Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
Scholar Journal Available online: www.journalsci.com Journal of Science and today's world ISSN 2322-326X
Research Article Aflatoxin M1 Contamination in Dairy Products Reza Kazemi Darsanaki1, Marjan Miri2 1
Young Researchers Club, Lahijan Branch, Islamic Azad University, Lahijan, Iran Department of Chemical Engineering, Dezful Branch, Islamic Azad University, Dezful, Iran Received: 23 May 2013 / Accepted: 25 May 2013 / Published: 27 May 2013
2
Copyright © 2013 Reza Kazemi Darsanaki et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract Mycotoxins are fungal secondary metabolites that if ingested can cause a variety of adverse effects on both humans and animals. Aflatoxins are toxic fungal metabolites found in foods and feeds. When ruminants eat AFB1-feedstuffs, they metabolise the toxin and excrete AFM1 in milk. To control AFM1 in foods it is necessary to reduce AFB1 contamination of feeds for dairy cattle by preventing fungal growth and AFB1 formation in agricultural commodities intended for animal use. Aflatoxin high concentration in milk and milk products cause widespread negative impact on public health. Therefore, it is necessary to establish strategies for reducing aflatoxin levels in animal feed and dairy products. In this paper, we review recent studies in aflatoxin M1 contamination in dairy products in Iran and various countries. Keywords: Aflatoxin M1, Dairy Products, Iran
Correspondence should be addressed to Reza Kazemi Darsanaki, Young Researchers Club, Lahijan Branch, Islamic Azad University, Lahijan, Iran; Email:
[email protected] . Tel: +989366201665.
500 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
1. Introduction Mycotoxins are large group of compounds, secondary metabolites of fungi, which can contaminate broad number of feed and food. Organization legislation regarding of permitting limit of mycotoxins in feed and food for animal and people in different countries depends of many factors, but it is directly associated with degree of developments and regulatory systems. from 200 compounds which are secondary metabolites of fungi, only a dozen have current importance from economic and public health point of view. Aflatoxins, as ones of the most investigate and most importance mycotoxins, occupy an important place [1, 2, 3]. Aflatoxins are a group of closely related hepatocarcenogenic bisdihydrofurano metabolites produced by certain species of Aspergillus especially by certain strains of Aspergillus flavus and Aspergillus parasiticus [4, 5]. Aspergillus species are capable of growing on a variety of substrates and under a variety of environmental conditions. Therefore, most foods are susceptible to aflatoxigenic fungi at some stage of production, processing, transportation and storage. The outbreak of aflatoxicosis in England in 1960 caused the death of a large population of livestock and led to the discovery of aflatoxin in groundnut meal contaminated by A. flavus. Subsequently, aflatoxins were found in other feeds, especially maize and cottonseed meal. Aflatoxin M1 (AFM1) in milk and milk products is considered to pose certain hygienic risks for human health [6, 7]. The common aflatoxins are B1, B2, G1, G2 and M1. Aflatoxins have sub-acute and chronic effects such as liver cancer, chronic hepatitis, jaundice, hepatomegaly and cirrhosis in humans, AFM1 is classified in Group 2 as a probable human carcinogen. Aflatoxin B1 (AFB1) is the most commonly occurring and the strongest carcinogenic amongst the aflatoxins [8, 9]. AFM1 is a major metabolite of AFB1, which is formed when animals ingest feed contaminated with AFB1. These metabolites are not destroyed during the pasteurization and heating process. The amount of AFM1 which is found in milk depends on several factors, such as animal breed, lactation period, mammary infections etc. AFM1 could be detected in milk 12-24 h after the AFB1 ingestion, reaching a high level after a few days. When AFB1 intake is stopped, the AFM1 concentration in milk decreases to an undetectable level after 72 h [4, 9, 11, 12]. The pollution level of AFM1 is differentiated further by hot and cold seasons, due to the fact that grass, pasture, weed and rough feeds are found more commonly in spring and summer than in winter. At the end of summer, greens are consumed more than concentrated feed, causing a decreased level of AFM1 in milk and milk products [4, 5, 13]. Many countries have established regulations to control the levels of AFB1in feeds and to have maximum permissible levels of AFM1 in milk to reduce this hazard. The European Community and Codex Alimentarius Commission prescribed that the maximum level of AFM1 in milk and milk products should not exceed 50 ng/L [14]. Maximum limits for AFM1 in milk and milk products in various countries shown in Table 1 [4].
