The problem of biogenic amines in fermented foods and the use of potential biogenic amine-degrading...

Trends in Food Science & Technology xx (2014) 1e10

Review

* Corresponding author.

http://dx.doi.org/10.1016/j.tifs.2014.07.0070924-2244/� 2014 Published by Elsevier Ltd.

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biogenic amine-degrading microorganisms as a solution, Trends in Foo

The problem of

biogenic amines in

fermented foods

and the use of

potential biogenic

amine-degrading

microorganisms as a

solution

Miguel A. Alvareza and
Ma Victoria Moreno-Arribasb,*
aInstituto de Productos L�acteos de Asturias,

IPLAeCSIC, Paseo R�ıo Linares s/n, 33300 Villaviciosa,

Asturias, Spain (e-mail: [email protected])bInstituto de Investigaci�on en Ciencias de la

Alimentaci�on (CIAL), CSIC-UAM, Nicol�as Cabrera, 9,

CEI UAM D CSIC, 28049 Madrid, Spain (e-mail:

[email protected])

Biogenic amines (BA) are low-molecular-weight nitrogenous

organic bases, which can accumulate in high concentration

in food due to microbial activity and cause toxic effects in con-

sumers. In some fermented foods it is difficult to prevent the

accumulation of BA since the microbiological/chemical/phys-

ical conditions of the fermentation can not be easily modified.

An alternative in such cases is the use of food microorganisms

that are able to degrade BA once they have been synthesized

in the food matrix. In this review, we examine the microorgan-

isms that have demonstrated the ability to degrade BA and

their technological relevance in fermented foods.

. V., Th

d Scien

IntroductionBiogenic amines (BA) are non-volatile low-molecular-weight nitrogenous organic bases, derived through decar-boxylation of corresponding amino acids. They can beboth formed and degraded as a result of normal metabolicactivities in humans, animals, plants and microorganisms.The responsible enzymes, amino acid decarboxylases, arewidely present in spoilage and other food microorganisms,i.e. naturally occurring and/or artificially added lactic acidbacteria (LAB) involved in fermentation in foods andbeverages.

The primary relevance of BA is that the consumption offoods or beverages containing a high concentration maycause food intoxication with symptoms including flushes,headaches, nausea, cardiac palpitations, and increased ordecreased blood pressure, among others (Ladero, Calles-Enriquez, Fern�andez, & Alvarez, 2010; Silla Santos,1996). Also, they may have a role in the depreciation ofthe organoleptic properties of foodstuff and are consideredindicators of quality and/or acceptability in some foods(Ruiz-Capillas & Jim�enez-Colmenero, 2004; Shalaby,1996).

Foods likely to contain high levels of biogenic aminesinclude fish, fish products and fermented foodstuffs (meat,dairy, some vegetables, beers and wines) (Bover-Cid,Hugas, Izquierdo-Pulido, & Vidal-Carou, 2000; Shalaby,1996; Silla Santos, 1996). The most important BAs foundin foods are histamine, tyramine, putrescine, cadaverineand phenylethylamine, which are produced by the decar-boxylation of histidine, tyrosine, ornithine, lysine andphenylalanine, respectively. Putrescine can also be formedthrough deimination of agmatine.

The production of BA has been associated with yeast,Gram-negative and Gram-positive bacteria. Thus, severalyeast species (Debaryomyces hansenii, Yarrowia lipolytica,Pichia jadinii or Geotrichum candidum) have beendescribed as potential BA producers (Gardini et al., 2006;Roig-Sagu�es, Molina, & Hernandez-Herrero, 2002; Suzziet al., 2003; Wyder, Bachmann, & Puhan, 1999).

Different species of Gram-negative bacteria that can befound in foods i.e. Escherichia coli, Hafnia alvei, Klebsiellapneumoniae, Morganella moorganii, Pseudomonas spp. orSerratia spp. are able to produce BA. However, the presenceof these species in food is a more general food-safety prob-lem that should be solved through good manufacturing prac-tices involving adequate hygienic measures (Linares et al.,

e problem of biogenic amines in fermented foods and the use of potential

ce & Technology (2014), http://dx.doi.org/10.1016/j.tifs.2014.07.007

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2 M.A. Alvarez, MaV. Moreno-Arribas / Trends in Food Science & Technology xx (2014) 1e10

2012). In fact, the concentration of BA is used as an indicatorof microbial spoilage in non-fermented food (Silla Santos,1996). In the case of fermented foods, Gram-negative bacte-ria are often inhibited due to the fermentation process itself(Adams & Nicolaides, 1997; Caplice & Fitzgerald, 1999),Gram-positive bacteria, and especially LAB, being mainlyresponsible for the production of BA (Linares, Mart�ın,Ladero, Alvarez, & Fern�andez, 2011). In fact, BA-producing LAB are normal microbiota of fermented foodsand may even be part of starter or adjunct cultures. Theycan even be responsible for organoleptic defects in foods,making the solution to the BA problemmore difficult to find.

