Salmonella in Food Environments in Canteens: A Focus on Antibiotic and Disinfectant Resistance Patterns Food related areas and food handlers in canteens were analysed for Salmonella

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Şebnem Pamuk
Metin Erdoğan
Yeliz Yıldırım
Nurhan Ertaş Onmaz


Antibiotic resistance, Disinfectant resistance, Food environments, Public health, Salmonella


The objective of this study was to determine the molecular characterization and antibiotic and disinfectant resistance potential of Salmonella isolates from food related areas in canteens.This study was performed in food related areas as well as food handlers in student canteens in University campus to trace source of Salmonella contamination with a special focus on antibiotic and disinfectant resistance of the isolates. Salmonella isolates were identified by conventional and molecular techniques. Genetic similarity, antibiotic and disinfectant resistance patterns of the isolates were performed by sequence analyzing, disc diffusion and PCR, respectively. Salmonella contamination was determined from hand (Newport and Infantis), knife handle (Newport) and grilled chicken (Koessen) samples. The identity of the 16S rRNA sequence of two Newport isolates (knife handle and hand) from Canteen 4 and Canteen 6 were found 100% identic. Multidrug resistance (MDR) was observed among all Salmonella isolates with resistance to at least five or more antibiotics. sugE and qacEΔ1 disinfectant genes were determined in 2 and 1 isolate respectively while cross-resistance to antibiotics and disinfectants in three isolates were detected. The results of this study indicate that the food-handlers and food preparation equipments may serve as reservoirs for cross-resistant Salmonella, a potential public health concern. Therefore, periodic training programmes should effectively be implemented for food handlers. Owing to the growing concern that antibiotic resistant mutants could be induced by improper disinfectant use, unnecessary and misuse of disinfectants should be avoided, especially on food contact surfaces.


