e-ISSN 2231-8526
ISSN 0128-7680
Pertanika Journal of Science & Technology, Volume 46, Issue 3, August 2023
DOI: https://doi.org/10.47836/pjtas.46.3.14
Keywords: Distribution, pathology, swollen head syndrome, turkey rhinotracheitis, vaccine
Published on: 30 August 2023
Avian metapneumovirus (aMPV) is one of the respiratory viruses that cause global economic losses in poultry production systems. Therefore, it was important to design a comprehensive review article that gives more information about aMPV infection regarding the distribution, susceptibility, transmission, pathogenesis, pathology, diagnosis, and prevention. The aMPV infection is characterized by respiratory and reproductive disorders in turkeys and chickens. The disease condition is turkey rhinotracheitis in turkeys and swollen head syndrome in chickens. Infection with aMPV is associated with worldwide economic losses, especially in complications with other infections or poor environmental conditions. The genus Metapneumovirus is a single-stranded enveloped RNA virus and contains A, B, C, and D subtypes. Meat and egg-type birds are susceptible to aMPV infection. The virus can transmit through aerosol, direct contact, mechanical, and vertical routes. The disease condition is characterized by respiratory manifestations, a decrease in egg production, growth retardation, increasing morbidity rate, and sometimes nervous signs and a high mortality rate, particularly in concurrent infections. Definitive diagnosis of aMPV is based mainly on isolation and identification methods, detection of the viral DNA, as well as seroconversion. Prevention of aMPV infection depends on adopting biosecurity measures and vaccination using inactivated, live attenuated, and recombinant or DNA vaccines.
Abdel-Azeem, A.-A. S., Franzo, G., Zotte, A. D., Drigo, M., Catelli, E., Lupini, C., Martini, M., & Cecchinato, M. (2014). First evidence of avian metapneumovirus subtype A infection in turkeys in Egypt. Tropical Animal Health and Production, 46, 1093–1097. https://doi.org/10.1007/s11250-014-0591-8
Abdelmoez, N., Shawky, M., Abdelhady, H., Lebdah, M., & Salama, S. (2019). Isolation and identification of some possible causative agents of swollen head syndrome (SHS) in broiler chickens in Egypt. Slovenian Veterinary Research, 56(22-Suppl), 781–788. https://doi.org/10.26873/SVR-819-2019
Al-Hasan, B. A., Alhatami, A. O., Abdulwahab, H. M., Bustani, G. S., & Alkuwaity, E. A. W. (2021). The first isolation and detection of Ornithobacterium rhinotracheale from swollen head syndrome-infected broiler flocks in Iraq. Veterinary World, 14(9), 2346–2355. https://doi.org/10.14202/vetworld.2021.2346-2355
Al-Hasan, B. A., Alhatami, A. O., Abdulwahab, H. M., Bustani, G. S., Hameed, M. A., & Jawad, A. H. (2022). First report of Avian metapneumovirus type B in Iraqi broiler flocks with swollen head syndrome. Veterinary World, 15(1), 16–21. https://doi.org/10.14202/vetworld.2022.16-21
Ali, M. Z., Park, J.-E., & Shin, H.-J. (2019). Serological survey of avian metapneumovirus infection in chickens in Bangladesh. Journal of Applied Poultry Research, 28(4), 1330–1334. https://doi.org/10.3382/japr/pfz050
Alkahalaf, A. N., Ward, L. A., Dearth, R. N., & Saif, Y. M. (2002). Pathogenicity, transmissibility, and tissue distribution of avian pneumovirus in turkey poults. Avian Diseases, 46(3), 650–659. https://doi.org/10.1637/0005-2086(2002)046[0650:PTATDO]2.0.CO;2
Aly, M. M., El-Zaher, A. A., & Amin, A. (1997). Studies on swollen head syndrome in Egypt 1. Serological survey and comparison between two ELISA kits for detection of antibody. Veterinary Medical Journal Giza, 45(2), 251-258.
Arafa, A.-S., Mady, W., Hussein, A., Tamam, S., & Madbouly, H. (2015). Molecular characterization of vaccine-derived mutants of avian metapneumoviruses isolated from turkeys in Egypt. American Journal of Virology, 4(1), 1–11. https://doi.org/10.3844/ajvsp.2015.1.11
Aung, Y. H., Liman, M., Neumann, U., & Rautenschlein, S. (2008). Reproducibility of swollen sinuses in broilers by experimental infection with avian metapneumovirus subtypes A and B of turkey origin and their comparative pathogenesis. Avian Pathology, 37(1), 65–74. https://doi.org/10.1080/03079450701802222
Awad, F., Baylis, M., Jones, R. C., & Ganapathy, K. (2014). Evaluation of flinders technology associates cards for storage and molecular detection of avian metapneumoviruses. Avian Pathology, 43(2), 125–129. https://doi.org/10.1080/03079457.2014.885114
Awad, F., Forrester, A., Baylis, M., Lemiere, S., Jones, R., & Ganapathy, K. (2015). Immune responses and interactions following simultaneous application of live Newcastle disease, infectious bronchitis and avian metapneumovirus vaccines in specific-pathogen-free chicks. Research in Veterinary Science, 98, 127–133. https://doi.org/10.1016/j.rvsc.2014.11.004
