Epidemiology and genetic variability of respiratory syncytial virus in Portugal, 2014-2018

Emma Sáez-López, Paula Cristóvão, Inês Costa, Pedro Pechirra, Patrícia Conde, Raquel Guiomar, Portuguese Laboratory Network for the Diagnosis of Influenza Infection, Maria João Peres, Regina Viseu, Paulo Lopes, Vânia Soares, Fátima Vale, Patricia Fonseca, Ludivina Freitas, Jose Alves, Maria Ana Pessanha, Cristina Toscano, Luísa Mota-Vieira, Rita Cabral Veloso, Rita Côrte-Real, Paula Branquinho, João Pereira-Vaz, Fernando Rodrigues, Mário Cunha, Luís Martins, Paula Mota, Ana Rita Couto, Jácome Bruges-Armas, Sofia Almeida, Débora Rodrigues, Emma Sáez-López, Paula Cristóvão, Inês Costa, Pedro Pechirra, Patrícia Conde, Raquel Guiomar, Portuguese Laboratory Network for the Diagnosis of Influenza Infection, Maria João Peres, Regina Viseu, Paulo Lopes, Vânia Soares, Fátima Vale, Patricia Fonseca, Ludivina Freitas, Jose Alves, Maria Ana Pessanha, Cristina Toscano, Luísa Mota-Vieira, Rita Cabral Veloso, Rita Côrte-Real, Paula Branquinho, João Pereira-Vaz, Fernando Rodrigues, Mário Cunha, Luís Martins, Paula Mota, Ana Rita Couto, Jácome Bruges-Armas, Sofia Almeida, Débora Rodrigues

Abstract

Introduction: Respiratory syncytial virus (RSV) is associated with substantial morbidity and mortality since it is a predominant viral agent causing respiratory tract infections in infants, young children and the elderly. Considering the availability of the RSV vaccines in the coming years, molecular understanding in RSV is necessary.

Objective: The objective of the present study was to describe RSV epidemiology and genotype variability in Portugal during the 2014/15-2017/18 period.

Material and methods: Epidemiological data and RSV-positive samples from patients with a respiratory infection were collected through the non-sentinel and sentinel influenza surveillance system (ISS). RSV detection, subtyping in A and B, and sequencing of the second hypervariable region (HVR2) of G gene were performed by molecular methods. Phylogenetic trees were generated using the Neighbor-Joining method and p-distance model on MEGA 7.0.

Results: RSV prevalence varied between the sentinel (2.5%, 97/3891) and the non-sentinel ISS (20.7%, 3138/16779), being higher (P < 0.0001) among children aged <5 years. Bronchiolitis (62.9%, 183/291) and influenza-like illness (24.6%, 14/57) were associated (P < 0.0001) with RSV laboratory confirmation among children aged <6 months and adults ≥65 years, respectively. The HVR2 was sequenced for 562 samples. RSV-A (46.4%, 261/562) and RSV-B (53.6%, 301/562) strains clustered mainly to ON1 (89.2%, 233/261) and BA9 (92%, 277/301) genotypes, respectively, although NA1 and BA10 were also present until 2015/2016.

Conclusion: The sequence and phylogenetic analysis reflected the relatively high diversity of Portuguese RSV strains. BA9 and ON1 genotypes, which have been circulating in Portugal since 2010/2011 and 2011/2012 respectively, predominated during the whole study period.

Keywords: BA9 genotype; Genetic diversity; Molecular epidemiology; ON1 genotype; Portugal; Respiratory syncytial virus.

Conflict of interest statement

None.

Copyright © 2019 Elsevier B.V. All rights reserved.

