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Türkiye'de tüketime sunulan perakende balıklarda stafilokok ve enterokok varlığı ve özellikleri

Year 2021, Issue: 28, 911 - 916, 30.11.2021
https://doi.org/10.31590/ejosat.1012061

Abstract

Araştırmamızda, Atlantik somonu (Salmo salar), palamut (Sarda sarda), deniz alabalığı (Salmo trutta) ve avrupa levreğinden (Dicentrararchus labrax) oluşan 247 balık örneğinden, toplam 163 (%66.0) Staphylococcus ve 52 (%21.0) Enterococcus izole edilmiştir. Staphylococcus izolatları, S. aureus (%8.0), S. intermedius (%6.7), S. warneri (%32.0), S. hemolyticus (%22.7), S. saprophyticus (%7.4), S. simulans ( %5.5), S. capitis (%5.5), S. xylosus (%4.9), S. epidermidis (%4.3), S. schleiferi (%1.8) ve S. caprae (%1.2) olarak adlandırılmıştır. Enterococcus izolatları ise, E. faecalis (%46.1), E. avium (%25.0), E. solitarius (%11.5), E. gallinarium (%7.7), E. casseliflavus (%6.0), E. maladoratus ( %1,9) ve E. flavescens (%1,9) olarak adlandırılmıştır. Staphylococcus izolatlarının çoğunda biyofilm oluşumu (%93.8), lipaz üretimi (%89.6), slime üretimi (%84.0), hemolitik aktivite (%69.9), DNaz aktivitesi (%63.1) ve proteaz üretimi (%57.0) tespit edilmiştir. Enterococcus izolatlarının sırasıyla %94,2'sinde, %90.3'ünde, %57.7'sinde, %36.5'inde ve %3.8'inde biyofilm oluşumu, slime oluşumu, DNaz aktivitesi, proteoliz ve hemoliz tespit edilmiştir. Enterococcus türlerinin hiçbirinde lipolitik aktivite belirlenmemiştir.

