Salmonella is a foodborne zoonotic pathogen that threatens food safety and public health. However, few people have conducted long-term and systematic studies on Salmonella contamination in food in Yantai City. In order to investigate the situation of Salmonella contamination in food and improve the ability of early warning and control of foodborne diseases, a total of 3420 samples from 20 categories were collected from 13 monitoring points in Yantai City, from 2010 to 2023. The difference in detection rate and bacterial strain of different monitoring points, different types, and different sources of samples was compared. Of the 3420 samples, 80 were positive with a detection rate of 2.34%. Salmonella detection rates were significantly different for samples collected at different monitoring sites. Salmonella was detected only in meat and meat products and catering food, and none of the other types were detected. The detection rate of Salmonella was higher in raw animal meat and raw poultry. Samples collected at the market stage had the highest detection rate (5.81%), and there was a significant difference in detection rate between samples from different sources (χ2 = 36.93, p < 0.05). Eighty-one strains of Salmonella were detected out of 3420 samples (2 different strains were detected in 1 positive sample). The serological test identified 8 groups and 27 serotypes. The dominant serum groups were group B 30.86% (25/81), group E1 23.46% (19/81), and group D 16.05% (13/81). The main dominant serotypes were Salmonellagive 17.28% (14/81), Salmonellaenteritidis 16.05% (13/81), and Salmonelladerby 13.58% (11/81). Meat and meat products and catering food were the main food products contaminated with Salmonella. The resulting secondary contamination is the hidden threat of foodborne diseases and should be given sufficient attention.
Get full access to this article
View all access options for this article.
References
1.
BillahMM, RahmanMS. Salmonella in the environment: A review on ecology, antimicrobial resistance, seafood contaminations, and human health implications. J Hazard Mater, 2024; 13(24):100407; doi: 10.1016/j.hazadv.2024.100407
2.
ChenQ, GongX, ZhengF, et al.Prevalence and characteristics of quinolone resistance in Salmonella isolated from retail foods in Lanzhou, China. J Food Prot, 2019; 82(9):1591–1597; doi: 10.4315/0362-028X.JFP-19-001
3.
ChenYZ, ShaoK, GuanB, et al.Survey on Salmonella contamination of food in field of distribution in Shandong in 2003 to 2008. Chin J Public Health Manag, 2010; 26(2):163–165.
4.
ChuY, WangD, HaoWH, et al.Prevalence, antibiotic resistance, virulence genes and molecular characteristics of Salmonella isolated from ducks and wild geese in China. Food Microbiol, 2024; 118:104423; doi: 10.1016/j.fm.2023.104423
5.
CooksonK, HofacreCL, Da CostaM, et al.Live Salmonella Typhimurium vaccination of broilers results in lower Salmonella prevalence on carcasses at commercial processing. J Appl Poultry Res, 2024; 33(1):100382; doi: 10.1016/j.japr.2023.100382
6.
CrumpJA, Sjölund-KarlssonM, GordonMA, et al.Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev, 2015; 28(4):901–937; doi: 10.1128/cmr.00002-15
7.
Dewey-MattiaD, ManikondaK, HallAJ, et al.Crowe Surveillance for foodborne disease outbreaks—United States, 2009-2015. MMWR Surveill Summ, 2018; 67(10):1–11; doi: 10.1558/5/mmwr.ss6710a1
8.
DingYF, ZhangYM, HuangCX, et al.An electrochemical biosensor based on phage-encoded protein RBP 41 for rapid and sensitive detection of Salmonella. Talanta, 2024; 270:125561; doi: 10.1016/j.talanta.2023.125561
9.
ElsayedMM, El-BasreyYFH, El-BazAH, et al.Ecological prevalence, genetic diversity, and multidrug resistance of Salmonella enteritidis recovered from broiler and layer chicken farms. Poult Sci, 2024; 103(2):103320; doi: 10.1016/j.psj.2023.103320
10.
European Food Safety Authority, European Centre for Disease Prevention and Control. The European Union one health 2022 zoonoses report. EFSA J, 2023; 21(12):e8442; doi: 10.2903/j.efsa.2023.8442
11.
FonsecaM, HeiderLC, StryhnH, et al.Frequency of isolation and phenotypic antimicrobial resistance of fecal Salmonella enterica recovered from dairy cattle in Canada. J Dairy Sci, 2023; doi: 10.3168/jds.2023-23937
12.
Gómez-BaltazarA, Godínez-OviedoA, Segura-GarcíaLE, et al.Genomic diversity of Salmonella enterica isolated from raw chicken at retail establishments in Mexico. Int J Food Microbiol, 2024; 411(2024):110526; doi: 10.1016/j.ijfoodmicro.2023.110526
13.
GroteA, PisconB, MansonAL, et al.Persistent Salmonella infections in humans are associated with mutations in the BarA/SirA regulatory pathway. Cell Host Microbe, 2024; 32(1):79–92.e7; doi: 10.1016/j.chom.2023.12.001
14.
