Evaluation of the Microbiological Quality of Poultry Imported into Togo and the Antibiotic Resistance of <i>Salmonella</i> spp. Isolated — Oak Academic Publishing
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Evaluation of the Microbiological Quality of Poultry Imported into Togo and the Antibiotic Resistance of <i>Salmonella</i> spp. Isolated
Laboratoire de Microbiologie des Aliments, de l’Eau et Produits Divers, Institut National d’Hygiène (INH), Lomé, Togo
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Laboratoire de Microbiologie des Aliments, de l’Eau et Produits Divers, Institut National d’Hygiène (INH), Lomé, Togo
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Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
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Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
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Laboratoire de Microbiologie des Aliments, de l’Eau et Produits Divers, Institut National d’Hygiène (INH), Lomé, Togo
,
Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
,
Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
,
Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
,
Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
,
Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
,
Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
1 Laboratoire de Microbiologie des Aliments, de l’Eau et Produits Divers, Institut National d’Hygiène (INH), Lomé, Togo
2 Laboratoire de Microbiologie des Aliments, de l’Eau et Produits Divers, Institut National d’Hygiène (INH), Lomé, Togo
3 Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
4 Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
5 Laboratoire de Microbiologie des Aliments, de l’Eau et Produits Divers, Institut National d’Hygiène (INH), Lomé, Togo
6 Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
7 Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
8 Laboratoire de Bactériologie Médicale de l’Institut National d’Hygiène (INH), Lomé, Togo
9 Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
10 Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
11 Laboratoire de Microbiologie et de Contrôle de la qualité des Denrées Alimentaires (LAMICODA), Université de Lomé, Lomé, Togo
In Togo, despite the government’s efforts, food requirements in terms of animal proteins are not covered by national production and are subject to huge imports of meat products. However, the hygienic quality of these imports is not guaranteed for the consumer. The aim of this study was to estimate the frequency of unhygienically unsatisfactory imported poultry and to determine the antibiotic resistance profile of Salmonella spp. strains. A total of 285 samples of imported poultry, including 55 chicken thighs, 10 chicken backbones, 25 chicken wings, 5 whole chickens, 30 sausages, 35 chicken forequarters, 95 chicken drumsticks and 30 guinea fowl wings, were analyzed using standard AFNOR routine methods. The following germs were tested: Total Aerobic Mesophilic Flora (TAMF), Anaerobic-Sulfite-Reducing (ASR), Escherichia coli , Staphylococcus aureus and Salmonella spp. Antibiotic susceptibility testing was carried out on Salmonella spp. strains isolated using the agar disk diffusion method (CA-SFM). Results showed 100% compliance for TAMF, coagulase-positive Staphylococci and Escherichia coli . On the other hand, 3.84% and 2.46% non-compliance were recorded for ASR and Salmonella respectively. Non-compliance with hygiene rules is generally thought to be the cause of meat contamination. Seven 7 strains of Salmonella were isolated, 5 of which were of the OMA serogroup, and the other two of the OMB and HMB groups. Antibiotic susceptibility tests revealed resistance to certain beta-lactam antibiotics and quinolones, in particular: cefalexin (28.57%), cefoxitin (14.28%), cefuroxime (28.57%), ceftazidime (28.57%), ceftriaxone (28.57%) and nalidixic acid (28.57%). This result may be explained by the uncontrolled use of B-lactam and quinolone antibiotics in poultry farming. As Salmonella spp. is a pathogenic enteric bacterium that causes food-borne illness in humans, resistance to third-generation cephalosporins remains a major public health problem.
Hanak, E., Boutrif, E., Fabre, P. and Pineiro, M. (2000) Food Safety Management in Developing Countries.
