Evil and allies: Opportunistic gulls as both spreaders and sentinels of antibiotic-resistant bacteria in human-transformed landscapes


Por: Martín- Vélez, V, Montalvo, T, Giralt, D, Ramírez, F, Giménez, J, Morral-Puigmal, C, Planell, R, Sabate, S, Bota, G, Navarro, J

Publicada: 1 nov 2024 Ahead of Print: 1 oct 2024
Resumen:
Human-transformed residuals, especially those derived from human waste (dumps), farmland, and livestock are involved in the emergence of antibiotic-resistant bacteria (ARB) in the environment. Wildlife can act as vectors of ARB dispersal through different environments, but also as sentinels to detect the early spread and determine ARB sources. The development of integrated monitoring programmes focused on wildlife would help to anticipate the risks of ARB to humans and livestock. We used the yellow-legged gull (Larus michahellis) as a model species to investigate and monitor the spatial patterns of ARB dispersal across an extensive farmland region located in northeastern Spain (Lleida). By integrating GPS tracking data and ARB clinical testing for 26 individuals within a network analysis framework, we modelled the risk of spatial pathogen spread through faeces during the bacteria-transmission latency period (16 days after sample collection). Additionally, we created a connectivity network to determine the main sources of ARB in the area, focusing on three main habitats of special risk for infection: dumps, livestock facilities, and irrigation ponds. Seven individuals were infected by Escherichia coli, with one also co-infected with Listeria monocytogenes and Salmonella spp. Potential pathogen dispersal distances ranged from 1.13 km to 23.13 km from the breeding colony. Our network analyses revealed 54 main nodes (i.e. high-risk habitats recurrently visited by tracked gulls) and 1182 links among them. Our findings revealed a high degree of connectivity between the breeding area, located in a shallow lake, and nearby dumps, highlighting them as significant contributors to ARB dispersal. Synthesis and applications: The integration of GPS data, pathogen testing and network analyses can shed further light on pathogen dynamics by creating spatial risk maps and identifying ARB sources. In combination with complementary molecular epidemiology techniques within a One Health framework, our approach can emerge as an important tool for monitoring ARB dynamics within highly human-transformed ecosystems. This may empower managers for the development of targeted ARB monitoring programmes and effective mitigation strategies, ultimately improving both animal and public health. Los residuos transformados por el ser humano, especialmente aquellos derivados de desechos humanos (vertederos), agricultura y ganader & iacute;a intensivas, est & aacute;n implicados en la aparici & oacute;n de bacterias resistentes a los antibi & oacute;ticos en el medio ambiente. La fauna silvestre puede actuar como vector de dispersi & oacute;n de bacterias resistentes en el entorno, pero tambi & eacute;n como centinela para detectar la propagaci & oacute;n temprana y determinar las fuentes de bacterias resistentes a antibi & oacute;ticos. El desarrollo de programas integrados de monitoreo utillizando fauna silvestre ayudar & iacute;a a anticipar los riesgos de transmision de bacterias resistentes a antibi & oacute;ticos a humanos y a instalaciones ganaderas. En este trabajo utilizamos la gaviota patiamarilla (Larus michahellis) como especie modelo para investigar y monitorear los patrones espaciales de dispersi & oacute;n de bacterias resistentes en una regi & oacute;n agr & iacute;cola ubicada en el noreste de Espa & ntilde;a (Lleida). Integrando datos de GPS y pruebas cl & iacute;nicas en 26 individuos, modelamos el riesgo de dispersi & oacute;n espacial de pat & oacute;genos a trav & eacute;s de heces durante el per & iacute;odo de latencia de transmisi & oacute;n bacteriana (16 d & iacute;as despu & eacute;s de la recolecci & oacute;n de muestras). Adicionalmente, creamos una red de conectividad para determinar las principales fuentes de resistencias a antibioticos en el & aacute;rea, enfoc & aacute;ndonos en tres h & aacute;bitats de especial riesgo: vertederos, instalaciones ganaderas y balsas de riego. Siete individuos estaban infectados con Escherichia coli, y uno tambi & eacute;n co-infectado con Listeria monocytogenes y Salmonella spp. Las distancias potenciales de dispersi & oacute;n de pat & oacute;genos variaron de 1,13 km a 23,13 km desde la colonia. Nuestros an & aacute;lisis de redes revelaron 54 nodos principales (h & aacute;bitats de alto riesgo visitados recurrentemente por las gaviotas marcadas) y 1182 enlaces entre ellos. Nuestros resultados revelaron un alto grado de conectividad entre la colonia y los vertederos cercanos, destac & aacute;ndolos como contribuyentes significativos a la dispersi & oacute;n de bacterias resistentes a antibi & oacute;ticos. S & iacute;ntesis y aplicaciones: La integraci & oacute;n de datos GPS, pruebas de pat & oacute;genos y pruebas cl & iacute;nicas puede arrojar luz sobre la din & aacute;mica de los pat & oacute;genos mediante la creaci & oacute;n de mapas de riesgo espacial e identificaci & oacute;n de fuentes de resistencias a antibi & oacute;ticos. En combinaci & oacute;n con t & eacute;cnicas complementarias de epidemiolog & iacute;a molecular dentro de un marco de "One Health", nuestro enfoque puede surgir como una herramienta importante para monitorear la din & aacute;mica de pat & oacute;genos en ecosistemas altamente transformados por humanos. Esto puede ayudar a los gestores para el desarrollo de programas de monitoreo espec & iacute;ficos de resistencias en el ambiente y estrategias de mitigaci & oacute;n efectivas, mejorando en & uacute;ltima instancia tanto la salud animal como la salud p & uacute;blica. The integration of GPS data, pathogen testing and network analyses can shed further light on pathogen dynamics by creating spatial risk maps and identifying ARB sources. In combination with complementary molecular epidemiology techniques within a One Health framework, our approach can emerge as an important tool for monitoring ARB dynamics within highly human-transformed ecosystems. This may empower managers for the development of targeted ARB monitoring prog

