Despite in recent decades, several studies on the concentration of aflatoxins M1(AFM1) in various milks have been studied, as we know, no systematic review, meta-analysis and carcinogenic risk assessment study was conducted in Iran till now.
In this study, a systematic review was conducted to collect, meta-analysis and carcinogenic risk assessment of the quantitative data regarding the prevalence and concentration of AFM1 in several types of milk produced in Iran.
In our study, the concentration and prevalence of AFM1 in different types of milk (Raw, pasteurized, and UHT) from 113 original articles in Iran using searching the Web of Science, PubMed, Scopus, Science Direct and Google Scholar (in Persian and English) databases from 2002 to august 2021 were collected. The concentration of AFM1 was meta-analyzed using the random effect model (REM) based on type of milk (raw, pasteurized and UHT) subgroups and Monte Carlo simulation (MCS) approach was used to assess safety risks and investigate carcinogenic effects of AFM1 using Crystal-Ball software (Version 11.1.3, Oracle, Inc., USA).
Summary and Outlook
The 113 original article (In English and Persian) were included in this review. Meta-analysis indicated lower and upper of AFM1 in subgroups of raw, pasteurized and UHT milk in Iran was 9, 720, 2.7, 230.2, 19.23, and 221.6 ng/kg respectively. The Point estimate for carcinogenic risk of AFM1 showed as result of age increasing, the carcinogenic risk of Aflatoxin M 1 decreases and concentration of Aflatoxin M1 (ng/liter), plays the most effective role in carcinogenic risk of AFM1.
The presence of AFM1 in milk and its products due to its high toxicity and carcinogenic properties is a public health concern that the results show that the risk of carcinogenesis is higher at younger ages (less than 20 years). As a result, there is a strong association between consumption of raw milk, pasteurized milk and UHT and the risk of cancer in children and adults in Iran.
The authors thank to Student Research Committee of Deputy of Research and Technology of Mazandaran University of Medical Sciences for their financial support.
Research funding: This research was supported by Deputy of Research and Technology of Mazandaran University of Medical Sciences (IR.MAZUMS.REC.1400.417).
Author contributions: Fatemeh Mortezazadeh searched databases, screened results and extract data. She wrote the manuscript with support from Fathollah Gholami-Borujeni. Fathollah Gholami-Borujeni conceived of the presented idea, developed the theory, Meta-Analysis, risk assessment, and supervised the findings of this work. All authors discussed the results and contributed to the final manuscript.
Competing interests: The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Informed consent: Informed consent is not applicable.
Ethical approval: The conducted research is not related to either human or animal use.
1. Mohamadi, H, Alizadeh, M, Rahimi, J, Qasri, S. Assessment of aflatoxin M1 levels in selected dairy products in north-western Iran. Int J Dairy Technol 2010;63:262–5. https://doi.org/10.1111/j.1471-0307.2009.00559.x.Search in Google Scholar
2. Rahimi, E, Nilchian, Z, Behzadnia, A. Presence of aflatoxin M1 in pasteurized and UHT milk commercialized in Shiraz, Khuzestan and Yazd, Iran. J Chem Health Risks 2012;1.10.1007/s12571-009-0028-9Search in Google Scholar
