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Ultraviolet irradiation detoxification of aflatoxins
Trends in Food Science & Technology xx (2014) 1e6
Review
Ultraviolet irradiation detoxification of aflatoxins: A review Enjie Diao, Xiangyang Li*,1, Zheng Zhang, Wenwen Ma, Ning Ji and Haizhou Dong*,1 College of Food Science & Engineering, Shandong Agricultural University, Taian 271018, PR China (Tel.: D86 538 8242850; e-mails: xiangyang_l@163. com, [email protected]) Ultraviolet (UV) irradiation as a non-thermal technology is widely applied in the food industry for disinfection. It also can be used to degrade aflatoxins in foods dues to its low cost, without residues, and minimizing the loss of quality in terms of flavor, color and nutritional value. This article reviews the UV detoxification efficiency of aflatoxins in foods and their safety after being irradiated. UV irradiation can effectively control aflatoxigenic fungi, and degrade their metabolites, namely aflatoxins. Several recent studies suggest that UV wavelength, irradiation intensity, exposure time, moisture contents of foods, types of aflatoxins, pH and thickness of irradiated foods, significantly affect UV detoxification efficiency. The applied research and advanced equipment development in UV detoxification will be the focal points in the future.
Introduction Aflatoxins are secondary metabolites produced by three species of Aspergillus, namely A. flavus, A. parasiticus and A. nomius (Rustom, 1997). They are acutely toxic, carcinogenic, mutagenic, teratogenic substances, and immunosuppressive to most mammalian species (Dichter, 1984; Groopman, Cain, & Kensler, 1988; Massey, Stewart, Daniels, & Ling, 1995; Shank, Wogan, Gibson, * Corresponding author. 1 These authors contributed equally to this work.
& Nondasuta, 1972). Since aflatoxins were found, people have been searching effective methods to prevent or control them. Several strategies for the reduction of aflatoxins have been previously reviewed and include diverse physical, chemical, and biological methods (Das & Mishra, 2000; Haskard, Binnion, & Ahokas, 2000; Netke, Roomi, Tsao, & Niedwiecki, 1997). One of the methods is the UV irradiation, which is considered to be practical and cost effective for the detoxification of contaminated foods on a large scale. This paper will provide a general review of the applications and efficiency of UV irradiation in decomposing aflatoxins in foods. The safety and quality of the foods after being irradiated by UV light were investigated. In addition, we summarized the factors influencing UV detoxification efficiency of aflatoxins in foods, and proposed the future research focus in the UV detoxification of aflatoxins. UV detoxification efficiency of aflatoxins The UV irradiation conditions of aflatoxins in various foods and detoxification efficiency are listed in Table 1. As an effective physical method, UV irradiation has been known for many years for the destruction of aflatoxins due to their photosensitivity (Andrellos, Beckwith, & Eppley, 1967; Van Der Zijden et al., 1962). The degradation of aflatoxins in coconut oil by sunlight was demonstrated under the laboratory and plant conditions (Samarajeewa & Arseculeratne, 1974; Samarajeewa, Arseculeratne, & Bandunatha, 1977; Samarajeewa, Jayatilaka, Ranjithan, Gamage, & Arseculeratne, 1985). Shantha and Murthy (1977) reported that the treatment of peanut oil with UV light for 2 h destroyed 40e45% of afatoxins initially present in the oil. Aflatoxin B1 (AFB1) in peanut oil (2 mg/kg) was degraded completely within 30 min under the intensity of 800 mw/ cm2 (Liu et al., 2011). A photodegradation reactor (365 nm, 36 Watt) developed by ourselves was used to decompose AFB1 in peanut oil, and found that AFB1 was decreased by 86.08% within 10 min (Diao et al., 2014). Irradiation of raw whole milk artificially contaminated with aflatoxin M1 (AFM1) with UV light for 20 min at 25 C decreased the amount of toxin by 60.7%, and its destruction attributes to the opening of the double bond in the terminal furan ring in AFMl (Yousef & Marth, 1986). Also, UV irradiation (30 min) of dried figs artificially contaminated with AFB1 (250 ppb) reduced the toxin level by 45.7% (Altug, Yousef, & Marth, 1990). AFB1 in red
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Aflatoxins and initial concentrations
Sources
UV irradiation conditions Wavelength
AFB1 (0.05, 0.2, 2 mg/kg) AFB1 (20.0 nmol/100 g powder)
Peanut oil 220e400 nm Red chili powder 365 nm
AFB1
(26.60e46.78 mg/kg, 10 3% MCb) Walnut, Almond, 265 nm Pistachio, Peanut (53.12e108.68 mg/kg, 16 3% MC)
AFB2
(0.31e4.32 mg/kg, 10 3% MC)
Intensity
Time
Reduction in aflatoxin content
References
100% 77% (30 min) and 87.8% (60 min) AFB1: 87.76e96.49% (10 3% MCb) 87.44e95.27% (16 3% MC)
Liu et al., 2011 Tripathi & Mishra, 2010 Jubeen et al., 2012
Temperature Thickness of foods
800 mw/cm2 30 min 82C n.p.a 30/60 min Ambient temperature 108 J/m2 45 min Room temperature
＜1 cm 30 cm n.p.
AFB2:
96.52e99.12% (10 3% MC) 96.03e99.88% (16 3% MC)
AFG1:
97.07%e100% (10 3% MC) 94.44e100% (16 3% MC)
AFG2:
100% (10 3% MC)
(0.4e16.81 mg/kg, 16 3% MC) AFG1 (0e3.88 mg/kg, 10 3% MC) (0.43e7.04 mg/kg, 16 3% MC) AFG2 (0e0.27 mg/kg, 10 3% MC) (0e0.29 mg/kg, 16 3% MC) Total
100% (16 3% MC)
(27.29e51.82 mg/kg, 10 3% MC)
Total:
25 C
1 cm
87.81e96.71% (10 3% MC) 87.99e92.31% (16 3% MC) 89.1% (containing 0.05%H2O2)
25 C Room temperature Room temperature
n.p. ＜3 mm
60.7% (H2O2-free milk) 45.7% 86.08%
1.6 mm
75%
(64.87e164.51 mg/kg, 16 3% MC) AFM1 (1 mg/kg)
Milk
365 nm
n.p.
n.p. 30 min 6.4 mw/cm2 10 min
AFB1 AFB1
(250 mg/kg) (51.96 mg/kg)
Dried figs Peanut oil
n.p. 365 nm
AFB1
(166e1250 mg/kg)
Coconut oil
365 nm (Solar) 10 cal/cm2
a b
Is not provided. Moisture content.
20 min
10 min
Yousef & Marth, 1986 Altug et al., 1990 Diao et al., 2014 Samarajeewa et al., 1985
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Table 1. UV degradation of aflatoxins in foods with different irradiation conditions.
