Document Type : Original Article
Authors
1 Laboratory of Materials, Processes, Catalysis, and Environment, University Sidi Mohamed Ben Abdellah, Higher School of Technology, Post office Box 2427 Fez, Morocco
2 Higher Institute of Nursing and Health Techniques of Fez, Regional Health Directorate, El Ghassani Hospital, 30000 Fez, Morocco
Abstract
Background: Food safety is a global concern due to the rise in foodborne diseases, with contamination of food contact surfaces being a significant factor. This study aimed to assess the hygienic conditions and bacteriological contamination levels on food contact surfaces in collective catering in Central Morocco.
Methods: A cross-sectional descriptive study was conducted across six restaurants. A total of 186 swab samples were taken from 17 types of food contact surfaces, including cutting boards, serving tables, knives, sinks, plates, and other utensils. The samples were taken according to ISO 18593:2018 and analyzed using selected culture media for aerobic mesophilic bacteria (AMC), Enterobacteriaceae, Staphylococcus aureus, Enterococcus faecalis, Pseudomonas spp, as well as the presence of Salmonella spp. and Listeria monocytogenes. The surfaces were classified based on compliance with hygiene standards.
Results: Sixty-seven samples (36%) exhibited more than 2.70 log10CFU/cm², indicating non-compliance with hygiene standards. Raw meat cutting boards, sinks, and salad preparation containers were identified as the most contaminated food contact surfaces, with non-compliance rates of 83.3%, 58.3%, and 54.2%, respectively. In contrast, glasses, plates, and baking worktops were the least contaminated, with compliance rates of 77.8%, 72.8%, and 66.7%, respectively. The isolated bacteria were Coagulasenegative staphylococci (28.5%), Escherichia coli (18,8%), S. aureus (7.5%), Klebsiella pneumoniae (4.8%), Pseudomonas aeruginosa (1.6%), E. faecalis (1.6%), Proteus mirabilis (1%), and Salmonella spp. (0.5%). No Listeria spp. contamination was detected. The mean levels of aerobic mesophilic bacteria, S. aureus, and Enterobacteriaceae ranged from 1.59 log10CFU/ cm² to 3.93 log10CFU/cm², 0 log10CFU/cm² to 1.49 log10CFU/cm², and between 1.55 and 4.34 log10CFU/cm², respectively.
Conclusion: This initial assessment of collective restaurants in Fez provides baseline data on environmentally hazardous microbes and will help food safety managers better implement effective control measures top revent contamination and safeguard public health.
Highlights
Rachid Amaiach (Google Scholar)
Keywords
- Amaiach R, El Ouali Lalami A, Fadil M, Bouslamti R, Lairini S. Food safety knowledge, attitudes, and practices among food handlers in collective catering in central Morocco. Heliyon. 2024; 10(23):e40739. doi: 10.1016/j.heliyon.2024.e40739. PUBMED PMID: 39687091. PUBMED CENTRAL PMCID: PMC11648122.
- Cissé G. Food-borne and water-borne diseases under climate change in low- and middle-income countries: Further efforts needed for reducing environmental health exposure risks. Acta Tropica. 2019; 194:181–188. doi: 10.1016/j.actatropica.2019.03.012. PUBMED PMID: 30946811. PUBMED CENTRAL PMCID: PMC7172250.
- Amaiach R, Lairini S, Fadil M, Benboubker M, Bouslamti R, El Amrani S, et al. Microbiological Profile and Hygienic Quality of Foodstuffs Marketed in Collective Catering in Central Morocco. Castillo A, editor. International Journal of Food Science. 2023; 2023:1–13. doi: 10.1155/2023/2820506.PUBMED PMID: 37122386. PUBMED CENTRAL PMCID: PMC10139816.
- Naska A, Katsoulis M, Orfanos P, Lachat C, Gedrich K, Rodrigues SSP, et al. Eating out is different from eating at home among individuals who occasionally eat out. A cross-sectional study among middle-aged adults from eleven European countries. Br J Nutr. 2015; 113(12):1951–64. doi: 10.1017/S0007114515000963. PUBMED PMID: 25907775.
- Tenna A, Amare K, Tekola H, Kidan YW, Melese D, Medhin G. Assessment of the Microbial Quality of Food Contact Surfaces (Utensils) of Hotels and Restaurants in Addis Ababa. Research Square. 2023. doi: 10.21203/rs.3.rs-2596388/v1.
- Angulo FJ, Jones TF, Angulo FJ. Eating in Restaurants: A Risk Factor for Foodborne Disease? Clinical Infectious Diseases. 2006; 43(10):1324–8. doi: 10.1086/508540. PUBMED PMID: 17051501.
- Wu Y, Wen J, Ma Y, Ma X, Chen Y. Epidemiology of foodborne disease outbreaks caused by Vibrio parahaemolyticus, China, 2003–2008. Food Control. 2014; 46:197–202. doi: 10.1016/j.foodcont.2014.05.023.
