Spatial clusters of human and livestock anthrax define high-risk areas requiring intervention in Lao Cai Province, Vietnam 1991-2022.

Anthrax, a widespread zoonosis in low and middle-income countries with low disease awareness and insufficient livestock vaccination coverage, has been known in Lao Cai Province in northern Vietnam for years before its apparent absence in 2009, which requires investigation as this infection is frequently reported from neighbouring provinces and countries. We aimed to describe the seasonal patterns of anthrax (1991-2008), compare livestock anthrax vaccine coverage to disease occurrence (1991- 2022), and delineate the high-risk areas to inform local disease surveillance in the province. We illustrated the seasonal pattern of anthrax and provided a comparison between livestock vaccine coverage and disease occurrence by purely spatial SaTScan (Poisson model, 25% population at risk) to detect spatial clusters of human and livestock anthrax using population derived from zonal statistics routines. The number of cases, crude cumulative incidence, and spatial clusters of human and livestock anthrax were mapped in QGIS. Results indicate peak anthrax incidence from May to October. Buffalo, domestic cattle, and horses accounted for 75% of total animal cases. Horse anthrax was more common in Lao Cai than in its neighbours and often occurred in years with human mortality. Vaccination covered less than 30% of the livestock population. We found an apparent pattern where anthrax was controlled from 1998-2003 with higher vaccine coverage (>20%) and identified spatial clusters of human and livestock anthrax in Muong Khuong, Bao Thang, and Bac Ha districts of Lao Cai. The local public health and veterinary agencies are recommended to revisit the high-risk areas and communicate with neighbouring provinces for a regional approach to anthrax surveillance and control.

Spatial epidemiology of human anthrax in Son La province, Vietnam, 2003-2022.

AIMS: Anthrax is reported with frequency but poorly understood in Southeast Asian countries including Vietnam. In Vietnam, anthrax surveillance is national. However, case detection, prevention, and control are implemented locally at the provincial level. Here, we describe the epidemiological characteristics, identify spatial clusters of human anthrax, and compare the variation in livestock anthrax vaccine coverage to disease incidence in humans and livestock using historical data in Son La province, Vietnam (2003-2020). METHODS AND RESULTS: Most human cases occurred between April and September. Most of the patients were male, aged 15-54 years old. The human cases were mainly reported by public district hospitals. There was a delay between disease onset and hospitalization of ~5 days. We identified spatial clusters of high-high incidence communes in the northern communes of the province using the local Moran's I statistic. The vaccine coverage sharply decreased across the study period. The province reported sporadic human anthrax outbreaks, while animal cases were only reported in 2005 and 2022. CONCLUSIONS: These results suggest underreporting for human and livestock anthrax in the province. Intersectoral information sharing is needed to aid livestock vaccination planning, which currently relies on reported livestock cases. The spatial clusters identify areas for targeted surveillance and livestock vaccination, while the seasonal case data suggest prioritizing vaccination campaigns for February or early March ahead of the April peak. A regional approach for studying the role of livestock trading between Son La and neighbouring provinces in anthrax occurrence is recommended.

Spatial analysis of human and livestock anthrax in Lai Chau province, Vietnam (2004-2021).

Anthrax is reported globally with varying disease intensity and seasonality among countries. In Vietnam, anthrax epidemiology and ecology remain understudied. We used historical data of human and livestock anthrax from 2004 to 2021 in Lai Chau province, to identify spatial clusters of human and livestock anthrax, describe epidemiological characteristics, and compare livestock anthrax vaccine coverage to human and livestock disease incidence. Local Moran's I (LISA) using spatial Bayes smoothed commune-level cumulative incidence (per 10,000) for the study period, epidemiological descriptive statistics, livestock vaccine coverage data, and annual incidence rates (per 10,000) at provincial level were used. LISA identified a human anthrax hotspot (high-high) in the southeast which did not overlap spatially with livestock anthrax hotspots in southeastern and northeastern communes. Most human cases were male, aged 15-59 years, handled sick animals, and/or consumed contaminated meat. Almost all cases were reported by grassroot health facilities with a delay of 6.3 days between exposure and case notification to the national surveillance system. 80 % of human cases were reported from June-October. The increase in disease incidence occurred shortly after livestock anthrax vaccine coverage decreased. This study informs vaccination strategy and targeted surveillance and control measures in newly identified high-risk areas and seasons of anthrax.

