<i>Aflatoxin</i> M1 (<i>Aspergillus parasiticus, flavus</i>) Occurrences in Milk and Milk Products and Its Possible Health Effects — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
<i>Aflatoxin</i> M1 (<i>Aspergillus parasiticus, flavus</i>) Occurrences in Milk and Milk Products and Its Possible Health Effects
Department of Human Nutrition, McGill University, Ste Anne-de-Bellevue, QC, Canada
,
Department of Human Nutrition, McGill University, Ste Anne-de-Bellevue, QC, Canada
,
Department of Animal Science, McGill University, Ste Anne-de-Bellevue, QC, Canada
1 Department of Human Nutrition, McGill University, Ste Anne-de-Bellevue, QC, Canada
2 Department of Human Nutrition, McGill University, Ste Anne-de-Bellevue, QC, Canada
3 Department of Animal Science, McGill University, Ste Anne-de-Bellevue, QC, Canada
Aflatoxin M1 (AFM1) occurrence in milk and milk products has been a major concern among food scientists over the past three decades owing to its possible health risk in humans. The well-documented AFM1 associated adverse health outcomes include hepatocarcinogens, mutagens genotoxins, mutagenicity, and teratogen. The paper reviews the occurrence of AFM1 in milk, milk products, and human milk in developing and developed countries, with its safety standards of regulation. The health associated risks with AFM1 are the important methods used in detecting and reducing AFM1 in milk and other milk products are presented.
Iheanacho, H., Dutton, M.F., Steenkamp, P.A., Steenkamp, L., Makun, H.A., Swart, A. and Mthombeni, J.Q. (2014) Real Time PCR of Nor~1 (aflD) Gene of Aflatoxin Producing Fungi and Its Correlative Quantization to Aflatoxin Levels in South African Compound Feeds. Journal of Microbiological Methods, 97, 63-67. https://doi.org/10.1016/j.mimet.2013.12.014
Njobeh, P.B., Dutton, M.F., Åberg, A.T. and Haggblo, P. (2012) Estimation of Multi-Mycotoxin Contamination in South African Compound Feeds. Toxins, 4, 836-848. https://doi.org/10.3390/toxins4100836
Redouane-Salah, S., Morgavi, D.P., Arhab, R., Messaï, A. and Boudra, H. (2015) Presence of Aflatoxin M1 in Raw, Reconstituted, and Powdered Milk Samples Collected in Algeria. Environmental Monitoring and Assessment, 187, Article No. 375. https://doi.org/10.1007/s10661-015-4627-y
Molina, A., Chavarría, G., Alfaro-Cascante, M., Leiva, A. and Granados-Chinchilla, F. (2019) Mycotoxins at the Start of the Food Chain in Costa Rica: Analysis of Six Fusarium Toxins and Ochratoxin A between 2013 and 2017 in Animal Feed and Aflatoxin M1 in Dairy Products. Toxins, 11, 312. https://doi.org/10.3390/toxins11060312
Yosef, T.A., Al-Julaifi, M.Z., Salah-El-Dein, W.M. and AL-Rizqi, A.M. (2013) Assessment of Aflatoxin M1 Residues in Raw Cow Milk at Al-Riyadh Area with Reference to Some Detoxification Applications. Life Science Journal, 10, 4365-4369.
Ghajarbeygi, P., Palizban, M., Mahmoudi, R., Khaniki G.J. and Pakbin, B. (2016) Aflatoxin M1 Contamination of Cow’s Raw Milk in Different Seasons from Qazvin Province, Iran. Journal of Biology Today’s World, 5, 173-176.
