Bacterial Production and Control of Biogenic Amines in Asian Fermented Soybean Foods
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foods Review Bacterial Production and Control of Biogenic Amines in Asian Fermented Soybean Foods Jae-Hyung Mah * , Young Kyoung Park, Young Hun Jin, Jun-Hee Lee and Han-Joon Hwang Department of Food and Biotechnology, Korea University, 2511 Sejong-ro, Sejong 30019, Korea; [email protected] (Y.K.P.); [email protected] (Y.H.J.); [email protected] (J.-H.L.); [email protected] (H.-J.H.) * Correspondence: [email protected]; Tel.: +82-44-860-1431 Received: 27 January 2019; Accepted: 19 February 2019; Published: 25 February 2019 Abstract: Fermented soybean foods possess significant health-promoting effects and are consumed worldwide, especially within Asia, but less attention has been paid to the safety of the foods. Since fermented soybean foods contain abundant amino acids and biogenic amine-producing microorganisms, it is necessary to understand the presence of biogenic amines in the foods. The amounts of biogenic amines in most products have been reported to be within safe levels. Conversely, certain products contain vasoactive biogenic amines greater than toxic levels. Nonetheless, government legislation regulating biogenic amines in fermented soybean foods is not found throughout the world. Therefore, it is necessary to provide strategies to reduce biogenic amine formation in the foods. Alongside numerous existing intervention methods, the use of Bacillus starter cultures capable of degrading and/or incapable of producing biogenic amines has been proposed as a guaranteed way to reduce biogenic amines in fermented soybean foods, considering that Bacillus species have been known as fermenting microorganisms responsible for biogenic amine formation in the foods. Molecular genetic studies of Bacillus genes involved in the formation and degradation of biogenic amines would be helpful in selecting starter cultures. This review summarizes the presence and control strategies of biogenic amines in fermented soybean foods. Keywords: food safety; biogenic amines; fermented soybean foods; intervention methods; control; starter culture; Bacillus spp. 1. Introduction Microbial fermentation is one of the oldest and most practical technologies used in food processing and preservation. However, fermentation of protein-rich raw materials such as fish, meat, and soybean commonly provides abundant precursor amino acids of biogenic amines. Even though most fermented foods have been found to be beneficial to human health, biogenic amines produced through fermentation and/or contamination of protein-rich raw materials by amino acid-decarboxylating microorganisms may cause intoxication symptoms in human unless they are detoxified by human intestinal amine oxidases, viz., detoxification system [1,2]. Thus, the presence of biogenic amines in fermented foods (and non-fermented foods as well) has become one of the most important food safety issues. According to old documents, the cultivation and use of soybeans, dating back to B.C., were launched in Manchuria on the north side of the Korean Peninsula and have spread to other regions of the world. Hence, a variety of fermented soybean foods have been developed and consumed in north-east Asian countries around the Korean Peninsula, and consequently humans in this region have steadily taken the fermented foods for a long period of time from hundreds to thousands of years, depending on the types of fermented soybean foods consumed [3]. Presently, fermented soybean foods Foods 2019, 8, 85; doi:10.3390/foods8020085 www.mdpi.com/journal/foods Foods 2019, 8, x FOR PEER REVIEW 2 of 15 Foods 2019, 8, 85 2 of 15 soybean foods are of public interest and consumed more frequently even in western leading countries because the fermented foods, particularly fermented soybean pastes, not only have been believed by aremany of publicpeople, interest but also and have consumed been scientifically more frequently proven evenby researcher in westerns to leading have health-promoting countries because and the - fermentedprotective foods,effects particularly[4]. However, fermented much less soybean attention pastes, has not been only paid have to beenthe safety believed issues by manyof fermented people, butsoybean also havefoods been[5]. scientifically proven by researchers to have health-promoting and -protective effectsFermented [4]. However, soybean much foods, less including attention various has been type paids of to fermented the safety soybean issues ofpastes fermented and soy soybean sauces, foodsare commonly [5]. made from whole soybeans containing abundant amino acids through microbial fermentation.Fermented If soybean the fermenting foods, including (or sometimes various typescontaminating) of fermented microorganisms soybean pastes