Public Health and Commercial Impact of Biogenic Amines in Fish

Abstract

Biogenic amines (BAs) are Nitrogen-containing organic compounds that are important in aquaculture and food. BAs are formed by decarboxylation through various chemical reactions with bacterial activities in protein-rich fish and other foods. Biogenic amines are more common in sea fish such as tuna, sardines and mackerel. The presence of biogenic amines has also been found in foods such as spoiled fruits and vegetables. Bacteria-induced histamine poisoning in fish causes allergies as well as various disorders such as headache, flushing, abdominal cramps and hypertension. Many cases of fish poisoning occur due to histamines formed in fish such as Mackerel (Scrombridae) consumed in daily life. Biogenic amines, which are objectionable in terms of food safety, are also formed in cheese, dairy products, fruits and vegetables and other foods rich in protein along with fish. In general, the level of 1000 mg/kg and above in foods is considered a critical and dangerous level for public health.

Keywords

• Histamine
• seafood
• putrescine
• spermidine
• cadaverine

Ethical Statement

Bu çalışma için etik kurul onayı alınmasına gerek yoktur

Balıklardaki Biyojenik Aminlerin Halk Sağlığı ve Ticari Etkisi

Abstract

Biyojenik Aminler (BA), su ürünlerinde, gıdalarda önemli biçimde üreyen Azot bileşimli organik bileşiklerdir. BA’lar, proteince zengin balık ve diğer gıdalardaki bakteriyel faaliyetlerle birlikte çeşitli kimyasal tepkimelerden oluşan dekarboksilasyonla oluşurlar. Biyojen aminler ton balığı, sardalya, uskumru gibi deniz balıklarında daha çok rastlanır. BA’ların varlığı aynı zamanda tüketilen bozulmuş meyve ve sebze gibi besinlerde de görüldüğü belirlenmiştir. Balıklarda oluşan bakteri kaynaklı histamin zehirlenmesi alerji ile birlikte aynı zamanda baş ağrısı, kızarma, karın krampları, hipertansiyon gibi çeşitli rahatsızlıklara da yol açmaktadır. Gündelik yaşamda tüketilen Uskumrugiller (Scrombridae) gibi balıklarda oluşan histaminler nedeniyle birçok balık zehirlenmesi durumu ortaya çıkmaktadır. Gıda güvenliği açısından sakıncalı olan BA’lar, balıklarla birlikte proteince zengin olan peynir, süt mamülleri, meyve-sebze ve diğer gıdalarda da oluşur. Genel olarak besinlerdeki 1000 mg/kg seviyesi ve üzeri, halk sağlığı açısından kritik ve tehlikeli bir düzey kabul edilir.

Keywords

• Histamin
• su ürünleri
• putresin
• spermidin
• kadaverin

Ethical Statement

Bu çalışma için etik kurul onayı alınmasına gerek yoktur.

References

1. Abuhlega, T.A., & Ali, M.R. (2022). Biogenic amines in fish: Prevention and reduction. Journal of Food Processing and Preservation, 46(10), e16883. https://doi.org/10.1111/jfpp.16883
2. Akan, S., & Demirağ, M.K. (2018). Gıdalarda Bulunan Biyojen Aminlerin Önemi ve Detoksifikasyon Mekanizmaları. Food and Health, 4(3), 166-175. https://doi.org/10.3153/FH18017
3. Aksu, H., Çolak, H., Vural, A., & Ergün, Ö. (2014). Uskumru balıklarının (Scomber scomber) histamin düzeyleri üzerine bir araştırma. Gıda ve Yem Bilimi Teknolojisi Dergisi, (6), 21-25.
4. Akyol, V., Kundakçı, A., & Ergönül, B. (2015). Gıdalarda Biyojen Aminler-Biogenic Amines in Foods. Celal Bayar University Journal of Science, 11(2), 294-305. https://doi.org/10.18466/cbujos.89924
5. Alper, N., & Temiz, A. (2001). Gıdalardaki biyojen aminler ve önemi. Türk Hijyen ve Deneysel Biyoloji Dergisi, 58(2), 71-80.
6. Arulkumar, A., Paramithiotis, S., & Paramasivam, S. (2023). Biogenic amines in fresh fish and fishery products and emerging control. Aquaculture and Fisheries, 8(4), 431-450. https://doi.org/10.1016/j.aaf.2021.02.001
7. Biji, K.B., Ravishankar, C.N., Venkateswarlu, R., Mohan, C.O., & Gopal, T.K. (2016). Biogenic amines in seafood: a review. Journal of food science and technology, 53(5), 2210–2218. https://doi.org/10.1007/s13197-016-2224-x
8. Bita, S., & Sharifian, S. (2024). Assessment of biogenic amines in commercial tuna fish: Influence of species, capture method, and processing on quality and safety. Food Chemistry, 435, 137576. https://doi.org/10.1016/j.foodchem.2023.137576

