Ege Journal of Fisheries and Aquatic Sciences
Research Article
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The impact of high pressure processing on the growth of Photobacterium phosphoreum and biogenic amine formation in marinated herring

Year 2020, Volume 37, Issue 4, 363 - 371, 15.12.2020

İlknur UÇAK Nalan GÖKOĞLU

https://doi.org/10.12714/egejfas.37.4.07

Abstract


The effects of high pressure processing (HPP) on Photobacterium phosphoreum growth and biogenic amine formation were evaluated in marinated herring (prepared with 2% acetic acid+8% NaCl; or 4% acetic acid+8% NaCl solutions). Marinated fish fillets were inoculated with P. phosphoreum, vaccum packaged and treated with HPP in different pressure levels (100, 300, and 500 MPa) and pressure holding times (5 and 10 min). Control was left as untreated for both marination group. All batches were stored at 4±1oC up to 3 months. The results showed that combined effect of HPP and 4% acetic acid had much more inhibitory effect on the growth of P. phosphoreum, especially pressure levels 300 and 500 MPa. During the storage period, H2S-producing bacteria growth was not observed in the groups subjected to 500 MPa pressure. Total psychrophilic bacteria did not grow in 500 MPa pressure treated group and 300 MPa 10 min pressure treated group prepared with 2% acetic acid during the storage period. Histamine was detected insignificant levels in the fillets marinated with 4% acetic acid and treated with HPP. Except for the control group tyramine formation was not found in the samples prepared with 4% acetic acid. Similarly, putrescine was not found in the samples prepared with 2% acetic acid and subjected to HPP treatment at the beginning of the storage. Cadaverine levels were found insignificant amount and 300 and 500 MPa pressure treatments suppressed the formation in 4% acetic acid treated groups compared with 2% acetic acid treated groups. The results of this study revealed that HPP in combination with 4% acetic acid had inhibitory effect on P. phosphoreum growth and suppressed the formation of histamine, tyramine, putrescine and cadaverine. 

Keywords

High pressure treatment, Photobacterium phosphoreum, herring, histamine, biogenic amine

