Abstract
Acute viral bronchiolitis is a common cause for infant hospital admissions. Of all etiological agents, respiratory syncytial virus (RSV) is commonly the most frequent. The present study assesses relationships between atmospheric factors and RSV infections in under 3-year-old patients admitted to the Inpatient Paediatric Service of Vila Real (North of Portugal). For this purpose, (1) clinical files of children admitted with a diagnosis of acute bronchiolitis from September 2005 to December 2015 (>10 years) were scrutinised and (2) local daily temperature/precipitation series, as well as six weather types controlling meteorological conditions in Portugal, were used. Fifty-five percent of all 770 admitted children were effectively infected with a given virus, whilst 48 % (367) were RSV+, i.e. 87 % of virus-infected children were RSV+. The bulk of incidence is verified in the first year of age (82 %, 302), slightly higher in males. RSV outbreaks are typically from December to March, but important inter-annual variability is found in both magnitude and shape. Although no clear connections were found between monthly temperatures/precipitation and RSV outbreaks apart from seasonality, a linkage to wintertime cold spells is apparent on a daily basis. Anomalously low minimum temperatures from the day of admittance back to 10 days before are observed. This relationship is supported by anomalously high occurrences of the E and AA weather types over the same period, which usually trigger dry and cold weather. These findings highlight some predictability in the RSV occurrences, revealing potential for modelling and risk assessments.
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Avendano CLF, Parra VJ, Padilla VC, Palomino MMA (2003) The influence of respiratory virus infections and environmental conditions on pediatric health care demand during winter-2002 in Santiago, Chile. Rev Med Chil 131:902–908. doi:10.4067/S0034-98872003000800010
Bacharier LB, Cohen R, Schweiger T, Yin-DeClue H, Christie C, Zheng J, Schechtman KB, Strunk RC, Castro M (2012) Determinants of asthma after severe respiratory syncytial virus bronchiolitis. J Allergy Clin Immunol 130:91–100. doi:10.1016/j.jaci.2012.02.010
Bawage SS, Tiwari PM, Pillai S, Dennis V, Singh SR (2013) Recent advances in diagnosis, prevention, and treatment of human respiratory syncytial virus. Adv Virol 2013:26–52. doi:10.1155/2013/595768
Carroll KN, Gebretsadik T, Griffin MR, Wu P, Dupont WD, Mitchel EF, Enriquez R, Hartert TV (2008) Increasing burden and risk factors for bronchiolitis-related medical visits in infants enrolled in a state health care insurance plan. Pediatrics 122:58–64. doi:10.1542/peds.2007-2087
Chen ZR, Zhu Y, Wang YQ, Zhou WF, Yan YD, Zhu CH, Zhang XL, Sun HP, Ji W (2014) Association of meteorological factors with childhood viral acute respiratory infections in subtropical China: an analysis over 11 years. Arch Virol 159:631–639. doi:10.1007/s00705-013-1863-8
Collins PL, Melero JA (2011) Progress in understanding and controlling respiratory syncytial virus: still crazy after all these years. Virus Res 162:80–99. doi:10.1016/j.virusres.2011.09.020
de Pablo F, Tomas C, Soriano LR, Diego L (2009) Winter circulation weather types and hospital admissions for cardiovascular, respiratory and digestive diseases in Salamanca, Spain. Int J Climatol 29:1692–1703. doi:10.1002/joc.1802
