Bacterial production and control of biogenic amines in Asian fermented soybean foods

Foods

Volumn 8, Issue 2, 2019, Pages

  Mah, Jae Hyung ^a   Park, Young Kyoung ^a   Jin, Young Hun ^a   Lee, Jun Hee ^a   Hwang, Han Joon ^a  

^a Korea University   (South Korea)

Author keywords

Bacillus spp; Biogenic amines; Control; Fermented soybean foods; Food safety; Intervention methods; Starter culture

Indexed keywords

EID: 85063199285     PISSN: None     EISSN: 23048158     Source Type: Journal    
DOI: 10.3390/foods8020085     Document Type: Review

References (90)

1. Joosten, H.M.L.J.; Nuñez, M. Prevention of histamine formation in cheese by bacteriocin-producing lactic acid bacteria. Appl. Environ. Microbiol. 1996, 62, 1178-1181. [PubMed]
2. Taylor, S.L.; Guthertz, L.S.; Leatherwood, H.; Tillman, F.; Lieber, E.R. Histamine production by foodborne bacterial species. J. Food Saf. 1978, 1, 173-187. [CrossRef]
3. Shin, D.; Jeong, D. Korean traditional fermented soybean products: Jang. J. Ethn. Foods 2015, 2, 2-7. [CrossRef]
4. Toro-Funes, N.; Bosch-Fuste, J.; Latorre-Moratalla, M.L.; Veciana-Nogués, M.T.; Vidal-Carou, M.C. Biologically active amines in fermented and non-fermented commercial soybean products from the Spanish market. Food Chem. 2015, 173, 1119-1124. [CrossRef] [PubMed]
5. Mah, J.-H. Fermented soybean foods: Significance of biogenic amines. Austin J. Nutr. Food Sci. 2015, 3, 1058.
6. Brink, B.; Damirik, C.; Joosten, H.M.L.J.; Huis In't Veld, J.H.J. Occurrence and formation of biologically active amines in foods. Int. J. Food Microbiol. 1990, 11, 73-84. [CrossRef]
7. Halász, A.; Baráth, Á.; Simon-Sarkadi, L.; Holzapfel, W. Biogenic amines and their production by microorganisms in food. Trends Food Sci. Technol. 1994, 5, 42-49. [CrossRef]
8. Gardini, F.; Özogul, Y.; Suzzi, G.; Tabanelli, G.; Özogul, F. Technological factors affecting biogenic amine content in foods: A review. Front. Microbiol. 2016, 7, 1218. [CrossRef] [PubMed]
9. Stratton, J.E.; Hutkins, R.W.; Taylor, S.L. Biogenic amines in cheese and other fermented foods: A review. J. Food Prot. 1991, 54, 460-470. [CrossRef]
10. Rice, S.L.; Eitenmiller, R.R.; Koehler, P.E. Biologically active amines in foods: A review. J. Milk Food Technol. 1976, 39, 353-358. [CrossRef]
11. Fernández-Reina, A.; Urdiales, J.; Sánchez-Jiménez, F. What we know and what we need to know about aromatic and cationic biogenic amines in the gastrointestinal tract. Foods 2018, 7, 145. [CrossRef] [PubMed]
12. Barbieri, F.; Montanari, C.; Gardini, F.; Tabanelli, G. Biogenic amine production by lactic acid bacteria: A Review. Foods 2019, 8, 17. [CrossRef] [PubMed]
13. Byun, B.Y.; Bai, X.; Mah, J.-H. Bacterial contribution to histamine and other biogenic amine content in Juk (Korean traditional congee) cooked with seafood. Food Sci. Biotechnol. 2013, 22, 1675-1681. [CrossRef]
14. U.S. Food and Drug Administration. Defect action levels for histamine in tuna: Availability of guide. Fed. Reg. 1982, 47, 40487-40488.
