Occurrence of Virulent and Antibiotic Resistant Staphylococcus aureus in Selected Ready-To-Eat Foods in Obio/Akpor, Rivers State, Nigeria
Issue: 2023 - Volume 15 [Issue 11]
Emmanuel Chukwuemeka Okoye
Department of Microbiology, Faculty of Science, University of Port Harcourt, East-West Road, P.M.B 5323, Rivers State, Nigeria.
Onoriode Christian Eruteya *
Department of Microbiology, Faculty of Science, University of Port Harcourt, East-West Road, P.M.B 5323, Rivers State, Nigeria.
*Author to whom correspondence should be addressed.
Aims: Ready-to-eat (RTE) foods contaminated with Staphylococcus aureus or its heat-stable toxins have been implicated in food-borne illnesses lately and are now a public health concern. This study is aimed at determining the microbial safety of RTE snacks (meat-pie, Egg-roll, Doughnut, Burns and Puff-puff) sold in Obio/Akpor LGA, Rivers State.
Study Design: This work is based on a completely randomized design with two replications and the average values calculated for the mean comparison.
Place and Duration of Study: Imadavistic Laboratory, Osaks House, East-West Road Port Harcourt, Nigeria, between December 2021 and November, 2022.
Methodology: A total of 100 samples of RTE food Snacks were randomly purchased and examined for proximate composition, microbial quality, and occurrence of antibiotic-resistant and virulent genes using standard conventional and molecular methods.
Results: Puff-puff had the highest moisture, fiber and ash content while egg-roll had the highest crude fat, also meat-pie had the highest carbohydrate and protein content. Microbial counts ranged from 3.5×103 to 1.5×106cfu/g with 44 samples unsatisfactory and 39 at borderline by food regulatory standard. Presumptive S. aureus count ranged from 1.4×103 to 4.6×106 cfu/g, with 5 classified as potentially hazardous, 14 as unsatisfactory and 49 as borderline, 16 as satisfactory, and 16 with no detection. The 34 confirmed S. aureus showed varying resistance to cloxacillin 31(91.18%), cefuroxime 28 (82.35%), ceftazidime and erythromycin 25 (73.53%), gentamicin 18 (52.94%) and augmentin 13 (38.24%). Multi-drug resistance ranged from 3 to 5 antibiotic classes. Nine isolates produced the expected band of 250bp with SEA while 3 produced the band of 400bp with SEB.
Conclusion: There is a correlation of statistically significant difference (p<0.5) between the four types of RTE food and enterotoxin A, therefore confirming that RTE foods serve as a reservoir of antibiotic resistant and virulence gene bearing S. aureus.
Keywords: Snacks, Staphylococcus aureus, virulence genes
How to Cite
Tsang D. Microbiological guidelines for ready-to-eat food. Road and Environmental Hygiene Department, Hongkong. 2002;115-116.
Puah SM, Chua K, Tan JA. Virulence factors and antibiotic susceptibility of Staphylococcus aureus isolates in ready-to-eat foods: Detection of S. aureus contamination and a high prevalence of virulence genes. Int J Environ Res Public Health. 2016;13(199):1-9.
Oje OJ, Ajibade VA, Fajilade OT, Ajenifuja OA. Microbiological analysis of ready-to-eat (TRE) foods vended in mobile outlet catering units from Nigeria. J. Adv. Food Sci. Technol. 2018;5:15-19.
Chajęcka-Wierzchowska W, Zadernowska A, Łaniewska-Trokenheim Ł. Diversity of antibiotic resistance genes in Enterococcus strains isolated from ready-to-eat meat products. J Food Sci. 2016; 81(11):2799-2807.
Giwa AS, Memon AG, Shaikh AA, Korai R, Maitlo GUG, Maitlo I, Ali S. Ahmed J. Microbiological survey of ready-to-eat foods and associated preparation surfaces in cafeterias of public sector universities. Environmental Pollutants and Bioavailability. 2021;33(1):11-18.
