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Staphylococcus Spp. from Wild Mammals in Aragón (Spain): Antibiotic Resistance Status

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Staphylococcus Spp. from Wild Mammals in Aragón (Spain): Antibiotic Resistance Status J Vet Res 64, 373-379, 2020 DOI:10.2478/jvetres-2020-0057 Staphylococcus spp. from wild mammals in Aragón (Spain): antibiotic resistance status Leticia Alcalá García1, Carmen Torres2, Antonio Rezusta López3, Carmelo Ortega Rodríguez1, Jesús Orós Espinosa1, Carmen Simón Valencia1 1Department of Animal Pathology, Infectious Diseases and Epidemiology, Veterinary Faculty of Zaragoza, 50013, Zaragoza, Spain 2Department of Food and Agriculture, Area of Biochemistry and Molecular Biology, University of La Rioja, 26006, Logroño, Spain 3Microbiology Service, Hospital Miguel Servet, IIS Aragón, Universidad de Zaragoza, 50009, Zaragoza, Spain [email protected] Received: March 1, 2020 Accepted: August 24, 2020 Abstract Introduction: Antimicrobial resistance is a global health threat. It has been studied in humans and domestic animals, but there is a lack of data on wild animals. The objective of this study is the elucidation of its patterns in Staphylococcus spp. isolated from wild mammals of the Autonomous Community of Aragón (Spain). Material and Methods: A total of 103 mammals (Artiodactyla, Carnivora, Chiroptera, Erinaceomorpha, and Lagomorpha) were studied. A recovery centre provided 32 and hunting 71. Nasal and faecal samples yielded 111 staphylococci, which were identified by matrix-assisted laser desorption/ionization–time of flight mass spectrometry. A susceptibility test to 11 antibiotics was carried out, and statistical analysis was performed. Results: Some differences were detected in bacterial prevalence depending on how the mammal fed. Artiodactyla, mainly hunted, were predisposed to carry coagulase-positive staphylococci. The staphylococci species recovered were resistant to at least two classes of antibiotics, and were disseminated in all of the geographical areas studied. Conclusion: Resistant staphylococci are widely distributed in the wild mammals in the areas of the study, but the resistance quantified in them is lower than that to be expected if the use of antibiotics in farms had a direct influence on the wildlife and its environment. On the other hand, resistance to antibiotics restricted to human use was widely disseminated in various wild animal species. Keywords: wild mammals, Staphylococcus spp., antibiotic resistance, epidemiology. Introduction negative Staphylococcus (CoNS) began to be considered as a source of resistance genes for humans and animals In a global world, it is wholly understood that (23). Generally speaking, misuse of antibiotics in animals, humans, and environment are interconnected. treatment of humans and animals is considered the main The World Health Organisation (WHO), World factor favouring the spread of resistant genes and Organisation for Animal Health (OIE), and Food and bacteria that will also reach the food chain and humans Agriculture Organisation (FAO), have joined efforts (8) (10, 27). Imprudent antimicrobial application examples to propose measures together against health risks at the included wrong dosage regimens, self-medication, and animal-human-ecosystems interface. The OIE developed the their incorrect use in intensive animal production. Skin “Strategy on Antimicrobial Resistance and Prudent Use and faeces of domestic animals contribute to the of Antimicrobials” in 2016, to survey the emergence of staphylococci spreading into the environment (10). antibiotic-resistant (AR) organisms (28). The WHO Wastewater is one important source of resistant genes published a list of the main resistant bacteria including and bacteria and, considering the continuous movement methicillin-resistant Staphylococcus aureus (MRSA), of people, animal and products around the world, it and a warning of its decreasing susceptibility to represents a significant path for the spread of genes and vancomycin in 2014 (29). A little later, coagulase- © 2020 L.A. García et al. This is an open access article distributed under the Creative Commons Attribution- NonCommercial-NoDerivs license (http://creativecommons.org/licenses/by-nc-nd/3.0/) 374 L.A. García et al./J Vet Res/64 (2020) 373-379 bacteria far away from the point where resistance was characterised in a previous paper (22), in which the originated (11, 16). phenotype/genotype of antimicrobial resistance, virulence The aim of this study was to detect the resistant gene content, and molecular typing of the isolates were phenotype profile of Staphylococci, with special reported. attention to methicillin-resistant coagulase-positive Statistical analysis. The frequency distribution of Staphylococcus (CoPS) isolated from wild mammals the main factors along with the detection of association from the Autonomous Community of Aragón (Spain), between the epidemiological data was recorded, and to look for factors affecting the pattern of bacterial Staphylococcus was isolated and the detected antibiotic resistance. resistance was calculated. That was performed with Epi Info 7.1.5.2 software (https://www.cdc.gov/epiinfo). Chi squared (χ2) was calculated for qualitative variables Material and Methods to detect the existence of association (P ≤ 0.05). Occasionally the Fisher exact test was applied. Study samples. Nasal and rectal samples from each of 103 wild mammals, making 206 samples in total, (Table 1) were collected in the Autonomous Community Results of Aragón (Spain) between 2012 and 2015. Samples from 32 animals were provided by the Centre of Wild There were 111 isolates recovered in which there Fauna Recovery of La Alfranca (CWFR-LA), Zaragoza were identified 15 different Staphylococcus species (Aragón, Spain), and material from 71 mammals was put from 15 mammal species (Tables 1 and 2), most of them at our disposal by veterinarians attending hunts. Samples retrieved from nasal swabs. A 73.7% proportion of were collected by means of sterile swabs in Amies samples of Carnivora (Table 1) rescued in the CWFR- medium, in the first hours after the animal’s arrival at the LA carried staphylococci (Table 1). The order CWFR-LA or immediately after its being killed as Lagomorpha gave a lower proportion of staphylococci hunting prey. Epidemiological data collected from the isolation by samples (35.0%) than other orders. More animals were species, order, animal age (neonates and than 60% of carnivorous (16/22), invertebrate-eater sub-yearlings < one year, young ˃ one year ˂ two years, (17/24), omnivorous (29/44), and piscivorous (5/8) and adult > two years), sex, basic type of diet animals had isolates recovered from them, while 40.9% (carnivorous, herbivorous, omnivorous, piscivorous, of herbivorous animals had (45/110) (P ≤ 0.05). A total invertebrate eater), and habituation to scavenging of 26 CoPS and 85 CoNS were isolated. The higher (carrion eaters). The mammals came from five different percentage of CoPS was obtained from hunted mammals geographical areas (classified by altitude). (84.6%; 22/26) and the order Artiodactyla (73.1%; Isolation and identification of staphylococci. 19/26). CoNS were found equally in both hunted Samples were seeded in mannitol salt agar, (CM0085, (n = 43) and rescued mammals (n = 42). The most Oxoid S.A., Spain), with and without oxacillin. Gram prevalent staphylococci were S. sciuri (30.6%) and stain, catalase, oxidase, and coagulase tests were S. aureus (20.7%) (Table 2). S. sciuri was isolated from performed. Selected colonies were sub-cultured in 11 different species while S. aureus was isolated from Columbia blood agar base (blood agar base sheep blood, hedgehog, mouflon, red deer, wild rabbit, and wild boar, PB0115, Oxoid S.A., Spain), in order to be identified in which the 50% of isolates were this species (11/22) by matrix-assisted laser desorption/ionisation–time of (Table 2). S. aureus predominated in 11 Artiodactyla flight mass spectrometry (MALDI-TOF MS) through (50.0%; 19/38) (Table 2), but none was isolated from the proteomic fingerprint on a Biotyper 3 system Carnivora. Wild rabbits carried a low percentage of (Bruker, USA), following the manufacturer’s S. aureus (7.9%; 3/38). instructions. Antibiotic phenotypical resistance to FA was high Antibiotic susceptibility test. Antibiotic resistance (64%), and in declining order resistance to other was tested by the Kirby–Bauer method, following the antibiotics was to PEN (42.3%), LIN (32.4%), instructions of the Clinical & Laboratory Standards FOX (20.7%), MUP (19.8%), and ERY (13.5%). The Institute (USA) (4). Penicillin (PEN, 10 U), cefoxitin remaining studied antibiotics showed lower than 10% of (FOX, 30 µg), teicoplanin (TEI, 30 µg), tetracycline isolates to be resistant, and the lower limit was (TE, 30 µg), erythromycin (ERY, 15 µg), clindamycin SXT – 0% (Table 3). A low prevalence of MDR (CLI, 2 µg), chloramphenicol (CL, 30 µg), gentamicin staphylococci isolates was detected in the studied (GEN, 10 µg), tobramycin (TOB, 10 µg), streptomycin population (7.2%; 8/111). The majority of FA-resistant (STR, 10 µg), lincomycin (LIN, 15 µg), ciprofloxacin isolates were CoNS (72.9%) (Table 4) obtained from (CIP, 5 µg), sulfamethoxazole-trimethoprim (SXT, rescued mammals (76.1%), where S. sciuri was 1.25–23.75 µg), fusidic acid (FA, 10 µg), and mupirocin predominant (P 0.05). The five isolates from the (MUP, 5 µg) were studied. A multidrug-resistant (MDR) common otter were resistant to FA (Table 3). isolate is defined as one with acquired non-susceptibility Staphylococci resistant to MUP were mainly isolated to at least one agent in three or more antimicrobial from hunted mammals (27.7%; 18/65) and categories (15). A total of 23 S. aureus isolates were L.A. García et al./J
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