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Clinical Sciences
Comorbidities in Severe Asthma: Frequency of Rhinitis, Nasal Polyposis, Gastroesophageal Reflux Disease, Vocal Cord Dysfunction and Bronchiectasis
Carla Bisaccioni, Marcelo Vivolo Aun, Edcarlos Cajuela, Jorge Kalil, Rosana Câmara Agondi, Pedro Giavina-Bianchi
Clinical Immunology and Allergy Department, Faculdade de Medicina da, Universidade de São Paulo - São Paulo/SP, Brazil, Emails:;, Tel: 55 11 3071.3189
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          "en" => "<p id="spara20" class="elsevierStyleSimplePara elsevierViewall">Severity of rhinitis symptoms among severe asthma patients &#40;defined according to the criteria established in Allergic Rhinitis and its Impact on Asthma &#8211; ARIA<a class="elsevierStyleCrossRef" href="#bib7">7</a>&#41;&#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">The prevalence of asthma is increasing in most countries&#46; The global prevalence ranges from 1 to 18&#37;&#44; which makes it a public health problem that has increasingly become of interest to researchers&#46;<a class="elsevierStyleCrossRef" href="#bib1">1</a> Around 10&#37; of asthma patients have severe asthma&#44; and some of these cases are defined as difficult-to-control asthma&#46;</p><p id="para20" class="elsevierStylePara elsevierViewall">Difficult-to-control severe asthma&#44; although accounting for no more than 5&#37; of all asthma cases&#44; is responsible for approximately 50&#37; of the overall costs related to asthma treatment&#46; It is also associated with greater morbidity and mortality&#46; The risk of requiring treatment in the emergency room and of requiring hospitalization is 15 and 20 times greater&#44; respectively&#44; for such patients than for those with less severe forms of asthma&#46;<a class="elsevierStyleCrossRef" href="#bib2">2</a>&#8211;<a class="elsevierStyleCrossRef" href="#bib5">5</a></p><p id="para30" class="elsevierStylePara elsevierViewall">In individuals with severe asthma&#44; comorbidities are common&#44; with the most prevalent being gastroesophageal reflux disease &#40;GERD&#41;&#44; sinusitis&#44; allergic rhinitis and nasal polyposis&#46; All of these can lead to worsening of the asthma symptoms&#46;<a class="elsevierStyleCrossRef" href="#bib6">6</a></p><p id="para40" class="elsevierStylePara elsevierViewall">Allergic rhinitis and allergic asthma are currently recognized as manifestations of a single entity&#58; chronic allergic respiratory disease&#44; also known as &#8220;united airway disease&#8221;&#46;<a class="elsevierStyleCrossRefs" href="#bib7">7&#44;8</a> The great majority of patients with asthma have rhinitis&#44; which is itself a risk factor for the development of asthma&#46;</p><p id="para50" class="elsevierStylePara elsevierViewall">Individuals with asthma often present with GERD&#44; which has been shown to exacerbate asthma through mechanisms involving vagal nerve stimulation &#40;esophagobronchial reflex&#41; or microaspiration of gastric contents into the upper airways&#46;<a class="elsevierStyleCrossRef" href="#bib9">9</a>&#8211;<a class="elsevierStyleCrossRef" href="#bib11">11</a></p><p id="para60" class="elsevierStylePara elsevierViewall">Other diseases that are rare and sometimes difficult to diagnose&#44; including vocal cord dysfunction &#40;VCD&#41; and allergic bronchopulmonary aspergillosis &#40;ABPA&#41;&#44; are also associated with worse asthma control&#46;</p><p id="para70" class="elsevierStylePara elsevierViewall">The features of VCD include episodes of involuntary paradoxical movements caused by vocal cord adduction during inspiration&#44; resulting in airway obstruction&#46; Although VCD can be seen in patients with asthma&#44; it can also occur in an isolated form in individuals without respiratory disease&#46;<a class="elsevierStyleCrossRefs" href="#bib12">12&#44;13</a></p><p id="para80" class="elsevierStylePara elsevierViewall">Aspirin-induced asthma &#40;AIA&#41; is a clinical entity characterized by asthma and intolerance to aspirin or nonsteroidal anti-inflammatory drugs &#40;NSAIDs&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib14">14</a> AIA and nasal polyposis are associated with an increase in asthma severity&#46;<a class="elsevierStyleCrossRefs" href="#bib14">14&#44;15</a></p><p