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

Author(s)

Ewbank, Ana Carolina ^[1] ; Esperon, Fernando ^[2] ; Sacristan, Carlos ^[1] ; Sacristan, Irene ^[3] ; Krul, Ricardo ^[4] ; de Macedo, Eduardo Cavalcante ^[5] ; Calatayud, Olga ^[2] ; Bueno, Irene ^[6] ; Strefezzi, Ricardo de Francisco ^[7] ; Catao-Dias, Jose Luiz ^[1]

Affiliation

^[1] Univ Sao Paulo, Sch Vet Med & Anim Sci, Dept Pathol, Lab Wildlife Comparat Pathol, Ave Prof Orlando Marques Paiva, 87 Butanta, BR-05508010 Sao Paulo, SP - Brazil

^[2] Anim Hlth Res Ctr INIA CISA, Grp Epidemiol & Environm Hlth, Madrid - Spain

^[3] Univ Andres Bello, Fac Ciencias Vida, Santiago - Chile

^[4] Parana State Univ, Ctr Studies Sea, Ornithol Lab, Maringa, Parana - Brazil

^[5] Brazilian Minist Environm, Chico Mendes Inst Biodivers Conservat ICMBio, Natal, RN - Brazil

^[6] Univ Minnesota, Coll Vet Med, Dept Vet & Biomed Sci, St Paul, MN 55108 - USA

^[7] Univ Sao Paulo, Fac Anim Sci & Food Engn, Dept Vet Med, Lab Comparat & Translat Oncol, Pirassununga - Brazil

• Document type: Journal article
• Source: Science of The Total Environment; v. 754, FEB 1 2021.
• Web of Science Citations: 0

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 = 0.01and 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 bla(TEM) (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. (C) 2020 Elsevier B.V. All rights reserved. (AU)

• FAPESP's process: 18/25885-9 - Identification and quantification of antimicrobial resistance genes in the microbiome of wild seabirds from Brazil: how do anthropogenic impacts affect these parameters?
• Grantee: Ana Carolina Ewbank
• Support Opportunities: Scholarships abroad - Research Internship - Doctorate
• FAPESP's process: 18/25069-7 - Study and characterization of selected emerging viral agents and potentially associated with hepatopathies in coastal, pelagic and mixed habitat cetaceans in Brazil
• Grantee: Carlos Sacristan Yague
• Support Opportunities: Scholarships in Brazil - Post-Doctoral
• FAPESP's process: 16/20956-0 - Identification and quantification of antimicrobial resistance genes in the microbiome of seabirds from the Southern-Southeastern coast of Brazil
• Grantee: Ana Carolina Ewbank
• Support Opportunities: Scholarships in Brazil - Doctorate