Skip to main content
Top
Published in: Archives of Virology 9/2018

01-09-2018 | Original Article

Saponin-adjuvanted vaccine protects chickens against velogenic Newcastle disease virus

Authors: Wahid H. El-Dabae, Hussein Aly Hussein, Mohammed A. Rohaim, Munir M. El-Safty, Nagwa S. Ata, Ismail M. Reda

Published in: Archives of Virology | Issue 9/2018

Login to get access

Abstract

Despite extensive vaccination campaigns, Newcastle disease virus (NDV) remains endemic in many countries worldwide, and factors that contribute to this failure include mismatched vaccines, partial immunization, and poor husbandry practices. In order to overcome the problem of genetic divergence between circulating field strains and vaccine strains, we saponin-adjuvanted an Egyptian field strain and assessed its safety and immunogenicity in chickens. Immunization of chickens with the vaccine followed by challenge with a velogenic reference strain revealed the potential of the saponin-adjuvanted vaccine to induce a strong immune response that resulted in complete protection of chickens. Importantly, in vaccinated chickens, virus shedding was abolished, providing an added advantage over the currently available commercial live-attenuated and inactivated vaccines, which are unable to prevent shedding. A histopathological investigation demonstrated that the vaccinated chickens had less-severe lesions than challenged unvaccinated and mock-vaccinated chickens. We propose using this formulation as an alternative and improved NDV vaccine platform that can be exploited to control disease not only in Egypt but also in other disease-endemic countries.
Appendix
Available only for authorised users
Literature
1.
go back to reference Aldous EW, Mynn JK, Banks J, Alexander DJ (2003) A molecular epidemiological study of avian paramyxovirus type 1 (Newcastle disease virus) isolates by phylogenetic analysis of a partial nucleotide sequence of the fusion protein gene. Avian Pathol 32:239–256CrossRefPubMed Aldous EW, Mynn JK, Banks J, Alexander DJ (2003) A molecular epidemiological study of avian paramyxovirus type 1 (Newcastle disease virus) isolates by phylogenetic analysis of a partial nucleotide sequence of the fusion protein gene. Avian Pathol 32:239–256CrossRefPubMed
2.
go back to reference Alexander DJ, Aldous EW, Fuller CM (2012) The long view, a selective review of 40 years of Newcastle disease research. Avian Pathol 41:329–335CrossRefPubMed Alexander DJ, Aldous EW, Fuller CM (2012) The long view, a selective review of 40 years of Newcastle disease research. Avian Pathol 41:329–335CrossRefPubMed
3.
go back to reference Anders S, John C (1998) Uptake and adjuvant activity of orally delivered saponin and ISCOM vaccines. Adv Drug Deliv Rev 34:321–338CrossRef Anders S, John C (1998) Uptake and adjuvant activity of orally delivered saponin and ISCOM vaccines. Adv Drug Deliv Rev 34:321–338CrossRef
4.
go back to reference Amarasinghe GK, Bào Y, Basler CF, Bavari S, Beer M, Bejerman N, Blasdell KR, Bochnowski A, Briese T, Bukreyev A, Calisher CH, Chandran K, Collins PL, Dietzgen RG, Dolnik O, Dürrwald R, Dye JM, Easton AJ, Ebihara H, Fang Q, Formenty P, Fouchier RM, Ghedin E, Harding RM, Hewson R, Higgins CM, Hong J, Horie M, James AP, Jiang D, Kobinger GP, Kondo H, Kurath G, Lamb RA, Lee B, Leroy EM, Li M, Maisner A, Mühlberger E, Netesov SV, Nowotny N, Patterson JL, Payne SL, Paweska JT, Pearson MN, Randall RE, Revill PA, Rima BK, Rota P, Rubbenstroth D, Schwemmle M, Smither SJ, Song Q, Stone DM, Takada A, Terregino C, Tesh RB, Tomonaga K, Tordo N, Towner JS, Vasilakis N, Volchkov VE, Wahl-Jensen V, Walker PJ, Wang B, Wang D, Wang F, Wang L, Werren JH, Whitfield AE, Yan Z, Ye G, Kuhn