The investigation of the presence of Listeria species in poultry farms and antimicrobial resistance profiles of Listeria monocytogenes strains

Yıl 2022, Cilt: 6 Sayı: 1, 26 - 34, 30.04.2022

Yavuz Çokal Elçin Günaydın Gülşen Goncagül

https://doi.org/10.30704/http-www-jivs-net.1075016

Cited By: 2

Öz

Listeria species are widespread in nature and found in various environments. In this study, the presence of Listeria species in poultry farms was investigated. For this purpose, a total of 332 samples including feces, feed, drinking water and nipple swab from 5 broiler flocks reared on the floor and 352 samples including feces, feed, drinking water and eggshell swab from 5 layer flocks reared in cages were obtained. A modified version of the USDA-FSIS MLG 8.13 method was used for the isolation of Listeria species from samples. As a result of the study, Listeria spp. was isolated from all broiler and layer flocks. Isolation of Listeria spp. was carried out from 18 of 190 feces samples (9.4%), 5 of 15 drinking water samples (33.3%), 3 of 102 nipple swab samples (2.9%) in broiler flocks, and 22 of 167 feces samples (13.1%), 2 of 25 feed samples (8%), 3 of 15 drinking water samples (20%), 3 of 145 eggshell swab samples (2%) in layer flocks. Isolates were identified by cultural and biochemical characters, and a total of 56 Listeria isolates were identified as 15 L. monocytogenes, 3 L. ivanovii, 19 L. innocua, 13 L. seeligeri, 2 L. welshimeri, and 4 L. grayi. The antibiotic resistance profiles of L. monocytogenes isolates to twelve antibiotics were detected by the disc diffusion method. L. monocytogenes isolates were found to exhibit the highest resistance to ciprofloxacin (33.3%) among twelve antibiotics, and three isolates (20%) were also multidrug resistant. Consequently, it was determined that Listeria species in poultry farms are common.

