - Univ Estadual Paulista, Departamento de Fisioterapia </p>
    <p><sup>II</sup>Faculdade de Ci&#234;ncias e Tecnologia - UNESP - Univ Estadual Paulista, Departamento de Educa&#231;&#227;o F&#237;sica, Presidente Prudente, S&#227;o Paulo </p>
    <p><sup>III</sup>Faculdade de Medicina de S&#227;o Jos&#233; do Rio Preto - Departamento de Cardiologia e Cirurgia Cardiovascular, S&#227;o Jos&#233; do Rio Preto, S&#227;o Paulo - Brasil</p>
    <p>
      <xref ref-type="corresp" rid="linkcorresp">Correspond&#234;ncia</xref>
    </p>
    <p>
      <bold>RESUMO</bold>
    </p>
    <p><bold>FUNDAMENTO:</bold> Obesidade promove altera&#231;&#245;es na modula&#231;&#227;o auton&#244;mica card&#237;aca. </p>
    <p><bold>OBJETIVO:</bold> Investigar a modula&#231;&#227;o auton&#244;mica de crian&#231;as obesas e eutr&#243;ficas por meio de &#237;ndices de variabilidade da frequ&#234;ncia card&#237;aca (VFC) obtidos por m&#233;todos geom&#233;tricos. </p>
    <p><bold>M&#201;TODOS:</bold> Foram analisados dados de 133 crian&#231;as, com idade entre 8 e 13 anos, divididas em dois grupos: obeso (n = 61) e eutr&#243;fico (n = 72), segundo o &#237;ndice de massa corporal para sexo e idade. Para a an&#225;lise da VFC, a frequ&#234;ncia card&#237;aca foi captada batimento-a-batimento. Os intervalos RR obtidos foram convertidos em figuras geom&#233;tricas e, a partir delas, foram calculados o &#237;ndice triangular (RRtri), interpola&#231;&#227;o triangular dos intervalos RR (TINN), os &#237;ndices SD1, SD2 e rela&#231;&#227;o SD1/SD2, obtidos do <italic>plot</italic> de Poincar&#233;. An&#225;lise visual do <italic>plot</italic> foi tamb&#233;m realizada. Realizaram-se o teste <italic>t</italic> de <italic>Student</italic> para dados n&#227;o pareados e o teste de Mann-Whitney, com n&#237;vel de signific&#226;ncia de 5,0%, para an&#225;lise dos dados. </p>
    <p><bold>RESULTADOS:</bold> Em crian&#231;as obesas, foram observadas redu&#231;&#245;es dos &#237;ndices RRtri (0,0730 <italic>vs</italic> 0,1084 [mediana]), TINN (171,80 &#177; 55,08 <italic>vs</italic> 218,26 &#177; 51,12), SD1 (19,93 &#177; 9,10 <italic>vs</italic> 24,10 &#177; 8,03) e SD2 (51,63 &#177; 16,53 <italic>vs</italic> 69,78 &#177; 17,19). A rela&#231;&#227;o SD1/SD2 n&#227;o apresentou diferen&#231;as significantes (0,3781 &#177; 0,12 <italic>vs</italic> 0,3467 &#177; 0,08). A an&#225;lise visual do <italic>plot</italic>, em crian&#231;as obesas, mostrou menor dispers&#227;o dos intervalos RR tanto batimento-a-batimento, como a longo prazo, indicando menor VFC. </p>
    <p><bold>CONCLUS&#195;O:</bold> Crian&#231;as obesas apresentaram modifica&#231;&#245;es no sistema nervoso aut&#244;nomo, caracterizadas por redu&#231;&#245;es na atividade parassimp&#225;tica e na variabilidade global. </p>
    <p><bold>Palavras-chave:</bold> Frequ&#234;ncia card&#237;aca, crian&#231;a, obesidade, &#237;ndice de massa corporal, sistema nervoso aut&#244;nomo.</p>
    <p>
      <bold>Introdu&#231;&#227;o</bold>
    </p>
    <p>Altera&#231;&#245;es na frequ&#234;ncia card&#237;aca, definidas como variabilidade da frequ&#234;ncia card&#237;aca (VFC), s&#227;o normais e esperadas e indicam a habilidade do cora&#231;&#227;o em responder aos m&#250;ltiplos est&#237;mulos fisiol&#243;gicos e ambientais, bem como compensar desordens induzidas por doen&#231;as<sup>1</sup>.</p>
    <p>Trata-se de uma medida n&#227;o invasiva que pode ser utilizada para identificar fen&#244;menos relacionados ao sistema nervoso aut&#244;nomo (SNA)<sup>2</sup>. Dentre os m&#233;todos utilizados para an&#225;lise da VFC, encontram-se os m&#233;todos geom&#233;tricos - &#237;ndice triangular (RRtri), interpola&#231;&#227;o triangular de histograma de intervalos NN (TINN) e <italic>plot</italic> de Poincar&#233; - os quais convertem os intervalos RR em padr&#245;es geom&#233;tricos e permitem analisar a VFC por meio das propriedades geom&#233;tricas ou gr&#225;ficas do padr&#227;o resultante<sup>2-4</sup>.</p>
    <p>O RRtri e o TINN s&#227;o calculados a partir da constru&#231;&#227;o de um histograma de densidade dos intervalos RR normais, que cont&#233;m no eixo x o comprimento dos intervalos RR, e no eixo y, a frequ&#234;ncia com que eles ocorreram. A uni&#227;o dos pontos das colunas do histograma forma uma figura semelhante a um tri&#226;ngulo do qual s&#227;o extra&#237;dos esses &#237;ndices<sup>2,4,5</sup>.</p>
    <p>O <italic>plot</italic> de Poincar&#233; &#233; uma representa&#231;&#227;o gr&#225;fica bidimensional da correla&#231;&#227;o entre intervalos RR consecutivos, em que cada intervalo &#233; plotado contra o pr&#243;ximo intervalo<sup>6,7</sup> e a sua an&#225;lise pode ser feita de forma qualitativa, por meio da avalia&#231;&#227;o da figura formada pelo seu atrator, a qual mostra o grau de complexidade dos intervalos RR<sup>8,9</sup>, ou quantitativa, pelo ajuste de uma elipse &#224; figura formada pelo <italic>plot</italic>, de onde se obt&#233;m os &#237;ndices: SD1, SD2 e a raz&#227;o SD1/SD2<sup>10,11</sup>. Al&#233;m disso, a an&#225;lise do <italic>plot</italic> de Poincar&#233; &#233; considerada por alguns autores como baseada na din&#226;mica n&#227;o linear<sup>7,12</sup>.</p>
    <p>A an&#225;lise da VFC por m&#233;todos n&#227;o lineares vem ganhando crescente interesse, pois existem evid&#234;ncias de que os mecanismos envolvidos na regula&#231;&#227;o cardiovascular provavelmente interagem entre si de modo n&#227;o linear<sup>13</sup>.</p>
    <p>Esses m&#233;todos descrevem as flutua&#231;&#245;es complexas do ritmo e conseguem separar estruturas de comportamento n&#227;o linear nas s&#233;ries temporais de batimentos card&#237;acos mais adequadamente do que os m&#233;todos lineares<sup>14</sup>. Tem sido especulado que a an&#225;lise de VFC baseada em m&#233;todos da din&#226;mica n&#227;o linear pode fornecer valiosas informa&#231;&#245;es para interpreta&#231;&#245;es fisiol&#243;gicas da VFC e para avalia&#231;&#227;o do risco de morte s&#250;bita<sup>7</sup>, al&#233;m de possibilitar melhor entendimento da natureza de sistemas din&#226;micos e complexos que ocorrem no corpo humano, tanto na sa&#250;de como na doen&#231;a<sup>15</sup>.</p>
    <p>Estudos t&#234;m demonstrado que a obesidade produz altera&#231;&#245;es na fun&#231;&#227;o do sistema nervoso aut&#244;nomo em crian&#231;as e adolescentes<sup>16,17</sup>. Tal condi&#231;&#227;o de desequil&#237;brio pode representar um fator negativo importante, j&#225; que o funcionamento auton&#244;mico controla parte das fun&#231;&#245;es internas do corpo e, nesse sentido, merece aten&#231;&#227;o. </p>
    <p>Os trabalhos envolvendo a obesidade em crian&#231;as e a an&#225;lise do SNA, por meio da avalia&#231;&#227;o da VFC, t&#234;m apresentado resultados controversos. Sekine e cols.<sup>18</sup>, analisando &#237;ndices de VFC no dom&#237;nio da frequ&#234;ncia, sugerem que elas t&#234;m maior atividade simp&#225;tica e menor atividade parassimp&#225;tica quando comparadas com crian&#231;as eutr&#243;ficas, enquanto que Nagai e cols.<sup>19</sup> e Nagai e Moritani<sup>20</sup> observaram atividades tanto simp&#225;tica quanto parassimp&#225;tica diminu&#237;das em crian&#231;as obesas. J&#225; Yakinci e cols.<sup>21</sup>, utilizando testes auton&#244;micos funcionais, observaram atividade simp&#225;tica normal e hipoatividade parassimp&#225;tica, e, mais recentemente, Kaufman e cols.<sup>16</sup> observaram aumento da rela&#231;&#227;o LF/HF e diminui&#231;&#227;o do &#237;ndice HF. Pascoal e cols.<sup>22</sup> constataram maior t&#244;nus card&#237;aco na posi&#231;&#227;o b&#237;pede quando comparadas crian&#231;as obesas com crian&#231;as eutr&#243;ficas.</p>
    <p>Esses trabalhos avaliam a VFC utilizando m&#233;todos lineares, entretanto, destaca-se que, ap&#243;s busca sistem&#225;tica em bases de dados pertinentes visando &#224; elabora&#231;&#227;o deste manuscrito, n&#227;o foram encontrados trabalhos que utilizam m&#233;todos geom&#233;tricos como forma de an&#225;lise.</p>
    <p>Sendo assim, com intuito de acrescentar elementos relacionados ao tema exposto na literatura, pretende-se, com este trabalho, investigar a modula&#231;&#227;o auton&#244;mica de crian&#231;as obesas e eutr&#243;ficas por meio de &#237;ndices de VFC obtidos atrav&#233;s de m&#233;todos geom&#233;tricos.</p>
    <p>
      <bold>M&#233;todos</bold>
    </p>
    <p>
      <bold>Popula&#231;&#227;o</bold>
    </p>
    <p>Para a realiza&#231;&#227;o deste trabalho, foram analisados dados de 133 crian&#231;as, independente do sexo, numa faixa et&#225;ria entre 08 e 13 anos. As crian&#231;as foram divididas em dois grupos segundo o estado nutricional: obesas e eutr&#243;ficas. A obesidade foi definida segundo os crit&#233;rios estabelecidos para idade e sexo por Cole e cols.<sup>23</sup>.</p>
    <p>O grupo obeso foi constitu&#237;do por 61 crian&#231;as, sendo 28 do sexo masculino (45,90%) e 33 do sexo feminino (54,10%), enquanto que o grupo eutr&#243;fico foi formado por 72 crian&#231;as (35 do sexo masculino [48,60%] e 37 do sexo feminino [51,40%]). As caracter&#237;sticas dessas crian&#231;as (idade, peso, altura e &#237;ndice de massa corp&#243;rea) podem ser visibilizadas na <xref ref-type="table" rid="tab01">Tabela 1</xref>.</p>
    <table-wrap id="tab01">
      <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gt01.jpg"/></table-wrap>
    <p>N&#227;o foram inclu&#237;das neste estudo, crian&#231;as com relato de pelo menos uma das seguintes caracter&#237;sticas: uso de medicamentos que influenciassem a atividade auton&#244;mica do cora&#231;&#227;o, como por exemplo, propranolol e atropina, infec&#231;&#245;es, doen&#231;as metab&#243;licas ou do sistema cardiorrespirat&#243;rio conhecidas.</p>
    <p>Os volunt&#225;rios e seus respons&#225;veis foram devidamente informados sobre os procedimentos e objetivos deste estudo, e ap&#243;s concordarem, o respons&#225;vel assinou um termo de consentimento livre e esclarecido. Todos os procedimentos utilizados foram aprovados pelo Comit&#234; de &#201;tica em Pesquisa da Faculdade de Ci&#234;ncias e Tecnologia - FCT/UNESP (Proc. n&#194;&#186; 187/2007).</p>
    <p>
      <bold>Protocolo experimental</bold>
    </p>
    <p>Antes do in&#237;cio do procedimento experimental, as crian&#231;as foram identificadas coletando-se as seguintes informa&#231;&#245;es: idade, sexo, peso, altura e &#237;ndice de massa corp&#243;rea. As medidas antropom&#233;tricas foram obtidas de acordo com as recomenda&#231;&#245;es descritas por Lohman e cols.<sup>24</sup>.</p>
    <p>O peso foi mensurado em uma balan&#231;a digital (FilizzolaPL 150, Filizzola Ltda., Brasil) com precis&#227;o de 0,1 kg, com as crian&#231;as usando roupas leves e sem sapatos. A altura foi mensurada usando um estadi&#244;metro com precis&#227;o de 0,1 cm e 2 metros de comprimento. O IMC foi calculado usando a seguinte f&#243;rmula: peso (kg)/altura (m)<sup>2</sup>.</p>
    <p>A coleta dos dados foi realizada em uma sala com temperatura entre 21&#194;&#176; C e 23&#194;&#176; C e umidade entre 40 e 60%. Ap&#243;s a avalia&#231;&#227;o inicial, foram explicados todos os procedimentos necess&#225;rios para realiza&#231;&#227;o da coleta de dados, que foi realizada de forma individual. As crian&#231;as foram orientadas a manterem-se em repouso, evitando conversarem durante a coleta.</p>
    <p>Ap&#243;s tais procedimentos, foi colocada no t&#243;rax das crian&#231;as, ao n&#237;vel do ter&#231;o distal do esterno, a cinta de capta&#231;&#227;o e, no seu pulso, o receptor de frequ&#234;ncia card&#237;aca Polar S810i (Polar Electro, Finl&#226;ndia), equipamento previamente validado para capta&#231;&#227;o da frequ&#234;ncia card&#237;aca batimento-a-batimento e a utiliza&#231;&#227;o dos seus dados para an&#225;lise da VFC em crian&#231;as e adultos<sup>25,26</sup>.</p>
    <p>Ap&#243;s a coloca&#231;&#227;o da cinta e do monitor, as crian&#231;as foram colocadas em dec&#250;bito dorsal em um colchonete e permaneceram em repouso e com respira&#231;&#227;o espont&#226;nea por 20 minutos. Ap&#243;s esse per&#237;odo de coleta, as crian&#231;as foram liberadas.</p>
    <p>Para an&#225;lise da VFC, o padr&#227;o de seu comportamento foi registrado batimento-a-batimento, durante todo o protocolo experimental, com uma taxa de amostragem de 1.000 Hz. Para an&#225;lise dos dados, foram utilizados 1.000 intervalos RR consecutivos, ap&#243;s ter sido feita filtragem digital, complementada por manual, para elimina&#231;&#227;o de batimentos ect&#243;picos prematuros e artefatos, e somente s&#233;ries com mais de 95,0% de batimentos sinusais foram inclu&#237;das no estudo<sup>27</sup>.</p>
    <p>
      <bold>An&#225;lise dos &#237;ndices de variabilidade da frequ&#234;ncia card&#237;aca</bold>
    </p>
    <p>A an&#225;lise da VFC foi realizada por meio dos m&#233;todos geom&#233;tricos: RRtri, TINN e <italic>plot</italic> de Poincar&#233; (SD1, SD2, rela&#231;&#227;o SD1/SD2). </p>
    <p>O RRtri foi calculado a partir da constru&#231;&#227;o de um histograma de densidade dos intervalos RR, o qual cont&#233;m no eixo horizontal todos os poss&#237;veis valores dos intervalos RR mensurados, em uma escala discreta com caixas de 7,8125 ms (1/128 segundos) e, no eixo vertical, a frequ&#234;ncia com que cada um deles ocorreu. A uni&#227;o dos pontos das colunas do histograma forma uma figura semelhante a um tri&#226;ngulo. O RRtri foi obtido dividindo-se o n&#250;mero total de intervalos RR utilizados para constru&#231;&#227;o do histograma pela frequ&#234;ncia modal dos mesmos (valor do intervalo RR que mais apareceu na s&#233;rie RR)<sup>2</sup>.</p>
    <p>O TINN consiste na medida da base de um tri&#226;ngulo, sendo o m&#233;todo da diferen&#231;a dos m&#237;nimos quadrados utilizado para determina&#231;&#227;o do tri&#226;ngulo<sup>2</sup>. O RRtri e o TINN expressam a variabilidade global dos intervalos RR<sup>2</sup>.</p>
    <p>O <italic>plot</italic> de Poincar&#233; &#233; um mapa de pontos em coordenadas cartesianas, constru&#237;do a partir dos valores dos intervalos RR obtidos, onde cada ponto &#233; representado no eixo <italic>x</italic> (horizontal/abcissa) pelo intervalo RR normal precedente e, no eixo <italic>y</italic> (vertical/ordenada), pelo intervalo RR seguinte.</p>
    <p>Para an&#225;lise quantitativa do <italic>plot,</italic> foi ajustada uma elipse aos pontos do gr&#225;fico, com centro determinado pela m&#233;dia dos intervalos RR, e foram calculados os &#237;ndices SD1, que mede o desvio-padr&#227;o das dist&#226;ncias dos pontos &#224; diagonal <italic>y </italic>= <italic>x</italic>, e SD2 que mede o desvio-padr&#227;o das dist&#226;ncias dos pontos &#224; reta <italic>y </italic>= -<italic>x </italic>+ <italic>RRm</italic>, onde <italic>RRm</italic> &#233; a m&#233;dia dos intervalos RR. O SD1 &#233; um &#237;ndice de registro instant&#226;neo da variabilidade batimento-a-batimento e representa a atividade parassimp&#225;tica, enquanto que o &#237;ndice SD2 representa a VFC, em registros de longa dura&#231;&#227;o, e reflete a variabilidade global. A rela&#231;&#227;o de ambos (SD1/SD2) mostra a raz&#227;o entre as varia&#231;&#245;es curta e longa dos intervalos RR<sup>1,11</sup>.</p>
    <p>A an&#225;lise qualitativa do <italic>plot</italic> foi feita por meio da an&#225;lise das figuras formadas pelo seu atrator, as quais foram descritas por Tulppo e cols.<sup>28</sup> em:</p>
    <disp-quote>