Makinde O, Ayeni I, Sulyok M, Krska R, Adeleke RA, Ezekiel CN. Microbiological safety of ready-to-eat foods in low- and middle-income countries: a comprehensive 10-year (2009 to 2018) review. Comp. Rev. Food Sci. Food Safety. 2020;19:703-732.
Ulusoy BH, Sancar BC, Ozturk M. Prevalence of staphylococcal enterotoxins in ready-to-eat foods sold in Istanbul. J. Food Prot. 2017;80(10):1734-1736.
WHO. Food Safety: What you should know. SEARO Library, World Health Organization, Regional Office for South-East Asia, Indraprastha Estate, Mahatma Gandhi Marg, New Delhi 110002, India; 2015.
CSPI. Antibiotic resistance in foodborne outbreaks, Washington DC. Available:https://cspi;net.org/resource/antibiotic- resistance. (Accessed on 15th March, 2022). 2013.
Economou V, Gousia P, Kansouzidou A, Sakkas H, Karanis P, Papadopoulou C. Prevalence, antimicrobial resistance and relation to indicator and pathogenic microorganisms of Salmonella enterica isolated from surface waters within an agricultural landscape. Int. J. Hyg. Environ. Health. 2013;216:435– 444.
Adams MR, Moss MO. Food Microbiology. 4th Edition. New Age International, New Delhi. 2009; 205- 207.
Ogidi OC, Oyetayo VO, Akinyele BJ. Microbial quality and antibiotic sensitivity pattern of isolated microorganisms from street foods sold in Akure Metropolis, Nigeria. Jordan J. Biol. Sci. 2016;9(4):227-234.
Hennekinne JA, Brun V, De Buyser ML, Dupuis A, Ostyn A, Dragacci S. Innovative application of mass spectrometry for the characterization of staphylococcal enterotoxins involved in food poisoning outbreaks. Appl. Environ. Microbiol. 2009; 75(3): 882-884.
Balaban N, Rasooly A. Staphylococcal enterotoxins. Int. J. Food Microbiol. 2000; 61(1):1-10.
Pinchuk IV, Beswick EJ, Reyes VE. Staphylococcal enterotoxins. Toxins. 2010; 2(8): 2177-2197.
Fisher EL, Otto M, Cheung GY. Basis of virulence in enterotoxin-mediated staphylococcal food poisoning. Front. Microbiol. 2018;9(436):1-18.
Coates T, Bax R, Coates A. Nasal decolonization of Staphylococcus aureus with mupirocin: strengths, weaknesses and future prospects. J. Antimicrob. Chemoth. 2009;64(1):9-15.
Obio/Akpor Embassy. Brief History of Obio/Akpor Local Government Area Available:http://obioakporembassy.com/index.php (Accessed on 10th December, 2021). 2012.
AOAC Official Methods of Analysis ―Association of Official Analytical Chemist. 18th edition. Washington, DC; Section 12.1.7; 968.08. 2005;4.1.28.
Odu NN, Assor P. Microbiological analysis of ready to eat food (cooked rice and beans) sold among different restaurant in University of Port Harcourt, Port Harcourt, Nigeria. Acad. Arena. 2013; 5(1): 62-66.
21. Todar K. Staphylococcus aureus and Staphylococcal disease. Todar’s online textbook of bacteriology. [Internet]. Available:http://www.textbookofbacteriology.net/staph.html. (Accessed on March 15th, 2022). 2008.
Ghaderpour A, MohdNasori KN, Chew LL, Chong VC, Thong KL, Chaj LC. Detection of multiple potentially pathogenic bacteria in Matang mangrove estuaries, Malaysia. Marine Poll. Bull. 2014;83:324-330.
Cheeshrough M. Microbial test in: District Laboratory Practice in Tropical Countries Part 2. Cambridge University press U.K. 2002; 123-140.
Shah M. Molecular pathogenesis of S. aureus and other staphylococci. J. Appl. Bacteriol. 2003;59:207-221.
