The Open Public Health Journal




ISSN: 1874-9445 ― Volume 13, 2020
RESEARCH ARTICLE

The Occurrence and Risk Assessment of Aflatoxin M1 in Yoghurt Samples from Hamadan, Iran



Ali Heshmati1, Amir Sasan Mozaffari Mozaffari Nejad2, *, Tayebeh Ghyasvand1
1 Department of Nutrition and Food Safety, Nutrition Health Research Center, Hamadan University of Medical Sciences and Health Services, Hamadan, Iran
2 Nutrition Health Research Center, Student Research Center, Hamadan University of Medical Sciences and Health Services, Hamadan, Iran

Abstract

Background:

Aflatoxin M1 (AFM1) is a hepatocarcinogenic and hydroxylated metabolite of aflatoxin B1, detected in milk and milk products.

Objectives:

The aim of our research was to determine the incidence and risk assessment of AFM1 through the consumption of yoghurt in Hamadan province of Iran.

Methods:

Fifty yoghurt samples were gathered from various areas of Hamadan province, Iran and tested for AFM1 by ELISA technique. The estimated daily intake (EDI) and the liver cancer incidence of aflatoxin M1 were determined.

Results:

AFM1 was detected in 43 (86%) samples, (mean: 28.56 ng/kg; range: <5-98.65 ng/kg). The level of AFM1 in 9 (18%) samples was above the maximum tolerance limit (50 ng/kg). The AFM1 intake through yoghurt consumption in various population groups ranged from 0.016 to 0.032 ng/kg bw/day in mean consumers and 0.019 to 0.046 ng/kg bw/day in high consumers.

Conclusion:

The AFM1 intake through yoghurt contributed a slight part from the overall incidence of liver cancer in the Iranian population. From the findings of the current study, it can be derived that although the high percentage of yoghurt samples in Iran proved to be contaminated with AFM1 contents, did not show a public health concern considering the European Commission (EC) and the Institute of Standards and Industrial Research of Iran (ISIRI) maximum limits.

Keywords: Aflatoxin M1, Yoghurt, ELISA, Hamadan, Risk assessment, European commission.


Article Information


Identifiers and Pagination:

Year: 2020
Volume: 13
First Page: 512
Last Page: 517
Publisher Id: TOPHJ-13-512
DOI: 10.2174/1874944502013010512

Article History:

Received Date: 27/5/2020
Revision Received Date: 19/7/2020
Acceptance Date: 27/7/2020
Electronic publication date: 22/09/2020
Collection year: 2020

© 2020 Heshmati et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at Nutrition Health Research Center, Student Research Center, Hamadan University of Medical Sciences and Health Services, Hamadan, Iran; Tel: +989120193652; E-mail: asmozafarinejad@yahoo.in





1. INTRODUCTION

Yoghurt is one of the most important and popular products among fermented dairy products, which has been used as food consumed by the world population for thousands of years. Yoghurt contains nearly all nutrients necessary to sustain life [1Czaja T, Baranowska M, Mazurek S, Szostak R. Determination of nutritional parameters of yoghurts by FT Raman spectroscopy. Spectrochim Acta A Mol Biomol Spectrosc 2018; 196: 413-7.
[http://dx.doi.org/10.1016/j.saa.2018.02.054] [PMID: 29499570]
, 2Pothuraju R, Yenuganti VR, Hussain SA, Sharma M. Fermented Milk in Protection Against Inflammatory Mechanisms in Obesity Immunity and Inflammation in Health and Disease 2018; 389-401.]. Also, it is a rich source of dietary minerals including vitamins (B6 and B12), calcium (Ca), magnesium (Mg), zinc (Zn), phosphorus (P), and potassium (K), and so many others [3Cano-Sancho G, Perelló G, Nadal M, Domingo J. Comparison of the nutritional composition and the concentrations of various contaminants in branded and private label yogurts. J Food Compos Anal 2015; 42: 71-7.
[http://dx.doi.org/10.1016/j.jfca.2015.03.008]
]. It is also a great source of essential amino acids of great biological modality, generally including premier protein levels toward milk. Nevertheless, on the useful effects of yoghurt consumption, a substantial number of studies have presented the presence of heavy metals and aflatoxin M1 in foodstuff, which is a subject of serious concern, which has been increasing over the last few years [3Cano-Sancho G, Perelló G, Nadal M, Domingo J. Comparison of the nutritional composition and the concentrations of various contaminants in branded and private label yogurts. J Food Compos Anal 2015; 42: 71-7.
[http://dx.doi.org/10.1016/j.jfca.2015.03.008]
].

