Frequency, serotyping, antibiogram, and seasonality of Salmonella isolated from red meat markets

Submitted: 27 March 2024
Accepted: 23 April 2024
Published: 4 June 2024
Abstract Views: 3491
PDF: 3495
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Bacterial pathogenic strains are as adaptable as Salmonella strains and cause diverse intestinal and extraintestinal diseases in humans and other mammals worldwide. Red meat and its products are important hosts for many zoonotic diseases. This work was designed to investigate the frequency, serotypes, and antimicrobial resistance profile of isolated Salmonella spp. in red meat (cattle, sheep, and goats) sold in Dhamar Governorate, Yemen. A total of 250 red meat samples were collected from the retail seller market between July and December 2022. All samples were transported immediately to the laboratory, subcultured on selective enrichment agar, and identified by serotyping and antimicrobial susceptibility tests via disk diffusion methods. The results indicated 26 positive samples of Salmonella out of the 250 samples (10.4%). Notably, isolates belong to ten various serotypes: S. Typhimurium 19.2%, S. Anatum 15.4%, S. Newport 11.5%, S. Enteritidis 11.5%, S. Muenchen 11.5%, S. Infantis 7.7%, S. Montevideo 7.7%, S. Dublin 7.7%, S. Senftenberg 3.9%, and S. Arizona 3.9%. The antibiotic resistance profile revealed that 57.5%, 53.9%, and 53.9% of isolates are resistant to erythromycin, tetracycline, and norfloxacin, respectively. This resistance among Salmonella spp. suggests a significant threat to health, which will in turn require an active safety measure and response. On the other hand, the seasonal variations “August and July” were found to be associated with an increased frequency of Salmonella isolation.

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AAP, 2024. Red book online outbreaks: salmonella outbreak linked to charcuterie meats. Available from: https://publications.aap.org/redbook/resources/28764/Red-Book-Online-Outbreaks-Salmonella-Outbreak.
Al-Gamal E, Saeed SB, Victor A, Long T, 2019. Prolonged grief disorder and its relationship with perceived social support and depression among university students. J Psychosoc Nurs Ment Health Serv 57:44-51. DOI: https://doi.org/10.3928/02793695-20181023-03
Al-Khadher A, 2015. Prevalence of Salmonella in human and foods of animal origin with antibiotic resistance patterns of isolated bacteria in Dhamar governorate , Yemen. Yemeni J of Agric Vet Sci 1.
Alfama ERG, Hessel CT, De Oliveira Elias S, Magalhães CRP, Santiago MFT, Anschau M, Tondo EC, 2019. Assessment of temperature distribution of cold and hot meals in food services and the prediction growth of Salmonella spp. and Listeria monocytogenes. Food Control 106:106725. DOI: https://doi.org/10.1016/j.foodcont.2019.106725
Almashhadany DA, Ba-Salamah HA, Shater AR, Al Sanabani AS, Abd Al Galil F, 2016. Prevalence of Listeria monocytogenes in red meat in Dhamar Governorate/Yemen. Int J Med Health Res 2:73-8.
Almashhadany DA, 2019. Occurrence and antimicrobial susceptibility of Salmonella isolates from grilled chicken meat sold at retail outlets in Erbil City, Kurdistan region, Iraq. Ital J Food Saf 8:8233. DOI: https://doi.org/10.4081/ijfs.2019.8233
Almashhadany DA 2021. Meat-borne diseases. In: Ranabhat CL. Meat and nutrition. IntechOpen, London.