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, 714-718. https://doi.org/10.1016/j.foodcont.2013.06.009
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, 1653-1656. https://doi.org/10.1016/j.foodcont.2011.03.024
Picinin, L.C.A., et al. (2013) Influence of Climate Conditions on Aflatoxin M1 Contamination in Raw Milk from Minas Gerais State, Brazil. Food Control, 31, 419-424. https://doi.org/10.1016/j.foodcont.2012.10.024
Akbar, N., et al. (2019) Occurrence and Seasonal Variations of Aflatoxin M1 in Milk from Punjab, Pakistan. Toxins, 11, 574. https://doi.org/10.3390/toxins11100574
Iqbal, S.Z. and Asi, M.R. (2013) Assessment of Aflatoxin M1 in Milk and Milk Products from Punjab, Pakistan. Food Control, 30, 235-239. https://doi.org/10.1016/j.foodcont.2012.06.026
Moudgil, P., Bedi, J.S., Aulakh, R.S. and Gill, J.P.S. (2019) Antibiotic Residues and Mycotoxins in Raw Milk in Punjab (India): A Rising Concern for Food Safety. Journal of Food Science Technology, 56, 5146-5151. https://doi.org/10.1007/s13197-019-03963-8
Chalyan, T., et al. (2019) AFM1 Detection in Milk by Fab’ FunctionalizedSi3N4 Asymmetric Mach-Zehnder Interferometric Biosensors. Toxins, 11, 409. https://doi.org/10.3390/toxins11070409
World Health Organization. Some Traditional Herbal Medicines, Some Mycotoxins, Naphthalene and Styrene, I.A.F.R.O. Cancer 2002. https://monographs.iarc.fr/wp-content/uploads/2018/06/mono90.pdf
Rahimi, E., et al. (2010) Occurrence of Aflatoxin M1 in Raw Milk of Five Dairy Species in Ahvaz, Iran. Food Chemical Toxicology, 48, 129-131. https://doi.org/10.1016/j.fct.2009.09.028
Zheng, N., Wang, J.-Q., Han, R.-W., Zhen, Y.-P., Xu, X.-M. and Sun, P. (2013) Survey of Aflatoxin M1 in Raw Milk in the Five Provinces of China. Food Additives Contaminants: Part B, 6, 110-115. https://doi.org/10.1080/19393210.2012.763191
Ruangwises, N. and Ruangwises, S. (2010) Aflatoxin M1 Contamination in Raw Milk within the Central Region of Thailand. Bulletin of Environmental Contamination Toxicology, 85, 195-198. https://doi.org/10.1007/s00128-010-0056-3
(2006) Commission Regulation (EC) No 1881/2006 of 19 December 2006 Setting Maximum Levels for Certain Contaminants in Foodstuffs.
Van Egmond, H., and Egmond, H. (1989) Aflatoxinm1: Occurrence, Toxicity, Regulation. Elsevier Applied Science, Amsterdam.
Abdallah, M.F., Girgin, G. and Baydar, T. (2019) Mycotoxin Detection in Maize, Commercial Feed, and Raw Dairy Milk Samples from Assiut City, Egypt. Veterinary Sciences, 6, 57. https://doi.org/10.3390/vetsci6020057
Santini, A., et al. (2013) Aflatoxin M1 in Raw, UHT Milk and Dairy Products in Sicily (Italy). Food Additives Contaminants: Part B, 6, 181-186. https://doi.org/10.1080/19393210.2013.780186
Turkoglu, C. and Keyvan, E. (2019) Determination of Aflatoxin M1 and Ochratoxin A in Raw, Pasteurized and UHT Milk in Turkey. Acta Scientiae Veterinariae, 47, 1626. https://doi.org/10.22456/1679-9216.89667
U.S. Food and Drug Administration (2018) The Dangers of Raw Milk: Unpasteurized Milk Can Pose a Serious Health Risk. 2018. https://www.fda.gov/food/buy-store-serve-safe-food/dangers-raw-milk-unpasteurized-milk-can-pose-serious-health-risk
Al Zuheir, I.M. and Omar, J.A.W. (2012) Presence of Aflatoxin M1 in Raw Milk for Human Consumption in Palestinian. Journal of Science Technology, 9, 201-205.
Nile, S.H., Park, S.W. and Khobragade, C.N. (2016) Occurrence and Analysis of Aflatoxin M1 in Milk Produced by Indian Dairy Species. Food and Agricultural Immunology, 27, 358-366. https://doi.org/10.1080/09540105.2015.1104655
Guo, L., et al. (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
Ansari, F., Pourjafar, H. and Christensen, L. (2019) A Study on the Aflatoxin M1 Rate and Seasonal Variation in Pasteurized Cow Milk from Northwestern Iran. Environmental Monitoring, 191, Article No. 6. https://doi.org/10.1007/s10661-018-7141-1
Lindahl, J.F., Kagera, I. and Grace, D. (2018) Aflatoxin M1 Levels in Different Marketed Milk Products in Nairobi, Kenya. Mycotoxin Research, 34, 289-295. https://doi.org/10.1007/s12550-018-0323-4
Anyango, G., Mutua, F., Kagera, I., Andang’O, P., Grace, D. and Lindahl, J.F. (2018) A Survey of Aflatoxin M1 Contamination in Raw Milk Produced in Urban and Peri-Urban Areas of Kisumu County, Kenya. Infection Ecology, 8, Article ID: 1547094. https://doi.org/10.1080/20008686.2018.1547094
Tajkarimi, M., Aliabadi-Sh, F., Salah Nejad, A., Poursoltani, H., Motallebi, A.A. and Mahdavi, H. (2008) Aflatoxin M1 Contamination in Winter and Summer Milk in 14 States in Iran. Food Control, 19, 1033-1036. https://doi.org/10.1016/j.foodcont.2007.10.011
Sharifzadeh, A., et al. (2017) Aflatoxin M1 Contamination Levels in Cheeses Sold in Isfahan Province, Iran. Osong Public Health Research Perspectives, 8, 260-263. https://doi.org/10.24171/j.phrp.2017.8.4.05
Yahyaraeyat, R., Khosravi, A.R., Torabi, S. and Shokri, H. (2017) Evaluation of the Contamination of Aflatoxin M1 Level in Raw Milk Samples by ELISA Method in Yazd Province. Journal of Veterinary Research, 72, 311-319.
