Shared infections at the wildlife–livestock interface and their impact on public health, economy, and biodiversity

Abstract

Shared infections at the livestock–wildlife interface are of major concern to public health, economy, and biodiversity. Over 20% of global animal production losses are caused by animal diseases. Factors such as exponential growth in animal and human populations, rapid urbanization, evolving farming systems, increased interaction of livestock and wildlife, ecosystem changes, globalization of animal and animal product trade, and shifts in pathogen–host ecology contribute to the emergence of new disease interfaces. The spread of shared infectious diseases in any interface is influenced by multiple factors and can occur within communities with a complex structure, often with many hosts involved in infections transmission dynamics. One Health focused collaborative efforts involving multiple disciplines can be effective in improving health of animal, human, and environment in general. Shared infections at the livestock–wildlife “interface” are commonly referred to as “spillover” or “cross-species transmitted” infections (Table 1). They underscore the interconnectedness of wildlife and livestock ecosystems and frequently impact multiple facets of public health, economy, and biodiversity. Lately, there has been a growing focus on these diseases, as evidenced by a multitude of publications on the subject (Wiethoelter et al. 2015). Understanding and, consequently, preventing these infections, is crucial for protecting animal health, safeguarding food security, and mitigating public health risks. Definition of terms Livestock and wildlife have coexisted, sharing and competing for resources in diverse ecosystems for millennia. However, as the human population continues to grow, resource sharing increasingly occurs at interfaces along the boundaries of heavily human-influenced environments (Vicente et al. 2021). Conversely, some changing dynamics, such as population increase of certain wildlife species, like the wild boar (Sus scrofa), have brought domestic and wild species into closer contact at these interconnecting interfaces, resulting in the spillover of infectious diseases (Santos et al. 2022). Animal production, contributing to more than 40% of the total global agriculture output, plays a vital role in supporting the livelihoods of over >20% of the world’s population (FAO 2023). According to the World Health Organization (WHO) reports, over 20% of global animal production losses are caused by different animal diseases (WHO 2023). Additionally, infectious diseases in animals that have zoonotic potential pose significant risk to public and global health. Notably, the majority (>75%) of emerging infectious diseases (EID) in the last century were zoonotic in nature (Jones et al. 2008). Gaining deeper insights into the epidemiology and ecology of shared infections is essential to prevent, curtail, and mitigate their impacts. A multifaceted approach, including wildlife disease surveillance, studies on disease ecology, and research on potential critical points of infections transmission at the interfaces, can prove effective in addressing many of these emerging and re-emerging diseases. There are numerous important and relevant multihost shared infections worldwide, caused by bacteria, viruses, or parasites (Figure 1). Over the past 30 years, several infections and subsequent diseases at the livestock–wildlife interface have gained prominence due to their global impact on economy and public health. Some of the primary livestock species (i.e., poultry, pigs, bovines, small ruminants) shared diseases are: Avian Influenza (AI), salmonellosis, and New Castle disease in poultry; African swine fever (ASF), Aujeszky’s disease, and Streptococcus suis infection in pigs; tuberculosis (TB), brucellosis, and Rift Valley fever (RVF) in bovines; and peste des petits ruminants (PPR), foot and mouth disease (FMD), and bluetongue disease in small ruminants. These diseases have a global distribution and affect various livestock and wildlife species. Here, we highlight one representative infectious disease from each of the four animal production (food) species that are included in the single list of notifiable diseases of the World Organization for Animal Health (WOAH 2023). Notable shared infections in the livestock–wildlife interface categorized by continent and total animal production by regions. Protein quantities are indicated in millions of tons. The upper image has been modified based on data from a FAO source (https://www.fao.org/gleam/es/). The selection of shared infections has been adapted from Vicente et al. (2021), focusing on beef, pork, chicken, small ruminants, and buffalo species. AI, commonly known as bird