E. Diao et al. / Trends in Food Science & Technology xx (2014) 1e6
chili powder was reduced by 87.8% by the enzymatic coupled with UV (365 nm) after 60 min of exposure (Tripathi & Mishra, 2010). Aflatoxin G2 (AFG2) was completely eliminated in all nut samples by UVC radiation (265 nm) after 15 min of exposure, while the aflatoxin G1 (AFG1) showed 100% degradation only in almond and pistachio. After 45 min of exposure, AFB1 showed a maximum reduction of 96.5% in almond and pistachio. The degradation of total aflatoxins and AFB1 were found to follow first order kinetics (Jubeen, Bhatti, Khan, Zahoor-Ul-Hassan, & Shahid, 2012). Atalla, Hassanein, El-Beih, and Youssef (2004) reported that aflatoxins in wheat grains were eliminated on exposure to UV short (254 nm), long wave (362 nm) for 30 min. Therefore, aflatoxins can be efficiently degraded by UV irradiation, and the degradation efficiency varied with the differences of irradiation conditions. The studies in UV photodegradation products of aflatoxins further verified its detoxification capacity. Samarajeewa, Sen, Cohen, and Wei (1990) found twelve photodegradation products formed from the UV irradiation of AFB1, and Liu et al. (2010) identified three major photodegradation products, i.e. P1 (C17H14O7), P2 (C16H14O6), and P3 (C16H12O7). In addition, Gawade (2010) used UV radiation to detoxify AFB1 in the presence of methylene blue, and generated photooxidised AFB1 product (POAFB1). Safety of aflatoxins after UV irradiation Most studies had verified that the toxicity of aflatoxins in foods was reduced or even lost after UV irradiation, and the photodegradation products were less toxic than the parent toxins to chick embryos (Andrellos et al., 1967). The mutagenic activity was completely lost for the residual AFB1 in peanut oil after UV irradiation (800 mw/cm2 for 30 min) (Liu et al., 2011). They also investigated the toxicity of photodegradation products of AFB1 in water (Pw) and peanut oil (PO) on HepG2 cells, and found the cytotoxicity of Pw and PO decreased about 40 and 100%, respectively. Their results showed that the Pw is less toxic than AFB1, and the PO has almost no toxicity (Liu et al., 2012). According to the results from the Ames test and cytotoxicity of HepG2 cells, we have obtained similar results after being irradiated of AFB1 in peanut oil using a photodegradation reactor (Diao et al., 2014). Tripathi and Mishra (2010) found that AFB1 molecule produced some changes after UV treatment, which lead to its conversion to less toxic residues that promoted maximum bacterial growth or minimum growth inhibition percentage. However, Gawade (2010) revealed that the photooxidised AFB1 product (POAFB1) has an enhanced cytotocicity on African green monkey kidney (VERO) cell suspension. The reasons result in the conflicting conclusion are unclear presently. Seen from the reported literature, most of the safety evaluation on aflatoxins in foods after being irradiated were done based on the Ames test, cytotoxicity, and animal
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embryos or organs. To ensure the safety of the irradiated foods, the research in the animal toxicology and epidemiology for aflatoxins and their photodegradation products need to be supplied in the future work. Effect of UV irradiation on food quality The use of any applicable treatment conditions should not cause undesirable alterations to the nutritional and organoleptic qualities of foods (Samarajeewa et al., 1990). UV irradiation initiates free radical oxidation and forms lipid radicals, superoxide radical (SOR), and H2O2, and then leads to cross linking in carbohydrate and protein, and peroxidation of unsaturated fatty acid. Therefore, there are obvious changes in the chemical composition of food components and product quality deterioration when the UV light treatment is applied in high dose (Kolakowska, 2003). However, seen from the other reported results, UV irradiation can not cause any adverse effects, especially if UV irradiation is applied in moderate amounts (Caminiti et al., 2012; Hakguder Taze, Unluturk, Buzrul, & Alpas, 2013; Krishnamurthy, 2006(chap. 2); Tripathi & Mishra, 2010). There were minimal quality changes of red chili powder after UV exposure for 30 min, and beyond that, indued the significant losses in ascorbic acid and carotene content (Tripathi & Mishra, 2010). Our research indicated that UV irradiation can increase significantly the lightness of peanut oil, which is consistent with the results reported by Caminiti et al. (2012). The acid values and peroxide values of the treated samples were increased slightly within acceptable levels for 10 min of exposure, while obviously destroyed the unsaturated fatty acids in various degrees (Shen et al., 2014). In addition, vitamin C is a lightsensitive vitamin in various fruit and vegetable blended juices and can be degraded by UV irradiation (Koutchma, 2008; Koutchma, Keller, Parisi, & Chirtel, 2004). Therefore, it is mandatory to properly optimize the detoxification process so that the safety of the foods is ensured and its quality is maintained. Factors influencing the UV detoxification efficiency of aflatoxins Irradiation wavelength There are three regions of UV light within the electromagnetic spectrum, namely UVA (315e400 nm), UVB (280e315 nm), and UVC (200e280 nm). Among the three regions, UVA owns the maximum penetration but the lowest energy, while UVC owns the highest energy but the minimum penetration. UVC is often used to control foodborne pathogens and spoilage organisms for food safety and shelf life extension due to its tremendous damage to the DNA of microorganism (Bintsis, LitopoulouTzanetaki, & Robinson, 2000; Choudhary & Bandla, 2012). According to the published literature, some researchers used UVC (254 nm or 265 nm) to inhibit the survival of A. parasiticus and other aflatoxigenic fungi, and then
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E. Diao et al. / Trends in Food Science & Technology xx (2014) 1e6
significantly reduced aflatoxin production in foods (Atalla et al., 2004; Basaran, 2009; Jubeen et al., 2012; Moreno, Ramos, Gonzalez, & Suarez, 1987; Samarajeewa & Gamage, 1988). While others used UVA (362 nm or 365 nm) to effectively reduce the aflatoxin in foods (Samarajeewa et al., 1985; Tripathi & Mishra, 2010; Yousef & Marth, 1986). From the overall results reported by Atalla et al. (2004), the inhibitory effect of UVC (254 nm) on aflatoxin production was better than that of UVA (362 nm). While our results showed that UVA (365 nm) was better than UVC (254 nm) in degrading AFB1 in peanut oil dues to the former having the stronger penetration than that of the latter. In addition, the different results from the two researches above mentioned may be also due to the different experimental conditions and the state of the irradiated products (such as solid or liquid). Generally, UVC is used to control aflatoxins by inhibiting the growth of aflatoxigenic fungi, while UVA is directly applied to degradation of aflatoxins in foods. Up to now, it is not reported that UVB is used to detoxify aflatoxins in foods dues to its weakness in penetration and energy. Irradiation time Irradiation time is one of the most important factors influencing the UV detoxification efficiency of aflatoxins. Generally, there is a proportional decrease in aflatoxin levels with the increase of UV exposure time (Atalla et al., 2004). AFB1, B2, G1, G2, and total aflatoxins in ground nut and tree nuts were all reduced significantly with the increase of exposure time, and the degradation of AFB1 and total aflatoxins followed the first order kinetics (Jubeen et al., 2012). Considering the quality of irradiated foods, the irradiation time should be restricted in a proper range. Normally, the detoxification of aflatoxin can be achieved within 10e60 min depending upon the conditions: state and thickness of the foods, UV wavelength and intensity, and contaminated levels of aflatoxins, and so on (Atalla et al., 2004; Jubeen et al., 2012; Liu et al., 2011; Moreno et al., 1987; Tripathi & Mishra, 2010). Irradiation intensity Irradiation intensity is the other one of the most important factors influencing the UV detoxification efficiency of aflatoxins. With the same as the irradiation time, the photodegradation efficiency is increased with the increase of UV intensity. Under the same power and wavelength of UV lamp, the irradiation intensity is closely related to the illumination distance between from light source to the surface of foods irradiated. Therefore, most researchers regulated the irradiation intensity by changing the illumination distance (Liu et al., 2011; Tripathi & Mishra, 2010). However, only partial literature provided the exact data of UV intensity (Table 1). Liu et al. (2011) obtained 200, 400, and 800 mw/cm2 of UV intensity by adjusting the illumination distance. The photodegradation rate of AFB1 is strongly affected by UV intensity, and it was lower following the
