Pigeon Rotavirus A as the cause of systemic infection in juvenile pigeons (young pigeon disease)

Abstract

Recent investigations suggested pigeon associated Rotavirus Typ A genotype G18P[17] (RVA) as a causative agent of the classical ‘young pigeon disease’ (YPD). YPD was first described in the late 1980 s as an acute, mainly seasonally recurring disorder of mostly juvenile domestic pigeons (Columba livia) with clinical signs such as anorexia, dairrhea, vomiting, congested crops, weight loss and occasionally mortality. Various studies in the past indicated a multifactorial nature of YPD. Several pathogens, such as pigeon circovirus 1, avian adenoviruses and Escherichia coli were also suggested, but none of these could reproduce the disease experimentally. However, the impact of other pathogens on the clinical development of YPD cannot be excluded and requires further investigation. This present review summarizes available information on RVA-induced disease in pigeons, its association with YPD, the transmission, and diagnosis of the infection, and on prophylactic strategies to prevent RVA outbreaks.

Zusammenfassung

Jüngst veröffentlichte Studien belegen, dass Rotavirus A des Genotyps G18P[17] (RVA) Erkrankungen hervorrufen kann, die dem klinischen Bild der Jungtaubenkrankheit (JTK) entsprechen. Bei der Jungtaubenkrankheit handelt es sich um eine meist saisonal wiederkehrende Erkrankung junger Haustauben, die erstmals Ende der 1980er Jahre beschrieben wurde und durch Appetitlosigkeit, Durchfall, Erbrechen, mit Futter und Wasser angestaute Kröpfe sowie Gewichtsverlust und eine hohe Mortalität gekennzeichnet ist. In der Vergangenheit wurde spekuliert, dass es sich bei der JTK um ein multifaktorielles Krankheitsgeschehen handeln könnte. Tauben-Circovirus 1, Adenoviren und Escherichia coli wurden beispielsweise als potenziell beteiligte Erreger diskutiert. Ein epidemiologischer Zusammenhang oder eine Reproduktion des Krankheitsbildes konnte jedoch nicht belegt werden. Ein Einfluss anderer Erreger auf den Verlauf der YPD kann jedoch zum jetzigen Zeitpunkt nicht ausgeschlossen werden und bedarf weiterer Untersuchungen.

Dieser Übersichtsartikel fasst die bisherigen Kenntnisse zur Geschichte der JTK, das durch Rotavirus Typ A induzierte Krankheitsbild, Übertragungsmöglichkeiten des RVA sowie Diagnose und Präventionsstrategien zur Vorbeugung von RVA-Ausbrüchen zusammen.

Key words

Pigeon-type Rotavirus A - young pigeon disease - mortality - transmission - vaccines - lineages

Schlüsselwörter

Taubentyp Rotavirus A - Jungtaubenkrankheit - Mortalität - Transmission - Impfung - Lineages

