Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-25T19:21:35.400Z Has data issue: false hasContentIssue false

Characterization of avian metapneumoviruses isolated in the USA

Published online by Cambridge University Press:  09 March 2007

Humphrey C. M. Lwamba
Affiliation:
Department of Veterinary Pathobiology, University of Minnesota, 1971 Commonwealth Avenue, St Paul, MN 55108, USA
Richard S. Bennett
Affiliation:
Department of Veterinary Pathobiology, University of Minnesota, 1971 Commonwealth Avenue, St Paul, MN 55108, USA
Dale C. Lauer
Affiliation:
Minnesota Poultry Testing Laboratory, Minnesota Board of Animal Health, Wilmar, MN 56201, USA.
David A. Halvorson
Affiliation:
Department of Veterinary Pathobiology, University of Minnesota, 1971 Commonwealth Avenue, St Paul, MN 55108, USA
M. Kariuki Njenga*
Affiliation:
Department of Veterinary Pathobiology, University of Minnesota, 1971 Commonwealth Avenue, St Paul, MN 55108, USA
*
*Corresponding author: Department of Veterinary Pathobiology, University of Minnesota, 1971 Commonwealth Avenue, St Paul, MN 55108, USA E-mail: [email protected]

Abstract

Avian pneumovirus (APV; officially known as turkey rhinotracheitis virus) is an emergent pathogen of birds in the USA that results in upper respiratory tract disease in turkeys. Six years after the first outbreak in the USA, the disease continues to ravage turkey flocks, primarily in the state of Minnesota. From 1997 to 2000, the industry recorded losses estimated at US$15 million per annum. Researchers have developed sensitive diagnostic techniques, including the enzyme-linked immunosorbent assay and the reverse transcriptase–polymerase chain reaction, which, when used together, are highly sensitive in detecting APV outbreaks in commercial turkey flocks. Phylogenetic analysis of the nucleotide and predicted amino acid sequence of 15 US viruses isolated between 1996 and 2000 demonstrated that the US viruses are relatively homogenous but different from the European APV subgroups A and B, resulting in the classification of US isolates into subgroup C. Infectious APV was isolated from sentinel waterfowls placed close to an infected commercial turkey farm and from wild Canada geese captured in Minnesota, suggesting that free-ranging birds may be involved in the spread of APV. Current efforts to prevent and control the infection include improving management and biosecurity practices and developing attenuated live and deletion mutant vaccines capable of conferring protection.

Type
Research Article
Copyright
Copyright © CAB International 2002

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, DJ Jr (1997). Newcastle disease and other Paramyxoviridae infections. In: Calnek, BW, Barnes, HJ, Beard, CW, McDougall, L and Saif, YM Jr (editors). In Diseases of Poultry, 10th edn. Ames (IA): State University Press, pp. 541569.Google Scholar
Alexander, DJ, Gough, RE, Wyeth, PJ, Lister, SA and Chettle, NJ (1986). Viruses associated with turkey rhinotracheitis in Great Britain. Veterinary Record 118: 217218.CrossRefGoogle ScholarPubMed
Ali, A and Reynolds, DL (1999). A reverse transcription–polymerase chain reaction assay for the detection of avian pneumovirus (Colorado strain). Avian Diseases 43: 600603.CrossRefGoogle ScholarPubMed
Anon (1985). Rhinotracheitis of unknown etiology in England and Wales (Preliminary report from the British Veterinary Poultry Association). Veterinary Record 117: 653654.Google Scholar