Aflatoxin M1 (AFM1) is one of the groups of mycotoxin produced by Aspergillus species, especially A. nomius, A. flavus and A. parasiticus and found in contaminated milk (breast and animal), and dairy products. Researchers have demonstrated that the concentration of AFM1 is a dangerous toxic and carcinogenic for humans and animals [4Kamkar A, Fallah AA, Mozaffari Nejad AS. The review of aflatoxin M1 contamination in milk and dairy products produced in Iran. Toxin Rev 2014; 33(4): 160-8.
[http://dx.doi.org/10.3109/15569543.2014.922580]
-8Nejad ASM, Heshmati A, Ghiasvand T. The occurrence and risk assessment of exposure to aflatoxin M1 in ultra-high temperature and pasteurized milk in Hamadan province of Iran. Osong Public Health Res Perspect 2019; 10(4): 228-33.
[http://dx.doi.org/10.24171/j.phrp.2019.10.4.05] [PMID: 31497494]
].

Many countries have implemented regulations to control the amount of mycotoxins groups among food and agricultural products, especially for AFM1 in milk products. These regulations differ among several countries with respect to their economic considerations [4Kamkar A, Fallah AA, Mozaffari Nejad AS. The review of aflatoxin M1 contamination in milk and dairy products produced in Iran. Toxin Rev 2014; 33(4): 160-8.
[http://dx.doi.org/10.3109/15569543.2014.922580]
, 7Tavakoli H, Kamkar A, Riazipour M, Mozaffari Nejad AS, Rafati H. Assessment of aflatoxin M1 levels by enzyme-linked immunosorbent assay in yoghurt consumed in Tehran, Iran. Asian J Chem 2013; 25(5): 2836-8.
[http://dx.doi.org/10.14233/ajchem.2013.14058]
, 9Heshmati A, Mozaffari Nejad AS. Ochratoxin A in dried grapes in Hamadan province, Iran. Food Addit Contam Part B Surveill 2015; 8(4): 255-9.
[http://dx.doi.org/10.1080/19393210.2015.1074945] [PMID: 26219951]
-12Mozaffari Nejad AS, Giri A. The measurement of Aflatoxin B1 in chilli and black peppers of qaemshahr, Iran. J Kerman Univ Med Sci 2015; 22(2): 185-93.]. Hence, the European Commission (EC) and the Institute of Standards and Industrial Research of Iran (ISIRI) have set a limit of 50 ng/kg for AFM1 in yoghurt varieties.

