Hemodynamic and ventilatory response to different levels of hypoxia and hypercapnia in carotid body-denervated rats

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The figure shows myeloperoxidase (MPO) activity in mice not subjected to MCAo (Sham) or subjected to MCAo with pre-administration of vehicle (Vehicle) or reparixin (30 mg/kg, s.c.) 60 minutes before MCAo procedures. The results are expressed as the means ± SEM (n = 6). * p<0.05 compared to Sham group. # p<0.05 compared to vehicle. (ANOVA followed by Newman-Keuls posthoc test)." ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Larissa Fonseca da Cunha Sousa, Fernanda Matos Coelho, David Henrique Rodrigues, Alline Cristina Campos, Lucíola da Silva Barcelos, Mauro Martins Teixeira, Milene Alvarenga Rachid, Antonio Lúcio Teixeira" "autores" => array:8 [ 0 => array:2 [ "nombre" => "Larissa Fonseca" "apellidos" => "da Cunha Sousa" ] 1 => array:2 [ "nombre" => "Fernanda Matos" "apellidos" => "Coelho" ] 2 => array:2 [ "nombre" => "David Henrique" "apellidos" => "Rodrigues" ] 3 => array:2 [ "nombre" => "Alline Cristina" "apellidos" => "Campos" ] 4 => array:2 [ "nombre" => "Lucíola" "apellidos" => "da Silva Barcelos" ] 5 => array:2 [ "nombre" => "Mauro Martins" "apellidos" => "Teixeira" ] 6 => array:2 [ "nombre" => "Milene" "apellidos" => "Alvarenga Rachid" ] 7 => array:2 [ "nombre" => "Antonio Lúcio" "apellidos" => "Teixeira" ] ] ] ] ] "idiomaDefecto" => "en" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1807593222020798?idApp=UINPBA00004N" "url" => "/18075932/0000006800000003/v1_202212011730/S1807593222020798/v1_202212011730/en/main.assets" ] "en" => array:20 [ "idiomaDefecto" => true "cabecera" => "BASIC RESEARCH" "titulo" => "Hemodynamic and ventilatory response to different levels of hypoxia and hypercapnia in carotid body-denervated rats" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "395" "paginaFinal" => "399" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "João Paulo J. Sabino, Mauro de Oliveira, Humberto Giusti, Mogens Lesner Glass, Helio C. Salgado, Rubens Fazan" "autores" => array:6 [ 0 => array:2 [ "nombre" => "João Paulo J." "apellidos" => "Sabino" ] 1 => array:2 [ "nombre" => "Mauro" "apellidos" => "de Oliveira" ] 2 => array:2 [ "nombre" => "Humberto" "apellidos" => "Giusti" ] 3 => array:2 [ "nombre" => "Mogens Lesner" "apellidos" => "Glass" ] 4 => array:2 [ "nombre" => "Helio C." "apellidos" => "Salgado" ] 5 => array:5 [ "nombre" => "Rubens" "apellidos" => "Fazan" "sufijo" => "Jr" "email" => array:1 [ 0 => "rfazan@usp.br" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "*" "identificador" => "cor1" ] ] ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Universidade de São Paulo, School of Medicine of Ribeirão Preto, Department of Physiology, São Paulo/SP, Brazil" "identificador" => "aff1" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor1" "etiqueta" => "*" "correspondencia" => "Tel.: 55 16 3602-3331" ] ] ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig1" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "cln-68-03-395-g001.jpeg" "Alto" => 1107 "Ancho" => 792 "Tamanyo" => 32219 ] ] "descripcion" => array:1 [ "en" => "Bar graph showing the changes in the mean arterial pressure (MAP) and heart rate (HR) in response to KCN in intact and carotid body-denervated (CBD) rats. *p<0.05 compared to intact rats." ] ] ] "textoCompleto" => "INTRODUCTIONPeripheral arterial chemoreceptors consist of aortic bodies situated in the aortic arch and carotid bifurcations (<a class="elsevierStyleCrossRef" href="#bib1">1</a>), while central chemoreceptors are located on the ventral surface of the medulla (<a class="elsevierStyleCrossRef" href="#bib2">2</a>). The chemoreceptors play an important role in the regulation of ventilation and circulation in response to changes in arterial O2 and/or CO2 (<a class="elsevierStyleCrossRefs" href="#bib2">2-4</a>).It has been well established that activation of the chemoreceptors under hypoxia or hypercapnia elicits an increase in pulmonary ventilation (PV) (<a class="elsevierStyleCrossRefs" href="#bib5">5-8</a>). Nevertheless, studies in rats have shown conflicting hemodynamic responses to hypoxia. While some studies have demonstrated that hypoxia elicits a decrease in the mean arterial pressure (MAP) combined with an increase in heart rate (HR) (<a class="elsevierStyleCrossRefs" href="#bib9">9-15</a>), others have shown an increase in MAP combined with a decrease in HR (<a class="elsevierStyleCrossRef" href="#bib16">16</a>,<a class="elsevierStyleCrossRef" href="#bib17">17</a>).In contrast, while there is general agreement that hypercapnia promotes a hypertensive response (<a class="elsevierStyleCrossRefs" href="#bib18">18-21</a>), there is no agreement concerning the HR response to hypercapnia. Studies have reported that bradycardia (<a class="elsevierStyleCrossRef" href="#bib22">22</a>,<a class="elsevierStyleCrossRef" href="#bib23">23</a>) or tachycardia (<a class="elsevierStyleCrossRef" href="#bib18">18</a>) was elicited by hypercapnia.Accordingly, the evident disagreement in the literature concerning the hemodynamic and ventilatory responses to hypoxia and hypercapnia requires further investigation and characterization of the role of the peripheral carotid chemoreceptors in these responses. Therefore, this study aimed to evaluate the hemodynamic and ventilatory responses to different levels of hypoxia and hypercapnia in conscious intact or carotid body-denervated (CBD) rats.MATERIALS AND METHODSExperiments were performed on male Wistar rats (270-300 g) housed individually with free access to food and water and maintained on a 12:12-h light-dark cycle. All experimental procedures were performed in accordance with the Guide for the Care and Use of Laboratory Animals [Dept. of Health, Education and Welfare, Publication No. (NIH) 85-23, Revised 1985. Office of Science and Health Reports, DRR/NIH, Bethesda, MD]. The experimental protocols used in this research were approved by the Committee of Ethics in Animal Research of the School of Medicine of Ribeirão Preto, University of São Paulo (protocol 053/2010).Two days before the experiments, the rats were anesthetized with tribromoethanol (250 mg.kg-1, i.p., Sigma, St. Louis, MO, USA), and bilateral ligature of the carotid body arteries was performed as described elsewhere (<a class="elsevierStyleCrossRef" href="#bib24">24</a>). Briefly, the carotid artery bifurcations were identified and isolated bilaterally. Then, the carotid body arteries were identified and tightly ligated with a suture line to block the arterial supply to the carotid bodies. The procedure was similar for rats that received the sham operation (intact), except that they did not undergo the ligature. After artery ligation, polyethylene catheters were inserted into the left femoral artery and vein for the direct measurement of arterial pressure (AP) and administration of potassium cyanide (KCN, 160 μg.kg-1, Merck, Darmstadt, Germany), respectively. Both catheters were tunneled subcutaneously and exteriorized through the back of the neck, and the surgical incision sites were closed by sutures.For the experiments, the rats were placed into a 3.9 L Plexiglas® chamber (with sealed exit ports for catheters), which allowed them to move freely. The arterial catheter was connected to a pressure transducer (MLT0380/D, ADInstruments, Sydney, Australia), and the amplified AP signal was fed to an IBM/PC connected to a Power Lab system (ML866, ADInstruments, Sydney, Australia) and continuously sampled (2 kHz). Different gas mixtures were allowed to easily pass through the chamber to change the gas concentration. The gas concentration inside the chamber was continuously measured with an O2 analyzer (GasAlertMax XT, Canada) and a CO2 analyzer (microCapStar CO2 Monitor, PA, USA). A flowmeter gas-mixing pump (Cameron, Canada) allowed for the injection of different gas concentrations into the chamber. To measure respiratory parameters, the airflow through the chamber was interrupted for a short time (∼1 min), and the inlet and outlet ports were sealed. Pressure oscillations caused by respiratory movements were detected by a differential pressure transducer (ML141, ADInstruments, Sydney, Australia) and were digitally recorded simultaneously with AP. Volume calibration was performed during each measurement by injecting a known air volume (1 mL) into the chamber. The tidal volume (TV) was calculated offline using the formula described by Malan (<a class="elsevierStyleCrossRef" href="#bib25">25</a>). The respiratory frequency (RF) was calculated from the extrapolation of the plethysmographic signal. Pulmonary ventilation (PV) was calculated as the product of TV and RF. MAP and HR were calculated from the arterial pulse pressure.Experimental ProtocolEach animal was individually placed into the plethysmographic chamber at 25°C and allowed to move freely while the chamber was flushed with humidified air (21% O2 and 79% N2, 1.2 L.min-1) for 