Antimicrobial resistance (AMR), often referred to as the “silent pandemic,” poses a severe threat to global public health (Laxminarayan, 2022). While AMR is a naturally occurring phenomenon, the widespread overuse and misuse of antimicrobials over the last 80 years have dramatically accelerated its emergence and spread (Christaki et al., 2020). Although AMR is a worldwide challenge affecting developed and developing countries, its prevalence differs significantly across regions (Frost et al., 2019). Reports show a rapid global increase in AMR and its relentless spread between countries (Aljeldah, 2022). The World Health Organization (WHO) has warned of a “post-antibiotic era” where common, previously treatable bacterial infections could become fatal (Shankar and Balasubramanium, 2014). This means that the impact of AMR on humans and animals is profound and complicated, leading to longer hospital stays, chronic infections, increased economic burdens, and increased mortality (Ferraz, 2024). If unchecked, AMR is projected to cause 10 million deaths by 2050 (O’Neill, 2016).

Escherichia coli (E. coli) is a key species for monitoring AMR globally (Anjum et al., 2021). As a member of the Enterobacteriaceae, E. coli has developed significant resistance to crucial broad-spectrum cephalosporins. This resistance is mainly due to plasmid-mediated extended-spectrum beta-lactamases (ESBLs) and both chromosomal and plasmid-encoded AmpC beta-lactamases (pAmpC), exacerbating the fight against AMR (Duggett et al., 2020). Interestingly, even though wild birds have limited direct exposure to antimicrobials, they have been identified as potential reservoirs of resistant E. coli. Often, these birds pick up resistant strains when foraging in polluted environments, like antimicrobial-treated fields (Blanco and Bautista, 2020), or contaminated surface water (Yuan et al., 2021). For instance, studies in Egypt found 100% genetic similarity between mcr-1-producing E. coli from a migratory bird and surface water collected from the same trapping sites (Ahmed et al., 2019). This suggests that wild birds, through their mobility and ecological adaptability, can acquire and spread AMR bacteria and genes to humans, livestock, and the environment.

To combat AMR, the WHO adopted a global action plan (GAP) in May 2015. The GAP comprised five interdependent objectives: (1) to improve awareness and understanding of AMR through effective communication, education and training; (2) to strengthen the knowledge and evidence base through surveillance and research; (3) to reduce the incidence of infection through effective sanitation, hygiene and infection prevention measures;(4) to optimize the use of antimicrobial medicines in human and animal health; and (5) to develop the economic case for sustainable investment that takes into account the needs of all countries and to increase investment in new medicines, diagnostic tools, vaccines and other interventions. The GAP objectives were adopted as national action plans (NAPs) by most countries in their fight against AMR (World Health Organization, 2015).

In 2020, the Quadripartite [the WHO, the Food and Agriculture Organization of the United Nations (FAO), the World Organization for Animal Health (OIE), and the United Nations Environment Programme (UNEP)] was formed. The Quadripartite urged the stakeholders, including policy-makers, technical staff, academics, researchers, members of civil society, private-sector representatives, development partners and donors, within member states to move from an early to a sustainable implementation phase through a sector-specific programme and a joint collaborative One Health approach at local, national, regional and global levels, guided by the 2015 GAP. To sustainably balance and optimize the health of humans, animals, plants, food production and environmental protection and ecosystem interfaces, the Quadripartite recommended (1) a robust governance structure to ensure accountability and acceleration of NAPs implementation in countries, (2) innovations to secure the future, (3) global collaborations for more effective action, (4) investments for a sustainable response and (5) to strengthen accountability and global governance. By 2021, about 84% of member states provided annual reports on the implementation of their multi-sectoral NAPs against AMR (World Health Organization, UNEP United Nations Environment Programme and World Organisation for Animal Health, 2023).

Despite their significant role in spreading AMR, wildlife, particularly wild birds, and the environment are often overlooked in health security strategies, which tend to primarily focus on humans, domestic animals, and plants. However, monitoring the carriage of resistant bacteria in wild birds should be a priority within the One Health approach to combat AMR (Guardia et al., 2024). Wild birds utilize eight major migratory routes globally, including the prominent East Atlantic, Black Sea-Mediterranean, and East Asia-East Africa flyways (Seleem et al., 2021). As birds traverse these routes, they can acquire and disseminate AMR bacteria and genes across international borders. Notably, Southeast Asia is a major hot spot for AMR in animals (Chua et al., 2021). Africa, serving as a major flyway for over two billion Palearctic migratory birds, plays a crucial role in the seasonal movement of these birds across the African-Eurasian flyway. This global movement makes migratory birds potential key contributors to the worldwide spread of AMR (Guilherme et al., 2023). The first AMR strains of E. coli in wildlife were isolated in pigeons in 1975 (Sato et al., 1978). Since then, numerous studies in various countries have recognized wild birds as potential reservoirs and disseminators of antimicrobial-resistant E. coli.