15. European Economic Commission (EEC). Council Directive 91/493/EEC of 22 July 1991 laying down the health conditions for the production and the placing on the market of fishery products. Off. J. Eur. Comm. 1991, 268, 15-34.
16. Shalaby, A.R. Significance of biogenic amines to food safety and human health. Food Res. Int. 1996, 29, 675-690. [CrossRef]
17. U.S. Food and Drug Administration (FDA). Fish and Fishery Products Hazards and Controls Guidance, 4th ed.; Center for Food Safety and Applied Nutrition: Rockville, MD, USA, 2011.
18. European Commision (EC). Commission Regulation No. 2073/2005 of 15th November 2005 on microbiological criteria for Foodstuffs. Off. J. Eur. Union 2005, L338, 1-25.
19. European Food Safety Authority (EFSA). Scientific opinion on risk based control of biogenic amine formation in fermented foods. EFSA J. 2011, 9, 2393-2486. [CrossRef]
20. Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO). Joint FAO/WHO Expert Meeting on the Public Health Risk of Histamine and Other Biogenic Amines from Fish and Fishery Products; FAO/WHO: Rome, Italy, 2013.
21. Codex. Discussion paper histamine. In Joint FAO/WHO Food Standards Programme, Codex Committee on Fish and Fishery Products, Thirty-Second Session (CX/FFP 12/32/14), Bali, Indonesia, 1-5 October 2012; FAO/WHO: Rome, Italy, 2012.
22. Food Standards Australia New Zealand (FSANZ). Imported Food Risk Statement Fish and Fish Products from the Families Specifies and Histamine; FSANZ: Canberra, Australia, 2016.
23. The Ministry of Food and Drug Safety (MFDS). Food Code, Notification No. 2017-57; MFDS: Osong, Korea, 2017.
24. China National Standards. GB 2733-2015 National Food Safety Standards for Fresh and Frozen Animal Aquatic Products; Standards Press of China: Beijing, China, 2016.
25. Bai, X.; Byun, B.Y.; Mah, J.-H. Formation and destruction of biogenic amines in Chunjang (a black soybean paste) and Jajang (a black soybean sauce). Food Chem. 2013, 141, 1026-1031. [CrossRef] [PubMed]
26. Byun, B.Y.; Bai, X.; Mah, J.-H. Occurrence of biogenic amines in Doubanjiang and Tofu. Food Sci. Biotechnol. 2013, 22, 55-62. [CrossRef]
27. Byun, B.Y.; Mah, J.-H. Occurrence of biogenic amines in Miso, Japanese traditional fermented soybean paste. J. Food Sci. 2012, 77, T216-T223. [CrossRef] [PubMed]
28. Cho, T.-Y.; Han, G.-H.; Bahn, K.-N.; Son, Y.-W.; Jang, M.-R.; Lee, C.-H.; Kim, S.-H.; Kim, D.-B.; Kim, S.-B. Evaluation of biogenic amines in Korean commercial fermented foods. Korean J. Food Sci. Technol. 2006, 38, 730-737.
29. Kim, T.-K.; Lee, J.-I.; Kim, J.-H.; Mah, J.-H.; Hwang, H.-J.; Kim, Y.-W. Comparison of ELISA and HPLC methods for the determination of biogenic amines in commercial Doenjang and Gochujang. Food Sci. Biotechnol. 2011, 20, 1747-1750. [CrossRef]
30. Ko, Y.-J.; Son, Y.-H.; Kim, E.-J.; Seol, H.-G.; Lee, G.-R.; Kim, D.-H.; Ryu, C.-H. Quality properties of commercial Chungkukjang in Korea. J. Agric. Life Sci. 2012, 46, 1-11.
31. Kung, H.-F.; Tsai, Y.-H.; Wei, C.-I. Histamine and other biogenic amines and histamine-forming bacteria in miso products. Food Chem. 2007, 101, 351-356. [CrossRef]
32. Lee, H.T.; Kim, J.H.; Lee, S.S. Analysis of microbiological contamination and biogenic amines content in traditional and commercial Doenjang. J. Food Hyg. Saf. 2009, 24, 102-109.