Tyramine biosynthesis is a species-level characteristic inEnterococcus faecalis, Enterococcus faecium and Entero-coccus durans, and putrescine synthesis was found to bea species-level trait of E. faecalis (Ladero, Fern�andezet al., 2012). Putrescine production by Lactococcus lactiscould have been a specific characteristic that was lost insome strains during the adaptation to the milk environmentby a process of reductive genome evolution (Ladero et al.,2011). However, within microbial groups, in many casesthe capacity to produce biogenic amines is a strain-specific characteristic, more widely distributed amongcertain genera and species, suggesting that horizontalgene transfer may account for their dissemination betweenstrains (Coton & Coton, 2009; Marcobal, de las Rivas,Moreno-Arribas, & Mu~noz, 2006).

Knowledge concerning the origin and factors involved inbiogenic amine production in fermented foods is well docu-mented, and recently several reviews on this topic havebeen published (Anc�ın-Azpilicueta, Gonz�alez-Marco, &Jim�enez-Moreno, 2008; Garc�ıa-Muruno & Mu~noz, 2012;Linares et al., 2011, 2012; Moreno-Arribas & Polo, 2010;Smit, Du Toit, & Du Toit, 2008; Spano et al., 2010). At pre-sent, a shared regulation limiting the amounts of BA infoods is still lacking, although their presence beyond thelimits recommended by scientific literature may have nega-tive commercial implications. For example, to minimizehistamine toxicological effects, it is suggested that its con-centration should not exceed 2 mg/l in fermented bever-ages, such as wine (ten Brink, Damink, Joosten, & Huisin’t Veld, 1990). The only country with a limit for hista-mine in wine (10 mg/l) was Switzerland until 2008, butcurrently there is no legal or regulatory limit for histaminecontent in wine in any country in the world.

Recently a qualitative risk assessment of biogenicamines in fermented foods was conducted by the EFSA(2011) (European Food Safety Authority) Panel on Biolog-ical Hazards (BIOHAZ). Using data from the scientificliterature, the BIOHAZ Panel concluded that the accumula-tion of BA in fermented foods is a complex process affectedby multiple factors and their interactions, the combinationof which are numerous, variable and product-specific.Hence, risk mitigation options, which are based on control-ling those factors/interactions, could not be considered andranked individually.

Please cite this article in press as: Alvarez, M. A., & Moreno-Arribas, M. V., Th

biogenic amine-degrading microorganisms as a solution, Trends in Food Scienc

Histamine and tyramine are considered as most toxicand particularly relevant for food safety. Putrescine andcadaverine are known to potentiate these effects. Moreover,these amines are thermostable and are not inactivated bythermal treatments used in food processing and preparation.Presently, only prevention and monitoring strategies enablethe control of BA formation in foods during the productionprocess and along the food chain. However, specific ‘cura-tive’ procedures able to eliminate already formed biogenicamines are required, and are therefore presented as a realsolution to this problem. Recent evidences displaying theability of food microorganisms to degrade BA are reported,although few data are available regarding their potentialtechnological interest for specific foods. Considering thecurrent interest by the food industry (and by consumers)in the search for tangible solutions to the problem of BAin foodstuffs, the main objective of this review is, briefly,to raise the particular problem of the BA in fermented foodsand to analyze and discuss the current knowledge on thedegradation of BA by food microorganisms, as well as toevaluate their practical applications to remove/reduce BAin the context of the modern food chain, with particularfocus on fermented foods.

Problems arising from the presence of biogenicamines in foods

BAare produced in nature bymicroorganisms, plants, andanimals, performing important physiological functions,including a number of crucial roles in the physiology of eu-karyotic cells (Table 1). Therefore, the intake of BA isnormal when we eat. Under normal conditions, BA ingestedwith food are rapidly detoxified by amine oxidases of the in-testinal mucosa. These enzymes are classified asmono (MAO) or diamine oxidases (DAO) depending onthe number of amino groups preferentially oxidized. Hista-mine can also be detoxified by methyl or acetyl-transferases (Linares et al., 2011). However, if these en-zymes are dysfunctional either genetically or due to theintake of inhibitors such as alcohol or certain antidepressantmedications, BA enter the systemic circulation and exerttheir toxic effect on different organs, causing serious humanhealth problems (Blackwell, 1963; Ladero, Calles-Enriquezet al., 2010; McCabe-Sellers, Staggs, & Bogle, 2006).Nevertheless, the most frequent risk from BA is that as theresult of uncontrolledmicrobial activity they can accumulatein high concentrations in certain foods, exceeding the capac-ity of the detoxification mechanisms and thereby exertingtheir toxic effect on consumers of such contaminated foods.BA can reach concentrations higher than 1000 mg kg�1

(Fern�andez, Fl�orez, Linares, Mayo, & Alvarez, 2006;Roig-Sagu�es et al., 2002; Shalaby, 1996), which undoubt-edly constitutes a health hazard. There is limited researchon the toxicity of BA and most focuses on histamine. More-over, it is noteworthy that intolerance levels depend on thecharacteristics of the individual. It is assumed that the intakeof foods with concentrations of histamine higher than


e & Technology (2014), http://dx.doi.org/10.1016/j.tifs.2014.07.007

Table 1. Biogenic amines in foods and their physiological and toxicological effects (adapted from Ladero, Calles-Enriquez et al., 2010; Ladero,Fern�andez et al., 2010; Ladero, Mart�ınez et al., 2010).