GuibourdencheM, RoggentinP, MikoleitM, et al.Supplement 2003–2007 (no. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol, 2010; 161(1):26–29; doi: 10.1016/j.resmic.2009.10.002
15.
HeB, ZhuT-T, LiangY, et al.Adaptive evolution in asymptomatic host confers MDR Salmonella with enhanced environmental persistence and virulence. Sci Total Environ, 2024; 908:168340; doi: 10.1016/j.scitotenv.2023.168340
16.
KgoaleDM, DuvenageS, PlessisEMD, et al.Serotype distribution, antimicrobial resistance, virulence genes, and genetic diversity of Salmonella spp. isolated from small-scale leafy green vegetable supply chains in South Africa. J Food Prot, 2024; 87(1):100195; doi: 10.1016/j.jfp.2023.100195
17.
LiH, TongZQ, LuLL, et al.Contamination status and serotype distribution of Salmonella in foods in Luoyang from 2015 to 2018. Henan J Prev Med, 2019; 30(10):797–800; doi: 10.1351/5/j.cnki.hnjpm.1006-8414.2019.010.023
18.
LiuCX, YaoKY, RenDX, et al.Prevalence and characterization of Salmonella from meat in slaughterhouses in Hangzhou, China. Int J Food Microbiol, 2022; 371:109649; doi: 10.1016/j.ijfoodmicro.2022.109649
19.
MajowiczSE, MustoJ, ScallanE, et al.The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis, 2010; 50(6):882–889; doi: 10.1086/650733
20.
MaoXD, HuJF, LiuXM. Estimation on disease burden of foodborne non-typhoid salmonellosis in China using literature review method. Chin J Dis Control Prev, 2011; 15(7):622–625. Available from: https://zhjbkz.ahmu.edu.cn/article/id/JBKZ201107021
21.
MengF, LyuF, BieX, et al.Advances in transcriptomic analysis of Salmonella biofilms and their correlation with food safety. Curr Opin Food Sci, 2024; 55:101110; doi: 10.1016/j.cofs.2023.101110
22.
MiJQ, YuZY, YuH, et al.Quorum sensing systems in foodborne Salmonella spp. and corresponding control strategies using Quorum Sensing inhibitors for food storage. Trends Food Sci Tech, 2024; 144(2024):104320; doi: 10.1016/j.tifs.2023.104320
23.
MiaoS, LiuL, FuZ. Prevalence of Salmonella in Chinese food commodities: A meta-analysis. J Food Prot, 2022; 85(5):859–870; doi: 10.4315/JFP-21-304
24.
Ministry of Health of the People’s Republic of China. PRC (the People’s Republic of China) National Standard 4789.4-2010 National food safety standard-Food microbiological examination: Salmonella. Standards Press of China; Beijing: 2010. Available from: http://down.foodmate.net/standard/sort/3/21703.html
National Health Commission of the People’s Republic of China. China Food and Drug Administration. PRC (the People’s Republic of China) National Standard 4789.4-2016 National food safety standard-Food microbiological examination: Salmonella. Standards Press of China, Beijing: 2016. Available from: http://down.foodmate.net/standard/sort/3/50369.html
27.
OkidiL, OngengD, MuliroPS, et al.Agroecology influences Salmonella food contamination with high exposure risk among children in Karamoja sub-region: A high diarrhoea prevalent locality in Uganda. Heliyon, 2022; 8(11):e11703; doi: 10.1016/j.heliyon.2022.e11703
28.
QiuY, WangYZ, ZhangLM, et al.Analysis of Salmonella contamination and serotype monitoring in foods in Langfang City, Hebei Province,2015-2017. Med Animal Control, 2019; 35(2):134–136; doi: 10.7629/yxdwfz201902008
29.
SallamKL, KasemNG, AbdelkhalekA, et al.Extensively drug-, ciprofloxacin-, cefotaxime-, and azithromycin-resistant Salmonella enterica serovars isolated from camel meat in Egypt. Int J Food Microbiol, 2024; 411(2024):110538; doi: 10.1016/j.ijfoodmicro.2023.110538
30.
ScallanE, HoekstraRM, AnguloFJ, et al.Foodborne illness acquired in the United States—Major pathogens. Emerg Infect Dis, 2011; 17(1):7–15; doi: 10.3201/eid1701.p11101
31.
ShaoXL, MengXH, HuH, et al.Analysis on six foodborne pathogens contamination in retail raw poultry and livestock meat in Pudong New Area of Shanghai from 2015–2018. Occupation Health, 2019; 36(19):2645–2648. Available from: www.cnki.com.cn/Article/CJFDTotal-ZYJK202019016.htm
32.
SilvaGBL, AlvarezLAC, CamposFV, et al.A sensitive gold nanoparticle-based lateral flow immunoassay for quantitative on-site detection of Salmonella in foods. Microchem J, 2024; 199:109952; doi: 10.1016/j.microc.2024.109952
33.
