Welcome to International Network for Natural Sciences | INNSpub

Occurence of aflatoxin M1 in Northern Africa: A short review

Research Paper | February 1, 2018

| Download 21

Redouane-Salah Sara, Messaï Ahmed, Abdeldjelil M-Cherif

Key Words:

Int. J. Biosci.12( 2), 63-74, February 2018

DOI: http://dx.doi.org/10.12692/ijb/12.2.63-74


IJB 2018 [Generate Certificate]


Moldy feed toxicosis was recognized as a serious livestock problem in the 1950’s. Mycotoxins are toxic metabolites synthesized by some naturally occurring fungi under suitable physical, chemical and biological factors. The Food and Agriculture Organization of the United Nations (FAO) estimated that approximately 25% of the cereals produced in the world are contaminated by mycotoxins. The aflatoxins constitute a group of fungal metabolites that have varied toxic properties. Among 17 aflatoxins isolated and identified, only 4 of them are well known and studied extensively ; B1, B2, G1 and G2. Aflatoxin B1 ingested by lactating animals is biotransformed in the liver to a monohydroxylated metabolite, aflatoxin M1 (AFM1), which is a toxic molecule excreted in the milk. Higher analytical costs of AFM1 are one of the reported reasons for unavailability of surveillance data in the majority of developing countries. In this review, occurrence of AFM1 in milk and milk products in northern Africa, as well as its metabolisme, properties and analytical methods are summarised.


Copyright © 2018
By Authors and International Network for
Natural Sciences (INNSPUB)
This article is published under the terms of the Creative
Commons Attribution Liscense 4.0

Occurence of aflatoxin M1 in Northern Africa: A short review

Abbès S, Ben Salah-Abbès J, Bouraouia Y, Oueslatia S, Oueslatia R. 2012. Natural occurrence of aflatoxins (B1 and M1) in feed, plasma and raw milk of lactating dairy cows in Beja, Tunisia, using ELISA. Food Additives and Contaminants : Part B5(1), 11–15. http://dx.doi.org/10.1080/19393210.2011.640756.

Agag BI. 2004. Mycotoxins In Foods And Feeds : 1-Aflatoxins. Assiut University Bulletin for Environmental Researches 7 (1), 173-206.

Aidoo KE, Mohamed SM, Candlish AA, Tester RF, Elgerbi AM. 2011. Occurrence of Fungi and Mycotoxins in Some Commercial Baby Foods in North Africa. Food and Nutrition Sciences 2, 751-758. http://dx.doi.org/10.4236/fns.2011.27103.

Alshannaq A, Yu YH. 2017. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food. International Journal of Environmental Research and Public Health 14, 632. http://dx.doi.org/10.3390/ijerph14060632.

Appell M, Mueller A. 2016. Mycotoxin analysis using imprinted materials technology: Recent developments. Journal of AOAC International 99, 861–864. http://dx.doi.org/10.5740/jaoacint.16-0113.

Applebaum RS, Marth EH. 1982. Use of sulfite or bentonite to eliminate aflatoxin M1 from naturally contaminated raw milk. Zeitschrift Fur Lebensmittel-Untersuchung Und -Forschung 174, 303–305. https://doi.org/10.1007/BF01042964.

Ardic M, Atasever M, Adiguzel G, Atasever M, Karakaya Y, Unsal C, Durmaz H. 2008. A Survey on the Presence of Aflatoxin M1 in Urfa Cheese. International Journal of Food Safety 10, 92-96.

Beltran E, Ibañez M, Sancho JV, Cortés MA, Yusa V, Hernández F. 2011. UHPLC-MS/Ms highly sensitive determination of aflatoxin, the aflatoxin metabolite M1 and ochratoxin A in baby food and milk. Food Chemistry 126(2), 737–744. https://doi.org/10.1016/j.foodchem.2010.11.056.

Bhatnagar D, Yu J, Ehrlich KC. 2002. Toxins of filamentous fungi. Chemical Immunololy 81, 167–206.