      <p>1. Figura na qual um aumento na dispers&#227;o dos intervalos RR &#233; observado com aumento nos intervalos, caracter&#237;stica de um <italic>plot</italic> normal.</p>
      <p>2. Figura com pequena dispers&#227;o global batimento-a-batimento e sem aumento da dispers&#227;o dos intervalos RR, a longo prazo.</p>
    </disp-quote>
    <p>O <italic>software</italic> HRV analysis - Vers&#227;o 2.0 foi utilizado para o c&#225;lculo desses &#237;ndices<sup>29</sup>.</p>
    <p>
      <bold>Tratamento estat&#237;stico</bold>
    </p>
    <p>Para compara&#231;&#227;o dos grupos, inicialmente foi determinada a normalidade dos dados por meio do teste Shapiro-Wilks. Quando a distribui&#231;&#227;o normal foi aceita, o teste t de <italic>Student</italic> para dados n&#227;o pareados foi aplicado (idade, altura, TINN, SD1, SD2 e rela&#231;&#227;o SD1/SD2) e nas situa&#231;&#245;es onde a distribui&#231;&#227;o normal n&#227;o foi aceita, foi aplicado o teste de Mann-Whitney (peso, IMC, RRTri). Diferen&#231;as nesses testes foram consideradas estatisticamente significantes quando o valor de "P" foi menor ou igual a 0,05.</p>
    <p>
      <bold>RESULTADOS</bold>
    </p>
    <p>A <xref ref-type="table" rid="tab02">Tabela 2</xref> mostra os valores obtidos para os &#237;ndices RRtri, TINN, SD1, SD2 e rela&#231;&#227;o SD1/SD2 dos grupos obeso e eutr&#243;fico. Observam-se valores significantemente menores para o grupo obeso em compara&#231;&#227;o ao grupo eutr&#243;fico, exceto para a rela&#231;&#227;o SD1/SD2 que n&#227;o apresentou diferen&#231;a estatisticamente significante entre os grupos. </p>
    <table-wrap id="tab02">
      <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gt02.jpg"/></table-wrap>
    <p>As <xref ref-type="fig" rid="aop07510fig01">Figuras 1</xref> e <xref ref-type="fig" rid="aop07510fig02">2</xref> mostram exemplos padr&#245;es do <italic>plot</italic> de Poincar&#233; para crian&#231;as obesas e controles.</p>
    <p content-type="asset">
      <fig id="aop07510fig01">
        <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gf01.jpg"/></fig>
    </p>
    <p content-type="asset">
      <fig id="aop07510fig02">
        <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gf02.jpg"/></fig>
    </p>
    <p>
      <bold>DISCUSS&#195;O</bold>
    </p>
    <p>Os resultados obtidos por meio dos &#237;ndices de VFC, no presente estudo, mostraram que nas crian&#231;as obesas analisadas ocorreram redu&#231;&#245;es dos &#237;ndices geom&#233;tricos, sugerindo que, nestas crian&#231;as, a variabilidade da frequ&#234;ncia card&#237;aca est&#225; reduzida.</p>
    <p>O &#237;ndice SD1, que representa o eixo transverso do <italic>plot</italic> de Poincar&#233;, mostra o desvio-padr&#227;o da variabilidade instant&#226;nea da frequ&#234;ncia card&#237;aca batimento-a-batimento<sup>11</sup> e indica a influ&#234;ncia parassimp&#225;tica sobre o n&#243;dulo sinoatrial<sup>10</sup>. Os menores valores do &#237;ndice SD1 em crian&#231;as obesas sugerem que, nestas crian&#231;as, a atividade parassimp&#225;tica est&#225; reduzida.</p>
    <p>Atividade parassimp&#225;tica diminu&#237;da em crian&#231;as obesas foi tamb&#233;m relatada por outros autores<sup>16,19,21</sup>. Tal redu&#231;&#227;o est&#225; associada ao aumento do risco para morbidade e mortalidade por todas as causas e ao desenvolvimento de v&#225;rios fatores de risco<sup>30</sup>.</p>
    <p>Martini e cols.<sup>31</sup> observaram que crian&#231;as obesas t&#234;m maiores valores de press&#227;o arterial, de glicose sangu&#237;nea, de insulina e de n&#237;veis de triglicer&#237;deos, e menores valores de lipoprote&#237;na de alta densidade (HDL), quando comparadas com crian&#231;as n&#227;o obesas. Paschoal e cols.<sup>22</sup> tamb&#233;m relataram menores valores de HDL e aumento de triglicer&#237;deos em crian&#231;as obesas. A presen&#231;a de tais caracter&#237;sticas em crian&#231;as portadoras de obesidade pode estar associada a altera&#231;&#245;es na atividade do SNA conforme afirma Sekine e cols.<sup>18</sup>.</p>
    <p>Os &#237;ndices SD2, TINN e RRtri tamb&#233;m apresentaram redu&#231;&#227;o nas crian&#231;as obesas em compara&#231;&#227;o com as crian&#231;as do grupo eutr&#243;fico. Esses &#237;ndices expressam a variabilidade global dos intervalos RR<sup>2,11</sup>, o que sugere que crian&#231;as obesas apresentam redu&#231;&#227;o da variabilidade global da frequ&#234;ncia card&#237;aca.</p>
    <p>Sekine e cols.<sup>18</sup> e Martini e cols.<sup>31</sup>, avaliando a variabilidade global em crian&#231;as obesas por meio do &#237;ndice SDNN (desvio padr&#227;o dos intervalos RR), n&#227;o encontraram diferen&#231;as estatisticamente significantes neste &#237;ndice, contudo os valores se apresentaram menores nestas crian&#231;as, em compara&#231;&#227;o com as n&#227;o obesas. Redu&#231;&#227;o significativa desse &#237;ndice foi relatada por Rabbia e cols.<sup>32</sup> em adolescentes obesos (idade de 13,9 &#177; 1,7 anos).</p>
    <p>Em crian&#231;as obesas, redu&#231;&#227;o na atividade simp&#225;tica foi descrita na literatura<sup>19,20</sup>. Este sistema participa do controle do metabolismo da glicose e da gordura<sup>33</sup> e menor atividade simp&#225;tica foi associada a menor gasto energ&#233;tico e, consequentemente, um balan&#231;o energ&#233;tico positivo e ganho de peso<sup>34</sup>.</p>
    <p>Quanto &#224; rela&#231;&#227;o SD1/SD2, as an&#225;lises mostraram que n&#227;o ocorreram diferen&#231;as significativas desse &#237;ndice quando comparado o grupo obeso com o grupo eutr&#243;fico, o que pode ser justificado pela redu&#231;&#227;o observada tanto no &#237;ndice SD1 quanto no SD2, em crian&#231;as obesas.</p>
    <p>A an&#225;lise visual do <italic>plot</italic> de Poincar&#233; mostrou nas crian&#231;as eutr&#243;ficas uma maior dispers&#227;o batimento-a-batimento dos intervalos RR, bem como maior dispers&#227;o dos intervalos RR a longo prazo, em compara&#231;&#227;o com as crian&#231;as obesas, indicando que estas crian&#231;as possuem maior VFC.</p>
    <p>Em indiv&#237;duos saud&#225;veis, em repouso, os intervalos entre os batimentos card&#237;acos s&#227;o bastante irregulares, sobretudo pela predomin&#226;ncia vagal na modula&#231;&#227;o card&#237;aca, fazendo com que se visualize, na plotagem de Poincar&#233;, uma nuvem de pontos com a forma aproximada de uma elipse<sup>28,35</sup>, o que pode ser observado nas crian&#231;as eutr&#243;ficas.</p>
    <p>Diferentemente do que foi observado nas crian&#231;as eutr&#243;ficas, as an&#225;lises das figuras do <italic>plot</italic> das crian&#231;as obesas mostraram menor dispers&#227;o dos intervalos RR, tanto batimento-a-batimento como a longo prazo, indicando menor VFC.</p>
    <p>Em resumo, os resultados deste trabalho sugerem que crian&#231;as obesas apresentam disfun&#231;&#245;es auton&#244;micas, caracterizadas por redu&#231;&#245;es na atividade parassimp&#225;tica e da variabilidade global. Tais achados, associados aos graves problemas que podem ser produzidos pela obesidade<sup>36</sup>, refor&#231;am a necessidade de tratamento da obesidade infantil e, neste sentido, a atividade f&#237;sica e uma dieta hipocal&#243;rica, fundamentadas em condutas apropriadas, podem ser ferramentas eficientes para reverter as altera&#231;&#245;es fisiol&#243;gicas provocadas pela obesidade. Esses procedimentos, al&#233;m de reduzir o peso corporal, levam &#224; diminui&#231;&#227;o da atividade simp&#225;tica e da press&#227;o arterial, melhoram a sensibilidade &#224; insulina, diminuem as concentra&#231;&#245;es plasm&#225;ticas de triglic&#233;rides e aumentam as de HDL-colesterol<sup>37-39</sup>, aspectos que podem ser ben&#233;ficos para amenizar ou eliminar os riscos produzidos pela obesidade.</p>
    <p>
      <bold>Conclus&#245;es</bold>
    </p>
    <p>Os resultados sugerem que crian&#231;as obesas apresentam modifica&#231;&#245;es no sistema nervoso aut&#244;nomo, caracterizadas por redu&#231;&#245;es na atividade parassimp&#225;tica e na variabilidade global, o que demonstra a necessidade de aten&#231;&#227;o precoce a estas crian&#231;as, para evitar complica&#231;&#245;es futuras.</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 foi financiado pela Funda&#231;&#227;o de Amparo &#224; Pesquisa do Estado de S&#227;o Paulo - Processo FAPESP n&#194;&#186; 2008/05414-0.</p>
    <p>
      <bold>Vincula&#231;&#227;o Acad&#234;mica</bold>
    </p>
    <p>N&#227;o h&#225; vincula&#231;&#227;o deste estudo a programas de p&#243;s-gradua&#231;&#227;o.</p>
    <p>
      <fn id="linkcorresp" fn-type="corresp">
        <p>Correspond&#234;ncia:</p>
        <p> Luiz Carlos Marques Vanderlei </p>
        <p> Rua Roberto Simonsen, 305 - Departamento de Fisioterapia </p>
        <p> 19060-900 - Presidente Prudente, SP - Brasil </p>
        <p> E-mail: </p>
        <p>
          <email xlink:href="lcmvanderlei@fct.unesp.br">lcmvanderlei@fct.unesp.br</email>
        </p>
      </fn>
    </p>
    <p> Artigo recebido em 16/09/09; revisado recebido em 12/11/09; aceito em 29/12/09.</p>
  </body>
  <back>
    <ref-list>
      <ref id="B1">
        <mixed-citation>1. Vanderlei LCM, Pastre CM, Hoshi RA, Carvalho TD, Godoy MF. No&#231;&#245;es b&#225;sicas de variabilidade da frequ&#234;ncia card&#237;aca e sua aplicabilidade cl&#237;nica. Rev Bras Cir Cardiovasc. 2009; 24 (2): 205-17.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>No&#231;&#245;es b&#225;sicas de variabilidade da frequ&#234;ncia card&#237;aca e sua aplicabilidade cl&#237;nica</article-title>
          <source>Rev Bras Cir Cardiovasc</source>
          <date>
            <year>2009</year>
          </date>
          <fpage>205</fpage>
          <lpage>17</lpage>
          <issue>2</issue>
          <volume>24</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Vanderlei</surname>
              <given-names>LCM</given-names>
            </name>
            <name>
              <surname>Pastre</surname>
              <given-names>CM</given-names>
            </name>
            <name>
              <surname>Hoshi</surname>
              <given-names>RA</given-names>
            </name>
            <name>
              <surname>Carvalho</surname>
              <given-names>TD</given-names>
            </name>
            <name>
              <surname>Godoy</surname>
              <given-names>MF</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B2">
        <mixed-citation>2. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation. 1996; 93 (5): 1043-65.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Heart rate variability: standards of measurement, physiological interpretation and clinical use</article-title>
          <source>Circulation</source>
          <date>
            <year>1996</year>
          </date>
          <fpage>1043</fpage>
          <lpage>65</lpage>
          <issue>5</issue>
          <volume>93</volume>
        </element-citation>
      </ref>
      <ref id="B3">
        <mixed-citation>3. Majercak I. The use of heart variability in cardiology. Bratisl Lek Listy. 2002; 103 (10): 368-77.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>The use of heart variability in cardiology</article-title>
          <source>Bratisl Lek Listy</source>
          <date>
            <year>2002</year>
          </date>
          <fpage>368</fpage>
          <lpage>77</lpage>
          <issue>10</issue>
          <volume>103</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Majercak</surname>
              <given-names>I</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B4">
        <mixed-citation>4. Rajendra Acharya U, Paul Joseph K, Kannathal N, Lim CM, Suri JS. Heart rate variability: a review. Med Biol Eng Comput. 2006; 44 (12): 1031-51.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Heart rate variability: a review</article-title>
          <source>Med Biol Eng Comput</source>
          <date>
            <year>2006</year>
          </date>
          <fpage>1031</fpage>
          <lpage>51</lpage>
          <issue>12</issue>
          <volume>44</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Rajendra Acharya</surname>
              <given-names>U</given-names>
            </name>
            <name>
              <surname>Paul Joseph</surname>
              <given-names>K</given-names>
            </name>
            <name>
              <surname>Kannathal</surname>
              <given-names>N</given-names>
            </name>
            <name>
              <surname>Lim</surname>
              <given-names>CM</given-names>
            </name>
            <name>
              <surname>Suri</surname>
              <given-names>JS</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B5">
        <mixed-citation>5. Rocha RM, Albuquerque DC, Albanesi Filho FM. Variabilidade da frequ&#234;ncia card&#237;aca e ritmo circadiano em pacientes com angina est&#225;vel. Rev SOCERJ. 2005; 18 (4): 429-42.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Variabilidade da frequ&#234;ncia card&#237;aca e ritmo circadiano em pacientes com angina est&#225;vel</article-title>
          <source>Rev SOCERJ</source>
          <date>
            <year>2005</year>
          </date>
          <fpage>429</fpage>
          <lpage>42</lpage>
          <issue>4</issue>
          <volume>18</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Rocha</surname>
              <given-names>RM</given-names>
            </name>
            <name>
              <surname>Albuquerque</surname>
              <given-names>DC</given-names>
            </name>
            <name>
              <surname>Albanesi Filho</surname>
              <given-names>FM</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B6">
        <mixed-citation>6. Lerma C, Infante O, P&#233;rez-Grovas H, Jos&#233; MV. Poincar&#233; plot indexes of heart rate variability capture dynamic adaptations after haemodialysis in chronic renal failure patients. Clin Physiol Funct Imaging. 2003; 23 (2): 72-80.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Poincar&#233; plot indexes of heart rate variability capture dynamic adaptations after haemodialysis in chronic renal failure patients</article-title>
          <source>Clin Physiol Funct Imaging</source>
          <date>
            <year>2003</year>
          </date>
          <fpage>72</fpage>
          <lpage>80</lpage>
          <issue>2</issue>
          <volume>23</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Lerma</surname>
              <given-names>C</given-names>
            </name>
            <name>
              <surname>Infante</surname>
              <given-names>O</given-names>
            </name>
            <name>
              <surname>P&#233;rez-Grovas</surname>
              <given-names>H</given-names>
            </name>
            <name>
              <surname>Jos&#233;</surname>
              <given-names>MV</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B7">
        <mixed-citation>7. Khaled AS, Owis MI, Mohamed ASA. Employing time-domain methods and poincar&#233; plot of heart rate variability signals to detect congestive heart failure. BIME Journal. 2006; 6 (1): 35-41.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Employing time-domain methods and poincar&#233; plot of heart rate variability signals to detect congestive heart failure</article-title>
          <source>BIME Journal</source>
          <date>
            <year>2006</year>
          </date>
          <fpage>35</fpage>
