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Original article
Nitric oxide metabolites in allergic rhinitis: The effect of pollen allergen exposure
G. Ciprandia,
Corresponding author
gio.cip@libero.it

Corresponding author.
, M. Toscab, D. Fuchsc
a Department of Internal Medicine, Azienda Ospedaliera Universitaria San Martino – University of Genoa, Genoa, Italy
b Pneumology and Allergy Unit, Istituto Giannina Gaslini, Genoa, Italy
c Division of Biological Chemistry, Biocenter, Innsbruck Medical University, Innsbruck, Austria
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Allergic rhinitis &#40;AR&#41; is typically an immune-mediated disease&#44; characterised by a dysregulation of T-cell responses&#46; An inflammatory cascade characterises AR&#58; the allergen exposure induces mast cell activation by allergen-specific IgE&#46; Activated mast cells release pro-inflammatory cytokines and chemotactic factors which induce an accumulation of inflammatory cells&#44; including eosinophils&#44; neutrophils&#44; basophils&#44; and lymphocytes in nasal mucosa&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> These inflammatory cells start a vicious cycle by producing more cytokines&#44; chemotactic factors&#44; and free radicals&#44; including superoxide anion &#40;O<span class="elsevierStyleInf">2</span><span class="elsevierStyleSup">&#8722;</span>&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2&#8211;4</span></a> These events cause an enhanced vascular permeability and persistent inflammation of the nasal mucosa&#44; finally resulting in obstruction&#46; Nasal obstruction may be considered the main relevant symptom in AR&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> Moreover&#44; with the progression of mucosal oedema&#44; a compression of blood vessels occurs&#44; thus the blood flow declines and renders in turn an ischemic insult to the nasal mucosa&#46;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> Both mucosal oedema and ischaemia determine the objective finding at rhinoscopy characterised by a pale and swollen mucosa&#46; Nasal obstruction is generated by vasodilation&#44; the secretion of nasal glands and by exudation from the mucosal vasculature&#46; A dense network of nerves surrounding these glands and blood vessels is believed to regulate nasal function&#46; Recently&#44; nitric oxide &#40;NO&#41; has been shown to be a co-transmitter of acetylcholine in parasympathetic nerve fibres of the central peripheral nervous system and can also modulate cholinergic effects in the vascular system and glands&#58; the so-called nitrergic innervation&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;8</span></a> When considering the causes for the reduced nasal blood flow&#44; it may include both the decrease in NO production and the mechanical compression&#44; since NO is a potent vasodilating factor&#44; generated by constitutive NO synthase in the endothelial cells&#46;<a class="elsevierStyleCrossRefs" href="#bib0045"><span class="elsevierStyleSup">9&#44;10</span></a> It has been reported that NO is reduced when the endothelium is impaired&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> However&#44; few studies have addressed the role of NO in AR&#46; A first study reported an increased concentration of NO&#44; in the exhaled air in untreated AR patients compared with normal subjects&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Increased NO production in nasal lavage fluid in the nose of patients with perennial AR was documented&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> A recent study investigated the serum concentrations of nitrite in patients with AR&#44;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> nitrite concentrations presenting an oxidation product of NO and other nitrogen-containing compounds&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">This preliminary study was performed in order to compare serum nitrite concentrations in seasonal AR &#40;SAR&#41; patients during and outside the pollen exposure season&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Materials and methods</span><p id="par0015" class="elsevierStylePara elsevierViewall">One hundred and two patients &#40;56 females&#44; 46 males&#44; median age&#58; 28&#46;7 years&#41; were included in this study&#58; 56 with SAR evaluated outside the pollen season and so without allergic inflammation and symptoms&#44; and 46 with SAR evaluated during the pollen season with symptoms&#46; AR diagnosis was made according to the Allergic Rhinitis and its Impact on Asthma &#40;ARIA&#41; document&#46;<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> All allergic patients were sensitised to pollens alone and suffered from moderate to severe persistent Allergic Rhinitis since at least four years ago&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The Ethical Committee approved the study and informed consent was obtained by each of the subjects&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Visual Analogue Scale &#40;VAS&#41; was used to quantify the subjective feeling of nasal obstruction&#44; as previously reported&#44;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> in patients exposed to pollen allergens&#46; It ranges from 0 &#40;no obstruction&#41; to 10 &#40;complete obstruction&#41;&#46; Patients