Figures

Fig. 1
Fig. 1
Weekly distribution of detected RSV cases between 2014 and 2018 during the influenza season through the Portuguese influenza surveillance system. RSV, Respiratory syncytial virus. (2-column fitting image).
Fig. 2
Fig. 2
Phylogenetic tree of RSV-A strains based on the C-terminal second hypervariable region (HVR2) of the G gene. (A) Complete phylogenetic tree, (B) ON1 strains. The phylogenetic tree was constructed with the Neighbor-Joining method with 1000 replicates for the bootstrap using MEGA 7.0. Only bootstrap values greater than 50 were represented at the branch nodes. The evolutionary distances were computed using the p-distance method and the scale bar represented the number of nucleotide substitutions per site. Reference strains (n = 50) were represented by a black circle. The accession number from GenBank, the country, the year and the genotype from reference strains are shown in the phylogenetic trees. Reference GA1 (AF233917, Z33431, X73354) strains served as outgroup strains. Sequences from this study with 100% nucleotide homology were represented with only one sequence. Different colors distinguished different periods (green, 2010-11; light blue, 2011-12; red, 2012-13; grey, 2013-14; turquoise, 2014-15; purple, 2015-16; orange, 2016-17; strong blue, 2017-18). A circle represented one sequence and a triangle represented more than one sequence from the same period with a bootstrap value greater than 50 (the number of sequences included is indicated between parentheses). Representative RSV-A sequences from this study were deposited in GenBank under accession numbers MN122441-MN122562. (In color online only, 2-column fitting image). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2
Fig. 2
Phylogenetic tree of RSV-A strains based on the C-terminal second hypervariable region (HVR2) of the G gene. (A) Complete phylogenetic tree, (B) ON1 strains. The phylogenetic tree was constructed with the Neighbor-Joining method with 1000 replicates for the bootstrap using MEGA 7.0. Only bootstrap values greater than 50 were represented at the branch nodes. The evolutionary distances were computed using the p-distance method and the scale bar represented the number of nucleotide substitutions per site. Reference strains (n = 50) were represented by a black circle. The accession number from GenBank, the country, the year and the genotype from reference strains are shown in the phylogenetic trees. Reference GA1 (AF233917, Z33431, X73354) strains served as outgroup strains. Sequences from this study with 100% nucleotide homology were represented with only one sequence. Different colors distinguished different periods (green, 2010-11; light blue, 2011-12; red, 2012-13; grey, 2013-14; turquoise, 2014-15; purple, 2015-16; orange, 2016-17; strong blue, 2017-18). A circle represented one sequence and a triangle represented more than one sequence from the same period with a bootstrap value greater than 50 (the number of sequences included is indicated between parentheses). Representative RSV-A sequences from this study were deposited in GenBank under accession numbers MN122441-MN122562. (In color online only, 2-column fitting image). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 3
Fig. 3
Phylogenetic tree of RSV-B strains based on the C-terminal second hypervariable region (HVR2) of the G gene. (A) Complete phylogenetic tree, (B) BA9 strains. The phylogenetic tree was constructed with the Neighbor-joining method with 1000 replicates for the bootstrap using MEGA 7.0. Only bootstrap values greater than 50 were represented at the branch nodes. The evolutionary distances were computed using the p-distance method and the scale bar represented the number of nucleotide substitutions per site. Reference strains (n = 76) were represented by a black circle. The accession number from GenBank, the country, the year and the genotype from reference strains are shown in the phylogenetic trees. Reference GB1 (AF065250, M73540) strains served as outgroup strains. Sequences from this study with 100% nucleotide homology were represented with only one sequence. Different colors distinguished different periods (turquoise, 2014-15; purple, 2015-16; orange, 2016-17; strong blue, 2017-18). A circle represented one sequence and a triangle represented more than one sequence from the same period with a bootstrap value greater than 50 (the number of sequences included is indicated between parentheses). Representative RSV-B sequences from this study were deposited in GenBank under accession numbers MN122563-MN122694. (In color online only, 2-column fitting image). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 3
Fig. 3
Phylogenetic tree of RSV-B strains based on the C-terminal second hypervariable region (HVR2) of the G gene. (A) Complete phylogenetic tree, (B) BA9 strains. The phylogenetic tree was constructed with the Neighbor-joining method with 1000 replicates for the bootstrap using MEGA 7.0. Only bootstrap values greater than 50 were represented at the branch nodes. The evolutionary distances were computed using the p-distance method and the scale bar represented the number of nucleotide substitutions per site. Reference strains (n = 76) were represented by a black circle. The accession number from GenBank, the country, the year and the genotype from reference strains are shown in the phylogenetic trees. Reference GB1 (AF065250, M73540) strains served as outgroup strains. Sequences from this study with 100% nucleotide homology were represented with only one sequence. Different colors distinguished different periods (turquoise, 2014-15; purple, 2015-16; orange, 2016-17; strong blue, 2017-18). A circle represented one sequence and a triangle represented more than one sequence from the same period with a bootstrap value greater than 50 (the number of sequences included is indicated between parentheses). Representative RSV-B sequences from this study were deposited in GenBank under accession numbers MN122563-MN122694. (In color online only, 2-column fitting image). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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https://www.ncbi.nlm.nih.gov/pmc/articles/instance/7106440/bin/mmc3_lrg.jpg