3. Hajmohammadi, M, Valizadeh, R, Naserian, A, Nourozi, ME, Rocha, RS, Oliveira, CA. Composition and occurrence of aflatoxin M1 in cow’s milk samples from Razavi Khorasan Province, Iran. Int J Dairy Technol 2020;73:40–5. https://doi.org/10.1111/1471-0307.12661.Search in Google Scholar
4. Mohamadi, H, Alizadeh, M. A study of the occurrence of aflatoxin M1 in dairy products marketed in Urmia, Iran. J Agric Sci Technol 2010;12:579–83.Search in Google Scholar
5. Riahi-Zanjani, B, Balali-Mood, M. Aflatoxin M1 contamination in commercial pasteurized milk from local markets in Fariman, Iran. Mycotoxin Res 2013;29:271–4. https://doi.org/10.1007/s12550-013-0179-6.Search in Google Scholar PubMed
6. Serraino, A, Bonilauri, P, Kerekes, K, Farkas, Z, Giacometti, F, Canever, A, et al.. Occurrence of aflatoxin M1 in raw milk marketed in Italy: exposure assessment and risk characterization. Front Microbiol 2019;10:2516. https://doi.org/10.3389/fmicb.2019.02516.Search in Google Scholar PubMed PubMed Central
7. Naz, N, Abbas, M, Rubab, A, Kanwal, K. Occurrence of aflatoxin M1 in milk-based mithae samples from Pakistan. Open Chem 2019;17:1140–5. https://doi.org/10.1515/chem-2019-0123.Search in Google Scholar
9. Mojkar, M, Safavizadeh, V. A survey on the occurrence of aflatoxin M1 in raw milk samples in Bafq and Bahabad, Iran. J Food Saf Hygiene 2019;5:175–8.Search in Google Scholar
10. Awaisheh, SS, Rahahleh, RJ, Algroom, RM, Al-Bakheit, AaA, Al-Khaza’leh, JM, Al-Dababseh, BA. Contamination level and exposure assessment to Aflatoxin M1 in Jordanian infant milk formulas. Italian J Food Saf 2019;8. https://doi.org/10.4081/ijfs.2019.8263.Search in Google Scholar PubMed PubMed Central
11. Abyaneh, HK, Bahonar, A, Noori, N, Yazdanpanah, H, AliAbadi, MHS. Exposure to Aflatoxin M1 through milk consumption in Tehran population, Iran. Iran J Pharm Res (IJPR) 2019;18:1332.Search in Google Scholar
12. Khaneghahi Abyaneh, H, Bahonar, A, Noori, N, Yazdanpanah, H, Shojaee Aliabadi, MH. Aflatoxin M1 in raw, pasteurized and UHT milk marketed in Iran. Food Addit Contam B 2019;12:236–44. https://doi.org/10.1080/19393210.2019.1611666.Search in Google Scholar PubMed
13. Nejad, 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;10:228. https://doi.org/10.24171/j.phrp.2019.10.4.05.Search in Google Scholar PubMed PubMed Central
14. Ahmadi, E. Potential public health risk due to consumption of contaminated bovine milk with aflatoxin M1 and Coxiella burnetii in the West of Iran. Int J Dairy Technol 2020;73:479–85. https://doi.org/10.1111/1471-0307.12687.Search in Google Scholar
16. Tadesse, S, Berhanu, T, Woldegiorgis, AZ. Aflatoxin M1 in milk and milk products marketed by local and industrial producers in Bishoftu town of Ethiopia. Food Control 2020;118:107386. https://doi.org/10.1016/j.foodcont.2020.107386.Search in Google Scholar
17. Tarannum, N, Nipa, MN, Das, S, Parveen, S. Aflatoxin M1 detection by ELISA in raw and processed milk in Bangladesh. Toxicol Rep 2020;7:1339–43. https://doi.org/10.1016/j.toxrep.2020.09.012.Search in Google Scholar PubMed PubMed Central
18. Mashak, Z, Sohi, HJ, Heshmati, A, Nejad, ASM. Assessment of AflatoxinM1 contamination in UHT flavored milk samples in Karaj, Iran. Iran J Pharm Res (IJPR) 2016;15:407.Search in Google Scholar
20. Shahbazi, Y, Nikousefat, Z, Karami, N. Occurrence, seasonal variation and risk assessment of exposure to aflatoxin M1 in Iranian traditional cheeses. Food Control 2017;79:356–62. https://doi.org/10.1016/j.foodcont.2017.04.021.Search in Google Scholar
