Antibiotic resistance profiling in Listeria monocytogenes isolates from white meat available in Pakistani retail markets

Document Type : Full paper (Original article)

Authors

1 MSc in Applied Microbiology, Department of Bioinformatics and Biosciences, Faculty of Health and Life Sciences, Capital University of Science and Technology, Islamabad, Pakistan

2 MSc in Microbiology and Immunology, Department of Bioinformatics and Biosciences, Faculty of Health and Life Sciences, Capital University of Science and Technology, Islamabad, Pakistan

3 Dr. Ikram-ul-Haq Institute of Industrial Biotechnology (IIIB), Government College University (GCU), Lahore, Pakistan

10.22099/ijvr.2025.50453.7450

Abstract

Background: Listeriosis is a disease that occurs in immunocompromised people, caused by a zoonotic bacterium, Listeria monocytogenes. The significance of its prevalence in raw meat lies in its potential to cause illness if the meat is undercooked, fails to reach the recommended internal temperature, or through cross-contamination. Aims: This study aims to assess the presence of L. monocytogenes in fresh chicken, fish, and frozen/ready-to-eat (RTE) meat sourced from the retail markets of two major cities in Pakistan. Methods: The identification was done by biochemical and molecular methods targeting two genes of Listeria Pathogenicity Island (LIP-1) i.e., prfa and hly genes by PCR and was sequence analyzed, isolates sequences were submitted to NCBI GenBank to get accession number (ON859912, ON933793, ON933794, ON933795, ON933790, ON933791, and ON933792). The antibiotic resistance of these isolates was confirmed against seven antibiotics using the Disk Diffusion Method. Results: The antibiotic susceptibility profile of these isolates shows that most of the isolates were resistant to Vancomycin (43.2%), Gentamycin (37.8%), and Erythromycin (18.9%). Conclusion: The study reveals a significant presence of L. monocytogenes in meat samples, accompanied by antibiotic resistance to commonly used antibiotics for listeriosis in Pakistan. This alarming situation poses serious hazards to public health.

