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Published in: Virology Journal 1/2011

Open Access 01-12-2011 | Research

Distribution of sialic acid receptors and influenza A virus of avian and swine origin in experimentally infected pigs

Authors: Ramona Trebbien, Lars E Larsen, Birgitte M Viuff

Published in: Virology Journal | Issue 1/2011

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Abstract

Background

Pigs are considered susceptible to influenza A virus infections from different host origins because earlier studies have shown that they have receptors for both avian (sialic acid-alpha-2,3-terminal saccharides (SA-alpha-2,3)) and swine/human (SA-alpha-2,6) influenza viruses in the upper respiratory tract. Furthermore, experimental and natural infections in pigs have been reported with influenza A virus from avian and human sources.

Methods

This study investigated the receptor distribution in the entire respiratory tract of pigs using specific lectins Maackia Amurensis (MAA) I, and II, and Sambucus Nigra (SNA). Furthermore, the predilection sites of swine influenza virus (SIV) subtypes H1N1 and H1N2 as well as avian influenza virus (AIV) subtype H4N6 were investigated in the respiratory tract of experimentally infected pigs using immunohistochemical methods.

Results

SIV antigen was widely distributed in bronchi, but was also present in epithelial cells of the nose, trachea, bronchioles, and alveolar type I and II epithelial cells in severely affected animals. AIV was found in the lower respiratory tract, especially in alveolar type II epithelial cells and occasionally in bronchiolar epithelial cells. SA-alpha-2,6 was the predominant receptor in all areas of the respiratory tract with an average of 80-100% lining at the epithelial cells. On the contrary, the SA-alpha-2,3 was not present (0%) at epithelial cells of nose, trachea, and most bronchi, but was found in small amounts in bronchioles, and in alveoli reaching an average of 20-40% at the epithelial cells. Interestingly, the receptor expression of both SA-alpha-2,3 and 2,6 was markedly diminished in influenza infected areas compared to non-infected areas.

