The occurrence of aflatoxin M1 in industrial and traditional fermented milk: A systematic review study

Published: June 6, 2023

By: Camilla de Souza 1, Amin Mousavi Khaneghah 2, Carlos Augusto Fernandes Oliveira 3 / 1 Department of Veterinary Medicine, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil; 2 Department of Food Science, School of Food Engineering, State University of Campinas, Campinas, SP, Brazil; 3 Department of Food Engineering, School of Animal Science and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil.

Summary

Aflatoxin M₁ (AFM₁) is a toxic secreted into the milk of animals fed with diets contaminated by aflatoxin B₁, which can cause some adverse health effects in humans. The occurrence of AFM₁ in dairy products varies based on several factors, including the fermentation process. In this article, the published citations from January 2000 to October 2020 regarding the AFM₁ occurrence in industrial and traditional fermented milk were systemically reviewed. According to the findings, a reducing trend in the AFM₁ contamination of fermented milk was observed over the years, mainly in traditional products. Despite this trend, further control measures besides the preventative approaches are needed to deal with the high levels of AFM₁ in fermented milk.

Keywords: AFM₁ ; yogurt; fermented milk; occurrence; contamination; food safety; traditional dairy products

Introduction

Aflatoxins are toxic, secondary metabolites synthesized by some fungi species in the genus Aspergillus, mainly those belonging to the species A. flavus, A. nomius, and A. parasiticus (Ismaiel et al., 2020). Aflatoxins are considered the most important mycotoxins, given their carcinogenic and hepatotoxic effects on animals and humans (Bhat et al., 2010). Among several types of aflatoxins, the most frequent ones found as natural contaminants of foodstuffs are aflatoxins B₁ (AFB₁), B₂ (AFB₂), G₁ (AFG₁), and G₂ (AFG₂) (Nejad et al., 2019). While AFB₁possesses the highest toxicity, this toxin is also classified as a Group 1 carcinogen by the International Agency for Research on Cancer (2002). In addition, AFM₁ and AFM₂ are produced by hepatic biotransformation of AFB₁and AFB₂, respectively, and maybe shed through the urine and milk of animals (Campagnollo et al., 2016; Imamura et al., 2015).

Milk and milk products have high nutritional and biological value, contributing to a balanced diet for human beings. Among dairy products, fermented milk is important, as it is consumed by a wide range of people, from infants to elders (Barukcic et al., 2018). Some fermented milk has, in their composition, probiotics that lead to improved digestibility, besides some other health-promoting factors, such as bioactive peptides and bacteriocins (Black, 2011). As AFM₁is highly stable through pasteurization, ultra-high temperature processing, and other processing methods used in dairy production, the toxin may be found not only in processed milk but also in dairy products (Jalili and Scotter, 2015). Yogurt and other fermented milk products are typically manufactured by fermentation of lactic acid in milk, both traditional and industrialized products with different levels of AFM₁, given the range of pH values and fermentation conditions (Govaris et al., 2002). However, studies related to AFM₁contents in these fermented products are scarce and controversial (Campagnollo et al., 2016; Mahmood Fashandi et al., 2018; Mousavi Khaneghah et al., 2017). Figure 1 presents an overview processing steps of fermented milk and some relevant points regarding the AFM₁contamination of these products.

When fermented milk is produced using milk contaminated with AFM₁, the mycotoxins are not eliminated at once, as they are resistant to most processing steps (Behfar et al., 2012). Therefore, to safeguard human health, maximum limits of AFM₁residues recommended in most countries range from 0 to 1.0 μg/L of milk (Iqbal et al., 2015). In the European Union (EU), the tolerable limit for AFM₁in milk is no more than 0.05 μg/L (European Commission, 2006), while in the United States and Brazil, a maximum level of 0.5 μg/L is accepted (Agência Nacional de vigilância sanitária, 2011; Food and Drug Administration, 2000).

Besides yogurts, other fermented products are also susceptible to AFM₁contamination, including traditional ones, such as Lala, kefir, and Doogh. Lala is traditional African fermented milk produced by natural fermentation or mesophilic cultures (Kuboka et al., 2019). Kefir is a dairy product rich in vitamins, essential amino acids, and minerals, made by fermenting the kefir grains (Gamba et al., 2016). Kefir is the most common probiotic product consumed in Europe and is associated with beneficial health effects related to homeostasis balance (Otles and Cagindi, 2003). Doogh is an Iranian fermented product made from yogurt added with potable water, sodium chloride, and probiotic cultures (Kiani et al., 2018). While several studies have been dedicated for evaluating the AFM₁levels in milk and other dairy products (Fallah, 2010; Kim et al., 2011; Rahmani et al., 2018), no systematical review was conducted to summarize the findings. Therefore, the current investigation was undertaken to systematically review the literature published in the last 20 years regarding the prevalence of AFM1 in industrial and traditional fermented milk globally.

Literature Search

A systematic literature search was conducted among some international databases such as PubMed, Science Direct, and Google Scholar (as gray literature) using the following key terms: “aflatoxins” OR “aflatoxin M₁ ” OR “mycotoxins” AND “Occurrence” OR “Contamination” OR “prevalence” OR “incidence” OR “fermented milk” OR “dairy products” OR “cultured dairy” OR “yogurt” OR “Kefir.” All relevant articles published from January 2000 to October 2020 that investigated the prevalence of AFM₁in fermented milk were retrieved and screened for eligibility. In addition, the reference lists of included articles were also manually searched to identify other suitable studies.

Figure 1. General processing flow chart of fermented milk and relevant steps regarding the aflatoxin M₁ (AFM₁) contamination during manufacture (in italic).

