journal article·2023-11-30Open access

Frequency and Antimicrobial Resistance Patterns of Foodborne Pathogens in Ready-to-Eat Foods: An Evolving Public Health Challenge

Adil Abalkhail

Applied Sciences· Volume 13· Issue 23

Abstract

Food products that are ready-to-eat have become increasingly popular in recent years due to their efficiency, affordability, and convenience. However, there are concerns about public health because certain products, particularly animal products, may contain antibiotic-resistant bacteria. This study aimed to quickly and accurately identify foodborne pathogens, such as Escherichia coli (E. coli) and Staphylococcus aureus (S. aureus), in samples of shawarma and chicken burgers using peptide mass fingerprinting (PMF) technology. Additionally, the prevalence and levels of antibiotic resistance in the pathogens were determined. The study utilized 300 samples obtained from fast food restaurants in Al Qassim, Saudi Arabia. A variety of methods were used to identify foodborne pathogens, including culture on specific media, bacterial counts by numerical dilutions of homogenized samples, and proteome identification by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS). The Kirby–Bauer method was applied to detect the susceptibility and resistance of the bacteria to various antibiotics. PCR was utilized to identify antimicrobial resistance genes such as blaTEM, tet(A), blaZ, and mecA in S. aureus and E. coli isolates. The percentage of E. coli, S. aureus, Salmonella, Listeria monocytogenes (L. monocytogenes), Acinetobacter baumannii (A. baumannii), and Hafnia alevei (H. alevei) was 34%, 31%, 10.67%, 7.33%, 6.67%, and 4%, respectively. Shawarma samples were found to contain the highest levels of pathogens, compared with chicken burger samples. According to the MBT Compass Flex Series Version 1.3 software, all isolates were identified with 100% accuracy. The log score for MBT identification ranged from 2.00 to 2.56. Among E. coli isolates, ampicillin, and penicillin had the highest resistance rate (100%), followed by tetracycline (35.29%). A number of antibiotics were reported to be resistant to S. aureus, including nalidixic acid (100%), followed by penicillin (96.77%), piperacillin (45.16%), and norfloxacin (32.26%). Some E. coli isolates were susceptible to tetracycline (49.02%), nalidixic acid (47.06%), and piperacillin (43.14%), whereas amikacin was the only drug that was effective against 32.72% of S. aureus isolates. The proportions of the blaTEM and tet(A) genes in E. coli isolates were 55.89% and 45.1%, respectively, whereas S. aureus strains did not possess either of these genes. However, 21.5% and 47.31% of blaz and mecA genes were present among various isolates of S. aureus, respectively. In contrast, E. coli strains did not possess either of these genes. In conclusion, the fast identification and antimicrobial profiles of the foodborne pathogens were useful in identifying which restaurants and fast food outlets may need to improve their food safety practices. Ultimately, our results will be used to devise targeted strategies to control foodborne pathogens.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Bacterial Identification and Susceptibility Testing · Identification and Quantification in Food · Salmonella and Campylobacter epidemiology

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Public Health, College of Public Health and Health Informatics, Qassim University, Al Bukayriyah 52741, Saudi Arabia

Funding

Deanship of Scientific Research, Qassim University

References (100+)