flu, is caused by avian influenza Type A virus (family: Orthomyxoviridae, genus: Alpha influenza virus). AI affects both domestic and wild birds worldwide and spreads through direct contact with infected bird secretions or indirectly via contaminated feed, air, and water. Increased outbreak occurrences at the interface between animal production (poultry) and wild and migratory birds with extensive geographical reach have contributed to the global spread of the virus (Bessière et al. 2022). In 2022, 67 countries across five continents reported H5N1 high pathogenic avian influenza outbreaks in poultry and wild birds. In 2023, an additional 14 countries reported outbreaks, mainly in the Americas, as the disease continued its southward expansion (EFSA 2023). Moreover, AI’s spread has been exacerbated by the rapid globalization of human migration and trade, resulting in significant economic losses. For instance, AI-related losses in the US exceeded $3 billion in 2015 (Böckmann 2021). Overall, the epidemiology of AI has undergone significant changes in recent years, rendering it as one of the most challenging pathogens from a global health perspective. Its impact is particularly pronounced on bird biodiversity and the poultry industry’s economy (Bessière et al. 2022). Given the unprecedented spread of the H5N1 strain of AI virus among birds and mammals, the United Nations Health agencies (FAO, WHO, and WOAH) are urging countries to take some immediate preventive actions, such as strengthening biosecurity measures and promoting good hygiene practices, implementing comprehensive immunization of poultry, rapid detection and reporting animal outbreaks, and establishing an effective One Health based influenza surveillance system (EFSA 2023). ASF is a highly contagious viral disease caused by a DNA virus (family: Asfarviridae, genus: Asfivirus) that affects both domestic pigs and wild boar. It is transmitted through direct and indirect contact, including through ticks. Outbreaks of ASF at the wildlife–livestock interface involving transmission between domestic and wild pigs have been commonly reported globally (Mugabi and Duffy 2023). ASF has traditionally been present in the African continent and had its first occurrence in the European Union in 2014. In August 2018, the virus was detected in the People’s Republic of China, and in 2021, the disease reappeared in the Americas (in the Dominican Republic and Haiti; WOAH 2022). It resulted in decrease in world pig meat production between 2018 and 2019 by 11 million tons. Pork is the second most widely consumed meat globally, having been recently overtaken by poultry meat (FAO 2023), and in recent years, ASF has emerged as one of the major challenges to the pork industry, leading to substantial economic losses, especially in Asian countries with recent continuous outbreaks reported since late 2018 (FAO 2022b). Estimated direct production loss due to ASF in the People’s Republic of China are expected to be around $55 billion to $130 billion (Weaver and Habib 2020). Lack of early detection system and containment strategies in many countries has helped spread of the disease. Proper biosecurity measures can be an effective universal preventive action to control ASF, since there is no treatment or vaccine for the disease (Urbano and Ferreira 2022). TB is a chronic bacterial disease caused by the Mycobacterium tuberculosis complex—of which M. tuberculosis and M. bovis predominantly infect humans and livestock, respectively. TB is one of the most important global zoonotic diseases affecting humans, livestock and wildlife, and with the emerging challenges associated with the antimicrobial resistance to various antibiotics, TB has emerged as one of the greatest threats to the global health (Lee et al. 2022). The highest prevalence of bovine TB is in Africa and some regions of Asia, but the disease is globally present. Historically, TB affected humans and livestock; however, it has extended to wildlife as well (Cowie et al. 2016). In humans, over 80% of cases and deaths are in low- and middle-income countries, but TB occurs in every part of the world (TB is the 13th leading cause of death and the second leading infectious killer after COVID-19) (WHO 2023). In livestock, complete elimination of the disease is complicated by the persistent infection of wild animals. Between January 2017 and June 2018, 82 (44%) of the 188 countries and territories that notified the OIE/WOAH of their bovine TB status had been affected, indicating disease widespread distribution (Murai et al. 2019). Some of the interesting interfaces where TB transmission is known to spill-over within and between species are: human-Asian elephant (Elephas maximus) (captive and wild) in Nepal and India, European badger (Meles meles)-cattle