A review of patulin, “the mycotoxin of apples”, and its methods of detection
Abstract
As a consequence of their development on food and feed, filamentous fungi are able to synthesize, as secondary metabolites, toxic elements with low molecular weight, named mycotoxins. The mycotoxin named patulin is synthesized by different fungal species, in different fruits, vegetables, cereals or nuts, but it is characteristic to apple fruits and derived products. Among the fungal species, the main patulin producer in apples is Penicillium expansum Link, which causes the blue mold (soft rot) in the fruits during storage period. With P. expansum contamination come several risks regarding financial losses for the farmers and the health of the consumers, in case of mycotoxin-contaminated product ingestion. Because of its chemical stability, heat-resistance and water-solubility, patulin can’t be destroyed completely by processing. The biggest worry about patulin is its possible presence not only in fruit juices and purees, but in baby food too. Taking into consideration the great number of negative effects patulin ingestion has on human health (immunodepressant, neurotoxic, teratogenic, gastrointestinal side effects and others), the EU needed to establish maximum tolerable levels in juices and other derivatives. As set by the European regulation 1425/2003, the highest accepted patulin level in apple juice is 50 µg/l, 25 µg/l in solid apple products and 10 µg/l in apple-based baby foods. For manufacturers and authorities, analytical procedures for patulin determination are important tools, in order to be able to provide high levels of food and feed safety. In the detection and quantification of patulin, various chromatographic techniques dominate, but alternatives, such as immunological assays and biosensors, start to gain more and more attention. This paper aims to provide a general overview of patulin and a brief description of the various methods used for its identification in apple-based products.
References
Al-Jaal, B., Salama, S., Al-Qasmi, N., & Jaganjac, M. (2019), Mycotoxin contamination of food and feed in the Gulf Cooperation Council countries and its detection. Toxicon, 171, pp. 43-50
Bacha, S. A. S., Li, Y., Nie, J., Xu, G., Han, L., & Farooq, S. (2023), Comprehensive review on patulin and Alternaria toxins in fruit and derived products. Frontiers in Plant Science, 14
Baert, K., De Meulenaer, B., Kamala, A., Kasase, C., & Devlieghere, F. (2006), Occurrence of Patulin in Organic, Conventional, and Handcrafted Apple Juices Marketed in Belgium. Journal of Food Protection, 69(6), pp. 1371-1378
Camara, J.S., Fernandes, P., Barros, N., & Perestrelo, R. (2023), An Improved Analytical Approach Based on µ-QuEChERS Combined with LC-ESI/MS for Monitoring the Occurrence and Levels of Patulin in Commercial Apple Juices. Separations, 10(3), 149
Coton, M., Bregier, T., Poirier, E., Debaets, S., Arnich, N., Coton, E., & Dantigny, P. (2020), Production and migration of patulin in Penicillium expansum molded apples during cold and ambient storage. International Journal of Food Microbiology, 313
Cunha, S. C., Faria, M. A., Pereira, V. L., Oliveira, T. M., Lima, A. C., & Pinto, E. (2014), Patulin assessment and fungi identification in organic and conventional fruits and derived products. Food Control, 44, pp.185-190
Daou, R., Joubrane, K., Maroun, R. G., Khabbaz, L. R., Ismail, A., & El Khoury, A. (2021), Mycotoxins: Factors influencing production and control strategies. AIMS Agriculture and Food, 6(1), pp. 416-447
dos Santos, I. D., Pizzutti, I. R., Dias, J. V., Fontana, M. E. Z., Brackmann, A., Anese, R. O., Thewes, F. R., Marques, L. N., & Cardoso, C. D. (2018), Patulin accumulation in apples under dynamic controlled atmosphere storage. Food Chemistry, 255, pp. 275-281
