Prevalence, genetic characterization, and antimicrobial resistance of Salmonella isolated from meat goats in the Northeastern region of Thailand https://doi.org/10.12982/VIS.2021.031

Main Article Content

Wattanasak Chamlakhorn
Patchara Phuektes
Seri Khang-Air
Sunpetch Angkititrakul

Abstract

This study aimed to determine the prevalence, genotypic diversity, and antimicrobial resistance pattern of Salmonella isolated from meat goats in the Northeastern region of Thailand. A total of 1,014 rectal swabs were collected from 30 meat goat farms during April to November, 2018. Salmonella was isolated and identified according to the International Organization for Standardization protocol (ISO-6579:2002/AMD:2017) and serotyped using a slide agglutination test following the Kauffmann-White scheme. An antimicrobial susceptibility test to determine minimal inhibitory concentration (MIC) of 12 antimicrobial agents was performed using a broth microdilution method following the CLSI protocol (2017). Pulsed-field gel electrophoresis (PFGE) of XbaI digested chromosomal DNA was used to determine genotypic diversity of the isolates. The overall prevalence of Salmonella in the meat goats was 1.28%. A total of 13 Salmonella isolates recovered from the meat goats belonged to 4 serovars includings. Weltevreden (n=4), S. Bovismorbificans (n=4), S. Paratyphi B (n=4), and S. Stanley (n=1). Antimicrobial susceptibility testing revealed 2 antibiogram patternS. Eleven Salmonella isolates were susceptible to all antimicrobial agents tested, except sulfamethoxazole, and the other 2 isolates were susceptible to all antimicrobials. Genetic characterization of 13 Salmonella isolates by PFGE revealed 9 PFGE patterns that were grouped into 4 major clusters, A, B, C and D, with an 80% similarity value. This study revealed a low prevalence of Salmonella in meat goats in the Northeastern region of Thailand. Salmonella isolates were susceptible to most antimicrobials tested, with a very high proportion of resistance to sulfamethoxazole being observed.

Article Details

How to Cite
Chamlakhorn, W. ., Phuektes, P. ., Khang-Air, S. ., & Angkititrakul, S. . (2021). Prevalence, genetic characterization, and antimicrobial resistance of Salmonella isolated from meat goats in the Northeastern region of Thailand: https://doi.org/10.12982/VIS.2021.031. Veterinary Integrative Sciences, 19(3), 363–378. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/251193
Section
Research Articles

References

Abulreesh, H.H., 2012. Salmonellae in the environment. In: Annous, B., J.B. Gurtler, J.B. Salmonella-Distribution, Adaptation, Control Measures and Molecular Technologies. pp. 19-50.

Al-Habsi, K., Jordan, D., Harb, A., Laird, T., Yang, R., O’Dea, M., Jacobson, C., Miller, D.W., Ryan, U., Abraham, S., 2018. Salmonella enterica isolates from Western Australian rangeland goats remain susceptible to critically important antimicrobials. Sci. Rep. 8(1), 15326.

Andino, A., Hanning, I., 2015. Salmonella enterica: survival, colonization, and virulence differences among serovars. Sci. World J. doi: 10.1155/2015/520179.

Bantawa, K., Sah,S.N., Limbu, D.S., Subba, P., Ghimire, A., 2019. Antibiotic resistance patterns of Staphylococcus aureus, Escherichia coli, Salmonella, Shigella and Vibrio isolated from chicken,pork, buffalo and goat meat in eastern Nepal. BMC Res. Notes. 12(1), 766.

Batz, M. B., Hoffmann, S., Morris, J. G., 2012. Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J. Food. Prot. 75(7), 1278–1291.

Chandra, M., Singh, B. R., Shankar, H., Agarwal, M., Agrawal, R. K., Sharma, G., Babu, N., 2006. Study on prevalence of Salmonella infection in goats. Small Rumin. Res. 65(1–2), 24-30.

Center for Disease Control and Prevention [CDC], 2017. Standard Operating Procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157(STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri. Available from: https://www.cdc.gov/pulsenet/pdf/ecoli-shigella-salmonella-pfge-protocol-508c.pdf. Retrieved on 20-12-2019.

