Spatiotemporal and risk analysis of H5 highly pathogenic avian influenza in Vietnam, 2014–2017

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Abstract

The aim of this study was to describe the spatiotemporal distribution of H5 HPAI outbreak reports for the period 2014–2017 and to identify factors associated with H5 HPAI outbreak reports. Throughout the study period, a total of 139 outbreaks of H5 HPAI in poultry were reported, due to either H5N1 (96 outbreaks) or H5N6 (43 outbreaks) subtype viruses. H5N1 HPAI outbreaks occurred in all areas of Vietnam while H5N6 HPAI outbreaks were only reported in the northern and central provinces. We counted the number of H5N1 and H5N6 outbreak report-positive districts per province over the four-year study period and calculated the provincial-level standardized morbidity ratio for H5N1 and H5N6 outbreak reports as the observed number of positive districts divided by the expected number. A mixed-effects, zero-inflated Poisson regression model was developed to identify risk factors for outbreak reports of each H5N1 and H5N6 subtype virus. Spatially correlated and uncorrelated random effects terms were included in this model to identify areas of the country where outbreak reports occurred after known risk factors had been accounted-for. The presence of an outbreak report in a province in the previous 6–12 months increased the provincial level H5N1 outbreak report risk by a factor of 2.42 (95% Bayesian credible interval [CrI] 1.27–4.60) while 1000 bird increases in the density of chickens decreased provincial level H5N6 outbreak report risk by a factor of 0.65 (95% CrI 0.38 to 0.97). We document distinctly different patterns in the spatial and temporal distribution of H5N1 and H5N6 outbreak reports. Most of the variation in H5N1 report risk was accounted-for by the fixed effects included in the zero-inflated Poisson model. In contrast, the amount of unaccounted-for risk in the H5N6 model was substantially greater than the H5N1 model. For H5N6 we recommend that targeted investigations should be carried out in provinces with relatively large spatially correlated random effect terms to identify likely determinants of disease. Similarly, investigations should be carried out in provinces with relatively low spatially correlated random effect terms to identify protective factors for disease and/or reasons for failure to report.

Introduction

Highly pathogenic avian influenza (HPAI) in Asia caused by H5Nx subtype viruses first emerged in 1996 in Guangdong, China. Viruses in this lineage (A/goose/Guangdong/1/1996 (H5N1), abbreviated as Gs/GD/96-lineage) consequently caused devastating morbidity/mortality in domestic poultry (Xu et al., 1999; Sims et al., 2005). Importantly, viruses in this lineage have spread globally via migratory wild birds and/or trade of poultry commodities, posing a major concern to the poultry industry worldwide (Lycett et al., 2016; Sims et al., 2017). In addition, H5 HPAI viruses pose a threat to human health due to their zoonotic potential (The World Health Organization (WHO, 2018).

In Vietnam, the first outbreaks of Gs/GD/96-lineage H5 HPAI in poultry were reported in late 2003. Thereafter the disease spread rapidly and triggered severe epidemics in domestic birds across the country between 2003 and 2005 (Nguyen, 2005). Despite intensive control efforts, H5 HPAI outbreaks continue to occur in Vietnam (The World Organization for Animal Health (OIE, 2018). Several studies have been carried out to clarify the ecological and epidemiological features of H5 HPAI in Vietnam, however the determinants of disease occurrence are still not fully understood. In some countries, H5 HPAI viruses are maintained through circulation in wild birds and domestic waterfowl such as ducks, Muscovy ducks and geese (Hulse-Post et al., 2005; Kida, 2008; Pantin-Jackwood et al., 2017). Limitations on identifying key risk factors and sources of H5 HPAI and incompletely effective interventions to limit the impact of identified risk factors have impeded control efforts for H5 HPAI in Vietnam (Pfeiffer et al., 2013; Sims et al., 2017).

A number of studies have demonstrated the complexity of agro-ecological, anthropogenic and topographic risk factors associated with H5 HPAI disease dynamics (Gilbert and Pfeiffer, 2012; Paul et al., 2014; Delabouglise et al., 2017). In particular, eco-anthropogenic interaction is thought to be one of the most important drivers for H5 HPAI spread (Pfeiffer et al., 2013; Delabouglise et al., 2017). A characteristic of Vietnamese agriculture is its traditional farming practice of intensive rice cultivation associated with poultry production, where ducks are used to scavenge leftover grains from rice paddies. This can lead to exposure of domestic poultry to infected waterfowl or wild birds (Sims et al., 2005; Pfeiffer et al., 2013). Furthermore, the Vietnamese poultry industry is comprised of large numbers of backyard and small-scale producers with approximately half of the households in rural areas raising backyard poultry (Otte et al., 2006). Continuous mixing of poultry species together with a low level of biosecurity in backyard flocks facilitates incursion and maintenance of H5 HPAI viruses, especially given that many of these birds are sold through live poultry markets that have limited or no control on the health status of birds submitted for sale.