9. Bush, R.K., & Taylor, S.L. (2003). Histamine, Encyclopedia of Food and Nutrition, Caballero, B., Ed. https://doi.org/10.1016/B0-12-227055-X/00597-6
10. Chaidoutis, E., Migdanis, A., Keramydas, D., & Papalexis, P. (2019). Biogenic amines in food as a public health concern An outline of histamine food poisoning. Archives of Hellenic Medicine/Arheia Ellenikes Iatrikes, 36(3). http://hdl.handle.net/11615/72374
11. Comas-Basté, O., Latorre-Moratalla, M.L., Sánchez-Pérez, S., Veciana-Nogués, M.T., & Vidal-Carou, M.D.C. (2019). Histamine and other biogenic amines in food. From scombroid poisoning to histamine intolerance. Biogenic amines, 1. https://doi.org/10.5772/intechopen.84333
12. Dasgupta, D. (2020). Histamine poisoning by bacteria. International Journal of Current Microbiology and Applied Sciences, 9, 3457-3458. https://doi.org/10.20546/ijcmas.2020.908.400
13. DeBeer, J., Bell, J.W., Nolte, F., Arcieri, J., & Correa, G. (2021). Histamine Limits by Country: A Survey and Review. Journal of food protection, 84(9), 1610–1628. https://doi.org/10.4315/JFP-21-129
14. Doeun, D., Davaatseren, M., & Chung, M.S. (2017). Biogenic amines in foods. Food science and biotechnology, 26(6), 1463–1474. https://doi.org/10.1007/s10068-017-0239-3
15. Durak-Dados, A., Michalski, M., & Osek, J. (2020). Histamine and other biogenic amines in food. Journal of Veterinary Research, 64(2), 281-288. https://doi.org/10.2478/jvetres-2020-0029
16. Düz, M., & Fidan, A. (2016). Biyojen Aminler ve Etkileri. Kocatepe Veterinary Journal, 9(2), 114 - 121. https://doi.org/10.5578/kvj.23113
17. EFSA. (2011). European Food Safety Authority. EFSA Panel on Biological Hazards (BIOHAZ). Scientific opinion on risk based control of biogenic amine formation in fermented foods. Efsa Journal, 9(10), 2393. https://doi.org/10.2903/j.efsa.2011.2393
18. Ercan, S.Ş., Soysal, Ç., & Bozkurt, H. (2017). Gıdalarda bulunan biyojen aminlerin insan sağlığı üzerine etkileri. Adıyaman Üniversitesi Sağlık Bilimleri Dergisi, 3(2), 534-550. https://doi.org/10.30569/adiyamansaglik.364782
19. Evangelista, W.P., Silva, T.M., Guidi, L.R., Tette, P.A., Byrro, R.M., Santiago-Silva, P., ... & Gloria, M.B.A. (2016). Quality assurance of histamine analysis in fresh and canned fish. Food chemistry, 211, 100-106. https://doi.org/10.1016/j.foodchem.2016.05.035
20. FAO/WHO. (2013). Food and Agriculture Organization of the United Nations/World Health Organization. Public health risks of histamine and other biogenic amines from fish and fishery products. 1-138. Retrieved from http://www.fao.org/docrep/018/i3390e/i3390e.pdf, Erişim tarihi; 09.02.2024.
21. FDA. (2001). Food and drug administration. Scombro toxin (histamine) formation. Health and human services food and drug administration and U.S. Department. In: Fish and fishery products hazards and controls guide. Washington, DC, P.H.S, 73-93. Retrieved from http://www.fda.gov/cder/Guidance/4252fnl.pdf
22. FDA. (2020). US Food & Drug Administration. Center for Food Safety and. Retrieved from https://www.fda.gov/food/cfsan-constituent-updates/fda-partners-california-department-food-and-agriculture-western-center-food-safety-and-california, Erişim tarihi; 09.02.2024
23. FDA. (2022). Food and Drug Administration Scombrotoxin (histamine) formation. In Fish and Fishery Products Hazards and Controls Guidance; Silver Spring, MD, USA, 113–152. Retrieved from https://www.fda.gov/media/80248/download