501 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
Table 1. Maximum limits for aflatoxin M 1 in milk and milk products in various countries
Country
Maximum limit (μg/kg or μg/l)
France
0.05 Adult’s milk 0.03 Children’s milk 0.05 Milk and products 0.25 Cheese 0.1 Children’s milk 0.5 Adult’s milk 0.050 Milk 0.50 Milk 0.050 Milk and milk products 0.250 Cheese 0.020 Butter 0.200 Cheese 0.050 Milk 0.050 Milk
Turkey Czech Republic Belgium USA Switzerland Netherlands Germany Australia
The presence of mycotoxins in dairy products may be the result of: Direct contamination Direct contamination of dairy products with mycotoxins may be the result of fungal growth used for fermentation or unintentional fungal growth. Indirect contamination Since the observation that dairy animals consuming feeds contaminated with AFB1 excrete AFM1 in their milk, various studies have been undertaken; they established that the variations in the carry-over rates are significant at both high and low levels of feed contamination with AFB1 [15]. In this paper, we review recent studies in AFM1 contamination in dairy products in Iran and various countries.
2. Methods of Analysis of AFM1 in Dairy Products Analysis for mycotoxins is essential to minimize the consumption of contaminated food and feed. Thin layer chromatography (TLC), gas chromatography (GC), high performance liquid chromatography (HPLC), liquid chromatography with mass spectrometry (LC-MS) and enzyme linked immunosorbent assay (ELISA) are the most common techniques for detecting AFM1 in milk and dairy products [16]. Sensitive microtiter plate immunoassays (ELISA format) are commercially available for a variety of mycotoxins including aflatoxins BG, aflatoxin M1, ochratoxin A, the fumonisins, zearalenone, deoxynivalenol, citrinin, and T-2 toxin. Most of these 502 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
kits rely on a competitive, heterogeneous ELISA format in which the toxin from the sample competes with a labelled toxin (such as toxin-enzyme conjugate) for a limited number of antibody-binding sites [17]. New screening techniques will be developed. Biosensors based on the use of monoclonal or polyclonal antibodies have seen a great development in the field of small molecules analytical determination and specifically in the mycotoxins analyses. Main advantages of biosensors technology in comparison with traditional analytical methods are fast detection, low cost assay, high sensitivity, their high selectivity, easy preparation and operation assay method [18, 19].
3. Biological Control of Aflatoxins Several approaches have been developed for decontamination of mycotoxins in foods. Though many approaches are available for mycotoxin decontamination, most of them are not widely available due to high cost or practical difficulties involved in detoxification process. Several strategies, including chemical, physical and biological control methods have been investigated to manage aflatoxins in foods. Biological detoxification of mycotoxins works mainly via two major processes, sorption and enzymatic degradation, both of which can be achieved by biological systems. Live microorganisms can absorb either by attaching the mycotoxin to their cell wall components or by active internalization and accumulation. Dead microorganisms too can absorb mycotoxins and this phenomenon can be exploited in the creation of biofilters for fluid decontamination or probiotics to bind and remove the mycotoxin from the intestine. Enzymatic degradation can be performed by either extra or intracellular enzymes. The degradation can be complete, the final product being CO2 and water. Alternatively, enzymatic modification can alter, reduce or completely eradicate toxicity. Several bacterial species, such as Bacillus, Lactobacilli, Pseudomonas, Ralstonia and Burkholderia spp., have shown the ability to inhibit fungal growth and production of aflatoxins by Aspergillus spp. under laboratory conditions [16].
4. AFM1 in Milk Milk, as a liquid, is a highly variable product that rapidly loses its quality and spoils if not to be treated. Since milk may be processed in numerous ways, the effects of storage and processing on stability and distribution of AFM1 are of great concern. Many researchers from different countries have carried out studies about the incidence of AFM1 in milk. Data from the studies on the occurrence of AFM1 in milk are reported in Table 2. The European Commission (EC) has approved a maximum admissible level of 50ng/l for AFM1 in Milk.
503 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
Table 2. Occurrence and content of AFM1 in milk samples
Year
Region
Technique
Sample No.