Sirma, A., et al. (2018) The Impacts of Aflatoxin Standards on Health and Nutrition in Sub-Saharan Africa: The Case of Kenya. Global Food Security, 18, 57-61. https://doi.org/10.1016/j.gfs.2018.08.001
Kuboka, M.M., et al. (2019) Occurrence of Aflatoxin M1 in Raw Milk Traded in Peri-Urban Nairobi, and the Effect of Boiling and Fermentation. Infection Ecology Epidemiology, 9, Article ID: 1625703. https://doi.org/10.1080/20008686.2019.1625703
Tsakiris, I.N., et al. (2013) Risk Assessment Scenarios of Children’ S Exposure to Aflatoxin M1 Residues in Different Milk Types from the Greek Market. Food Chemical Toxicology, 56, 261-265. https://doi.org/10.1016/j.fct.2013.02.024
Cano-Sancho, G., et al. (2010) Occurrence of Aflatoxin M1 and Exposure Assessment in Catalonia (Spain). Revistaiberoamericana de Micología, 27, 130-135. https://doi.org/10.1016/j.riam.2010.05.003
Lynda, E.C., Chinwe, A.S. and Ekeanyanwu, R.C. (2020) Levels of Aflatoxin M1 and Selected Heavy Metals (Pb, Cd, Cr, Cu, Zn, Fe, As, and Hg) in the Breast Milk of Lactating Mothers in South Eastern, Nigeria. Food Control, 112, Article ID: 107150. https://doi.org/10.1016/j.foodcont.2020.107150
Ortiz, J., et al. (2018) Multiple Mycotoxin Exposure of Infants and Young Children via Breastfeeding and Complementary/Weaning Foods Consumption in Ecuadorian Highlands. Food Chemical Toxicology, 118, 541-548. https://doi.org/10.1016/j.fct.2018.06.008
Radonić, J.R., et al. (2017) Occurrence of Aflatoxin M1 in Human Milk Samples in Vojvodina, Serbia: Estimation of Average Daily Intake by Babies. Journal of Environmental Science Health, Part B, 52, 59-63. https://doi.org/10.1080/03601234.2016.1229454
Tomerak, R.H., Shaban, H.H., Khalafallah, O.A. and El Shazly, M.N. (2011) Assessment of Exposure of Egyptian Infants to Aflatoxin M1 through Breast Milk. The Journal of the Egyptian Public Health Association, 86, 51-55. https://doi.org/10.1097/01.EPX.0000399138.90797.40
Bogalho, F., et al. (2018) Exposure Assessment of Portuguese Infants to Aflatoxin M1 in Breast Milk and Maternal Social-Demographical and Food Consumption Determinants. Food Control, 90, 140-145. https://doi.org/10.1016/j.foodcont.2018.02.043
Fakhri, Y., et al. (2019) Aflatoxin M1 in Human Breast Milk: A Global Systematic Review, Meta-Analysis, and Risk Assessment Study (Monte Carlo Simulation). Trends in Food Science & Technology, 88, 333-342. https://doi.org/10.1016/j.tifs.2019.03.013
Akhtar, S., et al. (2017) Determination of Aflatoxin M1 and Heavy Metals in Infant Formula Milk Brands Available in Pakistani Markets. Korean Journal for Food Science of Animal Resources, 37, 79-86. https://doi.org/10.5851/kosfa.2017.37.1.79