JH (2017) Taxonomy of the order Mononegavirales: update 2017. Arch Virol 162(8):2493–2504. https://doi.org/10.1007/s00705-017-3311-7 CrossRefPubMedPubMedCentral Amarasinghe GK, Bào Y, Basler CF, Bavari S, Beer M, Bejerman N, Blasdell KR, Bochnowski A, Briese T, Bukreyev A, Calisher CH, Chandran K, Collins PL, Dietzgen RG, Dolnik O, Dürrwald R, Dye JM, Easton AJ, Ebihara H, Fang Q, Formenty P, Fouchier RM, Ghedin E, Harding RM, Hewson R, Higgins CM, Hong J, Horie M, James AP, Jiang D, Kobinger GP, Kondo H, Kurath G, Lamb RA, Lee B, Leroy EM, Li M, Maisner A, Mühlberger E, Netesov SV, Nowotny N, Patterson JL, Payne SL, Paweska JT, Pearson MN, Randall RE, Revill PA, Rima BK, Rota P, Rubbenstroth D, Schwemmle M, Smither SJ, Song Q, Stone DM, Takada A, Terregino C, Tesh RB, Tomonaga K, Tordo N, Towner JS, Vasilakis N, Volchkov VE, Wahl-Jensen V, Walker PJ, Wang B, Wang D, Wang F, Wang L, Werren JH, Whitfield AE, Yan Z, Ye G, Kuhn JH (2017) Taxonomy of the order Mononegavirales: update 2017. Arch Virol 162(8):2493–2504. https://​doi.​org/​10.​1007/​s00705-017-3311-7 CrossRefPubMedPubMedCentral
5.
go back to reference Bwala DG, Clift S, Duncan NM, Bisschop SP, Oludayo FF (2012) Determination of the distribution of lentogenic vaccine and virulent Newcastle disease virus antigen in the oviduct of SPF and commercial hen using immunohistochemistry. Res Vet Sci 93:520–528CrossRefPubMed Bwala DG, Clift S, Duncan NM, Bisschop SP, Oludayo FF (2012) Determination of the distribution of lentogenic vaccine and virulent Newcastle disease virus antigen in the oviduct of SPF and commercial hen using immunohistochemistry. Res Vet Sci 93:520–528CrossRefPubMed
6.
go back to reference Cary AR, Leonardo S, Ingrid C, Corrie CB, Darrell RK, David LS, Daniel JK, Patti JM, Claudio LA (2011) Virulent Newcastle disease virus elicits a strong innate immune response in chickens. J Gen Virol 92:931–939CrossRef Cary AR, Leonardo S, Ingrid C, Corrie CB, Darrell RK, David LS, Daniel JK, Patti JM, Claudio LA (2011) Virulent Newcastle disease virus elicits a strong innate immune response in chickens. J Gen Virol 92:931–939CrossRef
7.
go back to reference Cattoli G, Fusaro A, Monne I, Molia S, Le Menach A, Maregeya B, Nchare A, Bangana I, Maina AG, Koffi JN, Thiam H, Bezeid OE, Salviato A, Nisi R (2010) Emergence of a new genetic lineage of Newcastle disease virus in West and Central Africa—implications for diagnosis and control. Vet Microbiol 142:168–176CrossRefPubMed Cattoli G, Fusaro A, Monne I, Molia S, Le Menach A, Maregeya B, Nchare A, Bangana I, Maina AG, Koffi JN, Thiam H, Bezeid OE, Salviato A, Nisi R (2010) Emergence of a new genetic lineage of Newcastle disease virus in West and Central Africa—implications for diagnosis and control. Vet Microbiol 142:168–176CrossRefPubMed
8.
go back to reference Courtney SC, Susta L, Gomez D, Hines NL, Pedersen JC, Brown CC, Miller PJ, Afonso CL (2013) Highly divergent virulent isolates of Newcastle disease virus from the Dominican Republic are members of a new genotype that may have evolved unnoticed for over 2 decades. J Clin Microbiol 51:508–517CrossRefPubMedPubMedCentral Courtney SC, Susta L, Gomez D, Hines NL, Pedersen JC, Brown CC, Miller PJ, Afonso CL (2013) Highly divergent virulent isolates of Newcastle disease virus from the Dominican Republic are members of a new genotype that may have evolved unnoticed for over 2 decades. J Clin Microbiol 51:508–517CrossRefPubMedPubMedCentral
9.
go back to reference Daubney R, Mansy W (1948) The occurrence of Newcastle disease in Egypt. J Comp Pathol Ther 58:189–200CrossRefPubMed Daubney R, Mansy W (1948) The occurrence of Newcastle disease in Egypt. J Comp Pathol Ther 58:189–200CrossRefPubMed
10.
