Defining the Epidemiology and Burden of Severe Respiratory Syncytial Virus Infection Among Infants and Children in Western Countries

Louis Bont, Paul A Checchia, Brigitte Fauroux, Josep Figueras-Aloy, Paolo Manzoni, Bosco Paes, Eric A F Simões, Xavier Carbonell-Estrany, Louis Bont, Paul A Checchia, Brigitte Fauroux, Josep Figueras-Aloy, Paolo Manzoni, Bosco Paes, Eric A F Simões, Xavier Carbonell-Estrany

Abstract

Introduction: The REGAL (RSV [respiratory syncytial virus] Evidence-a Geographical Archive of the Literature) series provides a comprehensive review of the published evidence in the field of RSV in Western countries over the last 20 years. This first of seven publications covers the epidemiology and burden of RSV infection.

Methods: A systematic review was undertaken for articles published between Jan 1, 1995 and Dec 31, 2015 across PubMed, Embase, The Cochrane Library, and Clinicaltrials.gov. Studies reporting data for hospital visits/admissions for RSV infection among children (≤18 years of age), as well as studies reporting RSV-associated morbidity, mortality, and risk factors were included. Study quality and strength of evidence (SOE) were graded using recognized criteria.

Result: 2315 studies were identified of which 98 were included. RSV was associated with 12-63% of all acute respiratory infections (ARIs) and 19-81% of all viral ARIs causing hospitalizations in children (high SOE). Annual RSV hospitalization (RSVH) rates increased with decreasing age and varied by a factor of 2-3 across seasons (high SOE). Studies were conflicting on whether the incidence of RSVH has increased, decreased, or remained stable over the last 20 years (moderate SOE). Length of hospital stay ranged from 2 to 11 days, with 2-12% of cases requiring intensive care unit admission (moderate SOE). Case-fatality rates were <0.5% (moderate SOE). Risk factors associated with RSVH included: male sex; age <6 months; birth during the first half of the RSV season; crowding/siblings; and day-care exposure (high SOE).

Conclusion: RSV infection remains a major burden on Western healthcare systems and has been associated with significant morbidity. Further studies focusing on the epidemiology of RSV infection (particularly in the outpatient setting), the impact of co-infection, better estimates of case-fatality rates and associated risk factors (all currently moderate/low SOE) are needed to determine the true burden of disease.

Funding: Abbvie.

Keywords: Acute respiratory infection; Bronchiolitis; Burden; Epidemiology; Lower respiratory tract infection; Respiratory syncytial virus.

Figures

Fig. 1
Fig. 1
PRISMA flow diagram: overall epidemiology and burden of severe respiratory syncytial virus (RSV) infection. The third reviewer (B. Rodgers-Gray) and X. Carbonell-Estrany were not required to resolve any disagreements during the review process

References

    1. Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, et al. Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet. 2010;375:1545–1555. doi: 10.1016/S0140-6736(10)60206-1.
    1. Haerskjold A, Kristensen K, Kamper-Jørgensen M, Andersen AMN, Ravn H, Stensballe LG. Risk factors for hospitalization for respiratory syncytial virus infection: a population-based cohort study of Danish children. Pediatr Infect Dis J. 2016;35:61–65.
    1. Glezen WP, Taber LH, Frank AL, Kasel JA. Risk of primary infection and reinfection with respiratory syncytial virus. Am J Dis Child. 1986;140:543–546.
    1. Gil-Prieto R, Gonzalez-Escalada A, Marín-García P, Gallardo-Pino C, Gil-de-Miguel A. Respiratory syncytial virus bronchiolitis in children up to 5 years of age in Spain: epidemiology and comorbidities: an observational study. Medicine (Baltimore) 2015;94:e831. doi: 10.1097/MD.0000000000000831.
    1. Simões EA, DeVincenzo JP, Boeckh M, Bont L, Crowe JE, Jr, Griffiths P, et al. Challenges and opportunities in developing respiratory syncytial virus therapeutics. J Infect Dis. 2015;211(Suppl 1):S1–S20. doi: 10.1093/infdis/jiu828.
    1. Vicente D, Montes M, Cilla G, Perez-Yarza EG, Perez-Trallero E. Hospitalization for respiratory syncytial virus in the paediatric population in Spain. Epidemiol Infect. 2003;131:867–872. doi: 10.1017/S0950268803008926.
    1. Fjaerli HO, Farstad T, Bratlid D. Hospitalisations for respiratory syncytial virus bronchiolitis in Akershus, Norway, 1993–2000: a population-based retrospective study. BMC Pediatr. 2004;4:25. doi: 10.1186/1471-2431-4-25.
