Identification of highly pathogenic avian influenza suitable areas for wild birds using species distribution models in South Korea.

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To the Editor: Wild migratory birds are reservoirs for low pathogenic avian influenza (LPAI) viruses (1), but their role in transmitting highly pathogenic avian influenza (HPAI) viruses is hotly debated and unclear (2–4). Beginning in July 2005, a clade of HPAI (H5N1) viruses rapidly expanded from an apparent focus in western People’s Republic of China and spread to the Middle East, Africa, and Europe (5). Genetic analysis of HPAI virus isolates from dead wild birds along major flyways indicated that the strains were closely related to the Qinghai H5N1 A/bar-headed goose/Qinghai/65/2005 virus (clade II) (GenBank accession no. {type:entrez-nucleotide,attrs:{text:DQ095622,term_id:70955434,term_text:DQ095622}}DQ095622). In addition to transmission to domestic poultry, HPAI (H5N1)–infected mute swans have been implicated in direct transmission to humans in Azerbaijan (6). The US Naval Medical Research Unit No. 3 and the Ministry of Environment of Egypt have collaborated since 2003 in obtaining samples from migratory birds to detect circulating influenza viruses. During the 2005–06 migratory birds season, 1,304 migratory birds were sampled from either live bird markets or cage birds trapped by fishermen in Port Said, Damietta, Fayoum, Arish, and Sharm el Sheikh (Appendix Figure, panel A. A total of 203 cloacal swab samples were positive for influenza A virus matrix gene when tested by real-time PCR, and 2 were also positive for the hemagglutinin 5 (H5) gene by using specific primers (7). Of the 2 migratory birds positive for the H5 gene, the first was a common teal (Anas crecca) captured in the Nile Delta region of Damietta in October 2005 (Appendix Figure, panel A). Sequencing of the H5 gene showed that this virus was an LPAI most closely related to strain A/mallard/Bavaria/1/2005(H5N2) (GenBank accession no. {type:entrez-nucleotide,attrs:{text:DQ387854,term_id:88656455,term_text:DQ387854}}DQ387854 (2). In January 2006, an influenza A H5 virus (weak positive result) was detected in another common teal (trapped in a cage by a fisherman) sampled from the Damietta region in December 2005 (Appendix Figure, panel A). The low viral load, coupled with the failure to isolate the virus, precluded the laboratory from conducting sequence analysis at the time on the basis of insufficient template material. After the outbreak of influenza A (H5N1) in poultry and humans in Egypt in February 2006, additional retrospective attempts to concentrate RNA were used to assess potential introduction scenarios. After multiple RNA extractions were conducted and the RNA was concentrated, this specimen was found to be positive for the neuraminidase 1 (N1) gene by real-time PCR. The hemagglutinin gene from both teal strains was sequenced (≈1,596 bp). Sequences were aligned with other influenza A (H5N1) strains from Egypt (9 from humans, 5 from chickens). Twenty other strains with high similarity and from different locations were selected by using a GenBank search algorithm and included in the alignment. A phylogenetic analysis was conducted by using the Kimura 2-parameter model. The LPAI H5 virus strain was used as an outgroup in a neighbor-joining phylogenetic tree. Bootstrap analysis with 500 replicates of sequence data was also conducted by using MEGA 3.1 software (8). Phylogenetic analysis showed clustering of the HPAI (H5N1) strains collected from 1 geographic region (country) (Appendix Figure, panel B). All HPAI (H5N1) strains from Egypt from humans or chickens analyzed clustered with a bootstrap support value of 98%. Furthermore, the A/Teal/Egypt/14051-NAMRU3/2006 (H5N1) strain (collected in December 2005; Appendix Figure, panel A) is an HPAI and is closely related to the parent of the group of viruses isolated in the early 2006 Egypt outbreak, with an average identity of 99.4% with all other strains from Egypt and a bootstrap support value of 96% (Appendix Figure, panel B). Despite the rapid spread of this clade (Qinghai-like strain) to many countries, since late 2005, strains analyzed in this study showed low-level genetic variation (<2%). Brown et al. reported that species can vary greatly in their response to HPAI (9). At least in ducks, it appears that viral shedding is highest in birds with clinical signs of infection, and lowest, as seen in the common teal infected with the HPAI strain in this study, in birds with subclinical infections. These subclinical infections may be due to flock immunity from previous exposure to LPAI H5 virus or genetic factors. This suggestion is conceivable in light of the LPAI H5 virus detected in the other teal a few months earlier. Such naturally resistant wild birds might serve as vectors for introduction of HPAI viruses into new locations. Data presented herein suggest that an HPAI virus may have been introduced into Egypt through a migratory bird. Whether poultry were infected before mid-February or the teal was infected with influenza A (H5N1) virus by a domesticated species is not unknown. The low degree of viral shedding indicates that detection of any influenza A (H5N1) virus in wild birds in a new region should be immediately followed up with efforts to characterize the virus to control the spread of new subtypes/strains of HPAI into new locations.