References

  • Atlas, R.M. & Parks, L.C. (1997). Handbook of Microbiologic al Media, 2nd ed. CRC Press, Boca Raton, Florida.
  • Dalgaard, P. (1993). Evaluation and prediction of microbial fish spoilage. Royal Veterinary
  • Dalgaard, P. (2000). Fresh and lightly preserved seafood. In C.M.D. Man, & A.A. Jones (Ed), Shelf life Evaluation of Foods (pp. 110-139). London: Aspen Publishers.
  • Eerola, S. Hinkkanen, R., Lindfors, E. & Hirvi, T. (1993). Liquid chromatographic determination of biogenic amines in dry sausages. Journal of AOAC International, 76, 575-577.
  • Erkan, N. Üretener, G. & Alpas, H. (2010). Effect of high pressure (HP) on the quality and shelf life of red mullet (Mullus surmelutus). Innovative Food Science and Emerging Technologies, 11, 259-264. DOI:10.1016/j.ifset.2010.01.001
  • Food and Drug Administration (FDA) (2011). http://www.fda.gov/FoodGuidance
  • ComplianceRegulatoryInformation/GuidanceDocuments/Seafood/FishandFisheriesProductsHazardsandControlsGuide/default.htm (19/08/2019)
  • Gudbjornsdottir, B. Jonsson, A. Hafsteinsson, H. & Heinz. (2010). Effect of high-pressure processing on Listeria spp. and on the textural and microstructural properties of cold smoked salmon. LWT - Food Science and Technology, 43, 366-374. DOI:10.1016/j.lwt.2009.08.015
  • Herland, H. Esaiassen, M. & Olsen, R.L. (2008). Muscle Quality and Storage Stability of Farmed Cod (Gadus morhua L.) Compared to Wild Cod. Journal of Aquatic Food Product Technology, 16, 55-66. DOI:10.1300/J030v16n04_06
  • Ibrahim Sallam, K. (2007). Antimicrobial and antioxidant effects of sodium acetate, sodium lactate, and sodium citrate in refrigerated sliced salmon. Food Control, 18, 566-575. DOI:10.1016/j.foodcont.2006.02.002
  • ICMSF (1982) Microorganisms in foods. Their significance and methods of enumeration, 2nd edn. London: Univ Toronto Pres.
  • Karim, N.U. Kennedy, T. Linton, M. Watson, S. Gault, N. & Patterson M.F. (2011). Effect of high pressure processing on the quality of herring (Clupea harengus) and haddock (Melanogrammus aeglefinus) stored on ice. Food Control, 22, 476-484. DOI:10.1016/j.foodcont.2010.09.030
  • Kim, D.H. Kim, K.B.W. & Ahn, D.H. (2013). Inhibitory effects of high-hydrostatic-pressure treatments on histamine production in mackerel (Scomber japonicus) muscle inoculated with Morganella morganii and Photobacterium phosphoreum. Food Control, 34, 307-311. DOI:10.1016/j.foodcont.2013.04.032
  • Kim, S.H. Barros-Velazquez, J. Ben-Gigirey, B. Eun, J.B. Jun, S.H. & Wei, C.I. (2003). Identification of the main bacteria contributing to histamine formation in seafood to ensure product safety. Food Science and Biotechnology, 12, 451-460.
  • Krizek, M. Matejkova, K. Vacha, F. & Dadakova, E. (2014). Biogenic amines formation in high-pressure processed pike flesh (Esox lucius) during storage. Food Chemistry, 151, 466-471. DOI:10.1016/j.foodchem.2013.11.094
  • Kural, A.G. & Chen, H. (2008a). Conditions for a 5-log reduction of Vibrio vulnificus in oysters through high hydrostatic pressure treatment. International Journal of Food Microbiology, 122, 180-187. DOI:10.1016/j.ijfoodmicro.2007.11.074
  • Kural, A.G. Shearer, A.E.H. Kingsley, D.H. & Chen, H. (2008b). Conditions for high pressure inactivation of Vibrio parahaemolyticus in oysters. International Journal of Food Microbiology, 127, 1-5. DOI:10.1016/j.ijfoodmicro.2008.05.003
  • Lougovois, V.P. & Kyrana, V.R. (2005). Freshness quality and spoilage of chill-stored fish. Food Policy, Control and Research, 1, 35-86.
  • Matejkova, K. Krizek, M. Vacha, F. & Dadakova, E. (2013). Effect of high-pressure treatment on biogenic amines formation in vacuum-packed trout flesh (Oncorhynchus mykiss). Food Chemistry, 137, 31-36. DOI:10.1016/j.foodchem.2012.10.011
  • Mengden, R. Röhner, A. Sudhaus, N. & Klein, G. (2015). High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus glanis). Innovative Food Science and Emerging Technologies, 32, 9-15. DOI:10.1016/j.ifset.2015.10.002
  • Onal, A. (2007). A review: current analytical methods for the determination of biogenic amines in food. Food Chemistry, 103, 1475-1486. DOI:10.1016/j.foodchem.2006.08.028
  • Reyes, J.E. Tabilo-Munizaga, G. Perez-Won, M. Maluenda, D. & Rocob, D. (2015). Effect of high hydrostatic pressure (HHP) treatments on microbiological shelf-life of chilled Chilean jack mackerel (Trachurus murphyi). Innovative Food Science and Emerging Technologies, 29, 107-112. DOI:10.1016/j.ifset.2015.01.010
  • Ruiz-Capillas, C, Colmenero, F.J. Carrascosa, A.V. & Munoz, R. (2007). Biogenic amine production in Spanish dry-cured ‘‘chorizo’’ sausage treated with high-pressure and kept in chilled storage. Meat Science, 77, 365-371. DOI:10.1016/j.meatsci.2007.03.027
  • Shalaby, A.R. (1996). Significance of biogenic amines to food safety and human health. Food Research International, 29, 675-690.
  • Ten Brink, B. Damirik, C. Joosten, H.M.L.J. & Huis Veld, H.J. (1990). Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology, 11, 73-84.
  • Tsai, Y.H. Lin, C.Y. Chang, S.C. Chen, H.C. Kung, H.F. & Wei, C.I. (2005). Occurrence of histamine and histamine-forming bacteria in salted mackerel in Taiwan. Food Microbiology, 22, 461-467. DOI:10.1016/j.fm.2004.11.003
  • Ucak, I. Gokoglu, N. Toepfl, S. & Galanakis, C.M. (2018). Inhibitory effects of high pressure processing on Photobacterium phosphoreum and Morganella psychrotolerans in vacuum packed herring (Clupea harengus). Journal of Food Safety, 38(6), 1-6. DOI:10.1111/jfs.12519
  • Ucak, I. Gokoglu, N. Toepfl, S. Kiessling, M. & Galanakis, C.M. (2019). Inhibitory effects of high pressure treatment on microbial growth and biogenic amine formation in marinated herring (Clupea harengus) inoculated with Morganella psychrotolerans. LWT- Food Science and Technology, 99, 50-56. DOI:10.1016/j.lwt.2018.09.058

