Compliance between Food and Feed Safety: Eight-Year Survey (2013–2021) of Aflatoxin M1 in Raw Milk and Aflatoxin B1 in Feed in Northern Italy
Abstract
:1. Introduction
2. Results
3. Discussion
3.1. AFM1 in Raw Milk in Northern Italy
3.2. AFM1 in Milk in Northern Italy—Year-on-Year Variation
4. Conclusions
5. Materials and Methods
5.1. Milk Samples
5.2. Sample Preparation
5.3. Enzyme-Linked Immunosorbent Assay Procedure
5.4. Evaluation of AFM1 Concentration
5.5. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bennett, J.W.; Klich, M. Mycotoxins. Clin. Microbiol. Rev. 2003, 16, 497–516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, X.D.; Su, P.; Shan, H. Mycotoxin Contamination of Maize in China. Compr. Rev. Food Sci. Food Saf. 2017, 16, 835–849. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liew, W.P.P.; Mohd-Redzwan, S. Mycotoxin: Its Impact on Gut Health and Microbiota. Front. Cell. Infect. Microbiol. 2018, 8, 60. [Google Scholar] [CrossRef] [Green Version]
- Pinotti, L.; Ferrari, L.; Rovere, N.; Fumagalli, F.; Mazzoleni, S.; Cheli, F. Advances in Understanding Key Contamination Risks in Animal Feed: Mycotoxins; Burleigh Doods: Cambridge, UK, 2021; pp. 151–186. [Google Scholar]
- Mousavi Khaneghah, A.; Fakhri, Y.; Gahruie, H.H.; Niakousari, M.; Sant’Ana, A.S. Mycotoxins in Cereal-Based Products during 24 Years (1983–2017): A Global Systematic Review. Trends Food Sci. Technol. 2019, 91, 95–105. [Google Scholar] [CrossRef]
- Kabak, B. Aflatoxin M1 and Ochratoxin A in Baby Formulae in Turkey: Occurrence and Safety Evaluation. Food Control 2012, 26, 182–187. [Google Scholar] [CrossRef]
- Pinotti, L.; Ottoboni, M.; Giromini, C.; Dell’Orto, V.; Cheli, F. Mycotoxin Contamination in the EU Feed Supply Chain: A Focus on Cereal Byproducts. Toxins 2016, 8, 45. [Google Scholar] [CrossRef] [Green Version]
- Bailly, S.; El Mahgubi, A.; Carvajal-Campos, A.; Lorber, S.; Puel, O.; Oswald, I.P.; Bailly, J.D.; Orlando, B. Occurrence and Identification of Aspergillus Section Flavi in the Context of the Emergence of Aflatoxins in French Maize. Toxins 2018, 10, 525. [Google Scholar] [CrossRef] [Green Version]
- Creppy, E.E. Update of Survey, Regulation and Toxic Effects of Mycotoxins in Europe. Toxicol. Lett. 2002, 127, 19–28. [Google Scholar] [CrossRef]
- Alshannaq, A.; Yu, J.H. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food. Int. J. Environ. Res. Public Health 2017, 14, 632. [Google Scholar] [CrossRef] [Green Version]
- Wild, C.P.; Baan, R.A.; Gelderblom, W.C.; Miller, J.D.; Riley, R.T.; Wu, F. Improving Public Health through Mycotoxin Control; International Agency for Research on Cancer: Lyon, France, 2012. [Google Scholar]
- Verduci, E.; Elios, S.D.; Cerrato, L.; Comberiati, P.; Calvani, M.; Palazzo, S.; Martelli, A.; Landi, M.; Trikamjee, T.; Peroni, D.G. Cow’s Milk Substitutes for Children: Nutritional Special Formula and Plant-Based Beverages. Nutrients 2019, 11, 1789. [Google Scholar] [CrossRef] [Green Version]
- Jaiswal, L.; Worku, M. Recent Perspective on Cow’s Milk Allergy and Dairy Nutrition. Crit. Rev. Food Sci. Nutr. 2022, 62, 7503–7517. [Google Scholar] [CrossRef]
- Mccullogh, N.; Boldon, R.; Haskell-ramsay, C.; James, L.; Stevenson, E. The Potential Nutrition-, Physical- and Health-Related Benefits of Cow’s Milk for Primary-School-Aged Children. Nutr. Res. Rev. 2022, 35, 50–69. [Google Scholar]
