EVALUATION OF ASPERGILLUS NIGER CONTAMINATION AND OCCURRENCE OF CITRININ IN RED CHILLI (CAPSICUM ANNUUM) SAMPLES
DOI:
https://doi.org/10.18006/2024.12(5).694.704Keywords:
Red chilli, Mycotoxin, Aspergillus, HPLC, FTIR, CitrininAbstract
Numerous Ascomycete fungi produce toxic, low-molecular-weight secondary metabolites known as mycotoxins. Mycotoxin contamination poses a global challenge to food safety, and growing regulatory expectations regarding the presence of mycotoxins in various products have spurred increased research into detecting these toxins in food and animal feed. Mycotoxin contamination has been reported in many significant spices, including chillies. However, most research has focused on aflatoxins as primary contaminants, highlighting the need to investigate other lesser-studied mycotoxins, such as citrinin and patulin. Consequently, the current study aimed to screen for fungal contamination in locally available red chilli varieties and detect the presence of mycotoxins. Random samples of red chilli were collected to isolate and identify the fungi responsible for producing mycotoxins. High-performance liquid chromatography (HPLC) techniques and Fourier transform infrared (FTIR) spectroscopy were employed to analyze the extracted mycotoxins qualitatively. Morphological and molecular characterization through 18S rRNA sequencing of the isolated samples confirmed the presence of Aspergillus niger in red chilli. HPLC and FTIR analyses of the red chilli samples confirmed the occurrence of citrinin. Very few studies have reported the production of Citrinin by A. niger in red chilli. Further research is necessary to conduct quantitative analyses and assess the effects of citrinin on human health.
References
Agriopoulou, S., Stamatelopoulou, E., & Varzakas, T. (2020). Advances in analysis and detection of major mycotoxins in foods. Foods, 9(4), 518. https://doi.org/10.3390/foods9040518.
Ajithkumar, K., Savitha, A.S., Renuka, M., Naik, M.K. (2023). Citrinin: A Potential Mycotoxin in Food and Feed with Possible Management Strategies to Combat Its Contamination. In D. Nagaraju, S. M. Yanjarappa, P. N. Achar, & A. M. Vaya (Eds.) Anti‐Mycotoxin Strategies for Food and Feed (pp 133-154). John Wiley & Sons, Hoboken, NJ 07030, USA https://doi.org/10.1002/9781394160839.ch6.
Akintola, A., Al-Dairi, M., Imtiaz, A., Al-Bulushi, I. M., Gibreel, T., Al-Sadi, A. M., & Velazhahan, R. (2024). The Extent of Aflatoxin B1 Contamination in Chilli (Capsicum annuum L.) and Consumer Awareness and Knowledge of Aflatoxins in Oman. Agriculture, 14(9), 1536-1549. https://doi.org/10.3390/agriculture14091536
Ali, N., & Degen, G.N. (2019). Citrinin biomarkers: A review of recent data and application to human exposure assessment. Archives of Toxicology, 93, 3057–3066.
Ałtyn, I., & Twarużek, M. (2020). Mycotoxin Contamination Concerns of Herbs and Medicinal Plants. Toxins, 12(3), 182-194.
Benkerroum, N. (2020). Chronic and acute toxicities of aflatoxins mechanisms of action. International Journal of Environmental Research and Public Health, 17(2), 423-450.
Bennett, J. W., & Klich, M. (2003). Mycotoxins. Clinical Microbiology Review, 16, 497-516.
Boonzaaijer, G., van Osenbruggen, W., Kleinnijenhuis, A., & van Dongen, W. (2008). An exploratory investigation of several mycotoxins and their natural occurrence in flavor ingredients and spices, using a multi-mycotoxin LC-MS/MS method. World Mycotoxin Journal, 1(2), 167–174.
Caldeirão, L., Sousa, J., Nunes, L.C., Godoy, H.T., Fernandes, J.O., & Cunha, S.C. (2021). Herbs and herbal infusions: Determination of natural contaminants (mycotoxins and trace elements) and evaluation of their exposure. Food Research International, 144, 110322.
Carballo, D., Fernández-Franzón, M., Ferrer, E., Pallarés, N., & Berrada, H. (2021). Dietary exposure to mycotoxins through alcoholic and non-alcoholic beverages in Valencia, Spain. Toxins, 13 (7), 438.
