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      Antimicrobial resistance in commensal Staphylococcus aureus from wild ungulates is driven by agricultural land cover and livestock farming.

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          Abstract

          Staphylococcus aureus is a human pathobiont (i.e., a commensal microorganism that is potentially pathogenic under certain conditions), a nosocomial pathogen and a leading cause of morbidity and mortality in humans. S. aureus is also a commensal and pathogen of companion animals and livestock. The dissemination of antimicrobial resistant (AMR) S. aureus, particularly methicillin-resistant (MRSA), has been associated to its ability for establishing new reservoirs, but limited attention has been devoted to the role of the environment. To fill this gap, we aimed to characterize animal carrier status, AMR phenotypes, predominant clonal lineages and their relationship with clinical and food-chain settings, as well as to find predictors of AMR occurrence. Nasal swabs (n = 254) from wild boar (n = 177), red deer (n = 54) and fallow deer (n = 23) hunted in Portugal, during the season 2019/2020, yielded an overall carrier proportion of 35.8%, ranging from 53.7% for red deer and 32.2% for wild boar to 21.7% for fallow deer. MRSA from wild boar and phenotypically linezolid-resistant S. aureus from wild boar and red deer were isolated, indicating that resistance to antimicrobials restricted to clinical practice also occurs in wildlife. The most prevalent genotypes were t11502/ST2678 (29.6%) and t12939/ST2678 (9.4%), previously reported in wild boar from Spain. Clonal lineages reported in humans and livestock, like CC1, CC5 or CC8 (19.1%) and ST425, CC133 or CC398 (23.5%), respectively, were also found. The sequence type ST544, previously restricted to humans, is described in wildlife for the first time. We also identified that land use (agricultural land cover), human driven disturbance (swine abundance) and host-related factors (sex) determine resistance occurrence. These findings suggest that antibiotics used in clinical settings, agriculture and livestock farming, spill over to wildlife, leading to AMR emergence, with potential biological, ecological, and human health effects. This work is one of the most comprehensive surveys in Europe of S. aureus occurrence and determinants among widely distributed wild ungulates.

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          Author and article information

          Journal
          Environ Pollut
          Environmental pollution (Barking, Essex : 1987)
          Elsevier BV
          1873-6424
          0269-7491
          Jun 15 2022
          : 303
          Affiliations
          [1 ] Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências da Universidade de Lisboa, 1749-016, Lisboa, Portugal; Biosystems and Integrative Sciences Institute (BioISI), Faculdade de Ciências da Universidade de Lisboa, 1749-016, Lisboa, Portugal.
          [2 ] Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências da Universidade de Lisboa, 1749-016, Lisboa, Portugal.
          [3 ] Department of Biology & Centre for Environmental and Marine Studies (CESAM), Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal.
          [4 ] Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências da Universidade de Lisboa, 1749-016, Lisboa, Portugal; Biosystems and Integrative Sciences Institute (BioISI), Faculdade de Ciências da Universidade de Lisboa, 1749-016, Lisboa, Portugal. Electronic address: mscunha@fc.ul.pt.
          Article
          S0269-7491(22)00330-X
          10.1016/j.envpol.2022.119116
          35276250
          de73dfe9-0058-46e6-be34-1061726faa47
          History

          MLST,Human perturbation,Ecological modelling,Antimicrobial resistance,Wildlife,Staphylococcus aureus,MRSA

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