Food as a passible source af H5N1 influenza virus infection in mammals


M. PENSAERT
C. S. KYRIAKIS
K. van REETH
Résumé

The recent infections of humans and other mammals with die highly padiogenic H5N1 avian influenza virus have raised questions about the safety of the consumption of poultry products. The aim of this review is to collect and present information regarding the risk of infection in humans with H5N1 virus via the oral route. The presence of virus in edible poultry products and the chances for viral entry via the gastrointestinal (GI) tract, from a pathogenetic point of view, are the main focus points. The transmission of H5N1 from poultry to humans is a rare event which has been associated with very close contact with infected animals. It is generally accepted that the most likely candidate routes for the virus entry are the oropharygeal and/or respiratory tract tissues where virus replication may occur and leading to clinical symptoms. However, the low number of human cases, compared to the high number of humans that have been exposed to H5N1 virus infected animals, shows clearly that a readily accessible portal of entry does not exist. The possibility of virus entry through the GI tract has been proposed, but, so far, no proof that the virus can replicate in the human intestines has been shown. The presence of diarrhoea in several patients and the detection of viral RNA in the intestines and rectal swabs of 3 patients do not allow one to safely conclude that the GI tract can serve as a portal of entry or a target organ. Furthermore, the occurrence of disease has not clearly or definitely been associated with the consumption of poultry meat in any human case. Feline species, on the other hand, have been naturally and experimentally infected after the consumption of infected poultry. However, also in these mammals, it was not established that the intestine is the initial portal of entry of the virus. In conclusion, the possibility that the intestinal tract serves as a portal of entry in mammals remains unlikely, since there is no convincing evidence that the GI tract tissues can support virus replication. It can, however, not be excluded that food containing virus may be a source of infection when passing oropharyngeal tissues, which have been identified as target sites for virus replication.

Article Details
  • Rubrique
  • Short Communication
Téléchargements
Les données relatives au téléchargement ne sont pas encore disponibles.
Références
Andries K, Pensaert MB(1980) Immunofluorescence studies on the pathogenesis of hemagglutinating encephalomyelitis virus infection in pigs after oronasal inoculation. Am J Vet Res.41:1372-8.
Apisarnthanarak A, Kitphati R, Thongphubeth K, Patoomanunt P, Anthanont P, Auwanit W, Thawatsupha P, Chittaganpitch M, Saeng-Aroon S, Waicharoen S, Apisarnthanarak P, Storch GA,
Mundy LM, Fraser VJ(2004) Atypical avian influenza (H5N1). Emerg Infect Pis., 10: 1321-4.
Baum LG, Paulson JC (1990) Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl., 40: 35-8.
Beard CW, Brugh M, Johnson DC(1984) Laboratory studies with the Pennsylvania avian influenza viruses (H5N2). Proceedings of the 88th Annual Conference of the United States Animal Health Association. 1984; Fort Worth, TZ, USA:462-473.
Beigel JH, Farrar J, Han AM, Hayden FG, Hyer R, de Jong MD, Lochindarat S, Nguyen TK, Nguyen TH, Tran ΤΗ, Nicoli A, Touch S, Yuen KY(2005) Writing Committee of the World Health Organization (WHO) Consultation on Human Influenza A/H5. Avian influenza A (H5N1) infection in humans. Ν Engl J Med., 353: 1374-85.
Cappucci DT Jr, Johnson DC, Brugh M, Smith TM, Jackson CF, Pearson JE, Senne DA(1985) Isolation of avian influenza virus (subtype H5N2) from chicken eggs during a natural outbreak.
Avian Pis., 29: 1195-200.
Choi YK, Nguyen TD, Ozaki H, Webby RJ, Puthavathana P, Buranathal C, Chaisingh A, Auewarakul P, Hanh NT, Ma SK, Hui PY, Guan Y, Peiris JS, Webster RG(2005) Studies of H5N1
Influenza Virus Infection of Pigs by Using Viruses Isolated in Vietnam and Thailand in 2004. Journal of Virolog, 10821-10825.
Connor RJ, Kawaoka Y, Webster RG, Paulson JC. (1994) Receptor specificity in human, avian and equine H2 and H3 influenza virus isolates. Virology., 1994 Nov 15; 205: 17-23.
de Jong MD, Bach VC, Phan TQ, Vo MH, Tran TT, Nguyen BH, Beld M, Le TP, Truong HK, Nguyen VV, Tran ΤΗ, Do QH, Farrar J (2005) Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. Ν Engl J Med., 352:686-91.
de Jong MD, Hien TT (2006) Avian influenza A (H5N1). Journal of Clinical Virology, 35: 2-13.