          <lpage>41</lpage>
          <issue>1</issue>
          <volume>6</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Khaled</surname>
              <given-names>AS</given-names>
            </name>
            <name>
              <surname>Owis</surname>
              <given-names>MI</given-names>
            </name>
            <name>
              <surname>Mohamed</surname>
              <given-names>ASA</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B8">
        <mixed-citation>8. Woo MA, Stevenson WG, Moser DK, Trelease RB, Harper RM. Patterns of beat to beat heart rate variability in advanced heart failure. Am Heart J. 1992; 123: 704-10.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Patterns of beat to beat heart rate variability in advanced heart failure</article-title>
          <source>Am Heart J</source>
          <date>
            <year>1992</year>
          </date>
          <fpage>704</fpage>
          <lpage>10</lpage>
          <volume>123</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Woo</surname>
              <given-names>MA</given-names>
            </name>
            <name>
              <surname>Stevenson</surname>
              <given-names>WG</given-names>
            </name>
            <name>
              <surname>Moser</surname>
              <given-names>DK</given-names>
            </name>
            <name>
              <surname>Trelease</surname>
              <given-names>RB</given-names>
            </name>
            <name>
              <surname>Harper</surname>
              <given-names>RM</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B9">
        <mixed-citation>9. Vito GD, Galloway SDR, Nimmo MA, Maas P, McMurray JJV. Effects of central sympathetic inhibition on heart rate variability during steady-state exercise in healthy humans. Clin Physiol Funct Imaging. 2002; 22: 32-8.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Effects of central sympathetic inhibition on heart rate variability during steady-state exercise in healthy humans</article-title>
          <source>Clin Physiol Funct Imaging</source>
          <date>
            <year>2002</year>
          </date>
          <fpage>32</fpage>
          <lpage>8</lpage>
          <volume>22</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Vito</surname>
              <given-names>GD</given-names>
            </name>
            <name>
              <surname>Galloway</surname>
              <given-names>SDR</given-names>
            </name>
            <name>
              <surname>Nimmo</surname>
              <given-names>MA</given-names>
            </name>
            <name>
              <surname>Maas</surname>
              <given-names>P</given-names>
            </name>
            <name>
              <surname>McMurray</surname>
              <given-names>JJV</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B10">
        <mixed-citation>10. Tulppo MP, Makikallio TH, Takala TES, Seppanen T, Huikuri HV. Quantitative beat-to-beat analysis of heart rate dynamics during exercise. Am J Physiol (Circ Physiol). 1996; 271 (7): H244-H252.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Quantitative beat-to-beat analysis of heart rate dynamics during exercise</article-title>
          <source>Am J Physiol (Circ Physiol)</source>
          <date>
            <year>1996</year>
          </date>
          <fpage>H244</fpage>
          <lpage>H252</lpage>
          <issue>7</issue>
          <volume>271</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Tulppo</surname>
              <given-names>MP</given-names>
            </name>
            <name>
              <surname>Makikallio</surname>
              <given-names>TH</given-names>
            </name>
            <name>
              <surname>Takala</surname>
              <given-names>TES</given-names>
            </name>
            <name>
              <surname>Seppanen</surname>
              <given-names>T</given-names>
            </name>
            <name>
              <surname>Huikuri</surname>
              <given-names>HV</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B11">
        <mixed-citation>11. Brunetto AF, Silva BM, Roseguini BT, Hirai DM, Guedes DP. Limiar ventilat&#243;rio e variabilidade da frequ&#234;ncia card&#237;aca em adolescentes. Rev Bras Med Esporte. 2005; 11 (1): 22-7.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Limiar ventilat&#243;rio e variabilidade da frequ&#234;ncia card&#237;aca em adolescentes</article-title>
          <source>Rev Bras Med Esporte</source>
          <date>
            <year>2005</year>
          </date>
          <fpage>22</fpage>
          <lpage>7</lpage>
          <issue>1</issue>
          <volume>11</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Brunetto</surname>
              <given-names>AF</given-names>
            </name>
            <name>
              <surname>Silva</surname>
              <given-names>BM</given-names>
            </name>
            <name>
              <surname>Roseguini</surname>
              <given-names>BT</given-names>
            </name>
            <name>
              <surname>Hirai</surname>
              <given-names>DM</given-names>
            </name>
            <name>
              <surname>Guedes</surname>
              <given-names>DP</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B12">
        <mixed-citation>12. Voss A, Schroeder R, Truebner S, Goernig M, Figulla HR, Schirdewan A. Comparison of nonlinear methods symbolic dynamics, detrended fluctuation, and Poincar&#233; plot analysis in risk stratification in patients with dilated cardiomyopathy. Chaos. 2007; 17 (1): 015120.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Comparison of nonlinear methods symbolic dynamics, detrended fluctuation, and Poincar&#233; plot analysis in risk stratification in patients with dilated cardiomyopathy</article-title>
          <source>Chaos</source>
          <date>
            <year>2007</year>
          </date>
          <fpage>015120</fpage>
          <issue>1</issue>
          <volume>17</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Voss</surname>
              <given-names>A</given-names>
            </name>
            <name>
              <surname>Schroeder</surname>
              <given-names>R</given-names>
            </name>
            <name>
              <surname>Truebner</surname>
              <given-names>S</given-names>
            </name>
            <name>
              <surname>Goernig</surname>
              <given-names>M</given-names>
            </name>
            <name>
              <surname>Figulla</surname>
              <given-names>HR</given-names>
            </name>
            <name>
              <surname>Schirdewan</surname>
              <given-names>A</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B13">
        <mixed-citation>13. Huikuri HV, Makikallio TH, Perkiomaki J. Measurement of heart rate variability by methods based on nonlinear dynamics. J Electrocardiol. 2003; 36 9 (Suppl): 95-9.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Measurement of heart rate variability by methods based on nonlinear dynamics</article-title>
          <source>J Electrocardiol.</source>
          <date>
            <year>2003</year>
          </date>
          <fpage>95</fpage>
          <lpage>9</lpage>
          <issue>9</issue>
          <volume>36</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Huikuri</surname>
              <given-names>HV</given-names>
            </name>
            <name>
              <surname>Makikallio</surname>
              <given-names>TH</given-names>
            </name>
            <name>
              <surname>Perkiomaki</surname>
              <given-names>J</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B14">
        <mixed-citation>14. Voss A, Kurths J, Kleiner HJ, Witt A, Wessel N, Saparin P, et al. The application of methods of non-linear dynamics for the improved and predictive recognition of patients threatened by sudden cardiac death. Cardiovasc Res. 1996; 31: 419-33.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>The application of methods of non-linear dynamics for the improved and predictive recognition of patients threatened by sudden cardiac death</article-title>
          <source>Cardiovasc Res</source>
          <date>
            <year>1996</year>
          </date>
          <fpage>419</fpage>
          <lpage>33</lpage>
          <volume>31</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Voss</surname>
              <given-names>A</given-names>
            </name>
            <name>
              <surname>Kurths</surname>
              <given-names>J</given-names>
            </name>
            <name>
              <surname>Kleiner</surname>
              <given-names>HJ</given-names>
            </name>
            <name>
              <surname>Witt</surname>
              <given-names>A</given-names>
            </name>
            <name>
              <surname>Wessel</surname>
              <given-names>N</given-names>
            </name>
            <name>
              <surname>Saparin</surname>
              <given-names>P</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B15">
        <mixed-citation>15. Higgins JP. Nonlinear systems in medicine. Yale J Biol Med. 2002; 75 (5-6): 247-60.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Nonlinear systems in medicine</article-title>
          <source>Yale J Biol Med</source>
          <date>
            <year>2002</year>
          </date>
          <fpage>247</fpage>
          <lpage>60</lpage>
          <issue>5-6</issue>
          <volume>75</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Higgins</surname>
              <given-names>JP</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B16">
        <mixed-citation>16. Kaufman CL, Kaiser DR, Steinberger J, Kelly AS, Dengel DR. Relationships of cardiac autonomic function with metabolic abnormalities in childhood obesity. Obesity. 2007; 15 (5): 1164-71.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Relationships of cardiac autonomic function with metabolic abnormalities in childhood obesity</article-title>
          <source>Obesity</source>
          <date>
            <year>2007</year>
          </date>
          <fpage>1164</fpage>
          <lpage>71</lpage>
          <issue>5</issue>
          <volume>15</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Kaufman</surname>
              <given-names>CL</given-names>
            </name>
            <name>
              <surname>Kaiser</surname>
              <given-names>DR</given-names>
            </name>
            <name>
              <surname>Steinberger</surname>
              <given-names>J</given-names>
            </name>
            <name>
              <surname>Kelly</surname>
              <given-names>AS</given-names>
            </name>
            <name>
              <surname>Dengel</surname>
              <given-names>DR</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B17">
        <mixed-citation>17. Tonhajzerova I, Javorka M, Trunkvalterova Z, Chroma O, Javorkova J, Lazarova Z, et al. Cardio-respiratory interaction and autonomic dysfunction in obesity. J Physiol Pharmac. 2008: 59 (Suppl 6): 709-18.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Cardio-respiratory interaction and autonomic dysfunction in obesity</article-title>
          <source>J Physiol Pharmac.</source>
          <date>
            <year>2008</year>
          </date>
          <fpage>709</fpage>
          <lpage>18</lpage>
          <volume>59</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Tonhajzerova</surname>
              <given-names>I</given-names>
            </name>
            <name>
              <surname>Javorka</surname>
              <given-names>M</given-names>
            </name>
            <name>
              <surname>Trunkvalterova</surname>
              <given-names>Z</given-names>
            </name>
            <name>
              <surname>Chroma</surname>
              <given-names>O</given-names>
            </name>
            <name>
              <surname>Javorkova</surname>
              <given-names>J</given-names>
            </name>
            <name>
              <surname>Lazarova</surname>
              <given-names>Z</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B18">
        <mixed-citation>18. Sekine M, Izumi I, Yamagami T, Kagamimori S. Obesity and cardiac autonomic nerve activity in healthy children: results of the Toyama Birth Cohort Study. Environm Health Prev Med. 2001; 6: 149-53.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Obesity and cardiac autonomic nerve activity in healthy children: results of the Toyama Birth Cohort Study</article-title>
          <source>Environm Health Prev Med</source>
          <date>
            <year>2001</year>
          </date>
          <fpage>149</fpage>
          <lpage>53</lpage>
          <volume>6</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Sekine</surname>
              <given-names>M</given-names>
            </name>
            <name>
              <surname>Izumi</surname>
              <given-names>I</given-names>
            </name>
            <name>
              <surname>Yamagami</surname>
              <given-names>T</given-names>
            </name>
            <name>
              <surname>Kagamimori</surname>
              <given-names>S</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B19">
        <mixed-citation>19. Nagai N, Matsumoto T, Kita H, Moritani T. Autonomic nervous system activity and the state and development of obesity in japanese school children. Obes Res. 2003; 11: 25-32.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Autonomic nervous system activity and the state and development of obesity in japanese school children</article-title>
          <source>Obes Res</source>
          <date>
            <year>2003</year>
          </date>
          <fpage>25</fpage>
          <lpage>32</lpage>
          <volume>11</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Nagai</surname>
              <given-names>N</given-names>
            </name>
            <name>
              <surname>Matsumoto</surname>
              <given-names>T</given-names>
            </name>
            <name>
              <surname>Kita</surname>
              <given-names>H</given-names>
            </name>
            <name>
              <surname>Moritani</surname>
              <given-names>T</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B20">
        <mixed-citation>20. Nagai N, Moritani T. Effect of physical activity on autonomic nervous system function in lean and obese children. Int J Obesity. 2004; 28: 27-33.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Effect of physical activity on autonomic nervous system function in lean and obese children</article-title>
          <source>Int J Obesity</source>
          <date>
            <year>2004</year>
          </date>
          <fpage>27</fpage>
          <lpage>33</lpage>
          <volume>28</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Nagai</surname>
              <given-names>N</given-names>
            </name>
            <name>
              <surname>Moritani</surname>
              <given-names>T</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B21">
