Research Article
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Investıgatıon of Natural Mycoflora and Aflatoxin Formation in Hazelnuts and Products

Year 2019, Volume: 40 Issue: 4, 967 - 977, 31.12.2019
https://doi.org/10.17776/csj.644503

Abstract

In this study, natural mycoflora of 30 raw and 50
roasted hazelnut, 20 hazelnut paste and 50 inner membrane samples and their
total aflatoxin contents were determined. In mycological isolations, 1.8-2.56%
of Aspergillus flavus and 42.7-65.44%
of A. niger were determined in the
raw hazelnut samples. A. flavus
(2.2-12.2%) and A. niger (33.3-74.5%)
were also detected in roasted hazelnut, while the percentages of these
microorganisms in hazelnut paste samples were 0-13.1% and 43.5-100.0%,
respectively. The ratio of A. flavus
and A. niger in inner membranes was
found to be 2.6-16.2% and 44.6-89.4%, respectively. Aflatoxin analysis showed
that the levels of aflatoxin were 2.11–10.03 ppb in raw hazelnut, 0.1–4.04 ppb
in roasted hazelnut, 0.2-6.02 ppb in hazelnut paste samples and 0.7-38.2 ppb in
inner membrane samples. While only one of the raw hazelnut, roasted hazelnut
and hazelnut paste samples had toxin above the legal limit, 100% of the inner
membrane samples showed different levels of aflatoxin contamination. Since
there is no limitation in the Turkish Food Codex on hazelnut inner membrane,
the amount of aflatoxin, which is higher than 10 ppb in 25 of the samples, was
considered to be high contamination. Kruskal Wallis and Mann Whitney U analyses
were used for statistical evaluation of the samples. There was a significant
difference in aflatoxin formation and moisture content between the samples in
different groups (p <0.05).

Supporting Institution

CÜBAP

Project Number

CÜBAP-434

Thanks

This study was accepted by the Institute of Science and Technology of Sivas Cumhuriyet University and supported financially by the Scientific Research Council of Sivas Cumhuriyet University (CÜBAP M-434).

