Review pubs.acs.org/JAFC
Presence of Ochratoxin A (OTA) Mycotoxin in Alcoholic Drinks from Southern European Countries: Wine and Beer Julia Bellver Soto,† Mónica Fernández-Franzón,§ María-José Ruiz,§ and Ana Juan-García*,§ †
Public Health Research Center, C/La Paz s/n, 46600 Alzira, Spain Laboratory of Food Chemistry and Toxicology, Faculty of Pharmacy, University of Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot, València, Spain
§
ABSTRACT: The main filamentous fungi producers of mycotoxins are Aspergillus spp., Penicillium spp., and Fusarium spp. Their effect can provoke a broad range of toxic properties including carcinogenicity and neurotoxicity, as well as reproductive and developmental toxicities. Ochratoxin A (OTA) is produced by Aspergillus and Penicillium spp. The purpose of this review was to evaluate the risk assessment of OTA in alcoholic drinks (beer and wine) by compiling the results obtained from studies and reviews related to the presence of OTA in these two drinks from southern European countries in the period 2005−2013 and comparing those results with the legislation available in the European Union. KEYWORDS: ochratoxin A, mycotoxins, beer, wine
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mycotoxins and also African regions in some kinds of food.11 In 1996 in a declaration by the Food and Agriculture Organization (FAO), it was indicated that 25% of the food harvest is contaminated by mycotoxins;12 nowadays, this value must be probably higher. In addition, economic losses have been associated with the presence of mycotoxins in food as well as human health risks, animal productivity, and commerce.13 Recent reviews found in the literature collect numerous aspects such as mycotoxin toxicity, clinical signs in different animal species, determination of different mycotoxins present in a food product, comparison between protocols, comparison of analytical techniques, and comparison of international legislation which tries to regulate the presence of mycotoxins in foods.14 The literature collects also reviews referred to general food but not including drinks. In recent years OTA analysis in wine and beer has been widely studied, and several research groups have focused their studies on these drinks; however, there is no review dealing with the OTA findings from recent years and its consumption, especially in the Mediterranean Arch. Nowadays, it seems impossible to avoid OTA contamination, although many efforts are made to reduce its levels. It has been demonstrated that chronic exposure to OTA might present a risk for human health, that OTA intake is related to diet and contamination levels in consumed food (incidence and OTA levels), and that varies according to country, region, and ethnicity. The purpose of this review was to evaluate the risk assessment of OTA in alcoholic drinks (beer and wine) by compiling the results obtained from studies and reviews related to the presence of OTA in these two drinks from southern European countries and especially from the Mediterranean
INTRODUCTION Mycotoxins are a group of naturally occurring toxic secondary metabolites present in food as contaminants of susceptible commodities. Mycotoxin contamination may occur as a result of environmental conditions during crop growth as well as improper harvesting, storage, and processing operations. The complex ecology of mold growth and mycotoxin production can produce mixtures of mycotoxins in foods and feeds, especially in cereals.1,2 Each fungi can produce more than one mycotoxin, and due to their high stability, fungi may not be on food but mycotoxins can still persist.3,4 The main filamentous fungi producers of mycotoxins are Aspergillus spp., Penicillium spp., and Fusarium spp., and their effects can provoke a broad range of toxic properties including carcinogenicity and neurotoxicity, as well as reproductive and developmental toxicities.5−7 Ochratoxin A (OTA) is produced by Aspergillus spp. and Penicillium spp. It is one of the most toxic mycotoxins and derives from 3,4-dihydrocumarin linked to an amide bond with an amino group of L-β-phenylalanine8 (see Figure 1).
Figure 1. Chemical structure of ochratoxin A (OTA).