Show source-provided references
1. Bintsis, T. (2017). Foodborne pathogens. AIMS Microbiol., 3.10.3934/microbiol.2017.3.529 ↗
2. Food safety issues in fresh produce supply chain with particular reference to sub-Saharan Africa10.1016/j.foodcont.2020.107737 ↗
3. Acinetobacter baumannii as a community foodborne pathogen: Peptide mass fingerprinting analysis, genotypic of biofilm formation and phenotypic pattern of antimicrobial resistance10.1016/j.sjbs.2020.11.052 ↗
4. Alzaben, F., Fat’hi, S., Elbehiry, A., Alsugair, M., Marzouk, E., Abalkhail, A., Almuzaini, A.M., Rawway, M., Ibrahem, M., and Sindi, W. (2022). Laboratory diagnostic methods and antibiotic resistance patterns of Staphylococcus aureus and Escherichia coli strains: An Evolving Human Health Challenge. Diagnostics, 12.10.3390/diagnostics12112645 ↗
5. Antibiogram and phylogenetic diversity of enterotoxigenic Staphylococcus aureus strains from milk products and public health implications10.1016/j.sjbs.2020.06.028 ↗
6. Enterotoxigenicity and antibiotic resistance of coagulase-negative staphylococci isolated from raw buffalo and cow milk10.1089/mdr.2019.0114 ↗
7. Elbehiry, A., Marzouk, E., Abdeen, E., Al-Dubaib, M., Alsayeqh, A., Ibrahem, M., Hamada, M., Alenzi, A., Moussa, I., and Hemeg, H.A. (2019). Proteomic characterization and discrimination of Aeromonas species recovered from meat and water samples with a spotlight on the antimicrobial resistance of Aeromonas hydrophila. Microbiologyopen, 8.10.1002/mbo3.782 ↗
8. Elbehiry, A., Abalkhail, A., Marzouk, E., Elmanssury, A.E., Almuzaini, A.M., Alfheeaid, H., Alshahrani, M.T., Huraysh, N., Ibrahem, M., and Alzaben, F. (2023). An Overview of the Public Health Challenges in Diagnosing and Controlling Human Foodborne Pathogens. Vaccines, 11.10.3390/vaccines11040725 ↗
9. Lebelo, K., Malebo, N., Mochane, M.J., and Masinde, M. (2021). Chemical contamination pathways and the food safety implications along the various stages of food production: A review. Int. J. Environ. Res. Public Health, 18.10.3390/ijerph18115795 ↗
10. Kamala, K., and Kumar, V.P. (2018). Microbial Contamination and Food Degradation, Elsevier.
11. Cardoso, M.J., Ferreira, V., Truninger, M., Maia, R., and Teixeira, P. (2021). Cross-contamination events of Campylobacter spp. in domestic kitchens associated with consumer handling practices of raw poultry. Int. J. Food Microbiol., 338.10.1016/j.ijfoodmicro.2020.108984 ↗
12. Food-Borne Diseases and their Impact on Health10.13005/bbra/3129 ↗
13. Chen, L., Wang, J., Zhang, R., Zhang, H., Qi, X., He, Y., and Chen, J. (2022). An 11-year analysis of bacterial foodborne disease outbreaks in Zhejiang Province, China. Foods, 11.10.3390/foods11162382 ↗
14. Qi, X., Alifu, X., Chen, J., Luo, W., Wang, J., Yu, Y., and Zhang, R. (2022). Descriptive study of foodborne disease using disease monitoring data in Zhejiang Province, China, 2016–2020. BMC Public Health, 22.10.1186/s12889-022-14226-1 ↗
15. Jaffee, S., Henson, S., Unnevehr, L., Grace, D., and Cassou, E. (2018). The Safe Food Imperative: Accelerating Progress in Low-and Middle-Income Countries, World Bank Publications.10.1596/978-1-4648-1345-0 ↗
16. Alhashim, L.A., Alshahrani, N.Z., Alshahrani, A.M., Khalil, S.N., Alrubayii, M.A., Alateeq, S.K., and Zakaria, O.M. (2022). Food safety knowledge and attitudes: A cross-sectional study among Saudi consumers from food trucks owned by productive families. Int. J. Environ. Res. Public Health, 19.10.3390/ijerph19074322 ↗
17. Incidence and antimicrobial susceptibility of Escherichia coli isolated from beef (meat muscle, liver and kidney) samples in Wa Abattoir, Ghana10.1080/23311932.2020.1718269 ↗
18. Current trends in sample preparation by solid-phase extraction techniques for the determination of antibiotic residues in foodstuffs: A review10.1080/10408398.2020.1798349 ↗
19. Application of liquid-liquid extraction for the determination of antibiotics in the foodstuff: Recent trends and developments10.1080/10408347.2020.1798211 ↗
20. Rajaei, M., Moosavy, M.-H., Gharajalar, S.N., and Khatibi, S.A. (2021). Antibiotic resistance in the pathogenic foodborne bacteria isolated from raw kebab and hamburger: Phenotypic and genotypic study. BMC Microbiol., 21.10.1186/s12866-021-02326-8 ↗