40-50 min of acclimatization. After the baseline measurements of respiratory parameters and AP, each animal was subjected to 3 levels of hypoxia (15, 10 and 6% of inhaled O2) and combined hypercapnia and hyperoxia (10% CO2+31% O2). The order of each episode of hypoxia or hypercapnia was chosen randomly, and the episodes were spaced 30 min apart.Hypoxia was achieved by switching the gas flushed through the chamber to 100% N2. Nitrogen flow was adjusted (2, 3.5 or 5 L.min-1) to achieve the desired level of hypoxia (15, 10 or 6%) within approximately 45 s. Hypercapnia plus hyperoxia (10% CO2+30% O2) was achieved by flushing the chamber with 50% CO2 and 50% O2 (2 L.min-1) for 45 s. Each period of chemoreceptor stimulation was held for 1 minute, and the respiratory parameters, MAP and HR were measured. Subsequently, the chamber was opened to atmospheric air, and the animals were given a 30-min recovery period. At the end of the experiment, intravenous KCN was administered to verify the efficacy of carotid body denervation, as described elsewhere (<a class="elsevierStyleCrossRef" href="#bib17">17</a>).Statistical AnalysisThe results are expressed as means±standard errors of the mean (SEM). Changes in the MAP and PV in response to hypoxia, hypercapnia and KCN were evaluated by the paired t-test. The comparison between CBD and the intact rats was evaluated by Student's t-test. p<0.05 was considered to be statistically significant.RESULTSHemodynamic responses to KCN in intact and CBD ratsThe baseline values for MAP and HR were similar between the intact (n = 8) and CBD rats (n = 7) and are shown in <a class="elsevierStyleCrossRef" href="#tbl1">Table 1</a>. KCN produced a hypertensive response combined with bradycardia in intact rats but did not change the MAP or HR in CBD rats (<a class="elsevierStyleCrossRef" href="#fig1">Figure 1</a>.<elsevierMultimedia ident="tbl1"></elsevierMultimedia><elsevierMultimedia ident="fig1"></elsevierMultimedia>Hemodynamic responses to different levels of hypoxia and hypercapniaHypoxia with 15% O2 elicited a small but significant hypotensive and tachycardic response that was similar between intact and CBD rats (<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>. Hypoxia with 10% O2 did not change the MAP but elicited a tachycardic response in intact rats. In CBD rats, 15% O2 elicited a marked decrease in AP and increased HR (<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>. The strongest hypoxia (6% O2) elicited a hypertensive and bradycardic response in intact rats and a decrease in MAP with no change in HR in CBD rats (<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>.<elsevierMultimedia ident="fig2"></elsevierMultimedia>Hypercapnia (10% CO2+31% O2) promoted an increase in the MAP and a decrease in HR, which was similar in intact and CBD rats (<a class="elsevierStyleCrossRef" href="#fig3">Figure 3</a>.<elsevierMultimedia ident="fig3"></elsevierMultimedia>Response of pulmonary ventilation to hypoxia and hypercapniaThe baseline values for PV were similar between the intact and CBD rats (<a class="elsevierStyleCrossRef" href="#tbl1">Table 1</a>. The 3 levels of hypoxia increased PV in both groups (<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>. However, the PV response elicited by 15% inhaled O2 was smaller than the responses elicited by 10% or 6% O2 in both groups. Moreover, peripheral chemoreceptor denervation attenuated the ventilatory responses in CBD rats (<a class="elsevierStyleCrossRef" href="#fig2">Figures 2</a>).Hypercapnia (10% CO2+31% O2) promoted a similar increase in PV in both groups (<a class="elsevierStyleCrossRef" href="#fig3">Figure 3</a>.DISCUSSIONThe major finding of this study is that the hemodynamic response varies markedly according to the level of hypoxia (i.e., AP and HR responses can change markedly depending on the level of hypoxia applied). Moreover, this study demonstrated that the hemodynamic and ventilatory responses to the combination of hypercapnia and hyperoxia did not depend on the peripheral carotid chemoreceptors.Hypoxia with 15% O2 produced slight but significant hypotension and tachycardia in intact and CBD rats. This finding suggests that the hemodynamic response to this level of hypoxia in rats does not depend on carotid chemoreceptor activation because a similar response was observed in CBD rats. In line with this study, Marshall and Metcalfe (<a class="elsevierStyleCrossRefs" href="#bib10">10-12</a>) also reported hypotension and tachycardia in response to 15% inhaled O2. The hypotensive response with 15% O2 might be explained by the release of adenosine from the skeletal muscle fibers (<a class="elsevierStyleCrossRef" href="#bib26">26</a>) or blood vessel walls (<a class="elsevierStyleCrossRef" href="#bib27">27</a>,<a class="elsevierStyleCrossRef" href="#bib28">28</a>). Adenosine acts on endothelial A1-receptors to stimulate the synthesis and release of NO, which ultimately induces vasodilation (<a class="elsevierStyleCrossRef" href="#bib29">29</a>). The tachycardia observed in intact and CBD rats exposed to 15% O2 might be due to the baroreflex, which is triggered by a drop in AP (<a class="elsevierStyleCrossRefs" href="#bib30">30-32</a>).Hypoxia with 10% O2 produced a similar hemodynamic response compared to 15% O2 (i.e., hypotension and tachycardia, except that the hypotensive response did not achieve statistical significance in the intact rats). Nevertheless, the decrease in AP in response to 10% O2 in the CBD rats was markedly greater compared to 10% O2 in the intact rats. The lack of a significant hypotensive response in the intact rats might be explained by sympathetic activation elicited by the peripheral chemoreceptors to counteract a decrease in total peripheral resistance triggered by the effect of hypoxia on skeletal muscle fibers (<a class="elsevierStyleCrossRef" href="#bib26">26</a>) or vasodilation of the blood vessel walls (<a class="elsevierStyleCrossRef" href="#bib27">27</a>,<a class="elsevierStyleCrossRef" href="#bib28">28</a>). The tachycardia in the intact rats could be due to the hypoxia-induced activation of the peripheral chemoreflex, which increases sympathetic activity and enhances the release of plasma catecholamines (<a class="elsevierStyleCrossRef" href="#bib33">33</a>). Studies on conscious intact rats have shown that hypoxia with 8 or 10% O2 for 30 min decreased the MAP and increased HR (<a class="elsevierStyleCrossRef" href="#bib9">9</a>,<a class="elsevierStyleCrossRef" href="#bib13">13</a>,<a class="elsevierStyleCrossRef" href="#bib14">14</a>). In addition, Sugimura et al. (<a class="elsevierStyleCrossRef" href="#bib34">34</a>) also observed that 10% inhaled O2 for 10 min elicited hypotension combined with tachycardia in conscious rats. However, the difference between the results from previous studies (<a class="elsevierStyleCrossRef" href="#bib9">9</a>,<a class="elsevierStyleCrossRef" href="#bib13">13</a>,<a class="elsevierStyleCrossRef" href="#bib14">14</a>,<a class="elsevierStyleCrossRef" href="#bib34">34</a>) and this study might be explained by the difference in the timeframe of exposure to hypoxia among the studies (1 min vs. 10 or 30 min). The hypotensive response caused by 10% O2 in the CBD rats might be explained by attenuation of the sympathetic vasoconstrictor outflow due to the removal of the carotid chemoreceptor drive. It has been shown that hypoxia increases adrenal sympathetic nerve activity and catecholamine secretion (<a class="elsevierStyleCrossRef" href="#bib33">33</a>), while sympathetic activation is not triggered in the absence of peripheral chemoreceptors in CBD rats. The tachycardia observed in the CBD rats exposed to 10% O2 may be due to the baroreflex, which is triggered by a fall in AP (<a class="elsevierStyleCrossRefs" href="#bib30">30-32</a>). Although the CBD rats do not have an active peripheral chemoreflex, their baroreflex is well preserved, which explains this reflex tachycardia.Hypoxia with 6% O2 in the conscious intact rats produced marked hypertension and bradycardia, while in the CBD rats, 6% O2 produced hypotension without any change in HR. The findings of this study in conscious intact rats are in line with previous studies (<a class="elsevierStyleCrossRef" href="#bib16">16</a>,<a class="elsevierStyleCrossRef" href="#bib17">17</a>), indicating that maximal peripheral chemoreceptor activation is attained with 6% to 7% of inhaled O2. Previous studies in anesthetized rats have demonstrated that hypoxia promotes hypotension and tachycardia (<a class="elsevierStyleCrossRefs" href="#bib10">10-12</a>). Nevertheless, the undesirable effect of anesthesia and the longer exposure of 3 min of hypoxia might explain the discrepancy in these results (<a class="elsevierStyleCrossRefs" href="#bib10">10-12</a>) compared to this study.Hypoxia with 6% O2 in conscious CBD rats produced significant hypotension without any change in HR. These findings were similar to the hemodynamic responses observed with 10% O2, except