- Ferrari, L.; Fumagalli, F.; Rizzi, N.; Grandi, E.; Vailati, S.; Manoni, M.; Ottoboni, M.; Cheli, F.; Pinotti, L. An Eight-Year Survey on Aflatoxin B1 Indicates High Feed Safety in Animal Feed and Forages in Northern Italy. Toxins 2022, 14, 763. [Google Scholar] [CrossRef] [PubMed]
- Tahir, N.I.; Hussain, S.; Javed, M.; Rehman, H.; Shahzady, T.G.; Parveen, B.; Ali, K.G. Nature of Aflatoxins: Their Extraction, Analysis, and Control. J. Food Saf. 2018, 38, e12561. [Google Scholar] [CrossRef]
- Saha Turna, N.; Wu, F. Aflatoxin M1 in Milk: A Global Occurrence, Intake, & Exposure Assessment. Trends Food Sci. Technol. 2021, 110, 183–192. [Google Scholar] [CrossRef]
- Drug Administration. Food and Drug Administration Guidance for Industry: Action Levels for Poisonous or Deleterious Substances in Human Food and Animal Feed; Food and Drug Administration: Silver Spring, MD, USA, 1978. [Google Scholar]
- European Commission. Commission Regulation No. 1881/2006 of 19 December 2006 Setting Maximum Levels for Certain Contaminants in Foodstuffs. Off. J. Eur. Union 2006, 364, 5–24. [Google Scholar]
- Popovic, R.; Radovanov, B.; Dunn, J.W. Food Scare Crisis: The Effect on Serbian Dairy Market. Int. Food Agribus. Manag. Rev. 2017, 20, 113–127. [Google Scholar] [CrossRef]
- Taylor, P.; Assessment, R.; Kim, E.K.; Shon, D.H.; Ryu, D.; Park, J.W.; Hwang, H.J.; Kim, Y.B. Food Additives and Contaminants: Chemistry, Occurrence of Aflatoxin M 1 in Korean Dairy Products Determined by ELISA and HPLC Occurrence of aflatoxin M 1 in Korean Dairy Products Determined by ELISA and HPLC. Food Addit. Contam. 2010, 17, 59–64. [Google Scholar] [CrossRef]
- Markaki, P.; Melissari, E. Occurrence of Aflatoxin M1 in Commercial Pasteurized Milk Determined with ELISA and HPLC. Food Addit. Contam. 1997, 14, 451–456. [Google Scholar] [CrossRef]
- Rodríguez Velasco, M.L.; Calonge Delso, M.M.; Ordónez Escudero, D. ELISA and HPLC Determination of the Occurrence of Aflatoxin M1 in Raw Cow’s Milk. Food Addit. Contam. 2003, 20, 276–280. [Google Scholar] [CrossRef]
- Zhang, D.H.; Li, P.W.; Zhang, Q.; Yang, Y.; Zhang, W.; Guan, D.; Ding, X.X. Extract-Free Immunochromatographic Assay for on-Site Tests of Aflatoxin M 1 in Milk. Anal. Methods 2012, 4, 3307–3313. [Google Scholar] [CrossRef]
- Zhang, X.; Wen, K.; Wang, Z.; Jiang, H.; Beier, R.C.; Shen, J. An Ultra-Sensitive Monoclonal Antibody-Based Fluorescent Microsphere Immunochromatographic Test Strip Assay for Detecting Aflatoxin M1 in Milk. Food Control 2016, 60, 588–595. [Google Scholar] [CrossRef]
- Su, Z.; Zhao, G.; Dou, W. Determination of Trace Aflatoxin M1 (AFM1) Residue in Milk by an Immunochromatographic Assay Based on (PEI/PSS)4 Red Silica Nanoparticles. Microchim. Acta 2020, 187, 658. [Google Scholar] [CrossRef]
- Pimpitak, U.; Rengpipat, S.; Phutong, S.; Buakeaw, A.; Komolpis, K. Development and Validation of a Lateral Flow Immunoassay for the Detection of Aflatoxin M1 in Raw and Commercialised Milks. Int. J. Dairy Technol. 2020, 73, 695–705. [Google Scholar] [CrossRef]
- Singh, H.; Singh, S.; Bhardwaj, S.K.; Kaur, G.; Khatri, M.; Deep, A.; Bhardwaj, N. Development of Carbon Quantum Dot-Based Lateral Flow Immunoassay for Sensitive Detection of Aflatoxin M1 in Milk. Food Chem. 2022, 393, 133374. [Google Scholar] [CrossRef]