Center for Disease Control and Prevention., 2019. Antibiotic resistance threats in the United States,2019. Atlanta, GA: U.S. Department of health and human services, CDC; 2019.

Clinical and Laboratory Standards Institute [CLSI]., 2017a. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 5th Ed. CLSI standard VET01-A5. Clinical and Laboratory Standards Institute. Wayne, Pennsylvania.

Clinical and Laboratory Standards Institute [CLSI], 2017b. Performance standards for antimicrobial susceptibility testing. 27th Ed. CLSI document M100-S27. Clinical and Laboratory Standards Institute. Wayne, Pennsylvania.

Duffy, L., Barlow, R., Fegan, N., Vanderlinde, P., 2009. Prevalence and serotypes of Salmonella associated with goats at two Australian abattoirs. Lett. Appl. Microbiol. 48(2), 193-197.

Davies, R.H, Dalziel, R., Gibbens, J.C., Wilesmith, J.W., Ryan, J.M., Evans, S.J., Byrne, C., Paiba, G.A., Pascoe, S.J., Teale, C.J., 2004. National survey for Salmonella in pigs, cattle and sheep at slaughter in Great Britain (1999–2000). J. Appl. Microbiol. 96, 750-760.

Demirbilek, S.K., 2018. Salmonellosis in Animals. DOI:10.5772/intechopen.72192.

Economou, V., Gousia, P., 2015. Agriculture and food animals as a source of antimicrobial-resistant bacteria. Infect. Drug Resist. 8, 49-61.

Elkenany, R., Elsayed, M.M., Zakaria, A.I., El-sayed, S.A., Rizk, M.A., 2019. Antimicrobial resistance profiles and virulence genotyping of Salmonella enterica serovars recovered from broiler chickens and chicken carcasses in Egypt. BMC Vet. Res. 15, 124.

Esmaeili, H. Rahmani, H.K., 2016. Detection of carriers in sheep and goat flocks of Bushehr and Lorestan Provinces, Iran. J. Med. Bacteriol. 5(3-4): 50-53.

Ferede, B., Desissa, F., Feleke, A., Moje, N., 2015. Prevalence and antimicrobial susceptibility of Salmonella isolates from apparently health slaughtered goats at Dire Dawa municipal abattoir, Eastern, Ethiopia. J. Microbiol. Antimicrob. 7(1), 1-5.

Ferede, B., Desissa, F., Feleke, A., Tadesse, G., Moje, N., 2017. Antibiotics and antibiotics resistance. J. Drug Metab. Toxicol. 8, 2 (Suppl).

Glenn, L.M., Lindsey, R.L., Frank F.J., Meinersmann, R.J., Englen, M.D., Fedorka-Cray, P.J., Frye, J.G., 2011. Analysis of antimicrobial resistance genes detected in multidrug-resistant Salmonella enterica Serovar Typhimurium isolated from food animals. Microb. Drug Resist. 17, 407-418.

Grimont, P.A., Weill, F.X., 2007. Antigenic Formulae of the Salmonella Serovars, WHO Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur, Paris, France.

Harbottle, H., White, D.G., McDermott, P.F., Walker, F.D., Zhao, S., 2006. Comparison of multilocus sequence typing, pulsed-field gel electrophoresis, and antimicrobial susceptibility typing for characterization of Salmonella enterica serotype Newport isolates. J. Clin. Microbiol. 44(7), 2449–2457.

Hoelzer, K., Switt, A.I.M., Wiedmann, M., 2011. Animal contact as a source of human non-

typhoidal Salmonellosis. Vet. Res. 42(1), 34.

Hong, S., Rovira, A., Davies, P., Ahlstrom, C., Muellner, P., Rendahl, A., 2016. Serotypes and antimicrobial resistance in Salmonella enterica recovered from clinical samples from cattle and swine in Minnesota, 2006 to 2015. Plos One. doi: 10.1371/journal.pone.0168016.