Biogenic amines Precursor Physiological effects Toxicological effects

Histamine Histidine Neurotransmitter, local hormone, gastric acid secretion,cell growth and differentiation, regulation of circadianrhythm, body temperature, food intake, learning andmemory, immune response, allergic reactions

Headaches, sweating, burning nasal secretion, facialflushing, right red rashes, dizziness, itching rashes,oedema (eyelids), urticaria, difficulty in swallowing,diarrhea, respiratory distress, bronchospasm,increased cardiac output, tachycardia, extrasystoles,blood pressure disorders

Tyramine Tyrosine Neurotransmitter, peripheral vasoconstriction, increasecardiac output, increase respiration, elevate bloodglucose, release of norepinephrine

Headaches, migraine, neurological disorders,nausea, vomiting, respiratory disorders, hypertension

Putrescine andCadaverine

Ornithineand Lysine

Regulation of gene expression, maturation ofintestine, cell growth and differentiation

Increased cardiac output, tachycardia, hypotension,carcinogenic effects

3M.A. Alvarez, MaV. Moreno-Arribas / Trends in Food Science & Technology xx (2014) 1e10

400 mg kg�1 is dangerous to health (Taylor, 1986). Furtherresearch demonstrated that 75 mg of pure oral histamine pro-voke symptoms in 50% of healthy females with no history offood intolerance (W€ohrl, Hemmer, Focke, Rappersberger, &Jarisch, 2004), and the intake of approximately 1000 mg ofhistamine is definitely associated with severe intoxications(Rauscher-Gabernig, Grossgut, Bauer, & Paulsen, 2009).

The effects of tyramine intake are known as “cheese re-action”, since it was first associated with cheese consump-tion (Blackwell, 1963), a food that can reach very highconcentrations of this BA. It has been described that tyra-mine concentrations over 125 mg kg�1 have effects inhealthy individuals, and a concentration of 6 mg kg�1 ispotentially toxic to patients treated with MAO inhibitors(McCabe-Sellers, 1986).

The effects of BA can be classified as reaction, intoler-ance, or intoxication or poisoning according to the severityof the symptoms (Ladero, Calles-Enriquez et al., 2010)(Table 1). Reaction symptoms include nausea, sweating,rashes, slight variations in blood pressure andmild headache.The symptoms of intolerance are more severe, includingvomiting, diarrhea, facial flushing, a bright red rash, bron-chospasms, tachycardia, oral burning, hypo or hypertensionand migraine. More exceptional intoxication may occur withhypertension, causing irreversible damage to the heart or thecentral nervous system (Blackwell, 1963).

Other pathologies e some really serious e have beenassociated with BA. The consumption of food with highconcentrations of histamine by individuals with low DAOactivity has been related to inflammatory diseases such asCrohn’s disease, ulcerative colitis and even to colorectalneoplasms (Maintz & Novak, 2007). Abnormally highlevels of tyramine in the brain have been associated withdepression, schizophrenia, Parkinson’s disease, and Reye’ssyndrome (Ladero, Calles-Enriquez et al., 2010). Second-ary amines such as putrescine and cadaverine can also reactwith nitrite to form carcinogenic nitrosamines (ten Brinket al., 1990). Moreover, there is increasing evidence thatputrescine could have a role in promoting the malignanttransformation of cells. Dietary putrescine increased themalignancy grade of adenomas in a murine model(Ignatenko et al., 2006). Colorectal cancer cells have a


biogenic amine-degrading microorganisms as a solution, Trends in Food Scien

higher polyamine content than the adjacent mucosa orequivalent normal tissue (Wallace & Caslake, 2001), high-lighting the possible importance of exogenous putrescine intheir development (Gerner & Meyskens, 2004). Elevatedconcentrations of putrescine have also been detected ingastric carcinomas caused by Helicobacter pylori and theputrescine levels are restored if the microbial infection iseliminated (Shah & Swiatlo, 2008).

Apart from the toxicological effects, BA could also havean effect on the intestinal microbiota. In fact, tyramine isknown to enhance the adherence of the enteropathogen E.coli 1057H to epithelial cells (Lyte, 2004). Putrescine hasbeen associated with virulence factors of Gram-positiveand Gram-negative pathogens (Shah & Swiatlo, 2008)and it has been proved that it can activate the swarmingphenotype needed for pathogenesis in some Proteus mirabi-lis mutants (Sturgill & Rather, 2004).

Since there are foods that are often contaminated withmore than one BA, another important problem that requiresfurther research is their synergistic effects. It is known thatputrescine and cadaverine play a role as diamine-oxidaseinhibitors and therefore act as enhancers of histaminetoxicity (Lehane & Olley, 2000).

Additionally, with regards to adverse health implica-tions, at elevated levels (50e100 mg/L) these compoundse mainly cadaverine and putrescine e also exert a consid-erable impact on the organoleptic properties of fermentedfoods. In some extreme cases, winemakers have statedthat affected wines lose their varietal characteristics, andthis can result in the formation of a metallic, meaty, or pu-trid aroma in the wine.