Arns, CW and Hafez, HM (1992). Swollen head syndrome in poultry flocks in Brazil. Proceedings of the 41st Western Poultry Disease Conference,Sacramento, CA, pp. 8183.Google Scholar
Bayon-Auboyer, MH, Arnauld, C, Toquin, D and Eterradossi, N (2000). Nucleotide sequences of the F, L, and G protein genes of two non-A/non-B avian pneumoviruses (APV) reveal a novel APV subgroup. Journal of General Virology 81: 27232733.CrossRefGoogle Scholar
Bennett, RS, McComb, B, Shin, H-J, Njenga, MK, Nagaraja, KV and Halvorson, DA (2002). Detection of avian pneumovirus in wild Canadian geese (Branta canadensis) and blue-winged teal (Anas discors). Avian Diseases 46: 10251029.CrossRefGoogle Scholar
Buys, SB and Du Preez, JH (1980). A preliminary report on the isolation of a virus causing sinusitis in turkeys in South Africa and attempts to attenuate the virus. Turkeys 28: 3646.Google Scholar
Buys, SB, Du Preez, JH and Els, HJ (1989). The isolation and attenuation of a virus causing turkey rhinotracheitis in turkeys in South Africa. Onderstepoort Journal of Veterinary Research 56: 8798.Google ScholarPubMed
Cadman, HF, Kelly, PJ, Zhou, R, Davelaar, F and Mason, PR (1994). A serosurvey using enzyme-linked immunosorbent assay for antibodies against poultry pathogens in ostriches (Struthio camelus) from Zimbabwe. Avian Diseases 38: 621625.CrossRefGoogle ScholarPubMed
Catelli, E, De Marco, MA, Delugo, M, Terregino, C and Guberi, V (2001). Serological evidence of avian pneumovirus infection in reared and free-living pheasants. Veterinary Record 149: 5658.CrossRefGoogle ScholarPubMed
Cavanagh, D and Barret, T (1988). Pneumovirus-like characteristics of the mRNA and proteins of turkey rhinotracheitis virus. Virus Research 11: 241256.CrossRefGoogle ScholarPubMed
Chary, P, Rautenschlein, S, Njenga, MK and Sharma, JM (2002). Pathogenic and immunosuppressive effects of avian pneumovirus in turkeys. Avian Diseases 46: 153161.CrossRefGoogle ScholarPubMed
Chettle, NJ and Wyeth, PJ (1988). Turkey rhinotracheitis: detection of antibodies using an ELISA test. British Veterinary Journal 144: 282287.CrossRefGoogle ScholarPubMed
Chiang, SJ, Dar, AM, Goyal, SM, Nagaraja, KV, Halvorson, DA and Kapur, V (2000). A modified enzyme-liked immunosorbent assay for the detection of avian pneumovirus antibodies. Journal of Veterinary Diagnostic Investigation 12: 381384.CrossRefGoogle Scholar
Collins, MS and Gough, RE (1988). Characterization of a virus associated with rhinotracheitis. Journal of General Virology 69: 909916.CrossRefGoogle ScholarPubMed
Collins, MS, Gough, RE and Alexander, DJ (1993). Antigenic differentiation of avian pneumovirus isolates using polyclonal antisera and mouse monoclonal antibodies. Avian Pathology 22: 469479.CrossRefGoogle ScholarPubMed
Collins, PL, McIntosh, K and Chanock, RM (1996). Respiratory syncytial virus. In: Fields, BN, Knipe, DM and Howeley, PM (editors). Field's Virology, 3rd edn. Philadelphia: Lippincott-Raven, pp. 13131351.Google Scholar
Cook, JKA and Cavanagh, D (2002). Detection and differentiation of avian pneumoviruses (metapneumoviruses). Avian Pathology 31: 117132.CrossRefGoogle ScholarPubMed
Cook, JKA, Holmes, HC, Finney, PM, Ellis, MM, Huggins, MB and Dolby, CA (1989). A live attenuated turkey rhinotracheitis virus vaccine. The use of the attenuated strains as an experimental vaccine. Avian Pathology 18: 523534.CrossRefGoogle ScholarPubMed
Cook, JKA, Ellis, MM and Huggins, MB (1991). The pathogenesis of turkey rhinotracheitis virus in turkey poults inoculated with the virus alone or together with two strains of bacteria. Avian Pathology 20: 155166.CrossRefGoogle ScholarPubMed