33. Oh, S.-J.; Mah, J.-H.; Kim, J.-H.; Kim, Y.-W.; Hwang, H.-J. Reduction of tyramine by addition of Schizandra chinensis Baillon in Cheonggukjang. J. Med. Food 2012, 15, 1109-1115. [CrossRef] [PubMed]
34. Shukla, S.; Park, H.-K.; Kim, J.-K.; Kim, M. Determination of biogenic amines in Korean traditional fermented soybean paste (Doenjang). Food Chem. Toxicol. 2010, 48, 1191-1195. [CrossRef] [PubMed]
35. Tsai, Y.-H.; Chang, S.-C.; Kung, H.-F. Histamine contents and histamine-forming bacteria in natto products in Taiwan. Food Control 2007, 28, 1026-1030. [CrossRef]
36. Tsai, Y.-H.; Kung, H.-F.; Chang, S.-C.; Lee, T.-M.; Wei, C.-I. Histamine formation by histamine-forming bacteria in douchi, a Chinese traditional fermented soybean product. Food Chem. 2007, 103, 1305-1311. [CrossRef]
37. Kim, B.; Byun, B.Y.; Mah, J.-H. Biogenic amine formation and bacterial contribution in Natto products. Food Chem. 2012, 135, 2005-2011. [CrossRef] [PubMed]
38. Shukla, S.; Kim, J.-K.; Kim, M. Occurrence of biogenic amines in soybean food products. In Soybean and Health; El-Shemy, H., Ed.; InTech: Rijeka, Croatia, 2011; pp. 182-184.
39. Onda, T.; Yanagida, F.; Shinohara, T.; Yokotsuka, K. Time series analysis of aerobic bacterial flora during Miso fermentation. Lett. Appl. Microbiol. 2003, 37, 162-168. [CrossRef] [PubMed]
40. Tamang, J.P. Diversity of fermented foods. In Fermented Foods and Beverages of the World; Tamang, J.P., Kailasapathy, K., Eds.; CRC Press: Boca Raton, FL, USA, 2010; pp. 41-84.
41. Ibe, A.; Nishima, T.; Kasai, N. Formation of tyramine and histamine during soybean paste (Miso) fermentation. Jpn. J. Toxicol. Environ. Health 1992, 38, 181-187. [CrossRef]
42. Ibe, A.; Nishima, T.; Kasai, N. Bacteriological properties of and amine-production conditions for tyramine-and histamine-producing bacterial strains isolated from soybean paste (Miso) starting materials. Jpn. J. Toxicol. Environ. Health 1992, 38, 403-409. [CrossRef]
43. Kang, H.-R.; Kim, H.-S.; Mah, J.-H.; Kim, Y.-W.; Hwang, H.-J. Tyramine reduction by tyrosine decarboxylase inhibitor in Enterococcus faecium for tyramine controlled cheonggukjang. Food Sci. Biotechnol. 2018, 27, 87-93. [CrossRef] [PubMed]
44. Oh, E.J.; Oh, M.-H.; Lee, J.M.; Cho, M.S.; Oh, S.S. Characterization of microorganisms in Eoyukjang. Korean J. Food Sci. Technol. 2008, 40, 656-660.
