Abstract
The human influenza pandemics of 1957 and 1968 were caused by reassortant viruses that possessed internal gene segments from avian and human strains. Whether genetic reassortment of human and avian influenza viruses occurs during interpandemic periods and how often humans are infected with such reassortants is not known. To provide this information, we used dot-blot hybridization, partial nucleotide sequencing and subsequent phylogenetic analysis to examine the 6 internal genes of 122 viruses isolated in humans between 1933 and 1992 primarily from Asia, Europe, and the Americas. The internal genes of A/New Jersey/11/76 isolated from a human fatality at Fort Dix, New Jersey in 1976 were found to be of porcine origin. Although none of the geographically and temporally diverse collection of 122 viruses was an avian-human or other reassortant, cognizance was made of the fact that there were two isolates from children from amongst 546 influenza A isolates obtained from The Netherlands from 1989–1994 which were influenza reassortants containing genes of avian origin, viruses which have infected European pigs since 1983–1985. Thus, genetic reassortment between avian and human influenza strains does occur in the emergence of pandemic and interpandemic influenza A viruses. However, in the interpandemic periods the reassortants have no survival advantage, and the circulating interpandemic influenza viruses in humans do not appear to accumulate avian influenza virus genes.
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Baum LG, Paulson JC. Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem (Jena) 1990; 89 (suppl): 35–38.
Bean WJ, Jr, Cox NJ, Kendal AP. Recombination of human influenza A viruses in nature. Nature 1980; 284:638–640.
Castrucci MR, Donatelli I, Sidoli L, Barigazzi G, Kawaoka Y, Webster RG. Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology 1993; 193: 503–506.
Centers for Disease Control. Influenza — Missouri. -MMWR 1976; 25: 376.
Centers for Disease Control. Influenza — Wisconsin.-MMWR 1976; 25: 392.
Centers for Disease Control. Influenza — Wisconsin.-MMWR 1976; 25: 402.
Claas ECJ, Kawaoka Y, de Jong JC, Masurel N, Webster RG. Infection of children with avian-human reassortant influenza A virus from pigs in Europe. Virology 1994; 204: 453–457.
Dacso CC, Couch RB, Six HR, Young JF, Quarles JM, Kasel JA. Sporadic occurrence of zoonotic swine influenza virus infections. J Clin Microbiol 1984; 20: 833–835.
Desselberger U, Nakajima K, Alfino P, Pedersen FS, Haseltine WA, Hannoun C, Palese P. Biochemical evidence that ‘new’ influenza virus strains in nature may arise by recombination (reassortment). Proc Natl Acad Sci USA 1978; 75: 3341–3345.
Dowdle WR, Hattwick MAW. Swine influenza virus infections in humans. J Infect Dis 1977; 136 (suppl): S386–389.
Gaydos JC, Hodder RA, Top FH, Jr, Allen RG, Soden VJ, Nowosiwsky T, Russell PK. Swine influenza A at Fort Dix, New Jersey (January–February 1976). II. Transmission and morbidity in units with cases. J Infect Dis 1977; 136 (suppl): S363–368.
Gaydos JC, Hodder RA, Top FH, Jr, Soden VJ, Allen RG, Bartley JD, Zabkar JH, Nowosiwsky T, Russell PK. Swine influenza A at Fort Dix, New Jersey (January–February 1976). I. Case finding and clinical study of cases. J Infect Dis 1977; 136 (suppl): S356–362.
Gorman OT, Bean WJ, Kawaoka Y, Donatelli I, Guo YJ, Webster RG. Evolution of influenza A virus nucleoprotein genes: implications for the origins of H1N1 human and classical swine viruses. J Virol 1991; 65: 3704–3714.
Gorman OT, Bean WJ, Kawaoka Y, Webster RG. Evolution of the nucleoprotein gene of influenza A virus. J Virol 1990; 64: 1487–1497.
Gorman OT, Donis RO, Kawaoka Y, Webster RG. Evolution of influenza A virus PB2 genes: implications for evolution of the ribonucleoprotein complex and Origin of human influenza A virus. J Virol 1990; 64:4893–4902.
Guo YJ, Xu XY, Cox NJ. Human influenza A (HIN2) viruses isolated from China. J Gen Virol 1992; 73 (pt 2): 383–387.
Hinshaw VS, Alexander DJ, Aymard M, Bachmann PA, Easterday BC, Hannoun C, Kida H, Lipkind M, MacKenzie JS, Nerome K, et al. Antigenic comparisons of swine-influenza-like H1N1 isolates from pigs, birds and humans: an international collaborative study. Bull World Health Organ 1984; 62: 871–878.
Hinshaw VS, Bean WJ Webster RG, Sriram G. Genetic reassortment of influenza A viruses in the intestinal tract of ducks. Virology 1980; 102: 412–419.
Hinshaw VS, Bean WJ, Jr, Webster RG, Easterday BC. The prevalence of influenza viruses in swine and the antigenic and genetic relatedness of influenza viruses from man and swine. Virology 1978; 84: 51–62.
Hinshaw VS, Webster RG, Bean WJ, Downie J, Senne DA. Swine influenza-like viruses in turkeys: potential source of virus for humans? Science 1983; 220: 206–208.
Hodder RA, Gaydos JC, Allen RG, Top FH, Jr, Nowosiwsky T, Russell PK. Swine influenza A at Fort Dix, New Jersey (January–February 1976). III. Extent of spread and duration of the outbreak. J Infect Dis 1977; 136 (suppl): S369–375.
Kawaoka Y, Krauss S, Webster RG. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 1989; 63: 4603–4608.