1999
Argentine
ELISA
1999-2000 2001-2002
Iran Japan
ELISA HPLC
77 Farm, Powdered and Pasteurized milk 186 Raw milk 208 Pasteurized milk
2002 2002-2003
Taiwan Brazil
HPLC HPLC
2003 2003 2004
North African Iran Iran
2004
Positive samples (%) 23% 63.97% 99.5%
Reference Lopez et al. [20] Ghiasian et al. [21] Nakajima et al. [22] Lan et al. [23] Shundo and Sabino [24] Elgerbi et al. [25]
90.9% 73.8%
HPLC
44 Fresh milk 107 Pasteurized, UHT and Raw milk 49 Raw milk
ELISA HPLC
624 Pasteurized milk 319 Raw milk
100% 54%
Turkey
ELISA
50 UHT milk
100%
2005 2005
Turkey Iran
ELISA ELISA
88.23% 100%
2005 2006 2006 2006 2007
Iran Turkey Iran Morocco Iran
ELISA ELISA ELISA HPLC ELISA
100% 84.54% 100% 88.8% 96.3%
Kamkar [30] Özdemir [31] Sefidgar et al. [32] Zinedine et al. [33] Oveisi et al. [34]
2007 2006-2007
Iran Iran
ELISA ELISA
100% 94.48%
2008
Iran
ELISA
85 Pasteurised milk 111 Pasteurised and UHT milk 52 UHT milk 110 Goat milk 72 Pasteurized Milk 54 Pasteurized milk 328 Pasteurized and Infant milk 42 Powdered milk 257 Raw and Pasteurized milk 100 UHT milk
Alborzi et al. [26] Tajkarimi et al. [27] Gundinc and Filazi [28] Celik et al. [5] Hashemi et al. [29]
2008
Iran
ELISA
196 milk
100%
2008 2008-2009
Iran Egypt
ELISA ELISA
49 UHT milk 50 Raw milk
100% 38%
2008-2009
Iran
ELISA
50 Pasteurized milk
84%
Kamkar [35] Mohammadian et al. [36] Tekinşen and Eken [37] Mohamadi Sani et al. [38] Movassagh [39] Amer and Ibrahim [40] Riazipour et al.
504 | P a g e
71.4%
67%
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
2009
Iran
ELISA
75 Pasteurized Milk
100%
2009 2009 2009 2009
Iran Iran Iran Iran
ELISA TLC HPLC HPLC
110 Pasteurized Milk 91 Pasteurized Milk 100 Pasteurized Milk 74 Raw and Pasteurized milk
100% 72.5% 100% 85.14%
2009
Sudan
HPLC
44 Cattle milk
95.45%
2010 2010-2011 2011
Iran Iran Iran
ELISA ELISA ELISA
122 Raw milk 60 Pasteurized milk 90 Raw milk
100% 40% 65.55%
2011 2011
Iran Iran
ELISA ELISA
100% 95.3%
2011
Palestine
ELISA
100 Raw milk 149 Pasteurized and UHT milk 40 Raw milk
2011
Iran
ELISA
42 Pasteurized milk
97.6%
2011-2012
Egypt
ELISA
96 UHT milk
82.30%
85%
[41] Behnamipour et al. [42] Karimi et al. [43] Fallah [44] Behfar et al. [45] Daraei Garmakhany et al. [46] Elzupir and Elhussein [47] Kamkar et al. [48] Rahimi et al. [49] Azizollahi ali abadi et al [16]. Panahi et al. [50] Rahimi et al. [51] Al zuheir and Abo omar [52] Mohamadi Sani et al. [53] Abdallah et al. [54]
Many authors showed that seasonal effect influences concentration of aflatoxin M1. They reported higher concentration of AFM1 in cold seasons as compared to hot seasons, the reason being in winters mostly milking animals are fed with compound feeds and thus concentration of AFB1increases which in turn enhances AFM1 concentration in milk [4, 27, 55, 56].
5. AFM1 in Yogurt The European Commission (EC) has approved a maximum admissible level of 50ng/l for AFM1 in yogurt. Many researchers from different countries have carried out studies about the incidence of AFM1 in yogurt. Data from the studies on the occurrence of AFM1 in milk are reported in Table 3.
505 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
Table 3. Occurrence and content of AFM1 in yogurt samples
Year
Region
Technique
Sample No.
