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Determining the timing of respiratory syncytial virus (RSV) epidemics: a systematic review, 2016 to 2021; method categorisation and identification of influencing factors
- Lisa Staadegaard1 , Michel Dückers1,2,3 , Jojanneke van Summeren1 , Rob van Gameren1 , Clarisse Demont4 , Mathieu Bangert4 , You Li5,6 , Jean-Sebastien Casalegno7 , Saverio Caini1 , John Paget1
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View Affiliations Hide AffiliationsAffiliations: 1 Netherlands Institute for Health Services Research (Nivel), Utrecht, The Netherlands 2 Faculty of Behavioural and Social Sciences, University of Groningen, Groningen, The Netherlands 3 ARQ National Psychotrauma Centre, Diemen, The Netherlands 4 Sanofi Pasteur, Lyon, France 5 National Vaccine Innovation Platform, School of Public Health, Nanjing Medical University, Nanjing, China 6 Centre for Global Health, Usher Institute, University of Edinburgh, Edinburgh, Scotland, United Kingdom 7 Hospices Civils de Lyon; Hôpital de la Croix-Rousse; Centre de Biologie Nord; Institut des Agents Infectieux; Laboratoire de Virologie, Lyon; FranceLisa Staadegaardstaadegaard nivel.nl
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Citation style for this article: Staadegaard Lisa, Dückers Michel, van Summeren Jojanneke, van Gameren Rob, Demont Clarisse, Bangert Mathieu, Li You, Casalegno Jean-Sebastien, Caini Saverio, Paget John. Determining the timing of respiratory syncytial virus (RSV) epidemics: a systematic review, 2016 to 2021; method categorisation and identification of influencing factors . Euro Surveill. 2024;29(5):pii=2300244. https://doi.org/10.2807/1560-7917.ES.2024.29.5.2300244 Received: 03 May 2023; Accepted: 23 Oct 2023
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Abstract
There is currently no standardised approach to estimate respiratory syncytial virus (RSV) epidemics’ timing (or seasonality), a critical information for their effective prevention and control.
We aimed to provide an overview of methods to define RSV seasonality and identify factors supporting method choice or interpretation/comparison of seasonal estimates.
We systematically searched PubMed and Embase (2016–2021) for studies using quantitative approaches to determine the start and end of RSV epidemics. Studies’ features (data-collection purpose, location, regional/(sub)national scope), methods, and assessment characteristics (case definitions, sampled population’s age, in/outpatient status, setting, diagnostics) were extracted. Methods were categorised by their need of a denominator (i.e. numbers of specimens tested) and their retrospective vs real-time application. Factors worth considering when choosing methods and assessing seasonal estimates were sought by analysing studies.
We included 32 articles presenting 49 seasonality estimates (18 thereof through the 10% positivity threshold method). Methods were classified into eight categories, two requiring a denominator (1 retrospective; 1 real-time) and six not (3 retrospective; 3 real-time). A wide range of assessment characteristics was observed. Several studies showed that seasonality estimates varied when methods differed, or data with dissimilar assessment characteristics were employed. Five factors (comprising study purpose, application time, assessment characteristics, healthcare system and policies, and context) were identified that could support method choice and result interpretation.
Methods and assessment characteristics used to define RSV seasonality are heterogeneous. Our categorisation of methods and proposed framework of factors may assist in choosing RSV seasonality methods and interpretating results.