References

  • Anonymous (2011) Fishery Statistics, Fisheries economy, production, amount and value exchanges (in Turkish), No: 10863, State Institute of Statistics Prime Ministry of Turkey Ankara.
  • Fonnesbech Vogel, B., Huss, H. H., Ojeniyi, B., Ahrens, P., and Gram, L. (2001). Elucidation of Listeria monocytogenes contamination routes in cold-smoked salmon processing plants detected by DNA-based typing methods. Applied and environmental microbiology, 67(6), 2586-2595.
  • Sudheesh, P. S., Al-Ghabshi, A., Al-Aboudi, N., Al-Gharabi, S., & Al-Khadhuri, H. (2013). Evaluation of food contact surface contamination and the presence of pathogenic bacteria in seafood retail outlets in the sultanate of oman. Adv. J. Food Sci., 5, 77.
  • Hammad, A. M., Shimamoto, T., & Shimamoto, T. (2014). Genetic characterization of antibiotic resistance and virulence factors in Enterococcus spp. from Japanese retail ready-to-eat raw fish. Food microbiology, 38, 62-66.
  • Simon, S. S., and Sanjeev, S. (2007). Prevalence of enterotoxigenic Staphylococcus aureus in fishery products and fish processing factory workers. Food control, 18(12), 1565-1568.
  • Červenka, L., Brožková, I., and Vytřasová, J. (2006). Effects of the principal ingredients of biscuits upon water activity. Journal of Food and Nutrition Research, 45(1), 39-43.
  • Vasudevan, P., Nair, M. K. M., Annamalai, T., & Venkitanarayanan, K. S. (2003). Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Veterinary microbiology, 92(1-2), 179-185.
  • Hammad, A. M., Watanabe, W., Fujii, T., & Shimamoto, T. (2012). Occurrence and characteristics of methicillin-resistant and-susceptible Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci from Japanese retail ready-to-eat raw fish. International journal of food microbiology, 156(3), 286-289.
  • Barbosa, J., Gibbs, P. A., & Teixeira, P. (2010). Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control, 21(5), 651-656.
  • Gundogan, N., Ataol, Ö., & Gunal, S. (2012). Determination of some virulence factors in staphylococci isolated from milk and meat products. Bestimmung von Virulenzfaktoren aus Staphylokokken-Isolaten von Milch-und Fleischprodukten. Archiv für Lebensmittelhygiene, 5(6), 182-186.
  • Gundogan, N., Ataol, O., & Torlak, F. O. (2013). Determination of Some Virulence Factors in Staphylococcus aureus, Enterococcus faecalis and E nterococcus faecium Isolated from Meat and Milk Products. Journal of Food Safety, 33(4), 387-393.
  • Ike, Y., Hashimoto, H., and Clewell, D. B. (1987). High incidence of hemolysin production by Enterococcus (Streptococcus) faecalis strains associated with human parenteral infections. Journal of clinical Microbiology, 25(8), 1524-1528.
  • Asha, P., Jyothis, M., & Shini, Z. (2013). A comparative study of virulence factors in enterococci from clinical and nonclinical sources. J. Pharm. Biomed. Sci, 29, 745-752.
  • Quinn, P. J., Carter, M. E., Markey, B., & Carter, G. R. (1994). Veterinary clinical microbiology. Wolfe Publication, London, UK, 254-258.
  • Christensen, G. D., Simpson, W. A., Younger, J. J., Baddour, L. M., Barrett, F. F., Melton, D. M., & Beachey, E. H. (1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. Journal of clinical microbiology, 22(6), 996-1006.
  • Saising, J., Singdam, S., Ongsakul, M., & Voravuthikunchai, S. P. (2012). Lipase, protease, and biofilm as the major virulence factors in staphylococci isolated from acne lesions. Bioscience trends, 6(4), 160-164.
  • Mhango, M., Mpuchane, S. F., & Mpuchane, B. A. (2010). Incidence of indicator organisms, opportunistic and pathogenic bacteria in fish. African Journal of Food, Agriculture, Nutrition and Development, 10(10).
  • Boari, C. A., Pereira, G. I., Valeriano, C., Silva, B. C., Morais, V. M. D., Figueiredo, H. C. P., & Piccoli, R. H. (2008). Bacterial ecology of tilapia fresh fillets and some factors that can influence their microbial quality. Food Science and Technology, 28, 863-867.
  • Himelbloom, B. H., & Crapo, C. A. (1998). Factors Influencing the Microbial Quality of Cold‐Smoked Salmon Strips. Journal of food science, 63(2), 356-358.
  • Grigoryan, Ę., Badalyan, G., & Andriasyan, D. (2010). Prevalence of Staphylococcus aureus in fish processing factory. Potravinárstvo (Slovak Republic).
  • Suzuki, Y., Kanda, N., & Furukawa, T. (2012). Abundance of Enterococcus species, Enterococcus faecalis and Enterococcus faecium, essential indicators of fecal pollution, in river water. Journal of Environmental Science and Health, Part A, 47(11), 1500-1505.
  • Cariolato, D., Andrighetto, C., & Lombardi, A. (2008). Occurrence of virulence factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control, 19(9), 886-892.
  • Kimiran-Erdem, A., Arslan, E. O., Yurudu, N. O. S., Zeybek, Z., Dogruoz, N., & Cotuk, A. (2007). Isolation and identification of enterococci from seawater samples: assessment of their resistance to antibiotics and heavy metals. Environmental Monitoring and Assessment, 125(1), 219-228.
  • Al Bulushi, I. M., Poole, S. E., Barlow, R., Deeth, H. C., & Dykes, G. A. (2010). Speciation of Gram-positive bacteria in fresh and ambient-stored sub-tropical marine fish. International Journal of Food Microbiology, 138(1-2), 32-38.
  • Valenzuela, A. S., Benomar, N., Abriouel, H., Cañamero, M. M., & Gálvez, A. (2010). Isolation and identification of Enterococcus faecium from seafoods: antimicrobial resistance and production of bacteriocin-like substances. Food microbiology, 27(7), 955-961.
  • Mol, S., & Sağlam, Ö. E. (2004). Investigating seafood marketing conditions in some important Turkish seafood markets in comparison with European countries. Turkish Journal of Fisheries and Aquatic Sciences, 4(2).
  • Çıtak, S., Varlık, Ö., & Gündoǧan, N. (2003). Slime production and DNase activity of staphylococci isolated from raw milk. Journal of food safety, 23(4), 281-288.
  • Ciftci, A., Findik, A., Onuk, E. E., & Savasan, S. (2009). Detection of methicillin resistance and slime factor production of Staphylococcus aureus in bovine mastitis. Brazilian Journal of Microbiology, 40, 254-261.
  • Necidová, L., Janštová, B., Karpíšková, S., Cupáková, Š., Dušková, M., & Karpíšková, R. (2009). Importance of Enterococcus spp. for forming a biofilm. Czech Journal of Food Sciences, 27(Special Issue 1).
  • Masniyom, P. (2011). Deterioration and shelf-life extension of fish and fishery products by modified atmosphere packaging. Sonklanakarin Journal of Science and Technology, 33(2), 181.
  • Batish, V. K., Chander, H., & Ranganathan, B. (1984). Prevalence of enterococci in frozen dairy products and their pathogenicity. Food Microbiology, 1(4), 269-276.
  • Ebrahimi, A., & Akhavan, T. M. (2009). Characteristics of staphylococci isolated from clinical and subclinical mastitis cows in Shahrekord, Iran. Iranıan Journal Of Veterınary Research, 10, (3), 273-277.
  • Türkyilmaz, S., & Kaya, O. (2006). Determination of some virulence factors in Staphylococcus spp. isolated from various clinical samples. Turkish Journal of Veterinary and Animal Sciences, 30(1), 127-132.
  • Ali-Vehmas, T., Vikerpuur, M., Pyörälä, S., & Atroshi, F. (2001). Characterization of hemolytic activity of Staphylococcus aureus strains isolated from bovine mastitic milk. Microbiological research, 155(4), 339-344.