Wingstrand, A., Neimann, J., Engberg, J., Nielsen, E.M., Gerner-Smidt, P., Wegener, H.C., et al. (2006) Fresh Chicken as Main Risk Factor for Campylobacteriosis, Denmark. Emerging Infectious Diseases, 12, 280-284. https://doi.org/10.3201/eid1202.050936
Bumona Zayukua, E., Di M’balu Umba, J., Nzau Kusika, C., Ndyanabo Masimango, T. and Ndongala Lufimpadio, J.G. (2019) Contribution à l’analyse microbiologique des poulets, des chinchards (Trachurus trachurus) et des poissons salés vendus à Kinshasa en vue de la sensibilisation à la méthode ISO-22000:2005 HACCP. Journal of Animal and Plant Sciences, 42, 7256-7268. https://doi.org/10.35759/JAnmPlSci.v42-2.7
Bhat, Z.F., Morton, J.D., Mason, S.L. and Bekhit, A.E.-D.A. (2019) Pulsed Electric Field Improved Protein Digestion of Beef during In-Vitro Gastrointestinal Simulation. LWT, 102, 45-51. https://doi.org/10.1016/j.lwt.2018.12.013
Purohit, A.S., Reed, C. and Mohan, A. (2016) Development and Evaluation of Quail Breakfast Sausage. LWT—Food Science and Technology, 69, 447-453. https://doi.org/10.1016/j.lwt.2016.01.058
Accueil-Ministère de l’Agriculture, de l’Elevage et du Développement Rural. https://agriculture.gouv.tg
Cardinale, E., Perrier, J.D., Aidara, A., Tall, F., Coudert, C., Gueye, I.L., et al. (2000) Identification d’une nouvelle salmonelle multirésistante dans une viande de poulet de chair au Sénégal. Revue d’élevage et de médecine vétérinaire des pays tropicaux, 53, 5-8. https://doi.org/10.19182/remvt.9764
Alloui, M.N., Szczurek, W. and Świątkiewicz, S. (2013) The Usefulness of Prebiotics and Probiotics in Modern Poultry Nutrition: A Review. Annals of Animal Science, 13, 17-32. https://doi.org/10.2478/v10220-012-0055-x
Abba, H., Somda, M.K., Antipas, B.B., Barro, N. and Traore, A.S. (2017) Prévalence et susceptibilité aux antibiotiques des souches de Salmonella spp. non typhiques isolées de la viande de poulets au Tchad. International Journal of Biological and Chemical Sciences, 11, 107-117. https://doi.org/10.4314/ijbcs.v11i1.9
(2023) Comité de l’antibiogramme de la Société Française de Microbiologie Recommandations Vétérinaires 2023—Recherche Google. https://www.sfm-microbiologie.org/wp-content/uploads/2023/06/CASFM_VET2023.pdf
Omorodion, N. and Odu, N.N. (2014) Microbiological Quality of Meats Sold in Port Harcourt Metropolis, Nigeria. Natural Sciences, 12, 58-62.
Kozačinski, L., Hadžiosmanović, M. and Zdolec, N. (2006) Microbiological Quality of Poultry Meat on the Croatian Market. Veterinarski Arhiv, 76, 305-313.
Bhandari, N., Nepali, D.B. and Paudyal, S. (2013) Assessment of Bacterial Load in Broiler Chicken Meat from the Retail Meat Shops in Chitwan, Nepal. International Journal of Infection and Microbiology, 2, 99-104. https://doi.org/10.3126/ijim.v2i3.8671
Sengupta, R., Das, R., Ganguly, S. and Mukhopadhayay, S.K. (2012) Commonly Occurring Bacterial Pathogens Affecting the Quality of Chicken Meat. International Journal of Chemical and Biochemical Sciences, 1, 21-23.
Adu-Gyamfi, A., Torgby-Tetteh, W. and Appiah, V. (2012) Microbiological Quality of Chicken Sold in Accra and Determination of D10-Value of E. coli. Food and Nutrition Sciences, 3, 693-698. https://doi.org/10.4236/fns.2012.35094
Kim, Y.-J., Whan, C.-J., Kim, H.-S., Kim, K.-Y., Yim, J.-H., Cho, S.-H., et al. (2016) Improvement of Karmali Agar by Supplementation with Tazobactam for Detecting Campylobacter in Raw Poultry. Journal of Food Protection, 79, 1982-1985. https://doi.org/10.4315/0362-028X.JFP-16-105
Siddiqui, M.A., Khan, L.A., Suradkar, U.S., Mendhe, M.S., Rindhe, S.N. and Sirsat, P.R. (2008) Bacterial Isolation and Their Antibiogram from Non-Specific Infection in Poultry of Marathwada Region. Veterinary World, 1, 52-53.
