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Journal of Consumer Protection and Food Safety

, Volume 14, Issue 4, pp 399–407 | Cite as

Prevalence of Salmonella spp. in Egyptian dairy products: molecular, antimicrobial profiles and a reduction trial using d-tryptophan

  • Mahmoud Elafify
  • Wageh Sobhy DarwishEmail author
  • Maha Al-Ashmawy
  • Mohammed Elsherbini
  • Shige Koseki
  • Shuso Kawamura
  • Adel Abdelkhalek
Research Article

Abstract

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.

Keywords

Antimicrobial profile Dairy products d-Tryptophan Heat stress Salmonella spp. 

Notes

Acknowledgements

This work was supported by Egypt–Japan Education Partnership “EJEP.

References

  1. Abd-Elghany SM, Sallam KI, Abd-Elkhalek A, Tamura T (2015) Occurrence, genetic characterization and antimicrobial resistance of Salmonella isolated from chicken meat and giblets. Epidemiol Infect 143:997–1003.  https://doi.org/10.1017/S0950268814001708 CrossRefPubMedGoogle Scholar
  2. Abdullahi M (2010) Incidence and antimicrobial susceptibility pattern of Salmonella species in children attending some hospitals in kano metropolis kano state—Nigeria. BAJOPAS 3:2–20.  https://doi.org/10.4314/bajopas.v3il.58787 CrossRefGoogle Scholar
  3. Aidaros H (2005) Global perspectives—the Middle East: Egypt. Rev Sci Tech Oie 24:589–596CrossRefGoogle Scholar
  4. Al-Nakhli HM, Al-Ogaily ZH, Nassar TJ (1999) Representative Salmonella serovars isolated from poultry and poultry environments in Saudi Arabia. Rev Sci Tech 18:700–709CrossRefGoogle Scholar
  5. Amin HS, Abd El-Rahman AA (2015) Molecular characterization of Salmonella Enterica isolated from chicken meat and its products by multiplex PCR. Alexandria J Vet Sci 46:155–160CrossRefGoogle Scholar
  6. 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
  7. Boor KJ (2001) ADSA foundation scholar award fluid dairy product quality and safety: looking to the future. J Dairy Sci 84:1–11.  https://doi.org/10.3168/jds.S0022-0302(01)74445-1 CrossRefPubMedGoogle Scholar
  8. Chen J, Kudo H, Kan K, Kawamura S, Koseki S (2018) Growth-inhibitory effect of d-Tryptophan on Vibrio spp. in shucked and live Oysters. Appl Environ Microbiol 19:e1543-18.  https://doi.org/10.1128/AEM.01543-18 CrossRefGoogle Scholar
  9. 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
  10. 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
  11. D’Amico DJ, Groves E, Donnelly CW (2008) Low incidence of foodborne pathogens of concern in raw milk utilized for farmstead cheese production. J Food Prot 8:1580–1589.  https://doi.org/10.4315/0362-028X-71.8.1580 CrossRefGoogle Scholar
  12. Darwish WS, Eldaly E, El-Abbasy M, Ikenaka Y, Ishizuka M (2013) Antibiotic residues in food: African scenario. Jpn J Vet Res 61:S13–S22PubMedGoogle Scholar
  13. Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122.  https://doi.org/10.1038/nrd1008 CrossRefGoogle Scholar
  14. Doosti A, Doosti E, Rahimi E, Dehkord P (2017) Frequency of antimicrobial-resistant genes in Salmonella Enteritidis isolated from traditional and industrial Iranian white cheeses. B Biol Sci 87:73–80.  https://doi.org/10.1007/s40011-015-0572-3 CrossRefGoogle Scholar
  15. El-Baz A, El-Sherbini M, Abdelkhalek A, Al-Ashmawy M (2017) Prevalence and molecular characterization of Salmonella serovars in milk and cheese in Mansoura city, Egypt. JAVAR 4:45–51.  https://doi.org/10.5455/javar.2017.d189 CrossRefGoogle Scholar
  16. Elhadidy M, Mohammed MA (2012) Shiga toxin-producing Escherichia coli from raw milk cheese in Egypt. Prevalence, molecular characterization and survival to stress conditions. Lett Appl Microbiol 56:120–127.  https://doi.org/10.1111/lam.12023 CrossRefPubMedGoogle Scholar
  17. Ellis A, Preston M, Borczyk M, Miller M, Stone P, Hatton B, Chagla A, Hockin JA (1998) Community outbreak of Salmonella berta associated with a soft cheese product. Epidemiol Infec 120:29–35CrossRefGoogle Scholar
  18. 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
  19. 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
  20. Fashae K, Ogunsola F, Aarestrup FM, Hendriksen RS (2010) Antimicrobial susceptibility and serovars of Salmonella from chickens and humans in Ibadan, Nigeria. J Infect Dev Countr 8:484–494CrossRefGoogle Scholar
  21. 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
  22. Forshell PL, Wierup M (2006) Salmonella contamination: a significant challenge to the global marketing of animal food products. Rev Sci Ech Oie 25:541–554CrossRefGoogle Scholar
  23. Ghosh S, Qureshi A, Purohit H (2019) d-Tryptophan governs biofilm formation rates and bacterial interaction in P. mendocina and S. aureus. J Biosci 44(1):3.  https://doi.org/10.1007/s12038-018-9841-7 CrossRefPubMedGoogle Scholar
  24. 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
  25. Jones RM, Wu H, Wentworth C, Luo L, Collier- Hyams L, Neish AS (2008) Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host Microbe 3:233–244.  https://doi.org/10.1016/j.chom.2008.02.016 CrossRefPubMedGoogle Scholar