Conclusions

A difference in predilection sites between SIV and AIV virus was found, and this difference was in accordance with the distribution of the SA-alpha-2,6 and SA-alpha-2,3 receptor, respectively. The results indicated that the distribution of influenza A virus receptors in pigs are similar to that of humans and therefore challenge the theory that the pig acts as a mixing vessel between human and avian influenza viruses. Furthermore, it was shown that AIV prefers to infect alveolar type II epithelial cells in pigs. This corresponds with findings in humans emphasising the resemblance between the two species.
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Literature
1.
go back to reference Alexander DJ: A review of avian influenza in different bird species. Vet microbiol 2000, 74: 3-13. 10.1016/S0378-1135(00)00160-7CrossRefPubMed Alexander DJ: A review of avian influenza in different bird species. Vet microbiol 2000, 74: 3-13. 10.1016/S0378-1135(00)00160-7CrossRefPubMed
2.
go back to reference Ito T, Kawaoka Y: Host-range barrier of influenza A viruses. Vet microbiol 2000, 74: 71-75. 10.1016/S0378-1135(00)00167-XCrossRefPubMed Ito T, Kawaoka Y: Host-range barrier of influenza A viruses. Vet microbiol 2000, 74: 71-75. 10.1016/S0378-1135(00)00167-XCrossRefPubMed
3.
go back to reference Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev 1992, 56: 152-179.PubMedCentralPubMed Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y: Evolution and ecology of influenza A viruses. Microbiol Rev 1992, 56: 152-179.PubMedCentralPubMed
4.
go back to reference Kuntz-Simon G, Madec F: Genetic and Antigenic Evolution of Swine Influenza Viruses in Europe and Evaluation of Their Zoonotic Potential. Zoonoses Public Health 2009, 56: 310-325. 10.1111/j.1863-2378.2009.01236.xCrossRefPubMed Kuntz-Simon G, Madec F: Genetic and Antigenic Evolution of Swine Influenza Viruses in Europe and Evaluation of Their Zoonotic Potential. Zoonoses Public Health 2009, 56: 310-325. 10.1111/j.1863-2378.2009.01236.xCrossRefPubMed
5.
go back to reference Brown IH: The epidemiology and evolution of influenza viruses in pigs. Vet microbiol 2000, 74: 29-46. 10.1016/S0378-1135(00)00164-4CrossRefPubMed Brown IH: The epidemiology and evolution of influenza viruses in pigs. Vet microbiol 2000, 74: 29-46. 10.1016/S0378-1135(00)00164-4CrossRefPubMed
6.
go back to reference Brown IH, Harris PA, McCauley JW, Alexander DJ: 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 1998, 79: 2947-2955.CrossRefPubMed Brown IH, Harris PA, McCauley JW, Alexander DJ: 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 1998, 79: 2947-2955.CrossRefPubMed
7.
go back to reference Hjulsager CK, Bragstad K, Bøtner A, Nielsen EO, Vigre H, Enøe C, et al.: New swine influenza A H1N2 reassortment found in Danish swine. In proceedings of International Pig Veterinary Society congress. Volume 1. Copenhagen; 2006:16-19. O.55-03 265-265. 2006 Hjulsager CK, Bragstad K, Bøtner A, Nielsen EO, Vigre H, Enøe C, et al.: New swine influenza A H1N2 reassortment found in Danish swine. In proceedings of International Pig Veterinary Society congress. Volume 1. Copenhagen; 2006:16-19. O.55-03 265-265. 2006
8.
go back to reference Ito T, Couceiro JNSS, Kelm S, Baum LG, Krauss S, Castrucci MR, et al.: Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. Journal of Virology 1998, 72: 7367-7373.PubMedCentralPubMed Ito T, Couceiro JNSS, Kelm S, Baum LG, Krauss S, Castrucci MR, et al.: Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. Journal of Virology 1998, 72: 7367-7373.PubMedCentralPubMed
9.
go back to reference Suzuki Y, Ito T, Suzuki T, Holland RE, Chambers TM, Kiso M, et al.: Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 2000, 74: 11825-11831. 10.1128/JVI.74.24.11825-11831.2000PubMedCentralCrossRefPubMed Suzuki Y, Ito T, Suzuki T, Holland RE, Chambers TM, Kiso M, et al.: Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 2000, 74: 11825-11831. 10.1128/JVI.74.24.11825-11831.2000PubMedCentralCrossRefPubMed
10.
go back to reference Shortridge KF, Gao P, Guan Y, Ito T, Kawaoka Y, Markwell D, et al.: Interspecies transmission of influenza viruses: H5N1 virus and a Hong Kong SAR perspective. Vet microbiol 2000, 74: 141-147. 10.1016/S0378-1135(00)00174-7CrossRefPubMed Shortridge KF, Gao P, Guan Y, Ito T, Kawaoka Y, Markwell D, et al.: Interspecies transmission of influenza viruses: H5N1 virus and a Hong Kong SAR perspective. Vet microbiol 2000, 74: 141-147. 10.1016/S0378-1135(00)00174-7CrossRefPubMed