        <mixed-citation>21. Yakinci C, Mungen B, Karabiber H, Tayfun M, Evereklioglu C. Autonomic nervous system functions in obese children. Brain Dev. 2000; 22: 151-3.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Autonomic nervous system functions in obese children</article-title>
          <source>Brain Dev</source>
          <date>
            <year>2000</year>
          </date>
          <fpage>151</fpage>
          <lpage>3</lpage>
          <volume>22</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Yakinci</surname>
              <given-names>C</given-names>
            </name>
            <name>
              <surname>Mungen</surname>
              <given-names>B</given-names>
            </name>
            <name>
              <surname>Karabiber</surname>
              <given-names>H</given-names>
            </name>
            <name>
              <surname>Tayfun</surname>
              <given-names>M</given-names>
            </name>
            <name>
              <surname>Evereklioglu</surname>
              <given-names>C</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B22">
        <mixed-citation>22. Paschoal MA, Trevizan PF, Scodeler NF. Variabilidade da frequ&#234;ncia card&#237;aca, l&#237;pides e capacidade f&#237;sica de crian&#231;as obesas e n&#227;o-obesas. Arq Bras Cardiol. 2009; 93 (3): 239-46.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Variabilidade da frequ&#234;ncia card&#237;aca, l&#237;pides e capacidade f&#237;sica de crian&#231;as obesas e n&#227;o-obesas</article-title>
          <source>Arq Bras Cardiol</source>
          <date>
            <year>2009</year>
          </date>
          <fpage>239</fpage>
          <lpage>46</lpage>
          <issue>3</issue>
          <volume>93</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Paschoal</surname>
              <given-names>MA</given-names>
            </name>
            <name>
              <surname>Trevizan</surname>
              <given-names>PF</given-names>
            </name>
            <name>
              <surname>Scodeler</surname>
              <given-names>NF</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B23">
        <mixed-citation>23. Cole TM, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ. 2000; 320 (6): 1-6.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Establishing a standard definition for child overweight and obesity worldwide: international survey</article-title>
          <source>BMJ</source>
          <date>
            <year>2000</year>
          </date>
          <fpage>1</fpage>
          <lpage>6</lpage>
          <issue>6</issue>
          <volume>320</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Cole</surname>
              <given-names>TM</given-names>
            </name>
            <name>
              <surname>Bellizzi</surname>
              <given-names>MC</given-names>
            </name>
            <name>
              <surname>Flegal</surname>
              <given-names>KM</given-names>
            </name>
            <name>
              <surname>Dietz</surname>
              <given-names>WH</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B24">
        <mixed-citation>24. Lohman TG, Roche AF, Martorell R. Anthropometric standardization reference manual. Champaign: Human Kinetics Books; 1988.</mixed-citation>
        <element-citation publication-type="book">
          <source>Anthropometric standardization reference manual</source>
          <date>
            <year>1988</year>
          </date>
          <person-group person-group-type="author">
            <name>
              <surname>Lohman</surname>
              <given-names>TG</given-names>
            </name>
            <name>
              <surname>Roche</surname>
              <given-names>AF</given-names>
            </name>
            <name>
              <surname>Martorell</surname>
              <given-names>R</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B25">
        <mixed-citation>25. Gamelin FX, Baquet G, Berthoin S, Bosquet L. Validity of the polar S810 to measure R-R intervals in children. Int J Sports Med. 2008; 29: 134-8.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Validity of the polar S810 to measure R-R intervals in children</article-title>
          <source>Int J Sports Med</source>
          <date>
            <year>2008</year>
          </date>
          <fpage>134</fpage>
          <lpage>8</lpage>
          <volume>29</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Gamelin</surname>
              <given-names>FX</given-names>
            </name>
            <name>
              <surname>Baquet</surname>
              <given-names>G</given-names>
            </name>
            <name>
              <surname>Berthoin</surname>
              <given-names>S</given-names>
            </name>
            <name>
              <surname>Bosquet</surname>
              <given-names>L</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B26">
        <mixed-citation>26. Vanderlei LCM, Silva RA, Pastre CM, Azevedo FM, Godoy MF. Comparison of the Polar S810i monitor and the ECG for the analysis of heart rate variability in the time and frequency domains. Braz J Med Biol Res. 2008; 41 (10): 854-9.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Comparison of the Polar S810i monitor and the ECG for the analysis of heart rate variability in the time and frequency domains</article-title>
          <source>Braz J Med Biol Res</source>
          <date>
            <year>2008</year>
          </date>
          <fpage>854</fpage>
          <lpage>9</lpage>
          <issue>10</issue>
          <volume>41</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Vanderlei</surname>
              <given-names>LCM</given-names>
            </name>
            <name>
              <surname>Silva</surname>
              <given-names>RA</given-names>
            </name>
            <name>
              <surname>Pastre</surname>
              <given-names>CM</given-names>
            </name>
            <name>
              <surname>Azevedo</surname>
              <given-names>FM</given-names>
            </name>
            <name>
              <surname>Godoy</surname>
              <given-names>MF</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B27">
        <mixed-citation>27. Godoy MF, Takakura IT, Correa PR. Relev&#226;ncia da an&#225;lise do comportamento din&#226;mico n&#227;o-linear (Teoria do Caos) como elemento progn&#243;stico de morbidade e mortalidade em pacientes submetidos &#224; cirurgia de revasculariza&#231;&#227;o mioc&#225;rdica. Arq Cienc Sa&#250;de. 2005; 12 (4): 167-71.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Relev&#226;ncia da an&#225;lise do comportamento din&#226;mico n&#227;o-linear (Teoria do Caos) como elemento progn&#243;stico de morbidade e mortalidade em pacientes submetidos &#224; cirurgia de revasculariza&#231;&#227;o mioc&#225;rdica</article-title>
          <source>Arq Cienc Sa&#250;de</source>
          <date>
            <year>2005</year>
          </date>
          <fpage>167</fpage>
          <lpage>71</lpage>
          <issue>4</issue>
          <volume>12</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Godoy</surname>
              <given-names>MF</given-names>
            </name>
            <name>
              <surname>Takakura</surname>
              <given-names>IT</given-names>
            </name>
            <name>
              <surname>Correa</surname>
              <given-names>PR</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B28">
        <mixed-citation>28. Tulppo MP, M&#228;kikallio TH, Sepp&#228;nen T, Laukkanen RT, Huikuri HV. Vagal modulation of heart rate during exercise: effects of age and physical fitness. Am J Physiol. 1998; 274 (2Pt 2): H424-9.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Vagal modulation of heart rate during exercise: effects of age and physical fitness</article-title>
          <source>Am J Physiol</source>
          <date>
            <year>1998</year>
          </date>
          <fpage>H424</fpage>
          <lpage>9</lpage>
          <issue>2 Pt 2</issue>
          <volume>274</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Tulppo</surname>
              <given-names>MP</given-names>
            </name>
            <name>
              <surname>M&#228;kikallio</surname>
              <given-names>TH</given-names>
            </name>
            <name>
              <surname>Sepp&#228;nen</surname>
              <given-names>T</given-names>
            </name>
            <name>
              <surname>Laukkanen</surname>
              <given-names>RT</given-names>
            </name>
            <name>
              <surname>Huikuri</surname>
              <given-names>HV</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B29">
        <mixed-citation>29. Niskanen JP, Tarvainen MP, Ranta-aho PO, Karjalainen PA. Software for advanced HRV analysis. Comp Meth Progr Biomed. 2004; 76: 73-81.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Software for advanced HRV analysis</article-title>
          <source>Comp Meth Progr Biomed</source>
          <date>
            <year>2004</year>
          </date>
          <fpage>73</fpage>
          <lpage>81</lpage>
          <volume>76</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Niskanen</surname>
              <given-names>JP</given-names>
            </name>
            <name>
              <surname>Tarvainen</surname>
              <given-names>MP</given-names>
            </name>
            <name>
              <surname>Ranta-aho</surname>
              <given-names>PO</given-names>
            </name>
            <name>
              <surname>Karjalainen</surname>
              <given-names>PA</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B30">
        <mixed-citation>30. Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol. 2007; 74: 224-42.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>The role of vagal function in the risk for cardiovascular disease and mortality</article-title>
          <source>Biol Psychol</source>
          <date>
            <year>2007</year>
          </date>
          <fpage>224</fpage>
          <lpage>42</lpage>
          <volume>74</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Thayer</surname>
              <given-names>JF</given-names>
            </name>
            <name>
              <surname>Lane</surname>
              <given-names>RD</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B31">
        <mixed-citation>31. Martini G, Riva P, Rabbia F, Molini V, Ferrero GB, Cerutti F, et al Heart rate variability in childhood obesity. Clin Auton Res. 2001; 11 (2): 87-91.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Heart rate variability in childhood obesity</article-title>
          <source>Clin Auton Res.</source>
          <date>
            <year>2001</year>
          </date>
          <fpage>87</fpage>
          <lpage>91</lpage>
          <issue>2</issue>
          <volume>11</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Martini</surname>
              <given-names>G</given-names>
            </name>
            <name>
              <surname>Riva</surname>
              <given-names>P</given-names>
            </name>
            <name>
              <surname>Rabbia</surname>
              <given-names>F</given-names>
            </name>
            <name>
              <surname>Molini</surname>
              <given-names>V</given-names>
            </name>
            <name>
              <surname>Ferrero</surname>
              <given-names>GB</given-names>
            </name>
            <name>
              <surname>Cerutti</surname>
              <given-names>F</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B32">
        <mixed-citation>32. Rabbia F, Silke B, Conterno A, Grosso T, De Vito B, Rabbone I, et al. Assessment of cardiac autonomic modulation during adolescent obesity. Obes Res. 2003; 11 (4): 541-8.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Assessment of cardiac autonomic modulation during adolescent obesity</article-title>
          <source>Obes Res</source>
          <date>
            <year>2003</year>
          </date>
          <fpage>541</fpage>
          <lpage>8</lpage>
          <issue>4</issue>
          <volume>11</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Rabbia</surname>
              <given-names>F</given-names>
            </name>
            <name>
              <surname>Silke</surname>
              <given-names>B</given-names>
            </name>
            <name>
              <surname>Conterno</surname>
              <given-names>A</given-names>
            </name>
            <name>
              <surname>Grosso</surname>
              <given-names>T</given-names>
            </name>
            <name>
              <surname>De Vito</surname>
              <given-names>B</given-names>
            </name>
            <name>
              <surname>Rabbone</surname>
              <given-names>I</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B33">
        <mixed-citation>33. Nonogaki K. New insight into sympathetic regulation of glucose and fat metabolism. Diabetologia. 2000; 43: 533-49.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>New insight into sympathetic regulation of glucose and fat metabolism</article-title>
          <source>Diabetologia</source>
          <date>
            <year>2000</year>
          </date>
          <fpage>533</fpage>
          <lpage>49</lpage>
          <volume>43</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Nonogaki</surname>
              <given-names>K</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B34">
        <mixed-citation>34. Peterson HR, Rothschild M, Weinberg CR, Fell RD, McLeish KR, Pfeifer MA. Body fat and the activity of the autonomic nervous system. N Engl J Med. 1988; 318: 1077-83.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Body fat and the activity of the autonomic nervous system</article-title>
          <source>N Engl J Med</source>
          <date>
            <year>1988</year>
          </date>
          <fpage>1077</fpage>
          <lpage>83</lpage>
          <volume>318</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Peterson</surname>
              <given-names>HR</given-names>
            </name>
            <name>
              <surname>Rothschild</surname>
              <given-names>M</given-names>
            </name>
            <name>
              <surname>Weinberg</surname>
              <given-names>CR</given-names>
            </name>
            <name>
              <surname>Fell</surname>
              <given-names>RD</given-names>
            </name>
            <name>
              <surname>McLeish</surname>
              <given-names>KR</given-names>
            </name>
            <name>
              <surname>Pfeifer</surname>
              <given-names>MA</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B35">
        <mixed-citation>35. Mourot L, Bouhaddi M, Perrey S, Rouillon JD, Regnard J. Quantitative Poincar&#233; plot analysis of heart rate: effect of endurance training. Eur J Appl Physiol. 2004; 91 (1): 79-87.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Quantitative Poincar&#233; plot analysis of heart rate: effect of endurance training</article-title>
          <source>Eur J Appl Physiol</source>
          <date>
            <year>2004</year>
          </date>