Figure 1. General processing flow chart of fermented milk and relevant steps regarding the aflatoxin M1 (AFM1) contamination during manufacture (in italic).

After excluding unsuitable articles due to irrelevant content, 150 full texts of potentially eligible articles were downloaded. Then, the downloaded citations were examined for inclusion and criteria of final eligibility. Inclusion criteria were: (1) availability of full-text article, (2) original cross-sectional research studies (not reviews), (3) reporting of AFM₁ prevalence among fermented, milk-based products, (4) indicating an accurate analytical method, and (5) published in the English in order to avoid any mistake during translation from other languages. The citations that did not meet these criteria were excluded. A total of 100 articles were excluded based on the abovementioned exclusion criteria according to PRISMA, as detailed in Figure 2. Finally, 50 articles that fulfilled the inclusion criteria were included in this review.

Figure 2. Flow chart describing the search and selection of articles evaluated in the study.

The Occurrence of Aflatoxin M₁ in Fermented Milk

Table 1 presents the worldwide prevalence of AFM₁ in yogurt and other fermented milk products during the last 20 years. Several studies reported a high prevalence of AFM₁ in yogurt and other traditional products in African countries. This is consistent with the high prevalence of AFB₁ reported in feedstuff used for dairy cows and AFM₁ in milk in the African continent (Muaz et al., 2021). In addition to the climatic conditions that favor fungal growth in several geographic areas in Africa, the lack of effective regulation of aflatoxins in the food chain and the low public awareness of this risk are among important factors that contribute to high prevalence of aflatoxins in African countries (Wild et al., 2015). In Egypt, 63% of the yogurt samples exceed the EU’s AFM₁ levels (Aiad and Aboelmakarem, 2013). The mean prevalence of AFM₁ in Egyptian yogurt samples was higher in the winter than in the summer. Coherently, higher AFM₁ levels in milk samples have also been reported in the winter season in different countries (Bilandzic et al., 2014; De Roma et al., 2017; Fallah, 2010; Ruangwises and Ruangwises, 2010). The reasons for such a higher prevalence of AFM₁ in milk and fermented products during the winter are not well established but may involve higher consumption of AFB₁ - contaminated feed by dairy cows during this period, as well as differences in the feed storage and diet composition, and rainfall effects (Fallah, 2010; Hajmohammadi et al., 2020). After incubation of Lactobacillus acidophilus and Bifidobacterium lactis into the fermented products, a decrease in mycotoxin prevalence was observed at the end of the storage period (Ibrahim et al., 2016). In this regard, the percentages of Egyptian Zabadi yogurt samples exceeding the European limits in 2016 and 2017 were 12.5 and 18.7, respectively. However, these prevalence data were lower in this product than in milk and cheese, mainly in the winter (Ismaiel et al., 2020). In Nigeria, 20 samples of yogurt were analyzed, and 10% were contaminated with AFM₁ (Anthony et al., 2016). In a study carried out in Nairobi, the capital of Kenya, AFM₁ was analyzed in samples of fermented milk and yogurt, and contamination was observed in levels above 0.05 μg/L (Langat et al., 2016). In Dagoretti and the Westland area belonging to Nairobi, 77 and 57% of Lala and yogurt, respectively, contained detectable levels of AFM₁ (Lindahl et al., 2018). In Nairobi, a study with pasteurized yogurt and Lala revealed that all samples had AFM₁ above the detection limit (5ng/kg). After undergoing an additional experimental fermentation, both products showed a significant reduction in AFM₁ prevalence (Kuboka et al., 2019). The prevalence of AFM₁ in yogurt and milk samples was evaluated in Burundi in the Republic of the Congo, and 29% of them showed levels much higher than the limits recommended by the EU (Udomkun et al., 2018).

Table 1. Occurrence of aflatoxin M₁ in yogurt and other fermented milks reported in the last 20 years.

The occurrence of aflatoxin M1 in industrial and traditional fermented milk: A systematic review study - Image 1

Click here to enlarge the image

Few studies considering the prevalence of AFM₁ in fermented milk produced in the Americas and European countries were conducted (Table 1). In Brazil, 95% of the samples of yogurt or dairy-based drinks from the Ribeirão Preto region were contaminated with AFM₁ (Iha et al., 2011). Interestingly, while the naturally contaminated yogurts from were incubated for 12 h, there was a reduction about 6% in the toxin levels (Iha et al., 2013). The fermentation process in yogurts contributes to reducing the concentration of AFM₁ due to factors such as low pH, production of organic acids, and the presence of bacteria that synthesize lactic acid and other byproducts of fermentation (Govaris et al., 2002).

As for the European countries, AFM₁ was detected in the Cataluña region of Spain among 2.8% of the samples analyzed, the only one region that showed contamination above that determined by the EU (Cano-Sancho et al., 2010). In another study, however, 33% of yogurt samples from the same Spanish region were contaminated with AFM₁, with none of them exceeding the European limits (Cano-Sancho et al., 2015). In samples of yogurt from Italian supermarkets analyzed in 1996, 61% showed levels of AFM1, but similar to Spain, none of them exceeded the limits determined by the EU (Galvano et al., 2001). In a study carried out in Portugal, 4.2% of the samples of plain yogurt and 33.3% of the samples of strawberry yogurt were contaminated with this toxin (Martins and Martins, 2004). In Serbia, the mean concentrations of AFM₁ in dairy products and fermented dairy drinks in 2015 were 0.018 and 0.019 µg/kg, respectively, with 5.86 and 2.64% of the samples exceeding the limits determined by the EU. It was also observed that the toxin levels were more significant in the winter and autumn in both products (Keskic et al., 2016).