Diez-Domingo J, Perez-Yarza EG, Melero JA, Sanchez-Luna M, Aguilar MD, Blasco AJ, Alfaro N, Lazaro P (2014) Social, economic, and health impact of the respiratory syncytial virus: a systematic search. BMC Infect Dis 14:40–50. doi:10.1186/s12879-014-0544-x
du Prel JB, Puppe W, Grondahl B, Knuf M, Weigl JA, Schaaff F, Schmitt HJ (2009) Are meteorological parameters associated with acute respiratory tract infections? Clin Infect Dis 49:861–868. doi:10.1086/605435
Espinoza JA, Bohmwald K, Cespedes PF, Gomez RS, Riquelme SA, Cortes CM, Valenzuela JA, Sandoval RA, Pancetti FC, Bueno SM, Riedel CA, Kalergis AM (2013) Impaired learning resulting from respiratory syncytial virus infection. Proc Natl Acad Sci U S A 110:9112–9117. doi:10.1073/pnas.1217508110
Feldman AS, Hartert TV, Gebretsadik T, Carroll KN, Minton PA, Woodward KB, Larkin EK, Miller EK, Valet RS (2015) Respiratory severity score separates upper versus lower respiratory tract infections and predicts measures of disease severity. Pediat Allergy Immunol Pulmonol 28:117–120. doi:10.1089/ped.2014.0463
Fraga H, Malheiro AC, Moutinho-Pereira J, Santos JA (2014) Climate factors driving wine production in the Portuguese Minho region. Agric For Meteorol 185:26–36. doi:10.1016/j.agrformet.2013.11.003
Haynes AK, Manangan AP, Iwane MK, Sturm-Ramirez K, Homaira N, Brooks WA, Luby S, Rahman M, Klena JD, Zhang YZ, Yu HG, Zhan FX, Dueger E, Mansour AM, Azazzy N, McCracken JP, Bryan JP, Lopez MR, Burton DC, Bigogo G, Breiman RF, Feikin DR, Njenga K, Montgomery J, Cohen AL, Moyes J, Pretorius M, Cohen C, Venter M, Chittaganpitch M, Thamthitiwat S, Sawatwong P, Baggett HC, Luber G, Gerber SI (2013) Respiratory syncytial virus circulation in seven countries with global disease detection regional centers. J Infect Dis 208:S246–S254. doi:10.1093/infdis/jit515
Hervas D, Reina J, Hervas JÁ (2012) Meteorologic conditions and respiratory syncytial virus activity. Pediatr Infect Dis J 31:E176–E181. doi:10.1097/INF.0b013e31825cef14
Holton JR, Hakim GJ (2013) An introduction to dynamic meteorology. Elsevier, Oxford, UK
Hurrell JW, Kushnir Y, Visbeck M (2001) The North Atlantic oscillation. Science 291:603–605. doi:10.1126/science.1058761
Hurwitz JL (2011) Respiratory syncytial virus vaccine development. Expert Rev Vaccines 10:1415–1433. doi:10.1586/erv.11.120
Huth R (2010) Synoptic-climatological applicability of circulation classifications from the COST733 collection: first results. Phys Chem Earth 35:388–394. doi:10.1016/j.pce.2009.11.013
Jackson DJ (2014) Early-life viral infections and the development of asthma: a target for asthma prevention? Curr Opin Allergy Clin Immunol 14:131–136. doi:10.1097/ACI.0000000000000047
Kistler R, Kalnay E, Collins W, Saha S, White G, Woollen J, Chelliah M, Ebisuzaki W, Kanamitsu M, Kousky V, van den Dool H, Jenne R, Fiorino M (2001) The NCEP-NCAR 50-year reanalysis: monthly means CD-ROM and documentation. Bull Am Meteorol Soc 82:247–267. doi:10.1175/1520-0477(2001)082<0247:TNNYRM>2.3.CO;2
Lanari M, Prinelli F, Adorni F, Di Santo S, Vandini S, Silvestri M, Musicco M, Facto I (2015) Risk factors for bronchiolitis hospitalization during the first year of life in a multicenter Italian birth cohort. Ital J Pediatr 41:40–50. doi:10.1186/s13052-015-0149-z
Lapillonne A, Regnault A, Gournay V, Gouyon JB, Gilet H, Anghelescu D, Miloradovich T, Arnould B, Moriette G (2012) Impact on parents of bronchiolitis hospitalization of full-term, preterm and congenital heart disease infants. BMC Pediatr 12:171–182. doi:10.1186/1471-2431-12-171