24. Filipec, S.V., Valinger, D., Mikac, L., Ivanda, M., Kljusurić, J.G., & Janči, T. (2021). Influence of sample matrix on determination of histamine in fish by surface enhanced Raman spectroscopy coupled with chemometric modelling. Foods, 10(8), 1767. https://doi.org/10.3390/foods10081767
25. Henney, J.E., Taylor, C.L., Boon, C.S., & Institute of Medicine (US) Committee on Strategies to Reduce Sodium Intake. (2010). Preservation and physical property roles of sodium in foods. In Strategies to reduce sodium intake in the United States. National Academies Press (US). 506 pp. http://doi.org/10.17226/12818
26. Houicher, A., Bensid, A., Regenstein, J.M., & Özogul, F. (2021). Control of biogenic amine production and bacterial growth in fish and seafood products using phytochemicals as biopreservatives: A review. Food Bioscience, 39, 100807. https://doi.org/10.1016/j.fbio.2020.100807
27. Hrubisko, M., Danis, R., Huorka, M., & Wawruch, M. (2021). Histamine Intolerance—The More We Know the Less We Know. A Review. Nutrients, 13(7), 2228. https://doi.org/10.3390/nu13072228
28. Hungerford, J.M. (2010). Scombroid poisoning: a review. Toxicon, 56(2), 231-243. https://doi.org/10.1016/j.toxicon.2010.02.006
29. Kim, Y.S., Kim, Y., Park, H., Park, J., & Lee, K.G. (2021). Effects of various pre-treatment and cooking on the levels of biogenic amines in Korean and Norwegian mackerel. Foods, 10(9), 2190. https://doi.org/10.3390/foods10092190
30. Köse, S., (2021). Biogenic Amines in Seafoods and Their Role in Human Health. Gıda Allerjenleri, Bulaşanları ve Halk Sağlığı Açısından Önemi, pp.1-16. Avrasya Üniversitesi Sempozyum bildiri kitabı, 24 - 25 Haziran, 63-78. Trabzon, Türkiye.
31. Kovacova-Hanuskova, E., Buday, T., Gavliakova, S., & Plevkova, J. (2015). Histamine, histamine intoxication and intolerance. Allergologia et immunopathologia, 43(5), 498-506. https://doi.org/10.1016/j.aller.2015.05.001
32. Learoussy, H.Y., Tfeil, H., Dartige, A., & Aarab, L. (2022). Histamine content in fresh and frozen pelagic species from the Mauritanian Atlantic Coast. Emirates Journal of Food and Agriculture, 34(8), 711-716. https://doi.org/10.9755/ejfa.2022.v34.i8.2920
33. Linares, D.M., del Rio, B., Redruello, B., Ladero, V., Martin, M.C., Fernandez, M., ... & Alvarez, M.A. (2016). Comparative analysis of the in vitro cytotoxicity of the dietary biogenic amines tyramine and histamine. Food chemistry, 197, 658-663. https://doi.org/10.1016/j.foodchem.2015.11.013
34. Liu, W., Wang, Q., Mei, J., & Xie, J. (2021). Shelf-life extension of refrigerated turbot (Scophthalmus maximus) by using weakly acidic electrolyzed water and active coatings containing daphnetin emulsions. Frontiers in Nutrition, 8, 696212. https://doi.org/10.3389/fnut.2021.696212
35. Lockley, A.K., & Bardsley, R.G. (2000). Novel method for the discrimination of tuna (Thunnus thynnus) and bonito (Sarda sarda) DNA. Journal of agricultural and food chemistry, 48(10), 4463–4468. https://doi.org/10.1021/jf000387p
36. Ma, X., Bi, J., Li, X., Zhang, G., Hao, H., & Hou, H. (2021). Contribution of microorganisms to biogenic amine accumulation during fish sauce fermentation and screening of novel starters. Foods, 10(11), 2572. https://doi.org/10.3390/foods10112572