21. Novel antimicrobial agents for combating antibiotic-resistant bacteria10.1016/j.addr.2022.114378 ↗
22. Nanomaterial-based therapeutics for antibiotic-resistant bacterial infections10.1038/s41579-020-0420-1 ↗
23. Antibiotics: Practice and opinions of Cambodian commercial farmers, animal feed retailers and veterinarians10.1186/s13756-016-0147-y ↗
24. World Health Organization report: Current crisis of antibiotic resistance10.1007/s12668-019-00658-4 ↗
25. Salam, M.A., Al-Amin, M.Y., Salam, M.T., Pawar, J.S., Akhter, N., Rabaan, A.A., and Alqumber, M.A. (2023). Antimicrobial Resistance: A Growing Serious Threat for Global Public Health. Healthcare, 11.10.20944/preprints202305.0555.v1 ↗
26. Importance of antibiotic residues in animal food10.1016/j.fct.2019.01.033 ↗
27. The public health issue of antibiotic residues in food and feed: Causes, consequences, and potential solutions
28. A review on antibiotic resistant and implication on food chain
29. Pathogenic bacteria in cheese, raw and pasteurised milk10.1002/vms3.604 ↗
30. Microbial load and antibiotic resistance in raw beef preparations from northwest Spain10.1002/fsn3.1319 ↗
31. Effect of commercial probiotic (Protexin®) on growth, survival and microbial quality of shrimp (Litopenaeus vannamei)
32. Good microbes, bad genes? The dissemination of antimicrobial resistance in the human microbiome10.1080/19490976.2022.2055944 ↗
33. Serwecińska, L. (2020). Antimicrobials and antibiotic-resistant bacteria: A risk to the environment and to public health. Water, 12.10.3390/w12123313 ↗
34. Pathogenicity, genetic typing, and antibiotic sensitivity of Vibrio alginolyticus isolated from Oreochromis niloticus and Tilapia zillii
35. Emerging MDR-Pseudomonas aeruginosa in fish commonly harbor opr L and tox A virulence genes and bla TEM, bla CTX-M, and tet A antibiotic-resistance genes10.1038/s41598-020-72264-4 ↗
36. The occurrence of the multidrug resistance (MDR) and the prevalence of virulence genes and QACs resistance genes in E. coli isolated from environmental and avian sources10.1186/s13568-019-0920-4 ↗
37. Bacteria antibiotic resistance: New challenges and opportunities for implant-associated orthopedic infections10.1002/jor.23656 ↗
38. Novovic, K., Mihajlovic, S., Vasiljevic, Z., Filipic, B., Begovic, J., and Jovcic, B. (2015). Carbapenem-resistant Acinetobacter baumannii from Serbia: Revision of CarO classification. PLoS ONE, 10.10.1371/journal.pone.0122793 ↗
39. Gelalcha, B.D., and Kerro Dego, O. (2022). Extended-Spectrum Beta-Lactamases Producing Enterobacteriaceae in the USA Dairy Cattle Farms and Implications for Public Health. Antibiotics, 11.10.3390/antibiotics11101313 ↗
40. Infectious Diseases Society of America guidance on the treatment of extended-spectrum β-lactamase producing Enterobacterales (ESBL-E), carbapenem-resistant Enterobacterales (CRE), and Pseudomonas aeruginosa with difficult-to-treat resistance (DTR-P. aeruginosa)10.1093/cid/ciaa1478 ↗
41. Food-borne diseases—The challenges of 20 years ago still persist while new ones continue to emerge10.1016/j.ijfoodmicro.2010.01.021 ↗
42. VacA and cagA genotypes status and antimicrobial resistance properties of Helicobacter pylori strains isolated from meat products in Isfahan province, Iran
43. Ready-to-eat street-vended food as a potential vehicle of bacterial pathogens and antimicrobial resistance: An exploratory study in Porto region, Portugal10.1016/j.ijfoodmicro.2015.04.016 ↗
44. Vitamin B12 intake from animal foods, biomarkers, and health aspects10.3389/fnut.2019.00093 ↗
45. Altaf Hussain, M., Wang, W., Sun, C., Gu, L., Liu, Z., Yu, T., Ahmad, Y., Jiang, Z., and Hou, J. (2020). Molecular Characterization Of Pathogenic Salmonella Spp From Raw Beef In Karachi, Pakistan. Antibiotics, 9.10.3390/antibiotics9020073 ↗
46. Prevalence of Listeria monocytogenes, Yersinia enterocolitica, Staphylococcus aureus, and Salmonella enterica Typhimurium in meat and meat products using multiplex polymerase chain reaction10.14202/vetworld.2017.927-931 ↗
