Prevalence of Bacterial Pathogens and Their Antibiogram Profile in Raw Buffalo Meat from Maharashtra State, India

Ravindra Zende^1, , Vilas Vaidya¹, Aishwarya Nair¹, V.H. Shukla¹, Mahendra Pal², Nidhi Panicker¹, Aparna Shirke¹ and Suren Tambe¹

¹Department of Veterinary Public Health, Mumbai Veterinary College, Parel, Mumbai, India -400012 Maharashtra Animal & Fishery Sciences University, Nagpur-440001

²Narayan Consultancy of Veterinary Public Health, and Microbiology, Bharuch, Gujarat, India

Cite this paper:
Ravindra Zende, Vilas Vaidya, Aishwarya Nair, V.H. Shukla, Mahendra Pal, Nidhi Panicker, Aparna Shirke and Suren Tambe. Prevalence of Bacterial Pathogens and Their Antibiogram Profile in Raw Buffalo Meat from Maharashtra State, India. American Journal of Food and Nutrition. 2025; 13(1):1-7. doi: 10.12691/ajfn-13-1-1

Abstract

Foods of animal origin are an extremely important source of protein to the public in developing countries. However, the safety and quality of meat can be severely compromised by microbial contamination. Moreover, the presence of antibiotic residues in meat poses a significant public health concern due to its effects on human health through direct or indirect consumption. This study investigates the prevalence of pathogenic microbes in raw buffalo meat and evaluates their antibiogram profiles to ensure meat safety. A total of 250 raw buffalo meat samples were collected from the slaughterhouses in Mumbai region. The samples were subjected to microbiological analysis for detection of common foodborne pathogens, including Bacillus spp., Salmonella spp., Escherichia coli, Listeria monocytogenes, Staphylococcus aureus and Pseudomonas spp. The most prevalent pathogen in buffalo meat was found to be Staphylococcus aureus (26.00 %), followed by Salmonella spp. (18.40 %), E. coli (11.2 %) and Bacillus cereus (16.40 %), while Pseudomonas spp. and Listeria monocytogenes were absent in the samples. The bacterial isolates were further subjected to antibiotic susceptibility testing using disc diffusion method and the antibiogram revealed varying resistance profiles (MAR index > 0.2) with significant resistance observed against conventionally used antibiotics such as chloramphenicol, amikacin, cefotaxim, co-trimaxole and gentamicin. The current study emphasizes on the need for implementation of stringent hygiene practices and effective collaboration to implement antimicrobial stewardship in meat production and processing industry. The study concluded that the importance of regular monitoring and implementation of corrective measures to enhance food safety and safeguard consumer health.

Keywords:
Antibiogram Buffalo meat Food safety MAR index Pathogens Public Health

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References:

