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      The Effect of Viral Infection on Exhaled Nitric Oxide in Children with Acute Asthma Exacerbations

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          Abstract

          Background

          Fraction of exhaled nitric oxide (F eno) level is used as an aid in the diagnosis and management of chronic asthma. Its role in acute asthma remains to be studied.

          Objective

          To determine whether F eno levels are elevated in children with asthma exacerbations compared with baseline, and whether there is a difference in F eno levels based on PCR positive (+) (respiratory virus isolated by PCR analysis) versus PCR negative (−) (respiratory virus not isolated by PCR analysis) status.

          Methods

          Children with a previous F eno level measurement while stable and who presented to an urgent care facility with an asthma exacerbation were enrolled. F eno levels, spirometry, and nasal swabs for viral PCR were obtained at the time of the exacerbation and following a course of prednisone. Data were available on 66 children. Linear mixed models were used to regress the outcomes of interest (FEV 1, FEV 1/forced vital capacity, forced expiratory flow at 25% to 75% of forced vital capacity, and natural log F eno) on detected virus (yes/no), visit (baseline, exacerbation, follow-up), and the interaction between the detected virus and visit.

          Results

          Compared with baseline, higher F eno values and lower lung function were found at the time of an exacerbation. A respiratory virus was detected in 59% of the exacerbations. The interaction between PCR (+) and PCR (−) groups and visit on log F eno was marginally significant ( P = .07). There was no difference in log F eno between the PCR (+) and PCR (−) groups at baseline, while higher log F eno was found in the PCR (−) group at the time of exacerbation and following prednisone ( P = .05 and .001, respectively).

          Conclusions

          Higher F eno concentration in PCR (−) exacerbations suggests an eosinophilic predominance in nonviral compared with viral exacerbations.

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          Most cited references34

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          Community study of role of viral infections in exacerbations of asthma in 9-11 year old children.

          S Johnston, P Pattemore, G. Sanderson … (1995)
          To study the association between upper and lower respiratory viral infections and acute exacerbations of asthma in schoolchildren in the community. Community based 13 month longitudinal study using diary card respiratory symptom and peak expiratory flow monitoring to allow early sampling for viruses. 108 Children aged 9-11 years who had reported wheeze or cough, or both, in a questionnaire. Southampton and surrounding community. Upper and lower respiratory viral infections detected by polymerase chain reaction or conventional methods, reported exacerbations of asthma, computer identified episodes of respiratory tract symptoms or peak flow reductions. Viruses were detected in 80% of reported episodes of reduced peak expiratory flow, 80% of reported episodes of wheeze, and in 85% of reported episodes of upper respiratory symptoms, cough, wheeze, and a fall in peak expiratory flow. The median duration of reported falls in peak expiratory flow was 14 days, and the median maximum fall in peak expiratory flow was 81 l/min. The most commonly identified virus type was rhinovirus. This study supports the hypothesis that upper respiratory viral infections are associated with 80-85% of asthma exacerbations in school age children.
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            Role of viral respiratory infections in asthma and asthma exacerbations

            William Busse, Robert Lemanske, James Gern (2010)
            Summary Viral respiratory tract infections are common and usually selflimited illnesses. For patients at risk of asthma, or with existing asthma, viral respiratory tract infections can have a profound effect on the expression of disease or loss of control. New evidence has shown that wheezing episodes early in life due to human rhinoviruses are a major risk factor for the later diagnosis of asthma at age 6 years. For those with existing asthma, exacerbations are a major cause of morbidity, can need acute care, and can, albeit rarely, result in death. Viral respiratory tract infections, predominantly those caused by human rhinoviruses, are associated with asthma exacerbations. There is also evidence that deficiencies in antiviral activity and the integrity of the airway epithelial barrier could make individuals with asthma more likely to have severe viral respiratory infections of the lower airway, and thus increase the risk of exacerbation. In view of the effect of respiratory viruses on many aspects of asthma, efforts to understand the mechanisms and risk factors by which these airway infections cause changes in airway pathophysiology are a first step towards improved treatment.
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              Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production.