that the increase in baseline HR did not reach statistical significance. Thus, due to the lack of activation of the peripheral chemoreceptors in CBD rats, the hypotensive response might be explained by the direct effect of hypoxia in the blood vessel wall (<a class="elsevierStyleCrossRef" href="#bib27">27</a>,<a class="elsevierStyleCrossRef" href="#bib28">28</a>) and endothelial cells to promote vasodilation (<a class="elsevierStyleCrossRef" href="#bib28">28</a>,<a class="elsevierStyleCrossRef" href="#bib35">35</a>).Hypercapnia (10% CO2+31% O2) increased MAP and decreased HR in intact and CBD rats. These findings indicate that the hemodynamic response to hypercapnia does not involve the peripheral carotid chemoreceptors but involves the central chemoreceptors. These results are in line with the previous findings of Walker and Brizzee (<a class="elsevierStyleCrossRef" href="#bib23">23</a>) in conscious rats.Ventilatory responsesHypoxia with 15, 10 and 6% O2 increased PV in the intact rats but attenuated the ventilatory response in CBD rats. These results indicate that in intact rats, PV is partially dependent on the peripheral carotid chemoreceptors because in the absence of this mechanism, the central chemoreceptors may have triggered the blunted response. It is worth mentioning that the findings concerning the PV responses observed in this study are in line with previous studies in intact and CBD rats (<a class="elsevierStyleCrossRef" href="#bib6">6</a>,<a class="elsevierStyleCrossRef" href="#bib7">7</a>,<a class="elsevierStyleCrossRef" href="#bib23">23</a>). In addition, recent studies have suggested a significant role for the peripheral chemoreceptors as an important mechanism for the ventilatory response during exposure to hypercapnia (<a class="elsevierStyleCrossRef" href="#bib36">36</a>,<a class="elsevierStyleCrossRef" href="#bib37">37</a>).Moreover, the response of PV to hypercapnia (10% CO2+31% O2) was similar in intact and CBD rats. Thus, the PV response to hypercapnia depends mainly on the central chemoreceptors. It is possible that the severity of hypercapnia makes the peripheral chemoreceptor less important in modulating the ventilatory response. A similar response was observed in previous studies on conscious intact rats, which indicated that hypercapnia with 6 to 7% CO2 increased PV but did not produce a significant difference in the ventilatory response compared to CBD rats (<a class="elsevierStyleCrossRefs" href="#bib7">7-8</a>).In summary, this study shows that the hemodynamic and ventilatory responses varied according to the level of hypoxia. Nevertheless, the hemodynamic and ventilatory responses to hypercapnia (10% CO2+31% O2) did not depend on peripheral carotid chemoreceptors.AUTHOR CONTRIBUTIONSSabino JP collected the data for this manuscript. Oliveira M and Giusti H provided technical support concerning the surgical procedures for vessel cannulation (Oliveira M) and carotid body denervation (Giusti H) and provided support during data acquisition. Glass ML provided valuable insight into data interpretation and manuscript revision. Fazan Jr R provided a substantial contribution to protocol design and data analysis. Salgado HC was the mentor of Sabino JP and was responsible for the conception of the rationale for the development of the study." "textoCompletoSecciones" => array:1 [ "secciones" => array:8 [ 0 => array:2 [ "identificador" => "xpalclavsec1582905" "titulo" => "KEYWORDS" ] 1 => array:2 [ "identificador" => "cesec10" "titulo" => "INTRODUCTION" ] 2 => array:3 [ "identificador" => "cesec20" "titulo" => "MATERIALS AND METHODS" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "cesec30" "titulo" => "Experimental Protocol" ] 1 => array:2 [ "identificador" => "cesec40" "titulo" => "Statistical Analysis" ] ] ] 3 => array:3 [ "identificador" => "cesec50" "titulo" => "RESULTS" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "cesec60" "titulo" => "Hemodynamic responses to KCN in intact and CBD rats" ] 1 => array:2 [ "identificador" => "cesec70" "titulo" => "Hemodynamic responses to different levels of hypoxia and hypercapnia" ] 2 => array:2 [ "identificador" => "cesec80" "titulo" => "Response of pulmonary ventilation to hypoxia and hypercapnia" ] ] ] 4 => array:3 [ "identificador" => "cesec90" "titulo" => "DISCUSSION" "secciones" => array:1 [ 0 => array:2 [ "identificador" => "cesec100" "titulo" => "Ventilatory responses" ] ] ] 5 => array:2 [ "identificador" => "cesec110" "titulo" => "AUTHOR CONTRIBUTIONS" ] 6 => array:2 [ "identificador" => "xack639605" "titulo" => "ACKNOWLEDGMENTS" ] 7 => array:1 [ "titulo" => "REFERENCES" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2012-09-28" "fechaAceptado" => "2012-11-25" "PalabrasClave" => array:1 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "KEYWORDS" "identificador" => "xpalclavsec1582905" "palabras" => array:4 [ 0 => "Arterial Pressure" 1 => "Heart Rate" 2 => "Pulmonary Ventilation" 3 => "Chemoreceptor Cells" ] ] ] ] "tieneResumen" => true "resumen" => array:1 [ "en" => array:2 [ "resumen" => "OBJECTIVEChemoreceptors play an important role in the autonomic modulation of circulatory and ventilatory responses to changes in arterial O2 and/or CO2. However, studies evaluating hemodynamic responses to hypoxia and hypercapnia in rats have shown inconsistent results. Our aim was to evaluate hemodynamic and respiratory responses to different levels of hypoxia and hypercapnia in conscious intact or carotid body-denervated rats. METHODSMale Wistar rats were submitted to bilateral ligature of carotid body arteries (or sham-operation) and received catheters into the left femoral artery and vein. After two days, each animal was placed into a plethysmographic chamber and, after baseline measurements of respiratory parameters and arterial pressure, each animal was subjected to three levels of hypoxia (15, 10 and 6% O2) and hypercapnia (10% CO2). RESULTSThe results indicated that 15% O2 decreased the mean arterial pressure and increased the heart rate (HR) in both intact (n = 8) and carotid body-denervated (n = 7) rats. In contrast, 10% O2 did not change the mean arterial pressure but still increased the HR in intact rats, and it decreased the mean arterial pressure and increased the heart rate in carotid body-denervated rats. Furthermore, 6% O2 increased the mean arterial pressure and decreased the HR in intact rats, but it decreased the mean arterial pressure and did not change the HR in carotid body-denervated rats. The 3 levels of hypoxia increased pulmonary ventilation in both groups, with attenuated responses in carotid body-denervated rats. Hypercapnia with 10% CO2 increased the mean arterial pressure and decreased HR similarly in both groups. Hypercapnia also increased pulmonary ventilation in both groups to the same extent. CONCLUSIONThis study demonstrates that the hemodynamic and ventilatory responses varied according to the level of hypoxia. Nevertheless, the hemodynamic and ventilatory responses to hypercapnia did not depend on the activation of the peripheral carotid chemoreceptors." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "ceabs10" "titulo" => "OBJECTIVE" ] 1 => array:2 [ "identificador" => "ceabs20" "titulo" => "METHODS" ] 2 => array:2 [ "identificador" => "ceabs30" "titulo" => "RESULTS" ] 3 => array:2 [ "identificador" => "ceabs40" "titulo" => "CONCLUSION" ] ] ] ] "NotaPie" => array:1 [ 0 => array:1 [ "nota" => "No potential conflict of interest was reported." ] ] "multimedia" => array:4 [ 0 => array:7 [ "identificador" => "fig1" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "cln-68-03-395-g001.jpeg" "Alto" => 1107 "Ancho" => 792 "Tamanyo" => 32219 ] ] "descripcion" => array:1 [ "en" => "Bar graph showing the changes in the mean arterial pressure (MAP) and heart rate (HR) in response to KCN in intact and carotid body-denervated (CBD) rats. *p<0.05 compared to intact rats." ] ] 1 => array:7 [ "identificador" => "fig2" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "cln-68-03-395-g002.jpeg" "Alto" => 1360 "Ancho" => 740 "Tamanyo" => 53710 ] ] "descripcion" => array:1 [ "en" => "Bar graph showing the changes in the mean arterial pressure (MAP, top), heart rate (HR, middle) and pulmonary ventilation (PV, bottom) in response to 3 levels of hypoxia (15%, 10% and 6% of inhaled O2) in intact and carotid body-denervated (CBD) rats. * p<0.05 compared to 15% O2.