Stewart Postharvest Review

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Published online 01 December 2008 doi: 10.2212/spr.2008.6.5 .... Levels of fumonisins B1 and B2 (FB1 and FB2, respectively) in different fractions of dry-milled corn. ... converted to N-(carboxymethyl)-fumonisin B1 [44]. Variable reductions of ...
Stewart Postharvest Review An international journal for reviews in postharvest biology and technology

Effects of processing on mycotoxins Dojin Ryu,1 Andreia Bianchini2 and Lloyd B Bullerman2* 1 2

Department of Nutrition and Food Sciences, Texas Woman's University, Denton, TX, USA Department of Food Science and Technology, University of Nebraska, Lincoln, NE, USA

Abstract Purpose of the review: This review summarises the effects of common food processes on several important mycotoxins. Findings: Aflatoxins, ochratoxin A, fumonisins, deoxynivalenol and zearalenone are commonly occurring secondary fungal metabolites known to be toxic to animals and humans. These mycotoxins are fairly heat stable and some level tends to remain in processed food products. While varying degrees of reduction have been documented during some food processes, including sorting, cleaning, milling, baking, canning, frying, roasting, brewing, nixtamalisation and extrusion, removal or destruction is not complete. The reduction of mycotoxins is generally correlated with the degree of heat employed in the process; however, heat energy alone may not cause complete elimination of mycotoxins during food processing. Extrusion cooking as a process has been shown to be effective in reducing most mycotoxins at temperatures above 150°C. Fumonisins, in particular, may be reduced significantly in the presence of a reducing sugar such as glucose, but the degradation or reaction mechanism is not fully understood. Directions for future research: Additional future research is needed to delineate the chemical and toxicological fate of mycotoxins and their degradation products during food processing to ensure the safety of processed foods. Keywords: mycotoxins; reduction; thermal processing; extrusion

Abbreviation High performance Liquid Chromatography HPLC *Correspondence to: Lloyd B Bullerman, Department of Food Science & Technology, 322 Food Industry Complex, University of Nebraska-Lincoln, Lincoln, NE 68583-0919. Tel: +1 402 472 2801; Fax: +1 402 472 1693; email: [email protected] Stewart Postharvest Review 2008, 6:5 Published online 01 December 2008 doi: 10.2212/spr.2008.6.5

© 2008 Stewart Postharvest Solutions (UK) Ltd.

Introduction Mycotoxins are toxic compounds produced by certain filamentous microfungi or moulds. Mycotoxins considered to be important, including aflatoxins, ochratoxins, fumonisins, deoxynivalenol and zearalenone, are produced mainly by three fungal genera, Aspergillus, Penicillium and Fusarium. These fungi are found in soil, dust and air in all agricultural areas worldwide. Some of these fungi may invade plants and cereal grains in the field during the growing season, as well as during postharvest handling processes such as drying and storage. Cereal grains are the most frequently affected commodity while all major crops and commodities may be contaminated with one or more mycotoxins (Table 1). These mycotoxins are heat stable in general so that they may not be destroyed by common processing methods including most thermal processes. The stable nature of mycotoxins often leads to contamination of products in downstream processes including finished products destined for human and animal consumption. Effects of common food processing on the important mycotoxins are discussed in this article.

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Table 1. Significant mycotoxins producing moulds and the commodities commonly contaminated. Mycotoxins

Major producing organisms

Commodities commonly affected

Aflatoxins

Aspergillus flavus, A. parasiticus, A. nomius

Corn, peanuts, tree nuts, rice, cottonseed

Ochratoxins

A. ochraceus, A. carbonarius, Penicillium verrucosum

Wheat, barley, oats, rye, sorghum, peanuts, peas, beans, green coffee beans, raisins, beer, wine, etc.