Procedures/strategies for surveillance and preventionof biogenic amine accumulation in foods

BA production in foods requires the availability ofprecursors (i.e. amino acids), the presence of bacteriasynthesizing amino acids decarboxylases, and favorableconditions for their growth and decarboxylating activity.As a strategy to control BA in foods, different methods(both analytical and based on molecular tools) have beendeveloped. These procedures allow the detection ofBA-producing bacteria strains and the quantification and




monitorization of amine production through the food chain,respectively.

The monitorization of BA concentrations of raw mate-rials and products along the food chain is not only neces-sary to evaluate the relevance of factors contributing toBA formation and accumulation, but also in order to getadvice about the need to implement different correctivestrategies. Among the analytical methods, chromatographictechniques, and in particular high-performance liquid chro-matography methods (HPLC) involving derivatization ofBA (either pre- or post-column), are the most commonand suitable methods for the analysis of BA in foods. Infact, the reference method specified in the European Com-mission Regulation (EC) No. 2073/2005 was for the deter-mination of histamine in fish and treated fishery productsusing HPLC after dansyl-derivatization. Later, in wines, areversed phase (RP)-HPLC method that used O-phthaldial-dehyde (OPA) for pre-column derivatization and detectionby fluorescence was adopted by the International Organiza-tion of Vine and Wine (OIV), allowing the simultaneousquantification of 18 biogenic amines (OIV/OENO 346/2009). Derivatization treatment with diethyl ethoxymethy-lenemalonate followed by ultra-HPLC allows the simulta-neous quantification of biogenic amines, amino acids, andammonium ions in cheese samples in under 10 min(Redruello et al., 2013). Validation of methods for BA anal-ysis is recommended for the different relevant food types,including the standardization and harmonization of proce-dures, external quality assessment and the availability ofcertified reference materials (EFSA, 2011).

Detection of amino acid decarboxylase-positive microor-ganisms, both involving in vitro differential growth mediaand specific PCR protocols based on the detection of gene-encoding decarboxylases, have been shown by several au-thors (Coton & Coton, 2005; de las Rivas, Marcobal,Carrascosa, & Mu~noz, 2006; Landete, Ferrer, & Pardo,2007; Landete, de las Rivas, Marcobal, & Mu~noz, 2007).For example, a multiplex PCR method for the simultaneousdetection of oenological LAB with the potential to producehistamine, tyramine and putrescine, has been reported(Marcobal, de las Rivas, Moreno-Arribas, & Mu~noz,2005). PCRmethods for the detection of BA-producing dairyLAB have also been developed (Fern�andez, Linares, &Alvarez, 2004, 2006). Furthermore, quantitative real-timePCR methods for the detection and quantification ofhistamine-producing (Ladero, Linares, Fern�andez, &Alvarez, 2008; Lucas, Claisse, & Lonvaud-Funel, 2008),tyramine-producing (Ladero, Mart�ınez, Mart�ın, Fern�andez,& Alvarez, 2010; Torriani et al., 2008) and putrescine-producing bacteria (Ladero, Ca~nedo et al., 2012) havebeen developed and successfully applied to different stagesof cheese manufacture, including the final product(Ladero, Fern�andez, Cuesta, & Alvarez, 2010).

The amount and type of biogenic amines formed infoods is strongly influenced by the intrinsic food character-istics, including pH, water activity, composition, and



microbiota, and by extrinsic parameters such as storagetime and temperature, which allow bacterial growth duringfood processing and storage. So, different procedures tolimit amine formation have been reported depending onthe particular foodstuff. Recently, the existing andemerging approaches for the control of BA in foods, withspecial emphasis on fish and meat products, have been re-viewed (Naila, Finlt, Fletcher, Bremer, & Meerdink,2010). They mainly include the control of temperaturebelow 5 �C, the use of food additives and preservatives,the application of hydrostatic pressures and irradiation,and altering conditions based on microbial modeling ofhistamine-producing bacteria. These methods only delaythe formation of BA in food, primarily through the inhibi-tion of bacteria or the decarboxylase enzyme activityresponsible for amine formation.