Al-jasser, M.S. (2012) Effect of Cooling and Freezing Temperatures on Microbial and Chemical Properties of Chicken Meat during Storage. Journal of Food Agriculture & Environment, 10, 113-116.
Fernandes, R.T.V., Arruda, A.M.V.D., Costa, M.K.D.O., Lima, P.D.O., Santos, L.O.G.D., Melo, A.D.S., et al. (2016) Physicochemical and Microbiological Parameters of Frozen and Chilled Chicken Meat. Revista Brasileira de Zootecnia, 45, 417-421. https://doi.org/10.1590/S1806-92902016000700009
Cohen, N., Ennaji, H., Bouchrif, B., Hassar, M. and Karib, H. (2007) Comparative Study of Microbiological Quality of Raw Poultry Meat at Various Seasons and for Different Slaughtering Processes in Casablanca (Morocco). Journal of Applied Poultry Research, 16, 502-508. https://doi.org/10.3382/japr.2006-00061
Javadi, A. and Safarmashaei, S. (2011) Microbial Profile of Marketed Broiler Meat. Middle-East Journal of Scientific Research, 9, 652-656.
Maharjan, S., Rayamajhee, B., Chhetri, V.S., Sherchan, S.P., Panta, O.P. and Karki, T.B. (2019) Microbial Quality of Poultry Meat in an ISO 22000:2005 Certified Poultry Processing Plant of Kathmandu Valley. Food Contamination, 6, Article No. 8. https://doi.org/10.1186/s40550-019-0078-5
Khallaf, M., Benbakhta, B., Nasri, I., Sarhane, B., Senouci, S. and Ennaji, M.M. (2014) Prévalence du Staphylococcus aureus isolé à partir de la viande de poulet commercialisée au niveau de Rabat, Morocco. International Journal of Innovation and Applied Studies, 7, 1665-1670.
Yar, D.D., JimahKwenin, W.K., Kwame Zanu, W., IddrisuBalali, G., Kwame Adepa, E. and Francis, G. (2021) Microbial Quality of Frozen Chicken Parts from Three Import Countries into the Kumasi Metropolis of Ghana. Microbiology Research Journal International, 31, 43-53. https://doi.org/10.9734/mrji/2021/v31i630326
Jansen, W., Woudstra, S., Müller, A., Grabowski, N., Schoo, G., Gerulat, B., et al. (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, e0192550. https://doi.org/10.1371/journal.pone.0192550
Saikia, P. and Joshi, S. (2010) Retail Market Poultry Meats of North-East India-A Microbiological Survey for Pathogenic Contaminants. Research Journal of Microbiology, 5, 36-43. https://doi.org/10.3923/jm.2010.36.43
Farley, J.E., Hayat, M.J., Sacamano, P.L., Ross, T. and Carroll, K. (2015) Prevalence and Risk Factors for Methicillin-Resistant Staphylococcus aureus in an HIV-Positive Cohort. American Journal of Infection Control, 43, 329-335. https://doi.org/10.1016/j.ajic.2014.12.024
Mahmoud, R., Saleh, A. and Alsadi, I. (2020) Assessment of Microbiological Quality of Imported Broiler Chicken Carcasses Retailed for Sale in Al Beida City, Libya. Damanhour Journal of Veterinary Sciences, 4, 16-19. https://doi.org/10.21608/djvs.2020.33638.1019
Egervärn, M., Börjesson, S., Byfors, S., Finn, M., Kaipe, C., Englund, S., et al. (2014) Escherichia coli with Extended-Spectrum Beta-Lactamases or Transferable AmpC Beta-Lactamases and Salmonella on Meat Imported into Sweden. International Journal of Food Microbiology, 171, 8-14. https://doi.org/10.1016/j.ijfoodmicro.2013.11.005
Helali, S., Sawelem Eid Alatawi, A. and Abdelghani, A. (2018) Pathogenic Escherichia coli Biosensor Detection on Chicken Food Samples. Journal of Food Safety, 38, e12510. https://doi.org/10.1111/jfs.12510
