*Aflatoxins in the Era of Climate Change: The Mediterranean Experience DOI: http://dx.doi.org/10.5772/intechopen.108534*

Mediterranean countries have adopted different regulations while specifically many European countries follow the European Commission legislation (**Table 1**).

#### **3. Climate change patterns' effects on aflatoxins**

#### **3.1 Preharvest effects**

Environmental conditions are the main driving factors of fungal attack patterns and mycotoxin contamination in foodstuff, therefore, emerging climatic conditions may induce changes in the dynamics of fungal colonization and mycotoxin production. Since the industrial revolution, production patterns and human activities including agricultural production, food processing, fossil fuel combustion, and others have been contributing to increased pollution and greenhouse gases emission. The increased accumulation of those gases in the atmosphere is the main driving factor of global warming and climate change.

With the change in climatic conditions, global warming is expected to induce an increase in global temperatures that are expected to rise by 1.5–4.5°C by the end of the twenty-first century [37], along with an increased accumulation of carbon dioxide in the atmosphere, increase in precipitation, the dominance of extreme weather conditions such as heat and cold waves, and an increase in the incidence of flooding and droughts [38].

Climate change patterns will have a direct effect on agriculture characterized by a decrease in plant resilience and yields, deterioration of crop quality, and an increase in pest and insect population, spread, and attacks [39]. Additionally, changes in global temperatures can lead to early maturing and ripening of crops in certain areas that will lead to a change in the patterns of harvest, drying, and storage.

All those factors, will in turn affect food security since a change in fungal attack and mycotoxin production properties are expected [40]. Hence, according to the European Food Safety Authority, some geographical regions will have advantageous effects while others will experience detrimental ones according to the forecasted environmental changes [41]. The Mediterranean region, specifically, was reported to be highly affected by the ongoing climate change as it was reported to be warming 20% faster than the global average by the "Mediterranean Action Plan Barcelona Convention" of the UN environment program creating a hotspot region of climate change. In addition to that, changes affecting the Mediterranean region include the increase in the frequency and intensity of droughts, the decrease in precipitation in the eastern Mediterranean coupled by an increase in temperature of 2–3°C [42]. The number of hot days characterized by temperatures above 30°C is also likely to increase in a number of countries including Spain, Morocco, Algeria, the center of Italy, the Balkans, and central Turkey [30].

As reported by Medina et al., Southern Europe and the Mediterranean basin will undergo significant changes that will eventually cause an increase in fungal colonization and mycotoxin frequency [43]. This change affects *Aspergillus species* colonization and aflatoxins production as warm conditions favor the attack and growth of their producers, leading to their frequency in regions once considered as temperate and different from their typical production areas in tropical and sub-tropical regions [44].

Additionally, climate change will reproduce suitable and favorable environmental conditions of droughts, high temperatures, and humidity for *Aspergillus* colonization and aflatoxins and their precursors' production. Indeed, droughts are

#### *Aflatoxins in the Era of Climate Change: The Mediterranean Experience DOI: http://dx.doi.org/10.5772/intechopen.108534*

considered an important trigger for biosynthesis of aflatoxins and according to Valencia-Quintana et al. the sudden change in precipitation and drought patterns followed by increased humidity, temperature, and CO2 levels will directly affect the expression of the regulatory and structural genes (*aflR* and *aflD*) implicated in aflatoxins biosynthesis [44]. The Mediterranean region already has marked summer droughts, prolonged heat waves, regular flooding, and varied precipitation volume [30]. However, those climatic patterns are all liable to intensify as according to the forecasts for the mid-twenty-first century, extreme drought situations will become more prevalent and the number of dry days is expected to increase by at least three weeks every year specifically on the northern shores of the western Mediterranean, in countries such as Portugal, Spain, France, Italy, Croatia, Montenegro, and Turkey which can increase the frequency of *Asperillius* sp. and aflatoxin contamination [30].

