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      Prevalence, Virulence Genes and Antimicrobial Resistance Profiles of Salmonella Serovars from Retail Beef in Selangor, Malaysia

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          Abstract

          The aim of the present study was to investigate the prevalence of Salmonella spp., Salmonella Enteritidis and Salmonella Typhimurium in retail beef from different retail markets of Selangor area, as well as, to assess their pathogenic potential and antimicrobial resistance. A total of 240 retail beef meat samples (chuck = 60; rib = 60; round = 60; sirloin = 60) were randomly collected. The multiplex polymerase chain reaction (mPCR) in combination with the most probable number (MPN) method was employed to detect Salmonella spp., S. Enteritidis and S. Typhimurium in the meat samples. The prevalence of Salmonella spp., S. Enteritidis and S. Typhimurium in 240 beef meat samples were 7.50, 1.25, and 0.83%, respectively. The microbial loads of total Salmonella was found in the range of <3 to 15 MPN/g. Eight different serovars of Salmonella were identified among the 23 isolates, and S. Agona was the predominant serovar (26.09%). Interestingly, all the Salmonella isolates were resistant to penicillin, erythromycin and vancomycin, but the sensitivity was observed for tetracycline, gentamicin and amoxicillin/clavulanic acid. All 23 isolates were resistant to at least three antibiotics. Two S. Typhimurium isolates (8.70%) exhibited the highest multiple antibiotic resistance (MAR) index value of 0.56 which shown resistance to nine antibiotics. PCR analysis of virulence genes showed that all Salmonella isolates (100%) were positive for the invA gene. Meanwhile, pefA was only identified in S. Enteritidis and S. Typhimurium. The findings in this study indicate that retail beef products tested were widely contaminated with multi-drug resistant (MDR) Salmonella and various virulence genes are present among the isolated Salmonella serovars.

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          Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods.

          Escherichia coli isolates taken from environments considered to have low and high enteric disease potential for humans were screened against 12 antibiotics to determine the prevalence of multiple antibiotic resistance among the isolates of these environments. It was determined that multiple-antibiotic-resistant E. coli organisms exist in large numbers within the major reservoirs of enteric diseases for humans while existing in comparatively low numbers elsewhere. These differences provide a method for distinguishing high-risk contamination of foods by indexing the frequency with which multiple-antibiotic-resistant E. coli organisms occur among isolates taken from a sample.
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            Prevalence and characterization of Salmonella serovars in retail meats of marketplace in Shaanxi, China.

            A total of 764 retail meat including 515 chicken, 91 pork, 78 beef and 80 lamb samples were collected in Shaanxi Province of China in 2007-2008 to determine the prevalence of Salmonella. The isolates were characterized using serotyping, antimicrobial susceptibility testing, and the presence of bla(CMY-2) and bla(TEM) and class I integrons. Selective serovars were further subtyped using PFGE. Approximately 54% (276) of chicken, 31% (28) of pork, 17% (13) of beef and 20% (16) of lamb samples were positive of Salmonella. Among 24 serovars identified, Enteritidis (31.5%) was most common, followed by Typhimurium (13.4%), Shubra (10.0%), Indiana (9.7%), Derby (9.5%) and Djugu (7.0%). Nearly 80% of the isolates (283) were resistant to at least one antimicrobial, and 53% (191) to more than three antimicrobials. Resistance was most frequently observed to sulfamethoxazole (67%), to trimethoprim/sulfamethoxazole (58%) and to tetracycline (56%). Furthermore, many isolates were resistant to nalidixic acid (35%), ciprofloxacin (21%) and ceftriaxone (16%). Most isolates of Shubra (89%) and Indiana (88%) were resistant to > or = 9 antimicrobials, compared to only 11% of Enteritidis and 9% of Infantis that showed similar resistance. Class I integrons were detected in 10% of the isolates, and contained aadA, tetR, dhfr, bla(PSE-1), bla(DHA-1) and bla(VEB-1) gene cassettes alone or various combinations. Ceftriaxone- and/or cefoperazone-resistant isolates (n=62) carried bla(TEM) (51.6%) and/or bla(CMY-2) (56.5%). A total of 116 PFGE patterns were generated among 210 selected isolates. Our findings indicated that Salmonella contamination was common in retail meats, and that the Salmonella isolates were phenotypically and genetically diverse. Additionally, many Salmonella isolates were resistant to multiple antimicrobials. 2010 Elsevier B.V. All rights reserved.
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              Prevalence and characterization of Salmonella species isolated from pigs, ducks and chickens in Sichuan Province, China.