Spatial and phylogenetic patterns reveal hidden infection sources of Bacillus anthracis in an anthrax outbreak in Son La province, Vietnam.

Bacillus anthracis, the bacterial cause of anthrax, is a zoonosis affecting livestock and wildlife often spilling over into humans. In Vietnam, anthrax has been nationally reportable since 2015 with cases occurring annually, mostly in the northern provinces. In April 2022, an outbreak was reported in Son La province following the butchering of a water buffalo, Bubalus bubalis. A total of 137 humans from three villages were likely exposed to contaminated meat from the animal. Early epidemiological investigations suggested a single animal was involved in all exposures. Five B. anthracis isolates were recovered from human clinical cases along with one from the buffalo hide, another from associated maggots, and one from soil at the carcass site. The isolates were whole genome sequenced, allowing global, regional, and local molecular epidemiological analyses of the outbreak strains. All recovered B. anthracis belong to the A.Br.001/002 lineage based on canonical single nucleotide polymorphism analysis (canSNP). Although not previously identified in Vietnam, this lineage has been identified in the nearby countries of China, India, Indonesia, Thailand, as well as Australia. A twenty-five marker multi-locus variable number tandem repeat analysis (MLVA-25) was used to investigate the relationship between human, soil, and buffalo strains. Locally, four MLVA-25 genotypes were identified from the eight isolates. This level of genetic diversity is unusual for the limited geography and timing of cases and differs from past literature using MLVA-25. The coupled spatial and phylogenetic data suggest this outbreak originated from multiple, likely undetected, animal sources. These findings were further supported by local news reports that identified at least two additional buffalo deaths beyond the initial animal sampled in response to the human cases. Future outbreak response should include intensive surveillance for additional animal cases and additional molecular epidemiological traceback to identify pathogen sources.

Informing One Health Anthrax Surveillance and Vaccination Strategy from Spatial Analysis of Anthrax in Humans and Livestock in Ha Giang Province, Vietnam (1999-2020).

Anthrax, caused by Bacillus anthracis, has a nearly global distribution but is understudied in Southeast Asia, including Vietnam. Here, we used historical data from 1999 to 2020 in Ha Giang, a province in northern Vietnam. The objectives were to describe the spatiotemporal patterns and epidemiology of human and livestock anthrax in the province and compare livestock vaccine coverage with human and livestock anthrax incidence. Annual incidence rates (per 10,000) for humans, buffalo/cattle, and goats were used to explore anthrax patterns and for comparison with livestock annual vaccine variations. A data subset describes anthrax epidemiology in humans by gender, age, source of infection, type of anthrax, admission site, and season. Zonal statistics and SaTScan were used to identify spatial and space-time clusters of human anthrax. SaTScan revealed space-time clusters in 1999, 2004, and 2007-2008 in the province, including in the northeastern, eastern, and western areas. Most human anthrax was reported between July and October. Most patients were male, aged 15-59 years, who had handled sick animals and/or consumed contaminated meat. High case-fatality rates were reported with gastrointestinal or respiratory cases. Our data suggest that vaccination in buffalo and cattle reduces the disease burden in humans and vaccinated animals but does not reduce the incidence in unvaccinated animals (goats). This study identified spatial areas of high risk for anthrax and can inform One Health surveillance and livestock vaccination planning in contextual settings similar to Ha Giang province.

Zoonotic pathogens and diseases detected in Vietnam, 2020-2021.

