1. Food and Health
  2. Arşiv
  3. Cilt 5, Sayı 4
Yıl 2019, Cilt 5 , Sayı 4, Sayfalar 227 - 238 2019-10-01

CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?

Fatma ÖZTÜRK [1] , Abdulkadir HALKMAN [2]

Öz

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.

Anahtar Kelimeler

Acid adaptation, Inorganic acids, HCl, Listeria monocytogenes, Sucuk

Kaynakça

  • AOAC. (2000). Official methods of analysis. The association of official analytical chemists (17th ed). Gaithersburg, MD, USA. Methods 925.10, 65.17, 974.24, 992.16
  • 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
  • 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.
  • Mikš-Krajnik, M., Feng, L.X.J., Bang, W.S., Yuk, H.G. (2017). Inactivation of Listeria monocytogenes and natural microbiota on raw salmon fillets using acidic electrolyzed water, ultraviolet light or/and ultrasounds. Food Control, 74, 54-60. https://doi.org/10.1016/j.foodcont.2016.11.033
  • No, D.S., Algburi, A., Huynh, P., Moret, A., Ringard, M., Comito, N., Chikindas, M.L. (2017). Antimicrobial efficacy of curcumin nanoparticles against Listeria monocytogenes is mediated by surface charge. Journal of Food Safety, 37(4), e12353. https://doi.org/10.1111/jfs.12353
  • O'Driscoll, B., Gahan, C.G., Hill, C. (1996). Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Applied and Environmental Microbiology, 62(5), 1693-1698.
  • Omac, B., Moreira, R.G., Castell-Perez, E. (2018). Quantifying growth of cold-adapted Listeria monocytogenes and Listeria innocua on fresh spinach leaves at refrigeration temperatures. Journal of Food Engineering, 224, 17-26. https://doi.org/10.1016/j.jfoodeng.2017.12.022
  • Omori, Y., Miake, K., Nakamura, H., Kage-Nakadai, E., Nishikawa, Y. (2017). Influence of lactic acid and post-treatment recovery time on the heat resistance of Listeria monocytogenes. International Journal of Food Microbiology, 257, 10-18. https://doi.org/10.1016/j.ijfoodmicro.2017.06.008 PMid:28633051
  • Park, J.S., Kim, J.E., Kim, K.S. (2017). Acid resistance and acid adaptation responses of foodborne Escherichia coli isolates. Journal of Food Safety, 37(4), e12352. https://doi.org/10.1111/jfs.12352
  • Öztürk, F., Halkman, A. (2015). Determination of the survival levels of acid-adapted Escherichia coli O157: H7in sucuk (Turkish-type fermented sausage). Turkish Journal of Veterinary and Animal Sciences, 39(4), 485-492. https://doi.org/10.3906/vet-1401-96
  • Phan-Thanh, L., Mahouin, F., Aligé, S. (2000). Acid responses of Listeria monocytogenes. International Journal of Food Microbiology, 55(1-3), 121-126. https://doi.org/10.1016/S0168-1605(00)00167-7
  • Porto-Fett, A.C.S., Hwang, C.A., Call, J.E., Juneja, V.K., Ingham, S.C., Ingham, B.H., Luchansky, J.B. (2008). Viability of multi-strain mixtures of Listeria monocytogenes, Salmonella typhimurium, or Escherichia coli O157:H7 inoculated into the batter or onto the surface of a soudjouk-style fermented semi-dry sausage. Food Microbiology, 25, 793-801. https://doi.org/10.1016/j.fm.2008.04.012 PMid:18620971
  • Santos, J.M., Gonçalves, M.C., Martins, H.A., Pinelli, J.J., Isidoro, S.R., Piccoli, R.H. (2018). Homologous and heterologous adaptation of Listeria spp. to essential oils of condiment plants. Advances in Microbiology, 8(08), 639. https://doi.org/10.4236/aim.2018.88043
  • Soyer, A., Ertaş, A.H., Üzümcüoglu, U. (2005). Effect of processing conditions on the quality of naturally fermented Turkish sausages (sucuks). Meat Science, 69(1), 135-141. https://doi.org/10.1016/j.meatsci.2004.06.015 PMid:22062649
  • Suo, Y., Gao, S., Baranzoni, G.M., Xie, Y., Liu, Y. (2018). Comparative transcriptome RNA-Seq analysis of Listeria monocytogenes with sodium lactate adaptation. Food Control, 91, 193-201. https://doi.org/10.1016/j.foodcont.2018.03.044
  • Tchuenchieu, A., Ngang, J.J.E., Juengue, M., Kamdem, S.S., Etoa, F.X. (2016). Effect of acid adaptation of Listeria monocytogenes on its mild thermal inactivation in a simulated fruit juice supplemented with carvacrol. British Microbiology Research Journal, 15, 1-10. https://doi.org/10.9734/BMRJ/2016/27272
  • Vialette, M., Pinon, A., Chasseignaux, E., Lange, M. (2003). Growths kinetics comparison of clinical and seafood Listeria monocytogenes isolates in acid and osmotic environment. International Journal of Food Microbiology, 82(2), 121-131. https://doi.org/10.1016/S0168-1605(02)00249-0
  • Yıldız-Turp, G., Serhatoğlu, M. (2008). Effect of replacing beef fat with hazelnut oil on quality characteristics of sucuk: A Turkish fermented sausage. Meat Science, 78, 447-454. https://doi.org/10.1016/j.meatsci.2007.07.013 PMid:22062464