On the other hand, elevated CO2 atmospheric levels can further lead to aflatoxin contamination, specifically, as reported by many studies, cause the environment where the crops are cultivated is expected to markedly change due to the elevated concentrations of CO2 that are projected to double or triple from a concentration of 350 ppm to a range of 700–1000 ppm [45]. According to Medina et al., AFB1 production was stimulated under climate change scenarios related to elevated CO2 levels, especially when coupled with drought stress [45]. The same study, showed no effect on the growth of *Aspergillus* sp. in case of increased CO2 levels, while the relative increase was reported in the structural *aflD* and the regulatory *aflR* genes, suggesting a significant impact on the biosynthetic pathway involved in aflatoxins production, particularly at an elevated temperature of 37°C and under water stress conditions [45]. In what relates to the Mediterranean region, the annual greenhouse gas emissions account for around 5.4 tonnes per capita, compared to 4 tonnes per capita as a global average [30]. Additionally, the northern part of the region is responsible for 70% of total Mediterranean CO2 emissions which is approximate 8% of the world's total emissions [30]. Certain countries are also expected to witness a blast in greenhouse gas emissions including Lebanon, Turkey, Algeria, Malta, and Tunisia [30]. Therefore, extra CO2 accumulation will result in the region and will affect fungal attack patterns in a way favoring *Aspegillus* sp. infections and the production of aflatoxins.

Finally, several studies suggest that global warming is causing pests and diseases to move towards the poles, which may lead to damage of staple crops and the decreased resilience of plants, making them more prone to infection with *Aspergillus* sp. and contamination with aflatoxins [38, 46].

#### **3.2 Harvest and postharvest effects**

The changed climatic conditions can lead to early maturing of the plant and can create favorable conditions for *Aspergillus* sp. infestation and aflatoxin production at time of harvest, especially upon the dominance of high temperatures and humidity. Following harvest, drying is considered an important stage in aflatoxin control, so upon reaching adequate water activity levels, crops can be admitted safely into storage. However, with the dominance of extreme environmental conditions, especially, high humidity, reaching adequate water activity before storage would be hard to achieve. Additionally, the sudden patterns of rainfall, precipitation, and dew can lead to the soaking of crops and the failure of the drying procedure specifically if sundrying was performed in the open fields [47].

The challenge, therefore, is preserving the crop from *Aspergillus* sp. at the time of storage since in case it was present, most likely it would keep on growing and metabolizing aflatoxins [48]. According to Magan et al., stored crops are usually alive respiring media during postharvest in storage facilities, therefore, it is extremely important to consider the interacting abiotic and biotic factors in assessing the changes related to climate change [47]. Notably, it is essential to control temperature and relative humidity during storage and maintain them at levels below 10°C and 70%, respectively, which would be challenging in traditional storage facilities prevalent in some Mediterranean countries in climate change scenarios [49]. Therefore, under uncontrolled storage conditions, such as in the presence of pests that are facilitated by increased attack patterns due to climate change scenarios, and upon the increased growth and multiplication of different bacterial and fungal species in the presence of elevated temperatures and humidity, increased water evaporation and condensation could result, leading to damp conditions that support *Aspergillus* sp. metabolism and growth, subsequent aflatoxin production, and the formation of internal pockets of contamination [49]. Therefore, with climate change scenarios, aflatoxin contamination is expected to increase in the Mediterranean basin during storage, specifically since countries of the region rely heavily on imports and storage of grains. This might lead to increased AFB1 in food and feed and subsequent AFM1 contamination of milk and dairy products.

#### **3.3 Recent occurrence data of aflatoxins in the Mediterranean region under changing climate scenarios**

Until recent years, aflatoxin contamination was not a food safety concern in the Mediterranean region, specifically in the European part, however, the change in climate patterns has altered this situation and created an increased risk of *Aspergillus* sp. attacks and aflatoxin contamination in regions once considered as temperate [50].

Many studies are indicating that aflatoxins are increasingly detected in parts of the Mediterranean, specifically, southern Europe, in quantities not observed before. In Italy, in 2003 and 2004, a set of dry and hot episodes led to the colonization of *A. flavus* and subsequent aflatoxin production in maize intended for animal feed [44, 51]. In Serbia, during the year 2012, and due to hot and dry weather, 69% of maize samples were contaminated with aflatoxins [38]. In Hungary as well, a reported increase in aflatoxin contamination was attributed to climate change conditions in 2012 [38]. In the summer season of the same year and due to elevated temperatures and drought conditions, a shift in fungal attack patterns was observed in Northern Italy, where a switch from *Fusarium* sp. to *A. flavus* was observed in maize that resulted in subsequent production of AFM1 in the dairy chain [45]. Similarly, an outbreak of aflatoxin contamination of maize was reported in the Balkan region in 2013 [37].

