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Investigation of the Presence of Staphylococcus aureus and Staphylococcal Enterotoxins in Raw Milk of Various Animal Species

Year 2024, Volume: 21 Issue: 2, 86 - 91, 02.08.2024
https://doi.org/10.32707/ercivet.1515151

Abstract

Staphylococcus aureus and Staphylococcal Enterotoxins (SE) are a serious public health issue associated with hospital- and community-acquired diseases. S. aureus, especially transmitted from dairy animals to raw milk, causes food poisoning in humans. In this study, the prevalence and disruption of S. aureus and SEs in 500 raw milk samples (cow milk= 200; sheep milk= 200; buffalo milk= 100), offered for sale in the Kayseri region, were investigated by PCR and ELISA methods. Coagulase positive S. aureus (CoPS) was isolated from 380 (76%) of the analysed milk samples. According to the PCR test, 136 (35.7%) of the CoPS isolates were identified as S. aureus, 52 of these iso-lates belonged to sheep, 48 to cow and 36 to buffalo milk. Among the 136 isolates, 16 of them found to contain at least one of the SE genes with the m-PCR method. It was determined that 6 of these genes were sea, 1 was seb, 4 was sec and 5 was sed. According to the ELISA test, enterotoxin distributions in raw milks are SEA: 2 cow’s, 1 sheep and 1 buffalo; SEC: 2 buffalo’s and 1 cow; SED: 1 cow and 2 sheep. As a result, this study revealed the presence of S. aureus and SEs in raw milk sold in the Kayseri region and shows the importance of reducing the risk of contamination through good manufacturing practices (GMP), personnel hygiene and training, sanitation of farms and equipment, ud-der hygiene and health and Hazard Analysis and Critical Control Points (HACCP) applications for food safety and public health in milk.

