Comparative Study of Aflatoxin M1 Carry-Over from Feed to Raw Milk in Cow, Buffalo, Sheep, and Goats in Different Areas of Baghdad Province
Main Article Content
Abstract
Mycotoxin aflatoxin B1 (AFB1) is a threat to food safety and human health because it is present in animal feed and is metabolized into aflatoxin M1 (AFM1), a more toxic form, during lactation. The aim of this study was to quantify AFM1 concentrations in raw milk of buffalos, cows, sheep, and goats sampled randomly from four regions within Baghdad Province, Iraq, and to compare these levels with the maximum allowable levels set forth by the European Commission (EC), the Iraqi Standard Specification (IQS), and the food and Drug Administration (FDA). The carry-over of AFB1 from feed to AFM1 in milk were also calculated for each of the studied species. A total of 200 random samples, including 50 each from cows, buffaloes, sheep, and goats, were collected from farms located in Zu'afraniya, Nahrawan, Abu Ghraib, and Fedhalia regions. AFM1 and AFB1 concentrations were determined using the enzyme-linked immunosorbent assay (ELISA). Raw milk samples from cows, sheep, buffaloes, and goats were all found to have AFM1 concentrations that were below the limits set by the EC, IQS, and FDA. Animal feed samples, on the other hand, had AFB1 concentrations of 10.08, 5.95, 4.27, and 7.10 ppb for buffaloes, cows, sheep, and goats, respectively. The observed carry-over rates ranged from 0.36% in goats to 0.78% in buffaloes to 0.66% in cows. Multiple factors, including animal species, are considered, and it is determined that a universal carry-over equation cannot be applied to all cases. Therefore, it is essential to regularly monitor AFM1 levels in milk from various animal species in order to lessen potential health risks. Furthermore, the study suggests enhancing agricultural and veterinary practices to better regulate feed quality for dairy animals.
Received: 14 October 2023
Revised: 22 November 2023
Accepted: 29 November 2023
Published: 28 December 2023
Downloads
Article Details
How to Cite
References
Food and Agriculture Organization of the United Nations. Milk and dairy products in human nutrition. Rome: FAO; 2013.
2. Bowen WH, Lawrence RA. Comparison of the cariogenicity of cola, honey, cow milk, human milk, and sucrose. Pediatrics. 2005;116(4):921-926. https://doi.org/10.1542/peds.2004-2462
3. Yang L, Wang Z. Advances in the total synthesis of aflatoxins. Front Chem. 2021;9:779765. https://doi.org/10.3389/fchem.2021.779765
4. Toso RE, Toribio MS, Diesser M, Borello AB, Ardoino SM. Affections in animals and humans due to ingestion or exposure to aflatoxins: Preventive measures to avoid toxic effects. Cienc Vet. 2018;20:51-67. https://doi.org/10.1111/1471-0307.12578
5. Rosim RE, De Oliveira CA, Corassin CH. Aflatoxin M1 and aflatoxin B1-lysine as biomarkers to evaluate the efficiency of adsorbents for aflatoxins: A review article. Ensaios e Ciência. 2018;22(3):171-178. http://dx.doi.org/10.17921/1415-6938.2018v22n3p171-178
6. Grim CJ. The hotspot for (global) one health in primary food production: Aflatoxin m1 in dairy products. Front Public Health. 2017;4:294. https://doi.org/10.3389/fpubh.2016.00294
7. Assaf JC, El Khoury A, Chokr A, Louka N, Atoui A. A novel method for elimination of aflatoxin M1 in milk using Lactobacillus rhamnosus GG biofilm. Int J Dairy Technol. 2019;72:248-56. https://doi.org/10.1111/1471-0307.12578
8. Kabak B, Özbey F. Aflatoxin M1 in UHT milk consumed in Turkey and first assessment of its bioaccessibility using an in vitro digestion model. Food Control. 2012;28(2):338-44. https://doi.org/10.1016/j.foodcont.2012.05.029