2002 2005 2007-2008 2009 2009
Taiwan Turkey Turkey Iran Iran
HPLC ELISA ELISA ELISA ELISA
24 177 80 50 28
Positive samples (%) 12.5% 65.38% 87.5% 100% 100%
2009 2011
Iran Iran
TLC ELISA
68 60
66.1% 98.33%
2011-2012 2012
Iran Iran
ELISA ELISA
60 40
80% 35%
2012
Iran
HPLC
120
100%
Reference Lan et al. [23] Akkaya et al. [57] Atasever et al. [58] Barjesteh et al. [59] Behnamipour et al. [42] Fallah [44] Issazadeh et al. [1] Rahimi [60] Nilchian and Rahimi [61] Tabari et al. [62]
6. AFM1 in Cheese Dairy products play a significant role in human diet since they are rich sources of bioavailable calcium and proteins. However, many of the previous studies has indicated the presence of AFM1 at high concentrations in dairy products [63]. Occurrence of AFM1 in cheese can be due to three possible causes: (1) AFM1 present in raw milk because of carryovers of AFB1 from contaminated cow feed to milk, (2) Synthesis of AF (B1, B2, G1 and G2) by A. flavus and A. parasiticus growing on cheese and (3) Occurrence of these toxins in dried milk used to enrich the milk which is being used in the production of cheese. Many researchers from different countries have carried out studies about the incidence of AFM1 in cheese [4]. Data from the studies on the occurrence of AFM1 in milk are reported in Table 3. The European Commission (EC) has approved a maximum admissible level of 250 ng/l for AFM1 in cheese. Table 4. Occurrence and content of AFM1 in cheese samples
Year
Region
Technique
Sample No.
1999 2002 2002
Spain Turkey Turkey
HPLC ELISA ELISA
35 63 400
506 | P a g e
Positive samples (%) 45.71% 44.44% 81.75%
Reference Jose Barrios et al. [64] Gurses et al. [65] Sarimehmetoglu et al. [11]
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
2003 2005 2005-2007 2007 2007 2007 2008 2009 2009 2009 2009 2009 2010 2011
North African Turkey Kuwait Portugal Turkey Turkey Turkey Iran Iran Iran Turkey Iran Turkey Iran
HPLC TLC ELISA HPLC HPLC ELISA ELISA ELISA ELISA ELISA ELISA TLC ELISA ELISA
20 50 40 128 46 304 132 210 88 70 80 72 127 90
75% 28% 80% 6.25% 69.6% 71.1% 82.6% 76.6% 53.4% 64.3% 48.7% 81.9% 28.3% 86.66%
2010-2011 2011-2012 2012
Iran Iran Iran
ELISA ELISA ELISA
61 80 40
55.73% 86.3% 40%
Elgerbi et al. [25] Filazi et al. [66] Dashti et al. [67] Martins et al. [68] Turgay et al. [69] Atasever et al. [70] Tekinşen and Eken [37] Fallah et al. [71] Rahimi et al. [72] Rahimi et al. [73] Hampikyan et al. [8] Fallah [44] Kursat et al. [74] Kazemi Darsanaki et al. [4] Rahimi et al. [51] Rahimi [60] Nilchian and Rahimi [61]
7. AFM1 in other products Many other milk products such as cream, butter, ice cream may contain AFM1. Some surveys conducted on the occurrence of AFM1 in milk products are reported in Table 5. Table 5. Occurrence and content of AFM1 in other products
Year
Region
Technique
Sample No.
2009 2009 2009 2009 2011-2012
Iran Iran Turkey Iran Iran
HPLC TLC ELISA TLC ELISA
225 Doogh 31 Butter 80 Butter 36 Ice cream 60 Ice cream
507 | P a g e
Positive samples (%) 100% 25.8% 82.5% 69.4% 56.7%
Reference Tabari et al. [75] Fallah [44] Atasever et al. [76] Fallah [44] Rahimi [60]
Journal of Science and today's world
2012
Iran
ELISA
2013, volume 2, issue 5, pages: 500-514
40 Ice cream
29%
Nilchian and Rahimi [61]
8. Conclusion Dairy products play a significant role in human diet since they are rich sources of bioavailable calcium and proteins. However, many of the previous studies has indicated the presence of AFM1 at high concentrations in dairy products. Aflatoxins are highly toxic, immunosuppressive, mutagenic, teratogenic and carcinogenic compounds. The main target organ for their toxicity and carcinogenicity is the liver, Milk and milk products, are a major nutrient for humans, especially children. According to results obtained, incidence and contamination levels of AFM1, seem to be a serious problem for public health. For this reason, milk and dairy products have to be inspected and controlled continuously for AFM1 contamination and animal feeds should be checked regularly for AFB1 and storage conditions of feeds must be taken under strict control.