Keywords

Main Subjects


Abdollahzadeh, E; Ojagh, SM; Hosseini, H; Irajian, G and Ghaemi, EA (2016). Prevalence and molecular characterization of Listeria spp. and Listeria monocytogenes isolated from fish, shrimp, and cooked ready-to-eat (RTE) aquatic products in Iran. LWT. 73: 205-211.
AbdulRazzaq, A; Shami, AM and Ghaima, KK (2022). Detection of vanA and vanB genes among vancomycin resistant Staphylococcus aureus isolated from clinical samples in Baghdad hospitals. Iraqi J. Biotechnol., 21: 3-4.
Al-Brefkani, AMT (2023). Study the antimicrobial resistance genes of Listeria monocytogenes isolated from industrial and clinical samples in Iraq. Iraqi J. Sci., 64: 594-604.
Authority, EFS (2017). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2016. EFSA J., 15: 12-19.
Bøtner, A; Brown, I; Capua, I; Doherr, MG; Domingo, M; Koch, G; Koenen, F; Mumford, E; Pensaert, M and Sharp, M (2010). EFSA panel animal health and welfare (AHAW); Scientific opinion on the pandemic (H1N1) 2009 influenza and its potential implications for animal health: EFSA-Q-2009-00935.
Chandio, TH; Soomro, AH; Bhutto, MB; Dewani, P and Shah, G (2007). Occurrence of Listeria monocytogenes in bovine milk in Hyderabad, Pakistan. Ann. Microbiol., 57: 341-344.
Clinical and Laboratory Standards Institute (CLSI) (2017) Performance Standards for Antimicrobial Susceptibility Testing. 27th Edition, Clinical and Laboratory Standards Institute, Wayne. Performance Standards for Antimicrobial Susceptibility Testing., 11(27th Edition). https://www.nih. org.pk/wp-content/uploads/02/CLSI-2017.pdf
Doumith, M; Buchrieser, C; Glaser, P; Jacquet, C and Martin, P (2004). Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J. Clin. Microbiol., 42: 3819-3822.
Du, X; Zhang, X; Wang, X; Su, Y; Li, P and Wang, S (2017). Isolation and characterization of Listeria monocytogenes in Chinese food obtained from the central area of China. Food Control. 74: 9-16.
Duran, N; Ozer, B; Duran, GG; Onlen, Y and Demir, C (2012). Antibiotic resistance genes and susceptibility patterns in Staphylococci. Indian J. Med. Res., 135: 389-420.
Elsayed, MM; Elkenany, RM; Zakaria, AI and Badawy, BM (2022). Epidemiological study on Listeria monocytogenes in Egyptian dairy cattle farms’ insights into genetic diversity of multi-antibiotic-resistant strains by ERIC-PCR. Environ. Sci. Pollut. Res. Int., 29: 54359-54377.
Fugaban, JII; Holzapfel, WH and Todorov, SD (2021). Probiotic potential and safety assessment of bacteriocinogenic Enterococcus faecium strains with antibacterial activity against Listeria and vancomycin-resistant Enterococci. Curr. Res. Microb. Sci., 2: 100070-1000101.
Garcia, O; Mahmood, K and Hemme, T (2003). A review of milk production in Pakistan with particular emphasis on small-scale producers, PPLPI Working Papers 23782, Food and Agriculture Organization of the United Nations, Pro-Poor livestock policy initiative.
Goh, SG; Kuan, CH; Loo, YY; Chang, WS; Lye, YL; Soopna, P; Tang, JYH; Nakaguchi, Y; Nishibuchi, M and Afsah-Hejri, L (2012). Listeria monocytogenes in retailed raw chicken meat in Malaysia. Poult. Sci., 91: 2686-2690.
Hoffmann, SA; Maculloch, B and Batz, M (2015). Economic burden of major foodborne illnesses acquired in the United States. United States Department of Agriculture, Economic Research Service.
Indrawattana, N; Nibaddhasobon, T; Sookrung, N; Chongsa-Nguan, M; Tungtrongchitr, A; Makino, S; Tungyong, W and Chaicumpa, W (2011). Prevalence of Listeria monocytogenes in raw meats marketed in Bangkok and characterization of the isolates by phenotypic and molecular methods. J. Health Popul. Nutr., 29: 26-29.
Jami, M; Ghanbari, M; Zunabovic, M; Domig, KJ and Kneifel, W (2014). Listeria monocytogenes in aquatic food products—a review. 13: 798-813.
Ji, S; Song, Z; Luo, L; Wang, Y; Li, L; Mao, P; Ye, C and Wang, Y (2023). Whole-genome sequencing reveals genomic characterization of Listeria monocytogenes from food in China. Front. Microbiol., 13: 1049843-1049854.
Jung, KS; Heu, SG; Roh, EJ; Kim, MH; Gil, HJ; Choi, NY; Lee, DH; Lim, JA; Ryu, JG and Kim, KH (2013). Survival of Salmonella enterica and Listeria monocytogenes in chicken and pig manure compost. Korean J. Soil Sci. Fert., 46: 469-473.
Kalorey, DR; Barbuddhe, SB; Kurkure, NV and Gunjal, PS (2005). Prevalence of Listeria monocytogenes in poultry meat in Vidharba region of India. XVIIth European Symposium on the Quality of Poultry Meat. Doorwerth. The Netherlands.
Kataoka, A; Wang, H; Elliott, PH; Whiting, RC and Hayman, MM (2017). Growth of Listeria monocytogenes in thawed frozen foods. J. Food Prot., 80: 447-453.
Kayode, AJ and Okoh, AI (2022). Assessment of multidrug-resistant Listeria monocytogenes in milk and milk product and one health perspective. PLoS One. 17: e0270993-0271009.
Mahmood, MS; Ahmed, AN and Hussain, I (2003). Prevalence of Listeria monocytogenes in poultry meat, poultry meat products and other related inanimates at Faisalabad. Pak. J. Nutr., 2: 346-349.
