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Review of Mycotoxins in Grapes and Grape Products

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Fernanda Cosme, Miguel Ribeiro, Luís Filipe-Ribeiro and Fernando M. Nunes

Submitted: 04 February 2024 Reviewed: 24 April 2024 Published: 15 May 2024

DOI: 10.5772/intechopen.1005454

Grapes and Grape Products - Chemistry and Technology IntechOpen
Grapes and Grape Products - Chemistry and Technology Edited by Fernanda Cosme

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Global Warming and the Wine Industry - Challenges, Innovations and Future Prospects [Working Title]

Fernanda Cosme, Fernando M. Nunes and Luís Filipe-Ribeiro

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Abstract

This review explores the presence of mycotoxins in grapes and grape products, focusing on various types such as ochratoxin A (OTA), aflatoxins, fumonisins, patulin, and others. The discussion encompasses multifaceted factors influencing mycotoxin occurrence, including environmental aspects, agricultural practices, and post-harvest handling. Advanced techniques for mycotoxin detection, such as chromatography and immunoassays, are explored, along with the challenges associated with these methods. Mitigation strategies, such as the implementation of good agricultural practices and good manufacturing practices, are presented. Additionally, emerging technologies for mycotoxin control are discussed, highlighting innovative approaches in the field. This overview aims to contribute to the complex realm of mycotoxins in grapes and grape products, offering a holistic understanding from detection to mitigation. The concluding remarks emphasize the significance of proactive measures to ensure the safety and quality of grape products regarding mycotoxin challenges.

Keywords

  • mycotoxins
  • grapes
  • grape products
  • mycotoxin detection
  • mitigation strategies

1. Introduction

Grape products encompass the grape berry and various products derived from grape berry processing, including wine, grape juice, distillates, vinegar, dried grapes, jams, and jellies. They can be susceptible to contamination with mycotoxins produced by specific fungi [1]. Literature data reveal the presence of various mycotoxin groups in grapes and nearly every type of commodity related to grapes [2, 3, 4, 5, 6, 7, 8, 9, 10]. Mycotoxins constitute a large and heterogeneous group of substances with diverse chemical structures and biological effects. They are low-molecular-weight secondary metabolites produced by filamentous fungi and can have toxic effects on humans, even at low concentrations. Mycotoxins are produced by a wide variety of fungal species, with the major fungal genera responsible for producing these substances being Aspergillus, Penicillium, Fusarium, and Alternaria [11, 12]. The genus Penicillium appears to be more prevalent in temperate and cold climates, such as those in northern Europe, whereas Aspergillus is more frequently associated with warmer and more humid regions [13].

When it comes to fresh table grapes meant for direct consumption, numerous articles address mycotoxigenic fungi and mycotoxin contamination [14, 15]. Several studies have also examined mycotoxins and the associated fungi in dried grapes [16, 17]. Juices rank as the third-largest source of exposure to OTA following cereals and wines. Given that juices are often consumed by children, there is an added need for awareness concerning mycotoxin presence [6, 16, 17, 18, 19]. Research studies are available for OTA [3, 20, 21, 22, 23, 24, 25], being the subject of the majority of mycotoxin research related to grapes and grape products, aflatoxins [7, 16, 17, 26, 27, 28], fumonisins [4, 8, 20, 21, 29, 30, 31] patulin [12, 32, 33], citrinin [2, 34, 35, 36], and Alternaria toxins [11].

Many mycotoxins are highly stable metabolites that can withstand technological processes due to their resistance to heat, physical, and chemical treatments, thus remaining in the final products [37], except for patulin in wine, as it is degraded during the fermentation process [38]. Nevertheless, studies considering the effects of climate change on toxigenic fungi remain a challenge. Furthermore, the co-occurrence of OTA and other mycotoxins in grape products needs to be assessed to verify the risk of human exposure to these compounds.

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2. Main types of mycotoxins found in grapes and grape products

Mycotoxins are considered among the most significant food contaminants due to their adverse impact on public health and food security. The molecular structures of mycotoxins vary widely, leading to a diverse range of effects on human health. The mycotoxins of greatest significance in grape and grape products include ochratoxin A, aflatoxins, fumonisin B2, and patulin [39].