Ball, C., Forrester, A., Herrmann, A., Lemiere, S., & Ganapathy, K. (2019). Comparative protective immunity provided by live vaccines of Newcastle disease virus or avian metapneumovirus when co-administered alongside classical and variant strains of infectious bronchitis virus in day-old broiler chicks. Vaccine, 37(52), 7566–7575. https://doi.org/10.1016/j.vaccine.2019.09.081
Banet-Noach, C., Simanov, L., & Perk, S. (2005). Characterization of Israeli avian metapneumovirus strains in turkeys and chickens. Avian Pathology, 34(3), 220–226. https://doi.org/10.1080/03079450500112625
Banet-Noach, C., Simanov, L., Laham-Karam, N., Perk, S., & Bacharach, E. (2009). Longitudinal survey of avian metapneumoviruses in poultry in Israel: Infiltration of field strains into vaccinated flocks. Avian Diseases, 53(2), 184–189. https://doi.org/10.1637/8466-090408-reg.1
Bäyon-Auboyer, M. H., Arnauld, C., Toquin, D., & 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(11), 2723–2733. https://doi.org/10.1099/0022-1317-81-11-2723
Bäyon-Auboyer, M. H., Jestin, V., Toquin, D., Cherbonnel, M., & Eterradossi, N. (1999). Comparison of F-, G- and N-based RT-PCR protocols with conventional virological procedures for the detection and typing of turkey rhinotracheitis virus. Archives of Virology, 144, 1091–1109. https://doi.org/10.1007/s007050050572
Bayraktar, E., Umar, S., Yilmaz, A., Turan, N., Franzo, G., Tucciarone, C. M., Cecchinato. M., Cakan, B., Iqbal, M., & Yilmaz, H. (2018). First molecular characterisation of avian metapneumovirus (aMPV) in Turkish broiler flocks. Avian Diseases, 62(4), 425–430. https://doi.org/10.1637/11915-061818-resnote.1
Bennett, R. S., LaRue, R., Shaw, D., Yu, Q., Nagaraja, K. V., Halvorson, D. A., & Njenga, M. K. (2005). A wild goose metapneumovirus containing a large attachment glycoprotein is avirulent but immunoprotective in domestic turkeys. Journal of Virology, 79(23), 14834-14842. https://doi.org/10.1128/jvi.79.23.14834-14842.2005
Bennett, R. S., Nezworski, J., Velayudhan, B. T., Nagaraja, K. V., Zeman, D. H., Dyer, N., Graham, T., Lauer, D. C., Njenga, M. K., & Halvorson, D. A. (2004). Evidence of avian pneumovirus spread beyond Minnesota among wild and domestic birds in central North America. Avian Diseases, 48(4), 902–908. https://doi.org/10.1637/7208-051804r
Bhattacharjee, P. S., Naylor, C. J., & Jones, R. C. (1994). A simple method for immunofluorescence staining of tracheal organ cultures for the rapid identification of infectious bronchitis virus. Avian Pathology, 23(3), 471–480. https://doi.org/10.1080/03079459408419017
Brown, P. A., Allée, C., Courtillon, C., Szerman, N., Lemaitre, E., Toquin, D., Mangart, J. M. M., Amelot, M., & Eterradossi, N. (2019). Host specificity of avian metapneumoviruses. Avian Pathology, 48(4), 311–318. https://doi.org/10.1080/03079457.2019.1584390
Buys, S. B., du Preez, J. H., & Els, H. J. (1989). The isolation and attenuation of a virus causing rhinotracheitis in turkeys in South Africa. Onderstepoort Journal of Veterinary Research, 56(2), 87–98.
Cadman, H. F., Kelly, P. J., Zhou, R., Davelaar, F., & Mason, P. R. (1994). A serosurvey using enzyme-linked immunosorbent assay for antibodies against poultry pathogens in ostriches (Struthio camelus) from Zimbabwe. Avian Diseases, 38(3), 621–625. https://doi.org/10.2307/1592088
Canuti, M., Kroyer, A. N. K., Ojkic, D., Whitney, H. G., Robertson, G. J., & Lang, A. S. (2019). Discovery and characterization of novel RNA viruses in aquatic North American wild birds. Viruses, 11(9), 768. https://doi.org/10.3390/v11090768
Catelli, E., Cecchinato, M., Savage, C. E., Jones, R. C., Naylor, C. J. (2006). Demonstration of loss of attenuation and extended field persistence of a live avian metapneumovirus vaccine. Vaccine, 24(42-43), 6476–6482. https://doi.org/10.1016/j.vaccine.2006.06.076
Catelli, E., Lupini, C., Cecchinato, M., Ricchizzi, E., Brown, P., & Naylor, C. J. (2010). Field avian Metapneumovirus evolution avoiding vaccine induced immunity. Vaccine, 28(4), 916– 921. https://doi.org/10.1016/j.vaccine.2009.10.149
Cecchinato, M., Lupini, C., Silveira, F., Listorti, V., Mescolini, G., Morandini, E., Franzo, G., & Catelli, E. (2018). Molecular characterization of avian metapneumovirus from Guinea fowls (Numida meleagridis). Pakistan Veterinary Journal, 38(4), 419–423. https://doi.org/10.29261/pakvetj/2018.088
Cha, R. M., Khatri, M., & Sharma, J. M. (2007). B-cell infiltration in the respiratory mucosa of turkeys exposed to subtype C avian metapneumovirus. Avian Diseases, 51(3), 764-770. https://doi.org/10.1637/0005-2086(2007)51[764:biitrm]2.0.co;2
Cha, R. M., Yu, Q., & Zsak, L. (2013). The pathogenicity of avian metapneumovirus subtype C wild bird isolates in domestic turkeys. Virology Journal, 10, 38. https://doi.org/10.1186/1743-422x-10-38
Chaboki, P. M., Ghalyanchilangeroudi, A., Karimi, V., Abdollahi, H., Maghsoudloo, H., Hosseini, H., Farahahni, R. K., Ghafouri, S. A., Falah, M. H., Rezaee, H., Jabbarifakhr, M., & Mousavi, F. S. (2018). Prevalence of avian metapneumovirus subtype B in live bird market in Gilan province, Iran. Veterinary Research Forum, 9(1), 93–97.
