Social, economic, and health impact of the respiratory syncytial virus: a systematic search

BMC Infectious Diseases

Pablo Lázaro⁵  Noelia Alfaro⁵  Antonio Javier Blasco⁵  María Dolores Aguilar⁵  Manuel Sánchez-Luna²  José A Melero⁴  Eduardo G Pérez-Yarza³  Javier Díez-Domingo¹ 

[1] Centre of Public Health Research of Valencia-FISABIO, Valencia, Spain;Neonatology Division, Hospital General Universitario Gregorio Marañón, Madrid, Spain;Department of Pediatrics, University of the Basque Country (UPV/EHU), San Sebastián, Spain;National Center of Microbiology and CIBER of Respiratory Diseases, Instituto de Salud Carlos III, Madrid, Spain;Advanced Techniques in Health Services Research, Madrid, Spain

关键词: Health impact;    Social impact;    Respiratory syncytial virus;   

Others  :  1122160
DOI  :  10.1186/s12879-014-0544-x

 received in 2013-09-28, accepted in 2014-10-06,  发布年份 2014

【 摘 要 】

Background

Bronchiolitis caused by the respiratory syncytial virus (RSV) and its related complications are common in infants born prematurely, with severe congenital heart disease, or bronchopulmonary dysplasia, as well as in immunosuppressed infants. There is a rich literature on the different aspects of RSV infection with a focus, for the most part, on specific risk populations. However, there is a need for a systematic global analysis of the impact of RSV infection in terms of use of resources and health impact on both children and adults. With this aim, we performed a systematic search of scientific evidence on the social, economic, and health impact of RSV infection.

Methods

A systematic search of the following databases was performed: MEDLINE, EMBASE, Spanish Medical Index, MEDES-MEDicina in Spanish, Cochrane Plus Library, and Google without time limits. We selected 421 abstracts based on the 6,598 articles identified. From these abstracts, 4 RSV experts selected the most relevant articles. They selected 65 articles. After reading the full articles, 23 of their references were also selected. Finally, one more article found through a literature information alert system was included.

Results

The information collected was summarized and organized into the following topics: 1. Impact on health (infections and respiratory complications, mid- to long-term lung function decline, recurrent wheezing, asthma, other complications such as otitis and rhino-conjunctivitis, and mortality; 2. Impact on resources (visits to primary care and specialists offices, emergency room visits, hospital admissions, ICU admissions, diagnostic tests, and treatments); 3. Impact on costs (direct and indirect costs); 4. Impact on quality of life; and 5. Strategies to reduce the impact (interventions on social and hygienic factors and prophylactic treatments).

Conclusions

We concluded that 1. The health impact of RSV infection is relevant and goes beyond the acute episode phase; 2. The health impact of RSV infection on children is much better documented than the impact on adults; 3. Further research is needed on mid- and long-term impact of RSV infection on the adult population, especially those at high-risk; 4. There is a need for interventions aimed at reducing the impact of RSV infection by targeting health education, information, and prophylaxis in high-risk populations.

