Ecological characterization of 175 low-pathogenicity avian influenza viruses isolated from wild birds in Mongolia, 2009-2013 and 2016-2018.

BACKGROUND: Since 2005, highly pathogenic avian influenza A H5N1 viruses have spread from Asia worldwide, infecting poultry, humans and wild birds. Subsequently, global interest in avian influenza (AI) surveillance increased. OBJECTIVES: Mongolia presents an opportunity to study viruses in wild birds because the country has very low densities of domestic poultry and supports large concentrations of migratory water birds. METHODS: We conducted AI surveillance in Mongolia over two time periods, 2009-2013 and 2016-2018, utilizing environmental fecal sampling. Fresh fecal samples were collected from water bird congregation sites. Hemagglutinin (HA) and neuraminidase (NA) subtypes of positive samples were identified through viral isolation or molecular assays, with pathogenicity determined by HA subtype or sequencing the HA cleavage site. RESULTS: A total of 10,222 samples were collected. Of these, 7,025 fecal samples were collected from 2009 to 2013, and 3,197 fecal samples were collected from 2016 to 2018. Testing revealed 175 (1.7%) positive samples for low-pathogenicity influenza A, including 118 samples from 2009 to 2013 (1.7%) and 57 samples from 2016 to 2018 (1.8%). HA and NA subtyping of all positives identified 11 subtypes of HA and nine subtypes of NA in 29 different combinations. Within periods, viruses were detected more frequently during the fall season than in the early summer. CONCLUSION: Mongolia's critical wild bird habitat is positioned as a crossroad of multiple migratory flyways. Our work demonstrates the feasibility of using an affordable environmental fecal sampling approach for AI surveillance and contributes to understanding the prevalence and ecology of low-pathogenicity avian influenza viruses in this important location, where birds from multiple flyways mix.

Comparison of vaccination schedules for foot-and-mouth disease among cattle and sheep in Mongolia.

Vaccines are a critical tool for the control strategy for foot-and-mouth disease (FMD) in Mongolia where sporadic outbreaks regularly occur. A two-dose primary vaccination course is recommended for most commercial vaccines though this can be logistically challenging to deliver among nomadic pastoralist systems which predominate in the country. Although there is evidence that very high potency vaccines can provide prolonged duration of immunity, this has not been demonstrated under field conditions using commercially available vaccines. This study compared neutralizing titres to a O/ME-SA/Panasia strain over a 6-month period following either a two-dose primary course or a single double-dose vaccination among Mongolian sheep and cattle using a 6.0 PD50 vaccine. Titers were not significantly different between groups except in sheep at six-months post vaccination when the single double-dose group had significantly lower titers. These results indicate the single double-dose regimen may be a cost-effective approach for vaccination campaigns supporting FMD control in Mongolia.

A field study evaluating the humoral immune response in Mongolian sheep vaccinated against sheeppox virus.

Sheeppox is a transboundary disease of small ruminants caused by infection with the capripoxvirus sheeppox virus. Sheeppox is found in Africa, the Middle East and Asia and is characterized by fever, multifocal cutaneous raised lesions and death. Vaccination with live attenuated capripoxvirus (CPPV) strains is an effective and widely used strategy to contol sheeppox outbreaks; however, there are few reports of post-vaccination field surveillance studies. This study used a commercially available enzyme-linked immunosorbent assay (ELISA) to examine quantitative and temporal features of the humoral response of sheep vaccinated with a live-attenuated CPPV strain in Mongolia. Four hundred samples were tested using the ELISA commercial kit, and a subset of 45 samples were also tested with a virus neutralization test (VNT). There was substantial agreement between the VNT and ELISA tests. Antibodies to CPPV were detected between 40 and 262 days post-vaccination. There was no significant difference between serological status (positive/negative) and sex or age; however, an inverse correlation was found between the length of time since vaccination and serological status. Animals between 90 and 180 days post-vaccination were more likely to be positive than animals greater than 180 days post-vaccination. Our results show that a commercial CPPV ELISA kit is a robust and reliable assay for post-CPPV vaccination surveillance in resource-restricted settings and provide temporal parameters to be considered when planning sheeppox post-vaccination monitoring programmes.

Socio-economic impact of Foot-and-Mouth Disease outbreaks and control measures: An analysis of Mongolian outbreaks in 2017.

Mongolia is a large landlocked country in Central Asia and has one of the highest per capita livestock ratios in the world. During 2017, reported foot-and-mouth disease (FMD) outbreaks in Mongolia increased considerably, prompting widespread disease control measures. This study estimates the socio-economic impact of FMD and subsequent control measures on Mongolian herders. The analysis encompassed quantification of the impact on subsistence farmers' livelihoods and food security and estimation of the national-level gross losses due to reaction and expenditure during 2017. Data were collected from 112 herders across eight provinces that reported disease. Seventy of these herders had cases of FMD, while 42 did not have FMD in their animals but were within quarantine zones. Overall, 86/112 herders reported not drinking milk for a period of time and 38/112 reduced their meat consumption. Furthermore, 55 herders (49.1%) had to borrow money to buy food, medicines and/or pay bills or bank loans. Among herders with FMD cases, the median attack rate was 31.7%, 3.8% and 0.59% in cattle, sheep and goats, respectively, with important differences across provinces. Herders with clinical cases before the winter had higher odds of reporting a reduction in their meat consumption. National-level gross losses due to FMD in 2017 were estimated using government data. The estimate of gross economic loss was 18.4 billion Mongolian-tugriks (US$7.35 million) which equates to approximately 0.65% of the Mongolian GDP. The FMD outbreaks combined with current control measures have negatively impacted herders' livelihoods (including herders with and without cases of FMD) which are likely to reduce stakeholder advocacy. Possible strategies that could be employed to ameliorate the negative effects of the current control policy were identified. The findings and approach are relevant to other FMD endemic regions aiming to control the disease.