          <fpage>79</fpage>
          <lpage>87</lpage>
          <issue>1</issue>
          <volume>91</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Mourot</surname>
              <given-names>L</given-names>
            </name>
            <name>
              <surname>Bouhaddi</surname>
              <given-names>M</given-names>
            </name>
            <name>
              <surname>Perrey</surname>
              <given-names>S</given-names>
            </name>
            <name>
              <surname>Rouillon</surname>
              <given-names>JD</given-names>
            </name>
            <name>
              <surname>Regnard</surname>
              <given-names>J</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B36">
        <mixed-citation>36. Daniels SR. Complications of obesity in children and adolescents. Int J Obes. 2009; 33 (Suppl 1): S60-S65.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Complications of obesity in children and adolescents</article-title>
          <source>Int J Obes</source>
          <date>
            <year>2009</year>
          </date>
          <fpage>S60</fpage>
          <lpage>S65</lpage>
          <volume>33</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Daniels</surname>
              <given-names>SR</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B37">
        <mixed-citation>37. Ribeiro MM, Silva AG, Santos NS, Guazzelle I, Matos LNJ, Trombetta IC, et al. Diet and exercise training restore blood pressure and vasodilatory responses during physiological maneuvers in obese children. Circulation. 2005; 111 (15): 1915-23.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Diet and exercise training restore blood pressure and vasodilatory responses during physiological maneuvers in obese children</article-title>
          <source>Circulation</source>
          <date>
            <year>2005</year>
          </date>
          <fpage>1915</fpage>
          <lpage>23</lpage>
          <issue>15</issue>
          <volume>111</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Ribeiro</surname>
              <given-names>MM</given-names>
            </name>
            <name>
              <surname>Silva</surname>
              <given-names>AG</given-names>
            </name>
            <name>
              <surname>Santos</surname>
              <given-names>NS</given-names>
            </name>
            <name>
              <surname>Guazzelle</surname>
              <given-names>I</given-names>
            </name>
            <name>
              <surname>Matos</surname>
              <given-names>LNJ</given-names>
            </name>
            <name>
              <surname>Trombetta</surname>
              <given-names>IC</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B38">
        <mixed-citation>38. Carnethon MR, Craft LL. Autonomic association between exercise and diabetes: autonomic nervous system function. Exerc Sport Sci Rev. 2008; 36 (1): 12-8.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Autonomic association between exercise and diabetes: autonomic nervous system function</article-title>
          <source>Exerc Sport Sci Rev</source>
          <date>
            <year>2008</year>
          </date>
          <fpage>12</fpage>
          <lpage>8</lpage>
          <issue>1</issue>
          <volume>36</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Carnethon</surname>
              <given-names>MR</given-names>
            </name>
            <name>
              <surname>Craft</surname>
              <given-names>LL</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
      <ref id="B39">
        <mixed-citation>39. Sichieri R, Souza RA. Estrat&#233;gias para preven&#231;&#227;o da obesidade em crian&#231;as e adolescentes. Cad Sa&#250;de P&#250;blica. 2008; 24(supl. 2): S209-S234.</mixed-citation>
        <element-citation publication-type="journal">
          <article-title>Estrat&#233;gias para preven&#231;&#227;o da obesidade em crian&#231;as e adolescentes</article-title>
          <source>Cad Sa&#250;de P&#250;blica</source>
          <date>
            <year>2008</year>
          </date>
          <fpage>S209</fpage>
          <lpage>S234</lpage>
          <volume>24</volume>
          <person-group person-group-type="author">
            <name>
              <surname>Sichieri</surname>
              <given-names>R</given-names>
            </name>
            <name>
              <surname>Souza</surname>
              <given-names>RA</given-names>
            </name>
          </person-group>
        </element-citation>
      </ref>
    </ref-list>
  </back>
  <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">Geometric indexes of heart rate variability in obese and eutrophic children</article-title>
      </title-group>
      <abstract xml:lang="en">
        <p>BACKGROUND: Obesity causes changes in cardiac autonomic modulation. OBJECTIVE: To investigate the autonomic modulation of eutrophic and obese children by means of indexes of heart rate variability (HRV) obtained through geometric methods. METHODS: We analyzed data from 133 children aged 8 to 13, divided into two groups: obese (n = 61) and eutrophic (n = 72) according to body mass index for age and sex. For the analysis of HRV, heart rate was recorded beat-to-beat. The RR intervals were transformed into geometric figures, and from them, we calculated the triangular index (RRtri), triangular interpolation of RR intervals (TINN), the indexes SD1, SD2 and SD1/SD2 ratio, obtained from the Poincar&#233; plot. Visual analysis of the plot was also performed. Student's t test was performed for unpaired data and Mann-Whitney's test, with significance level of 5.0%, for data analysis. RESULTS: In obese children, RRtri indexes were proven to be reduced (0.0730 vs 0.1084 [median]), TINN (171.80 &#177; 55.08 vs 218.26 &#177; 51.12), SD1 (19.93 &#177; 9.10 vs 24.10 &#177; 8.03) and SD2 (51.63 &#177; 16.53 vs 69.78 &#177; 17.19). The SD1/SD2 ratio showed no significant differences (0.3781 &#177; 0.12 vs 0.3467 &#177; 0.08). Visual analysis of the plot, in obese children, revealed a smaller dispersion of RR intervals both beat-to-beat, and in the long term, indicating lower HRV. CONCLUSION: Obese children presented changes in the autonomic nervous system characterized by decreases in parasympathetic activity and overall variability.</p>
      </abstract>
      <kwd-group xml:lang="en">
        <kwd>Heart rate</kwd>
        <kwd>child</kwd>
        <kwd>obesity</kwd>
        <kwd>body mass index</kwd>
        <kwd>autonomic nervous system</kwd>
      </kwd-group>
    </front-stub>
    <body>
      <p>
        <bold>ORIGINAL ARTICLE</bold>
      </p>
      <p><undefined id="linkinicio-body2"/>Geometric indexes of heart rate variability in obese and eutrophic children</p>
      <p>
        <bold>Luiz Carlos Marques Vanderlei<sup>I</sup>; Carlos Marcelo Pastre<sup>I</sup>; Ismael Forte Freitas J&#250;nior<sup>II</sup>; Moacir Fernandes de Godoy<sup>III</sup></bold>
      </p>
      <p><sup>I</sup>Faculdade de Ci&#234;ncias e Tecnologia - UNESP - Univ Estadual Paulista, Departamento de Fisioterapia</p>
      <p><sup>II</sup>Faculdade de Ci&#234;ncias e Tecnologia - UNESP - Univ Estadual Paulista, Departamento de Educa&#231;&#227;o F&#237;sica, Presidente Prudente, S&#227;o Paulo</p>
      <p><sup>III</sup>Faculdade de Medicina de S&#227;o Jos&#233; do Rio Preto - Departamento de Cardiologia e Cirurgia Cardiovascular, S&#227;o Jos&#233; do Rio Preto, S&#227;o Paulo - Brazil</p>
      <p>Mailing address</p>
      <p>
        <bold>ABSTRACT</bold>
      </p>
      <p><bold>BACKGROUND:</bold> Obesity causes changes in cardiac autonomic modulation.</p>
      <p><bold>OBJECTIVE:</bold> To investigate the autonomic modulation of eutrophic and obese children by means of indexes of heart rate variability (HRV) obtained through geometric methods.</p>
      <p><bold>METHODS:</bold> We analyzed data from 133 children aged 8 to 13, divided into two groups: obese (n = 61) and eutrophic (n = 72) according to body mass index for age and sex. For the analysis of HRV, heart rate was recorded beat-to-beat. The RR intervals were transformed into geometric figures, and from them, we calculated the triangular index (RRtri), triangular interpolation of RR intervals (TINN), the indexes SD1, SD2 and SD1/SD2 ratio, obtained from the Poincar&#233; plot. Visual analysis of the plot was also performed. Student's t test was performed for unpaired data and Mann-Whitney's test, with significance level of 5.0%, for data analysis.</p>
      <p><bold>RESULTS:</bold> In obese children, RRtri indexes were proven to be reduced (0.0730 <italic>vs</italic> 0.1084 [median]), TINN (171.80 &#194;&#177; 55.08 <italic>vs</italic> 218.26 &#194;&#177; 51.12), SD1 (19.93 &#194;&#177; 9.10 <italic>vs</italic> 24.10 &#194;&#177; 8.03) and SD2 (51.63 &#194;&#177; 16.53 <italic>vs</italic> 69.78 &#194;&#177; 17.19). The SD1/SD2 ratio showed no significant differences (0.3781 &#194;&#177; 0.12 <italic>vs</italic> 0.3467 &#194;&#177; 0.08). Visual analysis of the plot, in obese children, revealed a smaller dispersion of RR intervals both beat-to-beat, and in the long term, indicating lower HRV.</p>
      <p><bold>CONCLUSION:</bold> Obese children presented changes in the autonomic nervous system characterized by decreases in parasympathetic activity and overall variability. </p>
      <p><bold>Key words:</bold> Heart rate; child; obesity; body mass index, autonomic nervous System.</p>
      <p>
        <bold>Introduction</bold>
      </p>
      <p>Changes in heart rate, defined as heart rate variability (HRV), are normal and expected and indicate the heart's ability to respond to multiple physiological and environmental stimuli, as well as compensate disorders induced by diseases<sup>1</sup>.</p>
      <p>It is a noninvasive measure that can be used to identify phenomena related to the autonomic nervous system (ANS)<sup>2</sup>. The methods used for HRV analysis include the geometric methods - triangular index (RRtri), triangular interpolation of NN interval histogram (TINN) and Poincar&#233; plot - which convert RR intervals into geometric patterns and allow analyzing HRV through the geometric or graphic properties of the resulting pattern<sup>2-4</sup>.</p>
      <p>The RRtri and TINN are calculated from the construction of a histogram of density of normal RR intervals, which contains on axis x the length of RR intervals, and on axis y, the frequency with which they occurred. Joining the points of the histogram columns forms a shape like a triangle from which these indexes are extracted<sup>2,4,5</sup>.</p>
      <p>The Poincar&#233; plot is a two-dimensional graphic representation of the correlation between consecutive RR intervals, in which each interval is plotted against the following interval<sup>6,7</sup> and its analysis can be done in a qualitative way, by assessing the shape formed by its attractor, which shows the degree of complexity of RR intervals<sup>8,9</sup>, or quantitative, by fitting an ellipse to the shape formed by the plot, from which the following indexes are produced: SD1, SD2 and the SD1/SD2 ratio<sup>10,11</sup>. Beside this, the analysis of the Poincar&#233; plot is considered by some authors as based on nonlinear dynamics<sup>7,12</sup>.</p>
      <p>HRV analysis by means of nonlinear methods has been gaining increasing interest, since there is evidence that the mechanisms involved in cardiovascular regulation probably interact in a nonlinear way<sup>13</sup>.</p>
      <p>These methods describe complex rhythm fluctuations and manage to separate nonlinear behavior structures in time series of heartbeats better than linear methods<sup>14</sup>. It has been speculated that HRV analysis based on nonlinear dynamics methods can provide valuable information for physiological interpretations of HRV and evaluation of risk of sudden death<sup>7</sup>, also enabling a better understanding of the nature of dynamic and complex systems occurring in healthy and sick human bodies<sup>15</sup>.</p>
      <p>Studies have shown that obesity causes changes in the function of the autonomic nervous system in children and adolescents<sup>16,17</sup>. Such a condition of imbalance may represent a major negative factor since the autonomic function controls some of the internal functions of the body and, accordingly, deserves attention. </p>
      <p>Studies involving obesity in children and analysis of ANS, through the evaluation of HRV, have shown controversial results. Sekine et al<sup>18</sup>, analyzing HRV indexes in the frequency domain, suggest that they have more sympathetic activity and less parasympathetic activity as compared with eutrophic children, while Nagai et al<sup>19</sup> and Nagai &amp; Moritani<sup>20</sup> observed both sympathetic and parasympathetic activities decreased in obese children. Yakinci et al<sup>21</sup>, using autonomic function tests, observed normal sympathetic activity and parasympathetic underactivity, and more recently, Kaufman et al<sup>16</sup> observed increase in LF/HF ratio and decreased HF index. Pascoal et al<sup>22</sup> found higher cardiac tone in the standing position when compared obese children with eutrophic children.</p>
      <p>These studies assess HRV using linear methods, however, it should be noted that, after a systematic search of relevant databases in order to prepare this manuscript, no studies were found using geometrical methods as a means of analysis.</p>
      <p>Hence, in order to add elements related to the theme exposed in literature, it is intended, with this study, to investigate the autonomic modulation in obese and eutrophic children through HRV indexes obtained by geometric methods.</p>
      <p>
        <bold>Methods</bold>
      </p>
      <p>
        <bold>Population</bold>
      </p>
      <p>For this study, we analyzed data from 133 children, regardless of gender, aged from 08 to 13. The children were divided into two groups according to nutritional status: obese and eutrophic. Obesity was defined according to criteria established for age and sex by Cole et al<sup>23</sup>.</p>
      <p>The obese group consisted of 61 children, 28 males (45.90%) and 33 females (54.10%), while the eutrophic group consisted of 72 children (35 males [48.60%] and 37 females [51.40%]). The characteristics of these children (age, weight, height and body mass index) can be seen in <xref ref-type="table" rid="tab01-body2">Table 1</xref>.</p>
      <table-wrap id="tab01-body2">
        <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gt01-en.jpg"/></table-wrap>
      <p>Children reporting at least one of the following characteristics were not included in this study: use of medications that would influence the autonomic activity of the heart, such as propranolol and atropine, infections, or metabolic diseases or cardiorespiratory system diseases.</p>
      <p>The volunteers and their guardians were fully informed about the procedures and purpose of this study and, after agreeing, their guardians signed an informed consent. All procedures were approved by the Research Ethics Committee of the School of Science and Technology - FCT/UNESP (Proc. No. 187/2007). </p>
      <p>
        <bold>Experimental protocol</bold>
      </p>
      <p>Before beginning the experimental procedure, children were identified by collecting the following information: age, sex, weight, height, and body mass index. Anthropometric measurements were obtained according to the recommendations described by Lohman et al<sup>24</sup>.</p>