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References
-
Li Y, Reeves RM, Wang X, Bassat Q, Brooks WA, Cohen C, et al. , RSV Global Epidemiology Network, RESCEU investigators. Global patterns in monthly activity of influenza virus, respiratory syncytial virus, parainfluenza virus, and metapneumovirus: a systematic analysis. Lancet Glob Health. 2019;7(8):e1031-45. https://doi.org/10.1016/S2214-109X(19)30264-5 PMID: 31303294
-
Li Y, Wang X, Blau DM, Caballero MT, Feikin DR, Gill CJ, et al. , Respiratory Virus Global Epidemiology Network, RESCEU investigators. Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in children younger than 5 years in 2019: a systematic analysis. Lancet. 2022;399(10340):2047-64. https://doi.org/10.1016/S0140-6736(22)00478-0 PMID: 35598608
-
Hall CB, Long CE, Schnabel KC. Respiratory syncytial virus infections in previously healthy working adults. Clin Infect Dis. 2001;33(6):792-6. https://doi.org/10.1086/322657 PMID: 11512084
-
Amand C, Tong S, Kieffer A, Kyaw MH. Healthcare resource use and economic burden attributable to respiratory syncytial virus in the United States: a claims database analysis. BMC Health Serv Res. 2018;18(1):294. https://doi.org/10.1186/s12913-018-3066-1 PMID: 29678177
-
Prasad N, Newbern EC, Trenholme AA, Thompson MG, McArthur C, Wong CA, et al. The health and economic burden of respiratory syncytial virus associated hospitalizations in adults. PLoS One. 2020;15(6):e0234235. https://doi.org/10.1371/journal.pone.0234235 PMID: 32525898
-
European Medicines Agency (EMA). New medicine to protect babies and infants from respiratory syncytial virus (RSV) infection. Amsterdam: EMA; 2022. [Accessed 16 Sep 2022]. Available from: https://www.ema.europa.eu/en/news/new-medicine-protect-babies-infants-respiratory-syncytial-virus-rsv-infection
-
Drysdale SB, Green CA, Sande CJ. Best practice in the prevention and management of paediatric respiratory syncytial virus infection. Ther Adv Infect Dis. 2016;3(2):63-71. https://doi.org/10.1177/2049936116630243 PMID: 27034777
-
RSV Vaccine and mAb Snapshot. [Accessed 16 Jun 2021]. Available from: https://www.path.org/resources/rsv-vaccine-and-mab-snapshot/
-
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. https://doi.org/10.1001/archpediatrics.2010.298 PMID: 21300647
-
Kieffer A, Beuvelet M, Sardesai A, Musci R, Milev S, Roiz J, et al. Expected Impact of Universal Immunization With Nirsevimab Against RSV-Related Outcomes and Costs Among All US Infants in Their First RSV Season: A Static Model. J Infect Dis. 2022;226(Suppl 2):S282-92. https://doi.org/10.1093/infdis/jiac216 PMID: 35968866
-
Teirlinck AC, Broberg EK, Stuwitz Berg A, Campbell H, Reeves RM, Carnahan A, et al. Recommendations for respiratory syncytial virus surveillance at the national level. Eur Respir J. 2021;58(3):2003766. https://doi.org/10.1183/13993003.03766-2020 PMID: 33888523
-
Vos LM, Teirlinck AC, Lozano JE, Vega T, Donker GA, Hoepelman AI, et al. Use of the moving epidemic method (MEM) to assess national surveillance data for respiratory syncytial virus (RSV) in the Netherlands, 2005 to 2017. Euro Surveill. 2019;24(20):1800469. https://doi.org/10.2807/1560-7917.ES.2019.24.20.1800469 PMID: 31115311
-
