Recurrent Rhinovirus Detections in Children Following a Rhinovirus-Induced Wheezing Exacerbation: A Retrospective Study
DOI:
https://doi.org/10.12974/2311-8687.2015.03.01.2Keywords:
Allergy, asthma, attack, childhood, respiratory virus, wheeze.Abstract
Introduction: It is unclear if children with a rhinovirus (RV)-induced wheezing exacerbation are more susceptible to viruses longitudinally, and whether a parental history of asthma and/or allergy impacts their susceptibility.
The objective of this study was to determine if RV, RV-A and RV-C related wheezing exacerbations in children were associated with prior or subsequent viral detections and investigate the role of parental history of asthma and allergy.
Materials and methods: Children presenting to hospital with acute wheeze were prospectively recruited and tested for respiratory viruses. Data on viruses detected in other respiratory samples (May 1997 to December 2012) were collected from hospital microbiology records and additional RV testing was performed on stored hospital respiratory samples (September 2009 to December 2012). A positive parental history was defined as either parent with self-reported asthma and/or allergy.
Results: At recruitment, RV was detected in 69.2% of samples from children with an acute wheezing episode (n=373, 0–16 years of age), with RV-C the most common virus (65.5%). Children with a history of parental asthma and/or allergy and RV at recruitment had a 14-fold increased incidence rate ratio (IRR) of subsequent RV detection (IRR 14.0, 95% CI 1.9–104.1; p=0.01) compared with children without RV at recruitment. Children without this parental history had a reduced incident rate ratio for samples assessed during this time (IRR 0.5, 95% CI 0.3–0.9; p=0.03).
Conclusion: Children with a parental history of asthma and/or allergy may become more susceptible to recurrent symptomatic RV infections.
References
Dougherty RH and Fahy JV. Acute Exacerbations of Asthma: Epidemiology, Biology and the Exacerbation-Prone Phenotype. Clin Exp Allergy 2009; 39:193-202. http://dx.doi.org/10.1111/j.1365-2222.2008.03157.x DOI: https://doi.org/10.1111/j.1365-2222.2008.03157.x
Bizzintino J, Lee WM, Laing IA, Vang F, Pappas T, Zhang G et al. Association between Human Rhinovirus C and Severity of Acute Asthma in Children. Eur Respir J 2011; 37:1037- 1042. http://dx.doi.org/10.1183/09031936.00092410 DOI: https://doi.org/10.1183/09031936.00092410
Mak RK, Tse LY, Lam WY, Wong GW, Chan PK and Leung TF. Clinical Spectrum of Human Rhinovirus Infections in Hospitalized Hong Kong Children. Pediatr Infect Dis J 2011; 30:749-753. http://dx.doi.org/10.1097/INF.0b013e31821b8c71 DOI: https://doi.org/10.1097/INF.0b013e31821b8c71
Iwane MK, Prill MM, Lu X, Miller EK, Edwards KM, Hall CB, et al. Human Rhinovirus Species Associated with Hospitalizations for Acute Respiratory Illness in Young US Children. J Infect Dis 2011; 204:1702-1710. http://dx.doi.org/10.1093/infdis/jir634 DOI: https://doi.org/10.1093/infdis/jir634
Lee WM, Grindle K, Pappas T, Marshall DJ, Moser MJ, Beaty EL, et al. High-Throughput, Sensitive, and Accurate Multiplex PCR-Microsphere Flow Cytometry System for Large-Scale Comprehensive Detection of Respiratory Viruses. J Clin Microbiol 2007; 45: 2626-2634. http://dx.doi.org/10.1128/JCM.02501-06 DOI: https://doi.org/10.1128/JCM.02501-06
Lee WM, Kiesner C, Pappas T, Lee I, Grindle K, Jartti T, et al. A Diverse Group of Previously Unrecognized Human Rhinoviruses are Common Causes of Respiratory Illnesses in Infants. PLoS One 2007; 2: e966. http://dx.doi.org/10.1371/journal.pone.0000966 DOI: https://doi.org/10.1371/journal.pone.0000966