Igbinosa, I.H., 2015. Prevalence and detection of antibiotic-resistance determinant in Salmonella isolated from food-producing animals. Trop. Anim. Health. Prod. 47(1), 37-43.

International Organization for Standardization., 2017. Microbiology of the food chain-horizontal method for the detection, Enumeration and Serotyping of Salmonella. Part 1: Detection of Salmonella. Available from: https://www.iso.org/standard/56712.html. Retrieved on 20-12-2019.

Jajere, S.M., Adamu, N.B., Atsanda, N.N., Onyilokwu, S.A., Gashua, M.M., Hambali, I.U., Mustapha, F.B., 2016. Prevalence and antimicrobial resistance profiles of Salmonella isolates in Apparently slaughtered food animals at Maiduguri central abattoir, Nigeria. Asian. Pac. J. Trop. Dis. 5(12), 996-1000.

John, A.C., Felicita, M.M, Kevin, W.J., Amy, L., Krueger, R.H., Jean, M.W, Ezra, J.B, and the emerging infections program NARMS working group., 2011. Antimicrobial resistance among invasive nontyphoidal Salmonella enterica Isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996 to 2007. Antimicrob. Agents Chemother. 55, 1148-1154.

Kassaye, B.K., Hassen, D.J., Leja, K.A., Tsegaye, B., 2015. Study on prevalence and distribution of Salmonella isolates from apparently healthy sheep and goats slaughtered at Addis Ababa Abattoir Enterprise, Ethiopia. J. Vet. Sci. Technol. 6(6), 1-5.

Mahmood, A.K., Khan, M.S., Khan, M.A. Bilal, M., 2014. Prevalence of Salmonella in diarrheic adult goats in field conditions. J. Anim. Plant. Sci. 24(1), 98-102.

Mathole, M.A., Muchadeyi, F.C., Mdladla, K., Malatji, D.P., Dzomba, E.F., Madoroba, E., 2017. Presence, distribution, serotype and antimicrobial resistance profiles of Salmonella among pigs, chickens and goats in South Africa. Food Control. 72, 219-224.

Molla, W., Molla, B., Alemayehu, D., Muckle, A., Cole, L., Wilkie, E., 2006. Occurrence and antimicrobial resistance of Salmonella serovars in apparently healthy slaughtered sheep and goats of central Ethiopia. Trop. Anim. Health Prod. 38(6), 455-462.

Musa, Z., Onyilokwu, S.A., Jauro, S., Yakubu, C., Musa, J.A., 2017. Occurrence of Salmonella in ruminants and camel meat in Maiduguri, Nigeria and their antibiotic resistant pattern. J. Adv. Vet. Anim. Res. 4(3), 227-233.

Mwanyika, G.O., Buza, J., Rugumisa, B.T., Luanda, C., Murutu, R., Lyimo, B., Subbiah, M., Call1, D.R., 2016. Recovery and prevalence of antibiotic-resistant Salmonella from fresh goat meat in Arusha, Tanzania. Afr. J. Microbiol. Res. 10(32), 1315-1321.

Nisbet, D.V., Ziprin, L., 2001. Foodborne Diseases Handbook Bacterial Pathogen. In: Huy,Y., Pierson, M.D., Gorham, J.R. New York: Marcel Dekker. pp. 265-284.

Nouichi, S., Hamdi, T.M., 2009. Superficial Bacterial Contamination of Ovine and Bovine carcasses at El-Harrach Slaughterhouse (Algeria). Eur. J. Sci. Res. 38, 474-485.

Nsofor, C.A., 2016. Pulsed-Field Gel Electrophoresis (PFGE): Principles and applications inmolecular epidemiology: a review. Int. J. Curr. Res. Med. Sci. 2(2), 38-51.

OIE., 2018. Salmonellosis in: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals chapter 3.9.8. 1735-1752.

Ola Sköld. 2001. Resistance to trimethoprim and sulfonamides. Vet. Res. 32 (3-4), 261-273.

