Research Article
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Pathogenic potential of Staphylococcus aureus strains isolated from unpackaged ice cream samples sold in Istanbul

Year 2024, , 77 - 84, 03.01.2024

Elif Ede Çintesun , Sine Özmen Togay

https://doi.org/10.3153/FH24007

Abstract

Ice cream is a widely consumed refreshing food, especially in the summer months, and it creates a suitable environment for microbial growth due to its high nutritional value, appropriate pH, and long storage time. This study aimed to evaluate the incidence of enterotoxigenic and meticillin-resistant Staphylococcus aureus in unpackaged ice cream samples sold in Istanbul, Turkey.
For that purpose, 101 unpackaged ice cream samples were collected and evaluated for coagulase activity, DNase activity, and methicillin resistance. Staphylococcus aureus is determined in 66 (65.3%) samples with a mean load of 3.2±1.0 log cfu/mL. 34.6% of samples exceeded the Turkish Food Codex (2009) limit, which ranged between 102 – 103 cfu/g. It was found that 61 (64.8%) of the S. aureus strains were coagulase positive, 21 (22.3%) were DNase positive, and 18 (19.1%) had methicillin resistance. The present study's findings revealed that unpackaged ice cream samples in Istanbul have high enterotoxin-producing potential with a high S. aureus load. The presence of Methicilin-resistant strains may represent a potential hazard to public health.

