Skip to main content
SpringerLink
Log in

Behavior of histamine-producing bacteria in shimesaba, raw mackerel salted and marinated in vinegar during processing and storage at various temperatures

  • Original Article
  • Food Science and Technology
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

To study the behavior of histamine-producing bacteria during the processing and storage of shimesaba, we inoculated histamine-producing bacteria into raw mackerel and then evaluated bacterial counts and histamine content at each shimesaba processing step. Six histamine-producing bacteria—Morganella morganii, Enterobacter aerogenes, Raoultella planticola, Photobacterium damselae (2 strains), and Photobacterium phosphoreum—were inoculated onto the surface of mackerel fillets at various cell densities (no inoculation, 104, and 107 cfu ml−1). The fillets were then treated according to the common procedure used for processing shimesaba. The concentration of NaCl in brine during the salting procedure was 10 % (w/v), and the main ingredients of the marinade broth were 27 % vinegar, 3.8 % sucrose, 0.3 % sodium glutamate, and 0.1 % sodium succinate. The level of histamine-producing bacteria and of histamine did not increase during the salting and marinating procedures. However, during the storage tests, histamine content increased remarkably in the shimesaba products stored at 10 °C for 3 days, and organoleptical degradation was also observed. However, significant deterioration, based on bacterial count, histamine content, and organoleptic evaluation, was not observed in samples stored at 5 °C. These results indicate that the use of traditional marinade broth during the processing of shimesaba and storage below 5 °C are effective methods for preventing histamine accumulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Fisheries Promotion Division, the Forestry and Fisheries Department, Aomori Prefectural Government (2011) Marine product processing in Aomori prefecture (in Japanese). Fisheries Promotion Division, the Forestry and Fisheries Department, Aomori Prefectural Government, Nagashima, Aomori

  2. Shimomura M, Tsuneki E, Itabashi F, Matsumoto J (1984) Changes in texture and proteins of wahoo meat during marination (in Japanese with English abstract). Cook Sci 17:105–112

    Google Scholar 

  3. Shimomura M, Matsumoto JJ (1985) Changes in texture and proteins during acid-salt curing of mackerel meat (in Japanese with English abstract). Nippon Suisan Gakkaishi 51:583–591

    Article  CAS  Google Scholar 

  4. Toyohara M, Murata M, Ando M, Kubota S, Sakaguchi M, Toyohara H (1999) Texture changes associated with insolubilization of sarcoplasmic proteins during salt-vinegar curing of fish. J Food Sci 64:804–807

    Article  CAS  Google Scholar 

  5. Taylor SL (1986) Histamine food poisoning: toxicology and clinical aspects. Crit Rev Toxicol 17:91–128

    Article  PubMed  CAS  Google Scholar 

  6. Silla Santos MH (1996) Biogenic amines: their importance in foods. Int J Food Microbiol 29:213–231

    Article  PubMed  CAS  Google Scholar 

  7. Lonvaud-Funel A, Joyeux A (1994) Histamine production by wine lactic acid bacteria. Isolation of a histamine-producing strain of Leuconostoc oenos. J Appl Microbiol 77:401–407

    Article  CAS  Google Scholar 

  8. Taylor SL, Keefe TJ, Windham ES, Howell JF (1982) Outbreak of histamine poisoning associated with consumption of Swiss cheese. J Food Prot 45:455–457

    Google Scholar 

  9. Summer SS, Speckhard M, Somers EB, Taylor SL (1985) Isolation of histamine-producing Lactobacillus buchneri from Swiss cheese implicated in a food poisoning outbreak. Appl Environ Microbiol 50:1094–1096

    Google Scholar 

  10. van Poelje PD, Snell EE (1990) Pyruvoyl-dependent enzyme. Annu Rev Biochem 59:29–59

    Article  PubMed  Google Scholar 

  11. Sato T, Fujii T, Masuda M, Okuzumi M (1994) Changes in numbers of histamine-metabolic bacteria and histamine content during storage of common mackerel. Fish Sci 60:299–302

    CAS  Google Scholar 

  12. Takahashi H, Kimura B, Yoshikawa M, Fujii T (2003) Cloning and sequencing of the histidine decarboxylase genes of Gram-negative, histamine-producing bacteria and their application in detection and identification of these organisms in fish. Appl Environ Microbiol 69:2568–2579

    Article  PubMed  CAS  Google Scholar 

  13. Torido Y, Takahashi T, Kuda T, Kimura B (2012) Analysis of the growth of histamine-producing bacteria and histamine accumulation in fish during storage at low temperatures. Food Control 26:174–177

    Article  CAS  Google Scholar 

  14. Ladero V, Calles M, Fernández M, Alvarez MA (2010) Toxicological effects of dietary biogenic amines. Curr Nutr Food Sci 6:145–156

    Article  CAS  Google Scholar 

  15. Spano G, Russo P, Lonvaud-Funel A, Lucas P, Alexandre H, Grandvalet C, Coton E, Coton M, Barnavon L, Bach B, Rattray F, Bunte A, Magni C, Ladero V, Alvarez M, Fernández M, Lopez P, de Palencia PF, Corbi A, Trip H, Lolkema JS (2010) Biogenic amines in fermented foods. Eur J Clin Nutr 64:S95–S100

    Article  PubMed  CAS  Google Scholar 

  16. Recsei PA, Moore WM, Snell EE (1983) Pyruvoyl-dependent histidine decarboxylases from Clostridium perfringens and Lactobacillus buchneri. J Biol Chem 258:439–444

    PubMed  CAS  Google Scholar 

  17. Huynh QK, Snell EE (1985) Pyruvoyl-dependent histidine decarboxylases. J Biol Chem 260:2798–2803

    PubMed  CAS  Google Scholar 

  18. Vanderslice P, Copeland WC, Robertus JD (1986) Cloning and nucleotide sequence of wild type and a mutant histidine decarboxylase from Lactobacillus 30a. J Biol Chem 261:15186–15191