【 授权许可】

   
2014 Díez-Domingo et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Diagnosis and management of bronchiolitis Pediatrics 2006, 118(4):1774-1793.
• [2]Evidence based clinical practice guideline for medical management of bronchiolitis in infants less than 1 year of age presenting with a first time episode. Children’s Hospital Medical Center, Cincinnati (OH); 2006.
• [3][http://www.aepap.org/gvr/pdf/bronquiolitis_p_gvr_4_2009.pdf] webcite Callen M, Torregrosa MJ, Bamonde L, Grupo de Vías Respiratorias: Diagnóstico y tratamiento en Atención Primaria. Protocolo del GvR (publicación P-GvR-4). []
• [4]Bronchiolitis in children: A national clinical guideline. SIGN, UK; 2006.
• [5]Bloemers BL, van Furth AM, Weijerman ME, Gemke RJ, Broers CJ, van den Ende K, Kimpen JL, Strengers JL, Bont LJ: Down syndrome: a novel risk factor for respiratory syncytial virus bronchiolitis - a prospective birth-cohort study. Pediatrics 2007, 120(4):e1076-e1081.
• [6]Flight WG, Mutton KJ, Isalska B, Bright-Thomas RJ, Jones AM: A comparison of three different specimen types for the diagnosis of viral respiratory infections in adults with cystic fibrosis. Thorax 2011, 66:A23-A24.
• [7]Nadal D, Wunderli W, Meurmann O, Briner J, Hirsiq J: Isolation of respiratory syncytial virus from liver tissue and extrahepatic biliary atresia material. Scand J Infect Dis 1990, 22(1):91-93.
• [8]Billings JL, Hertz MI, Savik K, Wendt CH: Respiratory viruses and chronic rejection in lung transplant recipients. J Heart Lung Transplant 2002, 21(5):559-566.
• [9]Agius G, Dindinaud G, Biggar RJ, Peyre R, Vaillant V, Ranger S, Poupet JY, Cisse MF, Castets M: An epidemic of respiratory syncytial virus in elderly people: clinical and serological findings. J Med Virol 1990, 30(2):117-127.
• [10]Falsey AR, Cunningham CK, Barker WH, Kouides RW, Yuen JB, Menegus M, Weiner LB, Bonville CA, Betts RF: Respiratory syncytial virus and influenza A infections in the hospitalized elderly. J Infect Dis 1995, 172(2):389-394.
• [11]Falsey AR, Treanor JJ, Betts RF, Walsh EE: Viral respiratory infections in the institutionalized elderly: clinical and epidemiologic findings. J Am Geriatr Soc 1992, 40(2):115-119.
• [12]Fransén H, Sterner G, Forsgren M, Heigl Z, Wolontis S, Svedmyr A, Tunevall G: Acute lower respiratory illness in elderly patients with respiratory syncytial virus infection. Acta Med Scand 1967, 182(3):323-330.
• [13]Fleming DM, Cross KW: Respiratory syncytial virus or influenza? Lancet 1993, 342(8886–8887):1507-1510.
• [14]Nicholson KG: Impact of influenza and respiratory syncytial virus on mortality in England and Wales from January 1975 to December 1990. Epidemiol Infect 1996, 116(1):51-63.
• [15]Englund JA, Sullivan CJ, Jordan MC, Dehner LP, Vercellotti GM, Balfour HH Jr: Respiratory syncytial virus infection in immunocompromised adults. Ann Intern Med 1988, 109(3):203-208.
• [16]Walsh EE, Falsey AR, Hennessey PA: Respiratory syncytial virus and other infections in persons with chronic cardiopulmonary disease. Am J Respir Crit Care Med 1999, 160(3):791-795.
• [17]Falsey AR, Walsh EE: Respiratory syncytial virus infection in adults. Clin Microbiol Rev 2000, 13(3):371-384.
• [18]Nair H, Nokes DJ, Gessner BD, Dherani M, Madhi SA, Singleton RJ, O’Brien KL, Roca A, Wright PF, Bruce N, Chandran A, Theodoratou E, Sutanto A, Sedyaningsih ER, Ngama M, Munywoki PK, Kartasasmita C, Simoes EA, Rudan I, Weber MW, Campbell H: Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: a systematic review and meta-analysis. Lancet 2010, 375(9725):1545-1555.
• [19]Prescott WA Jr, Doloresco F, Brown J, Paladino JA: Cost effectiveness of respiratory syncytial virus prophylaxis: a critical and systematic review. PharmacoEconomics 2010, 28(4):279-293.
