Skip to main content
Top
Published in: Archives of Virology 4/2018

01-04-2018 | Review

Regional, age and respiratory-secretion-specific prevalence of respiratory viruses associated with asthma exacerbation: a literature review

Authors: Xue-yan Zheng, Yan-jun Xu, Wei-jie Guan, Li-feng Lin

Published in: Archives of Virology | Issue 4/2018

Login to get access

Abstract

Despite increased understanding of how viral infection is involved in asthma exacerbations, it is less clear which viruses are involved and to what extent they contribute to asthma exacerbations. Here, we sought to determine the prevalence of different respiratory viruses during asthma exacerbations. Systematic computerized searches of the literature up to June 2017 without language limitation were performed. The primary focus was on the prevalence of respiratory viruses, including AdV (adenovirus), BoV (bocavirus), CoV (coronavirus), CMV (cytomegalovirus), EnV (enterovirus), HSV (herpes simplex virus), IfV (influenza virus), MpV (metapneumovirus), PiV (parainfluenzavirus), RV (rhinovirus) and RSV (respiratory syncytial virus) during asthma exacerbations. We also examined the prevalence of viral infection stratified by age, geographic region, type of respiratory secretion, and detection method. Sixty articles were included in the final analysis. During asthma exacerbations, the mean prevalence of AdV, BoV, CoV, CMV, EnV, HSV, IfV, MpV, PiV, RV and RSV was 3.8%, 6.9%, 8.4%, 7.2%, 10.1%, 12.3%, 10.0%, 5.3%, 5.6%, 42.1% and 13.6%, respectively. EnV, MPV, RV and RSV were more prevalent in children, whereas AdV, BoV, CoV, IfV and PiV were more frequently present in adults. RV was the major virus detected globally, except in Africa. RV could be detected in both the upper and lower airway. Polymerase chain reaction was the most sensitive method for detecting viral infection. Our findings indicate the need to develop prophylactic polyvalent or polyvirus (including RV, EnV, IfV and RSV) vaccines that produce herd immunity and reduce the healthcare burden associated with virus-induced asthma exacerbations.
Appendix
Available only for authorised users
Literature
1.
go back to reference Castillo JR, Peters SP, Busse WW (2017) Asthma exacerbations: pathogenesis, prevention, and treatment. J Allergy Clin Immunol Pract 5:918–927CrossRef Castillo JR, Peters SP, Busse WW (2017) Asthma exacerbations: pathogenesis, prevention, and treatment. J Allergy Clin Immunol Pract 5:918–927CrossRef
2.
go back to reference Masoli M, Fabian D, Holt S, Beasley R (2004) Global Initiative for Asthma (GINA) Program. The global burden of asthma: executive summary of the GINA Dissemination Committee Report. Allergy 59:469–478CrossRef Masoli M, Fabian D, Holt S, Beasley R (2004) Global Initiative for Asthma (GINA) Program. The global burden of asthma: executive summary of the GINA Dissemination Committee Report. Allergy 59:469–478CrossRef
3.
go back to reference GBD 2015 Chronic Respiratory Disease Collaborators (2017) Global, regional, and national deaths, prevalence, disability-adjusted life years, and years lived with disability for chronic obstructive pulmonary disease and asthma, 1990–2015: a systematic analysis for the Global Burden of Disease Study. Lancet Respir Med 5(9):691–706CrossRef GBD 2015 Chronic Respiratory Disease Collaborators (2017) Global, regional, and national deaths, prevalence, disability-adjusted life years, and years lived with disability for chronic obstructive pulmonary disease and asthma, 1990–2015: a systematic analysis for the Global Burden of Disease Study. Lancet Respir Med 5(9):691–706CrossRef
4.