11.
go back to reference Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, et al.: Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. The Lancet 2004, 363: 587-593. 10.1016/S0140-6736(04)15589-XCrossRef Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, et al.: Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. The Lancet 2004, 363: 587-593. 10.1016/S0140-6736(04)15589-XCrossRef
12.
go back to reference Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, et al.: Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 1998, 279: 393-396. 10.1126/science.279.5349.393CrossRefPubMed Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, et al.: Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 1998, 279: 393-396. 10.1126/science.279.5349.393CrossRefPubMed
13.
go back to reference Rogers GN, D'Souza BL: Receptor binding properties of human and animal H1 influenza virus isolates. Virology 1989, 173: 317-322. 10.1016/0042-6822(89)90249-3CrossRefPubMed Rogers GN, D'Souza BL: Receptor binding properties of human and animal H1 influenza virus isolates. Virology 1989, 173: 317-322. 10.1016/0042-6822(89)90249-3CrossRefPubMed
14.
go back to reference Gambaryan AS, Karasin AI, Tuzikov AB, Chinarev AA, Pazynina GV, Bovin NV, et al.: Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus Research 2005, 114: 15-22. 10.1016/j.virusres.2005.05.005CrossRefPubMed Gambaryan AS, Karasin AI, Tuzikov AB, Chinarev AA, Pazynina GV, Bovin NV, et al.: Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus Research 2005, 114: 15-22. 10.1016/j.virusres.2005.05.005CrossRefPubMed
15.
go back to reference Rogers GN, Paulson JC: Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127: 361-373. 10.1016/0042-6822(83)90150-2CrossRefPubMed Rogers GN, Paulson JC: Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 1983, 127: 361-373. 10.1016/0042-6822(83)90150-2CrossRefPubMed
16.
go back to reference Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, et al.: Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 2006, 355: 1143-1155. 10.1016/j.jmb.2005.11.002CrossRefPubMed Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, et al.: Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 2006, 355: 1143-1155. 10.1016/j.jmb.2005.11.002CrossRefPubMed
17.
go back to reference Van Poucke S, Nicholls J, Nauwynck H, Van Reeth K: Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. Virology Journal 2010, 7: 38. 10.1186/1743-422X-7-38PubMedCentralCrossRefPubMed Van Poucke S, Nicholls J, Nauwynck H, Van Reeth K: Replication of avian, human and swine influenza viruses in porcine respiratory explants and association with sialic acid distribution. Virology Journal 2010, 7: 38. 10.1186/1743-422X-7-38PubMedCentralCrossRefPubMed
18.
go back to reference Nelli R, Kuchipudi S, White G, Perez B, Dunham S, Chang KC: Comparative distribution of human and avian type sialic acid influenza receptors in the pig. BMC Veterinary Research 2010, 6: 4. 10.1186/1746-6148-6-4PubMedCentralCrossRefPubMed Nelli R, Kuchipudi S, White G, Perez B, Dunham S, Chang KC: Comparative distribution of human and avian type sialic acid influenza receptors in the pig. BMC Veterinary Research 2010, 6: 4. 10.1186/1746-6148-6-4PubMedCentralCrossRefPubMed
19.
go back to reference Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, Sakai-Tagawa Y, et al.: Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 2006, 444: 378-382. 10.1038/nature05264CrossRefPubMed Yamada S, Suzuki Y, Suzuki T, Le MQ, Nidom CA, Sakai-Tagawa Y, et al.: Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature 2006, 444: 378-382. 10.1038/nature05264CrossRefPubMed
20.
go back to reference Bateman AC, Busch MG, Karasin AI, Bovin N, Olsen CW: Amino Acid 226 in the Hemagglutinin of H4N6 Influenza Virus Determines Binding Affinity for {alpha}2,6-Linked Sialic Acid and Infectivity Levels in Primary Swine and Human Respiratory Epithelial Cells. J Virol 2008, 82: 8204-8209. 10.1128/JVI.00718-08PubMedCentralCrossRefPubMed Bateman AC, Busch MG, Karasin AI, Bovin N, Olsen CW: Amino Acid 226 in the Hemagglutinin of H4N6 Influenza Virus Determines Binding Affinity for {alpha}2,6-Linked Sialic Acid and Infectivity Levels in Primary Swine and Human Respiratory Epithelial Cells. J Virol 2008, 82: 8204-8209. 10.1128/JVI.00718-08PubMedCentralCrossRefPubMed