were asked to position a cross on a line corresponding to their own perception of nasal obstruction&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Concentrations of the stable NO metabolite nitrite were determined in serum applying the Griess reaction assay&#46;<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">17&#44;18</span></a> Using a Griess reaction system &#40;Promega&#41;&#44; sulphanilamide was quantitatively converted to a diazonium salt by reaction with NO<span class="elsevierStyleInf">2</span><span class="elsevierStyleSup">&#8722;</span> in acid &#40;phosphoric acid&#41; conditions&#46; The diazonium salt was then coupled to <span class="elsevierStyleItalic">N</span>&#40;1-naphthyl&#41; ethylenediamine dihydrochloride &#40;NED&#41;&#44; forming an azo dye that was read at 540<span class="elsevierStyleHsp" style=""></span>nm in a spectrophotometer&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Statistical analysis was performed using the statistical software package Medcalc 9 &#40;Frank Schoonjans&#44; BE&#41;&#46; Descriptive statistics were first performed&#44; and quantitative parameters were reported as the medians &#40;MD&#41; with interquartile ranges &#40;IQR&#41; due to the skewed distribution&#46; Comparison of the nitrite concentrations in the two groups of patients was performed by the non-parametric Wilcoxon test&#46; Correlation between quantitative variables was evaluated by means of the Spearman&#39;s correlation coefficient &#40;<span class="elsevierStyleItalic">r</span>s&#41;&#46; All tests were two sided and a <span class="elsevierStyleItalic">p</span>-value less than 0&#46;05 was considered statistically significant&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Results</span><p id="par0040" class="elsevierStylePara elsevierViewall">Serum nitrite concentrations significantly differed between SAR patients evaluated outside the pollen season &#40;MD&#58; 28&#46;9<span class="elsevierStyleHsp" style=""></span>&#956;M&#44; IQR&#58; 18&#46;9-50&#46;9<span class="elsevierStyleHsp" style=""></span>&#956;M&#41; compared to those obtained during the pollen season &#40;MD&#58; 7&#46;25<span class="elsevierStyleHsp" style=""></span>&#956;M&#44; IQR&#58; 4&#46;4-13&#46;9<span class="elsevierStyleHsp" style=""></span>&#956;M&#59; <span class="elsevierStyleItalic">U</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;6&#46;78&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#59; <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0045" class="elsevierStylePara elsevierViewall">Moreover&#44; there was a significant correlation between serum nitrite concentrations and VAS in SAR patients evaluated during the pollen season &#40;<span class="elsevierStyleItalic">r</span>s<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;0&#46;941&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#46; <a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Discussion</span><p id="par0050" class="elsevierStylePara elsevierViewall">Allergic Rhinitis is sustained by an inflammatory reaction&#46; Various populations of effector and regulatory T-cells have been shown to play a crucial role in allergic inflammation&#44; mainly concerning Th2-type cells&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> Th2-derived cytokines&#44; such as IL-4 and IL-13&#44; are the primary pathogenic factors in inducing&#44; maintaining&#44; and amplifying inflammatory allergic inflammation&#46; IL-4 and IL-13 orchestrate allergic inflammation promoting IgE synthesis&#44; up-regulating adhesion molecules selective for eosinophil recruitment&#44; and causing increased mucus production and airway hyperreactivity&#46; Therefore&#44; a cascade of inflammatory phenomena sustains the symptom occurrence&#44; mainly concerning nasal obstruction&#46; In fact&#44; nasal obstruction severity is directly related to the intensity of allergic inflammation&#46; Pollen allergy is characterised by more intense severity of both symptoms and nasal inflammation than AR due to perennial allergens&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> In this regard&#44; the inflammatory oedema easily induces a compression of nasal blood vessels&#46; This pathophysiological mechanism could partially explain the findings of this study&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Our study confirms and extends the earlier data reported by Unal et al&#46; on a small group of SAR patients presenting with higher nitrite concentrations than healthy controls&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> Moreover&#44; we demonstrated a significant correlation between nitrite concentrations and symptom severity as assessed by the VAS&#46; Increased nitrite concentrations could indicate higher activity of NOS in SAR patients outside the pollen season&#44; which is suppressed during the pollen exposure season&#46; According to the hypothesis of a shifted balance of Th1&#47;Th2-type immunity during acute allergic responses&#44; one might expect diminished production of Th1-type cytokine interferon&#8211;&#947; &#40;IFN-&#947;&#41; in the patients during seasonal exposure&#46; So the decline of nitrite concentrations during the pollen season could be well explained by an increased Th2-type cytokine profile with lower IFN-&#947; production&#46; Such