Kida H, Ito T, Yasuda J, Shimizu Y, Itakura C, Shortridge KF, Kawaoka Y, Webster RG. Potential for transmission of avian influenza viruses to pigs. J Gen Virol 1994; 75: 2183–2188.
Kundin WD. Hong Kong A-2 influenza virus infection among swine during a human epidemic in Taiwan. Nature 1970; 228: 857.
Li XS, Zhao CY, Gao HM, Zhang YQ, Ishida M, Kanegae Y, Endo A, Nerome R, Omoe K, Nerome K. Origin and evolutionary characteristics of antigenic reassortant influenza A (HIN2) viruses isolated from man in China. J Gen Virol 1992; 73 (pt 6): 1329–1337.
McKinney WP, Volkert P, Kaufman J. Fatal swine influenza pneumonia during late pregnancy. Arch Intern Med 1990; 150: 213–215.
Nakajima K, Desselberger U, Palese P. Recent human influenza A (H1N1) viruses are closely related genetically to strains isolated in 1950. Nature 1978; 274: 334–339.
Nakajima K, Nakajima S, Shortridge KF, Kendal AP. Further genetic evidence for maintenance of early Hong Kong-like influenza A (H3N2) strains in swine until 1976. Virology 1982; 116: 562–572.
Nerome K, Ishida M, Nakayama M, Oya A, Kanai C, Suwicha K. Antigenic and genetic analysis of A/Hong Kong (H3N2) influenza viruses isolated from swine and man. J Gen Virol 1981; 56: 441–445.
O'Brien RJ, Noble GR, Easterday BC, et al. Swine-like influenza virus infection in a Wisconsin farm family. J Infect Dis 1977; 136: S390–395.
Patriarca PA, Kendal AP, Zakowski PC, Cox NJ, Trautman MS, Cherry JD, Auerbach DM, McCusker J, Belliveau RR, Kappus KD. Lack of significant person-to-person spread of swine influenza-like virus following fatal infection in an immunocompromised child. Am J Epidemiol 1984; 119: 152–158.
Rota PA, Rocha EP, Harmon MW, Hinshaw VS, Sheerar MG, Kawaoka Y, Cox NJ, Smith TF. Laboratory characterization of a swine influenza virus isolated from a fatal case of human influenza. J Clin Microbiol 1989; 27: 1413–1416.
Scholtissek C, Burger H, Bachmann PA, Hannoun C. Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology 1983; 129: 521–523.
Scholtissek C, Burger H, Kistner O, Shortridge KF. The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 1985; 147: 287–294.
Scholtissek C, Rohde W, Von Hoyningen V, Rott R. On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 1978; 87: 13–20.
Shortridge KF, Stuart-Harris CH. An influenza epicentre? Lancet 1982; 2: 812–813.
Shu LL, Lin YP, Shortridge KF, Webster RG. Evidence for interspecies transmission and reassortment of influenza A viruses in pigs in Southern China. Virology 1994; 202: 825–833.
Smith JW. Swine influenza in Hodgkin's disease. N Engl J Med 1976; 295: 732.
Smith TF, Burgert EO, Dowdle WR, Noble GR, Campbell RJ, Van Scoy RE. Isolation of swine influenza virus from autopsy lung tissue of man. N Engl J Med 1976; 294: 708–710.
Sugimura T, Yonemochi H, Ogawa T, Tanaka Y, Kumagai T. Isolation of a recombinant influenza virus (Hsw 1 N2) from swine in Japan. Arch Virol 1980; 66: 271–274.
Thompson RL, Sande MA, Wenzel RP, Hoke CH, Gwaltney JM. Swine influenza infection in civilians: report of two cases. N Engl J Med 1976; 295: 714–715.
Top FH, Jr, Russell PK. Swine influenza A at Fort Dix, New Jersey (January–February 1967). IV. Summary and speculation. J Infect Dis 1977; 136 (suppl): S376–380.
Webster RG, Laver WG. Antigenic variation of influenza viruses. In: Kilbourne ED (ed), The influenza viruses and influenza. New York: Academic Press, 1975: 269–314.
Wells DL, Hopfensperger DJ, Arden NH, Harmon MW, Davis JP, Tipple MA, Schonberger LB. Swine influenza virus infections. JAMA 1991; pp265: pp478–481.
Wentworth DE, Thompson BL, Xu X, Regnery HL, Cooley AJ, McGregor MW, Cox NJ, Hinshaw VS. An influenza A (H1N1) virus, closely related to swine influenza virus, responsible for a fatal case of human influenza. J Virol 1994; 68: 2051–2058.
Wright SM, Kawaoka Y, Sharp GB, Senne DA, Webster RG. Interspecies transmission and reassortment of influenza A viruses in pigs and turkeys in the United States. Am J Epidemiol 1992; 136: 488–497.
Xu X, Rocha EP, Regenery HL, Kendal AP, Cox NJ. Genetic and antigenic analyses of influenza A (H1N1) viruses, 1986–1991. Virus Res 1993; 28: 37–55.
Young JF, Palese P. Evolution of human influenza A viruses in nature: recombination contributes to genetic variation of H1N1 strains. Proc Natl Acad Sci USA 1979; 76: 6547–6551.
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Shu, L.P., Sharp, G.B., Lin, Y.P. et al. Genetic reassortment in pandemic and interpandemic influenza viruses. Eur J Epidemiol 12, 63–70 (1996). https://doi.org/10.1007/BF00144430
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DOI: https://doi.org/10.1007/BF00144430