References [1] Issazadeh, K., R. kazemi Darsanaki, M. R. Majid Khoshkholgh Pahlaviani, 2012. Occurrence of aflatoxin M1 levels in local yogurt samples in Gilan Province, Iran. Annals of Biological Research., 3 (8):3853-3855. [2] Hussein, H.S., J.M. Brasel, 2001. Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology., 167: 101–134. [3] Polovinski-Horvatović, M., V. Jurić, D. Glamočić, 2009. Two year study of incidence of aflatoxin M1 in milk the region of Serbia. Biotechnology in Animal Husbandry., 25: 713-718. [4] Azizollahi Aliabadi, M., K. Issazadeh, R. Kazemi Darsanaki, M. Laleh Rokhi, A. Amini, 2012. Determination of Aflatoxin M 1Levels in White Cheese Samples by ELISA in Gilan Province, Iran. Global Veterinaria., 8 (7): 707-710. [5] Celik, T.H., B. Sarimehmetoglu, O. Kuplulu, 2005. Aflatoxin M1 contamination in pasteurised milk. Veterinarski Arhiv., 75: 57-65. [6] Chakrabarty, A. B., 1981. Detoxification of aflatoxin in Corn. Journal of Food Protection., 44: 173-176. [7] Kocabas, C. N., B. E. Sekerel, 2003. Does systemic exposure to aflatoxin B1 cause allergic sensitization? Allergy., 58: 363.
508 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
[8] Hampikyan, H., E. Baris Bingol, O. Cetin, H. Colak, 2010. Determination of aflatoxin M1 levels in Turkish white, kashar and tulum cheeses, Journal of Food Agriculture and Environment., 8: 13-15. [9] Laleh rokhi, M., R. Kazemi Darsanaki, M. Mohammadi, M. Hassani Kolavani, K. Issazadeh, M. Azizollahi Aliabadi, 2013. Determination of Aflatoxin M1 Levels in Raw Milk Samples in Gilan, Iran. Advanced Studies in Biology., 5: 151-156. [10] Gunsen, U., I. Buyukyoruk, 2002. Aflatoxins in retail food products in Bursa, Turkey.Vet. Human Toxicol., 44: 289–290. [11] Sarimehmetoglu, B., O. Kuplulu, T.H. Celik, 2004. Detection of aflatoxin M1 in cheese samples by ELISA. Food Control., 15: 45-49. [12] Sibanda, L., S. De Saeger, C. Van Peteghem, 1999. Development of a portable field immunoassay for the detection of aflatoxin M1 in milk. Int. J. Food Microbiol., 48: 203-209. [13] Galvano, F., V. Galofaro, G. Galvano, 1996. Occurrence and stability of aflatoxin M1 in milk and milk products: A worldwide review. J Food Protect., 59: 1079-1090. [14] European Commission (EC), 2006. Setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Union., 364: 5-24. [15] Van Egmond, H.P., 1989. Aflatoxin M1: occurrence, toxicity, regulation. In: Van Egmond, H.P. (Ed.), Mycotoxins in dairy products. Elsevier Applied Science, London and New York., 11– 55. [16] Azizollahi Aliabadi M., F. Alikhani, M. Mohammadi, R. Kazemi Darsanaki, 2013. Biological Control of Aflatoxins. European Journal of Experimental Biology., 3(2):162-166. [17] Pittet, A., 2005. Modern methods and trends in mycotoxin analysis. 117th annual conference of the society of Food and Environmental Chemistry. 424–444. [18] Pacheco, I.T., 2011. Aflatoxins, Detection, Measurement and Control. Published by InTech, Croatia., 93-160. [19] Paddle, B., 1996. Biosensors for chemical and biological agents of defence interest. Biosensors and Bioelectronics.,11:1079-1113. [20] Lopez, C.E., L.L. Ramos, S.S. Ramadan, L.C. Bulacio, 2003. Presence of aflatoxin M1 in milk for human consumption in Argentina. Food Control., 14: 31–34. [21] Ghiasian, S.A., A.H. Maghsood, T.R. Neyestani, S.H. Mirhendi, 2007. Occurrence of aflatoxin M1 in raw milk during the summer and winter seasons in Hamedan, Iran. Journal of Food Safety., 27: 188–198. 509 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