Fumonisins

Fusarium verticillioides, F. proliferatum, F. subglutinans

Corn, wheat, barley, rice

Deoxynivalenol (vomitoxin)

F. graminearum, F. culmorum, F. crookwellense

Wheat, barley, rye

Zearalenone

F. graminearum, F. culmorum, F. crookwellense

Corn

Non-thermal processes Physical separation and cleaning Removal of contaminated or damaged kernels by sorting and cleaning may lower mycotoxin concentrations without altering the product. Combination of physical separation techniques including density segregation and colour sorting could reduce aflatoxin contents in peanuts by up to 99% [1]. In general, grains are cleaned to remove kernels with extensive mould growth, broken kernels and fine materials. According to Sydenham et al. [2], cleaning reduced fumonisin concentrations in corn by 26–69%. Cleaning prior to milling can also reduce deoxynivalenol concentrations by 5.5–19% from scab infested wheat and barley kernels [3]. In comparison, cleaning reduced the ochratoxin A content in barley by only 2–3% [4]. While it may be an effective means to reduce the levels of contamination of some mycotoxins, the extent of the reduction is variable and the efficiency of cleaning is generally dependent on the initial condition of the grain or extent of contamination. Dry and wet milling Similar to other physical separation and cleaning methods, milling processes do not destroy or completely remove all mycotoxins but rather redistribute the toxins into different milled fractions. Hence, mycotoxins tend to be concentrated in certain fractions, particularly in germ and bran in the dry milling process [3–6]. Katta et al., [5] demonstrated this with fumonisins in dry milling of corn where the highest amount of fumonisins was found in the fines followed by the bran and germ with a similar pattern of redistribution for both fumonisin B1 and B2 (Figure 1). All three of these fractions are commonly used for animal feed or oil extraction. Different sizes of grits and flour that may be destined for human consumption had lesser amounts of fumonisins than the unmilled corn. More recently, Brera et al. [7] reported similar distributions of fumonisin B1 during an industrial scale dry milling process of corn. Similar trends in redistribution of other mycotoxins, including aflatoxins, ochratoxin A, deoxynivalenol and

zearalenone, during dry milling of wheat, barley and other cereal grains have also been previously documented [3, 4, 6, 8–10]. In wet milling of corn, mycotoxins may be dissolved into the excess amount of water during steeping and distributed among the byproducts of the process. This is particularly true for the water-soluble mycotoxins, fumonisins and deoxynivalenol. Bennett et al. [11] reported that fumonisins in contaminated corn were dissolved into the steep water or distributed to the gluten, fibre and germ fractions, leaving no detectable amounts in the starch. In general, the highest concentration of mycotoxins, including aflatoxins, may be found in steep water followed by fibre, gluten and germ, while the starch fraction tends to be relatively free of mycotoxins [6, 12]. Fermentation Ethanol fermentation by yeast has little or no direct impact on the level of mycotoxins. In general, mycotoxins tend to concentrate in the distillers grains and other by-products. According to Lillehoj et al. [13], aflatoxin was not detected in distilled alcohol but accumulated mainly in spent grains. Murthy et al. [14] also reported that 55% of aflatoxin B1 was detected in wet grains and 45% in thin stillage after 60 h of fermentation. Similarly, when corn naturally contaminated with fumonisin B1 was fermented to produce ethanol, fumonisin B1 was not found in the distilled ethanol but was found in about a two-fold concentration of the original amount in the distiller’s grains [15]. Unlike ethanol fermentation using yeasts, lactic acid fermentation may lead to a significant reduction in the concentration of aflatoxin B1 by as much as 75% [16]. During the brewing process, fumonisins B1 and B2 added to wort were stable through fermentation and remained in the beer with negligible uptake of the toxins by the yeast [17]. The losses of fumonisins B1 and B2 were estimated to be 3– 28% and 9–17%, respectively, during an 8-day fermentation period using Saccharomyces cerevisiae. In the same study, a 2–13% reduction of ochratoxin A was observed. Fermentation of corn naturally contaminated with zearalenone using S. 2

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Figure 1. Levels of fumonisins B1 and B2 (FB1 and FB2, respectively) in different fractions of dry-milled corn. Data from Katta et al. [5].