Tonon, K.M., Savi, G.D. and Scussel, V.M. (2018) Application of A LC-MS/MS Method for Multi-Mycotoxin Analysis in Infant Formula and Milk-Based Products for Young Children Commercialized in Southern Brazil. Journal of Environmental Science and Health, Part B, 53, 685-691. https://doi.org/10.1080/03601234.2018.1474560
Ul Hassan, Z., Al Thani, R., Atia, F.A., Al Meer, S., Migheli, Q. and Jaoua, S. (2018) Co-Occurrence of Mycotoxins in Commercial Formula Milk and Cereal-Based Baby Food on the Qatar Market. Food Additives & Contaminant: Part B, 11, 191-197. https://doi.org/10.1080/19393210.2018.1437785
Gunbeaj, E.E.M., et al. (2018) Effect of Storage on the Level of Aflatoxin M1 in Milk and Other Dairy Products Sold at Tripoli Province, Libya. Journal of Pure Applied Microbiology, 12, 1959-1965. https://doi.org/10.22207/JPAM.12.4.32
Iqbal, S.Z., Jinapa, S., Pirouz, A.A. and Ahmad Faizala, A.R. (2015) Aflatoxin M1 in Milk and Dairy Products, Occurrence and Recent Challenges: A Review. Trends in Food Science & Technology, 46, 110-119. https://doi.org/10.1016/j.tifs.2015.08.005
Milicevic, D., Jankovic, S., Muric, K., Petrovic, Z., Petronijevic, R., Raseta, M. and Djinovic-Stojanovic, J. (2019) Safety of Milk and Whey from Zlatibor Region in Relation to Aflatoxin M1 Contamination: A Seasonal Study. IOP Conference Series: Earth and Environmental Science, 333, Article ID: 012077. https://doi.org/10.1088/1755-1315/333/1/012077
Škrbić, B., Antić, I. and Živanćev, J. (2015) Presence of Aflatoxin M1 in White and Hard Cheese Samples from Serbia. Food Control, 50, 111-117. https://doi.org/10.1016/j.foodcont.2014.08.031
Fernandes, A.M., et al. (2012) Distribution and Stability of Aflatoxin M1 during Processing and Storage of Minas Frescal Cheese. Food Control, 24, 104-108. https://doi.org/10.1016/j.foodcont.2011.09.010
Cavallarin, L., et al. (2014) Transfer of Aflatoxin M1 from Milk to Ripened Cheese in Three Italian Traditional Production Methods. Food Control, 38, 174-177. https://doi.org/10.1016/j.foodcont.2013.10.008
Iha, M.H., et al. (2013) Aflatoxin M1 in Milk and Distribution and Stability of Aflatoxin M1 during Production and Storage of Yoghurt and Cheese. Food Control, 29, 1-6. https://doi.org/10.1016/j.foodcont.2012.05.058
ChavarríA, G., et al. (2017) Distribution, Stability, and Protein Interactions of Aflatoxin M1 in Fresh Cheese. Food Control, 73, 581-586. https://doi.org/10.1016/j.foodcont.2016.09.005
Cattaneo, T.M.P., et al. (2013) Behavior of Aflatoxin M1 in Dairy Wastes Subjected to Different Technological Treatments: Ricotta Cheese Production, Ultrafiltration and Spray-Drying. Food Control, 32, 77-82. https://doi.org/10.1016/j.foodcont.2012.11.007
Movassaghghazani, M. andGhorbiani, M. (2017) Incidence of Aflatoxin M1 in Human and Cow Milk in Kashan, Iran. Journal of Food Quality Hazards Control, 4, 99-102.