    1. Greenough A, Alexander J, Burgess S, Bytham J, Chetcuti PAJ, Hagan J, et al. Health care utilisation of prematurely born, preschool children related to hospitalisation for RSV infection. Arch Dis Child. 2004;89:673–678. doi: 10.1136/adc.2003.036129.
    1. Paramore LC, Ciuryla V, Ciesla G, Liu L. Economic impact of respiratory syncytial virus-related illness in the US: an analysis of national databases. Pharmacoeconomics. 2004;22:275–284. doi: 10.2165/00019053-200422050-00001.
    1. Horn SD, Smout RJ. Effect of prematurity on respiratory syncytial virus hospital resource use and outcomes. J Pediatrics. 2003;143(5 Suppl):S133–S141. doi: 10.1067/S0022-3476(03)00509-2.
    1. Thorburn K. Pre-existing disease is associated with a significantly higher risk of death in severe respiratory syncytial virus infection. Arch Dis Child. 2009;94:99–103. doi: 10.1136/adc.2008.139188.
    1. Hervás D, Reina J, Yañez A, del Valle JM, Figuerola J, Hervás JA. Epidemiology of hospitalization for acute bronchiolitis in children: differences between RSV and non-RSV bronchiolitis. Eur J Clin Microbiol Infect Dis. 2012;31:1975–1981. doi: 10.1007/s10096-011-1529-y.
    1. Murray J, Bottle A, Sharland M, Modi N, Aylin P, Majeed A, Saxena S, Medicines for Neonates Investigator Group Risk factors for hospital admission with RSV bronchiolitis in England: a population-based birth cohort study. PLoS One. 2014;9:e89186. doi: 10.1371/journal.pone.0089186.
    1. Hall CB, Weinberg GA, Iwane MK, Blumkin AK, Edwards KM, Staat MA, et al. The burden of respiratory syncytial virus infection in young children. N Engl J Med. 2009;360:588–598. doi: 10.1056/NEJMoa0804877.
    1. Hall CB. The burgeoning burden of respiratory syncytial virus among children. Infect Disord Drug Targets. 2012;12:92–97. doi: 10.2174/187152612800100099.
    1. Hall CB, Weinberg GA, Blumkin AK, Edwards KM, Staat MA, Schultz AF, et al. Respiratory syncytial virus-associated hospitalizations among children less than 24 months of age. Pediatrics. 2013;132:e341–e348. doi: 10.1542/peds.2013-0303.
    1. Broadbent L, Groves H, Shields MD, Power UF. Respiratory syncytial virus, an ongoing medical dilemma: an expert commentary on respiratory syncytial virus prophylactic and therapeutic pharmaceuticals currently in clinical trials. Influenza Other Respir Viruses. 2015;9:169–178. doi: 10.1111/irv.12313.
    1. World Health Organization. Research needs for the Battle against Respiratory Viruses (BRaVe). Background document 2013. . Accessed 6 Apr 2016.
    1. The IMpact-RSV Study Group Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. Pediatrics. 1998;102:531–537. doi: 10.1542/peds.102.3.531.
    1. Committee on Infectious Diseases and Bronchiolitis Guidelines Committee Updated guidance for palivizumab prophylaxis among infants and young children at increased risk of hospitalization for respiratory syncytial virus infection. Pediatrics. 2014;134:415–420. doi: 10.1542/peds.2014-1665.
    1. Modjarrad K, Giersing B, Kaslow DC, Smith PG, Moorthy VS, WHO RSV Vaccine Consultation Expert Group WHO consultation on respiratory syncytial virus vaccine development report from a World Health Organization Meeting held on 23–24 March 2015. Vaccine. 2016;4(34):190–197. doi: 10.1016/j.vaccine.2015.05.093.
    1. OCEBM Levels of Evidence Working Group. The Oxford 2011 levels of evidence. Oxford Centre for Evidence-Based Medicine. . Accessed Aug 2015.
    1. OCEBM Levels of Evidence Working Group. The Oxford 2009 Levels of Evidence. Oxford Centre for Evidence-Based Medicine . Accessed Jan 2016.
    1. Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17:1–12. doi: 10.1016/0197-2456(95)00134-4.
    1. Viswanathan M, Berkman ND, Dryden DM, Hartling L. Assessing risk of bias and confounding in observational studies of interventions or exposures: further development of the RTI Item Bank. Methods Research Report. (Prepared by RTI–UNC Evidence-based Practice Center under Contract No. 290-2007-10056-I). AHRQ Publication No. 13-EHC106-EF. Rockville, MD: Agency for Healthcare Research and Quality. 2013. . Accessed Jan 2016.