[22] Nakajima, M., S. Tabata, H. Akiyama, Y. Itoh, T. Tanaka. H. Sunagawa, T. Tyonan, T. Yoshizawa, S. Kumagai, 2004. Occurrence of aflatoxin M1 in domestic milk in Japan during the winter season. Food Addit Contam., 21(5): 472-478. [23] Lan, C.L., M.L. Fang, M.F. You, C.S. Daniel Yang, 2004. Survey of Aflatoxin M1 Contamination of Dairy Products in Taiwan. Journal of Food and Drug Analysis., 12(2): 154160. [24] Shundo, L., M. Sabino, 2006. Aflatoxin M1 in milk by immunoaffinty column cleanup with TLC/HPLC determination. Brazilian Journal of Microbiology., 37:164-167. [25] Elgerbi, A.M., K.E. Aidooa, A.A.G. Candlisha, R.F. Testera, 2004. Occurrence of aflatoxin M1 in randomly selected North African milk and cheese samples. Food Additives and Contaminants., 21(6): 592-597. [26] Alborzi, S., B. Pourabbas, M. Rashidi, B. Astaneh, 2006. Aflatoxin M1 contamination in pasteurized milk in Shiraz (south of Iran). Food Control., 17(7): 582-584. [27] Tajkarimi, M., F. Aliabadi-Sh, A. Salah Nejad, H. Poursoltani, A.A. Motallebi, H. Mahdavi, 2008. Aflatoxin M1 contamination in winter and summer milk in 14 states in Iran. Food Control., 19: 1033-1036. [28] Gundinc, U., A. Filazi, 2009. Detection of Aflatoxin M1 Concentrations in UHT Milk Consumed in Turkey Markets by ELISA. Pakistan Journal of Biological Sciences., 12: 653-656. [29] Gholampour Azizi, I., S.H. Khoushnevis, S.J. Hashemi, 2007. Aflatoxin M1 level in pasteurized and sterilized milk of Babol city. Tehran University Medical Journal., 65: 20-24. [30] Kamkar, A., 2008. The study of aflatoxin M1 in UHT milk samples by ELISA. J.Vet.Res., 63(2): 7-12. [31] Özdemir, M., 2007. Determination of aflatoxin M1 levels in goat milk consumed in Kilis province. Ankara Üniv Vet Fak Derg., 54: 99-103. [32] Sefidgar, S.A.A., M. Mirzae, M. Assmar, S.R. Naddaf, 2011. Aflatoxin M1 in Pasteurized Milk in Babol city, Mazandaran Province, Iran. Iranian J Publ Health., 40:115-118. [33] Zinedine, A., L. González-Osnaya, J.M. Soriano, J.C. Moltó, L. Idrissi, J. Mañes, 2007. Presence of aflatoxin M1 in pasteurized milk from Morocco. International Journal of Food Microbiology., 114: 25-29. [34] Oveisi, M.R., B. Jannat, N. Sadeghi, M. Hajimahmoodi, A. Nikzad, 2007. Presence of aflatoxin M1 in milk and infant milk products in Tehran, Iran. Food Control., 18: 1216–1218.
510 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
[35] Kamkar, A., 2007. Detection of aflatoxin M1 in powdered milk samples by ELISA. Pajouhesh & Sazandegi., 79: 174-180. [36] Mohammadian, B., M. Khezri, N. Ghasemipour, Sh. Mafakheri, P. Poorghafour Langroudi, 2010. Aflatoxin M1 contamination of raw and pasteurized milk produced in Sanandaj, Iran. Archives of Razi Institute., 65(2): 99-104. [37] Tekinşen, K.K., H.S. Eken, 2008. Aflatoxin M1 levels in UHT milk and kashar cheese consumed in Turkey. Food and chemical toxicology., 46: 3287-3289. [38] Mohamadi Sani, A., H. Nikpooyan, R. Moshiri, 2010. Aflatoxin M 1 contamination and antibiotic residue in milk in Khorasan province, Iran. Food and Chemical Toxicology., 48(8): 2130-2132. [39] Movassagh, M.H., 2011. Presence of aflatoxin in UHT milk in Tabriz (Northwest of Iran). Journal of Food Safety., 31(2): 238–241. [40] Amr Amer, A., M.A. Ekbal Ibrahim, 2010. Determination of aflatoxin M1 in raw milk and traditional cheeses retailed in Egyptian markets. Journal of Toxicology and Environmental Health Sciences., 2(4): 50-53. [41] Riazipour, M., H.R. Tavakkoli, M. Razzaghi Abyane, H. Rafati, S.M. Sadr Momtaz, 2010. Measuring the amount of M1 Aflatoxin in pasteurized milks. Kowsar