[1]	Carbas, B., Cardoso, L., & Coelho, A. C. (2012). Investigation on the knowledge associated with foodborne diseases in consumers of northeastern Portugal. Food Control, 30 (1), 54-57.
[2]	Angenent, L. T., Mau, M., George, U., Zahn, J. A., & Raskin, L. (2008). Effect of the presence of the antimicrobial tylosin in swine waste on anaerobic treatment. Water Research, 42, 2377–2384.
[3]	Kemper, N., Färber, H., Skutlarek, D., & Krieter, J. (2008). Analysis of antibiotic residues in liquid manure and leachate of dairy farms in northern Germany. Agricultural Water Management, 95, 1288–1292.
[4]	Landers, T. F., Cohen, B., Wittum, T. E., & Larson, E. L. (2012). A review of antibiotic use in food animals: Perspective, policy, and potential. Public Health Reports, 127 (1), 4-22.
[5]	Visa, I. (Ed.). (2014). Sustainable Energy in the Built Environment-Steps Towards NZEB: Proceedings of the Conference for Sustainable Energy (CSE) 2014. [Viewed on 10th July, 2024].
[6]	Saud, B., Paudel, G., Khichaju, S., Bajracharya, D., Dhungana, G., Awasthi, M. S., & Shrestha, V. (2019). Multidrug-resistant bacteria from raw meat of buffalo and chicken in Nepal. Veterinary Medicine International, 1, 7960268.
[7]	Ondon, B. S., Li, S., Zhou, Q., & Li, F. (2021). Sources of antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARGs) in the soil: A review of the spreading mechanism and human health risks. Reviews of Environmental Contamination and Toxicology, 256, 121-153.
[8]	Thakur, S. D., & Panda, A. K. (2017). Rational use of antimicrobials in animal production: A prerequisite to stem the tide of antimicrobial resistance. Current Science, 113(10), 1846-1857.
[9]	Hao, H., Cheng, G., Iqbal, Z., Ai, X., Hussain, H. I., Huang, L., & Yuan, Z. (2014). Benefits and risks of antimicrobial use in food-producing animals. Frontiers in Microbiology, 5, 288.
[10]	Hower, S., Phillips, M. C., Brodsky, M., Dameron, A., Tamargo, M. A., Salazar, N. C., & Plano, L. R. (2013). Clonally related methicillin-resistant Staphylococcus aureus isolated from short-finned pilot whales (Globicephala macrorhynchus), human volunteers, and a bayfront cetacean rehabilitation facility. Microbial Ecology, 65(4), 1024-1038.
[11]	Verkade, E., & Kluytmans, J. (2014). Livestock-associated Staphylococcus aureus CC398: Animal reservoirs and human infections. Infection, Genetics and Evolution, 21, 523-530.
[12]	Clinical Laboratory and Standards Institute. (2019). Performance standards for antimicrobial susceptibility testing (29th ed).
[13]	Kabir, A. B. M. (2017). A study on the prospect of Escherichia coli isolated from raw beef samples as a potential reservoir of antibiotic resistance (Doctoral dissertation, BRAC University). Retrieved on 15th July, 2024, from [BRAC University Digital Repository].
[14]	Naas, H. T., Edarhoby, R. A., Garbaj, A. M., Azwai, S. M., Abolghait, S. K., Gammoudi, F. T., & Eldaghayes, I. M. (2019). Occurrence, characterization, and antibiogram of Staphylococcus aureus in meat, meat products, and some seafood from Libyan retail markets. Veterinary World, 12(6), 925.
[15]	Hassan, M. K., Jahan, L., Sultana, P., Hasan, A., & Siddique, M. P. (2021). Detection and antibiogram of different bacterial agents from market goat meat. Research in Agriculture Livestock and Fisheries, 8(1), 135-143.
[16]	Swati Singh, S. S., Kshirsagar, D. P., Brahmbhatt, M. N., Nayak, J. B., & Chatur, Y. A. (2015). Isolation and characterization of Salmonella spp. from buffalo meat samples. Buffalo Bulletin, 34(3), 301-302.
[17]	Eruteya, O. C., Odunfa, S. A., & Lahor, J. (2014). Listeria spp. in raw cow and goat meat in Port Harcourt, Nigeria. British Biotechnology Journal, 4(2), 204-214.
[18]	Arslan, S., Eyi, A., & Özdemir, F. (2011). Spoilage potentials and antimicrobial resistance of Pseudomonas spp. isolated from cheeses. Journal of Dairy Science, 94(12), 5851-5856.
[19]	Holt, J. G., Krieg, N. R., Sneath, P. H. A., Staley, J. T., & Williams, S. T. (1994). Bergey’s Manual of Determinative Bacteriology (9th ed.). Williams and Wilkins Press.
[20]	Singh, S. K., Ekka, R., Mishra, M., & Mohapatra, H. (2017). Association study of multiple antibiotic resistance and virulence: a strategy to assess the extent of risk posed by bacterial population in aquatic environment. Environmental monitoring and assessment, 189, 1-12.
