Investigation of Enterotoxigenic Coagulase-negative Staphylococci Isolated from Local and Imported Dairy Products; a Microbiological Study
https://doi.org/10.24017/science.2020.2.8
Abstract views: 1091 / PDF downloads: 628Abstract
Coagulase negative staphylococci (CNS) have been recorded as a conveying vector for virulence genes and have been implicated in some cases of food poisoning. Research interest in CNS has increased over the past decade following their implication in infections in animals and humans. This study was aimed to detect CNS isolated from 150 dairy products (yoghurt, several types of cheese, Lork, and Serezh) in Sulaimani and Halabja governorate. Thirteen isolates out of 150 samples were identified as CNS using the VITEK® 2 system as an identification method. Results revealed that the most common isolates species including Staphylococcus saprophyticus, Staphylococcus sciuri and Staphylococcus xylosus each species have been identified in 3 samples separately (23%), followed by Staphylococcus vitulinus was in 2 samples (15%), Staphylococcus equorum found in 1 sample (8%), and Staphylococcus gallinarum also was in one sample (8%). The isolated CNS did not have enterotoxins type A to E according to RIDASCREEN kit test. Studying the growth limits of S. saprophyticus and S. vitulinus results showed that S. saprophyticus grew better at pH levels (5,6,7) at (25?,37?) and low NaCl concentration (5%), while low bacterial activity was observed at pH 4 at all temperatures and NaCl concentrations and also at 4? at all pH and NaCl levels. S. vitulinus behaviour was almost the same as S. saprophyticus but, S. vitulinus was able to tolerate different NaCl concentrations and overall had higher bacterial activity in all parameter’s interactions than S. saprophyticus. Investigating the effect of acetic acid and lactic acid on the growth of previous species where studied, S. saprophyticus grew better in different concentrations of L.A but S. vitulinus showed more activity than S. saprophyticus in A.A and the growth of both species inhibited at 0.4% of L.A at the first 24 hours of incubation.
Keywords:
Coagulase-negative staphylococci, Dairy products, pH, temperature, NaCl, acetic acid, lactic acid.
References
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https://doi.org/10.14202/vetworld.2018.1214-1221
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https://doi.org/10.1016/B978-0-12-813547-1.00006-6
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https://doi.org/10.1016/j.ijid.2007.09.018
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https://doi.org/10.1089/fpd.2004.1.241
[10] Cunha, e. Peresi, R. A. O. Calsolari, and J. P. A. Júnior, "DETECTION OF ENTEROTOXINS GENES IN COAGULASE-NEGATIVE STAPHYLOCOCCI ISOLATED FROM FOODS," Brazilian Journal of Microbiology, vol. 37, pp. 70-74, 2006.
https://doi.org/10.1590/S1517-83822006000100013
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https://doi.org/10.1016/S0934-8840(11)80789-9
[12] M. Hugas and J. M. Monfort, "Bacterial starter cultures for meat fermentation," Food Chemistry, vol. 59, no. 4, pp. 547-554, 1997/08/01/ 1997.
https://doi.org/10.1016/S0308-8146(97)00005-8
[13] F. Irlinger, "Safety assessment of dairy microorganisms: coagulase-negative staphylococci," Int J Food Microbiol, vol. 126, no. 3, pp. 302-10, Sep 1 2008.
https://doi.org/10.1016/j.ijfoodmicro.2007.08.016
[14] E. T. Ryser, S. Maisnier-Patin, J. J. Gratadoux, and J. Richard, "Isolation and identification of cheese-smear bacteria inhibitory to Listeria spp," International Journal of Food Microbiology, vol. 21, no. 3, pp. 237-246, 1994/02/01/ 1994.
https://doi.org/10.1016/0168-1605(94)90030-2
[15] W. Bockelmann, "Development of defined surface starter cultures for the ripening of smear cheeses," (in eng), International dairy journal, vol. 12, no. 2/3, pp. 123-131, 2002 2002.
https://doi.org/10.1016/S0958-6946(01)00152-2
[16] D. Ercolini, P. J. Hill, and C. E. Dodd, "Bacterial community structure and location in Stilton cheese," Appl Environ Microbiol, vol. 69, no. 6, pp. 3540-8, Jun 2003.
https://doi.org/10.1128/AEM.69.6.3540-3548.2003
[17] D. Roberts and M. Greenwood, Practical Food Microbiology, Third ed. Blackwell, 2003.
https://doi.org/10.1002/9780470757512
[18] J. G. Collee, A. G. Fraser, B. P. Marison, and A. Simmons, Practical medical microbiology, 14th ed. New york: Churchill Livingston Inc, 1996.
