Three subtypes of influenza A viruses, H1N1, H1N2 and H3N2, co-evolve in pigs in Europe. H1N2 viruses isolated from pigs in France and Italy since 1997 were closely related to the H1N2 viruses which emerged in the UK in 1994. In particular, the close relationship of the neuraminidases (NAs) of these viruses to the NA of a previous UK H3N2 swine virus indicated that they had not acquired the NA from H3N2 swine viruses circulating in continental Europe. Moreover, antigenic and genetic heterogeneity among the H1N2 viruses appeared to be due in part to multiple introductions of viruses from the UK. On the other hand, comparisons of internal gene sequences indicated genetic exchange between the H1N2 viruses and co-circulating H1N1 and/or H3N2 subtypes. Most genes of the earlier (1997–1998) H1N2 isolates were more closely related to those of a contemporary French H1N1 isolate, whereas the genes of later (1999–2000) isolates, including the HAs of some H1N2 viruses, were closely related to those of a distinct H1N1 antigenic variant which emerged in France in 1999. In contrast, an H3N2 virus isolated in France in 1999 was closely related antigenically and genetically to contemporary human A/Sydney/5/97-like viruses. These studies reveal interesting parallels between genetic and antigenic drift of H1N1 viruses in pig and human populations, and provide further examples of the contribution of genetic reassortment to the antigenic and genetic diversity of swine influenza viruses and the importance of the complement of internal genes in the evolution of epizootic strains.
BelsheR. B.,
Hall SmithM.,
HallC. B.,
BettsR.,
HayA. J.1988; Genetic basis of resistance to rimantadine emerging during treatment of influenza virus infection. Journal of Virology 62:1508–1512
BrownI. H.,
ChakravertyP.,
HarrisP. A.,
AlexanderD. J.1995; Disease outbreaks in pigs in Great Britain due to an influenza A virus of H1N2 subtype. Veterinary Record 136:328–329
BrownI. H.,
HarrisP. A.,
McCauleyJ. W.,
AlexanderD. J.1998; Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. Journal of General Virology 79:2947–2955
CampitelliL.,
DonatelliI.,
FoniE.,
CastrucciM. R.,
FabianiC.,
KawaokaY.,
KraussS.,
WebsterR. G.1997; Continued evolution of H1N1 and H3N2 influenza viruses in pigs in Italy. Virology 232:310–318
CastrucciM. R.,
DonatelliI.,
SidoliL.,
BarigazziG.,
KawaokaY.,
WebsterR. G.1993; Genetic reassortant between avian and human influenza A viruses in Italian pigs. Virology 193:503–506
ClaasE. C. J.,
KawokaY.,
De JongJ. C.,
MasurelN.,
WebsterR. G.1994; Infection of children with avian-human reassortant influenza virus from pigs in Europe. Virology 204:453–457
FerrariM.,
LosioM. N.,
GualandiG. L.,
Di LerniaR.,
ManocchioI.1989; General characteristics and viral susceptibility of a newborn pig kidney (NPK) continuous culture. Microbiologica 12:329–334
GoldfieldM.,
BartleyJ. D.,
PizuttiW.,
BlackH. C.,
AltmanR.,
HalperinW. E.1977; Influenza in New Jersey in 1976: isolations of influenza A/New Jersey/76 virus at Fort Dix. Journal of Infectious Diseases 136:347–355
GourreauJ. M.,
KaiserC.,
ValetteM.,
DouglasA. R.,
LabieJ.,
AymardM.1994; Isolation of two H1N2 influenza viruses from swine in France. Archives of Virology 135:365–382
GregoryV.,
LimW.,
CameronK.,
BennettM.,
MarozinS.,
KlimovA.,
HallH.,
CoxN.,
HayA.,
LinY. P.2001; Infection of a child in Hong Kong by an influenza A H3N2 virus closely related to viruses circulating in European pigs. Journal of General Virology 82:1397–1406
HayA. J.,
GregoryV.,
DouglasA. R.,
LinY. P.2001; Evolution of human influenza viruses. Philosophical Transactions of the Royal Society of London B Biological Sciences 356:1861–1870
ItoT.,
KawaokaY.,