21.
go back to reference Connor RJ, Kawaoka Y, Webster RG, Paulson JC: Receptor Specificity in Human, Avian and Equine H2 and H3 Influenza Virus Isolates. Virology 1994, 205: 17-23. 10.1006/viro.1994.1615CrossRefPubMed Connor RJ, Kawaoka Y, Webster RG, Paulson JC: Receptor Specificity in Human, Avian and Equine H2 and H3 Influenza Virus Isolates. Virology 1994, 205: 17-23. 10.1006/viro.1994.1615CrossRefPubMed
22.
go back to reference Nicholls JM, Peiris JSM, Guan Y: Sialic acid and receptor expression on the respiratory tract in normal subjects and H5N1 and non-avian influenza patients. Hong Kong Med J 2009, 15: 16-20.PubMed Nicholls JM, Peiris JSM, Guan Y: Sialic acid and receptor expression on the respiratory tract in normal subjects and H5N1 and non-avian influenza patients. Hong Kong Med J 2009, 15: 16-20.PubMed
23.
go back to reference Nicholls JM, Bourne J, Chen H, Guan Y, Peiris JSM: Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respir Res 2007.,8(73): Nicholls JM, Bourne J, Chen H, Guan Y, Peiris JSM: Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses. Respir Res 2007.,8(73):
24.
go back to reference Nicholls JM, Chan RWY, Russell RJ, Air GM, Peiris JSM: Evolving complexities of influenza virus and its receptors. Trends in Microbiology 2008, 16: 149-157. 10.1016/j.tim.2008.01.008CrossRefPubMed Nicholls JM, Chan RWY, Russell RJ, Air GM, Peiris JSM: Evolving complexities of influenza virus and its receptors. Trends in Microbiology 2008, 16: 149-157. 10.1016/j.tim.2008.01.008CrossRefPubMed
25.
go back to reference Ladekjær-Mikkelsen A-S, Nielsen J, Stadejek T, Storgaard T, Krakowka S, Ellis J, et al.: Reproduction of postweaning multisystemic wasting syndrome (PMWS) in immunostimulated and non-immunostimulated 3-week-old piglets experimentally infected with porcine circovirus type 2 (PCV2). Veterinary Microbiology 2002, 89: 97-114. 10.1016/S0378-1135(02)00174-8CrossRefPubMed Ladekjær-Mikkelsen A-S, Nielsen J, Stadejek T, Storgaard T, Krakowka S, Ellis J, et al.: Reproduction of postweaning multisystemic wasting syndrome (PMWS) in immunostimulated and non-immunostimulated 3-week-old piglets experimentally infected with porcine circovirus type 2 (PCV2). Veterinary Microbiology 2002, 89: 97-114. 10.1016/S0378-1135(02)00174-8CrossRefPubMed
26.
go back to reference Kuchipudi SV, Nelli R, White GA, Bain M, Chang KC, Dunham S: Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission. Journal of Molecular and Genetic Medicine 2009, 3: 143-151.PubMedCentralCrossRefPubMed Kuchipudi SV, Nelli R, White GA, Bain M, Chang KC, Dunham S: Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission. Journal of Molecular and Genetic Medicine 2009, 3: 143-151.PubMedCentralCrossRefPubMed
27.
go back to reference Altman DG: Practical statistics for medical research. 1st edition. Chapman & Hall/CRC; 1999. Altman DG: Practical statistics for medical research. 1st edition. Chapman & Hall/CRC; 1999.
28.
go back to reference Viuff B, Tjornehoj K, Larsen LE, Rontved CM, Uttenthal A, Ronsholt L, et al.: Replication and clearance of respiratory syncytial virus: apoptosis is an important pathway of virus clearance after experimental infection with bovine respiratory syncytial virus. Am J Pathol 2002, 161: 2195-2207. 10.1016/S0002-9440(10)64496-3PubMedCentralCrossRefPubMed Viuff B, Tjornehoj K, Larsen LE, Rontved CM, Uttenthal A, Ronsholt L, et al.: Replication and clearance of respiratory syncytial virus: apoptosis is an important pathway of virus clearance after experimental infection with bovine respiratory syncytial virus. Am J Pathol 2002, 161: 2195-2207. 10.1016/S0002-9440(10)64496-3PubMedCentralCrossRefPubMed
29.
go back to reference Auewarakul P, Suptawiwat O, Kongchanagul A, Sangma C, Suzuki Y, Ungchusak K, et al.: An Avian Influenza H5N1 Virus That Binds to a Human-Type Receptor. J Virol 2007, 81: 9950-9955. 10.1128/JVI.00468-07PubMedCentralCrossRefPubMed Auewarakul P, Suptawiwat O, Kongchanagul A, Sangma C, Suzuki Y, Ungchusak K, et al.: An Avian Influenza H5N1 Virus That Binds to a Human-Type Receptor. J Virol 2007, 81: 9950-9955. 10.1128/JVI.00468-07PubMedCentralCrossRefPubMed