9. Ajwad AM, Assumaidaee NM, Ali NM, Ahmed SW. Zearalenone mycotoxicosis: Pathophysiology and immunotoxicity. Iraqi J Vet Med. 2020;44(1):29-38. https://doi.org/10.30539/ijvm.v44i1.932
10. Alnaemi HS. Estimation of aflatoxin M1 levels in some dairy products manufactured from raw milk experimentally inoculated with toxin. Iraqi J Vet Med. 2019;43(1):50-58. https://doi.org/10.30539/iraqijvm.v43i1.471
11. Khalaf AM, Minati MH. First report of three kinds of mycotoxins dioxynivalenol, nivalenol and fumonisin B2 in seeds of seven wheat cultivars in Iraq. Iraqi J Vet Med. 2019;43(1):43-49. https://doi.org/10.30539/iraqijvm.v43i1.469
12. Al-Kaisie IB, Khalid J. Study of important moulds isolated from milk and its products in Baghdad – with experimental study the pathogenesis of Aspergillus fumigatus moulds in mice. Iraqi J Vet Med. 2005;29(2):68-80. https://doi.org/10.30539/iraqijvm.v29i2.854
13. Vaz A, Cabral Silva A, Rodrigues A, Venâncio A. Detection methods for aflatoxin M1 in dairy products. Microorganisms. 2020;8(2):246. https://doi.org/10.3390/microorganisms8020246
14. Gao YN, Wang JQ, Li SL, Zhang YD, Zheng N. Aflatoxin M1 cytotoxicity against human intestinal Caco-2 cells is enhanced in the presence of other mycotoxins. Food Chem Toxicol. 2016;96:79-89. https://doi.org/10.1016/j.fct.2016.07.019
15. Branch F, Darsanaki RK, Mohammadi M, Kolavani MH, Issazadeh K, Aliabadi MA, et al. Determination of aflatoxin M1 levels in raw milk samples in Gilan, Iran. Adv Stud Biol. 2013;5:151-156. https://doi.org/10.12988/asb.2013.13013
16. Marchese S, Polo A, Ariano A, Velotto S, Costantini S, Severino L. Aflatoxin B1 and M1: Biological properties and their involvement in cancer development. Toxins. 2018;10(6):214. https://doi.org/10.3390/toxins10060214
17. Guo L, Wang Y, Fei P, Liu J, Ren D. A survey on the aflatoxin M1 occurrence in raw milk and dairy products from water buffalo in South China. Food Control. 2019;105:159-163. https://doi.org/10.1016/j.foodcont.2019.05.033
18. Diaz DE, Hagler WM, Blackwelder JT, Eve JA, Hopkins BA, Anderson KL, et al. Aflatoxin binders II: Reduction of aflatoxin M1 in milk by sequestering agents of cows consuming aflatoxin in feed. Mycopathologia. 2004;157:233-241. https://doi.org/10.1023/B:MYCO.0000020587.93872.59
19. Masoero F, Gallo A, Moschini M, Piva G, Diaz D. Carryover of aflatoxin from feed to milk in dairy cows with low or high somatic cell counts. Animal. 2007;1:1344-13450. https://doi.org/10.1017/S1751731107000663
20. Sumantri I, Murti TW, van der Poel AFB, Boehm J, Agus A. Carry-over of aflatoxin B1-feed into aflatoxin M1-milk in dairy cows treated with natural sources of aflatoxin and bentonite. J Indones Trop Anim Agric. 2012;37:271-277. https://doi.org/10.14710/jitaa.37.4.271-277
21. Xiong JL, Wang YM, Nennich TD, Li Y, Liu JX. Transfer of dietary aflatoxin B1 to milk aflatoxin M1 and effect of inclusion of adsorbent in the diet of dairy cows. J Dairy Sci. 2015;98:2545-55. https://doi.org/10.3168/jds.2013-7842
22. Guo W, Fan Z, Fan K, Meng J, Nie D, Tangni EK, et al. In vivo kinetics and biotransformation of aflatoxin B1 in dairy cows based on the establishment of a reliable UHPLC-MS/MS method. Front Chem. 2021;9:809480. https://doi.org/10.3389/fchem.2021.80948
23. Bervis N, Lorán S, Juan T, Carramiñana JJ, Herrera A, Ariño A, et al. Field monitoring of aflatoxins in feed and milk of high-yielding dairy cows under two feeding systems. Toxins. 2021;13:201. https://doi.org/10.3390/toxins1303020
24. Gurbay A, Sabuncuoglu SA, Girgin G, Sahin G, Yiğit S, Yurdakök M, et al. Exposure of newborns to aflatoxin M1 and B1 from mothers' breast milk in Ankara, Turkey. Food Chem Toxicol. 2010;48:314-319.