Chacón, J. L., Brandão, P. E., Buim, M., Villarreal, L., & Ferreira A. J. (2007). Detection by reverse transcriptase-polymerase chain reaction and molecular characterization of subtype B avian metapneumovirus isolated in Brazil. Avian Pathology, 36(5), 383–387. https://doi.org/10.1080/03079450701589142
Chacón, J. L., Mizuma, M., Vejarano, M. P., Toquín, D., Eterradossi, N., Patnayak, D. P., Goyal, S. M., & Ferreira, A. J. (2011). Avian metapneumovirus subtypes circulating in Brazilian vaccinated and non-vaccinated chicken and turkey farms. Avian Diseases, 55(1), 82–89. https://doi.org/10.1637/9501-081310-reg.1
Chary, P., Njenga, M. K., & Sharma, J. M. (2005). Protection by recombinant viral proteins against a respiratory challenge with virulent avian metapneumovirus. Veterinary Immunology and Immunopathology, 108(3-4), 427–432. https://doi.org/10.1016/j.vetimm.2005.06.012
Chary, P., Rautenschlein, S., & Sharma, J. M. (2002). Reduced efficacy of hemorrhagic enteritis virus vaccine in turkeys exposed to avian pneumovirus. Avian Diseases, 46(2), 353–359. https://doi.org/10.1637/0005-2086(2002)046[0353:reohev]2.0.co;2
Chary, P., Rautenschlein, S., Njenga, M. K., & Sharma, J. M. (2002). Pathogenic and immunosuppressive effects of avian pneumovirus in turkeys. Avian Diseases, 46(1), 153– 161. https://doi.org/10.1637/0005-2086(2002)046[0153:paieoa]2.0.co;2
Choi, K. S., Kim, J. W., Lee, E. K., Jeon, W. J., Park, M. J., Lyoo, Y. N., & Kwon, J. H. (2010). Development of competitive ELISA for detection of avian metapneumovirus antibodies in chicken. Journal of Bacteriology and Virology, 40(3), 131–143. http://doi.org/10.4167/jbv.2010.40.3.131
Cook, J. K. A. (2000). Avian pneumovirus infections of turkeys and chickens. The Veterinary Journal, 160(2), 118–125. https://doi.org/10.1053/tvjl.2000.0486
Cook, J. K. A., & Cavanagh, D. (2002). Detection and differentiation of avian pneumoviruses (metapneumoviruses). Avian Pathology, 31(2), 117–132. https://doi.org/10.1080/03079450120118603
Cook, J. K. A., Chesher, J., Orthel, F., Woods, M. A., Orbell, S. J., Baxendale, W., & Huggins, M. B. (2000). Avian pneumovirus infection of laying hens: Experimental studies. Avian Pathology, 29(6), 545–556. https://doi.org/10.1080/03079450020016788
Cook, J. K. A., Huggins, M. B., Orbell, S. J., & Senne, D. A. (1999). Preliminary antigenic characterization of an avian pneumovirus isolated from commercial turkeys in Colorado, USA. Avian Pathology, 28(6), 607–617. https://doi.org/10.1080/03079459994407
Cook, J. K. A., Huggins, M. B., Orbell, S. J., Mawditt, K., & Cavanagh, D. (2001). Infectious bronchitis virus vaccine interferes with the replication of avian pneumovirus vaccine in domestic fowl. Avian Pathology, 30(3), 233–242. https://doi.org/10.1080/03079450120054640
Cook, J. K. A., Huggins, M. B., Wood, M. A., Orbell, S. J., & Mockett, A. P. A. (1995). Protection provided by a commercially available vaccine against different strains of turkey rhinotracheitis virus. Veterinary Record, 136(15), 392–393. https://doi.org/10.1136/vr.136.15.392
Cook, J. K. A., Orthel, F., Orbell, S., Woods, M. A., & Huggins, M. B. (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, 25(2), 231–243. https://doi.org/10.1080/03079459608419138
Cook, J. K. A., Jones, B. V., Ellis, M. M., Jing, L., & Cavanagh, D. (1993). Antigenic differentiation of strains of turkey rhinotracheitis virus using monoclonal antibodies. Avian Pathology, 22(2), 257–273. https://doi.org/10.1080/03079459308418919
Coswig, L. T., dos Santos, M. B., Hafez, H. M., Ferreira, H. L., & Arns, C. W. (2010). Propagation of avian metapneumovirus subtypes A and B using chicken embryo related and other cell systems. Journal of Virological Methods, 167(1), 1–4. https://doi.org/10.1016/j.jviromet.2010.02.018
Croville, G., Foret, C., Heuillard, P., Senet, A., Delpont, M., Mouahid, M., Ducatez, M., Kichou, F., & Guerin, J. (2018). Disclosing respiratory co-infections: A broad-range panel assay for avian respiratory pathogens on a nanofluidic PCR platform. Avian Pathology, 47(3), 253–260. https://doi.org/10.1080/03079457.2018.1430891
Dani, M. A. C., Arns, C. W., & Durigon, E. L. (1999). Molecular characterization of Brazilian avian pneumovirus isolates using reverse transcription-polymerase chain reaction, restriction endonuclease analysis and sequencing of a G gene fragment. Avian Pathology, 28(5), 473–476. https://doi.org/10.1080/03079459994498
Darebaghi, A., Chashmi, S. H. E., Kafshdozan, K., & Hosseini, H. (2021). Molecular detection of avian metapneumovirus in Semnan broiler farms. Iranian Journal of Veterinary Medicine, 15(1), 27–34. https://doi.org/10.22059/ijvm.2020.302556.1005087
dos Santos, M. B, Martini M.C., Ferreira, H. L., da Silva, L. H., Fellipe, P. A., Spilki, F. R., & Arns, C.W. (2012). Brazilian avian metapneumovirus subtypes A and B: Experimental infection of broilers and evaluation of vaccine efficacy. Pesquisa Veterinária Brasileira, 32(12), 1257–1262. https://doi.org/10.1590/S0100-736X2012001200008
Felippe, P. A., Silva, L. H., Santos, M. B., Sakata, S. T., & Arns, C. W. (2011). Detection of and phylogenetic studies with avian metapneumovirus recovered from feral pigeons and wild birds in Brazil. Avian Pathology, 40(5), 445–452. https://doi.org/10.1080/03079457.2011.596812
Franzo, G., Legnardi, M., Mescolini, G., Tucciarone, C. M., Lupini, C., Quaglia, G., Catelli, E., & Cecchinato, M. (2020). Avian Metapneumovirus subtype B around Europe: A phylodynamic reconstruction. Veterinary Research, 51, 88. https://doi.org/10.1186%2Fs13567-020-00817-6
Franzo, G., Tucciarone, C. M., Enache, M., Bejan, V., Ramon, G., Koutoulis, K. C., & Cecchinato, M. (2017). First report of avian metapneumovirus subtype B field strain in a Romanian broiler flock during an outbreak of respiratory disease. Avian Diseases, 61(2), 250–254. https://doi.org/10.1637/11557-121216-resnote.1
Ganapathy, K., & Jones R. C. (2007). Vaccination of chicks with live attenuated subtype B avian metapneumovirus vaccines: Protection against challenge and immune responses can be unrelated to vaccine dose. Avian Diseases, 51(3), 733–737. https://doi.org/10.1637/0005-2086(2007)51[733:vocwla]2.0.co;2
Ganapathy, K., Bufton, A., Pearson, A., Lemiere, S., & Jones, R. C. (2010). Vaccination of commercial broiler chicks against avian metapneumovirus infection: A comparison of drinking water, spray and oculo-oral delivery methods. Vaccine, 28(23), 3944–3948. https://doi.org/10.1016/j.vaccine.2010.03.065
Ganapathy, K., Cargill, P., Montiel, E., & Jones, R. C. (2005). Interaction between live avian pneumovirus and Newcastle disease virus vaccines in specific pathogen free chickens. Avian Pathology, 34(4), 297–302. https://doi.org/10.1080/03079450500178824
Ganapathy, K., Cox, W. J., Gough, R. E., Cargill, P., Montiel, E., & Jones, R. C. (2007). Protection in specific pathogen free chickens with live avian metapneumovirus and Newcastle disease virus vaccines applied singly or in combination. Avian Pathology, 36(4), 313–317. https://doi.org/10.1080/03079450701460781
Gharaibeh, S. M., & Algharaibeh, G. R. (2007). Serological and molecular detection of avian pneumovirus in chickens with respiratory disease in Jordan. Poultry Science, 86(8), 1677–1681. https://doi.org/10.1093/ps/86.8.1677
Gharaibeh, S., & Shamoun, M. (2012). Avian metapneumovirus subtype B experimental infection and tissue distribution in chickens, sparrows, and pigeons. Veterinary Pathology, 49(4), 704–709. https://doi.org/10.1177/0300985811402845
Giraud, P., Bennejean, G., Guittet, M., & Toquin, D. (1986). Turkey rhinotracheitis in France: Preliminary investigations on a ciliostatic virus. Veterinary Record, 119(24), 606–607.
Gough, R. E., Drury, S. E., Aldous, E. W., & Laing, P. (2001). Isolation and identification of avian pneumovirus from pheasants. Veterinary Record, 149(10), 312.
Govindarajan, D., & Samal, S. K. (2004). Sequence analysis of the large polymerase (L) protein of the US strain of avian metapneumovirus indicates a close resemblance to that of the human metapneumovirus. Virus Research, 105(1), 59–66. https://doi.org/10.1016/j.virusres.2004.04.014
Graziosi, G., Mescolini, G., Silveira, F., Lupini, C., Tucciarone, C. M., Franzo, G., Cecchinato, M., Legnardi, M., Gobbo, F., Terregino, C., & Catelli, E. (2022). First detection of avian metapneumovirus subtype C Eurasian lineage in a Eurasian wigeon (Mareca penelope) wintering in Northeastern Italy: An additional hint on the role of migrating birds in the viral epidemiology. Avian Pathology, 51(3), 283–290. https://doi.org/10.1080/03079457.2022.2051429
Guionie, O., Toquin, D., Sellal, E., Bouley, S., Zwingelstein, F., Allee, C., Bougeard, S., Lemiere, S., & Eterradossi, N. (2007). Laboratory evaluation of a quantitative real-time reverse transcription PCR assay for the detection and identification of the four subgroups of avian metapneumovirus. Journal of Virological Methods, 139(2), 150–158. https://doi.org/10.1016/j.jviromet.2006.09.022
Hess, M., Huggins, M. B., & Heincz, U. (2004). Hatchability, serology and virus excretion following in ovo vaccination of chickens with an avian metapneumovirus vaccine. Avian Pathology, 33(6), 576–580. https://doi.org/10.1080/03079450400013220
Hosseini, H., & Ghalyanchi-Langeroudi, A. (2012). Detection and molecular characterization of avian metapneumovirus in Iran: The first report. Iranian Journal of Virology, 6(2), 26–31. https://doi.org/10.21859/isv.6.2.26
Hosseini, H., Ghalyanchilangeroudi, A., & Mousavi, F. S. (2017). Characterization of Iranian avian metapneumovirus based on fusion gene (F). Iranian Journal of Virology, 11(1), 39-43.
Hu, H., Roth J. P., Zsak, L., & Yu, Q. (2017). Engineered Newcastle disease virus expressing the F and G proteins of AMPV-C confers protection against challenges in turkeys. Scientific Reports, 7, 4025. https://doi.org/10.1038/s41598-017-04267-7
Hu, H., Roth, J. P., Estevez, C. N., Zsak, L., Liu, B., & Yu, Q. (2011). Generation and evaluation of a recombinant Newcastle disease virus expressing the glycoprotein (G) of avian metapneumovirus subgroup C as a bivalent vaccine in turkeys. Vaccine, 29(47), 8624–8633. https://doi.org/10.1016/j.vaccine.2011.09.007
Jardine, C. M., Parmley, E. J., Buchanan, T., Nituch, L., & Ojkic, D. (2018). Avian metapneumovirus subtype C in wild waterfowl in Ontario, Canada. Transboundary and Emerging Diseases, 65(4), 1098–1102. https://doi.org/10.1111/tbed.12832
Jirjis, F. F., Noll, S. L., Halvorson, D. A., Nagaraja, K. V., & Shaw, D. P. (2002). Pathogenesis of avian pneumovirus infection in turkeys. Veterinary Pathology, 39(3), 300–310. https://doi.org/10.1354/vp.39-3-300
Jirjis, F. F., Noll, S. L., Halvorson, D. A., Nagaraja, K. V., Martin, F., & Shaw, D. P. (2004). Effects of bacterial coinfection on the pathogenesis of avian pneumovirus infection in turkeys. Avian Diseases, 48(1), 34–49. https://doi.org/10.1637/7017
Jirjis, F. F., Noll, S. L., Halvorson, D. A., Nagaraja, K. V., Townsend, E. L., Sheikh, A. M., & Shaw, D. P. (2000). Avian pneumovirus infection in Minnesota turkeys: Experimental reproduction of the disease. Avian Diseases, 44(1), 222–226. https://doi.org/10.2307/1592530
Jones, R. C. (2010). Viral respiratory diseases (ILT, aMPV infections, IB): Are they ever under control? British Poultry Science, 51(1), 1–11. https://doi.org/10.1080/00071660903541378
Jones, R. C., Baxter-Jones, C., Savage, C. E., Kelly, D. F., & Wilding, G. P. (1987). Experimental infection of chickens with a ciliostatic agent isolated from turkeys with rhinotracheitis. Veterinary Record, 120(13), 301–302. https://doi.org/10.1136/vr.120.13.301
Jones, R. C., Naylor, C. J., Al-Afaleq, A., Worthington, K. J., & Jones, R. (1992). Effect of cyclophosphamide immunosuppression on the immunity of turkeys to viral rhinotracheitis. Research in Veterinary Science, 53(1), 38–41. https://doi.org/10.1016/0034-5288(92)90081-c
Jones, R. C., Naylor, C. J., Bradbury, J. M., Savage, C. E., Worthington, K., & Williams, R. A. (1991). Isolation of a turkey rhinotracheitis-like virus from broiler breeder chickens in England. Veterinary Record, 129(23), 509–510.