Dybing JK, Schultz-Cherry S, Swayne DE, Suarez DL, Perdue ML(2000) Distinct pathogenesis of Hong Kong-origin H5N1 viruses in mice compared to that of other highly pathogenic H5 avian influenza viruses. J Virol., 74: 1443-50.
Ellis TM, Bousfield RB, Bissett LA, Dyrting KC, Luk GS, Tsim ST, Sturm-Ramirez K, Webster RG, Guan Y, Malik Peiris JS (2004) Investigation of outbreaks of highly pathogenic H5N1 avian
influenza in waterfowl and wild birds in Hong Kong in late 2002. Avian Pathology, 33: 492-505.
Fiszon B, Hannoun C, Garcia-Sastre A, Villar E, Cabezas JA (1989) Comparison of biological and physical properties of human and animal A(H1N1) influenza viruses. Res Virol., 140: 395-404.
Gao P, Watanabe S, Ito Τ, Goto Η, Wells Κ, McGregor M, Cooley AJ, Kawaoka Y(1999) Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J Virol., 73: 3184-9.
Gesser RM, Koo SC. (1996) Oral inoculation with herpes simplex virus type 1 infects enteric neuron and mucosal nerve fibers within the gastrointestinal tract in mice. J Virol. 1996 Jun;70(6):
-102.
Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E(2005) Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol., 79: 2191-8.
Hayden F, Croisier A(2005) Transmission of avian influenza viruses to and between humans. J Infect Dis., 192: 1311-4.
Hinshaw VS, Webster RG, Easterday BC, Bean WJ Jr(1981) Replication of avian influenza A viruses in mammals. Infect Immun., 34: 354-61.
Horby P. Update on Epidemiological Aspects of H5N1(2005) Proceedings of the 18th European Meeting and its Prevention, La Baule, France Ito Τ, Couceiro JN, Keim S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y(1998) Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol., 72: 7367-73.
Kawaoka Y, Bordwell E, Webster RG (1987) Intestinal replication of influenza A viruses in two mammalian species. Brief report. Arch Virol., 93: 303-8.
Keawcharoen J, Oraveerakul K, Kuiken T, Fouchier RA, Amonsin A, Payungporn S, Noppornpanth S, Wattanodorn S, Theambooniers A, Tantilertcharoen R, Pattanarangsan R, Arya
N, Ratanakorn P, Osterhaus DM, Poovorawan Y (2004) Avian influenza H5N1 in tigers and leopards. Emerg Infect Dis., 10:2189-91.
Kishida N, Sakoda Y, Isoda N, Matsuda K, Eto M, Sunaga Y, Umemura T, Kida H(2005) Pathogenicity of H5 influenza viruses for ducks. Arch Virol., 150: 1383-92.
Koopmans M, Wilbrink B, Conyn M, Natrop G., Van der Nat H, Vennema H, Meijer A, Van Steenbergen J, Fouchier R, Osterhaus A. Bosman A(2004) Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. The Lancet, 363:5870-593.
Kuiken T, Rimmelzwaan G, van Riel D, van Amerongen G, Baars M, Fouchier R, Osterhaus A. (2004) Avian H5N1 influenza in cats. Science, 306: 241.
Laudert E, Halvorson D, Sivanandan V, Shaw D(1993) Comparative evaluation of tissue trophism characteristics in turkeys and mallard ducks after intravenous inoculation of type A influenza
viruses. Avian Dis. ,37:773-80.
Lee JS, Hanson RP (1975) Effects of bile and gastrointestinal secretions on the infectivity of Newcastle disease virus. Infect Immun., 11: 692-7.
Lipatov AS, Krauss S, Guan Y, Peiris M, Rehg JE, Perez DR, Webster RG. (2003) Neurovirulence in mice of H5N1 influenza virus genotypes isolated from Hong Kong poultry in 2001. J Virol., 77: 3816-23.
Liu J, Xiao H, Lei F, Zhu Q, Qin K, Zhang XW, Zhang XL, Zhao D, Wang G, Feng Y, Ma J, Liu W, Wang J, Gao GF(2005) Highly pathogenic H5N1 influenza virus infection in migratory birds. Science., 309:1206.