Khan, M., Nazir, J., Anjum, A.A., Ahmad, M., Nawaz, M. and Shabbir, M.Z. (2015) Toxinotyping and Antimicrobial Susceptibility of Enterotoxigenic Clostridium perfringens Isolates from Mutton, Beef and Chicken Meat. Journal of Food Science and Technology, 52, 5323-5328. https://doi.org/10.1007/s13197-014-1584-3
Miwa, N., Nishina, T., Kubo, S., Atsumi, M. and Honda, H. (1998) Amount of Enterotoxigenic Clostridium perfringens in Meat Detected by Nested PCR. International Journal of Food Microbiology, 42, 195-200. https://doi.org/10.1016/S0168-1605(98)00082-8
Singh, R.V., Bhilegaonkar, K.N. and Agarwal, R.K. (2005) Studies on Occurrence and Characterization of Clostridium perfringens from Select Meats. Journal of Food Safety, 25, 146-156. https://doi.org/10.1111/j.1745-4565.2005.00560.x
Billon, J. and Poumeyrol, M. (1981) Evolution de l’origine des toxi-infections et intoxications alimentaires au cours des dernières années. Etude des 543 cas examinés au Laboratoire Central d’Hygiène Alimentaire durant les années 1974-1980. Bulletin de l’Académie Vétérinaire de France, 134, 425-435. https://doi.org/10.4267/2042/65656
Adeyanju, G.T. and Ishola, O. (2014) Salmonella and Escherichia coli Contamination of Poultry Meat from a Processing Plant and Retail Markets in Ibadan, Oyo State, Nigeria. SpringerPlus, 3, 139. https://doi.org/10.1186/2193-1801-3-139
Elgroud, R., Zerdoumi, F., Benazzouz, M., Bouzitouna-Bentchouala, C., Granier, S.A., Frémy, S., et al. (2009) Characteristics of Salmonella Contamination of Broilers and Slaughterhouses in the Region of Constantine (Algeria). Zoonoses and Public Health, 56, 84-93. https://doi.org/10.1111/j.1863-2378.2008.01164.x
Noenchat, P., Direksin, K. and Sornplang, P. (2023) The Phenotypic and Genotypic Antimicrobial Resistance Patterns of Salmonella Isolated from Chickens and Meat at Poultry Slaughter Houses in Japan and Thailand. Veterinary World, 16, 1527-1533.
Akbar, A. and Anal, A.K. (2014) Zinc Oxide Nanoparticles Loaded Active Packaging, a Challenge Study against Salmonella typhimurium and Staphylococcus aureus in Ready-to-Eat Poultry Meat. Food Control, 38, 88-95. https://doi.org/10.1016/j.foodcont.2013.09.065
Rouger, A., Tresse, O. and Zagorec, M. (2017) Bacterial Contaminants of Poultry Meat: Sources, Species, and Dynamics. Microorganisms, 5, Article No. 50. https://doi.org/10.3390/microorganisms5030050
Jørgensen, F., McLauchlin, J., Verlander, N.Q., Aird, H., Balasegaram, S., Chattaway, M.A., et al. (2022) Levels and Genotypes of Salmonella and Levels of Escherichia coli in Frozen Ready-to-Cook Chicken and Turkey Products in England Tested in 2020 in Relation to an Outbreak of S. enteritidis. International Journal of Food Microbiology, 369, Article ID: 109609. https://doi.org/10.1016/j.ijfoodmicro.2022.109609
Ramtahal, M.A., Amoako, D.G., Akebe, A.L.K., Somboro, A.M., Bester, L.A. and Essack, S.Y. (2022) A Public Health Insight into Salmonella in Poultry in Africa: A Review of the Past Decade: 2010-2020. Microbial Drug Resistance, 28, 710-733. https://doi.org/10.1089/mdr.2021.0384