Leecaster M, Gesteland P, Greene T, Walton N, Gundlapalli A, Rolfs R, Byington C, Samore M (2011) Modeling the variations in pediatric respiratory syncytial virus seasonal epidemics. BMC Infect Dis 11:105–114. doi:10.1186/1471-2334-11-105
Legand A, Briand S, Shindo N, Brooks WA, de Jong MD, Farrar J, Aguilera X, Hayden FG (2013) Addressing the public health burden of respiratory viruses: the Battle against Respiratory Viruses (BRaVe) initiative. Futur Virol 8:953–968. doi:10.2217/fvl.13.85
Marguet C, Lubrano M, Gueudin M, Le Roux P, Deschildre A, Forget C, Couderc L, Siret D, Donnou MD, Bubenheim M, Vabret A, Freymuth F (2009) In very young infants severity of acute bronchiolitis depends on carried viruses. Plos One 4, e4596. doi:10.1371/journal.pone.0004596
Meerhoff TJ, Paget JW, Kimpen JL, Schellevis F (2009) Variation of respiratory syncytial virus and the relation with meteorological factors in different winter seasons. Pediatr Infect Dis J 28:860–866. doi:10.1097/INF.0b013e3181a3e949
Noyola DE, Mandeville PB (2008) Effect of climatological factors on respiratory syncytial virus epidemics. Epidemiol Infect 136:1328–1332. doi:10.1017/S0950268807000143
Oymar K, Skjerven HO, Mikalsen IB (2014) Acute bronchiolitis in infants, a review. Scand J Trauma Resusc Emerg Med 22:23–33. doi:10.1186/1757-7241-22-23
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Koppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. doi:10.5194/hess-11-1633-2007
Peltola V, Reunanen T, Ziegler T, Silvennoinen H, Heikkinen T (2005) Accuracy of clinical diagnosis of influenza in outpatient children. Clin Infect Dis 41:1198–1200. doi:10.1086/444508
Philipp A, Bartholy J, Beck C, Erpicum M, Esteban P, Fettweis X, Huth R, James P, Jourdain S, Kreienkamp F, Krennert T, Lykoudis S, Michalides SC, Pianko-Kluczynska K, Post P, Alvarez DR, Schiemann R, Spekat A, Tymvios FS (2010) Cost733cat-A database of weather and circulation type classifications. Phys Chem Earth 35:360–373. doi:10.1016/j.pce.2009.12.010
Pitzer VE, Viboud C, Alonso WJ, Wilcox T, Metcalf CJ, Steiner CA, Haynes AK, Grenfell BT (2015) Environmental drivers of the spatiotemporal dynamics of respiratory syncytial virus in the United States. PLoS Pathog 11, e1004591. doi:10.1371/journal.ppat.1004591
Popow-Kraupp T, Aberle JH (2011) Diagnosis of respiratory syncytial virus infection. Open Microbiol J 5:128–134. doi:10.2174/1874285801105010128
Santos JA, Corte-Real J (2006) Temperature extremes in Europe and wintertime large-scale atmospheric circulation: HadCM3 future scenarios. Clim Res 31:3–18. doi:10.3354/cr031003
Santos JA, Corte-Real J, Leite SM (2005) Weather regimes and their connection to the winter rainfall in Portugal. Int J Climatol 25:33–50. doi:10.1002/joc.1101
Santos JA, Andrade C, Corte-Real J, Leite S (2009) The role of large-scale eddies in the occurrence of winter precipitation deficits in Portugal. Int J Climatol 29:1493–1507. doi:10.1002/joc.1818
Santos JA, Woollings T, Pinto JG (2013) Are the Winters 2010 and 2012 archetypes exhibiting extreme opposite behavior of the North Atlantic jet stream? Mon Weather Rev 141:3626–3640. doi:10.1175/MWR-D-13-00024.1
Santos JA, Pfahl S, Pinto JG, Wernli H (2015) Mechanisms underlying temperature extremes in Iberia: a Lagrangian perspective. Tellus Ser A Dyn Meteorol Oceanogr 67:26032–26047. doi:10.3402/tellusa.v67.26032
Simoes EAF, DeVincenzo JP, Boeckh M, Bont L, Crowe JE, Griffiths P, Hayden FG, Hodinka RL, Smyth RL, Spencer K, Thirstrup S, Walsh EE, Whitley RJ (2015) Challenges and opportunities in developing respiratory syncytial virus therapeutics. J Infect Dis 211:S1–S20. doi:10.1093/infdis/jiu828