Yüksek basınç işleminin ringa marinatında Photobacterium phosphoreum gelişimi ve biyojen amin üretimi üzerine etkisi

Year 2020, Volume 37, Issue 4, 363 - 371, 15.12.2020

İlknur UÇAK Nalan GÖKOĞLU

https://doi.org/10.12714/egejfas.37.4.07

Abstract


Yüksek hidrostatik basınç işleminin (HPP) ringa marinatında (2% asetik asit+8% NaCl ve 4% asetik asit+8% NaCl solüsyonları ile hazırlanan) Photobacterium phosphoreum gelişimi ve biyojen amin oluşumu üzerine etkileri değerlendirilmiştir. P. phosphoreum ile inoküle edilmiş marine edilmiş balık filetolarına, farklı sürelerde (5 ve 10 dk) ve farklı düzeylerde (100, 300 ve 500 MPa) basınç uygulanmıştır. Her iki marinasyon grubunda da kontrol basınç uygulanmadan bırakılmıştır. Tüm örnekler 4±1oC’de 3 ay depolanmışlardır. Sonuçlar, özellikle 300 ve 500 MPa basınç düzeyleri olmak üzere HPP ve %4 asetik asitin kombine etkisinin P. phosphoreum gelişimi üzerine daha fazla inhibitor etkisi olduğunu göstermiştir. Depolama boyunca 500 MPa basınç uygulanan gruplarda H2S üreten bakteri gelişiminin olmadığını gözlenmiştir. %2 asetik asit ile hazırlanarak 300 MPa 10 dk ve 500 MPa basınç uygulanan gruplarda toplam psikrofilik bakterilere depolama süresince gelişememiştir. %4 asetik asit ile hazırlanan ve HPP uygulanan gruplarda histamine düzeyi önemsiz seviyelerde bulunmuştur. %4 asetik asitle marine edilen gruplarda kontrol grubu dışında tiramin oluşumu gözlenmemiştir. Benzer şekilde %2 asetik asitle hazırlanan ve HPP uygulanan gruplarda da depolama başlangıcında putresin bulunmamıştır. Kadaverin miktarı önemsiz düzeylerde bulunmuş ve %2 asetik asit uygulanan gruplara kıyasla %4 asetik uygulanan gruplarda 300, 500 MPa basınç uygulaması kadaverin oluşumunu baskılamıştır. Bu çalışmanın sonuçları, HPP uygulaması ile %4 asetik asitin kombine bir şekilde kullanımının P. phosphoreum gelişimi ile histamin, tiramin, putresin ve kadaverin oluşumunu baskıladığını göstermektedir.