In fermented foods, the selection of LAB involved in thefermentation process is mainly approached by adopting mi-crobial starters lacking the pathways to degrade precursoramino acids (Del Prete, Constantini, Cecchini, Morassut,& Garc�ıa-Moruno, 2009; Fern�andez, Linares, Rodr�ıguez,& Alvarez, 2007; Landete, Ferrer et al., 2007; Landete, delas Rivas et al., 2007; Moreno-Arribas, Polo, Jorganes, &Mu~noz, 2003; Novella-Rodr�ıguez, Veneciana-Nogu�es,Trujillo-Mesa, & Vidal-Carou, 2002). PCR methods maybe used for the characterization and selection of starter cul-tures. However, in an attempt to control BA, microorganismsintended to be used as starter cultures in any fermented foodshould be confirmed as not producing BA and be able tooutgrow autochthonous microbiota under conditions of pro-duction and storage (Gardini, Martuscelli, Crudele,Paparella, & Suzzi, 2002; Marcobal, Mart�ın-�Alvarez, Polo,Mu~noz, & Moreno-Arribas, 2006; Moreno-Arribas & Polo,2008). Also, during the manufacturing of food, all the oper-ations leading to an increase of substrates or to favorableconditions for microbial growth should be limited andavoided, for example: by reducing the number of BA pro-ducers via the pasteurization of milk to be used in cheesemanufacture, reducing the amount of proteolytic activity(thus reducing the availability of the amino acid precursorof BAs), and by reducing ripening times (Fern�andez et al.,2007). During wine production, surveillance of parametersthat influence bacterial growth, such as pH, Ta, presence oforganic acids, and/or some typical oenological practicessuch as maceration or prolonged contact with yeast leeshave been proposed to prevent LAB proteolytic activityand decarboxylase activity (Mart�ın-�Alvarez, Marcobal,Polo, & Moreno-Arribas, 2006). Other strategies, such asadding sulphites, have been recommended for reducing BAaccumulation in wine and cider. In spite of limited publishedinformation, it seems that biogenic production in ciders mayalso be controlled by the use of technological regimes andpractices limiting precursor amino acid content (Garai,Due~nas, Irastoza, Mart�ın-�Alvarez, & Moreno-Arribas,2006; Garai, Irastoza, Due~nas, Mart�ın-�Alvarez, & Moreno-Arribas, 2013).




In brief, all aspects of fermented food processing(including additives, ingredients, fermentation and ripeningor storage conditions) and distribution should be adjustedand balanced in each particular product to avoid/minimizepotential enhancing effects on BA formation and to enabledominance of starter cultures where used. However, thereare some practical limitations on the use of some of thesemethods depending on the resources available and the char-acteristics of the desirable fermented food. The assessmentof other novel strategies needs to be further investigated.

Ability of food microorganisms to degrade biogenicamines

Based on the fact that amino oxidases are responsible forthe detoxification of dietary BA, and enzymes with thesame activity have also been found in bacteria, the firstworks in this direction focused on the screening of such ac-tivities in microorganisms isolated from food. Table 2 sum-marizes the studies reporting BA degradation by foodmicroorganisms. Voigt and Eitenmiller (1978) analyzedbacteria isolated from dairy products and came to theconclusion that these bacteria generally lack amino oxi-dases. Moreover, those few bacteria in which amino-oxi-dase activities were found also have tyrosine or histidinedecarboxylase activity and, therefore, are potential pro-ducers of BA. It was a couple of decades later Leuschner,Heidel, and Hammes (1998) found food isolates belongingto the species Lactobacillus plantarum, Lactobacillus sakei,Lactobacillus pentosus, Pediococcus acidilactici, Rhodo-coccus sp., Arthrobacter sp., Micrococcus sp., Brevibacte-rium linens, and G. candidum with the ability to degradein vitro tyramine and histamine. The same group studiedthe potential of the B. linens strains to degrade histamineand tyramine during the surface ripening of Munster

Table 2. Studies reporting biogenic amines degradation by food microorg

Biogenic amine Species

Histamine Tyramine Lactobacillus plantarum, L. sakei, L. penPediococcus acidilactici, RhodococcusArthrobacter sp., Micrococcus sp.,Brevibacterium linens, Geotrichum cand

Histamine Tyramine B. linensHistamine L. sakeiHistamine Bacillus amyloliquefaciens,

Staphylococcus carnosusPutrescine Cadaverine B. subtilis, St. intermediusHistamine B. amyloliquefaciens, St. carnosusHistamine St. xylosusTyramine L. casei, L. plantarumHistamine Tyramine L. caseiHistamine Tyramine Putrescine L. casei, L. hilgardii, P. parvulus,

Oenococcus oeni, L. plantarum,P. pentosaceus

Histamine Tyramine Putrescine L. caseiTyramine Putrescine L. plantarumHistamine Tyramine Putrescine Penicillium citrinum, Alternaria sp.,

Phoma sp., Ulocladium chartarum,Epicoccum nigrum



cheese, showing for the first time the possibility of usingBA-degrading microorganisms to reduce the BA contentin food (Leuschner & Hammes, 1998).