are and significantly soy sauces, arecapable commonly of decarboxylating made from whole amino soybeans acids, the containing resultant abundant fermented amino soybean acids foods through may microbial contain fermentation.unignorable amounts If the fermenting of biogenic (or am sometimesines. Indeed, contaminating) the presence microorganisms of biogenic amines are significantly seems to be capable quite offrequent decarboxylating and inevitable amino in acids, fermented the resultant soybean fermented foods. Therefore, soybean foods the maypresent contain review unignorable provides amountsinformation of biogenic on the amines.presence, Indeed, bacterial the presenceproduction, of biogenicand control amines strategies seems to of be biogenic quite frequent amines and in inevitablefermented insoybean fermented foods, soybean especially foods. focusing Therefore, on fermented the present soybean review pastes provides usually information considered on the as presence,heathy foods. bacterial production, and control strategies of biogenic amines in fermented soybean foods, especially focusing on fermented soybean pastes usually considered as heathy foods. 2. A Brief on Biogenic Amines 2. A Brief on Biogenic Amines Biogenic amines are defined as harmful nitrogenous compounds produced mainly by bacterial decarboxylationBiogenic amines of amino are defined acids in as various harmful foods. nitrogenous The bacterial compounds decarboxylation produced mainly of amino by bacterialacids to decarboxylationbiogenic amines ofhave amino been acids well inillustrated various foods.in literature The bacterialand can be decarboxylation found elsewhere of amino[6–8]. Biogenic acids to biogenicamines are amines also endogenous have been well and illustrated indispensable in literature components and can of living be found cells, elsewhere and consequently [6–8]. Biogenic most aminesfood materials, are also endogenousincluding fruit, and vegetables, indispensable and componentsgrains, contain of livingdifferent cells, levels and consequentlyof biogenic amines most fooddepending materials, on their including variety, fruit, maturity vegetables, and cultivatio and grains,n condition contain [7]. different Usual levelsintake ofof biogenicdietary biogenic amines dependingamines generally on their causes variety, no maturity adverse andreactions cultivation because condition human [ 7intestinal]. Usual intake amine of oxidases, dietary biogenic such as aminesmonoamine generally oxidase causes (MAO), no adverse diamine reactions oxidase because (DAO) humanand polyamine intestinal amineoxidase oxidases, (PAO), suchquickly as monoaminemetabolize and oxidase detoxify (MAO), the diaminebiogenic oxidase amines. (DAO) If the andcapacity polyamine of amine-metabolizing oxidase (PAO), quickly enzymes metabolize is over- andsaturated detoxify and/or the biogenicthe metabolic amines. activity If the is capacityimpaired of by amine-metabolizing specific inhibitors, vasoactive enzymes isbiogenic over-saturated amines, and/orincluding the histamine, metabolic tyramine activity is and impaired β-phenylethylamine, by specific inhibitors, may cause vasoactive food intoxication biogenic amines, and in including turn be histamine,considered tyramine to be toxic and substancesβ-phenylethylamine, in humans [1,2]. may causeFurthermore, food intoxication the toxicity and of in biogenic turn be amines considered can tobe beenhanced toxic substances by putrefactive in humans biogenic [1,2]. Furthermore, amines such the as toxicity putrescine of biogenic and cadaverine amines can [9]. be enhancedThe most bycommon putrefactive symptoms biogenic of biogenic amines such amine as putrescineintoxication and in cadaverinehuman are[ 9nausea,]. The most respiratory common distress, symptoms hot offlushes, biogenic sweating, amine intoxicationheart palpitation, in human headache, are nausea, a bright respiratory red rash, distress, oral burning, hot flushes, and sweating,hypo- or hearthypertension palpitation, [10]. headache, Figure 1 aschematically bright red rash, illustra oral burning,tes the detoxification and hypo- or hypertensionand toxicological [10]. Figurerisks of1 schematicallybiogenic amines. illustrates the detoxification and toxicological risks of biogenic amines. FigureFigure 1. 1.Detoxification Detoxification and and toxicological toxicological risks ofrisks biogenic of biogenic amines. amines. *: Metabolic *: Metabolic inactivation inactivation of biogenic aminesof biogenic through amines oxidative through deamination oxidative by oxidases. deamination†: Incapacitation by oxidases. of intestinal †: detoxicationIncapacitation system of throughintestinal saturation detoxication by biogenic system amines through or inhibition satura by antidepressanttion by biogenic medications. amines BA: or Biogenic inhibition amines.