21. Moslehi, R, Stagnar, C, Srinivasan, S, Radziszowski, P, Carpenter, DO. The possible role of arsenic and gene-arsenic interactions in susceptibility to breast cancer: a systematic review. Rev Environ Health 2021;36:523–34. https://doi.org/10.1515/reveh-2020-0080.Search in Google Scholar PubMed PubMed Central
22. Kua, KP, Lee, DSWH. Home environmental interventions for prevention of respiratory tract infections: a systematic review and meta-analysis. Rev Environ Health 2021;36:297–307. https://doi.org/10.1515/reveh-2020-0169.Search in Google Scholar PubMed
23. Mollayusefian, I, Ranaei, V, Pilevar, Z, Cabral-Pinto, MM, Rostami, A, Nematolahi, A, et al.. The concentration of aflatoxin M1 in raw and pasteurized milk: a worldwide systematic review and meta-analysis. Trends Food Sci Technol 2021;115:22–30. https://doi.org/10.1016/j.tifs.2021.06.033.Search in Google Scholar
24. Shalyari, N, Alinejad, A, Hashemi, AHG, RadFard, M, Dehghani, M. Health risk assessment of nitrate in groundwater resources of Iranshahr using Monte Carlo simulation and geographic information system (GIS). MethodsX 2019;6:1812–21. https://doi.org/10.1016/j.mex.2019.07.024.Search in Google Scholar PubMed PubMed Central
25. ATSDR. Public health assessment guidance manual Appendix G: calculating exposure doses (2005 Update). 2005.Search in Google Scholar
26. Bashiry, M, Javanmardi, F, Sadeghi, E, Shokri, S, Hossieni, H, Oliveira, CA, et al.. The prevalence of aflatoxins in commercial baby food products: a global systematic review, meta-analysis, and risk assessment study. Trends Food Sci Technol 2021;114:100–15. https://doi.org/10.1016/j.tifs.2021.05.014.Search in Google Scholar
27. Moodi, M, Salmani, F, Norozi, E, Zeinali, T. Predictors of functional dairy product consumption among Iranian consumers. Int Dairy J 2021;121:105061. https://doi.org/10.1016/j.idairyj.2021.105061.Search in Google Scholar
28. Abedi, A-S, Nasseri, E, Esfarjani, F, Mohammadi-Nasrabadi, F, Hashemi Moosavi, M, Hoseini, H. A systematic review and meta-analysis of lead and cadmium concentrations in cow milk in Iran and human health risk assessment. Environ Sci Pollut Control Ser 2020;27:10147–59. https://doi.org/10.1007/s11356-020-07989-w.Search in Google Scholar PubMed
29. Nazari, A, Nourouzi, H, Movahedi, M, Khaksarian, M. Measurement of aflatoxin M1 in raw and pasteurized cow milk samples by HPLC. Yafteh 2007;9:49–56.Search in Google Scholar
30. Mahmoudi, R, Zare, P. Total and M1 aflatoxins contamination in meat and milk buffalo were slaughtered in the Northwest of Iran. J Food Res 2014;24:8–11.Search in Google Scholar
31. Behfar, A, Nazari Khorasgani, Z, Alemzadeh, Z, Goudarzi, M, Ebrahimi, R, Tarhani, N. Determination of aflatoxin m1 levels in produced pasteurized milk in ahvaz city by using HPLC. Jundishapur J Nat Pharm Prod 2012;7:80–4.10.5812/jjnpp.4707Search in Google Scholar
32. Sefidgar, SAA, Mirzae, M, Assmar, M, Naddaf, SR. Aflatoxin M1 in pasteurized milk in Babol city, Mazandaran province, Iran. Iran J Public Health 2011;40:115–8.Search in Google Scholar
33. Gholampour, A, Khoushnevis, S, Hashemi, S. Aflatoxin M1 level in pasteurized and sterilized milk of Babol city. Tehran Univ Med J TUMS Publ 2008;65:20–4.Search in Google Scholar
34. Tomašević, I, Petrović, J, Jovetić, M, Raičević, S, Milojević, M, Miočinović, J. 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. https://doi.org/10.1016/j.foodcont.2015.03.017.Search in Google Scholar