The immediate detection of contamination is one of the beneficial methods to control aflatoxin M1 [13Ben Aissa S, Mars A, Catanante G, Marty J-L, Raouafi N. Design of a redox-active surface for ultrasensitive redox capacitive aptasensing of aflatoxin M1 in milk. Talanta 2019; 195: 525-32.
[http://dx.doi.org/10.1016/j.talanta.2018.11.026] [PMID: 30625578]
]. The current detection methods such as enzyme-linked immunosorbent assay (ELISA), high-performance liquid chromatography (HPLC), and thin-layer chromatography (TLC) are generally performed for the AFM1 analysis [4Kamkar A, Fallah AA, Mozaffari Nejad AS. The review of aflatoxin M1 contamination in milk and dairy products produced in Iran. Toxin Rev 2014; 33(4): 160-8.
[http://dx.doi.org/10.3109/15569543.2014.922580]
-8Nejad ASM, Heshmati A, Ghiasvand T. The occurrence and risk assessment of exposure to aflatoxin M1 in ultra-high temperature and pasteurized milk in Hamadan province of Iran. Osong Public Health Res Perspect 2019; 10(4): 228-33.
[http://dx.doi.org/10.24171/j.phrp.2019.10.4.05] [PMID: 31497494]
, 11Mozaffari Nejad AS, Bayat M, Ahmadi AA. Investigation of Aflatoxin B-1 in Spices Marketed in Hyderabad, India by ELISA Method. J Pure Appl Microbiol 2013; 7(4): 3219-23.-14Mozaffari Nejad AS, Sabouri Ghannad M, Kamkar A. Determination of aflatoxin B1 levels in Iranian and Indian spices by ELISA method. Toxin Rev 2014; 33(4): 151-4.
[http://dx.doi.org/10.3109/15569543.2014.942319]
]. In Iran, the ELISA technique is the most usual and popular among researchers because it is an ordinary, rapid, and low-cost technique for the survey of AFM1 [4Kamkar A, Fallah AA, Mozaffari Nejad AS. The review of aflatoxin M1 contamination in milk and dairy products produced in Iran. Toxin Rev 2014; 33(4): 160-8.
[http://dx.doi.org/10.3109/15569543.2014.922580]
-8Nejad ASM, Heshmati A, Ghiasvand T. The occurrence and risk assessment of exposure to aflatoxin M1 in ultra-high temperature and pasteurized milk in Hamadan province of Iran. Osong Public Health Res Perspect 2019; 10(4): 228-33.
[http://dx.doi.org/10.24171/j.phrp.2019.10.4.05] [PMID: 31497494]
, 15Moosavy M, Roostaee N, Katiraee F, Habibi-Asl B, Mostafavi H, et al. Aflatoxin M1 occurrence in pasteurized milk from various dairy factories in Iran. Int Food Res J 2013; 20(6): 3351.].

The aim of the current survey was to evaluate the occurrence and risk assessment of exposure of AFM1 through the consumption of yoghurt in the Hamadan province of Iran.

2. MATERIALS AND METHODS

2.1. Sample Collection

The current research is a cross-sectional study. For this purpose, 50 yoghurt samples were randomly purchased from supermarkets located in popular markets in different parts of Hamadan province, Iran, from October 2017 to August 2018. Eventually, all samples were carried to the lab and kept in the refrigerator at 4 oC. All samples were analyzed for AFM1 before the expiration date of the samples. All procedures of study were approved by the Ethics Committee of Hamadan University of Medical Sciences with No. IR.UMSHA.REC.1396.617.

2.2. Methods

The quantitative measurement of AFM1 in samples was distinguished by competitive ELISA using AFM1 test kit (RIDASCREEN® AFM1 Art. No.: R1121, R-Biopharm, Darmstadt, Germany). The preparation of the yoghurt samples and AFM1 measurement were performed according to the method described by the kit manufacturer. The mean lower limit of detection (LOD) for AFM1 in yoghurt was 5 ng/kg.

2.3. Risk Assessment for Exposure to AFM1 Through Yoghurt

The risk of AFM1 intake through yoghurt was carried out by the deterministic approach and calculated according to the following equation [16Cano-Sancho G, Marin S, Ramos AJ, Peris-Vicente J, Sanchis V. Occurrence of aflatoxin M1 and exposure assessment in Catalonia (Spain). Rev Iberoam Micol 2010; 27(3): 130-5.
[http://dx.doi.org/10.1016/j.riam.2010.05.003] [PMID: 20601075]
, 17Guo Y, Yuan Y, Yue T. Aflatoxin m1 in milk products in china and dietary risk assessment. J Food Prot 2013; 76(5): 849-53.
[http://dx.doi.org/10.4315/0362-028X.JFP-12-419] [PMID: 23643127]
]:

AFM1 intake (ng/kg bw/day) = the concentration of AFM1 in yoghurt (ng/kg) × 95th percentile (for high consumers) or mean (for mean consumers) of per capita yoghurt consumption (kg)/ body weight (kg) Equation 1.

95th percentile (for high consumers) or mean (for mean consumers) of per capital yoghurt consumption was obtained by food frequency questionnaires (FFQ), Before the study, FFQ was prepared and given to people with different age-sex groups to complete it during a month. The people were randomly selected. For all participants in FFQ study, written informed consent was obtained.

For risk assessment, AFM1 value in yoghurt samples in which the concentration of this mycotoxin was lower than LOD was considered as LOD [17Guo Y, Yuan Y, Yue T. Aflatoxin m1 in milk products in china and dietary risk assessment. J Food Prot 2013; 76(5): 849-53.
[http://dx.doi.org/10.4315/0362-028X.JFP-12-419] [PMID: 23643127]
].