Almashhadany DA, Osman AA, 2019. Isolation, serotyping, and antibiogram of Salmonella isolates from raw milk sold at retail vending in Erbil city, Iraq. Bulletin UASVM Animal Sci Biotechnol 76:116-22. DOI: https://doi.org/10.15835/buasvmcn-asb:0020.19
Almashhadany DA, Mayas SM, Ali NL, 2022a. Isolation and identification of Helicobacter pylori from raw chicken meat in Dhamar Governorate, Yemen. Ital J Food Saf 11:10220. DOI: https://doi.org/10.4081/ijfs.2022.10220
Almashhadany DA, Zefenkey ZF, Odhah MNA, 2022b. Epidemiological study of human brucellosis among febrile patients in Erbil-Kurdistan region, Iraq. J Infect Dev Ctries 16:1185-90. DOI: https://doi.org/10.3855/jidc.15669
Ammar A, Abdeen E, Abo‐Shama U, Fekry E, Kotb Elmahallawy E, 2019. Molecular characterization of virulence and antibiotic resistance genes among Salmonella serovars isolated from broilers in Egypt. Lett Appl Microbiol 68:188-95. DOI: https://doi.org/10.1111/lam.13106
Balasubramanian R, Im J, Lee J-S, Jeon HJ, Mogeni OD, Kim JH, Rakotozandrindrainy R, Baker S, Marks F, 2019. The global burden and epidemiology of invasive non-typhoidal Salmonella infections. Human Vaccin Immunother 15:1421-6. DOI: https://doi.org/10.1080/21645515.2018.1504717
Ballout R, Toufeili I, Kharroubi SA, Kassem II, 2023. Raw meat consumption and food safety challenges: a survey of knowledge, attitudes, and practices of consumers in Lebanon. Foods 13:118. DOI: https://doi.org/10.3390/foods13010118
Bell RL, Jarvis KG, Ottesen AR, McFarland MA, Brown EW, 2016. Recent and emerging innovations in Salmonella detection: a food and environmental perspective. Microb Biotechnol 9:279-92. DOI: https://doi.org/10.1111/1751-7915.12359
Bosilevac JM, Gassem MA, Al Sheddy IA, Almaiman SA, Al-Mohizea IS, Alowaimer A, Koohmaraie M. Prevalence of Escherichia coli O157:H7 and Salmonella in camels, cattle, goats, and sheep harvested for meat in Riyadh. J Food Prot 2015;78:89-96. DOI: https://doi.org/10.4315/0362-028X.JFP-14-176
CDC, 2024. Salmonella. Investigation details. Available from: https://www.cdc.gov/salmonella/charcuterie-meats-01-24/details.html.
Chlebicz A, Śliżewska K, 2018. Campylobacteriosis, salmonellosis, yersiniosis, and listeriosis as zoonotic foodborne diseases: a review. Int J Environ Res Public Health 15:863. DOI: https://doi.org/10.3390/ijerph15050863
Coburn B, Grassl GA, Finlay B, 2007. Salmonella, the host and disease: a brief review. Immunol Cell Biol 85:112-8. DOI: https://doi.org/10.1038/sj.icb.7100007
DOH, 2024. 2024 Salmonella multistate outbreak linked to Italian-style charcuterie meats. Available from: https://doh.wa.gov/you-and-your-family/illness-and-disease-z/foodborne-illness/outbreaks/2024-salmonella-charcuterie-meats.
Doyle MP, Loneragan GH, Scott HM, Singer RS, 2013. Antimicrobial resistance: challenges and perspectives. Compr Rev Foof Sci Food Saf 12:234-48. DOI: https://doi.org/10.1111/1541-4337.12008
El-Bagoury N, Ahmed SI, Ahmed Abu Ali O, El-Hadad S, Fallatah AM, Mersal G, Ibrahim MM, Wysocka J, Ryl J, Boukherroub R, 2019. The influence of microstructure on the passive layer chemistry and corrosion resistance for some titanium-based alloys. Materials 12:1233. DOI: https://doi.org/10.3390/ma12081233
Elsayed MM, El-Basrey FH, El-Baz AH, Dowidar HA, Shami A, Al-Saeed FA, Alsamghan A, Salem HM, Alhazmi WA, El-Tarabily KA, Khedr HE, 2024. Ecological prevalence, genetic diversity, and multidrug resistance of Salmonella enteritidis recovered from broiler and layer chicken farms. Poultry Sci 103:103320. DOI: https://doi.org/10.1016/j.psj.2023.103320
El-Prince E, Hussein MF, Abd El-Rahman AM, 2019. Incidence of Salmonella species in table eggs and some egg-based products. JAVR 9:1-7.
