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Background: Annual influenza vaccination is the most effective way to prevent influenza. Influenza vaccines have traditionally included the hemagglutinins (HA) and neuraminidases (NA) from the two A viruses (H1N1 and H3N2) and either B Yamagata or B Victoria. Mismatches between circulating isolates of influenza B and the vaccines are very common. Taking 2017/2018 winter in northern hemisphere as an example, this study was designed to find out the reasons for mismatch between the trivalent influenza vaccine (TIV) and most of the epidemic isolates at that time, and to discuss if there are some optimized programs for seasonal influenza vaccines. Methods: HA and NA sequences of the seasonal isolates circulating from December 1, 2017 to February 28, 2018, and in the previously other 7 winters in northern hemisphere from Global Initiative on Sharing All Influenza Data (GISAID) and the influenza database of National Center for Biotechnology Information (NCBI). Phylogenetic trees and genetic distances were constructed or calculated by using MAFFT and MEGA 6.0 software. Results: Influenza B composition in the TIV recommendation mismatched most of circulating viruses in 2017/2018 winter; the vaccine strain was from the B/Victoria lineage, while most of epidemic isolates were from the B/Yamagata lineage. The epidemic lineage of influenza B reached its peak a little late in the previous winter might be responsible for this mismatch. During 2010–2018, the mean genetic distances between epidemic isolates of influenza A (H1N1 and H3N2) and the vaccines were no higher than 0.02375 ± 0.00341 in both HA and NA. However, concerning influenza B virus, when forecasting done well, the mean genetic distances between epidemic isolates and the vaccines were no higher than 0.02368 ± 0.00272; otherwise, the distances could reach 0.13695 ± 0.00238. Conclusion: When applying quadrivalent influenza vaccines (QIVs) for vaccination, the recommendations of compositions for influenza B could be altered and assessed once in 3 or 4 years; when economic burden was considered intensively and TIVs were utilized, the recommended compositions for influenza B could be announced in April or May, rather than in February or March as now. Keywords: Seasonal influenza, Northern hemisphere, Vaccine, Influenza B Background influenza-related respiratory illnesses annually, higher Influenza (flu) is a contagious acute respiratory infection, than the previous estimate of 250,000 to 500,000 [1, 2]. causing considerable global morbidity, mortality and Influenza viruses, the pathogens which are responsible economic burden every year. According to a new esti- for these infections, belong to the Orthomyxoviridae mate based on a robust, multinational survey, between family and are widely distributed among mammals and 291,000 and 646,000 people worldwide die from seasonal birds. They are divided into 4 different types A, B, C, and D based on variation in their expressed matrix and nucleoproteins, and the vast majority of human disease * Correspondence: firstname.lastname@example.org Department of Public Health Microbiology, School of Public Health, Fudan is caused by types A and B [3, 4]. Since 1977, four sub- University, Shanghai 200032, China types or lineages viruses–two A viruses (H1N1 and School of Public Health, Fudan University, Key Laboratory of Public Health Safety, Ministry of Education, Shanghai 200032, China Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. He et al. Antimicrobial Resistance and Infection Control (2019) 8:164 Page 2 of 7 H3N2) and two B viruses (B Yamagata and B Victoria) and NA genes of influenza viruses by reverse transcription co-circulate annually and globally . polymerase chain reaction, and an additional procedure It is widely accepted that an annual influenza vaccin- includes consideration of antigenic mismatch between ation is the most effective way to prevent influenza . vaccine strains and actual epidemic strains, enables people Influenza vaccines have traditionally included the hem- to early identify the strain divergences from the recom- agglutinins and neuraminidases from the two influenza mended vaccine this year and to forecast the new compos- A viruses (H1N1 and H3N2) and either Yamagata ition for next winter [5, 12, 13]. The whole procedure will lineage or Victoria lineage of influenza B virus. In both be completed in February or March, and the recom- influenza A and B, there exists possibilities of mismatch mended compositions of vaccine for the next winter in between epidemic isolates and vaccine strains. When an- northern hemisphere are announced soon . Hence, tigens in a vaccine match those of circulating isolates, exactly identifying the genetic and antigenic characteristics the vaccine is considered as effective. However, antigens