37. Maintz, L., & Novak, N. (2007). Histamine and histamine intolerance. The American journal of clinical nutrition, 85(5), 1185-1196. https://doi.org/10.1093/ajcn/85.5.1185
38. Marquardt, D.L. (1983). Histamine. Clinical Reviews in Allergy, 1, 343-351. https://doi.org/10.1007/BF02991225
39. McKay, D.M., & Bienenstock, J. (1994). The interaction between mast cells and nerves in the gastrointestinal tract. Immunology today, 15(11), 533-538. https://doi.org/10.1016/0167-5699(94)90210-0
40. Öksüz, A., Alkan, Ş.B., Taşkın, H., & Ayrancı, M. (2015). Yaşam boyu sağlıklı ve dengeli beslenme için balık tüketiminin önemi. Food and Health. 4(1), 43-62. https://doi.org/10.3153/JFHS18006
41. Omer, A.K., Mohammed, R.R., Ameen, P.S.M., Abas, Z.A., & Ekici, K. (2021). Presence of biogenic amines in food and their public health implications: A review. Journal of food protection, 84(9), 1539-1548. https://doi.org/10.4315/JFP-21-047
42. Özdestan, Ö., & Üren, A., 2014. Gıdalarda Biyojenaminlerle İlgili Yasal Düzenlemeler. Gıda ve yem bilimi teknolojisi dergisi. 12, 27-40.
43. Özogul, Y., Özogul, F., Saad, B., & Tofalo, R. (2019). Biogenic amines in food: analysis, occurrence and toxicity. The Royal Society of Chemistry; London, UK: 2020. pp. 1–17. https://doi.org/10.1039/9781788015813-00001
44. Panula, P., Chazot, P.L., Cowart, M., Gutzmer, R., Leurs, R., Liu, W.L., ... & Haas, H.L. (2015). International union of basic and clinical pharmacology. XCVIII. Histamine receptors. Pharmacological reviews, 67(3), 601-655. https://doi.org/10.1124/pr.114.010249
45. Patel, P., Komorowski, A.S., & Mack, D.P. (2023). An allergist's approach to food poisoning. Annals of Allergy, Asthma & Immunology, 130(4), 444-451. https://doi.org/10.1016/B978-0-323-96018-2.00010-9
46. Pearce, F.L. (1991). Biological effects of histamine: an overview. Agents and actions, 33, 4–7. https://doi.org/10.1007/BF01993112
47. Rachmawati, N., Powell, S., Ross, T., & Tamplin, M. (2023). Characterization of Histamine-Producing Bacteria Isolated During Processing of Indonesian Salted-Boiled Longtail (Thunnus sp.) and Eastern Little Tuna (Euthynnus sp.). Journal of Aquatic Food Product Technology, 32(3), 349-358. https://doi.org/10.1080/10498850.2023.2219248
48. Rai, K.P., Pradhan, H.R., Sharma, B.K., & Rijal, S.K. (2013). Histamine in foods: Its safety and human health implications. Journal of Food Science and Technology Nepal, 8, 1-11. https://doi.org/10.3390/foods8020062
49. Ridolo, E., Martignago, I., Senna, G., & Ricci, G. (2016). Scombroid syndrome: it seems to be fish allergy but... it isn’t. Current Opinion in Allergy and Clinical Immunology, 16(5), 516-521. https://doi.org/10.1097/ACI.0000000000000297
50. Ruiz-Capillas, C., & Herrero, A.M. (2019). Impact of biogenic amines on food quality and safety. Foods, 8(2), 62. https://doi.org/10.3390/foods8020062
51. Ruiz-Capillas, C., & Jiménez-Colmenero, F. (2009). Biogenic amines in seafood products. In Handbook of seafood and seafood products analysis. CRC Press. pp. 851-868.
52. Ruiz-Salmón, I., Laso, J., Margallo, M., Villanueva-Rey, P., Rodríguez, E., Quinteiro, P., ... & Aldaco, R. (2021). Life cycle assessment of fish and seafood processed products–a review of methodologies and new challenges. Science of the Total Environment, 761, 144094. https://doi.org/10.1016/j.scitotenv.2020.144094