go back to reference Diel DG, da Silva LH, Liu H, Wang Z, Miller PJ, Afonso CL (2012) Genetic diversity of avian paramyxovirus type 1, proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol 12:1770–1779CrossRefPubMed Diel DG, da Silva LH, Liu H, Wang Z, Miller PJ, Afonso CL (2012) Genetic diversity of avian paramyxovirus type 1, proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol 12:1770–1779CrossRefPubMed
11.
go back to reference Dimitrov KM, Afonso CL, Yu Q, Miller PJ (2017) Newcastle disease vaccines-A solved problem or a continuous challenge? Vet Microbiol 206:126–136CrossRefPubMed Dimitrov KM, Afonso CL, Yu Q, Miller PJ (2017) Newcastle disease vaccines-A solved problem or a continuous challenge? Vet Microbiol 206:126–136CrossRefPubMed
12.
go back to reference Fenwick GR, Price KR, Tsukamoto C, Okubo K (1991) Saponins. In: Mello FJPD, Duffus CM, Duffus JH (eds) Saponins in toxic substances in crop plants. The Royal Society of Chemistry, Cambridge, pp 285–327CrossRef Fenwick GR, Price KR, Tsukamoto C, Okubo K (1991) Saponins. In: Mello FJPD, Duffus CM, Duffus JH (eds) Saponins in toxic substances in crop plants. The Royal Society of Chemistry, Cambridge, pp 285–327CrossRef
13.
go back to reference Francis G, Kerem Z, Makkar HPS, Becker K (2002) The biological action of saponins in animal system: a review. Br J Nutr 88:587–605CrossRefPubMed Francis G, Kerem Z, Makkar HPS, Becker K (2002) The biological action of saponins in animal system: a review. Br J Nutr 88:587–605CrossRefPubMed
14.
go back to reference Ganar K, Das M, Sinha S, Kumar S (2014) Newcastle disease virus current status and our understanding. Virus Res 184:71–81CrossRefPubMed Ganar K, Das M, Sinha S, Kumar S (2014) Newcastle disease virus current status and our understanding. Virus Res 184:71–81CrossRefPubMed
15.
go back to reference Haridas V, Arntzen CJ, Gutterman JU (2001) Avicins, a family of triterpenoid saponins from Acacia victoriae (Bentham), inhibit activation of nuclear factor-kappa B by inhibiting both its nuclear localization and ability to bind DNA. Proc Natl Acad Sci USA 98:11557–11562CrossRefPubMed Haridas V, Arntzen CJ, Gutterman JU (2001) Avicins, a family of triterpenoid saponins from Acacia victoriae (Bentham), inhibit activation of nuclear factor-kappa B by inhibiting both its nuclear localization and ability to bind DNA. Proc Natl Acad Sci USA 98:11557–11562CrossRefPubMed
16.
go back to reference Hu Z, Hu J, Hu S, Song Q, Ding P, Zhu J, Liu X, Wang X, Liu X (2015) High levels of virus replication and an intense inflammatory response contribute to the severe pathology in lymphoid tissues caused by Newcastle disease virus genotype VIId. Arch Virol 160:639–648CrossRefPubMed Hu Z, Hu J, Hu S, Song Q, Ding P, Zhu J, Liu X, Wang X, Liu X (2015) High levels of virus replication and an intense inflammatory response contribute to the severe pathology in lymphoid tissues caused by Newcastle disease virus genotype VIId. Arch Virol 160:639–648CrossRefPubMed
17.
go back to reference Hussein HA, El-Sanousi AA, Youssif AA, Shalaby MA, Saber MS, Reda IM (2005) Sequence analysis of fusion and matrix protein genes of the velogenic viscerotropic Newcastle disease virus Egyptian strain sr/76. Int J Virol 1:38CrossRef Hussein HA, El-Sanousi AA, Youssif AA, Shalaby MA, Saber MS, Reda IM (2005) Sequence analysis of fusion and matrix protein genes of the velogenic viscerotropic Newcastle disease virus Egyptian strain sr/76. Int J Virol 1:38CrossRef
18.