in the UK, wild boar-cattle in the Iberian Peninsula, white-tailed deer (Odocoileus virginianus)-cattle in the United States, and African buffalo (Syncerus caffer)-cattle in South Africa (Cowie et al., 2016; Santos et al., 2022; Rajbhandari et al., 2023). There is inadequate data showing the scale of economic loss due to bovine TB in developing countries; however, in countries with a large livestock population such as Ethiopia, the loss is substantial (Azami and Zinsstag 2018). PPR is caused by a RNA virus (family: Paramyxoviridae, genus: Morbillivirus) that affects 80% of the world’s sheep and goat population (Soula et al. 2018). PPR is highly contagious with a high mortality rate. Additionally, it also affects many of the wild ungulate species and pose both conservation and ecological threat. PPR is currently considered as one of the main animal transboundary infections that pose a direct threat to livestock production in many developing countries, particularly in western Africa and south Asia (Banyard et al. 2010), but also in Europe and the Middle East. The annual global economic impact of PPR has been estimated to be between US$1.4 and 2.1 billion (FAO 2022a). In 2015, the Peste des petits Ruminants Global Eradication Programme (PPR-GEP) was established and implemented by the FAO and the WOAH. Since then, strategic plans (vaccination, diagnosis, and surveillance and monitoring) have been implemented, and currently, 10 of the 67 countries with active or recent evidence of PPR infection have had no outbreaks between 2015 and 2019, supporting the positive impact of the control measures (FAO 2022a). The lack of knowledge regarding the role of wildlife in the epidemiology of this and other diseases at the wildlife–livestock interface hinders the implementation of necessary integrated disease control and management interventions for livestock. The emergence of new infection/disease interfaces is driven by several factors, including exponential growth in animal and human populations, rapid urbanization, evolving farming systems, closer integration between livestock and wildlife, encroachment into forests, shifts in ecosystems, globalization of animal and animal product trade, and changes in pathogen-host ecology. These factors also increase the likelihood of pathogen transmission between livestock and wildlife populations. Currently, over a quarter of the world’s ice-free land, equivalent to over half of the agricultural land, is designated for livestock grazing, while roughly one-third of croplands are utilized for livestock feed production (FAO 2023). The global livestock population encompasses nearly 1.5 billion cattle, 2.2 billion small ruminants, over 35 billion chickens, and nearly 1 billion pigs. World meat [defined as the flesh of animals (excluding fish) used for food] production reached 337 million tons in 2020, up 45%, or 104 million tons compared with 2000, with chicken meat representing more than half the increase (FAO, 2022b). This increasing demand for production has resulted in habitat loss caused by the expansion of agriculture and livestock operations, forcing wild animals to seek food and shelter in proximity to animal production areas. Consequently, species are now experiencing higher levels of intermingling, leading to an increase in infection transmission (Figure 2). Simultaneously, wildlife populations, particularly ungulates, have been on the rise due to various factors such as declining legal hunting accompanied by a decrease in social acceptance (Gortázar et al. 2015). Elevated densities and expanded geographical distributions of susceptible hosts can also contribute to the proliferation of pathogens and the circulation of new variants and mutations (Baker et al. 2022). Traditional models for inter-species or vector-borne disease dynamics have typically operated on the assumption that the transmission rate is proportional to the local abundances of both the donor and recipient species (Becker et al. 2019). promoting the of livestock and wildlife the integration of various including pathogen control in production implementation of biosecurity practices, and interfaces resulting from the expansion of in livestock and wildlife species. and interfaces between animal production and wildlife habitat higher likelihood of pathogen spillover and of African (ASF), caused by a DNA between wild boar and pigs at a interface is a good of such A biosecurity in the animal production and of between wildlife habitat and livestock can mitigate such pathogen spillover and transmission human, and health are and on the health of the ecosystems is global the and of species within a is any in human This is driven by human such as of for and the for local or 2021). 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