Eng SK, Pusparajah P, Ab Mutalib NS, Ser H-L, Chan KG, Lee LH, 2015. Salmonella: a review on pathogenesis, epidemiology, and antibiotic resistance. Front Life Sci 8:284-93. DOI: https://doi.org/10.1080/21553769.2015.1051243
Fatima A, Saleem M, Nawaz S, Khalid L, Riaz S, Sajid I, 2023. Prevalence and antibiotics resistance status of Salmonella in raw meat consumed in various areas of Lahore, Pakistan. Scientific Reports 13:22205. DOI: https://doi.org/10.1038/s41598-023-49487-2
Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F, 2018. Biofilms in the food industry: health aspects and control methods. Front MicrobioL 9:898. DOI: https://doi.org/10.3389/fmicb.2018.00898
Garba B, Habibullah S, Saidu B, Suleiman N, 2019. Effect of mastitis on some hematological and biochemical parameters of Red Sokoto goats. Vet World 12:572-7. DOI: https://doi.org/10.14202/vetworld.2019.572-577
Garba B, Salihu M, Saidu B, Rambo U, 2020. Health hazards of abattoir effluents discharged from the Sokoto central abattoir, Nigeria. Sokoto J Vet Sci 18:47-52. DOI: https://doi.org/10.4314/sokjvs.v18i1.7
González-Santamarina B, García-Soto S, Hotzel H, Meemken D, Fries R, Tomaso H, 2021. Salmonella Derby: a comparative genomic analysis of strains from Germany. Front Microbiol 12:591929. DOI: https://doi.org/10.3389/fmicb.2021.591929
Granato D, Putnik P, Kovačević DB, Santos JS, Calado V, Rocha RS, Cruz AGD, Jarvis B, Rodionova OY, Pomerantsev A, 2018. Trends in chemometrics: food authentication, microbiology, and effects of processing. Compr Revi Food Sci Food Saf 17:663-77. DOI: https://doi.org/10.1111/1541-4337.12341
Hanoun AT, Al-Samrraae IaA, 2019. Isolation and identification of Escherichia coli and Salmonella typhimurium from sheep in Baghdad city. Iraqi J Vet Med 43:124-9. DOI: https://doi.org/10.30539/iraqijvm.v43i1.482
Hawwas HAEH, Aboueisha AKM, Fadel HM, El‑Mahallawy HS, 2022. Salmonella serovars in sheep and goats and their probable zoonotic potential to humans in Suez Canal Area, Egypt. Acta Vet Scand 64:17. DOI: https://doi.org/10.1186/s13028-022-00637-y
Heikinheimo A, Lindström M, Granum PE, Korkeala H, 2006. Humans as a reservoir for enterotoxin gene–carrying Clostridium perfringens type A. Emerg Infect Dis 12:1724-9. DOI: https://doi.org/10.3201/eid1211.060478
Hohmann EL, 2001. Nontyphoidal salmonellosis. Clin Infect Dis 32:263-9. DOI: https://doi.org/10.1086/318457
Hugho EA, Kumburu HH, Thomas K, Lukambagire AS, Hald T, Mmbaga BT, 2024. High diversity of Salmonella spp. from children with diarrhea, food, and environmental sources in Kilimanjaro–Tanzania: one health approach. Front Microbiol 14:1277019. DOI: https://doi.org/10.3389/fmicb.2023.1277019
Judd M, Hoekstra R, Mahon B, Fields P, Wong K, 2019. Epidemiologic patterns of human Salmonella serotype diversity in the USA, 1996–2016. Epidemiol Infect 147:e187. DOI: https://doi.org/10.1017/S0950268819000724
Kadry M, Nader SM, Dorgham SM, Kandil MM, 2019. Molecular diversity of the invA gene obtained from human and egg samples. Vet World 12:1033-8. DOI: https://doi.org/10.14202/vetworld.2019.1033-1038
Kassaye BK, Hassen DJ, Leja KA, 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 Veterinar Sci Technol 6:268. DOI: https://doi.org/10.4172/2157-7579.1000268
Little C, Richardson J, Owen R, De Pinna E, Threlfall E, 2008. Campylobacter and Salmonella in raw red meats in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003-2005. Food Microbiol 25:538-43. DOI: https://doi.org/10.1016/j.fm.2008.01.001
Liu H, Whitehouse CA, Li B, 2018. Presence and persistence of Salmonella in water: the impact on microbial quality of water and food safety. Front Public Health 6:159. DOI: https://doi.org/10.3389/fpubh.2018.00159
Mikoleit M, 2010. WHO global foodborne infections network. A WHO network building capacity to detect, control, and prevent foodborne and other enteric infections from farm to table” laboratory protocol: “isolation of Salmonella and Shigella from Faecal specimens”. Enteric diseases laboratory branch, Centers for Disease Control and Prevention. Atlanta, GA.