47. Review on major food-borne zoonotic bacterial pathogens10.1155/2020/4674235 ↗
48. A comparative study of the antibacterial properties of milk from different domestic animals10.1111/1471-0307.12757 ↗
49. Occurrence and spread of antibiotic-resistant bacteria on animal farms and in their vicinity in Poland and Ukraine10.1007/s11356-021-17773-z ↗
50. Multidrug-resistant pathogens in the food supply10.1089/fpd.2014.1865 ↗
51. Global contributors to antibiotic resistance10.4103/jgid.jgid_110_18 ↗
52. Environmental antibiotics and resistance genes as emerging contaminants: Methods of detection and bioremediation
53. Hitchins, A.D., Jinneman, K., and Chen, Y. (2017). Bacteriological Analytical Manual, FDA.
54. Microbial quality of poultry meat in an ISO 22000: 2005 certified poultry processing plant of Kathmandu valley10.1186/s40550-019-0078-5 ↗
55. BAM: Enumeration of Escherichia coli and the Coliform Bacteria
56. Matrix-assisted laser desorption ionization time-of-flight mass spectrometry for bacterial strain characterization10.1016/j.meegid.2012.10.012 ↗
57. Antibiotic susceptibility testing by a standardized single disk method10.1093/ajcp/45.4_ts.493 ↗
58. Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement
59. Surveillance for foodborne disease outbreaks—United States, 2009–201510.15585/mmwr.ss6710a1 ↗
60. Using photocatalyst metal oxides as antimicrobial surface coatings to ensure food safety—Opportunities and challenges10.1111/1541-4337.12267 ↗
61. Augustin, J.-C., Kooh, P., Bayeux, T., Guillier, L., Meyer, T., Jourdan-Da Silva, N., Villena, I., Sanaa, M., and Cerf, O. (2020). Contribution of foods and poor food-handling practices to the burden of foodborne infectious diseases in France. Foods, 9.10.3390/foods9111644 ↗
62. Application of MALDI-TOF MS fingerprinting as a quick tool for identification and clustering of foodborne pathogens isolated from food products
63. Evaluation of rapid tests for monitoring alterations in meat quality during storage10.4315/0362-028X-40.12.843 ↗
64. Albrecht, A., Mittler, M., Hebel, M., Waldhans, C., Herbert, U., and Kreyenschmidt, J. (2021). A Multi-Model Approach to Implement a Dynamic Shelf Life Criterion in Meat Supply Chains. Foods, 10.10.3390/foods10112740 ↗
65. Residential bacteria on surfaces in the food industry and their implications for food safety and quality10.1111/1541-4337.12283 ↗
66. Farrah, S.R. (2006). Viruses in Foods, Springer.
67. Rotavirus detection in environmental water samples by tangential flow ultrafiltration and RT-nested PCR10.1007/s10661-009-0885-x ↗
68. Relationship between F-specific RNA phage genogroups, faecal pollution indicators and human adenoviruses in river water10.1016/j.watres.2008.12.011 ↗
69. De Giglio, O., Caggiano, G., Bagordo, F., Barbuti, G., Brigida, S., Lugoli, F., Grassi, T., La Rosa, G., Lucentini, L., and Uricchio, V.F. (2017). Enteric viruses and fecal bacteria indicators to assess groundwater quality and suitability for irrigation. Int. J. Environ. Res. Public Health, 14.10.3390/ijerph14060558 ↗
70. Assessment of groundwater quality in the coastal area of Sindh province, Pakistan10.1007/s10661-015-5061-x ↗
71. Jansen, W., Woudstra, S., Müller, A., Grabowski, N., Schoo, G., Gerulat, B., Klein, G., and Kehrenberg, C. (2018). The safety and quality of pork and poultry meat imports for the common European market received at border inspection post Hamburg Harbour between 2014 and 2015. PLoS ONE, 13.10.1371/journal.pone.0192550 ↗
72. Parafati, L., Palmeri, R., Trippa, D., Restuccia, C., and Fallico, B. (2019). Quality maintenance of beef burger patties by direct addiction or encapsulation of a prickly pear fruit extract. Front. Microbiol., 10.10.3389/fmicb.2019.01760 ↗
73. The microbiological condition of minced pork prepared at retail stores in Athens, Greece10.1016/j.meatsci.2012.02.036 ↗
74. The microbial quality of fast food and traditional fast food
75. Microbiological safety of street vended foods in Jigjiga City, Eastern Ethiopia10.4314/ejhs.v26i2.10 ↗
76. The contribution of fast growing, psychrotrophic microorganisms on biodiversity of refrigerated raw cow’s milk with high bacterial counts and their food spoilage potential10.1016/j.fm.2018.10.019 ↗
