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      Enterotoxigenicity and Antimicrobial Resistance of Staphylococcus aureus Isolated from Retail Food in China

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          Abstract

          Staphylococcus aureus is one of the most common causes of zoonotic agent in the world, which are attributable to the contamination of food with enterotoxins. In this study, a total of 1,150 S. aureus isolates were cultured from 27,000 retail foods items from 203 cities of 24 provinces in China in 2015 and were test for antimicrobial susceptibility. Additionally, the role of the genes responsible for the staphylococcal enterotoxins (SEA to SEE), methicillin resistance ( mecA) and the toxigenic capabilities were also assessed. The results showed that 4.3% retail foods were contaminated with S. aureus, and 7.9% retail foods isolates were mecA positive. Some 97.6% of S. aureus isolates were resistant to at least one antimicrobial compound, and 57.5% of these were multi drug resistant (MDR). Resistance to penicillin (83.7%, 963/1,150), was common, followed by linezolid (67.7%, 778/1,150) and erythromycin (52.1%, 599/1,150). The isolates cultured from raw meats showed high levels of resistant to tetracycline (42.8%), ciprofloxacin (17.4%), and chloramphenicol (12.0%) and expressed a MDR phenotype (62.4%). A total of 29.7% S. aureus isolates harbored the classical SEs genes ( sea, seb, sec, and sed). The sea and seb genes were the most frequent SEs genes detected. Of note, 22% of the SEs genes positive S. aureus harbored two or three SEs genes, and 16 isolates were confirmed with the capacity to simultaneously produce two or three enterotoxin types. Moreover, nearly 50% of the MRSA isolates were positive for at least one SE gene in this study. Therefore, it is important to monitor the antimicrobial susceptibility and enterotoxigenicity of MDR S. aureus and MRSA in the food chain and to use these data to develop food safety measures, designed to reduce the contamination and transmission of this bacterium.

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          Most cited references51

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          Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus.

          The impact of globalization on the emergence and spread of pathogens is an important veterinary and public health issue. Staphylococcus aureus is a notorious human pathogen associated with serious nosocomial and community-acquired infections. In addition, S. aureus is a major cause of animal diseases including skeletal infections of poultry, which are a large economic burden on the global broiler chicken industry. Here, we provide evidence that the majority of S. aureus isolates from broiler chickens are the descendants of a single human-to-poultry host jump that occurred approximately 38 years ago (range, 30 to 63 years ago) by a subtype of the worldwide human ST5 clonal lineage unique to Poland. In contrast to human subtypes of the ST5 radiation, which demonstrate strong geographic clustering, the poultry ST5 clade was distributed in different continents, consistent with wide dissemination via the global poultry industry distribution network. The poultry ST5 clade has undergone genetic diversification from its human progenitor strain by acquisition of novel mobile genetic elements from an avian-specific accessory gene pool, and by the inactivation of several proteins important for human disease pathogenesis. These genetic events have resulted in enhanced resistance to killing by chicken heterophils, reflecting avian host-adaptive evolution. Taken together, we have determined the evolutionary history of a major new animal pathogen that has undergone rapid avian host adaptation and intercontinental dissemination. These data provide a new paradigm for the impact of human activities on the emergence of animal pathogens.
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            New epidemiology of Staphylococcus aureus infection in Asia.