References

  • Ahmed AAH, Maharik NMS, Valero A, Kamal SM. Incidence of enterotoxigenic Staphylococcus aureus in milk and Egyptian artisanal dairy products. Food Control 2019; 104: 20-7.
  • Asiimwe BB, Baldan R, Trovato A. Prevalence and molecular characteristics of Staphylococcus aureus, including methicillin resistant strains, isolated from bulk can milk and raw milk products in pasto-ral communities of South-West Uganda. BMC Infect Dis 2017; 17: 422.
  • Bianchi DM, Gallina S, Bellio A, Chiesa F, Civera T, Decastelli L. Enterotoxin gene profiles of Staphylococcus aureus isolated from milk and dairy products in Italy. Lett Appl Microbiol 2014; 58: 190-6.
  • Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, Vimercati C, Castiglioni B. Development of a multiplex PCR assay for the identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy products. Mol Cell Pro-bes 2005; 19(5), 299-305.
  • Dhanashekar R, Akkinepalli S, Nellutla A. Milk-borne infections. An analysis of their potential effect on the milk industry. Germs 2012; 2(3): 101.
  • Ertaş N, Gönülalan Z. Kayseri ilinde satılan çiğ sütler-de Staphylococcus aureus ve enterotoksinlerinin varlığı üzerine araştırmalar. Fırat Univ Sağlık Bilim Vet Derg 2010; 24(1): 11-5.
  • Féraudet Tarisse C, Goulard-Huet C, Nia Y, Devilliers K, Marcé D, Dambrune C, Simon S. Highly sensitive and specific detection of staphylococcal entero-toxins SEA, SEG, SEH, and SEI by immunoassay. Toxins 2021; 13(2): 130.
  • Garcia SN, Osburn BI, Jay-Russell MT. One health for food safety, food security, and sustainable food production. Front Sustain Food Syst 2020; 4: 1.
  • Goto M, Hayashidani H, Takatori K, Hara‐Kudo Y. Rapid detection of enterotoxigenic Staphylococcus aureus harbouring genes for four classical entero-toxins, SEA, SEB, SEC and SED, by loop‐mediated isothermal amplification assay. Lett Appl Microbiol 2007; 45(1): 100-7.
  • Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: cha-racterization and outbreak investigation. FEMS Microbiol Rev 2012; 36(4): 815-36.
  • Kaya H, Ertaş Onmaz N, Gönülalan Z, Al S. Kayseri ilinde tüketime sunulan tavuk etlerinde Staphylo-coccus aureus ve enterotoksin varlığının araştırıl-ması. Erciyes Üniv Vet Fak Derg 2015; 12(2): 93-8.
  • Keyvan E, Yurdakul O, Şen E. Staphylococcal enterotoxins and enterotoxigenic Staphylococcus aureus in raw milk: A screening study. Kocatepe Vet J 2020; 13(2): 104-9.
  • Kou X, Cai H, Huang S, Ni Y, Luo B, Qian H. Prevalence and characteristics of Staphylococcus aureus ısolated from retail raw milk in Northern Xinjiang, China. Front Microbiol 2021; 12: 2187.
  • Liu H, Li S, Meng L, Dong L, Zhao S, Lan X. Prevalence, antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from dairy herds in northern China. J Dairy Sci 2017; 100: 8796-803.
  • Liu C, Shen Y, Yang M, Chi K, Guo N. Hazard of Staphylococcal enterotoxins in food and promising strategies for natural products against virulence. J Agric Food Chem 2022; 70(8): 2450-65.
  • Morandi S, Brasca M, Lodi R, Cremonesi P, Castigli-oni B. Detection of classical enterotoxins and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products. Vet Microbiol 2007; 124(1-2): 66-72.
  • Normanno G, Firinu A, Virgilio S, Mula G, Dambrosio A, Poggiu A, Celano GV. Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol 2005; 98(1): 73-9.
  • Oliveira D, Borges A, Simões M. Staphylococcus aureus toxins and their molecular activity in infectious diseases. Toxins 2018; 10(6): 252.
  • Oliveira R, Pinho E, Almeida G, Azevedo NF, Almei-da C. Prevalence and diversity of Staphylococcus aureus and staphylococcal enterotoxins in raw milk from Northern Portugal. Front Microbiol 2022; 13: 703.
  • Omwenga I, Aboge GO, Mitema ES, Obiero G, Ngaywa C, Ngwili N, Bett B. Staphylococcus au-reus enterotoxin genes detected in milk from vari-ous livestock species in northern pastoral region of Kenya. Food Control 2019; 103: 126-32.
  • Rahimi E, Momtaz H, Shakerian A, Kavyani HR. The detection of classical enterotoxins of Staphylococ-cus aureus in raw cow milk using the ELISA met-hod. Turkish J Vet Anim Sci 2012; 36(3): 319-22.
  • Sankomkai W, Boonyanugomol W, Kraisriwattana K, Nutchanon J, Boonsam K, Kaewbutra S, Wongboot W. Characterisation of classical enterotoxins, virulence activity, and antibiotic susceptibility of Staphylococcus aureus isolated from Thai fermen-ted pork sausages, clinical samples, and healthy carriers in northeastern Thailand. J Vet Res 2020; 64(2): 289.
  • Sudhanthiramani S, Swetha CS, Bharathy S. Preva-lence of antibiotic resistant Staphylococcus aureus from raw milk samples collected from the local ven-dors in the region of Tirupathi, India. Vet World 2015; 8(4): 478-81.
  • TGK (Türk Gıda Kodeksi) 2000. Mikrobiyolojik Kriter-ler Tebliği. Tarım ve Köy İşleri Bakanlığı, 23960, Tebliğ No: 2001-19, Ankara, Türkiye.
  • Yıbar A, Küçük SC. Çiğ süt ve pastörize süt tüketimi-nin halk sağlığı üzerine etkileri. Food and Health 2019; 5(3): 197-204.
  • Yildirim T, Sadati F, Kocaman B, Siriken B. Staphylococcus aureus and Staphylococcal enterotoxin detection in raw milk and cheese origin coagulase positive isolates. IJSL 2019; 1(1): 30-41.
  • Yin HY, Fang TJ, Wen HW. Combined multiplex loop‐mediated isothermal amplification with lateral flow assay to detect sea and seb genes of enterotoxic Staphylococcus aureus. Lett Appl Microbiol 2016; 63(1): 16-24.
  • Zeinhom M, Abed A. Prevalence, characterization, and control of Staphylococcus aureus isolated from raw milk and Egyptian soft cheese. J Vet Med Res 2020; 27(2): 152-60.
  • Zhang J, Wang J, Jin J, Li X, Zhang H, Shi X, Zhao C. Prevalence, antibiotic resistance, and entero-toxin genes of Staphylococcus aureus isolated from milk and dairy products worldwide: A systematic review and meta-analysis. Food Res Int 2022; 162: 111969.

Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus aureus ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması

Year 2024, Volume: 21 Issue: 2, 86 - 91, 02.08.2024
https://doi.org/10.32707/ercivet.1515151

Abstract

Staphylococcus aureus ve Stafilokokal Enterotoksinler (SE), hastane ve toplum kaynaklı hastalıklarla ilişkili ciddi bir halk sağlığı sorunudur. Özellikle süt hayvanlarından çiğ süte geçen S. aureus, insanlarda gıda zehirlenmelerine yol açmaktadır. Bu çalışmada, Kayseri bölgesinde satışa sunulan 500 çiğ süt örneğindeki (inek sütü=200; koyun sütü=200; manda sütü= 100) S. aureus ve SE’lerin prevalans ve çeşitliliği PCR ve ELISA yöntemleri ile araştırıldı. Analiz edilen süt örneklerinin 380’inden (%76) koagülaz pozitif S. aureus (KPS) izole edildi. PCR testi ile KPS izolatlarının 136’sı (%35.7) S. aureus olarak identifiye edildi. Bu izolatların 52’si koyun, 48’i inek ve 36’sı manda sütlerine ait idi. Belirlenen 136 izolatın m-PCR metodu ile incelenmesi sonucunda, 16 izolatın SE genlerinden en az birini içerdiği gözlendi. Bu genlerin 6’sının sea, 1’inin seb, 4’ünün sec ve 5’inin sed geni olduğu belirlendi. ELISA testi sonucu, çiğ sütlerdeki ente-rotoksin dağılımları ise; SEA: 2 inek, 1 koyun ve 1 manda; SEC: 2 manda ve 1 inek; SED: 1 inek ve 2 koyun şeklinde idi. Sonuç olarak bu çalışma, Kayseri bölgesinde satışa sunulan çiğ sütlerde S. aureus ve SE’lerin varlığını ortaya ko-yarak, sütte gıda güvenliği ve halk sağlığı için iyi üretim uygulamaları (Good manufacturing practices; GMP), personel hijyeni ve eğitimi, çiftlik ve ekipmanların sanitasyonu, meme hijyeni ve sağlığı ve tehlike analizleri ve kritik kontrol nok-taları (Hazard Analysis and Critical Control Points; HACCP) uygulamaları ile kontaminasyon riskinin azaltılmasının önemini göstermektedir.

