Research Article
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Year 2019, Volume: 5 Issue: 4, 227 - 238, 01.10.2019

Fatma Öztürk , Abdulkadir Halkman

https://doi.org/10.3153/FH19024

Abstract

References

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  • Berk, P.A., De Jonge, R., Zwietering, M.H., Abee, T., Kieboom, J. (2005). Acid resistance variability among isolates of Salmonella enterica serovar Typhimurium DT104. Journal of Applied Microbiology, 99(4), 859-866. https://doi.org/10.1111/j.1365-2672.2005.02658.x PMid:16162237
  • Cacace, G., Mazzeo, M.F., Sorrentino, A., Spada, V., Malorni, A., Siciliano, R.A. (2010). Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. Journal of Proteomics, 73(10), 2021-2030. https://doi.org/10.1016/j.jprot.2010.06.011 PMid:20620249
  • Calicioglu, M., Sofos, J.N., Samelis, J., Kendall, P.A., Smith, G.C. (2002). Destruction of acid-and non-adapted Listeria monocytogenes during drying and storage of beef jerky. Food Microbiology, 19(6), 545-559. https://doi.org/10.1006/fmic.2002.0510
  • Cataldo, G., Conte, M.P., Chiarini, F., Seganti, L., Ammendolia, M.G., Superti, F., Longhi, C. (2007). Acid adaptation and survival of Listeria monocytogenes in Italian‐style soft cheeses. Journal of Applied Microbiology, 103(1), 185-193. https://doi.org/10.1111/j.1365-2672.2006.03218.x PMid:17584464
  • Calvo, T., Álvarez-Ordóñez, A., Prieto, M., González-Raurich, M., López, M. (2016). Influence of processing parameters and stress adaptation on the inactivation of Listeria monocytogenes by Non-Thermal Atmospheric Plasma (NTAP). Food Research International, 89, 631-637. https://doi.org/10.1016/j.foodres.2016.09.014 PMid:28460960
  • Cheng, H.Y., Yu, R.C., Chou, C.C. (2003). Increased acid tolerance of Escherichia coli O157:H7 as affected by acid adaptation time and conditions of acid challenge. Food Research International, 36(1), 49-56. https://doi.org/10.1016/S0963-9969(02)00107-2
  • Chung, D., Cho, T.J., Rhee, M.S. (2018). Citrus fruit extracts with carvacrol and thymol eliminated 7-log acid-adapted Escherichia coli O157: H7, Salmonella typhimurium, and Listeria monocytogenes: A potential of effective natural antibacterial agents. Food Research International, 107, 578-588. https://doi.org/10.1016/j.foodres.2018.03.011 PMid:29580522
  • Dalmış, Ü., Soyer, A. (2008). Effect of processing methods and starter culture (Staphylococcus xylosus and Pediococcus pentosaceus) on proteolytic changes in Turkish sausages (sucuk) during ripening and storage. Meat Science, 80, 345-354. https://doi.org/10.1016/j.meatsci.2007.12.022 PMid:22063339
  • Drevets, D.A., Bronze, M.S. (2008). Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunology & Medical Microbiology, 53(2), 151-165. https://doi.org/10.1111/j.1574-695X.2008.00404.x PMid:18462388
  • Ensoy, Ü. (2004). Hindi sucuğu üretiminde starter kültür kullanımı ve ısıl işlem uygulamasının ürün karakteristikleri üzerine etkisi. Doktora Tezi, Ankara Üniversitesi Gıda Mühendisliği Anabilim Dalı, 138 s., Ankara.
  • Erkmen, O. (2009). Survival of Staphylococcus aureus and aerobic bacteria in sucuks made from starter culture and Thymbra spicata during manufacturing and storage. Food and Bioproducts Processing, 87, 62-67. https://doi.org/10.1016/j.fbp.2008.02.006
  • Erol I, Çelik T.H, Şireli U.T, Özdemir H. (1999). Bakteriyosin oluşturan starter kültürlerin fermente Türk sucuklarında Listeria monocytogenes üzerine etkisi. Turkish Journal of Veterinary and Animal Science, 23, 793-802.
  • Ferrari, E., Walter, M.C., Huptas, C., Scherer, S., Müller-Herbst, S. (2017). Complete circular genome sequence and temperature ındependent adaptation to anaerobiosis of Listeria weihenstephanensis DSM 24698. Frontiers in Microbiology, 8, 1672. https://doi.org/10.3389/fmicb.2017.01672 PMid:28919887 PMCid:PMC5585140
  • Francis, G.A., O'beirne, D. (2001). Effects of acid adaptation on the survival of Listeria monocytogenes on modified atmosphere packaged vegetables. International Journal of Food Science & Ttechnology, 36(5), 477-487. https://doi.org/10.1046/j.1365-2621.2001.00489.x
  • Gahan, C.G., Hill, C. (2014). Listeria monocytogenes: survival and adaptation in the gastrointestinal tract. Frontiers in Cellular and Infection Microbiology, 4(9), 1-7. https://doi.org/10.3389/fcimb.2014.00009 PMid:24551601 PMCid:PMC3913888