Sloan C, Moore ML, Hartert T (2011) Impact of pollution, climate, and sociodemographic factors on spatiotemporal dynamics of seasonal respiratory viruses. Clin Transl Sci 4:48–54. doi:10.1111/j.1752-8062.2010.00257.x
Stempel HE, Martin ET, Kuypers J, Englund JA, Zerr DM (2009) Multiple viral respiratory pathogens in children with bronchiolitis. Acta Paediatr 98:123–126. doi:10.1111/j.1651-2227.2008.01023.x
Stewart PDS (2016) Seasonality and selective trends in viral acute respiratory tract infections. Med Hypotheses 86:104–119. doi:10.1016/j.mehy.2015.11.005
Svensson C, Berg K, Sigurs N, Trollfors B (2015) Incidence, risk factors and hospital burden in children under five years of age hospitalised with respiratory syncytial virus infections. Acta Paediatr 104:922–926. doi:10.1111/apa.13061
Vandini S, Corvaglia L, Alessandroni R, Aquilano G, Marsico C, Spinelli M, Lanari M, Faldella G (2013) Respiratory syncytial virus infection in infants and correlation with meteorological factors and air pollutants. Ital J Pediatr 39:1–6. doi:10.1186/1824-7288-39-1
Walton NA, Poynton MR, Gesteland PH, Maloney C, Staes C, Facelli JC (2010) Predicting the start week of respiratory syncytial virus outbreaks using real time weather variables. BMC Med Inf Decis 10:68–76. doi:10.1186/1472-6947-10-68
Weinberger DM, Klugman KP, Steiner CA, Simonsen L, Viboud C (2015) Association between respiratory syncytial virus activity and pneumococcal disease in infants: a time series analysis of US hospitalization data. PLoS Med 12, e1001776. doi:10.1371/journal.pmed.1001776
Welliver RC (2007) Temperature, humidity, and ultraviolet B radiation predict community respiratory syncytial virus activity. Pediatr Infect Dis J 26:S29–S35. doi:10.1097/INF.0b013e318157da59
Welliver RC (2009) The relationship of meteorological conditions to the epidemic activity of respiratory syncytial virus. Paediatr Respir Rev 10:6–8
WHO (2013) Research needs for the battle against respiratory viruses (BRaVe). In: WHO, ed. Geneva: World Health Organization
Yui I, Fujino M, Sawada A, Nakayama T (2014) Novel clinical features of recurrent human respiratory syncytial virus infections. J Med Virol 86(9):1629–1638. doi:10.1002/jmv.23809
Yusuf S, Piedimonte G, Auais A, Demmler G, Krishnan S, Van Caeseele P, Singleton R, Broor S, Parveen S, Avendano L, Parra J, Chavez-Bueno S, De Sierra TM, Simoes EAF, Shaha S, Welliver R (2007) The relationship of meteorological conditions to the epidemic activity of respiratory syncytial virus. Epidemiol Infect 135:1077–1090. doi:10.1017/S095026880600776X
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This work is supported by European Investment Funds by FEDER/COMPETE/POCI—Operational Competitiveness and Internationalization Programme, under Project POCI-01-0145-FEDER-006958 and National Funds by FCT—Portuguese Foundation for Science and Technology, under the project UID/AGR/04033/2013. The authors also thank CHTMAD for providing the paediatric admission data and IPMA for providing the meteorological data for the Vila Real weather station.
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Oliveira-Santos, M., Santos, J.A., Soares, J. et al. Influence of meteorological conditions on RSV infection in Portugal. Int J Biometeorol 60, 1807–1817 (2016). https://doi.org/10.1007/s00484-016-1168-1
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DOI: https://doi.org/10.1007/s00484-016-1168-1