Prevalence and molecular characterization of typhoidal and non-typhoidal Salmonella isolated from meat and environmental samples of retail shops of Lahore Punjab, Pakistan
DOI:
https://doi.org/10.12834/VetIt.2392.14037.1Keywords:
Prevalence, Zoonotic, Salmonella, Retail shopsAbstract
Non-typhoidal Salmonellae are important foodborne bacterial pathogens that can cause bacteremia, gastroenteritis, and subsequent infection. The aim of the study was to determine the prevalence of Salmonella in the live bird market and retail shops of Lahore (Pakistan). A total of 720 samples of chicken meat, chopping board, cages, hands, and transportation vans were collected. Salmonella was recovered from 103 (14.36%) samples. The highest prevalence (33.33%) was found in transportation van samples followed by chicken meat samples (17.26%). In the towns of Lahore, the highest prevalence was found in Samanabad Town (19%) followed by Data Ganj Bakhsh Town (17%) with the lowest in Gulberg Town (6.9%). Salmonella Typhimurium was most common (35.92%) followed by S. Enteritidis (25.24%), S. Dublin (14.56%), S. Gallinarum biovar Gallinarum (8.74%), and untyped Salmonella species (15.53%). This was the first baseline study of the prevalence of non-typhoidal Salmonella at the live bird market and retail shops of Lahore. Implementation of appropriate control measures is required at both the human side and poultry food production chain to reduce the burden and transmission of the zoonotic Salmonellae.
References
Abatcha M.G., Effarizah M.E. & Rusul G. 2018. Prevalence, antimicrobial resistance, resistance genes and class 1 integrons of Salmonella serovars in leafy vegetables, chicken carcasses and related processing environments in Malaysian fresh food markets. Food Control, 91, 170-180.
Abdi R.D., Mengstie F., Beyi A.F., Beyene T., Waktole H., Mammo B., Ayana D. & Abunna F. 2017. Determination of the sources and antimicrobial resistance patterns of Salmonella isolated from the poultry industry in Southern Ethiopia. BMC Infect Dis, 17, 352.
Acheson D. & Hohmann E.L. 2001. Nontyphoidal Salmonellosis. Clin Infect Dis, 32, 263-269.
Ak N.O., Cliver D.O. & Kaspar C.W. 1994. Cutting boards of plastic and wood contaminated experimentally with bacteria. J Food Protect, 57, 16-22.
Akhtar F., Hussain I. & Rahman S. U. 2010. Prevalence and Antibiogram Studies of Salmonella Enteritidis Isolated from Human and Poultry Sources. Pakistan Vet J, 30 (1), 25-28.
Alali W. Q., Gaydashov R., Petrova E., Panin A., Tugarinov O., Kulikovskii A., Mamleeva D., Walls I. & Doyle M. P. 2012. Prevalence of Salmonella on retail chicken meat in Russian Federation. J Food Protect, 75(8), 1469–1473.
Alvarez J., Sota M., Vivanco A. B., Perales I., Cisterna R., Rementeria A. & Garaizar J. 2004. Development of a multiplex PCR technique for detection and epidemiological typing of salmonella in human clinical samples. J Clin Microbiol, 42(4), 1734–1738.
Antunes P., Mourão J., Campos J. & Peixe L. 2016. Salmonellosis: the role of poultry meat. Clin Microbiol Infect, 22, 110-121.
Asif M., Rahman H. & Qasim M. 2017. Molecular detection and antimicrobial resistance profile of zoonotic Salmonella enteritidis isolated from broiler chickens in Kohat, Pakistan. Journal Chinese Medical Association, 80, 303-306.
Beach J.C., Murano E.A. & Acuff G.R. 2002. Prevalence of Salmonella and Campylobacter in Beef Cattle from Transport to Slaughter. J Food Protect, 65, 1687-1693.
Brunette G.W. 2017. CDC Yellow Book 2018: health information for international travel. Oxford University Press.
Corry J. E., Allen V. M., Hudson W. R., Breslin M. F. & Davies R. H. 2002. Sources of Salmonella on broiler carcasses during transportation and processing: modes of contamination and methods of control. J Appl Microbiol, 92(3), 424–432.
de Freitas C.G., Santana Â.P., da Silva P.H.C., Gonçalves V. S., Barros MdeA., Torres F. A., Murata L. S. & Perecmanis S. 2010. PCR multiplex for detection of Salmonella Enteritidis, Typhi and Typhimurium and occurrence in poultry meat. Int J Food Microbiol, 139, 15-22.