      <p>Weight was measured on a digital scale (Filizzola PL 150, Filizzola Ltda., Brazil) with a precision of 0.1 kg, with children wearing light clothes and barefoot. Height was measured using a stadiometer with precision of 0.1 cm and 2 meters in length. BMI was calculated using the following formula: weight (kg)/height (m)<sup>2</sup>.</p>
      <p>Data collection was performed in a room with temperature between 21&#194;&#176; C and 23&#194;&#176; C and humidity between 40 and 60%. After the initial assessment, we explained all the procedures necessary to collect the data, which was done individually. The children were instructed to remain at rest, avoid talks during the collection.</p>
      <p>After these procedures, the recording strap was placed on the children's chest at the sternal angle. On their wrist, the heart rate receiver Polar S810i (Polar Electro, Finland). This equipment had been previously validated to record the beat-to-beat heart frequency and use their data for analysis of HRV in children and adults<sup>25,26</sup>. </p>
      <p>After placing the strap and the monitor, the children were placed supine on a mat and remained at rest with spontaneous breathing for 20 minutes. After the collection period, the children were discharged.</p>
      <p>For HRV analysis, the pattern of their behavior was recorded beat-to-beat throughout the experimental protocol, with a sampling rate of 1,000 Hz. For data analysis, we used 1,000 consecutive RR intervals after digital filtering, complemented with manual filtering, to eliminate premature and artifact ectopic beats, and only series with more than 95.0% of sinus beats were included in the study<sup>27</sup>.</p>
      <p>
        <bold>Analysis of heart rate variability indexes</bold>
      </p>
      <p>HRV analysis was performed by means of geometrical methods: RRtri, TINN and Poincar&#233; plot (SD1, SD2, SD1/SD2 ratio). </p>
      <p>The RRtri was calculated from the construction of a density histogram of RR intervals, which contains the horizontal axis of all possible values of RR intervals measured on a discrete scale with 7,8125 ms boxes (1/128 seconds) and on the vertical axis, the frequency with which each occurred. The union of points of the histogram columns forms a shape like a triangle. The RRtri was obtained by dividing the total number of RR intervals used to construct the histogram by their modal frequency (RR interval value that most frequently appeared on RR)<sup>2</sup>. </p>
      <p>The TINN consists of the measure of the base of a triangle. The method of least squares is used to determine the triangle<sup>2</sup>. The RRtri and the TINN express the overall variability of RR intervals<sup>2</sup>.</p>
      <p>The Poincar&#233; plot is a map of points in Cartesian coordinates, constructed from the values of RR intervals obtained, where each point is represented on axis x (horizontal/abscissa) by the previous normal RR interval, and on axis y (vertical/coordinate), by the following RR interval. </p>
      <p>For quantitative analysis of the plot, an ellipse was fitted to the points of the chart, with the center determined by the average RR intervals, and the SD1 indexes were calculated to measure the standard deviation of the distances of the points to the diagonal y = x, and SD2 measures the standard deviation of the distances of points to the line y = - x + RRm, where RRm is the average of RR intervals. The SD1 is an index of instantaneous recording of the variability of beat-to-beat and represents parasympathetic activity, while the index SD2 represents HRV in long-term records, and reflects the overall variability. Their ratio (SD1/SD2) shows the ratio between short and long variations of RR intervals<sup>1,11</sup>.</p>
      <p>The qualitative analysis of the plot was made through the analysis of the figures formed by its attractor, which were described by Tulppo et al<sup>28</sup> in:</p>
      <p>Figure in which an increase in the dispersion of RR intervals is observed with increased intervals, characteristic of a normal plot.</p>
      <p>Small figure with beat-to-beat global dispersion without increased dispersion of RR intervals in the long term.</p>
      <p>The HRV analysis software - Version 2.0 was used to calculate these indexes<sup>29</sup>.</p>
      <p>
        <bold>Statistical treatment</bold>
      </p>
      <p>To compare the groups, the normality of data was initially determined using the Shapiro-Wilks test. When normal distribution was accepted, Student's t test for unpaired data was applied (age, height, TINN, SD1, SD2 and SD1/SD2 ratio) and in situations where normal distribution was not accepted, we applied Mann-Whitney's test (weight, BMI, RRTri). Differences in these tests were considered statistically significant when the value of "P" was smaller than or equal to 0.05.</p>
      <p>
        <bold>Results</bold>
      </p>
      <p><xref ref-type="table" rid="tab02-body2">Table 2</xref> shows the values for the indexes RRtri, TINN, SD1, SD2 and SD1/SD2 ratio for obese and eutrophic groups. The study found significantly lower values for the obese group compared to the eutrophic group, except for the SD1/SD2 ratio, which presented no statistically significant difference between groups. </p>
      <table-wrap id="tab02-body2">
        <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gt02-en.jpg"/></table-wrap>
      <p><xref ref-type="fig" rid="en_aop07510fig01-body2">Figures 1</xref> and <xref ref-type="fig" rid="en_aop07510fig02-body2">2</xref> show examples of Poincar&#233; plot patterns for obese children and controls.</p>
      <p content-type="asset">
        <fig id="en_aop07510fig01-body2">
          <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gf01-en.jpg"/></fig>
      </p>
      <p content-type="asset">
        <fig id="en_aop07510fig02-body2">
          <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gf02-en.jpg"/></fig>
      </p>
      <p>
        <bold>Discussion</bold>
      </p>
      <p>The results obtained by means of HRV indexes showed that the obese children analyzed presented decreased geometric indexes, suggesting that in these children, the heart rate variability is reduced.</p>
      <p>The SD1 index, which represents the transverse axis of the Poincar&#233; plot shows the standard deviation of the instantaneous variability of the beat-to-beat heart rate<sup>11</sup> and indicates the parasympathetic influence on the sinoatrial node<sup>10</sup>. The lowest values of the SD1 index in obese children suggest that in these children, the parasympathetic activity is reduced.</p>
      <p>Decreased parasympathetic activity in obese children was also reported by other authors<sup>16,19,21</sup>. Such reduction is associated with increased risk for morbidity and mortality from all causes and development of several risk factors<sup>30</sup>. </p>
      <p>Martini et al<sup>31</sup> observed that obese children have higher blood pressure, blood glucose, insulin and triglyceride levels and lower levels of high density lipoprotein (HDL) when compared with non-obese children. Paschoal et al<sup>22</sup> also reported lower levels of HDL and increased triglycerides in obese children. The presence of such characteristics in children with obesity may be associated with changes in ANS activity as stated by Sekine et al<sup>18</sup>.</p>
      <p>The indexes SD2, TINN and RRtri also showed reduction in obese children compared with eutrophic children. These indexes express the overall variability of RR intervals<sup>2,11</sup>, suggesting that obese children have reduced the overall variability of heart rate.</p>
      <p>Sekine et al<sup>18</sup> and Martini et al<sup>31</sup>, evaluating the overall variability in obese children through the SDNN index (standard deviation of RR intervals), found no statistically significant differences in this index, however these values were lower in these children, compared with non-obese children. Significant reduction of this index was reported by Rabbia et al<sup>32</sup> in obese adolescents (aged 13.9 &#194;&#177; 1.7). </p>
      <p>In obese children, reduction in sympathetic activity was described in literature<sup>19,20</sup>. This system participates in the control of glucose metabolism and fat<sup>33</sup> and a lower level of sympathetic activity was associated with lower energy expenditure and therefore a positive energy balance and weight gain<sup>34</sup>.</p>
      <p>Concerning the SD1/SD2 ratio, the analyses showed no significant differences of this index when comparing the obese group against the eutrophic group, which can be explained by the reduction observed in both the SD1 and in the SD2 indexes in obese children.</p>
      <p>The visual analysis of Poincar&#233; plot revealed that eutrophic children have a greater beat-to-beat dispersion of RR intervals, as well as greater dispersion of RR intervals in the long term, compared with obese children, indicating that these children have higher HRV.</p>
      <p>In healthy individuals at rest, the intervals between beats are very irregular, especially by the vagal predominance in heart modulation, which makes it possible to see, in Poincar&#233; plot, a cloud of points with the approximate shape of an ellipse<sup>28,35</sup>, which can be observed in eutrophic children.</p>
      <p>Unlike what was observed in eutrophic children, analyses of figures from the plot of obese children showed less dispersion of RR intervals, both beat-to-beat and in the long term, implying lower HRV.</p>
      <p>In summary, the findings of this study suggest that obese children have autonomic dysfunctions characterized by decreased parasympathetic activity and overall variability. These findings, coupled with the serious problems that can be produced by obesity<sup>36</sup>, reinforce the need for treatment of childhood obesity and in this sense, physical activity and a hypocaloric diet, based on appropriate behaviors, can be powerful tools to reverse the physiological changes caused by obesity. These procedures reduce body weight and leading to reduced sympathetic activity and blood pressure, improving insulin sensitivity, decreasing plasma concentrations of triglycerides and increasing HDL-cholesterol concentrations<sup>37-39</sup>, which may be beneficial to alleviate or eliminate the risks produced by obesity.</p>
      <p>
        <bold>Conclusions</bold>
      </p>
      <p>The results suggest that obese children present changes in the autonomic nervous system, characterized by decreases in parasympathetic activity and overall variability, which demonstrates the need for early attention to these children, to avoid future complications.</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>This study was funded by FAPESP - <italic>Processo FAPESP</italic> No. 2008/05414-0.</p>
      <p>
        <bold>Study Association</bold>
      </p>
      <p>This study is not associated with any post-graduation program.</p>
      <p>
        <bold>References</bold>
      </p>
    </body>
  </sub-article>
  <sub-article article-type="translation" id="TRes" xml:lang="es">
    <front-stub>
      <article-categories/>
      <title-group>
        <article-title xml:lang="es">&#205;ndices geom&#233;tricos de variabilidad de la frecuencia card&#237;aca en ni&#241;os obesos y eutr&#243;ficos</article-title>
      </title-group>
      <abstract xml:lang="es">
        <p>FUNDAMENTO: Obesidad promueve alteraciones en la modulaci&#243;n auton&#243;mica card&#237;aca. OBJETIVO: Investigar la modulaci&#243;n auton&#243;mica de ni&#241;os obesos y eutr&#243;ficos por medio de &#237;ndices de variabilidad de la frecuencia card&#237;aca (VFC) obtenidos por m&#233;todos geom&#233;tricos. M&#201;TODOS: Fueron analizados datos de 133 ni&#241;os, de edad entre 8 y 13 a&#241;os, divididos en dos grupos: obeso (n = 61) y eutr&#243;fico (n = 72), seg&#250;n el &#237;ndice de masa corporal para sexo y edad. Para el an&#225;lisis de la VFC, la frecuencia card&#237;aca fue captada latido-a-latido. Los intervalos RR obtenidos fueron convertidos en figuras geom&#233;tricas y, a partir de ellas, fueron calculados el &#237;ndice triangular (RRtri), interpolaci&#243;n triangular de los intervalos RR (TINN), los &#237;ndices SD1, SD2 y relaci&#243;n SD1/SD2, obtenidos del plot de Poincar&#233;. Fue tambi&#233;n realizado an&#225;lisis visual del plot . Se realizaron el test t de Student para datos no apareados y el test de Mann-Whitney, con nivel de significancia de 5,0%, para an&#225;lisis de los datos. RESULTADOS: En ni&#241;os obesos, fueron observadas reducciones de los &#237;ndices RRtri (0,0730 vs 0,1084 [media]), TINN (171,80 &#177; 55,08 vs 218,26 &#177; 51,12), SD1 (19,93 &#177; 9,10 vs 24,10 &#177; 8,03) y SD2 (51,63 &#177; 16,53 vs 69,78 &#177; 17,19). La relaci&#243;n SD1/SD2 no present&#243; diferencias significativas (0,3781 &#177; 0,12 vs 0,3467 &#177; 0,08). El an&#225;lisis visual del plot, en ni&#241;os obesos, mostr&#243; menor dispersi&#243;n de los intervalos RR tanto latido-a-latido, como a largo plazo, indicando menor VFC. CONCLUSI&#211;N: Ni&#241;os obesos presentaron modificaciones en el sistema nervioso aut&#243;nomo, caracterizadas por reducciones en la actividad parasimp&#225;tica y en la variabilidad global.</p>
      </abstract>
      <kwd-group xml:lang="es">
        <kwd>Frecuencia card&#237;aca</kwd>
        <kwd>ni&#241;o</kwd>
        <kwd>obesidad</kwd>
        <kwd>&#237;ndice de masa corporal</kwd>
        <kwd>sistema nervioso aut&#243;nomo</kwd>
      </kwd-group>
    </front-stub>
    <body>
      <p>
        <bold>ART&#205;CULO ORIGINAL</bold>
      </p>
      <p>
        <bold>&#205;ndices geom&#233;tricos de variabilidad de la frecuencia card&#237;aca en ni&#241;os obesos y eutr&#243;ficos</bold>
      </p>
      <p>
        <bold>Luiz Carlos Marques Vanderlei<sup>I</sup>; Carlos Marcelo Pastre<sup>I</sup>; Ismael Forte Freitas J&#250;nior<sup>II</sup>; Moacir Fernandes de Godoy<sup>III</sup></bold>
      </p>
      <p><sup>I</sup>Faculdade de Ci&#234;ncias e Tecnologia - UNESP - Univ Estadual Paulista, Departamento de Fisioterapia</p>
      <p><sup>II</sup>Faculdade de Ci&#234;ncias e Tecnologia - UNESP - Univ Estadual Paulista, Departamento de Educa&#231;&#227;o F&#237;sica Presidente Prudente, S&#227;o Paulo</p>
      <p><sup>III</sup>Faculdade de Medicina de S&#227;o Jos&#233; do Rio Preto - Departamento de Cardiologia e Cirurgia Cardiovascular, S&#227;o Jos&#233; do Rio Preto, S&#227;o Paulo - Brasil</p>
      <p>
        <xref ref-type="corresp" rid="end-body3">Correspondencia</xref>
      </p>
      <p>
        <bold>RESUMEN</bold>
      </p>
      <p><bold>FUNDAMENTO:</bold> Obesidad promueve alteraciones en la modulaci&#243;n auton&#243;mica card&#237;aca.</p>
      <p><bold>OBJETIVO:</bold> Investigar la modulaci&#243;n auton&#243;mica de ni&#241;os obesos y eutr&#243;ficos por medio de &#237;ndices de variabilidad de la frecuencia card&#237;aca (VFC) obtenidos por m&#233;todos geom&#233;tricos.</p>
