DISPATCHESFigure 1. Phylogenetic trees of the hemagglutinin (A) and neuraminidase (B) genes of swine influenza viruses (SIVs). The 8 genomesegment sequences of the A/Pavia/07/2014 strain (black dot, in bold) were submitted to GenBank under accession nos. KJ623706–KJ623713. Scale bars indicate nucleotide substitutions per site.1, polymerase base 2, polymerase, nucleoprotein, matrix,and nonstructural genes showed that the A/Pavia/07/2014strain clustered within the European avian-like SIVs, includingH1N1, H1N2 and H3N2 subtypes (online TechnicalAppendix Figure 1, http://wwwnc.cdc.gov/EID/article/21/7/14-0981-Techapp1.<strong>pdf</strong>).The HA gene of the A/Pavia/07/2014 strain is 567aa long and has antigenic sites identical to those of SIVA(H3N2) strains that circulated in swine in Italy during2013 (Figure 2, http://wwwnc.cdc.gov/EID/article/21/7/14-0981/F2.htm).In addition, the pattern of A/Pavia/07/2014 glycosylation sites in the HA is identical tothat in the A/swine/Italy/282811/2013 HA sequence anddifferent from the human influenza A/Brisbane/10/2007strain (online Technical Appendix Figure 2).In December 2013, respiratory symptoms were observedmainly in piglets and weaning pigs on the farm thatthe patient visited, a farrow-to-finish pig farm where 400sows were reared. The various production phases (mating,gestation, farrowing, nursery, and growing/finishing) werelocated in separated buildings. Forty-two nasal swab sampleswere collected at the end of January 2014 from pigs atall production phases. Considering that clinical signs wereobserved in piglets and weaning pigs, most samples (30samples) were collected from weaning pigs. Influenza Areal-time RT-PCR yielded negative results, probably becausesamples were collected ≈2 months after clinical signsappeared. Serologic investigations were performed on 29serum samples from sows of different ages in mid-May thatwere collected within a national monitoring plan for Aujeszkydisease. Samples were tested by hemagglutination-inhibition test according to standard procedures (12) byusing A/Pavia/07/2014 and the reference SIVs A/swine/CA/3633/84 H3N2, A/swine/Italy/1521/98 H1N2, and A/swine/Finistere/2899/82 as antigens. Two-fold serum dilutionswere tested starting at 1:20. All animals showedantibodies against H3 (137.16 geometric mean vs. A/Pavia/07/2014and 84.2 vs. A/swine/CA/3633/84), whereas15 of 29 serum samples that originated from the oldestanimals also yielded positive results for A(H1N1) SIV. Noantibodies against A(H1N2) SIV were detected.ConclusionsThe swine influenza A(H3N2) viruses present in Europesince 1984 resulted from a genomic reassortment betweenhuman-like swine H3N2 viruses and avian-like swineH1N1 viruses (13). Until 2011, only 3 episodes of SIVH3N2 infection had been reported in the Netherlands andSwitzerland (1,2). Recently, in 2011 the emergence of anew SIV H3N2 variant was reported in the United Statesthat had limited person-to-person transmission (14). Herewe report a case of SIV H3N2 infection in a human hostin January 2014 in Italy. In this patient, the presence of anuncommon influenza strain was suspected after the failureof molecular typing in the presence of high influenza load.The SIV strain identified here correlated with strains circulatingin pigs during the 2013–14 influenza season in Italy.In addition, serologic results on pig serum collected from afarm close to the patient’s home suggested a recent exposurewith an H3N2 strain similar to the A/Pavia/07/2014isolate. These virologic and serologic data suggest that localpigs were the source of human infection.1190 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 7, July 2015
Swine Influenza, ItalyIn agreement with previous observations (1,2), the EuropeanH3N2 swine viruses seem to cause a benign diseasewith mild influenza-like symptoms in humans. In addition,the SIV strain we identified was found only in an immunocompromisedpatient. The uncomplicated clinical coursemight not be uncommon in immunocompromised patients.Indeed, in 2 epidemiologically correlated immunocompromisedpatients, the emergence of human influenza H3N2-resistant strains was associated with opposite clinical outcomes:1 patient had mild upper respiratory syndrome; theother died of severe acute respiratory distress syndrome(15). On the other hand, on the basis of the observationthat none of the patient’s family members and co-workersshowed respiratory infection, we can hypothesize that immuneimpairment of the patient could have favored thezoonotic transmission of the SIV strain. Surveillance ofcirculating SIVs and monitoring of occupationally exposedworkers are 2 important tools to prevent spread of potentialpandemic viruses.Additional members of the Influenza Study Group who contributeddata: Alessia Griello, Marta Premoli, Franscesca Rovida,Bianca Mariani (SS Virologia Molecolare, SC Microbiologia eVirologia, Fondazione IRCCS Policlinico San Matteo, Pavia,Italy); Francesca Manola Adella (Dipartimento di Virologia,Istituto Zooprofilattico Sperimentale della Lombardia ed EmiliaRomagna, Brescia, Italy); Anna Maria Belloni (Azienda SanitariaLocale); Maria Gramegna, Liliana Coppola, AlessandraPiatti, Laura Gemma Brenzoni (DG