OTA can be mainly present in foods such as cereals, grapes, coffee, spices, and, cocoa. In cereals, it is mainly produced by Penicillium verrucosum and in grapes, coffee, and cocoa, by Aspergillus carbonarius.9 Its presence in alcoholic beverages is mainly in red wine followed by rosé wine and white wine.10 It is also common to find OTA in any kind of food of animal origin fed contaminated feed. Although it is found throughout the world, European regions are the most affected by these © 2014 American Chemical Society
Received: Revised: Accepted: Published: 7643
January 15, 2014 July 11, 2014 July 20, 2014 July 20, 2014 dx.doi.org/10.1021/jf501737h | J. Agric. Food Chem. 2014, 62, 7643−7651
Journal of Agricultural and Food Chemistry
Review
Table 1. Incidence, Range, and Median Concentration of OTA in Beer country (ref) Spain24
product beer with alcohol without alcohol
Spain20
beer from Spain imported
Spain19
beer from Spain imported
Italy25 Italy55 Turkey21
beer beer beer from Turkey imported
Czech Republic17 Hungary23 a
beer beer
no. of samples
incidence (%)
range (ng/mL)
median (ng/mL)
31 21 10 88 31 57 69 35 34 106 30 35 31 4 115 25
77 67 100 82.9 83.8 82.5 100 100 100 67.9 16.7 14 13 25 39 100
0.205a 0.205a 0.152 0.007−0.204 0.007−0.147 0.007−0.204 0.008−0.498 ni ni 0.002−0.189 0.2 ng/mL (see Table 1). A beer study from the Czech Republic17 reveals that the incidence (39%) correlates with data obtained from the European Commission (2002) and only one pale beer sample presented the highest value: 0.2438 ng/mL. Other studies outside the region of interest in this review have been consulted, and it is interesting to observe that in a study in which beers from different origins (United States,
Arch, in the period of 2005−2013, and comparing those results with the legislation available in the European Union (EU).
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PRESENCE OF OTA IN BEER Beer is a drink obtained from must alcoholic fermentation, mainly elaborated from germ barley solely or mixed with other cereals, starchy substances, yeast, and water. It is the third most consumed drink around the world after water and tea. In 2012, there were 182.69 million of kiloliters consumed, Asia being the continent that registered the highest consumption (33.6%), followed by Europe (27.7%), Latin America (16.215%), and North America (14.5%); nonetheless, the highest beer consumers per capita are found in the Czech Republic followed by Germany.15 In the past two decades there have been several studies confirming the presence of OTA mycotoxin in beers from all over the world. It has been stated in the European Commission’s report that beer consumption contributes 5% of OTA intake.16 The origin of OTA mycotoxin in beer comes from contamination of prime material used for its processing as barley, malt, or cereal derivatives. Contaminated barley grains contain ochratoxigenic strains from A. ochraceus and P. verrucosum, which are transferred to beer. OTA provided by these strains on cereals is stable through the cooking process, but it suffers a reduction during beer production and, as a consequence, during fermentation it is the yeast that retains the original content of OTA (eliminating between 2 and 19% of OTA) and the rest is transmitted to the final consumable beer.17 The EU has not established limits for OTA in beer, because its presence in this drink should be controlled in another more appropriate phase of its production chain, specifically in malt prime material (Directive (UE) No. 105/2010);18 however, several countries have established maximum permitted limits of OTA in beer, for example, The Netherlands (0.3 ng/mL), Finland (0.5 ng/mL), or Italy (0.2 ng/mL), and in research studies several authors have assumed a recommended limit of 0.2 ng/mL.19,20 Incidence and Presence of OTA in Beer. In this review, only published papers related to OTA in beer or wine from southern Europe, and more specifically from the Mediterranean 7644
dx.doi.org/10.1021/jf501737h | J. Agric. Food Chem. 2014, 62, 7643−7651
Journal of Agricultural and Food Chemistry
Review
Table 2. OTA Intake Estimation for Beer Consumed (Data Taken from Table 1) country (ref) 24
Spain Spain20 Spain19 Italy25 Turkey21 Hungary23 a
body wt (kg)
consumption (mL/day)
OTA median (ng/g)
60 60 60 60 60 60
500 500d 500d 197 200 33
0.044 0.036 0.070 0.019 0.02 0.127
OTA DIa median (ng/kg bw/day) % OTA TDIb (17.2 ng/kg bw/day) % SCFc 0.36 0.29 0.58 0.06 0.011 0.42
2.09 1.7 3.4 0.36 2.44 0.06
7.2 5.9 11.6 1.24 8.4 0.22
DI, daily intake. bTDI, tolerable daily intake. cSCF, Scientific Committee on Food. dCollected from Araguas et al.24
When studies of beers from outside Europe were examined, such as a study carried out in Korea,15,63 OTA intake associated with beer consumption was very low, but it was recommended to develop a new evaluation attending to actual consumption data in recent years as the Asian population has experienced a remarkable increase of consumption in beer.15 In summary, beer seems not to constitute an important factor for OTA exposure in the population, but it is an additional source to control and consider for OTA mycotoxin intake calculation.
