The contamination of fresh produce with antibiotic-resistant bacteria is of particular concern as they are often eaten raw and can be a source for foodborne diseases. Tetracyclines have been largely used in humans, animals and plants which might have accelerated microbial resistance to them. Enterococci and Escherichia coli can be used as indicators to monitor contamination of the fresh produce with tetracycline-resistant bacteria. The investigation related to this issue is very scarce in Oman. This study aimed at identifying tetracycline-resistant enterococci and E. coli in fresh produce at the market place. Thirty-one enterococci and ten E. coli were isolated from local (Oman) and imported fruits and vegetables (N= 105). Using the standard Kirby-Bauer disc diffusion method, resistance to tetracycline was found in 6 (19 %) enterococci, isolated from cucumber, lettuce and radish, and 5 (50 %) E. coli, obtained from cabbage, lettuce and radish. Genetic analysis revealed the presence of tetracycline resistance genes, tet(A) and tet(K), in E. coli and tet(K), tet(L) and tet(M) in enterococci, including Enterococcus sulfureus, Enterococcus mundtii, Enterococcus casseli avus and Enterococcus faecalis. The integron integrase IntI 1 gene, which is known to facilitate the dissemination of antibiotic resistance genes among bacteria, was detected in 2 isolates of E. coli. These results demonstrated the capability of fresh produce to act as a potential source for disseminating tetracycline or possibly other antibiotic-resistant bacteria through the food chain. Thus, control strategies are needed to reduce exposure of the public to such microorganisms.
Abriouel H, Ben Omar N, Molinos A, Lopez R, Grande M, Martinez-Viedma P, et al. Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal pop-ulations from raw fruit and vegetable foods, water and soil, and clinical samples. International Journal of Food Microbiology. 2008;(1–2):38–49.
2.
Asadollahi P, Razavi S, Asadollahi K, Pourshafie M, Talebi M. Rise of antibiotic resistance in clinical enterococcal isolates during 2001-2016 in iran: A review. New microbes and new infections. 2018;92–9.
3.
Al-Bahry S, Al-Mashani B, Al-Ansari A, Elshafie A, Mahmoud I, Al-Bahry S, et al. Biomonitoring marine habitats in reference to antibiotic resistant bacteria and ampicillin resistance determinants from oviductal fluid of the nesting green sea turtle, chelonia mydas. Asian Pacific Journal of Tropical Medicine. 2013;(9):1308–15.
4.
Ben Said L, Klibi N, Dziri R, Borgo F, Boudabous A, Ben Slama K, et al. Prevalence, antimicrobial resistance and genetic lineages of enterococcus spp. from vegetable food, soil and irrigation water in farm environments in tunisia. Journal of the Science of Food and Agriculture. 2016;(5):1627–33.
5.
Bezanson G, Macinnis R, Potter G, Hughes T. Presence and potential for horizontal transfer of antibiotic resistance in oxidase-positive bacteria populating raw salad vegetables. International Journal of Food Microbiology. 2008;(1–2):37–42.
6.
Campos J, Mourao J, Pestana N, Peixe L, Novais C, Antunes P. Microbiological quality of ready-to-eat salads: An underestimated vehicle of bacteria and clinically relevant antibiotic resistance genes. International Journal of Food Microbiology. 2013;(3):464–70.
7.
Cauwerts K, Decostere A, De Graef E, Haesebrouck F, Pasmans F. High prevalence of tetracycline resistance in enterococcus isolates from broilers carrying the erm(b) gene. Avian Pathology. 2007;(5):395-U73.
8.
Cdc. 2014;
9.
Chewapreecha C. Your gut microbiota are what you eat. Nature Reviews Microbiology. 2014;(1):3186.
10.
Clsi. 2015;
11.
Forslund K, Sunagawa S, Kultima J, Mende D, Arumugam M, Typas A, et al. Country-specific antibiotic use practices impact the human gut resistome. Genome Research. 2013;(7):1163–9.
12.
Gasparrini A, Markley J, Kumar H, Wang B, Fang L, Irum S, et al. Tetracycline-inactivating enzymes from environmental, human commensal, and pathogenic bacteria cause broad-spectrum tetracycline resistance. Communications Biology. 2020;3–4.
13.
Gaze W, Abdouslam N, Hawkey P, Wellington E. Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrobial Agents and Chemotherapy. 2005;(5):1802–7.
14.
Gillings M, Holley M, Stokes H. Evidence for dynamic exchange of qac gene cassettes between class 1 integrons and other integrons in freshwater biofilms. FEMS microbiology letters. 2009;(2):282–8.
15.
Hassan S, Altalhi A, Gherbawy Y, El-Deeb B. Bacterial load of fresh vegetables and their resistance to the currently used antibiotics in saudi arabia. Foodborne Pathogens and Disease. 2011;(9):1011–8.
16.
Hernandez M, Borrull F, Calull M. Analysis of antibiotics in biological samples by capillary electrophoresis. Tractrends in Analytical Chemistry. 2003;(7):702–7.
17.