Grilc E, Prosenc Trilar K, Lajovic J, Sočan M. Determining the seasonality of respiratory syncytial virus in Slovenia. Influenza Other Respir Viruses. 2021;15(1):56-63. https://doi.org/10.1111/irv.12779 PMID: 32656961
-
Renko M, Tapiainen T. Change in respiratory syncytial virus seasonality in Finland. Acta Paediatr. 2020;109(1):202-3. https://doi.org/10.1111/apa.14983 PMID: 31441534
-
van Summeren J, Meijer A, Aspelund G, Casalegno JS, Erna G, Hoang U, et al. , VRS study group in Lyon. Low levels of respiratory syncytial virus activity in Europe during the 2020/21 season: what can we expect in the coming summer and autumn/winter? Euro Surveill. 2021;26(29):2100639. https://doi.org/10.2807/1560-7917.ES.2021.26.29.2100639 PMID: 34296672
-
Miyama T, Iritani N, Nishio T, Ukai T, Satsuki Y, Miyata H, et al. Seasonal shift in epidemics of respiratory syncytial virus infection in Japan. Epidemiol Infect. 2021;149:e55. https://doi.org/10.1017/S0950268821000340 PMID: 33568242
-
Abu-Raya B, Viñeta Paramo M, Reicherz F, Lavoie PM. Why has the epidemiology of RSV changed during the COVID-19 pandemic? EClinicalMedicine. 2023;61:102089. https://doi.org/10.1016/j.eclinm.2023.102089 PMID: 37483545
-
Hamid S, Winn A, Parikh R, Jones JM, McMorrow M, Prill MM, et al. Seasonality of Respiratory Syncytial Virus - United States, 2017-2023. MMWR Morb Mortal Wkly Rep. 2023;72(14):355-61. https://doi.org/10.15585/mmwr.mm7214a1 PMID: 37022977
-
Eden JS, Sikazwe C, Xie R, Deng YM, Sullivan SG, Michie A, et al. , Australian RSV study group. Off-season RSV epidemics in Australia after easing of COVID-19 restrictions. Nat Commun. 2022;13(1):2884. https://doi.org/10.1038/s41467-022-30485-3 PMID: 35610217
-
Rose EB, Wheatley A, Langley G, Gerber S, Haynes A. Respiratory Syncytial Virus Seasonality - United States, 2014-2017. MMWR Morb Mortal Wkly Rep. 2018;67(2):71-6. https://doi.org/10.15585/mmwr.mm6702a4 PMID: 29346336
-
World Health Organization (WHO). Global Epidemiological Surveillance Standards for Influenza. Geneva: WHO; 2013.
-
Midgley CM, Haynes AK, Baumgardner JL, Chommanard C, Demas SW, Prill MM, et al. Determining the seasonality of respiratory syncytial virus in the United States: The impact of increased molecular testing. J Infect Dis. 2017;216(3):345-55. https://doi.org/10.1093/infdis/jix275 PMID: 28859428
-
Ambrose CS, Steed LL, Brandon M, Frye K, Olajide IR, Thomson G. National and regional modeling of distinct RSV seasonality thresholds for antigen and PCR testing in the United States. J Clin Virol. 2019;120:68-77. https://doi.org/10.1016/j.jcv.2019.09.010 PMID: 31590113
-
Grijalva CG, Poehling KA, Edwards KM, Weinberg GA, Staat MA, Iwane MK, et al. Accuracy and interpretation of rapid influenza tests in children. Pediatrics. 2007;119(1):e6-11. https://doi.org/10.1542/peds.2006-1694 PMID: 17200259
-
Broberg EK, Waris M, Johansen K, Snacken R, Penttinen P, European Influenza Surveillance Network. Seasonality and geographical spread of respiratory syncytial virus epidemics in 15 European countries, 2010 to 2016. Euro Surveill. 2018;23(5):17-00284. https://doi.org/10.2807/1560-7917.ES.2018.23.5.17-00284 PMID: 29409569
-
Baumeister E, Duque J, Varela T, Palekar R, Couto P, Savy V, et al. Timing of respiratory syncytial virus and influenza epidemic activity in five regions of Argentina, 2007-2016. Influenza Other Respir Viruses. 2019;13(1):10-7. https://doi.org/10.1111/irv.12596 PMID: 30051595