Filiaciones:
Martín- Vélez, V:
 CSIC, Inst Ciencies Mar ICM, Barcelona, Spain

Montalvo, T:
 Agencia Salut Publ Barcelona ASPB, Barcelona, Spain

 CIBER Epidemiol & Salud Publ, Madrid, Spain

 Inst Invest Biomed St Pau IIB St Pau, Barcelona, Spain

Giralt, D:
 Ctr Ciencia & Tecnol Forestal Catalunya CTFC, Grup Biol Conservacio GBiC, Solsona, Spain

Ramírez, F:
 CSIC, Inst Ciencies Mar ICM, Barcelona, Spain

Giménez, J:
 Inst Espanol Oceanog IEO CSIC, Ctr Oceanog Malaga COMA, Malaga, Spain

Morral-Puigmal, C:
 Agencia Salut Publ Barcelona ASPB, Barcelona, Spain

Planell, R:
 Agencia Salut Publ Barcelona ASPB, Barcelona, Spain

 Inst Invest Biomed St Pau IIB St Pau, Barcelona, Spain

Sabate, S:
 Agencia Salut Publ Barcelona ASPB, Barcelona, Spain

 Inst Invest Biomed St Pau IIB St Pau, Barcelona, Spain

Bota, G:
 Ctr Ciencia & Tecnol Forestal Catalunya CTFC, Grup Biol Conservacio GBiC, Solsona, Spain

Navarro, J:
 CSIC, Inst Ciencies Mar ICM, Barcelona, Spain
ISSN: 00218901
Editorial
WILEY, 111 RIVER ST, HOBOKEN 07030-5774, NJ USA, Reino Unido
Tipo de documento: Article
Volumen: 61 Número: 11
Páginas: 2809-2821
WOS Id: 001322501300001
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