Prevalence of Salmonella spp. in Egyptian dairy products: molecular, antimicrobial profiles and a reduction trial using d-tryptophan
- 47 Downloads
The study aims to determine the prevalence and serotypes of Salmonella spp. in milk and dairy products sold on Egyptian markets, characterize their virulence-associated genes, and assess their antimicrobial profile. Furthermore, d-tryptophan was used as a new approach for controlling the growth of Salmonella in combination with heat stress. A total of 125 samples (raw market milk, bulk tank milk, Kareish cheese, white soft cheese, and small scale ice cream, 25 each) were used for assessing the prevalence of Salmonella spp. Nine Salmonella isolates with different serotypes were recovered from bulk tank milk (4/9; 44.44%) and Kariesh cheese (5/9; 55.55%), respectively. Antimicrobial susceptibility testing indicated that all isolates were resistant to streptomycin and erythromycin. PCR analysis revealed that 100%, 66.67% and 88.89% of the obtained isolates possessed invA, avrA and stn genes, respectively. d-Tryptophan (40 mM) in combination with heat stress had a significant inhibitory effect on Salmonella enterica subsp. enterica serovar Typhimurium (S. Typhimurium) added to control milk samples. The results indicate insufficient hygienic measures adopted during handling by dairies in Egypt. Therefore, strict hygienic approaches are recommended during milking, processing and distribution of dairy products in Egypt. A synergistic effect of d-tryptophan and heat stress is considered as a promising tool for controlling growth of Salmonella in milk.
KeywordsAntimicrobial profile Dairy products d-Tryptophan Heat stress Salmonella spp.
This work was supported by Egypt–Japan Education Partnership “EJEP”.
- Ben-Barak Z, Streckel W, Yaron S, Cohen S, Prager R, Tschäpe H (2006) The expression of the virulence-associated effector protein gene avrA is dependent on a Salmonella enterica specific regulatory function. J Med Microbiol 296:25–38. https://doi.org/10.1016/j.ijmm.2005.08.004 CrossRefGoogle Scholar
- Cody SH, Abbott SL, Marfin AA, Schulz B, Wagner P, Robbins K, Boetani JC, Vugia DJ (1999) Two outbreaks of multidrug-resistant Salmonella serotype typhimurium DT104 infections linked to raw-milk cheeses in north California. JAMA 19:1085–1089Google Scholar
- Corte FV, De Fabrizio SV, Salvatori DM, Alzamora SM (2004) Survival of Listeria innocua in apple juice as affected by vanillin or potassium sorbate. J Food Saf 24:1–15. https://doi.org/10.1111/j.1745-4565.2004.tb00372.x CrossRefGoogle Scholar
- El-Wehedy SE, Darwish WS, Tharwat AE, Hafez A-EE (2019) Hygienic status of meat served at hospitals and its improvement after HACCP implementation. Jap J Vet Res 67(1):61–73Google Scholar
- Fardsanei F, Dallal M, Douraghi M, Memariani H, Bakhshi B, Salehi T, Nikkhahi F (2018) Antimicrobial resistance, virulence genes and genetic relatedness of Salmonella enterica Enteritidis isolates recovered from human gasteroenteritis in Tehran, Iran. JGAR 12:220–226. https://doi.org/10.1016/j.jgar.2017.10.005 CrossRefGoogle Scholar
- Ferreira CS, Pequini MRS, Nuñez S, Parra HS, Chacon R, David ID, Torre DE, Pedroso AC, Ferreira AJ (2017) A comparative survey between non-systemic Salmonella spp. (paratyphoid group) and systemic Salmonella Pullorum and S. Gallinarum with a focus on virulence genes. Pesq Vet Bras 10:1064–1068. https://doi.org/10.1590/s0100-736x2017001000004 CrossRefGoogle Scholar
- Huehn S, Ragione RM, Anjum M, Saunders M, Woodward MJ, Bunge C, Helmuth R, Hauser E, Guerra B, Beutlich J, Brisabois A, Peters T, Svensson L, Madajczak G, Litrup E, Imre A, Herrera-Leon S, Mevius D, Newell DG, Malorny B (2010) Virulotyping and antimicrobial resistance typing of Salmonella enterica serovars relevant to human health in Europe. Food Borne Pathog Dis 7:523–525. https://doi.org/10.1089/fpd.2009.0447 CrossRefGoogle Scholar
- Kauffman G (1974) Kauffman white scheme. WHO. Pd 172, 1, rev. 1. Acta Pathol Microbiol Scand B 61:385Google Scholar
- Kreig N, Holt J (1984) Bergey’s manual of systemic bacteriology, vol 1. William and Wilkins, BaltimoreGoogle Scholar
- Murugkar HV, Rahman H, Dutta PK (2003) Distribution of virulence genes in Salmonella serovars isolated from man and animals. IFRJ 117:66–70Google Scholar
- National Committee for Clinical Laboratory Standards (2001) Performance standards for antimicrobial susceptibility testing. Eleventh Informational Supplement. Disk diffusion, M100-S11. NCCLS, Villanova, PA, USAGoogle Scholar
- Omar D, Al-Ashmawy M, Ramadan H, El-Sherbiny M (2018) Occurrence and PCR identification of Salmonella spp. from milk and dairy products in Mansoura, Egypt. Food Res Int 25:446–452Google Scholar
- Quinn PJ, Markey BK, Carter ME, Donnelly WJC, Leonard FC (2002) Veterinary microbiology and microbial disease. Blackwell Science Ltd, OxfordGoogle Scholar
- Rahn K, De Grandis SA, Clarke RC, Mc Ewen SA, Galan JE, Ginocchio C, Curtiss R, Gyles CL (1992) Amplification of an invA gene sequence of Salmonella Typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Mol Cell Probe 6:271–279. https://doi.org/10.1016/0890-8508(92)90002-F CrossRefGoogle Scholar
- Rohrbach B, Draughon F, Davidson P, Oliver S (1992) Prevalence of Listeria monocytogenes, Campylobacter jejuni, Yersinia enterocoiitica, and Salmonella in bulk tank milk: risk factors and risk of human exposure. J Food Protect 2:93–97. https://doi.org/10.4315/0362-028X-55.2.93 CrossRefGoogle Scholar
- Shin JH, Chang S, Kang SK (2004) Application of antimicrobial ice for reduction of foodborne pathogens (Escherichia coli O157:H7, Salmonella Typhimurium, Listeria monocytogenes) on the surface of fish. Appl Microbiol 97:916–922. https://doi.org/10.1111/j.1365-2672.2004.02343.x CrossRefGoogle Scholar
- Srivani R (2011) Studies on antimicrobial susceptibility pattern of Salmonella isolates from Chennai, India. Inter J Pharm Bio Sci 2:435–442Google Scholar
- Streckel W, Wolff AC, Prager R, Tietze E, Tschäpe H (2004) Expression profiles of effector proteins SopB, SopD1, SopE1, and AvrA differ with systemic, enteric, and epidemic strains of Salmonella enterica. Mol Nutr Food Res 48:496–503. https://doi.org/10.1002/mnfr.200400035 CrossRefPubMedGoogle Scholar