go back to reference Hussein HA, Emara MM, Rohaim MA (2014) Molecular Characterization of Newcastle Disease Virus Genotype VIID in Avian influenza H5N1 Infected Broiler Flock in Egypt. Int J Virol 10:46–54CrossRef Hussein HA, Emara MM, Rohaim MA (2014) Molecular Characterization of Newcastle Disease Virus Genotype VIID in Avian influenza H5N1 Infected Broiler Flock in Egypt. Int J Virol 10:46–54CrossRef
19.
go back to reference Kapczynski DR, Afonso CL, Miller PJ (2013) Immune responses of poultry to Newcastle disease virus. Dev Comp Immunol 41:447–453CrossRefPubMed Kapczynski DR, Afonso CL, Miller PJ (2013) Immune responses of poultry to Newcastle disease virus. Dev Comp Immunol 41:447–453CrossRefPubMed
20.
go back to reference Kapczynski DR, King DJ (2005) Protection of chickens against overt clinical disease and determination of viral shedding following vaccination with commercially available Newcastle disease virus vaccines upon challenge with highly virulent virus from the California 2002 exotic Newcastle disease outbreak. Vaccine 23:3424–3433CrossRefPubMed Kapczynski DR, King DJ (2005) Protection of chickens against overt clinical disease and determination of viral shedding following vaccination with commercially available Newcastle disease virus vaccines upon challenge with highly virulent virus from the California 2002 exotic Newcastle disease outbreak. Vaccine 23:3424–3433CrossRefPubMed
21.
go back to reference Kensil CR (1996) Saponins as vaccine adjuvants. Crit Rev Ther Drug Carrier Syst 13:1–55PubMed Kensil CR (1996) Saponins as vaccine adjuvants. Crit Rev Ther Drug Carrier Syst 13:1–55PubMed
22.
go back to reference Kong X, Hu Y, Rui R, Wang D, Li X (2004) Effects of Chinese herbal medicinal ingredients on peripheral lymphocyte proliferation and serum antibody titer after vaccination in chicken. Int Immunopharmacol 4(7):975–982CrossRefPubMed Kong X, Hu Y, Rui R, Wang D, Li X (2004) Effects of Chinese herbal medicinal ingredients on peripheral lymphocyte proliferation and serum antibody titer after vaccination in chicken. Int Immunopharmacol 4(7):975–982CrossRefPubMed
23.
go back to reference Miller PJ, Estevez C, Yu Q, Suarez DL, King DJ (2009) Comparison of viral shedding following vaccination with inactivated and live Newcastle disease vaccines formulated with wild-type and recombinant viruses. Avian Dis 53:39–49CrossRefPubMed Miller PJ, Estevez C, Yu Q, Suarez DL, King DJ (2009) Comparison of viral shedding following vaccination with inactivated and live Newcastle disease vaccines formulated with wild-type and recombinant viruses. Avian Dis 53:39–49CrossRefPubMed
24.
go back to reference Miller PJ, King DJ, Afonso CL, Suarez DL (2007) Antigenic differences among Newcastle disease virus strains of different genotypes used in vaccine formulation affect viral shedding after a virulent challenge. Vaccine 25:7238–7246CrossRefPubMed Miller PJ, King DJ, Afonso CL, Suarez DL (2007) Antigenic differences among Newcastle disease virus strains of different genotypes used in vaccine formulation affect viral shedding after a virulent challenge. Vaccine 25:7238–7246CrossRefPubMed
25.
go back to reference Mohamed MH, Kumar S, Paldurai A, Megahed MM, Ghanem IA, Lebdah MA, Samal SK (2009) Complete genome sequence of a virulent Newcastle disease virus isolated from an outbreak in chickens in Egypt. Virus Genes 39:234–237CrossRefPubMed Mohamed MH, Kumar S, Paldurai A, Megahed MM, Ghanem IA, Lebdah MA, Samal SK (2009) Complete genome sequence of a virulent Newcastle disease virus isolated from an outbreak in chickens in Egypt. Virus Genes 39:234–237CrossRefPubMed
26.
go back to reference Mohamed MH, Kumar S, Paldurai A, Samal SK (2011) Sequence analysis of fusion protein gene of Newcastle disease virus isolated from outbreaks in Egypt during 2006. Virol J 8:237CrossRefPubMedPubMedCentral Mohamed MH, Kumar S, Paldurai A, Samal SK (2011) Sequence analysis of fusion protein gene of Newcastle disease virus isolated from outbreaks in Egypt during 2006. Virol J 8:237CrossRefPubMedPubMedCentral
27.