Keywords

Ice cream Staphylococcus aureus Coagulase DNase Methicillin Resistance

References

  • Ahmed, A.A.-H., Maharik, N.M.S., Valero, A., & Kamal, S.M. (2019). Incidence of enterotoxigenic Staphylococcus aureus in milk and Egyptian artisanal dairy products. Food Control, 104, 20–27. https://doi.org/10.1016/j.foodcont.2019.04.017
  • Al-Ashmawy, M.A., Sallam, K.I., Abd-Elghany, S.M., Elhadidy, M., & Tamura, T. (2016). Prevalence, molecular characterization, and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolated from milk and dairy products. Foodborne Pathogens and Disease, 13(3), 156–162. https://doi.org/10.1089/fpd.2015.2038
  • Al-Bahry, S., Mahmoud, I., Al-Musharafi, S., & Sivakumar, N. (2014). Staphylococcus aureus contamination during food preparation, processing and handling. International Journal of Chemical Engineering and Applications, 5(5), 388. https://doi.org/10.7763/IJCEA.2014.V5.415
  • Algammal, A.M., Hetta, H.F., Elkelish, A., Alkhalifah, D.H.H., Hozzein, W.N., Batiha, G. E.-S., El Nahhas, N., & Mabrok, M.A. (2020). Methicillin-Resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infection and Drug Resistance, 3255–3265. https://doi.org/10.2147/IDR.S272733
  • Anonymous. Ministry of Food, Agriculture and Livestock Turkish Food Codex Microbiological Criteria Regulation. T.C. Official Gazette, 2009.
  • Bartolomeoli, I., Maifreni, M., Frigo, F., Urli, G., & Marino, M. (2009). Occurrence and characterization of Staphylococcus aureus isolated from raw milk for cheesemaking. International Journal of Dairy Technology, 62(3), 366–371. https://doi.org/10.1111/j.1471-0307.2009.00498.x
  • Bingöl, K.K., & Toğay, S.Ö. (2017). Urfa peynirlerinden izole edilen Staphylococcus aureus suşlarında enterotoksin üretim potansiyeli ve metisilin dirençliliği. Akademik Gıda, 15(1), 29–35. https://doi.org/10.24323/akademik-gida.305772
  • Cretenet, M., Even, S., & Le Loir, Y. (2011). Unveiling Staphylococcus aureus enterotoxin production in dairy products: A review of recent advances to face new challenges. Dairy Science & Technology, 91(2), 127–150. https://doi.org/10.1007/s13594-011-0014-9
  • Fetsch, A., Contzen, M., Hartelt, K., Kleiser, A., Maassen, S., Rau, J., Kraushaar, B., Layer, F., & Strommenger, B. (2014). Staphylococcus aureus food-poisoning outbreak associated with the consumption of ice-cream. International Journal of Food Microbiology, 187, 1–6. https://doi.org/10.1016/j.ijfoodmicro.2014.06.017
  • Fındık, A. (2022). Tek Sağlık Yaklaşımında Antibiyotik Dirençliliği. Doğanın Sesi, 5(10), 53–64.
  • Gücükoğlu, A., Çadirci, Ö., Terzi, G., Kevenk, T.O., & Alişarli, M. (2013). Determination of enterotoxigenic and methicillin resistant Staphylococcus aureus in ice cream. Journal of Food Science, 78(5), M738–M741. https://doi.org/10.1111/1750-3841.12093
  • Güçlü, D., Güneş-Bayır, A., Erdoğan, Ö., & Özkan, B. (2022). Determination of microbiological quality of ıce cream sold in Istanbul and their evaluation in terms of public health. KASAV International Journal of Health Sciences, 5(3), 86-93.
  • Gündoğan, N., Citak, S., & Turan, E. (2006). Slime production, DNase activity and antibiotic resistance of Staphylococcus aureus isolated from raw milk, pasteurised milk and ice cream samples. Food Control, 17(5), 389–392. https://doi.org/10.1016/j.foodcont.2005.01.006
  • Hunt, K., Schelin, J., Rådström, P., Butler, F., & Jordan, K. (2012). Classical enterotoxins of coagulase-positive Staphylococcus aureus isolates from raw milk and products for raw milk cheese production in Ireland. Dairy Science & Technology, 1–13. https://doi.org/10.1007/s13594-012-0067-4
  • İrfan, E., & İşeri, Ö. (2004). Stafilokokal enterotoksinler. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 51(3), 239–249.
  • Kateete, D.P., Kimani, C.N., Katabazi, F.A., Okeng, A., Okee, M.S., Nanteza, A., Joloba, M.L., & Najjuka, F.C. (2010). Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Annals of Clinical Microbiology and Antimicrobials, 9(1), 1–7. https://doi.org/10.1186/1476-0711-9-23
  • Lee, A.S., De Lencastre, H., Garau, J., Kluytmans, J., Malhotra-Kumar, S., Peschel, A., & Harbarth, S. (2018). Methicillin-resistant Staphylococcus aureus. Nature Reviews Disease Primers, 4(1), 1–23. https://doi.org/10.1038/nrdp.2018.33
  • Lee, J.H. (2003). Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Applied and Environmental Microbiology, 69(11), 6489–6494. https://doi.org/10.1128/AEM.69.11.6489-6494.2003
  • Li, H., Tang, T., Stegger, M., Dalsgaard, A., Liu, T., & Leisner, J.J. (2021). Characterization of antimicrobial-resistant Staphylococcus aureus from retail foods in Beijing, China. Food Microbiology, 93, 103603. https://doi.org/10.1016/j.fm.2020.103603