References

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  • [2] Alasavar C., Shahidi F., Liyanapathirana C.M., Oshima T., Turkish Tombul Hazelnut (Corylus Avellena L.) 1. Compositional Characteristics, Journal of Agricultural and Food Chemistry, 51(2003) 3790–3796.
  • [3] Alasalvar C, Amaral JS, Shahidi F.. Functional lipid characteristics of Turkish Tombul hazelnut (Corylus avellana L.). J Agric Food Chem. 54 (2006) 10117–10183.
  • [4] Durak I., Köksal I., Kacmaz M., Büyükkocak S., Cimen B.M.Y., Ozturk H.S., Hazelnut supplementation enhances plasma antioxidant potential and lowers plasma cholesterol levels. Clinica Chimica Acta. 284 (1999) 113–115.
  • [5] Maguire L.S., O’Sullvian S.M., Galvin K., O’Connor T.P., Brien N.M., Fatty acid profile, tocopherol, squalene, and phytosterol content of walnut, almonds, peanuts, hazelnuts, and macadamia nut. Int J Food Sci. 3 (2004) 171–178.
  • [6] Shahidi F., Alasalvar C., Liyana-Patharina C.M., Antioxidant and phytochemicals in hazelnut kernel (Corylus avellana L.) and hazelnut by-products. J Agric Food Chem. 55 (2007) 1212–1220.
  • [7] Quillien J.F., Mycotoxins. (2002) http://www.fevia.be/pdf/20pagers/synth/mycotoxins.pdf.
  • [8] Hussain I., and Anwar J., A study on contamination of aflatoxin M1 in raw milk in the Punjab province of Pakistan. Food Control 19 (2008) 393–395.
  • [9] Samuel M.S., Sivaramakrishna A., Mehta, A., Degradation and detoxification of aflatoxin B1 by Pseudomonas putida. Int. Biodeterioration and Biodegradation, 86 (2014) 202-209.
  • [10] Bullerman L.B., Schroeder L. L., Park K.Y., Formation and Control of Mycotoxins in Food, Journal of Food Protection, 47 (1984) 637-646.
  • [11] Severns D. E., Clements M. J., Lambert R. J., and White D. G., Comparison of Aspergillus ear rot and aflatoxin contamination in grain of high oil and normal oil corn hybrids. J. Food Prot. 66 (2003) 637–643.
  • [12] Alsuhaibani, A.M.A., Effects of Storage Periods and Temperature on Mold Prevalence and Aflatoxin Contamination in Nuts. Pak. J. Nutr., 17 (2018) 219-227.
  • [13] Amaike S.A., and Keller N.P., Aspergillus flavus. Annu.Rev.Phytopath. 49 (2011)107–133.
  • [14] Kensler T.W., Roebuck B.D., Wogan G.N., and Groopman J.D., Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology. Toxicol.Sci.120 (2011) 28–48.
  • [15] Roze L.V., Hong S.Y., and Linz J.E., Aflatoxin biosynthesis: current frontiers. Annu. Rev. Food Sci.Technol.4 (2013) 293–311.
  • [16] IARC., Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins, in IARC Monographs on The Evaluation of Carcinogenic Risks to Humans, 56 (1993) 489–521.
  • [17] Afsah-Hejri L., Jinap S., Arzandeh S., Mirhosseini H., Optimization of HPLC conditions for quantitative analysis of aflatoxins in contaminated peanut. Food Control, 22 (2011) 381-388.
  • [18] Ding X., Peiwu L., Bai Y., Zhou H., Aflatoxin B1 in post-harvest peanuts and dietary risk in China. Food Control, 23 (2012) 143-148.
  • [19] Chen Y.C., Liao C.D., Lin H.Y., Chiueh L.C., Survey of aflatoxin contamination in peanut products in Taiwan from 1997 to 2011. Journal of Food and Drug Analysis, 21 (2013) 247-252.
  • [20] Torres A.M., Barros G.G.. Palacios S.A. Chulze S.N., Battilani P., Review on pre- and post-harvest management of peanuts to minimize aflatoxin contamination. Food Research International, 62 (2014) 11-19.
  • [21] Kumar P., Dipendra K.M., Madhu K., Tapan K.M., and Sang G.K., Aflatoxins: A Global Concern for Food Safety, Human Health and Their Management. Frontiers in Microbiology, 2 (7) (2017) 2170.
  • [22] Bakker F.W., Grains and Grain Quality. CIGR Handbook of Agricultural Engineering, Volume IV Agro-Processing Engineering. The American Society of Agricult. Eng. (1999) 1-3.
  • [23] Özkaya H., Analitik Gıda Kalite Kontrolü, Ankara Üniv. Ziraat Fak. Yay. 108 s., Ankara.
  • [24] Raper K.B. and Fennell, D.I., The Genus Aspergillus. Robert E. Krieger Publishing Company Huntington, New York, (1977) 686.
  • [25] Samson R.A. and Pitt I.J., Modern Concepts in Penicillium and Aspergillus Classification, NATO ASI Series, Plenum Press, New York and London, 185 (1990) 478.
  • [26] Samson R.A, Stolk A.C., Hadlock R., Revision of The Subsection Fasciculata of Penicillium and Some Allied Species, Stud. Mycol. Baarn, 11 (1976) 1-47.
  • [27] Pitt J.I. A Laboratory Guide to Common Penicillium Species, Food Science, Australia, Mycologia, 93 (2000) 689–703.
  • [28] Barnet H.L. and Hunter B.B., Illustrated Genera of Imperfect Fungi, Third Edition, Burgess Publishing Company (1997).
  • [29] Çetin Ö., Nazlı B., Bostan K., Alperden İ., Depolamanın Çiğ İç Fındığın Kalitesi Üzerine Etkileri, İst. Vet. Fak. Der., 26 (2000) 413-419.
  • [30] Aluç M., Aluç S., Akçakoca, Ordu ve Giresun Yörelerinde Yetiştirilen Fındıklarda Aflatoksin Düzeyinin Belirlenmesi Üzerine Bir Çalışma, Ulusal Mikotoksin Sempozyumu. İstanbul (2003) 60-67.
  • [31] Heperkan D., The Importance of Mycotoxins and a Brief History of Mycotoxin Studies in Turkey, The Bulletin İstanbul Tech. Uni.,54 (2003) 18-27.
  • [32] Gürsoy, N., Çiğ ve Kavrulmuş Fındıklardaki Mikoflora ve Aflatoksin Bulaşıklıklarının Değerlendirilmesi, Türkiye 10. Gıda Kongresi (2008) Erzurum.
  • [33] Jimenez M., Mateo R., Quero, A., Huerta T., Hernandez E., Mycotoxins and Mycotoxigenic Moulds in Nuts and Sunflower Seeds for Human Consumption, Mycopathologia,115 (1991) 121-7.
  • [34] Deabes M,. and Al- Habib R., Toxigenic Fungi and Aflatoxin Associated to Nuts in Saudi Arabia, Journal of American Science, 7 (2011) 658-665.
  • [35] Gürses M., Mycoflora and Aflatoxin Content of Hazelnuts, Walnuts, Peanuts, Almonds and Roasted Chickpeas (Leblebi) Sold in Turkey, J. of Food Properties, 9 (2006) 39-399.
  • [36] Ostadrahimi A., Ashrafnejad F., Kazemi A., Sargheini N., Mahdavi R., Farshchian M., Aflatoxin in raw and salt-roasted nuts (pistachios, peanuts and walnuts) sold in markets of Tabriz, İran. Jundishapur. J Microbiol. 7 (2014) 8674.
  • [37] Abdel Hafez A.I.I., Saber S.M., Mycoflora and Mycotoxin of Hazelnut (Corylus Avellana L.) and Walnut (Juglans Regia L.) Seeds in Egypt, 148 (1993) 137-147.
  • [38] Demir C., Şimşek O., Hamzacebi H ., Fındıkta Küf Florası ve Aflatoksin Oluşumlarının Araştırılması. Gıda 22 (2002) 291-295.
  • [39] Şimşek O., Arici M., Demir C., Mycoflora of Hazelnut ( Corylus avellana L.) and Aflatoxin Content in Hazelnut Kernels Artifically Infected with Aspergillus parasiticus, Food Science and Technology, 46 (2002) 194-196.
  • [40] Ayçiçek H., Aksoy A., Saygı S., Determination of Aflatoxin Levels in Some Dairy and Food Products Which Consumed in Ankara, Turkey, Food Control, 16 (2005) 263-266.
  • [41] Sanchis V., Quilez M. L., Viladrich R., Vinas I., Canela R., Hazelnuts as Possible Substrate for Aflatoxin Production, Journal Food Protection, 51 (1988) 289-292.
  • [42] Reddy M.J., Shetty H.S., Role of Seed Lipids in Aspergillus parasiticus Growth and Aflatoxin Production, Journal of the Science of Food and Agriculture, 59 (1992) 177 -181.
  • [43] Baltaci C., İlyasoğlu H., Cavrar S., Aflatoxin levels in raw and processed hazelnuts in Turkey. Food Additives and Contaminants: Part B 5 (2012) 83–86
  • [44] Çöpür Y., Tozluoglu A., Özkan M., Evaluating pretreatment techniques for converting hazelnut husks to bioethanol. Bioresource Technology, 129 (2013) 182–90.
  • [45] Velioğlu S.D., Güner K.G., Velioğlu H.M., Çelikyurt G., Fındık Zarının Fırıncılık Ürünlerinde Kullanımı. Journal of Tekirdag Agricultural Faculty, 14 (2017) 34-38.
  • [46] Özer H., Fındıklara Uygulanan Fiziksel ve Isıl Süreçlerde Aflatoksinler Üzerinde Etkisi, Doktora Tezi, Yıldız Teknik Üniversitesi Fen Bilimleri Enstitüsü, İstanbul (2009) 119.
  • [47] Vural A., Çakmak Ö., Erkan M. E., Aydın A. İstanbul Bölgesinde Tüketime Sunulan Fındık Ezmelerinde Aflatoksin Düzeylerinin Belirlenmesi, II. Ulusal Mikotoksin Sempozyumu Bildiriler Kitabı (2005) 178.
  • [48] Günşen U. and Büyükyörük I., Aflatoxins in Retail Food Products in Bursa, Turkey, Veterinary and Human Toxicology, 44 (2002) 289–290.
  • [49] [49] Yu J., Chang, P.K., Bhatnagar, D., Cleveland, T.E., Cloning of a sugar utilization gene cluster in Aspergillus parasiticus. Biochim. Biophys. Acta 1493 (2000) 211–214.
Year 2019, Volume: 40 Issue: 4, 967 - 977, 31.12.2019
https://doi.org/10.17776/csj.644503

Abstract

Project Number

CÜBAP-434

References

  • [1] TUIK., Agricultural production values. www.tuik.gov.tr (2016). (Access date: 09/09/2018).
  • [2] Alasavar C., Shahidi F., Liyanapathirana C.M., Oshima T., Turkish Tombul Hazelnut (Corylus Avellena L.) 1. Compositional Characteristics, Journal of Agricultural and Food Chemistry, 51(2003) 3790–3796.
  • [3] Alasalvar C, Amaral JS, Shahidi F.. Functional lipid characteristics of Turkish Tombul hazelnut (Corylus avellana L.). J Agric Food Chem. 54 (2006) 10117–10183.
  • [4] Durak I., Köksal I., Kacmaz M., Büyükkocak S., Cimen B.M.Y., Ozturk H.S., Hazelnut supplementation enhances plasma antioxidant potential and lowers plasma cholesterol levels. Clinica Chimica Acta. 284 (1999) 113–115.
  • [5] Maguire L.S., O’Sullvian S.M., Galvin K., O’Connor T.P., Brien N.M., Fatty acid profile, tocopherol, squalene, and phytosterol content of walnut, almonds, peanuts, hazelnuts, and macadamia nut. Int J Food Sci. 3 (2004) 171–178.
  • [6] Shahidi F., Alasalvar C., Liyana-Patharina C.M., Antioxidant and phytochemicals in hazelnut kernel (Corylus avellana L.) and hazelnut by-products. J Agric Food Chem. 55 (2007) 1212–1220.
  • [7] Quillien J.F., Mycotoxins. (2002) http://www.fevia.be/pdf/20pagers/synth/mycotoxins.pdf.
  • [8] Hussain I., and Anwar J., A study on contamination of aflatoxin M1 in raw milk in the Punjab province of Pakistan. Food Control 19 (2008) 393–395.
  • [9] Samuel M.S., Sivaramakrishna A., Mehta, A., Degradation and detoxification of aflatoxin B1 by Pseudomonas putida. Int. Biodeterioration and Biodegradation, 86 (2014) 202-209.
  • [10] Bullerman L.B., Schroeder L. L., Park K.Y., Formation and Control of Mycotoxins in Food, Journal of Food Protection, 47 (1984) 637-646.
  • [11] Severns D. E., Clements M. J., Lambert R. J., and White D. G., Comparison of Aspergillus ear rot and aflatoxin contamination in grain of high oil and normal oil corn hybrids. J. Food Prot. 66 (2003) 637–643.
  • [12] Alsuhaibani, A.M.A., Effects of Storage Periods and Temperature on Mold Prevalence and Aflatoxin Contamination in Nuts. Pak. J. Nutr., 17 (2018) 219-227.
  • [13] Amaike S.A., and Keller N.P., Aspergillus flavus. Annu.Rev.Phytopath. 49 (2011)107–133.
  • [14] Kensler T.W., Roebuck B.D., Wogan G.N., and Groopman J.D., Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology. Toxicol.Sci.120 (2011) 28–48.
  • [15] Roze L.V., Hong S.Y., and Linz J.E., Aflatoxin biosynthesis: current frontiers. Annu. Rev. Food Sci.Technol.4 (2013) 293–311.
  • [16] IARC., Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins, in IARC Monographs on The Evaluation of Carcinogenic Risks to Humans, 56 (1993) 489–521.
  • [17] Afsah-Hejri L., Jinap S., Arzandeh S., Mirhosseini H., Optimization of HPLC conditions for quantitative analysis of aflatoxins in contaminated peanut. Food Control, 22 (2011) 381-388.
  • [18] Ding X., Peiwu L., Bai Y., Zhou H., Aflatoxin B1 in post-harvest peanuts and dietary risk in China. Food Control, 23 (2012) 143-148.
  • [19] Chen Y.C., Liao C.D., Lin H.Y., Chiueh L.C., Survey of aflatoxin contamination in peanut products in Taiwan from 1997 to 2011. Journal of Food and Drug Analysis, 21 (2013) 247-252.
  • [20] Torres A.M., Barros G.G.. Palacios S.A. Chulze S.N., Battilani P., Review on pre- and post-harvest management of peanuts to minimize aflatoxin contamination. Food Research International, 62 (2014) 11-19.
  • [21] Kumar P., Dipendra K.M., Madhu K., Tapan K.M., and Sang G.K., Aflatoxins: A Global Concern for Food Safety, Human Health and Their Management. Frontiers in Microbiology, 2 (7) (2017) 2170.
  • [22] Bakker F.W., Grains and Grain Quality. CIGR Handbook of Agricultural Engineering, Volume IV Agro-Processing Engineering. The American Society of Agricult. Eng. (1999) 1-3.
  • [23] Özkaya H., Analitik Gıda Kalite Kontrolü, Ankara Üniv. Ziraat Fak. Yay. 108 s., Ankara.
  • [24] Raper K.B. and Fennell, D.I., The Genus Aspergillus. Robert E. Krieger Publishing Company Huntington, New York, (1977) 686.
  • [25] Samson R.A. and Pitt I.J., Modern Concepts in Penicillium and Aspergillus Classification, NATO ASI Series, Plenum Press, New York and London, 185 (1990) 478.
  • [26] Samson R.A, Stolk A.C., Hadlock R., Revision of The Subsection Fasciculata of Penicillium and Some Allied Species, Stud. Mycol. Baarn, 11 (1976) 1-47.
  • [27] Pitt J.I. A Laboratory Guide to Common Penicillium Species, Food Science, Australia, Mycologia, 93 (2000) 689–703.
  • [28] Barnet H.L. and Hunter B.B., Illustrated Genera of Imperfect Fungi, Third Edition, Burgess Publishing Company (1997).
  • [29] Çetin Ö., Nazlı B., Bostan K., Alperden İ., Depolamanın Çiğ İç Fındığın Kalitesi Üzerine Etkileri, İst. Vet. Fak. Der., 26 (2000) 413-419.
  • [30] Aluç M., Aluç S., Akçakoca, Ordu ve Giresun Yörelerinde Yetiştirilen Fındıklarda Aflatoksin Düzeyinin Belirlenmesi Üzerine Bir Çalışma, Ulusal Mikotoksin Sempozyumu. İstanbul (2003) 60-67.
  • [31] Heperkan D., The Importance of Mycotoxins and a Brief History of Mycotoxin Studies in Turkey, The Bulletin İstanbul Tech. Uni.,54 (2003) 18-27.
  • [32] Gürsoy, N., Çiğ ve Kavrulmuş Fındıklardaki Mikoflora ve Aflatoksin Bulaşıklıklarının Değerlendirilmesi, Türkiye 10. Gıda Kongresi (2008) Erzurum.
  • [33] Jimenez M., Mateo R., Quero, A., Huerta T., Hernandez E., Mycotoxins and Mycotoxigenic Moulds in Nuts and Sunflower Seeds for Human Consumption, Mycopathologia,115 (1991) 121-7.
  • [34] Deabes M,. and Al- Habib R., Toxigenic Fungi and Aflatoxin Associated to Nuts in Saudi Arabia, Journal of American Science, 7 (2011) 658-665.
  • [35] Gürses M., Mycoflora and Aflatoxin Content of Hazelnuts, Walnuts, Peanuts, Almonds and Roasted Chickpeas (Leblebi) Sold in Turkey, J. of Food Properties, 9 (2006) 39-399.
  • [36] Ostadrahimi A., Ashrafnejad F., Kazemi A., Sargheini N., Mahdavi R., Farshchian M., Aflatoxin in raw and salt-roasted nuts (pistachios, peanuts and walnuts) sold in markets of Tabriz, İran. Jundishapur. J Microbiol. 7 (2014) 8674.
  • [37] Abdel Hafez A.I.I., Saber S.M., Mycoflora and Mycotoxin of Hazelnut (Corylus Avellana L.) and Walnut (Juglans Regia L.) Seeds in Egypt, 148 (1993) 137-147.
  • [38] Demir C., Şimşek O., Hamzacebi H ., Fındıkta Küf Florası ve Aflatoksin Oluşumlarının Araştırılması. Gıda 22 (2002) 291-295.
  • [39] Şimşek O., Arici M., Demir C., Mycoflora of Hazelnut ( Corylus avellana L.) and Aflatoxin Content in Hazelnut Kernels Artifically Infected with Aspergillus parasiticus, Food Science and Technology, 46 (2002) 194-196.
  • [40] Ayçiçek H., Aksoy A., Saygı S., Determination of Aflatoxin Levels in Some Dairy and Food Products Which Consumed in Ankara, Turkey, Food Control, 16 (2005) 263-266.
  • [41] Sanchis V., Quilez M. L., Viladrich R., Vinas I., Canela R., Hazelnuts as Possible Substrate for Aflatoxin Production, Journal Food Protection, 51 (1988) 289-292.
  • [42] Reddy M.J., Shetty H.S., Role of Seed Lipids in Aspergillus parasiticus Growth and Aflatoxin Production, Journal of the Science of Food and Agriculture, 59 (1992) 177 -181.
  • [43] Baltaci C., İlyasoğlu H., Cavrar S., Aflatoxin levels in raw and processed hazelnuts in Turkey. Food Additives and Contaminants: Part B 5 (2012) 83–86
  • [44] Çöpür Y., Tozluoglu A., Özkan M., Evaluating pretreatment techniques for converting hazelnut husks to bioethanol. Bioresource Technology, 129 (2013) 182–90.
  • [45] Velioğlu S.D., Güner K.G., Velioğlu H.M., Çelikyurt G., Fındık Zarının Fırıncılık Ürünlerinde Kullanımı. Journal of Tekirdag Agricultural Faculty, 14 (2017) 34-38.
  • [46] Özer H., Fındıklara Uygulanan Fiziksel ve Isıl Süreçlerde Aflatoksinler Üzerinde Etkisi, Doktora Tezi, Yıldız Teknik Üniversitesi Fen Bilimleri Enstitüsü, İstanbul (2009) 119.
  • [47] Vural A., Çakmak Ö., Erkan M. E., Aydın A. İstanbul Bölgesinde Tüketime Sunulan Fındık Ezmelerinde Aflatoksin Düzeylerinin Belirlenmesi, II. Ulusal Mikotoksin Sempozyumu Bildiriler Kitabı (2005) 178.
  • [48] Günşen U. and Büyükyörük I., Aflatoxins in Retail Food Products in Bursa, Turkey, Veterinary and Human Toxicology, 44 (2002) 289–290.
  • [49] [49] Yu J., Chang, P.K., Bhatnagar, D., Cleveland, T.E., Cloning of a sugar utilization gene cluster in Aspergillus parasiticus. Biochim. Biophys. Acta 1493 (2000) 211–214.
There are 49 citations in total.

Details

Primary Language English
Journal Section Engineering Sciences
Authors

Z. Seba Keskin 0000-0003-1334-5158

Nevcihan Gürsoy 0000-0002-6573-0763

Project Number CÜBAP-434
Publication Date December 31, 2019
Submission Date November 8, 2019
Acceptance Date December 11, 2019
Published in Issue Year 2019Volume: 40 Issue: 4

Cite

APA Keskin, Z. S., & Gürsoy, N. (2019). Investıgatıon of Natural Mycoflora and Aflatoxin Formation in Hazelnuts and Products. Cumhuriyet Science Journal, 40(4), 967-977. https://doi.org/10.17776/csj.644503