  • Gahan, C.G., O'Driscoll, B., Hill, C. (1996). Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Applied and Environmental Microbiology, 62(9), 3128-3132.
  • Giaouris, E., Chorianopoulos, N., Nychas, G.J. (2014). Impact of acid adaptation on attachment of Listeria monocytogenes to stainless steel during long-term incubation under low or moderate temperature conditions and on subsequent recalcitrance of attached cells to lethal acid treatments. International Journal of Food Microbiology, 171, 1-7. https://doi.org/10.1016/j.ijfoodmicro.2013.11.013 PMid:24296256
  • Guariglia-Oropeza, V., Orsi, R.H., Guldimann, C., Wiedmann, M., Boor, K.J. (2018). The Listeria monocytogenes bile stimulon under acidic conditions is characterized by strain-specific patterns and the upregulation of motility, cell wall modification functions, and the prfa regulon. Frontiers in Microbiology, 9(120), 1-18. https://doi.org/10.3389/fmicb.2018.00120 PMid:29467736 PMCid:PMC5808219
  • Hampikyan, H., Uğur, M. (2007). The effect of nisin on L. monocytogenes in Turkish fermented sausages (sucuks). Meat Science, 76, 327-332. https://doi.org/10.1016/j.meatsci.2006.11.014 PMid:22064303
  • Harrigan W.F. (1998). Laboratory methods in food microbiology. 3rd ed. San Diego, CA, USA: Academic Press
  • Hingston, P., Chen, J., Allen, K., Hansen, L.T., Wang, S. (2017). Strand specific RNA-sequencing and membrane lipid profiling reveals growth phase-dependent cold stress response mechanisms in Listeria monocytogenes. PloS One, 12(6), e0180123. https://doi.org/10.1371/journal.pone.0180123 PMid:28662112 PMCid:PMC5491136
  • Ijabadeniyi, O.A., Mnyandu, E. (2017). Inactivation of heat adapted and chlorine adapted Listeria monocytogenes ATCC 7644 on tomatoes using sodium dodecyl sulphate, levulinic acid and sodium hypochlorite solution. Italian Journal of Food Safety, 6(2), 65-69. https://doi.org/10.4081/ijfs.2017.5916 PMid:28713785 PMCid:PMC5505079
  • Kapetanakou, A.E., Gkerekou, M.A., Vitzilaiou, E.S., Skandamis, P.N. (2017). Assessing the capacity of growth, survival, and acid adaptive response of Listeria monocytogenes during storage of various cheeses and subsequent simulated gastric digestion. International Journal of Food Microbiology, 246, 50-63. https://doi.org/10.1016/j.ijfoodmicro.2017.01.015 PMid:28189900
  • Kara, R., Akkaya, L. (2010). Geleneksel ve ısıl işlem uygulanarak üretilen Türk sucuklarında Salmonella typhimurium'un gelişimi. Gıda Teknolojileri Elektronik Dergisi, 5(3), 1-8.
  • Karabiyikli, Ş., Değırmencı, H., Karapinar, M. (2017). Inactivation of Listeria monocytogenes in Black Mulberry (Morus nigra) juice. Journal of Food Processing and Preservation, 41(1), e12840. https://doi.org/10.1111/jfpp.12840
  • Kaya, M., Gökalp, H.Y. (2004). Sucuk ürtiminde starter kültür kullanımının ve farklı nitrit dozlarının Listeria monocytogenes'in gelişimi üzerine etkisi. Turkish Journal of Veterinary and Animal Sciences, 28(6), 1121-1127.
  • Koutsoumanis, K.P., Kendall, P.A., Sofos, J.N. (2003). Effect of food processing-related stresses on acid tolerance of Listeria monocytogenes. Applied and Environmental Microbiology, 69(12), 7514-7516. https://doi.org/10.1128/AEM.69.12.7514-7516.2003 PMid:14660405 PMCid:PMC309912
  • Koutsoumanis, K.P., Sofos, J.N. (2004). Comparative acid stress response of Listeria monocytogenes, Escherichia coli O157: H7 and Salmonella typhimurium after habituation at different pH conditions. Letters in Applied Microbiology, 38(4), 321-326. https://doi.org/10.1111/j.1472-765X.2004.01491.x PMid:15214733
  • Lee, I.S., Slonczewski, J.L., Foster, J.W. (1994). A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium. Journal of Bacteriology, 176(5), 1422-1426. https://doi.org/10.1128/jb.176.5.1422-1426.1994 PMid:8113183 PMCid:PMC205208
  • Leyer, G.J., Wang, L.L., Johnson, E.A. (1995). Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. Applied and Environmental Microbiology, 61(10), 3752-3755.
  • Lindqvist, R., Lindblad, M. (2009). Inactivation of Escherichia coli, Listeria monocytogenes and Yersinia enterocolitica in fermented sausages during maturation/storage. International Journal of Food Microbiology, 129(1), 59-67. https://doi.org/10.1016/j.ijfoodmicro.2008.11.011 PMid:19064299
  • Lou, Y., Yousef, A.E. (1997). Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Applied Environmental Microbiology, 63(4), 1252-1255.
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CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?