id="para90" class="elsevierStylePara elsevierViewall">Asthma and bronchiectasis coexist in many patients&#44; and it has been shown that bronchiectasis can contribute to severe and difficult-to-control asthma with pulmonary complications&#46;<a class="elsevierStyleCrossRef" href="#bib16">16</a></p><p id="para100" class="elsevierStylePara elsevierViewall">In order to improve the treatment of patients with severe asthma and to control the disease&#44; comorbidities must be taken into consideration&#44; and it is important to treat these conditions simultaneously&#46;</p><p id="para110" class="elsevierStylePara elsevierViewall">We investigated the occurrence of rhinitis&#44; intolerance to NSAIDs&#44; nasal polyposis&#44; GERD&#44; VCD and bronchiectasis in patients with severe asthma&#46;</p></span><span id="cesec20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle70">MATERIALS AND METHODS</span><p id="para120" class="elsevierStylePara elsevierViewall">We conducted a retrospective analysis of data obtained from electronic medical records between January 2006 and June 2008 for patients who met the 2008 Global Initiative for Asthma &#40;GINA&#41; criteria for diagnosis of severe persistent asthma&#46;<a class="elsevierStyleCrossRef" href="#bib1">1</a></p><p id="para130" class="elsevierStylePara elsevierViewall">The patients were asked about symptoms of rhinitis&#44; GERD and intolerance to NSAIDs&#46; Rhinorrhea&#44; nasal pruritus&#44; sneezing and congestion were all considered to be symptoms consistent with rhinitis&#46; The severity and frequency of the symptoms were defined according to the criteria established in the World Health Organization review entitled Allergic Rhinitis and Its Impact on Asthma &#40;ARIA&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib7">7</a> Regurgitation&#44; heartburn and retrosternal discomfort were considered to be suggestive of GERD&#46; Only patients presenting specific complaints of exacerbation resulting from the use of aspirin or NSAIDs were considered to be intolerant to those medications&#46;</p><p id="para140" class="elsevierStylePara elsevierViewall">A diagnosis of VCD was suspected in patients who reported worsening of symptoms or attacks in situations of emotional stress&#44; were refractory to routine asthma treatment&#44; presented cervical inspiratory wheezing&#44; and had a peripheral oxygen saturation that remained above 95&#37; even during severe attacks&#46; Suspicion of VCD was also raised for patients in whom spirometry revealed flattening of the inspiratory loop of the flow-volume curve&#44; which is suggestive of extrathoracic obstruction&#44; and in those presenting a difficult-to-control clinical profile with normal or only slightly altered pulmonary function&#46; Thus&#44; VCD was considered when there was a discrepancy between clinical features&#44; laboratory exams and treatment&#46;</p><p id="para150" class="elsevierStylePara elsevierViewall">The study also included esophagogastroduodenoscopy &#40;EGD&#41;&#44; videolaryngoscopy and high-resolution computed tomography &#40;CT&#41; scans of the chest&#46; Findings that could be consistent with GERD varied from mild to severe esophagitis&#44; as seen under direct EGD visualization&#46; Other clinical findings suggestive of GERD were seen under videolaryngoscopy as mild to severe posterior laryngitis&#46; The results of endoscopic examination of the larynx were considered consistent with VCD when there was two-thirds closure of the vocal cords with a diamond-shaped opening occurring posteriorly during inspiration&#46; The same examination was used to confirm the presence of nasal polyps&#46; We also evaluated CT scans of the chest in order to identify bronchiectasis&#46;</p></span><span id="cesec30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle80">RESULTS</span><p id="para160" class="elsevierStylePara elsevierViewall">We evaluated 245 patients&#44; 194 females and 51 males&#44; all of whom were being treated with inhaled corticosteroids&#46; Six patients &#40;2&#46;5&#37;&#41; were also receiving oral corticosteroids in an attempt to control their asthma&#46; The mean patient age was 57&#46;8 years&#44; with a range of 21&#8211;85 years&#46; Lung function tests and levels of asthma control are summarized in <a class="elsevierStyleCrossRef" href="#t1-cln64_8p769">table 