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Reappearance of Influenza B/Victoria/2/87-Lineage Viruses

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Reappearance of Influenza B/Victoria/2/87-Lineage Viruses Epidemiol. Infect. (2005), 133, 263–271. f 2004 Cambridge University Press DOI: 10.1017/S0950268804003462 Printed in the United Kingdom Reappearance of influenza B/Victoria/2/87-lineage viruses: epidemic activity, genetic diversity and vaccination efficacy in the Finnish Defence Forces N. IKONEN 1,R.PYHA¨LA¨1*, T. AXELIN 2, M. KLEEMOLA1 AND H. KORPELA2 1 National Public Health Institute, Helsinki, Finland 2 Research Institute of Military Medicine, Central Military Hospital, Helsinki, Finland (Accepted 2 November 2004) SUMMARY A new B/Shangdong/7/97-like influenza virus (Victoria/2/87 lineage) predominated during the 2002/2003 epidemic season in Finland and was estimated to account for 2246 of the 13 496 feverish upper respiratory tract infections (URIs) occurring among conscripts in the Finnish army. The incidence (1716/10 000 conscripts) was indicative of moderate epidemic activity at most. Analysis of the cross-reactive antibodies induced in 1988 suggests that the basis of the protection was probably established during the childhood of the conscripts. Vaccination in autumn 2002 prevented 42% of the URIs during the influenza B outbreak and 71% (95% CI 42–85) of infections interpreted as influenza B. Despite the low genetic variability of the Shangdong/7/97- like viruses, breakages of a potential glycosylation site in haemagglutinin (HA1, position 197) were frequent; their biological significance is discussed. The Shangdong/7/97-like strains were HA1/NA reassortants, as were also the less abundant strains that for HA1 belonged to the B/Yamagata/16/88 lineage. A further reassortment, which probably emerged during the outbreak in one of the garrisons, supports our hypothesis that circumstances in these settings may especially favour the emergence of diversity by reassortment. INTRODUCTION 1987/1988 [7]. After low-intensity local outbreaks due to these viruses in 1989/1990 [8], the first outbreak of During the epidemic season of 2001/2002, two influ- Yamagata-lineage virus occurred in Finland in 1990/ enza B virus variants that had evolved from a common 1991 [9]. The global re-emergence of the Victoria- ancestor in the 1970s [1, 2] circulated in Europe [3–6]. lineage viruses from East Asia in 2001/2002 resulted The B/Sichuan/379/99-like viruses belonged to the B/ in a change in the recommended composition of Yamagata/16/88 lineage and were closely related to influenza virus vaccines for use in autumn 2002, when the viruses of the previous epidemic seasons. The a B/Hong Kong/330/2001-like virus (B/Shangdong/7/ B/Hong Kong/330/2001-like viruses belonged to the 97) was substituted for the B/Sichuan/379/99-like B/Victoria/2/87 lineage. This lineage had disappeared vaccine virus [10]. In spring 2002, the B/Hong Kong/ from Europe in the early 1990s and was then replaced 330/2001-like viruses predominated in many parts by the Yamagata lineage. The last intense outbreak of of the world [3] but were not isolated in Finland [11] Victoria-lineage virus in Finland occurred during (Ikonen et al., unpublished data). The re-expansion of the Victoria-lineage viruses was * Author for correspondence: Dr R. Pyha¨la¨, National Influenza epidemiologically an interesting new situation. One Centre, National Public Health Institute, Mannerheimintie 166, FIN-00300 Helsinki, Finland. could expect that the B/Hong Kong/330/2001-like (Email: reijo.pyhala@ktl.fi) viruses would be capable of infecting children with no Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 28 Sep 2021 at 13:12:06, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268804003462 264 R. Pyha¨la¨and others antigenic experience of the Victoria-lineage viruses, 59 of the 522 URI patients (11.3%) noted during the but the ability of the virus to infect older age groups continuous 15-week observation period (weeks 2–16, was less axiomatic. Our study focuses on conscripts 2003). With these measures a total of 299 NPAs were in the Finnish Defence Forces who had been between collected during the 6-month study period in 2002/ 5 and 7 years of age during the last intense outbreak 2003 from 13 garrisons and one military hospital (re- of Victoria-lineage viruses during 1987/1988. We in- ferred to as military units hereafter). Acute and con- vestigated to what extent Victoria- and Yamagata- valescent sera were collected from 213 patients and the lineage viruses were responsible for upper respiratory total number of patients who donated either NPAs or tract infections (URIs) in the Finnish Defence Forces paired sera or both was 302. The case definition was during 2002/2003 as well as the genetic diversity the same as that applied for monitoring of URIs. We of these viruses in garrisons scattered throughout recommended that the NPAs be taken