Loeffen W, de Boer E, Koch G. (2004) Transmission of a highly pathogenic avian influenza virus to swine in the Netherlands. Proceedings of the in-between congress of the International Society for Animal Hygiene. ,St. Malo, France: 329-30
Lu H, Dunn PA, Wallner-Pendleton EA, Henzler DJ, Kradel DC, Liu J, Shaw DP, Miller Ρ (2004) Investigation of H7N2 avian influenza outbreaks in two broiler breeder flocks in Pennsylvania,
-02. Avian Pis., 48: 26-33.
Lu H, Castro AE, Pennick K, Liu J, Yang Q, Dunn P, Weinstock D, Henzler D (2003) Survival of avian influenza virus H7N2 in SPF chickens and their environments. Avian Dis., 47: 1015-21.
Lu X, Tumpey TM, Morken Τ, Zaki SR, Cox NJ, Katz JM(1999). A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J Virol.,73:5903-11.
Maines TR, Lu XH, Erb SM, Edwards L, Guarner J, Greer PW, Nguyen DC, Szretter KJ, Chen LM, Thawatsupha P, Chittaganpitch M, Waicharoen S, Nguyen DT, Nguyen Τ, Nguyen HH, Kim JH, Hoang LT, Kang C, Phuong LS, Lim W, Zaki S, Donis RO, Cox NJ, Katz JM, Tumpey TM (2005) Avian influenza (H5N1) viruses isolated from humans in Asia in 2004 exhibit increased virulence in mammals. J Virol., 79: 11788-800.
Mase M, Imada T, Nakamura K, Tanimura N, Imai K, Tsukamoto K, Yamaguchi S (2005) Experimental assessment of the pathogenicity of H5N1 influenza A viruses isolated in Japan.
Avian Pis., 49: 582-4.
Matrosovich M, Zhou N, Kawaoka Y, Webster R (1999) The surface glycoproteins of H5 influenza viruses isolated from humans, chickens and wild aquatic birds have distinguishable properties. J Virol., 73: 1146-55.
Matrosovich MN, Matrosovich TY, Gray T, Roberts NA, Klenk HD. (2004) Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci USA., 101:4620-4.
Mettenleiter TC. (2003) Pathogenesis of neurotropic herpesviruses: role of viral glycoproteins in neuroinvasion and transneuronal spread. Virus Res.,92: 197-206.
Moses HE, Brandley CA, Jones EE. (1948) The isolation and identification of fowl plague virus. American Journal of Veterinary Research, 9: 314-328.
Muramoto Y, Ozaki H, Takada A, Park CH, Sunden Y, Umemura Τ, Kawaoka Y, Matsuda H, Kida H. (2006) Highly Pathogenic H5N1 Influenza Virus Causes Coagulopathy in Chickens.
Microbiol Immunol., 50: 73-81.
Narayan O, Lang G, Rouse BT (1969) A new influenza A virus infection in turkeys. IV. Experimental susceptibility of domestic birds to virus strain turkey-Ontario 7732-1966. Arch Gesamte Virusforsch., 26: 149-65.
Nishimura H, Itamura S, Iwasaki T, Kurata T, Tashiro M (2000) Characterization of human influenza A (H5N1) virus infection in mice: neuro-, pneumo- and adipotropic infection. J Gen Virol., 81: 2503-10.
Perkins LE, Swayne DE (2001) Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Vet Pathol., 38: 149-64.
Perkins LE, Swayne DE (2002) Pathogenicity of a Hong Kong-origin H5N1 highly pathogenic avian influenza virus for emus, geese, ducks and pigeons. Avian Dis., 46: 53-63.
Rimmelzwaan GF, Kuiken T, van Amerongen G, Bestebroer TM, Fouchier RA, Osterhaus AD (2002) Pathogenesis of influenza A (H5N1) virus infection in a primate model. J Virol., 75: 6687-91.
Rimmelzwaan GF, van Riel D, Baars M, Bestebroer TM, van Amerongen G, Fouchier RA, Osterhaus AD, Kuiken Τ (2006) Influenza A Virus (H5N1) Infection in Cats Causes Systemic
Disease with Potential Novel Routes of Virus Spread within and between Hosts. Am J Pathol., 168: 176-83.
Scholtissek C (1985) Stability of infectious influenza A viruses at low pH and at elevated temperature. Vaccine., 3: 215-8.
Sims LD, Domenech J, Benigno C, Kahn S, Kamata A, Lubroth J, Martin V, Roeder Ρ (2005) Origin and evolution of highly pathogenic H5N1 avian influenza in Asia. Vet Ree, 157:159-64.