Sanità, Regione Lombardia,Milan, Italy); Mario Luini (Organizzazione Mondiale per laSalute degli Animali, Laboratorio di riferimento per l’InfluenzaSuina, Istituto Zooprofilattico Sperimentale della Lombardiaed Emilia Romagna, Parma, Italy); Emanuela Foni and LauraBaioni (Istituto Zooprofilattico Sperimentale della Lombardia edEmilia Romagna, Parma, Italy)AcknowledgmentsWe thank the Direzione Generale Sanità, Regione Lombardia;the physicians and veterinarians of the Azienda Sanitaria Localeinvolved in case management; and all the collaborators in thecase definition. We thank Daniela Sartori for manuscript editingand Laurene Kelly for English revision.This study was supported by grants from the Ministero della Salute,Fondazione IRCCS Policlinico San Matteo, Ricerca Corrente(grant no. 80622), Progetto Cariplo 2011-0517, Milan, Italy, andby a grant from the Ministero della Salute, IZSLER PRC2012002.Dr. Piralla is a clinical virologist at the Molecular Virology Unitof the Fondazione IRCCS Policlinico San Matteo in Pavia, Italy.His main research interests include molecular epidemiology of respiratoryviruses, the study of virus evolution and interaction withthe host, and design of next-generation sequencing protocols tostudy virus evolution and new pathogen discovery.References1. Zell R, Scholtissek C, Ludwig S. Genetics, evolution, and the zoonoticcapacity of European swine influenza viruses. Curr Top MicrobiolImmunol. 2013;370:29–55. http://dx.doi.org/10.1007/82_2012_2672. Myers KP, Olsen CW, Gray GC. Cases of swine influenza inhumans: a review of the literature. Clin Infect Dis. 2007;44:1084–8. http://dx.doi.org/10.1086/5128133. Krumbholz A, Lange J, Dürrwald R, Walther M, Muller TH,Kuhnel D, et al. Prevalence of antibodies to European porcineinfluenza viruses in humans living in high pig density areas ofGermany. Med Microbiol Immunol (Berl). 2014;203:13–24.http://dx.doi.org/10.1007/s00430-013-0309-y4. Gerloff NA, Kremer JR, Charpentier E, Sausy A, Olinger CM,Weicherding P, et al. Swine influenza virus antibodies in humans,western Europe, 2009. Emerg Infect Dis. 2011;17:403–11.http://dx.doi.org/10.3201/eid1703.1008515. Piralla A, Baldanti F, Gerna G. Phylogenetic patterns of humanrespiratory picornavirus species, including the newly identifiedgroup C rhinoviruses, during a 1-year surveillance of a hospitalizedpatient population in Italy. J Clin Microbiol. 2011;49:373–6.http://dx.doi.org/10.1128/JCM.01814-106. World Health Organization. CDC protocol of realtime RTPCRfor influenza A(H1N1). 2009 Oct 6 [cited 2009 Dec 15].http://www.who.int/csr/resources/publications/swineflu/CDCRealtimeRTPCR_SwineH1Assay-2009_20090430.<strong>pdf</strong>7. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR. Universal primerset for the full-length amplification of all influenza A viruses. ArchVirol. 2001;146:2275–89. http://dx.doi.org/10.1007/s0070501700028. Lycett SJ, Baillie G, Coulter E, Bhatt S, Kellam P, McCauley JW,et al. Estimating reassortment rates in co-circulating Eurasianswine influenza viruses. J Gen Virol. 2012;93:2326–36.http://dx.doi.org/10.1099/vir.0.044503-09. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W,Gascuel O. New algorithms and methods to estimate maximum-likelihoodphylogenies: assessing the performance of PhyML 3.0. SystBiol. 2010;59:307–21. http://dx.doi.org/10.1093/sysbio/syq01010. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S.MEGA5: molecular evolutionary genetics analysis using maximumlikelihood, evolutionary distance, and maximum parsimonymethods. Mol Biol Evol. 2011;28:2731–9. http://dx.doi.org/10.1093/molbev/msr12111 Tharakaraman K, Raman R, Stebbins NW, Viswanathan K,Sasisekharan V, Sasisekharan R. Antigenically intact hemagglutinin incirculating avian and swine influenza viruses and potential for H3N2pandemic. Sci Rep. 2013;3:1822. http://dx.doi.org/10.1038/srep0182212. World Organisation for Animal Health. Manual of diagnostic testsand vaccines for terrestrial animals. Chapter 2.08.08. Swine influenza[cited 2014 Jun 6]. http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.08.08_SWINE_INFLUENZA.<strong>pdf</strong>13. Castrucci MR, Donatelli I, Sidoli L, Barigazzi G, Kawaoka Y,Webster RG. Genetic reassortant between avian and humaninfluenza a viruses in Italian pigs. Virology. 1993;193:503–6.http://dx.doi.org/10.1006/viro.1993.115514. Epperson S, Jhung M, Richards S, Quinlisk P, Ball L, Moll M,et al. Human infections with influenza A(H3N2) variant virusin the United States, 2011–2012. Clin Infect Dis. 2013;57(Suppl 1):S4–11. http://dx.doi.org/10.1093/cid/cit27215. Piralla A, Gozalo-Margüello M, Fiorina L, Rovida F, Muzzi A,Colombo AA, et al. Different drug-resistant influenza A(H3N2)variants in two immunocompromised patients treated with oseltamivirduring the 2011–2012 influenza season in Italy. J Clin Virol.2013;58:132–7. http://dx.doi.org/10.1016/j.jcv.2013.06.003Address for correspondence: Fausto Baldanti, SS Virologia Molecolare,SC Microbiologia e Virologia, Fondazione IRCCS Policlinico San Matteo,via Taramelli 5, 27100 Pavia, Italy; email: f.baldanti@smatteo.pv.itEmerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 7, July 2015 1191
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