Surveillance of mycotoxin contaminants and mycotoxigenic fungi in agricultural produce
Main Article Content
Keywords
garlic, mycotoxins, onion, potato, pumpkin, tomato
Abstract
Food crops, including vegetables, are prone to attack by pathogenic and mycotoxigenic fungi and represent a food safety and public health risk. The study aimed to detect and quantify mycotoxins in vegetables widely consumed in Mauritius. Diseased samples of garlic, onion, potato, pumpkin and tomato were collected post-harvest. Following microscopic identification of the suspect pathogen(s), samples were tested for mycotoxins by ELISA. Results demonstrated a high mean level of citrinin in garlic (5,448.6 μg/kg) and ochratoxin in onion (9.25 μg/kg), which exceeded the permissible limits, thus pointing to potential health risks associated with the consumption of these vegetables.
References
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De Medeiros F.H.V., Martins S.J., Zucchi T.D., de Melo I.S., Batista L.R and da Cruz Machado J. 2012. Biological Control of Mycotoxin-Producing Molds. Cienc. e Agrotecnologia. 36(5): 483–497. 10.1590/S1413-70542012000500001
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Eskola M., Kos G., Elliott C.T., Hajslova J., Mayar S. and Krska R. 2019. Worldwide contamination of food crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%. Crit. Rev. Food Sci. Nutr. 1–17.
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Gherbawy Y., Elhariry H., Kocsube S., Bahobial A., El Deeb B., Alralhi A., Varga J. and Vagvolgyi C. 2015. Molecular Characterization of Black Aspergillus Species from Onion and Their Potential for Ochratoxin A and Fumonisin B2 Production. Foodborne Pathog. Dis. 0(0): 1–10.
Gibbs N.M. 2013. Errors in the interpretation of ‘no statistically significant difference. Anaesth Intensive Care. 41:151–153. 10.1177/0310057X1304100203
Guo C., Liu Y., Jiang Y., Li R., Pang M., Liu Y. and Dong J. 2016. Fusarium species identification and fumonisin production in maize kernels from Shandong Province, China, from 2012 to 2014. Food Addit Contam Part B Surveill. 9(3):203–209. 10.1080/19393210.2016.1175515
Gupta S., Aggarwal R. and Ahluwalia P. 2009. Assessing the mycotoxin producing potential of pathogens causing vegetable rots. Indian Phytopathol. 62(2):137–143.
Jésus A.A., Beaulys F. and Adolphe Z. 2020. Antifungal activities of endophytic fungi isolated from plantain tissues on Fusarium solani a potential pathogen. Nat. Microbiol. 1(3):96–106.
Jeswel P. and Kumar D. 2016. Mycotoxins and their Producing Fungi from Spices of Bihar (India). Int. J. Biotech. Biomed. Sci. 2(2):174–177.
Ji X., Deng T., Xiao Y., Jin C., Lyu W., Wu Z., Wang W., Wang X., He Q. and Yang H. 2023. Emerging Alternaria and Fusarium mycotoxins in tomatoes and derived tomato products from the China market: Occurrence, methods of determination, and risk evaluation. Food Control. 145:109464. 10.1016/j.foodcont.2022.109464
Kifer D., Sulyok M., Jaksic D., Krska, R. and Klaric M.S. 2021. Fungi and their metabolites in grain from individual households in Croatia. Food Addit Contam Part B Surveill. 14(2):98–109.
Lacetera N. 2019. Impact of climate change on animal health and welfare. Anim. Front. 9(1): 26–31. 10.1093/af/vfy030
Liu Y., Yamdeu J.H.G., Gong Y.Y. and Orfila C. 2020. A review of postharvest approaches to reduce fungal and mycotoxin contamination of foods. Compr. Rev. Food Sci. Food Saf. 1–40.
Luo S., Du H., Kebede H., Liu Y. and Xing F. 2021. Contamination status of major mycotoxins in agricultural product and food stuff in Europe. Food Control. 125:108120.