References

  • Ahmed AAH, Maharik NMS, Valero A, Kamal SM. Incidence of enterotoxigenic Staphylococcus aureus in milk and Egyptian artisanal dairy products. Food Control 2019; 104: 20-7.
  • Asiimwe BB, Baldan R, Trovato A. Prevalence and molecular characteristics of Staphylococcus aureus, including methicillin resistant strains, isolated from bulk can milk and raw milk products in pasto-ral communities of South-West Uganda. BMC Infect Dis 2017; 17: 422.
  • Bianchi DM, Gallina S, Bellio A, Chiesa F, Civera T, Decastelli L. Enterotoxin gene profiles of Staphylococcus aureus isolated from milk and dairy products in Italy. Lett Appl Microbiol 2014; 58: 190-6.
  • Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, Vimercati C, Castiglioni B. Development of a multiplex PCR assay for the identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy products. Mol Cell Pro-bes 2005; 19(5), 299-305.
  • Dhanashekar R, Akkinepalli S, Nellutla A. Milk-borne infections. An analysis of their potential effect on the milk industry. Germs 2012; 2(3): 101.
  • Ertaş N, Gönülalan Z. Kayseri ilinde satılan çiğ sütler-de Staphylococcus aureus ve enterotoksinlerinin varlığı üzerine araştırmalar. Fırat Univ Sağlık Bilim Vet Derg 2010; 24(1): 11-5.
  • Féraudet Tarisse C, Goulard-Huet C, Nia Y, Devilliers K, Marcé D, Dambrune C, Simon S. Highly sensitive and specific detection of staphylococcal entero-toxins SEA, SEG, SEH, and SEI by immunoassay. Toxins 2021; 13(2): 130.
  • Garcia SN, Osburn BI, Jay-Russell MT. One health for food safety, food security, and sustainable food production. Front Sustain Food Syst 2020; 4: 1.
  • Goto M, Hayashidani H, Takatori K, Hara‐Kudo Y. Rapid detection of enterotoxigenic Staphylococcus aureus harbouring genes for four classical entero-toxins, SEA, SEB, SEC and SED, by loop‐mediated isothermal amplification assay. Lett Appl Microbiol 2007; 45(1): 100-7.
  • Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: cha-racterization and outbreak investigation. FEMS Microbiol Rev 2012; 36(4): 815-36.
  • Kaya H, Ertaş Onmaz N, Gönülalan Z, Al S. Kayseri ilinde tüketime sunulan tavuk etlerinde Staphylo-coccus aureus ve enterotoksin varlığının araştırıl-ması. Erciyes Üniv Vet Fak Derg 2015; 12(2): 93-8.
  • Keyvan E, Yurdakul O, Şen E. Staphylococcal enterotoxins and enterotoxigenic Staphylococcus aureus in raw milk: A screening study. Kocatepe Vet J 2020; 13(2): 104-9.
  • Kou X, Cai H, Huang S, Ni Y, Luo B, Qian H. Prevalence and characteristics of Staphylococcus aureus ısolated from retail raw milk in Northern Xinjiang, China. Front Microbiol 2021; 12: 2187.
  • Liu H, Li S, Meng L, Dong L, Zhao S, Lan X. Prevalence, antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from dairy herds in northern China. J Dairy Sci 2017; 100: 8796-803.
  • Liu C, Shen Y, Yang M, Chi K, Guo N. Hazard of Staphylococcal enterotoxins in food and promising strategies for natural products against virulence. J Agric Food Chem 2022; 70(8): 2450-65.
  • Morandi S, Brasca M, Lodi R, Cremonesi P, Castigli-oni B. Detection of classical enterotoxins and identification of enterotoxin genes in Staphylococcus aureus from milk and dairy products. Vet Microbiol 2007; 124(1-2): 66-72.
  • Normanno G, Firinu A, Virgilio S, Mula G, Dambrosio A, Poggiu A, Celano GV. Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol 2005; 98(1): 73-9.
  • Oliveira D, Borges A, Simões M. Staphylococcus aureus toxins and their molecular activity in infectious diseases. Toxins 2018; 10(6): 252.
  • Oliveira R, Pinho E, Almeida G, Azevedo NF, Almei-da C. Prevalence and diversity of Staphylococcus aureus and staphylococcal enterotoxins in raw milk from Northern Portugal. Front Microbiol 2022; 13: 703.
  • Omwenga I, Aboge GO, Mitema ES, Obiero G, Ngaywa C, Ngwili N, Bett B. Staphylococcus au-reus enterotoxin genes detected in milk from vari-ous livestock species in northern pastoral region of Kenya. Food Control 2019; 103: 126-32.
  • Rahimi E, Momtaz H, Shakerian A, Kavyani HR. The detection of classical enterotoxins of Staphylococ-cus aureus in raw cow milk using the ELISA met-hod. Turkish J Vet Anim Sci 2012; 36(3): 319-22.
  • Sankomkai W, Boonyanugomol W, Kraisriwattana K, Nutchanon J, Boonsam K, Kaewbutra S, Wongboot W. Characterisation of classical enterotoxins, virulence activity, and antibiotic susceptibility of Staphylococcus aureus isolated from Thai fermen-ted pork sausages, clinical samples, and healthy carriers in northeastern Thailand. J Vet Res 2020; 64(2): 289.
  • Sudhanthiramani S, Swetha CS, Bharathy S. Preva-lence of antibiotic resistant Staphylococcus aureus from raw milk samples collected from the local ven-dors in the region of Tirupathi, India. Vet World 2015; 8(4): 478-81.
  • TGK (Türk Gıda Kodeksi) 2000. Mikrobiyolojik Kriter-ler Tebliği. Tarım ve Köy İşleri Bakanlığı, 23960, Tebliğ No: 2001-19, Ankara, Türkiye.
  • Yıbar A, Küçük SC. Çiğ süt ve pastörize süt tüketimi-nin halk sağlığı üzerine etkileri. Food and Health 2019; 5(3): 197-204.
  • Yildirim T, Sadati F, Kocaman B, Siriken B. Staphylococcus aureus and Staphylococcal enterotoxin detection in raw milk and cheese origin coagulase positive isolates. IJSL 2019; 1(1): 30-41.
  • Yin HY, Fang TJ, Wen HW. Combined multiplex loop‐mediated isothermal amplification with lateral flow assay to detect sea and seb genes of enterotoxic Staphylococcus aureus. Lett Appl Microbiol 2016; 63(1): 16-24.
  • Zeinhom M, Abed A. Prevalence, characterization, and control of Staphylococcus aureus isolated from raw milk and Egyptian soft cheese. J Vet Med Res 2020; 27(2): 152-60.
  • Zhang J, Wang J, Jin J, Li X, Zhang H, Shi X, Zhao C. Prevalence, antibiotic resistance, and entero-toxin genes of Staphylococcus aureus isolated from milk and dairy products worldwide: A systematic review and meta-analysis. Food Res Int 2022; 162: 111969.
There are 29 citations in total.