go back to reference Johnston SL, Pattemore PK, Sanderson G, Smith S, Lampe F, Josephs L, Symington P, O’Toole S, Myint SH, Tyrrell DA (1995) Community study of role of viral infections in exacerbations of asthma in 9–11 year old children. BMJ 310:1225–1229CrossRef Johnston SL, Pattemore PK, Sanderson G, Smith S, Lampe F, Josephs L, Symington P, O’Toole S, Myint SH, Tyrrell DA (1995) Community study of role of viral infections in exacerbations of asthma in 9–11 year old children. BMJ 310:1225–1229CrossRef
5.
go back to reference Papadopoulos NG, Christodoulou I, Rohde G, Agache I, Almqvist C, Bruno A, Bonini S, Bont L, Bossios A, Bousquet J, Braido F, Brusselle G, Canonica GW, Carlsen KH, Chanez P, Fokkens WJ, Garcia-Garcia M, Gjomarkaj M, Haahtela T, Holgate ST, Johnston SL, Konstantinou G, Kowalski M, Lewandowska-Polak A, Lødrup-Carlsen K, Mäkelä M, Malkusova I, Mullol J, Nieto A, Eller E, Ozdemir C, Panzner P, Popov T, Psarras S, Roumpedaki E, Rukhadze M, Stipic-Markovic A, Todo Bom A, Toskala E, van Cauwenberge P, van Drunen C, Watelet JB, Xatzipsalti M, Xepapadaki P, Zuberbier T (2011) Viruses and bacteria in acute asthma exacerbations—a GA2LEN-DARE systematic review. Allergy 66:458–468CrossRef Papadopoulos NG, Christodoulou I, Rohde G, Agache I, Almqvist C, Bruno A, Bonini S, Bont L, Bossios A, Bousquet J, Braido F, Brusselle G, Canonica GW, Carlsen KH, Chanez P, Fokkens WJ, Garcia-Garcia M, Gjomarkaj M, Haahtela T, Holgate ST, Johnston SL, Konstantinou G, Kowalski M, Lewandowska-Polak A, Lødrup-Carlsen K, Mäkelä M, Malkusova I, Mullol J, Nieto A, Eller E, Ozdemir C, Panzner P, Popov T, Psarras S, Roumpedaki E, Rukhadze M, Stipic-Markovic A, Todo Bom A, Toskala E, van Cauwenberge P, van Drunen C, Watelet JB, Xatzipsalti M, Xepapadaki P, Zuberbier T (2011) Viruses and bacteria in acute asthma exacerbations—a GA2LEN-DARE systematic review. Allergy 66:458–468CrossRef
6.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535CrossRef Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535CrossRef
7.
go back to reference Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM, QUADAS-2 Group (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536CrossRef Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM, QUADAS-2 Group (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536CrossRef
8.
go back to reference Sanchez-Padilla E, Grais RF, Guerin PJ, Steele AD, Burny ME, Luquero FJ (2009) Burden of disease and circulating serotypes of rotavirus infection in sub-Saharan Africa: systematic review and meta-analysis. Lancet Infect Dis 9:567–576CrossRef Sanchez-Padilla E, Grais RF, Guerin PJ, Steele AD, Burny ME, Luquero FJ (2009) Burden of disease and circulating serotypes of rotavirus infection in sub-Saharan Africa: systematic review and meta-analysis. Lancet Infect Dis 9:567–576CrossRef
9.
go back to reference DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188CrossRef DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188CrossRef
10.
go back to reference Tang JW, Lam TT, Zaraket H, Lipkin WI, Drews SJ, Hatchette TF, Heraud JM, Koopmans MP, )INSPIRE investigators (2017) Global epidemiology of non-influenza RNA respiratory viruses: data gaps and a growing need for surveillance. Lancet Infect Dis S1473–3099(17):302–384 Tang JW, Lam TT, Zaraket H, Lipkin WI, Drews SJ, Hatchette TF, Heraud JM, Koopmans MP, )INSPIRE investigators (2017) Global epidemiology of non-influenza RNA respiratory viruses: data gaps and a growing need for surveillance. Lancet Infect Dis S1473–3099(17):302–384
11.
go back to reference Wildenbeest JG, van der Schee MP, Hashimoto S, Benschop KS, Minnaar RP, Sprikkelman AB, Haarman EG, van Aalderen WM, Sterk PJ, Pajkrt D, Wolthers KC (2016) Prevalence of rhinoviruses in young children of an unselected birth cohort from the Netherlands. Clin Microbiol Infect 22:736.e9–736.e15CrossRef Wildenbeest JG, van der Schee MP, Hashimoto S, Benschop KS, Minnaar RP, Sprikkelman AB, Haarman EG, van Aalderen WM, Sterk PJ, Pajkrt D, Wolthers KC (2016) Prevalence of rhinoviruses in young children of an unselected birth cohort from the Netherlands. Clin Microbiol Infect 22:736.e9–736.e15CrossRef