Chatterjee, S., Dhole, A., Krishnan, A.A., & Banerjee, K. (2023). Mycotoxin Monitoring, Regulation and Analysis in India: A Success Story. Foods, 12, 705. https://doi.org/10.3390/foods12040705
Chen, L., Guo, W., Zheng, Y., Zhou, J., Liu, T., et al. (2020). Occurrence and Characterization of Fungi and Mycotoxins in Contaminated Medicinal Herbs. Toxins, 12(1), 30.
Commission Regulation (EU) 2019/1901 of 7 November 2019 amending Regulation (EC) No 1881/2006 as regards maximum levels of citrinin in food supplements based on rice fermented with red yeast Monascus purpureus (Text with EEA relevance). Retrieved from http://data.europa.eu/eli/reg/2019/1901/oj
Dandashire S.B., & Almajir, I.R. (2020). Aflatoxins and aflatoxigenic fungal contamination of common poultry feed products in Katsina State, Nigeria. Novel Research in Microbiology Journal, 4(1), 653-665.
Darab, Y., Zainal Abidin. M.A., Tan Y.H., & Kamaruzaman S. (2010). Evaluation of the detection techniques of toxigenic Aspergillus isolates. African Journal of Biotechnology, 9 (45), 7654-7659. DOI: 10.5897/AJB10.1128.
Darsana R., & Chandrasehar, G. (2021). Isolation and characterization of contaminant mycoflora from stored red peppers. Journal of Pure and Applied Microbiology, 15(3), 1187-1197. doi: 10.22207/JPAM.15.3.08
Department of Agriculture, Cooperation and Farmers Welfare. (2018). Horticultural Statistics at a Glance 2018, Ministry of Agriculture & Farmers Welfare, Government of India, pp. 1-490
Dey, D. K., Kang, J. I., Bajpai, V. K., Kim, K., Lee, H., Sonwal, S., & Shukla, S. (2022). Mycotoxins in food and feed: toxicity, preventive challenges, and advanced detection techniques for associated diseases. Critical Reviews in Food Science and Nutrition, 63(27), 8489–8510.
Doughari, J. H. (2015) The Occurrence, Properties and Significance of Citrinin Mycotoxin. Plant Pathology and Microbiology, 6 (11), 321. doi:10.4172/21577471.1000321
Enamullah, S.M., Rahman, A., Sahar, N. & Ehteshamul-Haque, S. (2022). Detection of aflatoxin contamination and incidence of fungi associated with red chilli available in local market of Karachi, Pakistan. Pakistan Journal of Botany, 54(6), 2335-2339. http://dx.doi.org/10.30848/PJB2022-6(14)
Eskola, M., Kos, G., Elliott, C.T., Hajlová, J., Mayar, S., & Krska, R. (2020). Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited 'FAO estimate' of 25. Critical Review in Food Science Nutrition, 60, 2773–2789.
FAOSTAT (2017). Agro-Statistics Database. Food and Agriculture Organization of the United Nations, Rome.
Golge, O., Hepsag, F. & Kabak, B. (2013). Incidence and level of aflatoxin contamination in chilli commercialized in Turkey. Food Control, 33 (2), 514-520. https://doi.org/10.1016/ j.foodcont.2013.03.048.
Hongyin, Z., Joseph, A., Qiya, Y., Lina, Z., Xiaoyun, Z., & Xiangfeng, Z. (2021). A review on Citrinin: Its occurrence, risk implications, analytical techniques, biosynthesis, physiochemical properties and control. Food Research International, 141, 110075. https://doi.org/10.1016/j.foodres.2020.110075.
Hossain, M.N., Talukder, A., Afroze, F., Rahim, M.M., Begum, S., Haque, M.Z., & Ahmed, M.M. (2018). Identification of aflatoxigenic fungi and detection of their aflatoxin in red chilli (Capsicum annuum) samples using direct cultural method and HPLC. Advances in Microbiology, 8(1), 42-53.
Hove, M., De Boevre, M., Lachat, C., Jacxsens, L., Nyanga, L.K., & De Saeger, S. (2016). Occurrence and risk assessment of mycotoxins in subsistence farmed maize from Zimbabwe. Food Control, 69, 36-44.
Kaya-Celiker, H., Mallikarjunan, P.K., Schmale III, D., & Christie, M.E. (2014).Discrimination of moldy peanuts with reference to aflatoxin using FTIR-ATR system. Food Control, 44, 64-71.