+p<0.05 compared to the same level of hypoxia in intact rats." ] ] 2 => array:7 [ "identificador" => "fig3" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "cln-68-03-395-g003.jpeg" "Alto" => 1671 "Ancho" => 685 "Tamanyo" => 40203 ] ] "descripcion" => array:1 [ "en" => "Bar graph showing the changes in the mean arterial pressure (MAP, top), heart rate (HR, middle) and pulmonary ventilation (PV, bottom) in response to hypercapnia (10% CO2+31% O2) in intact and carotid body-denervated (CBD) rats. *p<0.05 compared to intact rats." ] ] 3 => array:7 [ "identificador" => "tbl1" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:1 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="bottom" scope="col"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="2" align="center" valign="bottom" scope="col">INTACT</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " colspan="2" align="center" valign="bottom" scope="col">CBD</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">INTACT \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">CBD \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="bottom" scope="col"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">MAP \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">HR \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">MAP \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">HR \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">PV \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">PV \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="middle" scope="col"> \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">mmHg \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">bpm \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">mmHg \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">bpm \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">(mL.kg-1.min-1) \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="center" valign="bottom" scope="col">(mL.kg-1.min-1) \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="bottom">KCN \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">100±2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">413±19 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">94±4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">426±25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="bottom"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="bottom"> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="bottom">15% O2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">101±4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">411±17 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">93±5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">415±20 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">1075±98 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">924±56 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="bottom">10% O2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">103±3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">398±10 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">99±4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">415±20 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">1024±61 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">1012±136 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="bottom">6% O2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">109±6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">394±8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">99±4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">427±23 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">961±81 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">935±141 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="bottom">10% CO2+31% O2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">103±4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">401±12 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">98±4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">439±24 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">918±105 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="center" valign="bottom">983±111 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] ] ] ] "descripcion" => array:1 [ "en" => "Baseline levels of mean arterial pressure (MAP), heart rate (HR) and pulmonary ventilation (PV) in intact and carotid body-denervated (CBD) rats before chemoreceptor stimulation with KCN, hypoxia and hypercapnia. The data are expressed as means±SEM." ] ] ] "bibliografia" => array:2 [ "titulo" => "REFERENCES" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "cebibsec10" "bibliografiaReferencia" => array:37 [ 0 => array:3 [ "identificador" => "bib1" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Peripheral chemoreflex in chronic heart failure: Friend and foe" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => """ SS Chugh \n \t\t\t\t\t\t\t\t """ 1 => """ TP Chua \n \t\t\t\t\t\t\t\t """ 2 => """ AJS Coats \n \t\t\t\t\t\t\t\t """ ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/s0002-8703(96)90333-6" "Revista" => array:7 [ "tituloSerie" => "Am Heart J" "fecha" => "1996" "volumen" => "132" "numero" => "4" "paginaInicial" => "900" "paginaFinal" => "904" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/8831388" "web" => "Medline" ] ] ] ] ] ] ] ] 1 => 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João Paulo J. Sabino, Mauro de Oliveira, Humberto Giusti, Mogens Lesner Glass, Helio C. Salgado, Rubens Fazan Jr

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rfazan@usp.br

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Universidade de São Paulo, School of Medicine of Ribeirão Preto, Department of Physiology, São Paulo/SP, Brazil

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    "cabecera" => "<span class="elsevierStyleTextfn">BASIC RESEARCH</span>"
    "titulo" => "Hemodynamic and ventilatory response to different levels of hypoxia and hypercapnia in carotid body-denervated rats"
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        "autoresLista" => "Jo&#227;o Paulo J&#46; Sabino, Mauro de Oliveira, Humberto Giusti, Mogens Lesner Glass, Helio C&#46; Salgado, Rubens Fazan"
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            "entidad" => "Universidade de S&#227;o Paulo&#44; School of Medicine of Ribeir&#227;o Preto&#44; Department of Physiology&#44; S&#227;o Paulo&#47;SP&#44; Brazil"
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          "en" => "<p id="spara10" class="elsevierStyleSimplePara elsevierViewall">Bar graph showing the changes in the mean arterial pressure &#40;MAP&#41; and heart rate &#40;HR&#41; in response to KCN in intact and carotid body-denervated &#40;CBD&#41; rats&#46; &#42;<span class="elsevierStyleItalic">p</span>&#60;0&#46;05 compared to intact rats&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="cesec10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle60">INTRODUCTION</span><p id="para10" class="elsevierStylePara elsevierViewall">Peripheral arterial chemoreceptors consist of aortic bodies situated in the aortic arch and carotid bifurcations &#40;<a class="elsevierStyleCrossRef" href="#bib1">1</a>&#41;&#44; while central chemoreceptors are located on the ventral surface of the medulla &#40;<a class="elsevierStyleCrossRef" href="#bib2">2</a>&#41;&#46; The chemoreceptors play an important role in the regulation of ventilation and circulation in response to changes in arterial O<span class="elsevierStyleInf">2</span> and&#47;or CO<span class="elsevierStyleInf">2</span> &#40;<a class="elsevierStyleCrossRefs" href="#bib2">2-4</a>&#41;&#46;</p><p id="para20" class="elsevierStylePara elsevierViewall">It has been well established that activation of the chemoreceptors under hypoxia or hypercapnia elicits an increase in pulmonary ventilation &#40;PV&#41; &#40;<a class="elsevierStyleCrossRefs" href="#bib5">5-8</a>&#41;&#46; Nevertheless&#44; studies in rats have shown conflicting hemodynamic responses to hypoxia&#46; While some studies have demonstrated that hypoxia elicits a decrease in the mean arterial pressure &#40;MAP&#41; combined with an increase in heart rate &#40;HR&#41; &#40;<a class="elsevierStyleCrossRefs" href="#bib9">9-15</a>&#41;&#44; others have shown an increase in MAP combined with a decrease in HR &#40;<a class="elsevierStyleCrossRef" href="#bib16">16</a>&#44;<a class="elsevierStyleCrossRef" href="#bib17">17</a>&#41;&#46;</p><p id="para30" class="elsevierStylePara elsevierViewall">In contrast&#44; while there is general agreement that hypercapnia promotes a hypertensive response &#40;<a class="elsevierStyleCrossRefs" href="#bib18">18-21</a>&#41;&#44; there is no agreement concerning the HR response to hypercapnia&#46; Studies have reported that bradycardia &#40;<a class="elsevierStyleCrossRef" href="#bib22">22</a>&#44;<a class="elsevierStyleCrossRef" href="#bib23">23</a>&#41; or tachycardia &#40;<a class="elsevierStyleCrossRef" href="#bib18">18</a>&#41; was elicited by hypercapnia&#46;</p><p id="para40" class="elsevierStylePara elsevierViewall">Accordingly&#44; the evident disagreement in the literature concerning the hemodynamic and ventilatory responses to hypoxia and hypercapnia requires further investigation and characterization of the role of the peripheral carotid chemoreceptors in these responses&#46; Therefore&#44; this study aimed to evaluate the hemodynamic and ventilatory responses to different levels of hypoxia and hypercapnia in conscious intact or carotid body-denervated &#40;CBD&#41; rats&#46;</p></span><span