This study describes an MCDA approach to determine the risk of environmental persistence and waterborne transmission of AIV in a wild/domestic bird interface in central Mexico. The AIVs spread within wild waterbird populations may lead to viral contamination of natural habitats (Ahrens et al., 2022). During the winter season, a high density of migrating Anseriformes cohabit with resident species in the Atarasquillo wetland (Gaytan-Cruz et al., 2020; SEMARNAT-CONANP, 2018). One of the most remarkable results is that the coldest month evidences a higher persistence risk of AIV. Previous research has found a strong effect of temperature on environmental viability (Dalziel et al., 2016; Martin et al., 2018). Virus may remain infective for a few days at > 20°C, a few weeks at 10°C, and for months at < 0°C in surface water (Nazir et al., 2010). Therefore, freshwater habitats could be a year-to-year reservoir of viruses to infect bird populations mainly in winter (Lang et al., 2008; Ramey et al., 2022).
Water sources represent a crucial environment in which infectious AIVs may reside outside of a biotic reservoir (Ramey et al., 2022). Recently, some mass mortality events in free-living mammal species such as the harbor seal are likely associated to environmental transmission of HPAI H5N1. Likewise, global HPAI outbreaks in poultry are possibly linked to indirect contact with wild birds (European Food Safety Authority et al., 2023). In our study, we did not attempt to record contact between household animals and wild birds. However, almost all the poultry farms close to the Atarasquillo wetland evidenced a higher transmission risk. This outcome is in line with Si et al. (2013), who reported the occurrence of outbreaks mostly in areas where the location of farms or animal trade areas overlap with habitats for wild birds. Therefore, animal populations close to wetlands pose a high risk of influenza outbreaks (Hassan et al., 2020).
Shallow water bodies represent an AIV transmission medium for aquatic wild birds. Fecal matter, plumage, and oropharyngeal excretions with viral particles potentiate viral transmission efficacy in surface waters (Ahrens et al., 2022). In our study, artificial ponds within poultry farms and channels of water evidenced a high risk of AIV persistence. Previous research has reported that a low viral titer suspended in the surface water is sufficient to start and set off an infection in wild ducks within a few days, mainly in a low volume of water. Small water bodies can hold moderate to high viral RNA loads for a long period due to a lower diluting effect on the virus available for infection compared to large water bodies (Ahrens et al., 2022).
A limited volume of accessible water may provide high viral titers and a long course of infection (Ahrens et al., 2022). According to Leung et al. (2007) poultry drinking water can provide higher isolation rates of the influenza virus than fecal droppings. Likewise, drinking water troughs may contain a great AIV subtype diversity (Mateus-Anzola et al., 2021). Interestingly, in our study, a very high-risk persistence score was found in some poultry farms’ drinking water. Experimental laboratory studies have reported AIV survivability of 8 − 48 hours in drinking water troughs, as well as a viral concentrating effect. Nevertheless, survival time depends on the level of chlorination and the organic content of the water (Ahrens et al., 2022; Leung et al., 2007).
Effluents constitute an important factor in viral dissemination among poultry. Animal slurry (a liquid mixture of feces and urine added to litter, feed residues, washing water, and rainwater) contributes to AIV dissemination on poultry farms (Schmitz et al., 2020). Environmental samples collected from sewage may have high nucleic acid positivity rates of influenza (Bo et al., 2021; Guo et al., 2021). However, complex environments with high content of biological material (manure or feces) may retain infectivity for shorter periods than natural water (Schmitz et al., 2020). This is consistent with our findings where a low persistence risk was evidenced in wastewater.
The application of experimental results to field realities is complicated by the complexity and scale of these ecosystems (Stallknecht et al., 2010). Physicochemical properties such as temperature, pH, conductivity, ammonia concentration, and salinity can affect virus survival in different liquid environments (Keeler et al., 2014; Ramey et al., 2022; Schmitz et al., 2020). Nevertheless, other identified and unidentified factors prevailing in natural surface water may contribute to the effect of environmental persistence on AIV transmission dynamics among hosts (Martin et al., 2018; Nazir et al., 2010). The AIV subtype and its pathogenicity, bird density, UV light, and presence of biological compounds (freshwater crabs and microbial flora) were not evaluated in the MCDA. Likewise, Further studies are required to assess the influence of viral, host, and biotic factors on AIV persistence and transmission in the wildlife-livestock interface.
In conclusion, the Atarasquillo wetland has eco-epidemiological factors that may enhance AIV survival and waterborne dissemination mainly in poultry farms close to the wetland. This MCDA provides valuable baseline information to identify the optimal environmental characteristics and high-risk areas for AIV spreading as well as to develop early intervention strategies.