Delahoy M.J., Wodnik B., McAliley L., Penakalapati G., Swarthout J., Freeman M. C. & Levy K. 2018. Pathogens transmitted in animal feces in low- and middle-income countries. Int J Hyg Environ Health, 221, 661-676.
Devleesschauwer B., Haagsma J. A., Mangen M.-J. J., Lake R. J. & Havelaar A. H. 2018. The Global Burden of Foodborne Disease. In Food Safety Economics : Incentives for a Safer Food Supply (T.Roberts, Ed.). Springer, 107–122,
Donado-Godoy P., Clavijo V., León M., Tafur M. A., Gonzales S., Hume M., Alali W., Walls I., Lo Fo Wong D. M. & Doyle M. P. 2012. Prevalence of Salmonella on retail broiler chicken meat carcasses in Colombia. J Food Protect, 75(6), 1134–1138.
Ejo M., Garedew L., Alebachew Z. & Worku W. 2016. Prevalence and Antimicrobial Resistance of Salmonella Isolated from Animal-Origin Food Items in Gondar, Ethiopia. BioMed Res Int, 8, 4290506.
Gallegos-Robles M.A., Morales-Loredo A., Alvarez-Ojeda G., Osuna-García J. A., Martínez I. O., Morales-Ramos L. H. & Fratamico P. 2009. PCR detection and microbiological isolation of Salmonella spp. from fresh beef and cantaloupes. J Food Sci, 74(1), M37–M40.
Garedew L., Hagos Z., Addis Z., Tesfaye R. & Zegeye B. 2015. Prevalence and antimicrobial susceptibility patterns of Salmonella isolates in association with hygienic status from butcher shops in Gondar town, Ethiopia. Antimicrob Resist Infect Control, 4, 21.
Ha J. S., Seo K. W., Kim Y. B., Kang M. S., Song C. S. & Lee Y. J. 2018. Prevalence and characterization of Salmonella in two integrated broiler operations in Korea. Ir Vet J, 71, 3.
Hald B., Wedderkopp A. & Madsen M. 2000. Thermophilic Campylobacter spp. in Danish broiler production: a cross-sectional survey and a retrospective analysis of risk factors for occurrence in broiler flocks. Avian Pathol, 29, 123-131.
Jalil H., Hussain S. & Siddiqi A. 2013. An empirical study of meat supply chain and prices pattern in Lahore (Pakistan): A case study. Journal of Supply Chain Management Systems, 2, 1-10.
Jarquin C., Alvarez D., Morales O., Morales A. J., López B., Donado P., Valencia M. F., Arévalo A., Muñoz F., Walls I., Doyle M. P. & Alali W. Q. 2015. Salmonella on raw poultry in retail markets in Guatemala: Levels, antibiotic susceptibility, and serovar distribution. J Food Protect, 78, 1642-1650.
Joshua G. & Ali Z. 2011. Avian diversity with the varying urban congestions of Lahore. J Anim Plant Sci, 21, 421-482.
Khan A.S., Georges K., Rahaman S., Abdela W. & Adesiyun A. A. 2018. Prevalence and serotypes of Salmonella spp. on chickens sold at retail outlets in Trinidad. PloS one, 13, e0202108.
Lamas A., Fernandez-No I.C., Miranda J.M., Vázquez B., Cepeda A. & Franco C. M. 2016. Prevalence, molecular characterization and antimicrobial resistance of Salmonella serovars isolated from northwestern Spanish broiler flocks (2011–2015). Poultry Sci, 95, 2097-2105.
Li K, Ye S, Alali WQ, Wang Y., Wang X., Xia X. & Yang B. 2017. Antimicrobial susceptibility, virulence gene and pulsed-field gel electrophoresis profiles of Salmonella enterica serovar Typhimurium recovered from retail raw chickens, China. Food Control , 72, 36-42.
Luu Q. H., Fries R., Padungtod P., Tran T. H., Kyule M. N., Baumann M. P. & Zessin K. H. 2006. Prevalence of Salmonella in retail chicken meat in Hanoi, Vietnam. Ann N Y Acad Sci, 1081, 257-261.
McCrea B. A., Tonooka K. H., VanWorth C., Boggs C. L., Atwill E. R. & Schrader J. S. 2006. Prevalence of Campylobacter and Salmonella species on farm, after transport, and at processing in specialty market poultry. Poultry Sci, 85(1), 136–143.