Ayrıntılar

Birincil Dil tr
Konular Gıda Bilimi ve Teknolojisi
Bölüm Research Articles
Yazarlar

Orcid: 0000-0003-4763-3801
Yazar: Fatma ÖZTÜRK (Sorumlu Yazar)
Kurum: İzmir Katip Celebi University, Faculty of Fisheries, Department of Fishing and Processing Technology, Ciğli, İzmir
Ülke: Turkey

Orcid: 0000-0001-9987-0732
Yazar: Abdulkadir HALKMAN
Kurum: Ankara University, Faculty of Engineering, Department of Food Engineering, Gölbaşı, Ankara
Ülke: Turkey
Tarihler

Başvuru Tarihi : 4 Nisan 2019
Kabul Tarihi : 4 Haziran 2019
Yayımlanma Tarihi : 1 Ekim 2019

Kaynak Göster

Bibtex @araştırma makalesi { jfhs549225, journal = {Food and Health}, issn = {}, eissn = {2602-2834}, address = {Vidin Caddesi No:28 D:4 Kocamustafapaşa 34107 Fatih İstanbul}, publisher = {Özkan ÖZDEN}, year = {2019}, volume = {5}, pages = {227 - 238}, doi = {10.3153/FH19024}, title = {CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?}, key = {cite}, author = {Öztürk, Fatma and Halkman, Abdulkadir} }
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 . DOI: 10.3153/FH19024
MLA Öztürk, F , Halkman, A . "CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?" . Food and Health 5 (2019 ): 227-238 <http://jfhs.scientificwebjournals.com/tr/pub/issue/46056/549225>
Chicago Öztürk, F , Halkman, A . "CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?". Food and Health 5 (2019 ): 227-238
RIS TY - JOUR T1 - CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)? AU - Fatma Öztürk , Abdulkadir Halkman Y1 - 2019 PY - 2019 N1 - doi: 10.3153/FH19024 DO - 10.3153/FH19024 T2 - Food and Health JF - Journal JO - JOR SP - 227 EP - 238 VL - 5 IS - 4 SN - -2602-2834 M3 - doi: 10.3153/FH19024 UR - https://doi.org/10.3153/FH19024 Y2 - 2019 ER -
EndNote %0 Food and Health CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)? %A Fatma Öztürk , Abdulkadir Halkman %T CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)? %D 2019 %J Food and Health %P -2602-2834 %V 5 %N 4 %R doi: 10.3153/FH19024 %U 10.3153/FH19024
ISNAD Öztürk, Fatma , Halkman, Abdulkadir . "CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?". Food and Health 5 / 4 (Ekim 2019): 227-238 . https://doi.org/10.3153/FH19024
AMA Öztürk F , Halkman A . CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?. Food Health. 2019; 5(4): 227-238.
Vancouver Öztürk F , Halkman A . CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?. Food and Health. 2019; 5(4): 227-238.
IEEE F. Öztürk ve A. Halkman , "CAN ACID ADAPTATION OF Listeria monocytogenes INCREASE SURVIVAL IN SUCUK (A TURKISH DRY-FERMENTED SAUSAGE)?", Food and Health, c. 5, sayı. 4, ss. 227-238, Eki. 2019, doi:10.3153/FH19024
Makalenin Yazarları
Fatma ÖZTÜRK [1]
Abdulkadir HALKMAN [2]
Makale Gönder
Arşiv
Editör Kurulu
İletişim
TR Dizin
TR Dizin

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