Bilandzic N, Varenina I, Solomun B. 2010. Aflatoxin M1 in raw milk in Croatia. Food Control 21 (9), 1279–1281. https://doi.org/10.1016/j.foodcont.2010.03.003.

Bram Van Der G, Sabine S, Heidi D, Edwin S, Gerben B, Ton Van O, Kees K. 2003. Biosensors and multiple mycotoxin analysis. Food Control 14 (4), 251–254. https://doi.org/10.1016/S0956-7135(03)00008-2.

Busby WF, Wogan GN. 1985. Chemical Carcinogens, Ed. Searle, G. (American Chemical Society, Washington, DC), 2nd Ed., 945-1136.

Campagnoli A, Cheli F, Savoini G, Crotti A, Pastori AG, Dell’Orto V. 2009. Application of an electronic nose to detection of aflatoxins in corn. Veterinary Research Communications 33(1), 273–275. http://dx.doi.org/10.1007/s11259-009-9305-5.

CAST, Council for Agric. Sci. and Technol. 1989. “Mycotoxins economic and health risks.” Task force report 116, 1989.

Cavaliere C, Foglia P, Pastorini E, Samperi R, Lagana A. 2006. Liquid chromatography/tandem mass spectrometric confirmatory method for determining aflatoxin M1 in cow milk-comparison between electrospray and atmospheric pressure photoionization sources. Journal of Chromatography A 1101(12), 69–78. http://dx.doi.org/10.1016/j.chroma.2005.09.060.

Chun HS, Choi EH, Chang HJ, Choi SW, Eremin SA. 2009. A fluorescence polarization immunoassay for the detection of zearalenone in corn. Analytica Chimica Acta 639, 83–89. https://doi.org/10.1016/j.aca.2009.02.048.

Codex Alimentarius Commission. 2001. Comments submitted on the draft maximum level for Aflatoxin M1 in milk. Codex committee on food additives and contaminants 33rd session. The Netherlands: Hague.

De Girolamo A, Lippolis V, Nordkvist E, Visconti A. 2009. Rapid and non-invasive analysis of deoxynivalenol in durum and common wheat by Fourier-Transform Near Infrared (FT-NIR) spectroscopy. Food Additives & Contaminants. Part A 26, 907–917. https://doi.org/10.1080/02652030902788946.

Devero A. 1999. Aflatoxins: The effects on human and animal health. Biol, 4900; Fall, 1999.

Dhanasekaran D, Shanmugapriya S, Thajuddin N, Panneerselvam A. 2011. Aflatoxins and Aflatoxicosis in Human and Animals, Aflatoxins – Biochemistry and Molecular Biology, Dr. Ramon G. Guevara-Gonzalez (Ed.), ISBN: 978-953-307-395-8.

Diniz Andrade P, Laine Gomez da Silva J, Dutra Caldas E. 2013. Simultaneous analysis of afaltoxins B1, B2, G1, G2, M1 and ochratoxin A in brest milk by highperformance liquid chromatography/fluorescende after liquid-liquid extraction with low temperature purification (LLE-LTP). Journal of Chromatography A 1304, 61–68. https://doi.org/10.1016/j.chroma.2013.06.049.

Ehrlich KC, Wei Q, Brown RL, Bhatnagar D. 2011. Inverse Correlation of Ability to Produce Aflatoxin and Aspergillus Colonization of Maize Seed. Food and Nutrition Sciences 2, 486-489. http://dx.doi.org/10.4236/fns.2011.25070.

Elgerbi AM, Aidoo KE, Candlish AAG, Tester RF. 2004. Occurrence of aflatoxin M-1 in randomly selected North African milk and cheese samples. Food Additives & Contaminants 21(6), 592–597. http://dx.doi.org/10.1080/02652030410001687690.

Elgerbi AM. 2005. Studies on Occurrence of Aflatoxins M1 in Milk Products and Effect of Lactobacilli and Related Genera on Toxin,” Ph D Thesis, Glasgow Caledonian University, Glasgow, 2005.