Sandel MK, McKillip JL. Virulence and recovery of Staphylococcus aureus relevant to the food industry using improvements on traditional approaches. Food Contr. 2004;15(1):5-10.
Oliveira CFD, Paim TGDS, Reiter KC, Rieger A, D'azevedo PA. Evaluation of four different DNA extraction methods in coagulase-negative staphylococci clinical isolates. Revista do Instituto de Medicina Tropical de São Paulo. 2014;56:29-33.
Sharma NK, Rees CE, Dodd CE. Development of a single-reaction multiplex PCR toxin typing assay for Staphylococcus aureus strains. Appl. Environ. Microbiol. 2000; 66(4): 1347-1353.
Jerraud S, Mougel C, Thioulouse J, Lina G, Maugenier H, Forey F, Nesme X, Etienn J, Vandenesch F. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (Alleles), and human disease. Infect. Immu. 2002;70(2):631–641.
Adame-Gómez R, Castro-Alarcón N, Vences-Velázquez A, Toribio-Jiménez J, Pérez-Valdespino A, Leyva-Vázquez MA, Ramírez-Peralta A. Genetic diversity and virulence factors of S. aureus isolated from food, humans, and animals. Int. J. Microbiol. 2020;5:1-10.
CLSI, C. Performance standards for antimicrobial disk susceptibility tests; approved standard. CLSI document M02-A11, 2012;950.
Israel OG, Samuel BC. Nutrient composition and microbiological evaluation of vended street foods in parts of Lagos State, Nigeria. Asian Food Sci. J. 2020; 17(1):1-14.
Pikuda OO, Ilelaboye NOA. Proximate composition of street snacks purchased from selected motor parks in Lagos. Pak. J. Nutr. 2009;8(10):1657-1660.
Adeyeye A, Ayoola PB. The nutritional composition of some street snacks in Nigeria. Adv. Food Energy Security. 2013;1-4.
Ajatta MA, Akinola SA, Osundahunsi OF. Proximate, functional and pasting properties of composite flours made from wheat, breadfruit and cassava starch. Appl. Trop. Agric. 2016;21(3):158-165.
35. Hossain S, Shishir MRI, Saifullah M, Kayshar MS, Tonmoy SW, Rahman A, Shams-Ud-Din M. Incorporation of coconut flour in plain cake and investigation of the effect of sugar and baking powder on its baking quality. Int. J. Food Nutr. 2016;5(1):31-38.
36. Udezo PC, Onigbinde AO, Adaramola FB, Aleshinloye AO, Jegede DO, Ogunnowo AA, Shokunbi OS and Adewumi AG. Nutritional investigation of three commonly consumed fast foods in two major fast-food restaurants in Lagos State, Nigeria. Chem. Int. 2019;5(1):81-86.
Olusanya JO. The nutrient composition of all vegetable-based snacks. Nig. J. Nutr. Sci. 1991;12(1):18–19.
Bello MO, Falade OS, Adewusi SRA, Olawore NO. Studies of some lesser-known Nigerian fruits. Afr. J. Biotechnol. 2008; 7(1): 3972−3979.
Afolabi WAO, Oyawoye OO, Sanni SA, Onabanjo OO. Proximate and cholesterol composition of selected fast foods sold in Nigeria. Nig. Food J. 2013;31(1):70–76.
Eke MO, Elechi JO. Food safety and quality evaluation of street vended meat pies sold in Lafia Metropolis, Nasarawa state, Nigeria. Int. J. Sci. Res. Biol Sci. 2021; 8(1): 88-98.
AOAC. Official Methods of Analysis. 15th Edition, Association of Official Analytical Chemist, Washington DC; 1990
42. Kiin-Kabari DB, Eke-Ejiofor J, Giami SY. Functional and pasting properties of wheat/plantain flours enriched with bambara groundnut protein concentrate. Int. J. Food Sci. Nutr. Eng. 2015;5(2):75-81.