    1. Higgins JPT, Altman DG (editors). Chapter 8: assessing risk of bias in included studies. In: Higgins JPT, Gree S, editors. Cochrane handbook for systematic reviews of interventions. Version 5.0.1 [updated September 2008]. The Cochrane Collaboration 2008. . Accessed Jan 2016.
    1. Constantopoulos AG, Kafetzis DA, Syrogiannopoulos GA, Roilides EJ, Malaka-Zafiriu EE, Sbyrakis SS, et al. Burden of respiratory syncytial viral infections on paediatric hospitals: a two-year prospective epidemiological study. Eur J Clin Microbiol Infect Dis. 2002;21:102–107. doi: 10.1007/s10096-001-0668-y.
    1. Salvador García C, Moreno Docóna A, Piñero JA, Alfayate Miguelez S, Iborra Bendicho MA. Aetiology of bronchiolitis in hospitalised children in South-East Spain. An Pediatr (Barc). 2012;77:386–390. doi: 10.1016/j.anpedi.2011.09.021.
    1. Weigl JA, Puppe W, Schmitt HJ. Incidence of respiratory syncytial virus-positive hospitalizations in Germany. Eur J Clin Microbiol Infect Dis. 2001;20:452–459.
    1. Zuccotti G, Dilillo D, Zappa A, Galli E, Amendola A, Martinelli M, et al. Epidemiological and clinical features of respiratory viral infections in hospitalized children during the circulation of influenza virus A(H1N1) 2009. Influenza Other Respir Viruses. 2011;5:e528–e534. doi: 10.1111/j.1750-2659.2011.00264.x.
    1. Frassanito A, Nicolai A, Nenna R, Cangiano G, Papasso S, Mancino E, et al. Acute viral respiratory tract infections and wheezing at follow-up in children <3 years. Eur Respir J. 2015;46(Suppl 59):PA1319. doi: 10.1183/13993003.congress-2015.PA1319.
    1. Ferrara M, Cangiano G, Papasso S, Nicolai A, Evangelisti M, Nenna R, et al. Bronchiolitis: a 9 years epidemic seasons analysis. Eur Respir J. 2014;44(Suppl 58):P1258.
    1. Lanari M, Giovannini M, Giuffré L, Marini A, Rondini G, Rossi GE, the Investigators R.A.DA.R. Study Group et al. Prevalence of respiratory syncytial virus infection in Italian infants hospitalized for acute lower respiratory tract infections, and association between respiratory syncytial virus infection risk factors and disease severity. Pediatr Pulmonol. 2002;33:458–465. doi: 10.1002/ppul.10047.
    1. Müller-Pebody B, Edmunds WJ, Zambon MC, Gay NJ, Crowcroft NS. Contribution of RSV to bronchiolitis and pneumonia-associated hospitalizations in English children, April 1995–March 1998. Epidemiol Infect. 2002;129:99–106. doi: 10.1017/S095026880200729X.
    1. Stockman LJ, Curns AT, Anderson LJ, Fischer-Langley G. Respiratory syncytial virus-associated hospitalizations among infants and young children in the United States, 1997–2006. Pediatr Infect Dis J. 2012;31:5–9. doi: 10.1097/INF.0b013e31822e68e6.
    1. Santibanez P, Gooch K, Vo P, Lorimer M, Sandino Y. Acute care utilization due to hospitalizations for pediatric lower respiratory tract infections in British Columbia, Canada. BMC Health Serv Res. 2012;12:451. doi: 10.1186/1472-6963-12-451.
    1. Ajayi-Obe EK, Coen PG, Handa R, Hawrami K, Aitken C, McIntosh EDG, et al. Influenza A and respiratory syncytial virus hospital burden in young children in East London. Epidemiol Infect. 2008;136:1046–1058. doi: 10.1017/S0950268807009557.
    1. Corsello G, Di Carlo P, Salsa L, Gabriele B, Meli L, Bruno S, et al. Respiratory syncytial virus infection in a Sicilian pediatric population: risk factors, epidemiology, and severity. Allergy Asthma Proc. 2008;29:205–210. doi: 10.2500/aap.2008.29.3101.
    1. Calvo C, Pozo F, García-García ML, Sanchez M, Lopez-Valero M, Pérez-Breña P. Detection of new respiratory viruses in hospitalized infants with bronchiolitis: a three-year prospective study. Acta Paediatr. 2010;99:883–887. doi: 10.1111/j.1651-2227.2010.01714.x.