Duncan, H., Agulló, C., Mercader. J. V., Abad-Somovilla, A., & Abad-Fuentes, A. (2024), Harnessing the Intrinsic Chemical Reactivity of the Mycotoxin Patulin for Immunosensing. Analytical Chemistry, 96(30), pp. 12370-12377
El-Shayed, R. A., Jebur, A., Kang. W., & El-Demerdash, F. (2022), An overview on the major mycotoxins in food products: characteristics, toxicity, and analysis. Journal of Future Foods, 2(2), pp. 91-102
Erdem, A. & Senturk, H. (2024), Smartphone-Controlled Aptasensor for Voltammetric Detection of Patulin in Apple Juice. Sensors, 24(3)
Freire, L. & Sant’Ana, A. de S. (2018), Modified mycotoxins: An updated review on their formation, detection, occurrence, and toxic effects. Food and Chemical Toxicology, 111, pp. 189-205
George, M. M., Nisha, K., Lekhana, S.M., & Gurikar, C. (2022), Patulin: A potentially harmful food contaminant. International Journal of Chemical Studies, 10(3), pp. 11-18
Hernando, A. V., Sun, W., & Abitbol, T. (2024), “You Are What You Eat”: How Fungal Adaptation Can Be Leveraged toward Myco-Material Properties. Global Challenges, 8(3)
Ismaiel, A. A. & Papenbrock, J. (2015), Mycotoxins: Producing Fungi and Mechanisms of Phytotoxicity. Agriculture, 5(3), pp. 492-537
Janik, E., Niemcewicz, M., Ceremuga, M., Stela, M., Saluk-Bijak, J., Siadkowski, A., & Bijak, M. (2021), Molecular Aspects of Mycotoxins—A Serious Problem for Human Health. International Journal of Molecular Sciences, 21(21)
Janik, E., Niemcewicz, M., Podogrocki, M., Ceremuga, M., Gorniak, L., Stela, M., & Bijak, M. (2021), The Existing Methods and Novel Approaches in Mycotoxins’ Detection. Molecules, 26(13)
Khan, R., Anwar, F., & Ghazali, F. M. (2024), A comprehensive review of mycotoxins: Toxicology, detection, and effective mitigation approaches. Heliyon, 10(8)
Kumar, D., Barad, S., Sionov, E., Keller, N. P., & Prusky, D. B. (2017), Does the Host Contribute to Modulation of Mycotoxin Production by Fruit Pathogens?. Toxins, 9(9)
Li, B., Chen, Y., Zhang, Z., Qin, G., Chen, T., & Tian, S. (2020), Molecular basis and regulation of pathogenicity and patulin biosynthesis in Penicillium expansum. Comprehensive Reviews in Food Science and Food Safety, 19(6), pp. 3416-3438
Li, N., Cui, R., Zhang, F., Meng, X., & Liu, B. (2022), Current situation and future challenges of patulin reduction-a review. Food Control, 138, 108996
Li, X., Li, H., Ma, W., Guo, Z., Li, X., Li, X., & Zhang, Q. (2018), Determination of patulin in apple juice by single-drop liquid-liquid-liquid microextraction coupled with liquid chromatography-mass spectrometry. Food Chemistry, 257, pp. 1-6
Mahato, D. K., Kamle, M., Sharma, B., Pandhi, S., Devi, S., Dhawan, K., Selvakumar, R., Mishra, D., Kumar, A., Arora, S., Singh, N. A., & Kumar, P. (2021), Patulin in Food: A mycotoxin concern for human health and its management strategies. Toxicon, 198, pp. 12-23
Marín, S., Mateo, E. M., Sanchis, V., Valle-Algarra, F. M., Ramos, A. J., & Jiménez, M. (2011), Patulin contamination in fruit derivatives, including baby food, from the Spanish market. Food Chemistry, 124(2), pp. 563-568
Morshedi, A., Shakerardekani, A., Karazhian, R., Morshedi, M., Valdes, M. E., Mohammadi-Moghaddam, T., & Kariminejad, M. (2023), Mycotoxins’ Contamination in Food and Feeds: A Review. Journal of Food Chemistry & Nanotechnology, 9(3), pp. 141-149
Notardonato, I., Gianfagna, S., Castoria, R., Ianiri, G., De Curtis, F., Russo, M. V., & Avino, P. (2021), Critical review of the analytical methods for determining the mycotoxin patulin in food matrices. Reviews in Analytical Chemistry, 40(1)
