Publication Cover
Journal of Environmental Science and Health, Part B
Pesticides, Food Contaminants, and Agricultural Wastes
Volume 56, 2021 - Issue 4
260
Views
7
CrossRef citations to date
0
Altmetric
Research Article

Aflatoxin M1 in Brazilian goat milk and health risk assessment

, , , ORCID Icon, ORCID Icon, , ORCID Icon, ORCID Icon & show all

References

  • Paiva, R. D. M.; de Sousa, J. E. R.; Ferreira, J.; Cunha, E. E.; de Paiva, M. P. S. L. M.; Gouveia, A. M. G.; Facó, O. Population Structure and Effect of Inbreeding on Milk Yield of Saanen Goats in Brazilian Production Systems. Small Rumin. Res. 2020, 192, 106194. DOI: 10.1016/j.smallrumres.2020.106194.
  • Rodrigues, N. P. A.; Givisiez, P. E. N.; Queiroga, R. C. R. E.; Azevedo, P. S.; Gebreyes, W. A.; Oliveira, C. J. B. Milk Adulteration: Detection of Bovine Milk in Bulk Goat Milk Produced by Smallholders in Northeastern Brazil by a Duplex PCR Assay. J. Dairy Sci. 2012, 95, 2749–2752. DOI: 10.3168/jds.2011-5235.
  • Lôbo, A. M. B. O.; Lôbo, R. N. B.; Facó, O.; Souza, V.; Alves, A. A. C.; Costa, A. C.; Albuquerque, M. A. M. Characterization of Milk Production and Composition of Four Exotic Goat Breeds in Brazil. Small Rumin. Res. 2017, 153, 9–16. DOI: 10.1016/j.smallrumres.2017.05.005.
  • Sousa, Y. R. F.; Medeiros, L. B.; Pintado, M. M. E.; Queiroga, R. C. R. E. Goat Milk Oligosaccharides: Composition, Analytical Methods and Bioactive and Nutritional Properties. Trends Food Sci. Technol. 2019, 92, 152–161. DOI: 10.1016/j.tifs.2019.07.052.
  • Clark, S.; Mora García, M. B. A 100-Year Review: Advances in Goat Milk Research. J. Dairy Sci. 2017, 100, 10026–10044. DOI: 10.3168/jds.2017-13287.
  • Fonteles, N. L. O.; Alves, S. P.; Madruga, M. S.; Queiroga, R. R. E.; Andrade, A. P.; Silva, D. S.; Leal, A. P.; Bessa, R. J. B.; Medeiros, A. N. Fatty Acid Composition of Polar and Neutral Meat Lipids of Goats Browsing in Native Pasture of Brazilian Semiarid. Meat Sci. 2018, 139, 149–156. DOI: 10.1016/j.meatsci.2018.01.021.
  • Neme, K.; Mohammed, A. Mycotoxin Occurrence in Grains and the Role of Postharvest Management as a Mitigation Strategies - A Review. Food Contr. 2017, 78, 412–425. DOI: 10.1016/j.foodcont.2017.03.012.
  • Luo, Y.; Liu, X.; Li, J. Updating Techniques on Controlling Mycotoxins: A Review. Food Contr. 2018, 89, 123–132. DOI: 10.1016/j.foodcont.2018.01.016.
  • Magnoli, A. P.; Poloni, V. L.; Cavaglieri, L. Impact of Mycotoxin Contamination in the Animal Feed Industry. Curr. Opin. Food Sci. 2019, 29, 99–108. DOI: 10.1016/j.cofs.2019.08.009.
  • Ünüsan, N. Systematic Review of Mycotoxins in Food and Feeds in Turkey. Food Contr. 2019, 97, 1–14. DOI: 10.1016/j.foodcont.2018.10.015.
  • Al-Jaal, B.; Salama, S.; Al-Qasmi, N.; Jaganjac, M. Mycotoxin Contamination of Food and Feed in the Gulf Cooperation Council Countries and Its Detection. Toxicon. 2019, 171, 43–50. DOI: 10.1016/j.toxicon.2019.10.003.