Jones, R. C., Williams, R. A., Baxter-Jones, C., Savage, C. E., & Wilding, G. P. (1988). Experimental infection of laying turkeys with rhinotracheitis virus: Distribution of virus in the tissues and serological response. Avian Pathology, 17(4), 841–850. https://doi.org/10.1080/03079458808436506
Kapczynski, D. R. (2004). Development of a virosome vaccine against avian metapneumovirus subtype C for protection in turkeys. Avian Diseases, 48(2), 332–343. https://doi.org/10.1637/7115
Kapczynski, D. R., & Sellers, H. S. (2003). Immunization of turkeys with a DNA vaccine expressing either the F or N gene of avian metapneumovirus. Avian Diseases, 47(4), 1376–1383. https://doi.org/10.1637/7033
Kapczynski, D. R., Perkins, L. L., & Sellers, H. S. (2008). Mucosal vaccination with formalin inactivated avian metapneumovirus subtype C does not protect turkeys following intranasal challenge. Avian Diseases, 52(1), 28–33. https://doi.org/10.1637/7821-122706-reg
Kuhn, J. H., Adkins, S., Agwanda, B. R., Al Kubrusli, R., Alkhovsky, S. V., Amarasinghe, G. K., Avšič-Županc, T., Ayllón, M. A., Bahl, J., Balkema-Buschmann, A., Ballinger, M. J., Basler, C. F., Bavari, S., Beer, M., Bejerman, N., Bennett, A. J., Bente, D. A., Bergeron, É., Bird, B. H., Blair, C. D., … Zhou, P. (2020). Taxonomic update for phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Archives of Virology, 165, 3023–3072. https://doi.org/10.1007/s00705-020-04731-2
Kwon, J.-S., Lee, H.-J., Jeong, S.-H., Park, J.-Y., Hong, Y.-H., Lee, Y.-J., & Song, C.-S. (2010). Isolation and characterization of avian metapneumovirus from chickens in Korea. Journal of Veterinary Science, 11(1), 59–66. https://doi.org/10.4142/jvs.2010.11.1.59
Legnardi, M., Allée, C., Franzo, G., Cecchinato, M., & Brown, P. (2021). Research Note: Detection of Avian metapneumovirus subgroup C specific antibodies in a mallard flock in Italy. Poultry Science, 100(7), 101186. https://doi.org/10.1016/j.psj.2021.101186
Lemaitre, E., Allée, C., Vabret, A., Eterradossi, N., & Brown P. A. (2018). Single reaction, real time RT-PCR detection of all known avian and human metapneumoviruses. Journal of Virological Methods, 251, 61–68. https://doi.org/10.1016/j.jviromet.2017.10.010
Liman, M., & Rautenschlein, S. (2007). Induction of local and systemic immune reactions following infection of turkeys with avian Metapneumovirus (aMPV) subtypes A and B. Veterinary Immunology and Immunopathology, 115(3-4), 273–285. https://doi.org/10.1016/j.vetimm.2006.12.001
Ling, R., & Pringle, C. R. (1988). Turkey rhinotracheitis virus: In vivo and in vitro polypeptide synthesis. Journal of General Virology, 69(4), 917–923. https://doi.org/10.1099/0022-1317-69-4-917
Listorti, V., Lupini, C., Cecchinato, M., Pesente, P., Rossi, G., Giovanardi, D., Naylor, C. J., & Catelli, E. (2014). Rapid detection of subtype B avian metapneumoviruses using RT-PCR restriction endonuclease digestion indicates field circulation of vaccine-derived viruses in older turkeys. Avian Pathology, 43(1), 51–56. https://doi.org/10.1080/03079457.2013.866212
Lupini, C., Cecchinato, M., Ricchizzi, E., Naylor, C. J., & Catelli, E. (2011). A turkey rhinotracheitis outbreak caused by the environmental spread of a vaccine-derived avian metapneumovirus. Avian Pathology, 40(5), 525–530. https://doi.org/10.1080/03079457.2011.607428
Lwamba, H. C. M., Alvarez, R., Wise, M. G., Yu, Q., Halvorson, D., Njenga, M. K., & Seal, B. S. (2005). Comparison of full-length genome sequence of Avian metapneumovirus subtype C with other paramyxoviruses. Virus Research, 107(1), 83–92. https://doi.org/10.1016/j.virusres.2004.07.002
Madbouly, H. M., Tamam, S. M., Hussein, A. S., Mady, W., & Arafa, A.-S. (2014). Immunomodular effect of fusion gene DNA vaccine of avian metapneumoviruses. Journal of Applied Poultry Research, 23(3), 478–485. https://doi.org/10.3382/japr.2014-00963
Majó, N., Allan, G. M., O’Loan, C. J., Pagès, A., & Ramis, A. J. (1995). A sequential histopathologic and immunocytochemical study of chickens, turkey poults, and broiler breeders experimentally infected with turkey rhinotracheitis virus. Avian Diseases, 39(4), 887–896. https://doi.org/10.2307/1592428
Marianna, A., Giovanni, F., Claudia, M. T., Zoi, P., Kostantinos, K., Mattia, C., & Ilias, C. (2019). Molecular epidemiology of infectious bronchitis virus and avian metapneumovirus in Greece. Poultry Science, 98(11), 5374–5384. https://doi.org/10.3382/ps/pez360
Mase, M., Yamaguchi, S., Tsukamoto, K., Imada, T., Imai, K., & Nakamura, K. (2003). Presence of avian pneumovirus subtypes A and B in Japan. Avian Diseases, 47(2), 481–484. https://doi.org/10.1637/0005-2086(2003)047[0481:poapsa]2.0.co;2
Mayahi, M., Momtaz, H., Jafari, R. A., & Zamani, P. (2017). Detection and subtyping avian metapneumovirus from turkeys in Iran. Veterinary Research Forum, 8(2), 105–108.