Europe, Australia, Canada, Mexico, South America, and Asia) were analyzed, no OTA levels were detected,26 coinciding with results obtained in studies performed on beers from China.27 OTA Levels in Beer. According to the published studies, OTA mean concentrations obtained in beer present few variations. The lowest OTA mean value achieved was
Presence of Ochratoxin A (OTA) Mycotoxin in Alcoholic Drinks from Southern European Countries: Wine and Beer Julia Bellver Soto,† Mónica Fernández-Franzón,§ María-José Ruiz,§ and Ana Juan-García*,§ †
Public Health Research Center, C/La Paz s/n, 46600 Alzira, Spain Laboratory of Food Chemistry and Toxicology, Faculty of Pharmacy, University of Valencia, Av. Vicent Andrés Estellés s/n, 46100 Burjassot, València, Spain
§
ABSTRACT: The main filamentous fungi producers of mycotoxins are Aspergillus spp., Penicillium spp., and Fusarium spp. Their effect can provoke a broad range of toxic properties including carcinogenicity and neurotoxicity, as well as reproductive and developmental toxicities. Ochratoxin A (OTA) is produced by Aspergillus and Penicillium spp. The purpose of this review was to evaluate the risk assessment of OTA in alcoholic drinks (beer and wine) by compiling the results obtained from studies and reviews related to the presence of OTA in these two drinks from southern European countries in the period 2005−2013 and comparing those results with the legislation available in the European Union. KEYWORDS: ochratoxin A, mycotoxins, beer, wine
■
mycotoxins and also African regions in some kinds of food.11 In 1996 in a declaration by the Food and Agriculture Organization (FAO), it was indicated that 25% of the food harvest is contaminated by mycotoxins;12 nowadays, this value must be probably higher. In addition, economic losses have been associated with the presence of mycotoxins in food as well as human health risks, animal productivity, and commerce.13 Recent reviews found in the literature collect numerous aspects such as mycotoxin toxicity, clinical signs in different animal species, determination of different mycotoxins present in a food product, comparison between protocols, comparison of analytical techniques, and comparison of international legislation which tries to regulate the presence of mycotoxins in foods.14 The literature collects also reviews referred to general food but not including drinks. In recent years OTA analysis in wine and beer has been widely studied, and several research groups have focused their studies on these drinks; however, there is no review dealing with the OTA findings from recent years and its consumption, especially in the Mediterranean Arch. Nowadays, it seems impossible to avoid OTA contamination, although many efforts are made to reduce its levels. It has been demonstrated that chronic exposure to OTA might present a risk for human health, that OTA intake is related to diet and contamination levels in consumed food (incidence and OTA levels), and that varies according to country, region, and ethnicity. The purpose of this review was to evaluate the risk assessment of OTA in alcoholic drinks (beer and wine) by compiling the results obtained from studies and reviews related to the presence of OTA in these two drinks from southern European countries and especially from the Mediterranean
INTRODUCTION Mycotoxins are a group of naturally occurring toxic secondary metabolites present in food as contaminants of susceptible commodities. Mycotoxin contamination may occur as a result of environmental conditions during crop growth as well as improper harvesting, storage, and processing operations. The complex ecology of mold growth and mycotoxin production can produce mixtures of mycotoxins in foods and feeds, especially in cereals.1,2 Each fungi can produce more than one mycotoxin, and due to their high stability, fungi may not be on food but mycotoxins can still persist.3,4 The main filamentous fungi producers of mycotoxins are Aspergillus spp., Penicillium spp., and Fusarium spp., and their effects can provoke a broad range of toxic properties including carcinogenicity and neurotoxicity, as well as reproductive and developmental toxicities.5−7 Ochratoxin A (OTA) is produced by Aspergillus spp. and Penicillium spp. It is one of the most toxic mycotoxins and derives from 3,4-dihydrocumarin linked to an amide bond with an amino group of L-β-phenylalanine8 (see Figure 1).
Figure 1. Chemical structure of ochratoxin A (OTA).