      <p><bold>M&#201;TODOS:</bold> Fueron analizados datos de 133 ni&#241;os, de edad entre 8 y 13 a&#241;os, divididos en dos grupos: obeso (n = 61) y eutr&#243;fico (n = 72), seg&#250;n el &#237;ndice de masa corporal para sexo y edad. Para el an&#225;lisis de la VFC, la frecuencia card&#237;aca fue captada latido-a-latido. Los intervalos RR obtenidos fueron convertidos en figuras geom&#233;tricas y, a partir de ellas, fueron calculados el &#237;ndice triangular (RRtri), interpolaci&#243;n triangular de los intervalos RR (TINN), los &#237;ndices SD1, SD2 y relaci&#243;n SD1/SD2, obtenidos del <italic>plot</italic> de Poincar&#233;. Fue tambi&#233;n realizado an&#225;lisis visual del <italic>plot</italic> . Se realizaron el test <italic>t</italic> de <italic>Student</italic> para datos no apareados y el test de Mann-Whitney, con nivel de significancia de 5,0%, para an&#225;lisis de los datos.</p>
      <p><bold>RESULTADOS:</bold> En ni&#241;os obesos, fueron observadas reducciones de los &#237;ndices RRtri (0,0730 <italic>vs</italic> 0,1084 [media]), TINN (171,80 &#177; 55,08 <italic>vs</italic> 218,26 &#177; 51,12), SD1 (19,93 &#177; 9,10 <italic>vs</italic> 24,10 &#177; 8,03) y SD2 (51,63 &#177; 16,53 <italic>vs</italic> 69,78 &#177; 17,19). La relaci&#243;n SD1/SD2 no present&#243; diferencias significativas (0,3781 &#177; 0,12 <italic>vs</italic> 0,3467 &#177; 0,08). El an&#225;lisis visual del <italic>plot</italic>, en ni&#241;os obesos, mostr&#243; menor dispersi&#243;n de los intervalos RR tanto latido-a-latido, como a largo plazo, indicando menor VFC.</p>
      <p><bold>CONCLUSI&#211;N:</bold> Ni&#241;os obesos presentaron modificaciones en el sistema nervioso aut&#243;nomo, caracterizadas por reducciones en la actividad parasimp&#225;tica y en la variabilidad global.</p>
      <p><bold>Palabras clave:</bold> Frecuencia card&#237;aca, ni&#241;o, obesidad, &#237;ndice de masa corporal, sistema nervioso aut&#243;nomo.</p>
      <p>
        <bold>Introducci&#243;n</bold>
      </p>
      <p>Alteraciones en la frecuencia card&#237;aca, definidas como variabilidad de la frecuencia card&#237;aca (VFC), son normales y esperadas e indican la habilidad del coraz&#243;n para responder a los m&#250;ltiples est&#237;mulos fisiol&#243;gicos y ambientales, as&#237; como compensar des&#243;rdenes inducidos por enfermedades<sup>1</sup>.</p>
      <p>Se trata de una medida no invasiva que puede ser utilizada para identificar fen&#243;menos relacionados con el sistema nervioso aut&#243;nomo (SNA)<sup>2</sup>. Entre los m&#233;todos utilizados para an&#225;lisis de la VFC, se encuentran los m&#233;todos geom&#233;tricos - &#237;ndice triangular (RRtri), interpolaci&#243;n triangular de histograma de intervalos NN (TINN) y <italic>plot</italic> de Poincar&#233; - los cuales convierten los intervalos RR en est&#225;ndares geom&#233;tricos y permiten analizar la VFC por medio de las propiedades geom&#233;tricas o gr&#225;ficas del est&#225;ndar resultante<sup>2-4</sup>.</p>
      <p>El RRtri y el TINN son calculados a partir de la construcci&#243;n de un histograma de densidad de los intervalos RR normales, que contienen en el eje x el largo de los intervalos RR, y en el eje y, la frecuencia con que ocurrieron. La uni&#243;n de los puntos de las columnas del histograma forma una figura semejante a un tri&#225;ngulo del cual son extra&#237;dos esos &#237;ndices<sup>2,4,5</sup>.</p>
      <p>El <italic>plot</italic> de Poincar&#233; es una representaci&#243;n gr&#225;fica bidimensional de la correlaci&#243;n entre intervalos RR consecutivos, en que cada intervalo es plotado contra el pr&#243;ximo intervalo<sup>6,7</sup> y su an&#225;lisis puede ser hecho de forma cualitativa, por medio de la evaluaci&#243;n de la figura formada por su atractor, la cual muestra el grado de complejidad de los intervalos RR<sup>8,9</sup>, o cuantitativa, por el ajuste de una elipse a la figura formada por el <italic>plot</italic>, de donde se obtienen los &#237;ndices: SD1, SD2 y la raz&#243;n SD1/SD2<sup>10,11</sup>. Adem&#225;s de eso, el an&#225;lisis del <italic>plot</italic> de Poincar&#233; es considerado por algunos autores como basado en la din&#225;mica no lineal<sup>7,12</sup>.</p>
      <p>El an&#225;lisis de la VFC por m&#233;todos no lineales viene ganando creciente inter&#233;s, pues existen evidencias de que los mecanismos envueltos en la regulaci&#243;n cardiovascular probablemente interact&#250;en entre s&#237; de modo no lineal<sup>13</sup>.</p>
      <p>Esos m&#233;todos describen las fluctuaciones complejas del ritmo y consiguen separar estructuras de comportamiento no lineal en las series temporales de latidos card&#237;acos m&#225;s adecuadamente que los m&#233;todos lineales<sup>14</sup>. SE ha especulado que el an&#225;lisis de VFC basado en m&#233;todos de la din&#225;mica no lineal puede proveer valiosas informaciones para interpretaciones fisiol&#243;gicas de la VFC y para evaluaci&#243;n del riesgo de muerte s&#250;bita<sup>7</sup>, adem&#225;s de posibilitar mejor entendimiento de la naturaleza de sistemas din&#225;micos y complejos que ocurren en el cuerpo humano, tanto en la salud como en la enfermedad<sup>15</sup>.</p>
      <p>Estudios han demostrado que la obesidad produce alteraciones en la funci&#243;n del sistema nervioso aut&#243;nomo en ni&#241;os y adolescentes<sup>16,17</sup>. Tal condici&#243;n de desequilibrio puede representar un factor negativo importante, ya que el funcionamiento auton&#243;mico controla parte de las funciones internas del cuerpo y, en ese sentido, merece atenci&#243;n.</p>
      <p>Los trabajos referidos a obesidad en ni&#241;os y el an&#225;lisis del SNA, por medio de la evaluaci&#243;n de la VFC, han presentado resultados controvertidos. Sekine et al<sup>18</sup>, analizando &#237;ndices de VFC en el dominio de la frecuencia, sugieren que tienen mayor actividad simp&#225;tica y menor actividad parasimp&#225;tica cuando es comparado con ni&#241;os eutr&#243;ficos, mientras que Nagai et al<sup>19</sup> y Nagai y Moritani<sup>20</sup> observaron actividades tanto simp&#225;tica cuanto parasimp&#225;tica disminuidas en ni&#241;os obesos. Ya Yakinci et al<sup>21</sup>, utilizando tests auton&#243;micos funcionales, observaron actividad simp&#225;tica normal e hipo actividad parasimp&#225;tica, y, m&#225;s recientemente, Kaufman et al<sup>16</sup> observaron aumento de la relaci&#243;n LF/HF y disminuci&#243;n del &#237;ndice HF. Pascoal et al<sup>22</sup> constataron mayor tono card&#237;aco en la posici&#243;n b&#237;peda cuando son comparados ni&#241;os obesos con ni&#241;os eutr&#243;ficos.</p>
      <p>Esos trabajos eval&#250;an la VFC utilizando m&#233;todos lineales, mientras, se destaca que, despu&#233;s de b&#250;squeda sistem&#225;tica en bases de datos pertinentes apuntando a la elaboraci&#243;n de este manuscrito, no fueron encontrados trabajos que utilicen m&#233;todos geom&#233;tricos como forma de an&#225;lisis.</p>
      <p>Siendo as&#237;, con el prop&#243;sito de acrecentar elementos relacionados al tema expuesto en la literatura, se pretende con este trabajo, investigar la modulaci&#243;n auton&#243;mica de ni&#241;os obesos t eutr&#243;ficos por medio de &#237;ndices de VFC obtenidos a trav&#233;s de m&#233;todos geom&#233;tricos.</p>
      <p>
        <bold>M&#233;todos</bold>
      </p>
      <p>
        <bold>Poblaci&#243;n</bold>
      </p>
      <p>Para la realizaci&#243;n de este trabajo, fueron analizados datos de 133 ni&#241;os, independientemente de sexo, en una franja etaria entre 8 y 13 a&#241;os. Los ni&#241;os fueron divididos en dos grupos seg&#250;n el estado nutricional: obesos y eutr&#243;ficos. La obesidad fue definida seg&#250;n los criterios establecidos para edad y sexo por Cole et al<sup>23</sup>.</p>
      <p>El grupo obeso fue constituido por 61 ni&#241;os, 28 del sexo masculino (45,90%) y 33 del sexo femenino (54,10%), mientras que el grupo eutr&#243;fico fue formado por 72 ni&#241;os (35 del sexo masculino [48,60%] y 37 del sexo femenino [51,40%]). Las caracter&#237;sticas de estos ni&#241;os (edad, peso, altura e &#237;ndice de masa corp&#243;rea) pueden ser vistos en la <xref ref-type="table" rid="tab1-body3">Tabla 1</xref>.</p>
      <table-wrap id="tab1-body3">
        <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gt01-es.jpg"/></table-wrap>
      <p>No fueron incluidos en este estudio, ni&#241;os con relato de por lo menos una de las siguientes caracter&#237;sticas: uso de medicamentos que influyesen en la actividad auton&#243;mica del coraz&#243;n, como por ejemplo, propranolol y atropina, infecciones, enfermedades metab&#243;licas o del sistema cardiorrespiratorio conocidas.</p>
      <p>Los voluntarios y sus responsables fueron debidamente informados sobre los procedimientos y objetivos de este estudio, y despu&#233;s de concordar, el responsable firm&#243; un t&#233;rmino de consentimiento libre y aclarado. Todos los procedimientos utilizados fueron aprobados por el Comit&#233; de &#201;tica en Investigaci&#243;n de la Facultad de Ciencias y Tecnolog&#237;a - FCT/UNESP (Proc. n&#186; 187/2007).</p>
      <p>
        <bold>Protocolo experimental</bold>
      </p>
      <p>Antes del comienzo del procedimiento experimental, los ni&#241;os fueron identificados recogiendo las siguientes informaciones: edad, sexo, peso, altura e &#237;ndice de masa corporal. Las medidas antropom&#233;tricas fueron obtenidas de acuerdo con las recomendaciones descriptas por Lohman et al<sup>24</sup>.</p>
      <p>El peso fue medido en una balanza digital (Filizzola PL 150, Filizzola Ltda., Brasil) con precisi&#243;n de 0,1 kg, con los ni&#241;os usando ropas livianas y sin zapatos. La altura fue medida usando un estadi&#243;metro con precisi&#243;n de 0,1 cm y 2 metros de largo. El IMC fue calculado usando la siguiente f&#243;rmula: peso (kg)/altura (m)<sup>2</sup>.</p>
      <p>La recolecci&#243;n de datos fue realizada en una sala con temperatura entre 21&#186;C y 23&#186; C y humedad entre 40 y 60%. Despu&#233;s de la evaluaci&#243;n inicial, fueron explicados todos los procedimientos necesarios para la realizaci&#243;n de la recolecci&#243;n de datos, que fue realizada de forma individual. Los ni&#241;os fueron orientados a mantenerse en reposo, evitando conversar durante la recolecci&#243;n.</p>
      <p>Despu&#233;s de tales procedimientos, fue colocada en el t&#243;rax de los ni&#241;os, al nivel del tercio distal del estern&#243;n, la cinta de captaci&#243;n y, en su mu&#241;eca, el receptor de frecuencia card&#237;aca Polar S810i (Polar Electro, Finlandia), equipamiento previamente validado para captaci&#243;n de la frecuencia card&#237;aca latido-a-latido y la utilizaci&#243;n de sus datos para an&#225;lisis de la VFC en ni&#241;os y adultos<sup>25,26</sup>.</p>
      <p>Despu&#233;s de la colocaci&#243;n de la cinta y del monitor, los ni&#241;os fueron colocados en dec&#250;bito dorsal en una colchoneta y permanecieron en reposo y con respiraci&#243;n espont&#225;nea 20 minutos. Despu&#233;s de ese per&#237;odo de recolecci&#243;n, los ni&#241;os fueron liberados.</p>
      <p>Para an&#225;lisis de la VFC, el est&#225;ndar de su comportamiento fue registrado latido-a-latido, durante todo el protocolo experimental, con una tasa de muestreo de 1.000 Hz. Para an&#225;lisis de los datos, fueron utilizados 1.000 intervalos RR consecutivos, despu&#233;s de haber sido hecho un filtrado digital, complementado por manual, para eliminaci&#243;n de latidos ect&#243;picos prematuros y artefactos, y solamente series con m&#225;s de 95,0% de latidos sinusales fueron incluidas en el estudio<sup>27</sup>.</p>
      <p>
        <bold>An&#225;lisis de los &#237;ndices de variabilidad de la frecuencia card&#237;aca</bold>
      </p>
      <p>El an&#225;lisis de la VFC fue realizado por medio de los m&#233;todos geom&#233;tricos: RRtri, TINN y <italic>plot</italic> de Poincar&#233; (SD1, SD2, relaci&#243;n SD1/SD2). </p>
      <p>El RRtri fue calculado a partir de la construcci&#243;n de un histograma de densidad de los intervalos RR, el cual contiene en el eje horizontal todos los posibles valores de los intervalos RR medidos, en una escala discreta con cajas de 7,8125 ms (1/128 segundos) y, en el eje vertical, la frecuencia con que ocurri&#243; cada uno de ellos. La uni&#243;n de los puntos de las columnas del histograma forma una figura semejante a un tri&#225;ngulo. El RRtri fue obtenido dividiendo el n&#250;mero total de intervalos RR utilizados para la construcci&#243;n del histograma por la frecuencia modal de los mismos (valor del intervalo RR que m&#225;s apareci&#243; en la serie RR)<sup>2</sup>.</p>
      <p>El TINN consiste en la medida de la base de un tri&#225;ngulo, siendo utilizado el m&#233;todo de la diferencia de los m&#237;nimos cuadrados para la determinaci&#243;n del tri&#225;ngulo<sup>2</sup>. El RRtri y el TINN expresan la variabilidad global de los intervalos RR<sup>2</sup>.</p>
      <p>El <italic>plot</italic> de Poincar&#233; es un mapa de puntos en coordenadas cartesianas, construido a partir de los valores de los intervalos RR obtenidos, donde cada punto es representado en el eje <italic>x</italic> (horizontal/abcisa) por el intervalo RR normal precedente y, en el eje <italic>y</italic> (vertical/ordenada), por el intervalo RR siguiente.</p>
      <p>Para an&#225;lisis cuantitativo del <italic>plot</italic>, fue ajustada una elipse a los puntos del gr&#225;fico, con centro determinado por la media de los intervalos RR, y fueron calculados los &#237;ndices SD1, que mide el desv&#237;o-est&#225;ndar de las distancias de los puntos a la diagonal <italic>y</italic> = <italic>x</italic>, y SD2 que mide el desv&#237;o-est&#225;ndar de las distancias de los puntos a la recta <italic>y</italic> = -<italic>x</italic> + <italic>RRm</italic>, donde <italic>RRm</italic> es la media de los intervalos RR. El SD1 es un &#237;ndice de registro instant&#225;neo de la variabilidad latido-a-latido y representa la actividad parasimp&#225;tica, mientras que el &#237;ndice SD2 representa la VFC, en registros de larga duraci&#243;n, y refleja la variabilidad global. La relaci&#243;n de ambos (SD1/SD2) muestra la raz&#243;n entre las variaciones corta y larga de los intervalos RR<sup>1,11</sup>.</p>
      <p>El an&#225;lisis cualitativo del <italic>plot</italic> fue hecho por medio del an&#225;lisis de las figuras formadas por su atractor, las cuales fueron descriptas por Tulppo et al<sup>28</sup> en:</p>
      <p>Figura en la cual un aumento en la dispersi&#243;n de los intervalos RR es observado con aumento en los intervalos, caracter&#237;stica de un <italic>plot</italic> normal.</p>
      <p>Figura con peque&#241;a dispersi&#243;n global latido-a-latido y sin aumento de la dispersi&#243;n de los intervalos RR, a largo plazo.</p>
      <p>El <italic>software</italic> HRV analysis - Versi&#243;n 2.0 fue utilizado para el c&#225;lculo de esos &#237;ndices<sup>29</sup>.</p>
      <p>
        <bold>Tratamiento estad&#237;stico</bold>
      </p>
      <p>Para comparaci&#243;n de los grupos, inicialmente fue determinada la normalidad de los datos por medio del test Shapiro-Wilks. Cuando la distribuci&#243;n normal fue aceptada, el test <italic>t</italic> de <italic>Student</italic> para datos no apareados fue aplicado (edad, altura, TINN, SD1, SD2 y relaci&#243;n SD1/SD2) y en las situaciones donde la distribuci&#243;n normal no fue aceptada, fue aplicado el test de Mann-Whitney (peso, IMC, RRTri). Diferencias en esos tests fueron consideradas estad&#237;sticamente significativas cuando el valor de "P" fue menor o igual a 0,05.</p>
      <p>
        <bold>Resultados</bold>
      </p>