Occurrence and characteristics of staphylococci and enterococci in retail fish used for human consumption in Turkey

Year 2021, Issue: 28, 911 - 916, 30.11.2021
https://doi.org/10.31590/ejosat.1012061

Abstract

A total of 163 (66.0 %) Staphylococcus isolates and 52 (21.0 %) Enterococcus isolates were isolated from 247 fish samples consisting of Atlantic salmon (Salmo salar), Atlantic bonito (Sarda sarda), Sea trout (Salmo trutta), and European seabass (Dicentrararchus labrax). The Staphylococcus isolates were identified as S. aureus (8.0 %), S. intermedius (6.7 %), S. warneri (32.0 %), S. hemolyticus (22.7 %), S. saprophyticus (7.4 %), S. simulans (5.5 %), S. capitis (5.5 %), S. xylosus (4.9 %), S. epidermidis (4.3 %), S. schleiferi (1.8 %) and S. caprae (1.2 %). The Enterococcus isolates were identified as E. faecalis (46.1 %), E. avium (25.0 %), E. solitarius (11.5 %), E. gallinarium (7.7 %), E. casseliflavus (6.0 %), E. maladoratus (1.9 %), and E. flavescens (1.9 %). The majority of Staphylococcus strains had biofilm formation (93.8 %), lipase production (89.6 %), slime production (84.0 %), hemolytic activity (69.9 %), DNase activity (63.1 %) and protease production (57.0 %). Biofilm formation, slime formation, DNase activity, proteolysis, and hemolysis were detected in 94.2 %, 90.3 %, 57.7 %, 36.5 %, and 3.8 % of Enterococcus strains, respectively. None of the Enterococcus species had lipolytic activity.

