The six major non-O157 serogroups of Shiga toxin–producing Escherichia coli (STEC) are responsible for serious foodborne outbreaks worldwide. This research aimed to detect the six major non-O157 STEC in ground beef, artisanal dairy products, lettuce, spinach, turkey, and chicken sold in northern Morocco. Real-time polymerase chain reaction was utilized to identify the presence of the stx1, stx2, eae, wzx O26, wzx O45, wzx O103, wbdl O111, wzx O121, and ihp1 O145 genes. Out of 310 samples analyzed, Shiga toxin (stx) was detected in 55 enrichments (17.74%), stx, and eae were detected in 54/310 enrichments (17.42%), stx, eae, and genes of at least one of the six serogroups were detected in 34/310 enrichments (10.97%). Among the food matrices analyzed, ground beef showed the highest contamination rate with stx, eae, and O serogroups 13/70 (18.6%), followed by dairy 17/100 (17.00%), turkey 3/40 (7.5%), and chicken 1/40 (2.5%). No O serogroups were detected in lettuce and spinach. The most frequent serogroup was O26 (22/34; 64.7%), followed by O145 (12/34; 35.3%), O45 (12/34; 35.3%), O121 (8/34; 23.5%), O103 (8/34; 23.5%), and O111 (6/34; 17.6%). A set of 32 STEC strains were isolated from nine positive samples (9/34; 26.5%). A high rate of food contamination with STEC may indicate firstly a high public health risk due to this pathogen in beef and dairy products and secondly a lack of compliance with standard hygiene practices. Consequently, it emphasizes the urgent need for rigorous monitoring and intervention measures aimed at mitigating the incidence of STEC contamination.
Arikè SalifouCF, BokoC, HouagaI, et al.Prevalence of Shiga Toxin–Producing Escherichia coli O157, O26 and O111 in Milk, Meat and Feces of Cattle, Sheep and Pigs Slaughtered in Benin. JABs, 2020; 152:15667–15675; doi: 10.35759/JABs.152.6
2.
ArraisBR, FerreiraMRA, SilvaTS, et al.Shiga Toxin–Producing Escherichia coli (STEC) and Salmonella Spp. in Lettuce. RSD, 2020; 9(7):e281974150; doi: 10.33448/rsd-v9i7.4150
3.
AyoadeF, OguzieJ, AkanoK, et al.Molecular Surveillance of Non-O157 Shiga Toxigenic Escherichia coli in Selected Chicken Abattoirs and Retail Outlets in Osogbo, Osun State, Nigeria. JFSH, 2022; doi: 10.18502/jfsh.v8i1.9957
4.
BergerCN, SodhaSV, ShawRK, et al.Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol, 2010; 12(9):2385–2397; doi: 10.1111/j.1462-2920.2010.02297.x
5.
BosilevacJM, KoohmaraieM. Prevalence and characterization of Non-O157 Shiga Toxin-Producing Escherichia coli Isolates from commercial ground Beef in the United States. Appl Environ Microbiol, 2011; 77(6):2103–2112; doi: 10.1128/AEM.02833-10
6.
BrooksJT, SowersEG, WellsJG, et al.Non‐O157 Shiga Toxin–producing Escherichia coli infections in the United States, 1983–2002. J Infect Dis, 2005; 192(8):1422–1429; doi: 10.1086/466536
7.
BrugèreH, AuvrayF, Mariani-KurkdjianP, et al.E. coli producteurs de shigatoxines (STEC): Définitions, virulence et propriétés des souches entérohémorragiques (EHEC). Bulletin épidémiologique, santé animale et alimentation/Spécial Risques alimentaires microbiologiques, 2011(50):23–29. https://be.anses.fr/sites/default/files/BEP-mg-BE50-art6.pdf
8.
DishanA, HizlisoyH, BarelM, et al.Biofilm formation, antibiotic resistance and genotyping of Shiga Toxin–producing Escherichia coli isolated from retail chicken meats. Br Poult Sci, 2023; 64(1):63–73; doi: 10.1080/00071668.2022.2116697
9.
EFSA BIOHAZ Panel, KoutsoumanisK, AllendeA, et al.Pathogenicity assessment of Shiga Toxin–producing Escherichia coli (STEC) and the public health risk posed by contamination of food with STEC. EFSA J, 2020; 18(1); doi: 10.2903/j.efsa.2020.5967
10.
EißenbergerK, MoenchD, DrissnerD, et al.Adherence factors of enterohemorrhagic Escherichia coli O157:H7 Strain Sakai influence its uptake into the roots of valerianella locusta grown in soil. Food Microbiol, 2018; 76:245–256; doi: 10.1016/j.fm.2018.05.016
11.
ElsayedMSAE, EldsoukySM, RoshdyT, et al.Genetic and antimicrobial resistance profiles of non-O157 Shiga Toxin–producing Escherichia coli from different sources in Egypt. BMC Microbiol, 2021; 21(1):257; doi: 10.1186/s12866-021-02308-w
12.
EtcheverríaAI, PadolaNL, SanzME, et al.Occurrence of Shiga Toxin–Producing E. coli (STEC) on carcasses and retail beef cuts in the marketing chain of beef in Argentina. Meat Sci, 2010; 86(2):418–421; doi: 10.1016/j.meatsci.2010.05.027
ForanoE, Chaucheyras-DurandF, BertinY, et al.Portage Des Escherichia coli Entérohémorragiques Par Les Ruminants et Effet de Probiotiques. Biol Aujourdhui, 2013; 207(4):261–267; doi: 10.1051/jbio/2013023
17.
GökmenM, İlhanZ, TavşanlıH, et al.Prevalence and molecular characterization of Shiga Toxin–producing Escherichia coli in animal source foods and green leafy vegetables. Food Sci Technol Int, 2024; 30(1):30–36; doi: 10.1177/10820132221125104
18.