45. Sarkar, P.; Tamang, J.P.; Cook, P.E.; Owens, J. Kinema-a traditional soybean fermented food: Proximate composition and microflora. Food Microbiol. 1994, 11, 47-55. [CrossRef]
46. Yoon, M.Y.; Kim, Y.J.; Hwang, H.-J. Properties and safety aspects of Enterococcus faecium strains isolated from Chungkukjang, a fermented soy product. LWT-Food Sci. Technol. 2008, 41, 925-933. [CrossRef]
47. Coton, E.; Coton, M. Multiplex PCR for colony direct detection of Gram-positive histamine-and tyramine-producing bacteria. J. Microbiol. Methods 2005, 63, 296-304. [CrossRef] [PubMed]
48. Komprda, T.; Sládková, P.; Petirová, E.; Dohnal, V.; Burdychová, R. Tyrosine-and histidine-decarboxylase positive lactic acid bacteria and enterococci in dry fermented sausages. Meat sci. 2010, 86, 870-877. [CrossRef] [PubMed]
49. Jeon, A.R.; Lee, J.H.; Mah, J.-H. Biogenic amine formation and bacterial contribution in Cheonggukjang, a Korean traditional fermented soybean food. LWT-Food Sci. Technol. 2018, 92, 282-289. [CrossRef]
50. Caruso, M.; Fiore, C.; Contursi, M.; Salzano, G.; Paparella, A.; Romano, P. Formation of biogenic amines as criteria for the selection of wine yeasts. World J. Microbiol. Biotechnol. 2002, 18, 159-163. [CrossRef]
51. Izquierdo-Pulido, M.; Font-Fábregas, J.; Vidal-Carou, C. Influence of Saccharomyces cerevisiae var. uvarum on histamine and tyramine formation during beer fermentation. Food Chem. 1995, 54, 51-54.
52. Nout, M.K.R.; Ruiker, M.M.W.; Bouwmeester, H.M.; Beljaars, P.R. Effect of processing conditions on the formation of biogenic amines and ethyl carbamate in soybean tempe. J. Food Saf. 1993, 33, 293-303. [CrossRef]
53. Fuell, C.; Elliott, K.A.; Hanfrey, C.C.; Franceschetti, M.; Michael, A.J. Polyamine biosynthetic diversity in plants and algae. Plant Physiol. Biochem. 2010, 48, 513-520. [CrossRef] [PubMed]
54. Kumar, A.; Taylor, M.A.; Arif, S.A.M.; Davies, H.V. Potato plants expressing antisense and sense S-adenosylmethionine decarboxylase (SAMDC) transgenes show altered levels of polyamines and ethylene: Antisense plants display abnormal phenotypes. Plant J. 1996, 9, 147-158. [CrossRef]
55. Kalaè, P.; Krausová, P. A review of dietary polyamines: Formation, implications for growth, and health and occurrence in foods. Food Chem. 2005, 90, 219-230.
56. Liu, Z.-F.; Wei, Y.-X.; Zhang, J.-J.; Liu, D.-H.; Hu, Y.-Q.; Ye, X.-Q. Changes in biogenic amines during the conventional production of stinky tofu. Int. J. Food Sci. Technol. 2011, 46, 687-694. [CrossRef]
57. Woolridge, D.P.; Vazquez-Laslop, N.; Markham, P.N.; Chevalier, M.S.; Gerner, E.W.; Neyfakh, A.A. Efflux of the natural polyamine spermidine facilitated by the Bacillus subtilis multidrug transporter Blt. J. Biol. Chem. 1997, 272, 8864-8866. [CrossRef] [PubMed]
58. Righetti, L.; Tassoni, A.; Bagni, N. Polyamines content in plant derived food: A comparison between soybean and Jerusalem artichoke. Food Chem. 2008, 111, 852-856. [CrossRef]
59. Kim, J.-H.; Ahn, H.-J.; Kim, D.-H.; Jo, C.; Yook, H.-S.; Park, H.-J.; Byun, M.-W. Irradiation effects on biogenic amines in Korean fermented soybean paste during fermentation. J. Food Sci. 2003, 68, 80-84. [CrossRef]
60. Kim, Y.S.; Cho, S.H.; Jeong, D.Y.; Uhm, T.-B. Isolation of biogenic amines-degrading strains of Bacillus subtilis and Bacillus amyloliquefaciens from traditionally fermented soybean products. Korean J. Microbiol. 2012, 48, 220-224. [CrossRef]
61. Shukla, S.; Lee, J.S.; Park, H.-K.; Yoo, J.-A.; Hong, S.-Y.; Kim, J.-K.; Kim, M. Effect of novel starter culture on reduction of biogenic amines, quality improvement, and sensory properties of Doenjang, a traditional Korean soybean fermented sauce variety. J. Food Sci. 2015, 80, M1794-M1803. [CrossRef] [PubMed]
62. Kim, S.-Y.; Kim, H.-E.; Kim, Y.-S. The potentials of Bacillus licheniformis strains for inhibition of B. cereus growth and reduction of biogenic amines in cheonggukjang (Korean fermented unsalted soybean paste). Food Control 2017, 79, 87-93.