Madarbokus S. and Ranghoo-Sanmukhiya V.M. 2012. Identification of Genetic Diversity among Papaya Varieties in Mauritius using Morphological and Molecular Markers. Int. J. Life Sci. Biotechnol. Pharma. Res. 1(4).
Meena M., Swapnil P. and Upadhyay R.S. 2017. Isolation, characterization and toxicological potential of Alternaria-mycotoxins (TeA, AOH and AME) in different Alternaria species from various regions of India. Sci. Rep. 7:8777.
Murugan L., Krishnan N., Venkataravanappa V., Saha S., Mishra A.K., Sharma B.K. and Rai A.B. 2020. Molecular characterization and race identification of Fusarium oxysporum f. sp. lycopersici infecting tomato in India. Biotechnol. 10:486. 10.1007/s13205-020-02475-z
Nirmaladevi D., Venkataramana M., Srivastava R.K., Uppalapati S.R., Gupta V.K., Yli Mattila T., Clement Tsui K.M., Srinivas C., Niranjana S.R. and Chandra N.S. 2016. Molecular phylogeny, pathogenicity and toxigenicity of Fusarium oxysporum f. sp. lycopersici. Sci. Rep. 6:21367. 10.1038/srep21367
Palou L. 2014. Penicillium digitatum, Penicillium italicum (Green Mold, Blue Mold). Ch. 2. In “Postharvest Decay Control Strategies”. S. Bautista-Baños (Ed.), p. 45. Academic Press, Elsevier, UK. 10.1016/B978-0-12-411552-1.00002-8
Plascencia-Jatomea M., Yépiz-Gómez M.S., Velez-Haro J.M. 2014. Aspergillus spp. (Black Mould). Ch. 8. In “Postharvest Decay Control Strategies”. S. Bautista-Baños (Ed.), p. 267. Academic Press, Elsevier, UK.
Rahmani A., Jinap S. and Soleimany F. 2009. Qualitative and Quanti-tative Analysis of Mycotoxins. Compr. Rev. Food Sci. Food Saf. 8: 202–251. 10.1111/j.1541-4337.2009.00079.x
Ristaino J.B., Madritch M., Trout C.L. and Parra G. 1998. PCR amplification of ribosomal DNA for species identification in the plant pathogen genus Phytophthora. Appl. Environ. Microbiol. 64(3):948–954. 10.1128/AEM.64.3.948-954.1998
Şengül Ü., Yalçın E., Şengül B. and Çavuşoğlu K. 2016. Investigation of aflatoxin contamination in maize flour consumed in Giresun, Turkey. Qual. Assur. Saf. Crop. Foods. 8(3):385–391.
Stefańczyk E., Sobkowiak S., Brylińska M. and Śliwka J. 2016. Diversity of Fusarium spp. associated with dry rot of potato tubers in Poland. Eur. J. Plant Pathol. 145:871–884. 10.1007/s10658-016-0875-0
Swamy S.D., Mahadevakumar S., Hemareddy H.B., Amruthesh K.N., Mamatha S., Kunjeti S.G., Swapnil R., Vasantha Kumar T. and Lakshmidevi N. 2020. First report of Fusarium equiseti–the incitant of post flowering stalkrot of maize (Zea mays L.) in India. Crop Prot. 129:105035. 10.1016/j.cropro.2019.105035
Takooree S.D., Neetoo H., Ranghoo-Sanmukhiya M., van der Waals J., Vojvodić M. and Bulajić A. 2021. First report of charcoal rot caused by Macrophomina phaseolina on potato tubers in Mauritius. Plant Dis. 105(9):2721. 10.1094/PDIS-02-21-0258-PDN
Takooree S.D., Neetoo H., Ranghoo-Sanmukhiya V.M., Vally V., Bulajić A., van der Waals J. 2022. A comparison of methods for the detection of Phytophthora infestans on potatoes in Mauritius. J. Agric. Sci. (Belgr.). 67(2):203–217. 10.2298/JAS2202203T
Tamura K., Stecher G., Peterson D., Filipski A. and Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30:2725–2729. 10.1093/molbev/mst197
Thompson J.D., Higgins D.G. and Gibson T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673–4680. 10.1093/nar/22.22.4673
Thrane U. 1999. Fusarium. Academic Press. 10.1006/rwfm.1999.0725
Troncoso-Rojas R. and Tiznado-Hernández M.E. 2014. Alternaria alternata (Black Rot, Black Spot). Postharvest Decay. 147–187. 10.1016/B978-0-12-411552-1.00005-3
Van de Perre E., Deschuyffeleer N., Jacxsens L., Vekeman F., van der Hauwaert W., Asam S., Rychlik M., Devlieghere F. and de Meulenaer B. 2013. Screening of moulds and mycotoxins in tomatoes, bell peppers, onions, soft red fruits and derived tomato products. Food Control. 37(1):165–170. 10.1016/j.foodcont.2013.09.034
Van Egmond H.P. and Jonker M.A. 2008. Worldwide Regulations on Aflatoxins-The Situation in 2002. J. Toxicol. Toxin Rev. 23(2–3), 273–293.
WHO. 2018. Mycotoxins. [Internet]. [retrieved on 2023 Sep 08]. Available from: https://www.who.int/news-room/fact-sheets/detail/mycotoxins
Woudenberg J.H.C., Groenewald J.Z., Binder M. and Crous P.W. 2013. Alternaria redefined. Stud. Mycol. 75:171–212.
Yang J., Li Y., Jiang Y., Duan X., Qu H., Yang B., Chen F. and Sivakumar D. 2014. Natural Occurrence, Analysis, and Prevention of Mycotoxins in Fruits and their Processed Products. Crit. Rev. Food Sci. Nutr. 54(1): 64–83. 10.1080/10408398.2011.569860
Youssef N.H. and Sabra M.A. 2022. Impact of Bacillus thuringiensis on inhibiting certain Alternaria alternata’s mycotoxins isolated from infected potatoes. Malays. J. Microbiol. 18(2):163–169.
Zohri A.A., Saber S.M and Abdel-Gawad K.M. 1992. Fungal Flora and Mycotoxins Associated with Onion (Allium cepa L.) in Egypt. Korean Mycol. 20:302–308.
Afolabi C.G., Ezekiel C.N., Ogunbiyi A.E., Oluwadairo O.J., Sulyok M. and Krska R. 2019. Fungi and mycotoxins in cowpea (Vigna unguiculata L) on Nigerian markets. Food Addit. Contam. Part B Surveill. 13(1): 52–58. 10.1080/19393210.2019.1690590
Alshannaq A. and Yu J.H. 2017. Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food. Int. J. Environ. Res. Public Health. 14(6): 632. 10.3390/ijerph14060632
Agricultural Marketing Board (AMB). 2021. Local ware potato specification. [Internet]. [retrieved on 2021 Sep 12]. Available from: https://ambmauritius.mu/portofolio/potato/
Agricultural Marketing Board (AMB). 2022. Vegetables and Spices. [Internet]. [retrieved on 2021 Sep 12]. Available from: https://ambmauritius.mu/products/
Amri E. and Lenoi S. 2016. Aflatoxin and Fumonisin Contamination of Sun-Dried Sweet Potato (Ipomoea batatas L.) Chips in Kahama District, Tanzania. Appl. Environ. Microbiol. 4(3): 55–62.
Barkai-Golan R. and Pasteur N. 2008. “Mycotoxins in Fruits and Vegetables” 1st ed. Burlington, The USA. 10.3920/WMJ2008.x018
Bryden W.L. 2012. Mycotoxin contamination of the feed supply chain: Implications for animal productivity and feed security. Anim. Feed Sci. Technol. 173: 134–158. 10.1016/j.anifeedsci.2011.12.014
Cinar A. and Onbaşı E. 2019. “Mycotoxins The Hidden Danger in Foods Mycotoxins and Food Safety” IntechOpen, Boston, United States. 10.5772/intechopen.89001
Darwish W.S., Ikenaka Y., Nakayama S.M.M. and Ishizuka M. 2014. An Overview on Mycotoxin Contamination of Foods in Africa. Toxicology. 76(6): 789–797. 10.1292/jvms.13-0563
De Medeiros F.H.V., Martins S.J., Zucchi T.D., de Melo I.S., Batista L.R and da Cruz Machado J. 2012. Biological Control of Mycotoxin-Producing Molds. Cienc. e Agrotecnologia. 36(5): 483–497. 10.1590/S1413-70542012000500001
Dombrink-Kurtzman M.A. 2008. Economic Aspects of Mycotoxins in Fruits and Vegetables. Ch. 2. In “Mycotoxins in Fruits and Vegetables”. R. Barkai-Golan and N. Paster (Ed.), p. 27. Academic Press, Elsevier, UK. 10.1016/B978-0-12-374126-4.00002-4
Duchenne R., Ranghoo-Sanmukhiya V.M. and Neetoo H. 2021. Impact of Climate Change and Climate Variability on Food Safety and Occurrence of Foodborne Diseases. Ch. 24. In “Food Security and Safety”. O. O. Babalola (Ed.), p. 461–462. Springer Nature, Switzerland AG.
El-Hassan K.I., El-Saman M.G., Mosa A.A. and Mostafa M.H. 2007. Variation among Fusarium spp. the Causal of Potato Tuber Dry Rot in their Pathogenicity and Mycotoxins Production. Egypt J. Phytopathol. 35(2): 53–68.
Eskola M., Kos G., Elliott C.T., Hajslova J., Mayar S. and Krska R. 2019. Worldwide contamination of food crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%. Crit. Rev. Food Sci. Nutr. 1–17.
European Commission (EC). 2006. Commission Recommendation 2006/576/EC of 17 August 2006 on the presence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products intended for animal feeding. Off. J. L. 229:7–9.
Commission Regulation (EU). 2006. 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off. J. L. 364: 5–24.
Commission Regulation (EU). 2010. No 165/2010 of 26/02/2010. Official Journal of the European Union. (50/8): 8–12.
Commission Recommendation (EU). 2013. No 2013/165/EU of 27 March 2013 on the presence of T-2 and HT-2 toxin in cereals and cereal products. Off. J. L. 91: 12–15.
Fernández-Cruz M.L., Marcia L.M. and Tadeo J.L. 2010. Mycotoxins in fruits and their processed products: Analysis, occurrence and health implications. J. Adv. Res. 1:113–122. 10.1016/j.jare.2010.03.002
Food and Agricultural Research and Extension Institute (FAREI). 2021. Le Guide Agricole. [Internet]. [retrieved on 2022 May 05]. Available from: http://farei.mu/apmis/publications/guide/guideinteractif/main.htm
Food Regulations. 1999. GN 173/1999. Regulations made by the ministry under Section 18 of the Food Act 1998.
Gherbawy Y., Elhariry H., Kocsube S., Bahobial A., El Deeb B., Alralhi A., Varga J. and Vagvolgyi C. 2015. Molecular Characterization of Black Aspergillus Species from Onion and Their Potential for Ochratoxin A and Fumonisin B2 Production. Foodborne Pathog. Dis. 0(0): 1–10.
Gibbs N.M. 2013. Errors in the interpretation of ‘no statistically significant difference. Anaesth Intensive Care. 41:151–153. 10.1177/0310057X1304100203
Guo C., Liu Y., Jiang Y., Li R., Pang M., Liu Y. and Dong J. 2016. Fusarium species identification and fumonisin production in maize kernels from Shandong Province, China, from 2012 to 2014. Food Addit Contam Part B Surveill. 9(3):203–209. 10.1080/19393210.2016.1175515
Gupta S., Aggarwal R. and Ahluwalia P. 2009. Assessing the mycotoxin producing potential of pathogens causing vegetable rots. Indian Phytopathol. 62(2):137–143.
Jésus A.A., Beaulys F. and Adolphe Z. 2020. Antifungal activities of endophytic fungi isolated from plantain tissues on Fusarium solani a potential pathogen. Nat. Microbiol. 1(3):96–106.
Jeswel P. and Kumar D. 2016. Mycotoxins and their Producing Fungi from Spices of Bihar (India). Int. J. Biotech. Biomed. Sci. 2(2):174–177.
Ji X., Deng T., Xiao Y., Jin C., Lyu W., Wu Z., Wang W., Wang X., He Q. and Yang H. 2023. Emerging Alternaria and Fusarium mycotoxins in tomatoes and derived tomato products from the China market: Occurrence, methods of determination, and risk evaluation. Food Control. 145:109464. 10.1016/j.foodcont.2022.109464
Kifer D., Sulyok M., Jaksic D., Krska, R. and Klaric M.S. 2021. Fungi and their metabolites in grain from individual households in Croatia. Food Addit Contam Part B Surveill. 14(2):98–109.
Lacetera N. 2019. Impact of climate change on animal health and welfare. Anim. Front. 9(1): 26–31. 10.1093/af/vfy030
Liu Y., Yamdeu J.H.G., Gong Y.Y. and Orfila C. 2020. A review of postharvest approaches to reduce fungal and mycotoxin contamination of foods. Compr. Rev. Food Sci. Food Saf. 1–40.
Luo S., Du H., Kebede H., Liu Y. and Xing F. 2021. Contamination status of major mycotoxins in agricultural product and food stuff in Europe. Food Control. 125:108120.
Madarbokus S. and Ranghoo-Sanmukhiya V.M. 2012. Identification of Genetic Diversity among Papaya Varieties in Mauritius using Morphological and Molecular Markers. Int. J. Life Sci. Biotechnol. Pharma. Res. 1(4).
Meena M., Swapnil P. and Upadhyay R.S. 2017. Isolation, characterization and toxicological potential of Alternaria-mycotoxins (TeA, AOH and AME) in different Alternaria species from various regions of India. Sci. Rep. 7:8777.
Murugan L., Krishnan N., Venkataravanappa V., Saha S., Mishra A.K., Sharma B.K. and Rai A.B. 2020. Molecular characterization and race identification of Fusarium oxysporum f. sp. lycopersici infecting tomato in India. Biotechnol. 10:486. 10.1007/s13205-020-02475-z
Nirmaladevi D., Venkataramana M., Srivastava R.K., Uppalapati S.R., Gupta V.K., Yli Mattila T., Clement Tsui K.M., Srinivas C., Niranjana S.R. and Chandra N.S. 2016. Molecular phylogeny, pathogenicity and toxigenicity of Fusarium oxysporum f. sp. lycopersici. Sci. Rep. 6:21367. 10.1038/srep21367
Palou L. 2014. Penicillium digitatum, Penicillium italicum (Green Mold, Blue Mold). Ch. 2. In “Postharvest Decay Control Strategies”. S. Bautista-Baños (Ed.), p. 45. Academic Press, Elsevier, UK. 10.1016/B978-0-12-411552-1.00002-8
Plascencia-Jatomea M., Yépiz-Gómez M.S., Velez-Haro J.M. 2014. Aspergillus spp. (Black Mould). Ch. 8. In “Postharvest Decay Control Strategies”. S. Bautista-Baños (Ed.), p. 267. Academic Press, Elsevier, UK.
Rahmani A., Jinap S. and Soleimany F. 2009. Qualitative and Quanti-tative Analysis of Mycotoxins. Compr. Rev. Food Sci. Food Saf. 8: 202–251. 10.1111/j.1541-4337.2009.00079.x
Ristaino J.B., Madritch M., Trout C.L. and Parra G. 1998. PCR amplification of ribosomal DNA for species identification in the plant pathogen genus Phytophthora. Appl. Environ. Microbiol. 64(3):948–954. 10.1128/AEM.64.3.948-954.1998
Şengül Ü., Yalçın E., Şengül B. and Çavuşoğlu K. 2016. Investigation of aflatoxin contamination in maize flour consumed in Giresun, Turkey. Qual. Assur. Saf. Crop. Foods. 8(3):385–391.
Stefańczyk E., Sobkowiak S., Brylińska M. and Śliwka J. 2016. Diversity of Fusarium spp. associated with dry rot of potato tubers in Poland. Eur. J. Plant Pathol. 145:871–884. 10.1007/s10658-016-0875-0
Swamy S.D., Mahadevakumar S., Hemareddy H.B., Amruthesh K.N., Mamatha S., Kunjeti S.G., Swapnil R., Vasantha Kumar T. and Lakshmidevi N. 2020. First report of Fusarium equiseti–the incitant of post flowering stalkrot of maize (Zea mays L.) in India. Crop Prot. 129:105035. 10.1016/j.cropro.2019.105035
Takooree S.D., Neetoo H., Ranghoo-Sanmukhiya M., van der Waals J., Vojvodić M. and Bulajić A. 2021. First report of charcoal rot caused by Macrophomina phaseolina on potato tubers in Mauritius. Plant Dis. 105(9):2721. 10.1094/PDIS-02-21-0258-PDN
Takooree S.D., Neetoo H., Ranghoo-Sanmukhiya V.M., Vally V., Bulajić A., van der Waals J. 2022. A comparison of methods for the detection of Phytophthora infestans on potatoes in Mauritius. J. Agric. Sci. (Belgr.). 67(2):203–217. 10.2298/JAS2202203T
Tamura K., Stecher G., Peterson D., Filipski A. and Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30:2725–2729. 10.1093/molbev/mst197
Thompson J.D., Higgins D.G. and Gibson T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673–4680. 10.1093/nar/22.22.4673
Thrane U. 1999. Fusarium. Academic Press. 10.1006/rwfm.1999.0725
Troncoso-Rojas R. and Tiznado-Hernández M.E. 2014. Alternaria alternata (Black Rot, Black Spot). Postharvest Decay. 147–187. 10.1016/B978-0-12-411552-1.00005-3
Van de Perre E., Deschuyffeleer N., Jacxsens L., Vekeman F., van der Hauwaert W., Asam S., Rychlik M., Devlieghere F. and de Meulenaer B. 2013. Screening of moulds and mycotoxins in tomatoes, bell peppers, onions, soft red fruits and derived tomato products. Food Control. 37(1):165–170. 10.1016/j.foodcont.2013.09.034
Van Egmond H.P. and Jonker M.A. 2008. Worldwide Regulations on Aflatoxins-The Situation in 2002. J. Toxicol. Toxin Rev. 23(2–3), 273–293.
WHO. 2018. Mycotoxins. [Internet]. [retrieved on 2023 Sep 08]. Available from: https://www.who.int/news-room/fact-sheets/detail/mycotoxins
Woudenberg J.H.C., Groenewald J.Z., Binder M. and Crous P.W. 2013. Alternaria redefined. Stud. Mycol. 75:171–212.
Yang J., Li Y., Jiang Y., Duan X., Qu H., Yang B., Chen F. and Sivakumar D. 2014. Natural Occurrence, Analysis, and Prevention of Mycotoxins in Fruits and their Processed Products. Crit. Rev. Food Sci. Nutr. 54(1): 64–83. 10.1080/10408398.2011.569860
Youssef N.H. and Sabra M.A. 2022. Impact of Bacillus thuringiensis on inhibiting certain Alternaria alternata’s mycotoxins isolated from infected potatoes. Malays. J. Microbiol. 18(2):163–169.
Zohri A.A., Saber S.M and Abdel-Gawad K.M. 1992. Fungal Flora and Mycotoxins Associated with Onion (Allium cepa L.) in Egypt. Korean Mycol. 20:302–308.
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