Keywords

Yüksek basınç uygulaması, Photobacterium phosphoreum, ringa, histamine, biyojen amin

References

  • Atlas, R.M. & Parks, L.C. (1997). Handbook of Microbiologic al Media, 2nd ed. CRC Press, Boca Raton, Florida.
  • Dalgaard, P. (1993). Evaluation and prediction of microbial fish spoilage. Royal Veterinary
  • Dalgaard, P. (2000). Fresh and lightly preserved seafood. In C.M.D. Man, & A.A. Jones (Ed), Shelf life Evaluation of Foods (pp. 110-139). London: Aspen Publishers.
  • Eerola, S. Hinkkanen, R., Lindfors, E. & Hirvi, T. (1993). Liquid chromatographic determination of biogenic amines in dry sausages. Journal of AOAC International, 76, 575-577.
  • Erkan, N. Üretener, G. & Alpas, H. (2010). Effect of high pressure (HP) on the quality and shelf life of red mullet (Mullus surmelutus). Innovative Food Science and Emerging Technologies, 11, 259-264. DOI:10.1016/j.ifset.2010.01.001
  • Food and Drug Administration (FDA) (2011). http://www.fda.gov/FoodGuidance
  • ComplianceRegulatoryInformation/GuidanceDocuments/Seafood/FishandFisheriesProductsHazardsandControlsGuide/default.htm (19/08/2019)
  • Gudbjornsdottir, B. Jonsson, A. Hafsteinsson, H. & Heinz. (2010). Effect of high-pressure processing on Listeria spp. and on the textural and microstructural properties of cold smoked salmon. LWT - Food Science and Technology, 43, 366-374. DOI:10.1016/j.lwt.2009.08.015
  • Herland, H. Esaiassen, M. & Olsen, R.L. (2008). Muscle Quality and Storage Stability of Farmed Cod (Gadus morhua L.) Compared to Wild Cod. Journal of Aquatic Food Product Technology, 16, 55-66. DOI:10.1300/J030v16n04_06
  • Ibrahim Sallam, K. (2007). Antimicrobial and antioxidant effects of sodium acetate, sodium lactate, and sodium citrate in refrigerated sliced salmon. Food Control, 18, 566-575. DOI:10.1016/j.foodcont.2006.02.002
  • ICMSF (1982) Microorganisms in foods. Their significance and methods of enumeration, 2nd edn. London: Univ Toronto Pres.
  • Karim, N.U. Kennedy, T. Linton, M. Watson, S. Gault, N. & Patterson M.F. (2011). Effect of high pressure processing on the quality of herring (Clupea harengus) and haddock (Melanogrammus aeglefinus) stored on ice. Food Control, 22, 476-484. DOI:10.1016/j.foodcont.2010.09.030
  • Kim, D.H. Kim, K.B.W. & Ahn, D.H. (2013). Inhibitory effects of high-hydrostatic-pressure treatments on histamine production in mackerel (Scomber japonicus) muscle inoculated with Morganella morganii and Photobacterium phosphoreum. Food Control, 34, 307-311. DOI:10.1016/j.foodcont.2013.04.032
  • Kim, S.H. Barros-Velazquez, J. Ben-Gigirey, B. Eun, J.B. Jun, S.H. & Wei, C.I. (2003). Identification of the main bacteria contributing to histamine formation in seafood to ensure product safety. Food Science and Biotechnology, 12, 451-460.
  • Krizek, M. Matejkova, K. Vacha, F. & Dadakova, E. (2014). Biogenic amines formation in high-pressure processed pike flesh (Esox lucius) during storage. Food Chemistry, 151, 466-471. DOI:10.1016/j.foodchem.2013.11.094
  • Kural, A.G. & Chen, H. (2008a). Conditions for a 5-log reduction of Vibrio vulnificus in oysters through high hydrostatic pressure treatment. International Journal of Food Microbiology, 122, 180-187. DOI:10.1016/j.ijfoodmicro.2007.11.074
  • Kural, A.G. Shearer, A.E.H. Kingsley, D.H. & Chen, H. (2008b). Conditions for high pressure inactivation of Vibrio parahaemolyticus in oysters. International Journal of Food Microbiology, 127, 1-5. DOI:10.1016/j.ijfoodmicro.2008.05.003