• [20]Broughton S, Roberts A, Fox G, Pollina E, Zuckerman M, Chaudhry S, Greenough A: Prospective study of healthcare utilisation and respiratory morbidity due to RSV infection in prematurely born infants. Thorax 2005, 60(12):1039-1044.
• [21]Medrano LC, García-Guereta L: Community-acquired respiratory infections in young children with congenital heart diseases in the palivizumab era: the Spanish 4-season civic epidemiologic study. Pediatr Infect Dis J 2010, 29(12):1077-1082.
• [22]Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE: Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 2005, 352(17):1749-1759.
• [23]Milstone AM, Perl TM, Valsamakis A: Epidemiology of respiratory viruses in children admitted to an infant/toddler unit. Am J Infect Control 2012, 40(5):462-464.
• [24]Widmer K, Zhu Y, Williams JV, Griffin MR, Edwards KM, Talbot HK: Rates of hospitalizations for respiratory syncytial virus, human metapneumovirus, and influenza virus in older adults. J Infect Dis 2012, 206(1):56-62.
• [25]Cilla G, Onate E, Pérez-Yarza EG, Montes M, Vicente D, Pérez-Trallero E: Viruses in community-acquired pneumonia in children aged less than 3 years old: High rate of viral coinfection. J Med Virol 2008, 80(10):1843-1849.
• [26]García-García ML, Calvo C, Pozo F, Villadangos PA, Pírez-Brena P, Casas I: Spectrum of respiratory viruses in children with community-acquired pneumonia. Pediatr Infect Dis J 2012, 31(8):808-813.
• [27]Johansson N, Kalin M, Hedlund J: Clinical impact of combined viral and bacterial infection in patients with community-acquired pneumonia. Scand J Infect Dis 2011, 43(8):609-615.
• [28]Edwards MR, Bartlett NW, Hussell T, Openshaw P, Johnston SL: The microbiology of asthma. Nat Rev Microbiol 2012, 10(7):459-471.
• [29]Calvo C, Pozo F, García-García ML, Sánchez M, López-Valero M, Pérez-Brena P, Casas I: Detection of new respiratory viruses in hospitalized infants with bronchiolitis: a three-year prospective study. Acta Paediatr 2010, 99(6):883-887.
• [30]de González DJ, Ochoa SC: Estudio de variabilidad en el abordaje de la bronquiolitis aguda en España en relación con la edad de los pacientes. An Pediatr (Barc ) 2010, 72(1):4-18.
• [31]Mansbach JM, Piedra PA, Teach SJ, Sullivan AF, Forgey T, Clark S, Espinola JA, Camargo CA Jr: Prospective multicenter study of viral etiology and hospital length of stay in children with severe bronchiolitis. Arch Pediatr Adolesc Med 2012, 166(8):700-706.
• [32]Bamberger E, Srugo I, Abu Raya B, Segal E, Chaim B, Kassis I, Kugelman A, Miron D: What is the clinical relevance of respiratory syncytial virus bronchiolitis?: findings from a multi-center, prospective study. Eur J Clin Microbiol Infect Dis 2012, 31(12):3323-3330.
• [33]Ralston S, Hill V: Incidence of apnea in infants hospitalized with respiratory syncytial virus bronchiolitis: a systematic review. J Pediatr 2009, 155(5):728-733.
• [34]Shefali-Patel D, Paris MA, Watson F, Peacock JL, Campbell M, Greenough A: RSV hospitalisation and healthcare utilisation in moderately prematurely born infants. Eur J Pediatr 2012, 171(7):1055-1061.
• [35]McManus TE, Marley AM, Baxter N, Christie SN, O’Neill HJ, Elborn JS, Coyle PV, Kidney JC: Respiratory viral infection in exacerbations of COPD. Respir Med 2008, 102(11):1575-1580.
• [36]Beckham JD, Cadena A, Lin J, Piedra PA, Glezen WP, Greenberg SB, Atmar RL: Respiratory viral infections in patients with chronic, obstructive pulmonary disease. J Infect 2005, 50(4):322-330.
• [37]Camargo CA Jr, Ginde AA, Clark S, Cartwright CP, Falsey AR, Niewoehner DE: Viral pathogens in acute exacerbations of chronic obstructive pulmonary disease. Intern Emerg Med 2008, 3(4):355-359.
• [38]De SG, Lampron N, La Forge J, Rouleau I, Bourbeau J, Weiss K, Barret B, Boivin G: Importance of viral and bacterial infections in chronic obstructive pulmonary disease exacerbations. J Clin Virol 2009, 46(2):129-133.