              This study aimed to analyze the prevalence of Salmonella isolated from different parts of the food production chain, and to characterize these isolates. A total of 165 Salmonella enterica isolates were identified from 1382 samples taken from conventional farms, abattoirs and retail markets from 2010 to 2011 in Sichuan, China. The Salmonella isolates were assayed for serotype, antimicrobial susceptibility, prevalence of class 1 integrons and β-lactamase genes, and subtyped using pulsed-field gel electrophoresis. Among these isolates, S. enterica serotypes Derby (76 isolates, 46%) and Typhimurium (16 isolates, 10%) were the most prevalent, and high antimicrobial resistance rates were observed for tetracycline (77%), sulfamethoxazole/trimethoprim (43%), nalidixic acid (41%) and spectinomycin (41%). Class 1 integrons were detected in 21% of these isolates, and contained gene cassettes dfrA12-aadA2, dfrA1-aadA1, dfrA1, blaPSE-1 and dfrA1/aadA2. blaOXA-1 was the most commonly identified β-lactamase gene (n=14), followed by blaTEM-1 (n=6), blaPSE-1 (n=4) and blaCMY-2 (n=1). A S. enterica serotype Indiana isolate derived from chicken from a market was positive for both blaOXA-1 and blaCMY-2, and resistant to nine tested antibiotics. The PFGE patterns were diverse. Our findings indicated that most isolates from different sampling sites were phenotypically and genetically diverse, and Salmonella was widespread and may transmit along the food production chain from farm to market. Isolates with decreased susceptibility to fluoroquinolones and extended-spectrum cephalosporins, which are used to fight foodborne Salmonella, pose a serious threat to public health. Copyright © 2013 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
                11 January 2018
                2017
                : 8
                : 2697
                Affiliations
                [1] 1Department of Food Science, Faculty of Food Science and Technology, Universiti Putra Malaysia , Serdang, Malaysia
                [2] 2Laboratory of Food Safety and Food Integrity, Institute of Tropical Agriculture and Food Security (ITAFoS), Universiti Putra Malaysia , Serdang, Malaysia
                [3] 3Department of Veterinary Pathology and Microbiology, Faculty of Veterinary Medicine, Universiti Putra Malaysia , Serdang, Malaysia
                [4] 4Department of Diagnostic and Allied Science, Faculty of Health and Life Science, Management and Science University , Shah Alam, Malaysia
                [5] 5Division of Applied Biomedical Sciences and Biotechnology, School of Health Sciences, International Medical University , Kuala Lumpur, Malaysia
                [6] 6Department of Agricultural and Food Science, Faculty of Science, Universiti Tunku Abdul Rahman , Kampar, Malaysia
                [7] 7Novel Antibiotic Laboratory, School of Diagnostic and Applied Health Sciences, Faculty of Health Sciences, Universiti Kebangsaan Malaysia , Kuala Lumpur, Malaysia
                [8] 8Department of Science and Technology Studies, Faculty of Science, University of Malaya , Kuala Lumpur, Malaysia
                Author notes

                Edited by: Giovanna Suzzi, Università di Teramo, Italy

                Reviewed by: Milan Zivko Baltić, Faculty of Veterinary Medicine, University of Belgrade, Serbia; Giorgia Perpetuini, Università di Teramo, Italy

                *Correspondence: Tze Y. Thung upmtty@ 123456yahoo.com

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

                Article
                10.3389/fmicb.2017.02697
                5770799
                29379488
                4a062d70-e06c-4fce-b0e0-c9bf2afd366b
                Copyright © 2018 Thung, Radu, Mahyudin, Rukayadi, Zakaria, Mazlan, Tan, Lee, Yeoh, Chin, Tan, Kuan, Basri and Wan Mohamed Radzi.

                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
                : 22 July 2017
                : 26 December 2017
                Page count
                Figures: 1, Tables: 6, Equations: 0, References: 32, Pages: 8, Words: 6157
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                beef meat,salmonella,multiplex pcr,prevalence,antimicrobial resistance,virulence gene

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