order: 800 > 400 > 200 mw/cm2. AFB1 (2 mg/kg) in peanut oil can be degraded completely in 30 min at the intensity of 800 mw/cm2, while it was reduced by about 85% and 79% at the intensity of 400 and 200 mw/cm2, respectively. However, a powerful irradiation intensity does cause serious deterioration in food quality, so the irradiation intensity and time must be balanced to ensure the quality and safety of irradiated foods. Type of aflatoxins Presently, 18 different types of aflatoxins have been identified, and the major members are AFB1, B2, G1, G2, M1, and M2 (Beuchat, 1978). They have similar chemical structure (i.e. bisfuranocoumarins). Different aflatoxins have the different sensitive to UV light with different wavelengths. AFB1 absorbs UV radiation at 222, 265 and 362 nm with the maximum absorption at 362 nm (Jubeen et al., 2012). Activation of AFB1 by irradiation at 362 nm amplifies its inclination to degradation (Lillard & Lantin, 1970). AFG1 has the same C8-9 double bond in the terminal furan ring as that of AFB1, which can also be degraded easily by UV light at 362 nm. In addition, AFB2 and G2 have the same structure in the terminal furan ring without the C8-9 double bond, which may be easily degraded by UVC (especially 254 nm), which were verified by the results reported by Atalla et al. (2004) and Jubeen et al. (2012). However, Basaran (2009) reported that the UV light of 254 nm did not affect AFG2 and AFB2 but significantly reduced AFG1 and AFB1. This may be due to difference in natural contamination in analyzed nut samples and a little variation in the wavelength of light source. Based on the different sensitivity of aflatoxins to UV light, the types of aflatoxins in contaminated foods must be identified firstly, and then choose the UV wavelength where they have the maximum absorption before irradiation to improve their detoxification efficiency. Moisture contents of irradiated foods Jubeen et al. (2012) investigated the photodegradation efficiency of aflatoxins in ground nut and tree nuts at two moisture levels, namely 10 3% and 16 3%. Seen from total aflatoxin or single toxin contents (i.e. AFG1, B1, and B2), their photodegradation efficiencies at 10 3% of moisture content are better than those at 16 3% of moisture content (Table 2), which is in agreement with the results reported by Atalla et al. (2004). The reason is that the growth of fungal and aflatoxin production are enhanced by factors such as high relative humidity, high moisture content and warm temperature, and Jubeen et al. (2012) had verified that the fungal count was significantly eminent at high moisture level (16 3%) in comparison to that at low moisture level (10 3%) in all samples of ground and tree nuts analyzed. Others It is essential to control the layer thickness of irradiated foods dues to UV light penetrates food materials only up to
Please cite this article in press as: Diao, E., et al., Ultraviolet irradiation detoxification of aflatoxins: A review, Trends in Food Science & Technology (2014), http://dx.doi.org/10.1016/j.tifs.2014.12.001
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Table 2. Percent decrease of aflatoxins in twelve week stored nuts adjusted at two moisture levels (%)a. Samples Walnut
Moisture 15 min of exposure Contents (%) AFG AFB AFG2 AFB2 1 1
10 16 Almond 10 16 Pistachio 10 16 Peanut 10 16 a b c
3 3 3 3 3 3 3 3
70.25 67.37 98.37 75.28 n.d.c 86.04 86.27 90.01
68.25 32.68 52.04 50.90 40.84 68.43 52.04 27.46
100 100 100 100 n.d. n.d. 100 100
68.96 68.95 92.65 22.31 91.32 16.51 92.64 94.79
30 min of exposure
45 min of exposure
b
Total
AFG1
AFB1
AFG2 AFB2
Total
AFG1
AFB1
AFG2 AFB2
Total
53.75 33.83 60.42 46.97 69.61 44.03 56.08 41.07
100 88.81 100 95.17 n.d. 95.34 95.09 98.20
79 70 86.57 75.56 73.78 88.42 86.57 86.84
100 100 100 100 n.d. n.d. 100 100
78.93 70.60 88.97 76.74 89.91 75.14 85.20 59.94
100 94.44 100 99.57 n.d. 100 97.06 99.55
87.76 87.76 96.49 87.44 91.42 95.27 96.49 89.53
100 100 100 100 n.d. n.d. 100 100
87.81 87.99 96.71 91.52 96.58 91.92 95.70 92.31
87.96 87.96 98.07 72.57 94.92 93.50 98.07 98.39
96.52 96.52 98.37 99.88 99.12 96.03 98.37 99.36
Source from the literature reported by Jubeen et al. (2012). “Total” represents total aflatoxins. n.d. is not detected.
several millimeters depending upon their optical properties. It can easily pass through water but difficultly penetrate milk and other turbid foods, so opaque or granular foods need to be presented as a thin layer or continuous stirring during irradiation detoxification (Liu et al., 2011; Yousef & Marth, 1986). For the liquid foods, their color or the turbidity reduces the penetration capacity of the UV light (Guerrero-Beltran & Barbosa-Canovas, 2004). Therefore, understanding how to enhance the penetration capacity of UV light is a critical step in improving its detoxification efficiency. In addition, AFB1 is reported to be highly sensitive to UV irradiation at a pH of less than 3 or greater than 10 (Lillard & Lantin, 1970). Reaction of AFM1 was not affected by changes in pH of the reaction medium in the range pH 3e7. Conversion of AFM1 to AFMx was only slightly affected by temperature in the range 0e60 C (Yousef & Marth, 1987). The initial concentration of AFB1 in peanut oil has not effect on the AFB1 photodegradation in the selected range from 0.05 to 2.0 mg/kg (Liu et al., 2011). Conclusions As a nonthermal sterilization method, UV pasteurization has been widely used in the food industry for food safety and shelf life extension. The recent research in UV irradiation detoxification of aflatoxins in foods have made it a viable option for commercial application in the food industry. UV irradiation destroys the C8-9 double bond in the terminal furan ring or opens the lactone ring of AFB1, which are essential for its toxic and carcinogenic activity. The toxicity of aflatoxins and their photodegradation products are significantly reduced or even disappeared without appreciable loss in quality or nutrient content of foods. Among the major aflatoxins, only the photodegradation products or pathways of AFB1 had been studied by some researchers. The photodegradation mechanisms of the other aflatoxins also need to be explored detailedly in the future work although having similar chemical structures. In addition, it is not enough for the safety evaluation of AFB1 and its products only done by Ames test and cytotoxicity, so more animal tests and epidemiological investigation need
to be done to further confirm their toxicity, and this seems to be the most crucial on this subject. To prove the efficiency of UV detoxification of aflatoxins in foods, the choice of UV wavelength, irradiation intensity, exposure time, type of aflatoxins, moisture content of foods, and other factors must be considered for the sake of safety, nutrients and sensory quality of foods. Generally, low energy UV light (UVA) is usually chosen to treat foods containing small amount of toxins for a relatively long time, and no significant loss in quality of irradiated foods. UVC is often used to control the growth of aflatoxigenic fungi, and then inhibits the production of aflatoxins in foods. Low moisture content or relative humidity in foods benefits the UV detoxification of aflatoxins. Based on the different sensitivity to UV light, different aflatoxins should be degraded by UV light with the corresponding UV wavelength. In addition, a thin layer for irradiated foods is necessary due to the weak penetration capacity of UV light. Presently, most studies in UV detoxification of aflatoxins are only restricted in the laboratory conditions, and it is rarely used in the plant for the large-scale application. Moreover, the research and development of UV detoxification equipment fall further behind the theoretical research, which hinders its application in the food industry. Therefore, to enhance its practical application, the applied research in UV detoxification should be enhanced. Acknowledgments Financial support for the authors’ work was obtained from the Agricultural Department of China, the Public Benefit Research Foundation (201203037) and the Agricultural Technology Innovation Project in Shandong Province. The authors are grateful to College of Food Science & Engineering, Shandong Agricultural University for excellent support. References Altug, T., Yousef, A. E., & Marth, E. H. (1990). Degradation of aflatoxin B1 in dried figs by sodium bisulfite with or without heat, ultraviolet energy or hydrogen peroxide. Journal of Food Protection, 53, 581e582.