References

  • Anonymous (2011) Fishery Statistics, Fisheries economy, production, amount and value exchanges (in Turkish), No: 10863, State Institute of Statistics Prime Ministry of Turkey Ankara.
  • Fonnesbech Vogel, B., Huss, H. H., Ojeniyi, B., Ahrens, P., and Gram, L. (2001). Elucidation of Listeria monocytogenes contamination routes in cold-smoked salmon processing plants detected by DNA-based typing methods. Applied and environmental microbiology, 67(6), 2586-2595.
  • Sudheesh, P. S., Al-Ghabshi, A., Al-Aboudi, N., Al-Gharabi, S., & Al-Khadhuri, H. (2013). Evaluation of food contact surface contamination and the presence of pathogenic bacteria in seafood retail outlets in the sultanate of oman. Adv. J. Food Sci., 5, 77.
  • Hammad, A. M., Shimamoto, T., & Shimamoto, T. (2014). Genetic characterization of antibiotic resistance and virulence factors in Enterococcus spp. from Japanese retail ready-to-eat raw fish. Food microbiology, 38, 62-66.
  • Simon, S. S., and Sanjeev, S. (2007). Prevalence of enterotoxigenic Staphylococcus aureus in fishery products and fish processing factory workers. Food control, 18(12), 1565-1568.
  • Červenka, L., Brožková, I., and Vytřasová, J. (2006). Effects of the principal ingredients of biscuits upon water activity. Journal of Food and Nutrition Research, 45(1), 39-43.
  • Vasudevan, P., Nair, M. K. M., Annamalai, T., & Venkitanarayanan, K. S. (2003). Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Veterinary microbiology, 92(1-2), 179-185.
  • Hammad, A. M., Watanabe, W., Fujii, T., & Shimamoto, T. (2012). Occurrence and characteristics of methicillin-resistant and-susceptible Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci from Japanese retail ready-to-eat raw fish. International journal of food microbiology, 156(3), 286-289.
  • Barbosa, J., Gibbs, P. A., & Teixeira, P. (2010). Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control, 21(5), 651-656.
  • Gundogan, N., Ataol, Ö., & Gunal, S. (2012). Determination of some virulence factors in staphylococci isolated from milk and meat products. Bestimmung von Virulenzfaktoren aus Staphylokokken-Isolaten von Milch-und Fleischprodukten. Archiv für Lebensmittelhygiene, 5(6), 182-186.
  • Gundogan, N., Ataol, O., & Torlak, F. O. (2013). Determination of Some Virulence Factors in Staphylococcus aureus, Enterococcus faecalis and E nterococcus faecium Isolated from Meat and Milk Products. Journal of Food Safety, 33(4), 387-393.
  • Ike, Y., Hashimoto, H., and Clewell, D. B. (1987). High incidence of hemolysin production by Enterococcus (Streptococcus) faecalis strains associated with human parenteral infections. Journal of clinical Microbiology, 25(8), 1524-1528.
  • Asha, P., Jyothis, M., & Shini, Z. (2013). A comparative study of virulence factors in enterococci from clinical and nonclinical sources. J. Pharm. Biomed. Sci, 29, 745-752.
  • Quinn, P. J., Carter, M. E., Markey, B., & Carter, G. R. (1994). Veterinary clinical microbiology. Wolfe Publication, London, UK, 254-258.
  • Christensen, G. D., Simpson, W. A., Younger, J. J., Baddour, L. M., Barrett, F. F., Melton, D. M., & Beachey, E. H. (1985). Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. Journal of clinical microbiology, 22(6), 996-1006.
  • Saising, J., Singdam, S., Ongsakul, M., & Voravuthikunchai, S. P. (2012). Lipase, protease, and biofilm as the major virulence factors in staphylococci isolated from acne lesions. Bioscience trends, 6(4), 160-164.
  • Mhango, M., Mpuchane, S. F., & Mpuchane, B. A. (2010). Incidence of indicator organisms, opportunistic and pathogenic bacteria in fish. African Journal of Food, Agriculture, Nutrition and Development, 10(10).
  • Boari, C. A., Pereira, G. I., Valeriano, C., Silva, B. C., Morais, V. M. D., Figueiredo, H. C. P., & Piccoli, R. H. (2008). Bacterial ecology of tilapia fresh fillets and some factors that can influence their microbial quality. Food Science and Technology, 28, 863-867.