2.1 Ochratoxin A

Ochratoxins constitute a group of toxic secondary metabolites produced by fungi. OTA stands out as the most toxic member of the ochratoxin group and has been extensively studied (Figure 1). It has been classified as a Group 2B carcinogen (i.e., a possible human carcinogen) by the International Agency for Research on Cancer (IARC) [40]. Nevertheless, OTA can be found in grape juice and wine due to grape contamination by toxigenic fungi [41]. The contamination of wine with OTA was initially reported in 1996 [42]. To address potential consumer risks linked to dietary exposure to OTA, the European Union has established maximum permitted levels for this mycotoxin in various grape products. These levels include 2 μg/kg in wine and grape juice, and 8 μg/kg in dried vine fruits (raisins, and sultanas) [43].

Figure 1.

Structure of ochratoxin A.

Dachery et al. [44] reviewed the occurrence of OTA in grape juice and wine and found that approximately 70% of samples may contain this toxin, with levels reaching up to ten times higher than the legal limits of 2 μg/L in the European Union [45]. Currently, wine is recognized as the second most significant source of human exposure to OTA, following cereals. Major producers of OTA in grapes and dried vine fruits are Aspergillus niger var. niger and Aspergillus carbonarius [46].

Several authors have determined OTA levels in red, white, rose, Jerez, and sweet wines from different countries. In red wine, the values ranged from 0.58–2.36 μg/L and 0.05–0.35 μg/L in Italy [47, 48], 0.07–2.00 μg/L in Greece [49], 0.004–0.18 μg/L and 0.06–0.14 μg/L in Spain [50, 51], 0.01–0.24 μg/L in France [48], 0.41–0.45 μg/L and n.d.–0.17 μg/L in Portugal [52, 53], 0.39–7.96 μg/L, 0.04–1.92 μg/L, n.d.–0.82 μg/L, and 2.72–7.40 μg/L in Turkey [54, 55, 56, 57], respectively; 0.02–4.82 μg/L in Argentina [58], 0.80–0.84 and 0.03–0.62 μg/L in Brazil [16, 59], 0.03–0.07 μg/L in Australia [48], 0.03–5.95 and n.d.–0.20 μg/L in China [60, 61], and 0.09–0.94 in Tunisia [62]. For white wine, the values ranged from 0.06–1.36 μg/L in Italy [47], 0.25–1.80 μg/L, 0.02–0.34 μg/L, n.d.–0.62 μg/L, and n.d.–4.41 μg/L in Turkey [54, 55, 56, 57], respectively, n.d.–0.03 μg/L in Brazil [16, 17], 0.03–0.07 and n.d.–0.36 μg/L in China [60, 61], and from 0.11–1.50 μg/L in Tunisia [62]. In rose wines from Turkey, the values of OTA ranged from 0.03–2.23 μg/L and from n.d.–0.16 μg/L [54, 56]. In Jerez wine from Spain, the levels of OTA ranged from 0.04–0.64 μg/L [50]. In sweet wine from Italy, they ranged from 0.21–1.56 μg/L, in Greece from n.d.–2.82 μg/L, and in Spain from 0.01–4.63 μg/L [63, 64, 65], respectively. OTA contamination can occur at any stage of the winemaking process, from the early colonization of mycotoxigenic fungi in grapes to the final steps in the wine process. Nevertheless, the main source of contamination in the final product results from the transfer of mycotoxins from grapes [66]. Furthermore, the winemaking process significantly influences OTA content [67, 68, 69], with higher concentrations reported in red wines (<0.01–7.63 μg/L), compared to rose (<0.01–2.40 μg/L) and white wines (<0.01–1.72 μg/L) in general [64, 70, 71, 72]. In a survey regarding the presence of OTA influenced by the type of wine, it was found that 25% of white wines, 40% of rosé, and 54% of red wines were contaminated with OTA [73]. For red wines, the maceration process can lead to an increase in OTA content (approximately 20%) [9] due to the extended contact between grape skins and grape juice, facilitating the solubility and diffusion of this mycotoxin from contaminated skins [74]. Conversely, the absence of maceration in white and rose wines appears to be a critical factor contributing to low OTA levels in these wines [6].