SnyderTR, BoktorSW, M’ikanathaNM. Salmonellosis outbreaks by food vehicle, serotype, season, and geographical location, United States, 1998 to 2015. J Food Prot, 2019; 82(7):1191–1199; doi: 10.4315/0362-028X.JFP-18-494
34.
SunCH. Nutrition and Food Hygiene. People’s Medical Publishing House: Beijing; 2017.
35.
SunJY, LiuSJ, ZhaoW, et al.Contamination surveillance and serotype distribution of Salmonella in food in Jilin Province from 2011 to 2018. J Food Saf Qual, 2019; 11(24):9377–9382; doi: 10.1981/2/j.cnki.jfsq11-5956/ts.2020.24.053
36.
U.S. Centers for Disease Control FoodNet Fast pathogen surveillance. (2023). Available from: wwwn.cdc.gov/foodnetfast/ [Last accessed: 5thSep, 2023].
37.
UcheIV, MacLennanCA, SaulA. A Systematic Review of the Incidence, Risk Factors and Case Fatality Rates of Invasive Nontyphoidal Salmonella (iNTS) Disease in Africa (1966 to 2014). PLoS Negl Trop Dis, 2017; 11(1):e0005118; doi: 10.1371/journal.pntd.0005118
38.
VialSL, DoerscherDR, SchroederCM, et al.Confounding role of Salmonella serotype Dublin testing results of boneless and ground beef purchased for the national school lunch program, October 2013 to July 2017. J Food Prot, 2020; 83(4):628–636; doi: 10.4315/0362-028X.JFP-19-359
39.
WalterEJS, GriffinPM, BruceBB, et al.Estimating the number of illnesses caused by agents transmitted commonly through food: A scoping review. Foodborne Pathog Dis, 2021; 18(12):841–858; doi: 10.1089/fpd.2021.0038
40.
WangW, ZhaoL, HuY, et al.Epidemiological study on prevalence, serovar diversity, multidrug resistance, and CTX-M-type extended-spectrum β-lactamases of Salmonella spp. from patients with diarrhea, food of animal origin, and pets in several provinces of China. Antimicrob Agents Chemother, 2020; 64(7):e00092; doi: 10.1128/AAC.00092-2020
41.
WuYF, YuanBJ. Investigation on Salmonella contamination in retail fresh chicken food in Nanjing. J Nanjing Med Univ (Natural Science), 2015; 35(2):284–287; doi: 10.7655/NYDXBNS20150235
XuDS, ChenLP, LuZH, et al.Prevalence and serotyping of Salmonella in retail food in Huzhou China. J Food Prot, 2024; 87(2):100219; doi: 10.1016/j.jfp.2024.100219
44.
YangDJ, LiN. National Food Contamination and Hazardous Factors Risk workbook 2013. Beijing: China Quality Inspection Press, Standards Press of China. 2012.
45.
YaoXT, JiangYY, TanDM, et al.Analysis of surveillance data of Salmonella in food sold in Guangxi Zhuang autonomous Regin from 2012 to 2017. Chin J Food Hygiene, 2019; 31(5):449–455; doi: 10.1359/0/j.cjfh.2019.05.010
46.
ZhangDZ, HuangJY, ZhouQ, et al.Analysis on serotypes and antibiotic resistance characteristics of food-borne Salmonella strains in Guizhou Province from 2016 to 2018. Chin J Microbiol Immunol, 2019; 39(10):737–742; doi: 10.3760/cma.j.issn.0254-5101.2019.10.003
47.
ZhangZH, LiJY, ZhouRS, et al.Serotyping and antimicrobial resistance profiling of multidrug-resistant non-typhoidal Salmonella from farm animals in Hunan, China. Antibiotics (Basel), 2023; 12(7):1178; doi: 10.3390/antibiotics12071178
ZhangF, MaGZ, PanL, et al.Surveillance and analysis for food - borne pathogens in retailed foods in Shaanxi province, 2002–2006. Chin J Public Health, 2008; 24(2):222–224. Available from: www.zgggws.com/cn/article/2008/2
50.
ZhongSH, FengSW, LiJ, et al.Investigation on serotype, drug resistance and drug resistance genes of Salmonella in livestock and poultry products in Guangxi. Chin J Animal Husbandry Vet Med, 2018; 45(3):770–780; doi: 10.1643/1/j.cnki.1671-7236.2018.03.027
51.
ZhouT, NiWL, NiG, et al.Serotyping and pulsed field gel electrophoresis typing of Salmonella in food in Honghe prefecture from 2011 to 2018. J Food Saf Qual, 2019; 10(20):7694–7700; doi: 10.1981/2/j.cnki.jfsq11-5956/ts.2019.22.043
52.
ZouYQS, YangZS, TianYP, et al.Drug resistance analysis of food-borne Salmonella in Yunnan from 2014 to 2018. J Food Saf Qual, 2019; 10(22):7601–7605.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