VinesA.,
IshikawaH.,
AsaiT.,
KidaH.1998; Continued circulation of reassortant H1N2 influenza viruses in pigs in Japan. Archives of Virology 143:1773–1782
KarasinA. I.,
OlsenC. W.,
AndersonG. A.2000a; Genetic characterization of an H1N2 influenza virus isolated from a pig in Indiana. Journal of Clinical Microbiology 38:2453–2456
KarasinA. I.,
SchuttenM. M.,
CooperL. A.,
SmithC. B.,
SubbaraoK.,
AndersonG. A.,
CarmanS.,
OlsenC. W.2000b; Genetic characterization of H3N2 influenza viruses isolated from pigs in North America, 1977–1999: evidence for wholly human and reassortant virus genotypes. Virus Research 68:71–85
KendalA. P.,
PereiraM. S.,
SkehelJ. J.1982Concepts and Procedures for Laboratory-based Influenza Surveillance Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention;
LinY. P.,
ShawM.,
GregoryV.,
CameronK.,
LimW.,
KlimovA.,
SubbaraoK.,
GuanY.,
KraussS.,
ShortridgeK.,
WebsterR.,
CoxN.,
HayA.2000; Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proceedings of the National Academy of Sciences, USA 97:9654–9658
MarozinS.,
GregoryV.,
CameronK.,
BennettM.,
ValetteM.,
AymardM.,
FoniE.,
BarigazziG.,
LinY.,
HayA.2001; Antigenic and genetic diversity among swine influenza viruses in Europe. In Options for the Control of Influenza IV Edited by
OsterhausA.,
CoxN.,
HampsonA.
Amsterdam: Elsevier Science; (in press)
NardelliL.,
PascucciS.,
GualandiG. L.,
LodaP.1978; Outbreaks of classical swine influenza in Italy in 1976. Zentralblatt für Veterinaermedizin Beiheft/Reihe B 25:853–857
NeromeK.,
YoshiokaY.,
SakamotoS.,
YasuharaM.,
OyaA.1985; Characterization of a 1980-swine recombinant influenza virus possessing H1 haemagglutinin and N2 neuraminidase similar to that of the earliest Hong Kong (H3N2) virus. Archives of Virology 86:197–211
OttisK.,
SidoliL.,
BachmannP. A.,
WebsterR. G.,
KaplanM. M.1982; Human influenza A viruses in pigs: isolation of a H3N2 strain antigenically related to A/England/42/72 and evidence for continuous circulation of human viruses in the pig population. Archives of Virology 73:103–108
OuchiA.,
NeromeK.,
KanegaeY.,
IshidaM.,
NeromeR.,
HayashiK.,
HashimotoT.,
KajiM.,
KajiY.,
InabaY.1996; Large outbreak of swine influenza in southern Japan caused by reassortant (H1N2) influenza viruses: its epizootic background and characterization of the causative viruses. Journal of General Virology 77:1751–1759
PensaertM.,
OttisK.,
VandeputteJ.,
KaplanM. M.,
BachmannP. A.1981; Evidence for the natural transmission of influenza A virus from wild ducks to swine and its potential importance for man. Bulletin of the World Health Organization 59:75–78
SugimuraT.,
YonemochiH.,
OgawaT.,
TanakaK.,
KumagaiT.1980; Isolation of a recombinant influenza virus (Hsw1N2) from swine in Japan. Archives of Virology 66:271–274
TumovaB.,
VeznikovaD.,
MensikJ.,
StumpaA.1980; Surveillance of influenza in pig herds in Czechoslovakia in 1974–1979. I. Introduction of influenza epidemic A (H3N2) viruses in pig herds. Zentralblatt für Veterinaermedizin Beiheft/Reihe B 27:517–523
WebbyR. J.,
SwensonS. L.,
KraussS. L.,
GerrishP. J.,
GoyalS. M.,
WebsterR. G.2000; Evolution of swine H3N2 influenza viruses in the United States. Journal of Virology 74:8243–8251
WellsD. L.,
HopfenspergerD. J.,
ArdenN. H.1991; Swine influenza virus infections: transmission from ill pigs to humans at a Wisconsin Agricultural Fair and subsequent probable person-person transmission. Journal of the American Medical Association 265:478–481
ZhouN. N.,
SenneD. A.,
LandgrafJ. S.,
SwensonS. L.,
EricksonG.,
RossowK.,
LiuL.,
YoonK.-Y.,
KraussS.,
WebsterR. G.1999; Genetic reassortment of avian, swine and human influenza A viruses in American pigs. Journal of Virology 73:8851–8856