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      Application of cold atmospheric plasma for decontamination of toxigenic fungi and mycotoxins: a systematic review

      systematic-review

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          Abstract

          Introduction

          Microbial contamination remains a vital challenge across the food production chain, particularly due to mycotoxins—secondary metabolites produced by several genera of fungi such as Aspergillus, Fusarium, Alternaria, and Penicillium. These toxins, including aflatoxins, fumonisins, ochratoxins, and trichothecenes (nivalenol, deoxynivalenol, T2, HT-2). These contaminants pose severe risks to human and animal health, with their potential to produce a variety of different toxic effects. Notably, up to 50% of global cereal production is affected by mycotoxin contamination, leading to significant economic losses. Current research focuses on innovative technologies to mitigate mycotoxins, with cold atmospheric pressure plasma emerging as a promising decontamination method.

          Method

          This systematic review aimed at describing recent advances in the application of cold atmospheric plasma for the decontamination of toxigenic fungi and mycotoxins.

          Results and discussion

          Cold atmospheric plasma offers a sustainable and cost effective solution to preserve food quality while inactivating toxigenic fungi and degrading mycotoxins. Through the generation of reactive oxygen and nitrogen species, cold plasma disrupts fungal cell integrity, hinders spore germination, and inhibits toxin biosynthesis. Additionally, cold atmospheric plasma-driven degradation of mycotoxins involves structural modifications, breaking key molecular bonds that reduce toxicity. The effectiveness of cold plasma depends on operational parameters and the specific characteristics of the treated food, with notable efficacy in degrading aflatoxin B 1 and deoxynivalenol by converting them into less toxic substances and inhibiting their spores and DNA responsible for their biosynthesis. While the data demonstrates that cold atmospheric plasma has minimal impact on food composition, further research is needed to fully assess the nature of the degradation products of mycotoxins, its influence on food quality attributes and to optimize application strategies for different products.

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          Most cited references114

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          Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation.

          Protocols of systematic reviews and meta-analyses allow for planning and documentation of review methods, act as a guard against arbitrary decision making during review conduct, enable readers to assess for the presence of selective reporting against completed reviews, and, when made publicly available, reduce duplication of efforts and potentially prompt collaboration. Evidence documenting the existence of selective reporting and excessive duplication of reviews on the same or similar topics is accumulating and many calls have been made in support of the documentation and public availability of review protocols. Several efforts have emerged in recent years to rectify these problems, including development of an international register for prospective reviews (PROSPERO) and launch of the first open access journal dedicated to the exclusive publication of systematic review products, including protocols (BioMed Central's Systematic Reviews). Furthering these efforts and building on the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) guidelines, an international group of experts has created a guideline to improve the transparency, accuracy, completeness, and frequency of documented systematic review and meta-analysis protocols--PRISMA-P (for protocols) 2015. The PRISMA-P checklist contains 17 items considered to be essential and minimum components of a systematic review or meta-analysis protocol.This PRISMA-P 2015 Explanation and Elaboration paper provides readers with a full understanding of and evidence about the necessity of each item as well as a model example from an existing published protocol. This paper should be read together with the PRISMA-P 2015 statement. Systematic review authors and assessors are strongly encouraged to make use of PRISMA-P when drafting and appraising review protocols. © BMJ Publishing Group Ltd 2014.
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            Mycotoxins as human carcinogens-the IARC Monographs classification.

            Humans are constantly exposed to mycotoxins (e.g. aflatoxins, ochratoxins), mainly via food intake of plant and animal origin. The health risks stemming from mycotoxins may result from their toxicity, in particular their carcinogenicity. In order to prevent these risks, the International Agency for Research on Cancer (IARC) in Lyon (France)-through its IARC Monographs programme-has performed the carcinogenic hazard assessment of some mycotoxins in humans, on the basis of epidemiological data, studies of cancer in experimental animals and mechanistic studies. The present article summarizes the carcinogenic hazard assessments of those mycotoxins, especially aflatoxins (aflatoxin B1, B2, G1, G2 and M1), fumonisins (fumonisin B1 and B2) and ochratoxin A (OTA). New information regarding the genotoxicity of OTA (formation of OTA-DNA adducts), the role of OTA in oxidative stress and the identification of epigenetic factors involved in OTA carcinogenesis-should they indeed provide strong evidence that OTA carcinogenicity is mediated by a mechanism that also operates in humans-could lead to the reclassification of OTA.
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              Some major mycotoxins and their mycotoxicoses--an overview.