Joint FAO/WHO Expert Committee on Food Additives (53rd: 1999: Rome, Italy) & World Health Organization (2000) Evaluation of Certain Food Additives and Contaminants: Fifty-Third Report of the Joint FAO/WHO Expert Committee on Food Additives. World Health Organization. https://apps.who.int/iris/handle/10665/42378
Daou, R., et al. (2020) Occurrence of Aflatoxin M1 in Raw, Pasteurized, UHT Cows’ Milk, and Dairy Products in Lebanon. Food Control, 111, Article ID: 107055. https://doi.org/10.1016/j.foodcont.2019.107055
Serraino, A., et al. (2019) Occurrence of Aflatoxin M1 in Raw Milk Marketed in Italy: Exposure Assessment and Risk Characterization. Frontiers in Microbiology, 10, 2516. https://doi.org/10.3389/fmicb.2019.02516
Gao, Y., et al. (2016) Aflatoxin M1 Cytotoxicity against Human Intestinal Caco-2 Cells Is Enhanced in the Presence of Other Mycotoxins. Food Chemical Toxicology, 96, 79-89. https://doi.org/10.1016/j.fct.2016.07.019
Pardakhti, A. and Maleki, S. (2019) Risk Assessment of Aflatoxin M1 Contamination of Milk in Iran. International Journal of Environmental Research, 13, 265-271. https://doi.org/10.1007/s41742-019-00172-1
Daou, R., et al. (2020) Occurrence of Aflatoxin M1 in Raw, Pasteurized, UHT Cows’ Milk, and Dairy Products in Lebanon. Food Control, 111, Article ID: 107055. https://doi.org/10.1016/j.foodcont.2019.107055
Nguyen, T., Flint, S. and Palmer, J. (2019) Control of Aflatoxin M1 in Milk by Novel Methods: A Review. Food Chemistry, 311, Article ID: 125984. https://doi.org/10.1016/j.foodchem.2019.125984
Corassin, C.H., et al. (2013) Efficiency of Saccharomyces Cerevisiae and Lactic Acid Bacteria Strains to Bind Aflatoxin M1 in UHT Skim Milk. Food Control, 31, 80-83. https://doi.org/10.1016/j.foodcont.2012.09.033
Ismail, A., et al. (2017) Effect of Different Microbial Concentrations on Binding of Aflatoxin M1 and Stability Testing. Food Control, 73, 492-496. https://doi.org/10.1016/j.foodcont.2016.08.040
Abdelmotilib, N.M., et al. (2018) Aflatoxin M1 Reduction in Milk by a Novel Combination of Probiotic Bacterial and Yeast Strains. European Journal of Nutrition Food Safety, 8, 83-99. https://doi.org/10.9734/EJNFS/2018/39486
Kuharić, Ž., et al. (2018) Removing Aflatoxin M1 from Milk with Native Lactic Acid Bacteria, Centrifugation, and Filtration. Archives of Industrial Hygiene and Toxicology, 69, 334-339. https://doi.org/10.2478/aiht-2018-69-3160
Shi, H., et al. (2017) Reduction of Aflatoxin in Corn by High Voltage Atmospheric Cold Plasma. Food Bioprocess Technology, 10, 1042-1052. https://doi.org/10.1007/s11947-017-1873-8
Škrbić, B., et al. (2014) Levels of Aflatoxin M1 in Different Types of Milk Collected in Serbia: Assessment of Human and Animal Exposure. Food Control, 40, 113-119. https://doi.org/10.1016/j.foodcont.2013.11.039
(2001) Codex Alimentarius Commission 33rd Session, H., Netherlands. Compliance Policy Guides. FDA, Comments Submitted on the Draft Maximum Level for Aflatoxin M1 in Milk. Codex Committee on Food Additives and Contaminants, 219. http://www.fao.org/tempref/codex/Reports/Alinorm01/al01_12e.pdf
(2004) Commission, E. Commission Regulation (EC) No. 683/2004 of 13 April 2004 Amending Regulation (EC) No 4662001 As Regards Aflatoxins and Ochratoxin A in Foods for Infants and Young Children.
Bahrami, R., Shahbazi, Y. and Nikousefat, Z. (2016) Aflatoxinm1 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
Londoño, V.A.G., et al. (2013) Aflatoxin M1 Survey on Randomly Collected Milk Powder Commercialized in Argentina and Brazil. Food Control, 34, 752-755. https://doi.org/10.1016/j.foodcont.2013.06.030
Sadia, A., et al. (2012) A Survey of Aflatoxin M1 in Milk and Sweets of Punjab, Pakistan. Food Control, 26, 235-240. https://doi.org/10.1016/j.foodcont.2012.01.055
Kocasari, F.S., Tasci, F. and Mor, F. (2012) Survey of Aflatoxin M1 in Milk and Dairy Products Consumed in Burdur, Turkey. International Journal of Dairy Technology, 65, 365-371. https://doi.org/10.1111/j.1471-0307.2012.00841.x
FDA (1996) U., CPG Sec 527.400 Whole Milk, Low Fat Milk, Skim Milk-Aflatoxin M1 (CPG 7106.210). FDA Compliance Policy Guides. FDA, Washington DC, 219. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cpg-sec-527400-whole-milk-lowfat-milk-skim-milk-aflatoxin-m1
Han, R., et al. (2013) Survey of Aflatoxin in Dairy Cow Feed and Raw Milk in China. Food Control, 34, 35-39. https://doi.org/10.1016/j.foodcont.2013.04.008
Iha, M.H., et al. (2011) Occurrence of Aflatoxin M1 in Dairy Products in Brazil. Food Control, 22, 1971-1974. https://doi.org/10.1016/j.foodcont.2011.05.013