Year 2019, Volume: 5 Issue: 4, 227 - 238, 01.10.2019

Fatma Öztürk , Abdulkadir Halkman

https://doi.org/10.3153/FH19024

Abstract

In this research, acid
resistance levels of Listeria
monocytogenes have been examined under the conditions of acid adaptations.
In addition, the effect of acid adaptation on the survival of L. monocytogenes in sucuk have also been
determined. L. monocytogenes were
adapted to pH 4.5 for the periods of 1, 2, 3 and 4 hours. The survival of L. monocytogenes that were adapted to
acid have been ascertained at pH 2.5, 3.0 and 3.5 respectively. It has been
found that HCl acid adaptations at pH 3.5 have resulted in no increase in the
survival of L. monocytogenes. A
three-hour adaptation process has led to an increase in survival level at pH 2.5
while 1, 2, 3 or 4-hour adaptation processes lead to an increase in survival
level at pH 3.0. However, it was found that the survival level of L. monocytogenes in sucuk did not
increase as a result of acid adaptation procedure. Acid adapted pathogens have
many risks for food safety and human health. 
These pathogens maintain their viability in acidic foods and cause
foodborne diseases. Therefore, understanding the mechanisms of acid adaptation
of pathogens will help to create more effective food safety systems and will
play a role in the prevention of foodborne diseases.

