Aflatoxin M1 Contamination in Dairy Products - Journal of Science and ...

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

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Correspondence should be addressed to Reza Kazemi Darsanaki, Young Researchers Club, Lahijan Branch, Islamic Azad University, Lahijan, Iran; Email: [email protected] . Tel: +989366201665.

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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].

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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



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.

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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.

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71.4%

67%



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.

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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

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Positive samples (%) 45.71% 44.44% 81.75%

Reference Jose Barrios et al. [64] Gurses et al. [65] Sarimehmetoglu et al. [11]



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

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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]


2012

Iran

ELISA


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.

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