    1. Díez Domingo J, Ridao López M, Ubeda Sansano I, Ballester Sanz A. Incidence and cost of hospitalizations for bronchiolitis and respiratory syncytial virus infections in the autonomous community of Valencia in Spain (2001 and 2002) An Pediatr (Barc). 2006;65:325–330. doi: 10.1157/13093515.
    1. García García ML, Ordobás Gabin M, Calvo Reya C, González Alvarez M, Aguilar Ruiz J, Arregui Sierra A, et al. Viral infection of the lower respiratory tract in hospitalized infants: etiology, clinical features and risk factors. An Esp Pediatr. 2001;55:101–107. doi: 10.1016/S1695-4033(01)77644-8.
    1. García-García ML, Calvo C, Pozo F, Villadangos PA, Pérez-Breña P, Casas I. Spectrum of respiratory viruses in children with community-acquired pneumonia. Pediatr Infect Dis J. 2012;31:808–813. doi: 10.1097/INF.0b013e3182568c67.
    1. Artiles-Campelo F, Pérez-González MC, Caballero-Hidalgo A, Pena-López MJ. Etiology of acute viral respiratory tract infections in children from Gran Canaria, the Canary Islands (Spain) Enferm Infec Microbiol Clin. 2006;24:556–561. doi: 10.1157/13093875.
    1. García CG, Bhore R, Soriano-Fallas A, Trost M, Chason R, Ramilo O, et al. Risk factors in children hospitalized with RSV bronchiolitis versus non-RSV bronchiolitis. Pediatrics. 2010;126:e1453–e1460. doi: 10.1542/peds.2010-0507.
    1. Iwane MK, Edwards KM, Szilagyi PG, Walker FJ, Griffin MR, Weinberg GA, New Vaccine Surveillance Network et al. Population-based surveillance for hospitalizations associated with respiratory syncytial virus, influenza virus, and parainfluenza viruses among young children. Pediatrics. 2004;113:1758–1764. doi: 10.1542/peds.113.6.1758.
    1. Mlinaric-Galinovic G, Vilibic-Cavlek T, Ljubin-Sternak S, Drazenovic V, Galinovic I, Tomic V, et al. Eleven consecutive years of respiratory syncytial virus outbreaks in Croatia. Pediatr Int. 2009;51:237–240. doi: 10.1111/j.1442-200X.2008.02723.x.
    1. Gooskens J, van der Ploeg V, Sukhai RN, Vossen ACTM, Eric CJ, Claas ECJ, et al. Clinical evaluation of viral acute respiratory tract infections in children presenting to the emergency department of a tertiary referral hospital in the Netherlands. BMC Pediatr. 2014;14:297. doi: 10.1186/s12887-014-0297-0.
    1. El-Hajje MJ, Lambe C, Moulin F, de Souremain N, Pons-Catalano C, Chalumeau M, et al. The burden of respiratory viral disease in hospitalized children in Paris. Eur J Pediatr. 2008;167:435–436. doi: 10.1007/s00431-007-0529-5.
    1. Zhou H, Thompson WW, Viboud CG, Ringholz CM, Cheng P-Y, Steiner C, et al. Hospitalizations associated with influenza and respiratory syncytial virus in the United States, 1993–2008. Clin Infect Dis. 2012;54:1427–1436. doi: 10.1093/cid/cis211.
    1. Medici MC, Arcangeletti MC, Rossi GA, Lanari M, Merollo R, Paparatti UD, Osservatorio VRS Study Group et al. Four year incidence of respiratory syncytial virus infection in infants and young children referred to emergency departments for lower respiratory tract diseases in Italy: the “Osservatorio VRS” Study (2000-2004) New Microbiol. 2006;29:35–43.
    1. Zomer-Kooijker K, Uiterwaal CS, van der Gugten AC, Wilbrink B, Bont LJ, van der Ent CK. Decreased lung function precedes severe respiratory syncytial virus infection and post-respiratory syncytial virus wheeze in term infants. Eur Respir J. 2014;44:666–674. doi: 10.1183/09031936.00009314.
    1. Tatochenko V, Uchaikin V, Gorelov A, Gudkov K, Campbell A, Schulz G, et al. Epidemiology of respiratory syncytial virus in children ≤2 years of age hospitalized with lower respiratory tract infections in the Russian Federation: a prospective, multicenter study. Clin Epidemiol. 2010;21(2):221–227.
