Seabirds as anthropization indicators in two different tropical biotopes: A One Health approach to the issue of antimicrobial resistance genes pollution in oceanic islands.

Affiliation

Ewbank AC(1), Esperón F(2), Sacristán C(3), Sacristán I(4), Krul R(5), Cavalcante de Macedo E(6), Calatayud O(7), Bueno I(8), de Francisco Strefezzi R(9), Catão-Dias JL(10).
Author information:
(1)Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil. Electronic address: [Email]
(2)Group of Epidemiology and Environmental Health, Animal Health Research Centre
(INIA-CISA), Madrid, Spain. Electronic address: [Email]
(3)Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil. Electronic address: [Email]
(4)Facultad de Ciencias de la Vida, Universidad Andres Bello, Santiago, Chile. Electronic address: [Email]
(5)Ornithology Laboratory, Center for Studies of the Sea, Paraná State University, Paraná State, Brazil. Electronic address: [Email]
(6)Chico Mendes Institute for Biodiversity Conservation
(ICMBio) - Brazilian Ministry of the Environment, Rocas Atol Biological Reserve, Rio Grande do Norte, Brazil. Electronic address: [Email]
(7)Group of Epidemiology and Environmental Health, Animal Health Research Centre
(INIA-CISA), Madrid, Spain. Electronic address: [Email]
(8)Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, Saint Paul, United States. Electronic address: [Email]
(9)Laboratory of Comparative and Translational Oncology, Department of Veterinary Medicine, Faculty of Animal Science and Food Engineering, University of São Paulo, Pirassununga, Brazil. Electronic address: [Email]
(10)Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil. Electronic address: [Email]

Abstract

Antimicrobial resistance is a quintessential One Health issue, among the most serious 21st century global threats to human health. Seabirds may act as sentinels of natural and anthropogenic changes in the marine ecosystem health, including pollution by antimicrobial resistance genes (ARGs). We used real time PCR to identify and quantify 22 plasmid-mediated ARGs in the gastrointestinal microbiome of six wild seabird species, comparing an anthropized (Fernando de Noronha Archipelago - FNA) and a pristine biotope (Rocas Atoll - ROA), Brazil. Of 257 birds, 218 (84.8%) were positive to at least one ARG. ARG classes encoding resistance to tetracyclines (75.1%), quinolones (10.5%) and phenicols (10.5%) were the most prevalent, with tetracyclines significantly greater than the remaining classes (p < 0.05). Genes tet(S) (29.2%), tet(A) (28.8%), and tet(B) (24.9%) were the most commonly found and had a significantly greater prevalence when compared to the remaining ARGs (p < 0.05). The anthropized biotope presented statistically significant higher prevalence of sulfonamide- and quinolone-encoding ARGs in comparison with the pristine (respectively, p = 0.01 and p = 0.03), and higher sulII gene prevalence (p = 0.04), consistent with anthropogenic pressure. Migratory species (only present in ROA) showed statistically significant higher mcr-1 (polymyxins) and blaTEM (betalactam) prevalences (respectively, p = 0.009 and p = 0.02), and mcr-1 percentage load (p = 0.0079) in comparison with non-migratory. To our knowledge, this is the largest ARGs survey based on direct detection and quantification in seabirds worldwide, and the first to evaluate non-synanthropic species in oceanic islands. This is the first detection of mcr-1 in wild free-ranging seabirds in Brazil and in free-ranging migratory non-synanthropic seabirds worldwide. Our findings show the importance of biological and ecological factors, highlighting the role of seabirds as anthropization sentinels and ARGs-pollution environmental indicators (even in a pristine biotope), and their involvement in the One Health epidemiological chain of ARGs.