12.
go back to reference Fernandes-Matano L, Monroy-Muñoz IE, Angeles-Martínez J, Sarquiz-Martinez B, Palomec-Nava ID, Pardavé-Alejandre HD, Santos Coy-Arechavaleta A, Santacruz-Tinoco CE, González-Ibarra J, González-Bonilla CR, Muñoz-Medina JE (2017) Prevalence of non-influenza respiratory viruses in acute respiratory infection cases in Mexico. PLoS One 12:e0176298CrossRef Fernandes-Matano L, Monroy-Muñoz IE, Angeles-Martínez J, Sarquiz-Martinez B, Palomec-Nava ID, Pardavé-Alejandre HD, Santos Coy-Arechavaleta A, Santacruz-Tinoco CE, González-Ibarra J, González-Bonilla CR, Muñoz-Medina JE (2017) Prevalence of non-influenza respiratory viruses in acute respiratory infection cases in Mexico. PLoS One 12:e0176298CrossRef
13.
go back to reference Colosia AD, Yang J, Hillson E, Mauskopf J, Copley-Merriman C, Shinde V, Stoddard J (2017) The epidemiology of medically attended respiratory syncytial virus in older adults in the United States: a systematic review. PLoS One 12:e0182321CrossRef Colosia AD, Yang J, Hillson E, Mauskopf J, Copley-Merriman C, Shinde V, Stoddard J (2017) The epidemiology of medically attended respiratory syncytial virus in older adults in the United States: a systematic review. PLoS One 12:e0182321CrossRef
15.
go back to reference Calvo C, García-García ML, Pozo F, Carballo D, Martínez-Monteserín E, Casas I (2016) Infections and coinfections by respiratory human bocavirus during eight seasons in hospitalized children. J Med Virol 88:2052–2058CrossRef Calvo C, García-García ML, Pozo F, Carballo D, Martínez-Monteserín E, Casas I (2016) Infections and coinfections by respiratory human bocavirus during eight seasons in hospitalized children. J Med Virol 88:2052–2058CrossRef
16.
go back to reference Vazquez-Perez JA, Ramirez-Gonzalez JE, Moreno-Valencia Y, Hernandez-Hernandez VA, Romero-Espinoza JA, Castillejos-Lopez M, Hernandez A, Perez-Padilla R, Oropeza-Lopez LE, Escobar-Escamilla N, Gonzalez-Villa M, Alejandre-Garcia A, Regalado-Pineda J, Santillan-Doherty P, Lopez-Martínez I, Diaz-Quiñonez A, Salas-Hernandez J (2016) EV-D68 infection in children with asthma exacerbation and pneumonia in Mexico City during 2014 autumn. Influ Other Respir Viruses 10:154–160CrossRef Vazquez-Perez JA, Ramirez-Gonzalez JE, Moreno-Valencia Y, Hernandez-Hernandez VA, Romero-Espinoza JA, Castillejos-Lopez M, Hernandez A, Perez-Padilla R, Oropeza-Lopez LE, Escobar-Escamilla N, Gonzalez-Villa M, Alejandre-Garcia A, Regalado-Pineda J, Santillan-Doherty P, Lopez-Martínez I, Diaz-Quiñonez A, Salas-Hernandez J (2016) EV-D68 infection in children with asthma exacerbation and pneumonia in Mexico City during 2014 autumn. Influ Other Respir Viruses 10:154–160CrossRef
17.
go back to reference Edwards KM, Zhu Y, Griffin MR, Weinberg GA, Hall CB, Szilagyi PG, Staat MA, Iwane M, Prill MM, Williams JV, Network New Vaccine Surveillance (2013) Burden of human metapneumovirus infection in young children. N Engl J Med 368:633–643CrossRef Edwards KM, Zhu Y, Griffin MR, Weinberg GA, Hall CB, Szilagyi PG, Staat MA, Iwane M, Prill MM, Williams JV, Network New Vaccine Surveillance (2013) Burden of human metapneumovirus infection in young children. N Engl J Med 368:633–643CrossRef
18.
go back to reference Lukkarinen M, Koistinen A, Turunen R, Lehtinen P, Vuorinen T, Jartti T (2017) Rhinovirus-induced first wheezing episode predicts atopic but not nonatopic asthma at school age. J Allergy Clin Immunol 140(4):988–995CrossRef Lukkarinen M, Koistinen A, Turunen R, Lehtinen P, Vuorinen T, Jartti T (2017) Rhinovirus-induced first wheezing episode predicts atopic but not nonatopic asthma at school age. J Allergy Clin Immunol 140(4):988–995CrossRef