    1. Bicer S, Giray T, Çöl D, Çiler Erdağ G, Vitrinel A, Yesim Gürol Y, et al. Virological and clinical characterizations of respiratory infections in hospitalized children. Ital J Pediatr. 2013;39:22. doi: 10.1186/1824-7288-39-22.
    1. Hacımustafaoğlu M, Celebi S, Bozdemir SE, Ozgür T, Ozcan I, Güray A, et al. RSV frequency in children below 2 years hospitalized for lower respiratory tract infections. Turk J Pediatr. 2013;55:130–139.
    1. Turkish Neonatal Society The seasonal variations of respiratory syncytial virus infections in Turkey: a 2-year epidemiological study. Turk J Pediatr. 2012;54:216–222.
    1. Resch B, Gusenleitner W, Mandl C, Müller W. Epidemiology of respiratory syncytial virus infection in Southern Austria. Pediatr Infect Dis J. 2000;19:587–588. doi: 10.1097/00006454-200006000-00030.
    1. Resch B, Gusenleitner W, Müller W. The impact of respiratory syncytial virus infection: a prospective study in hospitalized infants younger than 2 years. Infection. 2002;30:193–197. doi: 10.1007/s15010-002-2122-1.
    1. Boyce TG, Mellen BG, Mitchel EF, Jr, Wright PF, Griffin MR. Rates of hospitalization for respiratory syncytial virus infection among children in medicaid. J Pediatr. 2000;137:865–870. doi: 10.1067/mpd.2000.110531.
    1. Fleming DM, Pannell RS, Elliot AJ, Cross KW. Respiratory illness associated with influenza and respiratory syncytial virus infection. Arch Dis Child. 2005;90:741–746. doi: 10.1136/adc.2004.063461.
    1. Bourgeois FT, Valim C, McAdam AJ, Mandl KD. Relative impact of influenza and respiratory syncytial virus in young children. Pediatrics. 2009;124:e1072–e1080. doi: 10.1542/peds.2008-3074.
    1. Svensson C, Berg K, Sigurs N, Trollfors B. Incidence, risk factors and hospital burden in children under five years of age hospitalised with respiratory syncytial virus infections. Acta Paediatr. 2015;104:922–926. doi: 10.1111/apa.13061.
    1. Leader S, Kohlhase K. Recent trends in severe respiratory syncytial virus (RSV) among US infants, 1997 to 2000. J Pediatr. 2003;143:S127–S132. doi: 10.1067/S0022-3476(03)00510-9.
    1. Deshpande SA, Northern V. The clinical and health economic burden of respiratory syncytial virus disease among children under 2 years of age in a defined geographical area. Arch Dis Child. 2003;88:1065–1069. doi: 10.1136/adc.88.12.1065.
    1. Grimaldi M, Cornet B, Milou C, Gouyon JB. Prospective regional study of an epidemic of respiratory syncytial virus (RSV) bronchiolitis. Arch Pediatr. 2002;9:572–580. doi: 10.1016/S0929-693X(01)00923-X.
    1. Johnson JI, Ratard R. Respiratory syncytial virus-associated hospitalizations in Louisiana. J La State Med Soc. 2012;164:268–273.
    1. Liese JG, Grill E, Fischer B, Roeckl-Wiedmann I, Carr D, Belohradsky BH. Incidence and risk factors of respiratory syncytial virus-related hospitalizations in premature infants in Germany. Eur J Pediatr. 2003;162:230–236.
    1. McCormick J, Tubman R. Readmission with respiratory syncytial virus (RSV) infection among graduates from a neonatal intensive care unit. Pediatr Pulmonol. 2002;34:262–266. doi: 10.1002/ppul.10169.
    1. Shay DK, Holman RC, Newman RD, Liu LL, Stout JW, Anderson LJ. Bronchiolitis-associated hospitalizations among US children, 1980–1996. JAMA. 1999;282:1440–1446. doi: 10.1001/jama.282.15.1440.
    1. Langley JM, LeBlanc JC, Smith B, Wang EEL. Increasing incidence of hospitalization for bronchiolitis among Canadian children, 1980–2000. J Infect Dis. 2003;188:1764–1767. doi: 10.1086/379740.
    1. Hasegawa K, Tsugawa Y, Brown DF, Mansbach JM, Camargo CA., Jr Trends in bronchiolitis hospitalizations in the United States, 2000–2009. Pediatrics. 2013;132:28–36. doi: 10.1542/peds.2012-3877.
    1. Fournel I, Soulias M, Bour JB, Gouyon JB, Huet F, Aho LS. Evolution of the number of rotavirus and respiratory syncytial virus infections in children hospitalised in a French university hospital between 1998 and 2005. Pathol Biol (Paris) 2010;58:406–414. doi: 10.1016/j.patbio.2008.10.003.