Vietnam has been identified as a country at high-risk for emergence and re-emergence of zoonotic diseases. The government of Vietnam recognized five priority zoonoses, including highly pathogenic avian influenza, rabies, leptospirosis, anthrax, and Streptococcus suis, and established a framework for One Health investigation and response to these diseases. From July 2020 to February 2021, quantitative data of zoonoses were collected from an online survey in 61 of 63 provinces based on either clinical diagnosis or laboratory confirmation. The responses were followed up by using in-depth interviews, and scientific literatures on zoonoses in Vietnam during 2010 to 2020 were reviewed. A total of 234 human health professionals and 95 animal health professionals responded to the survey. The proportion of clinical-based respondents was higher than laboratory-based respondents in both human health (130/234, 55.6%) and animal health (65/95, 68.4%) sectors. There were differences in the reported frequency of zoonoses between human and animal health professionals, and between clinical-based and laboratory-based respondents. Rabies was the most serious zoonotic disease based on the number of human cases and the geographic distribution. No human cases of avian influenza infection have been reported since 2015, although the H5 subtype viruses have been found in poultry. Besides, some bacterial, fungal, and parasitic zoonoses were detected in both humans and animals. Out of the 75 zoonoses identified, we recommend that the original five prioritized zoonoses, plus 24 additional zoonoses, should be targeted for future prevention, detection, and control under One Health approach in Vietnam.

Zoonotic Flavivirus Exposure in Peri-Urban and Suburban Pig-Keeping in Hanoi, Vietnam, and the Knowledge and Preventive Practices of Pig Farmers.

Mosquito-borne diseases (MBDs), including those caused by flaviviruses, remain human health problems for developing and urbanizing economies. This cross-sectional study examined risks of flavivirus exposure through a survey regarding knowledge and practices of pig farmers, and serological analysis of pigs in peri-urban and suburban Hanoi city. A total of 636 pig sera from 179 pig farms in 4 districts, namely, Chuong My, Dan Phuong, Ha Dong, and Bac Tu Liem, were analyzed by a competitive ELISA designed for flavivirus antibody detection. The results indicated a low level of awareness about MBDs among pig farmers, and a high seroprevalence in pigs at 88.5% (95%CI = 85.8-90.9%). Moreover, common practices of pig owners to prevent mosquitoes at home and farm did not show a significant reduction in flavivirus exposure in pigs. At animal level, significant associations between seropositive pigs and the farms with more than 60 pigs, and the district location were found. Farm-level multivariable analysis did not identify significant risk factors for flavivirus exposure. The study suggests that improving awareness of pig owners about MBDs in Hanoi city may be warranted to reduce the risk for MBD flavivirus infections in both humans and pigs.

The Distribution and Composition of Vector Abundance in Hanoi City, Vietnam: Association with Livestock Keeping and Flavivirus Detection.

BACKGROUND: Dengue virus and Japanese encephalitis virus are two common flaviviruses that are spread widely by Aedes and Culex mosquitoes. Livestock keeping is vital for cities; however, it can pose the risk of increasing the mosquito population. Our study explored how livestock keeping in and around a large city is associated with the presence of mosquitoes and the risk of them spreading flaviviruses. METHODS: An entomological study was conducted in 6 districts with 233 households with livestock, and 280 households without livestock, in Hanoi city. BG-Sentinel traps and CDC light traps were used to collect mosquitoes close to animal farms and human habitats. Adult mosquitoes were counted, identified to species level, and grouped into 385 pools, which were screened for flaviviruses using a pan-flavivirus qPCR protocol and sequencing. RESULTS: A total of 12,861 adult mosquitoes were collected at the 513 households, with 5 different genera collected, of which the Culex genus was the most abundant. Our study found that there was a positive association between livestock keeping and the size of the mosquito population-most predominantly between pig rearing and Culex species (p < 0.001). One pool of Cx. tritaeniorhynchus, collected in a peri-urban district, was found to be positive for Japanese encephalitis virus. CONCLUSIONS: The risk of flavivirus transmission in urban areas of Hanoi city due to the spread of Culex and Aedes mosquitoes could be facilitated by livestock keeping.

Optimizing the early detection of low pathogenic avian influenza H7N9 virus in live bird markets.