53. Santos, M.S. (1996). Biogenic amines: their importance in foods. International journal of food microbiology, 29(2-3), 213-231. https://doi.org/10.1016/0168-1605(95)00032-1
54. Shulpekova, Y.O., Nechaev, V.M., Popova, I.R., Deeva, T.A., Kopylov, A.T., Malsagova, K. A., ... & Ivashkin, V.T. (2021). Food intolerance: The role of histamine. Nutrients, 13(9), 3207. https://doi.org/10.3390/nu13093207
55. Sivasankar, B. (2002). Food processing and preservation. Prentice-Hall of India Pvt.Ltd. New Delhi, pp: 372.
56. SURKOOP, (2023). Su ürünleri kooperatifleri. Türkiye’de su ürünleri üretimi ve Dünya’daki yeri. Retrieved from https://www.sur.coop/gazete/SURKOOP_NISAN_2023.pdf, Erişim tarihi; 07.02.2024.
57. Tabanelli, G. (2020). Biogenic amines and food quality: Emerging challenges and public health concerns. Foods, 9(7), 859. https://doi.org/10.3390/foods9070859
58. Terzi, G. (2008). Deniz ürünlerine bağlı zehirlenmeler ve etkileri. Türk Hijyen ve Deneysel Biyoloji Dergisi. 65 (1), 51-60
59. TGK. (2011). Türk Gıda Kodeksi. Türk gıda kodeksi mikrobiyolojik kriterler yönetmeliği. Resmî Gazete (3. Mükerrer), Sayı: 28157. Retrieved from https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-6.htm, Erişim tarihi; 07.02.2024.
60. TRIDGE, 2022. HS Code: 030487 - Fish fillets; frozen, tunas (of the genus Thunnus), skipjack or stripe-bellied bonito (Euthynnus (Katsuwonus) pelamis). Retrieved from https://www.tridge.com/intelligences/atlantic-bluefin-tuna/export, Erişim tarihi; 07.02.2024.
61. TÜİK, 2022. Türkiye İstatistik Kurumu, Su Ürünleri İstatistikleri 2022 verileri. Retrieved from https://data.tuik.gov.tr/Bulten/Index?p=Fishery-Products-2022-49678, Erişim tarihi; 07.02.2024.
62. Turantaş, F., & Öksüz, A. (1998). Balık ve balık ürünlerinde Biyojen aminler ve amin üretiminde rol oynayan bakteriler. Gıda Teknolojisi, 3(5), 58-65.
63. Ubuka, T. (2021). Histamine. In Handbook of Hormones. Academic Press. pp. 1057-1059. https://doi.org/10.1016/B978-0-12-820649-2.00294-1
64. Uçar, Y., Durmuş, M., Küley, & Korkmaz, K. (2022). Inhibitory Effect of Rosemary Essential Oil and Its Nanoemulsion on the Formation of Biogenic Amines by Food-Borne Pathogens and Fish Spoilage Bacteria. Yuzuncu Yil University Journal of Agricultural Sciences, 32(1), 199-212. https://doi.org/10.29133/yyutbd.1035443
65. Veggeland, F., & Borgen, S.O. (2005). Negotiating international food standards: the World Trade Organization's impact on the Codex Alimentarius Commission. Governance, 18(4), 675-708.
66. Vinci, G., & Maddaloni, L. (2020). Biogenic amines in alcohol-free beverages. Beverages, 6(1), 17. https://doi.org/10.3390/beverages6010017
67. Visciano, P., Schirone, M., & Paparella, A. (2020). An overview of histamine and other biogenic amines in fish and fish products. Foods, 9(12), 1795. https://doi.org/doi:10.3390/foods9121795
68. Vlieg-Boerstra, B.J., Van der Heide, S., Oude Elberink, J.N., Kluin-Nelemans, J.C., & Dubois, A.E. (2005). Mastocytosis and adverse reactions to biogenic amines and histamine-releasing foods: what is the evidence. The Netherlands journal of medicine, 63(7), 244-9.
69. Yongmei, L., Xin, L., Xiaohong, C., Mei, J., Chao, L., & Mingsheng, D. (2007). A survey of biogenic amines in Chinese rice wines. Food Chemistry, 100(4), 1424-1428. https://doi.org/10.1016/j.foodchem.2005.11.035