    1. Ortiz de Lejarazu R, Rojo S, Bermejo-Martín JF, Almansa R, Solis P, Tamames S, et al. Trend and seasonality of respiratory syncytial virus in Valladolid (Spain) during 1993–2010. Acta Pediatr Esp. 2012;70:1–8.
    1. Centers for Disease Control and Prevention (CDC) Respiratory syncytial virus—United States, July 2007–June 2011. MMWR Morb Mortal Wkly Rep. 2011;60:1203–1206.
    1. Centers for Disease Control and Prevention (CDC) Respiratory syncytial virus activity—United States, July 2011–January 2013. MMWR Morb Mortal Wkly Rep. 2013;62:141–144.
    1. Alonso A, Andres JM, Garmendia JR, Diez I, Gil JM, Ardura J. Bronchiolitis due to respiratory syncytial virus in hospitalized children: a study of seasonal rhythm. Acta Paediatr. 2007;96:731–735. doi: 10.1111/j.1651-2227.2007.00266.x.
    1. Calvo C, García-García ML, Pozo F, Paula G, Molinero M, Caldéron A, et al. Respiratory syncytial virus coinfections with rhinovirus and human bocavirus in hospitalized children. Medicine (Baltimore). 2015;94:e1788. doi: 10.1097/MD.0000000000001788.
    1. Tanner H, Boxall E, Osman H. Respiratory viral infections during the 2009–2010 winter season in Central England, UK: incidence and patterns of multiple virus coinfections. Eur J Clin Microbiol Infect Dis. 2012;3:3001–3006. doi: 10.1007/s10096-012-1653-3.
    1. Thorburn K, Harigopal S, Reddy V, Taylor N, van Saene HKF. High incidence of pulmonary bacterial co-infection in children with severe respiratory syncytial virus (RSV) bronchiolitis. Thorax. 2006;61:611–615. doi: 10.1136/thx.2005.048397.
    1. Weigl JA, Puppe W, Rockahr S, Schmitt HJ. Burden of disease in hospitalized RSV-positive children in Germany. Klin Padiatr. 2002;214:334–342. doi: 10.1055/s-2002-35365.
    1. Martínez-Roig A, Salvadó M, Caballero-Rabasco MA, Sánchez-Buenavida A, López-Segura N, Bonet-Alcaina M. Viral coinfection in childhood respiratory tract infections. Arch Bronconeumol. 2015;51:5–9. doi: 10.1016/j.arbres.2014.01.018.
    1. Calvo C, García-García ML, Blanco C, Vázquez MC, Frías ME, Pérez-Breña P, et al. Multiple simultaneous viral infections in infants with acute respiratory tract infections in Spain. J Clin Virol. 2008;42:268–272. doi: 10.1016/j.jcv.2008.03.012.
    1. Asner SA, Rose W, Petrich A, Richardson S, Tran DJ. Is virus coinfection a predictor of severity in children with viral respiratory infections? Clin Microbiol Infect. 2015;21:264.e1–6.
    1. Kristensen K, Dahm T, Frederiksen PS, Ibsen J, Iyore E, Mller Jensen E, et al. Epidemiology of respiratory syncytial virus infection requiring hospitalization in East Denmark. Pediatr Infect Dis J. 1998;17:996–1000. doi: 10.1097/00006454-199811000-00006.
    1. Tsolia MN, Kafetzis D, Danelatou K, Astra H, Kallergi K, Spyridis P, et al. Epidemiology of respiratory syncytial virus bronchiolitis in hospitalized infants in Greece. Eur J Epidemiol. 2003;18:55–61. doi: 10.1023/A:1022556215190.
    1. Flores P, Rebelo-de-Andrade H, Gonçalves P, Guiomar R, Carvalho C, Sousa EN, et al. Bronchiolitis caused by respiratory syncytial virus in an area of Portugal: epidemiology, clinical features, and risk factors. Eur J Clin Microbiol Infect Dis. 2004;23:39–45. doi: 10.1007/s10096-003-1040-1.
    1. Eriksson M, Bennet R, Rotzén-Ostlund M, von Sydow M, Wirgart BZ. Population-based rates of severe respiratory syncytial virus infection in children with and without risk factors, and outcome in a tertiary care setting. Acta Paediatr. 2002;91:593–598. doi: 10.1111/j.1651-2227.2002.tb03282.x.