  • Martin, J.G.P., e Silva, G. de O., da Fonseca, C.R., Morales, C.B., Silva, C.S.P., Miquelluti, D.L., & Porto, E. (2016). Efficiency of a cleaning protocol for the removal of enterotoxigenic Staphylococcus aureus strains in dairy plants. International Journal of Food Microbiology, 238, 295–301. https://doi.org/10.1016/j.ijfoodmicro.2016.09.018
  • Masihinejad, A., Bonyadian, M., & Motamedifar, M. (2023). Detection of genes encoding enterotoxins (SEA-D) in Staphylococcus aureus strains isolated from workers’ nasal samples and creamy pastries of Shiraz confectioneries. Iranian Journal of Microbiology, 15(2), 251. https://doi.org/10.18502/ijm.v15i2.12477
  • Meyrand, A., Atrache, V., Bavai, C., Montet, M., & Vernozy‐Rozand, C. (1999). An automated method for the detection of staphylococcal heat stable deoxyribonuclease in dairy products. Letters in Applied Microbiology, 29(4), 216–220. https://doi.org/10.1046/j.1365-2672.1999.00595.x
  • Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A., Poggiu, A., Decastelli, L., Mioni, R., Scuota, S., & Bolzoni, G. (2005). Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology, 98(1), 73–79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008
  • Perry, J.D., Davies, A., Butterworth, L.A., Hopley, A.L., Nicholson, A., & Gould, F.K. (2004). Development and evaluation of a chromogenic agar medium for methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology, 42(10), 4519–4523. https://doi.org/10.1128/JCM.42.10.4519-4523.2004
  • Qian, J., Wu, Z., Zhu, Y., & Liu, C. (2023). One Health: A holistic approach for food safety in livestock. Science in One Health, 100015. https://doi.org/10.1016/j.soh.2023.100015
  • Rahimi, E. (2013). Enterotoxigenicity of Staphylococcus aureus isolated from traditional and commercial dairy products marketed in Iran. Brazilian Journal of Microbiology, 44, 393–399. https://doi.org/10.1590/S1517-83822013000200008
  • Salehian, M., Salehifar, E., Esfahanizadeh, M., Karimzadeh, L., Rezaei, R., & Molanejad, M. (2013). Microbial contamination in traditional ice cream and effective factors. Journal of Mazandaran University of Medical Sciences, 23(99), 18–33.
  • Samir, H., Younis, W., Sultan, S., & Abd El-Azeem, M. (2018). Isolation of Staphylococcus aureus from ice-cream samples. Journal of Veterinary and Animal Research, 1, 204.
  • Sergelidis, D., & Angelidis, A. (2017). Methicillin‐resistant Staphylococcus aureus: A controversial food‐borne pathogen. Letters in Applied Microbiology, 64(6), 409–418. https://doi.org/10.1111/lam.12735
  • Shaheen, S., Jaffer, M., Aslam, B., Hussain, K., Khan, A., Ashfaq, M., Ulfat, M., Sardar, A.A., Ahmad, M., & Zafar, M. (2018). Microbial assessment of pathogenic bacterial growth in ice cream and kulfa. Microscopy Research and Technique, 81(12), 1501–1505. https://doi.org/10.1002/jemt.23150
  • Sperber, W. zH, & Tatini, S. (1975). Interpretation of the tube coagulase test for identification of Staphylococcus aureus. Applied Microbiology, 29(4), 502–505. https://doi.org/10.1128/am.29.4.502-505.1975
  • Turkish Food Codex. (2011). Food Codex Regulation on Microbiological Criteria, Official Gazette (29.12.2011/28157). Available at: https://www.mevzuat.gov.tr/File/GeneratePdf?mevzuatNo=15690&mevzuatTur=KurumVeKurulusYonetmeligi&mevzuatTertip=5 (accessed 2023, July 18).
  • Veras, J.F., do Carmo, L.S., Tong, L.C., Shupp, J.W., Cummings, C., Dos Santos, D.A., Cerqueira, M.M.O.P., Cantini, A., Nicoli, J.R., & Jett, M. (2008). A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais, Brazil. International Journal of Infectious Diseases, 12(4), 410–415. https://doi.org/10.1016/j.ijid.2007.09.018
  • Winn, W., Allen, S., & Janda, W. (2006). Woods: Koneman’s Color Atlas and Textbook of Diagnostic Microbiology, 6. Baskı.
  • Zhang, J., Wang, J., Jin, J., Li, X., Zhang, H., & Zhao, C. (2022). Prevalence, antibiotic resistance, and enterotoxin genes of Staphylococcus aureus isolated from milk and dairy products worldwide: A systematic review and meta-analysis. Food Research International, 111969. https://doi.org/10.1016/j.foodres.2022.111969
  • Zhang, P., Liu, X., Zhang, M., Kou, M., Chang, G., Wan, Y., Xu, X., Ruan, F., Wang, Y., & Wang, X. (2022). Prevalence, antimicrobial resistance, and molecular characteristics of staphylococcus aureus and methicillin-resistant staphylococcus aureus from retail ice cream in Shaanxi Province, China. Foodborne Pathogens and Disease, 19(3), 217–225. https://doi.org/10.1089/fpd.2021.0069