uvarum resulted in no destruction of the mycotoxin, and concentrations of the toxin in the recovered solids were about twice the levels in the original corn [18]. No carry-over residue of zearalenone was detected in the distilled ethanol. However, significant amounts of zearalenone may be converted to β-zearalenol by several strains of S. cerevisiae during fermentation of koji and wort [19, 20]. Thermal processes Baking, canning, frying and roasting The application of heat is the most common method of conventional food processing, and includes boiling, baking, canning, frying and roasting. Extrusion cooking, which is also a thermal process, is discussed separately since this process also utilises pressure and mechanical energy (shear) simultaneously with heat. Other methods that use heat as a part of the process, eg, nixtamalisation, in conjunction with alkaline treatment will also be discussed separately. The effects of heat on the stability of several mycotoxins during various thermal processes have been reported [21–24]. Aflatoxins are very heat stable compounds. During ordinary cooking or boiling of polished rice under atmospheric pressure, reduction of aflatoxin B1 averaged 34% while greater reduction was achieved by pressure cooking, ranging from 78–88% [25, 26]. In an earlier study with naturally contaminated cornmeal and corn grits, baking of corn muffins and boiling reduced aflatoxin B1 by 13 and 28%, respectively, while frying the boiled grits resulted in 34–53% total reduction [27]. Variable reduction of aflatoxin B1 during roasting has been reported, as the process conditions, ie, temperature and time, vary widely depending on the commodity and end use. The reduction of aflatoxin in pistachio nuts ranged from 17–63% during roasting at 90–150°C for 30–120 min [28]. In the comparison of different roasting methods, the greatest reduction of total aflatoxins B1, B2, G1 and G2 in naturally contaminated green coffee beans was achieved by traditional roasting at 180ºC for 10 min (56%) followed by oven roast-

ing at 150°C for 15 min (48%), and household microwave oven roasting for 4 min (42%) [29]. Ochratoxin is stable during bread baking, with no apparent loss or reduction [4, 30], while baking of biscuits resulted in about two-thirds of the toxin being destroyed or immobilised [31]. During pressure cooking of beans in water, up to 84% reduction of ochratoxin A was achieved [32]. Similar results were reported by autoclaving oatmeal with 50% water which gave a 74% reduction of ochratoxin, while autoclaving dry oatmeal or rice cereal gave greater losses of about 87% [33]. The reduction of ochratoxin A during roasting of green coffee beans is highly variable ranging from 13–93% due to an array of different factors and techniques, including the variety and moisture content of the beans as well as the degree of contamination, temperature and time [34, 35]. Within the range, greater reduction of ochratoxin A was observed with higher temperatures and longer times during roasting such as the process used to make darker beans for espresso coffee [36]. Stability of fumonisin B1 during various thermal processes has been documented. Boiling of Fusarium verticillioides culture material for 30 min and subsequent drying at 60°C for 24 h did not change the fumonisin B1 concentration [37]. The reduction of fumonisin B1 is considered to be a first order reaction when heated at 100–200°C for up to 60 min in aqueous buffered model systems at pH 4, 7 and 10 [22]. According to this study, fumonisin B1 was least stable at pH 4, followed by pH 10 and 7, respectively, while greater than 90% reduction was observed after 60 min at 175°C at all pH levels. Using a domestic pressure cooker did not affect fumonisin concentration in cooking polenta [7]. Canning of cream style corn and whole kernel corn reduced fumonisin B1

Figure 2. Percentage (%) fumonisin B1 remaining in spiked grits before cooking, after cooking and after toasting during the production of corn flakes with and without sugars. S + M + HF = Sucrose in combination with maltose and high fructose corn syrup. G + M + HF = Glucose in combination with maltose and high fructose corn syrup. Data from Castelo [52].