id="cesec20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle70">MATERIALS AND METHODS</span><p id="para50" class="elsevierStylePara elsevierViewall">Experiments were performed on male Wistar rats &#40;270-300 g&#41; housed individually with free access to food and water and maintained on a 12&#58;12-h light-dark cycle&#46; All experimental procedures were performed in accordance with the Guide for the Care and Use of Laboratory Animals &#91;Dept&#46; of Health&#44; Education and Welfare&#44; Publication No&#46; &#40;NIH&#41; 85-23&#44; Revised 1985&#46; Office of Science and Health Reports&#44; DRR&#47;NIH&#44; Bethesda&#44; MD&#93;&#46; The experimental protocols used in this research were approved by the Committee of Ethics in Animal Research of the School of Medicine of Ribeir&#227;o Preto&#44; University of S&#227;o Paulo &#40;protocol 053&#47;2010&#41;&#46;</p><p id="para60" class="elsevierStylePara elsevierViewall">Two days before the experiments&#44; the rats were anesthetized with tribromoethanol &#40;250 mg&#46;kg<span class="elsevierStyleSup">-1</span>&#44; i&#46;p&#46;&#44; Sigma&#44; St&#46; Louis&#44; MO&#44; USA&#41;&#44; and bilateral ligature of the carotid body arteries was performed as described elsewhere &#40;<a class="elsevierStyleCrossRef" href="#bib24">24</a>&#41;&#46; Briefly&#44; the carotid artery bifurcations were identified and isolated bilaterally&#46; Then&#44; the carotid body arteries were identified and tightly ligated with a suture line to block the arterial supply to the carotid bodies&#46; The procedure was similar for rats that received the sham operation &#40;intact&#41;&#44; except that they did not undergo the ligature&#46; After artery ligation&#44; polyethylene catheters were inserted into the left femoral artery and vein for the direct measurement of arterial pressure &#40;AP&#41; and administration of potassium cyanide &#40;KCN&#44; 160 &#956;g&#46;kg<span class="elsevierStyleSup">-1</span>&#44; Merck&#44; Darmstadt&#44; Germany&#41;&#44; respectively&#46; Both catheters were tunneled subcutaneously and exteriorized through the back of the neck&#44; and the surgical incision sites were closed by sutures&#46;</p><p id="para70" class="elsevierStylePara elsevierViewall">For the experiments&#44; the rats were placed into a 3&#46;9 L Plexiglas<span class="elsevierStyleBold">&#174;</span> chamber &#40;with sealed exit ports for catheters&#41;&#44; which allowed them to move freely&#46; The arterial catheter was connected to a pressure transducer &#40;MLT0380&#47;D&#44; ADInstruments&#44; Sydney&#44; Australia&#41;&#44; and the amplified AP signal was fed to an IBM&#47;PC connected to a Power Lab system &#40;ML866&#44; ADInstruments&#44; Sydney&#44; Australia&#41; and continuously sampled &#40;2 kHz&#41;&#46; Different gas mixtures were allowed to easily pass through the chamber to change the gas concentration&#46; The gas concentration inside the chamber was continuously measured with an O<span class="elsevierStyleInf">2</span> analyzer &#40;GasAlertMax XT&#44; Canada&#41; and a CO<span class="elsevierStyleInf">2</span> analyzer &#40;microCapStar CO<span class="elsevierStyleInf">2</span> Monitor&#44; PA&#44; USA&#41;&#46; A flowmeter gas-mixing pump &#40;Cameron&#44; Canada&#41; allowed for the injection of different gas concentrations into the chamber&#46; To measure respiratory parameters&#44; the airflow through the chamber was interrupted for a short time &#40;&#8764;1 min&#41;&#44; and the inlet and outlet ports were sealed&#46; Pressure oscillations caused by respiratory movements were detected by a differential pressure transducer &#40;ML141&#44; ADInstruments&#44; Sydney&#44; Australia&#41; and were digitally recorded simultaneously with AP&#46; Volume calibration was performed during each measurement by injecting a known air volume &#40;1 mL&#41; into the chamber&#46; The tidal volume &#40;TV&#41; was calculated offline using the formula described by Malan &#40;<a class="elsevierStyleCrossRef" href="#bib25">25</a>&#41;&#46; The respiratory frequency &#40;RF&#41; was calculated from the extrapolation of the plethysmographic signal&#46; Pulmonary ventilation &#40;PV&#41; was calculated as the product of TV and RF&#46; MAP and HR were calculated from the arterial pulse pressure&#46;</p><span id="cesec30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle80">Experimental Protocol</span><p id="para80" class="elsevierStylePara elsevierViewall">Each animal was individually placed into the plethysmographic chamber at 25&#176;C and allowed to move freely while the chamber was flushed with humidified air &#40;21&#37; O<span class="elsevierStyleInf">2</span> and 79&#37; N<span class="elsevierStyleInf">2</span>&#44; 1&#46;2 L&#46;min<span class="elsevierStyleSup">-1</span>&#41; for 40-50 min of acclimatization&#46; After the baseline measurements of respiratory parameters and AP&#44; each animal was subjected to 3 levels of hypoxia &#40;15&#44; 10 and 6&#37; of inhaled O<span class="elsevierStyleInf">2</span>&#41; and combined hypercapnia and hyperoxia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span>&#41;&#46; The order of each episode of hypoxia or hypercapnia was chosen randomly&#44; and the episodes were spaced 30 min apart&#46;</p><p id="para90" class="elsevierStylePara elsevierViewall">Hypoxia was achieved by switching the gas flushed through the chamber to 100&#37; N<span class="elsevierStyleInf">2</span>&#46; Nitrogen flow was adjusted &#40;2&#44; 3&#46;5 or 5 L&#46;min<span class="elsevierStyleSup">-1</span>&#41; to achieve the desired level of hypoxia &#40;15&#44; 10 or 6&#37;&#41; within approximately 45 s&#46; Hypercapnia plus hyperoxia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;30&#37; O<span class="elsevierStyleInf">2</span>&#41; was achieved by flushing the chamber with 50&#37; CO<span class="elsevierStyleInf">2</span> and 50&#37; O<span class="elsevierStyleInf">2</span> &#40;2 L&#46;min<span class="elsevierStyleSup">-1</span>&#41; for 45 s&#46; Each period of chemoreceptor stimulation was held for 1 minute&#44; and the respiratory parameters&#44; MAP and HR were measured&#46; Subsequently&#44; the chamber was opened to atmospheric air&#44; and the animals were given a 30-min recovery period&#46; At the end of the experiment&#44; intravenous KCN was administered to verify the efficacy of carotid body denervation&#44; as described elsewhere &#40;<a class="elsevierStyleCrossRef" href="#bib17">17</a>&#41;&#46;</p></span><span id="cesec40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle90">Statistical Analysis</span><p id="para100" class="elsevierStylePara elsevierViewall">The results are expressed as means&#177;standard errors of the mean &#40;SEM&#41;&#46; Changes in the MAP and PV in response to hypoxia&#44; hypercapnia and KCN were evaluated by the paired t-test&#46; The comparison between CBD and the intact rats was evaluated by Student&#39;s t-test&#46; <span class="elsevierStyleItalic">p</span>&#60;0&#46;05 was considered to be statistically significant&#46;</p></span></span><span id="cesec50" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle100">RESULTS</span><span id="cesec60" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle110">Hemodynamic responses to KCN in intact and CBD rats</span><p id="para110" class="elsevierStylePara elsevierViewall">The baseline values for MAP and HR were similar between the intact &#40;n&#8202;&#61;&#8202;8&#41; and CBD rats &#40;n&#8202;&#61;&#8202;7&#41; and are shown in <a class="elsevierStyleCrossRef" href="#tbl1">Table 1</a>&#46; KCN produced a hypertensive response combined with bradycardia in intact rats but did not change the MAP or HR in CBD rats &#40;<a class="elsevierStyleCrossRef" href="#fig1">Figure 1</a>&#46;</p><elsevierMultimedia ident="tbl1"></elsevierMultimedia><elsevierMultimedia ident="fig1"></elsevierMultimedia></span><span id="cesec70" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle120">Hemodynamic responses to different levels of hypoxia and hypercapnia</span><p id="para120" class="elsevierStylePara elsevierViewall">Hypoxia with 15&#37; O<span class="elsevierStyleInf">2</span> elicited a small but significant hypotensive and tachycardic response that was similar between intact and CBD rats &#40;<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>&#46; Hypoxia with 10&#37; O<span class="elsevierStyleInf">2</span> did not change the MAP but elicited a tachycardic response in intact rats&#46; In CBD rats&#44; 15&#37; O<span class="elsevierStyleInf">2</span> elicited a marked decrease in AP and increased HR &#40;<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>&#46; The strongest hypoxia &#40;6&#37; O<span class="elsevierStyleInf">2</span>&#41; elicited a hypertensive and bradycardic response in intact rats and a decrease in MAP with no change in HR in CBD rats &#40;<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>&#46;</p><elsevierMultimedia ident="fig2"></elsevierMultimedia><p id="para130" class="elsevierStylePara