Phylogenetic and pathogenic characterization of a pigeon paramyxovirus type 1 isolate reveals cross-species transmission and potential outbreak risks in the northwest region of China

Abstract

Pigeon paramyxovirus type-1 (PPMV-1) is enzootic in pigeons, causing severe economic loss in the poultry industry in many countries. However, the exact epidemic process of PPMV-1 transmission is still unclear. In this study, we analyzed the complete genome of the PPMV-1/SX-01/15 isolate. Sequence results show that the virus genome contains 15,192 nucleotides, with the gene order 3'-NP-P-M-F-HN-L-5'. Phylogenetic analysis revealed that this genome belongs to subgenotype VIc in class II. The mean death time (MDT) and intracerebral pathogenicity index (ICPI) were 62.4 h and 1.13, respectively, indicating that this isolate is a mesogenic PPMV-1 strain. To our knowledge, this is the first report of a subgenotype VIc mesogenic PPMV-1 strain circulating in commercial pigeon flocks in the northwest region of China. In a comparative infection experiment, the morbidity and mortality rates were 100% and 80%, respectively, in 4-week-old pigeons, whereas they were 50% and 30%, respectively, in 5-week-old chickens. Furthermore, this virus caused severe neurological symptoms in a 4-week-old pigeon and mild neurological symptoms in a 5-week-old chicken. A histopathological examination of the brain showed a classical nonsuppurative encephalitis lesion. The pattern of viral shedding, and viral load, and virus distribution differed between infected chickens and pigeons. Genomic characteristics suggest that there was cross-species transmission of PPMV-1 subgenotype VIc in this region at least from the years 2006 to 2015.

Evolutionary Dynamics and Age-Dependent Pathogenesis of Sub-Genotype VI.2.1.1.2.2 PPMV-1 in Pigeons

“…However, a recent study showed that the pathogenicity and transmission of virulent NDVs had no significant differences in young and adult chickens [45]. In our study, we found that age at infection had an impact on the outcome of PPMV-1 infection in pigeons, which was generally consistent with clinical cases in which the morbidity and mortality of younger pigeons were significantly higher than those of older pigeons [13,18]. These results indicated that the age of birds might affect PPMV-1, but not other NDV infections.…”

“…At 3 and 7 days post-infection (DPI), we euthanized three inoculated pigeons and determined the virus titers in the brain and lungs. To detect virus shedding, oropharyngeal and cloacal swabs were collected at 3,5,7,9,11,13,17, and 21 DPI and suspended in 1000 µL PBS with antibiotics (penicillin and amphotericin B, 4000 U/mL; streptomycin, 2 mg/mL). All collected samples were stored at −80 • C until further use.…”

“…Shedding of the GZ08 virus could be detected in both oropharyngeal and cloacal swabs of inoculated 3-, 6-, and 12-week-old pigeons during the experimentation period (Table 3). To determine virus shedding in inoculated pigeons of different ages, oropharyngeal and cloacal swabs were collected from all chickens at 3,5,7,9,11,13,17, and 21 DPI. Shedding of the GZ08 virus could be detected in both oropharyngeal and cloacal swabs of inoculated 3-, 6-, and 12-week-old pigeons during the experimentation period (Table 3).…”

Global phylodynamic analysis of avian paramyxovirus-1 provides evidence of inter-host transmission and intercontinental spatial diffusion

“…Along with three class I sequences without a recorded host, the sequences collected from the latter four host groups were categorized into an ambiguous group (i.e., "other avian taxa" henceforth) given small sample sizes. The majority of class II viruses collected between 2006 and 2016 originated from Anseriformes (171), domestic chickens (569), Columbiformes (220), other Galliformes (34), Psittaciformes (11), and Suliformes (19) hosts. Similar to class I, 43 class II sequences from rare or unrecorded host groups were collected into the other avian taxa category.…”

“…This suggests that though the initial transmission of wild bird virus into a domestic population may not have significant epidemiological consequences, the repeated transference of virulent viruses between domestic and wild birds likely affects global APMV-1 dynamics. Even though other investigations have found evidence for APMV-1 migration between hosts and geographic regions [9,12,[16][17][18][19], a globally-distributed analysis of APMV-1 viral migration has not yet been performed. Presence of virulent APMV-1 in poultry is reportable to the World Organisation for Animal Health (OIE) and may result in trade restrictions [20]; therefore, understanding the patterns of viral migration between world regions and host types would be useful for efforts directed towards preventing and limiting the spread of ND among wild and domestic birds.…”