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Andrellos, P. J., Beckwith, A. C., & Eppley, R. M. (1967). Photochemical changes of aflatoxin B1. Journal-Association Official Analytical Chemists, 50, 346e350. Atalla, M. M., Hassanein, N. M., El-Beih, A. A., & Youssef, Y. A. (2004). Effect of fluorescent and UV light on mycotoxin production under different relative humidities in wheat grains. International Journal of Agriculture and Biology, 6(6), 1006e1012. Basaran, P. (2009). Reduction of Aspergillus parasiticus on hazelnut surface by UV-C treatment. International Journal of Food Science and Technology, 44(9), 1857e1863. Beuchat, L. R. (1978). Food and beverage mycology. Westport, Conn: AVI Publishing Co. Bintsis, T., Litopoulou-Tzanetaki, E., & Robinson, R. (2000). Existing and potential applications of the ultraviolet light in the food industry-A critical review. Journal of the Science of Food and Agriculture, 80, 637e645. Caminiti, I. M., Palgan, I., Mu~ noz, A., Noci, F., Whyte, P., Morgan, D. J., et al. (2012). The effect of ultraviolet light on microbial inactivation and quality attributes of apple juice. Food and Bioprocess Technology, 5(2), 680e686. Choudhary, R., & Bandla, S. (2012). Ultraviolet pasteurization for food industry. International Journal of Food Science and Nutrition Engineering, 2(1), 12e15. Das, C., & Mishra, H. N. (2000). Effect of aflatoxin B1 detoxification on the physicochemical properties and quality of ground nut meal. Food Chemistry, 70, 483e487. Diao, E. J., Shen, X. Zh, Zhang, Zh, Ji, N., Ma, W. W., & Dong, H. Zh (2014). Safety evaluation of aflatoxin B1 in peanut oil after ultraviolet irradiation detoxification in a photodegradation reactor. International Journal of Food Science and Technology, . http:// dx.doi.org/10.1111/ijfs.12648. Dichter, C. R. (1984). Risk estimates of liver cancer due to aflatoxin exposure from peanuts and peanut products. Food and Chemical Toxicology, 22, 431e437. Gawade, S. P. (2010). Photodynamic studies on aflatoxin B1 using UV radiation in the presence of methylene blue. Indian Journal of Pharmaceutical Education and Research, 44(2), 142e147. Groopman, J. D., Cain, L. G., & Kensler, T. W. (1988). Aflatoxin exposure in human populations: measurements and relationship to cancer. Critical Reviews in Toxicology, 19, 113e146. Guerrero-Beltran, J. A., & Barbosa-Canovas, G. V. (2004). Review: advantages and limitations on processing food by UV light. Food Science and Technology International, 10(3), 137e147. Hakguder Taze, B., Unluturk, S., Buzrul, S., & Alpas, H. (2013). The impact of UV-C irradiation on spoilage microorganisms and colour of orange juice. Journal of Food Science and Technology, . http:// dx.doi.org/10.1007/s13197-013-1095-7. Haskard, C., Binnion, C., & Ahokas, J. (2000). Factors affecting the sequestration of aflatoxin by Lactobacillus rhamnosus strain GG. ChemicoeBiological Interactions, 128, 39e49. Jubeen, F., Bhatti, I. A., Khan, M. Z., Zahoor-Ul-Hassan, & Shahid, M. (2012). Effect of UVC irradiation on aflatoxins in groundnut (Arachis hypogea) and tree nuts (Juglans regia, Prunus duclus and Pistachio vera). Journal of the Chemical Society of Pakistan, 34(6), 1366e1374. Kolakowska, A. (2003). Lipid oxidation in food systems. In Chemical and functional properties of food lipids (pp. 133e168). New York: CRC Press. Koutchma, T. (2008). UV light for processing foods. InIUVA news, 10(4), 24e29. Koutchma, T., Keller, S., Parisi, B., & Chirtel, S. (2004). Ultraviolet disinfection of juice products in laminar and turbulent flow reactors. Innovative Food Science and Emerging Technologies, 5, 179e189. Krishnamurthy, K. (2006). Decontamination of milk and water by pulsed UV-light and infrared heating (PhD thesis), (pp. 23e44). Pennsylvania State University.
Lillard, D. A., & Lantin, R. S. (1970). Some chemical characteristics and biological effects of photomodified aflatoxins. Journal of the Association of Analytical Chemists, 53, 1060e1063. Liu, R. J., Jin, Q. Zh, Huang, J. H., Liu, Y. F., Wang, X. G., Mao, W. Y., et al. (2011). Photodegradation of aflatoxin B1 in peanut oil. European Food Research and Technology, 232, 843e849. Liu, R. J., Jin, Q. Zh, Huang, J. H., Liu, Y. F., Wang, X. G., Zhou, X. L., et al. (2012). In vitro toxicity of aflatoxin B1 and its photodegradation products in HepG2 cells. Journal of Applied Toxicology, 32, 276e281. Liu, R. J., Jin, Q. Zh, Tao, G. J., Shan, L., Huang, J. H., Liu, Y. F., et al. (2010). Photodegradation kinetics and byproducts identification of the aflatoxin B1 in aqueous medium by UPLC-Q-TOF MS. Journal of Mass Spectrometry, 45, 553e559. Massey, T. E., Stewart, R. K., Daniels, J. M., & Ling, L. (1995). Biochemical and molecular aspects of mammalian susceptibility to aflatoxin Bl carcinogenicity. Proceedings of the Society for Experimental Biology and Medicine, 208(3), 213e227. Moreno, M. A., Ramos, M. D. C., Gonzalez, A., & Suarez, G. (1987). Effect of ultraviolet light irradiation on viability and aflatoxin production by Aspergillus parasiticus. Canadian Journal of Microbiology, 33, 927e929. Netke, S. P., Roomi, M. W., Tsao, C., & Niedwiecki, A. (1997). Ascorbic acid protects Guinea pigs from acute aflatoxin toxicity. Toxicology and Applied Pharmacology, 143, 429e435. Rustom, I. Y. S. (1997). Aflatoxin in food and feed: occurrence, legislation and inactivation by physical methods. Food Chemistry, 59(1), 57e67. Samarajeewa, U., & Arseculeratne, S. N. (1974). Control of aflatoxin contamination. 2. Detoxification of aflatoxin contaminated coconut oil. Proceedings of the Ceylon Association for the Advancement of Science, 30, 36, (abstract). Samarajeewa, U., Arseculeratne, S. N., & Bandunatha, C. H. S. R. (1977). Degradation of aflatoxin in coconut oil and copra meal. Journal of the National Science Council of Sri Lanka, 5, 1e12. Samarajeewa, U., & Gamage, T. V. (1988). Combination of solvent and radiation effects on degradation of aflatoxin B1. Mircen Journal of Applied Microbiology and Biotechnology, 4(2), 203e208. Samarajeewa, U., Jayatilaka, C. L. V., Ranjithan, A., Gamage, T. V., & Arseculeratne, S. N. (1985). A pilot plant for detoxification of aflatoxin B1-contaminated coconut oil by solar irradiation. MIRCEN Journal, 1, 333e343. Samarajeewa, U., Sen, A. C., Cohen, M. D., & Wei, C. I. (1990). Detoxification of aflatoxins in foods and feeds by physical and chemical methods. Journal of Food Protection, 53, 489e501. Shank, R. C., Wogan, G. N., Gibson, J. B., & Nondasuta, A. (1972). Dietary aflatoxins and human liver cancer II. Aflatoxins in market foods and foodstuffs of Thailand and Hong Kong. Food and Cosmetics Toxicology, 10, 61e69. Shantha, T., & Murthy, V. S. (1977). Photo-destruction of aflatoxin in groundnut oil. Indian Journal of Technology, 15, 453e454. Shen, X. Zh., Diao, E. J., Zhang, Zh., Ji, N., Ma, W. W., & Dong, H. Zh. (2014). Effects of UV-irradiation detoxification in a photodegradation reactor on quality of peanut oil. International Food Research Journal, 21(6), 2311e2314. Tripathi, S., & Mishra, H. N. (2010). Enzymatic coupled with UV degradation aflatoxin B1 in red chili powder. Journal of Food Quality, 33, 186e203. Van Der Zijden, A. S. M., Blanche Koelensmid, W. A. A., Boldingh, J., Barrett, C. B., Ord, W. O., & Philp, J. (1962). Aspergillus Flavus and Turkey X disease: isolation in crystalline form of a toxin responsible for Turkey X disease. Nature, 195, 1060e1062. Yousef, A. E., & Marth, E. H. (1986). Use of ultraviolet energy to degrade aflatoxin M1 in raw or heated milk with and without added peroxide. Journal of Dairy Science, 69(9), 2243e2247. Yousef, A. E., & Marth, E. H. (1987). Kinetics of interaction of aflatoxin Ml in aqueous solutions irradiated with ultraviolet energy. Journal of Agricultural and Food Chemistry, 35, 785e789.