-
Obando-Pacheco P, Justicia-Grande AJ, Rivero-Calle I, Rodríguez-Tenreiro C, Sly P, Ramilo O, et al. Respiratory Syncytial Virus Seasonality: A Global Overview. J Infect Dis. 2018;217(9):1356-64. https://doi.org/10.1093/infdis/jiy056 PMID: 29390105
-
Bollyky TJ, Hulland EN, Barber RM, Collins JK, Kiernan S, Moses M, et al. , COVID-19 National Preparedness Collaborators. Pandemic preparedness and COVID-19: an exploratory analysis of infection and fatality rates, and contextual factors associated with preparedness in 177 countries, from Jan 1, 2020, to Sept 30, 2021. Lancet. 2022;399(10334):1489-512. https://doi.org/10.1016/S0140-6736(22)00172-6 PMID: 35120592
-
European Medicines Agency (EMA). First RSV vaccine to protect infants up to 6 months of age and older adults. Amsterdam: EMA. [Accessed 11 Oct 2023]. Available from: https://www.ema.europa.eu/en/news/first-rsv-vaccine-protect-infants-6-months-age-older-adults
-
United States Food and Drug Administration (FDA). FDA Approves First Vaccine for Pregnant Individuals to Prevent RSV in Infants. Rockville: FDA. [Accessed 11 Oct 2023]. Available from: https://www.fda.gov/news-events/press-announcements/fda-approves-first-vaccine-pregnant-individuals-prevent-rsv-infants
-
Centers for Disease Control and Prevention (CDC). Frequently Asked Questions About RSV Vaccine for Adults. Atlanta: CDC. [Accessed 11 Oct 2023]. Available from: https://www.cdc.gov/vaccines/vpd/rsv/hcp/older-adults-faqs.html
-
Wu SL, Mertens AN, Crider YS, Nguyen A, Pokpongkiat NN, Djajadi S, et al. Substantial underestimation of SARS-CoV-2 infection in the United States. Nat Commun. 2020;11(1):4507. https://doi.org/10.1038/s41467-020-18272-4 PMID: 32908126
-
Staadegaard L, Caini S, Wangchuk S, Thapa B, de Almeida WAF, de Carvalho FC, et al. The Global Epidemiology of RSV in Community and Hospitalized Care: Findings From 15 Countries. Open Forum Infect Dis. 2021;8(7):ofab159. https://doi.org/10.1093/ofid/ofab159 PMID: 34337092
-
Simpson RB, Gottlieb J, Zhou B, Hartwick MA, Naumova EN. Completeness of open access FluNet influenza surveillance data for Pan-America in 2005-2019. Sci Rep. 2021;11(1):795. https://doi.org/10.1038/s41598-020-80842-9 PMID: 33437025
-
Healthcare access and quality by level of healthcare spending, 2017. [Accessed 28 Feb 2023]. Available from: https://ourworldindata.org/grapher/haq-by-level-of-healthcare-spending-endpoints?country=NLD~DEU~FRA~ITA~USA
-
World Bank Group - International Development. Poverty, & Sustainability. [Accessed 28 Feb 2023]. Available from: https://www.worldbank.org/en/home
-
Paget J, Staadegaard L, Wang X, Li Y, van Pomeren T, van Summeren J, et al. Global and national influenza-associated hospitalisation rates: Estimates for 40 countries and administrative regions. J Glob Health. 2023;13:04003. https://doi.org/10.7189/jogh.13.04003 PMID: 36701368
-
Li Y, Hodgson D, Wang X, Atkins KE, Feikin DR, Nair H. Respiratory syncytial virus seasonality and prevention strategy planning for passive immunisation of infants in low-income and middle-income countries: a modelling study. Lancet Infect Dis. 2021;21(9):1303-12. https://doi.org/10.1016/S1473-3099(20)30703-9 PMID: 33965062
-