• [39]Hutchinson AF, Ghimire AK, Thompson MA, Black JF, Brand CA, Lowe AJ, Smallwood DM, Vlahos R, Bozinovski S, Brown GV, Anderson GP, Irving LB: A community-based, time-matched, case-control study of respiratory viruses and exacerbations of COPD. Respir Med 2007, 101(12):2472-2481.
• [40]Mohan A, Chandra S, Agarwal D, Guleria R, Broor S, Gaur B, Pandey RM: Prevalence of viral infection detected by PCR and RT-PCR in patients with acute exacerbation of COPD: a systematic review. Respirology 2010, 15(3):536-542.
• [41]Pérez-Yarza EG, Moreno A, Lázaro P, Mejías A, Ramilo O: The association between respiratory syncytial virus infection and the development of childhood asthma: a systematic review of the literature. Pediatr Infect Dis J 2007, 26(8):733-739.
• [42]Carbonell-Estrany X, Bont L, Doering G, Gouyon JB, Lanari M: Clinical relevance of prevention of respiratory syncytial virus lower respiratory tract infection in preterm infants born between 33 and 35 weeks gestational age. Eur J Clin Microbiol Infect Dis 2008, 27(10):891-899.
• [43]Busse WW, Lemanske J, Gern JE: Role of viral respiratory infections in asthma and asthma exacerbations. Lancet 2010, 376(9743):826-834.
• [44]Bacharier LB, Cohen R, Schweiger T, Yin-Declue H, Christie C, Zheng J, Schechtman KB, Strunk RC, Castro M: Determinants of asthma after severe respiratory syncytial virus bronchiolitis. J Allergy Clin Immunol 2012, 130(1):91-100.
• [45]Sigurs N, Aljassim F, Kjellman B, Robinson PD, Sigurbergsson F, Bjarnason R, Gustafsson PM: Asthma and allergy patterns over 18 years after severe RSV bronchiolitis in the first year of life. Thorax 2010, 65(12):1045-1052.
• [46]Checchia PA, Nalysnyk L, Fernandes AW, Mahadevia PJ, Xu Y, Fahrbach K, Welliver RC Sr: Mortality and morbidity among infants at high risk for severe respiratory syncytial virus infection receiving prophylaxis with palivizumab: a systematic literature review and meta-analysis. Pediatr Crit Care Med 2011, 12(5):580-588.
• [47]Figueras J, Carbonell X, Quero J, Fernández B, Guzmán J, Echániz I, Doménech E: FLIP-2 Study: risk factors linked to respiratory syncytial virus infection requiring hospitalization in premature infants born in Spain at a gestational age of 32 to 35 weeks. Pediatr Infect Dis J 2008, 27(9):788-793.
• [48]Carbonell-Estrany X, Quero J: Hospitalization rates for respiratory syncytial virus infection in premature infants born during two consecutive seasons. Pediatr Infect Dis J 2001, 20(9):874-879.
• [49]Thorburn K, Eisenhut M, Riordan A: Mortality and morbidity of nosocomial respiratory syncytial virus (RSV) infection in ventilated children - A ten year 50. perspective. Minerva Anestesiol 2012, 78(7):782-789.
• [50]Walsh EE, Falsey AR: Respiratory Syncytial Virus infection in adult populations. Infect Disord Drug Targets 2012, 12(2):98-102.
• [51]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(5):275-284.
• [52]Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants Pediatrics 1998, 102(3 Pt 1):531-537.
• [53]Gomaa MA, Galal O, Mahmoud MS: Risk of acute otitis media in relation to acute bronchiolitis in children. Int J Pediatr Otorhinolaryngol 2012, 76(1):49-51.
• [54]Zhou H, Thompson WW, Viboud CG, Ringholz CM, Cheng PY, Steiner C, Abedi GR, Anderson LJ, Brammer L, Shay DK: Hospitalizations associated with influenza and respiratory syncytial virus in the United States, 1993-2008. Clin Infect Dis 2012, 54(10):1427-1436.
• [55]Hampp C, Kauf TL, Saidi AS, Winterstein AG: Cost-effectiveness of respiratory syncytial virus prophylaxis in various indications. Arch Pediatr Adolesc Med 2011, 165(6):498-505.
• [56]García CG, Bhore R, Soriano-Fallas A, Trost M, Chason R, Ramilo O, Mejias A: Risk factors in children hospitalized with RSV bronchiolitis versus non-RSV bronchiolitis. Pediatrics 2010, 126(6):e1453-e1460.