References

    1. Mufson M.A., Orvell C., Rafnar B., Norrby E. Two distinct subtypes of human respiratory syncytial virus. J. Gen. Virol. 1985;66:2111–2124. doi: 10.1099/0022-1317-66-10-2111.
    1. Borchers A.T., Chang C., Gershwin M.E., Gershwin L.J. Respiratory syncytial virus—a comprehensive review. Clin. Rev. Allergy Immunol. 2013;45:331–379. doi: 10.1007/s12016-013-8368-9.
    1. Asgari N., Mardy S., Arnott A., Vong S., Naughtin M., Touch S., Guillard B., Sovann L., Rith S., Chu S., Deubel V., Frutos R., Buchy P., Buecher C., Borand L., Beaute J. A study of the genetic variability of human respiratory syncytial virus (HRSV) in Cambodia reveals the existence of a new HRSV group B genotype. J. Clin. Microbiol. 2011;49:3504–3513. doi: 10.1128/jcm.01131-11.
    1. Trento A., Ábrego L., Rodriguez-Fernandez R., González-Sánchez M.I., González-Martínez F., Delfraro A., Pascale J.M., Arbiza J., Melero J.A. Conservation of G-protein epitopes in respiratory syncytial virus (Group A) despite broad genetic diversity: is antibody selection involved in virus evolution? J. Virol. 2015;89:7776–7785. doi: 10.1128/jvi.00467-15.
    1. Venter M., Madhi S.A., Tiemessen C.T., Schoub B.D. Genetic diversity and molecular epidemiology of respiratory syncytial virus over four consecutive seasons in South Africa : identi cation of new subgroup A and B genotypes. J. Gen. Virol. 2001;1997:2117–2124. doi: 10.1099/0022-1317-82-9-2117.
    1. Zhang Z.Y., Du L.N., Chen X., Zhao Y., Liu E.M., Yang X.Q., Zhao X. Genetic variability of respiratory syncytial viruses (RSV) prevalent in Southwestern China from 2006 to 2009: emergence of subgroup B and A RSV as dominant strains. J. Clin. Microbiol. 2010;48:1201–1207. doi: 10.1128/JCM.02258-09.
    1. Choi Y.-K., Choi E.H., Baek Y.H., Song M.-S., Lee J.H., Han H.-S., Pascua P.N.Q., Hahn Y.-S., Park S.-J., Kim S.-Y., Jang H.-L., Kwon H., Ahn B.-H., Woo S.-I., Shin K.-S. Prevalence and genetic characterization of respiratory syncytial virus (RSV) in hospitalized children in Korea. Arch. Virol. 2012;157:1039–1050. doi: 10.1007/s00705-012-1267-1.
    1. Cui G., Zhu R., Qian Y., Deng J., Zhao L., Sun Y., Wang F. Genetic variation in attachment glycoprotein genes of human respiratory syncytial virus subgroups A and B in children in recent five consecutive years. PLoS One. 2013;8 doi: 10.1371/journal.pone.0075020.
    1. Auksornkitti V., Kamprasert N., Thongkomplew S., Suwannakarn K., Theamboonlers A., Samransamruajkij R., Poovorawan Y. Molecular characterization of human respiratory syncytial virus, 2010-2011: identification of genotype ON1 and a new subgroup B genotype in Thailand. Arch. Virol. 2014;159:499–507. doi: 10.1007/s00705-013-1773-9.
    1. Gimferrer L., Andrés C., Campins M., Codina M.G., Rodrigo J.A., Melendo S., Martin M.C., Fuentes F., Saiz M.R., Esperalba J., Bruguera A., Vilca L.M., Armadans L., Pumarola T., Antón A. Circulation of a novel human respiratory syncytial virus Group B genotype during the 2014–2015 season in Catalonia (Spain) Clin. Microbiol. Infect. 2016;22:97. doi: 10.1016/j.cmi.2015.09.013. e5-97.e8.
    1. Arbiza J., Castillo J., Pascale J.M., Delfraro A., López-Vergès S., Franco D., Ábrego L.E., Moreno B., Castillo M. Genetic variability of human respiratory syncytial virus group B in Panama reveals a novel genotype BA14. J. Med. Virol. 2017;89:1734–1742. doi: 10.1002/jmv.24838.
    1. Shi T., McAllister D.A., O’Brien K.L., Simoes E.A.F., Madhi S.A. Global, regional, and national disease burden estimates of acute lower respiratory infections due to respiratory syncytial virus in young children in 2015: a systematic review and modelling study. Lancet. 2017;390:946–958. doi: 10.1016/S0140-6736(17)30938-8.
    1. Broberg E.K., Waris M., Johansen K., Snacken R., Penttinen P., Influenza E., Network S., Broberg E., Eeva B., Matti W., Kari J., René S., Pasi P. Seasonality and geographical spread of respiratory syncytial virus epidemics in 15 European countries, 2010 to 2016. Euro Surveill. 2018 doi: 10.2807/1560-7917.
    1. Shi T., Denouel A., Tietjen A.K., Campbell I., Moran E., Li X., Campbell H., Demont C., Nyawanda B.O., Chu H.Y., Stoszek S.K., Krishnan A., Openshaw P., Falsey A.R., Nair H., Nair H., Campbell H., Shi T., Zhang S., Li Y., Openshaw P., Wedzicha J., Falsey A., Miller M., Beutels P., Bont L., Pollard A., Molero E., Martinon-Torres F., Heikkinen T., Meijer A., Fischer T.K., van den Berge M., Giaquinto C., Mikolajczyk R., Hackett J., Cai B., Knirsch C., Leach A., Stoszek S.K., Gallichan S., Kieffer A., Demont C., Denouel A., Cheret A., Gavart S., Aerssens J., Fuentes R., Rosen B. Global disease burden estimates of respiratory syncytial virus–associated acute respiratory infection in older adults in 2015: a systematic review and meta-analysis. J. Infect. Dis. 2019 doi: 10.1093/infdis/jiz059.
    1. European Centre for Disease Prevention and Control (ECDC) Workshop on burden of RSV disease in Europe. ECDC Expert Consultation Meeting; Stockholm. 23-24 November; 2015. pp. 1–22. ECDC RSV surv and burden of disease workshop 23-24 Nov.pdf.
    1. Direção-Geral da Saúde . 2015. Atualização de norma DGS: prescrição de Palivizumab para prevenção de infeção pelo vírus sincicial respiratório em crianças de risco | a enfermagem e as leis. (accessed November 21, 2017)
    1. C.O.I.D.A.B.G American Academy of Pediatrics Committee on Infectious Diseases, American Academy of Pediatrics 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. World Health Organization Preferred product characteristics for respiratory syncytial virus (RSV) Vaccines. 2017:1–16.
    1. Rezaee F., Linfield D.T., Harford T.J., Piedimonte G. Ongoing developments in RSV prophylaxis: a clinician’s analysis. Curr. Opin. Virol. 2017;24:70–78. doi: 10.1016/j.coviro.2017.03.015.
    1. Tripp R.A., Power U.F., Openshaw P.J.M., Kauvar L.M. Respiratory syncytial virus: targeting the G protein provides a new approach for an old problem. J. Virol. 2018;92 doi: 10.1128/JVI.01302-17.
    1. 2018. I-MOVE in Europe. . (accessed June 17, 2019)
    1. European Commission . 2018. Commission Implementing Decision (EU) 2018/945 of 22 June 2018 on the Communicable Diseases and Related Special Health Issues to Be Covered by Epidemiological Surveillance As Well As Relevant Case Definitions. 1–74.
    1. Gunson R.N., Collins T.C., Carman W.F. Real-time RT-PCR detection of 12 respiratory viral infections in four triplex reactions. J. Clin. Virol. 2005;33:341–344. doi: 10.1016/j.jcv.2004.11.025.
    1. Östlund M.R., Lindell A.T., Stenler S., Riedel H.M., Wirgart B.Z., Grillner L. Molecular epidemiology and genetic variability of respiratory syncytial virus (RSV) in Stockholm, 2002–2003. J. Med. Virol. 2008;80:159–167. doi: 10.1002/jmv.21066.
    1. Trento A., Casas I., Calderon A., Garcia-Garcia M.L., Calvo C., Perez-Brena P., Melero J.A. Ten years of global evolution of the human respiratory syncytial virus BA genotype with a 60-Nucleotide duplication in the G protein gene. J. Virol. 2010;84:7500–7512. doi: 10.1128/JVI.00345-10.
    1. Peret T.C., Golub J.A., Anderson L.J., Hall C.B., Schnabel K.C. Circulation patterns of genetically distinct group A and B strains of human respiratory syncytial virus in a community. J. Gen. Virol. 1998;79:2221–2229. doi: 10.1099/0022-1317-79-9-2221.
    1. Guiomar R., Cristóvão P., Conde P., Pechirra P. Molecular epidemiology of respiratory syncytial virus between 2010–2015, in Portugal. J. Clin. Virol. 2015;70 doi: 10.1016/j.jcv.2015.07.117. S49.
    1. Bellei N., Carraro E., Perosa A., Watanabe A., Arruda E., Granato C. Acute respiratory infection and influenza-like illness viral etiologies in Brazilian adults. J. Med. Virol. 2008;80:1824–1827. doi: 10.1002/jmv.21295.
    1. Noh J.Y., Song J.Y., Cheong H.J., Choi W.S., Lee J., Lee J.-S., Wie S.-H., Jeong H.W., Kim Y.K., Choi S.H., Han S.B., So B.-H., Kim H., Kim W.J. Laboratory surveillance of influenza-like illness in seven teaching hospitals, South Korea: 2011-2012 season. PLoS One. 2013;8 doi: 10.1371/journal.pone.0064295.
    1. Yu X., Kou Y., Xia D., Li J., Yang X., Zhou Y., He X. Human respiratory syncytial virus in children with lower respiratory tract infections or influenza-like illness and its co-infection characteristics with viruses and atypical bacteria in Hangzhou, China. J. Clin. Virol. 2015;69:1–6. doi: 10.1016/j.jcv.2015.05.015.
    1. Vos L.M., Teirlinck A.C., Lozano J.E., Vega T., Donker G.A., Hoepelman A.I., Bont L.J., Oosterheert J.J., Meijer A. Use of the moving epidemic method (MEM) to assess national surveillance data for respiratory syncytial virus (RSV) in the Netherlands, 2005 to 2017. Eurosurveillance. 2019;24 doi: 10.2807/1560-7917.ES.2019.24.20.1800469.
    1. Sáez-López E., Pechirra P., Costa I., Cristóvão P., Machado A., Rodrigues A.P., Guiomar R. Evaluation of ECDC Influenza-like illness (ILI) case definition to detect respiratory syncytial virus (RSV) infection through the Influenza Surveillance System in Portugal. Eur. Sci. Conf. Appl. Infect. Dis. Epidemiol. Abstract. 2018:623.
    1. Fall A., Dia N., Cisse E.H.A.K., Kiori D.E., Sarr F.D., Sy S., Goudiaby D., Richard V., Niang M.N. Epidemiology and molecular characterization of human respiratory syncytial virus in Senegal after four consecutive years of surveillance, 2012–2015. PLoS One. 2016;11 doi: 10.1371/JOURNAL.PONE.0157163.
    1. Thongpan I., Suntronwong N., Vichaiwattana P., Wanlapakorn N., Vongpunsawad S., Poovorawan Y. Respiratory syncytial virus, human metapneumovirus, and influenza virus infection in Bangkok, 2016-2017. PeerJ. 2019;7:e6748. doi: 10.7717/peerj.6748.
    1. Gimferrer L., Vila J., Piñana M., Andrés C., Rodrigo-Pendás J.A., Peremiquel-Trillas P., Codina M.G., del C Martín M., Esperalba J., Fuentes F., Rubio S., Campins-Martí M., Pumarola T., Antón A. Virological surveillance of human respiratory syncytial virus A and B at a tertiary hospital in Catalonia (Spain) during five consecutive seasons (2013–2018) Future Microbiol. 2019;14:373–381. doi: 10.2217/fmb-2018-0261.
    1. Babu B.V.S., Gunasekaran P., Venkataraman P., Mohana S., Kiruba R., Ruban K., Magesh S., Indhumathi C., Anupama C., Sheriff A., Arunagiri K., Kaveri K. Prevalence and molecular characterization of circulating respiratory syncytial virus (RSV) in Chennai, South India during 2011-2014. Biosci. Biotechnol. Res. Asia. 2016;13:1055–1062. doi: 10.13005/bbra/2132.
    1. Patil S.L., Balakrishnan A. Genetic characterization respiratory syncytial virus in Kerala, the southern part of India. J. Med. Virol. 2017;89:2092–2097. doi: 10.1002/jmv.24842.
    1. Tabatabai J., Prifert C., Pfeil J., Grulich-Henn J., Schnitzler P. Novel respiratory syncytial virus (RSV) genotype ON1 predominates in germany during winter season 2012-13. PLoS One. 2014;9 doi: 10.1371/journal.pone.0109191.
    1. Fan R., Fan C., Zhang J., Wen B., Lei Y., Liu C., Chen L., Liu W., Wang C., Qu X. Respiratory syncytial virus subtype ON1/NA1/BA9 predominates in hospitalized children with lower respiratory tract infections. J. Med. Virol. 2017;89:213–221. doi: 10.1002/jmv.24619.
    1. Korsun N., Angelova S., Tzotcheva I., Georgieva I., Lazova S., Parina S., Alexiev I., Perenovska P. Prevalence and genetic characterisation of respiratory syncytial viruses circulating in Bulgaria during the 2014/15 and 2015/16 winter seasons. Pathog. Glob. Health. 2017;7724:1–11. doi: 10.1080/20477724.2017.1375708.
    1. Obodai E., Odoom J.K., Adiku T., Goka B., Wolff T., Biere B., Schweiger B., Reiche J. The significance of human respiratory syncytial virus (HRSV) in children from Ghana with acute lower respiratory tract infection: a molecular epidemiological analysis, 2006 and 2013-2014. PLoS One. 2018;13:1–17. doi: 10.1371/journal.pone.0203788.
    1. Cristóvão P., Pereira D., Pechirra P., Pereira-Vaz J., Correia L., Rodrigues F., Andrade G., Côrte-Real R., Branquinho P., Peres M.J., Viseu R., Balseiro M.J., Mota P., Guiomar R. Molecular characterization of respiratory syncytial virus during 2015-2016 season in Portugal. J. Clin. Virol. 2016;82 doi: 10.1016/j.jcv.2016.08.244. S122.
    1. Papadopoulos N.G., Gourgiotis D., Javadyan A., Bossios A., Kallergi K., Psarras S., Tsolia M.N., Kafetzis D. Does respiratory syncytial virus subtype influences the severity of acute bronchiolitis in hospitalized infants? Respir. Med. 2004;98:879–882. doi: 10.1016/j.rmed.2004.01.009.
    1. Ogunsemowo O., Olaleye D.O., Odaibo G.N. Human respiratory syncytial virus subtypes A and B infection among children attending primary and secondary health care facilities in Ibadan, Nigeria. Arch. Basic Appl. Med. 2018;6:73–78. (accessed May 8, 2019)
    1. Esposito S., Piralla A., Zampiero A., Bianchini S., Di Pietro G., Scala A., Pinzani R., Fossali E., Baldanti F., Principi N. Characteristics and their clinical relevance of respiratory syncytial virus types and genotypes circulating in Northern Italy in five consecutive winter seasons. PLoS One. 2015;10 doi: 10.1371/journal.pone.0129369.
    1. Vos L.M., Bont L.J., Viveen M., Kuil S.D., Oosterheert J.J., Coenjaerts F.E.J., Hoepelman A.I.M. High epidemic burden of RSV disease coinciding with genetic alterations causing amino acid substitutions in the RSV G-protein during the 2016/2017 season in the Netherlands. J. Clin. Virol. 2019;112:20–26. doi: 10.1016/j.jcv.2019.01.007.
    1. Houspie L., Lemey P., Keyaerts E., Reijmen E., Vergote V., Vankeerberghen A., Vaeyens F., De Beenhouwer H., Van Ranst M. Circulation of HRSV in Belgium: from multiple genotype circulation to prolonged circulation of predominant genotypes. PLoS One. 2013;8 doi: 10.1371/journal.pone.0060416.
    1. Kim Y.-J., Kim D.-W., Lee W.-J., Yun M.-R., Lee H.Y., Lee H.S., Jung H.-D., Kim K. Rapid replacement of human respiratory syncytial virus A with the ON1 genotype having 72 nucleotide duplication in G gene. Infect. Genet. Evol. 2014;26:103–112. doi: 10.1016/j.meegid.2014.05.007.