19.
go back to reference Shi T, McAllister DA, O’Brien KL, et al. RSV Global Epidemiology Network (2017) Global, regional and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in young children in 2015: a systematic review and modelling study. Lancet 390(10098):946–958 Shi T, McAllister DA, O’Brien KL, et al. RSV Global Epidemiology Network (2017) Global, regional and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in young children in 2015: a systematic review and modelling study. Lancet 390(10098):946–958
21.
go back to reference Iaconelli M, Divizia M, Della Libera S, Di Bonito P, La Rosa G (2016) Frequent detection and genetic diversity of human bocavirus in urban sewage samples. Food Environ Virol 8:289–295CrossRef Iaconelli M, Divizia M, Della Libera S, Di Bonito P, La Rosa G (2016) Frequent detection and genetic diversity of human bocavirus in urban sewage samples. Food Environ Virol 8:289–295CrossRef
22.
go back to reference Phyu WK, Ong KC, Wong KT (2017) Modelling person-to-person transmission in an Enterovirus A71 orally infected hamster model of hand-foot-and-mouth disease and encephalomyelitis. Emerg Microbes Infect 6:e62CrossRef Phyu WK, Ong KC, Wong KT (2017) Modelling person-to-person transmission in an Enterovirus A71 orally infected hamster model of hand-foot-and-mouth disease and encephalomyelitis. Emerg Microbes Infect 6:e62CrossRef
23.
go back to reference Lee WM, Grindle K, Pappas T, Marshall DJ, Moser MJ, Beaty EL, Shult PA, Prudent JR, Gern JE (2007) High-throughput, sensitive, and accurate multiplex PCR-microsphere flow cytometry system for large-scale comprehensive detection of respiratory viruses. J Clin Microbiol 45:2626–2634CrossRef Lee WM, Grindle K, Pappas T, Marshall DJ, Moser MJ, Beaty EL, Shult PA, Prudent JR, Gern JE (2007) High-throughput, sensitive, and accurate multiplex PCR-microsphere flow cytometry system for large-scale comprehensive detection of respiratory viruses. J Clin Microbiol 45:2626–2634CrossRef
24.
go back to reference de Crom SC, Obihara CC, de Moor RA, Veldkamp EJ, van Furth AM, Rossen JW (2013) Prospective comparison of the detection rates of human enterovirus and parechovirus RT-qPCR and viral culture in different pediatric specimens. J Clin Virol 58:449–454CrossRef de Crom SC, Obihara CC, de Moor RA, Veldkamp EJ, van Furth AM, Rossen JW (2013) Prospective comparison of the detection rates of human enterovirus and parechovirus RT-qPCR and viral culture in different pediatric specimens. J Clin Virol 58:449–454CrossRef
25.
go back to reference van der Schans CP (2007) Bronchial mucus transport. Respir Care 52:1150–1156PubMed van der Schans CP (2007) Bronchial mucus transport. Respir Care 52:1150–1156PubMed
26.
go back to reference Ahern W, Bird T, Court S, Gardner PS, McQuillin J (1970) Pathological changes in virus infections of the lower respiratory tract in children. J Clin Invest 23:7–18 Ahern W, Bird T, Court S, Gardner PS, McQuillin J (1970) Pathological changes in virus infections of the lower respiratory tract in children. J Clin Invest 23:7–18
27.
go back to reference Thornton DJ, Rousseau K, McGuckin MA (2008) Structure and function of the polymeric mucins in airways mucus. Annu Rev Physiol 70:459–486CrossRef Thornton DJ, Rousseau K, McGuckin MA (2008) Structure and function of the polymeric mucins in airways mucus. Annu Rev Physiol 70:459–486CrossRef
28.
go back to reference Jackson DJ, Johnston SL (2010) The role of viruses in acute exacerbations of asthma. J Allergy Clin Immunol 125:1178–1187CrossRef Jackson DJ, Johnston SL (2010) The role of viruses in acute exacerbations of asthma. J Allergy Clin Immunol 125:1178–1187CrossRef
29.