• [57]Mahadevia PJ, Masaquel AS, Polak MJ, Weiner LB: Cost utility of palivizumab prophylaxis among pre-term infants in the United States: A national policy perspective. J Med Econ 2012, 15(5):987-996.
• [58]Lázaro P, Figueras J, Doménech E, Closa R, Echániz I, Wood MA, Fitch K: Coste-efectividad de palivizumab para prevenir el virus respiratorio sincitial en niños prematuros y niños con enfermedad pulmonar crónica en España. Pharmacoecon Span Res Artic 2007, 4(2):59-70.
• [59]Nuijten MJ, Wittenberg W: Cost effectiveness of palivizumab in Spain: an analysis using observational data. Eur J Health Econ 2010, 11(1):105-115.
• [60]Lázaro P, Figueras J, Doménech E, Echániz I, Closa R, Wood M, Fitch K: La eficiencia (coste-efectividad) de palivizumab como profilaxis para la infección por virus respiratorio sincitial en prematuros de 32-35 semanas en España. Anales de Pediatría 2006, 65(4):316-324.
• [61]Blanken M, Bont L, Rovers M: The cost-effectiveness of palivizumab in the prevention of respiratory syncytial virus bronchiolitis: A systematic review. Curr Respir Med Rev 2011, 7(3):203-212.
• [62]Wang D, Bayliss S, Meads C: Palivizumab for immunoprophylaxis of respiratory syncytial virus (RSV) bronchiolitis in high-risk infants and young children: a systematic review and additional economic modelling of subgroup analyses. Health Technol Assess 2011, 15(5):iii-124.
• [63]Raya OL, Marquez CS, Navarro-Caballero JA, Villegas PR: Cost-effectiveness of palivizumab in the prevention of hospital admissions for syncytial respiratory virus in pre-term babies born at 32 to 35 weeks. Agencia de Evaluación de Tecnologías Sanitarias de Andalucía, Sevilla; 2006.
• [64]Pons JM, Tebe C, Paladio N, Garcia-Altes A, Danes I, Valls IS: Meta-analysis of passive immunoprophylaxis in paediatric patients at risk of severe RSV infection. Acta Paediatr 2011, 100(3):324-329.
• [65]Smart KA, Lanctot KL, Paes BA: The cost effectiveness of palivizumab: a systematic review of the evidence. J Med Econ 2010, 13(3):453-463.
• [66]Groothuis JR, Fryzek JP, Makari D, Steffey D, Martone WJ: Respiratory syncytial virus hospitalization trends in infants with chronic lung disease of infancy, 1998-2008. Clin Epidemiol 2011, 3(1):245-250.
• [67]Hennus MP, Bem RA, Bos AP, van Vught AJ: Life-threatening respiratory syncytial virus disease in children. Curr Respir Med Rev 2011, 7(3):187-195.
• [68]Stensballe LG, Simonsen JB, Thomsen SF, Larsen AM, Lysdal SH, Aaby P, Kyvik KO, Skytthe A, Backer V, Bisgaard H: The causal direction in the association between respiratory syncytial virus hospitalization and asthma. J Allergy Clin Immunol 2009, 123(1):131-137.
• [69]Simoes EA, Carbonell-Estrany X, Rieger CH, Mitchell I, Fredrick L, Groothuis JR: The effect of respiratory syncytial virus on subsequent recurrent wheezing in atopic and nonatopic children. J Allergy Clin Immunol 2010, 126(2):256-262.
• [70]Krilov LR, Palazzi DL, Fernandes AW, Klein RW, Mahadevia PJ: Prevalence of respiratory syncytial virus (RSV) risk factors and cost implications of immunoprophylaxis to infants 32 to 35 weeks gestation for health plans in the United States. Value Health 2010, 13(1):77-86.
• [71]DiFranza JR, Masaquel A, Barrett AM, Colosia AD, Mahadevia PJ: Systematic literature review assessing tobacco smoke exposure as a risk factor for serious respiratory syncytial virus disease among infants and young children. BMC Pediatr 2012, 12:81.
• [72]Robinson KA, Odelola OA, Saldanha IJ, McKoy NA: Palivizumab for prophylaxis against respiratory syncytial virus infection in children with cystic fibrosis. Cochrane Database Syst Rev 2012, 2:CD007743.
• [73]Eisenhut M: Extrapulmonary manifestations of severe respiratory syncytial virus infection–a systematic review. Crit Care 2006, 10(4):R107.