Controlling Highly Pathogenic Avian Influenza, Bangladesh

BackgroundNational surveillance of avian influenza virus (AIV) in South Korea has been annually conducted for the early detection of AIV and responses to the introduction of highly pathogenic avian influenza (HPAI) virus. In this study, we report on a nationwide surveillance study of AIV in domestic poultry and wild birds in South Korea between 2012 and 2014.MethodsDuring the surveillance programs between 2012 and 2014, 141,560 samples were collected. Of these, 102,199 were from poultry farms, 8215 were from LBMs, and 31,146 were from wild bird habitats. The virus isolation was performed by inoculation of embryonated chicken eggs and AIV isolates were detected using hemagglutination assay. For subtying of AIV, the hemagglutinin and neuraminidase genes were confirmed by sequencing. Phylogenetic analysis of the H5 subtypes was performed using 28 H5 AIV isolates.ResultsBetween 2012 and 2014, a total of 819 AIV were isolated from 141,560 samples. Virus isolation rates for AIV were 0.6, 0.4, 0.1, and 2.7% in wild birds (n = 202), domestic ducks (n = 387), minor poultry (n = 11), and the live bird market (LBM) (n = 219), respectively. In wild birds, various subtypes were found including H1–H7 and H9–H13. The major subtypes were H5 (n = 48, 23.9%: N3 (n = 4) and N8 (n = 44)), H4 (n = 39, 19.4%), and H1 (n = 29, 14.4%). In domestic poultry, mainly ducks, the H5N8 (n = 275, 59.3%), H3 (n = 30, 17.2%), and H6 (n = 53, 11.4%) subtypes were predominantly found. The most frequently detected subtypes in LBM, primarily Korean native chicken, were H9 (n = 169, 77.2%). H3 (n = 10, 4%) and H6 (n = 30, 13.7%) were also isolated in LBM. Overall, the prevalence of AIV was found to be higher between winter and spring and in western parts of South Korea. The unusual high prevalence of the H5 subtype of AIV was due to the large scale outbreak of H5N8 HPAI in wild birds and domestic poultry in 2014.ConclusionsEnhanced surveillance and application of effective control measures in wild birds and domestic poultry, including LBM, should be implemented to control AI and eradicate HPAI.

Highly pathogenic avian influenza (HPAI), a zoonotic disease, is a major threat to humans and poultry health worldwide. In January 2014, HPAI virus subtype H5N8 first infected poultry farms in South Korea, and 393 outbreaks, overall, were reported with enormous economic damage in the poultry industry. We analyzed the spatiotemporal distribution of HPAI H5N8 outbreaks in poultry farms using the global and local spatiotemporal interaction analyses in the first (January to July 2014) and second (September 2014 to June 2015) outbreak waves. The space–time K-function analyses revealed significant interactions within three days and in an over-40 km space–time window between the two study periods. The excess risk attributable value (D0) was maintained despite the distance in the case of HPAI H5N8 in South Korea. Eleven spatiotemporal clusters were identified, and the results showed that the HPAI introduction was from the southwestern region, and spread to the middle region, in South Korea. This spatiotemporal interaction indicates that the HPAI epidemic in South Korea was mostly characterized by short period transmission, regardless of the distance. This finding supports strict control strategies such as preemptive depopulation, and poultry movement tracking. Further studies are needed to understand HPAI disease transmission patterns.

Wild aquatic birds, a natural reservoir of avian influenza viruses (AIVs), transmit AIVs to poultry farms, causing huge economic losses. Therefore, the prevalence and genetic characteristics of AIVs isolated from wild birds in South Korea from October 2019 to March 2020 were investigated and analyzed. Fresh avian fecal samples (3256) were collected by active monitoring of 11 wild bird habitats. Twenty-eight AIVs were isolated. Seven HA and eight NA subtypes were identified. All AIV hosts were Anseriformes species. The HA cleavage site of 20 representative AIVs was encoded by non-multi-basic amino acid sequences. Phylogenetic analysis of the eight segment genes of the AIVs showed that most genes clustered within the Eurasian lineage. However, the HA gene of H10 viruses and NS gene of four viruses clustered within the American lineage, indicating intercontinental reassortment of AIVs. Representative viruses likely to infect mammals were selected and evaluated for pathogenicity in mice. JB21-58 (H5N3), JB42-93 (H9N2), and JB32-81 (H11N2) were isolated from the lungs, but JB31-69 (H11N9) was not isolated from the lungs until the end of the experiment at 14 dpi. None of infected mice showed clinical sign and histopathological change in the lung. In addition, viral antigens were not detected in lungs of all mice at 14 dpi. These data suggest that LPAIVs derived from wild birds are unlikely to be transmitted to mammals. However, because LPAIVs can reportedly infect mammals, including humans, continuous surveillance and monitoring of AIVs are necessary, despite their low pathogenicity.