Staadegaard L, Caini S, Wangchuk S, Thapa B, de Almeida WAF, de Carvalho FC, et al. Defining the seasonality of respiratory syncytial virus around the world: National and subnational surveillance data from 12 countries. Influenza Other Respir Viruses. 2021;15(6):732-41. https://doi.org/10.1111/irv.12885 PMID: 34255934
-
Chadha M, Hirve S, Bancej C, Barr I, Baumeister E, Caetano B, et al. , WHO RSV Surveillance Group. Human respiratory syncytial virus and influenza seasonality patterns-Early findings from the WHO global respiratory syncytial virus surveillance. Influenza Other Respir Viruses. 2020;14(6):638-46. https://doi.org/10.1111/irv.12726 PMID: 32163226
-
Broberg E, Johansen K, Adlhoch C, Snacken R, Penttinen P. Seasonality of respiratory syncytial virus infection in the EU/EEA, 2010-2016. J Clin Virol. 2016;82:S116-7. https://doi.org/10.1016/j.jcv.2016.08.234
-
Baker RE, Mahmud AS, Wagner CE, Yang W, Pitzer VE, Viboud C, et al. Epidemic dynamics of respiratory syncytial virus in current and future climates. Nat Commun. 2019;10(1):5512. https://doi.org/10.1038/s41467-019-13562-y PMID: 31797866
-
Harcourt SE, Morbey RA, Smith GE, Loveridge P, Green HK, Pebody R, et al. Developing influenza and respiratory syncytial virus activity thresholds for syndromic surveillance in England. Epidemiol Infect. 2019;147:e163. https://doi.org/10.1017/S0950268819000542 PMID: 31063101
-
Glick AF, Kjelleren S, Hofstetter AM, Subramony A. RSV Hospitalizations in Comparison With Regional RSV Activity and Inpatient Palivizumab Administration, 2010-2013. Hosp Pediatr. 2017;7(5):271-8. https://doi.org/10.1542/hpeds.2016-0124 PMID: 28381595
-
Glatman-Freedman A, Kaufman Z, Applbaum Y, Dichtiar R, Steiman A, Gordon E-S, et al. Respiratory Syncytial Virus hospitalization burden: a nation-wide population-based analysis, 2000-2017. J Infect. 2020;81(2):297-303. https://doi.org/10.1016/j.jinf.2020.05.078 PMID: 32504738
-
Reis J, Yamana T, Kandula S, Shaman J. Superensemble forecast of respiratory syncytial virus outbreaks at national, regional, and state levels in the United States. Epidemics. 2019;26:1-8. https://doi.org/10.1016/j.epidem.2018.07.001 PMID: 30025885
-
Gentile Á, Lucion MF, Juárez MDV, Castellano V, Bakir J, Pacchiotti A, et al. Virus sincicial respiratorio en niños nacidos prematuros: 19 años de vigilancia epidemiológica activa en un hospital pediátrico. [Respiratory syncytial virus in preterm infants: 19 years of active epidemiological surveillance in a children’s hospital]. Arch Argent Pediatr. 2020;118(6):386-92. PMID: 33231045
-
Haynes AK, Fowlkes AL, Schneider E, Mutuc JD, Armstrong GL, Gerber SI. Human Metapneumovirus Circulation in the United States, 2008 to 2014. Pediatrics. 2016;137(5):e20152927. https://doi.org/10.1542/peds.2015-2927 PMID: 27244790
-
Olajide I, Ambrose C, Dube C. New method for determining respiratory syncytial virus seasonality in the United States: Results from RSV alert, a hospital-based laboratory surveillance program. J Manag Care Spec Pharm. 2018;24(10A):S67. Available at: https://www.jmcp.org/doi/epdf/10.18553/jmcp.2018.24.10-a.s1
-
Paz-Bailey G, Adams L, Munoz J, Lozier M, Olsen S, Blanton L, et al. Trends in influenza and other respiratory viruses in Southern Puerto Rico, 2012-2017. Am J Trop Med Hyg. 2018;99(4):524. Available at: https://www.embase.com/records?subaction=viewrecord&id=L627541364
-