A couple of years later, four L. sakei strains able todegrade histamine in a model system were isolated fromnaturally fermented fish pastes (Dapkevicius, Nout,Rombouts, Houben, & Wymenga, 2000). Histamine degra-dation by two of these isolates was assayed in ensiled fishslurry and the authors concluded that their use for fishsilage could successfully reduce the risk of this BA. Bacil-lus amyloliquefaciens and Staphylococcus carnosus able todegrade histamine, and Staphylococcus intermedius and Ba-cillus subtilis able to degrade putrescine and cadaverine,were isolated from another fish product, a Malaysian fishsauce (Zaman, Bakar, Selamat, & Bakar, 2010). Later,they found that B. amyloliquefaciens and St. carnosus iso-lates are able to reduce the accumulation of histamine inlaboratory fish sauce fermentation (Zaman, Bakar, Jinap,& Bakar, 2011). Strains of other species of the genus Staph-ylococcus, i.e. Staphylococcus xylosus, isolated from arti-sanal fermented sausages produced in Italy were alsofound to be capable of degrading histamine (Martuscelli,Crudele1, Gardini, & Suzzi, 2000). The use of one of thesestrains as a starter culture in dried sausages slightly reducesthe BA content (Gardini et al., 2002). Lactobacillus caseiand L. plantarum strains, also isolated from artisanal fer-mented sausages e but in this case produced in Argentinae can degrade tyramine, although with different efficiency(Fadda, Vignolo, & Oliver, 2001). Kocuria varians andMicrococcus varians strains from the same samples arealso able to degrade tyramine, but are at the same time tyra-mine and/or histamine producers. It is remarkable thatresting cells of one L. casei strain degraded 98% of a2.5 mM tyramine solution in 96 h. Strains of L. casei

anisms.

Matrix Reference

tosus,sp.,

idum

In vitro Leuschner et al., 1998

Munster cheese Leuschner & Hammes, 1998Ensiled fish slurry Dapkevicius et al., 2000In vitro Zaman et al., 2010

In vitro Zaman et al., 2010Fish sauce fermentation Zaman et al., 2011In vitro Martuscelli et al., 2000In vitro Fadda et al., 2001Cabrales cheese model Herrero-Fresno et al., 2012Culture media Garc�ıa-Ruiz et al., 2011

Wine Garc�ıa-Ruiz et al., 2011In vitro Capozzi et al., 2012In vitro/Commercial wines Cueva et al., 2012




from very different sources were also able to degrade BA.The inoculation of an L. casei strain from a commercialpreparation can lower the BA concentration in differentvegetable silages performed in the laboratory (Nishino,Hattori, Wada, & Touno, 2007), although the authors sug-gest this may be a specific antagonism of L. casei againstBA-producing microorganisms. Samples of differentcheeses were screened for the presence of BA-degradingLAB and, surprisingly, the 17 isolates that were able todegrade tyramine and histamine were identified by 16SrRNA sequencing as L. casei (Herrero-Fresno et al.,2012). Two of these strains were checked in a mini-cheese model verifying that both avoid tyramine and hista-mine accumulation over four months of ripening. A collec-tion of wine-associated LAB was screened for their BA-degrading ability, verifying that one L. casei, one Lactoba-cillus hilgardii, one Pediococcus parvulus, one Oenococcusoeni, two L. plantarum, and three Pediococcus pentosaceusstrains significantly degrade histamine, tyramine or putres-cine in culture media (Garc�ıa-Ruiz, Gonz�alez-Rompinelli,Bartolom�e, & Moreno-Arribas, 2011). However, in malo-lactic fermentation experiments, the BA-degrading abilitywas confirmed only for L. casei. In a different work, butalso from wine, two strains of L. plantarum that candegrade tyramine and putrescine were isolated (Capozziet al., 2012). Furthermore, it was verified that these strainscan survive in a wine-like medium and show a useful apti-tude to degrade malic acid. In the vineyard ecosystem werealso found fungi with the ability to degrade BA (Cuevaet al., 2012). Species of Penicillium citrinum, Alternariasp., Phoma sp., Ulocladium chartarum and Epicoccum nig-rum can degrade at least two different primary amines in amicrofermentation system.

Enzymatic activities involved on biogenic aminesdegradation

Monoamine-oxidases (MAO, E.C. 1.4.3.4.) are flavopro-teins that catalyze the oxidative deamination of a number ofbiogenic and dietary monoamines forming the correspond-ing aldehydes, hydrogen peroxide and ammonia. In humansthere are two separate MAO isoforms (MAO-A, MAO-B),which exhibit different but overlapping substrate and inhib-itor specificities (Wang, Billett, Borchert, Hartmut, &Christoph, 2013). As already indicated above, the intestinalmucosa has mono and diamino oxidases that catabolize BAand are well characterized. However, information concern-ing the identification and biochemical characterization ofenzymatic activities involved on BA reduction in foods isvery scarce. Most of the studies attributed these enzymaticactivities to amine oxidases.

In 2004, Sekiguchi, Makita, Yamarura, and Matsumoto(2004) identified a histamine oxidase in the actinobacteriaArthrobacter crystallopoietes KAIT-B-007. Histamine oxi-dase catalyzes the oxidative deamination of histamine-eimidazole acetaldehyde with the simultaneous productionof ammonia and hydrogen peroxide. The enzyme was very



thermostable (the activity was stable at 65 �C and 70 �C)and fully stable over the pH range of 6e9. The enzymewas a copper-containing protein and it was suggested thatCu2þ is essential for the expression of histamine oxidase ac-tivity. Van Hellemond, van Djk, Heuts, Janssen, and Fraaije(2008) also characterize a putrescine oxidase from Rhodo-coccus erythropolis NCIMB 11540. The purified enzymewas shown to be a soluble dimeric flavoprotein consistingof subunits of 50 kDa and contains non-covalently boundflavin adenine dinucleotide as a co-factor. Most recently,the enzymes responsible for putrescine degradation in winewere isolated and purified from L. plantarum andP. acidilac-tici and were also identified as multicopper oxidases(Callej�on, Sendra, Ferrer, & Pardo, 2014).