go back to reference Munir M (2013) Mononegaviruses of veterinary importance, chapter 2. In: Zohari S, Munir M (eds) Pathobiology and molecular diagnosis, vol I. Avian paramyxoviruses serotype 1 to 10. CAB eBooks, pp 15–37 Munir M (2013) Mononegaviruses of veterinary importance, chapter 2. In: Zohari S, Munir M (eds) Pathobiology and molecular diagnosis, vol I. Avian paramyxoviruses serotype 1 to 10. CAB eBooks, pp 15–37
28.
go back to reference Oda K, Matsuda H, Murakami T, Katayama S, Ohgitani T, Yoshikawa M (2000) Adjuvant and haemolytic activities of 47 saponins derived from medicinal and food plants. Biol Chem 381:67–74CrossRefPubMed Oda K, Matsuda H, Murakami T, Katayama S, Ohgitani T, Yoshikawa M (2000) Adjuvant and haemolytic activities of 47 saponins derived from medicinal and food plants. Biol Chem 381:67–74CrossRefPubMed
29.
go back to reference OIE (2012) Newcastle disease (version adopted by the World Assembly of Delegates of the OIE in May 2012). OIE terrestrial manual OIE (2012) Newcastle disease (version adopted by the World Assembly of Delegates of the OIE in May 2012). OIE terrestrial manual
30.
go back to reference Orabi A, Hussein A, Saleh AA, Abu El-Magd M, Munir M (2017) Evolutionary insights into the fusion protein of Newcastle disease virus isolated from vaccinated chickens in 2016 in Egypt. Arch Virol 162:3069–3079CrossRefPubMed Orabi A, Hussein A, Saleh AA, Abu El-Magd M, Munir M (2017) Evolutionary insights into the fusion protein of Newcastle disease virus isolated from vaccinated chickens in 2016 in Egypt. Arch Virol 162:3069–3079CrossRefPubMed
32.
go back to reference Qin ZM, Tan LT, Xu HY, Ma BC, Wang YL, Yuan XY, Liu WJ (2008) Pathotypical characterization and molecular epidemiology of Newcastle disease virus isolates from different hosts in China from 1996 to 2005. J Clin Microbiol 46:601–611CrossRefPubMed Qin ZM, Tan LT, Xu HY, Ma BC, Wang YL, Yuan XY, Liu WJ (2008) Pathotypical characterization and molecular epidemiology of Newcastle disease virus isolates from different hosts in China from 1996 to 2005. J Clin Microbiol 46:601–611CrossRefPubMed
33.
go back to reference Radwan MM, Darwish SF, El-Sabagh IM, El-Sanousi AA, Shalaby MA (2013) Isolation and molecular characterization of Newcastle disease virus genotypes II and VIId in Egypt between 2011 and 2012. Virus Genes 47:311–316CrossRefPubMed Radwan MM, Darwish SF, El-Sabagh IM, El-Sanousi AA, Shalaby MA (2013) Isolation and molecular characterization of Newcastle disease virus genotypes II and VIId in Egypt between 2011 and 2012. Virus Genes 47:311–316CrossRefPubMed
34.
go back to reference Rivera E, Daggfeldt A, Hu S (2003) Ginseng extractin aluminiumhydroxide adjuvanted vaccines improves the antibody response of pigs to porcine parvovirus and Erysipelothrix rhusiopathiae. Vet Immunol Immunopathol 91:19–27CrossRefPubMed Rivera E, Daggfeldt A, Hu S (2003) Ginseng extractin aluminiumhydroxide adjuvanted vaccines improves the antibody response of pigs to porcine parvovirus and Erysipelothrix rhusiopathiae. Vet Immunol Immunopathol 91:19–27CrossRefPubMed
35.
go back to reference Rivera E, Hu S, Concha C (2003) Ginseng and aluminium hydroxide act synergistically as vaccine adjuvants. Vaccine 21:1149–1157CrossRefPubMed Rivera E, Hu S, Concha C (2003) Ginseng and aluminium hydroxide act synergistically as vaccine adjuvants. Vaccine 21:1149–1157CrossRefPubMed
36.
go back to reference Rohaim MA, El Naggar RF, Helal AM, Hussein HA, Munir M (2017) Reverse spillover of avian viral vaccine strains from domesticated poultry to wild birds. Vaccine 35:3523–3527CrossRefPubMed Rohaim MA, El Naggar RF, Helal AM, Hussein HA, Munir M (2017) Reverse spillover of avian viral vaccine strains from domesticated poultry to wild birds. Vaccine 35:3523–3527CrossRefPubMed
37.