Anahtar Kelimeler

Listeria spp., broiler, layer flock, prevalence, antimicrobial resistance

Kaynakça

• Alonso-Hernando, A., Prieto, M., García-Fernández, C., Alonso-Calleja, C. & Capita, R. (2012). Increase over time in the prevalence of multiple antibiotic resistance among isolates of Listeria monocytogenes from poultry in Spain. Food Control, 23, 37-41.
• Anonymous (2020). Balıkesir İlinde Tarım ve Hayvancılık. 2018 yılı TÜİK verilerine göre Balıkesir İli’nde öne çıkan ürünler. Balıkesir İl Tarım ve Orman Müdürlüğü, https://balikesir.tarimorman.gov.tr/Belgeler/Faaliyet%20Faporu/Bal%C4%B1kesir%20Tar%C4%B1m%20ve%20Hayvanc%C4%B1l%C4%B1k%20.pdf. Accessed July 01, 2020.
• Arslan, S. & Baytur, S. (2019). Prevalence and antimicrobial resistance of Listeria species and subtyping and virulence factors of Listeria monocytogenes from retail meat. Journal of Food Safety, 39: e12578.
• Aury, K., Bouquin, S.L., Toquin, M-T., Huneau-Salaün, A., Nôtre, Y.L., Allain, V., Petetin, I., Fravalo, P. & Chemaly, M. (2011). Risk factors for Listeria monocytogenes contamination in French laying hens and broiler flocks. Preventive Veterinary Medicine, 98, 271–278.
• Bertrand, S., Huys, G., Y de, M., D’Haene, K., Tardy, F., Vrints, M., Swings, J. & Collard, J-M. (2005). Detection and characterization of tet (M) in tetracycline-resistant Listeria strains from human and food-processing origins in Belgium and France. Journal of Medical Microbiology, 54, 1151–1156.
• Chemaly, M., Toquin, M-T., Nôtre, Y.L. & Fravalo, P. (2008). Prevalence of Listeria monocytogenes in Poultry Production in France. Journal of Food Protection, 71 (10),1996–2000.
• Clinical and Laboratory Standards Institute (CLSI) (2014). Performance standards for antimicrobial susceptibility testing; twenty forth informational supplement, Clinical and Laboratory Standards Institute, M100-S24, 34, 1. Wayne, PA, USA.
• Cokal, Y., Caner, V., Sen, A., Cetin, C. & Telli, M. (2011). The presence of Campylobacter jejuni in broiler houses: Results of a longitudinal study. African Journal of Microbiology Research, 5 (4): 389-393.
• Cooper, G., Charlton, B., Bickford, A., Cardona, C., Barton, J., Channing-Santiago, S. & Walker, R. (1992). Listeriosis in California broiler chickens. Journal of Veterinary Diagnostic Investigation, 4, 343-345.
• Cox, N.A., Bailey, J.S. & Berrang, M.E. (1997). The presence of Listeria monocytogenes in the integrated poultry industry. Journal of Applied Poultry Research, 6, 116–119.
• Dahshan, H., Merwad, A.M.A. & Mohamed, S.T. (2016). Listeria species in broiler poultry farms: potential public health hazards. Journal of Microbioogy and Biotechnology, 26 (9), 1551–1556.
• Datta, A. & Burall, L. (2018). Current trends in foodborne human listeriosis. Food Safety, 6, 1, 1-6. Dhama, K., Verma, A.K., Rajagunalan, S., Kumar, A., Tiwari, R., Chakraborty, S. & Kumar, R. (2013). Listeria monocytogenes infection in poultry and its public health importance with special reference to foodborne zoonoses. Pakistan Journal of Biological Sciences, 16 (7), 301-308.
• Dhama, K., Karthik, K., Tiwaric, R., Shabbird, M.Z., Barbuddhee, S., Malikf, S.V.S. & Singhg, R.K. (2015). Listeriosis in animals, its public health significance (food-borne zoonosis) and advances in diagnosis and control: a comprehensive review. Veterinary Quarterly, 35, 211-235.
• Dhanashree, B., Otta, S.K., Karunasagar, I., Goebel, W. & Karunasagar, I. (2003). Incidence of Listeria spp. in clinical and food samples in Mangalore, India. Food Microbiology, 20: 447-453.
• Esteban, J.I., Oporto, B., Aduriz, G., Juste, R.A. & Hurtado, A. (2008). A survey of food-borne pathogens in free-range poultry farms. International Journal of Food Microbiology, 123 (1-2), 177-182.
• European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2015). Break point tables for interpretation of MICs and zone diameter. Version 5.0, valid from 2015-01-01.
• Fallah, A.A., Saei-Dehkordi, S.S., Rahnama, M., Tahmasby, H. & Mahzounieh, M. (2012). Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control, 28, 327-332.
• Farber, J.M., Daley, E. & Coates, F. (1992). Presence of Listeria spp. in whole eggs and wash water samples from Ontario and Quebec. Food Research International, 25 (2), 143-145.
• Gasanov, U., Hughes, D. & Hansbro, P.M. (2005). Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review. FEMS Microbiology Reviews, 29, 851-875.
• Gião, M.S. & Keevil, C.W. (2014). Listeria monocytogenes can form biofilms in tap water and enter into the viable but non-cultivable state. Microbial Ecology, 67: 603–611.
• Gücükoğlu, A., Çadırcı, Ö., Gülel, G.T., Uyanık, T. & Kanat, S. (2020). Serotyping and antibiotic resistance profile of Listeria monocytogenes isolated from organic chicken meat. Kafkas Universitesi Veteriner Fakültesi Dergisi, 26 (4), 499-505.
• Gwida, M., Lüth, S., El-Ashker, M., Zakaria, A., El-Gohary, F., Elsayed, M., Kleta, S. & Dahouk, S.A. (2020). Contamination pathways can be traced a long the poultry processing chain by whole genome sequencing of Listeria innocua. Microorganisms, 8, 414.
• Hof, H., Nichterlien, T. & Krestschmar, M. (1997). Management of listeriosis. Clinical Microbiology Reviews, 10, 345–357.
• Ishola, O.O., Mosugu, J.I. & Adesokan, H.K. (2016). Prevalence and antibiotic susceptibility profiles of Listeria monocytogenes contamination of chicken flocks and meat in OyoState, south-western Nigeria: Public health implications. Journal of Preventive Medicine and Hygiene, 57, E157-E163.
• Kalender H. (2003). Detection of Listeria monocytogenes in faeces from chickens, sheep and cattle in Elazığ province. Turkish Journal of Veterinary and Animal Sciences, 27, 449-451.