[21]	Likhitha, P., Nayak, J. B., & Thakur, S. (2022). Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in retail buffalo meat in Anand, India. The Pharma Innovation Journal, 11(6), 17-20.
[22]	Zehra, A., Gulzar, M., Singh, R., & Kaur, S. (2019). Methicillin-susceptible and methicillin-resistant Staphylococcus aureus from the retail meat shops and customers. International Journal of Current Microbiology and Applied Sciences, 8, 1929-1939.
[23]	Raji, M. A., Garaween, G., Ehricht, R., Monecke, S., Shibl, A. M., & Senok, A. (2016). Genetic characterization of Staphylococcus aureus isolated from retail meat in Riyadh, Saudi Arabia. Frontiers in Microbiology, 7, 911.
[24]	Thapaliya, D., Forshey, B. M., Kadariya, J., Quick, M. K., Farina, S., O’Brien, A., Nair, R., & Smith, T. C. (2017). Prevalence and molecular characterization of Staphylococcus aureus in commercially available meat over a one-year period in Iowa, USA. Food Microbiology, 65, 122-129.
[25]	Jaja, I. F., Jaja, C. J. I., Chigor, N. V., Anyanwu, M. U., Maduabuchi, E. K., Oguttu, J. W., & Green, E. (2020). Antimicrobial resistance phenotype of Staphylococcus aureus and Escherichia coli isolates obtained from meat in the formal and informal sectors in South Africa. BioMed Research International, 2020(1), 3979482.
[26]	Khan, J. A., Rathore, R. S., Ahmad, I., Gill, R., Husain, F. M., & Akhtar, J. (2022). High prevalence of multidrug-resistant Staphylococcus aureus from buffalo beef sold at retail butcheries in Northern India. Acta Scientific Microbiology, 5(10), 2581-3226.
[27]	Eyi, A., & Arslan, S. (2012). Prevalence of Escherichia coli in retail poultry meat, ground beef, and beef. Medycyna Weterynaryjna Veterinary Medicine Science and Practice, 68(4), 237-240.
[28]	Maharjan, M., Joshi, V., Joshi, D. D., & Manandhar, P. (2006). Prevalence of Salmonella species in various raw meat samples of a local market in Kathmandu. Annals of the New York Academy of Sciences, 1081(1), 249-256.
[29]	Mohammed, T., Zakaria, A., Abd-Elghany, S., & Sallam, K. (2023). Prevalence, genetic characterization, and antibiogram of Salmonella enterica recovered from buffalo meat. Mansoura Veterinary Journal, 24(1), 14-21.
[30]	Suthar, A. P., Kumar, R., Savalia, C. V., Nayak, D. N., & Kalyani, I. H. (2022). Determination of prevalence and multidrug resistance phenotypes of Bacillus cereus in raw chicken meat and swabs of human subjects. Pharma Innovation, 11(12), 1159-1164.
[31]	Al-Humam, N. A., Reda, L., Mohamed, R. E., El-Ghareeb, W. R., Darwish, W. S., & Ibrahim, N. A. (2021). Prevalence and antibiogram of Listeria monocytogenes in retailed buffalo raw meat and mince with a protection trial using nisin, and gingerol. Buffalo Bulletin, 40(4), 47-57.
[32]	De Cesare, A., Parisi, A., Mioni, R., Comin, D., Lucchi, A., & Manfreda, G. (2017). Listeria monocytogenes circulating in rabbit meat products and slaughterhouses in Italy: Prevalence data and comparison among typing results. Foodborne Pathogens and Disease, 14(3), 167-176.
[33]	Liu, Y., Sun, W., Sun, T., Gorris, L. G., Wang, X., Liu, B., & Dong, Q. (2020). The prevalence of Listeria monocytogenes in meat products in China: A systematic literature review and novel meta-analysis approach. International Journal of Food Microbiology, 312, 108358.
[34]	Poursina, S., Ahmadi, M., Fazeli, F., & Ariaii, P. (2022). Prevalence and antibiotic resistance of Pseudomonas aeruginosa isolates from raw meat samples of small ruminants. Journal of Pharmaceutical Negative Results, 13(9), 9742-9748.
[35]	Al-Zoubi, M. S., Al-Tayyar, I. A., Hussein, E., Al Jabali, A., & Khudairat, S. (2015). Antimicrobial susceptibility pattern of Staphylococcus aureus isolated from clinical specimens in Northern area of Jordan. Iranian Journal of Microbiology, 7(5), 265.
[36]	Nurjadi, D., Schäfer, J., Friedrich-Jänicke, B., Mueller, A., Neumayr, A., Calvo-Cano, A., & Zanger, P. (2015). Predominance of dfrG as determinant of trimethoprim resistance in imported Staphylococcus aureus. Clinical Microbiology and Infection, 21(12), 1095-e5.
[37]	Thwala, T., Madoroba, E., Basson, A., & Butaye, P. (2021). Prevalence and characteristics of Staphylococcus aureus associated with meat and meat products in African countries: A review. Antibiotics, 10(9), 1108.
[38]	Khanal, S., Kandel, M., & Shah, M. P. (2019). Antibiogram pattern of Escherichia coli, Salmonella spp., and Staphylococcus spp. isolates from broiler chicken. Nepalese Veterinary Journal, 36, 105-110.
