ORIGINAL RESEARCH ARTICLE: Detection of Methicillin-Resistant Staphylococcus Aureus and Extended-Spectrum Beta-Lactamase Producers from Ready-to-Eat Roasted Beef in Ibadan North, Nigeria

Olumuyiwa S. Alabi, Abiola O. Obisesan, Bamidele T. Odumosu


Ready-to-eat roasted beef popularly called ‘Suya’ in Nigeria is a highly nutritive food and hence, prone to microbial contamination when handled in an unhygienic manner by the vendors. Extended-spectrum beta-lactamase (ESBL) producers and methicillin-resistant Staphylococcus aureus have been reported in both community and hospital settings in Nigeria. This study investigated their occurrence as microbial contaminants in ready-to-eat roasted beef in Ibadan North local government area (LGA) of Oyo state, Nigeria. Fifty (50) samples were purposively collected randomly in four different locations in Ibadan North LGA from 1st to 31st of November, 2019. Aerobic and coliform bacterial counts, isolation, identification and antibiotic susceptibility testing were done using standard microbiological techniques. Phenotypically, methicillin resistant Staphylococcus aureus was detected by cefoxitin-disc-diffusion and ESBL-producers by double-disc synergy. MecA/C and selected ESBL (TEM, SHV and CTX-M) genes were detected by PCR technique. The mean total aerobic and coliform bacterial counts ranged from 1.5 × 106 to 7.8 × 106 cfu/g and 0.8 × 102 to 1.3 × 103 cfu/g respectively. Thirty-eight (38) bacteria were isolated: Staphylococcus aureus (15.8%), Pseudomonas spp. (42.1%), Klebsiella spp. (36.8%) and Bacillus spp. (5.3%). Four (66.7%) of the Staphylococcus aureus were MecA mediated methicillin-resistant strains and 20 (66.7%) of the Gram-negatives were ESBL-producers with 9 (30%) harbouring TEM and SHV and 15 (50%) CTX-M genes. Occurrence of MRSA and ESBL-producers in ready-to-eat roasted beef in Ibadan north is of serious public health concern.


Ready-to-eat beef, bacteriological examination, ESBL, MRSA, MDR

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Adenaike O, Olonitola OS, Ameh JB, & Whong CMZ (2013). Incidence of Extended Spectrum β-lactamase Producing Bacteria and Multidrug Resistance Strains from Processed Meat ‘Suya’ Sold in a University Community. The International Journal of Engineering and Science. 2(12): 1-6.

Adesoji AT, Ogunjobi AA, & Olatoye IO (2015). Molecular characterization of selected multidrug resistant Pseudomonas from water distribution systems in southwestern Nigeria. Annals of Clinical Microbiology and Antimicrobials. 14(39): 1 - 11. DOI 10.1186/s12941-015-0102-4

Adewumi GA, Quadri RA, & Oguntoyinbo FA (2009). Antibiotic sensitivity pattern of Bacillus species isolated from solid substrate fermentation of cassava for gari production. African Journal of Microbiology Research. 3(11): 840-843.

Amadi LO, Singabele FO, Elechi R, & Ngerebara NN (2016). Bacterial status and antibacterial susceptibility profiles of selected pathogens associated with suya meat samples purchased in Bori metropolis, Rivers State, Nigeria. International Research Journal of Public and Environmental Health. 3(2): 14-19.

Clinical Laboratory Standard Institute - CLSI (2017). Performance Standards for Antimicrobial Susceptibility Testing: Twenty-Seventh edition. CLSI Supplement M100. Wayne, Pennsylvania, USA: Clinical and Laboratory Standards Institute, 2017.

Cuny C, Layer F, Strommenger B, & Witte W. (2011). Rare occurrence of methicillin-resistant Staphylococcus aureus CC130 with a novel mec A homologue in humans in Germany. PloS ONE, 6(9): e24360. doi:10.1371/journal.pone.0024360

D’Andrea MM, Literacka E, Zioga A, Giani T, Baraniak A, Fiett J, Sadowy E, Tassios PT, Rossolini GM, Gniadkowski M, & Miriagou V (2011).

Evolution and spread of a multidrug-resistant Proteus mirabilis clone with chromosomal AmpC-type cephalosporinases in Europe. Antimicrobial Agents and Chemotherapy. 55: 2735–2742.