Details

Primary Language Turkish
Subjects Veterinary Food Hygiene and Technology
Journal Section Articles
Authors

Candan Güngör 0000-0002-4321-2770

Dursun Alp Gündoğ 0000-0002-1581-1813

Yasin Özkaya 0000-0002-4746-5492

Nurhan Ertaş Onmaz 0000-0002-4679-6548

Publication Date August 2, 2024
Submission Date December 6, 2023
Acceptance Date February 26, 2024
Published in Issue Year 2024 Volume: 21 Issue: 2

Cite

APA Güngör, C., Gündoğ, D. A., Özkaya, Y., Ertaş Onmaz, N. (2024). Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus aureus ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 21(2), 86-91. https://doi.org/10.32707/ercivet.1515151
AMA Güngör C, Gündoğ DA, Özkaya Y, Ertaş Onmaz N. Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus aureus ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması. Erciyes Üniv Vet Fak Derg. August 2024;21(2):86-91. doi:10.32707/ercivet.1515151
Chicago Güngör, Candan, Dursun Alp Gündoğ, Yasin Özkaya, and Nurhan Ertaş Onmaz. “Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus Aureus Ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 21, no. 2 (August 2024): 86-91. https://doi.org/10.32707/ercivet.1515151.
EndNote Güngör C, Gündoğ DA, Özkaya Y, Ertaş Onmaz N (August 1, 2024) Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus aureus ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 21 2 86–91.
IEEE C. Güngör, D. A. Gündoğ, Y. Özkaya, and N. Ertaş Onmaz, “Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus aureus ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması”, Erciyes Üniv Vet Fak Derg, vol. 21, no. 2, pp. 86–91, 2024, doi: 10.32707/ercivet.1515151.
ISNAD Güngör, Candan et al. “Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus Aureus Ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 21/2 (August 2024), 86-91. https://doi.org/10.32707/ercivet.1515151.
JAMA Güngör C, Gündoğ DA, Özkaya Y, Ertaş Onmaz N. Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus aureus ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması. Erciyes Üniv Vet Fak Derg. 2024;21:86–91.
MLA Güngör, Candan et al. “Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus Aureus Ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, vol. 21, no. 2, 2024, pp. 86-91, doi:10.32707/ercivet.1515151.
Vancouver Güngör C, Gündoğ DA, Özkaya Y, Ertaş Onmaz N. Çeşitli Hayvan Türlerine Ait Çiğ Sütlerde Staphylococcus aureus ve Stafilokokal Enterotoksinlerin Varlığının Araştırılması. Erciyes Üniv Vet Fak Derg. 2024;21(2):86-91.