go back to reference Rohaim MA, El-Naggar RF, Helal AM, Hussein HA, Le-Blanc N (2016) Genetic characterization of pigeon paramyxovirus type 1 in Egypt. Br J Virol 3:27–32CrossRef Rohaim MA, El-Naggar RF, Helal AM, Hussein HA, Le-Blanc N (2016) Genetic characterization of pigeon paramyxovirus type 1 in Egypt. Br J Virol 3:27–32CrossRef
38.
go back to reference Roy P, Venugopalan AT, Koteeswaran A (1999) Efficacy of live adjuvanted mesogenic Newcastle disease vaccine in chicken. Vaccine 17:2674–2676CrossRefPubMed Roy P, Venugopalan AT, Koteeswaran A (1999) Efficacy of live adjuvanted mesogenic Newcastle disease vaccine in chicken. Vaccine 17:2674–2676CrossRefPubMed
39.
go back to reference Rui Z, Juan P, Jingliang S, Jixun Z, Xiaoting W, Shouping Z, Xiaojiao L, Guozhong Z (2010) Phylogenetic characterization of Newcastle disease virus isolated in the mainland of China during 2001–2009. Vet Microbiol 141:246–257CrossRefPubMed Rui Z, Juan P, Jingliang S, Jixun Z, Xiaoting W, Shouping Z, Xiaojiao L, Guozhong Z (2010) Phylogenetic characterization of Newcastle disease virus isolated in the mainland of China during 2001–2009. Vet Microbiol 141:246–257CrossRefPubMed
40.
go back to reference Samina I, Khinich Y, Gutter B, Michael A, Peleg BA (1999) Day-old vaccination with live-in-oil vaccines, Newcastle disease (ND) and infectious bursal disease (IBD) in chicks and ND in turkey poults. Avian Pathol 28:73–78CrossRefPubMed Samina I, Khinich Y, Gutter B, Michael A, Peleg BA (1999) Day-old vaccination with live-in-oil vaccines, Newcastle disease (ND) and infectious bursal disease (IBD) in chicks and ND in turkey poults. Avian Pathol 28:73–78CrossRefPubMed
41.
go back to reference Suzuki K, Okada HI, Tada T, Mase T, Nakamura M, Kubo K, Tsukamoto M (2009) Association of increased pathogenicity of Asian H5N1 highly pathogenic avian influenza viruses in chickens with highly efficient viral replication accompanied by early destruction of innate immune responses. J Virol 83(15):7475–7486CrossRefPubMedPubMedCentral Suzuki K, Okada HI, Tada T, Mase T, Nakamura M, Kubo K, Tsukamoto M (2009) Association of increased pathogenicity of Asian H5N1 highly pathogenic avian influenza viruses in chickens with highly efficient viral replication accompanied by early destruction of innate immune responses. J Virol 83(15):7475–7486CrossRefPubMedPubMedCentral
42.
go back to reference Villegas P, Purchase HG (1989) Titration of biological suspension. In: Purchase HG, Lawrence H, Domermuth CH, James Pearson E (eds) A laboratory manual for the isolation and identification of avian pathogens. American Association of Avian Pathologists, University of Pennsylvania, New Bolton Center, Kennett Square, pp 186–191 Villegas P, Purchase HG (1989) Titration of biological suspension. In: Purchase HG, Lawrence H, Domermuth CH, James Pearson E (eds) A laboratory manual for the isolation and identification of avian pathogens. American Association of Avian Pathologists, University of Pennsylvania, New Bolton Center, Kennett Square, pp 186–191
43.
go back to reference Wise MG, Suarez DL, Seal BS, Pedersen JC, Senne DA, King DJ, Kapczynski DR, Spackman E (2004) Development of a real-time reverse-transcription PCR for detection of newcastle disease virus RNA in clinical samples. J Clin Microbiol 42:329–338CrossRefPubMedPubMedCentral Wise MG, Suarez DL, Seal BS, Pedersen JC, Senne DA, King DJ, Kapczynski DR, Spackman E (2004) Development of a real-time reverse-transcription PCR for detection of newcastle disease virus RNA in clinical samples. J Clin Microbiol 42:329–338CrossRefPubMedPubMedCentral
44.
