journal article·2022-03-10Open access

Virulence Factors and Antimicrobial Resistance in Salmonella Species Isolated from Retail Beef in Selected KwaZulu-Natal Municipality Areas, South Africa

Serisha Naidoo, Patrick Butaye, Tsolanku S. Maliehe, Kudakwashe Magwedere, Albert K. Basson, Evelyn Madoroba

Applied Sciences· Volume 12· Issue 6

Abstract

Salmonellosis and antimicrobial resistance caused by non-typhoidal Salmonella are public health concerns. This study aimed at determining prevalence, serovars, virulence factors and antimicrobial resistance of Salmonella from beef products. Four-hundred beef samples from 25 retail outlets in KwaZulu-Natal, South Africa were analyzed for Salmonella using standard methods, confirmation with matrix-assisted laser desorption ionization–time of flight and serotyping according to the White–Kauffmann–Le Minor scheme. The Kirby Bauer disk diffusion method was used to determine antimicrobial resistance against Cefotaxime, Kanamycin, Ampicillin, Amoxicillin, Trimethoprim Sulfamethoxazole, Ciprofloxacin, Chloramphenicol, Gentamicin Cefoxitin and Tetracycline. A polymerase chain reaction was performed to detect invA, agfA, lpfA, hilA, sivH, sefA, sopE, and spvC virulence genes. Salmonella was observed in 1.25% (5/400) of the samples. Four serovars (Enteritidis, Hadar, Heidelberg, Stanley) were identified. Almost all Salmonella were susceptible to all antimicrobials except S. Enteritidis isolate that was resistant to Tetracycline, Ampicillin and Amoxicillin. All Salmonella isolates carried at least two virulence factors. The findings indicate low Salmonella prevalence in meat from selected KZN retail beef; however, routine surveillance to monitor risk associated with virulence factors is required to mitigate potential outbreaks. The resistant S. Enteritidis highlights a need to routinely monitor antimicrobial resistance in order to enhance human health.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Salmonella and Campylobacter epidemiology · Antibiotic Resistance in Bacteria · Vibrio bacteria research studies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Biochemistry and Microbiology, University of Zululand, Private Bag X1001, KwaDlangezwa 3886, South Africa

Department of Pathobiology, Pharmacology and Zoological Medicine, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, B9820 Merelbeke, Belgium

Department of Biomedical Sciences, Ross University School of Veterianry Medicine, Basseterre 00334, Saint Kitts and Nevis

Directorate of Veterinary Public Health, Department of Agriculture, Land Reform and Rural Development, Pretoria 0001, South Africa

Funding

Red Meat Research and Development South Africa (RMRDSA) and the Department of Trade and Industry - Technology and Human Resource for Industry Programme (DTI - THRIP).

References (43)