Chi H, Chung C-H, Lin Y-J, Lin C-H. Seasonal peaks and risk factors of respiratory syncytial virus infections related hospitalization of preterm infants in Taiwan. PLoS One. 2018;13(5):e0197410. https://doi.org/10.1371/journal.pone.0197410 PMID: 29746578
-
Yu J, Liu C, Xiao Y, Xiang Z, Zhou H, Chen L, et al. Respiratory Syncytial Virus Seasonality, Beijing, China, 2007-2015. Emerg Infect Dis. 2019;25(6):1127-35. https://doi.org/10.3201/eid2506.180532 PMID: 31107230
-
Wrotek A, Czajkowska M, Jackowska T. Seasonality of Respiratory Syncytial Virus Hospitalization. Adv Exp Med Biol. 2020;1279:93-100. https://doi.org/10.1007/5584_2020_503 PMID: 32170670
-
Gentile A, Lucion MF, Juarez MDV, Areso MS, Bakir J, Viegas M, et al. Burden of Respiratory Syncytial Virus Disease and Mortality Risk Factors in Argentina: 18 Years of Active Surveillance in a Children’s Hospital. Pediatr Infect Dis J. 2019;38(6):589-94. https://doi.org/10.1097/INF.0000000000002271 PMID: 30672892
-
Pellegrinelli L, Galli C, Bubba L, Cereda D, Anselmi G, Binda S, et al. Respiratory syncytial virus in influenza-like illness cases: Epidemiology and molecular analyses of four consecutive winter seasons (2014-2015/2017-2018) in Lombardy (Northern Italy). J Med Virol. 2020;92(12):2999-3006. https://doi.org/10.1002/jmv.25917 PMID: 32314816
-
Callahan ZY, Smith TK, Ingersoll C, Gardner R, Korgenski EK, Sloan CD. Comparative Seasonal Respiratory Virus Epidemic Timing in Utah. Viruses. 2020;12(3):275. https://doi.org/10.3390/v12030275 PMID: 32121465
-
Ramaekers K, Keyaerts E, Rector A, Borremans A, Beuselinck K, Lagrou K, et al. Prevalence and seasonality of six respiratory viruses during five consecutive epidemic seasons in Belgium. J Clin Virol. 2017;94:72-8. https://doi.org/10.1016/j.jcv.2017.07.011 PMID: 28772168
-
Shapiro D, Bodinayake CK, Nagahawatte A, Devasiri V, Kurukulasooriya R, Hsiang J, et al. Burden and Seasonality of Viral Acute Respiratory Tract Infections among Outpatients in Southern Sri Lanka. Am J Trop Med Hyg. 2017;97(1):88-96. https://doi.org/10.4269/ajtmh.17-0032 PMID: 28719323
-
Rose EB, Nyawanda BO, Munywoki PK, Murunga N, Bigogo GM, Otieno NA, et al. Respiratory syncytial virus seasonality in three epidemiological zones of Kenya. Influenza Other Respir Viruses. 2021;15(2):195-201. https://doi.org/10.1111/irv.12810 PMID: 33305543
-
Ferrero F, Torres F, Abrutzky R, Ossorio MF, Marcos A, Ferrario C, et al. Seasonality of respiratory syncytial virus in Buenos Aires. Relationship with global climate change. Arch Argent Pediatr. 2016;114(1):52-5. PMID: 26914075
-
Montgomery AS, Lustik MB, Jones MU, Horseman TS. Respiratory Viral Pathogens in Children Evaluated at Military Treatment Facilities in Oahu, Hawaii From 2014 to 2018: Seasonality and Climatic Factors. J Pediatric Infect Dis Soc. 2021;10(4):517-20. https://doi.org/10.1093/jpids/piaa131 PMID: 33219667
-
Servia-Dopazo M, Purriños-Hermida MJ, Pérez S, García J, Malvar-Pintos A, Daporta MT, et al. Utilidad de la vigilancia microbiológica del virus respiratorio sincitial en Galicia (España): 2008-2017. [Usefulness of the microbiological surveillance of respiratory syncytial virus in Galicia (Spain): 2008-2017]. Gac Sanit. 2020;34(5):474-9. https://doi.org/10.1016/j.gaceta.2018.11.009 PMID: 30737055
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