[39]	Alipourfard, I., & Nili, N. Y. (2010). Antibiogram of extended spectrum beta-lactamase (ESBL) producing Escherichia coli and Klebsiella pneumoniae isolated from hospital samples. Bangladesh Journal of Medical Microbiology, 4(1), 32-36.
[40]	Kamble, G. A., Shah, R. C., & Tumane, P. M. (2013). Characterization and antibiogram study of Escherichia coli clinical isolates. Blood, 25(1), 24.
[41]	Zanella, A., Alborali, G. L., Bardotti, M., Candotti, P., Guadagnini, P. F., Martino, P. A., & Stonfer, M. (2000). Severe Escherichia coli O111 septicaemia and polyserositis in hens at the start of lay. Avian Pathology, 29(4), 311-317.
[42]	Abhadionmhen, A. O., Imarenezor, E. P. K., Brown, S. T. C., Lana, O. E., & Usiabulu, O. Q. (2024). Molecular identification of invA gene from Salmonella species isolated from human sources in Southern Taraba, North-East Nigeria. Asian Journal of Research in Infectious Diseases, 15(3), 7-16.
[43]	Abdeen, E., Elmonir, W., Suelam, I. I. A., & Mousa, W. S. (2018). Antibiogram and genetic diversity of Salmonella enterica with zoonotic potential isolated from morbid native chickens and pigeons in Egypt. Journal of Applied Microbiology, 124(5), 1265-1273.
[44]	Akhtar, F., Hussain, I., Khan, A., & Rahman, S. U. (2010). Prevalence and antibiogram studies of Salmonella enteritidis isolated from human and poultry sources. Pakistan Veterinary Journal, 30(1), 25-28.
[45]	Shaibu, A. O., Okolocha, E. C., Maikai, B. V., & Olufemi, O. T. (2021). Isolation and antibiogram of Salmonella species from slaughtered cattle and the processing environment in Abuja abattoirs, Nigeria. Food Control, 125, 107972.
[46]	Gebremedhin, E. Z., Soboka, G. T., Borana, B. M., Marami, L. M., Sarba, E. J., Tadese, N. D., & Ambecha, H. A. (2021). Prevalence, risk factors, and antibiogram of nontyphoidal Salmonella from beef in Ambo and Holeta Towns, Oromia Region, Ethiopia. International Journal of Microbiology, 2021(1), 6626373.
[47]	Weber, D. J., Saviteer, S. M., Rutala, W. A., & Thomann, C. A. (1988). In vitro susceptibility of Bacillus spp. to selected antimicrobial agents. Antimicrobial Agents and Chemotherapy, 32(5), 642-645.
[48]	Rather, M. A., Aulakh, R. S., Gill, J. P., & Ghatak, S. (2012). Enterotoxin gene profile and antibiogram of Bacillus cereus strains isolated from raw meats and meat products. Journal of Food Safety, 32(1), 22-28.
[49]	Osama, R., Ahmed, M., Abdulmawjood, A., & Al-Ashmawy, M. (2020). Prevalence and antimicrobial resistance of Bacillus cereus in milk and dairy products. Mansoura Veterinary Medical Journal, 21(2), 11-18.
[50]	Joseph, A. A., Odimayo, M. S., Olokoba, L. B., Olokoba, A. B., & Popoola, G. O. (2017). Multiple antibiotic resistance index of Escherichia coli isolates in a tertiary hospital in southwest Nigeria. Medical Journal of Zambia, 44(4), 225-232.
[51]	Nwankwo, C. C., Ezeonuegbu, B. A., & Owei, M. D. (2024). Antibiogram of foodborne pathogenic bacteria isolated from raw pork and beef meat. Magna Scientia Advanced Research and Reviews, 11(1), 325-338.
[52]	Hassanien, F. M., Nada, S. M., & Abd-Elsattar, A. M. (2016). Incidence of E. coli in some meat products. Benha Veterinary Medical Journal, 30(1), 104-108.
[53]	Jolapamo, O. T., & Osatoyinbo, O. O. (2023). Isolation, identification, and antibiogram of bacterial pathogens from cow meat obtained from different market sources. Achievers Journal of Scientific Research, 5(2), 72-79.
[54]	Algammal, A. M., Eid, H. M., Alghamdi, S., Ghabban, H., Alatawy, R., Almanzalawi, E. A., & El-Tarabili, R. M. (2024). Meat and meat products as potential sources of emerging MDR Bacillus cereus: groEL gene sequencing, toxigenic and antimicrobial resistance. BMC Microbiology, 24(1), 50.
[55]	Abdel-Atty, N. S., Abdulmalek, E. M., Taha, R. M., Hassan, A. H., & Adawy, A. A. (2023). Predominance and antimicrobial resistance profiles of Salmonella and E. coli from meat and meat products. Journal of Advanced Veterinary Research, 13(4), 647-655.
[56]	Cameron, A., & McAllister, T. A. (2016). Antimicrobial usage and resistance in beef production. Journal of Animal Science and Biotechnology, 7(68), 1-22.
[57]	Argudín, M. A., Deplano, A., Meghraoui, A., Dodémont, M., Heinrichs, A., Denis, O., & Roisin, S. (2017). Bacteria from animals as a pool of antimicrobial resistance genes. Antibiotics, 6(2), 12.