Kumar, S., & Suresh, D. (2019). Isolation, identification and detection of aflatoxin from date palm (Phoenix dactylifera l.). International Journal of Pharma and Bio Sciences, 10(3), 158–164.
Kutama, A.S., Muhammad A., Sani, M.D., & Mai –Abba, I. A. (2022). Isolation and identification of aflatoxin producing fungi from different foodstuffs at Shuwarin Market, Jigawa State, Nigeria. Dutse Journal of Pure and Applied Sciences, 8(1b), 9-15. https://doi.org/10.4314/dujopas.v8i1b.2
Lasram, S., Hajri, H., & Hamdi, Z. (2022). Aflatoxins and Ochratoxin A in Red Chilli (Capsicum) Powder from Tunisia: Co-Occurrence and Fungal Associated Microbiota. Journal of Food Quality and Hazards Control, 9 (1), 32-42.
Lee, H.S., Nguyen-Viet, H., Lindahl, J., Thanh, H.M., Khanh, T.N., Hien, L.T.T., & Grace, D. (2017). A survey of aflatoxin B1 in maize and awareness of aflatoxins in Vietnam. World Mycotoxin Journal, 10 (2), 195-202.
Lee, S., Kim, G. & Moon, J. (2013). Performance improvement of the one-dot lateral flow immunoassay for aflatoxin B1 by using a smartphone-based reading system. Sensors, 13(4), 5109-5116.
Li, Y., Zhang, X., Nie, J., Bacha, S.A.S., Yan, Z., & Gao, G. (2020). Occurrence and co-occurrence of mycotoxins in apple and apple products from China. Food Control, 118, 107354.
Li, Y., Zhou, Y.C., Yang, M.H., & Ou-Yang, Z. (2012). Natural occurrence of citrinin in widely consumed traditional Chinese food red yeast rice, medicinal plants and their related products. Food Chemistry, 132 (2),1040-1045. https://doi.org/10.1016/j.foodchem.2011.11.051.
Liew, W.P., & Sabran, M.R. (2022). Recent advances in immunoassay-based mycotoxin analysis and toxicogenomic technologies. Journal of Food Drug Analysis, 30(4), 23, 549-561.
Lomont, J. P., Ralbovsky, N. M., Guza, C., Saha-Shah, A., Burzynski, J., Konietzko, J., Wang, S., McHugh, P. C., Mangion, I., & Smith, J. A. (2022). Process monitoring of polysaccharide deketalization for vaccine bioconjugation development using in situ analytical methodology. Journal of Pharmaceutical and Biomedical Analysis, 209, 114533. https://doi.org/10.1016/ j.jpba.2021.114533
Mair, C., Norris, M., Donnelly, C., Leeman, D., Brown, P., Marley, E., Milligan, C., & Mackay, N. (2021). Assessment of Citrinin in Spices and Infant Cereals Using Immunoaffinity Column Clean-Up with HPLC Fluorescence Detection. Toxins, 13, 715. https://doi.org/10.3390/toxins13100715
Marin, S., Ramos, A.J., Cano-Sancho, G., & Sanchis, V. (2013). Mycotoxins: Occurrence, toxicology, and exposure assessment. Food and Chemical Toxicology, 60, 218–237.
Meerpoel, C., & Vidal, A. (2021). Dietary exposure assessment and risk characterization of citrinin and ochratoxin A in Belgium. Food and Chemical Toxicology, 147, 111914.
Moradi, M., Fani, S. R., Dargahi, R., Moghadam, M., & Sherafati, A. (2017). A simple procedure to evaluate competitiveness of toxigenic and atoxigenic isolates of Aspergillus flavus in solid and liquid media. Journal of Chemical Health Risks, 7, 105–112.
Myresiotis, C.K., Testempasis, S., Vryzas, Z., Karaoglanidis, G.S., & Papadopoulou-Mourkidou, E. (2015). Determination of mycotoxins in pomegranate fruits and juices using a QuEChERS-based method. Food Chemistry, 182, 81–88.
Omar, S. S (2016). Aflatoxin M1 levels in raw milk, pasteurized milk and infant formula. Italian Journal of Food Safety, 5(3), 5788.
Omotayo, O.P., Omotayo, A.O., Mwanza, M., & Babalola, O.O. (2019). Prevalence of mycotoxins and their consequences on human health. Toxicological Research, 35(1),1-7.