Starick E, Werner Ο (2003) Detection of H7 avian influenza virus directly from poultry specimens. Avian Dis., 47: 1187-9.
Stieneke-Grober A, Vey M, Angliker H, Shaw E, Thomas G, Roberts C, Klenk HD, Garten W (1992) Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J., 11: 2407-14.
Suzuki Y (2005) Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull., 28:399-408.
Swayne DE, Beck JR (2004) Heat inactivation of avian influenza and Newcastle disease viruses in egg products. Avian Pathol., 33:512-8.
Swayne DE, Beck JR(2005) Experimental study to determine if lowpathogenicity and high-pathogenicity avian influenza viruses can be present in chicken breast and thigh meat following intranasal virus inoculation. Avian Dis., 49: 81-5.
Tanaka H, Park CH, Ninomiya A, Ozaki H, Takada A, Umemura T, Kida H(2003) Neurotropism of the 1997 Hong Kong H5N1 influenza virus in mice. Vet Microbiol., 95: 1-13.
Thanawongnuwech R, Amonsin A, Tantilertcharoen R, Damrongwatanapokin S, Theamboonlers A, Payungporn S, Nanthapornphiphat K, Ratanamungklanon S, Tunak E, Songserm T, Vivatthanavanich V, Lekdumrongsak T, Kesdangsakonwut S, Tunhikorn S, Poovorawan Y (2005) Probable tiger-to-tiger transmission of avian influenza H5N1. Emerg Infect Dis., 11:699-701
The World Health Organization (WHO); http://www.who.int Tian G, Zhang S, Li Y, Bu Z, Liu P, Zhou J, Li C, Shi J, Yu K, Chen H (2005) Protective efficacy in chickens, geese and ducks of an
H5Nl-inactivated vaccine developed by reverse genetics. Virology., 341: 153-62.
Tran ΤΗ, Nguyen TL, Nguyen TD, Luong TS, Pham PM, Nguyen VC, Pham TS, Vo CD, Le TQ, Ngo TT, Dao BK, Le PP, Nguyen TT, Hoang TL, Cao VT, Le TG, Nguyen DT, Le ΗΝ, Nguyen
KT, Le HS, Le VT, Christiane D, Tran TT, Menno de J, Schultsz C, Cheng Ρ, Lim W, Horby P, Farrar J; World Health Organization International Avian Influenza Investigative Team. Avian influenza A (H5N1) in 10 patients in Vietnam. Ν Engl J Med. 2004; 350: 1179-88.
Tumpey TM, Suarez DL, Perkins LE, Senne DA, Lee JG, Lee YJ, Mo IP, Sung HW, Swayne DE(2002) Characterization of a highly pathogenic H5N1 avian influenza A virus isolated from duck meat. J Virol., 76: 6344-55.
Tumpey TM, Suarez DL, Perkins LE, Senne DA, Lee J, Lee YJ, Mo IP, Sung HW, Swayne DE(2003) Evaluation of a highpathogenicity H5N1 avian influenza A virus isolated from duck
meat. Avian Pis., 47: 951-5.
Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, Nicholls JM, Chokephaibulkit K, Vanprapar N, Auewarakul P(2005) Influenza A H5N1 replication sites in
humans. Emerg Infect Dis., 11: 1036-41.
Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG (1978). Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology., 84: 268-78.
Webster RG, Guan Y, Peiris M, Walker D, Krauss S, Zhou NN, Govorkova EA, Ellis TM, Dyrting KC, Sit T, Perez DR, Shortridge KF. (2002) Characterization of H5N1 influenza viruses that continue to circulate in geese in southeastern China. J Virol., 76: 118-26.
White MR, Crouch E, van Eijk M, Hartshorn M, Pemberton L, Tornoe I, Holmskov U, Hartshorn KL(2005) Cooperative antiinfluenza activities of respiratory innate immune proteins and neuraminidase inhibitor. Am J Physiol Lung Cell Mol Physiol., 288: L831-40.
Zambon MC(2001) The pathogenesis of influenza in humans. Rev Med Virol., 11:227-41.
Ziegler AF, Davison S, Acland H, Eckroade RJ(1999) Characteristics of H7N2 (non-pathogenic) avian influenza virus infections in commercial layers, in Pennsylvania, 1997-98. Avian Dis., 43:142-9.
Zitzow LA, Rowe T, Morken T, Shieh WJ, Zaki S, Katz JM(2002) Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J Virol., 76: 4420-9.
Articles les plus lus par le même auteur ou la même autrice