It is well-known that highly pathogenic avian influenza (HPAI) strains can arise from low pathogenic strains (LPAI) during epidemics in poultry farms. Despite this, the possibility that partial cross-immunity triggered by previous exposure to LPAI viruses may reduce the pathogenicity of HPAI and thus enhance its persistence has been generally overlooked in both empirical and theoretical work on avian influenza. We propose a simple mathematical model to investigate the interacting dynamics of HPAI and LPAI strains of avian influenza in small-scale poultry farms. Through the analysis of a deterministic ordinary differential equations model, we show that: (1) for a wide range of realistic model parameters, the reduction in pathogenicity yielded by previous LPAI infection might allow an HPAI strain that would not be able to persist in a host population when alone (ℜ0 < 1) to invade and co-exist in the host population along with the LPAI strain and (2) the coexistence between the HPAI and LPAI strains may be characterized by multiyear periodicity. Because simulations showed that troughs between epidemics can be deep, with only a fraction of existing flocks infected by the HPAI strain, we also ran an individual-based stochastic version of the dynamical model to analyze the potential for natural fade-out of the HPAI strain. The analysis of the stochastic model confirms the prediction that previous exposure to a LPAI strain can significantly increase the duration of the epidemics by an HPAI strain before it fades from the population.

International audience

Worldwide, wild birds are frequently suspected to be involved in the occurrence of outbreaks of different diseases in captive-bred birds although proofs are lacking and most of the dedicated studies are insufficiently conclusive to confirm or characterize the roles of wild birds in such outbreaks. The aim of this study was to assess and compare, for the most abundant peridomestic wild birds, the different exposure routes for avian influenza and Newcastle disease viruses in conservation breeding sites of Houbara bustards in the United Arab Emirates. To do so, we considered all of the potential pathways by which captive bustards could be exposed to avian influenza and Newcastle disease viruses by wild birds, and ran a comparative study of the likelihood of exposure via each of the pathways considered. We merged data from an ecological study dedicated to local wild bird communities with an analysis of the contacts between wild birds and captive bustards and with a prevalence survey of avian influenza and Newcastle disease viruses in wild bird populations. We also extracted data from an extensive review of the scientific literature and by the elicitation of expert opinion. Overall, this analysis highlighted those captive bustards had a high risk of being exposed to pathogens by wild birds. This risk was higher for Newcastle disease virus than avian influenza virus, and House sparrows represented the riskiest species for the transmission of both viruses through direct exposure from direct contact with an infectious bird that got inside the aviary and indirect exposure from consumption of water contaminated from the faeces of an infected bird that got inside the aviary for Newcastle disease virus and avian influenza virus, respectively. These results also reaffirm the need to implement biosecurity measures to limit contacts between wild and captive birds and highlight priority targets for a thoughtful and efficient sanitary management strategy.

Highly Pathogenic Avian Influenza (HPAI) subtype H5N8 outbreaks occurred in poultry farms in South Korea in 2014 resulting in significant damage to the poultry industry. Between 2014 and 2016, the pandemic disease caused significant economic loss and social disruption. To evaluate the risk factors for HPAI infection in broiler duck farms, we conducted a retrospective case-control study on broiler duck farms. Forty-three farms with confirmed laboratories on premises were selected as the case group, and 43 HPAI-negative farms were designated as the control group. Control farms were matched based on farm location and were within a 3-km radius from the case premises. Spatial and environmental factors were characterized by site visit and plotted through a geographic information system (GIS). Univariable and multivariable logistic regression models were developed to assess possible risk factors associated with HPAI broiler duck farm infection. Four final variables were identified as risk factors in a final multivariable logistic model: "Farms with ≥7 flocks" (odds ratio [OR]=6.99, 95% confidence interval [CI] 1.34-37.04), "Farm owner with ≥15years of raising poultry career" (OR=7.91, 95% CI 1.69-37.14), "Presence of any poultry farms located within 500m of the farm" (OR=6.30, 95% CI 1.08-36.93) and "Not using a faecal removal service" (OR=27.78, 95% CI 3.89-198.80). This highlights that the HPAI H5N8 outbreaks in South Korea were associated with farm owner education, number of flocks and facilities and farm biosecurity. Awareness of these factors may help to reduce the spread of HPAI H5N8 across broiler duck farms in Korea during epidemics. Greater understanding of the risk factors for H5N8 may improve farm vulnerability to HPAI and other subtypes and help to establish policies to prevent re-occurrence. These findings are relevant to global prevention recommendations and intervention protocols.