of the isolates established in the former winter is essential contained in the vaccine do not always match the circu- to accurately forecast the compositions of vaccine for the lating ones. Mismatched seasons may lead to reduced next year. In order to find out the reasons for match or uptake of influenza vaccination and severe influenza epi- mismatch between vaccines and epidemic strains, we demics, and estimating the prevention that can be tracked the epidemic isolates in the northern hemisphere, achieved during mismatched influenza seasons is of mainly including Asia, North America, and Europe from prime public health importance [7–9]. In this study, December 2016 to February 2018. based on the genetic features of the circulating viruses in Seasonal epidemics associated viruses, including the northern hemisphere in the winter of 2017/2018, we isolates of influenza A(H1N1), A(H3N2), and influenza aimed to discuss if there are some optimized programs B viruses and the corresponding ones in the recommen- for seasonal influenza vaccines. dation compositions of TIVs in the previous 8 years were also analyzed, and the isolation sites were restricted to Methods the Northern Hemisphere. According to their lineage/ Study design and nucleotide sequences collection subtype, as well as the year, HA and NA sequences of In northern hemisphere, human transmission of seasonal the seasonal epidemic isolates in northern hemisphere influenza occurs in winter months but the exact time and were downloaded from GISAID and the influenza data- duration usually varies by country and by year. In the USA, base of NCBI. After clicking Species/Abbrv button in China, and many European countries, winter epidemic can Molecular Evolutionary Genetic Analysis (MEGA) soft- begin as early as October, but it does not reach the peak ware version 6.0, the first 500 sequences of each lineage/ until a rapid increase occurs in December. Typically, the subtype and each year are remained for the purpose of peaks can last until February of the next year, and then the random sampling, and the sequences are all remained winter in northern hemisphere is often determined from when less than 500. December to the next February . Therefore, in this study, we collected HA and NA sequences of the seasonal Phylogenetic analysis isolates from December 1, 2017 to February 28, 2018 in Sequences were aligned using FFT-NS-2 methods of both Global Initiative on Sharing All Influenza Data program MAFFT. Phylogenetic trees were constructed (GISAID, http://platform.gisaid.org/epi3/frontend#3b9e09) using Neighbor-joining method based on the Kimura 2- and the influenza database of National Center for Biotech- parameter model as implemented in MEGA 6.0, with nology Information (NCBI, https://www.ncbi.nlm.nih.gov/ the settings as gamma distributed and complete deletion genomes/FLU/Database/nph-select.cgi?go=database). Infor- for missing data treatment. Robustness of the trees was mation about the vaccine composition was referred to the assessed using bootstrap analysis of 700 replicates. Vaccine Position Papers in website of WHO (http://www. Mean genetic distances between a single/group of vac- who.int/immunization/documents/positionpapers/en/). cine(s) and the groups of epidemic isolates in different Recommendation compositions of the trivalent influenza years or periods in the Northern Hemisphere were calcu- vaccine (TIV) for 2017/2018 winter included an A/Mich- lated by MEGA 6.0 under the set of Kimura 2-parameter igan/45/2015pdm09-like virus (H1N1), an A/Hong Kong/ model, gamma distributed, 700 bootstrap replications, and 4801/2014-like virus (H3N2) and a B/Brisbane/60/2008-like complete deletion for missing data treatment. (from the B/Victoria lineage) virus. Recommendations for influenza vaccine composition Results are updated annually [5, 11]. The Global Influenza Surveil- Match or mismatch between vaccine and epidemic lance and Response System (GISRS) of World Health isolates Organization (WHO) is responsible for rolling the identifi- Phylogenetic trees demonstrated an interesting image cation of circulating influenza viruses. Detection for HA when dealt on the same evolutionary scale; the branches He et al. Antimicrobial Resistance and Infection Control (2019) 8:164 Page 3 of 7 of two trees of influenza B virus were as almost 5 times which was recommended as the composition of flu B width as those of other trees. The epidemic isolates of vaccine for 2015/2016 seasonal epidemic, might be the influenza B virus demonstrated quite a difference from right one for the flu B in 2017/2018 winter (Table 2). the corresponding compositions in the TIV than those Moreover, viruses of B/Wisconsin/1/2010-like for of others (Fig. 1). Data of genetic distances also proved winter of 2012/2013, B/Massachusetts/02/2012-like these results (Tables 1 and 2). Influenza B virus in the for winters of 2013/2014 and 2014/2015, and B/Phu- TIV recommendation mismatched most circulating vi- ket/3073/2013-like for winter of 2015/2016, were all ruses in 2017/2018 winter; the vaccine strain was from of the B/Yamagata lineage. The mean genetic dis- the B/Victoria lineage, while most of epidemic isolates tances between them and the similar lineage seasonal were from the B/Yamagata lineage. isolates established from the recent eight years were Throughout the winter, isolates of influenza A(H1N1) 0.01638 ± 0.00236(HA) and 0.01769 ± 0.00198(NA). were genetically similar to the selected vaccine virus A/ The mean genetic distances between B/Brisbane/60/ Michigan/45/2015pdm09-like, with the mean genetic 2008-like virus, which was recommended for winters distances between them being 0.01516 ± 0.00299(HA) of 2010–2012, 2016/2017 and 2017/2018, and the and 0.00858 ± 0.00224(NA). Mean genetic distances be- similar lineage seasonal isolates established from the tween the seasonal isolates of influenza A(H3N2) and recent eight years were 0.01167 ± 0.00218(HA) and the selected vaccine virus A/Hong Kong/4801/2014-like 0.00958 ± 0.00137(NA) (Table 2). It indicated that iso- were 0.01229 ± 0.00239(HA) and 0.01782 ± 0.00354(NA) lates of influenza B virus were very heterogeneous be- (Table 2). tween B/Yamagata and B/Victoria lineage, but they shared close phylogenetic relationships within the Reasons for mismatch between the recommended flu B same lineage. compositions of vaccine and the epidemic isolates As manifested in Fig. 2, the proportion of B/Victoria Discussion lineage continued to rise from the winter epidemic of Although varying from year-to-year, influenza B gener- 2016/2017 in most continents of northern hemisphere ally causes up to one-third of influenza infections each other than Asia, according to this trend, B/Victoria season. Some studies focused on specific areas have also lineage was strong likely to be the predominate in next shown that it may be the predominant type every four winter. It is understandable that B/Brisbane/60/2008- years approximately [5, 14, 15]. In early outbreak of the like, which is a strain from B/Victoria lineage, would be 2017/2018 winter, seasonal flu in the Northern Hemi- recommended as the influenza B composition in the sphere was caused mainly by influenza B viruses; accord- TIV. Unexpectedly, after April, the proportion of B/ ing to this study and other reports [16–18], epidemic Victoria lineage undergone a significantly continuous de- isolates of them mismatched the recommendation com- cline, whereas isolates from B/Yamagata lineage had positions of vaccine in most northern hemisphere areas. been climbing steadily; the alternation performed dras- It implies that the recommended TIV for 2017/2018 tically in July and August, and then the Yamagata lineage winter possibly could not protect the vaccinated well of flu B became the dominated one in the winter epi- against the epidemic influenza B isolates. This was demic of 2017/2018. exactly the case in both the mainland of China and the Hong Kong Special Administrative Region (SAR), where Seasonal epidemics associated viruses in the previous 8 the recommendation of TIV was applied. Until mid- years in northern hemisphere January of 2018, more than 80% of seasonal infections According to the calculation, as far as influenza reported in both areas were of influenza B [16, 17]. A(H1N1) and A(H3N2) were concerned, the mean gen- Two antigenically distinct influenza B virus lineages etic distances between epidemic isolates and the vaccines had been reported to co-circulate since 2001, from were no higher than 0.02375 ± 0.00341 in both HA and then on, selecting the B strain for inclusion in TIVs NA. With regards to influenza B virus, when forecasting has variable success, and the vaccine strains that did done well, somewhat like to bet rightly, the mean genetic not match the circulating ones have been reported in distances between epidemic isolates and the vaccines seven seasonal epidemics in the Northern Hemisphere were no higher than 0.02368 ± 0.00272, and they might [8, 10, 14, 19]. A quadrivalent influenza vaccine (QIV), protect the vaccinator well against the epidemic isolates. which included both lineages of influenza B virus, Otherwise, when forecasting did not work well, the dis- might be the most suitable for prevention seasonal flu tances between the vaccine strains and the circulating in the Northern Hemisphere, even if there is a less ac- isolates could reach 0.13695 ± 0.00238, as that of the curate prediction about them. As we analyzed, isolates winter epidemic in 2015/2016. Genetic distances also within the same lineage often share very close phylo- demonstrated that the B/Phuket/3073/2013-like virus, genetic relationships. This