Cook, JKA, Huggins, MB, Woods, MA, Orbell, SJ and Mockett, AP (1995). Protection provided by a commercially available vaccine against different strains of turkey rhinotracheitis virus. Veterinary Record 25: 231243.Google Scholar
Cook, JKA, Orthel, F, Orbell, SJ, Woods, MA and Huggins, MB (1996). An experimental turkey rhinotracheitis (TRT) infection in breeding turkeys and the prevention of its clinical effects using live-attenuated and inactivated TRT vaccines. Avian Pathology 136: 392393.Google Scholar
Cook, JKA, Huggins, MB, Orbell, SJ and Senne, DA (1999). Preliminary antigenic characterization of an avian pneumovirus isolated from commercial turkeys in Colorado, USA. Avian Pathology 28: 607617.CrossRefGoogle ScholarPubMed
Dani, MA, Durigon, EL and Arns, CW (1999). Molecular characterization of Brazilian avian pneumovirus isolates: comparison between immunochemiluminiscent Southern blot and nested PCR. Journal of Virological Methods 79: 237241.CrossRefGoogle Scholar
Dar, A, Tune, K, Panigrahy, B, Goyal, SM and Kapur, V (2001). PCR-based detection of an emerging avian pneumovirus in US turkey flocks. Journal of Veterinary Diagnostic Investigation 13: 201205.CrossRefGoogle ScholarPubMed
Decanini, EL, Miranda, EC and Le Gros, FX (1991). Swollen head syndrome in heavy breeders in Mexico. In: Proceedings of the 40th Western Poultry Disease Conference,Acapulco, Mexico, pp. 158159.Google Scholar
Edson, RK (1997). Experience with avian pneumovirus. In: Proceedings of the 101st Annual Meeting of the United States Animal Health Association,Louisville (KY), pp. 471472.Google Scholar
El Houadfi, M, Hamam, J, Vanmarche, J and Cook, JKA (1991). Swollen head syndrome in broiler chicken in Morocco. In: Proceedings of 40th Western Poultry Disease Conference,Acapulco, Mexico, pp. 126127.Google Scholar
Giraud, P and Bennejean, G (1986). Turkey rhinotracheitis in France: preliminary investigations on ciliostatic virus. Veterinary Record 119: 606607.Google ScholarPubMed
Gough, RE, Collins, MS, Cox, WJ and Chettle, NJ (1988). Experimental infection of turkeys, chickens, ducks, geese, guinea fowl, pheasants, and pigeons with turkey rhinotracheitis virus. Veterinary Record 123: 5859.CrossRefGoogle ScholarPubMed
Goyal, SM, Chiang, S, Dar, AM, Nagaraja, KV, Shaw, DP, Halvorson, DA and Kapur, V (2000). Isolation of avian pneumovirus from an outbreak of respiratory illness in Minnesota turkeys. Journal of Veterinary Diagnostic Investigation 12: 166168.CrossRefGoogle ScholarPubMed
Grant, M and Baxter-Jones, C (1987). An enzyme-linked immunosorbent assay for the serodiagnosis of turkey rhinotracheitis infection. Veterinary Record 120: 279280.CrossRefGoogle ScholarPubMed
Gulati, BR, Cameron, KT, Seal, BS, Goyal, SM, Halvorson, DA and Njenga, MK (2000). Development of highly sensitive and specific enzyme-linked immunosorbent assay based on recombinant matrix protein for detection of avian pneumovirus. Journal of Clinical Microbiology 38: 40104014.CrossRefGoogle ScholarPubMed
Gulati, BR, Munir, S, Patnayak, DP, Goyal, SM and Kapur, V (2001). Detection of antibodies to US Isolates of avian pneumovirus by recombinant nucleotide protein-based sandwich enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 39: 29672970.CrossRefGoogle Scholar
Gulati, BR, Patnayak, DP, Sheikh, AM, Poss, PE and Goyal, SM (2001). Protective efficacy of high-passage avian pneumovirus (APV/MN/turkey/1-a/97) in turkeys. Avian Diseases 45: 593597.CrossRefGoogle ScholarPubMed