    1. Brooks AM, McBride JT, McConnochie KM, Aviram M, Long C, Hall CB. Predicting deterioration in previously healthy infants hospitalized with respiratory syncytial virus infection. Pediatrics. 1999;104:463–467. doi: 10.1542/peds.104.3.463.
    1. Gijtenbeek RG, Kerstjens JM, Reijneveld SA, Duiverman EJ, Bos AF, Vrijlandt EJLE. RSV infection among children born moderately preterm in a community-based cohort. Eur J Pediatr. 2015;174:435–442. doi: 10.1007/s00431-014-2415-2.
    1. Brandenburg AH, Jeannet P-Y, Steensel-Moll HAV, Ott A, Rothbarth PH, Wunderli W, et al. Local variability in respiratory syncytial virus disease severity. Arch Dis Child. 1997;77:410–414. doi: 10.1136/adc.77.5.410.
    1. Wang EE, Law BJ, Stephens D. Pediatric Investigators Collaborative Network on Infections in Canada (PICNIC) prospective study of risk factors and outcomes in patients hospitalized with respiratory syncytial viral lower respiratory tract infection. J Pediatr. 1995;126:212–219. doi: 10.1016/S0022-3476(95)70547-3.
    1. Soilly AL, Ferdynus C, Desplanches O, Grimaldi M, Gouyon JB. Paediatric intensive care admissions for respiratory syncytial virus bronchiolitis in France: results of a retrospective survey and evaluation of the validity of a medical information system programme. Epidemiol Infect. 2012;140:608–616. doi: 10.1017/S0950268811001208.
    1. Berger A, Obwegeser E, Aberle SW, Langgartner M, Popow-Kraupp T. Nosocomial transmission of respiratory syncytial virus in neonatal intensive care and intermediate care units: a prospective epidemiologic study. Pediatr Infect Dis J. 2010;29:669–670. doi: 10.1097/INF.0b013e3181d76d61.
    1. Simon A, Müller A, Khurana K, Engelhart S, Exner M, Schildgen O, DSM RSV Paed Study Group et al. Nosocomial infection: a risk factor for a complicated course in children with respiratory syncytial virus infection—results from a prospective multicenter German surveillance. Int J Hyg Environ Health. 2008;211(3–4):241–250. doi: 10.1016/j.ijheh.2007.07.020.
    1. Alan S, Erdeve O, Cakir U, Akduman H, Zenciroglu A, Akcakus M, et al. Outcome of the Respiratory Syncytial Virus related acute lower respiratory tract infection among hospitalized newborns: a prospective multicenter study. J Matern Fetal Neonatal Med. 2015;12:1–8. doi: 10.3109/14767058.2015.1109619.
    1. Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2095–2128. doi: 10.1016/S0140-6736(12)61728-0.
    1. Thompson WW, Shay DK, Weintraub E, et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA. 2003;289:179–186. doi: 10.1001/jama.289.2.179.
    1. Berkley JA, Munywoki P, Ngama M, et al. Viral etiology of severe pneumonia among Kenyan infants and children. JAMA. 2010;303:2051–2057. doi: 10.1001/jama.2010.675.
    1. Nokes DJ, Ngama M, Bett A, et al. Incidence and severity of respiratory syncytial virus pneumonia in rural Kenyan children identified through hospital surveillance. Clin Infect Dis. 2009;49:1341–1349. doi: 10.1086/606055.
    1. Shay DK, Holman RC, Roosevelt GE, Clarke MJ, Andersen LJ. Bronchiolitis-associated mortality and estimates of respiratory syncytial virus-associated deaths among US children, 1979–1997. J Infect Dis. 2001;183:16–22. doi: 10.1086/317655.
    1. Fryzek JP, Martone WJ, Groothuis JR. Trends in chronologic age and infant respiratory syncytial virus hospitalization: an 8-year cohort study. Adv Ther. 2011;28:195–201. doi: 10.1007/s12325-010-0106-6.
    1. Bradley JP, Bacherier LB, Bonfiglio J, Schechtman KB, Strunk R, Storch G, et al. Severity of respiratory syncytial virus is affected by cigarette smoke exposure and atopy. Pediatrics. 2005;115:7–14.
    1. von Linstow ML, Høgh M, Nordbø SA, Eugen-Olsen J, Koch A, Høgh B. A community study of clinical traits and risk factors for human metapneumovirus and respiratory syncytial virus infection during the first year of life. Eur J Pediatr. 2008;167:1125–1133. doi: 10.1007/s00431-007-0643-4.
    1. Schuurhof A, Bont L, Siezen CL, Hodemaekers H, van Houwelingen HC, Kimman TG, et al. Interleukin-9 polymorphism in infants with respiratory syncytial virus infection: an opposite effect in boys and girls. Pediatr Pulmonol. 2010;45:608–613.