Mir IA, Kashyap SK, Maherchandani S, 2015. Isolation, serotype diversity and antibiogram of Salmonella enterica isolated from different species of poultry in India. Asian Pac J Trop Biomed 5:561-7. DOI: https://doi.org/10.1016/j.apjtb.2015.03.010
Musawa AI, Bashiru G, Al-Rasheed A, Yakubu Y, Jibril AH, Ballah FM, Sidi S, Lawal N, Bala JA, Odhah MN, Muhammad N, Umar M, 2021. Prevalence and antimicrobial susceptibility profiling of salmonella isolated from poultry products sold in sokoto metropolis, Nigeria. J Anim Health Prod 9:148-55. DOI: https://doi.org/10.17582/journal.jahp/2021/9.2.148.155
Nair A, Balasaravanan T, Malik SS, Mohan V, Kumar M, Vergis J, Rawool DB, 2015. Isolation and identification of Salmonella from diarrheagenic infants and young animals, sewage waste, and fresh vegetables. Vet World 8:669-73. DOI: https://doi.org/10.14202/vetworld.2015.669-673
Ngogo FA, Joachim A, Abade AM, Rumisha SF, Mizinduko MM, Majigo MV, 2020. Factors associated with Salmonella infection in patients with gastrointestinal complaints seeking health care at regional hospital in Southern Highland of Tanzania. BMC Infect Dis 20:135. DOI: https://doi.org/10.1186/s12879-020-4849-7
Peruzy MF, La Tela I, Carullo MR, Ioele S, Proroga YTR, Balestrieri A, Murru N, 2023. Occurrence and distribution of Salmonella serovars associated with human infection isolated from irrigation waters and food-producing animals in southern Italy: eleven-year monitoring (2011-2021). Ital J Food Saf 12:11538. DOI: https://doi.org/10.4081/ijfs.2023.11538
Reda M, Mohamed S, 2014. Bacteriological studies of Salmonella typhimurium isolated from cow calves and lambs. Assiut Vet Med J 60:47-53. DOI: https://doi.org/10.21608/avmj.2014.170521
Regalado-Pineda ID, Rodarte-Medina R, Resendiz-Nava CN, Saenz-Garcia CE, Castañeda-Serrano P, Nava GM, 2020. Three-year longitudinal study: prevalence of Salmonella enterica in chicken meat is higher in supermarkets than in wet markets from Mexico. Foods 9:264. DOI: https://doi.org/10.3390/foods9030264
Sahu C, Jain V, Mishra P, Prasad KN, 2018. Clinical and laboratory standards institute versus European committee for antimicrobial susceptibility testing guidelines for interpretation of carbapenem antimicrobial susceptibility results for Escherichia coli in urinary tract infection (UTI). J Lab Physicians 10:289-93. DOI: https://doi.org/10.4103/JLP.JLP_176_17
Serter B, Önen A, Ilhak OI, 2024. Antimicrobial efficacy of postbiotics of lactic acid bacteria and their effects on food safety and shelf life of chicken meat. Ann Animal Sci 24:277-87. DOI: https://doi.org/10.2478/aoas-2023-0081
Shmeleva E, 2020. The influence of climate change on the spread of human salmonellosis (mini-review). Acta Agraria Kaposváriensis 24:89-107. DOI: https://doi.org/10.31914/aak.2492
Silva JL, Vieira BS, Carvalho FT, Carvalho RC, Figueiredo EE, 2021. Salmonella behavior in meat during cool storage: a systematic review and meta-analysis. Animals 12:2902. DOI: https://doi.org/10.3390/ani12212902