McDougall, J. S., & Cook, J. K. (1986). Turkey rhinotracheitis: Preliminary investigations. Veterinary Record, 118(8), 206–207. https://doi.org/10.1136/vr.118.8.206
Mernizi, A., Bouziane, S., Fathi, H., Criado, L.G., Bouslikhane, M., Ghram, A., Catelli, E., Mouahid, M., & Nassik, S. (2022). First seroepidemiological and risk factor survey of avian metapneumovirus circulation in Moroccan broiler farms. Veterinarski Glasnik, 77(1), 51-68. https://doi.org/10.2298/VETGL220307009M
Mescolini, G., Lupini, C., Franzo, G., Quaglia, G., Legnardi, M., Cecchinato, M., Tucciarone, C. M., Blanco, A., Turblin, V., Biarnés, M., Tatone, F., Falchieri, M., & Catelli, E. (2021). What is new on molecular characteristics of Avian metapneumovirus strains circulating in Europe? Transboundary and Emerging Diseases, 68(3), 1314–1322. https://doi.org/10.1111/tbed.13788
Mo, J., Angelichio, M., Gow, L., Leathers, V., & Jackwood, M. W. (2022). Quantitative real-time PCR assays for the concurrent diagnosis of infectious laryngotracheitis virus, Newcastle disease virus and avian metapneumovirus in poultry. Journal of Veterinary Science, 23(2), e21. https://doi.org/10.4142/jvs.21153
Morley, A. J., & Thomson, D. K., (1984). Swollen-head syndrome in broiler chickens. Avian Diseases, 28(1), 238–243.
Nagy, A., Abdallah, F., Sweed, K., Salama, A., & Omar, M. (2018). Seroprevelance of avian metapneumovirus in Egyptian chicken and duck flocks with a reference on economic impact. Journal of Virological Sciences, 4, 8–14.
Naylor, C. J., & Jones, R. C. (1993). Turkey rhinotracheitis: A review. Veterinary Bulletin, 63, 439–449.
Naylor, C. J., Shaw, K., Britton, P., & Cavanagh, D. (1997). Appearance of type B avian pneumovirus in Great Britain. Avian Pathology, 26(2), 327–338. https://doi.org/10.1080/03079459708419215
Naylor, C. J., Worthington, K. J., & Jones, R. C. (1997). Failure of maternal antibodies to protect young turkey poults against challenge with turkey rhinotracheitis virus. Avian Diseases, 41(4), 968–971. https://doi.org/10.2307/1592354
Ongor, H., Karahan, M., Kalin, R., Bulut, H., & Cetinkaya, B. (2010). Detection of avian metapneumovirus subtypes in turkeys using RT-PCR. Veterinary Record, 166(12), 363–366. https://doi.org/10.1136/vr.c1607
Owoade, A. A., Ducatez, M. F., & Muller, C. P. (2006). Seroprevalence of avian influenza virus, infectious bronchitis virus, reovirus, avian pneumovirus, infectious laryngotracheitis virus, and avian leukosis virus in Nigerian poultry. Avian Diseases, 50(2), 222–227. https://doi.org/10.1637/7412-071505r.1
Pedersen, J. C., Reynolds, D. L., & Ali, A. (2000). The sensitivity and specificity of a reverse transcriptase-polymerase chain reaction assay for the avian pneumovirus (Colorado strain). Avian Diseases, 44(3), 681–685. https://doi.org/10.2307/1593111
Pringle, C. R. (1998). Virus taxonomy — San Diego 1998. Archives of Virology, 143, 1449–1459. https://doi.org/10.1007/s007050050389
Qingzhong, Y., Barrett, T., Brown, T. D., Cook, J. K., Green, P., Skinner, M. A., & Cavanagh, D. (1994). Protection against turkey rhinotracheitis pneumovirus (TRTV) induced by a fowlpox virus recombinant expressing the TRTV fusion glycoprotein (F). Vaccine, 12(6), 569–573. https://doi.org/10.1016/0264-410x(94)90319-0
Rautenschlein, S., Aung, Y. H., & Haase, C. (2011). Local and systemic immune responses following infection of broiler-type chickens with avian Metapneumovirus subtypes A and B. Veterinary Immunology and Immunopathology, 140(1-2), 10–22. https://doi.org/10.1016/j.vetimm.2010.11.003
Retallack, H., Clubb, S., & DeRisi, J. L. (2019). Genome sequence of a divergent avian metapneumovirus from a monk parakeet (Myiopsitta monachus). Microbiology Resource Announcements, 8(16), e00284-19. https://doi.org/10.1128/mra.00284-19
Rizotto, L. S., Simão, R. M., Scagion, G. P., Simasaki, A. A., Caserta, L. C., Benassi, J. C., Arns, C. W., & Ferreira, H. L. (2019). Detection of avian metapneumovirus subtype A from wild birds in the state of São Paulo. Brazilian Journal of Veterinary Research, 39(3), 209–213. https://doi.org/10.1590/1678-5150-PVB-6021
Roussan, D. A., Haddad, R., & Khawaldeh, G. (2008). Molecular survey of avian respiratory pathogens in commercial broiler chicken flocks with respiratory diseases in Jordan. Poultry Science, 87(3), 444–448. https://doi.org/10.3382/ps.2007-00415
Rubbenstroth, D., & Rautenschlein S. (2009). Investigations on the protective role of passively transferred antibodies against avian metapneumovirus infection in turkeys. Avian Pathology, 38(6), 427–436. https://doi.org/10.1080/03079450903349204
Seal, B. S. (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(1-2), 45–52. https://doi.org/10.1016/s0168-1702(98)00098-7
Seifi, S., & Boroomand, Z. (2015). The role of avian metapneumovirus in respiratory complex disease circulating in broilers in Northern Iran. Trakia Journal of Science, 13(2), 175–179. https://doi.org/10.15547/tjs.2015.02.011
Sheikhi, N., & Masoudian, A. (2011). Seroprevalence of avian metapneumovirus infection in some broiler breeder flocks of Iran. Journal of Comparative Pathobiology Iran, 8(1), 431–437.