  • Himelbloom, B. H., & Crapo, C. A. (1998). Factors Influencing the Microbial Quality of Cold‐Smoked Salmon Strips. Journal of food science, 63(2), 356-358.
  • Grigoryan, Ę., Badalyan, G., & Andriasyan, D. (2010). Prevalence of Staphylococcus aureus in fish processing factory. Potravinárstvo (Slovak Republic).
  • Suzuki, Y., Kanda, N., & Furukawa, T. (2012). Abundance of Enterococcus species, Enterococcus faecalis and Enterococcus faecium, essential indicators of fecal pollution, in river water. Journal of Environmental Science and Health, Part A, 47(11), 1500-1505.
  • Cariolato, D., Andrighetto, C., & Lombardi, A. (2008). Occurrence of virulence factors and antibiotic resistances in Enterococcus faecalis and Enterococcus faecium collected from dairy and human samples in North Italy. Food Control, 19(9), 886-892.
  • Kimiran-Erdem, A., Arslan, E. O., Yurudu, N. O. S., Zeybek, Z., Dogruoz, N., & Cotuk, A. (2007). Isolation and identification of enterococci from seawater samples: assessment of their resistance to antibiotics and heavy metals. Environmental Monitoring and Assessment, 125(1), 219-228.
  • Al Bulushi, I. M., Poole, S. E., Barlow, R., Deeth, H. C., & Dykes, G. A. (2010). Speciation of Gram-positive bacteria in fresh and ambient-stored sub-tropical marine fish. International Journal of Food Microbiology, 138(1-2), 32-38.
  • Valenzuela, A. S., Benomar, N., Abriouel, H., Cañamero, M. M., & Gálvez, A. (2010). Isolation and identification of Enterococcus faecium from seafoods: antimicrobial resistance and production of bacteriocin-like substances. Food microbiology, 27(7), 955-961.
  • Mol, S., & Sağlam, Ö. E. (2004). Investigating seafood marketing conditions in some important Turkish seafood markets in comparison with European countries. Turkish Journal of Fisheries and Aquatic Sciences, 4(2).
  • Çıtak, S., Varlık, Ö., & Gündoǧan, N. (2003). Slime production and DNase activity of staphylococci isolated from raw milk. Journal of food safety, 23(4), 281-288.
  • Ciftci, A., Findik, A., Onuk, E. E., & Savasan, S. (2009). Detection of methicillin resistance and slime factor production of Staphylococcus aureus in bovine mastitis. Brazilian Journal of Microbiology, 40, 254-261.
  • Necidová, L., Janštová, B., Karpíšková, S., Cupáková, Š., Dušková, M., & Karpíšková, R. (2009). Importance of Enterococcus spp. for forming a biofilm. Czech Journal of Food Sciences, 27(Special Issue 1).
  • Masniyom, P. (2011). Deterioration and shelf-life extension of fish and fishery products by modified atmosphere packaging. Sonklanakarin Journal of Science and Technology, 33(2), 181.
  • Batish, V. K., Chander, H., & Ranganathan, B. (1984). Prevalence of enterococci in frozen dairy products and their pathogenicity. Food Microbiology, 1(4), 269-276.
  • Ebrahimi, A., & Akhavan, T. M. (2009). Characteristics of staphylococci isolated from clinical and subclinical mastitis cows in Shahrekord, Iran. Iranıan Journal Of Veterınary Research, 10, (3), 273-277.
  • Türkyilmaz, S., & Kaya, O. (2006). Determination of some virulence factors in Staphylococcus spp. isolated from various clinical samples. Turkish Journal of Veterinary and Animal Sciences, 30(1), 127-132.
  • Ali-Vehmas, T., Vikerpuur, M., Pyörälä, S., & Atroshi, F. (2001). Characterization of hemolytic activity of Staphylococcus aureus strains isolated from bovine mastitic milk. Microbiological research, 155(4), 339-344.
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Details

Primary Language English
Subjects Engineering
Journal Section Articles
Authors

Meryem Burcu Külahcı 0000-0002-5007-5209

Neslihan Gündoğan 0000-0002-0691-4917

Publication Date November 30, 2021
Published in Issue Year 2021 Issue: 28

Cite

APA Külahcı, M. B., & Gündoğan, N. (2021). Occurrence and characteristics of staphylococci and enterococci in retail fish used for human consumption in Turkey. Avrupa Bilim Ve Teknoloji Dergisi(28), 911-916. https://doi.org/10.31590/ejosat.1012061