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Figure 3. Effects of temperature and screw speed on fumonisin B1 (FB1) recovery during extrusion cooking of corn grits. Data from Katta et al. [65].

by 9 and 15%, respectively. No significant reduction was observed during baking corn muffins at 204°C for 20 min while baking corn bread at 232°C for 20 min showed a 48% decrease in fumonisin levels [38]. In an earlier study, baking corn muffins at 175 and 200°C resulted in 16 and 28% reductions of fumonisin, respectively. Frying corn masa at 140– 170°C for up to 6 min did not reduce fumonisins, while frying tortilla chips at 190°C for 15 min resulted in a 67% reduction of fumonisin [39]. Unlike other mycotoxins, fumonisins may undergo a common Maillard reaction with its primary amine group when heated in the presence of a reducing sugar [40]. Howard et al. [41] suggested that fumonisin B1 reacts with reducing sugars to form a stable reaction product, N-(carboxymethyl)fumonisin B1. In the reaction between fumonisin B1 and glucose, N-(1-deoxy-D-fructos-1-yl) fumonisin B1 has been identified as a major product [42, 43], which may be further converted to N-(carboxymethyl)-fumonisin B1 [44]. Variable reductions of deoxynivalenol, ranging from 0 to 35%, were observed during traditional baking processes for cookies and bread [9, 45]. In addition, baking of Egyptian bread at 350°C for 2 min and sponge cake at 170°C for 30 min resulted in no significant reduction of deoxynivalenol [46, 47]. Canning of cream style corn showed a slight (12%) reduction of deoxynivalenol while canning baby food and dog food gave no reduction [48].

pressure cooking and toasting, respectively [49]. Similar reductions of fumonisin B1 and B2 ranging from 60 to 70% during the entire process were reported by De Girolamo et al. [50]. According to Meister [51], reduction of fumonisin during cooking and roasting resulted in 20–65% and 6–35%, respectively. In another study, up to 89% reduction of fumonisin B1 was achieved during the process by addition of glucose as shown in Figure 2 [52]. It should be noted that the significant reduction of fumonisin might be attributed to binding of the toxin to the matrix rather than destruction. The occurrence of such matrix-bound or “hidden” fumonisins in commercial corn flake samples was reported by Kim et al. [53]. Nixtamalisation Production of tortillas by alkaline cooking or traditional nixtamalisation has been shown to be effective in reducing mycotoxin contents in corn depending on the levels of calcium hydroxide (lime) and heat employed. Torres et al. [54] reported significant reductions of aflatoxin during this process – approximately 52% in the tortillas, 84% in the tortilla chips, and 79% in the corn chips. In another study, the levels of aflatoxin B1, aflatoxin M1 and aflatoxin B1-8,9-dihydrodiol were reduced by 94, 90 and 93%, respectively, and the reduction during nixtamalisation was augmented by adding 1.5% hydrogen peroxide [55]. However, Méndez-Albores et al. [56] observed reformation of aflatoxins in tortillas and masa by 34 and 57%, respectively, by acidification after a 93% reduction with the traditional Mexican nixtamalisation process. Hendrich et al. [57] reported 99% reduction of fumonisin B1 in cultured corn during nixtamalisation with 1.2% lime and cooking at 100°C for 1 h. They also observed formation of hydrolysed fumonisin B1, as a main reaction product that led to no reduction of toxicity in rats. Nixtamalisation was also effective in reducing zearalenone as almost complete reduction was observed in naturally contaminated corn by 2% calcium hydroxide treatment [58].

Figure 4. Percent (%) fumonisin B1 remaining in corn grits extruded at 160°C. Glucose concentration (0, 2.5, 5, 7.5 and 10%) and screw speed (40, 60 and 80 rpm) were variables. Data from Castelo et al. [66].

Corn flake processing Corn flakes, one of the most common breakfast cereals, are unique in their preparation methods, employing pressure cooking, typically at 18 psi steam pressure for 2 h, followed by air drying (65°C), flaking and toasting (>300°C for about 50 sec). Depending on the presence of sugars, the reduction of aflatoxin ranged from 64 to 67% and 78 to 85% during 4

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Extrusion Unlike other food processing methods, extrusion cooking, or simply extrusion, employs high heat (commonly 120– 220°C), high pressure (commonly 100–2,000 psi) and mechanical shear energy (torque) simultaneously. Raw ingredients are rapidly processed while they are forced through the heated barrel under high pressure by a rotating screw or screws and exit the extruder with a sudden release of pressure as finished product. The whole process typically takes less than a few minutes to complete in most commercial applications and is being used extensively in the production of breakfast cereals, snack foods, pet foods and textured foods. Factors affecting the extrusion process include characteristics of raw ingredients (eg, size, shape and moisture content), feed rate, temperature and screw speed (or residence time).