In Southeast Asia, surveillance at live bird markets (LBMs) has been identified as crucial for detecting avian influenza viruses (AIV) and reducing the risk of human infections. However, the design of effective surveillance systems in LBMs remains complex given the rapid turn-over of poultry. We developed a deterministic transmission model to provide guidance for optimizing AIV surveillance efforts. The model was calibrated to fit one of the largest LBMs in northern Vietnam at high risk of low pathogenic H7N9 virus introduction from China to identify the surveillance strategy that optimizes H7N9 detection. Results show that (i) using a portable diagnostic device would slightly reduce the number of infected birds leaving the LBM before the first detection, as compared to a laboratory-based diagnostic strategy, (ii) H7N9 detection could become more timely by sampling birds staying overnight, just before new susceptible birds are introduced at the beginning of a working day, and (iii) banning birds staying overnight would represent an effective intervention to reduce the risk of H7N9 spread but would decrease the likelihood of virus detection if introduced. These strategies should receive high priority in Vietnam and other Asian countries at risk of H7N9 introduction.

Dogs as Sentinels for Flavivirus Exposure in Urban, Peri-Urban and Rural Hanoi, Vietnam.

Diseases caused by flaviviruses, including dengue fever and Japanese encephalitis, are major health problems in Vietnam. This cross-sectional study explored the feasibility of domestic dogs as sentinels to better understand risks of mosquito-borne diseases in Hanoi city. A total of 475 dogs serum samples from 221 households in six districts of Hanoi were analyzed by a competitive enzyme-linked immunosorbent assay (cELISA) for antibodies to the pr-E protein of West Nile virus and other flaviviruses due to cross-reactivity. The overall flavivirus seroprevalence in the dog population was 70.7% (95% CI = 66.4-74.8%). At the animal level, significant associations between seropositive dogs and district location, age, breed and keeping practice were determined. At the household level, the major risk factors were rural and peri-urban locations, presence of pigs, coil burning and households without mosquito-borne disease experience (p < 0.05). Mosquito control by using larvicides or electric traps could lower seropositivity, but other measures did not contribute to significant risk mitigation of flavivirus exposure in dogs. These results will support better control of mosquito-borne diseases in Hanoi, and they indicate that dogs can be used as sentinels for flavivirus exposure.

A stochastic network-based model to simulate farm-level transmission of African swine fever virus in Vietnam.

African swine fever virus is highly contagious, and mortality rates reach up to 100% depending on the host, virus dose, and the transmission routes. The main objective of this study was to develop a network-based simulation model for the farm-level transmission of ASF virus to evaluate the impact of changes in farm connectivity on ASF spread in Vietnam. A hypothetical population of 1,000 pig farms was created and used for the network-based simulation, where each farm represented a node, and the connection between farms represented an edge. The three scenarios modelled in this way (baseline, low, and high) evaluated the impact of connectivity on disease transmission. The median number of infected farms was higher as the connectivity increased (low: 659, baseline: 968 and high: 993). In addition, we evaluated the impact of the culling strategy on the number of infected farms. A total of four scenarios were simulated depending on the timing of culling after a farm was infected. We found that the timing of culling at 16, 12, 8, and 6 weeks had resulted in a reduction of the number of median infected farms by 81.92%, 91.63%, 100%, and 100%, respectively. Finally, our evaluation of the implication of stability of ties between farms indicated that if the farms were to have the same trading partners for at least six months could significantly reduce the median number of infected farms to two (95th percentile: 413) than in the basic model. Our study showed that pig movements among farms had a significant influence on the transmission dynamics of ASF virus. In addition, we found that the either timing of culling, reduction in the number of trading partners each farm had, or decreased mean contact rate during the outbreaks were essential to prevent or stop further outbreaks.

A stochastic simulation model of African swine fever transmission in domestic pig farms in the Red River Delta region in Vietnam.

The main objectives of this study were to model various scenarios of African swine fever (ASF) virus transmission among farms in Vietnam and to evaluate the impact of control strategies using North American Animal Disease Spread Model (NAADSM). A total of 7,882 pig farms in the Red River Delta (RRD) region were obtained from the General Statistics Office, and then, random points corresponding to the number of farms in each province were generated as exact farm locations were not available. A total of 10 models were developed, including movement control scenarios. In addition, we conducted sensitivity analysis to assess the impact of indirect contact transmission probability (TP). Overall, the indirect contact exhibited an important role in transmitting the ASF virus. In order to minimize ASF transmission between farms, we found that movement restriction needed to reach a certain level (approximately between 50% and 75%) and that the restriction had to be applied in a timely manner. This study offers valuable insight into how ASF virus can be transmitted via direct and indirect contact and controlled among farms under the various simulation scenarios. Our results suggest that the enforcement of movement restriction was an effective control measure as soon as the outbreaks were reported. In addition, this study provided evidence that high standards of biosecurity can contribute to the reduction of disease spread.