The Vietnamese poultry industry has experienced rapid growth in recent years, mainly due to an increase in the number of intensively managed, commercial sector farms. While total bird numbers have increased, commercial sector farms still account for only a relatively small proportion (approximately 3.25%) of the total number of poultry farms in Vietnam (The World Bank, 2017). Anthropogenic factors such as cultural practices, food preferences and trading activities are important drivers of H5 HPAI spread (Fournie et al., 2016; Delabouglise et al., 2017; Meyer et al., 2018). In regards to topography, several characteristics have been identified as likely risk factors for H5 HPAI, including the density of paddy fields, proximity of poultry flocks to water, annual precipitation and elevation (Loth et al., 2011; Paul et al., 2014). Places where H5 HPAI viruses remain endemic tend to have complex poultry production and marketing chains, few restrictions on movement and veterinary services that are still developing the capacity to monitor all poultry flocks (Food and Agriculture Organization of the United Nations (FAO, 2011).

In Vietnam, a number of studies have been carried out to describe and explain the spatiotemporal distribution of outbreak occurrence during the early phase of the H5 HPAI epidemic (Pfeiffer et al., 2007; Minh et al., 2009). Most recently, Mellor et al. (2018) investigated the spatiotemporal epidemiology of H5N1 and H5N6 HPAI viruses using active surveillance programs deployed in live bird markets during 2011–2015. Because H5 HPAI outbreaks continue to occur throughout Vietnam, there is a need to provide better understanding of characteristics that increase the risk of disease.

With this background, the objectives of this study were to: (1) describe the spatial and temporal distribution of H5 HPAI outbreaks at the provincial level in Vietnam for the period 2014–2017; and (2) identify risk factors for H5 HPAI outbreak reports. Outcomes of this study provide impetus for targeted assessments of provinces identified as either low or high risk of H5 HPAI. In particular, for low risk provinces it is of critical importance to identify characteristics that are truly protective for disease and/or determine if low risk is simply a consequence of failure to report.

Section snippets

Study areas and period

Administrative units of Vietnam are organized into three hierarchical levels: provinces/centrally-governed cities, districts and communes (wards). The country is comprised of 63 provinces/centrally-governed cities, 678 districts and 10,805 communes (according to the Geographic Information System (GIS) data). The spatial unit of interest in this study was the province. Provincial level datasets and digital maps were retrieved from the open-source DIVA GIS website.1

Descriptive analysis of H5N1 and H5N6 HPAI outbreaks

For the period 2014 to 2017 a total of 139 H5 HPAI outbreaks, caused by one of the two H5N1 or H5N6 subtype viruses, were reported in all regions of Vietnam. There was considerable variation in the number of outbreak reports per region, per year and quarter for each subtype virus (Fig. 1A and Supplementary Fig. 1A–D). Six provinces (Dak Lak, Ha Tinh, Nghe An and Quang Ngai in the central region and Can Tho, Vinh Long in the South) had more than six outbreak reports in all years, accounting for

Discussion

After triggering enormous devastation in 2003 and 2004, H5 HPAI viruses have persisted and caused significant damage to the poultry industry and occasional human deaths in Vietnam. The disease is constantly changing in association with variability of viral strains and dynamics, changes in the composition and distribution of the host population and the effect of interventions to control disease such as the use of vaccination. For these reasons, there is a need to continuously monitor the

Conclusion

A total of 139 H5 HPAI outbreaks were reported in all regions of Vietnam during the period 2014–2017. All of the H5 HPAI outbreaks were caused by one of the two subtype viruses, H5N1 and/or H5N6. The frequency of outbreak reports of H5N1 and H5N6 varied by province, year and quarter. We document distinctly different patterns in the spatial and temporal distribution of H5N1 and H5N6 outbreak reports. Most of the variation in H5N1 report risk was accounted-for by the fixed effects included in the

Conflict of interest

The authors have declared that no competing interests exist.

Acknowledgments

We are grateful to the Vietnamese Department of Animal Health (DAH). We sincerely thank Drs. Pham Van Dong and Nguyen Thu Thuy from DAH for their supports. We also thank the Program for Leading Graduate Schools (F01) from the Japanese Society for the Promotion of Science (JSPS) and the Japanese Initiative for Global Research Network on Infectious Diseases (J-GRID) from the Japanese Agency for Medical Research and Development (AMED) for supporting our international collaborative activities.

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