Pal, S., Singh, N., & Ansari, K. M. (2017), Toxicological effect of Patulin mycotoxin on mammalian system: An Overview. Toxicology Research, 6(6), pp. 764-771
Piemontese, L., Solfrizzo, M., & Visconti, A. (2005), Occurrence of patulin in conventional and organic fruit products in Italy and subsequent exposure assessment. Food Additives & Contaminants, 22(5), pp. 437-442
Piqué, E., Vargas-Murga, L., Gómez-Catalán, J., de Lapuente, J., & Llobet, J.M. (2013), Occurrence of patulin in organic and conventional apple-based food marketed in Catalonia and exposure assessment. Food and Chemical Toxicology, 60, pp. 199-204
Przybylska, A., Chrustek, A., Olszewska-Słonina, D., Koba, M., & Kruszewski, S. (2021), Determination of patulin in products containing dried fruits by Enzyme-Linked Immunosorbent Assay technique Patulin in dried fruits. Food Science & Technology, 9(8), pp. 4211-4220
Puel, O., Galtier, P., & Oswald, I. P. (2010), Biosynthesis and Toxicological Effects of Patulin. Toxins, 2(4), pp. 613-631
Raiola, A., Tenore, G. C., Manyes, L., Meca, G., & Ritieni, A. (2015), Risk analysis of main mycotoxins occurring in food for children: An overview. Food and Chemical Toxicology, 84, pp. 169-180
Ramalingam, S., Bahuguna, A., & Kim, M. (2019), The effects of mycotoxin patulin on cells and cellular components. Trends in Food Science & Technology, 83, pp. 99-113
Saleh, I. & Goktepe, I. (2019), Health risk assessment of Patulin intake through apples and apple-based foods sold in Qatar. Heliyon, 5(11)
Saleh, I. & Goktepe, I. (2019), The characteristics, occurrence, and toxicological effects of patulin. Food and Chemical Toxicology, 129, pp. 301-311
Sant’Ana, A. de S., Rosenthal, A., & de Massaguer, P. R. (2008), The fate of patulin in apple juice processing: A review. Food Research International, 41, pp. 441-453
Shi, H., Schwab, W., Liu, N., & Yu, P. (2019), Major ergot alkaloids in naturally contaminated cool-season barley grain grown under a cold climate condition in western Canada, explored with near-infrared (NIR) and fourier transform mid-infrared (ATR-FT/MIR) spectroscopy. Food Control, 102
Singh, J. & Mehta, A. (2020), Rapid and sensitive detection of mycotoxins by advanced and emerging analytical methods: A review. Food Science & Nutrition, 8(5), pp. 2183-2204
Sohrabi, H., Arbabzadeh, O., Khaaki, P., Khataee, A., Majidi, M. R., & Orooji, Y. (2021), Patulin and Trichothecene: characteristics, occurrence, toxic effects and detection capabilities via clinical, analytical and nanostructured electrochemical sensing/biosensing assays in foodstuffs. Critical Reviews in Food Science and Technology, 62(20), pp. 5540-5598
Tangni, E.K., Masquelier, J., & Van Hoeck, E. (2023), Analysis of Patulin in Apple Products Marketed in Belgium: Intra-Laboratory Validation Study and Occurrence. Toxins, 15(6), 368
Vidal, A., Ouhibi, S., Ghali, R., Hedhili, A., De Saeger, S., & De Boevre, M. (2019), The mycotoxin patulin: An updated short review on occurrence, toxicity and analytical challenges. Food and Chemical Toxicology, 129, pp. 249-256
Wright, S. A. (2015), Patulin in food. Current Opinion in Food Science, 5, pp. 105-109
Zhang, H., Mahunu, G. K., Castoria, R., Apaliya, M. T., & Yang, Q. (2017), Augmentation of biocontrol agents with physical methods against postharvest diseases of fruits and vegetables. Trends in Food Science & Technology, 69, pp. 36-45
Zheng, X., Wei, W., Zhou, W., Li, H., Rao, S., Gao, L., & Yang, Z. (2021), Prevention and detoxification of patulin in apple and its products: A review. Food Research International, 140
https://faolex.fao.org/docs/pdf/eur68134.pdf
https://fas.usda.gov/data/production?commodity=almonds&commodity=apples
https://food.ec.europa.eu/document/download/236fc2fe-b079-49fd-a86d-95dd8c2e7c11_en