elsevierViewall">Hypercapnia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span>&#41; promoted an increase in the MAP and a decrease in HR&#44; which was similar in intact and CBD rats &#40;<a class="elsevierStyleCrossRef" href="#fig3">Figure 3</a>&#46;</p><elsevierMultimedia ident="fig3"></elsevierMultimedia></span><span id="cesec80" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle130">Response of pulmonary ventilation to hypoxia and hypercapnia</span><p id="para140" class="elsevierStylePara elsevierViewall">The baseline values for PV were similar between the intact and CBD rats &#40;<a class="elsevierStyleCrossRef" href="#tbl1">Table 1</a>&#46; The 3 levels of hypoxia increased PV in both groups &#40;<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>&#46; However&#44; the PV response elicited by 15&#37; inhaled O<span class="elsevierStyleInf">2</span> was smaller than the responses elicited by 10&#37; or 6&#37; O<span class="elsevierStyleInf">2</span> in both groups&#46; Moreover&#44; peripheral chemoreceptor denervation attenuated the ventilatory responses in CBD rats &#40;<a class="elsevierStyleCrossRef" href="#fig2">Figures 2</a>&#41;&#46;</p><p id="para150" class="elsevierStylePara elsevierViewall">Hypercapnia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span>&#41; promoted a similar increase in PV in both groups &#40;<a class="elsevierStyleCrossRef" href="#fig3">Figure 3</a>&#46;</p></span></span><span id="cesec90" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle140">DISCUSSION</span><p id="para160" class="elsevierStylePara elsevierViewall">The major finding of this study is that the hemodynamic response varies markedly according to the level of hypoxia &#40;i&#46;e&#46;&#44; AP and HR responses can change markedly depending on the level of hypoxia applied&#41;&#46; Moreover&#44; this study demonstrated that the hemodynamic and ventilatory responses to the combination of hypercapnia and hyperoxia did not depend on the peripheral carotid chemoreceptors&#46;</p><p id="para170" class="elsevierStylePara elsevierViewall">Hypoxia with 15&#37; O<span class="elsevierStyleInf">2</span> produced slight but significant hypotension and tachycardia in intact and CBD rats&#46; This finding suggests that the hemodynamic response to this level of hypoxia in rats does not depend on carotid chemoreceptor activation because a similar response was observed in CBD rats&#46; In line with this study&#44; Marshall and Metcalfe &#40;<a class="elsevierStyleCrossRefs" href="#bib10">10-12</a>&#41; also reported hypotension and tachycardia in response to 15&#37; inhaled O<span class="elsevierStyleInf">2</span>&#46; The hypotensive response with 15&#37; O<span class="elsevierStyleInf">2</span> might be explained by the release of adenosine from the skeletal muscle fibers &#40;<a class="elsevierStyleCrossRef" href="#bib26">26</a>&#41; or blood vessel walls &#40;<a class="elsevierStyleCrossRef" href="#bib27">27</a>&#44;<a class="elsevierStyleCrossRef" href="#bib28">28</a>&#41;&#46; Adenosine acts on endothelial A<span class="elsevierStyleInf">1</span>-receptors to stimulate the synthesis and release of NO&#44; which ultimately induces vasodilation &#40;<a class="elsevierStyleCrossRef" href="#bib29">29</a>&#41;&#46; The tachycardia observed in intact and CBD rats exposed to 15&#37; O<span class="elsevierStyleInf">2</span> might be due to the baroreflex&#44; which is triggered by a drop in AP &#40;<a class="elsevierStyleCrossRefs" href="#bib30">30-32</a>&#41;&#46;</p><p id="para180" class="elsevierStylePara elsevierViewall">Hypoxia with 10&#37; O<span class="elsevierStyleInf">2</span> produced a similar hemodynamic response compared to 15&#37; O<span class="elsevierStyleInf">2</span> &#40;i&#46;e&#46;&#44; hypotension and tachycardia&#44; except that the hypotensive response did not achieve statistical significance in the intact rats&#41;&#46; Nevertheless&#44; the decrease in AP in response to 10&#37; O<span class="elsevierStyleInf">2</span> in the CBD rats was markedly greater compared to 10&#37; O<span class="elsevierStyleInf">2</span> in the intact rats&#46; The lack of a significant hypotensive response in the intact rats might be explained by sympathetic activation elicited by the peripheral chemoreceptors to counteract a decrease in total peripheral resistance triggered by the effect of hypoxia on skeletal muscle fibers &#40;<a class="elsevierStyleCrossRef" href="#bib26">26</a>&#41; or vasodilation of the blood vessel walls &#40;<a class="elsevierStyleCrossRef" href="#bib27">27</a>&#44;<a class="elsevierStyleCrossRef" href="#bib28">28</a>&#41;&#46; The tachycardia in the intact rats could be due to the hypoxia-induced activation of the peripheral chemoreflex&#44; which increases sympathetic activity and enhances the release of plasma catecholamines &#40;<a class="elsevierStyleCrossRef" href="#bib33">33</a>&#41;&#46; Studies on conscious intact rats have shown that hypoxia with 8 or 10&#37; O<span class="elsevierStyleInf">2</span> for 30 min decreased the MAP and increased HR &#40;<a class="elsevierStyleCrossRef" href="#bib9">9</a>&#44;<a class="elsevierStyleCrossRef" href="#bib13">13</a>&#44;<a class="elsevierStyleCrossRef" href="#bib14">14</a>&#41;&#46; In addition&#44; Sugimura et al&#46; &#40;<a class="elsevierStyleCrossRef" href="#bib34">34</a>&#41; also observed that 10&#37; inhaled O<span class="elsevierStyleInf">2</span> for 10 min elicited hypotension combined with tachycardia in conscious rats&#46; However&#44; the difference between the results from previous studies &#40;<a class="elsevierStyleCrossRef" href="#bib9">9</a>&#44;<a class="elsevierStyleCrossRef" href="#bib13">13</a>&#44;<a class="elsevierStyleCrossRef" href="#bib14">14</a>&#44;<a class="elsevierStyleCrossRef" href="#bib34">34</a>&#41; and this study might be explained by the difference in the timeframe of exposure to hypoxia among the studies &#40;1 min <span class="elsevierStyleItalic">vs&#46;</span> 10 or 30 min&#41;&#46; The hypotensive response caused by 10&#37; O<span class="elsevierStyleInf">2</span> in the CBD rats might be explained by attenuation of the sympathetic vasoconstrictor outflow due to the removal of the carotid chemoreceptor drive&#46; It has been shown that hypoxia increases adrenal sympathetic nerve activity and catecholamine secretion &#40;<a class="elsevierStyleCrossRef" href="#bib33">33</a>&#41;&#44; while sympathetic activation is not triggered in the absence of peripheral chemoreceptors in CBD rats&#46; The tachycardia observed in the CBD rats exposed to 10&#37; O<span class="elsevierStyleInf">2</span> may be due to the baroreflex&#44; which is triggered by a fall in AP &#40;<a class="elsevierStyleCrossRefs" href="#bib30">30-32</a>&#41;&#46; Although the CBD rats do not have an active peripheral chemoreflex&#44; their baroreflex is well preserved&#44; which explains this reflex tachycardia&#46;</p><p id="para190" class="elsevierStylePara elsevierViewall">Hypoxia with 6&#37; O<span class="elsevierStyleInf">2</span> in the conscious intact rats produced marked hypertension and bradycardia&#44; while in the CBD rats&#44; 6&#37; O<span class="elsevierStyleInf">2</span> produced hypotension without any change in HR&#46; The findings of this study in conscious intact rats are in line with previous studies &#40;<a class="elsevierStyleCrossRef" href="#bib16">16</a>&#44;<a class="elsevierStyleCrossRef" href="#bib17">17</a>&#41;&#44; indicating that maximal peripheral chemoreceptor activation is attained with 6&#37; to 7&#37; of inhaled O<span class="elsevierStyleInf">2</span>&#46; Previous studies in anesthetized rats have demonstrated that hypoxia promotes hypotension and tachycardia &#40;<a class="elsevierStyleCrossRefs" href="#bib10">10-12</a>&#41;&#46; Nevertheless&#44; the undesirable effect of anesthesia and the longer exposure of 3 min of hypoxia might explain the discrepancy in these results &#40;<a class="elsevierStyleCrossRefs" href="#bib10">10-12</a>&#41; compared to this study&#46;</p><p id="para200" class="elsevierStylePara elsevierViewall">Hypoxia with 6&#37; O<span class="elsevierStyleInf">2</span> in conscious CBD rats produced significant hypotension without any change in HR&#46; These findings were similar to the hemodynamic responses observed with 10&#37; O<span class="elsevierStyleInf">2</span>&#44; except that the increase in baseline HR did not reach statistical significance&#46; Thus&#44; due to the lack of activation of the peripheral chemoreceptors in CBD rats&#44; the hypotensive response might be explained by the direct effect of hypoxia in the blood vessel wall &#40;<a class="elsevierStyleCrossRef" href="#bib27">27</a>&#44;<a class="elsevierStyleCrossRef" href="#bib28">28</a>&#41; and endothelial cells to promote vasodilation &#40;<a class="elsevierStyleCrossRef" href="#bib28">28</a>&#44;<a class="elsevierStyleCrossRef" href="#bib35">35</a>&#41;&#46;</p><p id="para210" class="elsevierStylePara