  • Lougovois, V.P. & Kyrana, V.R. (2005). Freshness quality and spoilage of chill-stored fish. Food Policy, Control and Research, 1, 35-86.
  • Matejkova, K. Krizek, M. Vacha, F. & Dadakova, E. (2013). Effect of high-pressure treatment on biogenic amines formation in vacuum-packed trout flesh (Oncorhynchus mykiss). Food Chemistry, 137, 31-36. DOI:10.1016/j.foodchem.2012.10.011
  • Mengden, R. Röhner, A. Sudhaus, N. & Klein, G. (2015). High-pressure processing of mild smoked rainbow trout fillets (Oncorhynchus mykiss) and fresh European catfish fillets (Silurus glanis). Innovative Food Science and Emerging Technologies, 32, 9-15. DOI:10.1016/j.ifset.2015.10.002
  • Onal, A. (2007). A review: current analytical methods for the determination of biogenic amines in food. Food Chemistry, 103, 1475-1486. DOI:10.1016/j.foodchem.2006.08.028
  • Reyes, J.E. Tabilo-Munizaga, G. Perez-Won, M. Maluenda, D. & Rocob, D. (2015). Effect of high hydrostatic pressure (HHP) treatments on microbiological shelf-life of chilled Chilean jack mackerel (Trachurus murphyi). Innovative Food Science and Emerging Technologies, 29, 107-112. DOI:10.1016/j.ifset.2015.01.010
  • Ruiz-Capillas, C, Colmenero, F.J. Carrascosa, A.V. & Munoz, R. (2007). Biogenic amine production in Spanish dry-cured ‘‘chorizo’’ sausage treated with high-pressure and kept in chilled storage. Meat Science, 77, 365-371. DOI:10.1016/j.meatsci.2007.03.027
  • Shalaby, A.R. (1996). Significance of biogenic amines to food safety and human health. Food Research International, 29, 675-690.
  • Ten Brink, B. Damirik, C. Joosten, H.M.L.J. & Huis Veld, H.J. (1990). Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology, 11, 73-84.
  • Tsai, Y.H. Lin, C.Y. Chang, S.C. Chen, H.C. Kung, H.F. & Wei, C.I. (2005). Occurrence of histamine and histamine-forming bacteria in salted mackerel in Taiwan. Food Microbiology, 22, 461-467. DOI:10.1016/j.fm.2004.11.003
  • Ucak, I. Gokoglu, N. Toepfl, S. & Galanakis, C.M. (2018). Inhibitory effects of high pressure processing on Photobacterium phosphoreum and Morganella psychrotolerans in vacuum packed herring (Clupea harengus). Journal of Food Safety, 38(6), 1-6. DOI:10.1111/jfs.12519
  • Ucak, I. Gokoglu, N. Toepfl, S. Kiessling, M. & Galanakis, C.M. (2019). Inhibitory effects of high pressure treatment on microbial growth and biogenic amine formation in marinated herring (Clupea harengus) inoculated with Morganella psychrotolerans. LWT- Food Science and Technology, 99, 50-56. DOI:10.1016/j.lwt.2018.09.058

Details

Primary Language English
Subjects Food Science and Technology
Journal Section Articles
Authors

İlknur UÇAK This is me (Primary Author)
NİĞDE ÖMER HALİSDEMİR ÜNİVERSİTESİ
0000-0002-9701-0824
Türkiye

Nalan GÖKOĞLU>
AKDENİZ ÜNİVERSİTESİ
0000-0002-7868-1972
Türkiye

Supporting Institution Scientific and Technological Research Council of Turkey (TUBITAK), Deutscher Akademischer Austauschdienst (DAAD), The Scientific Research Projects Administration Unit of Akdeniz University
Project Number FDK-2015-273
Publication Date December 15, 2020
Submission Date March 16, 2020
Acceptance Date May 8, 2020
Published in Issue Year 2020, Volume 37Issue 4

Cite

APA Uçak, İ. & Gökoğlu, N. (2020). The impact of high pressure processing on the growth of Photobacterium phosphoreum and biogenic amine formation in marinated herring . Ege Journal of Fisheries and Aquatic Sciences , 37 (4) , 363-371 . DOI: 10.12714/egejfas.37.4.07