OTA can be mainly present in foods such as cereals, grapes, coffee, spices, and, cocoa. In cereals, it is mainly produced by Penicillium verrucosum and in grapes, coffee, and cocoa, by Aspergillus carbonarius.9 Its presence in alcoholic beverages is mainly in red wine followed by rosé wine and white wine.10 It is also common to find OTA in any kind of food of animal origin fed contaminated feed. Although it is found throughout the world, European regions are the most affected by these © 2014 American Chemical Society
Received: Revised: Accepted: Published: 7643
January 15, 2014 July 11, 2014 July 20, 2014 July 20, 2014 dx.doi.org/10.1021/jf501737h | J. Agric. Food Chem. 2014, 62, 7643−7651
Journal of Agricultural and Food Chemistry
Review
Table 1. Incidence, Range, and Median Concentration of OTA in Beer country (ref) Spain24
product beer with alcohol without alcohol
Spain20
beer from Spain imported
Spain19
beer from Spain imported
Italy25 Italy55 Turkey21
beer beer beer from Turkey imported
Czech Republic17 Hungary23 a
beer beer
no. of samples
incidence (%)
range (ng/mL)
median (ng/mL)
31 21 10 88 31 57 69 35 34 106 30 35 31 4 115 25
77 67 100 82.9 83.8 82.5 100 100 100 67.9 16.7 14 13 25 39 100
0.205a 0.205a 0.152 0.007−0.204 0.007−0.147 0.007−0.204 0.008−0.498 ni ni 0.002−0.189 0.2 ng/mL (see Table 1). A beer study from the Czech Republic17 reveals that the incidence (39%) correlates with data obtained from the European Commission (2002) and only one pale beer sample presented the highest value: 0.2438 ng/mL. Other studies outside the region of interest in this review have been consulted, and it is interesting to observe that in a study in which beers from different origins (United States,
Arch, in the period of 2005−2013, and comparing those results with the legislation available in the European Union (EU).
■
PRESENCE OF OTA IN BEER Beer is a drink obtained from must alcoholic fermentation, mainly elaborated from germ barley solely or mixed with other cereals, starchy substances, yeast, and water. It is the third most consumed drink around the world after water and tea. In 2012, there were 182.69 million of kiloliters consumed, Asia being the continent that registered the highest consumption (33.6%), followed by Europe (27.7%), Latin America (16.215%), and North America (14.5%); nonetheless, the highest beer consumers per capita are found in the Czech Republic followed by Germany.15 In the past two decades there have been several studies confirming the presence of OTA mycotoxin in beers from all over the world. It has been stated in the European Commission’s report that beer consumption contributes 5% of OTA intake.16 The origin of OTA mycotoxin in beer comes from contamination of prime material used for its processing as barley, malt, or cereal derivatives. Contaminated barley grains contain ochratoxigenic strains from A. ochraceus and P. verrucosum, which are transferred to beer. OTA provided by these strains on cereals is stable through the cooking process, but it suffers a reduction during beer production and, as a consequence, during fermentation it is the yeast that retains the original content of OTA (eliminating between 2 and 19% of OTA) and the rest is transmitted to the final consumable beer.17 The EU has not established limits for OTA in beer, because its presence in this drink should be controlled in another more appropriate phase of its production chain, specifically in malt prime material (Directive (UE) No. 105/2010);18 however, several countries have established maximum permitted limits of OTA in beer, for example, The Netherlands (0.3 ng/mL), Finland (0.5 ng/mL), or Italy (0.2 ng/mL), and in research studies several authors have assumed a recommended limit of 0.2 ng/mL.19,20 Incidence and Presence of OTA in Beer. In this review, only published papers related to OTA in beer or wine from southern Europe, and more specifically from the Mediterranean 7644
dx.doi.org/10.1021/jf501737h | J. Agric. Food Chem. 2014, 62, 7643−7651
Journal of Agricultural and Food Chemistry
Review
Table 2. OTA Intake Estimation for Beer Consumed (Data Taken from Table 1) country (ref) 24
Spain Spain20 Spain19 Italy25 Turkey21 Hungary23 a
body wt (kg)
consumption (mL/day)
OTA median (ng/g)
60 60 60 60 60 60
500 500d 500d 197 200 33
0.044 0.036 0.070 0.019 0.02 0.127
OTA DIa median (ng/kg bw/day) % OTA TDIb (17.2 ng/kg bw/day) % SCFc 0.36 0.29 0.58 0.06 0.011 0.42
2.09 1.7 3.4 0.36 2.44 0.06
7.2 5.9 11.6 1.24 8.4 0.22
DI, daily intake. bTDI, tolerable daily intake. cSCF, Scientific Committee on Food. dCollected from Araguas et al.24
When studies of beers from outside Europe were examined, such as a study carried out in Korea,15,63 OTA intake associated with beer consumption was very low, but it was recommended to develop a new evaluation attending to actual consumption data in recent years as the Asian population has experienced a remarkable increase of consumption in beer.15 In summary, beer seems not to constitute an important factor for OTA exposure in the population, but it is an additional source to control and consider for OTA mycotoxin intake calculation.
Europe, Australia, Canada, Mexico, South America, and Asia) were analyzed, no OTA levels were detected,26 coinciding with results obtained in studies performed on beers from China.27 OTA Levels in Beer. According to the published studies, OTA mean concentrations obtained in beer present few variations. The lowest OTA mean value achieved was