In 2015, several noncompliances with the limits specified by the European Commission were also reported in North Italy [37]. Additionally, in the last years, the dominance of hot and dry seasons led to *A. flavus* infections in maize in several Mediterranean countries including Romania and Spain [52]. *A. flavus* infection was also observed in gape vineyards in Lebanon due to increased temperatures where usually *A. carbonarius* that generally produce ochratoxin A are traditionally detected [53].

According to Battilani et al., that investigated the probability of emergence of AFB1 in European cereals due to climate change, there will be a clear increase in the

#### *Aflatoxins in the Era of Climate Change: The Mediterranean Experience DOI: http://dx.doi.org/10.5772/intechopen.108534*

risk of aflatoxin contamination in countries such as Spain, Italy, Greece, Portugal, Bulgaria, Cyprus, ad Turkey [41].

The increased risk of AFB1 contamination is most likely to appear as well as AFM1 contamination in milk and dairy products. Several previous studies as well have reported AFM1 contamination in a number of Mediterranean countries. For example, AFM1 contamination was reported in countries such as Spain, Turkey, Lebanon, Egypt, and Syria where AFM1 was found in 33%, 12%, 59%, 38%, and 14% of raw milk samples, respectively [54, 55]. Also, AFM1 levels in raw milk samples from Bosnia and Herzegovina and Croatia were reported at 6.22 ng/kg and 5.65 ng/kg, respectively [56]. Additionally, AFM1 contamination was reported in dairy products from the region; in Lebanon, Portugal, Italy, and Turkey AFM1 was reported in 66%, 4%, 80%, and 40% of different dairy products, respectively [55–57]. The contamination with AFM1 can be directly attributed to AFB1 presence in animal feed that might be due to on-field or during storage contamination.

## **4. Aflatoxins economic impact and control**

#### **4.1 Impact on global food chain and economy**

Mycotoxins prevalence presents a global issue and contamination of crops takes place worldwide impacting the economy significantly. The Food and Agriculture Organization of the United Nations estimated that "approximately 25% of cereals produced around the world are contaminated with mycotoxins". However, recently, Eskola et al. reported that this figure underestimates worldwide occurrence and considered that 60–80% of crops are contaminated above detectable levels [58]. Eskola et al. attributed this increase to improvements in analytical methods' sensitivity in addition to the possible impact of climate change [58]. In the United States of America, for example, mycotoxins result in crop losses that average 932 million dollars per year and worldwide annual losses due to those natural toxins amount to around 1 billion metric tons of food and food products as estimated by the Food and Agriculture Organization (FAO). More specifically, losses due to aflatoxin contamination in maize top up to 160 million dollars annually in the U.S.A. [50]. Developing regions, such as Africa where losses are alarming, might be affected seriously by aflatoxin contamination problems due to several aspects including; export rejections, a subsequent decrease in the market value of contaminated products, and decrease in crops marketability. This effect was evident since according to Gbashi et al., losses in sub-Saharan Africa amount to a total of 450 million dollars representing 38% of global losses in agricultural commodities due to aflatoxins [50, 59]. The presence of aflatoxins may disrupt the world trade system, as well, since many basic foodstuffs such as vegetables, fruits, dried fruits, nuts, oilseeds, cocoa beans, coffee beans, herbs, spices, milk, dairy products, beer, and animal feed can be contaminated. And ideally, to get rid of aflatoxins, contaminated commodities should be destroyed resulting, therefore, in huge losses. Alternatively, in some cases contaminated crops are redirected to be used as animal feed, the thing that may cause undesirable consequences including reduced growth rates, illness in animals, and the carry-over of residues or byproducts of aflatoxins into animal products such as milk and dairy products that further augment the economic problem of mycotoxins. In addition to that, aflatoxins impact economy due to the cost of analysis and strategies in order to control it, and to the burden it could add to healthcare cost due to health problems it induce.