Pereira, V. L., Fernandes, J.O., & Cunha, S.C. (2014). Mycotoxins in cereals and related foodstuffs: A review on occurrence and recent methods of analysis. Trends in Food Science and Technology, 36(2), 96–136.
Pickova, D., Ostry, V., Toman, J., & Malir, F. (2021). Aflatoxins: history, significant milestones, recent data on their toxicity and ways to mitigation. Toxins, 13(6), 399.
Rajarajan, P. N., Rajasekaran, K. M., & Devi, N. K. A. (2013). Isolation and quantification of aflatoxin from Aspergillus flavus infected stored peanuts. Indian Journal of Pharmaceutical and Biological Research, 1(04), 76.
Rajarajan, P., Sylvia, K., Periasamy, M.P., & Subramanian, M. (2021). Detection of aflatoxin producing Aspergillus flavus from animal feed in Karnataka, India. Environmental Analysis Health and Toxicology, 36(3), e2021017. DOI: https://doi.org/10.5620/eaht.2021017
Rajendran, S., Shunmugam, G., Vaikuntavasen, P., Palanisamy, J., & Subbiah. S. (2021). Isolation and Screening of Chilli Pepper for Fungal Contamination and Aflatoxin Production. International Journal of Plant & Soil Science, 33(9), 20-25. https://doi.org/10.9734/ijpss/2021/v33i930462
Rasheva, T.V., Nedeva, T.S., Hallet, J.N., & Kujumdzieva, A.V. (2003).Characterization of a non-pigment producing Monascus purpureus mutant strain. Antonie van Leeuwenhoek, 83, 333–340.
Richard, J.L. (2007). Some major mycotoxins and their mycotoxicoses- An overview. International Journal of Food Microbiology, 119(1-2), 3-10.
Rocha, A. R., Cardoso, M.S., Júnior, J.A.S., Júnior, E. A. G., Maciel, L. F., & Menezes-Filho, J.A. (2023). Occurrence of aflatoxins B1, B2, G1, and G2 in beers produced in Brazil and their carcinogenic risk evaluation. Food Control, 145, 109348.
Romagnoli, B., Menna, V., Gruppioni. N., & Bergamini, C. (2007) Aflatoxins in Spices, Aromatic Herbs, Herbs-Teas and Medicinal Plants Marketed in Italy. Food Control, 18, 697-701. https://doi.org/10.1016/j.foodcont.2006.02.020
Ruan, H., Lu, Q., Wu, J., Qin, J., Sui, M., et al. (2022). Hepatotoxicity of food-borne mycotoxins: molecular mechanism, anti-hepatotoxic medicines and target prediction. Critical Reviews in Food Science and Nutrition, 62(9), 2281-2308.
Sadhasivam, S., Barda, O., Zakin, V., Reifen, R., & Sionov, E. (2021). Rapid detection and quantification of patulin and citrinin contamination in fruits. Molecules, 26, 4545. https://doi.org/10.3390/molecules26154545
Sadhasivam, S., Britzi, M., Zakin, V., Kostyukovsky, M., Trostanetsky, A., Quinn, E., & Sionov, E. (2017). Rapid detection and identification of mycotoxigenic fungi and mycotoxins in stored wheat grain. Toxins, 9(10): 10. https://doi.org/10.3390/ toxins9100302
Sahu, P.K., Purohit, S., Tripathy, S., Mishra, D. P., & Acharya, B. (2023). Current Trends in HPLC for Quality Control of Spices. In O. Núñez, S. Sentellas, M. Granados, & J. Saurina (Eds.) High Performance Liquid Chromatography - Recent Advances and Applications. Intech open publication. DOI: 10.5772/ intechopen.110897.
Samyal, S., & Sumbali, G. (2020). Mycological Society of India, Toxigenic mycoflora and natural co-occurrence of toxins in red chillies from Jammu and Kashmir. Kavaka, 54, 89–95. doi:10.36460/Kavaka/54/2020/89-95,
Samyal, S., & Sumbali, G. (2021). Natural incidence of Aspergilli, Penicilli, Fusaria and their multiple toxins in the seeds of dried red chillies (Capsicum annuum Linn.) from Jammu and Kashmir (UT). Indian Phytopathology, 74, 95–102. DOI: https://doi.org/10.1007/s42360-020-00291-2
Schmidt-Heydt, M., Cramer, B., Graf, I., Lerch, S., Humpf, H. U., & Geisen, R. (2012).Wavelength-dependent degradation of ochratoxin and citrinin by light in vitro and in vivo and its implications on Penicillium. Toxins, 4(12), 1535–1551.
Setlem, S.K., & Ramlal, S. (2022).Isolation, extraction and identification of aflatoxin producing Aspergillus fungi by HPLC analysis and its sequencing. Clinical Case Reports International, 6, 1393.
Shekhar, M., Singh, N., Dutta, R., Kumar, S., & Mahajan, V. (2017). Comparative study of qualitative and quantitative methods to determine toxicity level of Aspergillus flavus isolates in maize. PLoS ONE, 12(12), e0189760. https://doi.org/10.1371/ journal.pone.0189760
Singh, P., & Cotty, P.J. (2017). Characterization of Aspergilli from dried red chillies (Capsicum spp.): Insights into the etiology of aflatoxin contamination. International Journal of Food Microbiology, 289, 145-153. https://doi.org/10.1016/ j.ijfoodmicro.2018.08.025.
Theumer, M.G., Henneb, Y., Khoury, L., Snini, S.P., Tadrist, S., et al. (2018). Genotoxicity of aflatoxins and their precursors in human cells. Toxicology Letters, 287, 100- 107.
Tola, M., & Kebede, B. (2016). Occurrence, importance and control of mycotoxins: A review. Cogent Food & Agriculture, 2(1), 1191103.
Tsehaynesh, T., Abdi, M., Hassen, S., & Taye, W. (2021). Aspergillus species and aflatoxin contamination in pepper (Capsicum annuuml.) in West Gojjam, Ethiopia. African Journal of Food, Agriculture, Nutrition and Development, 21(1), 17178-17194. DOI: https://doi.org/10.18697/ajfand.96.18815
Wang, W., Chen, Q., Zhang, X., Zhang, H., Huang, Q., Li, D., & Yao, J. (2014).Comparison of extraction methods for analysis of citrinin in red fermented rice. Food Chemistry, 157, 408–412. https://doi.org/10.1016/j.foodchem.2014.02.060.
Wang, Y., Wang, B., Wang, P., Hua, Z., Zhang S., Wang, X., Yang, X., & Zhang, C. (2024). Review of neurotoxicity of T-2 toxin. Mycotoxin Research, 40(1), 85-95. doi: 10.1007/s12550-024-00518-5.
Watanabe, T. (2018). Pictorial Atlas of Soilborne Fungal Plant Pathogens and Diseases. CRC Press.
Weidemann, D.K., Weaver, V.M., & Fadrowski, J.J. (2016).Toxic environmental exposures and kidney health in children. Pediatric Nephrology, 31, 2043–2054.
Wokorach, G., Landschoot, S., Anena, J., Audenaert, K., Echodu, R., & Haesaert, G. (2021). Mycotoxin profile of staple grains in northern Uganda: Understanding the level of human exposure and potential risks. Food Control, 122, 107813.
Yogendrarajah, P. (2015). Risk assessment of mycotoxins and predictive mycology in Sri Lankan spices: Chilli and Pepper. PhD dissertation, Faculty of Bioscience Engineering, Ghent University, Belgium.
Younis, M. R., Wang, C., Younis, M.A., & Xia, X.H. (2020).Use of biosensors for mycotoxins analysis in food stuff. In A. Wu, & W. S. Khan (Eds.) Nanobiosensors: From design to applications (pp. 171-201). Wiley-VCH Verlag GmbH & Co. KGaA, Boschstr. 12, 69469 Weinheim, Germany. https://doi.org/10.1002/ 9783527345137.ch8.
Zhang, X., Li, Y., Wang, H., Gu, X., Zheng, X., et al. (2016). Screening and identification of novel Ochratoxin A producing fungi from grapes. Toxins, 8, 333.
Zhao, Z., Yang, X., Zhao, X., Chen, L., Bai, B., Zhou, C., & Wang, J. (2018). Method development and validation for the analysis of emerging and traditional fusarium mycotoxins in pepper, potato, tomato, and cucumber by UPLC-MS/MS. Food Analytical Methods, 11, 1780–1788.
Downloads
Published
How to Cite
License
Copyright (c) 2024 Journal of Experimental Biology and Agricultural Sciences
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