30.
go back to reference Ito T, Suzuki Y, Suzuki T, Takada A, Horimoto T, Wells K, et al.: Recognition of N-glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J Virol 2000, 74: 9300-9305. 10.1128/JVI.74.19.9300-9305.2000PubMedCentralCrossRefPubMed Ito T, Suzuki Y, Suzuki T, Takada A, Horimoto T, Wells K, et al.: Recognition of N-glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J Virol 2000, 74: 9300-9305. 10.1128/JVI.74.19.9300-9305.2000PubMedCentralCrossRefPubMed
31.
go back to reference Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y: Influenza virus receptors in the human airway. Nature 2006, 440: 435-436. 10.1038/440435aCrossRefPubMed Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y: Influenza virus receptors in the human airway. Nature 2006, 440: 435-436. 10.1038/440435aCrossRefPubMed
32.
go back to reference Guo CT, Takahashi N, Yagi H, Kato K, Takahashi T, Yi SQ, et al.: The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 2007, 17: 713-724. 10.1093/glycob/cwm038CrossRefPubMed Guo CT, Takahashi N, Yagi H, Kato K, Takahashi T, Yi SQ, et al.: The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. Glycobiology 2007, 17: 713-724. 10.1093/glycob/cwm038CrossRefPubMed
33.
go back to reference Yao L, Korteweg C, Hsueh W, Gu J: Avian influenza receptor expression in H5N1-infected and noninfected human tissues. FASEB 2008, 22: 733-740.CrossRef Yao L, Korteweg C, Hsueh W, Gu J: Avian influenza receptor expression in H5N1-infected and noninfected human tissues. FASEB 2008, 22: 733-740.CrossRef
34.
go back to reference Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, et al.: Influenza A H5N1 Replication Sites in Humans. Emerg Infect Dis 2005, 11: 1036-1041.PubMedCentralCrossRefPubMed Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, et al.: Influenza A H5N1 Replication Sites in Humans. Emerg Infect Dis 2005, 11: 1036-1041.PubMedCentralCrossRefPubMed
35.
go back to reference Gu J, Xie Z, Gao Z, Liu J, Korteweg C, Ye J, et al.: H5N1 infection of the respiratory tract and beyond: a molecular pathology study. The Lancet 2007, 370: 1137-1145. 10.1016/S0140-6736(07)61515-3CrossRef Gu J, Xie Z, Gao Z, Liu J, Korteweg C, Ye J, et al.: H5N1 infection of the respiratory tract and beyond: a molecular pathology study. The Lancet 2007, 370: 1137-1145. 10.1016/S0140-6736(07)61515-3CrossRef
36.
go back to reference Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, et al.: Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. Journal of Virology 2000, 74: 8502-8512. 10.1128/JVI.74.18.8502-8512.2000PubMedCentralCrossRefPubMed Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, et al.: Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. Journal of Virology 2000, 74: 8502-8512. 10.1128/JVI.74.18.8502-8512.2000PubMedCentralCrossRefPubMed
37.
go back to reference Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, et al.: Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 1997, 233: 224-234. 10.1006/viro.1997.8580CrossRefPubMed Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, et al.: Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 1997, 233: 224-234. 10.1006/viro.1997.8580CrossRefPubMed
38.
go back to reference Mounts A-W, Kwong H, Izurieta H-S, Ho Y, Au T, Lee M, et al.: Case-Control Study of Risk Factors for Avian Influenza A (H5N1) Disease, Hong Kong, 1997. The Journal of Infectious Diseases 1999, 180: 505-508. 10.1086/314903CrossRefPubMed Mounts A-W, Kwong H, Izurieta H-S, Ho Y, Au T, Lee M, et al.: Case-Control Study of Risk Factors for Avian Influenza A (H5N1) Disease, Hong Kong, 1997. The Journal of Infectious Diseases 1999, 180: 505-508. 10.1086/314903CrossRefPubMed
39.
go back to reference Dinh PN, Long HT, Tien NTK, Hien NT, Mai LTQ, Phong LH, et al.: Risk factors for human infection with avian influenza A H5N1, Vietnam, 2004. Emerg Infect Dis 2006, 12: 1841-1847.PubMedCentralCrossRefPubMed Dinh PN, Long HT, Tien NTK, Hien NT, Mai LTQ, Phong LH, et al.: Risk factors for human infection with avian influenza A H5N1, Vietnam, 2004. Emerg Infect Dis 2006, 12: 1841-1847.PubMedCentralCrossRefPubMed
40.