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1.Dao HTA, Yen PT. Study of Salmonella, Campylobacter, and Escherichia coli contamination in raw food available in factories, schools, and hospital canteens in Hanoi, Vietnam. Ann NY. Acad Sci 2006; 1081(1): 262-265.
2.Kirk MD, Pires SM, Black RE, Caipo M, Crump JA, Devleesschauwer B, Döpfer D, Fazil A, Fischer-Walker CL, Hald T, Hall AJ, Keddy KH, Lake RJ, Lanata CF, Torgerson PR, Havelaar AH, Angulo FJ. World Health Organization estimates of the global and regional disease burden of 22 foodborne bacterial, protozoal, and viral diseases, 2010: a data synthesis. PLoS Med 2015; 12(12): e1001921.
3. Langridge GC, Wain J, Nair S. Invasive salmonellosis in humans. Eco Sal Plus 2012; 5(1).
4. Bula-Rudas FJ, Rathore MH, Maraqa NF. Salmonella infections in childhood. Adv Pediatr 2015; 62(1): 29-58.
5. Hawkey J, Edwards DJ, Dimovski K, Hiley L, Billman-Jacobe H, Hogg G, Holt KE. Evidence of microevolution of Salmonella Typhimurium during a series of egg-associated outbreaks linked to a single chicken farm. BMC Genomics 2013; 14(1): 1-15.
6. Padungtod P, Kadohira M, Hill G. Livestock production and foodborne diseases from food animals in Thailand. J Vet Med Sci, 2008; 70(9): 873-879.
7. McKee SR, Townsend JC, Bilgili S.F. Use of a scald additive to reduce levels of Salmonella Typhimurium during poultry processing. Poult Sci J 2008; 87(8): 1672-1677.
8. Arguello H, Carvajal A, Collazos JA, García-Feliz C, Rubio P. Prevalence and serovars of Salmonella Enterica on pig carcasses, slaughtered pigs and the environment of four Spanish slaughterhouses. Food Res Int 2012; 45(2): 905-912.
9. Hernández M, Gómez-Laguna J, Luque, I, Herrera-León S, Maldonado A, Reguillo L, Astorga RJ. Salmonella prevalence and characterization in a free-range pig processing plant: tracking in trucks, lairage, slaughter line and quartering. Int J Food Microbiol 2013; 162(1): 48-54.
10. Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SC. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int 2012; 45(2): 502-531.
11. Gerba CP. Quaternary ammonium biocides: efficacy in application. Appl Environ Microbiol 2015; 81(2): 464-469.
12. Zhang C, Cui F, Zeng GM, Jiang M, Yang ZZ, Yu ZG, Zhu MY, Shen LQ. Quaternary ammonium compounds (QACs): a review on occurrence, fate and toxicity in the environment. Sci. Total Environ 2015; 518: 352-362.
13. Morente EO, Fernández-Fuentes MA, Burgos MJG, Abriouel H, Pulido RP, Galvez A. Biocide tolerance in bacteria. Int J Food Microbiol 2013; 162(1): 13-25.
14. Sveum WH, Moberg LJ, Rude RA, Frank JF. Microbiological monitoring of the food processing environment. In: Vanderzant C, Splittstoesser DF (Ed): Compendium of methods for the microbiological examination of foods. 51-74. Public Health Association, Washington, 1992.
15. International Standard Organization (ISO) 6579, Microbiological of food and animal feeding stuffs-horizontal method for the detection of Salmonella spp. International Standards Organization. 1-50. Geneva, Switzerland, 2002.
16. Kalendar R, Lee D, Schulman AH. Fast PCR software for PCR primer and probe design and repeat search. G3 2009; 3(1): 1-14.
17. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symp Ser 1999; 41: 95-98.
18. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007; 24(8): 1596-1599.
19. Bauer AW, Kirby WMM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 1966; 45(4): 493-6.
20. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. Twentieth Informational Supplement, M100-S20, 2010.
21. World Health Organization (WHO). Food Hygiene, Food and Agriculture Organization. Pan European Conference on food safety and quality, Italy, 2002.
22. Birhaneselassie M, Williams D. A study of Salmonella carriage among asymptomatic food-handlers in southern Ethiopia. Int J Nutr Food Sci 2013; 2(5): 243-245.https://doi: 10.11648/j.ijnfs.20130205.15
23. Woh PY, Thong KL, Behnke JM, Lewis JW, Zain SNM. Characterization of nontyphoidal Salmonella isolates from asymptomatic migrant food handlers in Peninsular Malaysia. J Food Prot 2017; 80(8): 1378-1383.
24. Santos M, Nogueira JR, Patarata L, Mayan O. Knowledge levels of food handlers in Portuguese school canteens and their self-reported behavior towards food safety. Int J Environ Health Res 2008; 18(6): 387-401.
25. Wirtanen G, Storgards E, Mattila-Sandholm T Biofilms. In: Caballero B, Trugo L, Finglas P. (Ed): Encyclopedia of Food Sciences and Nutrition. 484-9. Academic Press, London, 2003.
26. Santana NG, Almeida RC, Ferreira JS, Almeida PF. Microbiological quality and safety of meals served to children and adoption of good manufacturing practices in public school catering in Brazil. Food Control 2009; 20(3): 255-261.
27. Nyenje ME, Odjadjare CE, Tanih NF, Green E, Ndip RN. Foodborne pathogens recovered from ready-to-eat foods from roadside cafeterias and retail outlets in Alice, Eastern Cape Province, South Africa: public health implications. Int J Environ Res Public Health 2012; 9(8): 2608-2619.
28. Velhner M, Potkonjak D, Stojanov I, Stojanović D, Petrović J, Kozoderović G. Salmonella control in poultry production and resistance monitoring in Serbia. Arch. Vet Sci 2011; 4(2): 11-22.
29. Campos J, Pichel M, Vaz TMI, Tavechio AT, Fernandes SA, Muñoz N, Rodriguez C, Realpec ME, Morenoc J, Arayad P, Fernándezd J, Fernándezd A, Campose E, Duartee F, Gustafsonf NW, Binsztein N, Gutierrez EP. Building PulseNet Latin America and Caribbean Salmonella regional database: First conclusions of genetic subtypes of S. Typhi, S. Typhimurium and S. Enteritidis circulating in six countries of the region. Food Res Int 2012; 45(2): 1030-1036.
30. Luvsansharav UO, Vieira A, Bennett S, Huang J, Healy JM, Hoekstra RM, Bruce BB, Cole D. Salmonella serotypes: A novel measure of association with foodborne transmission. Foodborne Pathog Dis 2020; 17(2): 151-155.
31. European Food Safety Authority, & European Centre for Disease Prevention and Control (EFSA). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2015. EFSA J 2016; 14(12): e04634.
32. Campioni F, Zoldan MM, Falcao JP. Characterization of Salmonella Enteritidis strains isolated from poultry and farm environments in Brazil. Epidemiol Infect 2014; 142(7): 1403-1410.
33. Davies R, Wales A. Antimicrobial resistance on farms: a review including biosecurity and the potential role of disinfectants in resistance selection. Compr Rev Food Sci Food Saf 2019; 18(3): 753-774.
34. Chuanchuen R, Khemtong S, Padungtod P. Occurrence of qacE/qacED1 genes and their correlation with class 1 integrons in Salmonella enterica isolates from poultry and swine. Southeast Asian J Trop Med Public Health 2007; 38: 855-862.
35. Long M, Lai H, Deng W, Zhou K, Li B, Liu S, Fan L, Wang H, Zou L. Disinfectant susceptibility of different Salmonella serotypes isolated from chicken and egg production chains. J Appl Microbiol 2016; 121(3): 672-681.
36. Fernandez Marquez, ML, Burgos MJG, Pulido RP, Gálvez A, López RL.,. Biocide tolerance and antibiotic resistance in Salmonella isolates from hen eggshells. Foodborne Pathog Dis 2017; 14(2): 89-95.
37. Deng W, Quan Y, Yang S, Guo L, Zhang X, Liu S, Chen S, Zhou K, He L, Li B, Gu Y, Zhao S, Zou L. Antibiotic resistance in Salmonella from retail foods of animal origin and its association with disinfectant and heavy metal resistance. Microb Drug Resist 2018; 24(6): 782-791.
38. Donaghy JA, Jagadeesan B, Goodburn K, Grunwald L, Jensen ON, Jespers AD, Kanagachandran K, Hervé Lafforgue H, Seefelder W, Quentin MC. Relationship of sanitizers, disinfectants, and cleaning agents with antimicrobial resistance. J. Food Prot 2019; 82(5): 889-902.
39. Knapp L, Amézquita A, McClure P, Stewart S, Maillard JY. Development of a protocol for predicting bacterial resistance to microbicides. Appl. Environ. Microbiol 2015; 81(8): 2652-2659.
40. Paul D, Chakraborty R, Mandal SM. Biocides and health-care agents are more than just antibiotics: Inducing cross to co-resistance in microbes. Ecotoxicol Environ Saf 2019; 174: 601-610.
41. Food and Drug Administration (FDA). Report of the FDA Retail Food Program Database of Foodborne Illness Risk Factors. US Food and Drug Administration, Center for Food Safety and Applied Nutrition, Washington DC, 2000.