The majority of data describing the prevalence of AFM₁ in fermented milk were provided by studies in Asian countries (Table 1). In Qatar, the incidence of AFM1 in yogurts was analyzed using an immunoenzymatic assay (ELISA); 76.1% of the samples were positive. However, none of them showed contamination levels above the EU maximum limits, posing no public health threats in this country (Hassan et al., 2018). AFM1 prevalence in yogurts produced with buffalo milk in different dairy factories in Southern China were evaluated, and none of the samples had levels greater than the limit of 500 ng/ kg determined in the country(Guo et al., 2019). Another study carried out with cow milk showed AFM1 levels inside the limit determined by this country and the EU (Zhou et al., 2019). In South Korea, 27.27% of the yogurt samples showed AFM₁, but none of them was above the limit determined by the Korean Ministry of Food and Drug Safety (0.5 μg/kg) (Kim-Soo et al., 2016). However, in a previous study, 83% of yogurt samples were contaminated by this toxin (Kim et al., 2000).

In the Mazandaran province of Iran, 100% of the pasteurized yogurt and local yogurt samples were contaminated with AFM₁ (Barjesteh et al., 2010). However, in another study in Iran, 20.6% of yogurt samples were contaminated with levels above the limits determined by the local regulations (0.05 µg/L) and were greater in the winter than the summer (Fallah, 2010). Moreover, samples of traditional and industrial yogurt and Doogh were evaluated, and the AFM₁ incidences in both these industrial products were greater in the autumn and winter than in traditional ones. As for Doogh samples, the contamination levels were low, and no significant seasonal effect was observed (Fallah et al., 2011). Seasonal factors may influence the presence of the toxin in these products, as some studies observed higher levels of contamination in milk samples in the autumn and winter compared with summer and spring (Kamkar, 2005). These variations may be related to the procedures during processing, degree of milk contamination, type of yogurt, fermentation conditions, geographic regions, season, country, and analytical methods used to detect these toxins (Di Guan et al., 2011). In general, yogurts have shown lower contamination levels with AFM₁ than cheese (Rabie et al., 2019), as the fermentation process contributes to reducing the concentration of AFM1 because of low pH and the production of fermentation-related byproducts such as organic acids, including lactic acid, among other factors (Campagnollo et al., 2016). In milk, AFM1 binds to casein, and the modifications on its structure caused by pH reduction during fermentation may lead to changes in this bound (Govaris et al., 2002). However, the exact mechanisms involved in the mycotoxin decontamination during the fermentation process are not entirely understood. Several experimental data indicate that aflatoxin reduction in fermented products occurs through its binding to the cell wall components of starter cultures, as reviewed by Muaz et al. (2021), or through degradation of the toxins by microbial enzymes into less toxic substances (Guo et al., 2020). The most studied bacteria with practical AFM₁-binding abilities are lactic acid bacteria belonging to the genus Levilactobacillus spp. (former Lactobacillus sp.) such as L. rhamnosus and L. plantarum (Sadiq et al., 2019). Regarding bio-detoxification, several species in the genera Pseudomonas, Rhodococcus, Streptomyces, Bacillus, and Pleurotus have been reported to be capable of degrading aflatoxins (Guo et al., 2020). However, these bacterial species are not allowed to be used as starter cultures in fermented foods. The combination of fermentation with some emerging technologies, such as ultrasound, ohmic heating, and cold plasma, has been proposed, aiming at improving aflatoxin’s detoxification (Gavahian et al., 2021).

In Shahr-e Kord, Iran, AFM₁ was detected in 35% of the yogurt samples, but not above the EU’s acceptable limit (Nilchian and Rahimi, 2012). In Gilan, another province of Iran, 63.33% of the yogurt samples were above the EU limits (Issazadeh et al., 2012). In central Iran, yogurt samples showed mean AFM1 contamination levels of 13.55 ng/kg (Arast et al., 2012). In Isfahan, 80% of the yogurt samples were contaminated with this toxin, and 5% of them were above the limit determined by the EU (Rahimi, 2014). In traditional Iranian yogurts, these toxin levels were more significant than in industrialized products (Mason et al., 2015). Still, in Iran, aflatoxins levels were evaluated in yogurt and Doogh samples, with 23.8 and 13.6%, respectively, yielding positive results (Bahrami et al., 2016). However, in Iran, 100% of the yogurt samples collected in 2014 were contaminated, with 22.22% above the AFM₁ limits determined by the EU (Nikbakht et al., 2016). On the other hand, 83.3% of the yogurt samples were positive for AFM₁ in another study, although none of them was above the limits determined by the Institute of Standards and Industrial Research of Iran (50 ng/L) (Sohrabi and Gharahkoli, 2016).

In Bagdad, the capital of Iraq, 100% of the yogurt samples from supermarkets were contaminated with AFM₁ (Jasim and Najim, 2014). A study carried out with local and imported yogurts in Iraq found that 75 and 50%, respectively, of the samples contained AFM₁ (Al-Mossawei et al., 2016). In Kuwait, one sample out of two yogurt samples produced in a local farm was contaminated with AFM₁ (Ivastava et al., 2001). In Lebanon, 32.81% of the samples analyzed showed the presence of AFM₁, with 6.25% of them exceeding the limits determined by the EU (El Khoury et al., 2011). Still, in Lebanon, 72% of the yogurt samples analyzed showed AFM₁, with 13% above the recommended limits (Hassan and Kassaify, 2014). In another study carried out in Lebanon with different yogurt types, it was observed that 64.3% of the samples were positive for AFM₁, and 35.7% were above the limits recommended by the EU. Strained yogurt, popularly consumed by the Lebanese population, showed 88.9% contaminated samples, with 81.5% above the EU acceptable limits. The authors suggested that these findings may be due to low-quality powdered milk in the production, leading to high levels of contamination in the final product. As for the yogurt drink Ayran, 88.9% of the samples were positive, with 44.4% above the EU recommended limits (Daou et al., 2020).