• Kanarat, S., Jitnupong, W. & Sukhapesna, J. (2011). Prevalence of Listeria monocytogenes in chicken production chain in Thailand. Thai Journal of Veterinary Medicine, 41 (2), 155-161.
• Iida, T., Kanzaki, M., Maruyama, T., Inoue, S. & Kaneuchi, C. (1991). Prevalence of Listeria monocytogenes in intestinal contents of healthy animals in Japan. The Journal of Veterinary Medical Science, 53 (5), 873–875.
• Linke, K., Rückerl, I., Brugger, K., Karpiskova, R., Walland, J., Muri-Klinger, S, Tichy, A., Wagner, M. & Stessla, B. (2014). Reservoirs of Listeria species in three environmental ecosystems. Applied and Environmental Microbiology, 80 (18), 5583–559.
• Locatelli, A., Lewis, M.A. & Rothrock, M.J. Jr. (2017). The distribution of Listeria in pasture-raised broile rfarm soils is potentially related to university of vermont medium enrichment bias toward Listeria innocua over Listeria monocytogenes. Frontiers in Veterinary Science, 4, 227.
• Lunde´n, J., Tolvanen, R. & Korkeala, H. (2004). Human listeriosis outbreaksl inked to dairy products in Europe. Journal of Dairy Science, 87 (E. Suppl.), E6–E11.
• Milillo, S., Stout, J., Hanning, I., Clement, A., Fortes, E., Den Bakker, H, Wiedmann, M. & Ricke, S.C. (2012). Listeria monocytogenes and hemolytic Listeria innocua in poultry. Poultry Science, 91(9), 2158–2163.
• Ojeniyi, B., Wegener, H.C., Jensen, N.E. & Bisgaard, M. (1996). Listeria monocytogenes in poultry and poultry products: epidemiological investigations in seven Danish abattoirs. The Journal of Applied Bacteriology, 80, 395-401.
• Olaimat, A.N., Al-Holy, M.A., Shahbaz, H.M., Al-Nabulsi, A.A., Abu Ghoush, M.H., Osaili, T.M., Ayyash, M.M. & Holley, R.A. (2018). Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: A comprehensive review. Comprahensive Reviews in Food Science and Food Safety, 17, 1277-1292.
• Oliveira, T.S., Varjão, L.M., Silva, L.N.N., Pereira, R.C.L., Hofer, E., Vallim D.C. & Almeida, R.C.C. (2018). Listeria monocytogenes at chicken slaughterhouse: Occurrence, genetic relationship among isolates and evaluation of antimicrobial susceptibility. Food Control, 88, 131-138.
• Orsi, R.H. & Wiedmann, M. (2016). Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Applied Microbiology and Biotechnology, 100, 5273–5287.
• Osman, K.M., Kappell, A.D., Fox, E.M., Orabi, A. & Samir, A. (2020). Prevalence, pathogenicity, virulence, antibiotic resistance, and phylogenetic analysis of biofilm-producing Listeria monocytogenes isolated from different ecological niches in Egypt: food, humans, animals, andenvironment. Pathogens, 9, 5.
• Perrin, M., Bemer, M. & Delemore. C. (2003). Fatal case of Listeria innocua bacteremia. Journal of Clinical Microbiology, 41, 5308-5309.
• Petersen, L. & Madsen, M. (2000). Listeria spp. in broiler flocks: recovery rates and species distribution investigated by conventional culture and the EiaFoss method. International Journal of Food Microbiology, 58, 113–116.
• Rocourt, J., Hof, H., Schrettenbrunner, A., Malinverni, R. & Bille, J. (1986). Acute purulent Listeria seeligeri meningitis in an immunocompetent adult. Schweizerische medizinische Wochenschrift, 116, 248–251.
• Schwaiger, K., Schmied, E-M.V. & Bauer, J. (2010). Comparative analysis on antibiotic resistance characteristics of Listeria spp. and Enterococcus spp. isolated from laying hens and eggs in conventional and organic keeping systems in Bavaria, Germany. Zoonoses and Public Health, 57, 171-180.
• Seifi, S (2012). Prevalence and risk factors for Listeria monocytogenes contamination in Iranian broiler flocks. Acta Scientiae Veterinariae, 40 (4), 1074. https://www.redalyc.org/articulo.oa?id=289023924009
• Siriken, B., Ayaz, N.D. & Erol, I. (2014). Listeria monocytogenes in retailed raw chicken meat in Turkey. Berliner und Munchener Tierarztliche Wochenschrift, 127 (1-2), 43-49.
• Skovgaard, N. & Morgen, C.A. (1988). Detection of Listeria spp. in faeces from animals, in feeds, and in rawfoods of animal origin. International Journal of Food Microbiology, 6 (3), 229-242.
• Soni, D.K., Singh, R.K., Singh, D.V. & Dubey, S.K. (2013). Characterization of Listeria monocytogenes isolated from Ganges water, human clinical and milk samples at Varanasi, India. Infections Genetics and Evolution, 14, 83–91.
• Şanlıbaba, P., Tezel, B.U. & Çakmak, G.A. (2018). Prevalence and antibiotic resistance of Listeria monocytogenes isolated from ready-to-eat foods in Turkey. Journal of Food Quality, Article ID: 7693782, 9 pages,
• United States Department of Agriculture (USDA) (2021): Isolation and identification of Listeria monocytogenes from red meat, poultry ready-to-eat siluriformes (fish) and egg products, and environmental samples. USDA Microbiology Laboratory Guidebook., MLG 8.13, 1-21, Effective Date: 10/01/21. https://www.fsis.usda.gov/sites/default/files/media_file/2021-09/MLG-8.13.pdf. Accessed February 2, 2021.
• Walsh, D., Duffy, G., Sheridan, J.J., Blair, I.S. & McDowell, D.A. (2001): Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail foods. Journal of Applied Microbioogy., 90, 517-522.
• Wang, G., Qian, W., Zhang, X., Wang, H., Ye, K., Bai, Y. & Zhou G. (2015). Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control, 50, 202-208.
• Yücel, N., Çitak, S. & Önder, M. (2005). Prevalence and antibiotic resistance of Listeria species in meat products in Ankara, Turkey. Food Microbiology, 22, 241-245.
• Zhu, Q., Gooneratne, R. & Hussain, M.A. (2017). Listeria monocytogenes in fresh produce: outbreaks, prevalence and contamination levels. Foods, 6, 21.
• Zimmer, M., Barnhart, H., Idris, U. & Lee, M.D. (2003). Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens. Avian Diseases. 47, 101-107.