Paul AA, Southgate DAT. McCance and Widdowson: The composition of foods 5th Edition. HMSO, London. 1985.
Centre for Food Safety. Food and Environmental Hygiene Department. Hong Kong.
Available:https://www.cfs.gov.hk/english/food_leg/files/food_leg_Microbiological_Guidelines_forFood_e.pdf. (Accessed on March 15th, 2022). 2014.
Awanye AM, Uwah EU. Prevalence and antibiotic resistance profile of food-borne pathogens obtained from street-vended food sold within a university campus in Southern Nigeria. World J. Pharm. Res. 2020;9(4):133- 144.
Obande GA, Umeh EU, Azua ET, Chuku A, Adikwu P. Incidence and antibiotic susceptibility pattern of Escherichia coli and Staphylococcus aureus isolated from meat pie sold in a Nigerian North Central town. Janaki Med. College J. Med. Sci. 2018; 6(1): 21-28.
Okeke OP, Yusuf KO, Ononye BU, Udeh NP, Ndudim GC. Evaluation of the microbial contamination of some snacks: A case study of Lagos Mainland, Lagos State, Nigeria. Evaluation. 2021;4(2):37-45.
Adolf JNP, Azis BS. Microbiological status of various foods served in elementary school based on social economic status differences in Karawaci Region, Tangerang District – Indonesia. Int. Food Res. J. 2012;19(1):65-70.
Phillips M. Analysis of microbial hazards related to time/temperature control of foods for safety. Com. Rev. Food Sci. Food Safety.2003; 2: 33-35.
Bryan FL, Tuefel P, Rooh S, Qadar F, Riaz S, Malik Z. Hazards and critical control points of food preparation and storage in homes in a village and a town in Pakistan. J. Food Prot. 2002;3:301-333.
Khali LGB, Mazhar KB. Flies and water as reservoirs for bacterial pathogens in urban and rural areas in and around Lahore, Pakistan. Epidemiol. Infect. 2005;113: 435-444.
Oranusi S, Omagbemi F, Eni AO. Microbiological safety evaluation of snacks sold in fast food shops in Ota, Ogun State, Nigeria. Res. J. Biol. Sci. 2011;6(7):309-313.
Aycicek H, Aksoy A, Saygi S. Determination of aflatoxin levels in some dairy and food products which consumed in Ankara, Turkey. Food Contr. 2005; 16(3):263-266.
Esemu SN, Njoh ST, Ndip LM, Keneh NK, Kfusi JA, Njukeng AP. Ready-to-eat foods: A potential vehicle for spread of coagulase-positive staphylococci and antibiotic-resistant Staphylococcus aureus in Buea municipality, South West Cameroon. BioRxiv.2021;8(1):88-98.
Nwachukwu E, Nwaigwe UV. Occurrence of Staphylococcus aureus in meat pie and eggroll sold in Umuahia Metropolis, Nigeria. Int J. Microbiol. Immunol. Res. 2013;1(4): 052-055.
Xing X, Li G, Zhang W, Wang X, Xia X, Yang B, Meng J. Prevalence, antimicrobial susceptibility, and enterotoxin gene detection of Staphylococcus aureus isolates in ready-to-eat foods in Shaanxi, People's Republic of China. J. Food Prot. 2014;77(2):331-334.
Temesgen E, Haimanot T, Derese D, Gebre K. Bacteriological quality of street foods and antimicrobial resistance of isolates in Hawassa, Ethiopia. Ethiop J Health Sci. 2016;26(6): 533-542.
Pantosti A, Sanchini A, Monaco M. Mechanisms of antibiotic resistance in Staphylococcus aureus. Future Microbiol. 2007;2(3):323–334.
Jassim SA, Kandala, NJ. Molecular detection of enterotoxin genes of multi-resistant Staphylococcus aureus isolates from different sources of food. Iraqi J. Sci. 2021;62(1):61-67.
Prescott M, Harley P, Kian D. Microbilogy,6th edition McGraw hill New York publishers USA. 2005;910.