happens partly because He et al. Antimicrobial Resistance and Infection Control (2019) 8:164 Page 4 of 7 Fig. 1 Phylogenetic trees of HA and NA of the seasonal influenza viruses in 2017/2018 winter on the same evolutionary scale. a- f correspond to N2, H3, NA of influenza B virus, HA of influenza B virus, H1, N1, respectively. Branches labelled by black dots are sequences of recommended compositions in the 8 years (2010/2011–2017/2018) vaccines within a single host species (i.e., human), influenza B need to be very strict in selecting the composition of virus need not to be subjected to multiple immune influenza B virus for recommendations, as long as the pressures from various species of hosts as that under- two lineages are included simultaneously. gone by influenza A virus when the host shift occurs Based on the above analysis, we here approve of the ap- . Partly because there are no reassortment mech- proach that to include both lineages of influenza B strains anism for HA or NA segment of influenza B viruses as in QIVs, as many researchers suggested [19, 23–26]. For ex- that for influenza A viruses so far [7, 21, 22]. Only by ample, B/Brisbane/60/2008(B/Victoria lineage) and B/Phu- accumulating immune pressure from a single species ket/3073/2013(B/Yamagata lineage) might be conceived as of host, acquisition of variation can be extremely lim- two compositions of influenza B vaccines over a consider- ited. This meant, unless the forecasting was failure at able period. The compositions do not need to be altered the lineage level, vaccines for influenza B might cross- annually but once in 3 or 4 years. This may greatly reduce react well with the epidemic isolates. This feature is the time cost for forecasting compositions of flu B vaccines. beneficial to application of QIVs, because it does not Indeed, since 2010, B/Brisbane/60/2008-like virus had been He et al. Antimicrobial Resistance and Infection Control (2019) 8:164 Page 5 of 7 Table 1 Records of epidemic isolate in 8 winters and the compositions of influenza B in northern hemisphere seasonal influenza vaccines, 2010–2018 Year HA NA Vaccine strain Lineage a b c Total VC YM Unk Total VC YM Unk 10/11 794 467 114 213 704 436 102 166 B/Brisbane/60/2008-like VC 11/12 688 197 204 287 567 176 168 223 B/Brisbane/60/2008-like VC 12/13 1208 234 709 265 699 171 458 70 B/Wisconsin/1/2010-like YM 13/14* 584 115 245 224 503 112 219 172 B/Massachusetts/2/2012-like YM 14/15* 1196 109 898 189 849 107 651 91 B/Massachusetts/2/2012-like YM 15/16* 2427 1269 739 419 1948 1098 714 136 B/Phuket/3073/2013-like YM 16/17* 1624 822 652 150 1406 746 599 61 B/Brisbane/60/2008-like VC 17/18* 5575 722 4300 553 4269 623 3483 163 B/Brisbane/60/2008-like VC a b VC, influenza B/Victoria lineage viruses, YM, influenza B/Yamagata viruses, Unk, unknown lineage influenza B viruses * Only the recommended compositions of influenza B in trivalent influenza vaccines (TIVs) for northern hemisphere seasonal flu were listed Data updated on September 10, 2019 recommended for 4 winters of 2010/2011, 2011/2012, influenza B composition of a TIV in advance for the 2016/2017, and 2017/2018, and another virus of B/Massa- next winter. Acquisition of immunity against temporary chusetts/02/2012-like had been recommended twice for circulating influenza B viruses might be responsible for seasonal epidemics of 2013/2014 and 2014/2015 . these uncertainties of match or mismatch [7, 19, 23]. However, QIVs are more expensive than TIVs, and Both TIVs vaccination and natural infection can lead to there must be an increased costs associated with the use an acquisition of immunity. Usually, in a seasonal out- of them [24, 25]. Especially in those underdeveloped break, as time goes on, vaccination population and nat- countries, the costs may be formidable to most of the ural infection population will simultaneously increase, population. In most continents of northern hemisphere, and the immunized population against the circulating vi- an epidemic lineage of influenza B often reaches its peak ruses will increase subsequently. A higher baseline of a little late at the end of the usual winter outbreak . immunized population will inevitably produce a relative This brings many uncertainties for forecasting the larger immune pressure to the temporary viruses; this Table 2 Genetic distances between circulating viruses and vaccines in northern hemisphere, 2010–2018 Vaccines vs Isolates HA NA H3N2 17/18 vs 17/18 (n = 500) 0.01229 ± 0.00239 0.01782 ± 0.00354 10–18 (n = 5) vs 17/18 (n = 500) 0.01940 ± 0.00267 0.01733 ± 0.00226 10–18 (n = 5) vs 13–18 (n = 4000) 0.01677 ± 0.00302 0.01323 ± 0.00212 H1N1 17/18 vs 17/18 (n = 500) 0.01516 ± 0.00299 0.00858 ± 0.00224 10–18 (n = 2) vs 17/18 (n = 500) 0.02375 ± 0.00341 0.01839 ± 0.00309 10–18 (n = 2) vs 10–18 (n = 4000) 0.01434 ± 0.00279 0.01495 ± 0.00326 * # Flu B V17/18 vs Y17/18 (n = 500) 0.11356 ± 0.00261 0.06874 ± 0.00470 V10–18 (n = 1) vs V17/18 (n = 500) 0.01367 ± 0.00272 0.01331 ± 0.00197 V10–18 (n = 1) vs V10–18 (n = 2122, 2022) 0.01167 ± 0.00218 0.00958 ± 0.00137 Y10–18 (n = 3) vs Y17/18 (n = 500) 0.02261 ± 0.00226 0.02024 ± 0.00260 Y10–18 (n = 3) vs Y10–18 (n = 2563, 2489) 0.01638 ± 0.00236 0.01769 ± 0.00198 Y15/16 vs V15/16 (n = 500) 0.13695 ± 0.00238 0.07425 ± 0.00328 Y10–15 (n = 2) vs Y17/18 (n = 500) 0.02368 ± 0.00272 0.02261 ± 0.00315 Y10–15 (n = 2) vs Y10–18 (n = 2563, 2489) 0.02362 ± 0.00218 0.02158 ± 0.00129 Y15/16 vs Y17/18 (n = 500) 0.01224 ± 0.00243 0.00926 ± 0.00218 Y15/16 vs Y10–18 (n = 2563, 2489) 0.00721 ± 0.00144 0.00715 ± 0.00101 * # V, influenza B/Victoria lineage viruses, Y, influenza B/Yamagata viruses It showed the great divergences between the vaccine strains and the seasonal isolates in 2017/2018 and 2015/2016 when the compositions of flu B in the recommended TIVs mismatched the epidemic isolates in the Northern Hemisphere He et al. Antimicrobial Resistance and Infection Control (2019) 8:164 Page 6 of 7 Fig. 2 Proportions of influenza B/Victoria and Yamagata lineages in northern hemisphere from December 2016 to February 2018. VC, influenza B/ Victoria lineage; YM, influenza B/Yamagata lineage. Curves in this figure reflected the rising (YM) and falling (VC) trends from December 2016 to February 2018 in northern hemisphere. In addition, the inflexions of these curves generally occurred between April and May may result in a pathogenic alternative of influenza B Conclusions virus, for reasons of there are only two lineages of them According to this study, we here put forward that when so far [28–30]. applying QIVs for vaccination, the recommendations of According to the compositional fluctuation of the circu- composition for influenza B could be altered and lating influenza B virus annually, we here urge an alterna- assessed once in 3 or 4 years. When economic burden tive approach that GISRS could recommended the was considered intensively and TIVs were utilized, the compositions of the TIVs later in April or May, rather recommended compositions of the vaccines could be an- than in February or March. In this way, the possibility of nounced in April or May, rather than in February or accurately forecasting the predominant viruses for the March as now. next season can be greatly improved, and mismatches could possibly be avoided. Nowadays, technology for vac- Acknowledgements We acknowledge the contributions of scientists and researchers from all over cine producing is becoming more and more reliable [31– the world for depositing the genomic sequences of influenza viruses in NCBI 33]. There should not be technical obstacles in producing Flu database and Global Initiative on Sharing All Influenza Data (GISAID) a large amount of vaccines in a relatively short time (2–3 EpiFlu™. We acknowledge these two databases for permitting us to use these genomic sequences freely and conveniently. months later). Through the technology of virus rescue to introduce the six internal genes from a donor strain with Consent to publication clear genetic background, low-temperature-adaptable in- All authors have approved publishing this short report in Antimicrobial fluenza vaccines can be produced. Not only can it be rap- Resistance & Infection Control, and there are no patients involved in this idly propagated under a relatively low temperature (34 °C) study. and then produced massively in a short term, but also the safety of it can be ensured effectively because of the clearly Authors’ contributions genetic background [11, 34]. For instance, in response of All authors made significant contributions to the conception, data emergencies during the outbreaks of pdm09H1N1 in acquisition, analysis and drafting of this manuscript and approve the final version submitted. C. X. conceived and designed the project. C. X. and G. H. 2009, China had manufactured more than two emergency developed the research question. C. X., P. Y., and Q. Y. collected the vaccines, and it had played a very positive role in rapid sequences and calculated them. All members of the group contributed to suspending of the spread in China . the analysis design and interpretation of the data. He et al. Antimicrobial Resistance and Infection Control (2019) 8:164 Page 7 of 7 Funding 16. Does the flu vaccine work? Mismatch between vaccine and the circulating This research was funded by the National Natural Science Foundation of B/Yamagata lineage influenza virus. http://www.xianjichina.com/news/ China (grant No. 81872673), the National Key Research and Development details_61175.html (in Chinese, accessed Jan 15, 2018). Program of China (grant No. 2017YFC1200203). 17. Science and Technology Daily. 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