In Malaysia, 40% of the yogurt samples collected in January 2014 were contaminated with AFM₁, although none of them was above the limits determined by the EU (Nadira et al., 2017). A study carried out in the winter and summer in Pakistan showed that 37 and 29% of the samples of yogurt, respectively, were contaminated with this toxin, and were above the country limits (0.05 μg/L) (Iqbal et al., 2013). In Punjab, a province of Pakistan, 47% of the yogurt samples were above the legal limits (Iqbal and Asi, 2013). Corroborating these findings, another study carried out in the winter and summer showed that plain yogurt and flavored yogurt samples were contaminated with AFM₁ by 20 and 16%, respectively, and were above the levels determined by the EU during the summer. In the winter, 27.7 and 40%, respectively, were above the EU limits, posing a considerable threat to the population’s health (Iqbal et al., 2017). In Taiwan, 12.5% of the samples of yogurt beverages were contaminated with AFM₁ but at low levels (Lin et al., 2004).

On the other hand, in Ankara, Turkey’s capital, 32% of the yogurt samples showed AFM1 levels above the country’s limit (Gurbay et al., 2006). Also, in Turkey, 11.53% of the yogurt samples, 9.52% of fruit yogurt samples, and 21.15% of strained yogurt samples showed AFM1 levels greater than those allowed by the existing regulations in the country (50 ng/kg) (Akkaya et al., 2006). Corroborating this finding, 20% of the yogurt samples evaluated in other studies showed contamination levels above the acceptable limits by Turkish Food Codex (2008) (50 ng/kg) (Atasever et al., 2011; Temamogullari and Kanici, 2014). Another study in Ankara showed that 89.5% of the yogurt samples were contaminated with AFM₁. Only 5 were above the limit determined by the local regulations (Sarica et al., 2015). On the other hand, in Turkey, only two yogurt samples and one sample of Ayran showed AFM₁, but the levels were below the EU limits (Sahin et al., 2016).

Concluding Remarks

Several studies regarding the prevalence of AFM₁ in industrial and traditional fermented milk were conducted worldwide in the past 20 years, indicating high frequencies of positive samples at low levels of contamination among different industrial and traditional fermented milk products. A decreasing trend in the contamination of fermented milk products was observed over the years, mainly in traditional products. However, AFM₁ contamination in fermented milk at levels higher than the recommended tolerable limits was reported in African and Asian countries. Continuous monitoring and controlling actions from both manufacturers and regulatory bodies are essential to reduce the AFM₁ contamination levels in industrial and traditional fermented milk. Further studies to improve fermentation performance to reduce the AFM₁ contents in contaminated milk and other similar products are recommended.

Conflict of interest statement

The authors declare that there are no conflicts of interest relevant to this study.

This article was originally published in Italian Journal of Food Science, 2021; 33 (SP1): 12–23. DOI 10.15586/ijfs.v33iSP1.1982. This is an Open Access article

References

Agência Nacional de Vigilância Sanitária, 2011. Resolução RDC nº 7, de 18 de fevereiro de 2011. Diário Oficial da União—Seção 1, nº 37, 22 de fevereiro de 2011. pp. 72–73. Available at: http:// bvsms.saude.gov.br/bvs/saudelegis/anvisa/2011/res0007_ 18_02_2011_rep.hml.

Akkaya, L., Birdane, Y.O., Oguz, H. and Cemek, M., 2006. The occurrence of aflatoxin M1 in yogurt samples from Afyonkarahisar, Turkey. No. 50, Bulletin Veterinary Institute, Pulawy, 50: 517–519. Available at: https://www.researchgate.net/publication/256841530_Occurrence_of_aflatoxin_M1_in_yogurt_samples_from_Afyonkarahisar_Turkey

Aiad, A.S. and Aboelmakarem, H., 2013. Aflatoxin M1 levels in milk and some dairy products in Alexandria city. Assiut Veterinary Medical Journal 59(139): 94–98. Available at: http://www.aun. edu.eg/journal_files/119_J_1147.pdf

Al-Mossawei, M.T., Al-Zubaidi, L.A., Hamza, I.S. and Abduljaleel, S.Y., 2016. Detection of AFM1 in milk and some dairy products in Iraq using different techniques. Advances in Life Science Technology 41: 74–81. Available at: https://www. iiste.org/Journals/index.php/ALST/article/view/28597/29359

Anthony, M.H., Ojochenemi, A.D., Mulunda, M., Oriyomi, S.T., Jideofor, N.F., Tunde, O. and Isah, A., 2016. Aflatoxin M1 in breast milk, cow milk, and milk products in Minna, Nigeria and their predisposing factors. Biochemistry Analytical Biochemistry 5(4): 1–7. https://doi.org/10.4172/2161-1009.1000303

Arast, Y., Mohammadian, M. and Behnamipour, S., 2012. Occurrence of aflatoxin M1 in two dairy products by ELISA in central part of Iran. Life Science Journal 9(3): 1831–1833. https://doi.org/10.7537/marslsj090312.265