1</a>&#46;</p><elsevierMultimedia ident="t1-cln64_8p769"></elsevierMultimedia><p id="para170" class="elsevierStylePara elsevierViewall">Rhinitis was seen in 224 patients &#40;91&#46;4&#37;&#41;&#44; and the majority of these patients had persistent and moderate-to-severe rhinitis &#40;<a class="elsevierStyleCrossRefs" href="#f1-cln64_8p769">Figures 1 and 2</a>&#41;&#46;</p><elsevierMultimedia ident="f2-cln64_8p769"></elsevierMultimedia><elsevierMultimedia ident="f1-cln64_8p769"></elsevierMultimedia><p id="para180" class="elsevierStylePara elsevierViewall">Intolerance to NSAIDs or nasal polyposis was found in 21 patients &#40;8&#46;5&#37;&#41;&#46; There were 13 patients with intolerance to NSAIDs who did not have nasal polyps&#44; and there were 3 patients with nasal polyposis who did not report intolerance to NSAIDs &#40;<a class="elsevierStyleCrossRef" href="#f3-cln64_8p769">Figure 3</a>&#41;&#46;</p><elsevierMultimedia ident="f3-cln64_8p769"></elsevierMultimedia><p id="para190" class="elsevierStylePara elsevierViewall">Symptoms of GERD were reported for 173 &#40;70&#46;6&#37;&#41; of the patients evaluated&#44; although the diagnosis of GERD was confirmed based on the previously cited criteria in just 58 &#40;33&#46;6&#37;&#41; &#40;<a class="elsevierStyleCrossRef" href="#f4-cln64_8p769">Figure 4</a>&#41;&#46;</p><elsevierMultimedia ident="f4-cln64_8p769"></elsevierMultimedia><p id="para200" class="elsevierStylePara elsevierViewall">Among the 245 asthma patients evaluated&#44; VCD was suspected in 16 &#40;6&#46;5&#37;&#41; and confirmed through videolaryngoscopy in 4 &#40;1&#46;6&#37;&#41;&#46;</p><p id="para210" class="elsevierStylePara elsevierViewall">CT scans of the chest were taken for 105 patients&#44; of whom 26 &#40;24&#46;8&#37;&#41; showed bronchiectasis&#46;</p></span><span id="cesec40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle90">DISCUSSION</span><p id="para220" class="elsevierStylePara elsevierViewall">Although only 10&#37; of asthma cases are classified as severe&#44; such cases are responsible for greater morbidity and mortality&#46; In addition&#44; other factors and comorbidities such as GERD&#44; rhinosinusitis and VCD contribute to poor asthma control&#44; although the exact impact these factors have on the severity of the disease has not been well established&#46;<a class="elsevierStyleCrossRef" href="#bib6">6</a></p><p id="para230" class="elsevierStylePara elsevierViewall">The prevalence of rhinitis among patients with asthma is around 75 to 80&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib7">7</a> Various studies have demonstrated that among atopic diseases&#44; asthma and rhinitis are the ones most often seen in combination&#46; In addition&#44; allergic rhinitis is considered a major risk factor for the development of asthma&#44; as has been well documented in various countries&#44; including Brazil&#44; in the International Study of Asthma and Allergy in Childhood&#46;<a class="elsevierStyleCrossRefs" href="#bib18">18&#44;19</a> The prevalence of rhinitis in the patients with severe asthma evaluated in the present study&#44; however&#44; was higher than that reported in the majority of studies found in the literature&#46; We believe that the high prevalence in our study can be attributed to the fact that our patient population had severe asthma&#46;<a class="elsevierStyleCrossRef" href="#bib7">7</a> Some studies have demonstrated that the presence of severe rhinitis in a patient with asthma is associated with a less favorable outcome&#46; It is also possible that the presence of more than one allergic respiratory disease will lead to an allergy specialist referral&#46; In addition&#44; it has been shown that the treatment of nasal symptoms can be beneficial to the lower respiratory tract&#44; reducing the number of emergency room visits and hospitalizations and limiting bronchial hyperresponsiveness&#46;<a class="elsevierStyleCrossRefs" href="#bib19">19&#44;20</a></p><p id="para240" class="elsevierStylePara elsevierViewall">Although hypersensitivity to NSAIDs and aspirin affects only 0&#46;6&#8211;2&#46;5&#37; of the general population of adults&#44; it occurs in 5&#8211;20&#37; of adults with asthma&#46;<a class="elsevierStyleCrossRef" href="#bib21">21</a> In our sample&#44; only 3&#46;2&#37; of