Publication History

Received: 07 July 2021

Accepted: 15 March 2022

Article published online:
06 September 2022

• References

• 1 Raue R, Schmidt V, Freick M. et al. A disease complex associated with pigeon circovirus infection, young pigeon disease syndrome. Avian Pathol 2005; 34: 418-425 DOI: 10.1080/03079450500267825.
• 2 Scullion FT, Scullion MG. Pathologic findings in racing pigeons (Columba livia domestica) with „young bird sickness“. J Avian Med Surg 2007; 21: 1-7 DOI: 10.1647/1082-6742(2007)21[1:PFIRPC]2.0.CO;2.
• 3 Rubbenstroth D, Mohr L. Pigeon-type Rotavirus A (RVA) G18P[17] causes ‘young pigeon disease syndrome’ (YPDS). In: Błaszczak B, Adamczyk K. eds 1st World Congress of the International Veterinary Pigeons Association: current problems in columbpathology. 1 ed.. Warsaw: Warsaw Chamber of Veterinary Medicine; 2020: 43-44
• 4 Rubbenstroth D, Peus E, Schramm E. et al. Identification of a novel clade of group A rotaviruses in fatally diseased domestic pigeons in Europe. Transbound Emerg Dis 2019; 66: 552-561 DOI: 10.1111/tbed.13065.
• 5 Schmidt V, Kumpel M, Cramer K. et al. Pigeon rotavirus A genotype G18P[17]-associated disease outbreaks after fancy pigeon shows in Germany – a case series. Tierarztl Prax Ausg K Kleintiere Heimtiere 2021; 49: 22-27 DOI: 10.1055/a-1339-0366.
• 6 Schmidt V, Schlomer J, Luken C. et al. Experimental infection of domestic pigeons with pigeon circovirus. Avian Dis 2008; 52: 380-386 DOI: 10.1637/8188-120407-Reg.
• 7 Zhang Z, Dai W, Wang S. et al. Epidemiology and genetic characteristics of pigeon circovirus (PiCV) in eastern China. Arch Virol 2015; 160: 199-206 DOI: 10.1007/s00705-014-2255-4.
• 8 Teske L, Rubbenstroth D, Meixner M. et al. Identification of a novel aviadenovirus, designated pigeon adenovirus 2 in domestic pigeons (Columba livia). Virus Res 2017; 227: 15-22 DOI: 10.1016/j.virusres.2016.09.024.
• 9 Stenzel TA, Pestka D, Tykalowski B. et al. Epidemiological investigation of selected pigeon viral infections in Poland. Vet Rec 2012; 171: 562 DOI: 10.1136/vr.100932.
• 10 Hess M, Prusas C, Monreal G. Growth analysis of adenoviruses isolated from pigeons in chicken cells and serological characterization of the isolates. Avian Pathol 1998; 27: 196-199 DOI: 10.1080/03079459808419323.
• 11 Capita R, Cordero J, Molina-Gonzalez D. et al. Phylogenetic Diversity, Antimicrobial Susceptibility and Virulence Characteristics of Escherichia coli Isolates from Pigeon Meat. Antibiotics (Basel) 2019; 8 DOI: 10.3390/antibiotics8040259.
• 12 Santos HM, Chen CC, Tsai CY. et al. Influence of pigeon interferon alpha (PiIFN-alpha) on pigeon circovirus (PiCV) replication and cytokine expression in Columba livia. Vet Microbiol 2020; 242: 108591 DOI: 10.1016/j.vetmic.2020.108591.
• 13 Stenzel T, Dziewulska D, Tykalowski B. et al. The Clinical Infection with Pigeon Circovirus (PiCV) Leads to Lymphocyte B Apoptosis But Has No Effect on Lymphocyte T Subpopulation. Pathogens 2020; 9 DOI: 10.3390/pathogens9080632.
• 14 McCowan C, Crameri S, Kocak A. et al. A novel group A rotavirus associated with acute illness and hepatic necrosis in pigeons (Columba livia), in Australia. PLoS One 2018; 13: e0203853 DOI: 10.1371/journal.pone.0203853.
• 15 Hunnam JC, Sloan S, McCowan CI. et al. The racing pigeon (Columba livia domestica) industry in Victoria, Australia, and epidemiology of a novel Group A rotavirus outbreak. Transbound Emerg Dis 2019; 66: 2058-2066 DOI: 10.1111/tbed.13254.