within 3 days of Finland. The efficacy of the updated influenza virus the onset of illness, as had been carried out in Finland vaccine against influenza B, estimated with the patients during previous epidemic seasons [12]. In practice, sampled and laboratory tests, and the effectiveness of 73% of the NPAs were collected within 3 days and the vaccine in reducing URIs was investigated in one 92% within 5 days. of the garrisons. Most of the NPAs (90%) were inoculated within 48 h, and the rest after a storage period of at most 1 week at x60 xC onto Madin–Darby canine kidney MATERIALS AND METHODS (MDCK) cell cultures for isolation of influenza viru- ses. With a few exceptions, all the cultures that did not Study population and clinical surveillance show haemagglutinating activity within 3–5 days after The monthly mean number of men who served in the inoculation had a second passage in MDCK cells; Finnish Defence Forces in garrisons scattered otherwise the cultivation procedure was as described throughout Finland varied from 17 445 to 20 113 previously [13]. Typing of the influenza isolates was conscripts during the study period from November performed with a haemagglutination inhibition (HI) 2002 to April 2003. The conscripts, whose enlistments assay as described previously [14] and supplemented were from 9 or 12 months, had entered the service at a afterwards [13] using rat antisera produced against mean age of 19.5 years. A minority had entered in B/Hong Kong/330/01 (Victoria lineage), B/Fin/141/ January 2002, most in July 2002 or in January 2003, 2002 (Yamagata lineage), A/New Caledonia/20/ when the study was in progress. Vaccinations against 99(H1N1) and A/Panama/2007/99(H3N2). A time- influenza were administered in autumn 2002 in two resolved fluoroimmunoassay was applied [15] when garrisons, where a total of 428 conscripts received the the NPAs were examined for the presence of several vaccine. The occurrence of URI among the conscripts microbial antigens: influenza A and B, respiratory was monitored in all garrisons. Case definition was syncytial virus, the adenovirus group and parainflu- feverishness and one or more of the following symp- enza virus types 1, 2 and 3. The paired sera were studied toms: cough, sore throat and/or myalgia. The first with a standard complement fixation technique [16] patient contact with a physician during each episode for the presence of antibodies to the same viruses as was recorded and the monthly case numbers were re- above. Of the agents examined serologically and in ported to the Research Institute of Military Medicine, antigen detection, the results for influenza B (and A) following established practice [12]. viruses are shown. The roles played by the other agents studied are of less concern here and, with the exception of the situation in the Pori Brigade where Virological surveillance the vaccination campaign was executed, will be dis- We recommended that health-care personnel of the cussed elsewhere (Kleemola et al., unpublished ob- garrisons collected nasopharyngeal aspirates (NPAs) servations). from 5 to 10 URI patients during the rising phase of every URI outbreak and some additional specimens Sequencing and phylogenetic analysis at a later phase. In addition, scattered samples were taken from sporadic cases. More extensive NPAs Of the 94 influenza B viral strains isolated from the were collected as part of vaccine investigations in the conscripts in 2002/2003, 28 strains together with three Pori Brigade, where these specimens were taken from strains isolated from civilian patients in late 2002, Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 28 Sep 2021 at 13:12:06, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268804003462 Influenza B/Victoria/2/87 lineage 265 when the garrison outbreaks had not yet begun, were 4000 120 analysed with nucleotide sequencing of the HA1 do- 3500 100 main of the viral haemagglutinin (accession numbers: 3000 AY744303 to AY744329 for Victoria lineage and 80 2500 AY744334 to AY744337 for Yamagata lineage). Of 2000 60 the 28 strains, 13 were analysed for partial nucleotide URI cases 1500 sequencies of viral neuraminidase (NA; accession 40 numbers AY744290 to AY744302). RNA extraction, 1000 20 cDNA synthesis, amplification procedures with poly- 500 NPAs (influenza B numbers) merase chain reaction and sequencing were performed 0 0 Nov. Dec. Jan. Feb. Mar. Apr. in our laboratory as previously described [13]. Prior 2002 2003 to RNA extraction and sequencing, the viruses were Fig. 1. Monthly numbers of upper respiratory tract infec- propagated through 2–4 passages in MDCK cell cul- tions (URI, ––––) among conscripts in the Finnish Defence tures. The sequences of the primers used for amplifi- Forces during the observation period from November 2002 cation and sequencing of NA and HA1 are available to April 2003 and monthly numbers of sampled patients on request.
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