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      Prevalence, Serotype, Antibiotic Susceptibility, and Genotype of Salmonella in Eggs From Poultry Farms and Marketplaces in Yangling, Shaanxi Province, China

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          Abstract

          Poultry products such as eggs provide essential nutrients to the human body and thus play vital roles in the human food network. Salmonella is one of the most notorious foodborne pathogens and has been found to be prevalent in eggs. To better understand the characteristics of Salmonella in eggs, we investigated the prevalence of Salmonella spp. in 814 fresh eggs collected from poultry farms and retail marketplaces in Yangling, Shaanxi Province, China. The serotype, genotype, and antibiotic susceptibilities of 61 Salmonella isolates recovered from the eggs were analyzed. The average detection rate of Salmonella-positive eggs was 5.6%, with 6.6% of the eggs collected from poultry farms and 5.1% from marketplaces. Thirteen serotypes were identified from the 61 isolates, among which Salmonella Typhimurium (24.5%) and Salmonella Indiana (22.9%) were the most prevalent serotypes. Other dominant serotypes included Salmonella Thompson (13.1%) and Salmonella Enteritidis (11.4%), with the remaining nine serotypes detected at low rates (1.6–4.9%). All the Salmonella isolates tested were resistant to sulfisoxazole (100.0%). The majority (77.1%) of the isolates were resistant to nalidixic acid, amoxicillin-clavulanate, and ampicillin, while nearly two-thirds (63.9–68.9%) were resistant to trimethoprim–sulfamethoxazole, kanamycin, tetracyclines, and chloramphenicol. The rate of resistance to ciprofloxacin was 40.1%; the resistance rates to streptomycin, ceftiofur, and ceftriaxone ranged from 21.3 to 26.2%; and those to gentamicin, amikacin, and cefoxitin were relatively low (3.3–16.4%). Forty-nine (80.3%) Salmonella isolates exhibited resistance to multiple antibiotics, 20 (32.8%) of which were resistant to at least 10 antibiotics. Subtyping by pulse-field gel electrophoresis revealed a close genetic relatedness of Salmonella isolates from poultry farms, in striking contrast to the high diversity of the isolates obtained from marketplaces. Isolates of the same serotype always shared identical genotype and antibiotic resistance profiles, even the ones that were recovered from eggs sampled at different locations and times. These findings indicate that diverse Salmonella spp. with high rates of multidrug resistance are prevalent in fresh eggs in the study area. More attention should be paid to egg production, transportation, and storage to prevent foodborne outbreaks caused by Salmonella.

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          Salmonella enterica: Survival, Colonization, and Virulence Differences among Serovars

          Data indicate that prevalence of specific serovars of Salmonella enterica in human foodborne illness is not correlated with their prevalence in feed. Given that feed is a suboptimal environment for S. enterica, it appears that survival in poultry feed may be an independent factor unrelated to virulence of specific serovars of Salmonella. Additionally, S. enterica serovars appear to have different host specificity and the ability to cause disease in those hosts is also serovar dependent. These differences among the serovars may be related to gene presence or absence and expression levels of those genes. With a better understanding of serovar specificity, mitigation methods can be implemented to control Salmonella at preharvest and postharvest levels.
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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
                04 August 2020
                2020
                : 11
                : 1482
                Affiliations
                [1] 1College of Food Science and Engineering, Northwest A&F University , Yangling, China
                [2] 2MOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology, Shanghai Jiao Tong University , Shanghai, China
                Author notes

                Edited by: Dario De Medici, Istituto Superiore di Sanità (ISS), Italy

                Reviewed by: Min Yue, Zhejiang University, China; Alejandro Castillo, Texas A&M University, United States

                *Correspondence: Baowei Yang, ybw090925@ 123456163.com

                These authors have contributed equally to this work and share first authorship

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

                Article
                10.3389/fmicb.2020.01482
                7438954
                32903897
                73ffb289-ff25-46f1-8967-ed5c4731d021
                Copyright © 2020 Li, Li, Zheng, Wang, Sheng, Shi, Shi, Niu and Yang.

                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) and the copyright owner(s) 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
                : 17 March 2020
                : 08 June 2020
                Page count
                Figures: 5, Tables: 2, Equations: 0, References: 55, Pages: 11, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                antibiotic resistance,eggs,genotype,salmonella,serotype
                Microbiology & Virology
                antibiotic resistance, eggs, genotype, salmonella, serotype

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