Year 2024, , 77 - 84, 03.01.2024

Elif Ede Çintesun , Sine Özmen Togay

https://doi.org/10.3153/FH24007

Abstract

References

  • Ahmed, A.A.-H., Maharik, N.M.S., Valero, A., & Kamal, S.M. (2019). Incidence of enterotoxigenic Staphylococcus aureus in milk and Egyptian artisanal dairy products. Food Control, 104, 20–27. https://doi.org/10.1016/j.foodcont.2019.04.017
  • Al-Ashmawy, M.A., Sallam, K.I., Abd-Elghany, S.M., Elhadidy, M., & Tamura, T. (2016). Prevalence, molecular characterization, and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolated from milk and dairy products. Foodborne Pathogens and Disease, 13(3), 156–162. https://doi.org/10.1089/fpd.2015.2038
  • Al-Bahry, S., Mahmoud, I., Al-Musharafi, S., & Sivakumar, N. (2014). Staphylococcus aureus contamination during food preparation, processing and handling. International Journal of Chemical Engineering and Applications, 5(5), 388. https://doi.org/10.7763/IJCEA.2014.V5.415
  • Algammal, A.M., Hetta, H.F., Elkelish, A., Alkhalifah, D.H.H., Hozzein, W.N., Batiha, G. E.-S., El Nahhas, N., & Mabrok, M.A. (2020). Methicillin-Resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infection and Drug Resistance, 3255–3265. https://doi.org/10.2147/IDR.S272733
  • Anonymous. Ministry of Food, Agriculture and Livestock Turkish Food Codex Microbiological Criteria Regulation. T.C. Official Gazette, 2009.
  • Bartolomeoli, I., Maifreni, M., Frigo, F., Urli, G., & Marino, M. (2009). Occurrence and characterization of Staphylococcus aureus isolated from raw milk for cheesemaking. International Journal of Dairy Technology, 62(3), 366–371. https://doi.org/10.1111/j.1471-0307.2009.00498.x
  • Bingöl, K.K., & Toğay, S.Ö. (2017). Urfa peynirlerinden izole edilen Staphylococcus aureus suşlarında enterotoksin üretim potansiyeli ve metisilin dirençliliği. Akademik Gıda, 15(1), 29–35. https://doi.org/10.24323/akademik-gida.305772
  • Cretenet, M., Even, S., & Le Loir, Y. (2011). Unveiling Staphylococcus aureus enterotoxin production in dairy products: A review of recent advances to face new challenges. Dairy Science & Technology, 91(2), 127–150. https://doi.org/10.1007/s13594-011-0014-9
  • Fetsch, A., Contzen, M., Hartelt, K., Kleiser, A., Maassen, S., Rau, J., Kraushaar, B., Layer, F., & Strommenger, B. (2014). Staphylococcus aureus food-poisoning outbreak associated with the consumption of ice-cream. International Journal of Food Microbiology, 187, 1–6. https://doi.org/10.1016/j.ijfoodmicro.2014.06.017
  • Fındık, A. (2022). Tek Sağlık Yaklaşımında Antibiyotik Dirençliliği. Doğanın Sesi, 5(10), 53–64.
  • Gücükoğlu, A., Çadirci, Ö., Terzi, G., Kevenk, T.O., & Alişarli, M. (2013). Determination of enterotoxigenic and methicillin resistant Staphylococcus aureus in ice cream. Journal of Food Science, 78(5), M738–M741. https://doi.org/10.1111/1750-3841.12093
  • Güçlü, D., Güneş-Bayır, A., Erdoğan, Ö., & Özkan, B. (2022). Determination of microbiological quality of ıce cream sold in Istanbul and their evaluation in terms of public health. KASAV International Journal of Health Sciences, 5(3), 86-93.
  • Gündoğan, N., Citak, S., & Turan, E. (2006). Slime production, DNase activity and antibiotic resistance of Staphylococcus aureus isolated from raw milk, pasteurised milk and ice cream samples. Food Control, 17(5), 389–392. https://doi.org/10.1016/j.foodcont.2005.01.006