Medical Journal., 15(2): 89-93. [42] Behnamipour, S., Y. Arast, M. Mohammadian, 2012. Occurence of aflatoxin M1 in two dairy products by ELISA in central part of Iran. Life Science Journal., 9(3): 1831-1833. [43] Karimi, G., M. Hassanzadeh, M. Teimuri, F. Nazari, A. Nili, 2007. Aflatoxin M1 Contamination in Pasteurized Milk in Mashhad, Iran. Iranian Journal of Pharmaceutical Sciences., 3(3): 153-156. [44] Fallah, A.A., 2010. Aflatoxin M1 contamination in dairy products marketed in Iran during winter and summer. Food Control., 21: 1478-1481. [45] Behfar, A., Z. Nazari Khorasgani, Z. Alemzadeh, M. Gudarzi, R. Ebrahimi, N. Tarhani, 2012. Determination of Aflatoxin M1 Levels in Produced Pasteurized Milk in Ahvaz City by Using HPLC. Jundishapur J Nat Pharm Prod., 7(2):80-84. [46] Daraei Garmakhany, A., H. Zighamian, R. Sarhangpour, M. Rasti, N. Aghajani, 2011. Occurrence of Aflatoxin M1 in Raw and pasteurized milk in Esfahan province of Iran. Minerva Biotecnologica., 23: 53-7. [47] Elzupir, A. O., A. M. Elhussein, 2010. Determination of aflatoxin M1 in dairy cattle milk in Khartoum State, Sudan. Food Control., 21 (6): 945-946. 511 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
[48] Kamkar, A., G.R. Jahed Khaniki, S.A. Alavi, 2011. Occurrence of aflatoxin M1 in raw milk produced in Ardebil of Iran. Iran. J. Environ. Health. Sci. Eng., 8(2): 123-128. [49] Rahimi, E., Z. Nilchian, A. Behzadnia, 2011. Presence of Aflatoxin M1 in Pasteurized and UHT Milk Commercialized in Shiraz, Khuzestan and Yazd, Iran. Journal of Chemical Health Risks., 1(1): 7-10. [50] Panahi, P., S. Kasaee, A. Mokhtari, A. Sharifi, A. Jangjou, 2011. Assessment of Aflatoxin M1Contamination in Raw Milk by ELISA in Urmia, Iran. American-Eurasian Journal of Toxicological Sciences., 3(4): 231-233. [51] Rahimi, E., M. Mohammadhosseini, M. Alimoradi, P. Rezaei, M. Arab, M.A. Goudarzi, M. Tarkesh Esfahani, Z. Torki, 2012. Aflatoxin M1 in Pasteurized Milk and White Cheese in Ahvaz, Iran. Global Veterinaria., 9(4): 384-387. [52] Al Zuheir, I.M., J. Abo Omar, 2012. Presence of Aflatoxin M1 in Raw Milk for Human Consumption in Palestine. Walailak J Sci & Tech., 9(3): 201‐205. [53] Mohamadi Sani, A., M. Khezri, H. Moradnia, 2012. Determination of AflatoxinM1 in Milk by ELISA Technique in Mashad (Northeast of Iran). ISRN Toxicology., 1-4. [54]. Abdallah M.I.M., M.S. Bazalou, M.Z. Al-Julaifi, 2012. Determination of aflatoxin M1 in concentrationals in full-fat cows UHT milk sold for consumption in najran-saudi regarding its public health significance. Egypt . J. of Appl. Sci., 27 (3): 40-54. [55] Hussain, I., J. Anwar, 2008. A study on contamination of aflatoxin M1 in raw milk in the Punjab province of Pakistan. Food Control., 19: 293-295. [56] Bilandzic, N., I. Varenina, B. Solomun, 2010. Aflatoxin M1 in raw milk in Croatia. Food Control., 21:1279–1281. [57] Akkaya, L., Y.O. Birdane, H. Oguz, M. Cemek, 2006. Occurrence of aflatoxin M1 in yogurt samples from afyonkarahisar, Turkey. Bull Vet Inst Pulawy., 50: 517-519. [58] Atasever, M.A., M. Atasever, K. Ozturan, 2011. Aflatoxin M1 levels in retail yoghurt and ayran in Erzurum in Turkey. Turk. J. Vet. Anim. Sci., 35(1): 59-62. [59] Barjesteh, M.H., I. Gholampour, E. Noshfar, 2010. Occurrence of aflatoxin M1 in pasteurized and local yogurt in mazandaran province (Northern of Iran) using ELISA. Global Veterinaria., 4 (5): 459-462. [60] Rahimi, E., 2012. Survey of the occurrence of aflatoxin M1 in dairy products marketed in Iran. Toxicol Ind Health., doi: 10.1177/0748233712462476.