2.2 Aflatoxins

There are approximately 20 types of aflatoxins; however, the four major aflatoxins found in foods are aflatoxin B1 (AFB1), aflatoxin B2 (AFB2), aflatoxin G1 (AFG1), and aflatoxin G2 (AFG2), identified based on their fluorescence under UV light (blue or green) and relative chromatographic mobility during thin-layer chromatography (Figure 2). Their chemical structure is very similar, classified as furanocoumarins due to the presence of a coumarin nucleus associated with a furan and lactone ring. AFB1 is the most potent natural carcinogen known and is typically the major aflatoxin produced by toxigenic strains, has been classified as a human carcinogen (Group 1) by the International Agency for Research on Cancer (IARC) [40]. Aflatoxins are produced through a polyketide pathway by numerous strains of Aspergillus flavus and Aspergillus parasiticus [75]. Notably, Aspergillus flavus is a prevalent contaminant in agriculture. Despite this threat, studies conducted in certain Mediterranean countries have reported a low incidence of Aspergillus flavus in vineyards and AFB1 in grapes and derived products [76]. However, El Khoury et al. [7] observed an increasing incidence of vineyards contaminated by Aspergillus flavus isolates and grapes containing AFB1. Aflatoxins and aflatoxin-producing strains have been detected in grapes and grape musts in North African countries—Lebanon, Morocco, and Tunisia—and in Asia—China [7, 77, 78, 79, 80]. AFB1 was detected in 40% of grape musts from twenty-seven vineyards in Lebanon, with levels below 0.46 μg/L [7]. In Tunisian vineyards, Aspergillus flavus constituted 23% of mycotoxin-producing fungi in grapes, generating AFB1 at concentrations ranging from 21 to 54 μg/g of the culture medium [78]. The current European Commission Regulation (EU) No 915/2023 sets maximum residue limits (MRLs) total aflatoxins (sum of B1, B2, G1, and G2) to 4 μg/kg and AFB1 to 2 μg/kg in dried fruit intended for direct human consumption. For dried fruits intended for sorting or other physical treatments before consumption or inclusion as an ingredient in food products, the MRLs are set at 10 μg/kg for total aflatoxins (sum of B1, B2, G1, and G2) and 5 μg/kg for AFB1 [43]. Therefore, it is crucial to comprehend the level of contamination with toxin-producing fungi to prevent the introduction of toxin contamination into the food chain. The occurrence of aflatoxins in wines has been reported in recent years [63, 81]. AFB1 was detected in red wine from Spain in the range of 1.25–13.43 μg/L [81]. In sweet wine from Italy, Di Stefano et al. [63] found AFB1 ranging from 0.017–0.035 μg/L, and AFB2 from 0.013–0.016 μg/L. A screening in different wines in Romania measured AFB1 ranging from 12.12 to 33.68 μg/L [82]. However, there is no established limit for aflatoxins in wines, and studies on the content of aflatoxins in wines are limited. While OTA currently remains the most prevalent mycotoxin in grapes, recent studies suggest that in certain European regions, AFB1 may eventually replace OTA as the primary concern due to climatic conditions, especially higher temperatures, which directly impact fungus development [1, 83].

Figure 2.

Structure of aflatoxins B1, B2, G1, and G2.

2.3 Fumonisins

Fumonisins were initially described and characterized in 1988 (Figure 3) [84, 85]. The fungus Aspergillus niger, involved in the production of fumonisin B2, has been found on grape skin surfaces [86]. They are believed to be synthesized through the condensation of the amino acid alanine into an acetate-derived precursor. Fumonisin B2 has already been detected in grapes, raisins, grape must, and wine [10, 87]. The amount of fumonisin B2 produced by aspergilli in grapes appears to be low (0.1–7.8 mg/kg) [10, 88]. Fumonisin B2 was found in 9 out of 45 red wine samples from Italy in the range of 0.4–2.4 μg/mL [89]. In a study performed by Mogensen et al. [10] on 77 wines from 13 different countries, the range of fumonisin B2 was from 1 to 20 μg/L. Also, Tamura et al. [90] found fumonisin B2 in both red and white wines.

Figure 3.

Structure of fumonisin B2.

2.4 Other mycotoxins

Patulin (Figure 4) is a water-soluble lactone produced via the polyketide metabolic pathway by many species, such as those within the Penicillium and Aspergillus genera, predominantly Aspergillus clavatus, Penicillium expansum, Penicillium clavigerum, and Byssochlamys fulva [91]. The Codex Alimentarius Commission [92] has recommended a maximum level of 50 μg/L for fruit juices and their products. In the case of fruit-based baby food, the European Union has strict legislation limiting the occurrence of patulin to a concentration of <10 μg/kg [43]. The results from Ostry et al. [34] showed that the occurrence of patulin and citrinin in the 23 grape must samples was 10 (43%) samples for patulin (range: 143–644 ng/g) and 2 (9%) samples for citrinin (range 2.5–3.5 ng/g).

Figure 4.

Structure of patulin (A) and Alternaria toxins (B).

Alternaria toxins (Figure 4) were detected in red and white wines in Argentina in the range of 13–18 μg/L by Broggi et al. [93]. In the Netherlands, in red wines, the range was 2–11 μg/L [94], and in Germany, the level ranged from 65 to 7.65 μg/L [95].

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3. Factors influencing mycotoxin presence in grapes and grape products

It has been demonstrated that environmental stress conditions, such as drought, insect infestation, mechanical damage, cultivar susceptibility, nutritional deficiencies, and unusual temperature, rainfall, or humidity, promote the dissemination of fungal populations, including those present on grapes and grape products. Indeed, alterations in farming practices may lead to increased stress on plants, consequently promoting fungal invasion and mycotoxin contamination [96]. The primary source of fungi in vineyards is soil [97]. Fungi are commonly found in the soil and on grape berries throughout the entire crop production cycle, although they face difficulty in penetrating healthy berries during early grape growth stages. Berries may develop microfissures and soften with ripening, thereby increasing nutrient availability and enabling further contamination by fungi. Their entry into the fruit is also facilitated by skin damage caused by insects, birds, or other factors such as rainfall or fungal infections [98]. Among these factors, insect pests have been confirmed to significantly contribute to fungal invasion of berries and their contamination with OTA. However, despite the numerous insect species that infest grapes [99], only a limited number of them, such as the European grapevine moth Lobesia botrana or mealybugs, have been linked to OTA contamination [100, 101]. The humidity in the vineyard may promote fungal proliferation, posing a significant concern [83]. Various factors, including weather conditions, harvest timing, biotic factors, agricultural and harvesting practices, or the type of wine, may also impact the final concentration of mycotoxins [102]. Importantly, winemaking practices, like maceration, can increase mycotoxin content in wines, and consequently, it is frequently detected in red wines, followed by rose and white wines. Additionally, Jiang et al. [80] suggested that the grape cultivar, especially its skin thickness, may affect the OTA levels found in wine. While numerous studies have explored factors influencing the occurrence of OTA in wine, there is a scarcity of research on aflatoxins, patulin, alternariol, and fumonisin B2 [1]. Additionally, it is possible that other mycotoxins may become more prevalent with the progression of climate change [103]. Therefore, there is a clear need for more information on the impact of climate change scenarios and environmental conditions such as temperature, water activity, and humidity on the fungal colonization, growth, and mycotoxin production by key mycotoxigenic species in the genera Aspergillus, Fusarium, Penicillium, and Alternaria [104, 105]. Aflatoxins may increase in temperate regions due to rising temperatures. For instance, in Italy during 2003 and 2004, hot and dry conditions led to Aspergillus flavus colonization and aflatoxin production [106].

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4. Detection and analysis of mycotoxins from grapes and grape products

Detection and analysis of mycotoxins from grapes and grape products are imperative for ensuring food safety. However, challenges in mycotoxin analysis exist, including the discovery of new mycotoxins without a fully understood toxicity profile, modifications that can hamper their identification, co-occurrence, and the complexity of matrices [107]. Analytical approaches, including sample preparation methods, have evolved to overcome some of these limitations, covering a wider range of mycotoxins. Two major trends in mycotoxin analysis can be identified. Firstly, methods based on chromatography, with high sensitivity and specificity, facilitate the separation and quantification of mycotoxins, especially when combined with mass spectrometry. The other trend is immunochemical-based methods, such as the Enzyme-Linked Immunosorbent Assay (ELISA), which offer rapid and cost-effective analyses [107, 108].

4.1 Sampling, sample preparation, and extraction

The sampling, preparation, and extraction of mycotoxins are crucial steps for ensuring precision and accuracy in analytical procedures, especially in solid samples where their occurrence is known to be highly heterogeneous. The sampling process is essential in the analysis of both whole and dried grapes. In this context, in addition to adequate sampling, homogenization of the sample is necessary, for example by grinding [109]. In the EU, there are regulations for the sampling method for the official control of OTA levels in dried grapes, grape juice, grape must, and wine [43]. However, in the case of wine, grape juice, and grape must, sampling is simpler due to the liquid nature of these products. An extraction and preconcentration step are often required before their analysis by chromatographic techniques. The selection of the extraction solvent depends on the physical and chemical characteristics of the analyte, solvent cost, and safety; organic solvents such as acetonitrile, methanol, acetone, ethyl acetate, and dichloromethane are generally used for mycotoxin extraction. In liquid matrices, it is common to use a liquid-liquid extraction (LLE) approach followed by a cleaning step using solid phase extraction (SPE) or immunoaffinity columns (IAC) [63]. In contrast, for solid samples such as dried grapes, the solid-liquid extraction (SLE) procedure is preferred before the cleaning step. It should be noted that highly sensitive and specific immunoassays, such as ELISA, may not necessitate a clean-up step. On the other hand, techniques with poor resolution, like thin-layer chromatography (TLC), will likely require thorough clean-up procedures. Newer techniques such as QuEChERS (which stands for Quick, Easy, Cheap, Effective, Rugged, and Safe) and dispersive liquid-liquid microextraction (DLLME) have also been successfully used for detecting important mycotoxins in wines [110, 111].

4.2 Chromatography-based methods

Mycotoxin separation is typically achieved through chromatographic methods, including thin-layer chromatography (TLC), gas chromatography (GC), or liquid chromatography (LC). Due to the non-volatile nature of many mycotoxins in grapes and grape products, such as OTA, samples are generally separated by TLC or LC and quantified using fluorescence or mass spectrometry (MS) [112]. TLC has become a largely neglected technique, although it is still used in some laboratories, especially in developing countries, and when combined with an ultraviolet (UV) or fluorescence scanner. It is an easy-to-use, fast, and highly versatile separation technique, particularly important in resource-limited settings. Unlike more complex techniques, TLC offers rapid results and requires minimal specialized equipment, making it accessible for various applications. Notably, TLC has proven important in detecting and quantifying aflatoxins at low levels. Nevertheless, it has been superseded by more advanced methods such as GC and high-performance liquid chromatography (HPLC). Regarding GC, which was previously widely used for multiple analyses of trichothecene, modern advancements in HPLC with UV and fluorescence detectors (FLD), and more recently, in MS, have effectively supplanted it. As a result, HPLC, namely reversed-phase HPLC (RP-HPLC), has become the main method for determining mycotoxins and remains so in most laboratories (Table 1) [108].

SampleSample preparationMycotoxinMethodReference/Year
GrapeQuEChERSAflatoxin (B1/B2/G1/G2), Cytochalasin (B, C, D), Diacetoxyscirpenol, Deoxynivalenol, 3-acetyl deoxynivalenol, 15-acetyl deoxynivalenol, Enniatin (A, A1, B, B1), Fusarenone X, HT-2/T-2 toxins, Neosolaniol, Ochratoxin (A, B, C)UHPLC-HRMS[110]/2024
WineLLEAflatoxin (B1, B2, G1, G2), Ochratoxin A, ZearalenoneUHPLC–MS/MS[113]/2022
WineSPEOchratoxin (A, B)HPLC-FLD[114]/2020
WineDilution and filtrationAflatoxin (B1, B2, G1, G2), Deoxynivalenol, Diacetoxyscirpenol, Fumonisin (B1, B2), HT-2/T-2 toxins, Ochratoxin A, Zearalenone; pesticides (n = 185)UHPLC–MS/MS[115]/2019
GrapeQuEChERSAlternariol, Alternariol monomethyl ether, Altenusin, Altenuene, Tentoxin, Tenuazonic acidUHPLC–MS/MS[11]/2019
Grape juice, wineSPEOchratoxin ALC-FLD[116]/2018
WineIACOchratoxin (A, B), Aflatoxin (B1, B2, G1, G2)HPLC-FLD[63]/2015

Table 1.

Examples of recent works on chromatography-based methods for mycotoxin determination in grapes and grape products.

Chromatographic techniques coupled with fluorescence detection are mainly used for confirmatory analyses, especially in the quantification of OTA. However, an additional confirmation step may be necessary to guarantee the identity of OTA. This confirmation is normally performed through derivatization with BF3 in methanol or with methanol in concentrated hydrochloric acid, both producing the methyl ester derivative of OTA [109].

More recently, ultra-high-performance liquid chromatography (UHPLC) coupled with high resolution mass spectrometry (HRMS) is considered the most advanced technique for the qualitative and quantitative analysis of mycotoxins, particularly for multiclass determination of mycotoxins, even in the presence of several interfering substances in complex samples. In fact, this state-of-the-art technique responds to current demands for multi-target techniques that guarantee specificity and sensitivity characteristics, while simultaneously allowing the identification of non-target compounds [107, 110]. This is of significant interest within the context of climate change. Anticipated shifts in climate variables, including temperature, rainfall, and atmospheric carbon dioxide levels, are expected to exert an influence on fungal growth and toxin production. The adoption of comprehensive analyses, rather than a focused approach, holds the potential to provide critical insights as these climate-induced changes progress [108, 117].

4.3 Immunochemical-based methods

Immunochemical-based methods serve as rapid initial screening tools, often provided in purpose-tailored kits. Leveraging the binding affinity between mycotoxins and specific antibodies, these methods facilitate rapid, in situ detection of prevalent mycotoxins in grapes and grape products. Despite their value in routine monitoring, they have limitations, such as the detection of many targets per sample and the inability to detect mycotoxins that are not included in the assay or those that have undergone chemical modifications. Nevertheless, they play a crucial role in rapid assessments, proving particularly beneficial in applications such as food safety and agricultural practices [112].

A widely used immunochemical method is ELISA. Commercially available ELISA-based kits for all regulated mycotoxins ensure food safety throughout the supply chain. ELISA, with its high sensitivity and specificity, is suitable for the quantitative measurement of various mycotoxins. Predominantly, classical and competitive inhibition formats are used, which perform better considering the limited epitope site display of mycotoxins [107].

Beyond ELISA, ongoing developments in immunochemical-based tests aim to create rapid, portable, and easy-to-operate systems. Among these, lateral flow immunoassays (LFIA), also known as lateral flow tests or immunochromatographic assays, are often used in on-site mycotoxin screening for grapes. LFIA provides fast results, easy operation, and requires minimal equipment. It involves moving the sample along a strip containing immobilized antibodies, generating a visible signal indicating the presence or absence of the target mycotoxin. LFIA, recognized for its simplicity and speed, is valuable for qualitative assessments, especially in scenarios requiring immediate results. However, its quantitative precision is limited [112, 118].

In the field of research, and with more limited market availability and commercial applications, biosensors use the selectivity and affinity of antibodies coupled to different sensor devices to determine prevalent mycotoxins. Biosensors based on synthetic ligands, designed to mimic the binding capacity of natural antibodies, also contribute to this growing field of research [119]. In general, biosensors come in various types and can face challenges including complex construction, costly labeling markers, and susceptibility to factors like temperature, pH, and immobilization support, which can affect sensitivity. Issues like cross-reactivity with similar compounds in the sample matrix, such as wine, can further complicate biosensor measurements, impacting their reliability. While biosensors hold promise, their broad practical application is still in development [120].

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5. Mitigation strategies for mycotoxins in grapes and grape products

5.1 Viticultural practices to minimize mycotoxins in grapes and grape products

There are many fungi on grapes in the vines, but the main problem from the viewpoint of mycotoxin contamination is the black Aspergilli, specifically Aspergillus carbonarius, A. niger, and A. welwitschiae [86, 121, 122]. These types of fungi can produce OTA, contaminating the grapes and respective grape products like wine, grape must, and dried grapes. High temperature, humidity, and the region of cultivation are crucial factors that influence OTA accumulation in grape berries. The intensity of Aspergillus rot is highly influenced by excessive irrigation and rainfall before the harvest, causing berry splitting. Additionally, wounds on berries generated by insect attacks allow preferential entry points for black Aspergilli. High OTA levels can occur in grapes gravely damaged by the grape moth, Lobesia botrana, especially in Mediterranean regions [121].

However, diverse practices and good management of cultivation, pruning, and adequate irrigation can reduce the levels of black Aspergilli in the soil, consequently minimizing contaminations of grapes by these fungi. There are several approaches to minimize damage to grapes, such as open vineyard canopies, grape varieties with resistant skin to avoid rain damage, and the control of insect attacks and fungal diseases (e.g., Botrytis bunch rot, mildew). These practices can decrease the incidence of Aspergillus rot in mature berries. The problem of OTA in table grapes can be significantly reduced by attentive visual inspection to avoid damaged and discolored berries. Storing table grapes at low temperatures (0°C) with the application of some sulfur dioxide can reduce the severity of attacks by black Aspergillus species on the grapes. Wine grapes present a lower risk of OTA contamination than dried vine fruit because the ratio of A. carbonarius to A. niger increases during the drying process [123]. The dominant species in vineyards at harvest is A. niger, which rarely produces OTA [124]. However, the grape drying process could increase the survival of A. carbonarius, and almost all strains of this species can produce OTA, frequently to a water activity of 0.92 [125]. In conclusion, for dried grapes production, it is important to avoid berry damage and implement a rapid drying process. Grape cleaning and grape selection are important to remove dark berries and reduce OTA levels in the final products [86, 121].

5.2 Strategies and treatments to mitigate the final content of mycotoxins in wine

An important mycotoxin frequently found in wines is OTA, which is limited to a maximum of 2.0 μg/L in the European Union. In winemaking, harvesting healthy grapes, followed by a rapid process and maintaining good clean conditions in the winery, is crucial to minimize OTA wine contamination. Many vinification operations, such as pressing grapes and clarification processes that remove solids in suspension, some grape proteins, and spent yeast, help eliminate a significant quantity of OTA [86, 121]. Therefore, prevention and avoiding its appearance in wines are essential; when present, more efficient treatments may be necessary to remove OTA and ensure safe levels for human consumption [14].

Thus, knowledge about OTA contamination and its appearance in wine and wine by-products is crucial to manage OTA risk in contaminated stock. In some winemaking experiences, only 4% of the OTA present in grapes continues into the wine; the majority is eliminated in the pressed grape pomace. However, OTA content remains constant in wine even after 1-year of aging and is also present in all liquid fractions collected during vinification (i.e., grape juice, free-run juice, and wine after first and second sedimentation) [121]. Various physical, chemical, and microbiological methods have been described for OTA elimination from food products [14, 66, 68, 126, 127, 128].

Biological methods utilize microorganisms such as yeast, bacteria, and fungi for the detoxification of mycotoxins [66, 129, 130]. Bacteria, such as Lactobacillus plantarum and Oenococcus oeni, could adsorb OTA, with polysaccharides and peptidoglycan presumably involved in toxin binding [131]. Del Prete et al. [131] investigated 15 strains of enological lactic acid bacteria to verify their in vitro capacity to remove OTA and observed Oenococcus oeni as the most effective, with OTA reductions of 28%. According to Piotrowska [132], thermally inactivated bacterial biomass has a higher binding capacity for OTA (46.2–59.8%). Another study shows that OTA biodegradation by Pediococcus parvulus UTAD 473 can utilize 100% of OTA (1000 μg/L) within 7 days at 30°C in MRS broth medium, and 80% of OTA (7 μg/L) after 6 days of incubation in grape juice. However, no obvious degradation of OTA (7 μg/L) was observed in synthetic wine, perhaps due to the presence of ethanol, which could inhibit the enzyme responsible for the OTA degradation [126].

There are some doubts in the literature about Saccharomyces cerevisiae biodegradation capacity because almost all works demonstrate only its adsorption capacity [66]. S. cerevisiae was responsible for biodegrading 41% of 0.3 mg OTA/L after 24 h at 30°C, but details were not provided about the mechanism involved [133]. During must fermentation, yeasts adsorbed a maximum of 21% of the added OTA [134]. Also, almost 30% of the added OTA was removed after extended contact with yeast biomass [135]. However, Csutorás et al. [136] also verified that OTA (4000 μg/mL) could be adsorbed by S. cerevisiae along the winemaking process (90 days) in 73, 85, and 90% in white, rosé, and red wine grape juices, respectively. Finally, Petruzzi et al. [137] conducted a review on OTA removal primarily by yeast products: live cells, cell walls, cell wall extracts, and yeast lees, and concluded that yeast biomass could be considered a good treatment due to its adsorbing capacity, attributed to specific macromolecules in the cell wall, such as β-glucans and mannoproteins.

Some physical treatments have shown efficacy in OTA removal, such as wine filtration through a 0.45 μm membrane, which can reduce about 80% of OTA in the wine [138]. Solfrizzo et al. [139] found that OTA levels in wine can be significantly reduced by the repassage of grape pomaces through the wine. They also observed that if the grape pomaces are from the same grape variety as the treated wine, there will not be any significant impact on wine quality; however, it is not a practical treatment due to logistics difficulties in the winery. Other physical treatments like pulsed light (PL) can also efficiently remove OTA from clarified grape juice. The factors of OTA degradation by PL were explored, and the OTA removal presents a performance of 95.29% after optimization by response surface methodology [140]. Also, radiation methods including ultraviolet radiation, gamma radiation, electron beam radiation, and X-ray radiation can be safe and efficient in removing mycotoxins from food [141]. Inorganic mineral adsorbents present an efficient means of OTA removal due to their large specific surface area and ion adsorption capacity, primarily aluminum silicate, hydrated sodium calcium aluminosilicate, bentonite, zeolite, diatomaceous earth [142, 143]. Some studies have been conducted, especially with activated carbon. Activated carbon can effectively reduce OTA levels in wine; however, it may have a negative impact on wine quality [144]. Activated carbon is used as a fining agent in enology [145] at the maximum dosage of 1 g/L. The adsorption capacity of activated carbon is strictly dependent on its physicochemical characteristics, especially, pore structure and size, magnitude, pore volume, and distribution on the surface area, which are crucial for its adsorption capacity and performance [146].