Nguyen D.T.A., Kanki M., Nguyen P.D., Le H. T., Ngo P. T., Tran D. N., Le N. H., Dang C. V., Kawai T., Kawahara R., Yonogi S., Hirai Y., Jinnai M., Yamasaki S., Kumeda Y. & Yamamoto Y. 2016. Prevalence, antibiotic resistance, and extended-spectrum and AmpC β-lactamase productivity of Salmonella isolates from raw meat and seafood samples in Ho Chi Minh City, Vietnam. Int J Food Microbiol, 236, 115-122.
Nidaullah H, Abirami N, Shamila-Syuhada AK, Chuah L.O., Nurul H., Tan T. P., Abidin F. W. Z. & Rusul G. 2017. Prevalence of Salmonella in poultry processing environments in wet markets in Penang and Perlis, Malaysia. Vet World, 10, 286-292.
Nisar M., Ahmad M. U. D., Mushtaq M. H., Shehzad W., Hussain A., Nasar M., Nagaraja K. V. & Goyal S. M. 2018. Occurrence of Campylobacter in retail meat in Lahore, Pakistan. Acta Trop, 185, 42–45.
Okareh O. & Erhahon O. 2015. Microbiological assessment of food and hand-swabs samples of school food vendors in Benin City, Nigeria. Food Public Health, 5, 23-28.
Phan T. T., Khai L. T., Ogasawara N., Tam N. T., Okatani A. T. Akiba M. & Hayashidani H. 2005. Contamination of Salmonella in retail meats and shrimps in the Mekong Delta, Vietnam. J Food Prot, 68(5), 1077–1080.
Shafini A., Son R., Mahyudin N., Rukayadi Y. & Tuan Zainazor T.C. 2017. Prevalence of Salmonella spp. in chicken and beef from retail outlets in Malaysia. Int Food Res J, 24, 437.
Shang K., Wei B., Jang H.-K. & Kang M. 2019. Phenotypic characteristics and genotypic correlation of antimicrobial resistant (AMR) Salmonella isolates from a poultry slaughterhouse and its downstream retail markets. Food Control, 100, 35-45.
Sharma J., Kumar D., Hussain S., Pathak A., Shukla M., Prasanna Kumar V., Anisha P.N., Rautela R., Upadhyay A.K. & Singh S.P. 2019. Prevalence, antimicrobial resistance and virulence genes characterization of nontyphoidal Salmonella isolated from retail chicken meat shops in Northern India. Food Control, 102, 104-111.
Soomro A.H., Khaskheli M., Bhutto B., Shah G. , Memon A. & Dewan P. 2010. Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry meat in Hyderabad, Pakistan. Turk J Vet Anim Sci, 34(5), 455-460.
Stegniy B., Gerilovych A., Arefyev V., Glebova K. & Potkonjak A. 2014. A method for detecting and typing of Salmonella by multiplex PCR. Arhiv Veterinarske Medicine, 7, 47-56.
Suresh T., Hatha A.M., Srinivasan D., Srinivasan S. & Lakshmanaperumalsamy P. 2004. Salmonella cross-contamination in retail chicken outlets and the efficacy of spice extracts on Salmonella enteritidis growth inhibition on various surfaces et al., 2004. Salmonella cross-contamination in retail chicken outlets and the efficacy of spice extracts on Salmonella enteritidis growth inhibition on various surfaces. Microbes Environments, 19, 286-291.
Ta Y.T., Nguyen T.T. & To P.B. 2012. Prevalence of Salmonella on Chicken Carcasses from Retail Markets in Vietnam. J Food Prot, 75, 1851-1854.
Ta Y.T., Nguyen T.T. & To P.B. 2014. Quantification, serovars, and antibiotic resistance of Salmonella isolated from retail raw chicken meat in Vietnam. J Food Prot, 77, 57-66.
Tabo D.A., Diguimbaye C.D. & Granier S.A. 2013. Prevalence and antimicrobial resistance of non-typhoidal Salmonella serotypes isolated from laying hens and broiler chicken farms in N'Djamena, Chad. Vet Microbiol, 166, 293-298.
Uddin M.N., Farooq M.M. & Waqas M. 2018. Antibiotic assays of Salmonella isolated from poultry chicken of various locations in districts Swat. Pure Appl Biol, 7, 78-84.
Van T.T.H., Moutafis G., Istivan T., Tran L. T. & Coloe P. J 2007. Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Appl Environ Microbiol, 73, 6885-6890.