Livestock Development in Hanoi City, Vietnam-Challenges and Policies.

The rapid urban growth of Hanoi city requires a livestock production system that ensures both food security and the livelihoods of dwellers. This paper reviews the existing policies for livestock production of Hanoi city and the changes in livestock population between 2014 and 2018 and identifies major challenges for livestock development of the city. While a remarkable increase of the livestock population in recent years is evident, the dominance of small-scale farms, the presence of animal diseases, the slow progress of transiting farms out of urban areas, as well as the lack of analysis of climate change and gender impacts are major challenges that could affect the livestock development of Hanoi.

A Mixed-Methods Approach to Understanding Knowledge of Mosquito-Borne Infections and Barriers for Protection in Hanoi, Vietnam.

Dengue is a growing problem in Hanoi, with cyclical epidemics of increasing frequency and magnitude. In June 2019, we conducted a cross-sectional survey using mixed methods to investigate how inhabitants of Hanoi perceive and respond to the risk of mosquito-borne diseases (MBD). A total of 117 participants recruited using a stratified random sampling method were interviewed in three districts of Hanoi. Knowledge and practices (KP) regarding MBDs were assessed using a pre-tested questionnaire. Inferential statistics were used to identify factors associated with KP scores and describe the relationship between variables. Additionally, a "risk-mapping" exercise was conducted in a subsample through semi-structured interviews and analyzed qualitatively and quantitatively using the System Effects platform. Factors significantly associated with knowledge scores were education and family history of MBDs. While knowledge and practice scores were found to be positively correlated in the statistical analysis, this was not corroborated by our observations on the field. The results also revealed gaps in knowledge about MBDs and vectors and highlighted a general feeling of powerlessness which prevented the adoption of protective behaviors. Therefore, educational interventions which provide concrete tools to empower communities should have a positive impact on improving vector control.

Temporal patterns and space-time cluster analysis of foot-and-mouth disease (FMD) cases from 2007 to 2017 in Vietnam.

In Vietnam, Foot-and-mouth disease (FMD) is endemic, but no nationwide studies have been conducted to assess the monthly variations and space-time clusters of FMD. The main objective was to identify the temporal patterns and space-time clusters of FMD from 2007 to 2017 using national surveillance data in Vietnam. A total of 163,733 cases were reported from 2007 to 2017. Among them, the proportion of buffaloes (43.31% of total reported cases; 70,909 cases) was highest followed by cattle (30.11%; 49,306 cases), pigs (26.67%; 43,662 cases) and sheep/goats (0.41%; 675 cases). The serotype O was widely distributed across the country while serotype A was observed in Northeast, Central and Southern part of Vietnam while Asia 1 has been not identified since 2007. For monthly variations, most cases were observed during the dry season (from November to March) except Central Highlands. Under the spatial window was set at 50%, a total of seven clusters were identified. The primary cluster was observed from Dec 2009 to Dec 2010 in the northwest (radius: 101.67 km), showing a ratio of 3.75. The secondary cluster was detected in the northeast region (radius: 76.54 km) with a ratio of 3.53 in Feb 2017. The 3rd cluster was the largest with a radius of 176.69 km and located in the southern part of Vietnam. Interestingly, the most temporal clusters included between December and March during the study period. Our findings provide better insight into the temporal patterns and distribution of clusters of FMD in Vietnam. This study provides useful information to policymakers on the hotspot areas and timing of outbreaks. It also identifies when and where national surveillance and control programmes could be implemented more efficiently for the prevention and control of FMD.

Urban livestock-keeping and dengue in urban and peri-urban Hanoi, Vietnam.