#### **4.2 Aflatoxin control across the food chain**

Aflatoxin production is generally unavoidable when the environmental conditions are permissible, however, some control strategies can be applied from the first stages of the food chain until the last stages which may decrease contamination of the final product (**Figure 4**) [39].

Starting from preharvest stage good agricultural practices can be applied including tiling, deep plowing, crop rotation, proper irrigation methods, weed removal, timing the production cycle, and use of high-quality seeds and disease-resistant cultivars, etc. [60–62] Following that, proper harvest is crucial to decrease the chances of contamination. Strategies at harvest include performing harvest in a dry weather and at a fast rate, checking for signs of fungal contamination and separating diseased crops from intact ones, and properly use clean equipment to avoid mechanical damage to crops [60]. Following that, drying should be performed in controlled conditions of temperature and humidity, and it is very crucial to reach the desired safe moisture content before storage [60].

Storage is a very critical stage for aflatoxin control. During that phase, controlled conditions of temperature and humidity should be applied to prevent fungal growth and subsequent mycotoxin production. *Aspergillus* sp. can become of important significance in case storage was done in classic silos and containers under uncontrolled conditions. According to Villers 2014, "Aflatoxin-producing molds grow exponentially in conventional multi-month storage as a result of a combination of heat and high humidity" leading, therefore, to increased aflatoxin contamination in storage [63]. Additionally, classic storage facilities are not well sealed and insulated against outer environmental factors, so this would lead to water evaporation due to grain metabolism followed by condensation which will eventually increase water activity of the crop and lead to the development of internal pockets of fungal contamination including *Aspergilluss* sp. That will lead to subsequent aflatoxins production and increased contamination [49]. Therefore, it is very important to control temperature and relative humidity and maintain them at levels below 10°C and 70%, respectively through the whole period of storage [39]. It is also essential to weatherproof and seal storage facilities against weather conditions and pest attacks.

Across the food chain, several decontamination methods could be applied, either biological, physical, or chemical to decrease aflatoxin contamination, however, up till now there is no technique developed that has proved to be simultaneously effective

**Figure 4.**

*Strategies to decrease aflatoxin contamination through the whole food chain [49].*

#### *Aflatoxins in the Era of Climate Change: The Mediterranean Experience DOI: http://dx.doi.org/10.5772/intechopen.108534*

and practical at the industrial scale [39]. Recently, increased concentration has been applied on the development of novel techniques that can be used to naturally bind aflatoxins in food. Examples of such developments include the usage of lactic acid bacteria [64] and their biofilms [65] to bind AFM1 in milk. In addition, other adsorbents such as chitin and shrimp shells were also highly effective in AFM1 removal from liquids [66]. As for processing, the highly stable nature of aflatoxins renders them highly resistant to any processing techniques including the application of heat in procedures like pasteurization.

Finally, and before admission to consumers, to ensure the safety of their population health, many countries around the world have set regulations for aflatoxin in food in the forms of maximum tolerable limits (MTL). These limits are established based on the fact that it is practically hard to achieve zero contamination in many foodstuff and those are decided according to the tolerable daily exposure to aflatoxins at levels that do not pose health risks.

### **5. Conclusion**

Climate change patterns are expected to induce changes creating more favorable conditions for *Aspergillus* sp. attacks, growth, and metabolism. Subsequently, aflatoxins production is expected to increase specifically AFB1. The Mediterranean region, once considered as a temperate region, is considered to be highly affected by the ongoing changes, therefore, contamination with AFB1 in several commodities is expected in addition to the contamination of AFM1 in the milk and dairy products chain which presents emerging threats on food safety, security, and trade.

Finally, more research is needed to determine emerging toxin production patterns, agricultural mitigation practices, and strategies to reduce the impact of contamination on consumers' health. Additionally, studies particularly designed to explore the fungal attack patterns and mycotoxin production tailored to the Mediterranean region are required.

### **Author details**

Rouaa Daou, Jean Claude Assaf\* and André El Khoury Faculty of Sciences, Centre d'Analyses et de Recherche (CAR), Unité de Recherche Technologies et Valorisation agro-Alimentaire (UR-TVA), Saint-Joseph University of Beirut, Mar Roukos, Lebanon

\*Address all correspondence to: jeanclaude.assaf@net.usj.edu.lb

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