            Not only is Asia the most populous region in the world, but inappropriate therapy, including self-medication with over-the-counter antimicrobial agents, is a common response to infectious diseases. The high antibiotic selective pressure among the overcrowded inhabitants creates an environment that is suitable for the rapid development and efficient spread of numerous multidrug-resistant pathogens. Indeed, Asia is among the regions with the highest prevalence rates of healthcare-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) and community-associated methicillin-resistant S. aureus (CA-MRSA) in the world. Most hospitals in Asia are endemic for multidrug-resistant methicillin-resistant S. aureus (MRSA), with an estimated proportion from 28% (in Hong Kong and Indonesia) to >70% (in Korea) among all clinical S. aureus isolates in the early 2010s. Isolates with reduced susceptibility or a high level of resistance to glycopeptides have also been increasingly identified in the past few years. In contrast, the proportion of MRSA among community-associated S. aureus infections in Asian countries varies markedly, from 35%. Two pandemic HA-MRSA clones, namely multilocus sequence type (ST) 239 and ST5, are disseminated internationally in Asia, whereas the molecular epidemiology of CA-MRSA in Asia is characterized by clonal heterogeneity, similar to that in Europe. In this review, the epidemiology of S. aureus in both healthcare facilities and communities in Asia is addressed, with an emphasis on the prevalence, clonal structure and antibiotic resistant profiles of the MRSA strains. The novel MRSA strains from livestock animals have been considered to constitute a public health threat in western countries. The emerging livestock-associated MRSA strains in Asia are also included in this review. © 2014 The Authors Clinical Microbiology and Infection © 2014 European Society of Clinical Microbiology and Infectious Diseases.
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              Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry.

              Methicillin-resistant S. aureus (MRSA) of clonal complex 398 (CC398) is emerging globally among production animals such as cattle, pigs and poultry as well as among humans. However, little is known about the prevalence of CC398 among methicillin sensitive S. aureus (MSSA) or the relative clonal distribution of S. aureus isolated from these three animal reservoirs. To study this, we have analyzed a random sample of S. aureus consisting of 296 epidemiologically unrelated isolates from infections and colonisation of pigs, cattle and poultry. These were examined and compared by spa and multi-locus sequence typing (MLST) and the result was compared to the most common spa types found among human blood isolates. Little overlap in spa types was seen between isolates from the three animal reservoirs or between animals and humans. Most of the porcine isolates had the spa types t034 (CC398), t1333 (CC30) and t337 (CC9), while the bovine isolates mainly had spa types t518 (CC50), t524 (CC97) and t529 (CC151). None of these spa types are common among human blood isolates in Denmark. Surprisingly, almost all of the poultry isolates (96%) belonged to CC5 (spa types t002 and t306), which is also known to be commonly found among human blood isolates and subsequent pulsed-field gel electrophoresis (PFGE) analysis identified indistinguishable PFGE patterns among a poultry isolate and selected human isolates. In conclusion, strains of MSSA CC398 were commonly present in pigs but not present at all in the other reservoirs tested. Copyright 2009 Elsevier B.V. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                21 November 2017
                2017
                : 8
                : 2256
                Affiliations
                [1] 1School of Public Health, Qingdao University , Qingdao, China
                [2] 2Key Laboratory of Food Safety Risk Assessment, Ministry of Health, China National Center for Food Safety Risk Assessment , Beijing, China
                [3] 3College of Veterinary Medicine, South China Agricultural University , Guangzhou, China
                [4] 4Kuiwen District Center for Disease Control and Prevention , Weifang, China
                [5] 5UCD-Centre for Food Safety, School of Public Health, Physiotherapy and Sports Science, University College Dublin , Dublin, Ireland
                [6] 6Institute for Global Food Security, School of Biological Sciences, Queen's University Belfast , Belfast, United Kingdom
                Author notes

                Edited by: David Rodriguez-Lazaro, University of Burgos, Spain

                Reviewed by: Learn-Han Lee, Monash University Malaysia, Malaysia; Beatrix Stessl, Veterinärmedizinische Universität Wien, Austria

                *Correspondence: Aiguo Ma magfood@ 123456126.com

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                †These authors have contributed equally to this work and should be regarded as co-first authors.

                Article
                10.3389/fmicb.2017.02256
                5702451
                28154559
                47e15c19-e407-4f2e-9f2a-2429d9372e0f
                Copyright © 2017 Wang, Baloch, Jiang, Zhang, Peng, Li, Fanning, Ma and Xu.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 12 July 2017
                : 31 October 2017
                Page count
                Figures: 3, Tables: 5, Equations: 0, References: 61, Pages: 11, Words: 8580
                Funding
                Funded by: Ministry of Science and Technology of the People's Republic of China 10.13039/501100002855
                Award ID: 2016YFD0401102
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                retail foods,staphylococcus aureus,enterotoxingenicity,methicillin-resistant staphylococcus aureus,antimicrobial resistance

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