Show source-provided references
1. Ferede, B. (2014). Isolation, Identification, Antimicrobial Susceptibility Test and Public Awareness of Salmonella on Raw Goat Meat at Dire Dawa Municipal Abattoir, Eastern Ethiopia. [Master’s Thesis, Addis Ababa University].
2. Gilchrist, J.J., and Maclennan, C.A. (2019). Invasive Nontyphoidal Salmonella Disease in Africa. EcoSal Plus, 8.10.1128/ecosalplus.esp-0007-2018 ↗
3. Keddy, K. (2016). Non typhoidal Salmonella and the African growth and opportunity act. Commun. Dis. Surveill. Bull., 14.
4. Outbreaks of Salmonella enteritidis infections in the United States, 1985–199110.1093/infdis/169.3.547 ↗
5. Quantitative distribution of Salmonella spp. and Escherichia coli on beef carcasses and raw beef at retail establishments10.1016/j.ijfoodmicro.2015.06.016 ↗
6. Salmonella serotypes isolated from minced meat beef, mutton and pork in Addis Ababa, Ethiopia
7. Occurrence, serotype diversity, and antimicrobial resistance of Salmonella in ground beef at retail stores in Jalisco State, Mexico10.4315/0362-028X.JFP-13-109 ↗
8. Siddiky, N.A., Sarker, M.S., Khan, M., Begum, R., Kabir, M.E., Karim, M.R., Rahman, M.T., Mahmud, A., and Samad, M.A. (2021). Virulence and Antimicrobial Resistance Profiles of Salmonella enterica Serovars Isolated from Chicken at Wet Markets in Dhaka, Bangladesh. Microorganisms, 9.10.3390/microorganisms9050952 ↗
9. Embracing diversity: Differences in virulence mechanisms, disease severity, and host adaptations contribute to the success of nontyphoidal Salmonella as a foodborne pathogen10.3389/fmicb.2019.01368 ↗
10. Evolution of Salmonella-host cell interactions through a dynamic bacterial genome10.3389/fcimb.2017.00428 ↗
11. Salmonella pathogenicity islands: Big virulence in small packages10.1016/S1286-4579(00)00273-2 ↗
12. Festa, R., Ambrosio, R.L., Lamas, A., Gratino, L., Palmieri, G., Franco, C.M., Cepeda, A., and Anastasio, A. (2021). A study on the antimicrobial and antibiofilm peptide 1018-K6 as potential alternative to antibiotics against food-pathogen Salmonella enterica. Foods, 10.10.3390/foods10061372 ↗
13. Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984–200210.3201/eid1106.041231 ↗
14. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance10.14202/vetworld.2019.504-521 ↗
15. (2020, January 22). DAFF Trends in the Agricultural Sector, Available online: https://www.daff.gov.za/Daffweb3/Portals/0/Statistics%20and%20Economic%20Analysis/Statistical%20Information/Trends%20in%20the%20Agricultural%20Sector%202017.pdf.
16. Kau, J.S. (2016). The growth prospects of the South African beef industry in an uncertain socio-economic environment. Annual Beef Bulletin, Department of Agriculture, Forestry and Fisheries.
17. Molecular detection of multidrug-resistant Salmonella isolated from livestock production systems in South Africa10.2147/IDR.S211618 ↗
18. How to calculate sample size for different study designs in medical research?10.4103/0253-7176.116232 ↗
19. Käsbohrer, A., Bernd-Alois, T., Appel, B., and Fetsch, A. (2010). Development of Harmonised Survey Methods for Food-Borne Pathogens in Foodstuffs in the European Union, European Food Safety Authority.10.2903/sp.efsa.2010.EN-83 ↗
20. (2017). Microbiology of the Food Chain–Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella–Part 1: Detection of Salmonella spp. (Standard No. EN ISO 6579-1).
21. Rapid classification and identification of Salmonellae at the species and subspecies levels by whole-cell matrix-assisted laser desorption ionization–time of flight mass spectrometry10.1128/AEM.01402-08 ↗
22. Grimont, P.A.D., and Weill, F.X. (2007). Antigenic Formulae of the Salmonella Serovars, World Health Organization Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur. [9th ed.].
23. Salmonella contamination, serovars and antimicrobial resistance profiles of cattle slaughtered in South Africa10.4102/ojvr.v83i1.1109 ↗
24. (2021, November 11). American Society of Microbiology 2016. Available online: https://asm.org/getattachment/2594ce26-bd44-47f6-8287-0657aa9185ad/Kirby-Bauer-Disk-Diffusion-Susceptibility-Test-Protocol-pdf.pdf.
25. CLSI (2017). CLSI Supplement M100: Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [27th ed.].
26. Amplification of invA gene of Salmonella by polymerase chain reaction (PCR) as a specific method for detection of Salmonella
27. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella Typhimurium10.1128/jb.177.8.2087-2097.1995 ↗
28. PCR detection of Salmonella enterica serotype Montevideo in and on raw tomatoes using primers derived from hilA10.1128/AEM.66.12.5248-5252.2000 ↗
29. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype Typhimurium: Identification of intestinal colonization and persistence determinants10.1128/IAI.71.2.629-640.2003 ↗
30. Detection and identification of Salmonella from poultry-related samples by PCR10.1016/S0378-1135(02)00028-7 ↗
31. Molecular properties of Salmonella enterica serotype Paratyphi B distinguish between its systemic and its enteric pathovars10.1128/JCM.41.9.4270-4278.2003 ↗
32. Virulence determinants invA and spvC in Salmonellae isolated from poultry products, wastewater, and human sources10.1128/aem.62.10.3768-3771.1996 ↗
33. Madoroba, E., Magwedere, K., Chaora, N.S., Matle, I., Muchadeyi, F., Mathole, M.A., and Pierneef, R. (2021). Microbial communities of meat and meat products: An exploratory analysis of the product quality and safety at selected enterprises in South Africa. Microorganisms, 9.10.3390/microorganisms9030507 ↗
34. Prevalence of Salmonellae on beef products at butcheries and their antibiotic resistance profiles10.1111/j.1365-2621.2000.tb13604.x ↗
35. Prevalence and antibiotic-resistance of Salmonella isolated from beef sampled from the slaughterhouse and from retailers in Dakar (Senegal)10.1016/j.ijfoodmicro.2006.04.018 ↗
36. Prevalence of Salmonella enterica and the hygienic indicator Escherichia coli in raw meat at markets in Ouagadougou, Burkina Faso10.4315/0362-028X.JFP-11-124 ↗
37. Peruzy, M.F., Capuano, F., Proroga, Y.T.R., Cristiano, D., Carullo, M.R., and Murru, N. (2020). Antimicrobial susceptibility testing for salmonella serovars isolated from food samples: Five-year monitoring (2015–2019). Antibiotics, 9.10.3390/antibiotics9070365 ↗
38. Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance10.1128/MMBR.65.2.232-260.2001 ↗
39. Isolation and molecular characterization of virulence-associated genes of Salmonella from buffalo meat samples in Western Region of India
40. Multicenter Validation of the Analytical Accuracy of Salmonella PCR: Towards an International Standard10.1128/AEM.69.1.290-296.2003 ↗
41. Amplification of an invA gene sequence of Salmonella Typhimurium by polymerase chain reaction as a specific method of detection of Salmonella10.1016/0890-8508(92)90002-F ↗
42. Cloning and molecular characterization of genes whose products allow Salmonella Typhimurium to penetrate tissue culture cells10.1073/pnas.86.16.6383 ↗
43. Distribution of the invA, -B, -C, and -D genes of Salmonella Typhimurium among other Salmonella serovars: invA mutants of Salmonella typhi are deficient for entry into mammalian cells10.1128/iai.59.9.2901-2908.1991 ↗