77. Understanding spoilage microbial community and spoilage mechanisms in foods of animal origin10.1111/1541-4337.12526 ↗
78. Microbial safety of ready-to-eat food sold by retailers in Thohoyandou, Limpopo province, South Africa10.1080/23311932.2023.2185965 ↗
79. Multidrug-resistant and clonal dispersion of enterotoxigenic Escherichia coli from ready-to-eat meat products in Duhok province, Iraq10.33899/ijvs.2022.133902.2321 ↗
80. Evaluation of antagonistic activity of an Egyptian probiotic Lactobacillus plantarum against bacteria isolated from ready-to-eat meat products10.4103/tmj.tmj_64_19 ↗
81. Contamination of ready-to-eat street food in Pakistan with Salmonella spp.: Implications for consumers and food safety10.1016/j.ijid.2021.03.062 ↗
82. Molecular characterization of antibiotic resistant Escherichia coli isolates recovered from food samples and outpatient clinics, KSA10.1016/j.sjbs.2018.01.016 ↗
83. The prevalence and antimicrobial resistance profiles of bacterial isolates from meat and meat products in Ethiopia: A systematic review and meta-analysis10.1186/s40550-019-0071-z ↗
84. Relationship between O-Serogroup and presence of pathogenic factor genes in Escherichia coli10.1111/j.1348-0421.1998.tb02360.x ↗
85. Ekici, G., and Dümen, E. (2019). The Universe of Escherichia coli, IntechOpen.
86. Comparative study of visual inspections and microbiological sampling in premises manufacturing and selling high-risk foods10.1017/S0950268800030880 ↗
87. Incidence of E. coli and Salmonellae in ready to eat fast foods10.21608/bvmj.2017.31107 ↗
88. Current pathogenic Escherichia coli foodborne outbreak cases and therapy development10.1007/s00203-017-1393-y ↗
89. Verocytotoxin-producing Escherichia coli: A veterinary view10.1111/j.1365-2672.2000.tb05330.x ↗
90. MALDI-TOF MS identification and tracking of food spoilers and food-borne pathogens10.1016/j.cofs.2016.11.004 ↗
91. MALDI-TOF MS–application in food microbiology
92. Feucherolles, M., Nennig, M., Becker, S.L., Martiny, D., Losch, S., Penny, C., Cauchie, H.-M., and Ragimbeau, C. (2022). Combination of MALDI-TOF mass spectrometry and machine learning for rapid antimicrobial resistance screening: The case of Campylobacter spp.. Front. Microbiol., 12.10.3389/fmicb.2021.804484 ↗
93. Detection of extended-spectrum-β-lactamase-producing Escherichia coli ST131 and ST405 clonal groups by matrix-assisted laser desorption ionization–time of flight mass spectrometry10.1128/JCM.03196-13 ↗
94. Ceballos-Garzón, A., Cortes, G., Morio, F., Zamora-Cruz, E.L., Linares, M.Y., Ariza, B.E., Valderrama, S.L., Garzón, J.R., Alvarez-Moreno, C.A., and Le Pape, P. (2019). Comparison between MALDI-TOF MS and MicroScan in the identification of emerging and multidrug resistant yeasts in a fourth-level hospital in Bogotá, Colombia. BMC Microbiol., 19.10.1186/s12866-019-1482-y ↗
95. Application of MALDI-TOF MS for identification of environmental bacteria: A review10.1016/j.jenvman.2021.114359 ↗
96. Review on matrix-assisted laser desorption/ionization time-of-flight mass spectrometry for the rapid screening of microbial species: A promising bioanalytical tool10.1016/j.microc.2020.105387 ↗
97. Comparison of two matrix-assisted laser desorption ionization-time of flight mass spectrometry methods with conventional phenotypic identification for routine identification of bacteria to the species level10.1128/JCM.01881-09 ↗
98. Pavlovic, M., Huber, I., Konrad, R., and Busch, U. (2013). Application of MALDI-TOF MS for the identification of food borne bacteria. Open Microbiol. J., 7.10.2174/1874285801307010135 ↗
99. Non-O157 Shiga toxin-producing Escherichia coli—A poorly appreciated enteric pathogen: Systematic review10.1016/j.ijid.2018.09.002 ↗
100. Garrine, M., Matambisso, G., Nobela, N., Vubil, D., Massora, S., Acácio, S., Nhampossa, T., Alonso, P., and Mandomando, I. (2020). Low frequency of enterohemorrhagic, enteroinvasive and diffusely adherent Escherichia coli in children under 5 years in rural Mozambique: A case-control study. BMC Infect. Dis., 20.10.1186/s12879-020-05380-1 ↗