  • Nguyen, T.; Flint, S.; Palmer, J. Control of Aflatoxin M1 in Milk by Novel Methods: A Review. Food Chem. 2020, 311, 125984. DOI: 10.1016/j.foodchem.2019.125984.
  • Iqbal, S. Z.; Jinap, S.; Pirouz, A. A.; Ahmad Faizal, A. R. Aflatoxin M1 in Milk and Dairy Products, Occurrence and Recent Challenges: A Review. Trends Food Sci. Technol. 2015, 46, 110–119. DOI: 10.1016/j.tifs.2015.08.005.
  • Min, L.; Li, D.; Tong, X.; Sun, H.; Chen, W.; Wang, G.; Zheng, N.; Wang, J. The Challenges of Global Occurrence of Aflatoxin M1Contamination and the Reduction of Aflatoxin M1 in Milk over the past Decade. Food Contr. 2020, 117, 107352. DOI: 10.1016/j.foodcont.2020.107352.
  • Deng, J.; Zhao, L.; Zhang, N.-Y.; Karrow, N. A.; Krumm, C. S.; Qi, D.-S.; Sun, L.-H. Aflatoxin B1 Metabolism: Regulation by Phase I and II Metabolizing Enzymes and Chemoprotective Agents. Mutat. Res. 2018, 778, 79–89. DOI: 10.1016/j.mrrev.2018.10.002.
  • Daou, R.; Afif, C.; Joubrane, K.; Khabbaz, L. R.; Maroun, R.; Ismail, A.; Khoury, A. E. Occurrence of Aflatoxin M1 in Raw, Pasteurized, UHT Cows’ Milk, and Dairy Products in Lebanon. Food Contr. 2020, 111, 107055. DOI: 10.1016/j.foodcont.2019.107055.
  • Fakhri, Y.; Rahmani, J.; Oliveira, C. A. F.; Franco, L. T.; Corassin, C. H.; Saba, S.; Rafique, J.; Mousavi Khaneghah, A. Aflatoxin M1 in Human Breast Milk: A Global Systematic Review, Meta-Analysis, and Risk Assessment Study (Monte Carlo Simulation). Trends Food Sci. Technol. 2019, 88, 333–342. DOI: 10.1016/j.tifs.2019.03.013.
  • International Agency for Research on Cancer (IARC). A Review of Human Carcinogens. Part F: Chemical Agents and Related Occupations. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans: Lyon, 2012; Vol. 100F.
  • Campagnollo, F. B.; Ganev, K. C.; Khaneghah, A. M.; Portela, J. B.; Cruz, A. G.; Granato, D.; Corassin, C. H.; Oliveira, C. A. F.; Sant'Ana, A. S. The Occurrence and Effect of Unit Operations for Dairy Products Processing on the Fate of Aflatoxin M1: A Review. Food Contr. 2016, 68, 310–329. DOI: 10.1016/j.foodcont.2016.04.007.
  • European Commission. Commission Regulation (EU) No 165/2010 of 26 February 2010 Amending Regulation (EC) No 1881/2006 Setting Maximum Levels for Certain Contaminants in Foodstuffs as Regards Aflatoxins. Official Journal of the European Union. Brussels, 2010, 8–12. https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2010:050:0008:0012:EN:PDF.
  • Food and Drug Administration (FDA). CPG Sec 527.400 Whole Milk, Lowfat Milk, Skim Milk - Aflatoxin M1. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cpg-sec-527400-whole-milk-lowfat-milk-skim-milk-aflatoxin-m1 (accessed Apr 18, 2020).
  • Brasil. Ministério Da Saúde. Resolução - RDC N° 7, de 18 de Fevereiro de 2011. Dispõe Sobre Limites Máximos Tolerados (LMT) Para Micotoxinas Em Alimentos.; Brasília, 2011.
  • National Research Council (NRC). Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids; National Academy Press: Washington, 2007.
  • de Sousa, Y. R. F.; da Silva Vasconcelos, M. A.; Costa, R. G.; de Azevedo Filho, C. A.; de Paiva, E. P.; Queiroga, R. d C. R. Sialic Acid Content of Goat Milk during Lactation. Livest. Sci. 2015, 177, 175–180. DOI: 10.1016/j.livsci.2015.04.005.