Technological relevance of biogenic amine-degradingmicroorganisms in fermented food production

A novel way to reduce the BA content of foods would beto eliminate them from the food matrix. This might be thestrategy of choice with those fermented foods in which it isdifficult to avoid the presence of BA-producing LABbecause they are part of the usual microbiota, and conse-quently BA are present at the final stages of themanufacturing process.

The use of BA-degrading bacteria has been proposed forthe production of fermented meats (Fadda et al., 2001;Gardini et al., 2002; Martuscelli et al., 2000). Amino-oxidase activity has even been suggested as a criterion forthe selection of starter cultures for sausage fermentation(Fadda et al., 2001; Gardini et al., 2002). However,although it has been found that the presence of certain start-ing cultures reduce BA content in a semi-industrial plant(Gardini et al., 2002), it is important to note that thereare no biochemical studies that demonstrate that amino ox-idase is the enzymatic activity responsible for BA reduc-tion. Neither has it been verified whether or not thephysico-chemical conditions during fermentation are suit-able for oxidase activity.

Accumulation of BA in fish is usually a problem offreshness and/or deficiencies in the cold chain (Hal�asz,Bar�ath, Simon-Sarkadi, & Holzapfel, 1994). However, infermented food derived from fish, the problem is similarto other fermented foods and the use of BA-degrading bac-teria has been proposed as a potential solution (Dapkeviciuset al., 2000; Zaman et al., 2010, 2011). The presence ofamino-oxidase activity has also been proposed as a crite-rion for the selection of starters (Zaman et al., 2010), butthis activity has not yet been characterized in the proposedBA-degrading bacteria. The same authors also emphasizethe importance of using fresh fish and hygienicmanufacturing practices (Zaman et al., 2011).

Cheese, especially that made from raw milk, is a partic-ular technological challenge because it is a complexecosystem involving many different microorganisms withdifferent metabolic machineries, including catabolic aminoacid enzymes yielding high amounts of biogenic amines.




Concentrations over 1 g/kg have been reported in cheese,with tyramine and histamine the most commonly presentand most abundant of all BAs (Fern�andez et al., 2007). Infact, blue cheeses and, in particular traditional Cabrales-type cheeses (made from rawmilk) accumulate high BA con-centrations, mainly because the tyramine-producing entero-cocci present in the raw milk used are responsible for theaccumulation of tyramine (Ladero, Fern�andez et al., 2010).The pasteurization of milk would lessen the problem, but itcould affect the organoleptic characteristics of the cheesesand, in fact, in many cases the rules of the Geographical In-dications and Designations of Origin do not allow it. Anotherfactor involved in the accumulation of BA in this type ofcheese is the high proteolysis of casein, generating a highrelease of amino acid substrates during their characteristiclong ripening period. Recently, Herrero-Fresno et al.(2012), identified L. casei strains that could be used as highlycompetitive adjunct cultures capable of reducing the contentof tyramine and histamine, the two most toxic BAs, incheese. Although more work is needed to identify and char-acterize their BA-degrading enzymatic activity, such a strat-egy might be particularly useful when making cheeses fromraw milk in which a specific non-starter microbiota is essen-tial for the organoleptic characteristics of the final product.In the particular case of blue cheeses, the growth of mold re-quires the presence of oxygen, which would also allow theactivity of amino oxidases.

At present, in the market there are no effective proce-dures or treatments used to limit the content of biogenicamines in wine. Enzymatic removal of amines may be asafe and economic way to eliminate these troublesomecompounds from wines and other fermented foods.Garc�ıa-Ruiz et al. (2011) reported for the first time the abil-ity of LAB of food origin (i.e. wine) to degrade putrescine.The biogenic amine-degrading ability of selected wineLAB strains did not appear to be associated with anamine-producing ability. As for cheese, L. casei seemedto be an interesting species displaying histamine, tyramineand putrescine breakdown, both in culture media conditionsand in model wine malolactic fermentation, suggesting itssuitability as a commercial malolactic starter. Meanwhile,the wine composition may interfere with the BA-degrading capacity of the wine strain L. casei (Garc�ıa-Ruiz et al., 2011). Further research is needed to provideconclusive evidence of the applicability of wine LAB bac-teria in real wine systems.