Shin, H.-J., Cameron, K. T., Jacobs, J. A., Turpin, E. A., Halvorson, D. A., Goyal, S. M., Nagaraja, K. V., Kumar, M. C., Lauer, D. C., Seal, B. S., & Njenga, M. K. (2002). Molecular epidemiology of subgroup C avian pneumoviruses isolated in the United States and comparison with subgroup A and B viruses. Journal of Clinical Microbiology, 40, 1687–1693. https://doi.org/10.1128/jcm.40.5.1687-1693.2002
Shin, H.-J., Njenga, M. K., McComb, B., Halvorson, D. A., & Nagaraja. K. V. (2000). Avian pneumovirus (APV) RNA from wild and sentinel birds in the United States has genetic homology with RNA from APV isolates from domestic turkeys. Journal of Clinical Microbiology, 38(11), 4282–4284. https://doi.org/10.1128/jcm.38.11.4282-4284.2000
Shin, H.-J., Rajashekara, G. F., Jirjis, F., Shaw, D. P., Goyal, S. M., Halvorson, D. A., & Nagaraja, K. V. (2000). Specific detection of avian pneumovirus (APV) US isolates by RT-PCR. Archives of Virology, 145, 1239–1246. https://doi.org/10.1007/s007050070123
Sid, H., Benachour, K., & Rautenschlein, S. (2015). Co-infection with multiple respiratory pathogens contributes to increased mortality rates in Algerian poultry flocks. Avian Diseases, 59(3), 440–446. https://doi.org/10.1637/11063-031615-case.1
Śmiałek, M., Kowalczyk, J., Gesek, M., Kaczorek-Łukowska, E., Dziewulska, D., Tykałowski, B., & Koncicki, A. (2021). The influence of maternally derived antibodies on protection against aMPV/A infection in TRT vaccinated turkeys. Poultry Science, 100(5), 101086. https://doi.org/10.1016/j.psj.2021.101086
Śmiałek, M., Pestka, D., Tykałowski, B., Stenzel, T., & Koncicki, A. (2015). Development of vaccine-induced immunity against TRT in turkeys depends remarkably on the level of maternal antibodies and the age of birds on the day of vaccination. BMC Veterinary Research, 11, 28. https://doi.org/10.1186/s12917-015-0345-5
Śmiałek, M., Tykałowski, B., Dziewulska, D., Kowalczyk, J., & Koncicki, A. (2020). IFNγ production profile in turkeys of different immunological status after TRT vaccination. Journal of Veterinary Research, 64(2), 239–245. https://doi.org/10.2478%2Fjvetres-2020-0040
Śmiałek, M., Tykałowski, B., Pestka, D., Welenc, J., Stenzel, T., & Koncicki, A. (2016). Three-step Anti-aMPV IgA expression profile evaluation in turkeys of different immunological status after TRT vaccination. Polish Journal of Veterinary Sciences, 19(3), 509–518. https://doi.org/10.1515/pjvs-2016-0064
Sugiyama, M., Koimaru, H., Shiba, M., Ono, E., Nagata, T., & Ito, T. (2006). Drop in egg production in chickens by experimental infection with avian metapneumovirus strain PLE8T1 derived from swollen head syndrome and the application to evaluate vaccine. Journal of Veterinary Medical Science, 68(8), 783–787. https://doi.org/10.1292/jvms.68.783
Sun, J., Wei, Y., Rauf, A., Zhang, Y., Ma, Y., Zhang, X., & Li, J. (2014). Methyltransferase-defective avian metapneumovirus vaccines provide complete protection against challenge with the homologous Colorado strain and the heterologous Minnesota strain. Journal of Virology, 88(21), 12348–12363. https://doi.org/10.1128/jvi.01095-14
Sun, S., Chen, F., Cao, S., Liu, J., Lei, W., Li, G., Song, Y., Lu, J., Liu, C., Qin, J., & Li, H. (2014). Isolation and characterization of a subtype C avian metapneumovirus circulating in Muscovy ducks in China. Veterinary Research, 45, 74. https://doi.org/10.1186/s13567-014-0074-y
Tamam, S. M., Hussein, A. S., Arafa, A. M., & Madbouly, H. M. (2015). Preparation and evaluation of inactivated avian Metapneumovirus vaccine from recently isolated Egyptian strain. Journal of Applied Poultry Research, 24(2), 168–176. https://doi.org/10.3382/japr/pfv019
Timms, L. M., Jahans, K. L., & Marshall, R. N. (1986). Evidence of immunosuppression in turkey poults affected by rhinotracheitis. Veterinary Record, 119(4), 91–92. https://doi.org/10.1136/vr.119.4.91
Toquin, D., Eterradossi, N., & Guittet, M. (1996). Use of a related ELISA antigen for efficient TRT serological testing following live vaccination. Veterinary Record, 139(3), 71–72. https://doi.org/10.1136/vr.139.3.71
Toquin, D., Guionie, O., Jestin, V., Zwingelstein, F., Allee, C., & Eterradossi, N. (2006). European and American subgroup C isolates of avian metapneumovirus belong to different genetic lineages. Virus Genes, 32, 97–103. https://doi.org/10.1007/s11262-005-5850-3
Townsend, E., Halvorson, D. A., Nagaraja, K. V., & Shaw, D. P. (2000). Susceptibility of an avian pneumovirus isolated from Minnesota turkeys to physical and chemical agents. Avian Diseases, 44(2), 336–342. https://doi.org/10.2307/1592548
Tucciarone, C. M., Andreopoulou, M., Franzo, G., Prentza, Z., Chaligiannis, I., & Cecchinato, M. (2017). First identification and molecular characterization of avian metapneumovirus subtype B from chickens in Greece. Avian Diseases, 61(3), 409–413. https://doi.org/10.1637/11631-032017-caser
Tucciarone, C. M., Franzo G., Lupini C., Alejo C. T., Listorti V., Mescolini G., Brandao P. E., Martini M., Catelli E., & Cecchinato M. (2018). Avian Metapneumovirus circulation in Italian broiler farms. Poultry Science, 97(2), 503–509. https://doi.org/10.3382/ps/pex350