35. Rahmani, J, Alipour, S, Miri, A, Fakhri, Y, Riahi, S-M, Keramati, H, et al.. The prevalence of aflatoxin M1 in milk of Middle East region: a systematic review, meta-analysis and probabilistic health risk assessment. Food Chem Toxicol 2018;118:653–66. https://doi.org/10.1016/j.fct.2018.06.016.Search in Google Scholar PubMed
36. Ismail, A, Akhtar, S, Levin, RE, Ismail, T, Riaz, M, Amir, M. Aflatoxin M1: prevalence and decontamination strategies in milk and milk products. Crit Rev Microbiol 2016;42:418–27. https://doi.org/10.3109/1040841x.2014.958051.Search in Google Scholar
37. Xiong, J, Zhang, X, Zhou, H, Lei, M, Liu, Y, Ye, C, et al.. Aflatoxin M1 in pasteurized, ESL and UHT milk products from central China during summer and winter seasons: prevalence and risk assessment of exposure in different age groups. Food Control 2021;125:107908. https://doi.org/10.1016/j.foodcont.2021.107908.Search in Google Scholar
38. Li, S, Min, L, Wang, P, Zhang, Y, Zheng, N, Wang, J. Occurrence of aflatoxin M1 in pasteurized and UHT milks in China in 2014–2015. Food Control 2017;78:94–9. https://doi.org/10.1016/j.foodcont.2017.02.042.Search in Google Scholar
39. Mannani, N, Tabarani, A, El Adlouni, C, Zinedine, A. Aflatoxin M1 in pasteurized and UHT milk marked in Morocco. Food Control 2021;124:107893. https://doi.org/10.1016/j.foodcont.2021.107893.Search in Google Scholar
40. Daou, R, Afif, C, Joubrane, K, Khabbaz, LR, Maroun, R, Ismail, A, et al.. Occurrence of aflatoxin M1 in raw, pasteurized, UHT cows’ milk, and dairy products in Lebanon. Food Control 2020;111:107055. https://doi.org/10.1016/j.foodcont.2019.107055.Search in Google Scholar
41. Lindahl, JF, Kagera, I, Grace, D. Aflatoxin M1 levels in different marketed milk products in Nairobi, Kenya. Mycotoxin Res 2018;34:289–95. https://doi.org/10.1007/s12550-018-0323-4.Search in Google Scholar PubMed PubMed Central
42. Sumon, AH, Islam, F, Mohanto, NC, Kathak, RR, Molla, NH, Rana, S, et al.. The presence of aflatoxin M1 in milk and milk products in Bangladesh. Toxins 2021;13:440. https://doi.org/10.3390/toxins13070440.Search in Google Scholar PubMed PubMed Central
43. Ahlberg, S, Grace, D, Kiarie, G, Kirino, Y, Lindahl, J. A risk assessment of aflatoxin M1 exposure in low and mid-income dairy consumers in Kenya. Toxins 2018;10:348. https://doi.org/10.3390/toxins10090348.Search in Google Scholar PubMed PubMed Central
44. Ertas, N, Gonulalan, Z, Yildirim, Y, Karadal, F. A survey of concentration of aflatoxin M1 in dairy products marketed in Turkey. Food Control 2011;22:1956–9. https://doi.org/10.1016/j.foodcont.2011.05.009.Search in Google Scholar
45. Hasheminya, S-M, Dehghannya, J. Strategies for decreasing aflatoxin in livestock feed and milk. Int Res J Appl Basic Sci 2013;4:1506–10.Search in Google Scholar
46. Hashemi, SMB, Amiri, MJ. A comparative adsorption study of aflatoxin B1 and aflatoxin G1 in almond butter fermented by Lactobacillus fermentum and Lactobacillus delbrueckii subsp. lactis. LWT 2020;128:109500. https://doi.org/10.1016/j.lwt.2020.109500.Search in Google Scholar
47. Govaris, A, Roussi, V, Koidis, P, Botsoglou, N. Distribution and stability of aflatoxin M1 during processing, ripening and storage of Telemes cheese. Food Addit Contam 2001;18:437–43. https://doi.org/10.1080/02652030010022700.Search in Google Scholar
48. Sohrabi, N, Gharahkoli, H. A seasonal study for determination of aflatoxin M1 level in dairy products in Iranshahr, Iran. Curr Med Mycol 2016;2:27. https://doi.org/10.18869/acadpub.cmm.2.3.27.Search in Google Scholar PubMed PubMed Central
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