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Review
Ultraviolet irradiation detoxification of aflatoxins: A review Enjie Diao, Xiangyang Li*,1, Zheng Zhang, Wenwen Ma, Ning Ji and Haizhou Dong*,1 College of Food Science & Engineering, Shandong Agricultural University, Taian 271018, PR China (Tel.: D86 538 8242850; e-mails: xiangyang_l@163. com, [email protected]) Ultraviolet (UV) irradiation as a non-thermal technology is widely applied in the food industry for disinfection. It also can be used to degrade aflatoxins in foods dues to its low cost, without residues, and minimizing the loss of quality in terms of flavor, color and nutritional value. This article reviews the UV detoxification efficiency of aflatoxins in foods and their safety after being irradiated. UV irradiation can effectively control aflatoxigenic fungi, and degrade their metabolites, namely aflatoxins. Several recent studies suggest that UV wavelength, irradiation intensity, exposure time, moisture contents of foods, types of aflatoxins, pH and thickness of irradiated foods, significantly affect UV detoxification efficiency. The applied research and advanced equipment development in UV detoxification will be the focal points in the future.
Introduction Aflatoxins are secondary metabolites produced by three species of Aspergillus, namely A. flavus, A. parasiticus and A. nomius (Rustom, 1997). They are acutely toxic, carcinogenic, mutagenic, teratogenic substances, and immunosuppressive to most mammalian species (Dichter, 1984; Groopman, Cain, & Kensler, 1988; Massey, Stewart, Daniels, & Ling, 1995; Shank, Wogan, Gibson, * Corresponding author. 1 These authors contributed equally to this work.
& Nondasuta, 1972). Since aflatoxins were found, people have been searching effective methods to prevent or control them. Several strategies for the reduction of aflatoxins have been previously reviewed and include diverse physical, chemical, and biological methods (Das & Mishra, 2000; Haskard, Binnion, & Ahokas, 2000; Netke, Roomi, Tsao, & Niedwiecki, 1997). One of the methods is the UV irradiation, which is considered to be practical and cost effective for the detoxification of contaminated foods on a large scale. This paper will provide a general review of the applications and efficiency of UV irradiation in decomposing aflatoxins in foods. The safety and quality of the foods after being irradiated by UV light were investigated. In addition, we summarized the factors influencing UV detoxification efficiency of aflatoxins in foods, and proposed the future research focus in the UV detoxification of aflatoxins. UV detoxification efficiency of aflatoxins The UV irradiation conditions of aflatoxins in various foods and detoxification efficiency are listed in Table 1. As an effective physical method, UV irradiation has been known for many years for the destruction of aflatoxins due to their photosensitivity (Andrellos, Beckwith, & Eppley, 1967; Van Der Zijden et al., 1962). The degradation of aflatoxins in coconut oil by sunlight was demonstrated under the laboratory and plant conditions (Samarajeewa & Arseculeratne, 1974; Samarajeewa, Arseculeratne, & Bandunatha, 1977; Samarajeewa, Jayatilaka, Ranjithan, Gamage, & Arseculeratne, 1985). Shantha and Murthy (1977) reported that the treatment of peanut oil with UV light for 2 h destroyed 40e45% of afatoxins initially present in the oil. Aflatoxin B1 (AFB1) in peanut oil (2 mg/kg) was degraded completely within 30 min under the intensity of 800 mw/ cm2 (Liu et al., 2011). A photodegradation reactor (365 nm, 36 Watt) developed by ourselves was used to decompose AFB1 in peanut oil, and found that AFB1 was decreased by 86.08% within 10 min (Diao et al., 2014). Irradiation of raw whole milk artificially contaminated with aflatoxin M1 (AFM1) with UV light for 20 min at 25 C decreased the amount of toxin by 60.7%, and its destruction attributes to the opening of the double bond in the terminal furan ring in AFMl (Yousef & Marth, 1986). Also, UV irradiation (30 min) of dried figs artificially contaminated with AFB1 (250 ppb) reduced the toxin level by 45.7% (Altug, Yousef, & Marth, 1990). AFB1 in red
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2
Aflatoxins and initial concentrations
Sources
UV irradiation conditions Wavelength
AFB1 (0.05, 0.2, 2 mg/kg) AFB1 (20.0 nmol/100 g powder)
Peanut oil 220e400 nm Red chili powder 365 nm
AFB1
(26.60e46.78 mg/kg, 10 3% MCb) Walnut, Almond, 265 nm Pistachio, Peanut (53.12e108.68 mg/kg, 16 3% MC)
AFB2
(0.31e4.32 mg/kg, 10 3% MC)
Intensity
Time
Reduction in aflatoxin content
References
100% 77% (30 min) and 87.8% (60 min) AFB1: 87.76e96.49% (10 3% MCb) 87.44e95.27% (16 3% MC)
Liu et al., 2011 Tripathi & Mishra, 2010 Jubeen et al., 2012
Temperature Thickness of foods
800 mw/cm2 30 min 82C n.p.a 30/60 min Ambient temperature 108 J/m2 45 min Room temperature
＜1 cm 30 cm n.p.
AFB2:
96.52e99.12% (10 3% MC) 96.03e99.88% (16 3% MC)
AFG1:
97.07%e100% (10 3% MC) 94.44e100% (16 3% MC)
AFG2:
100% (10 3% MC)
(0.4e16.81 mg/kg, 16 3% MC) AFG1 (0e3.88 mg/kg, 10 3% MC) (0.43e7.04 mg/kg, 16 3% MC) AFG2 (0e0.27 mg/kg, 10 3% MC) (0e0.29 mg/kg, 16 3% MC) Total
100% (16 3% MC)
(27.29e51.82 mg/kg, 10 3% MC)
Total:
25 C
1 cm
87.81e96.71% (10 3% MC) 87.99e92.31% (16 3% MC) 89.1% (containing 0.05%H2O2)
25 C Room temperature Room temperature
n.p. ＜3 mm
60.7% (H2O2-free milk) 45.7% 86.08%
1.6 mm
75%
(64.87e164.51 mg/kg, 16 3% MC) AFM1 (1 mg/kg)
Milk
365 nm
n.p.
n.p. 30 min 6.4 mw/cm2 10 min
AFB1 AFB1
(250 mg/kg) (51.96 mg/kg)
Dried figs Peanut oil
n.p. 365 nm
AFB1
(166e1250 mg/kg)
Coconut oil
365 nm (Solar) 10 cal/cm2
a b
Is not provided. Moisture content.
20 min
10 min
Yousef & Marth, 1986 Altug et al., 1990 Diao et al., 2014 Samarajeewa et al., 1985
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Table 1. UV degradation of aflatoxins in foods with different irradiation conditions.