63. Kang, H.-R.; Lee, Y.-L.; Hwang, H.-J. Potential for application as a starter culture of tyramine-reducing strain. J. Korean Soc. Food Sci. Nutr. 2017, 46, 1561-1567. [CrossRef]
64. Mah, J.-H.; Hwang, H.-J. Effects of food additives on biogenic amine formation in Myeolchi-jeot, a salted and fermented anchovy (Engraulis japonicus). Food Chem. 2009, 114, 168-173. [CrossRef]
65. Mah, J.-H.; Kim, Y.J.; Hwang, H.-J. Inhibitory effects of garlic and other spices on biogenic amine production in Myeolchi-jeot, Korean salted and fermented anchovy product. Food Control 2009, 20, 449-454. [CrossRef]
66. Wendakoon, C.N.; Sakaguchi, M. Combined effect of sodium chloride and clove on growth and biogenic amine formation of Enterobacter aerogenes in mackerel muscle extract. J. Food Prot. 1993, 56, 410-413. [CrossRef]
67. Wendakoon, C.N.; Sakaguchi, M. Combined effects of cloves with potassium sorbate and sodium benzoate on the growth and biogenic amine production of Enterobacter aerogenes. Biosci. Biotechnol. Biochem. 1993, 57, 678-679. [CrossRef]
68. Rabie, M.A.; Siliha, H.; el-Saidy, S.; el-Badawy, A.A.; Malcata, F.X. Effects of ?-irradiation upon biogenic amine formation in Egyptian ripened sausages during storage. Innov. Food Sci. Emerg. Technol. 2010, 11, 661-665. [CrossRef]
69. Novella-Rodriguez, S.; Veciana-Nogués, M.T.; Saldo, J.; Vidal-Carou, M.C. Effects of high hydrostatic pressure treatments on biogenic amine contents in goat cheeses during ripening. J. Agric. Food Chem. 2002, 50, 7288-7292. [CrossRef] [PubMed]
70. Ruiz-Capillas, C.; Colmenero, F.J.; Carrascosa, A.V.; Muñoz, R. Biogenic amine production in Spanish dry-cured “chorizo” sausage treated with high-pressure and kept in chilled storage. Meat Sci. 2007, 77, 365-371. [CrossRef] [PubMed]
71. ? C. Eur. Food Res. Technol. 2006, 223, 683-689. [CrossRef]
72. Ruiz-Capillas, C.; Pintado, T.; Jiménez-Colmenero, F. Biogenic amine formation in refrigerated fresh sausage “chorizo” keeps in modified atmosphere. J. Food Biochem. 2012, 36, 449-457. [CrossRef]
73. Ayhan, K.; Kolsarici, N.; Özkan, G.A. The effects of a starter culture on the formation of biogenic amines in Turkish soudjoucks. Meat Sci. 1999, 53, 183-188. [CrossRef]
74. Bover-Cid, S.; Izquierdo-Pulido, M.; Vidal-Carou, M.C. Effect of proteolytic starter cultures of Staphylococcus spp. on biogenic amine formation during the ripening of dry fermented sausages. Int. J. Food Microbiol. 1999, 46, 95-104. [CrossRef]
75. Gardini, F.; Martuscelli, M.; Crudele, M.A.; Pararella, A.; Suzzi, G. Use of Staphylococcus xylosus as a starter culture in dried sausages: Effect on the biogenic amine content. Meat Sci. 2002, 61, 275-283. [CrossRef]
76. Mah, J.-H.; Hwang, H.-J. Inhibition of biogenic amine formation in a salted and fermented anchovy by Staphylococcus xylosus as a protective culture. Food Control 2009, 20, 796-801. [CrossRef]
77. Alvarez, M.A.; Moreno-Arribas, M.V. The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading microorganisms as a solution. Trends Food Sci. Technol. 2014, 39, 146-155. [CrossRef]
78. Naila, A.; Flint, S.; Fletcher, G.; Bremer, P.; Meerdink, G. Control of biogenic amines in food-existing and emerging approaches. J. Food Sci. 2010, 75, R139-R150. [CrossRef] [PubMed]
79. Stadnik, J. Significance of biogenic amines in fermented foods and methods of their control. In Beneficial Microbes in Fermented and Functional Foods; Rai, V.R., Bai, J.A., Eds.; CRC Press: Boca Raton, FL, USA, 2014; pp. 149-163.