the patients reported asthma exacerbation after the use of NSAIDs&#59; however&#44; this finding might indicate that many patients are not able to perceive such exacerbation&#44; as has previously been demonstrated&#46; In a study conducted in Europe involving 500 patients diagnosed with aspirin-intolerant asthma&#44; 90 &#40;18&#37;&#41; were unable to perceive worsening symptoms prior to the provocation test&#46;<a class="elsevierStyleCrossRef" href="#bib21">21</a> In the present study&#44; only the clinical profile of NSAID-induced bronchospasm was considered&#46; None of the patients underwent a challenge test&#46;</p><p id="para250" class="elsevierStylePara elsevierViewall">Asthma and GERD frequently coexist&#46;<a class="elsevierStyleCrossRef" href="#bib22">22</a> Concomitance between symptoms of dyspnea and reflux is quite common&#44; and large-scale studies have shown that the degree of reflux can be as much as 60&#37; greater in those with asthma as compared to individuals without asthma&#46;<a class="elsevierStyleCrossRef" href="#bib23">23</a> In a study conducted in the United Kingdom&#44; the prevalence of GERD symptoms among patients with difficult-to-control asthma was found to be 75&#37;&#44; which is comparable to the findings in our sample&#46;<a class="elsevierStyleCrossRef" href="#bib24">24</a> In the same study&#44; however&#44; 24-h pH-metry revealed the true prevalence to be only 55&#37;&#46; In the present study&#44; the patients were submitted to EGD and videolaryngoscopy&#44; through which 58 patients &#40;23&#46;6&#37;&#41; were diagnosed with concomitant asthma and GERD&#46; Not all of our patients&#44; however&#44; underwent these tests&#46;</p><p id="para260" class="elsevierStylePara elsevierViewall">Despite the fact that VCD has been increasingly studied&#44; its prevalence has yet to be well defined&#46; In Brazil&#44; the reported prevalence of VCD is around 17&#46;5&#37; among patients with severe asthma&#46;<a class="elsevierStyleCrossRef" href="#bib12">12</a> In our study&#44; the patient charts indicated that VCD was suspected in only 6&#46;5&#37; of cases&#46; We believe that VCD is under-diagnosed&#44; however&#44; since the diagnosis was confirmed in more than 16 patients at our outpatient clinic&#46;<a class="elsevierStyleCrossRefs" href="#bib25">25&#44;26</a></p><p id="para270" class="elsevierStylePara elsevierViewall">It is common to see abnormal CT scan results in those with asthma&#44; as previously reported by several authors&#46; In addition to abnormalities such as hyperinflation&#44; mucoid impaction&#44; acinar pattern&#44; lobar collapse and bronchial wall thickening&#44; which are expected in patients with asthma&#44; other less common findings such as bronchiectasis are increasing in frequency&#46; The reported incidence of bronchiectasis among asthma patients is between 37&#37; and 65&#37;&#46; The use of CT for the diagnosis of bronchiectasis has been validated in various studies in which the patients were submitted to CT and bronchogram&#46;<a class="elsevierStyleCrossRef" href="#bib27">27</a></p><p id="para280" class="elsevierStylePara elsevierViewall">Autopsy studies have shown that 15&#8211;20&#37; of patients who died from exacerbation of asthma had bronchiectasis&#44; most often in the upper lobes&#46; One hypothesis to explain the prevalence of bronchial dilation in asthma patients is destruction of the bronchi by an inflammatory process or recurrent infection&#46; In our study&#44; 24&#46;8&#37; of 105 patients who underwent CT showed bronchiectasis&#46; Some of these patients could have also had ABPA&#44; which is difficult to diagnose&#46; It has been reported that the majority of patients do not meet all of the diagnostic criteria simultaneously&#44; and many such patients are receiving corticosteroid therapy&#44; which can mask the symptoms&#46;<a class="elsevierStyleCrossRef" href="#bib27">27</a></p></span><span id="cesec50" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle100">CONCLUSIONS</span><p id="para290" class="elsevierStylePara elsevierViewall">Rhinitis and GERD were the most common comorbidities observed&#44; in addition to bronchiectasis&#46; Therefore&#44; in patients with severe asthma&#44; associated diseases should be investigated as the cause of respiratory symptoms and uncontrolled asthma&#46;</p></span></span>"