ElMarnissi B, Belkhou R, Morgavi DP, Bennani L, Boudra H. 2012. Occurrence of aflatoxin M1 in raw milk collected from traditional dairies in Morocco. Food and Chemical Toxicology 50(8), 2819–2821. http://dx.doi.org/10.1016/j.fct.2012.05.031.

Elzupir AO, Elhussein AM. 2010. Determination of aflatoxin M1 in dairy cattle milk in Khartoum State, Sudan. Food Control 21, 945–946. https://doi.org/10.1016/j.foodcont.2009.11.013.

Fallah 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.

FDA. 2005. Sec. 527.400 Whole milk, low fat milk, skim milk–aflatoxin M1 (CPG 7106.10). Available from Accessed20 Apr 2009. www.fda.gov/ora/compliance_ref/cpg/cpgfod/cpg527-400.html.

Firmin S, Morgavi DP, Yiannikouris A, Boudra H. 2011. Effectiveness of modified yeast cell wall extracts to reduce aflatoxin B1 absorption in dairy ewes. Journal of Dairy Science 94, 5611–5619. http://dx.doi.org/10.3168/jds.2011-4446.

Gallot J, Abenhaïm L, Guillou M. 2000. Guide de bonnes pratiques d’hygiène dans l’industrie de semoulerie de blé dur. Édition: Les journaux officiaux, 105-108.

Galtier P, Loiseau N, Oswald IP, Puel O. 2005. Toxicology of mycotoxins, hazards and risks in human and animal food. Bulletin de l’Académie Vétérinaire de France, Tome 159 – N°1.

Ghareeb K, Elmalt LM, Awad WA, Böhm J. 2013. Prevalence of aflatoxin M1 in raw milk produced in tropical state (Qena, Egypt) and imported milk powder. Journal of Veterinary and Animal Sciences 3(12), 1–4.

Giovati L, Magliani W, Ciociola T, Santinoli C, Conti S, Polonelli L. 2015. AFM1 in Milk: Physical, Biological, and Prophylactic Methods to Mitigate Contamination. Toxins 7, 4330-4349. http://dx.doi.org/10.3390/toxins7104330.

Gonçalves BL, Gonçalves JL, Rosim RE, Cappato LP, Cruz AG, Oliveira CAF, Corassin CH. 2017. Effects of different sources of Saccharomyces cerevisiae biomass on milk production, composition, and aflatoxin M1 excretion in milk from dairy cows fed aflatoxin B1. Journal of Dairy Science 100, 1–8. https://doi.org/10.3168/jds.2016-12215.

Groopman JD, Donahuet PR, Zhu J, Chen J, Wogant GN. 1985. Aflatoxin metabolism in humans: Detection of metabolites and nucleic acid adducts in urine by affinity chromatography. Proceedings of the National Academy of Sciences of the USA 82, 6492-6496.

International Agency for Research on Cancer (IARC). 2002. Aflatoxins. IARC Monograph on the Evaluation of Carcinogenic Risks to Humans. 82, IARC, World Health Organization, Lyon, 171.

Ismail A, Akhtar S, Levin RE, Ismail T, Riaz M, Amir M. 2015. Aflatoxin M1: Prevalence and decontamination strategies in milk and milk products. Critical Reviews in Microbiology, Early Online: 1–10. http://dx.doi.org/10.3109/1040841X.2014.958051.

Istamboulié G, Paniel N, Zara L, Granados LR,Barthelmebs L, Noguer T. 2016. Development of an impedimetric aptasensor for the determination of aflatoxin M1 in milk. Talanta 146, 464–469. https://doi.org/10.1016/j.talanta.2015.09.012.

Jiang W, Wang Z, Nolke G, Zhang J, Niu L, Shen J. 2013. Simultaneous determination of aflatoxin B1 and aflatoxin M1 in food matrices by enzyme linked immunosorbent assay. Food Analytical Methods 6, 767–774. https://doi.org/10.1007/s12161-012-9484-5.