25. Van Egmond HP. Rationale for regulatory programmes for mycotoxins in human foods and animal feeds. Food Addit Contam. 1993;10:29-36. https://doi.org/10.1080/02652039309374127
26. Mahdi MR, Atiyah AJ. Biodegradation of lycopene on AFB1 naturally contaminated feed and their residue in liver and muscles tissues of local male rabbits. Ann RSCB. 2021;25(2):385-389.
27. Hussein NA, Atiyah AJ. The effect of N-carbamylglutamate supplement on carryover of aflatoxin B1 in liver and muscle tissues of male rabbits fed with contaminated diet by AFB1. Plant Arch. 2020;20(2):4653-4659.
28. Mahmood S, Atiyah AJ. Ameliorative effect of aqueous Myrtus communis extract on AFB1 residue in liver and kidney and some blood biochemical parameter of local male rabbits feeding naturally contaminated by mycotoxins. Biochem Cell Arch. 2021;21(2):4163-4169.
29. Mikhlif BA, Atiyah AJ. Histopathology in female rabbits: Effect of L-arginine and N-carbamoyl glutamate on kidney and liver induced aflatoxin B1. Online J Vet Res. 2019;23(6):578-584.
30. Huang S, Nan Z, Caiyun F, Ming C, Shang W, Adil J, et al. Effects of aflatoxin B1 combined with ochratoxin A and/or zearalenone on metabolism, immune function, and antioxidant status in lactating dairy goats. Astralas J Anim Sci. 2018;31(4):505-513. https://doi.org/10.5713/ajas.17.0279
31. European Commission. Commission regulation 2001/466/EC of 8 March 2001 setting maximum levels for certain contaminants in foodstuffs (Text with EEA relevance). Off J Eur Commun. 2001;L 77:1-13.
32. FDA, U.S. Guidance for industry: Action levels for poisonous or deleterious substances in human food and animal feed. Food and Drug Administration; 2011 Apr. Available from: http://www.fda.gov/Food/GuidanceComplianceRegulatoryInformation/GuidanceDocuments/ChemicalContaminantsandPesticides/ucm077969.htm
33. Food and Agriculture Organization of the United Nations. Worldwide regulations for mycotoxins in food and feed. Rome: FAO; 2003.
34. Iqbal SZ, Asi MR, Arino A, Akram N, Zuber M. Aflatoxin contamination in different fractions of rice from Pakistan and estimation of dietary intakes. Mycotoxin Res. 2012;28(3):175-180. https://doi.org/10.1007/s12550-012-0131-1
35. World Health Organization. Children's health and the environment, WHO training package for the health sector. Geneva: WHO; 2011.
36. Panariti E. Seasonal variations of aflatoxin M1 in the farm milk in Albania. Arh Hig Rada Toksikol. 2001;52(1):37-41.
37. Battacone G, Nudda A, Palomba M, Pascale M, Nicolussi P, Pulina G. Transfer of aflatoxin B1 from feed to milk and from milk to curd and whey in dairy sheep fed artificially contaminated concentrates. J Dairy Sci. 2005;88:3063-3069. https://doi.org/10.3168/jds.S0022-0302(05)72987-8
38. Virdis S, Scarano C, Spanu V, Murittu G, Spanu C, Ibba I, et al. A survey on aflatoxin M1 content in sheep and goat milk produced in Sardinia region, Italy (2005-2013). Ital J Food Saf. 2014;3:4517. https://doi.org/10.4081/ijfs.2014.4517
39. Mugerwa S, Kabirizi J, Zziwa E. Effect of supplementing lactating goats fed on aflatoxin contaminated feed with calcium bentonite and activated charcoal on aflatoxin M concentration, excretion and carryover in milk. Uganda J Agric Sci. 2015;16:83-92. https://doi.org/10.4314/ujas.v16i1.6
40. Pietri A, Bertuzzi T, Fortunati P, Gualla A. Excretion pattern of aflatoxins in buffalo milk and carry-over in mozzarella cheese. Ital J Anim Sci. 2003;2(Suppl 1):302-304.