    "textoCompletoSecciones" => array:1 [
      "secciones" => array:7 [
        0 => array:2 [
          "identificador" => "xpalclavsec1585127"
          "titulo" => "KEYWORDS&#58;"
        ]
        1 => array:2 [
          "identificador" => "cesec10"
          "titulo" => "INTRODUCTION"
        ]
        2 => array:2 [
          "identificador" => "cesec20"
          "titulo" => "MATERIALS AND METHODS"
        ]
        3 => array:2 [
          "identificador" => "cesec30"
          "titulo" => "RESULTS"
        ]
        4 => array:2 [
          "identificador" => "cesec40"
          "titulo" => "DISCUSSION"
        ]
        5 => array:2 [
          "identificador" => "cesec50"
          "titulo" => "CONCLUSIONS"
        ]
        6 => array:1 [
          "titulo" => "REFERENCES"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2009-04-26"
    "fechaAceptado" => "2009-05-15"
    "PalabrasClave" => array:1 [
      "en" => array:1 [
        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "KEYWORDS&#58;"
          "identificador" => "xpalclavsec1585127"
          "palabras" => array:5 [
            0 => "Severe Asthma"
            1 => "Rhinitis"
            2 => "NSAIDs Intolerance"
            3 => "Gastroesophageal Reflux Disease"
            4 => "Bronchiectasis"
          ]
        ]
      ]
    ]
    "tieneResumen" => true
    "resumen" => array:1 [
      "en" => array:2 [
        "resumen" => "<span id="ceabs10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle10">OBJECTIVES</span><p id="spara70" class="elsevierStyleSimplePara elsevierViewall">Severe asthma is found in approximately 10&#37; of patients with asthma&#46; Some factors associated with worse asthma control include rhinitis&#44; gastroesophageal reflux disease&#44; vocal cord dysfunction &#40;VCD&#41;&#44; nasal polyposis and bronchiectasis&#46; Therefore&#44; we evaluated the prevalence of these illnesses in patients with severe asthma&#46;</p></span> <span id="ceabs20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle20">METHODS</span><p id="spara80" class="elsevierStyleSimplePara elsevierViewall">We conducted a retrospective analysis of data obtained from electronic medical records of patients with severe asthma between January 2006 and June 2008&#46; Symptoms of rhinitis and gastroesophageal reflux disease were evaluated as well as intolerance to nonsteroidal anti-inflammatory drugs&#46; We evaluated the results of esophagogastroduodenoscopy&#44; videolaryngoscopy and CT scans of the chest in order to confirm gastroesophageal reflux disease&#44; nasal polyposis&#44; vocal cord dysfunction and bronchiectasis&#46;</p></span> <span id="ceabs30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle30">RESULTS</span><p id="spara90" class="elsevierStyleSimplePara elsevierViewall">We evaluated 245 patients&#46; Rhinitis symptoms were present in 224 patients &#40;91&#46;4&#37;&#41;&#59; 18 &#40;7&#46;3&#37;&#41; had intolerance to nonsteroidal anti-inflammatory drugs&#44; and 8 &#40;3&#46;3&#37;&#41; had nasal polyposis&#46; Symptoms of gastroesophageal reflux disease were reported for 173 &#40;70&#46;6&#37;&#41; patients&#44; although the diagnosis of gastroesophageal reflux disease was confirmed based on esophagogastroduodenoscopy or laryngoscopy findings in just 58 &#40;33&#46;6&#37;&#41; patients&#46; Vocal cord dysfunction was suspected in 16 &#40;6&#46;5&#37;&#41; and confirmed through laryngoscopy in 4 &#40;1&#46;6&#37;&#41;&#46; The patient records provided CT scans of the chest for 105 patients&#44; and 26 &#40;24&#46;8&#37;&#41; showed bronchiectasis&#46;</p></span> <span id="ceabs40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle40">DISCUSSION</span><p id="spara100" class="elsevierStyleSimplePara elsevierViewall">Rhinitis and gastroesophageal reflux disease were the most common comorbidities observed&#44; in addition to bronchiectasis&#46; Therefore&#44; in patients with severe asthma&#44; associated diseases should be investigated as the cause of respiratory symptoms and uncontrolled asthma&#46;</p></span>"
        "secciones" => array:4 [
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            "identificador" => "ceabs10"
            "titulo" => "OBJECTIVES"
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            "titulo" => "METHODS"