Heffels-Redman, U, Neuman, U, Braune, S, Cook, JKA and Pruter, J (1998). Serological evidence for the susceptibility of sea gulls to avian pneumovirus (APV) infection. In: Kaleta, E and Heffels-Redman, U (editors). Proceedings of the International Symposium on Infectious Bronchitis and Pneumovirus Infections in Poultry,Rauischholshausen,Germany, pp. 2325.Google Scholar
Jing, L, Cook, JK, TDK Shaw, K and Cavanagh, D (1993). Detection of turkey rhinotracheitis virus in turkeys using polymerase chain reaction. Avian Pathology 22: 771783.CrossRefGoogle ScholarPubMed
Jirjis, FE, Noll, SL, Halvorson, DA, Nagaraja, KV, Townsend, EL, Sheikh, AM and Shaw, DP (2000). Avian pneumovirus infection in Minnesota turkeys: experimental reproduction of the disease. Avian Diseases 44: 222226.CrossRefGoogle ScholarPubMed
Jirjis, FE, Noll, SL, Martin, F, Halvorson, DA, Nagaraja, KV and Shaw, DP (2001). Vaccination of turkeys with an avian pneumovirus isolate from the United States. Avian Diseases 45: 10061013.CrossRefGoogle ScholarPubMed
Jirjis, FE, Noll, SL, Halvorson, DA, Nagaraja, KV, Townsend, EL and Shaw, DP (2002). Pathogenesis of avian pneumovirus infection in turkeys. Veterinary Pathology 39: 300301.CrossRefGoogle ScholarPubMed
Jones, RC, Naylor, CJ, al-Afaleq, A, Worthington, KJ and Jones, R (1992). Effect of cyclophosphamide on the immunosuppression on the immunity of turkeys to viral rhinotracheitis. Research in Veterinary Science 53: 3841.CrossRefGoogle ScholarPubMed
Juhasz, K and Easton, AJ (1994). Extensive sequence variation in the attachment (G) protein gene of avian pneumovirus: evidence for two distinct subgroups. Journal of General Virology 75: 28732880.CrossRefGoogle ScholarPubMed
Kleven, SH (1997). Report of the Committee. Transmissible Diseases of Poultry and Other Avian Species. In: Proceedings of US Animal Health Association. 101st Annual meeting,Richmond, Va.Pat Campbell and Associates and Spectrum Press, pp.486491.Google Scholar
Lauer, DC (2001). Incidence of avian pneumovirus. In: Minnesota Poultry Testing Laboratory Monthly Report. Wilmar (MN): Minnesota Board of Animal Health.Google Scholar
Li, J, Cook, JKA, Brown, DK, Kathleen, S and Cavanagh, D (1993). Detection of turkey rhinotracheitis virus in turkeys using polymerase chain reaction. Avian Pathology 22: 771783.Google Scholar
Ling, R, Easton, AJ and Pringle, CR (1992). Sequence analysis of the 22K, SH and G genes of turkey rhinotracheitis virus and their intergenic regions reveal a gene order different from that of other pneumoviruses. Journal of General Virology 73: 17091715.CrossRefGoogle Scholar
Lwamba, HCM, Halvorson, DA, Nagaraja, KV, Turpin, EA, Swayne, D, Seal, BS and Njenga, MK (2002). Antigenic cross-reactivity among avian pneumoviruses of subgroups A, B, and C at the matrix but not nucleocapsid proteins. Avian Diseases 46: 725729.CrossRefGoogle Scholar
Mase, M, Asahi, S, Imai, K, Nakamura, K and Yamaguchi, S (1996). Detection of turkey rhinotracheitis from chickens with swollen head syndrome by reverse transcriptase–polymerase chain reaction (RT-PCR). Journal of Veterinary Medical Science 58: 359361.CrossRefGoogle ScholarPubMed
McDougall, JS and Cook, JKA (1986). Turkey rhinotracheitis: preliminary investigations. Veterinary Record 118: 206207.CrossRefGoogle ScholarPubMed
Naylor, CJ and Jones, RC (1993). Turkey rhinotracheitis: a review. Veterinary Bulletin 63: 339349.Google Scholar