elsevierViewall">Hypercapnia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span>&#41; increased MAP and decreased HR in intact and CBD rats&#46; These findings indicate that the hemodynamic response to hypercapnia does not involve the peripheral carotid chemoreceptors but involves the central chemoreceptors&#46; These results are in line with the previous findings of Walker and Brizzee &#40;<a class="elsevierStyleCrossRef" href="#bib23">23</a>&#41; in conscious rats&#46;</p><span id="cesec100" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle150">Ventilatory responses</span><p id="para220" class="elsevierStylePara elsevierViewall">Hypoxia with 15&#44; 10 and 6&#37; O<span class="elsevierStyleInf">2</span> increased PV in the intact rats but attenuated the ventilatory response in CBD rats&#46; These results indicate that in intact rats&#44; PV is partially dependent on the peripheral carotid chemoreceptors because in the absence of this mechanism&#44; the central chemoreceptors may have triggered the blunted response&#46; It is worth mentioning that the findings concerning the PV responses observed in this study are in line with previous studies in intact and CBD rats &#40;<a class="elsevierStyleCrossRef" href="#bib6">6</a>&#44;<a class="elsevierStyleCrossRef" href="#bib7">7</a>&#44;<a class="elsevierStyleCrossRef" href="#bib23">23</a>&#41;&#46; In addition&#44; recent studies have suggested a significant role for the peripheral chemoreceptors as an important mechanism for the ventilatory response during exposure to hypercapnia &#40;<a class="elsevierStyleCrossRef" href="#bib36">36</a>&#44;<a class="elsevierStyleCrossRef" href="#bib37">37</a>&#41;&#46;</p><p id="para230" class="elsevierStylePara elsevierViewall">Moreover&#44; the response of PV to hypercapnia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span>&#41; was similar in intact and CBD rats&#46; Thus&#44; the PV response to hypercapnia depends mainly on the central chemoreceptors&#46; It is possible that the severity of hypercapnia makes the peripheral chemoreceptor less important in modulating the ventilatory response&#46; A similar response was observed in previous studies on conscious intact rats&#44; which indicated that hypercapnia with 6 to 7&#37; CO<span class="elsevierStyleInf">2</span> increased PV but did not produce a significant difference in the ventilatory response compared to CBD rats &#40;<a class="elsevierStyleCrossRefs" href="#bib7">7-8</a>&#41;&#46;</p><p id="para240" class="elsevierStylePara elsevierViewall">In summary&#44; this study shows that the hemodynamic and ventilatory responses varied according to the level of hypoxia&#46; Nevertheless&#44; the hemodynamic and ventilatory responses to hypercapnia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span>&#41; did not depend on peripheral carotid chemoreceptors&#46;</p></span></span><span id="cesec110" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle160">AUTHOR CONTRIBUTIONS</span><p id="para250" class="elsevierStylePara elsevierViewall">Sabino JP collected the data for this manuscript&#46; Oliveira M and Giusti H provided technical support concerning the surgical procedures for vessel cannulation &#40;Oliveira M&#41; and carotid body denervation &#40;Giusti H&#41; and provided support during data acquisition&#46; Glass ML provided valuable insight into data interpretation and manuscript revision&#46; Fazan Jr R provided a substantial contribution to protocol design and data analysis&#46; Salgado HC was the mentor of Sabino JP and was responsible for the conception of the rationale for the development of the study&#46;</p></span></span>"
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            0 => array:2 [
              "identificador" => "cesec30"
              "titulo" => "Experimental Protocol"
            ]
            1 => array:2 [
              "identificador" => "cesec40"
              "titulo" => "Statistical Analysis"
            ]
          ]
        ]
        3 => array:3 [
          "identificador" => "cesec50"
          "titulo" => "RESULTS"
          "secciones" => array:3 [
            0 => array:2 [
              "identificador" => "cesec60"
              "titulo" => "Hemodynamic responses to KCN in intact and CBD rats"
            ]
            1 => array:2 [
              "identificador" => "cesec70"
              "titulo" => "Hemodynamic responses to different levels of hypoxia and hypercapnia"
            ]
            2 => array:2 [
              "identificador" => "cesec80"
              "titulo" => "Response of pulmonary ventilation to hypoxia and hypercapnia"
            ]
          ]
        ]
        4 => array:3 [
          "identificador" => "cesec90"
          "titulo" => "DISCUSSION"
          "secciones" => array:1 [
            0 => array:2 [
              "identificador" => "cesec100"
              "titulo" => "Ventilatory responses"
            ]
          ]
        ]
        5 => array:2 [
          "identificador" => "cesec110"
          "titulo" => "AUTHOR CONTRIBUTIONS"
        ]
        6 => array:2 [
          "identificador" => "xack639605"
          "titulo" => "ACKNOWLEDGMENTS"
        ]
        7 => array:1 [
          "titulo" => "REFERENCES"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2012-09-28"
    "fechaAceptado" => "2012-11-25"
    "PalabrasClave" => array:1 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "KEYWORDS"
          "identificador" => "xpalclavsec1582905"
          "palabras" => array:4 [
            0 => "Arterial Pressure"
            1 => "Heart Rate"
            2 => "Pulmonary Ventilation"
            3 => "Chemoreceptor Cells"
          ]
        ]
      ]
    ]
    "tieneResumen" => true
    "resumen" => array:1 [
      "en" => array:2 [
        "resumen" => "<span id="ceabs10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle10">OBJECTIVE</span><p id="spara50" class="elsevierStyleSimplePara elsevierViewall">Chemoreceptors play an important role in the autonomic modulation of circulatory and ventilatory responses to changes in arterial O<span class="elsevierStyleInf">2</span> and&#47;or CO<span class="elsevierStyleInf">2</span>&#46; However&#44; studies evaluating hemodynamic responses to hypoxia and hypercapnia in rats have shown inconsistent results&#46; Our aim was to evaluate hemodynamic and respiratory responses to different levels of hypoxia and hypercapnia in conscious intact or carotid body-denervated rats&#46;</p></span> <span id="ceabs20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle20">METHODS</span><p id="spara60" class="elsevierStyleSimplePara elsevierViewall">Male Wistar rats were submitted to bilateral ligature of carotid body arteries &#40;or sham-operation&#41; and received catheters into the left femoral artery and vein&#46; After two days&#44; each animal was placed into a plethysmographic chamber and&#44; after baseline measurements of respiratory parameters and arterial pressure&#44; each animal was subjected to three levels of hypoxia &#40;15&#44; 10 and 6&#37; O<span class="elsevierStyleInf">2</span>&#41; and hypercapnia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#41;&#46;</p></span> <span id="ceabs30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle30">RESULTS</span><p id="spara70" class="elsevierStyleSimplePara elsevierViewall">The results indicated that 15&#37; O<span class="elsevierStyleInf">2</span> decreased the mean arterial pressure and increased the heart rate &#40;HR&#41; in both intact &#40;n&#8202;&#61;&#8202;8&#41; and carotid body-denervated &#40;n&#8202;&#61;&#8202;7&#41; rats&#46; In contrast&#44; 10&#37; O<span class="elsevierStyleInf">2</span> did not change the mean arterial pressure but still increased the HR in intact rats&#44; and it decreased the mean arterial pressure and increased the heart rate in carotid body-denervated rats&#46; Furthermore&#44; 6&#37; O<span class="elsevierStyleInf">2</span> increased the mean arterial pressure and decreased the HR in intact rats&#44; but it decreased the mean arterial pressure and did not change the HR in carotid body-denervated rats&#46; The 3 levels of hypoxia increased pulmonary ventilation in both groups&#44; with attenuated responses in carotid body-denervated rats&#46; Hypercapnia with 10&#37; CO<span class="elsevierStyleInf">2</span> increased the mean arterial pressure and decreased HR similarly in both groups&#46; Hypercapnia also increased pulmonary ventilation in both groups to the same extent&#46;</p></span> <span id="ceabs40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle40">CONCLUSION</span><p id="spara80" class="elsevierStyleSimplePara elsevierViewall">This study demonstrates that the hemodynamic and ventilatory responses varied according to the level of hypoxia&#46; Nevertheless&#44; the hemodynamic and ventilatory responses to hypercapnia did not depend on the activation of the peripheral carotid chemoreceptors&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "ceabs10"
            "titulo" => "OBJECTIVE"