Miller EK. New Human Rhinovirus Species and their Significance in Asthma Exacerbation and Airway Remodeling. Immunol Allergy Clin North Am 2010; 30: 541- 552, vii. http://dx.doi.org/10.1016/j.iac.2010.08.007 DOI: https://doi.org/10.1016/j.iac.2010.08.007
Smuts HE, Workman LJ and Zar HJ. Human Rhinovirus Infection in Young African Children with Acute Wheezing. BMC Infect Dis 2011; 11: 65. http://dx.doi.org/10.1186/1471-2334-11-65 DOI: https://doi.org/10.1186/1471-2334-11-65
Van der Gugten AC, van der Zalm MM, Uiterwaal CS, Wilbrink B, Rossen JW and van der Ent CK. Human Rhinovirus and Wheezing: Short and Long-Term Associations in Children. Pediatr Infect Dis J 2013; 32: 827- 33. http://dx.doi.org/10.1097/inf.0b013e318290620e DOI: https://doi.org/10.1097/INF.0b013e318290620e
Midulla F, Pierangeli A, Cangiano G, Bonci E, Salvadei S, Scagnolari C, et al. Rhinovirus Bronchiolitis and Recurrent Wheezing: 1-Year Follow-Up. Eur Respir J 2012; 39: 396- 402. http://dx.doi.org/10.1183/09031936.00188210 DOI: https://doi.org/10.1183/09031936.00188210
Carroll KN, Gebretsadik T, Minton P, Woodward K, Liu Z, Miller EK, et al. Influence of Maternal Asthma on the Cause and Severity of Infant Acute Respiratory Tract Infections. J Allergy Clin Immunol 2012; 129: 1236-1242. http://dx.doi.org/10.1016/j.jaci.2012.01.045 DOI: https://doi.org/10.1016/j.jaci.2012.01.045
Jartti T, Lee WM, Pappas T, Evans M, Lemanske RF Jr and Gern JE. Serial Viral Infections in Infants with Recurrent Respiratory Illnesses. Eur Respir J 2008; 32: 314-320. http://dx.doi.org/10.1183/09031936.00161907 DOI: https://doi.org/10.1183/09031936.00161907
Kusel MM, de Klerk NH, Kebadze T, Vohma V, Holt PG, Johnston SL et al. Early-life Respiratory Viral Infections, Atopic Sensitization, and Risk of Subsequent Development of Persistent Asthma. J Allergy Clin Immunol 2007; 119: 1105-1110. http://dx.doi.org/10.1016/j.jaci.2006.12.669 DOI: https://doi.org/10.1016/j.jaci.2006.12.669
Johnston SL, Pattemore PK, Sanderson G, Smith S, Campbell MJ, Josephs LK, et al. The Relationship between Upper Respiratory Infections and Hospital Admissions for Asthma: a time-trend analysis. Am J Respir Crit Care Med 1996; 154: 654-660. http://dx.doi.org/10.1164/ajrccm.154.3.8810601 DOI: https://doi.org/10.1164/ajrccm.154.3.8810601
Khetsuriani N, Kazerouni NN, Erdman DD, Lu X, Redd SC, Anderson LJ et al. Prevalence of Viral Respiratory Tract Infections in Children with Asthma. J Allergy Clin Immunol 2007; 119: 314-321. http://dx.doi.org/10.1016/j.jaci.2006.08.041 DOI: https://doi.org/10.1016/j.jaci.2006.08.041
Heymann PW, Carper HT, Murphy DD, Platts-Mills TA, Patrie J, McLaughlin AP, et al. Viral Infections in Relation to Age, Atopy, and Season of Admission among Children Hospitalized for Wheezing. J Allergy Clin Immunol 2004; 114: 239-247. http://dx.doi.org/10.1016/j.jaci.2004.04.006 DOI: https://doi.org/10.1016/j.jaci.2004.04.006
Durrani SR, Montville DJ, Pratt AS, Sahu S, DeVries MK, Rajamanickam V, et al. Innate Immune Responses to Rhinovirus are Reduced by the High-Affinity IgE Receptor in Allergic Asthmatic Children. J Allergy Clin Immunol 2012; 130: 489-495. http://dx.doi.org/10.1016/j.jaci.2012.05.023 DOI: https://doi.org/10.1016/j.jaci.2012.05.023
McIntyre CL, McWilliam Leitch EC, Savolainen-Kopra C, Hovi T and Simmonds P. Analysis of Genetic Diversity and Sites of Recombination in Human Rhinovirus Species C. J Virol 2010; 84:10297-10310. http://dx.doi.org/10.1128/JVI.00962-10 DOI: https://doi.org/10.1128/JVI.00962-10
Cox DW, Bizzintino J, Ferrari G, Khoo SK, Zhang G, Whelan S, et al. Human Rhinovirus Species C Infection in Young Children with Acute Wheeze is Associated with Increased Acute Respiratory Hospital admissions. Am J Respir Crit Care Med 2013; 188: 1358-1364. http://dx.doi.org/10.1164/rccm.201303-0498OC DOI: https://doi.org/10.1164/rccm.201303-0498OC