      <p>La <xref ref-type="table" rid="tab2-body3">Tabla 2</xref> muestra los valores obtenidos para los &#237;ndices RRtri, TINN, SD1, SD2 y relaci&#243;n SD1/SD2 de los grupos obeso y eutr&#243;fico. Se observan valores significativamente menores para el grupo obeso en comparaci&#243;n al grupo eutr&#243;fico, excepto para la relaci&#243;n SD1/SD2 que no present&#243; diferencia estad&#237;sticamente significativa entre los grupos.</p>
      <table-wrap id="tab2-body3">
        <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gt02-es.jpg"/></table-wrap>
      <p>Las <xref ref-type="fig" rid="es_a06fig01-body3">Figuras 1</xref> y <xref ref-type="fig" rid="es_a06fig02-body3">2</xref> muestran ejemplos est&#225;ndares del <italic>plot</italic> de Poincar&#233; para ni&#241;os obesos y controles.</p>
      <p content-type="asset">
        <fig id="es_a06fig01-body3">
          <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gf01-es.jpg"/></fig>
      </p>
      <p content-type="asset">
        <fig id="es_a06fig02-body3">
          <graphic xlink:href="1678-4170-abc-95-01-0035-00082-gf02-es.jpg"/></fig>
      </p>
      <p>
        <bold>Discusi&#243;n</bold>
      </p>
      <p>Los resultados obtenidos por medio de los &#237;ndices de VFC, en el presente estudio, mostraron que en los ni&#241;os obesos analizados ocurrieron reducciones de los &#237;ndices geom&#233;tricos, sugiriendo que, en estos ni&#241;os, la variabilidad de la frecuencia card&#237;aca est&#225; reducida.</p>
      <p>El &#237;ndice SD1, que representa el eje transverso del <italic>plot</italic> de Poincar&#233;, muestra el desv&#237;o-est&#225;ndar de la variabilidad instant&#225;nea de la frecuencia card&#237;aca latido-a-latido<sup>11</sup> e indica la influencia parasimp&#225;tica sobre el n&#243;dulo sinoatrial<sup>10</sup>. Los menores valores del &#237;ndice SD1 en ni&#241;os obesos sugieren que, en estos ni&#241;os, la actividad parasimp&#225;tica est&#225; reducida.</p>
      <p>Actividad parasimp&#225;tica disminuida en ni&#241;os obesos fue tambi&#233;n relatada por otros autores<sup>16,19,21</sup>. Tal reducci&#243;n est&#225; asociada al aumento del riesgo para morbilidad y mortalidad por todas las causas y al desarrollo de varios factores de riesgo<sup>30</sup>.</p>
      <p>Martini et al<sup>31</sup> observaron que ni&#241;os obesos tienen mayores valores de presi&#243;n arterial, de glucosa sangu&#237;nea, de insulina y de niveles de triglic&#233;ridos, y menores valores de lipoprote&#237;na de alta densidad (HDL), cuando es comparada con ni&#241;os no obesos. Paschoal et al<sup>22</sup> tambi&#233;n relataron menores valores de HDL y aumento de triglic&#233;ridos en ni&#241;os obesos. La presencia de tales caracter&#237;sticas en ni&#241;os portadores de obesidad puede estar asociada a alteraciones en la actividad del SNA seg&#250;n afirma Sekine et al<sup>18</sup>.</p>
      <p>Los &#237;ndices SD2, TINN y RRtri tambi&#233;n presentaron reducci&#243;n en los ni&#241;os obesos en comparaci&#243;n con los ni&#241;os del grupo eutr&#243;fico. Esos &#237;ndices expresan la variabilidad global de los intervalos RR<sup>2,11</sup>, lo que sugiere que ni&#241;os obesos presentan reducci&#243;n de la variabilidad global de la frecuencia card&#237;aca.</p>
      <p>Sekine et al<sup>18</sup> y Martini et al<sup>31</sup>, evaluando la variabilidad global en ni&#241;os obesos por medio del &#237;ndice SDNN (desv&#237;o-est&#225;ndar de los intervalos RR), no encontraron diferencias estad&#237;sticamente significativas en este &#237;ndice, con todo los valores se presentaron menores en estos ni&#241;os, en comparaci&#243;n con los no obesos. Reducci&#243;n significativa de ese &#237;ndice fue relatada por Rabbia et al<sup>32</sup> en adolescentes obesos (edad de 13,9 &#177; 1,7 a&#241;os).</p>
      <p>Fue descripta en la literatura una reducci&#243;n en la actividad simp&#225;tica en ni&#241;os obesos<sup>19,20</sup>. Este sistema participa del control del metabolismo de la glucosa y de la grasa<sup>33</sup> y menor actividad simp&#225;tica fue asociada a menor gasto energ&#233;tico y, consecuentemente, un balance energ&#233;tico positivo y aumento de peso<sup>34</sup>.</p>
      <p>En cuanto a la relaci&#243;n SD1/SD2, los an&#225;lisis mostraron que no ocurrieron diferencias significativas de ese &#237;ndice cuando fue comparado el grupo obeso con el grupo eutr&#243;fico, lo que puede ser justificado por la reducci&#243;n observada tanto en el &#237;ndice SD1 como en el SD2, en ni&#241;os obesos.</p>
      <p>El an&#225;lisis visual del <italic>plot</italic> de Poincar&#233; mostr&#243; en los ni&#241;os eutr&#243;ficos una mayor dispersi&#243;n latido-a-latido de los intervalos RR, as&#237; como mayor dispersi&#243;n de los intervalos RR a largo plazo, en comparaci&#243;n con los ni&#241;os obesos, indicando que estos ni&#241;os poseen mayor VFC.</p>
      <p>En individuos saludables, en reposo, los intervalos entre los latidos card&#237;acos son bastante irregulares, sobre todo por el predominio vagal en la modulaci&#243;n card&#237;aca, haciendo que se visualice, en el plot de Poincar&#233;, una nube de puntos con la forma aproximada de una elipse<sup>28,35</sup>, lo que puede ser observado en los ni&#241;os eutr&#243;ficos.</p>
      <p>A diferencia de lo que fue observado en los ni&#241;os eutr&#243;ficos, los an&#225;lisis de las figuras del <italic>plot</italic> de los ni&#241;os obesos mostraron menor dispersi&#243;n de los intervalos RR, tanto latido-a-latido como a largo plazo, indicando menor VFC.</p>
      <p>En resumen, los resultados de este trabajo sugieren que ni&#241;os obesos presentan disfunciones auton&#243;micas, caracterizadas por reducciones en la actividad parasimp&#225;tica y de la variabilidad global. Tales hallazgos, asociados a los graves problemas que pueden ser producidos por la obesidad<sup>36</sup>, refuerzan la necesidad de tratamiento de la obesidad infantil y, en este sentido, la actividad f&#237;sica y una dieta hipocal&#243;rica, fundamentadas en conductas apropiadas, pueden ser herramientas eficientes para revertir las alteraciones fisiol&#243;gicas provocadas por la obesidad. Esos procedimientos, adem&#225;s de reducir el peso corporal, llevan a la disminuci&#243;n de la actividad simp&#225;tica y de la presi&#243;n arterial, mejoran la sensibilidad a la insulina, disminuyen las concentraciones plasm&#225;ticas de triglic&#233;ridos y aumentan las de HDL-colesterol<sup>37-39</sup>, aspectos que pueden ser ben&#233;ficos para aliviar o eliminar los riesgos producidos por la obesidad.</p>
      <p>
        <bold>Conclusiones</bold>
      </p>
      <p>Los resultados sugieren que ni&#241;os obesos presentan modificaciones en el sistema nervioso aut&#243;nomo, caracterizadas por reducciones en la actividad parasimp&#225;tica y en la variabilidad global, lo que demuestra la necesidad de atenci&#243;n precoz a estos ni&#241;os, para evitar complicaciones futuras.</p>
      <p>
        <bold>Potencial Conflicto de Intereses</bold>
      </p>
      <p>Declaro no haber conflicto de intereses pertinentes.</p>
      <p>
        <bold>Fuentes de Financiaci&#243;n</bold>
      </p>
      <p>El presente estudio fue financiado por la <italic>Funda&#231;&#227;o de Amparo &#224; Pesquisa do Estado de S&#227;o Paulo</italic> - Proceso FAPESP n&#186; 2008/05414-0.</p>
      <p>
        <bold>Vinculaci&#243;n Acad&#233;mica</bold>
      </p>
      <p>No hay vinculaci&#243;n de este estudio con programas de post-grado.</p>
      <p>
        <bold>Referencias</bold>
      </p>
      <p>1. Vanderlei LCM, Pastre CM, Hoshi RA, Carvalho TD, Godoy MF. No&#231;&#245;es b&#225;sicas de variabilidade da frequ&#234;ncia card&#237;aca e sua aplicabilidade cl&#237;nica. Rev Bras Cir Cardiovasc. 2009; 24 (2): 205-17.</p>
      <p>2. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation. 1996; 93 (5): 1043-65.</p>
      <p>3. Majercak I. The use of heart variability in cardiology. Bratisl Lek Listy. 2002; 103 (10): 368-77.</p>
      <p>4. Rajendra Acharya U, Paul Joseph K, Kannathal N, Lim CM, Suri JS. Heart rate variability: a review. Med Biol Eng Comput. 2006; 44 (12): 1031-51.</p>
      <p>5. Rocha RM, Albuquerque DC, Albanesi Filho FM. Variabilidade da frequ&#234;ncia card&#237;aca e ritmo circadiano em pacientes com angina est&#225;vel. Rev SOCERJ. 2005; 18 (4): 429-42.</p>
      <p>6. Lerma C, Infante O, P&#233;rez-Grovas H, Jos&#233; MV. Poincar&#233; plot indexes of heart rate variability capture dynamic adaptations after haemodialysis in chronic renal failure patients. Clin Physiol Funct Imaging. 2003; 23 (2): 72-80.</p>
      <p>7. Khaled AS, Owis MI, Mohamed ASA. Employing time-domain methods and poincar&#233; plot of heart rate variability signals to detect congestive heart failure. BIME Journal. 2006; 6 (1): 35-41.</p>
      <p>8. Woo MA, Stevenson WG, Moser DK, Trelease RB, Harper RM. Patterns of beat to beat heart rate variability in advanced heart failure. Am Heart J. 1992; 123: 704-10.</p>
      <p>9. Vito GD, Galloway SDR, Nimmo MA, Maas P, McMurray JJV. Effects of central sympathetic inhibition on heart rate variability during steady-state exercise in healthy humans. Clin Physiol Funct Imaging. 2002; 22: 32-8.</p>
      <p>10. Tulppo MP, Makikallio TH, Takala TES, Seppanen T, Huikuri HV. Quantitative beat-to-beat analysis of heart rate dynamics during exercise. Am J Physiol (Circ Physiol). 1996; 271 (7): H244-H252.</p>
      <p>11. Brunetto AF, Silva BM, Roseguini BT, Hirai DM, Guedes DP. Limiar ventilat&#243;rio e variabilidade da frequ&#234;ncia card&#237;aca em adolescentes. Rev Bras Med Esporte. 2005; 11 (1): 22-7.</p>
      <p>12. Voss A, Schroeder R, Truebner S, Goernig M, Figulla HR, Schirdewan A. Comparison of nonlinear methods symbolic dynamics, detrended fluctuation, and Poincar&#233; plot analysis in risk stratification in patients with dilated cardiomyopathy. Chaos. 2007; 17 (1): 015120.</p>
      <p>13. Huikuri HV, Makikallio TH, Perkiomaki J. Measurement of heart rate variability by methods based on nonlinear dynamics. J Electrocardiol. 2003; 36 9 (Suppl): 95-9.</p>
      <p>14. Voss A, Kurths J, Kleiner HJ, Witt A, Wessel N, Saparin P, et al. The application of methods of non-linear dynamics for the improved and predictive recognition of patients threatened by sudden cardiac death. Cardiovasc Res. 1996; 31: 419-33.</p>
      <p>15. Higgins JP. Nonlinear systems in medicine. Yale J Biol Med. 2002; 75 (5-6): 247-60.</p>
      <p>16. Kaufman CL, Kaiser DR, Steinberger J, Kelly AS, Dengel DR. Relationships of cardiac autonomic function with metabolic abnormalities in childhood obesity. Obesity. 2007; 15 (5): 1164-71.</p>
      <p>17. Tonhajzerova I, Javorka M, Trunkvalterova Z, Chroma O, Javorkova J, Lazarova Z, et al. Cardio-respiratory interaction and autonomic dysfunction in obesity. J Physiol Pharmac. 2008: 59 (Suppl 6): 709-18.</p>
      <p>18. Sekine M, Izumi I, Yamagami T, Kagamimori S. Obesity and cardiac autonomic nerve activity in healthy children: results of the Toyama Birth Cohort Study. Environm Health Prev Med. 2001; 6: 149-53.</p>
      <p>19. Nagai N, Matsumoto T, Kita H, Moritani T. Autonomic nervous system activity and the state and development of obesity in japanese school children. Obes Res. 2003; 11: 25-32.</p>
      <p>20. Nagai N, Moritani T. Effect of physical activity on autonomic nervous system function in lean and obese children. Int J Obesity. 2004; 28: 27-33.</p>
      <p>21. Yakinci C, Mungen B, Karabiber H, Tayfun M, Evereklioglu C. Autonomic nervous system functions in obese children. Brain Dev. 2000; 22: 151-3.</p>
      <p>22. Paschoal MA, Trevizan PF, Scodeler NF. Variabilidade da frequ&#234;ncia card&#237;aca, l&#237;pides e capacidade f&#237;sica de crian&#231;as obesas e n&#227;o-obesas. Arq Bras Cardiol. 2009; 93 (3): 239-46.</p>
      <p>23. Cole TM, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ. 2000; 320 (6): 1-6.</p>
      <p>24. Lohman TG, Roche AF, Martorell R. Anthropometric standardization reference manual. Champaign: Human Kinetics Books; 1988.</p>
      <p>25. Gamelin FX, Baquet G, Berthoin S, Bosquet L. Validity of the polar S810 to measure R-R intervals in children. Int J Sports Med. 2008; 29: 134-8.</p>
      <p>26. Vanderlei LCM, Silva RA, Pastre CM, Azevedo FM, Godoy MF. Comparison of the Polar S810i monitor and the ECG for the analysis of heart rate variability in the time and frequency domains. Braz J Med Biol Res. 2008; 41 (10): 854-9.</p>
      <p>27. Godoy MF, Takakura IT, Correa PR. Relev&#226;ncia da an&#225;lise do comportamento din&#226;mico n&#227;o-linear (Teoria do Caos) como elemento progn&#243;stico de morbidade e mortalidade em pacientes submetidos &#224; cirurgia de revasculariza&#231;&#227;o mioc&#225;rdica. Arq Cienc Sa&#250;de. 2005; 12 (4): 167-71.</p>
      <p>28. Tulppo MP, M&#228;kikallio TH, Sepp&#228;nen T, Laukkanen RT, Huikuri HV. Vagal modulation of heart rate during exercise: effects of age and physical fitness. Am J Physiol. 1998; 274 (2Pt 2): H424-9.</p>
      <p>29. Niskanen JP, Tarvainen MP, Ranta-aho PO, Karjalainen PA. Software for advanced HRV analysis. Comp Meth Progr Biomed. 2004; 76: 73-81.</p>
      <p>30. Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol. 2007; 74: 224-42.</p>
      <p>31. Martini G, Riva P, Rabbia F, Molini V, Ferrero GB, Cerutti F, et al Heart rate variability in childhood obesity. Clin Auton Res. 2001; 11 (2): 87-91.</p>
      <p>32. Rabbia F, Silke B, Conterno A, Grosso T, De Vito B, Rabbone I, et al. Assessment of cardiac autonomic modulation during adolescent obesity. Obes Res. 2003; 11 (4): 541-8.</p>
      <p>33. Nonogaki K. New insight into sympathetic regulation of glucose and fat metabolism. Diabetologia. 2000; 43: 533-49.</p>
      <p>34. Peterson HR, Rothschild M, Weinberg CR, Fell RD, McLeish KR, Pfeifer MA. Body fat and the activity of the autonomic nervous system. N Engl J Med. 1988; 318: 1077-83.</p>
      <p>35. Mourot L, Bouhaddi M, Perrey S, Rouillon JD, Regnard J. Quantitative Poincar&#233; plot analysis of heart rate: effect of endurance training. Eur J Appl Physiol. 2004; 91 (1): 79-87.</p>
      <p>36. Daniels SR. Complications of obesity in children and adolescents. Int J Obes. 2009; 33 (Suppl 1): S60-S65.</p>
      <p>37. Ribeiro MM, Silva AG, Santos NS, Guazzelle I, Matos LNJ, Trombetta IC, et al. Diet and exercise training restore blood pressure and vasodilatory responses during physiological maneuvers in obese children. Circulation. 2005; 111 (15): 1915-23.</p>
      <p>38. Carnethon MR, Craft LL. Autonomic association between exercise and diabetes: autonomic nervous system function. Exerc Sport Sci Rev. 2008; 36 (1): 12-8.</p>
      <p>39. Sichieri R, Souza RA. Estrat&#233;gias para preven&#231;&#227;o da obesidade em crian&#231;as e adolescentes. Cad Sa&#250;de P&#250;blica. 2008; 24(supl. 2): S209-S234.</p>
      <p>
        <fn id="end-body3" fn-type="corresp">
          <label>
            <bold>Correspondencia:</bold>
          </label>
          <p> Luiz Carlos Marques Vanderlei</p>
          <p> Departamento de Fisioterapia</p>
          <p> Rua Roberto Simonsen, 305</p>
          <p> 19060-900 - Presidente Prudente, SP - Brasil</p>
          <p> E-mail: </p>
          <p>
            <email xlink:href="lcmvanderlei@fct.unesp.br">lcmvanderlei@fct.unesp.br</email>
          </p>
        </fn>
      </p>
      <p>Art&#237;culo recibido el 16/09/09; revisado recibido el 12/11/09; aceptado el 29/12/09.</p>
    </body>
  </sub-article>
</article>