Atasever, M.A., Atasever, M. and Özturan, K., 2011. Aflatoxin M1 levels in retail yoghurt and ayran in Erzurum in Turkey. Turkish Journal of Veterinary and Animal Sciences 35(1): 59–62. Available at: https://journals.tubitak.gov.tr/veterinary/issues/ vet-11-35-1/vet-35-1-8-0906-96.pdf

Bahrami, R., Shahbazi, Y. and Nikousefat, Z., 2016. Aflatoxin M1 in milk and traditional dairy products from west part of Iran: occurrence and seasonal variation with an emphasis on risk assessment of human exposure. Food Control 62: 250–256. https://doi.org/10.1016/j.foodcont.2015.10.039

Barjesteh, M.H., Azizi, I.G. and Noshfar, E., 2010. Occurrence of aflatoxin M1 in pasteurized and local yogurt in Mazandaran province (northern Iran) using ELISA. Global Veterinaria 4(5): 459–462. Available at: http://idosi.org/gv/gv4(5)10/7.pdf

Barukčić, I., Bilandžić, N., Markov, K., Jakopović, K.L. and Božanić, R., 2018. Reduction in aflatoxin M1 concentration during production and storage of selected fermented milks. International Journal of Dairy Technology 71(3): 734–740. https://doi.org/10.1111/1471-0307.12490

Behfar, A., Khorasgani, Z.N., Alemzadeh, Z., Goudarzi, M., Ebrahimi, R. and Tarhani, N., 2012. Determination of aflatoxin M1 levels in produced pasteurized milk in Ahvaz City by using HPLC. Jundishapur Journal of Natural Pharmaceutical Products 7(2): 80–84. https://doi.org/10.5812/jjnpp.4707

Bhat, R., Rai, R.V. and Karim, A., 2010. Mycotoxins in food and feed: present status and future concerns. Comprehensive Reviews in Food Science and Food Safety 9(1): 57–81. https://doi. org/10.1111/j.1541-4337.2009.00094.x

Bilandzic, N., Bozic, D., Dokic, M., Sedak, M., Kolanovic, B.S., Varenina, I., Tankovic, S. and Cvetnic, Z., 2014. Seasonal effect on aflatoxin M1 contamination in raw and UHT milk from Croatia. Food Control 40: 260–264. https://doi.org/10.1016/j. foodcont.2013.12.002

Black, E.P., 2011. Dairy—fermented products. In: Heldman, D.R., Wheeler, M.B. and Hoover, D.G. (ed.), Encyclopedia of biotechnology in agriculture and food. Publishing Taylor and Francis, New York, pp. 195–199.

Campagnollo, F.B., Ganev, K.C., Khaneghah, A.M., Portella, J., Cruz, A.G., Granato, D., Corassin, C.H., Oliveira, C.A.F. and Sant’Ana, A.S., 2016. The occurrence and effect of unit operations for dairy products processing on the fate of aflatoxin M1 : a review. Food Control 68: 310–329. https://doi.org/10.1016/j. foodcont.2016.04.007

Cano-Sancho, G., Marin, S., Ramos, A.J., Peris-Vicente, J. and Sanchis, V., 2010. Occurrence of aflatoxin M1 and exposure assessment in Catalonia (Spain). Revista Iberoamericana de Micología 27(3): 130–135. https://doi.org/10.1016/j. riam.2010.05.003

Cano-Sancho, G., Perelló, G., Nadal, M. and Domingo, J.L., 2015. Comparison of the nutritional composition and the concentrations of various contaminants in branded and private label yogurts. Journal of Food Composition and Analysis 42: 71–77. https://doi.org/10.1016/j.jfca.2015.03.008

Daou, R., Afif, C., Joubrane, K., Khabbaz, L.R., Maroun, R., Ismail, A. and El Khoury, A., 2020. Occurrence of aflatoxin M1 in raw, pasteurized, UHT cows’ milk, and dairy products in Lebanon. Food Control 111: 5–29. https://doi.org/10.1016/j. foodcont.2019.107055

De Roma, A., Rossini, C., Ritieni, A., Gallo, P. and Esposito, M., 2017. A survey on the aflatoxin M1 occurrence and seasonal variation in buffalo and cow milk from Southern Italy. Food Control 81: 30–33. https://doi.org/10.1016/j.foodcont.2017.05.034

Di Guan, P.L., Zhang, Q., Wen, Z., Daohong Z. and Jun, J., 2011. An ultra-sensitive monoclonal antibody-based competitive enzyme Immunoassay for aflatoxin M1 in milk and infant milk products. Food Chemistry 125: 1359–1364. https://doi.org/10.1016/j. foodchem.2010.10.006

El Khoury, A., Atoui, A. and Yaghi, J., 2011. Analysis of aflatoxin M1 in milk and yogurt and AFM1 reduction by lactic acid bacteria used in Lebanese industry. Food Control 22(10): 1695–1699. https://doi.org/10.1016/j.foodcont.2011.04.001

European Commission, 2020. Available at: https://eur-lex.europa. eu/legal-content/EN/ALL/?uri=celex%3A32006R1881.

Fallah, A.A., 2010. Aflatoxin M1 contamination in dairy products marketed in Iran during winter and summer. Food Control 21: 1478–1481. https://doi.org/10.1016/j.foodcont.2010.04.017

Fallah, A.A., Rahnama, M., Jafari, T. and Saei-Dehkordi, S.S., 2011. Seasonal variation of aflatoxin M1 contamination in industrial and traditional Iranian dairy products. Food Control 22(10): 1653–1656. https://doi.org/10.1016/j.foodcont.2011.03.024

Food and Drug Administration Industry, 2000. Activities staff booklet. Available at: http://www.cfsan.fda.gov/~lrd/fdaact.html#afla.