go back to reference Leigh R, Oyelusi W, Wiehler S, Koetzler R, Zaheer RS, Newton R, Proud D (2008) Human rhinovirus infection enhances airway epithelial cell production of growth factors involved in airway remodeling. J Allergy Clin Immunol 121:1238–1245CrossRef Leigh R, Oyelusi W, Wiehler S, Koetzler R, Zaheer RS, Newton R, Proud D (2008) Human rhinovirus infection enhances airway epithelial cell production of growth factors involved in airway remodeling. J Allergy Clin Immunol 121:1238–1245CrossRef
30.
go back to reference Nicholas B, Skipp P, Mould R, Rennard S, Davies DE, O’Connor CD, Djukanovic R (2006) Shotgun proteomic analysis of human-induced sputum. Proteomics 6:4390–4401CrossRef Nicholas B, Skipp P, Mould R, Rennard S, Davies DE, O’Connor CD, Djukanovic R (2006) Shotgun proteomic analysis of human-induced sputum. Proteomics 6:4390–4401CrossRef
31.
go back to reference Mazur NI, Martinón-Torres F, Baraldi E, Fauroux B, Greenough A, Heikkinen T, Manzoni P, Mejias A, Nair H, Papadopoulos NG, Polack FP, Ramilo O, Sharland M, Stein R, Madhi SA, Bont L, Respiratory Syncytial Virus Network (ReSViNET) (2015) Lower respiratory tract infection caused by respiratory syncytial virus: current management and new therapeutics. Lancet Respir Med 3:888–900CrossRef Mazur NI, Martinón-Torres F, Baraldi E, Fauroux B, Greenough A, Heikkinen T, Manzoni P, Mejias A, Nair H, Papadopoulos NG, Polack FP, Ramilo O, Sharland M, Stein R, Madhi SA, Bont L, Respiratory Syncytial Virus Network (ReSViNET) (2015) Lower respiratory tract infection caused by respiratory syncytial virus: current management and new therapeutics. Lancet Respir Med 3:888–900CrossRef
32.
go back to reference Moss RB (2016) Enterovirus 68 infection-association with asthma. J Allergy Clin Immunol Pract 4:226–228CrossRef Moss RB (2016) Enterovirus 68 infection-association with asthma. J Allergy Clin Immunol Pract 4:226–228CrossRef
33.
go back to reference Rouphael NG, Paine M, Mosley R, Henry S, McAllister DV, Kalluri H, Pewin W, Frew PM, Yu T, Thornburg NJ, Kabbani S, Lai L, Vassilieva EV, Skountzou I, Compans RW, Mulligan MJ, Prausnitz MR, TIV-MNP 2015 Study Group (2017) The safety, immunogenicity, and acceptability of inactivated influenza vaccine delivered by microneedle patch (TIV-MNP 2015): a randomised, partly blinded, placebo-controlled, phase 1 trial. Lancet 390:649–658CrossRef Rouphael NG, Paine M, Mosley R, Henry S, McAllister DV, Kalluri H, Pewin W, Frew PM, Yu T, Thornburg NJ, Kabbani S, Lai L, Vassilieva EV, Skountzou I, Compans RW, Mulligan MJ, Prausnitz MR, TIV-MNP 2015 Study Group (2017) The safety, immunogenicity, and acceptability of inactivated influenza vaccine delivered by microneedle patch (TIV-MNP 2015): a randomised, partly blinded, placebo-controlled, phase 1 trial. Lancet 390:649–658CrossRef
34.
go back to reference Lee S, Nguyen MT, Currier MG, Jenkins JB, Strobert EA, Kajon AE, Madan-Lala R, Bochkov YA, Gern JE, Roy K, Lu X, Erdman DD, Spearman P, Moore ML (2016) A polyvalent inactivated rhinovirus vaccine is broadly immunogenic in rhesus macaques. Nat Commun 7:12838CrossRef Lee S, Nguyen MT, Currier MG, Jenkins JB, Strobert EA, Kajon AE, Madan-Lala R, Bochkov YA, Gern JE, Roy K, Lu X, Erdman DD, Spearman P, Moore ML (2016) A polyvalent inactivated rhinovirus vaccine is broadly immunogenic in rhesus macaques. Nat Commun 7:12838CrossRef
Metadata
Title
Regional, age and respiratory-secretion-specific prevalence of respiratory viruses associated with asthma exacerbation: a literature review
Authors
Xue-yan Zheng
Yan-jun Xu
Wei-jie Guan
Li-feng Lin
Publication date
01-04-2018
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 4/2018
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-017-3700-y

Other articles of this Issue 4/2018

Archives of Virology 4/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine