Detection and characterization of type B influenza virus from influenza-like illness cases during the 2017–2018 winter influenza season in Beijing, China
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In the winter of 2017-2018, there was significant influenza activity in China, resulting in unprecedented usage of influenza rapid antigen tests (IRAT) and neuraminidase inhibitors (NAIs). The aim of this study was to characterize the most prevalent influenza virus type in a clinical setting with respect to diagnosis and concomitant NAI treatment. From Dec 2017 to Jan 2018, 3257 patients with influenza-like illness (ILI) were screened using IRAT. We summarized and compared the results with the last influenza season. Subtyping of influenza B viruses and identification of NAI drug resistance mutations were carried out by sequencing the HA and NA genes and aligning these with genetic isotypes. The performance of IRAT and RT-PCR was compared. Screening results indicated that influenza B virus was the leading cause of this influenza epidemic, with children being more susceptible to infection than adults. Phylogenetic analysis revealed that the prevailing influenza B virus belonged to the Yamagata lineage and were genetically similar to strains isolated from North America in the same influenza season. Cross-continental spread of influenza/B/Yamagata occurred. NAI resistance mutations were not identified in the 18 samples analyzed. The current antiviral protocol was still effective for influenza B control. RT-PCR positivity was significantly higher than that of IRAT (P = 0.004). IRAT and RT-PCR had a consistency rate of 86.9%, with the consistency rates of the positive and negative cases being 54.3% and 97.3%, respectively. Clinicians should be alert to the possibility of obtaining false negative results when using IRAT, and RT-PCR is recommended to improve the accuracy of pathogen detection.
We thank our colleagues at the pediatric and respiratory departments for assistance with sample collection. We also appreciate Yihuan Dong at the Affiliated High School of Peking University for her help with RNA extraction and PCR analysis.
This work was supported by Beijing Municipal Science and Technology Commission Program of China (Grant no. Z181100001718148).
Compliance with ethical standards
Conflict of interest
The authors declare no potential conflicts of interest.
The study was approved by the IRB in Beijing Tsinghua Chang-gung Hospital.
- 6.Orsi A, Colomba GME, Pojero F, Calamusa G, Alicino C, Trucchi C, Canepa P, Ansaldi F, Vitale F, Tramuto F (2018) Trends of influenza B during the 2010–2016 seasons in 2 regions of north and south Italy: the impact of the vaccine mismatch on influenza immunisation strategy. Hum Vaccin Immunother 14(3):523–531. https://doi.org/10.1080/21645515.2017.1342907 Google Scholar
- 9.Orsi A, Gme C, Pojero F, Calamusa G, Alicino C, Trucchi C, Canepa P, Ansaldi F, Vitale F, Tramuto F (2017) Trends of influenza B during the 2010–2016 seasons in two regions of north and south Italy: the impact of the vaccine mismatch on influenza immunisation strategy. Hum Vaccin Immunother 14(3):523–531. https://doi.org/10.1080/21645515.2017.1342907 Google Scholar
- 10.Rota PA, Wallis TR, Harmon MW, Rota JS, Kendal AP, Nerome K (1990) Cocirculation of two distinct evolutionary lineages of influenza type B virus since 1983. Virology 175(1):59–68Google Scholar
- 11.Xi-Yan LI, Cheng YH, Tan MJ, Wang Z, Huang WJ, Guo JF, Wei HJ, Xiao N, Lan Y, Zhao X (2014) Antigenic and genetic characteristics of influenza B virus in the mainland of China, 2012–2013. Dis Surveill 29(1):14–20. https://doi.org/10.13242/j.cnki.bingduxuebao.002349 Google Scholar
- 13.Zhu D, Zhao XY, Yao Y, Dai FF, He H, Li RQ, Jin RH, Liang LC, Li N (2013) A new factor influencing pathogen detection by molecular assay in children with both mild and severe hand, foot, and mouth disease. Diagn Microbiol Infect Dis 76(2):162–167. https://doi.org/10.1016/j.diagmicrobio.2013.02.011 Google Scholar
- 15.Cohen JM, Silva ML, Caini S, Ciblak M, Mosnier A, Daviaud I, Matias G, Badur S, Valette M, Enouf V (2015) Striking similarities in the presentation and duration of illness of influenza A and B in the community: a study based on sentinel surveillance networks in France and Turkey, 2010–2012. PLoS One 10(10):0139431. https://doi.org/10.1371/journal.pone.0139431 Google Scholar
- 16.Su S, Chaves SS, Perez A, D’Mello T, Kirley PD, Youseyhindes K, Farley MM, Harris M, Sharangpani R, Lynfield R (2014) Comparing clinical characteristics between hospitalized adults with laboratory-confirmed influenza A and B virus infection. Clin Infect Dis 59(2):252. https://doi.org/10.1093/cid/ciu269 Google Scholar
- 20.McCullers JA, Saito T, Iverson AR (2004) Multiple genotypes of influenza B virus circulated between 1979 and 2003. J Virol 78(23):12817–12828. https://doi.org/10.1128/JVI.78.23.12817-12828.2004 Google Scholar
- 21.Nerome R, Hiromoto Y, Sugita S, Tanabe N, Ishida M, Matsumoto M, Lindstrom SE, Takahashi T, Nerome KJAOV (1998) Evolutionary characteristics of influenza B virus since its first isolation in 1940: dynamic circulation of deletion and insertion mechanism. Adv Virol 143(8):1569–1583Google Scholar
- 22.Recommended composition of influenza virus vaccines for use in the 2002–2003 season (2002). Wkly Epidemiol Rec 77(8):62Google Scholar
- 23.Nakagawa N, Kubota R, Maeda A, Nakagawa T, Okuno YJJOCM (2000) Heterogeneity of influenza B virus strains in one epidemic season differentiated by monoclonal antibodies and nucleotide sequences. J Clin Microbiol 38(9):3467–3469Google Scholar
- 24.Hy M, Yy L, Jy Y (2008) Molecular and antigenic characteristics of influenza B virus isolated in Zhejiang province in 2006. Chin J Epidemiol 29(4):413–414Google Scholar
- 27.Mao HY, Zhou M, Zhang YJ, Chen Y, Xu CP, Li Z, Yan JY, Lu YY (2011) Genetic variation of the hemagglutinin and neuraminidase of influenza B viruses isolated in Zhejiang province during 1999–2010. Chin J Epidemiol 32(4):376–381Google Scholar
- 28.Juan Y, Yiu Chung L, Peng W, Luzhao F, Xiling W, Tao C, Sheikh TA, Zhibin P, Vicky JF, Juanjuan Z, Yangni H, Eric HYL, Ying Q, Jing Y, Jiandong Z, Hui J, Hongjie Y, Benjamin JC (2018) Variation in influenza B virus epidemiology by lineage, China. Emerg Infect Dis J 24(8):1536. https://doi.org/10.3201/eid2408.180063 Google Scholar
- 29.Skowronski DM, Janjua NZ, Sabaiduc S, De SG, Winter AL, Gubbay JB, Dickinson JA, Fonseca K, Charest H, Bastien N (2014) Influenza A/subtype and B/lineage effectiveness estimates for the 2011-2012 trivalent vaccine cross-season and cross-lineage protection with unchanged vaccine. J Infect Dis 210(1):126. https://doi.org/10.1093/infdis/jiu048 Google Scholar
- 31.Yan-Ning LV, Peng XM, Liang HJ, Yang P, Gui-Lan LU, Cui SJ, Shi WX, Huang F, Pang XH (2011) Analysis on the characteristics of HA gene of influenza virus B circulated in Beijing area from 2009 to 2010. Chin J Dis Control Prevent 15(8):689–694Google Scholar
- 32.Chen J, Yang K, Zhang M, Shen C, Chen J, Wang G, Huang S, Zhang M, Xiong H, Chen H, Chen Y, Xia N (2018) Rapid identification of imported influenza viruses at Xiamen International Airport via an active surveillance program. Clin Microbiol Infect 24(3):289–294. https://doi.org/10.1016/j.cmi.2017.05.027 Google Scholar
- 33.Ishiguro N, Koseki N, Kaiho M, Ariga T, Kikuta H, Oba K, Togashi T, Morita K, Inagawa A, Okamura A, Yamazaki S, Shida S, Konno M, Kawamura N, Ishizaka A, Takada K, Tsubakihara K, Nagano N, Shibata M, Furuyama H, Matsuzono Y, Koike A, Murashita M, Hatae Y, Arioka H, Yamanaka T, Watanabe T, Tabata Y, Kumita Y, Hazama K, Akutsu Y, Aoyagi H, Tobise C, Azuma K, Yasoshima K, Sawada Y, Uetsuji K, Tsuchida A, Tsuchiyama A, Yasuda K, Odagawa Y, Yoshioka M (2018) Clinical effectiveness of four neuraminidase inhibitors (oseltamivir, zanamivir, laninamivir, and peramivir) for children with influenza A and B in the 2014–2015 to 2016–2017 influenza seasons in Japan. J Infect Chemother 24(6):449–457. https://doi.org/10.1016/j.jiac.2018.01.013 Google Scholar
- 38.Sakai-Tagawa Y, Yamayoshi S, Kawakami C, Le MQ, Uchida Y, Saito T, Nidom CA, Humaira I, Toohey-Kurth K, Arafa AS, Liu MT, Shu Y, Kawaoka Y (2017) Reactivity and sensitivity of commercially available influenza rapid diagnostic tests in Japan. Sci Rep 7(1):14483. https://doi.org/10.1038/s41598-017-14536-0 Google Scholar
- 39.Noh JY, Choi WS, Lee J, Kim HL, Song JY, Cheong HJ, Kim WJ (2015) Clinical performance of the Sofia™ Influenza A + B FIA in adult patients with influenza-like illness. Diagn Microbiol Infect Dis 83(2):130–132. https://doi.org/10.1016/j.diagmicrobio.2015.05.016 Google Scholar
- 40.Lewandrowski K, Tamerius J, Menegus M, Olivo PD, Lollar R, Lee-Lewandrowski E (2013) Detection of influenza A and B viruses with the Sofia AnalyzerA novel, rapid immunofluorescence-based in vitro diagnostic device. Am J Clin Pathol 139(5):684–689. https://doi.org/10.1309/AJCP7ZTLJCP3LLMA Google Scholar
- 43.Hassan F, Nguyen A, Formanek A, Bell JJ, Selvarangan R (2014) Comparison of the BD Veritor System for Flu A+B with the Alere BinaxNOW Influenza A&B Card for Detection of Influenza A and B Viruses in Respiratory Specimens from Pediatric Patients. J Clin Microbiol 52(3):906–910. https://doi.org/10.1128/jcm.02484-13 Google Scholar
- 44.Dunn J, Obuekwe J, Baun T, Rogers J, Patel T, Snow L (2014) Prompt detection of influenza A and B viruses using the BD Veritor™ System Flu A+B, Quidel® Sofia® Influenza A+B FIA, and Alere BinaxNOW® Influenza A&B compared to real-time reverse transcription-polymerase chain reaction (RT-PCR). Diagn Microbiol Infect Dis 79(1):10–13. https://doi.org/10.1016/j.diagmicrobio.2014.01.018 Google Scholar
- 45.Akaishi Y, Matsumoto T, Harada Y, Hirayama Y (2016) Evaluation of the rapid influenza detection tests GOLD SIGN FLU and Quick Navi-Flu for the detection of influenza A and B virus antigens in adults during the influenza season. Int J Infect Dis 52:55–58. https://doi.org/10.1016/j.ijid.2016.10.002 Google Scholar