speculation would also fit to the earlier described elevation of serum tryptophan concentrations in SAR patients outside the pollen season&#46;<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;22</span></a> It is well documented that NO production strongly interferes with expression of tryptophan-degrading enzyme indoleamine&#40;2&#44;3&#41;-dioxygenase &#40;IDO&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> Thus&#44; when nitrite concentrations are higher in SAR patients outside the pollen season and due to higher NO production&#44; an inhibition of IDO is likely and as a consequence tryptophan concentrations would increase&#46; But still one has to keep in mind that increased nitrite concentrations can develop not only when NO production is manipulated&#44; they represent a summary readout for the turn-over of nitrogen-containing amino acids and are thus of low specificity for NOS&#44; and further studies are clearly needed to clarify the issues discussed&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">Moreover&#44; patients evaluated during the pollen season have an intense nasal inflammation that could reduce the production of NO&#46; To support this hypothesis there is a relationship between NO metabolites and perception of obstruction&#46; The more intense the obstruction is&#44; the more NO metabolism is impaired&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">However&#44; this preliminary study has two main limitations&#58; &#40;i&#41; serum NO metabolites were assessed in two different groups of patients and not in the same patients during and out of the pollen season&#44; &#40;ii&#41; serum NO metabolites concentrations were not compared with nasal NO&#46; On the other hand&#44; the aim of the current preliminary study was to consider a more easy and available procedure &#40;such as serum assessment&#41; than nasal NO measurement&#44; which requires specific instruments&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">In conclusion&#44; this preliminary study demonstrates that serum NO metabolism depends on allergen exposure&#46; Therefore&#44; further studies should be performed to confirm these preliminary findings&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Conflict of interest</span><p id="par0075" class="elsevierStylePara elsevierViewall">There is no conflict of interest for any author&#46;</p></span></span>"
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          "titulo" => "Introduction"
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          "titulo" => "Materials and methods"
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        4 => array:2 [
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        5 => array:2 [
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          "identificador" => "xack31847"
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        "titulo" => "Abstract"
        "resumen" => "<span class="elsevierStyleSectionTitle">Background</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Seasonal allergic rhinitis &#40;SAR&#41; is characterised by an inflammation consequent to allergen exposure&#46; Nitric oxide may be involved in allergic inflammation&#46;</p> <span class="elsevierStyleSectionTitle">Objective</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">This study evaluated the serum nitrite concentrations in SAR patients during and outside pollen exposure in order to estimate activity of nitric oxide synthases&#46;</p> <span class="elsevierStyleSectionTitle">Methods</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">One hundred and two &#40;56 females&#44; 46 males&#44; median age&#58; 28&#46;7 years&#41; were included in this study&#58; 56 with SAR evaluated outside the pollen season and so without allergic inflammation and symptoms&#44; and 46 with SAR evaluated during the pollen season with symptoms&#46; Serum concentrations of nitrite were measured and in those patients exposed to pollens&#44; results were compared to scores of the Visual Analogue Scale for nasal obstruction perception&#46;</p> <span class="elsevierStyleSectionTitle">Results</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Serum nitrite concentrations were higher in SAR patients evaluated outside the pollen season &#40;<span class="elsevierStyleItalic">U</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;6&#46;78&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#41;&#44; moreover&#44; there was a significant relationship between nasal obstruction perception and nitrite in patients evaluated during the pollen season&#46;</p> <span class="elsevierStyleSectionTitle">Conclusion</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">This preliminary study demonstrates that serum nitric oxide metabolism depends on allergen exposure&#46;</p>"
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        "texto" => "<p id="par0080" class="elsevierStylePara elsevierViewall">The authors wish to thank Vania Giunta and Mara DeAmici &#40;Clinica Pediatrica&#44; Fondazione IRCCS Policlinico S&#46; Matteo&#44; Pavia&#41; and Maria Gleinser &#40;Innsbruck Medical University&#41; for outstanding statistical and technical support&#46;</p>"
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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