Tucciarone, C. M., Franzo, G., Legnardi, M., Pasotto, D., Lupini, C., Catelli, E., Quaglia, G., Graziosi, G., Dal Molin, E., Gobbo, F., & Cecchinato, M. (2022). Molecular survey on A, B, C and new avian metapneumovirus (aMPV) subtypes in wild birds of northern-central Italy. Veterinary Science, 9(7), 373. https://doi.org/10.3390/vetsci9070373
Turpin, E. A., Stallknecht, D. E., Slemons, R. D., Zsak, L., & Swayne, D. E. (2008). Evidence of avian metapneumovirus subtype C infection of wild birds in Georgia, South Carolina, Arkansas and Ohio, USA. Avian Pathology, 37(3), 343–351. https://doi.org/10.1080/03079450802068566
Umar, S., Teillaud, A., Aslam, H. B., Guerin, J. L., & Ducatez, M. F. (2019). Molecular epidemiology of respiratory viruses in commercial chicken flocks in Pakistan from 2014 through to 2016. BMC Veterinary Research, 15, 351. https://doi.org/10.1186/s12917-019-2103-6
van Boheemen, S., Bestebroer, T. M., Verhagen, J. H., Osterhaus, A. D. M. E., Pas, S. D., Herfst, S., & Fouchier, R. A. M. (2012). A family-wide RT-PCR assay for detection of paramyxoviruses and application to a large-scale surveillance study. PLOS One, 7(4), e34961. https://doi.org/10.1371/journal.pone.0034961
Van de Zande, S., Nauwynck, H., Cavanagh, D., & Pensaert, M. (1998). Infections and reinfections with avian pneumovirus subtype A and B on Belgian turkey farms and relation to respiratory problems. Zentralblatt fur Veterinarmedizin Reihe B, 5(1-10), 621–626. https://doi.org/10.1111/j.1439-0450.1998.tb00835.x
Van de Zande, S., Nauwynck, H., Naylor, C., & Pensaert, M. (2000). Duration of cross-protection between subtypes A and B avian pneumovirus in turkeys. Veterinary Record, 147(5), 132–134. https://doi.org/10.1136/vr.147.5.132
Velayudhan, B. T., Lopes, V. C., Noll, S. L., Halvorson, D. A., & Nagaraja, K. V. (2003). Avian pneumovirus and its survival in poultry litter. Avian Diseases, 47(3), 764–768. https://doi.org/10.1637/7042
Velayudhan, B. T., McComb, B., Bennett, R. S., Lopes, V. C., Shaw, D., Halvorson, D. A., & Nagaraja, K. V. (2005). Emergence of a virulent type C avian metapneumovirus in turkeys in Minnesota. Avian Diseases, 49(4), 520–526. https://doi.org/10.1637/7388-052805r.1
Villarreal, L.Y., Brandão, P. E., Chacón, J. L., Assayag, M. S., Maiorka, P. C., Rafi, P., Saidenberg, A. B., Jones, R. C., & Ferreira, A. J. (2007). Orchitis in roosters with reduced fertility associated with avian infectious bronchitis virus and avian metapneumovirus infections. Avian Diseases, 51(4), 900–904. https://doi.org/10.1637/7815-121306-regr4.1
Wei, L., Zhu, S., Yan, X., Wang, J., Zhang, C., Liu, S., She, R., Hu, F., Quan, R., & Liu, J. (2013). Avian metapneumovirus subgroup C infection in chickens, China. Emerging Infectious Diseases, 19(7), 1092–1094. https://doi.org/10.3201/eid1907.121126
World Organisation for Animal Health. (2022). Turkey rhinotracheitis (avian metapneumovirus infections). WOAH. https://www.woah.org/fileadmin/Home/fr/Health_standards/tahm/3.03.15_TURKEY_RHRHI.pdf
Youssef, N. M. A., & Ahmed, M. H. H. (1996). Serological studies on flocks showing depressed egg production. Veterinary Medical Journal Giza, 44(4), 719–726.
Yu, M., Xing, L., Chang, F., Bao, Y., Wang, S., He, X., Wang, J., Wang, S., Liu, Y., Farooque, M., Pan, Q., Wang, Y., Gao, L., Qi, X., Hussain, A., Li, K., Liu, C., Zhang, Y., Cui, H., … Gao, Y. (2019). Genomic sequence and pathogenicity of the first avian metapneumovirus subtype B isolated from chicken in China. Veterinary Microbiology, 228, 32–38. https://doi.org/10.1016/j.vetmic.2018.11.009
Yu, Q., Roth, J. P., Hu, H., Estevez, C. N., Zhao, W., & Zsak, L. (2013). Protection by recombinant Newcastle disease viruses (NDV) expressing the glycoprotein (G) of avian metapneumovirus (aMPV) subtype A or B against challenge with virulent NDV and aMPV. World Journal of Vaccines, 3(4), 130–139. https://doi.org/10.4236/wjv.2013.34018
Zahirabadi, S. J., Akbariazad, G., Hosseini, H., Ghalavand, M., Tat, M., Hashemzadeh, M. S., & Dorostkar, R. (2017). Detection and molecular identification of avian metapneumovirus in commercial flocks of Qazvin. Bioscience Biotechnology Research Communications, 10(2), 100-104.
Zhang, L., Peeples, M. E., Boucher, R. C., Collins, P. L., & Pickles, R. J. (2002). Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. Journal of Virology, 76(11), 5654–5666. https://doi.org/10.1128/jvi.76.11.5654-5666.2002
Zhang, Y., Sun, J., Wei, Y., & Li, J. (2016). A reverse genetics approach for the design of methyltransferase-defective live attenuated avian metapneumovirus vaccines. In S. Thomas (Ed.), Vaccine design: Methods in molecular biology (Vol. 1404, pp. 103–121). Humana. https://doi.org/10.1007/978-1-4939-3389-1_7
Zuo, Z. H., Zhang, T. Y., Guo, Y. X., Chu, J., Qu, G. G., Miao, L. Z., & He, C. (2018). Serosurvey of Avian metapneumovirus, Orithobacterium rhinotracheale, and Chlamydia psittaci and their potential association with avian airsacculitis. Biomedical and Environmental Sciences, 31(5), 403–406. https://doi.org/10.3967/bes2018.053
ISSN 0128-7680
e-ISSN 2231-8526