  26. Kan K, Chen J, Kawamura S, Koseki S (2018) Characteristics of d-Tryptophan as an antibacterial agent: effect of sodium chloride concentration and temperature on Escherichia coli growth inhibition. J Food Protect 81:25–30.  https://doi.org/10.4315/0362-028X.JFP-17-229 CrossRefGoogle Scholar
  27. Karns JS, Van Kessel JS, McCluskey BJ, Perdue ML (2005) Prevalence of Salmonella enterica in bulk tank milk from US dairies as determined by polymerase chain reaction. J Dairy Sci 88:3475–3479CrossRefGoogle Scholar
  28. Kauffman G (1974) Kauffman white scheme. WHO. Pd 172, 1, rev. 1. Acta Pathol Microbiol Scand B 61:385Google Scholar
  29. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R (2010) d-amino acids trigger biofilm disassembly. Science 328(5978):627–629.  https://doi.org/10.1126/science.1188628 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Koseki S, Nakamura N, Shiina T (2015) Growth inhibition of Listeria monocytogenes, Salmonella enterica, and Escherichia coli O157:H7 by d-tryptophan as an incompatible solute. J Food Protect 4:819–824.  https://doi.org/10.4315/0362-028X.JFP-14-374 CrossRefGoogle Scholar
  31. Kousta M, Mataragas M, Skandamis P, Drosinos EH (2010) Prevalence and sources of cheese contamination with pathogens at farm and processing levels. Food Control 21:805–815.  https://doi.org/10.1016/j.foodcont.2009.11.015 CrossRefGoogle Scholar
  32. Kreig N, Holt J (1984) Bergey’s manual of systemic bacteriology, vol 1. William and Wilkins, BaltimoreGoogle Scholar
  33. Lam H, Oh DC, Cava F, Takacs CN, Clardy J (2009) d-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552–1555.  https://doi.org/10.1126/science.1178123 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Meldrum RJ, Wilson I (2007) Salmonella and Campylobacter in United Kingdom retail raw chicken in 2005. J Food Protect 8:1937–1939.  https://doi.org/10.4315/0362-028X-70.8.1937 CrossRefGoogle Scholar
  35. Miranda J, Mondragon A, Martinez B, Guarddon M, Rodriguez JA (2009) Prevalence and antimicrobial resistance patterns of Salmonella from different raw foods in Mexico. J Food Protect 5:966–971.  https://doi.org/10.4315/0362-028X-72.5.966 CrossRefGoogle Scholar
  36. Moon K, Delaquis P, Poivonen T, Stanich K (2006) Effect of vanillin on the fate of Listeria monocytogenes and Escherichia coli O157:H7 in a model apple juice medium and in apple juice. Food Microbiol 23:169–174.  https://doi.org/10.1016/j.fm.2005.02.005 CrossRefPubMedGoogle Scholar
  37. Murugkar HV, Rahman H, Dutta PK (2003) Distribution of virulence genes in Salmonella serovars isolated from man and animals. IFRJ 117:66–70Google Scholar
  38. 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
  39. 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
  40. Peleg M (2006) Advanced quantitative microbiology for foods and biosystems: models for predictive growth and inactivation, 1st edn. CRC Press, Taylor and Francis, Boca Raton.  https://doi.org/10.1201/9781420005370 CrossRefGoogle Scholar
  41. Pompilio A, Scocchi M, Pomponio S, Guida F, Diprimio A, Fiscarelli E, Gennaro R, Bonaventura G (2011) Antibacterial and anti-biofilm effects of cathelicidin peptides against pathogens isolated from cystic fibrosis patients. Peptides 32:1807–1814CrossRefGoogle Scholar
  42. Quinn PJ, Markey BK, Carter ME, Donnelly WJC, Leonard FC (2002) Veterinary microbiology and microbial disease. Blackwell Science Ltd, OxfordGoogle Scholar
  43. 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
  44. 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
  45. Shanmugasamy M, Velayutham T, Rajeswar J (2011) Inv A gene specific PCR for detection of Salmonella from broilers. Vet World 4:562–564.  https://doi.org/10.5455/vetworld.2011.562-564 CrossRefGoogle Scholar
  46. 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
  47. Singh A, Yadav S, Singh S, Bharti P (2010) Prevalence of Salmonella in chicken eggs collected from poultry farms and marketing channels and their antimicrobial resistance. Food Res Inter 43:2027–2030CrossRefGoogle Scholar
  48. Srivani R (2011) Studies on antimicrobial susceptibility pattern of Salmonella isolates from Chennai, India. Inter J Pharm Bio Sci 2:435–442Google Scholar
  49. 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
  50. Van Kessel JA, Karns JS, Gorski L (2004) Prevalence of Salmonellae, Listeria monocytogenes and fecal coliforms in bulk tank milk on US dairies. J Dairy Sci 87:2822–2830.  https://doi.org/10.3168/jds.S0022-0302(04)73410-4 CrossRefPubMedGoogle Scholar
  51. Yan H, Li L, Alam MJ, Shinoda S, Miyoshi S (2010) Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. Int J Food Microbiol 143:230–234.  https://doi.org/10.1016/j.ijfoodmicro.2010.07.034 CrossRefPubMedGoogle Scholar

Copyright information

© Bundesamt für Verbraucherschutz und Lebensmittelsicherheit (BVL) 2019

Authors and Affiliations

  1. 1.Department of Food Hygiene and Control, Faculty of Veterinary MedicineMansoura UniversityMansouraEgypt
  2. 2.Graduate School of Agricultural ScienceHokkaido UniversitySapporoJapan
  3. 3.Food Control Department, Faculty of Veterinary MedicineZagazig UniversityZagazigEgypt

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