The use of amino oxidases to reduce BA in foods hasbeen also considered. The preparation and industrial appli-cations of the amino oxidase of Aspergillus niger IMI17454was described in 1985 (Hobson & Anderson, 1985).Although the authors proposed its use in foods, such ascheese, beer, must and yeast extracts, specific data demon-strating the usefulness under real food production condi-tions were not reported. Dapkevicius et al. (2000)attempted to reduce histamine in ensiled fish slurry (pH4.5) by using commercial diamine oxidase purified from



porcine kidney, but it was unsuccessful, limiting its use tofood with higher pH values. Lately, a procedure based onthe use of an enzymatic extract from P. citrinum CIAL-274,760, isolated from vineyards, which added to thewine reduces or even completely eliminate BA in syntheticwines has been reported (Moreno-Arribas et al., 2012). Theenzymatic extract is easily obtainable by means of filtrationculture of the fungus. Previously, the fungi were grown indefined media using a selection of free amines (i.e. hista-mine, tyramine and putrescine) as the sole nitrogen sourceusing a microfermentation system. The potential of P. citri-num CIAL-274,760 (CECT 20782) extracts for BA detoxi-fication of wines was further demonstrated in commercialred and white wines. Interestingly, in this study, histamine,tyramine and particularly putrescine were significantlydegraded in red wine treated with fungi BA-degrading ex-tracts (up to 40, 20 and 70% degradation, respectively) un-der conditions with a lower presence of oxygen (Cuevaet al., 2012). Later, the efficiency and specificity of theenzymatic extract regarding its ability to degrade BA inwinery scale conditions has been tested (unpublished re-sults). In fact, at winery Ta (close to 16 �C) and wine pHconditions (pH 3.5), the fungi’s enzymatic extract wasable to significantly and simultaneously reduced the con-centration of histamine, tyramine and putrescine after48 h treatment of a red wine following industrial scalemalolactic fermentation in stainless steel tanks (unpub-lished results). The non-production of mycotoxins (i.e.ochratoxin A, OTA) by this BA-degrading strain was alsodemonstrated. Further, no significant changes was observedin the phenolic and volatile composition of the wine, sug-gesting that the use of the BA-degrading enzymatic extractdid not affect the organoleptic properties of the final prod-uct. The identification of the enzymatic activities involved,as well as the provision of procedures’ formulation of theenzymes to avoid the accumulation of BA in wines andother fermented foods, is underway. The use of such prod-ucts together with a combination of control measures (i.e.high-quality raw materials and appropriate manufacturingpractices) might afford the best way of producing productswith reduced BA-associated risks.

Conclusions and future challengesFermented foods and beverages have a high probability of

accumulating high concentrations of BA, which is undoubt-edly a health hazard for consumers. There are many factorsthat favor the accumulation of BA in these products (Linareset al., 2012; Mart�ın-�Alvarez et al., 2006), and unfortunatelyit is not always possible to modify those factors in order toavoid it. Thus, for example, the presence of BA-producingmicroorganisms in some raw-milk cheeses can not beavoided. Nor can the accumulation of decarboxylation sub-strate amino acids be prevented, because proteolysis isessential for the desired organoleptic characteristics ofcheeses. Likewise, some oenological practices widely usedto improve wine quality (by increasing wine complexity),




such as storage with lees and skin maceration, strongly influ-enced BA concentration. Thus, currently, in many areas andworld wineries, it is very difficult or not viable to find wineswithout any BAwhich maintain all their sensory properties.It is therefore important to seek alternatives for those fer-mented foods and beverages, in which the accumulation ofBA seems inevitable. In this context, and as we have seenthroughout this review, the use of LAB capable of degradingBA in the fermented matrix itself is a promising alternative,as has been proven in cheese and wines (Cueva et al., 2012;Herrero-Fresno et al., 2012). However, more studies areneeded in order to prove their feasibility and technologicalrelevance during the production of fermented foods.

Right now, the main challenge is to identify the catabolicactivities responsible for BA degradation. Recent inter-esting approaches reported the possibility to reduce BA inwines by using multicopper oxidases from LAB (Callej�onet al., 2014). However, it is important to note that manyof the published works assume that such activities are oxi-dases without experimental confirmation. Furthermore, ox-idases might not be the ideal BA-degrading activities,because the environmental conditions in fermented foodand beverage matrices are not physiologically optimal forthem, i.e. with low oxygen concentration, low pH value,presence of NaCl and glucose (Leuschner et al., 1998).The design of immobilization and stabilization enzyme pro-tocols may also contribute to enhancing the performance ofthese interesting enzymatic activities in such adverse foodconditions. It is also important to characterize the productsof the reactions since some, such as hydrogen peroxide, arenot desirable because they may cause color and aroma fail-ures. Therefore, it is necessary to properly and thoroughlycharacterize the biochemistry of BA degradation pathwaysand then evaluate whether they could be really useful in theconditions under which individual food fermentations areperformed.

The studies published to date indicate that the ability ofLAB to degrade BA is a strain characteristic. Furthermore,it was found that some of these strains have the undesirableability to produce BA. In this regard, next-generation DNA-sequencing techniques offer promising alternatives. Thesequence of the genomes of BA-degrading strains wouldallow the identification of undesirable genes in food bacte-ria, such as those responsible for the biosynthesis of BA. Itwould also establish whether they are chromosome orplasmid encoded and, therefore, whether they have stableor unstable characteristics, and would check for the absenceof undesirable genes, such as those encoding aminoacyldecarboxylases.

AcknowledgmentThis work was performed with the financial support of

the Spanish Ministry of Economy and Competitiveness(AGL2010-18430, AGL2012-40172-C02-01 and PRI-PI-BAR-2011-1358).



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