  • Pitt, J. I.; Hocking, A. D. Fungi and Food Spoilage, 3rd ed.; Springer: New York, 2009.
  • Klich, M. A.; Pitt, J. I. A Laboratory Guide to Common Aspergillus Species and Their Teleomorphs; Commonwealth Scientific and Industrial Research Organization, Division of Food Processing: North Ryde, 1988.
  • Klich, M. A. Identification of Common Aspergillus Species; Centraalbureau voor Schimmelcultures: Utrecht, 2002.
  • Pitt, J. I. A Laboratory Guide to Common Penicillium Species, 3rd ed.; Commonwealth Scientific and Industrial Research Organization, Division of Food Processing: North Ryde, 2000.
  • Houbraken, J.; de Vries, R. P.; Samson, R. A. Modern Taxonomy of Biotechnologically Important Aspergillus and Penicillium Species, 1st ed.; Elsevier Inc: London, 2014; Vol. 86. DOI: 10.1016/B978-0-12-800262-9.00004-4.
  • Michlig, N.; Signorini, M.; Gaggiotti, M.; Chiericatti, C.; Basílico, J. C.; Repetti, M. R.; Beldomenico, H. R. Risk Factors Associated with the Presence of Aflatoxin M1 in Raw Bulk Milk from Argentina. Food Contr. 2016, 64, 151–156. DOI: 10.1016/j.foodcont.2015.12.025.
  • de Oliveira, C. P.; Soares, N. F. F.; de Oliveira, T. V.; Baffa Júnior, J. C.; da Silva, W. A. Aflatoxin M1 Occurrence in Ultra High Temperature (UHT) Treated Fluid Milk from Minas Gerais/Brazil. Food Contr. 2013, 30, 90–92. DOI: 10.1016/j.foodcont.2012.07.026.
  • Ghazani, M. H. M. Aflatoxin M1 Contamination in Pasteurized Milk in Tabriz (Northwest of Iran). Food Chem. Toxicol. 2009, 47, 1624–1625. DOI: 10.1016/j.fct.2009.04.011.
  • Mariante, A. S.; McManus, C.; Mendonça, J. F. Country Report on the State of Animal Genetic Resources Brasil; Embrapa Genetic Resources and Biotechnology, 2003, 92. https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/185437/4/doc099.pdf.
  • Food and Agricultura Organization of the United Nations (FAO). Milk and Dairy Products in Human Nutrition; Muehlhoff, E., Bennett, A., McMahon, D., Eds.; FAO: Rome, 2013. DOI: 10.1016/b978-0-12-436703-6.50013-2.
  • Walpole, S. C.; Prieto-Merino, D.; Edwards, P.; Cleland, J.; Stevens, G.; Roberts, I. The Weight of Nations: An Estimation of Adult Human Biomass. BMC Publ. Health. 2012, 12, 439–436. DOI: 10.1186/1471-2458-12-439.
  • Brasil. Guia Alimentar Para Crianças Menores de Dois Anos; Brasília, 2002.
  • Ishikawa, A.; Takabayashi-Yamashita, C.; Ono, E.; Bagatin, A.; Rigobello, F.; Kawamura, O.; Hirooka, E.; Itano, E. Exposure Assessment of Infants to Aflatoxin M1 through Consumption of Breast Milk and Infant Powdered Milk in Brazil. Toxins (Basel) 2016, 8, 246. DOI: 10.3390/toxins8090246.
  • European Food Safety Authority (EFSA). Statement on the Applicability of the Margin of Exposure Approach for the Safety Assessment of Impurities Which Are Both Genotoxic and Carcinogenic in Substances Added to Food/Feed. EFSA J. 2012, 10, 6–10. DOI: 10.2903/j.efsa.2012.2578.
  • Kuiper-Goodman, T. Uncertainties in the Risk Assessment of Three Mycotoxins: Aflatoxin, Ochratoxin, and Zearalenone. Can. J. Physiol. Pharmacol. 1990, 68, 1017–1024. DOI: 10.1139/y90-155.
  • European Food Safety Authority (EFSA). Scientific Opinion on the Risks to Public Health Related to the Presence of Aflatoxins in Food. EFSA J. 2019, 2019, 1–138.
  • Škrbić, B.; Živančev, J.; Antić, I.; Godula, M. Levels of Aflatoxin M1 in Different Types of Milk Collected in Serbia: Assessment of Human and Animal Exposure. Food Contr. 2014, 40, 113–119. DOI: 10.1016/j.foodcont.2013.11.039.
  • R Core Team. R: A Language and Environment for Statistical Computing. R Found. Stat. Comput.: Vienna, 2019.
  • Pereyra, C. M.; Cavaglieri, L. R.; Chiacchiera, S. M.; Dalcero, A. M. Fungi and Mycotoxins in Feed Intended for Sows at Different Reproductive Stages in Argentina. Vet. Med. Int. 2010, 2010, 569108–569107. DOI: 10.4061/2010/569108.
  • del Palacio, A.; Bettucci, L.; Pan, D. Fusarium and Aspergillus Mycotoxins Contaminating Wheat Silage for Dairy Cattle Feeding in Uruguay. Braz. J. Microbiol. 2016, 47, 1000–1005. DOI: 10.1016/j.bjm.2016.06.004.
  • Variane, A. C. F.; Dos Santos, F. C.; de Castro, F. F.; Barbosa-Tessmann, I. P.; dos Santos, G. T.; Dos Santo Pozza, M. S. The Occurrence of Aflatoxigenic Aspergillus Spp. in Dairy Cattle Feed in Southern Brazil. Braz. J. Microbiol. 2018, 49, 919–928. DOI: 10.1016/j.bjm.2018.05.005.
  • Astoreca, A. L.; Dalcero, A. M.; Pinto, V. F.; Vaamonde, G. A Survey on Distribution and Toxigenicity of Aspergillus Section Flavi in Poultry Feeds. Int. J. Food Microbiol. 2011, 146, 38–43. DOI: 10.1016/j.ijfoodmicro.2011.01.034.
  • da Silva, J. L.; Aparecido, C. C.; Hansen, D.; Pereira, T. A. M.; Felicio, J. D.; Gonçalez, E. Identification of Toxigenic Aspergillus Species from Diet Dairy Goat Using a Polyphasic Approach. Cienc. Rural 2015, 45, 1466–1471. DOI: 10.1590/0103-8478cr20140581.
  • Moretti, A.; Susca, A.; Mulé, G.; Logrieco, A. F.; Proctor, R. H. Molecular Biodiversity of Mycotoxigenic Fungi That Threaten Food Safety. Int. J. Food Microbiol. 2013, 167, 57–66. DOI: 10.1016/j.ijfoodmicro.2013.06.033.
  • Rosa, C. A. R.; Ribeiro, J. M. M.; Fraga, M. J.; Gatti, M.; Cavaglieri, L. R.; Magnoli, C. E.; Dalcero, A. M.; Lopes, C. W. G. Mycoflora of Poultry Feeds and Ochratoxin-Producing Ability of Isolated Aspergillus and Penicillium Species. Vet. Microbiol. 2006, 113, 89–96. DOI: 10.1016/j.vetmic.2005.10.031.
  • Peng, W.-X.; Marchal, J. L. M.; van der Poel, A. F. B. Strategies to Prevent and Reduce Mycotoxins for Compound Feed Manufacturing. Anim. Feed Sci. Technol. 2018, 237, 129–153. DOI: 10.1016/j.anifeedsci.2018.01.017.
  • Iheanacho, H. E.; Njobeh, P. B.; Dutton, F. M.; Steenkamp, P. A.; Steenkamp, L.; Mthombeni, J. Q.; Daru, B. H.; Makun, A. H. Morphological and Molecular Identification of Filamentous Aspergillus flavus and Aspergillus parasiticus Isolated from Compound Feeds in South Africa. Food Microbiol. 2014, 44, 180–184. DOI: 10.1016/j.fm.2014.05.019.
  • Omeiza, G. K.; Kabir, J.; Kwaga, J. K. P.; Kwanashie, C. N.; Mwanza, M.; Ngoma, L. A Risk Assessment Study of the Occurrence and Distribution of Aflatoxigenic Aspergillus flavus and Aflatoxin B1 in Dairy Cattle Feeds in a Central Northern State, Nigeria. Toxicol. Rep. 2018, 5, 846–856. DOI: 10.1016/j.toxrep.2018.08.011.
  • Ezekiel, C. N.; Atehnkeng, J.; Odebode, A. C.; Bandyopadhyay, R. Distribution of Aflatoxigenic Aspergillus Section Flavi in Commercial Poultry Feed in Nigeria. Int. J. Food Microbiol. 2014, 189, 18–25. DOI: 10.1016/j.ijfoodmicro.2014.07.026.
  • Zulkifli, N. A.; Zakaria, L. Morphological and Molecular Diversity of Aspergillus from Corn Grain Used as Livestock Feed. HAYATI J. Biosci. 2017, 24, 26–34. DOI: 10.1016/j.hjb.2017.05.002.
  • Kumar, V.; Basu, M. S.; Rajendran, T. P. Mycotoxin Research and Mycoflora in Some Commercially Important Agricultural Commodities. Crop Prot. 2008, 27, 891–905. DOI: 10.1016/j.cropro.2007.12.011.
  • Riba, A.; Bouras, N.; Mokrane, S.; Mathieu, F.; Lebrihi, A.; Sabaou, N. Aspergillus Section Flavi and Aflatoxins in Algerian Wheat and Derived Products. Food Chem. Toxicol. 2010, 48, 2772–2777. DOI: 10.1016/j.fct.2010.07.005.
  • Gholampour Azizi, I.; Shateri, S.; Mousavizadeh, M. Isolation and Identification of the Mycotoxigenic and Non-Mycotoxigenic Fungi from Foodstuff and Feedstuff in Mazandaran Province, Northern Iran. Afr. J. Microbiol. Res. 2012, 6, 3993–3999. DOI: 10.5897/AJMR11.1278..
  • Picinin, L. C. A.; Cerqueira, M. M. O. P.; Vargas, E. A.; Lana, Â. M. Q.; Toaldo, I. M.; Bordignon-Luiz, M. T. Influence of Climate Conditions on Aflatoxin M1 Contamination in Raw Milk from Minas Gerais State, Brazil. Food Contr. 2013, 31, 419–424. DOI: 10.1016/j.foodcont.2012.10.024.
  • Oliveira, C. A. F.; Ferraz, J. C. O. Occurrence of Aflatoxin M1 in Pasteurised, UHT Milk and Milk Powder from Goat Origin. Food Contr. 2007, 18, 375–378. DOI: 10.1016/j.foodcont.2005.11.003.
  • Bilandžić, N.; Božić, Đ.; Đokić, M.; Sedak, M.; Kolanović, B. S.; Varenina, I.; Cvetnić, Ž. Assessment of Aflatoxin M1 Contamination in the Milk of Four Dairy Species in Croatia. Food Contr. 2014, 43, 18–21. DOI: 10.1016/j.foodcont.2014.02.044.
  • Virdis, S.; Corgiolu, G.; Scarano, C.; Pilo, A. L.; De Santis, E. P. L. Occurrence of Aflatoxin M1 in Tank Bulk Goat Milk and Ripened Goat Cheese. Food Contr. 2008, 19, 44–49. DOI: 10.1016/j.foodcont.2007.02.001.
  • Fallah, A. A.; Rahnama, M.; Jafari, T.; Saei-Dehkordi, S. S. Seasonal Variation of Aflatoxin M1 Contamination in Industrial and Traditional Iranian Dairy Products. Food Contr. 2011, 22, 1653–1656. DOI: 10.1016/j.foodcont.2011.03.024.
  • Rahimi, E.; Bonyadian, M.; Rafei, M.; Kazemeini, H. R. Occurrence of Aflatoxin M1 in Raw Milk of Five Dairy Species in Ahvaz, Iran. Food Chem. Toxicol. 2010, 48, 129–131. DOI: 10.1016/j.fct.2009.09.028.
  • Ghanem, I.; Orfi, M. Aflatoxin M1 in Raw, Pasteurized and Powdered Milk Available in the Syrian Market. Food Contr. 2009, 20, 603–605. DOI: 10.1016/j.foodcont.2008.08.018.
  • Kos, J.; Lević, J.; Đuragić, O.; Kokić, B.; Miladinović, I. Miladinović, I. Occurrence and Estimation of Aflatoxin M1 Exposure in Milk in Serbia. Food Contr. 2014, 38, 41–46. DOI: 10.1016/j.foodcont.2013.09.060.
  • Motawee, M. M.; Bauer, J.; McMahon, D. J. Survey of Aflatoxin M1 in Cow, Goat, Buffalo and Camel Milks in Ismailia-Egypt. Bull. Environ. Contam. Toxicol. 2009, 83, 766–769. DOI: 10.1007/s00128-009-9840-3.
  • Hussain, I.; Anwar, J.; Asi, M. R.; Munawar, M. A.; Kashif, M. Aflatoxin M1 Contamination in Milk from Five Dairy Species in Pakistan. Food Contr. 2010, 21, 122–124. DOI: 10.1016/j.foodcont.2008.12.004.
  • Malissiova, E.; Tsakalof, A.; Arvanitoyannis, I. S.; Katsafliaka, A.; Katsioulis, A.; Tserkezou, P.; Koureas, M.; Govaris, A.; Hadjichristodoulou, C. Monitoring Aflatoxin M1 Levels in Ewe’s and Goat’s Milk in Thessaly, Greece; Potential Risk Factors under Organic and Conventional Production Schemes. Food Contr. 2013, 34, 241–248. DOI: 10.1016/j.foodcont.2013.04.035.
  • Battacone, G.; Nudda, A.; Rassu, S. P. G.; Decandia, M.; Pulina, G. Excretion Pattern of Aflatoxin M1 in Milk of Goats Fed a Single Dose of Aflatoxin B1. J. Dairy Sci. 2012, 95, 2656–2661. DOI: 10.3168/jds.2011-5003.
  • Bilandžić, N.; Varenina, I.; Solomun, B. Aflatoxin M1 in Raw Milk in Croatia. Food Contr. 2010, 21, 1279–1281. DOI: 10.1016/j.foodcont.2010.03.003.
  • Fallah, A. A. Aflatoxin M1 Contamination in Dairy Products Marketed in Iran during Winter and Summer. Food Contr. 2010, 21, 1478–1481. DOI: 10.1016/j.foodcont.2010.04.017.
  • Khaneghahi Abyaneh, H.; Bahonar, A.; Noori, N.; Yazdanpanah, H.; Shojaee AliAbadi, M. H. The Overall and Variations of Aflatoxin M1 Contamination of Milk in Iran: A Systematic Review and Meta-Analysis Study. Food Chem. 2020, 310, 125848. DOI: 10.1016/j.foodchem.2019.125848.
  • Unusan, N. Occurrence of Aflatoxin M1 in UHT Milk in Turkey. Food Chem. Toxicol. 2006, 44, 1897–1900. DOI: 10.1016/j.fct.2006.06.010.
  • Bilandžić, N.; Božić, Đ.; Đokić, M.; Sedak, M.; Kolanović, B. S.; Varenina, I.; Tanković, S.; Cvetnić, Ž. Seasonal Effect on Aflatoxin M1 Contamination in Raw and UHT Milk from Croatia. Food Contr. 2014, 40, 260–264. DOI: 10.1016/j.foodcont.2013.12.002.
  • World Health Organization (WHO). The World Health Organization’s Infant Feeding Recommendation. https://www.who.int/nutrition/topics/infantfeeding_recommendation/en/. (accessed Oct 29, 2020).
  • Verruck, S.; Dantas, A.; Prudencio, E. S. Functionality of the Components from Goat’s Milk, Recent Advances for Functional Dairy Products Development and Its Implications on Human Health. J. Funct. Foods 2019, 52, 243–257. DOI: 10.1016/j.jff.2018.11.017.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.