E. Diao et al. / Trends in Food Science & Technology xx (2014) 1e6
chili powder was reduced by 87.8% by the enzymatic coupled with UV (365 nm) after 60 min of exposure (Tripathi & Mishra, 2010). Aflatoxin G2 (AFG2) was completely eliminated in all nut samples by UVC radiation (265 nm) after 15 min of exposure, while the aflatoxin G1 (AFG1) showed 100% degradation only in almond and pistachio. After 45 min of exposure, AFB1 showed a maximum reduction of 96.5% in almond and pistachio. The degradation of total aflatoxins and AFB1 were found to follow first order kinetics (Jubeen, Bhatti, Khan, Zahoor-Ul-Hassan, & Shahid, 2012). Atalla, Hassanein, El-Beih, and Youssef (2004) reported that aflatoxins in wheat grains were eliminated on exposure to UV short (254 nm), long wave (362 nm) for 30 min. Therefore, aflatoxins can be efficiently degraded by UV irradiation, and the degradation efficiency varied with the differences of irradiation conditions. The studies in UV photodegradation products of aflatoxins further verified its detoxification capacity. Samarajeewa, Sen, Cohen, and Wei (1990) found twelve photodegradation products formed from the UV irradiation of AFB1, and Liu et al. (2010) identified three major photodegradation products, i.e. P1 (C17H14O7), P2 (C16H14O6), and P3 (C16H12O7). In addition, Gawade (2010) used UV radiation to detoxify AFB1 in the presence of methylene blue, and generated photooxidised AFB1 product (POAFB1). Safety of aflatoxins after UV irradiation Most studies had verified that the toxicity of aflatoxins in foods was reduced or even lost after UV irradiation, and the photodegradation products were less toxic than the parent toxins to chick embryos (Andrellos et al., 1967). The mutagenic activity was completely lost for the residual AFB1 in peanut oil after UV irradiation (800 mw/cm2 for 30 min) (Liu et al., 2011). They also investigated the toxicity of photodegradation products of AFB1 in water (Pw) and peanut oil (PO) on HepG2 cells, and found the cytotoxicity of Pw and PO decreased about 40 and 100%, respectively. Their results showed that the Pw is less toxic than AFB1, and the PO has almost no toxicity (Liu et al., 2012). According to the results from the Ames test and cytotoxicity of HepG2 cells, we have obtained similar results after being irradiated of AFB1 in peanut oil using a photodegradation reactor (Diao et al., 2014). Tripathi and Mishra (2010) found that AFB1 molecule produced some changes after UV treatment, which lead to its conversion to less toxic residues that promoted maximum bacterial growth or minimum growth inhibition percentage. However, Gawade (2010) revealed that the photooxidised AFB1 product (POAFB1) has an enhanced cytotocicity on African green monkey kidney (VERO) cell suspension. The reasons result in the conflicting conclusion are unclear presently. Seen from the reported literature, most of the safety evaluation on aflatoxins in foods after being irradiated were done based on the Ames test, cytotoxicity, and animal
3
embryos or organs. To ensure the safety of the irradiated foods, the research in the animal toxicology and epidemiology for aflatoxins and their photodegradation products need to be supplied in the future work. Effect of UV irradiation on food quality The use of any applicable treatment conditions should not cause undesirable alterations to the nutritional and organoleptic qualities of foods (Samarajeewa et al., 1990). UV irradiation initiates free radical oxidation and forms lipid radicals, superoxide radical (SOR), and H2O2, and then leads to cross linking in carbohydrate and protein, and peroxidation of unsaturated fatty acid. Therefore, there are obvious changes in the chemical composition of food components and product quality deterioration when the UV light treatment is applied in high dose (Kolakowska, 2003). However, seen from the other reported results, UV irradiation can not cause any adverse effects, especially if UV irradiation is applied in moderate amounts (Caminiti et al., 2012; Hakguder Taze, Unluturk, Buzrul, & Alpas, 2013; Krishnamurthy, 2006(chap. 2); Tripathi & Mishra, 2010). There were minimal quality changes of red chili powder after UV exposure for 30 min, and beyond that, indued the significant losses in ascorbic acid and carotene content (Tripathi & Mishra, 2010). Our research indicated that UV irradiation can increase significantly the lightness of peanut oil, which is consistent with the results reported by Caminiti et al. (2012). The acid values and peroxide values of the treated samples were increased slightly within acceptable levels for 10 min of exposure, while obviously destroyed the unsaturated fatty acids in various degrees (Shen et al., 2014). In addition, vitamin C is a lightsensitive vitamin in various fruit and vegetable blended juices and can be degraded by UV irradiation (Koutchma, 2008; Koutchma, Keller, Parisi, & Chirtel, 2004). Therefore, it is mandatory to properly optimize the detoxification process so that the safety of the foods is ensured and its quality is maintained. Factors influencing the UV detoxification efficiency of aflatoxins Irradiation wavelength There are three regions of UV light within the electromagnetic spectrum, namely UVA (315e400 nm), UVB (280e315 nm), and UVC (200e280 nm). Among the three regions, UVA owns the maximum penetration but the lowest energy, while UVC owns the highest energy but the minimum penetration. UVC is often used to control foodborne pathogens and spoilage organisms for food safety and shelf life extension due to its tremendous damage to the DNA of microorganism (Bintsis, LitopoulouTzanetaki, & Robinson, 2000; Choudhary & Bandla, 2012). According to the published literature, some researchers used UVC (254 nm or 265 nm) to inhibit the survival of A. parasiticus and other aflatoxigenic fungi, and then
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E. Diao et al. / Trends in Food Science & Technology xx (2014) 1e6
significantly reduced aflatoxin production in foods (Atalla et al., 2004; Basaran, 2009; Jubeen et al., 2012; Moreno, Ramos, Gonzalez, & Suarez, 1987; Samarajeewa & Gamage, 1988). While others used UVA (362 nm or 365 nm) to effectively reduce the aflatoxin in foods (Samarajeewa et al., 1985; Tripathi & Mishra, 2010; Yousef & Marth, 1986). From the overall results reported by Atalla et al. (2004), the inhibitory effect of UVC (254 nm) on aflatoxin production was better than that of UVA (362 nm). While our results showed that UVA (365 nm) was better than UVC (254 nm) in degrading AFB1 in peanut oil dues to the former having the stronger penetration than that of the latter. In addition, the different results from the two researches above mentioned may be also due to the different experimental conditions and the state of the irradiated products (such as solid or liquid). Generally, UVC is used to control aflatoxins by inhibiting the growth of aflatoxigenic fungi, while UVA is directly applied to degradation of aflatoxins in foods. Up to now, it is not reported that UVB is used to detoxify aflatoxins in foods dues to its weakness in penetration and energy. Irradiation time Irradiation time is one of the most important factors influencing the UV detoxification efficiency of aflatoxins. Generally, there is a proportional decrease in aflatoxin levels with the increase of UV exposure time (Atalla et al., 2004). AFB1, B2, G1, G2, and total aflatoxins in ground nut and tree nuts were all reduced significantly with the increase of exposure time, and the degradation of AFB1 and total aflatoxins followed the first order kinetics (Jubeen et al., 2012). Considering the quality of irradiated foods, the irradiation time should be restricted in a proper range. Normally, the detoxification of aflatoxin can be achieved within 10e60 min depending upon the conditions: state and thickness of the foods, UV wavelength and intensity, and contaminated levels of aflatoxins, and so on (Atalla et al., 2004; Jubeen et al., 2012; Liu et al., 2011; Moreno et al., 1987; Tripathi & Mishra, 2010). Irradiation intensity Irradiation intensity is the other one of the most important factors influencing the UV detoxification efficiency of aflatoxins. With the same as the irradiation time, the photodegradation efficiency is increased with the increase of UV intensity. Under the same power and wavelength of UV lamp, the irradiation intensity is closely related to the illumination distance between from light source to the surface of foods irradiated. Therefore, most researchers regulated the irradiation intensity by changing the illumination distance (Liu et al., 2011; Tripathi & Mishra, 2010). However, only partial literature provided the exact data of UV intensity (Table 1). Liu et al. (2011) obtained 200, 400, and 800 mw/cm2 of UV intensity by adjusting the illumination distance. The photodegradation rate of AFB1 is strongly affected by UV intensity, and it was lower following the