go back to reference Yin J, Jin H, Kang Y, Xiao C, Zhao L, Li X, Ding Z, Yang F, Zhu Q, Wang B (2006) Efficacy of modified levamisole adjuvant on inactivated virus vaccine. Viral Immunol 19:525–535CrossRefPubMed Yin J, Jin H, Kang Y, Xiao C, Zhao L, Li X, Ding Z, Yang F, Zhu Q, Wang B (2006) Efficacy of modified levamisole adjuvant on inactivated virus vaccine. Viral Immunol 19:525–535CrossRefPubMed
45.
go back to reference Yoshiki Y, Kudou S, Okubo K (1998) Relationship between chemical structures and biological activities of triterpenoid saponins from soybean (review). Biosci Biotechnol Biochem 62:2291–2299CrossRefPubMed Yoshiki Y, Kudou S, Okubo K (1998) Relationship between chemical structures and biological activities of triterpenoid saponins from soybean (review). Biosci Biotechnol Biochem 62:2291–2299CrossRefPubMed
46.
go back to reference Yui S, Ubukata K, Hodono K, Kitahara M, Mimaki Y, Kuroda M, Sashida Y, Yamazaki M (2001) Macrophage- oriented cytotoxic activity of novel triterpene saponins extracted from roots of Securidaca inappendiculata. Int Immunopharmacol 1:1989–2000CrossRefPubMed Yui S, Ubukata K, Hodono K, Kitahara M, Mimaki Y, Kuroda M, Sashida Y, Yamazaki M (2001) Macrophage- oriented cytotoxic activity of novel triterpene saponins extracted from roots of Securidaca inappendiculata. Int Immunopharmacol 1:1989–2000CrossRefPubMed
47.
go back to reference Yu J, Shi FS, Hu S (2015) Improved immune responses to a bivalent vaccine of Newcastle disease and avian influenza in chickens by ginseng stem-leaf saponins. Vet Immunol Immunopathol 167(3–4):147–155CrossRefPubMed Yu J, Shi FS, Hu S (2015) Improved immune responses to a bivalent vaccine of Newcastle disease and avian influenza in chickens by ginseng stem-leaf saponins. Vet Immunol Immunopathol 167(3–4):147–155CrossRefPubMed
48.
go back to reference Zhai L, Li Y, Wang W, Wang Y, Hu S (2011) Effect of oral administration of ginseng stem-and-leaf saponins (GSLS) on the immune responses to Newcastle disease vaccine in chickens. Vaccine 29(31):5007–5014CrossRefPubMed Zhai L, Li Y, Wang W, Wang Y, Hu S (2011) Effect of oral administration of ginseng stem-and-leaf saponins (GSLS) on the immune responses to Newcastle disease vaccine in chickens. Vaccine 29(31):5007–5014CrossRefPubMed
49.
go back to reference Zhang X, Zhang X, Yang Q (2007) Effect of compound mucosal immune adjuvant on mucosal and systemic immune responses in chicken orally vaccinated with attenuated Newcastle-disease vaccine. Vaccine 25:3254–3262CrossRefPubMed Zhang X, Zhang X, Yang Q (2007) Effect of compound mucosal immune adjuvant on mucosal and systemic immune responses in chicken orally vaccinated with attenuated Newcastle-disease vaccine. Vaccine 25:3254–3262CrossRefPubMed
50.
go back to reference Zhao J, Wohlford-Lenane C, Zhao J, Fleming E, Lane TE, McCray PB Jr, Perlman S (2012) Intranasal treatment with poly(I·C) protects aged mice from lethal respiratory virus infections. J Virol 86(21):11416–11424CrossRefPubMedPubMedCentral Zhao J, Wohlford-Lenane C, Zhao J, Fleming E, Lane TE, McCray PB Jr, Perlman S (2012) Intranasal treatment with poly(I·C) protects aged mice from lethal respiratory virus infections. J Virol 86(21):11416–11424CrossRefPubMedPubMedCentral
Metadata
Title
Saponin-adjuvanted vaccine protects chickens against velogenic Newcastle disease virus
Authors
Wahid H. El-Dabae
Hussein Aly Hussein
Mohammed A. Rohaim
Munir M. El-Safty
Nagwa S. Ata
Ismail M. Reda
Publication date
01-09-2018
Publisher
Springer Vienna
Published in
Archives of Virology / Issue 9/2018
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-018-3917-4

Other articles of this Issue 9/2018

Archives of Virology 9/2018 Go to the issue