Galvano et al. [147] verified that activated carbon demonstrates effective absorption of OTA in a model solution (1 milligram of activated carbon can remove 125 μg of OTA). However, the complexity of the wine matrix, particularly in red wines, could significantly reduce the OTA adsorption capacity of activated carbons due to the presence of many phenolic compounds. Seven commercially available deodorizing activated carbons were tested to optimize OTA removal from white and red wines at high levels of OTA (10.0 μg/L) [144]. The study showed that 1 g/L of activated carbon can remove 100% of OTA in white wines. It was also observed that activated carbon efficiency was less dependent on activated carbon physicochemical characteristics. However, in red wines, only one activated carbon tested could remove 100%, whereas the activated carbon with a higher abundance of mesopores exhibited better performance in OTA removal. The lower efficiency in red wines was associated with the competition of red wine anthocyanins for activated carbons mesopores [143].

AFB1 and AFB2 are two highly toxic mycotoxins that have been sometimes found in wines. For example, AFB1 was present in 23% of the analyzed wines, and 21, 40, and 37% of the wines also contained AFG1, AFB2, and AFG2, respectively. The concentration of these aflatoxins averaged 0.025, 0.043, 0.015, and 0.027 μg/L for AFB1, AFG1, AFB2, and AFG2, respectively [148]. Previous studies have shown that the processing applied to grape products may influence aflatoxin levels. For instance, Heshmati et al. [149] observed a significant effect on aflatoxins removal during pekmez preparation, resulting in a significant reduction of AFB1, AFB2, AFG1, and AFG2 by up to 60.4, 76.7, 76.3, and 86.7%, respectively [149]. Interesting results were also obtained [150] during vinegar production from grapes, where they found that the values of AFB1, AFB2, AFG1, and AFG2 were significantly reduced by 76.20, 71.06, 69.26, and 75.85%, respectively. Alcoholic fermentation had the most significant effect on aflatoxin reduction during vinegar production, decreasing AFB1, AFB2, AFG1, and AFG2 by 41.87, 45.34, 45.37, and 46.52%, respectively. Currently, no authorized treatmenta are available for removing aflatoxins from wines. Several authorized fining agents like potassium caseinate, chitosan, bentonite, and activated carbon were tested for aflatoxins removal (AFB1 and AFB2). Interestingly, the work showed that the fining agents’ performance in aflatoxins removal was dependent on the wine matrix, more so in white wine than in red wine. The most efficient fining agent was bentonite, which could remove 10 μg/L from white wine (100% of AFB1) and 82% of AFB2 from red wine. The impact of bentonite on white wine chromatic characteristics was low (color difference, ΔE* = 1.35). However, the treatment with bentonite could have a significant impact on red wine chromatic characteristics (ΔE* = 4.80) due to the considerable reduction of total anthocyanins, decreasing the respective wine color intensity by 1.5 points [151].

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6. Conclusions

The presence of fungal contamination in vineyards can elevate health risks attributed to mycotoxins in grapes and their respective products. Among them, OTA is the most frequently reported mycotoxin in grapes and grape products, and this compound is regulated in several countries. OTA is initially removed from grape juice by its adsorption onto solid parts of grapes by yeasts and bacteria responsible for alcoholic or malolactic fermentation, which are usually removed from the wine during stabilization and bottling. When these mycotoxins persiste in the final wine, they can be efficiently removed by fining, for example, activated carbons. However, some studies have indicated the co-occurrence of other mycotoxins such as aflatoxins, fumonisin, and patulin, indicating that these metabolites cannot be disregarded. The presence of patulin is primarily a preharvest issue in table grapes and grape juice. More studies focusing on mycotoxin presence are needed, as well as research on the possible effects of processing grapes and grapes products on mycotoxin levels, which may become a future concern for the grape and grape products industries. It is also important to consider the scenario of climate change, as fungal development in grapes and grape products may deviate from the current situation in each region worldwide.

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Acknowledgments

FCT-Portugal, CQ-VR (UIDB/00616/2020 and UIDP/00616/2020). (https://doi.org/10.54499/UIDP/00616/2020 and https://doi.org/10.54499/UIDB/00616/2020) and Project Vine&Wine Portugal—Driving Sustainable Growth Through Smart Innovation, Application n. ° C644866286 00000011, co-financed in the scope of the Mobilizing Agendas for Business Innovation, under Reg. (EU) 2021/241, in the Plano de Recuperação e Resiliência (PRR) to Portugal, na sua componente 5—Capitalização e Inovação Empresarial.

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Conflict of interest

The authors declare no conflict of interest.

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Written By

Fernanda Cosme, Miguel Ribeiro, Luís Filipe-Ribeiro and Fernando M. Nunes

Submitted: 04 February 2024 Reviewed: 24 April 2024 Published: 15 May 2024

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