• [74]Hu J, Robinson JL: Treatment of respiratory syncytial virus with palivizumab: a systematic review. World J Pediatr 2010, 6(4):296-300.
• [75]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, Lodrup-Carlsen K, Mäkelä M, Malkusova I, Mullol J, Nieto A, Eller E, et al.: Viruses and bacteria in acute asthma exacerbations–a GA(2) LEN-DARE systematic review. Allergy 2011, 66(4):458-468.
• [76]Wang D, Cummins C, Bayliss S, Sandercock J, Burls A: Immunoprophylaxis against respiratory syncytial virus (RSV) with palivizumab in children: a systematic review and economic evaluation. Health Technol Assess 2008, 12(36):iii. ix-x, 1-86
• [77]Carbonell-Estrany X, Simoes EA, Dagan R, Hall CB, Harris B, Hultquist M, Connor EM, Losonsky GA: Motavizumab for prophylaxis of respiratory syncytial virus in high-risk children: a noninferiority trial. Pediatrics 2010, 125(1):e35-e51.
• [78]Feltes TF, Sondheimer HM, Tulloh RM, Harris BS, Jensen KM, Losonsky GA, Griffin MP: A randomized controlled trial of motavizumab versus palivizumab for the prophylaxis of serious respiratory syncytial virus disease in children with hemodynamically significant congenital heart disease. Pediatr Res 2011, 70(2):186-191.
• [79]Poorisrisak P, Halkjaer LB, Thomsen SF, Stensballe LG, Kyvik KO, Skytthe A, Schioetz PO, Bisgaard H: Causal direction between respiratory syncytial virus bronchiolitis and asthma studied in monozygotic twins. Chest 2010, 138(2):338-344.
• [80]Carbonell-Estrany X, Simoes EA, Fullarton JR, Ferdynus C, Gouyon JB: Validation of a model to predict hospitalization due to RSV of infants born at 33-35 weeks’ gestation. J Perinat Med 2010, 38(4):411-417.
• [81]Shay DK, Holman RC, Newman RD, Liu LL, Stout JW, Anderson LJ: Bronchiolitis-associated hospitalizations among US children, 1980-1996. JAMA 1999, 282(15):1440-1446.
• [82]Shay DK, Holman RC, Roosevelt GE, Clarke MJ, Anderson LJ: Bronchiolitis-associated mortality and estimates of respiratory syncytial virus-associated deaths among US children, 1979-1997. J Infect Dis 2001, 183(1):16-22.
• [83]Hall CB, Weinberg GA, Iwane MK, Blumkin AK, Edwards KM, Staat MA, Auinger P, Griffin MR, Poehling KA, Erdman D, Grijalva CG, Zhu Y, Szilagyi P: The burden of respiratory syncytial virus infection in young children. N Engl J Med 2009, 360(6):588-598.
• [84]Willson DF, Landrigan CP, Horn SD, Smout RJ: Complications in infants hospitalized for bronchiolitis or respiratory syncytial virus pneumonia. J Pediatr 2003, 143(Suppl 5):S142-S149.
• [85]Korppi M, Piippo-Savolainen E, Korhonen K, Remes S: Respiratory morbidity 20 years after RSV infection in infancy. Pediatr Pulmonol 2004, 38(2):155-160.
• [86]Osundwa VM, Dawod ST, Ehlayel M: Recurrent wheezing in children with respiratory syncytial virus (RSV) bronchiolitis in Qatar. Eur J Pediatr 1993, 152(12):1001-1003.
• [87]Henderson J, Hilliard TN, Sherriff A, Stalker D, Al SN, Thomas HM: Hospitalization for RSV bronchiolitis before 12 months of age and subsequent asthma, atopy and wheeze: a longitudinal birth cohort study. Pediatr Allergy Immunol 2005, 16(5):386-392.
• [88]Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, Printz MC, Lee WM, Shult PA, Reisdorf E, Carlson-Dakes KT, Salazar LP, DaSilva DF, Tisler CJ, Gern JE, Lemanske RF Jr: Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 2008, 178(7):667-672.
• [89]Kusel MM, de Klerk NH, Kebadze T, Vohma V, Holt PG, Johnston SL, Sly PD: Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol 2007, 119(5):1105-1110.
• [90]Stein RT, Sherrill D, Morgan WJ, Holberg CJ, Halonen M, Taussig LM, Wright AL, Martinez FD: Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 1999, 354(9178):541-545.