African Swine Fever in Mongolia: Course of the Epidemic and Applied Control Measures.

African swine fever (ASF) is spreading rapidly in Asia and was confirmed in Mongolia on 10 January 2019. Following the outbreak confirmation, a state emergency committee was established with representation from municipal authorities and other relevant authorities including the General Authority for Veterinary Services, National Emergency Management Agency, General Agency for Specialized Inspection, and the Ministry of Environment and Tourism. The committee provided recommendations and coordinated closely with the State Central Veterinary Laboratory to ensure quick outbreak investigation and response. In addition to outbreak investigations, sampling took place at farms and food premises and suggests a link between the outbreaks and swill feeding practices among backyard pig farmers. Upon government request, the Food and Agriculture Organization of the United Nations (FAO) deployed an expert team to assist in identifying risk factors for the disease spread and provide recommendations as how to improve disease prevention and response. Following the control measures from the involved agencies, the epidemic was successfully controlled and declared over on 11 April 2019. In total, the epidemic affected 83 pig farming households and led to a total of 2862 dead or culled pigs in eleven districts of seven provinces in Mongolia.

Immunogenicity of imported foot-and-mouth vaccines in different species in Mongolia.

Foot-and-mouth disease (FMD) is a high impact viral disease of livestock for which vaccines are extensively used in control. Mongolia has regular incursions of FMD virus that are typically limited to the eastern region although large epidemics are occasionally reported in the normally disease-free western areas. Vaccines are imported and form an important component of the control strategy. In 2015, post-vaccination monitoring guidelines were published by the FAO-OIE recommending approaches for assessing the appropriateness of imported vaccines including small-scale immunogenicity studies. This study used these recommended approaches to guide the use of vaccine adjuvant type and the need for a one or two dose primary course in the national control programme considering cattle, sheep and Bactrian camels and also whether these vaccines were appropriate for the FMD virus lineages considered high risk to Mongolia (A/ASIA/Sea-97; O/SEA/Mya-98; O/ME-SA/PanAsia; O/ME-SA/Ind-2001). The results of these immunogenicity studies indicated that in cattle and sheep, oil-adjuvanted vaccines led to higher and more persistent neutralisation titres that were satisfactory against the target lineages if a two-dose primary course was utilised. In contrast, aqueous-adjuvanted vaccines were associated with lower titres that likely required a booster after 3 months. Levels of antibodies in Bactrian camels were significantly lower although it is unknown how these may correlate with protection under experimental or field exposure conditions. The results of this study have implications for vaccine policy in Mongolia and suggest further studies on the role of Bactrian camels in the epidemiology of FMD are necessary to indicate if further research on FMD vaccines are needed in this species.

Outbreak of Peste des Petits Ruminants among Critically Endangered Mongolian Saiga and Other Wild Ungulates, Mongolia, 2016-2017.

The 2016-2017 introduction of peste des petits ruminants virus (PPRV) into livestock in Mongolia was followed by mass mortality of the critically endangered Mongolian saiga antelope and other rare wild ungulates. To assess the nature and population effects of this outbreak among wild ungulates, we collected clinical, histopathologic, epidemiologic, and ecological evidence. Molecular characterization confirmed that the causative agent was PPRV lineage IV. The spatiotemporal patterns of cases among wildlife were similar to those among livestock affected by the PPRV outbreak, suggesting spillover of virus from livestock at multiple locations and time points and subsequent spread among wild ungulates. Estimates of saiga abundance suggested a population decline of 80%, raising substantial concerns for the species' survival. Consideration of the entire ungulate community (wild and domestic) is essential for elucidating the epidemiology of PPRV in Mongolia, addressing the threats to wild ungulate conservation, and achieving global PPRV eradication.

Molecular Characterization of Avian Paramyxovirus Types 4 and 8 Isolated from Wild Migratory Waterfowl in Mongolia.

Avian paramyxoviruses (APMVs) constitute some of the most globally prevalent avian viruses and are frequently isolated from wild migratory bird species. Using 1,907 fresh fecal samples collected during the 2012 avian influenza surveillance program, we identified two serotypes of APMV: APMV-4 ( n=10) and APMV-8 ( n=1). Sequences for these isolates phylogenetically clustered with Asian APMV-4 and APMV-8 recently isolated from wild birds in Korea, Japan, China, and Kazakhstan. Analysis by DNA barcoding indicated that the Mongolian APMV-4 and APMV-8 strains were isolated from Anseriformes species including Mallards ( Anas platyrhynchos) and Whooper Swans ( Cygnus cygnus). The close genetic relatedness to Asian isolates, and to similar host species, suggested that wild bird species in the Anatidae family might play an important role as a natural reservoir in the spread of APMV-4 and APMV-8. However, we did not find conclusive evidence to support this hypothesis owing to the limited number of strains that could be isolated. Enhanced surveillance of poultry and wild bird populations in Asia is therefore crucial for the understanding of global AMPV transmission, ecology, evolution, and epidemiology.

First genetic characterization of peste des petits ruminants virus from Mongolia.

Between August and September 2016 pathological samples were collected from sheep and goats following suspected peste des petits ruminants (PPR) outbreaks in western Mongolia. RT-PCR followed by sequencing and phylogenetic analysis of the samples confirmed the presence of a PPR virus belonging to lineage IV. A full genome analysis of the viral RNA from one of the samples revealed a high similarity (99.0-99.5%) with PPR viruses currently circulating in China (2013-2015) indicating a common origin. This is the first genetic characterization of PPR virus in Mongolia and the data generated will have important implications for control and management of the disease in the region.