go back to reference Haines DM, Waters EH, Clark EG: Immunohistochemical detection of swine influenza A virus in formalin-fixed and paraffin-embedded tissues. Can J Vet Res 1993, 57: 33-36.PubMedCentralPubMed Haines DM, Waters EH, Clark EG: Immunohistochemical detection of swine influenza A virus in formalin-fixed and paraffin-embedded tissues. Can J Vet Res 1993, 57: 33-36.PubMedCentralPubMed
41.
go back to reference Jung K, Ha Y, Chae C: Pathogenesis of swine influenza virus subtype H1N2 infection in pigs. J comp Pathol 2005, 132: 179-184. 10.1016/j.jcpa.2004.09.008CrossRefPubMed Jung K, Ha Y, Chae C: Pathogenesis of swine influenza virus subtype H1N2 infection in pigs. J comp Pathol 2005, 132: 179-184. 10.1016/j.jcpa.2004.09.008CrossRefPubMed
42.
go back to reference Jung T, Choi C, Chae C: Localization of swine influenza virus in naturally infected pigs. Vet Pathol 2002, 39: 10-16. 10.1354/vp.39-1-10CrossRefPubMed Jung T, Choi C, Chae C: Localization of swine influenza virus in naturally infected pigs. Vet Pathol 2002, 39: 10-16. 10.1354/vp.39-1-10CrossRefPubMed
43.
go back to reference Vincent LL, Janke BH, Paul PS, Halbur PG: A monoclonal-antibody-based immunohistochemical method for the detection of swine influenza virus in formalin-fixed, paraffin-embedded tissues. J Vet Diagn Invest 1997, 9: 191-195. 10.1177/104063879700900214CrossRefPubMed Vincent LL, Janke BH, Paul PS, Halbur PG: A monoclonal-antibody-based immunohistochemical method for the detection of swine influenza virus in formalin-fixed, paraffin-embedded tissues. J Vet Diagn Invest 1997, 9: 191-195. 10.1177/104063879700900214CrossRefPubMed
44.
go back to reference Larochelle R, Sauvageau R, Magar R: Immunohistochemical detection of swine influenza virus and porcine reproductive and respiratory syndrome virus in porcine proliferative and necrotizing pneumonia cases from Quebec. Can Vet J 1994, 35: 513-515.PubMedCentralPubMed Larochelle R, Sauvageau R, Magar R: Immunohistochemical detection of swine influenza virus and porcine reproductive and respiratory syndrome virus in porcine proliferative and necrotizing pneumonia cases from Quebec. Can Vet J 1994, 35: 513-515.PubMedCentralPubMed
45.
go back to reference De Vleeschauwer A, Atanasova K, Van Borm S, van den Berg T, Rasmussen TB, Uttenthal Å, et al.: Comparative Pathogenesis of an Avian H5N2 and a Swine H1N1 Influenza Virus in Pigs. PLoS ONE 2009, 4: e6662. 10.1371/journal.pone.0006662PubMedCentralCrossRefPubMed De Vleeschauwer A, Atanasova K, Van Borm S, van den Berg T, Rasmussen TB, Uttenthal Å, et al.: Comparative Pathogenesis of an Avian H5N2 and a Swine H1N1 Influenza Virus in Pigs. PLoS ONE 2009, 4: e6662. 10.1371/journal.pone.0006662PubMedCentralCrossRefPubMed
46.
go back to reference Isoda N, Sakoda Y, Kishida N, Bai GR, Matsuda K, Umemura T, et al.: Pathogenicity of a highly pathogenic avian influenza virus, A/chicken/Yamaguchi/7/04 (H5N1) in different species of birds and mammals. Archives of Virology 2006, 151: 1267-1279. 10.1007/s00705-005-0723-6CrossRefPubMed Isoda N, Sakoda Y, Kishida N, Bai GR, Matsuda K, Umemura T, et al.: Pathogenicity of a highly pathogenic avian influenza virus, A/chicken/Yamaguchi/7/04 (H5N1) in different species of birds and mammals. Archives of Virology 2006, 151: 1267-1279. 10.1007/s00705-005-0723-6CrossRefPubMed
47.
go back to reference Piwpankaew YOTT, Monteerarat YUWA, Suptawiwat ORNP, Puthavathana PILA, Uipresertkul MONG, Auewarakul PRAS: Distribution of viral RNA, sialic acid receptor, and pathology in H5N1 avian influenza patients. APMIS 2010, 118: 895-902. 10.1111/j.1600-0463.2010.02676.xCrossRefPubMed Piwpankaew YOTT, Monteerarat YUWA, Suptawiwat ORNP, Puthavathana PILA, Uipresertkul MONG, Auewarakul PRAS: Distribution of viral RNA, sialic acid receptor, and pathology in H5N1 avian influenza patients. APMIS 2010, 118: 895-902. 10.1111/j.1600-0463.2010.02676.xCrossRefPubMed
Metadata
Title
Distribution of sialic acid receptors and influenza A virus of avian and swine origin in experimentally infected pigs
Authors
Ramona Trebbien
Lars E Larsen
Birgitte M Viuff
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2011
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-8-434

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WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

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Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine