Volume 11, Issue 1 (March 2024)
J. Food Qual. Hazards Control 2024, 11(1): 59-68 |
Back to browse issues page
Ethics code: (NASRI) grant R&D_2022/17
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Mato L, Damani Z, Spahiu J, Halimi E, Seiti B, Topi D. High Prevalence of Mycotoxigenic Fungi and Aflatoxin B1 Contamination in Corn and Wheat Grains Grown to Albania: Implications for Food Safety. J. Food Qual. Hazards Control 2024; 11 (1) :59-68
URL: http://jfqhc.ssu.ac.ir/article-1-1165-en.html
URL: http://jfqhc.ssu.ac.ir/article-1-1165-en.html
University of Tirana, Natural Sciences Faculty, Chemistry Department, Blvd. Zog 1, Tirana, 1,016, Albania , dritan.topi@unitir.edu.al
Abstract: (381 Views)
Background: Today, mycotoxins are considered critical contaminants in foodstuffs produced by fungi, highlighting the importance of food safety to human health. The toxigenic fungi invasion and mycotoxin production are highly variable and depend on climate, plant, and agronomic practices. Among these, Aflatoxins (AFs) are considered the most potent toxins. This study investigated the fungi presence and AFB1 contamination in corn and wheat grown in Albania during the 2022 harvesting year.
Methods: Wheat samples were collected during the summer, while corn during the autumn, and further analyzed. Mycological contamination assessment applied the Verband Deutscher Landëirtschaftlicher Untersuchungs ̶ und Forschungsanstalten (VDLUFA) procedures. The AFB1 levels were measured using the Enzyme-Linked Immunosorbent Assay (ELISA) method. The MATLAB R2016b software was applied to perform statistical analysis. The Estimated Daily Intake on AFB1 was calculated to evaluate human exposure.
Results: The genera Alternaria, Aspergillus, Cladosporium, Fusarium, and Penicillium were isolated, with higher rates of contamination in corn and the highest frequency Penicillium genus (77.89%). The Korça region presented a higher fungal load, 104 Colony Forming Unit (CFU)/g in corn. The AFB1 incidence (88.23%) in corn, was significantly higher than in wheat (4.91%). Additionally, the maximum level in corn was found 69.120 μg/kg, while in wheat, only 0.402 μg/kg. None of the wheat samples, in contrast to the 41.18% of corn samples, exceeded the threshold when referring to the respective Maximum Residue Levels.
Conclusions: Our observation indicates a higher rate of AFB1 contamination in corn than in wheat. The high concentration levels and contamination incidence in corn require targeted interventions to reduce the AFB1 amounts. Strengthened regulation based on scientific evidence can reduce contamination outbreaks, economic implications, and potential benefits, such as increased consumer trust. Our study indicates that the exposure to AFB1 originates from corn consumption among the adult population.
DOI: 10.18502/jfqhc.11.1.14996
Methods: Wheat samples were collected during the summer, while corn during the autumn, and further analyzed. Mycological contamination assessment applied the Verband Deutscher Landëirtschaftlicher Untersuchungs ̶ und Forschungsanstalten (VDLUFA) procedures. The AFB1 levels were measured using the Enzyme-Linked Immunosorbent Assay (ELISA) method. The MATLAB R2016b software was applied to perform statistical analysis. The Estimated Daily Intake on AFB1 was calculated to evaluate human exposure.
Results: The genera Alternaria, Aspergillus, Cladosporium, Fusarium, and Penicillium were isolated, with higher rates of contamination in corn and the highest frequency Penicillium genus (77.89%). The Korça region presented a higher fungal load, 104 Colony Forming Unit (CFU)/g in corn. The AFB1 incidence (88.23%) in corn, was significantly higher than in wheat (4.91%). Additionally, the maximum level in corn was found 69.120 μg/kg, while in wheat, only 0.402 μg/kg. None of the wheat samples, in contrast to the 41.18% of corn samples, exceeded the threshold when referring to the respective Maximum Residue Levels.
Conclusions: Our observation indicates a higher rate of AFB1 contamination in corn than in wheat. The high concentration levels and contamination incidence in corn require targeted interventions to reduce the AFB1 amounts. Strengthened regulation based on scientific evidence can reduce contamination outbreaks, economic implications, and potential benefits, such as increased consumer trust. Our study indicates that the exposure to AFB1 originates from corn consumption among the adult population.
DOI: 10.18502/jfqhc.11.1.14996
Type of Study: Original article |
Subject:
Special
Received: 23/11/06 | Accepted: 24/03/20 | Published: 24/03/26
Received: 23/11/06 | Accepted: 24/03/20 | Published: 24/03/26
References
1. Abdallah M.F., Girgin G., Baydar T., Krska R., Sulyok M. (2017). Occurrence of multiple mycotoxins and other fungal metabolites in animal feed and maize samples from Egypt using LC-MS/MS. Journal of Science of Food and Agriculture. 97: 4419-4428. [DOI: 10.1002/jsfa.8293] [DOI:10.1002/jsfa.8293] [PMID]
2. Alameri M.M., Kong A.S.-Y., Aljaafari M.N., Al Ali H., Eid K., Al Sallagi M., Cheng W.-H., Abushelaibi A., Erin Lim S.-H., Loh J.-Y., Lai K.-S. (2023). Aflatoxin contamination: an overview on health issues, detection and management strategies. Toxins. 15: 246. [DOI: 10.3390/toxins15040246] [DOI:10.3390/toxins15040246] [PMID] [PMCID]
3. Alkadri D., Rubert J., Prodi A., Pisi A., Mañes J., Soler C. (2014). Natural co-occurrence of mycotoxins in wheat grains from Italy and Syria. Food Chemistry. 157: 111-118. [DOI: 10.1016/j.foodchem.2014.01.052] [DOI:10.1016/j.foodchem.2014.01.052] [PMID]
4. Bandyopadhyay R., Ortega-Beltran A., Akande A., Mutegi C., Atehnkeng J., Kaptoge L., Senghor A.L., Adhikari B.N., Cotty P.J. (2016). Biological control of aflatoxins in Africa: current status and potential challenges in the face of climate change. World Mycotoxin Journal. 9: 771-789. [DOI: 10.3920/ WMJ2016.2130] [DOI:10.3920/WMJ2016.2130]
5. Battilani P., Toscano P., Van Der Fels-Klerx H.J., Moretti A., Camardo Leggieri M., Brera C., Rortais A., Goumperis T., Robinson T. (2016). Aflatoxin B1 contamination in maize in Europe increases due to climate change. Scientific Reports. 6: 24328. [DOI: 10.1038/srep24328] [DOI:10.1038/srep24328] [PMID] [PMCID]
6. Bhatnagar-Mathur P., Sunkara S., Bhatnagar-Panwar M., Waliyar F., Kumar Sharma K. (2015). Biotechnological advances for combating Aspergillus flavus and aflatoxin contamination in crops. Plant Science. 234: 119-132. [DOI: 10.1016/ j.plantsci.2015.02.009] [DOI:10.1016/j.plantsci.2015.02.009] [PMID]
7. Bricher J.L. (2010). Ensuring global food safety-a public health priority and a global responsibility. In: Boisrobert C.E., Stjepanovic A., Oh S., Lelieveld H.L. (Editors). Ensuring global food safety. Academic Press, Cambridge, Massachusetts, USA. pp: 1-4. [DOI:10.1016/B978-0-12-374845-4.00001-1]
8. Chulze S.N. (2010). Strategies to reduce mycotoxin levels in maize during storage: a review. Food Additives and Contaminants: Part A. 27: 651-657. [DOI: 10.1080/ 19440040903573032] [DOI:10.1080/19440040903573032] [PMID]
9. Čonková E., Laciaková A., Štyriak I., Czerwiecki L., Wilczyńska G. (2006). Fungal contamination and the levels of mycotoxins (DON and OTA) in cereal samples from Poland and East Slovakia. Czech Journal of Food Sciences. 24: 33-40. [DOI: 10.17221/3291-CJFS] [DOI:10.17221/3291-CJFS]
10. Cotty P.J., Antilla L., Wakelyn P.J. (2007). Competitive exclusion of aflatoxin producers: farmer driven research and development. In: Vincent C., Goettel N., Lazarovits G. (Editors). Biological control: a global perspective. CAB International, London, UK. pp: 241-253. [DOI: 10.1079/ 9781845932657.0241] [DOI:10.1079/9781845932657.0241]
11. De Rijk T.C., Van Egmond H.P., Van Der Fels-Klerx H.J., Herbes R., De Nijs M., Samson R., Slate A.B., Van Der Spiegel M. (2015). A study of the 2013 western European issue of aflatoxin contamination of maize from the Balkan area. World Mycotoxin Journal. 8: 641-651. [DOI: 10.3920/ WMJ2015.1903] [DOI:10.3920/WMJ2015.1903]
12. Eaton D.L., Beima K.M., Bammler T.K., Riley R.T., Voss K.A. (2018). Hepatotoxic mycotoxins. In: McQueen C.A. (Editor). Comprehensive toxicology, 3rd Edition. Elsevier, Oxford, U.K. pp: 483-521. [DOI: 10.1016/B978-0-12-801238-3.64337-4] [DOI:10.1016/B978-0-12-801238-3.64337-4]
13. ESFA Panel on Contaminants in the Food Chain (CONTAM)., Schrenk D., Bignami M., Bodin L., Chipman J.K., Mazo J.D., Grasl-Kraupp B., Hogstrand C., Hoogenboom L., Leblanc J.-C., Nebbia C.S., Nielsen E., et.al. (2020). Risk assessment of aflatoxins in food. EFSA Journal. 18: 6040. [DOI: 10.2903/j.efsa.2020.6040] [DOI:10.2903/j.efsa.2020.6040] [PMID]
14. European Commission (EC). (2006). Commission regulation (EC) No 401/2006 of 23 February 2006 laying down the methods of sampling and analysis for the official control of the levels of mycotoxins in foodstuffs. Office Journal of European :union:. L 70: 12-34. (Accessed 28 August 2023).
15. European Commission (EC). (2023). Commission regulation (EU) 2023/915 of 25 April 2023 on maximum levels for specific contaminants in food and repealing Regulation (EC) No 1881/2006. Office Journal of European :union:. L 119: 103-157. (Accessed 28 August 2023).
16. Food and Agriculture Organization (FAO). (2004). Worldwide regulations for mycotoxins in food and feed in 2003. FAO Food and Nutrition Paper 81. Rome, Italy. URL: https://www.fao.org/3/y5499e/y5499e00.htm.
17. Gagiu V., Mateescu E., Armeanu I., Dobre A.A., Smeu I., Cucu M.E., Oprea O.A., Iorga E., Belc N. (2018). Post-harvest contamination with mycotoxins in the context of the geographic and agroclimatic conditions in Romania. Toxins. 10: 533. [DOI: 10.3390/toxins10120533] [DOI:10.3390/toxins10120533] [PMID] [PMCID]
18. Groopman J.D., Wogan G.N. (2016). Aflatoxins: a global public health problem. In: Caballero B., Finglas P.M., Toldrá F. (Editors). Encyclopedia of food and health. Elsevier, Oxford, U.K. pp: 68-72. [DOI: 10.1016/B978-0-12-384947-2.00015-5] [DOI:10.1016/B978-0-12-384947-2.00015-5]
19. Gruber-Dorninger C., Jenkins T., Schatzmayr G. (2019). Global mycotoxin occurrence in feed: a ten-year survey. Toxins. 11: 375. [DOI: 10.3390/toxins11070375] [DOI:10.3390/toxins11070375] [PMID] [PMCID]
20. Héraud F., Barraj L.M., Moy G.G. (2013). GEMS/food consumption cluster diets. In: Moy G., Vannoort R.W (Editors). Total diet studies. Springer, New York. pp: 427-434. [DOI: 10.1007/978-1-4419-7689-5_43] [DOI:10.1007/978-1-4419-7689-5_43]
21. International Agency for Research on Cancer (IARC). (2012). Chemical agents and related occupations. A review of human carcinogens. IARC monographs on the evaluation of carcinogenic risks to humans. 100F. Lyon, France. URL: www.ncbi.nlm.nih.gov/books/NBK304416/.
22. Janić Hajnal E., Kos J., Krulj J., Krstović S., Jajić I., Pezo L., Šarić B., Nedeljković N. (2017). Aflatoxins contamination of maize in Serbia: the impact of weather conditions in 2015. Food Additives and Contaminants: Part A. 34: 1999-2010. [DOI: 10.1080/19440049.2017.1331047] [DOI:10.1080/19440049.2017.1331047] [PMID]
23. Jedidi I., Soldevilla C., Lahouar A., Marín P., González-Jaén M.T., Said S. (2018). Mycoflora isolation and molecular characterization of aspergillus and fusarium species in Tunisian cereals. Saudi Journal of Biological Sciences. 25: 868-874. [DOI: 10.1016/j.sjbs.2017.11.050] [DOI:10.1016/j.sjbs.2017.11.050] [PMID] [PMCID]
24. Jiang D., Li F., Zheng F., Zhou J., Li L., Shen F., Chen J., Li W. (2019). Occurrence and dietary exposure assessment of multiple mycotoxins in corn-based food products from Shandong, China. Food Additives and Contaminants: Part B. 12: 10-17. [DOI: 10.1080/19393210.2018.1503341] [DOI:10.1080/19393210.2018.1503341] [PMID]
25. Joint Expert Committee on Food Additives (JECFA). (2018). Safety evaluation of specific contaminants in food: prepared by the eighty-third meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA). WHO Food Additives Series, Rome, Italy, 74, pp: 3-280.[URL: https://www.who.int/publications/i/item/9789241660747]
26. Joshaghani H., Namjoo M., Rostami M., Kohsar F., Niknejad F. (2013). Mycoflora of fungal contamination in wheat storage (silos) in Golestan province, north of Iran. Jundishapur Journal of Microbiology. 6: e6334. [DOI: 10.5812/jjm.6334] [DOI:10.5812/jjm.6334]
27. Kos J.J., Škrinjar M.M., Mandić A.I., Mišan A.Č., Bursić V.P., Šarić B.M., Janić Hajnal E.P. (2014). Presence of aflatoxins in cereals from Serbia. Food and Feed Research. 41: 31-38. [DOI: 10.5937/FFR1401031K] [DOI:10.5937/FFR1401031K]
28. Kovač M., Bulaič M., Nevistič A., Rot T., Babič J., Panjičko M., Kovač T., Šarkanj B. (2022). Regulated mycotoxin occurrence and co-occurrence in Croatian cereals. Toxins. 14: 112. [DOI: 10.3390/toxins14020112] [DOI:10.3390/toxins14020112] [PMID] [PMCID]
29. Leggieri M.C., Toscano P., Battilani P. (2021). Predicted aflatoxin B1 increase in Europe due to climate change: actions and reactions at global level. Toxins. 13: 292. [DOI: 10.3390/ toxins13040292] [DOI:10.3390/toxins13040292] [PMID] [PMCID]
30. Liu Y., Wu F. (2010). Global burden of aflatoxin-induced hepatocellular carcinoma: a risk assessment. Environmental Health Perspective. 118: 818-824. [DOI: 10.1289/ehp. 0901388] [DOI:10.1289/ehp.0901388] [PMID] [PMCID]
31. Luo S., Du H., Kebede H., Liu Y., Xing F. (2021). Contamination status of major mycotoxins in agricultural products and foodstuff in Europe. Food Control. 127: 108120. [DOI: 10.1016/j.foodcont.2021.108120] [DOI:10.1016/j.foodcont.2021.108120]
32. Magnussen A., Parsi M.A. (2013). Aflatoxins, hepatocellular carcinoma and public health. World Journal of Gastroenterology. 19: 1508-1512. [DOI: 10.3748/wjg.v19. i10.1508] [DOI:10.3748/wjg.v19.i10.1508] [PMID] [PMCID]
33. Mahato D.K., Lee K.E., Kamle M., Devi S., Dewangan K.N., Kumar P., Kang S.G. (2019). Aflatoxins in food and feed: an overview on prevalence, detection and control strategies. Frontiers in Microbiology. 10: 2266. [DOI: 10.3389/ fmicb.2019.02266] [DOI:10.3389/fmicb.2019.02266]
34. Mannaa M., Kim K.D. (2017). Influence of temperature and water activity on deleterious fungi and mycotoxin production during grain storage. Mycobiology. 45: 240-254. [DOI: 10.5941/ MYCO.2017.45.4.240] [DOI:10.5941/MYCO.2017.45.4.240]
35. Nazhand A., Durazzo A., Lucarini M., Souto E.B., Santini A. (2020). Characteristics, occurrence, detection, and detoxification of aflatoxins in foods and feeds. Foods. 9: 644. [DOI: 10.3390/foods9050644] [DOI:10.3390/foods9050644] [PMID] [PMCID]
36. Owolabi I.O., Karoonuthaisiri N., Elliott C.T., Petchkongkaew A. (2023). A 10-year analysis of RASFF notifications for mycotoxins in nuts. Trend in key mycotoxins and impacted countries. Food Research International. 172: 112915. [DOI: 10.1016/ j.foodres.2023.112915] [DOI:10.1016/j.foodres.2023.112915] [PMID]
37. Patial V., Asrani R.K., Thakur M. (2018). Foodborne mycotoxicosis: pathologies and public health impact. In: Holban A.M., Grumezescu A.M. (Editors). Handbook of food bioengineering, foodborne diseases. 15. Academic Press, Cambridge, Massachusetts, USA. pp: 239-274. [DOI:10.1016/B978-0-12-811444-5.00009-9]
38. Perrone G., Ferrara M., Medina A., Pascale M., Magan N. (2020). Toxigenic fungi and mycotoxins in a climate change scenario: ecology, genomics, distribution, prediction and prevention of the risk. Microorganisms. 8: 1496. [DOI: 10.3390/ microorganisms8101496] [DOI:10.3390/microorganisms8101496]
39. Pitt J.I., Taniwaki M.H., Cole M.B. (2013). Mycotoxin production in major crops as influenced by growing, harvesting, storage and processing, with emphasis on the achievement food safety objectives. Food Control. 32: 205-215. [DOI: 10.1016/j.foodcont.2012.11.023] [DOI:10.1016/j.foodcont.2012.11.023]
40. Piva G., Battilani P., Pietri A. (2006). Emerging issues in southern Europe: aflatoxins in Italy. In: Barug D., Bhatnagar D., Van Egmond H.P. Van Der Kamp J.W., Van Osenbruggen W.A., Visconti A. (Editors). The mycotoxin factbook. Food and Feed Topics; Wageningen Academic Publishers, Wageningen, The Netherlands. pp. 139-153. [DOI:10.3920/9789086865871_009]
41. Pleadin J., Vulić A., Perši N., Škrivanko M., Capek B., Cvetnić Ž. (2015). Annual and regional variations of aflatoxin B1 levels seen in grains and feed coming from Croatian dairy farms over a 5-year period. Food Control. 47: 221-225. [DOI: 10.1016/j.foodcont.2014.07.017] [DOI:10.1016/j.foodcont.2014.07.017]
42. Różewicz M., Wyzińska M., Grabiński J. (2021). The most important fungal diseases of cereals-problems and possible solutions. Agronomy. 11: 714. [DOI: 10.3390/agronomy11040714] [DOI:10.3390/agronomy11040714]
43. Serrano A.B., Font G., Ruiz M.J., Ferrer E. (2012). Co-occurrence and risk assessment of mycotoxins in food and diet from Mediterranean area. Food Chemistry. 135: 423-429. [DOI: 10.1016/j.foodchem.2012.03.064] [DOI:10.1016/j.foodchem.2012.03.064] [PMID]
44. Shabeer S., Asad S., Jamal A., Ali A. (2022). Aflatoxin contamination, its impact and management strategies: an updated review. Toxins. 14: 307. [DOI: 10.3390/ toxins14050307] [DOI:10.3390/toxins14050307] [PMID] [PMCID]
45. Sun X. D., Su P., Shan H. (2017). Mycotoxin contamination of maize in China. Comprehensive Review in Food Science and Food Safety. 16: 835-849. [DOI: 10.1111/1541-4337.12286] [DOI:10.1111/1541-4337.12286] [PMID]
46. Topi D., Babic J., Jakovac-Strajn B., Tavčar-Kalcher G. (2023). Incidence of aflatoxins and ochratoxin A in wheat and corn from Albania. Toxins. 15: 567. [DOI: 10.3390/ toxins15090567] [DOI:10.3390/toxins15090567] [PMID] [PMCID]
47. Topi D., Spahiu J., Rexhepi A., Marku N. (2022). Two-year survey of aflatoxin M1 in milk marketed in Albania and human exposure assessment. Food Control. 136: 108831. [DOI: 10.1016/j.foodcont.2022.108831] [DOI:10.1016/j.foodcont.2022.108831]
48. Topi D., Tavčar-Kalcher G., Pavšič-Vrtač K., Babič J., Jakovac-Strajn B. (2019). Alternaria mycotoxins in grains from Albania: alternariol, alternariol monomethyl ether, tenuazonic acid, and tentoxin. World Mycotoxin Journal. 12: 89-99. [DOI: 10.3920/WMJ2018.2342] [DOI:10.3920/WMJ2018.2342]
49. Udovicki B., Tomic N., Spirovic Trifunovic B., Despotovic S., Jovanovic J., Jacxsens L., Rajkovic A. (2021). Risk assessment of dietary exposure to aflatoxin B1 in Serbia. Food and Chemical Toxicology. 151: 112116. [DOI: 10.1016/j.fct.2021.112116] [DOI:10.1016/j.fct.2021.112116] [PMID]
50. VDLUFA (2007a). Standard operating procedure for identifying bacteria, yeasts, moulds, and dematiaceae as product-typical and spoilage-indicating microorganisms in feeds. In VDLUFA Method Book III Suppl. No. 7 (chap. 28.1.3., 11). VDLUFA, Darmstadt, Germany.
51. VDLUFA (2007b). Standard operation procedure for the enumeration of microorganisms using solid culture media. In VDLUFA Method Book III Suppl. No. 7 (chap. 28.1.1., 14). VDLUFA, Darmstadt, Germany.
52. VDLUFA (2007c). Standard operation procedure to enumerate bacteria, yeasts, moulds, and Dematiaceae. In VDLUFA Method Book III Suppl. No. 7 (chap. 28.1.2., 18). VDLUFA, Darmstadt, Germany
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