          ]
          1 => array:2 [
            "identificador" => "ceabs20"
            "titulo" => "METHODS"
          ]
          2 => array:2 [
            "identificador" => "ceabs30"
            "titulo" => "RESULTS"
          ]
          3 => array:2 [
            "identificador" => "ceabs40"
            "titulo" => "CONCLUSION"
          ]
        ]
      ]
    ]
    "NotaPie" => array:1 [
      0 => array:1 [
        "nota" => "<p class="elsevierStyleNotepara" id="cenpara10">No potential conflict of interest was reported&#46;</p>"
      ]
    ]
    "multimedia" => array:4 [
      0 => array:7 [
        "identificador" => "fig1"
        "etiqueta" => "Figure 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "cln-68-03-395-g001.jpeg"
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        "descripcion" => array:1 [
          "en" => "<p id="spara10" class="elsevierStyleSimplePara elsevierViewall">Bar graph showing the changes in the mean arterial pressure &#40;MAP&#41; and heart rate &#40;HR&#41; in response to KCN in intact and carotid body-denervated &#40;CBD&#41; rats&#46; &#42;<span class="elsevierStyleItalic">p</span>&#60;0&#46;05 compared to intact rats&#46;</p>"
        ]
      ]
      1 => array:7 [
        "identificador" => "fig2"
        "etiqueta" => "Figure 2"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "cln-68-03-395-g002.jpeg"
            "Alto" => 1360
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            "Tamanyo" => 53710
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spara20" class="elsevierStyleSimplePara elsevierViewall">Bar graph showing the changes in the mean arterial pressure &#40;MAP&#44; top&#41;&#44; heart rate &#40;HR&#44; middle&#41; and pulmonary ventilation &#40;PV&#44; bottom&#41; in response to 3 levels of hypoxia &#40;15&#37;&#44; 10&#37; and 6&#37; of inhaled O<span class="elsevierStyleInf">2</span>&#41; in intact and carotid body-denervated &#40;CBD&#41; rats&#46; &#42; <span class="elsevierStyleItalic">p</span>&#60;0&#46;05 compared to 15&#37; O<span class="elsevierStyleInf">2</span>&#46;&#43;<span class="elsevierStyleItalic">p</span>&#60;0&#46;05 compared to the same level of hypoxia in intact rats&#46;</p>"
        ]
      ]
      2 => array:7 [
        "identificador" => "fig3"
        "etiqueta" => "Figure 3"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "cln-68-03-395-g003.jpeg"
            "Alto" => 1671
            "Ancho" => 685
            "Tamanyo" => 40203
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spara30" class="elsevierStyleSimplePara elsevierViewall">Bar graph showing the changes in the mean arterial pressure &#40;MAP&#44; top&#41;&#44; heart rate &#40;HR&#44; middle&#41; and pulmonary ventilation &#40;PV&#44; bottom&#41; in response to hypercapnia &#40;10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span>&#41; in intact and carotid body-denervated &#40;CBD&#41; rats&#46; &#42;<span class="elsevierStyleItalic">p</span>&#60;0&#46;05 compared to intact rats&#46;</p>"
        ]
      ]
      3 => array:7 [
        "identificador" => "tbl1"
        "etiqueta" => "Table 1"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "tabla" => array:1 [
          "tablatextoimagen" => array:1 [
            0 => array:1 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="bottom" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="center" valign="bottom" scope="col">INTACT</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="center" valign="bottom" scope="col">CBD</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">INTACT&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">CBD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="bottom" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">MAP&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">HR&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">MAP&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">HR&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">PV&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">PV&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="middle" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">mmHg&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">bpm&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">mmHg&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">bpm&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">&#40;mL&#46;kg<span class="elsevierStyleSup">-1</span>&#46;min<span class="elsevierStyleSup">-1</span>&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="bottom" scope="col">&#40;mL&#46;kg<span class="elsevierStyleSup">-1</span>&#46;min<span class="elsevierStyleSup">-1</span>&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="bottom"><span class="elsevierStyleBold">KCN</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">100&#177;2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">413&#177;19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">94&#177;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">426&#177;25&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="bottom">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="bottom">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="bottom"><span class="elsevierStyleBold">15&#37; O<span class="elsevierStyleInf">2</span></span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">101&#177;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">411&#177;17&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">93&#177;5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">415&#177;20&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">1075&#177;98&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">924&#177;56&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="bottom"><span class="elsevierStyleBold">10&#37; O<span class="elsevierStyleInf">2</span></span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">103&#177;3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">398&#177;10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">99&#177;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">415&#177;20&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">1024&#177;61&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">1012&#177;136&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="bottom"><span class="elsevierStyleBold">6&#37; O<span class="elsevierStyleInf">2</span></span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">109&#177;6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">394&#177;8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">99&#177;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">427&#177;23&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">961&#177;81&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">935&#177;141&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="bottom"><span class="elsevierStyleBold">10&#37; CO<span class="elsevierStyleInf">2</span>&#43;31&#37; O<span class="elsevierStyleInf">2</span></span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">103&#177;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">401&#177;12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">98&#177;4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">439&#177;24&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">918&#177;105&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="bottom">983&#177;111&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spara40" class="elsevierStyleSimplePara elsevierViewall">Baseline levels of mean arterial pressure &#40;MAP&#41;&#44; heart rate &#40;HR&#41; and pulmonary ventilation &#40;PV&#41; in intact and carotid body-denervated &#40;CBD&#41; rats before chemoreceptor stimulation with KCN&#44; hypoxia and hypercapnia&#46; The data are expressed as means&#177;SEM&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "REFERENCES"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "cebibsec10"
          "bibliografiaReferencia" => array:37 [
            0 => array:3 [
              "identificador" => "bib1"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Peripheral chemoreflex in chronic heart failure&#58; Friend and foe"
                      "autores" => array:1 [
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Article information

ISSN: 18075932
Original language: English

DOI:10.6061/clinics/2013(03)OA18

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Year/Month	Html	Pdf	Total

2024 November	9	2	11
2024 October	43	25	68
2024 September	26	20	46
2024 August	37	17	54
2024 July	29	19	48
2024 June	38	26	64
2024 May	36	19	55
2024 April	41	25	66
2024 March	41	9	50
2024 February	48	21	69
2024 January	20	16	36
2023 December	22	28	50
2023 November	16	28	44
2023 October	31	22	53
2023 September	28	26	54
2023 August	10	4	14
2023 July	21	28	49
2023 June	25	16	41
2023 May	35	6	41
2023 April	19	5	24
2023 March	4	13	17
2023 February	3	15	18
2023 January	3	2	5
2022 December	29	0	29

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