Matle, I; Mbatha, KR and Madoroba, E (2020). A review of Listeria monocytogenes from meat and meat products: Epidemiology, virulence factors, antimicrobial resistance and diagnosis. Onderstepoort J. Vet. Res., 87: 1-20.
Meghdadi, H; Khosravi, AD; Sheikh, AF; Alami, A and Nassirabady, N (2019). Isolation and characterization of Listeria monocytogenes from environmental and clinical sources by culture and PCR-RFLP methods. Iran J. Microbiol., 11: 7-17.
Moreno, LZ; Paixao, R; Sena de Gobbi, DD; Raimundo, DC; Porfida Ferreira, TS; Micke Moreno, A; Hofer, E; dos Reis, CMF; Matté, GR and Matte, MH (2014). Phenotypic and genotypic characterization of atypical Listeria monocytogenes and Listeria innocua isolated from swine slaughterhouses and meat markets. Biomed Res. Int., 2014: 129-148.
Mpundu, P; Muma, JB; Mukubesa, AN; Kainga, H; Mudenda, S; Bumbangi, FN; Muleya, W; Katemangwe, P and Munyeme, M (2022). Antibiotic resistance patterns of Listeria species isolated from broiler abattoirs in Lusaka, Zambia. Antibiotics. 11: 591-610.
O’Grady, J; Ruttledge, M; Sedano-Balbas, S; Smith, TJ; Barry, T and Maher, M (2009). Rapid detection of Listeria monocytogenes in food using culture enrichment combined with real-time PCR. Food Microbiol., 26: 4-7.
Olaimat, AN; Al-Holy, MA; Shahbaz, HM; Al-Nabulsi, AA; Abu Ghoush, MH; Osaili, TM; Ayyash, MM and Holley, RA (2018). Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: a comprehensive review. Compr. Rev. Food Sci. Food Saf., 17: 1277-1292.
Oliveira, TS; Varjao, LM; da Silva, LNN; de C. L. Pereira, R; Hofer, E; Vallim, DC and de Castro Almeida, RC (2018). Listeria monocytogenes at chicken slaughterhouse: Occurrence, genetic relationship among isolates and evaluation of antimicrobial susceptibility. Food Control. 88: 131-138.
Osaili, TM; Alaboudi, AR and Nesiar, EA (2011). Prevalence of Listeria spp. and antibiotic susceptibility of Listeria monocytogenes isolated from raw chicken and ready-to-eat chicken products in Jordan. Food Control. 22: 586-590.
Samad, A; Asmat, R; Naeem, M; Ali, H; Mustafa, MZ; Abbas, F; Raza, J and Asmat, MT (2020). Isolation and identification of Listeria monocytogenes from raw vegetables and meat sold in Quetta, Pakistan. Pak. J. Zool., 52: 817-820.
Schlegelova, J; Vlkova, H; Babak, V; Holasova, M; Jaglic, Z; Stosova, T and Sauer, P (2008). Resistance to erythromycin of Staphylococcus spp. isolates from the food chain. Vet. Med. (Praha), 53: 307-315.
Shamloo, E; Hosseini, H; Moghadam, ZA; Larsen, MH; Haslberger, A and Alebouyeh, M (2019). Importance of Listeria monocytogenes in food safety: A review of its prevalence, detection, and antibiotic resistance. Iran. J. Vet. Res., 20: 241-253.
Skowron, K; Wiktorczyk, N; Grudlewska, K; Wałecka-
Zacharska, E; Paluszak, Z; Kruszewski, S and Gospodarek-Komkowska, E
(2019). Phenotypic and genotypic evaluation of Listeria monocytogenes strains isolated from fish and fish processing plants. Ann. Microbiol., 69: 469-482.
Sohaib, M and Jamil, F (2017). An insight of meat industry in Pakistan with special reference to halal meat: a comprehensive review. Korean J. Food Sci. Anim. Resour., 37: 329-345.
Swaminathan, B and Gerner-Smidt, P (2007). The epidemiology of human listeriosis. Microbes Infect., 9: 1236-1243.
Swetha, CS; Madhava Rao, T; Krishnaiah, N and Vijaya Kumar, A (2012). Detection of Listeria monocytogenes in fish samples by PCR assay. Ann. Biol. Res., 3: 1880-1884.
Swetha, CS; Porteen, K; Elango, A; Ronald, BSM; Kumar, TMAS; Milton, AP and Sureshkannan, S (2021). Genetic diversity, virulence and distribution of antimicrobial resistance among Listeria monocytogenes isolated from milk, beef, and bovine farm environment. Iran. J. Vet. Res., 22: 1-25.
Uyttendaele, M; Busschaert, P; Valero, A; Geeraerd, AH; Vermeulen, A; Jacxsens, L; Goh, KK; De Loy, A; Van Impe, JF and Devlieghere, F (2009). Prevalence and challenge tests of Listeria monocytogenes in Belgian produced and retailed mayonnaise-based deli-salads, cooked meat products and smoked fish between 2005 and 2007. Int. J. Food Microbiol., 133: 94-104.
Wieczorek, K and Osek, J (2017). Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from fresh and smoked fish in Poland. Food Microbiol., 64: 164-171.
Yan, H; Neogi, SB; Mo, Z; Guan, W; Shen, Z; Zhang, S; Li, L; Yamasaki, S; Shi, L and Zhong, N (2010). Prevalence and characterization of antimicrobial resistance of foodborne Listeria monocytogenes isolates in Hebei province of Northern China, 2005-2007. Int. J. Food Microbiol., 144: 310-316.
Zafar, N; Nawaz, Z; Anam, S; Kanwar, R; Ali, A; Mudassar, M; Javid, MT; Zafar, A and Tariq, A (2020). Prevalence, molecular characterization and antibiogram study of Listeria monocytogenes isolated from raw milk and milk products. PAB (Pure and Applied Biology). 9: 1982-1987.
Zakrzewski, AJ; Gajewska, J; Chajęcka-Wierzchowska, W; Załuski, D and Zadernowska, A (2023). Prevalence of Listeria monocytogenes and other Listeria species in fish, fish products and fish processing environment: A systematic review and meta-analysis. Sci. Total Environ., 907: 167912-167920.