This systematic review examines the current data on the role of migratory and resident wild birds as potential reservoirs of resistant E. coli and its associated genes globally. It specifically focuses on resistance to ESBL and other WHO CIA List. The review further evaluates evidence suggesting wild birds as potential disseminators of resistant E. coli, especially in studies that genetically link resistant strains found in wild birds to those in other One Health sectors. The review analyzes resistance patterns by geographic locations, wild bird species, income-indexes of countries, socio-economic, behavioral, and political influences on the occurrence of AMR in wild birds, and evidence of phylogenetic relationships that indicate cross-border transmission or involvement in the broader quintessential One Health AMR matrix. Finally, based on the analyzed data, the review provides recommendations for integrating wild birds into the One Health strategies to combat AMR.

We performed a systematic review following the Preferred Reporting Items for Systematic Reviews (PRISMA; Page et al., 2021; Supplementary Table 1). The two authors defined the research questions, objectives, search strategy, and inclusion/exclusion criteria.

Antimicrobial resistance E. coli has been found in wild birds for nearly five decades, with the first isolation reported in pigeons in 1975 (Sato et al., 1978). This review identified 51 studies examining AMR E. coli in wild birds, including both migratory and resident populations. Research remains limited in LMICs except in Nigeria, Egypt, and Bangladesh. Interestingly, despite fewer studies, wild birds in LMICs showed higher levels of AMR E. coli, suggesting a link between AMR burden and poor water, sanitation, and hygiene (WASH) infrastructure, poor antimicrobial regulation, and limited healthcare resources. For example, Bangladesh records extensive antimicrobial use in agriculture and minimal waste management (Hasan et al., 2014), while Nigeria lacks proper regulations on antimicrobial use in both human and veterinary medicine (Fashae et al., 2021). In contrast, HICs enforce stricter regulations on AMR use and maintain better WASH systems, contributing to lower AMR levels (Stedt et al., 2014). However, one HIC study recorded a deviation from this trend, where European Starlings from commercial feedlots across five USA states showed high AMR levels (Chandler et al., 2020). Additionally, most studies in both HICs and LMICs focused on non-water birds, probably due to; their proximity to human activities such as landfills, farms, abattoirs, dump sites, agricultural run-offs, urban centers, direct or indirect contact with humans, domestic and companion animals, and their diverse ecological niches and feeding habits.

The presence of phenotypic and genotypic resistant E. coli in wild birds across all continents highlights their potential role as reservoirs for AMR and a public health concern for humans, animals, and the environment. A major concern is E. coli’s ability to acquire and spread resistances to the WHO CIA List for human medicine. ESBL-producing E. coli are particularly problematic as mobile genetic elements (MGEs) facilitate the transfer of these resistances, making E. coli both a donor and recipient of AMR in horizontal gene transfer (Guenther et al., 2017). ESBL-producing E. coli, once confined to clinical settings, are now increasingly found in wild birds (Guenther et al., 2017). Furthermore, MGEs enable efficient transfer of these resistance across different species and ecosystems (Báez et al., 2015), contributing to the rise of extended-spectrum beta-lactam resistances within the One Health framework (Hasan et al., 2016; Atterby et al., 2017; Fahim et al., 2019; Belmahdi et al., 2022). Migratory birds may further accelerate this spread by carrying AMR genes across regions as white storks migrate between Europe and North Africa (Bouaziz et al., 2018), brown-headed gulls migrate through Tajikistan, Southern China, Pakistan, India, Bangladesh, Myanmar, Sri Lanka, Vietnam and Thailand (Hasan et al., 2014); franklin’s gulls migrate from North America to the Chilean coast (Báez et al., 2015); while different migratory bird species transit the Arabian Peninsula from Africa, Asia and Europe (Elsohaby et al., 2021). Even resident wild birds, though not involved in the long-range AMR spread, can contribute to local transmission to other One Health sectors (Hasan et al., 2016; Oh et al., 2016; Fahim et al., 2019). This calls for preventive and sustainable measures under the One Health framework, guided by the WHO’s GAPs and the Quadripartite in the fight against AMR spread.