order: 800 > 400 > 200 mw/cm2. AFB1 (2 mg/kg) in peanut oil can be degraded completely in 30 min at the intensity of 800 mw/cm2, while it was reduced by about 85% and 79% at the intensity of 400 and 200 mw/cm2, respectively. However, a powerful irradiation intensity does cause serious deterioration in food quality, so the irradiation intensity and time must be balanced to ensure the quality and safety of irradiated foods. Type of aflatoxins Presently, 18 different types of aflatoxins have been identified, and the major members are AFB1, B2, G1, G2, M1, and M2 (Beuchat, 1978). They have similar chemical structure (i.e. bisfuranocoumarins). Different aflatoxins have the different sensitive to UV light with different wavelengths. AFB1 absorbs UV radiation at 222, 265 and 362 nm with the maximum absorption at 362 nm (Jubeen et al., 2012). Activation of AFB1 by irradiation at 362 nm amplifies its inclination to degradation (Lillard & Lantin, 1970). AFG1 has the same C8-9 double bond in the terminal furan ring as that of AFB1, which can also be degraded easily by UV light at 362 nm. In addition, AFB2 and G2 have the same structure in the terminal furan ring without the C8-9 double bond, which may be easily degraded by UVC (especially 254 nm), which were verified by the results reported by Atalla et al. (2004) and Jubeen et al. (2012). However, Basaran (2009) reported that the UV light of 254 nm did not affect AFG2 and AFB2 but significantly reduced AFG1 and AFB1. This may be due to difference in natural contamination in analyzed nut samples and a little variation in the wavelength of light source. Based on the different sensitivity of aflatoxins to UV light, the types of aflatoxins in contaminated foods must be identified firstly, and then choose the UV wavelength where they have the maximum absorption before irradiation to improve their detoxification efficiency. Moisture contents of irradiated foods Jubeen et al. (2012) investigated the photodegradation efficiency of aflatoxins in ground nut and tree nuts at two moisture levels, namely 10 3% and 16 3%. Seen from total aflatoxin or single toxin contents (i.e. AFG1, B1, and B2), their photodegradation efficiencies at 10 3% of moisture content are better than those at 16 3% of moisture content (Table 2), which is in agreement with the results reported by Atalla et al. (2004). The reason is that the growth of fungal and aflatoxin production are enhanced by factors such as high relative humidity, high moisture content and warm temperature, and Jubeen et al. (2012) had verified that the fungal count was significantly eminent at high moisture level (16 3%) in comparison to that at low moisture level (10 3%) in all samples of ground and tree nuts analyzed. Others It is essential to control the layer thickness of irradiated foods dues to UV light penetrates food materials only up to
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5
Table 2. Percent decrease of aflatoxins in twelve week stored nuts adjusted at two moisture levels (%)a. Samples Walnut
Moisture 15 min of exposure Contents (%) AFG AFB AFG2 AFB2 1 1
10 16 Almond 10 16 Pistachio 10 16 Peanut 10 16 a b c
3 3 3 3 3 3 3 3
70.25 67.37 98.37 75.28 n.d.c 86.04 86.27 90.01
68.25 32.68 52.04 50.90 40.84 68.43 52.04 27.46
100 100 100 100 n.d. n.d. 100 100
68.96 68.95 92.65 22.31 91.32 16.51 92.64 94.79
30 min of exposure
45 min of exposure
b
Total
AFG1
AFB1
AFG2 AFB2
Total
AFG1
AFB1
AFG2 AFB2
Total
53.75 33.83 60.42 46.97 69.61 44.03 56.08 41.07
100 88.81 100 95.17 n.d. 95.34 95.09 98.20
79 70 86.57 75.56 73.78 88.42 86.57 86.84
100 100 100 100 n.d. n.d. 100 100
78.93 70.60 88.97 76.74 89.91 75.14 85.20 59.94
100 94.44 100 99.57 n.d. 100 97.06 99.55
87.76 87.76 96.49 87.44 91.42 95.27 96.49 89.53
100 100 100 100 n.d. n.d. 100 100
87.81 87.99 96.71 91.52 96.58 91.92 95.70 92.31
87.96 87.96 98.07 72.57 94.92 93.50 98.07 98.39
96.52 96.52 98.37 99.88 99.12 96.03 98.37 99.36
Source from the literature reported by Jubeen et al. (2012). “Total” represents total aflatoxins. n.d. is not detected.
several millimeters depending upon their optical properties. It can easily pass through water but difficultly penetrate milk and other turbid foods, so opaque or granular foods need to be presented as a thin layer or continuous stirring during irradiation detoxification (Liu et al., 2011; Yousef & Marth, 1986). For the liquid foods, their color or the turbidity reduces the penetration capacity of the UV light (Guerrero-Beltran & Barbosa-Canovas, 2004). Therefore, understanding how to enhance the penetration capacity of UV light is a critical step in improving its detoxification efficiency. In addition, AFB1 is reported to be highly sensitive to UV irradiation at a pH of less than 3 or greater than 10 (Lillard & Lantin, 1970). Reaction of AFM1 was not affected by changes in pH of the reaction medium in the range pH 3e7. Conversion of AFM1 to AFMx was only slightly affected by temperature in the range 0e60 C (Yousef & Marth, 1987). The initial concentration of AFB1 in peanut oil has not effect on the AFB1 photodegradation in the selected range from 0.05 to 2.0 mg/kg (Liu et al., 2011). Conclusions As a nonthermal sterilization method, UV pasteurization has been widely used in the food industry for food safety and shelf life extension. The recent research in UV irradiation detoxification of aflatoxins in foods have made it a viable option for commercial application in the food industry. UV irradiation destroys the C8-9 double bond in the terminal furan ring or opens the lactone ring of AFB1, which are essential for its toxic and carcinogenic activity. The toxicity of aflatoxins and their photodegradation products are significantly reduced or even disappeared without appreciable loss in quality or nutrient content of foods. Among the major aflatoxins, only the photodegradation products or pathways of AFB1 had been studied by some researchers. The photodegradation mechanisms of the other aflatoxins also need to be explored detailedly in the future work although having similar chemical structures. In addition, it is not enough for the safety evaluation of AFB1 and its products only done by Ames test and cytotoxicity, so more animal tests and epidemiological investigation need
to be done to further confirm their toxicity, and this seems to be the most crucial on this subject. To prove the efficiency of UV detoxification of aflatoxins in foods, the choice of UV wavelength, irradiation intensity, exposure time, type of aflatoxins, moisture content of foods, and other factors must be considered for the sake of safety, nutrients and sensory quality of foods. Generally, low energy UV light (UVA) is usually chosen to treat foods containing small amount of toxins for a relatively long time, and no significant loss in quality of irradiated foods. UVC is often used to control the growth of aflatoxigenic fungi, and then inhibits the production of aflatoxins in foods. Low moisture content or relative humidity in foods benefits the UV detoxification of aflatoxins. Based on the different sensitivity to UV light, different aflatoxins should be degraded by UV light with the corresponding UV wavelength. In addition, a thin layer for irradiated foods is necessary due to the weak penetration capacity of UV light. Presently, most studies in UV detoxification of aflatoxins are only restricted in the laboratory conditions, and it is rarely used in the plant for the large-scale application. Moreover, the research and development of UV detoxification equipment fall further behind the theoretical research, which hinders its application in the food industry. Therefore, to enhance its practical application, the applied research in UV detoxification should be enhanced. Acknowledgments Financial support for the authors’ work was obtained from the Agricultural Department of China, the Public Benefit Research Foundation (201203037) and the Agricultural Technology Innovation Project in Shandong Province. The authors are grateful to College of Food Science & Engineering, Shandong Agricultural University for excellent support. References Altug, T., Yousef, A. E., & Marth, E. H. (1990). Degradation of aflatoxin B1 in dried figs by sodium bisulfite with or without heat, ultraviolet energy or hydrogen peroxide. Journal of Food Protection, 53, 581e582.