    1. Choudhuri JA, Ogden LG, Ruttenber AJ, Thomas DS, Todd JK, Simoes EA. Effect of altitude on hospitalizations for respiratory syncytial virus infection. Pediatrics. 2006;117:349–356. doi: 10.1542/peds.2004-2795.
    1. Kristensen K, Fisker N, Haerskjold A, Henrik R, Simoes EAF, Stensballe L. Caesarean section and hospitalization for respiratory syncytial virus infection: a population-based study. Pediatr Infect Dis J. 2015;34:145–148. doi: 10.1097/INF.0000000000000552.
    1. Iwane MK, Chaves SS, Szilagyi PG, Edwards KM, Hall CB, Staat MA, et al. Disparities between black and white children in hospitalizations associated with acute respiratory illness and laboratory-confirmed influenza and respiratory syncytial virus in 3 US counties—2002–2009. Am J Epidemiol. 2013;177:656–665. doi: 10.1093/aje/kws299.
    1. Sangaré L, Curtis MP, Ahmad S. Hospitalization for respiratory syncytial virus among California infants: disparities related to race, insurance, and geography. J Pediatr. 2006;149:373–377. doi: 10.1016/j.jpeds.2006.04.063.
    1. Nielsen HE, Siersma V, Andersen S, Gahrn-Hansen B, Mordhorst CH, Nørgaard-Pedersen B, et al. Respiratory syncytial virus infection—risk factors for hospital admission: a case-control study. Acta Paediatr. 2003;92:1314–1321. doi: 10.1111/j.1651-2227.2003.tb00502.x.
    1. Rossi GA, Medici MC, Arcangeletti MC, Lanari M, Merolla R, Paparatti U, et al. Risk factors for severe RSV-induced lower respiratory tract infection over four consecutive epidemics. Eur J Pediatr. 2007;166:1267–1272. doi: 10.1007/s00431-007-0418-y.
    1. Cilla G, Sarasua A, Montes M, Arostegui N, Vicente D, Pérez-Yarza E, et al. Risk factors for hospitalization due to respiratory syncytial virus infection among infants in the Basque Country, Spain. Epidemiol Infect. 2006;134:506–513. doi: 10.1017/S0950268805005571.
    1. Belderbos ME, Houben ML, Wilbrink B, Lentjes E, Bloemen EM, Kimpen JL, et al. Cord blood vitamin D deficiency is associated with respiratory syncytial virus bronchiolitis. Pediatrics. 2011;127:e1513–e1520. doi: 10.1542/peds.2010-3054.
    1. Stensballe LG, Kristensen K, Simoes EA, Jensen H, Nielsen J, Benn CS, et al. Atopic disposition, wheezing, and subsequent respiratory syncytial virus hospitalization in Danish children younger than 18 months: a nested case-control study. Pediatrics. 2006;118:e1360–e1368. doi: 10.1542/peds.2006-0907.
    1. Trefny P, Stricker T, Baerlocher C, Sennhauser FH. Family history of atopy and clinical course of RSV infection in ambulatory and hospitalized infants. Pediatr Pulmonol. 2000;30:302–306. doi: 10.1002/1099-0496(200010)30:4<302::AID-PPUL5>;2-R.
    1. Lapeña S, Robles MB, Castañón L, Martínez JP, Reguero S, Alonso MP, et al. Climatic factors and lower respiratory tract infection due to respiratory syncytial virus in hospitalised infants in northern Spain. Eur J Epidemiol. 2005;20:271–276. doi: 10.1007/s10654-004-4539-6.
    1. Vandini S, Corvaglia L, Alessandroni R, Aquilano G, Marsico C, Spinelli M, et al. Respiratory syncytial virus infection in infants and correlation with meteorological factors and air pollutants. Ital J Pediatr. 2013;39:1. doi: 10.1186/1824-7288-39-1.
    1. Karr CJ, Rudra CB, Miller KA, Gould TR, Larson T, Sathyanarayana S, et al. Infant exposure to fine particulate matter and traffic and risk of hospitalization for RSV bronchiolitis in a region with lower ambient air pollution. Environ Res. 2009;109:321–327. doi: 10.1016/j.envres.2008.11.006.
    1. Jansson L, Nilsson P, Olsson M. Socioeconomic environmental factors and hospitalization for acute bronchiolitis during infancy. Acta Paediatr. 2002;91:335–338. doi: 10.1111/j.1651-2227.2002.tb01725.x.

Source: PubMed

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