- Maggira, M.; Sakaridis, I.; Ioannidou, M.; Samouris, G. Comparative Evaluation of Three Commercial Elisa Kits Used for the Detection of Aflatoxins B1, B2, G1, and G2 in Feedstuffs and Comparison with an HPLC Method. Vet. Sci. 2022, 9, 104. [Google Scholar] [CrossRef] [PubMed]
- Givens, D.I. The Role of Animal Nutrition in Improving the Nutritive Value of Animal-Derived Foods in Relation to Chronic Disease. Proc. Nutr. Soc. 2005, 64, 395–402. [Google Scholar] [CrossRef]
- Haug, A.; Høstmark, A.T.; Harstad, O.M. Bovine Milk in Human Nutrition—A Review. Lipids Health Dis. 2007, 6, 25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Min, L.; Fink-Gremmels, J.; Li, D.; Tong, X.; Tang, J.; Nan, X.; Yu, Z.; Chen, W.; Wang, G. An Overview of Aflatoxin B1 Biotransformation and Aflatoxin M1 Secretion in Lactating Dairy Cows. Anim. Nutr. 2021, 7, 42–48. [Google Scholar] [CrossRef]
- Min, L.; Li, D.; Tong, X.; Sun, H.; Chen, W.; Wang, G.; Zheng, N.; Wang, J. The Challenges of Global Occurrence of Aflatoxin M1 Contamination and the Reduction of Aflatoxin M1 in Milk over the Past Decade. Food Control 2020, 117, 107352. [Google Scholar] [CrossRef]
- Nuryono, N.; Agus, A.; Wedhastri, S.; Maryudani, Y.B.; Sigit Setyabudi, F.M.C.; Böhm, J.; Razzazi-Fazeli, E. A Limited Survey of Aflatoxin M1 in Milk from Indonesia by ELISA. Food Control 2009, 20, 721–724. [Google Scholar] [CrossRef]
- Tarannum, N.; Nipa, M.N.; Das, S.; Parveen, S. Aflatoxin M1 Detection by ELISA in Raw and Processed Milk in Bangladesh. Toxicol. Rep. 2020, 7, 1339–1343. [Google Scholar] [CrossRef] [PubMed]
- Lutfullah, G.; Hussain, A. Studies on Contamination Level of Aflatoxins in Some Cereals and Beans of Pakistan. Food Control 2012, 23, 32–36. [Google Scholar] [CrossRef]
- Fumagalli, F.; Ottoboni, M.; Pinotti, L.; Cheli, F. Integrated Mycotoxin Management System in the Feed Supply Chain: Innovative Approaches. Toxins 2021, 13, 572. [Google Scholar] [CrossRef] [PubMed]
- Britzi, M.; Friedman, S.; Miron, J.; Solomon, R.; Cuneah, O.; Shimshoni, J.A.; Soback, S.; Ashkenazi, R.; Armer, S.; Shlosberg, A. Carry-over of Aflatoxin B1 to Aflatoxin M1 in High Yielding Israeli Cows in Mid- and Late-Lactation. Toxins 2013, 5, 173–183. [Google Scholar] [CrossRef]
- Bianco, G.; Russo, R.; Marzocco, S.; Velotto, S.; Autore, G.; Severino, L. Modulation of Macrophage Activity by Aflatoxins B1 and B2 and Their Metabolites Aflatoxins M1 and M2. Toxicon 2012, 59, 644–650. [Google Scholar] [CrossRef]
- Bognanno, M.; Fauci, L.; La Ritieni, A.; Tafuri, A.; De Lorenzo, A.; Micari, P.; Renzo, L.D.; Ciappellano, S.; Sarullo, V.; Galvano, F. Survey of the Occurrence of Aflatoxin M1 in Ovine Milk by HPLC and Its Confirmation by MS. Mol. Nutr. Food Res. 2006, 50, 300–305. [Google Scholar] [CrossRef] [PubMed]
- Chaytor, A.C.; Hansen, J.A.; Van Heugten, E.; See, M.T.; Kim, S.W. Occurrence and Decontamination of Mycotoxins in Swine Feed. Asian-Australas. J. Anim. Sci. 2011, 24, 723–738. [Google Scholar] [CrossRef]
- Prandini, A.; Tansini, G.; Sigolo, S.; Filippi, L.; Laporta, M.; Piva, G. On the Occurrence of Aflatoxin M1 in Milk and Dairy Products. Food Chem. Toxicol. 2009, 47, 984–991. [Google Scholar] [CrossRef]
- Serraino, A.; Bonilauri, P.; Kerekes, K.; Farkas, Z.; Giacometti, F.; Canever, A.; Zambrini, A.V.; Ambrus, Á. Occurrence of Aflatoxin M1 in Raw Milk Marketed in Italy: Exposure Assessment and Risk Characterization. Front. Microbiol. 2019, 10, 2516. [Google Scholar] [CrossRef]
- Armorini, S.; Altafini, A.; Zaghini, A.; Roncada, P. Occurrence of Aflatoxin M1 in Conventional and Organic Milk Offered for Sale in Italy. Mycotoxin Res. 2016, 32, 237–246. [Google Scholar] [CrossRef]
- Bervis, N.; Lorán, S.; Juan, T.; Carramiñana, J.J.; Herrera, A.; Ariño, A.; Herrera, M. Field Monitoring of Aflatoxins in Feed and Milk of High-Yielding Dairy Cows under Two Feeding Systems. Toxins 2021, 13, 201. [Google Scholar] [CrossRef] [PubMed]
- Giorni, P.; Magan, N.; Pietri, A.; Bertuzzi, T.; Battilani, P. Studies on Aspergillus Section Flavi Isolated from Maize in Northern Italy. Int. J. Food Microbiol. 2007, 113, 330–338. [Google Scholar] [CrossRef] [PubMed]
- Ottoboni, M.; Pinotti, L.; Tretola, M.; Giromini, C.; Fusi, E.; Rebucci, R.; Grillo, M.; Tassoni, L.; Foresta, S.; Gastaldello, S.; et al. Combining E-Nose and Lateral Flow Immunoassays (LFIAs) for Rapid Occurrence/Co-Occurrence Aflatoxin and Fumonisin Detection in Maize. Toxins 2018, 10, 416. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Locatelli, S.; Scarpino, V.; Lanzanova, C.; Romano, E.; Reyneri, A. Multi-Mycotoxin Long-Term Monitoring Survey on North-Italian Maize over an 11-Year Period (2011–2021): The Co-Occurrence of Regulated, Masked and Emerging Mycotoxins and Fungal Metabolites. Toxins 2022, 14, 520. [Google Scholar] [CrossRef] [PubMed]
- Procedure Straordinarie Contro il Rischio Aflatossine. Available online: https://www.anmvioggi.it/images/INFORMATIVA_AFLATOSSINA_AGLI_ALLEVATORI.pdf (accessed on 10 February 2023).
AFM1 Concentration (ng/L) | ||||
---|---|---|---|---|
Very Low Risk (<25) | Low Risk (25–40) | Moderate Risk (40–50) | High Risk (>50) | |
Number of samples | 92,823 | 2002 | 390 | 667 |
Percentage of samples (%) | 96.8 | 2.1 | 0.4 | 0.7 |
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Ferrari, L.; Rizzi, N.; Grandi, E.; Clerici, E.; Tirloni, E.; Stella, S.; Bernardi, C.E.M.; Pinotti, L. Compliance between Food and Feed Safety: Eight-Year Survey (2013–2021) of Aflatoxin M1 in Raw Milk and Aflatoxin B1 in Feed in Northern Italy. Toxins 2023, 15, 168. https://doi.org/10.3390/toxins15030168
Ferrari L, Rizzi N, Grandi E, Clerici E, Tirloni E, Stella S, Bernardi CEM, Pinotti L. Compliance between Food and Feed Safety: Eight-Year Survey (2013–2021) of Aflatoxin M1 in Raw Milk and Aflatoxin B1 in Feed in Northern Italy. Toxins. 2023; 15(3):168. https://doi.org/10.3390/toxins15030168
Chicago/Turabian StyleFerrari, Luca, Nicoletta Rizzi, Elisa Grandi, Eleonora Clerici, Erica Tirloni, Simone Stella, Cristian Edoardo Maria Bernardi, and Luciano Pinotti. 2023. "Compliance between Food and Feed Safety: Eight-Year Survey (2013–2021) of Aflatoxin M1 in Raw Milk and Aflatoxin B1 in Feed in Northern Italy" Toxins 15, no. 3: 168. https://doi.org/10.3390/toxins15030168
APA StyleFerrari, L., Rizzi, N., Grandi, E., Clerici, E., Tirloni, E., Stella, S., Bernardi, C. E. M., & Pinotti, L. (2023). Compliance between Food and Feed Safety: Eight-Year Survey (2013–2021) of Aflatoxin M1 in Raw Milk and Aflatoxin B1 in Feed in Northern Italy. Toxins, 15(3), 168. https://doi.org/10.3390/toxins15030168