  • Hunt, K., Schelin, J., Rådström, P., Butler, F., & Jordan, K. (2012). Classical enterotoxins of coagulase-positive Staphylococcus aureus isolates from raw milk and products for raw milk cheese production in Ireland. Dairy Science & Technology, 1–13. https://doi.org/10.1007/s13594-012-0067-4
  • İrfan, E., & İşeri, Ö. (2004). Stafilokokal enterotoksinler. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 51(3), 239–249.
  • Kateete, D.P., Kimani, C.N., Katabazi, F.A., Okeng, A., Okee, M.S., Nanteza, A., Joloba, M.L., & Najjuka, F.C. (2010). Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Annals of Clinical Microbiology and Antimicrobials, 9(1), 1–7. https://doi.org/10.1186/1476-0711-9-23
  • Lee, A.S., De Lencastre, H., Garau, J., Kluytmans, J., Malhotra-Kumar, S., Peschel, A., & Harbarth, S. (2018). Methicillin-resistant Staphylococcus aureus. Nature Reviews Disease Primers, 4(1), 1–23. https://doi.org/10.1038/nrdp.2018.33
  • Lee, J.H. (2003). Methicillin (oxacillin)-resistant Staphylococcus aureus strains isolated from major food animals and their potential transmission to humans. Applied and Environmental Microbiology, 69(11), 6489–6494. https://doi.org/10.1128/AEM.69.11.6489-6494.2003
  • Li, H., Tang, T., Stegger, M., Dalsgaard, A., Liu, T., & Leisner, J.J. (2021). Characterization of antimicrobial-resistant Staphylococcus aureus from retail foods in Beijing, China. Food Microbiology, 93, 103603. https://doi.org/10.1016/j.fm.2020.103603
  • Martin, J.G.P., e Silva, G. de O., da Fonseca, C.R., Morales, C.B., Silva, C.S.P., Miquelluti, D.L., & Porto, E. (2016). Efficiency of a cleaning protocol for the removal of enterotoxigenic Staphylococcus aureus strains in dairy plants. International Journal of Food Microbiology, 238, 295–301. https://doi.org/10.1016/j.ijfoodmicro.2016.09.018
  • Masihinejad, A., Bonyadian, M., & Motamedifar, M. (2023). Detection of genes encoding enterotoxins (SEA-D) in Staphylococcus aureus strains isolated from workers’ nasal samples and creamy pastries of Shiraz confectioneries. Iranian Journal of Microbiology, 15(2), 251. https://doi.org/10.18502/ijm.v15i2.12477
  • Meyrand, A., Atrache, V., Bavai, C., Montet, M., & Vernozy‐Rozand, C. (1999). An automated method for the detection of staphylococcal heat stable deoxyribonuclease in dairy products. Letters in Applied Microbiology, 29(4), 216–220. https://doi.org/10.1046/j.1365-2672.1999.00595.x
  • Normanno, G., Firinu, A., Virgilio, S., Mula, G., Dambrosio, A., Poggiu, A., Decastelli, L., Mioni, R., Scuota, S., & Bolzoni, G. (2005). Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology, 98(1), 73–79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008
  • Perry, J.D., Davies, A., Butterworth, L.A., Hopley, A.L., Nicholson, A., & Gould, F.K. (2004). Development and evaluation of a chromogenic agar medium for methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology, 42(10), 4519–4523. https://doi.org/10.1128/JCM.42.10.4519-4523.2004
  • Qian, J., Wu, Z., Zhu, Y., & Liu, C. (2023). One Health: A holistic approach for food safety in livestock. Science in One Health, 100015. https://doi.org/10.1016/j.soh.2023.100015
  • Rahimi, E. (2013). Enterotoxigenicity of Staphylococcus aureus isolated from traditional and commercial dairy products marketed in Iran. Brazilian Journal of Microbiology, 44, 393–399. https://doi.org/10.1590/S1517-83822013000200008