Galvano, F., Galofaro, V., Ritieni, A., Bognanno, M., De Angelis, A. and Galvano, G., 2001. Survey of the occurrence of aflatoxin M1 in dairy products marketed in Italy: second year of observation. Food Additives and Contaminants 18(7): 644–646. https://doi. org/10.1080/02652030110035381

Gamba, R.R., Caro, C.A., Martínez, O.L., Moretti, A.F., Giannuzzi, L., De Antoni, G.L. and Peláez, A.L., 2016. Antifungal effect of kefir fermented milk and shelf life improvement of corn arepas. International Journal of Food Microbiology 235: 85–92. https://doi.org/10.1016/j.ijfoodmicro.2016.06.038

Gavahian, M., Mathad, G.N., Oliveira, C.A.F. and Mousavi Khaneghah, A., 2021. Combinations of emerging technologies with fermentation: interaction effects for detoxification of mycotoxins? Food Research International 141: 110104. https://doi. org/10.1016/j.foodres.2021.110104

Govaris, A., Roussi, V., Koidis, P.A. and Botsoglou, N.A., 2002. Distribution and stability of aflatoxin M1 during production and storage of youghurt. Food Additives and Contaminants 19(11): 1043–1050. https://doi.org/10.1080/0265203021000007831

Guo, L., Wang, Y., Fei, P., Liu, J. and Ren, D., 2019. A survey on the aflatoxin M1 occurrence in raw milk and dairy products from water buffalo in South China. Food Control 105: 159–163. https://doi.org/10.1016/j.foodcont.2019.05.033

Gürbay, A., Engin, A.B., Çağlayan, A. and Şahin, G., 2006. Aflatoxin M1 levels in commonly consumed cheese and yogurt samples in Ankara, Turkey. Ecology of Food and Nutrition 45(6): 449–459. https://doi.org/10.1080/03670240600985274

Hajmohammadi, M., Valizadeh, R., Naserian, A., Nourozi, M.E., Rocha, R.S. and Oliveira, C.A.F., 2020. Composition and occurrence of aflatoxin M1 in cow’s milk samples from Razavi Khorasan Province, Iran. International Journal of Dairy Technology 73: 40–45. https://doi.org/10.1111/1471-0307.12661

Hassan, H.F. and Kassaify, Z., 2014. The risks associated with aflatoxins M1 occurrence in Lebanese dairy products. Food Control 37: 68–72. https://doi.org/10.1016/j.foodcont.2013.08.022

Hassan, Z.U., Al-Thani, R., Atia, F.A., Almeer, S., Balmas, V., Migheli, Q. and Jaoua, S., 2018. Evidence of low levels of aflatoxin M1 in milk and dairy products marketed in Qatar. Food Control 92: 25–29. https://doi.org/10.1016/j.foodcont.2018.04.038

Ibrahim, D.K., El-Zamik, F.I., Mohamed, G.E. and Abdl El-Basit, H.M., 2016. Determination of aflatoxin M1 levels in milk and some dairy products. Zagazig Journal of Agricultural Research 43(1): 151– 163. https://doi.org/10.21608/zjar.2016.101576

Iha, M.H., Barbosa, C.B., Okada, I.A. and Trucksess, M.W., 2011. Occurrence of aflatoxin M1 in dairy products in Brazil. Food Control 22(12): 1971–1974. https://doi.org/10.1016/j. foodcont.2011.05.013

Iha, M.H., Barbosa, C.B., Okada, I.A. and Trucksess, M.W., 2013. Aflatoxin M1 in milk and distribution and stability of aflatoxin M1 during production and storage of yoghurt and cheese. Food Control 29(1): 1–6. https://doi.org/10.1016/j. foodcont.2012.05.058

Imamura, K.B., Ton. J.C.V. and Glannon, J.A., 2015. Incidence of aflatoxins in peanuts (Arachis hypogaea L) in the state of São Paulo. Revista Analítica 75: 49–54.

International Agency for Research on Cancer, 2002. Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 82: 171–175. Available at: https://publications.iarc.fr/Book-And-Report-Series/Iarc-Monographs-OnThe-Identification-Of-Carcinogenic-Hazards-To-Humans/ Some-Traditional-Herbal-Medicines-Some-MycotoxinsNaphthalene-And-Styrene-2002

Iqbal, S.Z. and Asi, M.R., 2013. Assessment of aflatoxin M1 in milk and milk products from Punjab, Pakistan. Food Control 30(1): 235–239. https://doi.org/10.1016/j.foodcont.2012.06.026

Iqbal, S.Z., Asi, M.R. and Jinap, S.J.F.C., 2013. Variation of aflatoxin M1 contamination in milk and milk products collected during winter and summer seasons. Food Control 34(2): 714–718. https://doi.org/10.1016/j.foodcont.2013.06.009

Iqbal, S.Z., Asi, M.R. and Malik, N., 2017. The seasonal variation of aflatoxin M1 in milk and dairy products and assessment of dietary intake in Punjab, Pakistan. Food Control 79: 292–296. https://doi.org/10.1016/j.foodcont.2017.04.015

Iqbal, S.Z., Jinap, S., Pirouz, A.A. and Faizal, A.A., 2015. Aflatoxin M1 in milk and dairy products, occurrence and recent challenges: a review. Trends in Food Science and Technology 46(1): 110–119. https://doi.org/10.1016/j.tifs.2015.08.005