Martin AC, Laing IA, Khoo SK, Zhang G, Rueter K, Teoh L, et al. Acute Asthma in Children: Relationships Among CD14 and CC16 Genotypes, Plasma Levels, and severity. Am J Respir Crit Care Med 2006; 173: 617-622. http://dx.doi.org/10.1164/rccm.200509-1367OC DOI: https://doi.org/10.1164/rccm.200509-1367OC
Reddel HK, Taylor DR, Bateman ED, Boulet LP, Boushey HA, Busse WW, et al. An official American Thoracic Society/European Respiratory Society Statement: Asthma Control and Exacerbations: Standardizing Endpoints for Clinical Asthma Trials and Clinical Practice. Am J Respir Crit Care Med 2009; 180: 59-99. http://dx.doi.org/10.1164/rccm.200801-060ST DOI: https://doi.org/10.1164/rccm.200801-060ST
Qureshi F, Pestian J, Davis P and Zaritsky A. Effect of Nebulized Ipratropium on the Hospitalization Rates of Children with Asthma. N Engl J Med 1998; 339: 1030-1035. http://dx.doi.org/10.1056/NEJM199810083391503 DOI: https://doi.org/10.1056/NEJM199810083391503
Ireland DC, Kent J and Nicholson KG. Improved Detection of Rhinoviruses in Nasal and Throat Swabs by Seminested RTPCR. J Med Virol 1993; 40: 96-101. http://dx.doi.org/10.1002/jmv.1890400204 DOI: https://doi.org/10.1002/jmv.1890400204
Bochkov YA, Grindle K, Vang F, Evans MD and Gern JE. Improved Molecular Typing Assay for Rhinovirus Species A, B, and C. J Clin Microbiol 2014; 52: 2461-2471. http://dx.doi.org/10.1128/JCM.00075-14 DOI: https://doi.org/10.1128/JCM.00075-14
Kiang D, Kalra I, Yagi S, Louie JK, Boushey H, Boothby J et al. Assay for 5' Noncoding Region Analysis of all Human Rhinovirus Prototype Strains. J Clin Microbiol 2008; 46: 3736-3745. http://dx.doi.org/10.1128/JCM.00674-08 DOI: https://doi.org/10.1128/JCM.00674-08
Jackson DJ, Evans MD, Gangnon RE, Tisler CJ, Pappas TE, Lee WM, et al. Evidence for a Causal Relationship between Allergic Sensitization and Rhinovirus Wheezing in Early Life. Am J Respir Crit Care Med 2012; 185: 281-285. http://dx.doi.org/10.1164/rccm.201104-0660OC DOI: https://doi.org/10.1164/rccm.201104-0660OC
Lemanske RF, Jr Jackson DJ, Gangnon RE, Evans MD, Li Z, Shult PA, et al. Rhinovirus Illnesses During Infancy Predict Subsequent Childhood Wheezing. J Allergy Clin Immunol 2005; 116: 571-577. http://dx.doi.org/10.1016/j.jaci.2005.06.024 DOI: https://doi.org/10.1016/j.jaci.2005.06.024
Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, et al. Wheezing Rhinovirus Illnesses in Early Life Predict Asthma Development in High-Risk children. Am J Respir Crit Care Med 2008; 178: 667-672. http://dx.doi.org/10.1164/rccm.200802-309OC DOI: https://doi.org/10.1164/rccm.200802-309OC
Soto-Quiros M, Avila L, Platts-Mills TA, Hunt JF, Erdman DD, Carper H, Murphy DD, O et al. High Titers of IgE Antibody to Dust Mite Allergen and Risk for Wheezing among Asthmatic Children Infected with Rhinovirus. J Allergy Clin Immunol 2012; 129: 1499-1505 e1495. DOI: https://doi.org/10.1016/j.jaci.2012.03.040
Arshad SH, Karmaus W, Raza A, Kurukulaaratchy RJ, Matthews SM, Holloway JW, et al. The Effect of Parental Allergy on Childhood Allergic Diseases Depends on the Sex of the Child. J Allergy Clin Immunol 2012; 130: 427-434 e426. DOI: https://doi.org/10.1016/j.jaci.2012.03.042
Olenec JP, Kim WK, Lee WM, Vang F, Pappas TE, Salazar LE, Evans MD, et al. Weekly Monitoring of Children with Asthma for Infections and Illness During Common Cold Seasons. J Allergy Clin Immunol 2010; 125: 1001-1006 e1001. DOI: https://doi.org/10.1016/j.jaci.2010.01.059
Iwasaki J, Smith WA, Khoo SK, Bizzintino J, Zhang G, Cox DW, et al. Comparison of Rhinovirus Antibody Titers in Children with Asthma Exacerbations and Species-Specific Rhinovirus Infection. J Allergy Clin Immunol 2014; 134: 25-32 e21. DOI: https://doi.org/10.1016/j.jaci.2014.03.014