The liver cancer incidence due to AFM1 consumption was estimated according to Equation 2 [17Guo Y, Yuan Y, Yue T. Aflatoxin m1 in milk products in china and dietary risk assessment. J Food Prot 2013; 76(5): 849-53.
[http://dx.doi.org/10.4315/0362-028X.JFP-12-419] [PMID: 23643127]
]:

Liver cancer incidence (cancers/yr/108 persons) = AFM1 intake (ng/kg bw/day) × potency

Potency= 0.001 × (1-P) + 0.03 × P

In these equations, the liver cancer potency of AFM1 in individuals positive for negative hepatitis B surface antigen (HBsAgz +) and individuals negative for negative hepatitis B surface antigen (HBsAgz -) was considered as 0.03 and 0.001 cancers/year/ ng of AFM1/ kg body weight/ day in a population of 100,000 [17Guo Y, Yuan Y, Yue T. Aflatoxin m1 in milk products in china and dietary risk assessment. J Food Prot 2013; 76(5): 849-53.
[http://dx.doi.org/10.4315/0362-028X.JFP-12-419] [PMID: 23643127]
]. According to previous studies, HBsAgz + prevalence rate in Iran was 1.7% [18Porolajal J, Majdzadeh R. Prevalence of chronic Hepatitis B infection in Iran. Majallah-i Ipidimiyuluzhi-i Iran 2009; 4(3): 1-8.].

2.4. Statistical Analysis

The concentrations of AFM1 in milk samples were analyzed by SPSS Statistics 16.0 for Windows. One-side t-test was applied to compare the mean concentration of AFM1 samples with the maximum acceptable amount of the ISIRI and European Union (50 ng/kg) regulation. Differences between values were considered significant at P ≤ 0.05.

3. RESULTS

The occurrence and levels of AFM1 in yoghurt samples consumed in Hamadan province are presented in Table 1. AFM1 was detected above an acceptable level of 86% (43/50) in the analyzed samples, ranging from <5 to 98.65 ng/kg. Levels of the AFM1 in 9 (18%) yoghurt samples exceeded the ISIRI and European union i.e. 50 ng/kg. On the other hand, considering the US FDA [19FDA S. 527. 400 Whole Milk, Low Fat Milk, Skim Milk–Aflatoxin M1 (CPG 710610) FDA/ORA Compliance Policy Guides 2005.] limits for AFM1 in milk (500 ng/l), none of the samples had levels above the maximum tolerance limit.

The AFM1 intakes through yoghurt in different age-sex groups of Iran population are shown in Table 2. The mean AFM1 intake in various population groups ranged from 0.016 to 0.032 ng/kg bw/day in mean consumers and 0.019 to 0.046 ng/kg bw/day in high consumers. Data regarding the potential liver cancer risk of AFM1 in yoghurt in the Iranian population were estimated and presented in Table 2.



Table 1
The occurrence of AFM1 in yoghurt samples from Hamadan (Iran) market.


Table 2
Exposure assessment for AFM1 intake in different sex-age groups of Iran population through yoghurt consumption using deterministic method.


Table 3
The occurrence and levels of aflatoxin M1 (ng/kg) in various yoghurt samples published in previous studies.


4. DISCUSSION

Yoghurt is a favorite fermented dairy product, which is used as part of the popular diet in Iran because yoghurt is useful to affect human’s health and has nutritional value. Various types of fermented dairy products have been made and consumed in individual households in Iran, Turkey, Qatar, Lebanon, and other Middle Eastern countries for centuries.