• [91]Fjaerli HO, Farstad T, Rod G, Ufert GK, Gulbrandsen P, Nakstad B: Acute bronchiolitis in infancy as risk factor for wheezing and reduced pulmonary function by seven years in Akershus County. Norway. BMC Pediatr 2005, 5:31.
• [92]Singleton RJ, Redding GJ, Lewis TC, Martinez P, Bulkow L, Morray B, Peters H, Gove J, Jones C, Stamey D, Talkington DF, DeMain J, Bernert JT, Butler JC: Sequelae of severe respiratory syncytial virus infection in infancy and early childhood among Alaska Native children. Pediatrics 2003, 112(2):285-290.
• [93]Sigurs N, Bjarnason R, Sigurbergsson F, Kjellman B, Bjorksten B: Asthma and immunoglobulin E antibodies after respiratory syncytial virus bronchiolitis: a prospective cohort study with matched controls. Pediatrics 1995, 95(4):500-505.
• [94]Sigurs N, Bjarnason R, Sigurbergsson F, Kjellman B: Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am J Respir Crit Care Med 2000, 161(5):1501-1507.
• [95]Sigurs N, Gustafsson PM, Bjarnason R, Lundberg F, Schmidt S, Sigurbergsson F, Kjellman B: Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med 2005, 171(2):137-141.
• [96]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(6):865-870.
• [97]Law BJ, Langley JM, Allen U, Paes B, Lee DS, Mitchell I, Sampalis J, Walti H, Robinson J, O’Brien K, Majaesic C, Caouette G, Frenette L, Le Saux N, Simmons B, Moisiuk S, Sankaran K, Ojah C, Singh AJ, Lebel MH, Bacheyie GS, Onyett H, Michaliszyn A, Manzi P, Parison D: The Pediatric Investigators Collaborative Network on Infections in Canada study of predictors of hospitalization for respiratory syncytial virus infection for infants born at 33 through 35 completed weeks of gestation. Pediatr Infect Dis J 2004, 23(9):806-814.
• [98]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(4):230-236.
• [99]Rossi GA, Medici MC, Arcangeletti MC, Lanari M, Merolla R, Paparatti UD, Silvestri M, Pistorio A, Chezzi C: Risk factors for severe RSV-induced lower respiratory tract infection over four consecutive epidemics. Eur J Pediatr 2007, 166(12):1267-1272.
• [100]Resch B, Pasnocht A, Gusenleitner W, Müller W: Rehospitalisations for respiratory disease and respiratory syncytial virus infection in preterm infants of 29-36 weeks gestational age. J Infect 2005, 50(5):397-403.
• [101]Horn SD, Smout RJ: Effect of prematurity on respiratory syncytial virus hospital resource use and outcomes. J Pediatr 2003, 143(Suppl 5):S133-S141.
• [102]Hammer J, Numa A, Newth CJ: Albuterol responsiveness in infants with respiratory failure caused by respiratory syncytial virus infection. J Pediatr 1995, 127(3):485-490.
• [103]Bont L, Steijn M, van Aalderen WM, Kimpen JL: Impact of wheezing after respiratory syncytial virus infection on health-related quality of life. Pediatr Infect Dis J 2004, 23(5):414-417.
• [104]Simon A, Khurana K, Wilkesmann A, Müller A, Engelhart S, Exner M, Schildgen O, Eis-Hübinger AM, Groothuis JR, Bode U: Nosocomial respiratory syncytial virus infection: impact of prospective surveillance and targeted infection control. Int J Hyg Environ Health 2006, 209(4):317-324.
• [105]Simoes EA, Groothuis JR, Carbonell-Estrany X, Rieger CH, Mitchell I, Fredrick LM, Kimpen JL: Palivizumab prophylaxis, respiratory syncytial virus, and subsequent recurrent wheezing. J Pediatr 2007, 151(1):34-42. 42.e1
• [106]Blanken MO, Rovers MM, Molenaar JM, Winkler-Seinstra PL, Meijer A, Kimpen JL, Bont L: Respiratory syncytial virus and recurrent wheeze in healthy preterm infants. N Engl J Med 2013, 368(19):1791-1799.
• [107][http://www.sign.ac.uk/methodology/checklists.html] webcite Scottish Intercollegiate Guidelines Network (SIGN): Critical appraisal: Notes and checklists..
• [108]Guía de Práctica Clínica sobre Bronquiolitis Aguda. Plan de Calidad para el Sistema Nacional de Salud del Ministerio de Sanidad y Política Social. Agència d’Avaluació de Tecnologia i Recerca Mèdiques, Barcelona; 2010.