[19] M. Ahmadi, S. M. R. Rohani, and N. Ayremlou, "Detection of Staphylococcus aureus in milk by PCR," Comparative Clinical Pathology, vol. 19, no. 1, pp. 91-94, 2009.
https://doi.org/10.1007/s00580-009-0901-0
[20] B. T. Cenci-Goga, A. Karama, P. V. Rossitto, R. A. Morgante, and J. S. Cullor, "Enterotoxin Production by Staphylococcus aureus Isolated from Mastitic Cows," Journal of Food Protection, vol. 66, no. 9, pp. 1693-1696, 2003.
https://doi.org/10.4315/0362-028X-66.9.1693
[21] A. Jamshidi, H. R. Kazerani, H. A. Seifi, and E. Moghaddas, "Growth limits of Staphylococcus aureus as a function of temperature, acetic acid, NaCl concentration, and inoculum level," Iranian Journal of Veterinary Research, vol. 9, no. 4, 2008.
[22] G. Q. Hussein, "Ecological and physiological study on Bacillus cereus isolate from local foods.," M. Sc., Colleage of Science, University of Baghdad, 1999.
[23] F. S. A. AL-Mayahy and H. H. AL-Galebi, "Bacterial contamination assessment of local and Imported diary productions in Al-Diwaniya markets," Journal of Kerbala University, vol. 7, no. 2, 2009.
[24] W. Bockelmann, U. Krusch, G. Engel, N. Klijn, G. Smit, and K. J. Heller, "The microflora of Tilsit cheese," vol. 4, 1997.
[25] S. Kunová, M. Ka?ániová, J. ?ubo?, P. Haš?ík, and ?. Lopašovský, "Evaluation of microbiological quality of selected cheeses during storage," Potravinarstvo, vol. 9, no. 1, 2015.
https://doi.org/10.5219/463
[26] N. Benkerroum, H. Oubel, and W. E. Sandine, "Effect of nisin on yogurt starter, and on growth and survival of Listeria monocytogenes during fermentation and storage of yogurt," Internet Journal of Food Safety V, vol. 1, pp. 1-5, 11/30 2002.
[27] A. Ruaro, C. Andrighetto, S. Torriani, and A. Lombardi, "Biodiversity and characterization of indigenous coagulase-negative staphylococci isolated from raw milk and cheese of North Italy," Food Microbiol, vol. 34, no. 1, pp. 106-11, May 2013.
https://doi.org/10.1016/j.fm.2012.11.013
[28] V. Perreten, N. Giampà, U. Schuler-Schmid, and M. Teuber, "Antibiotic Resistance Genes in Coagulase-negative Staphylococci Isolated from Food," Systematic and Applied Microbiology, vol. 21, no. 1, pp. 113-120, 1998.
https://doi.org/10.1016/S0723-2020(98)80014-3
[29] M. A. El-Zamkan, A. G. Mubarak, and A. O. Ali, "Prevalence and phylogenetic relationship among methicillin- and vancomycin-resistant Staphylococci isolated from hospital's dairy food, food handlers, and patients," J Adv Vet Anim Res, vol. 6, no. 4, pp. 463-473, Dec 2019.
https://doi.org/10.5455/javar.2019.f369
[30] S. Argaw, M. Addis, and H. Degefu, "Identification and Antimicrobial Resistance Pattern of Staphylococci Isolated From Cottage Cheese (Ayib) and Yoghurt (Ergo) in Selected Districts of Jimma Zone, Ethiopia," Health Science Journal, vol. 12, no. 1, 2018.
https://doi.org/10.21767/1791-809X.1000549
[31] S. P. Onen and O. Aygun, "Enterotoxin Producing Ability And Antimicrobial Susceptibility Of Coagulase Negative Staphylococci Isolated From Goat Milk, Cheese And Salted Yoghurt In Turkey," INTERNATIONAL JOURNAL OF SCIENTIFIC & TECHNOLOGY RESEARCH, vol. 6, no. 10, 2017.