Naylor, CJ, Al-Ankari, A, al-Afaleq, A, Bradbury, J and Jones, R (1992). Exacerbation of Mycoplasma gallisepticum infection in turkeys by rhinotracheitis virus. Avian Pathology 21: 295305.CrossRefGoogle ScholarPubMed
Naylor, CJ, Worthington, KJ and Jones, RC (1997). Failure of maternal antibodies to protect young turkey poults against challenge with turkey rhinotracheitis. Avian Diseases 41: 968971.CrossRefGoogle ScholarPubMed
Nissen, MD, Siebert, DJ, Mackay, IM, Sloots, TP and Withers, SJ (2002). Evidence of human metapneumovirus in Australian children. Medical Journal of Australia 176: 188.CrossRefGoogle ScholarPubMed
Panigrahy, B, Senne, DA, Pedersen, JC, Gidlewski, T and Edson, RK (2000). Experimental and serologic observations on avian pneumovirus (APV/turkey/Colorado/97) infection in turkeys. Avian Diseases 44: 1722.CrossRefGoogle ScholarPubMed
Patnayak, DP, Sheik, AM, Gulati, BR and Goyal, SM (2002). Experimental and field evaluation of a live vaccine against avian pneumovirus. Avian Pathology 31: 377382.CrossRefGoogle ScholarPubMed
Peret, TCT, Boivin, G, Li, Y, Couillard, M, Humphrey, C, Osterhaus, ADME, Erdman, DD and Anderson, LJ (2002). Characterization of human metapneumoviruses isolated from patients in North America. Journal of Infectious Diseases 185: 16601663.CrossRefGoogle ScholarPubMed
Picault, JP, Giraud, P, Guittet, M, Bennejean, G, Lamande, J, Toquin, D and Gueguen, C (1987). Isolation of a TRTV-like virus from chickens with swollen head syndrome. Veterinary Record 121: 135.CrossRefGoogle ScholarPubMed
Pringle, CR (1998). Virus taxonomy—San Diego 1998. Archives of Virology 143: 14491459.CrossRefGoogle ScholarPubMed
Qingzhong, Y, Barrett, T, Brown, TD, Cook, JKA, Green, P, Skinner, MA and Cavanagh, D (1994). Protection against turkey rhinotracheitis pneumovirus (TRTV) induced by a fowl pox virus recombinant expressing the TRTV fusion glycoprotein (F). Vaccine 12: 569573.CrossRefGoogle ScholarPubMed
Randhawa, JS, Marriott, AC, Pringle, CR and Easton, AJ (1997). Rescue of synthetic minireplicons establishes the absence of NS1 and NS2 genes from avian pneumovirus. Journal of Virology 71: 98499854.CrossRefGoogle ScholarPubMed
Seal, BS (1998). Matrix protein gene nucleotide and predicted amino acid sequence demonstrate that the first US avian pneumovirus isolate is distinct from European strains. Virus Research 58: 4552.CrossRefGoogle ScholarPubMed
Seal, BS (2000). Avian pneumoviruses and emergence of a new type in the United States of America. Animal Health Research Reviews 1: 6772.CrossRefGoogle ScholarPubMed
Senne, DA, Edson, RK, Pedersen, JC and Panigrahy, B (1997). Avian pneumovirus update. In: Proceedings of 134th Annual Conference.Schaumburg, Illinois:American Veterinary Medical Association, p. 190.Google Scholar
Shin, HJ, Njenga, MK, McComb, B, Halvorson, DA and Nagaraja, KV (2000). Avian pneumovirus RNA from wild and sentinel birds in the US has genetic homology with APV isolates from domestic turkeys. Journal of Clinical Microbiology 38: 42824284.CrossRefGoogle Scholar
Shin, HJ, Rajashekara, G, Jirjis, FF, Shaw, DP, Goyal, SM, Halvorson, DA and Nagaraja, KV (2000). Specific detection of avian pneumovirus (APV) US isolates by RT-PCR. Archives of Virology 145: 12391246.CrossRefGoogle ScholarPubMed
Shin, HJ, Nagaraja, KV, McComb, B, Halvorson, DA, Jirjis, FF, Shaw, DP, Seal, BS and Njenga, MK (2002). Isolation of avian pneumovirus from mallard ducks that is genetically similar to viruses isolated from neighboring commercial turkeys. Virus Research 83: 207212.CrossRefGoogle ScholarPubMed