    1. Gaymard A., Bouscambert-Duchamp M., Pichon M., Frobert E., Vallee J., Lina B., Casalegno J.S., Morfin F. Genetic characterization of respiratory syncytial virus highlights a new BA genotype and emergence of the ON1 genotype in Lyon, France, between 2010 and 2014. J. Clin. Virol. 2018;102:12–18. doi: 10.1016/j.jcv.2018.02.004.
    1. Haider M.S.H., Khan W.H., Deeba F., Ali S., Ahmed A., Naqvi I.H., Dohare R., Alsenaidy H.A., Alsenaidy A.M., Broor S., Parveen S. BA9 lineage of respiratory syncytial virus from across the globe and its evolutionary dynamics. PLoS One. 2018;13:1–22. doi: 10.1371/journal.pone.0193525.
    1. Slovic A., Ivancic-Jelecki J., Ljubin-Sternak S., Galinović G.M., Forcic D. A molecular epidemiological study of human respiratory syncytial virus in Croatia, 2011–2014. Infect. Genet. Evol. 2016;44:76–84. doi: 10.1016/j.meegid.2016.06.036.
    1. Frabasile S., Delfraro A., Facal L., Videla C., Galiano M., De Sierra M.J., Ruchansky D., Vitureira N., Berois M., Carballal G., Russi J., Arbiza J. Antigenic and genetic variability of human respiratory syncytial viruses (group A) isolated in Uruguay and Argentina: 1993-2001. J. Med. Virol. 2003;71:305–312. doi: 10.1002/jmv.10484.
    1. Tan L., Lemey P., Houspie L., Viveen M.C., Jansen N.J.G., van Loon A.M., Wiertz E., van Bleek G.M., Martin D.P., Coenjaerts F.E. Genetic variability among complete human respiratory syncytial virus subgroup A genomes: bridging molecular evolutionary dynamics and epidemiology. PLoS One. 2012;7 doi: 10.1371/journal.pone.0051439.
    1. Ogunsemowo O., Olaleye D.O., Odaibo G.N. Genetic diversity of human respiratory syncytial virus circulating among children in Ibadan, Nigeria. PLoS One. 2018;13 doi: 10.1371/journal.pone.0191494.
    1. Abou-El-Hassan H., Massaad E., Soudani N., Assaf-Casals A., Shaker R., Khoury M.L., Ghanem S., Karam M., Andary R., Saito R., Dbaibo G., Zaraket H. Detection of ON1 and novel genotypes of human respiratory syncytial virus and emergence of palivizumab resistance in Lebanon. PLoS One. 2019;14:1–18. doi: 10.1371/journal.pone.0212687.
    1. Malasao R., Okamoto M., Chaimongkol N., Imamura T., Tohma K., Dapat I., Dapat C., Suzuki A., Saito M., Saito M., Tamaki R., Pedrera-Rico G.A.G., Aniceto R., Quicho R.F.N., Segubre-Mercado E., Lupisan S., Oshitani H. Molecular characterization of human respiratory syncytial virus in the Philippines, 2012-2013. PLoS One. 2015;10 doi: 10.1371/journal.pone.0142192.
    1. Eshaghi A.R., Duvvuri V.R., Lai R., Nadarajah J.T., Li A., Patel S.N., Low D.E., Gubbay J.B. Genetic variability of human respiratory syncytial virus a strains circulating in Ontario: a novel genotype with a 72 nucleotide G gene duplication. PLoS One. 2012;7 doi: 10.1371/journal.pone.0032807.
    1. Thongpan I., Mauleekoonphairoj J., Vichiwattana P., Korkong S., Wasitthankasem R., Vongpunsawad S., Poovorawan Y. Respiratory syncytial virus genotypes NA1, ON1, and BA9 are prevalent in Thailand, 2012–2015. PeerJ. 2017;5:e3970. doi: 10.7717/peerj.3970.
    1. Dapat I.C., Shobugawa Y., Sano Y., Saito R., Sasaki A., Suzuki Y., Kumaki A., Zaraket H., Dapat C., Oguma T., Yamaguchi M., Suzuki H. New genotypes within respiratory syncytial virus group B genotype BA in Niigata, Japan. J. Clin. Microbiol. 2010;48:3423–3427. doi: 10.1128/JCM.00646-10.
    1. Hotard A.L., Laikhter E., Brooks K., Hartert T.V., Moore M.L. Functional analysis of the 60-nucleotide duplication in the respiratory syncytial virus Buenos Aires strain attachment glycoprotein. J. Virol. 2015;89:8258–8266. doi: 10.1128/JVI.01045-15.

Source: PubMed

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