Keywords

Acid adaptation Inorganic acids HCl Listeria monocytogenes Sucuk

References

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  • Bergholz, T.M., Shah, M.K., Burall, L.S., Rakic-Martinez, M., Datta, A.R. (2018). Genomic and phenotypic diversity of Listeria monocytogenes clonal complexes associated with human listeriosis. Applied Microbiology and Biotechnology, 102(8), 3475-3485. https://doi.org/10.1007/s00253-018-8852-5 PMid:29500754
  • Berk, P.A., De Jonge, R., Zwietering, M.H., Abee, T., Kieboom, J. (2005). Acid resistance variability among isolates of Salmonella enterica serovar Typhimurium DT104. Journal of Applied Microbiology, 99(4), 859-866. https://doi.org/10.1111/j.1365-2672.2005.02658.x PMid:16162237
  • Cacace, G., Mazzeo, M.F., Sorrentino, A., Spada, V., Malorni, A., Siciliano, R.A. (2010). Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. Journal of Proteomics, 73(10), 2021-2030. https://doi.org/10.1016/j.jprot.2010.06.011 PMid:20620249
  • Calicioglu, M., Sofos, J.N., Samelis, J., Kendall, P.A., Smith, G.C. (2002). Destruction of acid-and non-adapted Listeria monocytogenes during drying and storage of beef jerky. Food Microbiology, 19(6), 545-559. https://doi.org/10.1006/fmic.2002.0510
  • Cataldo, G., Conte, M.P., Chiarini, F., Seganti, L., Ammendolia, M.G., Superti, F., Longhi, C. (2007). Acid adaptation and survival of Listeria monocytogenes in Italian‐style soft cheeses. Journal of Applied Microbiology, 103(1), 185-193. https://doi.org/10.1111/j.1365-2672.2006.03218.x PMid:17584464
  • Calvo, T., Álvarez-Ordóñez, A., Prieto, M., González-Raurich, M., López, M. (2016). Influence of processing parameters and stress adaptation on the inactivation of Listeria monocytogenes by Non-Thermal Atmospheric Plasma (NTAP). Food Research International, 89, 631-637. https://doi.org/10.1016/j.foodres.2016.09.014 PMid:28460960
  • Cheng, H.Y., Yu, R.C., Chou, C.C. (2003). Increased acid tolerance of Escherichia coli O157:H7 as affected by acid adaptation time and conditions of acid challenge. Food Research International, 36(1), 49-56. https://doi.org/10.1016/S0963-9969(02)00107-2
  • Chung, D., Cho, T.J., Rhee, M.S. (2018). Citrus fruit extracts with carvacrol and thymol eliminated 7-log acid-adapted Escherichia coli O157: H7, Salmonella typhimurium, and Listeria monocytogenes: A potential of effective natural antibacterial agents. Food Research International, 107, 578-588. https://doi.org/10.1016/j.foodres.2018.03.011 PMid:29580522
  • Dalmış, Ü., Soyer, A. (2008). Effect of processing methods and starter culture (Staphylococcus xylosus and Pediococcus pentosaceus) on proteolytic changes in Turkish sausages (sucuk) during ripening and storage. Meat Science, 80, 345-354. https://doi.org/10.1016/j.meatsci.2007.12.022 PMid:22063339
  • Drevets, D.A., Bronze, M.S. (2008). Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunology & Medical Microbiology, 53(2), 151-165. https://doi.org/10.1111/j.1574-695X.2008.00404.x PMid:18462388
  • Ensoy, Ü. (2004). Hindi sucuğu üretiminde starter kültür kullanımı ve ısıl işlem uygulamasının ürün karakteristikleri üzerine etkisi. Doktora Tezi, Ankara Üniversitesi Gıda Mühendisliği Anabilim Dalı, 138 s., Ankara.
  • Erkmen, O. (2009). Survival of Staphylococcus aureus and aerobic bacteria in sucuks made from starter culture and Thymbra spicata during manufacturing and storage. Food and Bioproducts Processing, 87, 62-67. https://doi.org/10.1016/j.fbp.2008.02.006
  • Erol I, Çelik T.H, Şireli U.T, Özdemir H. (1999). Bakteriyosin oluşturan starter kültürlerin fermente Türk sucuklarında Listeria monocytogenes üzerine etkisi. Turkish Journal of Veterinary and Animal Science, 23, 793-802.
  • Ferrari, E., Walter, M.C., Huptas, C., Scherer, S., Müller-Herbst, S. (2017). Complete circular genome sequence and temperature ındependent adaptation to anaerobiosis of Listeria weihenstephanensis DSM 24698. Frontiers in Microbiology, 8, 1672. https://doi.org/10.3389/fmicb.2017.01672 PMid:28919887 PMCid:PMC5585140
  • Francis, G.A., O'beirne, D. (2001). Effects of acid adaptation on the survival of Listeria monocytogenes on modified atmosphere packaged vegetables. International Journal of Food Science & Ttechnology, 36(5), 477-487. https://doi.org/10.1046/j.1365-2621.2001.00489.x
  • Gahan, C.G., Hill, C. (2014). Listeria monocytogenes: survival and adaptation in the gastrointestinal tract. Frontiers in Cellular and Infection Microbiology, 4(9), 1-7. https://doi.org/10.3389/fcimb.2014.00009 PMid:24551601 PMCid:PMC3913888