Davis SL, Perri MB, Donabedian SM, Manierski C, Singh A, Vager D, Haque NZ, Speirs K, Muder RR, Robison-Dunn B, Hayden MK, & Zervos MJ (2007). Epidemiology and outcomes of community-associated methicillin-resistant Staphylococcus aureus infection. Journal of Clinical Microbiology. 45: 1705–1711.

Edema MA, Osho AT, & Dialo CI (2008). Evaluation of microbial hazards associated with the processing of suya (a grilled meat product). Scientific Res and Essays. 3(12): 621 – 626.

Egbebi AO & Seidu KT (2011). Microbiological evaluation of Suya (dried smoked meat) sold in Ado and Akure South West Nigeria. European J. Exp. Biol. 1(4): 1-5.

Eke SO, Irabor JI, Okoye M, Aitufe OF, & Ekoh SN (2013). The microbial status of commercial ‘Suya’ meat products in Ekpoma, Edo, Nigeria. Int. J. Community Res. 2(1): 18-21.

Eromo T, Tassew H, Daka D, & Kibru G, (2016). Bacteriological quality of street foods and antimicrobial resistance of isolates in Hawassa, Ethiopia. Ethiopian journal of health sciences, 26(6): 533-542.

Igbinosa EO, Beshiru A, Akporehe LU, Oviasogie FE, & Igbinosa OO (2016). Prevalence of methicillin-resistant Staphylococcus aureus and other Staphylococcus species in raw meat samples intended for human consumption in Benin City, Nigeria: implications for public health. International Journal of Environmental Research and Public Health, 13(10): 949.

Inyang CU, Igyor MA, & Uma EN (2005). Bacterial Quality of a Smoked Meat product (‘Suya’). Nig. Food J. 23: 239-242.

Kock R, Harlizius J, Bressan N, Laerberg R, Wieler LH, Witte W, Deurenberg RH, Voss A, Becker K, & Friedrich AW (2009). Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Europian Journal of Clinical Microbiology and Infectious Disease. 28: 1375–1382.

Kolawole DO, Adeyanju A, Schaumburg F, Akinyoola AL, Lawal OO, Amusa YB, Koch R, & Becker K (2013). Characterization of Colonizing Staphylococcus aureus Isolated from Surgical Wards’ Patients in a Nigerian University Hospital. PLoS ONE. 8(7): e68721. doi:10.1371/journal.pone.0068721.

Lambrechts AA, Human IS, Doughari JH, & Lues JFR (2014). Bacterial contamination of the hands of food handlers as indicator of hand washing efficacy in some convenient food industries. Pakistan Journal of Medical Sciences. 30(4): 755-758. doi: http://dx.doi.org/10.12669/pjms.304.4400

Machado E, Coque TM, Canton R, Sousa JC, & Peixe L (2004). Emergence of CTX-M Beta-lactamase-producing Enterobacteriaceae in Portugal: report of an Escherichia coli isolates harbouring blaCTX-M-14. Clinical Microbiology and Infection. 10: 755–757.

Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, & Monnet DL (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection. 18: 268–281.

Marshall BM, Ochieng DJ, & Levy SB (2009). Commensals: Underappreciated Reservoir of Antibiotic Resistance. Microbe. 4(5): 231-238. Available at: http://www.bioquest.org/summer2010/wp-content/blogs.dir/files/2010/02/Commensals.pdf.

Maynard C, Fairbrother JM, Bekal S, Sanschagrin F, Levesque RC, Brousseau R, Masson L, Lariviere S, & Harel J (2003). Antimicrobial Resistance Genes in Enterotoxigenic Escherichia coli O149:K91 Isolates Obtained over a 23-Year Period from Pigs. Antimicrobial Agents and Chemotherapy. 47(10): 3214–3221. DOI: 10.1128/AAC.47.10.3214–3221.2003.

Mayr D, Margesin R, Klingsbichel E, Hartungen E, Jenewein D, Schinner F, & Mark TD (2003). Rapid detection of meat spoilage by measuring volatile organic compounds by using proton transfer reaction mass spectrometery. Applied and Environmental Microbiology. 69(8): 4697–4705. doi: 10.1128/AEM.69.8.4697-4705.2003

Mendonca N, Joana L, Vera M, & Eugenia F (2007). The Antimicrobial Resistance Surveillance Program in Portugal, Manuela C. Spread of extended-spectrum beta-lactamase CTX-M-producing Escherichia coli clinical isolates in community and nosocomial environments in Portugal. Antimicrobial Agents and Chemotherapy. 51: 1946-1955.