Despite increasing reports of AMR E. coli in wild birds globally, the origin of these resistant traits remains largely unknown. Only 49% of the studies suggested the potential sources of AMR contamination, and a mere 27.5% verified these hypotheses. The detection of resistant E. coli even in wild birds from remote areas (Atterby et al., 2016), further complicates the understanding of transmission pathways. Despite this, numerous studies have established a correlation between high levels of AMR E. coli in wild birds and human-impacted environments. These environments include; agricultural fields (Vogt et al., 2018, 2019; Fahim et al., 2019; Blanco and Bautista, 2020; Chandler et al., 2020; Elsohaby et al., 2021; Anueyiagu et al., 2023), dumps (Stedt et al., 2014; Merkeviciene et al., 2018), abattoirs (Fashae et al., 2021), industrial areas (Stedt et al., 2014), contaminated water bodies (Ahmed et al., 2019; Nabil et al., 2020; Yuan et al., 2021) landfills (Bonnedahl et al., 2014), and areas with high human density such as cities (Belmahdi et al., 2022; Tarabai et al., 2023) and beaches (Hasan et al., 2014; Hasan et al., 2016; Mukerji et al., 2019). Fortunately, some sequencing studies have confirmed genetic links between the AMR E. coli isolated in wild birds and their hypothesized sources (Supplementary Table 4). This evidence strongly suggests that human activities and their associated environments are major contributors of AMR in wild bird populations. Even in protected areas with minimal human interaction (Machado et al., 2018; Gambino et al., 2021; Suenaga et al., 2019; Yapicier et al., 2022), studies have found that wild birds carry resistant E. coli strains. This suggests two main possibilities: either the birds are a natural reservoirs for these resistant strains, or migratory birds are the primary way these strains are being spread to such isolated regions. Further research is vital to fully understand these complex transmission dynamics and develop effective mitigation strategies.

The ubiquity of AMR and their associated genes in the natural ecosystems makes it challenging to trace the exchanges of AMR-associated genes between humans, animals, and the environment, hindering the identification of emerging resistant genes and spread (Vittecoq et al., 2016; Laborda et al., 2022). Our review data indicates wild birds often acquire AMR strains through foraging and direct contact with contaminated environments. Water is considered a key transmission route of AMR to wild birds. This can be through direct consumption of contaminated water or by carrying antimicrobial residues on their feathers or legs in the case of water birds. This phenomenon was observed with aquatic egrets, which transported resistant E. coli from the contaminated Jin River to park soil (Wu et al., 2018). These water bodies often receive discharge from domestic wastewater treatment plants (Fashae et al., 2021), hospital and pharmaceutical wastewaters, and agricultural run-offs (Elsohaby et al., 2021). Additionally, wild birds can acquire AMR from agricultural run-offs, which may contain sub-therapeutic concentrations of antimicrobials either in manure or animal feed. This has been demonstrated by the isolation of AMR E. coli in migratory birds transiting through Asfar Lake, a large artificial water body formed from the agriculture and livestock drainage water of the earthen drainage network in Saudi Arabia (Elsohaby et al., 2021). Other significant sources of AMR for the birds include untreated landfills (Atterby et al., 2016), dumps, abattoirs, and carcass dumps. These sites often contain human and animal fecal matter and food waste that might be rich in AMR bacteria. It has been suggested that scavengers feeding on livestock carcasses might ingest antimicrobials present in such carcasses (Blanco and Bautista, 2020). Contaminated soil could be a major hot spot of AMR to wild birds and accounts for 30% of AMR genes (Han et al., 2022). As wild birds soak up AMR bacteria from these contaminated sources, they eventually become “ecological sponges,” capable of acquiring and disseminating AMR. The genetic similarities in bird isolates and those in environmental samples (like surface water) further confirm these acquisition pathways (Ahmed et al., 2019; Yuan et al., 2021).

Unfortunately, several research gaps significantly hinder understanding the origin and spread of AMR E. coli in wild birds. Our review reveals a stark lack of longitudinal studies, absence of satellite-tracking for studied wild birds, and limited WGS studies. The high cost and time required likely contribute to this scarcity. Despite these challenges, tracing the origins of AMR in wild birds is crucial in informing concerted efforts when developing effective preventive measures within the One Health framework. Future research should therefore prioritize small-scale and longitudinal designs, integration of satellite-tracking, and increased adoption of WGS to enable better tracking of the origins and cross-boundary movement of AMR in wild bird populations and other One Health sectors. By focusing on these areas, researchers can establish a robust foundation for informing more effective and sustainable strategies to limit the spread of AMR in natural ecosystems.

These findings confirm that, indeed, wild birds are potential reservoirs of resistant E. coli. The observed bioaccumulation of resistant E. coli within these avian populations, coupled with their ability to disseminate AMR across various One Health domains, underscores the urgency to mitigate environmental pollution impacts on AMR. Given that wild birds are not directly subjected to antimicrobial therapeutic interventions, the effective management of AMR in these populations necessitates proactive surveillance facilitated by multi-sectoral collaborations under a comprehensive One-Health framework. This strategic approach aligns intrinsically with the “Zero Pollution Vision for 2050: A Healthy Planet for All.” This vision emphasizes that pollution is a significant catalyst for AMR, and, conversely, pollution abatement is fundamental to ameliorating the AMR crisis. The inherent connection between a healthy environment and the prevalence of AMR is a core tenet of the One Health concept, which acknowledges the indivisible link between human, animal, plant, and environmental health. Therefore, safeguarding avian populations from AMR through environmental remediation will concurrently advance the overarching objectives of One Health and contribute to a healthier planet (European Commission, 2021).