          ]
          2 => array:2 [
            "identificador" => "ceabs30"
            "titulo" => "RESULTS"
          ]
          3 => array:2 [
            "identificador" => "ceabs40"
            "titulo" => "DISCUSSION"
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        ]
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          "en" => "<p id="spara10" class="elsevierStyleSimplePara elsevierViewall">Frequency of rhinitis symptoms among severe asthma patients &#40;defined according to the criteria established in Allergic Rhinitis and its Impact on Asthma &#8211; ARIA<a class="elsevierStyleCrossRef" href="#bib7">7</a>&#41;</p>"
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          "en" => "<p id="spara20" class="elsevierStyleSimplePara elsevierViewall">Severity of rhinitis symptoms among severe asthma patients &#40;defined according to the criteria established in Allergic Rhinitis and its Impact on Asthma &#8211; ARIA<a class="elsevierStyleCrossRef" href="#bib7">7</a>&#41;&#46;</p>"
        ]
      ]
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        "identificador" => "f3-cln64_8p769"
        "etiqueta" => "Figure 3"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr3.jpeg"
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          "en" => "<p id="spara30" class="elsevierStyleSimplePara elsevierViewall">Frequency of intolerance to nonsteroidal anti-inflammatory drugs &#40;NSAIDs&#41; and nasal polyposis&#46; &#9827; White color represents intolerance to NSAIDs&#59; &#9824; Black color represents nasal polyposis</p>"
        ]
      ]
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        "etiqueta" => "Figure 4"
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          "en" => "<p id="spara40" class="elsevierStyleSimplePara elsevierViewall">Patients with gastroesophageal reflux disease &#40;GERD&#41; symptoms and investigation with esophagogastroduodenoscopy &#40;EGD&#41; and videolaryngoscopy&#46; Confirmation of GERD was based on findings of esophagitis or laryngitis</p>"
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        "tabla" => array:3 [
          "leyenda" => "<p id="spara60" class="elsevierStyleSimplePara elsevierViewall">ICS&#44; inhaled corticosteroid&#59; OCS&#44; oral corticosteroid&#59; FEV1&#44; forced expiratory volume in 1s</p>"
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                  <table border="0" frame="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">n &#40;female&#47;male&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">245 &#40;194&#47;51&#41;&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="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Age &#40;years&#41;&#44; median &#40;range&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">57&#46;8 &#40;21 &#8211; 85&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " colspan="2" align="left" valign="\n
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                  \t\t\t\t">Corticosteroid treatment</td></tr><tr title="table-row"><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Under ICS treatment&#44; n &#40;&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">245 &#40;100&#37;&#41;&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="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Under OCS treatment&#44; n &#40;&#37;&#41;&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="\n
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                  \t\t\t\t">6 &#40;2&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">3&#46;0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Partly controlled&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spara50" class="elsevierStyleSimplePara elsevierViewall">Demographic data&#44; baseline characteristics&#44; corticosteroid treatment and lung function &#40;all patients&#41;</p>"
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                          "autores" => array:6 [
                            0 => """
                              ED Bateman \n
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                              """
                            1 => """
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es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos