Contamination of common spices by aflatoxigenic fungi and aflatoxin B1 in Algeria
Main Article Content
Keywords
Aspergillus, HPLC-FLD, mycotoxins
Abstract
Spices are usually produced in areas where the climatic conditions are favourable to growth of toxigenic fungi and production of mycotoxins. This study assesses the occurrence of aflatoxigenic fungi and aflatoxin B1 (AFB1) in spices marketed in Algeria. A total of 44 spice samples (4 for each type of spice) composed of aniseed, black pepper, caraway, cinnamon, coriander, cumin, ginger, red pepper, saffron, sweet cumin, and sweet pepper were collected from four popular markets located in Algeria. Mycological analysis of the spice was by dilution plating while AFB1 contamination levels were determined by high-performance liquid chromatography coupled with fluorescence detection (HPLC-FLD) after post-column derivatisation. The commonly isolated fungi were species of Aspergillus (56.4%), Penicillium (25.1%), Mucor (12.8%) and Eurotium (5.7%). Species belonging to Aspergillus section Flavi represented 28.9% of the total Aspergilli. The aflatoxin producing ability of isolates belonging to Aspergillus section Flavi was determined on coconut agar medium and confirmed by thin layer chromatography and HPLC-FLD. Ninety-four isolates (38.4%) of the 245 Aspergillus section Flavi examined produced aflatoxins. The most frequent chemotypes (84%) correspond to isolates able to produce both aflatoxin B and cyclopiazonic acid followed by the producers of only aflatoxin B. Twenty-three (63.9%) of the 36 spices contained AFB1 at levels ranging from 0.10 to 26.50 ?g/kg. Two saffron (24.34 and 26.50 ?g/kg) and two sweet cumin (14.65 and 19.07 ?g/kg) samples were above the Algerian regulatory limit of 10 ?g/kg. This work represents the first report about the occurrence of aflatoxigenic fungi and AFB1 in the common spices in Algeria.
References
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Bircan, C., 2005. The determination of aflatoxins in spices by immunoaffinity column extraction using HPLC. International Journal of Food Science and Technology 40: 929-934.
Calvo, A.M., Bok, J., Brooks, W. and Keller, N.P, 2004. VeA is required for toxin and sclerotial production in Aspergillus parasiticus. Applied and Environmental Microbiology 70: 4733-4739.
Cardwell, K.F. and Cotty, P.J., 2002. Distribution of Aspergillus section Flavi among field soils from the four agroecological zones of the Republic of Benin West Africa. Plant Disease 86: 434-439.
Cho, S.H., Lee, C.H., Jang, M.R., Son, Y.W., Lee, S.M., Choi, I.S., So-Hee Kim, S.H, and Kim, D.B., 2008. Aflatoxin contamination in spices and processed spice products commercialized in Korea. Food Chemistry 107: 1283-1288.
Colak, H., Bingol, E.B., Hampikyan, H. and Nazli, B., 2006. Determination of aflatoxin contamination in red-scaled, red and black pepper by ELISA and HPLC. Journal of Food and Drug Analysis 14: 292-296.
Criseo, G., Bagnara, A. and Bisignano, G., 2001. Differentiation of aflatoxin-producing and non-producing strains of Aspergillus flavusgroup. Letters in Applied Microbiology 33: 291-295.
El Mahgubi, A., Puel, O., Bailly, S., Tadrist, S., Querin, A., Ouadia, A., Oswald, I.P. and Bailly, J.D., 2013. Distribution and toxigenicity of Aspergillus section Flavi in spices marketed in Morocco. Food Control 32: 143-148.
El-Kady, S.S., El-Maraghy, M. and Eman Mostafa, M., 1992. Contribution of the mesophilic fungi of different spices in Egypt. Mycopathologia 120: 93-101.
Elshafie, A.E., Al-Rashdi, T.A., Al-Bahry S.N. and Bakheit, C.S., 2002. Fungi and aflatoxins associated with spices in the Sultanate of Oman. Mycopathologia 155: 155-160.
European Commission (EC), 2006. Commission Regulation no. 1881/2006 of December 19th (2006) Setting maximum levels of certain contaminants in foodstuffs. Official Journal of the European Union L364: 5-24.
Fazekas, B., Tar, A. and Kovacs, M., 2005. Aflatoxin and ochratoxin A content of spices in Hungary. Food Additives and Contaminants 22: 856-868.
Fente, C.A., Ordaz, J.J., Vazquez, B.I., Franco, C.M. and Cepeda, A., 2001. New additive for culture media for rapid identification of aflatoxin-producing Aspergillus strains. Applied and Environmental Microbiology 67: 58-62.
Food and Agriculture Organization (FAO), 2004. Regulations for mycotoxins in food and feed in 2003. FAO Food and Nutrition Paper 81. FAO, Rome, Italy.
Garrido, D., Jordal, M. and Poza, R., 1992. Mold flora and aflatoxin-producing strains of Aspergillus flavus in spices and herbs. Journal of Food Protection 55: 451-452.
Giorni, P., Magan, N., Pietri, A., Bertuzzi, T. and Battilani, P., 2007. Studies on Aspergillus section Flavi isolated from maize in northern Italy. International Journal of Food Microbiology 113: 330-338.
Hammami, W., Fiori, S., Al Thani, R., Ali Kali, N., Balmas, V., Migheli, Q. and Jaoua,S., 2014. Fungal and aflatoxin contamination of marketed spices. Food Control 37: 177-181.
Hashem, M. and Alamri, S., 2010. Contamination of common spices in Saudi Arabia markets with potential mycotoxin-producing fungi. Saudi Journal of Biological Sciences 17: 167-175.
Hitokoto, H., Morozumi, S., Wauke, T., Sakai, S. and Kurata, H. 1978. Fungal contamination and mycotoxin detection of powdered of herbal drugs. Applied and Environmental Microbiology 36: 252-256.
Horn, B.W., 2003. Ecology and population biology of aflatoxigenic fungi in soil. Journal of Toxicology – Toxin Reviews 22: 351-379.
Hua, S.T., 2003. Biocontrol of Aspergillus flavus by saprophytic yeast, progress from laboratory bioassay to field trial. In: Proceedings of the 3rd Fungal Genomics, 4th Fumonisin, and 16th Aflatoxin Elimination Workshops, October 13-15, 2003, Savannah, GA, USA.
Juglal, S., Govinden, R. and Odhav, B., 2002. Spice oils for the control of co-occurring mycotoxin-producing fungi. Journal of Food Protection 65: 683-687.
King, A.D., Hocking, A.D. and Pitt, J.I. 1979. Dichloran-rose bengal medium for enumeration and isolation of molds from foods. Applied and Environmental Microbiology 37: 959-964.
Klich, M.A, 2002. Identification of common Aspergillus species. Centraal Bureau voor Schimmel Cultures, Utrecht, the Netherlands.
Klich, M.A., 2007. Environmental and developmental factors influencing aflatoxin production by Aspergillus flavus and Aspergillus parasiticus. Mycoscience 48: 71-80.
Kong, W., Wei, R., Logrieco A., Wei J, Jing, W., Xiaoe X. and Yanga, M., 2014. Occurrence of toxigenic fungi and determination of mycotoxins by HPLC-FLD in functional foods and spices in China markets. Food Control 28: 354-361.
Kursun, O. and Mutlu, A.G., 2010. Aflatoxin in spices marketed in the west Mediterranean region of Turkey. Journal of Animal and Veterinary Advances 9: 2979-2981.
Madhyastha, M.S. and Bhat, R.V., 1985. Evaluation of substrate potentiality and inhibitory effects to identify high risk spices for aflatoxin contamination. Journal of Food Science 50: 376-378.
Magan, N. and Aldred, D., 2005. Conditions of formation of ochratoxin A in drying, transport and in different commodities. Food Additives and Contaminants 22 Suppl. 1: 10-16.
Martins, M.L., Martins, H.M. and Bernardo, F., 2001. Aflatoxins in spices marketed in Portugal. Food Additives and Contaminants 18: 315-319.
Musaiger, A.O., Al-Jedah, J.H., and De Souza, R., 2008. Occurrence of contaminants in foods commonly consumed in Bahrain. Food Control 19: 854-861.
Nguyen, M.T., Tozlovanu, M., Luyen Tran, T. and Pfohl-Leszkowicz, A., 2007. Occurrence of aflatoxin B1, citrinin and ochratoxin A in rice in five provinces of the central region of Vietnam. Food Chemistry 105: 42-47.
O’Riordan, M.J. and Wilkinson, M.G., 2008. A survey of the incidence and level of aflatoxin contamination in a range of imported spice preparations on the Irish retail market. Food Chemistry 107: 1429-1435.
Ozbey, F. and Kabak, B., 2012. Natural co-occurrence of aflatoxins and ochratoxin A in spices. Food Control 28: 354-361.
Pildain, M.B., Frisvad, J.C., Vaamonde, G., Cabral, J., Varga, D. and Samson, R.A., 2008. Two novel aflatoxin-producing Aspergillusspecies from Argentinean peanuts. International Journal of Systematic and Evolutionary Microbiology 58: 725-735.
Pildain, M.B., Vaamonde, G. and Cabral, D., 2004. Analysis of population structure of Aspergillus flavus from peanut based on vegetative compatibility, geographic origin: mycotoxin and sclerotia production. International Journal of Food Microbiology 93: 33-40.
Pitt, J.I. and Hocking, A.D., 1997. Fungi and food spoilage (2nd Ed.). Blackie Academic and Professional, London, UK, pp. 505-507.
Prelle, A., Spadaro, D., Garibaldi, A. and Gullino, M.L, 2014. Co-occurrence of aflatoxins and ochratoxine A in spices commercialized in Italy. Food Control 39: 192-197.
Riba, A., Bouras, N., Mokrane, S., Mathieu, F., Lebrihi, A. and Sabaou, N., 2010. Aspergillus section Flavi and aflatoxins in Algerian wheat and derived products. Food and Chemical Toxicology 48: 2772-2777.
Richard, J.L., Bhatnagar, D., Peterson, S. and Sandor, G., 1992. Assessment of aflatoxin and cyclopiazonic acid production by Aspergillus flavus isolates from Hungary. Mycopathologia 120: 183-188.
Romagnoli, B., Menna, V., Gruppioni, N. and Bergamini, C., 2007. Aflatoxins in spices, aromatic herbs, herb-teas and medicinal plants marketed in Italy. Food Control 18: 697-701.
Samson, R.A., Houbraken, J.A, Kuijpers, A.F.A., Frank, M.J. and Frisvad, J.C., 2004. New ochratoxin A or sclerotium producing species in Aspergillus section Nigri. Studies in Mycology 50: 45-61.
Saxena, J. and Mehrotra, B.S., 1989. Screening of spices commonly marketed in India for natural occurrence of mycotoxins. Journal of Food Composition and Analysis 2: 286-292.
Sugita-Konishi, Y., Sato, T., Saito, S., Nakajima, M., Tabata, S., Tanaka, T., Norizuki, H, Itoh, Y, Kai, S, Sugiyama K, Kamata, Y, Yoshiike, N. and Kumagai, S., 2010. Exposure to aflatoxins in Japan: risk assessment for aflatoxin B1. Food Additives and Contaminants Part A 27: 365-372.
Varga, J., Frisvad, J.C. and Samsom, R.A., 2011. Two new aflatoxin producing species and an overview of Aspergillus section Flavi. Studies in Mycology 69: 57-80.
Zinedine, A., Brera, C., Elakhdari, S., Catano, C., Debegnac, F.R., Angelini, S., De Santis, B., Faid, M., Benlemlih, M, Minardi, V. and Miraglia, M., 2006. Natural occurrence of mycotoxins in cereals and spices commercialized in Morocco. Food Control 17: 868-874.
Aydin, A., Erkan, M.E., Baskaya, R., and Ciftcioglu, G., 2007. Determination of aflatoxin B1 levels in powdered red pepper. Food Control 18: 1015-1018.
Aziz, N.H., Youssef, Y.A., El-Fouly, M.Z. and Moussa, L.A., 1998. Contamination of some common medicinal plant samples and spices by fungi and their mycotoxins. Botanical Bulletin of Academia Sinica 39: 279-285.
Bartine, H. and Tantataoui-Elaraki, A., 1997. Growth and toxinogenesis of Aspergillus flavus isolates on selected spices. Journal of Environmental Pathology, Toxicology and Oncology 16: 61-65.
Bircan, C., 2005. The determination of aflatoxins in spices by immunoaffinity column extraction using HPLC. International Journal of Food Science and Technology 40: 929-934.
Calvo, A.M., Bok, J., Brooks, W. and Keller, N.P, 2004. VeA is required for toxin and sclerotial production in Aspergillus parasiticus. Applied and Environmental Microbiology 70: 4733-4739.
Cardwell, K.F. and Cotty, P.J., 2002. Distribution of Aspergillus section Flavi among field soils from the four agroecological zones of the Republic of Benin West Africa. Plant Disease 86: 434-439.
Cho, S.H., Lee, C.H., Jang, M.R., Son, Y.W., Lee, S.M., Choi, I.S., So-Hee Kim, S.H, and Kim, D.B., 2008. Aflatoxin contamination in spices and processed spice products commercialized in Korea. Food Chemistry 107: 1283-1288.
Colak, H., Bingol, E.B., Hampikyan, H. and Nazli, B., 2006. Determination of aflatoxin contamination in red-scaled, red and black pepper by ELISA and HPLC. Journal of Food and Drug Analysis 14: 292-296.
Criseo, G., Bagnara, A. and Bisignano, G., 2001. Differentiation of aflatoxin-producing and non-producing strains of Aspergillus flavusgroup. Letters in Applied Microbiology 33: 291-295.
El Mahgubi, A., Puel, O., Bailly, S., Tadrist, S., Querin, A., Ouadia, A., Oswald, I.P. and Bailly, J.D., 2013. Distribution and toxigenicity of Aspergillus section Flavi in spices marketed in Morocco. Food Control 32: 143-148.
El-Kady, S.S., El-Maraghy, M. and Eman Mostafa, M., 1992. Contribution of the mesophilic fungi of different spices in Egypt. Mycopathologia 120: 93-101.
Elshafie, A.E., Al-Rashdi, T.A., Al-Bahry S.N. and Bakheit, C.S., 2002. Fungi and aflatoxins associated with spices in the Sultanate of Oman. Mycopathologia 155: 155-160.
European Commission (EC), 2006. Commission Regulation no. 1881/2006 of December 19th (2006) Setting maximum levels of certain contaminants in foodstuffs. Official Journal of the European Union L364: 5-24.
Fazekas, B., Tar, A. and Kovacs, M., 2005. Aflatoxin and ochratoxin A content of spices in Hungary. Food Additives and Contaminants 22: 856-868.
Fente, C.A., Ordaz, J.J., Vazquez, B.I., Franco, C.M. and Cepeda, A., 2001. New additive for culture media for rapid identification of aflatoxin-producing Aspergillus strains. Applied and Environmental Microbiology 67: 58-62.
Food and Agriculture Organization (FAO), 2004. Regulations for mycotoxins in food and feed in 2003. FAO Food and Nutrition Paper 81. FAO, Rome, Italy.
Garrido, D., Jordal, M. and Poza, R., 1992. Mold flora and aflatoxin-producing strains of Aspergillus flavus in spices and herbs. Journal of Food Protection 55: 451-452.
Giorni, P., Magan, N., Pietri, A., Bertuzzi, T. and Battilani, P., 2007. Studies on Aspergillus section Flavi isolated from maize in northern Italy. International Journal of Food Microbiology 113: 330-338.
Hammami, W., Fiori, S., Al Thani, R., Ali Kali, N., Balmas, V., Migheli, Q. and Jaoua,S., 2014. Fungal and aflatoxin contamination of marketed spices. Food Control 37: 177-181.
Hashem, M. and Alamri, S., 2010. Contamination of common spices in Saudi Arabia markets with potential mycotoxin-producing fungi. Saudi Journal of Biological Sciences 17: 167-175.
Hitokoto, H., Morozumi, S., Wauke, T., Sakai, S. and Kurata, H. 1978. Fungal contamination and mycotoxin detection of powdered of herbal drugs. Applied and Environmental Microbiology 36: 252-256.
Horn, B.W., 2003. Ecology and population biology of aflatoxigenic fungi in soil. Journal of Toxicology – Toxin Reviews 22: 351-379.
Hua, S.T., 2003. Biocontrol of Aspergillus flavus by saprophytic yeast, progress from laboratory bioassay to field trial. In: Proceedings of the 3rd Fungal Genomics, 4th Fumonisin, and 16th Aflatoxin Elimination Workshops, October 13-15, 2003, Savannah, GA, USA.
Juglal, S., Govinden, R. and Odhav, B., 2002. Spice oils for the control of co-occurring mycotoxin-producing fungi. Journal of Food Protection 65: 683-687.
King, A.D., Hocking, A.D. and Pitt, J.I. 1979. Dichloran-rose bengal medium for enumeration and isolation of molds from foods. Applied and Environmental Microbiology 37: 959-964.
Klich, M.A, 2002. Identification of common Aspergillus species. Centraal Bureau voor Schimmel Cultures, Utrecht, the Netherlands.
Klich, M.A., 2007. Environmental and developmental factors influencing aflatoxin production by Aspergillus flavus and Aspergillus parasiticus. Mycoscience 48: 71-80.
Kong, W., Wei, R., Logrieco A., Wei J, Jing, W., Xiaoe X. and Yanga, M., 2014. Occurrence of toxigenic fungi and determination of mycotoxins by HPLC-FLD in functional foods and spices in China markets. Food Control 28: 354-361.
Kursun, O. and Mutlu, A.G., 2010. Aflatoxin in spices marketed in the west Mediterranean region of Turkey. Journal of Animal and Veterinary Advances 9: 2979-2981.
Madhyastha, M.S. and Bhat, R.V., 1985. Evaluation of substrate potentiality and inhibitory effects to identify high risk spices for aflatoxin contamination. Journal of Food Science 50: 376-378.
Magan, N. and Aldred, D., 2005. Conditions of formation of ochratoxin A in drying, transport and in different commodities. Food Additives and Contaminants 22 Suppl. 1: 10-16.
Martins, M.L., Martins, H.M. and Bernardo, F., 2001. Aflatoxins in spices marketed in Portugal. Food Additives and Contaminants 18: 315-319.
Musaiger, A.O., Al-Jedah, J.H., and De Souza, R., 2008. Occurrence of contaminants in foods commonly consumed in Bahrain. Food Control 19: 854-861.
Nguyen, M.T., Tozlovanu, M., Luyen Tran, T. and Pfohl-Leszkowicz, A., 2007. Occurrence of aflatoxin B1, citrinin and ochratoxin A in rice in five provinces of the central region of Vietnam. Food Chemistry 105: 42-47.
O’Riordan, M.J. and Wilkinson, M.G., 2008. A survey of the incidence and level of aflatoxin contamination in a range of imported spice preparations on the Irish retail market. Food Chemistry 107: 1429-1435.
Ozbey, F. and Kabak, B., 2012. Natural co-occurrence of aflatoxins and ochratoxin A in spices. Food Control 28: 354-361.
Pildain, M.B., Frisvad, J.C., Vaamonde, G., Cabral, J., Varga, D. and Samson, R.A., 2008. Two novel aflatoxin-producing Aspergillusspecies from Argentinean peanuts. International Journal of Systematic and Evolutionary Microbiology 58: 725-735.
Pildain, M.B., Vaamonde, G. and Cabral, D., 2004. Analysis of population structure of Aspergillus flavus from peanut based on vegetative compatibility, geographic origin: mycotoxin and sclerotia production. International Journal of Food Microbiology 93: 33-40.
Pitt, J.I. and Hocking, A.D., 1997. Fungi and food spoilage (2nd Ed.). Blackie Academic and Professional, London, UK, pp. 505-507.
Prelle, A., Spadaro, D., Garibaldi, A. and Gullino, M.L, 2014. Co-occurrence of aflatoxins and ochratoxine A in spices commercialized in Italy. Food Control 39: 192-197.
Riba, A., Bouras, N., Mokrane, S., Mathieu, F., Lebrihi, A. and Sabaou, N., 2010. Aspergillus section Flavi and aflatoxins in Algerian wheat and derived products. Food and Chemical Toxicology 48: 2772-2777.
Richard, J.L., Bhatnagar, D., Peterson, S. and Sandor, G., 1992. Assessment of aflatoxin and cyclopiazonic acid production by Aspergillus flavus isolates from Hungary. Mycopathologia 120: 183-188.
Romagnoli, B., Menna, V., Gruppioni, N. and Bergamini, C., 2007. Aflatoxins in spices, aromatic herbs, herb-teas and medicinal plants marketed in Italy. Food Control 18: 697-701.
Samson, R.A., Houbraken, J.A, Kuijpers, A.F.A., Frank, M.J. and Frisvad, J.C., 2004. New ochratoxin A or sclerotium producing species in Aspergillus section Nigri. Studies in Mycology 50: 45-61.
Saxena, J. and Mehrotra, B.S., 1989. Screening of spices commonly marketed in India for natural occurrence of mycotoxins. Journal of Food Composition and Analysis 2: 286-292.
Sugita-Konishi, Y., Sato, T., Saito, S., Nakajima, M., Tabata, S., Tanaka, T., Norizuki, H, Itoh, Y, Kai, S, Sugiyama K, Kamata, Y, Yoshiike, N. and Kumagai, S., 2010. Exposure to aflatoxins in Japan: risk assessment for aflatoxin B1. Food Additives and Contaminants Part A 27: 365-372.
Varga, J., Frisvad, J.C. and Samsom, R.A., 2011. Two new aflatoxin producing species and an overview of Aspergillus section Flavi. Studies in Mycology 69: 57-80.
Zinedine, A., Brera, C., Elakhdari, S., Catano, C., Debegnac, F.R., Angelini, S., De Santis, B., Faid, M., Benlemlih, M, Minardi, V. and Miraglia, M., 2006. Natural occurrence of mycotoxins in cereals and spices commercialized in Morocco. Food Control 17: 868-874.
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Aug 11, 2015
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