Consequences and global risks of highly pathogenic avian influenza outbreaks in poultry in the United Kingdom

Early detection of highly pathogenic avian influenza (HPAI) infection in commercial poultry flocks is a critical component of outbreak control. Reducing the time to detect HPAI infection can reduce the risk of disease transmission to other flocks. The timeliness of different types of detection triggers could be dependent on clinical signs that are first observed in a flock, signs that might vary due to HPAI virus strain characteristics. We developed a stochastic disease transmission model to evaluate how transmission characteristics of various HPAI strains might effect the relative importance of increased mortality, drop in egg production, or daily real-time reverse transcriptase (RRT)-PCR testing, toward detecting HPAI infection in a commercial table-egg layer flock. On average, daily RRT-PCR testing resulted in the shortest time to detection (from 3.5 to 6.1 days) depending on the HPAI virus strain and was less variable over a range of transmission parameters compared with other triggers evaluated. Our results indicate that a trigger to detect a drop in egg production would be useful for HPAI virus strains with long infectious periods (6-8 days) and including an egg-drop detection trigger in emergency response plans would lead to earlier and consistent reporting in some cases. We discuss implications for outbreak control and risk of HPAI spread attributed to different HPAI strain characteristics where an increase in mortality or a drop in egg production or both would be among the first clinical signs observed in an infected flock.

Since 2003, highly pathogenic avian influenza (HPAI) virus outbreaks have occurred five times in Korea, with four HPAI H5N1 outbreaks and one HPAI H5N8 outbreak. Migratory birds have been suggested to be the first source of HPAI in Korea. Here, we surveyed migratory wild birds for the presence of AI and compared regional AI prevalence in wild birds from September 2012 to April 2014 for birds having migratory pathways in South Korea. Finally, we investigated the prevalence of AI in migratory birds before and after HPAI H5N8 outbreaks. Overall, we captured 1617 migratory wild birds, while 18,817 feces samples and 74 dead birds were collected from major wild bird habitats. A total of 21 HPAI viruses were isolated from dead birds, and 86 low pathogenic AI (LPAI) viruses were isolated from captured birds and from feces samples. Spatiotemporal distribution analysis revealed that AI viruses were spread southward until December, but tended to shift north after January, consistent with the movement of migratory birds in South Korea. Furthermore, we found that LPAI virus prevalences within wild birds were notably higher in 2013-2014 than the previous prevalence during the northward migration season. The data from our study demonstrate the importance of the surveillance of AI in wild birds. Future studies including in-depth genetic analysis in combination with evaluation of the movement and ecology of migratory birds might help us to bridge the gaps in our knowledge and better explain, predict, and ultimately prevent future HPAI outbreaks.

The 3 patients infected with W135 in our study did not receive bivalent meningococcal vaccines. W135 meningococcal disease appears to be an emerging problem that should be investigated epidemiologically. These patients highlight the need for further epidemiologic surveillance to monitor changes in the incidence of meningococcal disease caused by W135 and for improved public health disease control strategies in the future.

BackgroundThe rapid and accurate identification of the H5 and H7 subtypes of avian influenza (AI) virus is an important step for the control and eradication of highly pathogenic AI outbreaks and for the surveillance of AI viruses that have the potential to undergo changes in pathogenicity in poultry and wild birds. Currently, real-time reverse transcription polymerase chain reaction (RRT-PCR) is routinely used for the rapid detection of the H5 and H7 genes, but misidentification is frequent for emergent isolates and viruses isolated from diverse regions due to the high sequence variation among AI viruses.FindingsIn this study, an RRT-PCR method was tested for the detection of matrix, H5 and H7 genes from diverse subtypes of AI viruses and from field samples obtained through AI surveillance in South Korea over the last four years. Both RRT-PCR and conventional experiment (virus isolation using egg inoculation followed by reverse transcription polymerase chain reaction) agreed on the virus-positive samples. And the comparison of the results with 174 clinical samples showed a high level of agreement without decreasing the specificity and sensitivity.ConclusionsThis assay could be useful tool for the rapid detection of AI using the field samples from domestic poultry and wild birds in South Korea, and continuous regional updates is needed to validate primer sets as the AI virus evolves.