Smith JL, 2017. Infectious dose and an aging population: susceptibility of the aged to foodborne pathogens. In: Gurtler JB, Doyle MP, Kornacki JL, eds. Foodborne pathogens: virulence factors and host susceptibility. Springer, Cham, Switezerland, pp 451-68. DOI: https://doi.org/10.1007/978-3-319-56836-2_16
Soufi L, Sáenz Y, De Toro M, Salah Abbassi M, Rojo-Bezares B, Vinué L, Bouchami O, Touati A, Ben Hassen A, Hammami S, 2012. Phenotypic and genotypic characterization of Salmonella enterica recovered from poultry meat in Tunisia and identification of new genetic traits. Vector Borne Zoonotic Dis 12:10-6. DOI: https://doi.org/10.1089/vbz.2011.0667
Su L-H, Chiu C-H, Chu C, Ou JT, 2004. Antimicrobial resistance in non typhoid Salmonella serotypes: a global challenge. Clin Infect Dis 39:546-51. DOI: https://doi.org/10.1086/422726
Tadesse G, Gebremedhin EZ, 2015. Prevalence of Salmonella in raw animal products in Ethiopia: a meta-analysis. BMC Res Notes 8:163. DOI: https://doi.org/10.1186/s13104-015-1127-7
Taha RR, Alghalibi SM, Saeedsaleh MG, 2013. Salmonella spp. in patients suffering from enteric fever and food poisoning in Thamar city, Yemen. East Mediterr Health J 19:88-93. DOI: https://doi.org/10.26719/2013.19.1.88
Tan SJ, Nordin S, Esah EM, Mahror N, 2022. Salmonella spp. in chicken: prevalence, antimicrobial resistance, and detection methods. Microbiol Res 13:691-705. DOI: https://doi.org/10.3390/microbiolres13040050
Van Duijkeren E, Wannet W, Heck M, Van Pelt W, Van Oldruitenborgh-Oosterbaan MS, Smit J, Houwers D, 2002. Sero types, phage types, and antibiotic susceptibilities of Salmonella strains isolated from horses in the Netherlands from 1993 to 2000. Vet Microbiol 86:203-12. DOI: https://doi.org/10.1016/S0378-1135(02)00007-X
Woldemariam E, Molla B, Alemayehu D, Muckle A, 2005. Prevalence and distribution of Salmonella in apparently healthy slaughtered sheep and goats in Debre Zeit, Ethiopia. Small Ruminant Res 58:19-24. DOI: https://doi.org/10.1016/j.smallrumres.2004.08.008
Xu Z, Wang M, Zhou C, Gu G, Liang J, Hou X, Wang M, Wei P, 2020. Prevalence and antimicrobial resistance of retail-meat-borne Salmonella in southern China during the years 2009–2016: the diversity of contamination and the resistance evolution of multidrug-resistant isolates. Int J Food Microbiol 333:108790. DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108790
Yang X, Huang J, Zhang Y, Liu S, Chen L, Xiao C, Zeng H, Wei X, Gu Q, Li Y, Wang J, Ding Y, Zhang J, Wu Q, 2020. Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. Sci Total Environ 713:136385. DOI: https://doi.org/10.1016/j.scitotenv.2019.136385

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1.
Almashhadany DA, Mohammed SH, Mala SF, Ahmed Odhah MN, Jalil Ahmood AA. Frequency, serotyping, antibiogram, and seasonality of <i>Salmonella</i> isolated from red meat markets. Ital J Food Safety [Internet]. 2024 Jun. 4 [cited 2024 Jul. 25];. Available from: https://www.pagepressjournals.org/ijfs/article/view/12521