Hoelzel C, Tetens J, Schwaiger K. Unraveling the role of vegetables in spreading antimicrobial-resistant bacteria: A need for quantitative risk assessment. Foodborne Pathogens and Disease. 2018;(11):671–88.
18.
Hussain M, Qureshi A. Health risks of heavy metal exposure and microbial contamination through consumption of vegetables irrigated with treated wastewater at dubai, uae. Environmental Science and Pollution Research. 2020;(10):11213–26.
19.
Jaglic Z, Cervinkova D. Genetic basis of resistance to quaternary ammonium compounds-the qac genes and their role: A review. Veterinarni Medicina. 2012;(6):275–81.
20.
Johnston L, Jaykus L. Antimicrobial resistance of enterococcus species isolated from produce. Applied and Environmental Microbiology. 2004;(5):3133–7.
21.
Jones-Dias D, Manageiro V, Ferreira E, Barreiro P, Vieira L, Moura I, et al. Architecture of class 1, 2, and 3 integrons from gram negative bacteria recovered among fruits and vegetables. Frontiers in Microbiology. 2016;
22.
Ijfs October. 2021;359–70.
23.
Jung Y, Matthews K. Potential transfer of extended spectrum betalactamase encoding gene, bla(shv18) gene, between klebsiella pneumoniae in raw foods. Food Microbiology. 2016;39–48.
24.
Karami N, Nowrouzian F, Adlerberth I, Wold A. Tetracycline resistance in escherichia coli and persistence in the infantile colonic microbiota. Antimicrobial Agents and Chemotherapy. 2006;(1):156–61.
25.
Khan S, Cao Q, Zheng Y, Huang Y, Zhu Y. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in beijing, china. Environmental Pollution. 2008;(3):686–92.
26.
Al-Kharousi Z, Guizani N, Al-Sadi A, Al-Bulushi I, Shaharoona B. Hiding in fresh fruits and vegetables: Opportunistic pathogens may cross geographical barriers. International journal of microbiology. 2016;
27.
Kohanski M, Dwyer D, Collins J. How antibiotics kill bacteria: From targets to networks. Nature Reviews Microbiology. 2010;(6):2333.
28.
Li X, Wang H. Tetracycline resistance associated with commensal bacteria from representative ready-toconsume deli and restaurant foods. 2010;(10):1841–8.
29.
Liu Y, Liu K, Lai J, Wu C, Shen J, Wang Y. Prevalence and antimicrobial resistance of enterococcus species of food animal origin from beijing and shandong province, china. Journal of Applied Microbiology. 2013;(2):555–63.
30.
Markley J, Wencewicz T. Frontiers in Microbiology. 2018;
31.
Ng L, Martin I, Alfa M, Mulvey M. Multiplex pcr for the detection of tetracycline resistant genes. Molecular and Cellular Probes. 2001;(4):209–15.
32.
O’flahertya E, Solimini A, Pantanella F, De Giusti M, Cummins E. Human exposure to antibiotic resistantescherichia coli through irrigated lettuce. Environment International. 2019;270–80.
33.
Olaimat A, Holley R. Factors influencing the microbial safety of fresh produce: A review. Food Microbiology. 2012;(1):1–19.
34.
Pan M, Chu L. Occurrence of antibiotics and antibiotic resistance genes in soils from wastewater irrigation areas in the pearl river delta region, southern china. Science of the Total Environment. 2018;145–52.
35.
Pesavento G, Calonico C, Ducci B, Magnanini A, Lo Nostro A. Prevalence and antibiotic resistance of enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiology. 2014;41.
36.
Roberts M. Update on acquired tetracycline resistance genes. Fems Microbiology Letters. 2005;(2):195–203.
37.
Roe M, Pillai S. Monitoring and identifying antibiotic resistance mechanisms in bacteria. Poultry Science. 2003;(4):622–6.
38.
Rosser S, Young H. Identification and characterization of class 1 integrons in bacteria from an aquatic environment. Journal of Antimicrobial Chemotherapy. 1999;(1):11–8.
39.
Dallal S, Shojaei M, Sharifi Yazdi M, Vahedi M, S. Microbial contamination of fresh vegetable and salad samples consumed in tehran, iran. Journal of food quality and hazards control. 2015;(4):139–43.
40.
Teuber M. Spread of antibiotic resistance with food-borne pathogens [Meeting on Evolution of Bacterial Virulence and Antibiotic Resistance, UNIV DELLA SVIZZER ITALIANA. Cellular and Molecular Life Sciences. 1999;(9–10):755–63.
41.
Tian Y, Yu H, Wang Z. Distribution of acquired antibiotic resistance genes among enterococcus spp. isolated from a hospital in baotou, china. BMC research notes. 2019;(1):27.
42.
Vincenti S, Raponi M, Sezzatini R, Giubbini G, Laurenti P. Enterobacteriaceae antibiotic resistance in readyto-eat foods collected from hospital and community canteens: Analysis of prevalence. Journal of Food Protection. 2018;(3):424–9.
43.
Zhang R, Eggleston K, Rotimi V, Zeckhauser R. Antibiotic resistance as a global threat: Evidence from china, kuwait and the united states. Globalization and Health. 2006;359–70.
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