Ismaiel, A.A., Tharwat, N.A., Sayed, M.A. and Gameh, S.A., 2020. Two-year survey on the seasonal incidence of aflatoxin M1 in traditional dairy products in Egypt. Journal of Food Science and Technology 1–8. https://doi.org/10.1007/s13197-020-04254-3

Issazadeh, K., Darsanaki, R.K. and Pahlaviani, M.K., 2012. Occurrence of aflatoxin M1 levels in local yogurt samples in Gilan Province, Iran. Annals Biological Research 3(8): 3853– 3855. Available at: https://www.scholarsresearchlibrary.com/ articles/occurrence-of-aflatoxin-m1-levels-in-local-yogurt-samples-in-gilan-province-iran.pdf

Ivastava Sr, V.P., Bu-Abbas, A., Al-Johar, W., Al-Mufti, S. and Siddiqui, M.K.J., 2001. Aflatoxin M1 contamination in commercial samples of milk and dairy products in Kuwait. Food Additives and Contaminants 18(11): 993–997. https://doi. org/10.1080/02652030110050357

Jalili, M. and Scotter, M., 2015. A review of aflatoxin M1 in liquid milk. Journal of Health Safety Environment 2: 283–295. Available at: https://core.ac.uk/download/pdf/270218742.pdf

Jasim, H.N. and Najim, N.H., 2014. The occurrence of aflatoxin M1 in milk, soft cheese and yoghurt in Baghdad Province by using ELISA test. The Iraqi Journal of Veterinary Medicine 38(2): 9–16. Available at: https://ijvm.iraqjournals.com/pdf_97461_ dd1011166024f7697ae076f16a9d0c60.html

Kamkar, A., 2005. A study on the occurrence of aflatoxin M1 in raw milk produced in Sarab city of Iran. Food Control 16(7): 593– 599. https://doi.org/10.1016/j.foodcont.2004.06.021

Keskić, T., Miočinović, J., Kos, A., Gavrić, M., Miloradović, Z. and Pudja, P., 2016. Seasonal variations of aflatoxin M1 in dairy products during 2015 in Serbia. Second International Symposium of Veterinary Medicine, Belgrade, pp. 226–232.

Kim, E.K., Shon, D.H., Ryu, D., Park, J.W., Hwang, H.J. and Kim, Y.B., 2000. Occurrence of aflatoxin M1 in Korean dairy products determined by ELISA and HPLC. Food Additives and Contaminants 17(1): 59–64. https://doi.org/10.1080/026520300283595

Kim–Soo, K.R.L.M. and Chung, H., 2016. Aflatoxin M1 levels in dairy products from South Korea determined by high performance liquid chromatography with fluorescence detection. Journal of Food and Nutrition Research 55(2): 171–180. https:// doi.org/10.1080/026520300283595

Kuboka, M.M., Imungi, J.K., Njue, L., Mutua, F., Grace, D. and Lindahl, J.F., 2019. Occurrence of aflatoxin M1 in raw milk traded in peri-urban Nairobi, and the effect of boiling and fermentation. Infection Ecology and Epidemiology 9(1): 1–8. https://doi. org/10.1080/20008686.2019.1625703

Langat, G., Tetsuhiro, M., Gonoi, T., Matiru, V. and Bii, C., 2016. Aflatoxin M1 contamination of milk and its products in Bomet County, Kenya. Advances in Microbiology 6(7): 528. https://doi. org/10.4236/aim.2016.67053

Lin, L.C., Liu, F.M., Fu, Y.M. and Shih, D.C., 2004. Survey of aflatoxin M1 contamination of dairy products in Taiwan. Journal of Food and Drug Analysis 12(2): 154–160. https://doi. org/10.38212/2224-6614.2652

Lindahl, J.F., Kagera, I.N. and Grace, D., 2018. Aflatoxin M1 levels in different marketed milk products in Nairobi, Kenya. Mycotoxin Research 34(4): 289–295. https://doi.org/10.1007/ s12550-018-0323-4

Mahmood Fashandi, H., Abbasi, R. and Mousavi Khaneghah, A., 2018. The detoxification of aflatoxin M1 by Lactobacillus acidophilus and Bifidobacterium spp.: a review. Journal of Food Processing and Preservation 42: e13704. https://doi.org/10.1111/ jfpp.13704

Martins, M.L. and Martins, H.M., 2004. Aflatoxin M1 in yoghurts in Portugal. International Journal of Food Microbiology 91(3): 315–317. https://doi.org/10.1016/S0168-1605(02)00363-X

Mason, S., Arjmandtalab, S., Hajimohammadi, B., Khosravi Arsanjani, A., Karami, S., Sayadi, M. and Oryan, A., 2015. Aflatoxin M1 contamination in industrial and traditional yogurts produced in Iran. Journal of Food Quality and Hazards Control 2(1): 11–14. Available at: http://jfqhc.com/article-1-107-en.pdf

Mousavi Khaneghah, A., Chaves, R.D. and Akbarirad, H., 2017. Detoxification of aflatoxin M1 (AFM1 ) in dairy base beverages (acidophilus milk) by using different types of lactic acid bacteria-mini review. Current Nutrition & Food Science 13: 78–81. https://doi.org/10.2174/1573401313666170102162930

Muaz, K., Riaz, M., Oliveira, C.A.F., Akhtar, S., Ali, S.W., Nadeem, H., Park, S. and Balasubramanian, B., 2021. Aflatoxin M1 in milk and dairy products: global occurrence and potential decontamination strategies. Toxin Reviews. https://doi.org/10.1 080/15569543.2021.1873387