Josephs RD, Ulberth F, Van Egmond HP, Emons H. 2005. Aflatoxin M1 in milk powders: Processing, homogeneity and stability testing of certified reference materials. Food Additives & Contaminants 22(9), 864–874. http://dx.doi.org/10.1080/02652030500166537

Kalla A. 2015. Isolation and Identification of Specific Pathogens, Presence of Antibiotics, Aflatoxins, Pesticide Residues and Industrial Contaminants in Supply Chain of Milk in Selected Coastal Districts of Andhra Pradesh. Advances in Bioscience and Biotechnology 6, 330-344. http://dx.doi.org/10.4236/abb.2015.64032.

Klich MA, Mullaney EJ, Daly CB, Cary JW. 2000. Molecular and physiological aspects of aflatoxin and sterigmatocystin biosynthesis by Aspergillus tamarii and A. ochraceoroseus. Applied Microbiology and Biotechnology 53, 605–609. https://doi.org/10.1007/s002530051664.

Kos J, Jani´c Hajnal E, Jaji´c I, Krstovi´c S, Mastilovi´c J, Šari´c B, Jovanov P. 2016. Comparison of ELISA, HPLC-FLD and HPLC-MS/MS methods for determination of aflatoxin M1 in natural contaminated milk samples. Acta Chimica Slovenica 63, 747–756. http://dx.doi.org/10.17344/acsi.2016.2451.

Lafont P, Siriwardana M, Lafont J. 1989. Genotoxicity of hydroxy-aflatoxins M1 and M4. Microbiology Alimentarius Nutrition 7, 1-8.

Laura A, Cristina G, Claudio B. 2016. Mycotoxin detection. Current Opinion in Biotechnology 37, 120–126. https://doi.org/10.1016/j.copbio.2015.11.005.

Logrieco A, Arrigan DWM, Brengel-Pesce K, Siciliano P, Tothill I. 2005. DNA arrays, electronic noses and tongues, biosensors and receptors for rapid detection of toxigenic fungi and mycotoxins: A review. Food Additives & Contaminants 22, 335–344. https://doi.org/10.1080/02652030500070176.

Maragos CM, Appell M. 2007. Capillary electrophoresis of themycotoxin zearalenone using cyclodextrin-enhanced fluorescence. Journal of Chromatography A 1143(1-2), 252–257. https://doi.org/10.1016/j.chroma.2006.12.085

Maragos CM, Busman M. 2010. Rapid and advanced tools for mycotoxin analysis: A review. Food Additives & Contaminants. Part A 27, 688–700. https://doi.org/10.1080/19440040903515934.

Mohammadi H, Alizadeh M, Bari MR, Khosrowshahi A, Tadjik H. 2009. Optimization of the Process Variables for Minimizing of the Aflatoxin M1 Content in Iranian White Brine Cheese. Journal of Agricultural Science and Technology 11, 181-190.

Mohammadi H. 2011. A Review of Aflatoxin M1, Milk, and Milk Products, Aflatoxins – Biochemistry and Molecular Biology, Dr. Ramon G. Guevara-Gonzalez (Ed.), ISBN: 978-953-307-395-8, In Tech, Available from: www.intechopen.com/books/aflatoxins-biochemistry-and-molecular-biology/a-review-of-aflatoxin-m1-milk-and-milk-products.

Moss OM. 2002. Risk assessment for aflatoxins in foodstuffs, International Biodeterioration & Biodegradation 50, 137-142. https://doi.org/10.1016/S0964-8305(02)00078-1.

Motawee MM, Bauer J, McMahon DJ. 2009. Survey of Aflatoxin M 1 in cow, goat, buffalo and camel milks in Ismailia-Egypt. Bulletin of Environmental Contamination and Toxicology 83, 766–769. https://doi.org/10.1007/s00128-009-9840-3.

Neal GE, Eaton DL, Judah DJ, Verma A. 1998. Metabolism and toxicity of aflatoxins M1 and B1 in human-derived in vitro systems. Toxicology and Applied Parmacology 151(1), 152-158. https://doi.org/10.1006/taap.1998.8440.