- Pichler J, Ziegler J, Aldrian U, Allerberger F. Evaluating levels of knowledge on food safety among food handlers from restaurants and various catering businesses in Vienna, Austria 2011/2012. Food Control. 2014 Jan 1;35(1):33–40. doi: 10.1016/j.foodcont.2013.06.034.
- Marriott NG, Schilling MW, Gravani RB. Food Contamination Sources. In: Principles of Food Sanitation. Springer International Publishing; 2018. p. 83–91. (Food Science Text Series). doi: 1007/978-3-319-67166-6.
- Baghapour MA, Mazloomi SM, Azizi K. Microbiological Quality of Food Contact Surfaces in A Hospital Kitchen in Shiraz, Iran, 2014. J Health Sci Surveillance Sys. 2015; 3(4):128-132.
- Losito P, Visciano P, Genualdo M, Satalino R, Migailo M, Ostuni A, et al. Evaluation of hygienic conditions of food contact surfaces in retail outlets: Six years of monitoring. LWT. 2017; 77:67–71. doi: 10.1016/j.lwt.2016.11.029.
- Saad M, See TP, Abdullah MFF, Nor NMd. Use of Rapid Microbial Kits for Regular Monitoring of Food-contact Surfaces towards Hygiene Practices. Procedia - Social and Behavioral Sciences. 2013; 105:273–83. doi: 10.1016/j.sbspro.2013.11.029.
- Simões M, Simões LC, Vieira MJ. A review of current and emergent biofilm control strategies. LWT - Food Science and Technology. 2010; 43(4):573–83. doi: 10.1016/j.lwt.2009.12.008.
- Lahou E, Jacxsens L, Daelman J, Landeghem FV, Uyttendaele M. Microbiological Performance of a Food Safety Management System in a Food Service Operation. Journal of Food Protection. 2012; 75(4):706–16. doi: 10.4315/0362-028X.JFP-11-260. PUBMED PMID: 22488059.
- Mohammed Rufai S, Wartu JR. Food contact surface contaminants: A review. FJS. 2024; 7(6):140–8. doi: 10.33003/fjs-2023-0706-2179.
- Gounadaki AS, Skandamis PN, Drosinos EH, Nychas GJE. Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. Food Microbiology. 2008; 25(2):313–23. doi: 10.1016/j.fm.2007.10.001. PUBMED PMID: 18206774.
- Carrasco E, Morales-Rueda A, García-Gimeno RM. Cross-contamination and recontamination by Salmonella in foods: A review. Food Research International. 2012; 45(2):545–56. doi: 10.1016/j.foodres.2011.11.004.
- Allam H, Al-Batanony M, Seif A, Awad E. Hand Contamination among Food Handlers. BMRJ. 2016; 13(5):1–8. doi: 10.9734/BMRJ/2016/24845.
- Popovic M, Baltic M, Gusman V, Andjelkovic R, Velicki R, Bjelanovic J, et al. Hygiene status of food contact surfaces in public school canteens in the city of Novi Sad, Serbia. VSP. 2022;79(9):883–9. doi: 10.2298/VSP200521050P.
- Sagoo SK, Little CL, Mitchell RT. Microbiological Quality of Open Ready-to-Eat Salad Vegetables: Effectiveness of Food Hygiene Training of Management. Journal of Food Protection. 2003; 66(9):1581–6. doi: 10.4315/0362-028X-66.9.1581. PUBMED PMID: 14503709.
- Da Vitória AG, De Souza Couto Oliveira J, De Faria CP, De São José JFB. Good practices and microbiological quality of food contact surfaces in public school kitchens. Journal of Food Safety. 2018; 38(5):e12486. doi: 10.1111/jfs.12486.
- Bukhari M, M. Banasser T, El-Bali M, A. Bulkhi R, A. Qamash R, Trenganno A, et al. Assessment of microbiological quality of food preparation process in some restaurants of Makkah city. Saudi Journal of Biological Sciences. 2021; 28(10):5993–7. doi: 10.1016/j.sjbs.2021.06.050. PUBMED PMID: 34588916. PUBMED CENTRAL PMCID: PMC8459123.
- Douini I, Squalli W, Mansouri I, Mounir M, Benka EM, Dakki M, et al. Diversity and Abundance of Breeding Birds, Habitat, and Nesting Substrate Selection in Urban Areas: A Relevant Case from the Southern Slope of the Mediterranean. Pellegrino I, editor. International Journal of Zoology. 2023; 2023:1–10. doi: 10.1155/2023/8554860.
- International Electrotechnical Commission. Iso 18593-2018. Microbiology of the Food Chain - Horizontal Methods for Surface Sampling. International Organization for Standardization, Geneva. [Internet]. Scribd. 2018 [cited 2024]. Available from: https://www.scribd.com/document/627672730/ISO-18593-2018.