Urban livestock provides an important source of food and income, but it may increase the risks for disease transmission. Vectors, such as mosquitoes, might increase and thereby cause an enhanced transmission of infectious diseases, such as dengue fever; considered the most important mosquito-borne viral disease globally. This cross-sectional study evaluated the awareness of dengue fever and investigated how the presence of dengue vectors is affected by the keeping of livestock in urban households in the city of Hanoi, Vietnam. From February to March 2018, during the season of lowest occurrence of dengue in Hanoi, 140 households were interviewed, of which 69 kept livestock. A general trend was observed; respondents living in the Dan Phuong district, a peri-urban district, had better knowledge and practice regarding dengue as compared to the urban Ha Dong district. In total, 3899 mosquitoes were collected and identified, of which 52 (1.33%) were Aedes species. A significant difference between the two districts was observed, with more households in Ha Dong having Aedes spp. mosquitoes (p = 0.02) and a higher incidence of dengue fever (p = 0.001). There was no significant association between livestock-rearing and the presence of Aedes spp. mosquitoes (p = 0.955), or between livestock-rearing and the incidence of dengue fever (p = 0.08). In conclusion, this study could not find any indication that households keeping livestock were at higher risk of dengue virus infections in Hanoi during the season of lowest occurrence of dengue, but clearly indicated the need of more information provided to urban inhabitants, particularly on personal protection.

Seasonal patterns and space-time clustering of porcine reproductive and respiratory syndrome (PRRS) cases from 2008 to 2016 in Vietnam.

Porcine reproductive and respiratory syndrome (PRRS) is an important disease in pig production and is endemic in Vietnam. No nationwide studies have been carried out to understand the spread of PRRS in Vietnam. The main objective of this study was to identify the seasonal patterns and space-time clusters of PRRS from 2008 to 2016 using national surveillance data in Vietnam. A total of 614,219 cases were reported during the period. There was a seasonal pattern with single peak by region (except North Central Coast, showing double peaks in March and June). The seasonal plots from the Northern regions showed a higher peak between March and April, whereas the four regions from Southern part displayed a higher peak between June and August. Overall, outbreaks from the northern part of Vietnam tended to occur 3-4 months earlier than the southern part. When the spatial window was set at 50%, space-time cluster analysis found that the first cluster occurred in the Red River Delta (RRD) (radius: 82.17 km; ratios: 5.5; period: Mar-May/2010) and the second (radius: 50.8 km; ratios: 10.61; period: Aug-Oct/2011) in the Mekong River Delta (MRD) region. Four other clusters were observed in the central and Southern parts. Our findings might provide better insight into the distribution of clusters and temporal patterns of PRRS in Vietnam. This study may provide policy makers with valuable information on the hotspot areas and timing of outbreaks. Also, it identifies when and where national control program could be implemented more efficiently by targeting resources for the prevention and control of PRRS.

Clade-level Spatial Modelling of HPAI H5N1 Dynamics in the Mekong Region Reveals New Patterns and Associations with Agro-Ecological Factors.

The highly pathogenic avian influenza (HPAI) H5N1 virus has been circulating in Asia since 2003 and diversified into several genetic lineages, or clades. Although the spatial distribution of its outbreaks was extensively studied, differences in clades were never previously taken into account. We developed models to quantify associations over time and space between different HPAI H5N1 viruses from clade 1, 2.3.4 and 2.3.2 and agro-ecological factors. We found that the distribution of clades in the Mekong region from 2004 to 2013 was strongly regionalised, defining specific epidemiological zones, or epizones. Clade 1 became entrenched in the Mekong Delta and was not supplanted by newer clades, in association with a relatively higher presence of domestic ducks. In contrast, two new clades were introduced (2.3.4 and 2.3.2) in northern Viet Nam and were associated with higher chicken density and more intensive chicken production systems. We suggest that differences in poultry production systems in these different epizones may explain these associations, along with differences in introduction pressure from neighbouring countries. The different distribution patterns found at the clade level would not be otherwise apparent through analysis treating all outbreaks equally, which requires improved linking of disease outbreak records and genetic sequence data.