Considering the present findings, we detected a high level of AFM1 contamination in yoghurt samples from Iran. In a prior survey, Cano-Sancho et al. [16Cano-Sancho G, Marin S, Ramos AJ, Peris-Vicente J, Sanchis V. Occurrence of aflatoxin M1 and exposure assessment in Catalonia (Spain). Rev Iberoam Micol 2010; 27(3): 130-5.
[http://dx.doi.org/10.1016/j.riam.2010.05.003] [PMID: 20601075]
] reported the lower level of AFM1 at a detectable level in yoghurt samples; but in a recent study, Altun et al. [20Altun SK, Temamoǧullari FK, Atasever M, Demirci M. Determination of Aflatoxin M1 levels in some cheese types and retail yoghurt samples. Res J Biotechnol 2017; 12(10): 47-52.] detected AFM1 in 100% of yoghurt samples. Various studies by other researchers from different countries have previously been conducted on high or low contamination levels of AFM1 in yoghurt. Table 3 shows the compilation of data level of AFM1 contamination in yoghurt samples from previous studies from several countries measured by different techniques including HPLC and ELISA.

Hassan and Kassaift [21Hassan HF, Kassaify Z. The risks associated with aflatoxins M1 occurrence in Lebanese dairy products. Food Control 2014; 37: 68-72.
[http://dx.doi.org/10.1016/j.foodcont.2013.08.022]
] from Lebanon using ELISA method reported that 49 (72%) of 68 samples of yoghurt were detected with AFM1 and in 9 (14%) samples, the amount of AFM1 was higher than the EU regulations (50 ng/kg), this result is approximately similar to our research results. The other survey from Iran by Tavakoli et al [7Tavakoli H, Kamkar A, Riazipour M, Mozaffari Nejad AS, Rafati H. Assessment of aflatoxin M1 levels by enzyme-linked immunosorbent assay in yoghurt consumed in Tehran, Iran. Asian J Chem 2013; 25(5): 2836-8.
[http://dx.doi.org/10.14233/ajchem.2013.14058]
] that were done with ELISA technique on 50 samples of yoghurt, 35 (70%) of samples were contaminated with AFM1. Also, 6 (17.4%) samples of yoghurt had greater AFM1 content than the limit allowed in European Union (EU) 50 (ng/kg).

The other obtained results reported by Tabari et al. [22Tabari M, Tabari K, Tabari O. Aflatoxin M1 determination in yoghurt produced in Guilan province of Iran using immunoaffinity column and high-performance liquid chromatography. Toxicol Ind Health 2013; 29(1): 72-6.
[http://dx.doi.org/10.1177/0748233712446729] [PMID: 22637575]
] determined AFM1 levels in 120 yoghurt samples from Guilan province in Iran using the ELISA method. They have reported that 100% of the samples found aflatoxin M1 by a mean concentration of 28.2 ng/kg. Also, 16 (13.3%) samples were above the permissible quantity according to the EC (50 ng/kg). However, this result is in contrast to our findings, that showed 86% (43/50) were contaminated with AFM1.The other conducted results were revealed in Serbia by Tomašević et al. [23Tomašević I, Petrović J, Jovetić M, et al. Two year survey on the occurrence and seasonal variation of aflatoxin M1 in milk and milk products in Serbia. Food Control 2015; 56: 64-70.
[http://dx.doi.org/10.1016/j.foodcont.2015.03.017]
], which were observed with ELISA, from 56 samples of yoghurt, all samples (100%) were contaminated with AFM1. Also, 22 (39.2%) samples were above the permissible level according to the EC (50 ng/kg). But, our results reported that approximately some of the yoghurt samples were contaminated with AFM1. This result from Serbia is similar to another study from Iran by Nikbakht et al. [24Nikbakht MR, Lachiniyan S, Rahbar S, et al. Aflatoxin M1 contamination in traditional yoghurts produced in Guilan province, Iran. Asian Journal of Pharmaceutical Research and Health Care 2016; 8(1)
[http://dx.doi.org/10.18311/ajprhc/2016/663]
]. They detected that all yoghurt samples (100%) were contaminated with AFM1; and also, 20 (22.22%) of the samples were above the permissible level according to EU (50 ng/kg).