              Simon D. Message, Vasile Laza-Stanca, Patrick Mallia … (2008)
              Acute exacerbations are the major cause of asthma morbidity, mortality, and health-care costs and are difficult to treat and prevent. The majority of asthma exacerbations are associated with rhinovirus (RV) infection, but evidence supporting a causal relationship is weak and mechanisms are poorly understood. We hypothesized that in asthmatic, but not normal, subjects RV infection would induce clinical, physiologic, and pathologic lower airway responses typical of an asthma exacerbation and that these changes would be related to virus replication and impaired T helper 1 (Th1)/IL-10 or augmented Th2 immune responses. We investigated physiologic, virologic, and immunopathologic responses to experimental RV infection in blood, induced sputum, and bronchial lavage in 10 asthmatic and 15 normal volunteers. RV infection induced significantly greater lower respiratory symptoms and lung function impairment and increases in bronchial hyperreactivity and eosinophilic lower airway inflammation in asthmatic compared with normal subjects. In asthmatic, but not normal, subjects virus load was significantly related to lower respiratory symptoms, bronchial hyperreactivity, and reductions in blood total and CD8(+) lymphocytes; lung function impairment was significantly related to neutrophilic and eosinophilic lower airway inflammation. The same virologic and clinical outcomes were strongly related to deficient IFN-gamma and IL-10 responses and to augmented IL-4, IL-5, and IL-13 responses. This study demonstrates increased RV-induced clinical illness severity in asthmatic compared with normal subjects, provides evidence of strong relationships between virus load, lower airway virus-induced inflammation and asthma exacerbation severity, and indicates augmented Th2 or impaired Th1 or IL-10 immunity are likely important mechanisms.
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                Author and article information

                Contributors
                Jonathan Malka
                Journal
                Journal ID (nlm-ta): J Allergy Clin Immunol Pract
                Journal ID (iso-abbrev): J Allergy Clin Immunol Pract
                Title: The Journal of Allergy and Clinical Immunology. in Practice
                Publisher: Elsevier Inc
                ISSN (Print): 2213-2198
                ISSN (Electronic): 2213-2201
                Publication date PMC-release: 26 July 2015
                Publication date (Print): Nov-Dec 2015
                Publication date (Electronic): 26 July 2015
                Volume: 3
                Issue: 6
                Pages: 913-919
                Affiliations
                [a ]Pediatric Associates, Aventura, Fla
                [b ]National Jewish Health, Denver, Colo
                [c ]Division of Allergy-Clinical Immunology, Denver, Colo
                [d ]Division of Clinical Pharmacology, Department of Pediatrics, Ira J. and Jacqueline Neimark Laboratory of Clinical Pharmacology in Pediatrics, Denver, Colo
                [e ]Department of Biostatistics and Bioinformatics, Denver, Colo
                [f ]Department of Nursing, Denver, Colo
                [g ]Molecular Diagnostics Advanced Diagnostic Laboratories, Denver, Colo
                [h ]Section of Allergy, Department of Pediatrics, Children's Hospital Colorado, Aurora, Colo
                Author notes
                [∗ ]Corresponding author: Jonathan Malka, MD, Pediatric Associates, 21097 NE 27th Court, Ste # 205, Denver, CO 80206. jmalka@ 123456pediatricassociates.com
                Article
                Publisher ID: S2213-2198(15)00274-3
                DOI: 10.1016/j.jaip.2015.05.029
                PMC ID: 7104006
                PubMed ID: 26216254
                SO-VID: 643bd42f-c1d4-4111-bea9-5880b07c5382
                Copyright © Copyright © 2015 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.
                License:

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

                History
                Date received : 28 July 2014
                Date revision received : 27 May 2015
                Date accepted : 29 May 2015
                Categories
                Subject: Article

                Keywords: childhood asthma,fraction of exhaled nitric oxide (feno),asthma exacerbations,ed, emergency department,fef25-75, forced expiratory flow at 25% to 75% of forced vital capacity,feno, fraction of exhaled nitric oxide,fvc, forced vital capacity,gc, glucocorticoid,pcr (+), respiratory virus isolated by pcr analysis,pcr (−), respiratory virus not isolated by pcr analysis
                Data availability:
                Keywords: childhood asthma, fraction of exhaled nitric oxide (feno), asthma exacerbations, ed, emergency department, fef25-75, forced expiratory flow at 25% to 75% of forced vital capacity, feno, fraction of exhaled nitric oxide, fvc, forced vital capacity, gc, glucocorticoid, pcr (+), respiratory virus isolated by pcr analysis, pcr (−), respiratory virus not isolated by pcr analysis

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