  • Gahan, C.G., O'Driscoll, B., Hill, C. (1996). Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Applied and Environmental Microbiology, 62(9), 3128-3132.
  • Giaouris, E., Chorianopoulos, N., Nychas, G.J. (2014). Impact of acid adaptation on attachment of Listeria monocytogenes to stainless steel during long-term incubation under low or moderate temperature conditions and on subsequent recalcitrance of attached cells to lethal acid treatments. International Journal of Food Microbiology, 171, 1-7. https://doi.org/10.1016/j.ijfoodmicro.2013.11.013 PMid:24296256
  • Guariglia-Oropeza, V., Orsi, R.H., Guldimann, C., Wiedmann, M., Boor, K.J. (2018). The Listeria monocytogenes bile stimulon under acidic conditions is characterized by strain-specific patterns and the upregulation of motility, cell wall modification functions, and the prfa regulon. Frontiers in Microbiology, 9(120), 1-18. https://doi.org/10.3389/fmicb.2018.00120 PMid:29467736 PMCid:PMC5808219
  • Hampikyan, H., Uğur, M. (2007). The effect of nisin on L. monocytogenes in Turkish fermented sausages (sucuks). Meat Science, 76, 327-332. https://doi.org/10.1016/j.meatsci.2006.11.014 PMid:22064303
  • Harrigan W.F. (1998). Laboratory methods in food microbiology. 3rd ed. San Diego, CA, USA: Academic Press
  • Hingston, P., Chen, J., Allen, K., Hansen, L.T., Wang, S. (2017). Strand specific RNA-sequencing and membrane lipid profiling reveals growth phase-dependent cold stress response mechanisms in Listeria monocytogenes. PloS One, 12(6), e0180123. https://doi.org/10.1371/journal.pone.0180123 PMid:28662112 PMCid:PMC5491136
  • Ijabadeniyi, O.A., Mnyandu, E. (2017). Inactivation of heat adapted and chlorine adapted Listeria monocytogenes ATCC 7644 on tomatoes using sodium dodecyl sulphate, levulinic acid and sodium hypochlorite solution. Italian Journal of Food Safety, 6(2), 65-69. https://doi.org/10.4081/ijfs.2017.5916 PMid:28713785 PMCid:PMC5505079
  • Kapetanakou, A.E., Gkerekou, M.A., Vitzilaiou, E.S., Skandamis, P.N. (2017). Assessing the capacity of growth, survival, and acid adaptive response of Listeria monocytogenes during storage of various cheeses and subsequent simulated gastric digestion. International Journal of Food Microbiology, 246, 50-63. https://doi.org/10.1016/j.ijfoodmicro.2017.01.015 PMid:28189900
  • Kara, R., Akkaya, L. (2010). Geleneksel ve ısıl işlem uygulanarak üretilen Türk sucuklarında Salmonella typhimurium'un gelişimi. Gıda Teknolojileri Elektronik Dergisi, 5(3), 1-8.
  • Karabiyikli, Ş., Değırmencı, H., Karapinar, M. (2017). Inactivation of Listeria monocytogenes in Black Mulberry (Morus nigra) juice. Journal of Food Processing and Preservation, 41(1), e12840. https://doi.org/10.1111/jfpp.12840
  • Kaya, M., Gökalp, H.Y. (2004). Sucuk ürtiminde starter kültür kullanımının ve farklı nitrit dozlarının Listeria monocytogenes'in gelişimi üzerine etkisi. Turkish Journal of Veterinary and Animal Sciences, 28(6), 1121-1127.
  • Koutsoumanis, K.P., Kendall, P.A., Sofos, J.N. (2003). Effect of food processing-related stresses on acid tolerance of Listeria monocytogenes. Applied and Environmental Microbiology, 69(12), 7514-7516. https://doi.org/10.1128/AEM.69.12.7514-7516.2003 PMid:14660405 PMCid:PMC309912
  • Koutsoumanis, K.P., Sofos, J.N. (2004). Comparative acid stress response of Listeria monocytogenes, Escherichia coli O157: H7 and Salmonella typhimurium after habituation at different pH conditions. Letters in Applied Microbiology, 38(4), 321-326. https://doi.org/10.1111/j.1472-765X.2004.01491.x PMid:15214733
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  • Leyer, G.J., Wang, L.L., Johnson, E.A. (1995). Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. Applied and Environmental Microbiology, 61(10), 3752-3755.
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There are 49 citations in total.

Details

Primary Language Turkish
Subjects Food Engineering
Journal Section Research Articles
Authors

Fatma Öztürk 0000-0003-4763-3801

Abdulkadir Halkman 0000-0001-9987-0732

Publication Date October 1, 2019
Submission Date April 4, 2019
Published in Issue Year 2019Volume: 5 Issue: 4

Cite

APA Öztürk, F., & Halkman, A. (2019). CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?. Food and Health, 5(4), 227-238. https://doi.org/10.3153/FH19024
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