              Mycotoxins likely have existed for as long as crops have been grown but recognition of the true chemical nature of such entities of fungal metabolism was not known until recent times. Conjecturally, there is historical evidence of their presence back as far as the time reported in the Dead Sea Scrolls. Evidence of their periodic, historical occurrence exists until the recognition of aflatoxins in the early 1960s. At that time mycotoxins were considered as a storage phenomenon whereby grains becoming moldy during storage allowed for the production of these secondary metabolites proven to be toxic when consumed by man and other animals. Subsequently, aflatoxins and mycotoxins of several kinds were found to be formed during development of crop plants in the field. The determination of which of the many known mycotoxins are significant can be based upon their frequency of occurrence and/or the severity of the disease that they produce, especially if they are known to be carcinogenic. Among the mycotoxins fitting into this major group would be the aflatoxins, deoxynivalenol, fumonisins, zearalenone, T-2 toxin, ochratoxin and certain ergot alkaloids. The diseases (mycotoxicoses) caused by these mycotoxins are quite varied and involve a wide range of susceptible animal species including humans. Most of these diseases occur after consumption of mycotoxin contaminated grain or products made from such grains but other routes of exposure exist. The diagnosis of mycotoxicoses may prove to be difficult because of the similarity of signs of disease to those caused by other agents. Therefore, diagnosis of a mycotoxicoses is dependent upon adequate testing for mycotoxins involving sampling, sample preparation and analysis.
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                Author and article information

                Contributors
                URI : http://loop.frontiersin.org/people/2884977/overviewRole: Role: Role: Role:
                URI : http://loop.frontiersin.org/people/1583529/overviewRole:
                URI : http://loop.frontiersin.org/people/445243/overviewRole: Role:
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                URI : http://loop.frontiersin.org/people/442506/overviewRole: Role: Role:
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                03 January 2025
                2024
                : 15
                : 1502915
                Affiliations
                [1] 1Laboratory of Food Microbiology and Mycotoxicology, Department of Food Engineering, School of Animal Science and Food Engineering, University of São Paulo , Pirassununga, Brazil
                [2] 2School of Physics, Engineering and Technology, University of York , York, United Kingdom
                [3] 3Department for Gaseous Electronics, Jožef Stefan Institute , Ljubljana, Slovenia
                Author notes

                Edited by: Gustavo Cordero-Bueso, University of Cádiz, Spain

                Reviewed by: Abhay K. Pandey, North Bengal Regional R&D Center, India

                Shengqian Sun, Yantai Institute of Technology, China

                Mengyue Guo, Chinese Academy of Medical Sciences and Peking Union Medical College, China

                *Correspondence: Carlos Augusto Fernandes de Oliveira, carlosaf@ 123456usp.br

                ORCID: Amanda Cristina Dias de Oliveira, orcid.org/0000-0001-6991-6218; Sher Ali, orcid.org/0000-0002-4604-9702; Carlos Humberto Corassin, orcid.org/0000-0001-9826-9224; Sana Ullah, orcid.org/0009-0002-7086-4894; Karina Nascimento Pereira, orcid.org/0000-0002-9609-7964; Carlos Augusto Fernandes de Oliveira, orcid.org/0000-0001-5779-5287

                Article
                10.3389/fmicb.2024.1502915
                11739521
                39831113
                24563969-b234-4c16-a454-6753f267befd
                Copyright © 2025 Oliveira, Ali, Corassin, Ullah, Pereira, Walsh, Hojnik and Oliveira.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 September 2024
                : 09 December 2024
                Page count
                Figures: 8, Tables: 3, Equations: 0, References: 115, Pages: 20, Words: 14076
                Funding
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo, doi 10.13039/501100001807;
                The authors declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) under grant numbers: 2022/03952-1, 2023/05989-2, and 2024/00896-9, as well as Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Financial Code 001.
                Categories
                Microbiology
                Systematic Review
                Custom metadata
                Food Microbiology

                Microbiology & Virology
                cap technology,mycotoxins,contamination,foodstuffs,detoxificationprotect
                Microbiology & Virology
                cap technology, mycotoxins, contamination, foodstuffs, detoxificationprotect

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