    PubMed  CAS  Google Scholar 

  19. Joosten HMLJ, Northolt MD (1989) Detection, growth, and amine-producing capacity of lactobacilli in cheese. Appl Environ Microbiol 55:2356–2359

    PubMed  CAS  Google Scholar 

  20. Konagaya Y, Kimura B, Ishida M, Fujii T (2002) Purification and properties of a histidine decarboxylase from Tetragenococcus muriaticus, a halophilic lactic acid bacterium. J Appl Microbiol 92:1136–1142

    Article  PubMed  CAS  Google Scholar 

  21. Satomi M, Furushita M, Oikawa H, Yoshikawa-Takahashi M, Yano Y (2008) Analysis of a 30 kbp plasmid encoding histidine decarboxylase gene in Tetragenococcus halophilus isolated from fish sauce. Int J Food Microbiol 126:202–209

    Article  PubMed  CAS  Google Scholar 

  22. Thyssen A, Ollevier F (2005) Genus II. Photobacterium. In: Brenner DJ et al (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn. Springer, New York, pp 546–551

    Google Scholar 

  23. Kim SH, Ben-Gigirey B, Barros-Velázquez J, Price RJ, An H (2000) Histamine and biogenic amine production by Morganella morganii isolated from temperature-abused Albacore. J Food Prot 63:244–251

    PubMed  CAS  Google Scholar 

  24. Lorca TA, Gingerich TM, Pierson MD, Flick GJ, Hackney CR, Summer SS (2001) Growth and histamine formation of Morganella morganii in determining the safety and quality of inoculated and uninoculated Bluefish (Pomatomus Saltatrix). J Food Prot 64:2015–2019

    PubMed  CAS  Google Scholar 

  25. Tsai Y-H, Chang S-C, Kung H-F, Wei C-I, Hwang D-F (2005) Histamine production by Enterobacter aerogenes in sailfish and milkfish at various storage temperatures. J Food Prot 684:1690–1695

    Google Scholar 

  26. Grimont PAD, Grimont F (2005) Genus XVΙ. Klebsiella. In: Brenner DJ et al (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn. Springer, New York, pp 685–693

    Google Scholar 

  27. Morii H, Izumi Y, Kasama K, Ishimoto R (1993) Factors influencing histamine formation by psychrotrophic luminous bacteria Photobacterium phosphoreum (in Japanese with English abstract). Nippon Suisan Gakkaishi 60:773–777

    Article  Google Scholar 

  28. Shimizu U (2001) Science of food microorganism-food microorganism, I-Basic edn (in Japanese). Saiwai syobo, Tokyo

  29. Kimura B, Konagaya Y, Fujii T (2001) Histamine formation by Tetragenococcus muriaticus, a halophilic lactic acid bacterium isolated from fish sauce. Int J Food Microbiol 70:71–77

    Article  PubMed  CAS  Google Scholar 

  30. Tsuruhashi K, Ooizumi T, Akahane Y, Sakai T (2003) Internal migration of sodium chloride, sorbitol and moisture in fish meat during soaking and cold preservation. Fish Sci 69:836–841

    Article  CAS  Google Scholar 

  31. Okuzumi M, Hiraishi A, Kobayashi T, Fujii T (1994) Photobacterium histaminum sp. nov., a histamine-producing marine bacterium. Int J Syst Bacteriol 44:631–636

    Article  CAS  Google Scholar 

  32. Fujii T, Kurihara K, Okuzumi M (1994) Viability and histidine decarboxylase activity of halophilic histamine-forming bacteria during frozen storage. J Food Prot 57:611–613

    CAS  Google Scholar 

  33. Kanki M, Yoda T, Tsukamoto T, Baba E (2007) Histidine decarboxylase and their role in accumulation of histamine in tuna and dried saury. Appl Environ Microbiol 73:1467–1473

    Article  PubMed  CAS  Google Scholar 

  34. Guirard BM, Snell EE (1987) Purification and properties of pyridoxal-5′-phosphate-dependent histidine decarboxylases from Klebsiella planticola and Enterobacter aerogenes. J Bacteriol 169:3963–3968

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. H. Takahashi, Tokyo University of Marine Science and Technology, for supplying the histamine-producing bacteria. We are also grateful to Y. Kado, Department of Agriculture, Forestry and Fisheries, Shimokita District Administration Office, Aomori Prefectural Government, for his assistance with the shimesaba processing. The technical assistance of N. Hatano and N. Sakai is gratefully acknowledged. This work was partly supported by a grant from the research project by the Ministry of Agriculture, Forestry and Fisheries (MAFF), Japan.

Author information

Authors and Affiliations

  1. Food Hygiene and Management Research Group, Research Center for Biochemistry and Food Technology, National Research Institute of Fisheries Science, Fisheries Research Agency, 2-12-4 Fukuura, Yokohama, Kanagawa, 236-8648, Japan

    Ayumi Furutani & Masataka Satomi

  2. Food Research Institute, Aomori Prefectural Industrial Technology Research Center, Hachinohe, Aomori, 031-0831, Japan

    Hisashi Matsubara & Satoru Ishikawa

Authors
  1. Ayumi Furutani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hisashi Matsubara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Satoru Ishikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masataka Satomi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masataka Satomi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Furutani, A., Matsubara, H., Ishikawa, S. et al. Behavior of histamine-producing bacteria in shimesaba, raw mackerel salted and marinated in vinegar during processing and storage at various temperatures. Fish Sci 79, 725–733 (2013). https://doi.org/10.1007/s12562-013-0643-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-013-0643-4

Keywords

Search

Navigation