Nadira, A.F., Rosita, J., Norhaizan, M.E. and Redzwan, S.M., 2017. Screening of aflatoxin M1 occurrence in selected milk and dairy products in Terengganu, Malaysia. Food Control 73: 209–214. https://doi.org/10.1016/j.foodcont.2016.08.004

Nejad, A.S.M., Heshmati, A. and Ghiasvand, T., 2019. The occurrence and risk assessment of exposure to aflatoxin M1 in ultrahigh temperature and pasteurized milk in Hamadan province of Iran. Osong Public Health and Research Perspectives 10(4): 228. https://doi.org/10.24171/j.phrp.2019.10.4.05

Nikbakht, M.R., Lachiniyan, S., Rahbar, S., Oubari, F., Rostami, Z. and Tajehmiri, A., 2016. Aflatoxin M1 contamination in traditional yoghurts produced in Guilan province, Iran. Asian Journal of Pharmaceutical Research and Health Care 8(1): 1–3. https:// doi.org/10.18311/ajprhc/2016/663

Nilchian, Z. and Rahimi, E., 2012. Aflatoxin M1 in yoghurts, cheese and ice-cream in Shahrekord-Iran. World Applied Sciences Journal 19(5): 621–624. Available at: https://citeseerx.ist.psu.edu/ viewdoc/download?doi=10.1.1.390.1323&rep=rep1&type=pdf

Otles, S. and Cagindi, O., 2003. Kefir: a probiotic dairy-composition, nutritional and therapeutic aspects. Pakistan Journal of Nutrition 2(2): 54–59. https://doi.org/10.3923/pjn.2003.54.59

Rabie, M., El-Wahed, A., Moustafa, M.G., El-Zahar, K. and AbdelZaher, A.M., 2019. The role of probiotic bacteria in protecting against aflatoxin M1 contamination in milk and certain dairy products. Journal of Food and Dairy Sciences 10(4): 93–99. https://doi.org/10.21608/jfds.2019.36183

Rahimi, E., 2014. Survey of the occurrence of aflatoxin M1 in dairy products marketed in Iran. Toxicology and Industrial Health 30(8): 750–754. https://doi.org/10.1177/0748233712462476

Rahmani, J., Alipour, S., Miri, A., Fakhri, Y., Riahi, S.-M., Keramati, H., Moradi, M., Amanidaz, N., Pouya, R.H., Bahmani, Z. and Mousavi Khaneghah, A., 2018. The prevalence of aflatoxin M1 in milk of Middle East region: a systematic review, meta-analysis and probabilistic health risk assessment. Food and Chemical Toxicology 118: 653–666. https://doi.org/10.1016/j. fct.2018.06.016

Ruangwises, N. and Ruangwises, S., 2010. Aflatoxin M1 contamination in raw milk within the central region of Thailand. Bulletin of Environmental Contamination and Toxicology 85: 195–198. https://doi.org/10.1007/s00128-010-0056-3

Sadiq, F.A., Yan, B., Tian, F., Zhao, J., Zhang, H. and Chen, W., 2019. Lactic acid bacteria as antifungal and anti-mycotoxigenic agents: a comprehensive review. Comprehensive Reviews in Food Science and Food Safety 18: 1403–1436. https://doi. org/10.1111/1541-4337.12481

Sahin, H.Z., Celik, M., Kotay, S. and Kabak, B., 2016. Aflatoxins in dairy cow feed, raw milk and milk products from Turkey. Food Additives and Contaminants: Part B 9(2): 152–158. https://doi. org/10.1080/19393210.2016.1152599

Sarica, D.Y., Has, O., Tasdelen, S. and Ezer, Ü., 2015. Occurrence of aflatoxin M1 in milk, white cheese and yoghurt from Ankara, Turkey markets. Biological and Chemical Research 36–49. Available at: http://www.ss-pub.org/wp-content/ uploads/2015/01/BCR2014103002.pdf

Sohrabi, N. and Gharahkoli, H., 2016. A seasonal study for determination of aflatoxin M1 level in dairy products in Iranshahr, Iran. Current Medical Mycology 2(3): 27. https://doi.org/10.18869/ acadpub.cmm.2.3.27

Temamogullari, F. and Kanici, A., 2014. Aflatoxin M1 in dairy products sold in Şanlıurfa, Turkey. Journal of Dairy Science 97(1): 162–165. https://doi.org/10.3168/jds.2012-6184

Udomkun, P., Mutegi, C., Wossen, T., Atehnkeng, J., Nabahungu, N.L., Njukwe, E. and Bandyopadhyay, R., 2018. Occurrence of aflatoxin in agricultural produce from local markets in Burundi and Eastern Democratic Republic of Congo. Food Science and Nutrition 6(8): 2227–2238. https://doi.org/10.1002/fsn3.787

Wild, C.P., Miller, J.D. and Groopman, J.D., 2015. Mycotoxin control in low-and middle-income countries. IARC Publications, Lyon, France. Available at: https://publications.iarc.fr/BookAnd-Report-Series/Iarc-Working-Group-Reports/MycotoxinControl-In-Low--And-Middle-income-Countries-2015

Zhou, Y., Xiong, S., Zhang, K., Feng, L., Chen, X., Wu, Y. and Xiong, Y., 2019. Quantum bead-based fluorescence-linked immunosorbent assay for ultrasensitive detection of aflatoxin M1 in pasteurized milk, yogurt, and milk powder. Journal of Dairy Science 102(5): 3985–3993. https://doi.org/10.3168/ jds.2018-16109