• 16 Rubbenstroth D, Ulrich R, Wylezich C. et al. First experimental proof of Rotavirus A (RVA) genotype G18P[17] inducing the clinical presentation of ‚young pigeon disease syndrome‘ (YPDS) in domestic pigeons (Columba livia). Transbound Emerg Dis 2020; 67: 1507-1516 DOI: 10.1111/tbed.13485.
• 17 Matthijnssens J, Otto PH, Ciarlet M. et al. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 2012; 157: 1177-1182 DOI: 10.1007/s00705-012-1273-3.
• 18 Dhama K, Saminathan M, Karthik K. et al. Avian rotavirus enteritis – an updated review. Vet Q 2015; 35: 142-158 DOI: 10.1080/01652176.2015.1046014.
• 19 Martella V, Banyai K, Matthijnssens J. et al. Zoonotic aspects of rotaviruses. Vet Microbiol 2010; 140: 246-255 DOI: 10.1016/j.vetmic.2009.08.028.
• 20 Schumann T, Hotzel H, Otto P. et al. Evidence of interspecies transmission and reassortment among avian group A rotaviruses. Virology 2009; 386: 334-343 DOI: 10.1016/j.virol.2009.01.040.
• 21 Ward RL, McNeal MM. VP6: A candidate rotavirus vaccine. J Infect Dis 2010; 202  Suppl: S101-107 DOI: 10.1086/653556.
• 22 Estes MK, Kapikian AZ. Rotaviruses. In: Knipe DM, Howley PM, Griffin DE. et al., Hrsg. Fields Virology. 5. Aufl.. Philadelphia: Lippincott Williams & Wilkins, Wolters Kluwer; 2007: 1917-1974
• 23 Day JM. Rotavirus Infections. In: Swayne DE. Hrsg. Diseases of Poultry. 14. Aufl.. Hoboken: Wiley-Blackwell; 2020: 408-415
• 24 Sadiq A, Bostan N, Yinda KC. et al. Rotavirus: Genetics, pathogenesis and vaccine advances. Rev Med Virol 2018; 28: e2003 DOI: 10.1002/rmv.2003.
• 25 Matthijnssens J, Ciarlet M, McDonald SM. et al. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 2011; 156: 1397-1413 DOI: 10.1007/s00705-011-1006-z.
• 26 Matthijnssens J, Ciarlet M, Rahman M. et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 2008; 153: 1621-1629 DOI: 10.1007/s00705-008-0155-1.
• 27 Pauly M, Oni OO, Sausy A. et al. Molecular epidemiology of Avian Rotaviruses Group A and D shed by different bird species in Nigeria. Virol J 2017; 14: 111 DOI: 10.1186/s12985-017-0778-5.
• 28 Phan TG, Vo NP, Boros A. et al. The viruses of wild pigeon droppings. PLoS One 2013; 8: e72787 DOI: 10.1371/journal.pone.0072787.
• 29 Blakey J, Crossley B, Rosenberger JK. et al. Rotavirus A Associated with Clinical Disease and Hepatic Necrosis in California Pigeons (Columba livia domestica). Avian Dis 2019; 63: 651-658 DOI: 10.1637/aviandiseases-D-19-00114.
• 30 McDonald SM, Nelson MI, Turner PE. et al. Reassortment in segmented RNA viruses: mechanisms and outcomes. Nat Rev Microbiol 2016; 14: 448-460 DOI: 10.1038/nrmicro.2016.46.
• 31 Mori Y, Borgan MA, Takayama M. et al. Roles of outer capsid proteins as determinants of pathogenicity and host range restriction of avian rotaviruses in a suckling mouse model. Virology 2003; 316: 126-134 DOI: 10.1016/j.virol.2003.08.006.
• 32 Minamoto N, Oki K, Tomita M. et al. Isolation and characterization of rotavirus from feral pigeon in mammalian cell cultures. Epidemiol Infect 1988; 100: 481-492 DOI: 10.1017/s0950268800067212.
• 33 Hansen RDE, Stidworthy MF, Jones R. et al. Rotavirus infection in a racing pigeon (Columba livia) in Great Britain during 2018. Veterinary Record Case Reports 2020; 8: 1-4 DOI: 10.1136/vetreccr-2020-001218.
• 34 Harzer M, Heenemann K, Sieg M. et al. Prevalence of pigeon rotavirus infections: animal exhibitions as a risk factor for pigeon flocks. Arch Virol 2021; 166: 65-72 DOI: 10.1007/s00705-020-04834-w.