Shin, HJ, Cameron, KT, Jacobs, JA, Turpin, EA, Halvorson, DA, Goyal, SM, Nagaraja, KV, Mahesh, CK, Lauer, DC, Seal, BS and Njenga, MK (2002). Molecular epidemiology of subgroup C avian pneumoviruses isolated from the United States and comparison with subgroup A and B viruses. Journal of Clinical Microbiology 40: 16871693.CrossRefGoogle ScholarPubMed
Stuart, JC (1989). Turkey rhinotracheitis (TRT) in Great Britain. In: Nixey, C and Grey, TC (editors). Recent Advances in Turkey Science. Poultry Science Symposium. London: World's Poultry Science Association and Working Group No. 10 of the European Federation of the Association. Series No. 21, pp. 217224.Google Scholar
Tanaka, M, Kokumai, N, Obi, T, Higashihara, R, Takuma, H, Hiramatsu, K and Shimizu, Y (1996). A serological survey of turkey rhinotracheitis infection in chicken in Japan. Journal of Veterinary Medical Science 58: 689691.CrossRefGoogle ScholarPubMed
Tanaka, M, Takuma, H, Kokumai, N, Oishi, E, Obi, T, Hiramatsu, K and Shimizu, Y (1995). Turkey rhinotracheitis virus isolated from broiler chicken with swollen head syndrome in Japan. Journal of Veterinary Medical Science 57: 939941.CrossRefGoogle ScholarPubMed
Timms, LM, Jahans, KL and Marshall, RN (1986). Evidence of immunosuppression in turkey poults affected by rhinotracheitis. Veterinary Record 119: 9192.CrossRefGoogle ScholarPubMed
Toquin, D, Bayon-Auboyer, MH, Eteradossi, N and Jestin, V (1999). Isolation of a pneumovirus from a Muscovy duck. Veterinary Record 145: 680.Google ScholarPubMed
Townsend, E, Halvorson, DA, Nagaraja, KV and Shaw, DP (2000). Susceptibility of an avian pneumovirus isolated from Minnesota turkeys to physical and chemical agents. Avian Diseases 44: 336342.CrossRefGoogle ScholarPubMed
Turpin, EA, Perkins, LE and Swayne, D (2001). Experimental infection of turkeys with avian pneumovirus and either Newcastle disease virus or Escherichia coli. Avian Diseases 46: 412422.CrossRefGoogle Scholar
van den Hoogen, BG, DeJong, JC, Groen, J, Kuiken, T, De Groot, R, Fouchier, RAM and Osterhaus, ADME (2001). A newly discovered human metapneumovirus isolated from young children with respiratory tract disease. Nature Medicine 7: 719724.CrossRefGoogle ScholarPubMed
van den Hoogen, BG, Bestebroer, TM, Osterhaus, ADME and Foucher, RAM (2002). Analysis of genome sequence of human metapneumovirus. Virology 295: 119132.CrossRefGoogle ScholarPubMed
van der Veen, RC (2001). Nitric oxide and T-helper cell immunity. International Immunopharmacology 1: 14911500.CrossRefGoogle ScholarPubMed
Weisman, Y, Strengel, C, Blumenkranz, R and Segal, Y (1988). Turkey rhinotracheitis (TRT) in turkey flocks in Israel—virus isolation and serological response. Proceedings of 37th Western Poultry Disease Conference,Davis, CA, pp. 6769.Google Scholar
Wilding, GP, Baxter-Jones, C and Grant, M (1986). Ciliostatic agent found in rhinotracheitis. Veterinary Record 118: 735.CrossRefGoogle ScholarPubMed
Williams, RA, Savage, CE and Jones, RC (1991). Development of a live attenuated vaccine against turkey rhinotracheitis. Avian Pathology 20: 4555.CrossRefGoogle ScholarPubMed
Wyeth, PJ, Gough, RE and Collins, MS (1987). Antibodies to TRT in chicken with swollen head syndrome. Veterinary Record 120: 286287.CrossRefGoogle ScholarPubMed
Yu, Q, Davis, PJ, Li, J and Cavanagh, D (1992). Cloning and sequencing of the matrix protein (M) gene of turkey rhinotracheitis virus reveal a gene order different from that of respiratory syncytial virus. Virology 186: 426434.CrossRefGoogle ScholarPubMed