As noted with corn flake processing, the significant reduction of fumonisins by extrusion with added glucose may not account for matrix bound fumonisins. Fumonisins that are conjugated with the matrix may not be extracted by solvents employed in conventional analytical techniques, including enzyme-linked immunosorbent assays (ELISA) or highperformance liquid chromatography (HPLC). In addition, reduced concentrations of fumonisin determined by HPLC may not be directly correlated to destruction of the compound due to the formation of fumonisin-sugar complexes via Maillard reaction. Murphy et al. [40] suggested that the primary amine in fumonisin, necessary for derivatisation to allow fluorescence detection with HPLC, will become unavailable if the Maillard reaction occurs. Consequently, such analytical methods may not present conclusive data on the reduction of fumonisin concentrations or its biological activity.

Buser and Abbas [59] reported an additional 33% reduction of aflatoxin in cottonseed when extrusion temperatures were increased to 160°C from 104°C, while the reduction may be maximised to 76% by modifying conditions. Extrusion of corn tortillas with 0, 0.3 and 0.5% lime reduced the level of aflatoxin B1 by 46, 74 and 85%, respectively [55]. More recently, Castells [60] observed that the reduction of aflatoxins in artificially contaminated rice meal ranged from 51 to 95% depending on the type of aflatoxin (B1, B2, G1 and G2) and the variables studied – initial moisture content of samples (24, 27 and 30%) and barrel temperature (140, 170 and 200°C).

The efficacy of extrusion in reducing fumonisin B1 in corn grits in the absence and presence (10%, dry weight basis) of glucose was recently evaluated [67]. Flaking corn grit samples artificially contaminated and fermented with F. verticillioides were extruded at 160°C and 60 rpm screw speed using a single screw extruder. The concentration of fumonisin B1 and its degradation products were identified and determined with a mass balance approach using liquid chromatographyfluorescence and liquid chromatography-mass spectrometry. Extrusion decreased fumonisin B1 by 21–37% while the same process with added glucose further decreased the toxin by 77–87%. The main degradation product in grits extruded with glucose was N-(deoxy-D-fructos-1-yl) fumonisin B1. In a subsequent bioassay using male Sprague-Dawley rats, corn grits extruded with glucose gave reduced toxicity of fumonisins as determined by severity of kidney lesions and kidney weights [68].

For ochratoxin A, reduction of 40% was reported during pilot scale extrusion of wholemeal wheat flour at varying temperatures (116–201°C) and moisture contents (17–25%) [61]. In comparison, the extrusion process was more effective in reducing zearalenone in artificially contaminated corn grits. Ryu et al. [62] examined two screw configurations in a laboratory scale twin screw extruder, using mixing and nonmixing screws. Greater reduction of zearalenone was achieved using mixing screws (66–83%) than with nonmixing screws (65–77%) when the grits were extruded at temperatures of 120, 140 and 160°C. Addition of additives may also play a significant role in reduction of mycotoxins during extrusion as >95% reduction of deoxynivalenol was observed at 150 and 180°C in the presence of 1% sodium metabisulphite [63]. The effects of extrusion on the fate of fumonisins have been documented in a series of different experiments. In general, a greater reduction of fumonisin B1 in corn grits was achieved with mixing screw configuration and increasing temperature and residence time (Figure 3) [64, 65]. In another study, Castelo et al. [66] reported that greater reduction of fumonisin B1 was obtained in the presence of glucose (45–67%) than fructose (32–52%) or sucrose (26–43%). Up to 93% reduction of fumonisin B1 was achieved during extrusion at 160°C with varying concentrations of glucose (2.5, 5.0, 7.0 and 10.0%) and screw speeds (40, 60 and 80 rpm) as shown in Figure 4.

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