41. Naveed S, Chohan KA, Jabbar MA, Ditta YA, Ahmed S, Ahmad N, et al. Aflatoxin M1 in Nili-Ravi buffaloes and its detoxification using organic and inorganic toxin binders. J Hell Vet Med Soc. 2018;69:873-878. https://doi.org/10.12681/jhvms.16848
42. Korgaonkar IA, Sarathchandra G, Ponnusamy P, Karunakaran V. Effective amelioration of aflatoxicosis by US CuraTox-FS as toxin binders in cattle feed. Indian Vet J. 2017;94(11):9-12.
43. Aslam N, Rodrigues I, McGill DM, Warriach HM, Cowling A, Haque A, et al. Transfer of aflatoxins from naturally contaminated feed to milk of Nili-Ravi buffaloes fed a mycotoxin binder. Anim Prod Sci. 2016;56:1637-16342. https://doi.org/10.1071/AN14909
44. Rodrigues RO, Ledoux DR, McFadden TB, Rottinghaus GE, Borutova R, Averkieva O. Feed additives containing sequestrant clay minerals and inactivated yeast reduce aflatoxin excretion in milk of dairy cows. J Dairy Sci. 2019;102:6614-6622. https://doi.org/10.3168/jds.2018-16151
45. Applebaum RS, Brackett RE, Wiseman DW, Marth EH. Responses of dairy cows to dietary aflatoxin: Feed intake and yield, toxin content, and quality of milk of cows treated with pure and impure aflatoxin. J Dairy Sci. 1982;65:1503-1508. https://doi.org/10.3168/jds.S0022-0302(82)82374-6
46. Masoero F, Gallo A, Moschini M, Piva G, Diaz D. Carryover of aflatoxin from feed to milk in dairy cows with low or high somatic cell counts. Animal. 2007;1:1344-13450.https://doi.org/10.1017/S1751731107000663
47. Van Eijkeren JCH, Bakker MI, Zeilmaker MJ. A simple steady-state model for carry-over of aflatoxins from feed to cow's milk. Food Addit Contam. 2006;23:833-838. https://doi.org/10.1080/02652030600779890
48. Bervis N, Lorán S, Juan T, Carramiñana JJ, Herrera A, Ariño A, et al. Field monitoring of aflatoxins in feed and milk of high-yielding dairy cows under two feeding systems. Toxins. 2021;13:201. https://doi.org/10.3390/toxins13030201
49. Flores-Flores ME, Lizarraga E, López de Cerain A, González-Peñas E. Presence of mycotoxins in animal milk: A review. Food Control. 2015;53:163-176. https://doi.org/10.1016/j.foodcont.2015.01.020
50. Campagnollo FB, Ganev KC, Khaneghah AM, Portela JB, Cruz AG, Granato D, et al. The occurrence and effect of unit operations for dairy products processing on the fate of aflatoxin M1: A review. Food Control. 2016;68:310-329. https://doi.org/10.1016/j.foodcont.2016.04.007
51. Ritzi M, Friedman S, Miron J, Solomon R, Cuneah O, Shimshoni JA, et al. Carry-over of aflatoxin B1 to aflatoxin M1 in high yielding Israeli cows in mid- and late-lactation. Toxins. 2013;5:173-183. https://doi.org/10.3390/toxins5010173
52. Hernández-Martínez R, Navarro I. Surveillance of aflatoxin content in dairy cow feedstuff from Navarra (Spain). Anim Feed Sci Technol. 2014;200:35-46. https://doi.org/10.1016/j.anifeedsci.2014.12.002
53. Fink-Gremmels J. Mycotoxins in cattle feeds and carry-over to dairy milk: A review. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2008;25:172-180. https://doi.org/10.1080/02652030701823142
54. European Food Safety Authority. Opinion of the scientific panel on contaminants in the food chain [CONTAM] related to aflatoxin B1 as undesirable substance in animal feed. EFSA J. 2004;2:39. https://doi.org/10.2903/j.efsa.2004.39