80. Carocho, M.; Barreiro, M.F.; Morales, P.; Ferreira, I.C. Adding molecules to food, pros and cons: A review on synthetic and natural food additives. Compr. Rev. Food Sci. Food Saf. 2014, 13, 377-399. [CrossRef]
81. Floros, J.D.; Newsome, R.; Fisher, W.; Barbosa-Cánovas, G.V.; Chen, H.; Dunne, C.P.; German, J.B.; Hall, R.L.; Heldman, D.R.; Karwe, M.V.; et al. Feeding the world today and tomorrow: The importance of food science and technology. Compr. Rev. Food Sci. Food Saf. 2010, 9, 572-599. [CrossRef]
82. Fang, S.-H.; Lai, Y.-J.; Chou, C.-C. The susceptibility of Streptococcus thermophilus 14085 to organic acid, simulated gastric juice, bile salt and disinfectant as influenced by cold shock treatment. Food Microbiol. 2013, 33, 55-60. [CrossRef] [PubMed]
83. Hansen, E.B. Commercial bacterial starter cultures for fermented foods of the future. Int. J. Food Microbiol. 2002, 78, 119-131. [CrossRef]
84. Leroy, F.; De Vuyst, L. Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci. Technol. 2004, 15, 67-78. [CrossRef]
85. Leroy, F.; Verluyten, J.; De Vuyst, L. Functional meat starter cultures for improved sausage fermentation. Int. J. Food Microbiol. 2006, 106, 270-285. [CrossRef] [PubMed]
86. Omafuvbe, B.O.; Abiose, S.H.; Shonukan, O.O. Fermentation of soybean (Glycine max) for soy-daddawa production by starter cultures of Bacillus. Food Microbiol. 2002, 19, 561-566. [CrossRef]
87. Tamang, J.P.; Nikkuni, S. Selection of starter cultures for the production of kinema, a fermented soybean food of the Himalaya. World J. Microbiol. Biotechnol. 1996, 12, 629-635. [CrossRef] [PubMed]
88. Eom, J.S.; Seo, B.Y.; Choi, H.S. Biogenic amine degradation by Bacillus species isolated from traditional fermented soybean food and detection of decarboxylase-related genes. J. Microbiol. Biotechnol. 2015, 25, 1519-1527. [CrossRef] [PubMed]
89. Yi-Chen, L.; Hsien-Feng, K.; Ya-Ling, H.; Chien-Hui, W.; Yu-Ru, H.; Yung-Hsiang, T. Reduction of biogenic amines during miso fermentation by Lactobacillus plantarum as a starter culture. J. Food Prot. 2016, 79, 1556-1561.
90. Ruiz-Capillas, C.; Herrero, A.M. Impact of biogenic amines on food quality and safety. Foods 2019, 8, 62. [CrossRef] [PubMed]