In a previous study performed in Iran, Mason et al. [25Mason S, Arjmandtalab S, Hajimohammadi B, et al. Aflatoxin M1 contamination in industrial and traditional yogurts produced in Iran. Journal of food quality and hazards control 2015; 2(1): 11-4.] revealed that in 37 (92.5%)out of 40 industrial yoghurt samples, aflatoxin M1 was detected in concentration between <5 and 71 ng/kg; and in 3 (7.5%) samples, the contamination level exceeded the maximum permissible limit (50 ng/kg). In agreement with our research, these reports proved a widespread incidence of aflatoxin M1 in yoghurt samples ready and consumed in Iran. Compared to some reports from several countries, our results showed higher contamination. In Turkey, for example, aflatoxin M1 was detected in 2 (3.3%) out of 60 yoghurt samples with a range of 24 to 28 ng/kg. Also, none of the samples had aflatoxin M1 above the maximum tolerance limit (50 ng/kg) set by the EU [26Sahin HZ, Celik M, Kotay S, Kabak B. Aflatoxins in dairy cow feed, raw milk and milk products from Turkey. Food Addit Contam Part B Surveill 2016; 9(2): 152-8.
[http://dx.doi.org/10.1080/19393210.2016.1152599] [PMID: 26883580]
]. In another survey from China using the ELISA method [17Guo Y, Yuan Y, Yue T. Aflatoxin m1 in milk products in china and dietary risk assessment. J Food Prot 2013; 76(5): 849-53.
[http://dx.doi.org/10.4315/0362-028X.JFP-12-419] [PMID: 23643127]
], it was observed that in 8 (4.49%), out of 178 samples, aflatoxin M1 was present. The contamination level was detected in 8 (4.49%) of the samples which were above 50 ng/kg according to the EU.

According to several studies carried out in different neighboring countries of Iran, Turkey Altun et al. [20Altun SK, Temamoǧullari FK, Atasever M, Demirci M. Determination of Aflatoxin M1 levels in some cheese types and retail yoghurt samples. Res J Biotechnol 2017; 12(10): 47-52.]; Tosun & Ayyildiz [27Tosun H, Ayyıldız T. Occurrence of aflatoxin M1 in organic dairy products. Qual Assur Saf Crops Foods 2013; 5(3): 215-9.
[http://dx.doi.org/10.3920/QAS2012.0147]
]; Atasever et al. [28Atasever MA, Atasever M. ÖZTURAN K. Aflatoxin M1 levels in retail yoghurt and ayran in Erzurum in Turkey. Turk J Vet Anim Sci 2011; 35(1): 59-62.] detected a high incidence of aflatoxin M1 in yoghurt samples (100%, 100% and 87.5%, respectively). These results were detected by the ELISA method.

As seen in Table 3, the contamination levels of aflatoxin M1 in yoghurt samples vary from one study to another. This variability can be explained by different factors such as geographical region, yoghurt-making procedures, analytical method employed and seasons variability [4Kamkar A, Fallah AA, Mozaffari Nejad AS. The review of aflatoxin M1 contamination in milk and dairy products produced in Iran. Toxin Rev 2014; 33(4): 160-8.
[http://dx.doi.org/10.3109/15569543.2014.922580]
, 29Fallah AA, Jafari T, Fallah A, Rahnama M. Determination of aflatoxin M1 levels in Iranian white and cream cheese. Food Chem Toxicol 2009; 47(8): 1872-5.
[http://dx.doi.org/10.1016/j.fct.2009.04.042] [PMID: 19426778]
]. On the other hand, the previous study by Iha et al. [30Iha MH, Barbosa CB, Okada IA, Trucksess MW. Aflatoxin M1 in milk and distribution and stability of aflatoxin M1 during production and storage of yoghurt and cheese. Food Control 2013; 29(1): 1-6.
[http://dx.doi.org/10.1016/j.foodcont.2012.05.058]
] showed that the process of fermentation of yoghurt has no effect on aflatoxin M1. Also, the other surveys revealed that the quality of raw materials in yoghurt is effective on the presence and levels of AFM1. It is also noted that little or no reduction in aflatoxin M1 levels occurs as a result of pasteurization [31Jasutiene I, Garmiene G, Kulikauskiene M. Pasteurisation and fermentation effects on Aflatoxin M1 stability. Milchwissenschaft 2006; 61(1): 75-9.].