• 35 Gough RE, Cox WJ, Devoy J. Isolation and identification of rotavirus from racing pigeons. Vet Rec 1992; 130: 273 DOI: 10.1136/vr.130.13.273.
• 36 Vindevogel HU, Dagenais L, Lansival B. et al. Incidence of rotavirus, adenovirus and herpesvirus infection in pigeons. Vet Rec 1981; 109: 285-286 DOI: 10.1136/vr.109.13.285.
• 37 Marlier D, Vindevogel H. Viral infections in pigeons. Vet J 2006; 172: 40-51 DOI: 10.1016/j.tvjl.2005.02.026.
• 38 Santos HM, Tsai CY, Catulin GEM. et al. Common bacterial, viral, and parasitic diseases in pigeons (Columba livia): A review of diagnostic and treatment strategies. Vet Microbiol 2020; 247: 108779 DOI: 10.1016/j.vetmic.2020.108779.
• 39 Ramig RF. Systemic rotavirus infection. Expert Rev Anti Infect Ther 2007; 5: 591-612 DOI: 10.1586/14787210.5.4.591.
• 40 Desselberger U. Rotaviruses. Virus Res 2014; 190: 75-96 DOI: 10.1016/j.virusres.2014.06.016.
• 41 Payment P, Morin E. Minimal infective dose of the OSU strain of porcine rotavirus. Arch Virol 1990; 112: 277-282 DOI: 10.1007/BF01323172.
• 42 Graham DY, Dufour GR, Estes MK. Minimal infective dose of rotavirus. Arch Virol 1987; 92: 261-271 DOI: 10.1007/BF01317483.
• 43 Ramig RF. The effects of host age, virus dose, and virus strain on heterologous rotavirus infection of suckling mice. Microb Pathog 1988; 4: 189-202 DOI: 10.1016/0882-4010(88)90069-1.
• 44 Estes MK, Graham DY, Smith EM. et al. Rotavirus stability and inactivation. J Gen Virol 1979; 43: 403-409 DOI: 10.1099/0022-1317-43-2-403.
• 45 Guy JS. Virus infections of the gastrointestinal tract of poultry. Poult Sci 1998; 77: 1166-1175 DOI: 10.1093/ps/77.8.1166.
• 46 Ramig RF. Pathogenesis of intestinal and systemic rotavirus infection. J Virol 2004; 78: 10213-10220 DOI: 10.1128/JVI.78.19.10213-10220.2004.
• 47 Desselberger U, Gray J. Viral gastroenteritis. Medicine (Abingdon) 2005; 33: 78-81 DOI: 10.1383/medc.33.4.78.64361.
• 48 Dhama K, Chauhan RS, Mahendran M. et al. Rotavirus diarrhea in bovines and other domestic animals. Vet Res Commun 2009; 33: 1-23 DOI: 10.1007/s11259-008-9070-x.
• 49 McNulty MS, Allan GM, Todd D. et al. Isolation and cell culture propagation of rotaviruses from turkeys and chickens. Arch Virol 1979; 61: 13-21 DOI: 10.1007/BF01320587.
• 50 Antonissen G, Haesendonck R, Devreese M. et al. The Impact of Deoxynivalenol on Pigeon Health: Occurrence in Feed, Toxicokinetics and Interaction with Salmonellosis. PLoS One 2016; 11: e0168205 DOI: 10.1371/journal.pone.0168205.
• 51 Lawrie A. Pigeons: systemic and non-infectious diseases. In: Chitty J, Lierz M. Hrsg. BSAVA Manual of Raptors, Pigeons and Passerine Birds. 1. Aufl.. British Smal Animal Veterinary Association; 2008: 334-346
• 52 Vereecken M, de Herdt P, Ducatelle R. Adenovirus infections in pigeons: A review. Avian Pathol 1998; 27: 333-338 DOI: 10.1080/03079459808419348.
• 53 Zhao P, Ma J, Guo Y. et al. Isolation and characterization of a herpesvirus from feral pigeons in China. Vet J 2015; 206: 417-419 DOI: 10.1016/j.tvjl.2015.09.017.
• 54 Feng N, Burns JW, Bracy L. et al. Comparison of mucosal and systemic humoral immune responses and subsequent protection in mice orally inoculated with a homologous or a heterologous rotavirus. J Virol 1994; 68: 7766-7773 DOI: 10.1128/JVI.68.12.7766-7773.1994.
• 55 Mitchell DB, Both GW. Completion of the genomic sequence of the simian rotavirus SA11: nucleotide sequences of segments 1, 2, and 3. Virology 1990; 177: 324-331 DOI: 10.1016/0042-6822(90)90487-c.