[32] C. Kurekci, "Short communication: Prevalence, antimicrobial resistance, and resistant traits of coagulase-negative staphylococci isolated from cheese samples in Turkey," J Dairy Sci, vol. 99, no. 4, pp. 2675-2679, Apr 2016.
https://doi.org/10.3168/jds.2015-10725
[33] R. S. Casaes Nunes, C. Pires de Souza, K. S. Pereira, E. M. Del Aguila, and V. M. Flosi Paschoalin, "Identification and molecular phylogeny of coagulase-negative staphylococci isolates from Minas Frescal cheese in southeastern Brazil: Superantigenic toxin production and antibiotic resistance," J Dairy Sci, vol. 99, no. 4, pp. 2641-2653, Apr 2016.
https://doi.org/10.3168/jds.2015-9693
[34] J. P. Rosec, J. P. Guiraud, C. Dalet, and N. Richard, "Enterotoxin production by staphylococci isolated from foods in France," International Journal of Food Microbiology, vol. 35, 1997.
https://doi.org/10.1016/S0168-1605(96)01234-2
[35] S. Even et al., "Low occurrence of safety hazards in coagulase negative staphylococci isolated from fermented foodstuffs," (in eng), International journal of food microbiology, vol. 139, no. 1-2, pp. 87-95, 2010/04// 2010.
https://doi.org/10.1016/j.ijfoodmicro.2010.02.019
[36] Blaiotta et al., "PCR detection of staphylococcal enterotoxin genes in Staphylococcus spp. strains isolated from meat and dairy products. Evidence for new variants of seG and seI in S. aureus AB-8802," J Appl Microbiol, vol. 97, no. 4, pp. 719-30, 2004.
https://doi.org/10.1111/j.1365-2672.2004.02349.x
[37] B. S. V. Souza et al., "The influence of pH on Staphylococcus saprophyticus iron metabolism and the production of siderophores," Microbes Infect, vol. 21, no. 10, pp. 456-463, Dec 2019.
https://doi.org/10.1016/j.micinf.2019.04.008
[38] D. A. Stavropoulou, P. Filippou, S. De Smet, L. De Vuyst, and F. Leroy, "Effect of temperature and pH on the community dynamics of coagulase-negative staphylococci during spontaneous meat fermentation in a model system," Food Microbiol, vol. 76, pp. 180-188, Dec 2018.
https://doi.org/10.1016/j.fm.2018.05.006
[39] L. A. Onyango, R. H. Dunstan, J. Gottfries, C. von Eiff, and T. K. Roberts, "Effect of Low Temperature on Growth and Ultra-Structure of Staphylococcus spp," PLoS ONE, vol. 7, no. 1, p. e29031, 2012.
https://doi.org/10.1371/journal.pone.0029031
[40] A. K. Søndergaard and L. H. Stahnke, "Growth and aroma production by Staphylococcus xylosus, S. carnosus and S. equorum; a comparative study in model systems," International Journal of Food Microbiology, vol. 75, pp. 99-109, 2002.
https://doi.org/10.1016/S0168-1605(01)00729-2
[41] G. Mauriello, A. Casaburi, G. Blaiotta, and F. Villani, "Isolation and technological properties of coagulase negative staphylococci from fermented sausages of Southern Italy," Meat Sci, vol. 67, no. 1, pp. 149-58, May 2004.
https://doi.org/10.1016/j.meatsci.2003.10.003
[42] E. Mani-López, H. S. García, and A. López-Malo, "Organic acids as antimicrobials to control Salmonella in meat and poultry products," (in eng), Food Research International (Ottawa, Ont.), vol. 45, no. 2, pp. 713-721, 2012/03// 2012.
https://doi.org/10.1016/j.foodres.2011.04.043
[43] D. O. Cliver, "Microbial Decontamination, Food Safety and antimicrobial Interventions," 2007.
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https://doi.org/10.1201/b12450
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How to Cite
[1]
N. S. Ali and H. H. Arif, “Investigation of Enterotoxigenic Coagulase-negative Staphylococci Isolated from Local and Imported Dairy Products; a Microbiological Study”, KJAR, vol. 5, no. 2, pp. 82–98, Dec. 2020, doi: 10.24017/science.2020.2.8.
Published
09-12-2020
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Section
Pure and Applied Science