Sasaki, Y., Kakizawa, H., Baba, Y., Ito, T., Haremaki, Y., Yonemichi, M., et al. (2021) Antimicrobial Resistance in Salmonella Isolated from Food Workers and Chicken Products in Japan. Antibiotics, 10, Article No. 1541. https://doi.org/10.3390/antibiotics10121541
Voss-Rech, D., Vaz, C.S.L., Alves, L., Coldebella, A., Leão, J.A., Rodrigues, D.P., et al. (2015) A Temporal Study of Salmonella enterica Serotypes from Broiler Farms in Brazil. Poultry Science, 94, 433-441. https://doi.org/10.3382/ps/peu081
Perin, A.P., Martins, B.T.F., Barreiros, M.A.B., Yamatogi, R.S., Nero, L.A. and dos Santos Bersot, L. (2020) Occurrence, Quantification, Pulse Types, and Antimicrobial Susceptibility of Salmonella sp. Isolated from Chicken Meat in the State of Paraná, Brazil. Brazilian Journal of Microbiology, 51, 335-345. https://doi.org/10.1007/s42770-019-00188-x
Bouda, S.C., Kagambèga, A., Bonifait, L., Gall, F.L., Ibrahim, H.B., Bako, E., et al. (2019) Prevalence and Antimicrobial Resistance of Salmonella enterica Isolated from Chicken and Guineafowl in Burkina Faso. International Journal of Microbiology and Biotechnology, 4, 64-71. https://doi.org/10.11648/j.ijmb.20190403.12
Kagambèga, A., Lienemann, T., Aulu, L., Traoré, A.S., Barro, N., Siitonen, A., et al. (2013) Prevalence and Characterization of Salmonella enterica from the Feces of Cattle, Poultry, Swine and Hedgehogs in Burkina Faso and Their Comparison to Human Salmonella Isolates. BMC Microbiology, 13, Article No. 253. https://doi.org/10.1186/1471-2180-13-253
Yang, X., Huang, J., Zhang, Y., Liu, S., Chen, L., Xiao, C., et al. (2020) Prevalence, Abundance, Serovars and Antimicrobial Resistance of Salmonella Isolated from Retail Raw Poultry Meat in China. Science of the Total Environment, 713, Article ID: 136385. https://doi.org/10.1016/j.scitotenv.2019.136385
Rau, R.B., Ribeiro, A.R., Dos Santos, A. and Barth, A.L. (2021) Antimicrobial Resistance of Salmonella from Poultry Meat in Brazil: Results of a Nationwide Survey. Epidemiology & Infection, 149, e228. https://doi.org/10.1017/S0950268821002156
Sodagari, H.R., Mashak, Z. and Ghadimianazar, A. (2015) Prevalence and Antimicrobial Resistance of Salmonella Serotypes Isolated from Retail Chicken Meat and Giblets in Iran. The Journal of Infection in Developing Countries, 9, 463-469. https://doi.org/10.3855/jidc.5945
Abd-Elghany, S.M., Sallam, K.I., Abd-Elkhalek, A. and Tamura, T. (2015) Occurrence, Genetic Characterization and Antimicrobial Resistance of Salmonella Isolated from Chicken Meat and Giblets. Epidemiology & Infection, 143, 997-1003. https://doi.org/10.1017/S0950268814001708
Ricke, S.C. and Calo, J.R. (2015) Antibiotic Resistance in Pathogenic Salmonella. In: Chen, C.-Y., Yan, X.H. and Jackson, C.R., Eds., Antimicrobial Resistance and Food Safety, Elsevier, Amsterdam, 37-53. https://doi.org/10.1016/B978-0-12-801214-7.00003-X
Lee, S.-K., Choi, D., Kim, H.-S., Kim, D.-H. and Seo, K.-H. (2016) Prevalence, Seasonal Occurrence, and Antimicrobial Resistance of Salmonella spp. Isolates Recovered from Chicken Carcasses Sampled at Major Poultry Processing Plants of South Korea. Foodborne Pathogens and Disease, 13, 544-550. https://doi.org/10.1089/fpd.2016.2144