Guzman-HernandezR, Contreras-RodriguezA, Hernandez-VelezR, et al.Mexican unpasteurized fresh cheeses are contaminated with salmonella Spp., non-O157 Shiga Toxin–producing Escherichia coli and potential uropathogenic E. coli Strains: A public health risk. Int J Food Microbiol, 2016; 237:10–16; doi: 10.1016/j.ijfoodmicro.2016.08.018
19.
ISO/TS 13136. Microbiology of food and animal feed—real-time Polymerase Chain Reaction (PCR)-based method for the detection of food-borne pathogens—horizontal method for the detection of Shiga Toxin–producing Escherichia coli (STEC) and the determination of O157, O111, O26, O103 and O145 serogroups. 2012. Available from: https://www.iso.org/standard/53328.html
LucatelliA, MonteDFM, AlvaresPP, et al.Virulent Shiga Toxin–producing Escherichia coli (STEC) O157:H7 ST11 isolated from ground beef in Brazil. Braz J Microbiol, 2024; 55(4):3513–3520; doi: 10.1007/s42770-024-01468-x
23.
MaJ, Mark IbekweA, CrowleyDE, et al.Persistence of Escherichia coli O157 and non-O157 strains in agricultural soils. Sci Total Environ, 2014; 490:822–829; doi: 10.1016/j.scitotenv.2014.05.069
24.
MadicJ, VingadassalonN, de GaramCP, et al.Detection of Shiga Toxin–producing Escherichia coli serotypes O26:H11, O103:H2, O111:H8, O145:H28, and O157:H7 in raw-milk cheeses by using multiplex real-time PCR. Appl Environ Microbiol, 2011; 77(6):2035–2041; doi: 10.1128/AEM.02089-10
25.
MajowiczSE, ScallanE, Jones-BittonA, et al.Global incidence of human Shiga Toxin–producing Escherichia coli infections and deaths: A systematic review and knowledge synthesis. Foodborne Pathog Dis, 2014; 11(6):447–455; doi: 10.1089/fpd.2013.1704
26.
MathusaEC, ChenY, EnacheE, et al.Non-O157 Shiga Toxin–producing in foods. J Food Prot, 2010; 73(9):1721–1736; doi: 10.4315/0362-028X-73.9.1721
Melton-CelsaAR. Shiga Toxin (Stx) Classification, Structure, and Function. Microbiol Spectr (SperandioV and HovdeCJ eds.) 2014; 2(4):10–1128; doi: 10.1128/microbiolspec.EHEC-0024-2013
29.
MohammedMA, SallamKI, EldalyEAZ, et al.Occurrence, serotypes and virulence genes of non-O157 Shiga Toxin–producing Escherichia coli in fresh beef, ground beef, and beef burger. Food Control, 2014; 37:182–187; doi: 10.1016/j.foodcont.2013.09.035
30.
OnyekaLO, AdesiyunAA, IsmailA, et al.Evidence for horizontal transmission and recirculation of Shiga Toxin–producing Escherichia coli in the beef production chain in South Africa Using whole genome sequencing. Pathogens, 2024; 13(9):732; doi: 10.3390/pathogens13090732
31.
OuarroudB, El MaadoudiM, BarakatA, et al.Shiga Toxin–producing Escherichia coli (STEC); virulence factors, pathologies caused and foods at risk: Review. In: International Conference on Advanced Intelligent Systems for Sustainable Development (AI2SD’2023). (EzziyyaniM, KacprzykJ, and BalasVE eds). Lecture Notes in Networks and Systems Springer Nature Switzerland: Cham; 2024; pp. 330–341; doi: 10.1007/978-3-031-52385-4_31
32.
PerelleS, DilasserF, GroutJ, et al.Screening food raw materials for the presence of the world’s most frequent clinical cases of Shiga Toxin-encoding Escherichia coli O26, O103, O111, O145 and O157. Int J Food Microbiol, 2007; 113(3):284–288; doi: 10.1016/j.ijfoodmicro.2006.08.014
33.
PiresSM, MajowiczS, GillA, et al.Global and regional source attribution of Shiga Toxin–producing Escherichia coli infections using analysis of outbreak surveillance data. Epidemiol Infect, 2019; 147:e236; doi: 10.1017/S095026881900116X
34.
RappD, RossCM, MacleanP, et al.Investigation of on-farm transmission routes for contamination of dairy cows with Top 7 Escherichia coli O-serogroups. Microb Ecol, 2021; 81(1):67–77; doi: 10.1007/s00248-020-01542-5
35.
SarwarA, AslamB, RasoolMH, et al.Non-O157 Shiga Toxin–producing E. coli Co-harboring BlaNMD-1 and Mcr-1 in various sources of food supply chain. Health Threat from Farm to Fork, 2024; doi: 10.20944/preprints202404.1814.v1
SokolovicM, ŠimpragaB, Amšel-ZelenikaT, et al.Prevalence and characterization of Shiga Toxin–producing Escherichia coli isolated from animal feed in Croatia. Microorganisms, 2022; 10(9):1839; doi: 10.3390/microorganisms10091839
38.
ToroM, RiveraD, JiménezMF, et al.Isolation and characterization of non-O157 Shiga Toxin–producing Escherichia coli (STEC) isolated from retail ground beef in Santiago, Chile. Food Microbiol, 2018; 75:55–60; doi: 10.1016/j.fm.2017.10.015
39.
TyagiD, KraftAL, Levadney SmithS, et al.Pre-harvest survival and post-harvest chlorine tolerance of enterohemorrhagic Escherichia coli on lettuce. Toxins (Basel), 2019; 11(11):675; doi: 10.3390/toxins11110675