- International Electrotechnical Commission. ISO/IEC 17025:2005(en), General requirements for the competence of testing and calibration laboratories [Internet]. 2005 [cited 2022]. Available from: https://www.iso.org/obp/ui/#iso:std:iso-iec:17025:ed-2:v1:en.
- Ospina JT, Fuentes Vanegas MA, Montoya DC, Pérez SR, Zuleta MMD. Food safety: Cleanliness and disinfection of food contact surfaces in gastronomy laboratories at a university in Colombia. Braz J Food Technol. 2024; 27:e2023124. doi: 10.1590/1981-6723.12423.
- Touimi GB, Bennani L, Berrada S, Benboubker M, Bennani B. Evaluation of hygienic conditions of food contact surfaces in a hospital kitchen in Morocco. Iran J Microbiol. 2019; 11(6):527-534. PUBMED PMID: 32148685. PUBMED CENTRAL PMCID: PMC7048956.
- Petruzzelli A, Osimani A, Tavoletti S, Clementi F, Vetrano V, Di Lullo S, et al. Microbiological quality assessment of meals and work surfaces in a school-deferred catering system. International Journal of Hospitality Management. 2018; 68:105–14. doi: 10.1016/j.ijhm.2017.10.003.
- Lani MN, Azmi MFM, Ibrahim R, Hassan Z. Microbiological Quality of Food Contact Surfaces At Selected Food Premises of Malaysian Heritage Food (‘Satar’) in Terengganu, Malaysia. IJES. 2014; 3(9):66–70.
- Wiatrowski M, Rosiak E, Czarniecka-Skubina E. Surface Hygiene Evaluation Method in Food Trucks as an Important Factor in the Assessment of Microbiological Risks in Mobile Gastronomy. Foods. 2023; 12(4):772. doi: 10.3390/foods12040772. PUBMED PMID: 36832855. PUBMED CENTRAL PMCID: PMC9955632.
- Rodríguez M, Valero A, Posada-Izquierdo GD, Carrasco E, Zurera G. Evaluation of Food Handler Practices and Microbiological Status of Ready-to-Eat Foods in Long-Term Care Facilities in the Andalusia Region of Spain. Journal of Food Protection. 2011; 74(9):1504–12. doi: 10.4315/0362-028X.JFP-10-468. PUBMED PMID: 21902920.
- Jovanovic J, Nikolic A, Brankovic Lazic I, Mrdovic B, Raseta M, Lilic S, et al. Food contact surfaces and food handler’s hygiene in one Serbian retail chain–estimation and trend. IOP Conf Ser: Earth Environ Sci. 2021; 854(1):012041. doi: 10.1088/1755-1315/854/1/012041.
- Vesković Moračanin S, Baltić T, Milojević L. Monitoring process hygiene in Serbian retail establishments. IOP Conf Ser: Earth Environ Sci. 2017; 85:012057. doi: 10.1088/1755-1315/85/1/012057.
- Zulfakar SS, Abd. Hamid NH, Sahani M. Microbiological Assessment of Food Contact Surfaces in Residential College Cafeterias at a Local University in Malaysia. JSKM. 2018; 16(02):33–8. doi: 10.17576/jskm-2018-1602-05.
- Tomasevic I, Kovačević DB, Jambrak AR, Szendrő K, Dalle Zotte A, Prodanov M, et al. Validation of novel food safety climate components and assessment of their indicators in Central and Eastern European food industry. Food Control. 2020; 117:107357. doi: 10.1016/j.foodcont.2020.107357.
- Paczosa MK, Mecsas J. Klebsiella pneumoniae: Going on the Offense with a Strong Defense. Microbiol Mol Biol Rev. 2016; 80(3):629–61. doi: 10.1128/MMBR.00078-15. PUBMED CENTRAL PMCID: PMC4981674. PUBMED PMID: 27307579.
- Meliani A, Bensoltane A. Review of Pseudomonas Attachment and Biofilm Formation in Food Industry. Poult Fish Wildl Sci. 2015; 03(01). doi: 10.4172/2375-446X.1000126.
- Haleem AM, Ali Hassan D, Al-Hiyali Comparative Assessment of Microbial Contamination from Swabs Collected within University Facilities. Journal of Health Science. 2013;3(2):25–8. doi: 10.5923/j.health.20130302.04.
- Fahim KM, Ahmed LI and Abdel-Salam AB. Influence of The Hygienic Status of Food Contact Surfaces and Handler’s Hands on The Microbial Safety of Ready to Eat Foods. Int J Vet Sci. 2022; 11(2):249–56. doi: 10.47278/journal.ijvs/2021.102.
- Amaiach R, Lairini S, Fadil M, Bouslamti R, El Akhal F, El Ouali Lalami A. Correlation between Major Bioactive Compounds in Essential Oils from Wild and Cultivated Moroccan Plants and their Antibacterial Efficacy against Foodborne Pathogens.Trop J Nat Prod Res. 2024; 8(10):8850 – 8866. doi: 10.26538/tjnpr/v8i10.30.