The incidence of liver cancer in Iran was 3.53 cancers per year per 105 persons or 3530 cancers/yr/108 persons [32Fazli Z, Fatemeh S, Abdi A, Pourhosseingholi M, Taghinejad H. Studying of liver cancer mortality and morbidity burden in Iran. Sci J Ilam Univ Med Sci 2012; 4(20): 117-22.] and AFM1 intake through yoghurt contributed 0.023-0.048 cancers/yr/108 person for mean consumers and 0.028-0.069 cancers/yr/108 person for high consumers. Therefore, our findings indicated AFM1 in yoghurt contributed a slight part from the overall incidence of liver cancer in the Iranian population. The intake of AFM1 and liver cancer incidence due to the consumption of this mycotoxin through yoghurt and milk was reported in other countries including China, Spain, Greece and Serbia [16Cano-Sancho G, Marin S, Ramos AJ, Peris-Vicente J, Sanchis V. Occurrence of aflatoxin M1 and exposure assessment in Catalonia (Spain). Rev Iberoam Micol 2010; 27(3): 130-5.
[http://dx.doi.org/10.1016/j.riam.2010.05.003] [PMID: 20601075]
, 17Guo Y, Yuan Y, Yue T. Aflatoxin m1 in milk products in china and dietary risk assessment. J Food Prot 2013; 76(5): 849-53.
[http://dx.doi.org/10.4315/0362-028X.JFP-12-419] [PMID: 23643127]
, 33Udovicki B, Djekic I, Kalogianni EP, Rajkovic A. Exposure assessment and risk characterization of Aflatoxin M1 intake through consumption of milk and yoghurt by student population in Serbia and Greece. Toxins (Basel) 2019; 11(4): 205.
[http://dx.doi.org/10.3390/toxins11040205] [PMID: 30959754]
]. The range of liver cancer incidence or hepatocellular carcinoma (HCC) due to AFM1 intake through milk and yoghurt was 0.025–0.033 case or cancers/yr/108 person in China that it was similar to our study while in Serbia and Greece was 3.6–0.4.7 and 0.7–0.9 case or cancers/yr/108 person, respectively that it was higher than the current study [17Guo Y, Yuan Y, Yue T. Aflatoxin m1 in milk products in china and dietary risk assessment. J Food Prot 2013; 76(5): 849-53.
[http://dx.doi.org/10.4315/0362-028X.JFP-12-419] [PMID: 23643127]
, 33Udovicki B, Djekic I, Kalogianni EP, Rajkovic A. Exposure assessment and risk characterization of Aflatoxin M1 intake through consumption of milk and yoghurt by student population in Serbia and Greece. Toxins (Basel) 2019; 11(4): 205.
[http://dx.doi.org/10.3390/toxins11040205] [PMID: 30959754]
]. The dispenses were related to the AFM1 level and consumption value of yoghurt.

CONCLUSION

From our findings of the current study, it can be derived that although a high percentage of yoghurt samples in Iran proved to have AFM1 contents, but it does not show a public health concern considering the European Commission (EC) and the Institute of Standards and Industrial Research of Iran (ISIRI) maximum limits. However, regarding the important role of milk, especially dairy products in the human diet, there is a huge concern about the presence of AFM1 in milk and dairy products. Hence, it is important to use fast methods in the detection of AFM1 in milk and dairy products; and also, the Iranian public health authorities have to monitor ceaselessly to detect AFM1 contamination.

AUTHORS’ CONTRIBUTIONS

Ali Heshmati, and Amir Sasan Mozaffari Nejad conceived, designed, analyzed, and interpreted the data; Tayebeh Ghyasvand and Amir Sasan Mozaffari Nejad performed data collection. Ali Heshmati and Amir Sasan Mozaffari Nejad wrote the first draft and finalized it. All authors read and approved the final manuscript.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

All procedures of the study were approved by the Ethics Committee of Hamadan University of Medical Sciences, Iran with No. IR.UMSHA.REC.1396.617.

HUMAN AND ANIMAL RIGHTS

Not applicable.

CONSENT FOR PUBLICATION

Not applicable.

AVAILABILITY OF DATA AND MATERIALS

The data that support the findings of this study are with the corresponding author, [ASMN], and can be made available on reasonable request.

FUNDING

The authors appreciate the Vice-Chancellor of Research and Technology of Hamadan University of Medical Sciences for financial support (Project No. 9609286051).

CONFLICT OF INTEREST

The authors declare no conflicts of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Declared none.

REFERENCES

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