  • Salehian, M., Salehifar, E., Esfahanizadeh, M., Karimzadeh, L., Rezaei, R., & Molanejad, M. (2013). Microbial contamination in traditional ice cream and effective factors. Journal of Mazandaran University of Medical Sciences, 23(99), 18–33.
  • Samir, H., Younis, W., Sultan, S., & Abd El-Azeem, M. (2018). Isolation of Staphylococcus aureus from ice-cream samples. Journal of Veterinary and Animal Research, 1, 204.
  • Sergelidis, D., & Angelidis, A. (2017). Methicillin‐resistant Staphylococcus aureus: A controversial food‐borne pathogen. Letters in Applied Microbiology, 64(6), 409–418. https://doi.org/10.1111/lam.12735
  • Shaheen, S., Jaffer, M., Aslam, B., Hussain, K., Khan, A., Ashfaq, M., Ulfat, M., Sardar, A.A., Ahmad, M., & Zafar, M. (2018). Microbial assessment of pathogenic bacterial growth in ice cream and kulfa. Microscopy Research and Technique, 81(12), 1501–1505. https://doi.org/10.1002/jemt.23150
  • Sperber, W. zH, & Tatini, S. (1975). Interpretation of the tube coagulase test for identification of Staphylococcus aureus. Applied Microbiology, 29(4), 502–505. https://doi.org/10.1128/am.29.4.502-505.1975
  • Turkish Food Codex. (2011). Food Codex Regulation on Microbiological Criteria, Official Gazette (29.12.2011/28157). Available at: https://www.mevzuat.gov.tr/File/GeneratePdf?mevzuatNo=15690&mevzuatTur=KurumVeKurulusYonetmeligi&mevzuatTertip=5 (accessed 2023, July 18).
  • Veras, J.F., do Carmo, L.S., Tong, L.C., Shupp, J.W., Cummings, C., Dos Santos, D.A., Cerqueira, M.M.O.P., Cantini, A., Nicoli, J.R., & Jett, M. (2008). A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais, Brazil. International Journal of Infectious Diseases, 12(4), 410–415. https://doi.org/10.1016/j.ijid.2007.09.018
  • Winn, W., Allen, S., & Janda, W. (2006). Woods: Koneman’s Color Atlas and Textbook of Diagnostic Microbiology, 6. Baskı.
  • Zhang, J., Wang, J., Jin, J., Li, X., Zhang, H., & Zhao, C. (2022). Prevalence, antibiotic resistance, and enterotoxin genes of Staphylococcus aureus isolated from milk and dairy products worldwide: A systematic review and meta-analysis. Food Research International, 111969. https://doi.org/10.1016/j.foodres.2022.111969
  • Zhang, P., Liu, X., Zhang, M., Kou, M., Chang, G., Wan, Y., Xu, X., Ruan, F., Wang, Y., & Wang, X. (2022). Prevalence, antimicrobial resistance, and molecular characteristics of staphylococcus aureus and methicillin-resistant staphylococcus aureus from retail ice cream in Shaanxi Province, China. Foodborne Pathogens and Disease, 19(3), 217–225. https://doi.org/10.1089/fpd.2021.0069
There are 36 citations in total.

Details

Primary Language English
Subjects Nutrition and Dietetics (Other)
Journal Section Research Articles
Authors

Elif Ede Çintesun 0000-0001-6103-2784

Sine Özmen Togay 0000-0002-8851-1803

Early Pub Date December 27, 2023
Publication Date January 3, 2024
Submission Date July 21, 2023
Published in Issue Year 2024

Cite

APA Ede Çintesun, E., & Özmen Togay, S. (2024). Pathogenic potential of Staphylococcus aureus strains isolated from unpackaged ice cream samples sold in Istanbul. Food and Health, 10(1), 77-84. https://doi.org/10.3153/FH24007

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