Padungtod, P., Kaneene, J.B., 2006. Salmonella in food animals and humans in northern Thailand. Int. J. Food Microbiol. 108(3), 346-354.

Popoff, M.Y., Le Minor, L., 2007. Antigenic Formulas of the Salmonella Serovars. 8th ed. WHO Collaborating Centre for Reference and Research on Salmonella, Pasteur Institute, France.

Patchanee, P., Tansiricharoenkul, K., Buawiratlert, T., Wiratsudakul, A., Angchokchatchawal, K., Yamsakul, P., Yano, T., Boonkhot, P., Rojanasatien, S., Tadee, P., 2016. Salmonella in pork retail outlets and dissemination of its pulsotypes through pig production chain in Chiang Mai and surrounding areas, Thailand. Prev. Vet. Med.130, 99-105.

Rodriguez, A., Pangloli, P., Richards, H.A, Mount, J.R., Draughon, F.A., 2006. Prevalence of Salmonella in diverse environmental farm samples. J. Food. Prot. 69(11), 2576-2580.

Saha, G.K., Paul, A.K., Samad, M.A., Islam, M.A., Khan, M.S., 2013. Prevalence of Salmonella associated with goats in Bangladesh. Suranaree J. Sci. Technol. 21(3), 193-199.

Sodagari, H.R., Wang, P., Robertson, I., Habib, I., Sahibzada, S., 2020. Non-Typhoidal Salmonella at the Human-Food-of-Animal-Origin Interface in Australia. Animals (Basel). 10(7):1192.

Stokes, H.W., Nesbo, C.L., Holley, M.B., Bahl, M.I., Gillings, M.R., Boucher, Y., 2006. Class 1 integrons potentially predating the associationwithTn402-like transposition genes are present in a sediment microbial community. J. Bacteriol. 188, 5722-5730.

Techasaensiri, C., Radhakrishnan, A., Als, D., Thisyakorn, U., 2018. Typhoidal Salmonella Trends in Thailand. Am. J. Trop. Med. Hyg. 99(3), 64-71.

Teklu, A., Negussies, H., 2011. Assessment of Risk Factors and Prevalence of Salmonella in Slaughtered Small Ruminants and Environment in an Export Abattoir, Modjo, Ethiopia. American-Eurasian J. Agric.&Environ. Sci. 10(6), 992-999.

Umeh, S., Enwuru, C.P., 2014. Antimicrobial Resistance Profile of Salmonella Isolates from livestock. Open. J. Med. Microbiol. 4, 242-248.

United States Department of Agriculture [USDA], 2013. Foodborne illness cost calculator: Salmonella. Available from: http://www.ers.usda.gov/topics/food-safety/foodborne-illness/salm intro.asp. Retrieved on 20-12-2018.

Wang, X., Biswas, S., Paudyal, N., Pan, H., Li, X., Fang, W., Yue, M., 2019. Antibiotic resistance in Salmonella Typhimurium isolates recovered from the food chain through national antimicrobial resistance monitoring system between 1996 and 2016. Front. Microbiol. 10, 985.

WHO., 2013. Fact Sheet No. 139. Food Safety Department WHO/Geneva.

Zare, P., Ghorbani-Choboghlo, H., Jaberi, S., Razzaghi, S., Mirzae, M., Mafuni, K., 2014. Occurrence and antimicrobial resistance of Salmonella spp. and Escherichia coli isolates in apparently healthy slaughtered Cattle, Sheep and Goats in East Azarbaijan Province. Int. J. Enteric. Pathog. doi: 10.17795/ijep15451.

Zelalem, A., Nigatu, K., Zufan, W., Haile, G., Alehegne, Y., Tesfu, K., 2011. Prevalence and antimicrobial resistance of Salmonella isolated from lactating cows and in contact humans in dairy farms of Addis Ababa: a cross sectional study. BMC Inf. Dis. 11, 222.

Zewdu, E., Cornelius, P., 2009. Antimicrobial resistance pattern of Salmonella serotypes isolated from food items and workers in Addis Ababa, Ethiopia. Trop. Anim. Hlth. Pro. 41, 241-249.