Mensah P, Mwamakamba L, Mohamed C, & Nsue-Milang D (2012). Public health and food safety in the WHO African region. African Journal of Food, Agriculture, Nutrition and Development. 12(4): 6317-6335.

Moshood AY, Tengku H, & Ibrahim H (2012). Isolation and Identification of Bacteria Associated with Balangu (Roasted meat Product) sold in Bauch, Nigeria. J. Pharm. 2(6): 38-48.

Population and Housing Census (2006). Population and Housing Census, Priority Table Volume III, Population Distribution by Sex, State, Local Government, and Senatorial District, National Population Commission (NPC) Abuja, Nigeria. Available:http://www.population.gov.ng/images/Vol%2003%20Table%20DSx%20LGAPop%20by%20SDistrict-PDF.pdf

Obayelu AE, Okoruwa VO, & Oni OA (2009). Analysis of rural and urban households’ food consumption differential in the North-Central, Nigeria. Journal of Development and Agricultural Economics. 1(2): 18-26.

Ogbolu DO, Daini OA, Ogunledun A, Alli AO, & Webber MA (2011). High levels of multidrug resistance in clinical isolates of Gram-negative pathogens from Nigeria. International Journal of Antimicrobial Agents. 37: 62-66.

Okesola AO & Makanjuola O (2009). Resistance to third-generation cephalosporins and other antibiotics by Enterobacteriaceae in Western Nigeria. American Journal of Infectious Diseases. 5: 17-20.

Okwori AEJ, Akele RY, Junaid SA, Agada GOD, Chollom SC, Etukudoh ES, Anejo-Okopi JA, & Adikwu TI (2014). Bacterial Aetiological Agents of Vended Foods in Vom, Plateau State, Nigeria. Journal of Dental and Medical Sciences. 13(11): 30-34.

Orogu JO & Oshilim AO (2017). Comparative study of bacteriological analysis in hawked suya meat and suya meat on a Barbeque stand. E3 Journal of Microbiology Research. 3(1): 5-8.

Penders J, Stobberingh EE, Savelkoul PHM, & Wolffs PFG (2013). The human microbiome as a reservoir of antimicrobial resistance. Frontiers in Microbiology. 4(87): 1-7. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3627978/pdf/fmicb-04-00087.pdf

Public Health Laboratory Service - PHLS (2000). Public Health Laboratory Service. Guidelines for the bacteriological quality of ready to eat foods sampled at the point of sale, Communicable Diseases and Public Health, 3: 3.

Salihu MD, Junaidu AU, Magaji AA, Aliyu RM, Yakubu Y, Shittu A, & Ibrahim MA (2010). Bacteriological quality of traditionally prepared fried ground Beef (Dambun nama) in Sokoto, Nigeria. Advance Journal of Food Science and Technology. 2(3): 145-147.

Shalini M & Singh R (2005). Antibiotic resistance in food lactic acid bacteria - a review. International Journal of Food Microbiology. 105: 281-295.

Sina H, Baba-Moussa F, Kayode AP, Noumavo PA, Sezan A, Hounhouigan JD, Kotchoni S O, Prevost G, & Baba-Moussa L (2011). Characterization of Staphylococcus aureus isolated from street foods: Toxin profile and prevalence of antibiotic resistance. Journal of Applied Biosciences. 46: 3133-3143.

Soge OO, Adeniyi BA, & Roberts MC (2006). New antibiotic resistance genes associated with CTX-M plasmids from uropathogenic Nigerian Klebsiella pneumoniae. Journal of Antimicrobial Chemotherapy. 58: 1048–1053.

Tassew H, Abdissa A, Beyene G, & Gebre-Selassie S (2010). Microbial flora and food borne pathogens on minced meat and their susceptibility to antimicrobial agents. Ethiopian Journal of Health Sciences. 20: 137-143.

Tijjani J, Arzai AH, & Sadiq NM (2012). Antimicrobial susceptibility pattern of extended-spectrum beta-lactamase producers in Gram negative urogenital isolates in Kano, Nigeria. Bayero Journal of Pure and Applied Sciences. 5: 20-25.

Umoh JU (2001). An overview of possible critical control points of ready-to-eat beef product of Northern Nigeria. International Conference on Food and Security. Conference center Ibadan, Nigeria, pp 109-115.

Uzeh RE, Ohenhen RE, & Adeniji OO (2006). Bacterial contamination of Tsire-Suya, a Nigerian Meat Product. Pakistian Journal of Nutrition. 5(5): 458-460.


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