Olsson J, Börjesson T, Lundstedt T, Schnürer J. 2002. Detection and quantification of ochratoxin A and deoxynivalenol in barley grains by GC-MS and electronic nose. International Journal of Food Microbiology 72, 203–214. https://doi.org/10.1016/S0168-1605(01)00685-7.

Orata F. 2016. Derivatization reactions and reagents for gas chromatography analysis. In Advanced Gas Chromatography. Progress in Agricultural, Biomedical and Industrial Applications, 1st Ed.; Mohd, M.A., Ed ; InTech: Rijeka, Croatia, 2012, 83–108.

Oyedele OA, Ezekiel CN, Sulyok M, Adetunji, MC, Warth B, Atanda OO, Krska R. 2017. Mycotoxin risk assessment for consumers of groundnut in domestic markets in Nigeria. International Journal of Food Microbiology 251, 24–32. https://doi.org/10.1016/j.ijfoodmicro.2017.03.020.

Patterson DSP, Roberts BA. 1970. The formation of aflatoxin B2a and G2a and their degradation products during the in vitro detoxification of aflatoxin by livers of certain avian and mammalian species. Food and cosmetics Toxicology 8, 527-538. https://doi.org/10.1016/S0015-6264(70)80041-4

Peng X, Bai S, Ding X, Zhang K. 2017. Pathological Impairment, Cell Cycle Arrest and Apoptosis of Thymus and Bursa of Fabricius Induced by Aflatoxin-Contaminated Corn in Broilers. International Journal of Environmental Research and Public Health 14, 77. http://dx.doi.org/10.3390/ijerph14010077.

Pérez E, Martínez-Peinado P, Marco F, Gras L, Sempere, JM, Mora J, Grindlay G. 2017. Determination of aflatoxin M1 in milk samples by means of an inductively coupled plasma mass spectrometry-based immunoassay. Food Chemistry 230, 721–727. https://doi.org/10.1016/j.foodchem.2017.03.078.

Phillips TD, Afriyie-Gyawu E, Williams J, Huebner H, Ankrah NA, Ofori-Adjei D, Jolly P, Johnson N, Taylor J,. 2008. Reducing human exposure to aflatoxin through the use of clay: A review. Food Additives & Contaminants. Part A 25, 134–145. https://doi.org/10.1080/02652030701567467.

Redouane-Salah S, Morgavi DP, Arhab R, Messaï A, Boudra H. 2015. Presence of aflatoxin M1 in raw, reconstituted, and powdered milk samples collected in Algeria. Environmental Monitoring and Assessment 187, 375. http://dx.doi.org/10.1007/s10661-015-4627-y.

Reid CX, Sparks DL, Williams WP, Brown AE. 2016. Single Corn Kernel Aflatoxin B1 Extraction and Analysis Method. Natural Resources 7, 405-410. http://dx.doi.org/10.4236/nr.2016.77035.

Reiter E, Zentek J, Razzazi E. 2009. Review of sample preparation and methods used for the analysis of aflatoxins in food and feed. Molecular Nutrition Food Research 53, 508–524. http://dx.doi.org/10.1002/mnfr.200800145.

Repussard C, Zbib N, Tardieu D, Guerre P. 2013.Les champignons endophytes du genre Neotyphodium et leurs toxines: généralités et problématique française. Revue de Médecine Vétérinaire 164 (12), 583-606.

Rice LG, Ross PF. 1994. Methods for Detection and Quantitation of Fumonisins in Corn, Cereal Products and Animal Excreta. Journal of Food Protection 57 (6), 536-540. https://doi.org/10.4315/0362-028X-57.6.536.

Riley RT, Pestka J. 2005. Mycotoxins: Metabolism, mechanisms and biochemical markers. In The Mycotoxin Blue Book. Vol. 1. 1st ed. D. E. Diaz, ed. University Press, Nottingham, UK, 279–294.

Salem DA. 2002. Natural occurrence of aflatoxins in feedstuffs and milk of dairy farms in Assiut province. Egypt. Wien Tierarztl Monatsschr 89, 86–91.

Sharma A, Catanante G, Hayat A, Istamboulié G, Ben Rejeb I, Bhand S, Marty JL. 2016. Development of structure switching aptamer assay for detection of aflatoxin M1 in milk sample. Talanta 158, 35–41. https://doi.org/10.1016/j.talanta.2016.05.043.

Sheng YJ, Eremin S, Mi TJ, Zhang SX, Shen JZ, Wang ZH. 2014. The development of a fluorescence polarization immunoassay for aflatoxin detection. Biomedical and Environmental Sciences 27, 126–129. https://doi.org/10.3967/bes2014.027.

Shephard GS. 2008. Determination of mycotoxins in human foods. Chemical Society Reviews 37, 2468–2477. https://doi.org/10.1039/B713084H

Shephard GS. 2016. Current Status of Mycotoxin Analysis: A Critical Review. Journal of AOAC International 99, 842–848. https://doi.org/10.5740/jaoacint.16-0111.

Sieger M, Kos G, Sulyok M, Godejohann M, Krska R, Mizaikoff B. 2017. Portable Infrared Laser Spectroscopy for On-site Mycotoxin Analysis. Scientific Reports 7, 44028. (2017). http://dx.doi.org/10.1038/srep44028

Stoloff L. 1980. Aflatoxin M in perspective. Journal of food protection 43 (3), 226-230. https://doi.org/10.4315/0362-028X-43.3.226.

Suliman SE, Abdalla MA. 2013. Presence of Aflatoxin M1 in Dairy Cattle Milk in Khatorum State-Sudan. International Journal of Scientific & Technology Research 2, 10-12.

Sweeney MJ, Dobson ADW. 1998. Mycotoxin Production by Aspergillus, Fusarium and Penicillium Species. International Journal of Food Microbiology 43(3), 141-158. http://dx.doi.org/:10.1016/S0168-1605(98)00112-3.

Vdovenko MM, Lu CC, Yu FY, Sakharov IY. 2014. Development of ultrasensitive direct chemiluminescent enzyme immunoassay for determination of aflatoxin M1 in milk. Food Chemistry 158, 310–314. https://doi.org/10.1016/j.foodchem.2014.02.128.

Visconti A, Lattanzio VMT, Pascale M, Haidukowski M. 2005. Analysis of T-2 and HT-2 toxins in cereal grains by immunoaffinity clean-up and liquid chromatography with fluorescence detection. Journal of Chromatography A 1075, 151–158. https://doi.org/10.1016/j.chroma.2005.04.009.

World Health Organization (WHO). 1979. Environmental Health Criteria, Safety evaluation of certain food additives, 1-127.

Yao H, Hruska Z, Diana Di Mavungu J. 2015. Developments in detection and determination of aflatoxins. World Mycotoxin Journal 8, 181–191. https://doi.org/10.3920/WMJ2014.1797.

Yiannikouris A, Jouany JP. 2002. Les mycotoxines dans les aliments des ruminants, leur devenir et leurs effets chez l’animal. INRA Production Animale 15 (1), 3-16.

Zbib N, Repussard C, Tardieu D, Guerre P. 2014. Toxicité des mycotoxines produites par des champignons endophytes du genre Neotyphodium. Revue de Médecine Vétérinaire 165 (3-4), 116-135.

Zheng MZ, Richard JL, Binder J. 2006. A review of rapid methods for the analysis of mycotoxins. Mycopathologia 161, 261–273. http://dx.doi.org/10.1007/s11046-006-0215-6

Zinedine A, Gonzales-Osnaya L, Soriano JM, Moltó JC, Idrissi L, Mañes J. 2007. Presence of aflatoxin M1 in pasteurized milk from Morocco. International Journal of Food Microbiology 114, 25-29. http://dx.doi.org/10.1016/j.ijfoodmicro.2006.11.001

Zinedine A, Idrissi L. 2007. Présence et réglementation des mycotoxines dans les aliments au Maroc: Situation actuelle et perspectives. Les Technologies de Laboratoire 7, 10-18.