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Andrellos, P. J., Beckwith, A. C., & Eppley, R. M. (1967). Photochemical changes of aflatoxin B1. Journal-Association Official Analytical Chemists, 50, 346e350. Atalla, M. M., Hassanein, N. M., El-Beih, A. A., & Youssef, Y. A. (2004). Effect of fluorescent and UV light on mycotoxin production under different relative humidities in wheat grains. International Journal of Agriculture and Biology, 6(6), 1006e1012. Basaran, P. (2009). Reduction of Aspergillus parasiticus on hazelnut surface by UV-C treatment. International Journal of Food Science and Technology, 44(9), 1857e1863. Beuchat, L. R. (1978). Food and beverage mycology. Westport, Conn: AVI Publishing Co. Bintsis, T., Litopoulou-Tzanetaki, E., & Robinson, R. (2000). Existing and potential applications of the ultraviolet light in the food industry-A critical review. Journal of the Science of Food and Agriculture, 80, 637e645. Caminiti, I. M., Palgan, I., Mu~ noz, A., Noci, F., Whyte, P., Morgan, D. J., et al. (2012). The effect of ultraviolet light on microbial inactivation and quality attributes of apple juice. Food and Bioprocess Technology, 5(2), 680e686. Choudhary, R., & Bandla, S. (2012). Ultraviolet pasteurization for food industry. International Journal of Food Science and Nutrition Engineering, 2(1), 12e15. Das, C., & Mishra, H. N. (2000). Effect of aflatoxin B1 detoxification on the physicochemical properties and quality of ground nut meal. Food Chemistry, 70, 483e487. Diao, E. J., Shen, X. Zh, Zhang, Zh, Ji, N., Ma, W. W., & Dong, H. Zh (2014). Safety evaluation of aflatoxin B1 in peanut oil after ultraviolet irradiation detoxification in a photodegradation reactor. International Journal of Food Science and Technology, . http:// dx.doi.org/10.1111/ijfs.12648. Dichter, C. R. (1984). Risk estimates of liver cancer due to aflatoxin exposure from peanuts and peanut products. Food and Chemical Toxicology, 22, 431e437. Gawade, S. P. (2010). Photodynamic studies on aflatoxin B1 using UV radiation in the presence of methylene blue. Indian Journal of Pharmaceutical Education and Research, 44(2), 142e147. Groopman, J. D., Cain, L. G., & Kensler, T. W. (1988). Aflatoxin exposure in human populations: measurements and relationship to cancer. Critical Reviews in Toxicology, 19, 113e146. Guerrero-Beltran, J. A., & Barbosa-Canovas, G. V. (2004). Review: advantages and limitations on processing food by UV light. Food Science and Technology International, 10(3), 137e147. Hakguder Taze, B., Unluturk, S., Buzrul, S., & Alpas, H. (2013). The impact of UV-C irradiation on spoilage microorganisms and colour of orange juice. Journal of Food Science and Technology, . http:// dx.doi.org/10.1007/s13197-013-1095-7. Haskard, C., Binnion, C., & Ahokas, J. (2000). Factors affecting the sequestration of aflatoxin by Lactobacillus rhamnosus strain GG. ChemicoeBiological Interactions, 128, 39e49. Jubeen, F., Bhatti, I. A., Khan, M. Z., Zahoor-Ul-Hassan, & Shahid, M. (2012). Effect of UVC irradiation on aflatoxins in groundnut (Arachis hypogea) and tree nuts (Juglans regia, Prunus duclus and Pistachio vera). Journal of the Chemical Society of Pakistan, 34(6), 1366e1374. Kolakowska, A. (2003). Lipid oxidation in food systems. In Chemical and functional properties of food lipids (pp. 133e168). New York: CRC Press. Koutchma, T. (2008). UV light for processing foods. InIUVA news, 10(4), 24e29. Koutchma, T., Keller, S., Parisi, B., & Chirtel, S. (2004). Ultraviolet disinfection of juice products in laminar and turbulent flow reactors. Innovative Food Science and Emerging Technologies, 5, 179e189. Krishnamurthy, K. (2006). Decontamination of milk and water by pulsed UV-light and infrared heating (PhD thesis), (pp. 23e44). Pennsylvania State University.
Lillard, D. A., & Lantin, R. S. (1970). Some chemical characteristics and biological effects of photomodified aflatoxins. Journal of the Association of Analytical Chemists, 53, 1060e1063. Liu, R. J., Jin, Q. Zh, Huang, J. H., Liu, Y. F., Wang, X. G., Mao, W. Y., et al. (2011). Photodegradation of aflatoxin B1 in peanut oil. European Food Research and Technology, 232, 843e849. Liu, R. J., Jin, Q. Zh, Huang, J. H., Liu, Y. F., Wang, X. G., Zhou, X. L., et al. (2012). In vitro toxicity of aflatoxin B1 and its photodegradation products in HepG2 cells. Journal of Applied Toxicology, 32, 276e281. Liu, R. J., Jin, Q. Zh, Tao, G. J., Shan, L., Huang, J. H., Liu, Y. F., et al. (2010). Photodegradation kinetics and byproducts identification of the aflatoxin B1 in aqueous medium by UPLC-Q-TOF MS. Journal of Mass Spectrometry, 45, 553e559. Massey, T. E., Stewart, R. K., Daniels, J. M., & Ling, L. (1995). Biochemical and molecular aspects of mammalian susceptibility to aflatoxin Bl carcinogenicity. Proceedings of the Society for Experimental Biology and Medicine, 208(3), 213e227. Moreno, M. A., Ramos, M. D. C., Gonzalez, A., & Suarez, G. (1987). Effect of ultraviolet light irradiation on viability and aflatoxin production by Aspergillus parasiticus. Canadian Journal of Microbiology, 33, 927e929. Netke, S. P., Roomi, M. W., Tsao, C., & Niedwiecki, A. (1997). Ascorbic acid protects Guinea pigs from acute aflatoxin toxicity. Toxicology and Applied Pharmacology, 143, 429e435. Rustom, I. Y. S. (1997). Aflatoxin in food and feed: occurrence, legislation and inactivation by physical methods. Food Chemistry, 59(1), 57e67. Samarajeewa, U., & Arseculeratne, S. N. (1974). Control of aflatoxin contamination. 2. Detoxification of aflatoxin contaminated coconut oil. Proceedings of the Ceylon Association for the Advancement of Science, 30, 36, (abstract). Samarajeewa, U., Arseculeratne, S. N., & Bandunatha, C. H. S. R. (1977). Degradation of aflatoxin in coconut oil and copra meal. Journal of the National Science Council of Sri Lanka, 5, 1e12. Samarajeewa, U., & Gamage, T. V. (1988). Combination of solvent and radiation effects on degradation of aflatoxin B1. Mircen Journal of Applied Microbiology and Biotechnology, 4(2), 203e208. Samarajeewa, U., Jayatilaka, C. L. V., Ranjithan, A., Gamage, T. V., & Arseculeratne, S. N. (1985). A pilot plant for detoxification of aflatoxin B1-contaminated coconut oil by solar irradiation. MIRCEN Journal, 1, 333e343. Samarajeewa, U., Sen, A. C., Cohen, M. D., & Wei, C. I. (1990). Detoxification of aflatoxins in foods and feeds by physical and chemical methods. Journal of Food Protection, 53, 489e501. Shank, R. C., Wogan, G. N., Gibson, J. B., & Nondasuta, A. (1972). Dietary aflatoxins and human liver cancer II. Aflatoxins in market foods and foodstuffs of Thailand and Hong Kong. Food and Cosmetics Toxicology, 10, 61e69. Shantha, T., & Murthy, V. S. (1977). Photo-destruction of aflatoxin in groundnut oil. Indian Journal of Technology, 15, 453e454. Shen, X. Zh., Diao, E. J., Zhang, Zh., Ji, N., Ma, W. W., & Dong, H. Zh. (2014). Effects of UV-irradiation detoxification in a photodegradation reactor on quality of peanut oil. International Food Research Journal, 21(6), 2311e2314. Tripathi, S., & Mishra, H. N. (2010). Enzymatic coupled with UV degradation aflatoxin B1 in red chili powder. Journal of Food Quality, 33, 186e203. Van Der Zijden, A. S. M., Blanche Koelensmid, W. A. A., Boldingh, J., Barrett, C. B., Ord, W. O., & Philp, J. (1962). Aspergillus Flavus and Turkey X disease: isolation in crystalline form of a toxin responsible for Turkey X disease. Nature, 195, 1060e1062. Yousef, A. E., & Marth, E. H. (1986). Use of ultraviolet energy to degrade aflatoxin M1 in raw or heated milk with and without added peroxide. Journal of Dairy Science, 69(9), 2243e2247. Yousef, A. E., & Marth, E. H. (1987). Kinetics of interaction of aflatoxin Ml in aqueous solutions irradiated with ultraviolet energy. Journal of Agricultural and Food Chemistry, 35, 785e789.
Please cite this article in press as: Diao, E., et al., Ultraviolet irradiation detoxification of aflatoxins: A review, Trends in Food Science & Technology (2014), http://dx.doi.org/10.1016/j.tifs.2014.12.001