512 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
[61] Nilchian, Z., E. Rahimi, 2012. Aflatoxin M1 in Yoghurts, Cheese and Ice-Cream in Shahrekord-Iran. World Applied Sciences Journal., 19 (5): 621-624. [62] Tabari, M., K. Tabari, O. Tabari, 2013. Aflatoxin M1 determination in yoghurt produced in Guilan province of Iran using immunoaffinity column and high-performance liquid chromatography. Toxicol Ind Health., 29(1):72-76. [63] Tekinsen, K.K., O.C. Tekinsen, 2005. Aflatoxin M1 in white pickle and Van otlu (herb) cheeses consumed in southeastern Turkey. Food Control., 16: 565-568. [64] Jose Barrios, M. M. Jesus Gualda, J.M. Cabanas, L.M. Medina, R. Jordano, 1996. Occurrence of Aflatoxin M1 in Cheeses from the South of Spain. Journal of Food Protection., 59(8): 898-900. [65] Gurses, M., A. Eerdogan. B. Cetin, 2004. Occurrence of Aflatoxin M1 in Some Cheese Types Sold in Erzurum, Turkey. Turk J Vet Anim Sci., 28: 527-530. [66] Filazi, A., S. Ince, F. Temamogullari, 2010. Survey of the occurrence of aflatoxin M1 in cheeses produced by dairy ewe’s milk in Urfa city, Turkey. Ankara Üniv Vet Fak Derg., 57: 197199. [67] Dashti, B., S. Al-Hamli, H. Alomirah, S. Al-Zenki, A. Bu Abbas, W. Sawaya, 2009. Levels of aflatoxin M1 in milk, cheese consumed in Kuwait and occurrence of total aflatoxin in local and imported animal feed. Food Control., 20: 686-690. [68] Martins, H.M., S.A. Magalhães, I. Almeida, M. Marques, M. M. Guerra, F. Bernardo, 2007. Aflatoxin M1 determination in cheese by immunoaffinity column clean-up coupled to highperformance liquid chromatography. RPCV., 102: 321-325. [69] Turgay, O., D.H. Aksakal, S. Sunnetci, A.B. Celik, 2010. A survey of afatoxin M1 levels in Kahramanmaraş cheese. Turk. J. Vet. Anim. Sci., 34(6): 497-500. [70] Atasever M.Y., G. Adiguzel, M. Atasever, K. Ozturan, 2010. Determination of Aflatoxin M1 Levels in Some Cheese Types Consumed in Erzurum – Turkey. Kafkas Univ Vet Fak Derg., 16 (Suppl-A): 87-91. [71] Fallah, A.A., T. jafari, A. Fallah, M. Rahnama, 2009. Determination of aflatoxin Ml levels in Iranian white and cream cheese. Food and Chemical Toxicology., 47: 1872-1875. [72] Rahimi, E., G. Karim, A. Shakerian, 2009. Occurrence of aflatoxin M1 in traditional cheese consumed in Esfahan, Iran. World Mycotoxin Journal., 2: 91-94. [73] Rahimi, E., M. Jafarian Dehkordi, A. Iranpoor, 2011. A Survey of Aflatoxin M1 Contamination in Iranian White Cheese. Food Technology & Nutrition., 8(4): 51-56.
513 | P a g e
Journal of Science and today's world
2013, volume 2, issue 5, pages: 500-514
[74] Kursat, K., C. Ramazan, K. Kaan Tekinsen, 2011. Detection of aflatoxin M1 levels by ELISA in white-brined Urfa cheese consumed in Turkey. Food Control., 22(12): 1883–1886. [75] Tabari, M., K. Tabari, O. Tabari, 2011. Occurrence of Aflatoxin M1 in Pasteurized Doogh Commercialized in Tehran, Iran. Australian Journal of Basic and Applied Sciences., 5(12): 17341737. [76] Atasever M.Y., M. Atasever, K. Ozturan, S. Urcar, 2010. Determination of Aflatoxin M1 Level in Butter Samples Consumed in Erzurum, Turkey. Kafkas Univ Vet Fak Derg., 16 (SupplA): 159-162.
514 | P a g e