Aflatoxins in the Era of Climate Change: The Mediterranean Experience

Abstract

Aspergilluss sp. is a fungi that attack crops on the field or during storage. Generally, those fungi are most frequent in tropical and subtropical regions where environmental factors characterized by high humidity and temperatures are favorable for their production. Aflatoxins are produced as their secondary metabolites including aflatoxin B1. Aflatoxins have been classified as carcinogenic to human by the International Agency for Research on Cancer due to their profound health effects, mainly, hepatocarcinogenicity. Hence, they contaminate a large share of the global food chain. Traditionally, aflatoxin contamination was not frequent in temperate regions such as the Mediterranean, however, with climate change patterns including elevated temperatures, increased humidity, and increased droughts, a shift in fungal attack patterns is expected in such areas in a way that favors Aspergillus sp. infestation and aflatoxin contamination. Therefore, with increased global warming more aflatoxin contamination is expected in the Mediterranean basin, specifically, the Sothern European countries.

1. Introduction

1.1 Aflatoxins

Aflatoxins (AFs) are a group of mycotoxins produced by Aspergillus species mainly by A. flavus and A. parasiticus [1] and to a lesser extent, by A. bombycis, A. ochraceoroseus, A. nomius, and A. pseudotamari [2]. Eighteen AFs have been identified so far, but the ones with major significance are aflatoxin B₁ (AFB1), aflatoxin B₂, aflatoxin G₁, aflatoxin G₂, aflatoxin M₁, and aflatoxin M₂ [1, 3]. AFs are difuranocoumarin molecules that are produced by the polyketide pathway of fungi. Molecular differences among AF groups exist; for example, the B-aflatoxins exhibit a cyclopentane ring while the G-aflatoxins have a lactone ring (Figure 1) [3]. In addition to that, B-aflatoxins display blue fluorescence under ultraviolet light, while G-aflatoxins exhibit a yellow-green one.

Figure 1.

Aflatoxins molecular structures.

Aspergillus species are very diverse and can adapt to a wide range of environmental conditions [4] but mainly they are found in hot humid climates typically in tropical and subtropical regions, most significantly, between 40°S and 40°N latitude [5]. Aspergillus sp. optimal growth happens at a temperature of 25°C with a minimum water activity of 0.75, however, their secondary metabolites production starts at 10–12°C with the most toxic metabolites produced at 25°C with 0.95 water activity [1]. Those growth patterns differ between different strains of Aspergillus sp., for example, optimal growth temperature of the most significant strains, A. flavus and A. parasiticus, occurs at 33°C and 35°C, respectively [6, 7].

On-field, normally, A. flavus, that naturally colonize the aerial parts of the plant including leaves and flowers, produces B aflatoxins while A. parasiticus, which are usually found in the soil environment, produce B and G aflatoxins. As for aflatoxin M₁ and M₂ they are produced in vivo as the hydroxylated metabolites of aflatoxins B₁ and B₂, respectively. Naturally, the colonization rate of Aspergillus sp. and the degree of contamination with AFs are determined by several factors including; temperature, a_w, and humidity. Additionally, contamination is promoted due to stress or physical damage to the crop especially due to drought episodes, insect infestation, rain showers during pre-harvest, poor harvest timing, and insufficient drying before storage [1]. Aspergillus species can further colonize the crop during storage, specifically under uncontrolled conditions that allow their domination such as increased humidity and temperature. Many types of crops and plants that are used as a source of human food or animal feed are prone to colonization by Aspergillus sp. and subsequent contamination with AFs, such as wheat, barley, maize, rice, sorghum, soy, peanuts, nuts, oilseeds, legumes, spices, herbs, etc. [1, 2, 8, 9, 10].

1.1.1 Aflatoxin B1 (AFB1)

Among all identified aflatoxins, AFB1 is considered the most common and it accounts for almost 75% of worldwide AF contamination in food and feed [3]. AFB1 production is the result of a complex biosynthetic pathway that involves at least 27 enzymatic reactions [11]. The genes responsible for enzymatic coding are grouped in a cluster and their expression depends on two cluster-specific regulators: aflR and aflS [11]. Additional genes are also involved in the pathway including aflD [11]. AFB1 is the most potent carcinogen among all mycotoxins [12, 13]. It is also the most hepatotoxic and hepatocarcinogenic agent, therefore, it poses the highest concern for food safety and health. Worldwide, AFB1 have been the main aflatoxin causing most cases of aflatoxicoses. According to Paulin et al., AFB1 can cause “acute toxicity, chronic toxicity, carcinogenicity, teratogenicity, genotoxicity, and immunotoxicity” [1]. Many epidemiological studies have demonstrated AFB1 as the major contributor to hepatocarcinoma cases [14] and it had been estimated that 4.2–28.2% of HCC cases worldwide are caused by AFB1 [15]. And due to its well-documented carcinogenicity, the IARC classified AFB1 as carcinogenic to humans (group 1) [16].

Upon intake of contaminated food, AFB1 gets rapidly absorbed through a passive mechanism in the gastrointestinal tract. It is then metabolized in the liver where it gets converted by cytochrome P-450 into aflatoxin-8, 9-epoxide, hydroxylated into a less potent form AFM1, and demethylated into aflatoxin P₁ that is excreted in the urine [12, 14]. The resulting epoxide is highly reactive so it binds to DNA or protein molecules. Binding to a protein molecule in the liver eventually causes hepatotoxicity while binding to a DNA molecule affects the genetic code through transversion of a guanine (G) molecule to thymine (T), therefore, mutating the P53 gene that codes for tumor suppression hence allowing the formation of tumors and leading eventually to hepatocellular carcinoma (HCC) (Figure 2) [12, 14, 17].

Figure 2.

AFB1 metabolism.

1.1.2 Aflatoxin M1 (AFM1)

AFM1 is the hydroxylated metabolite of AFB1 formed in the liver (Figures 2 and 3). Once produced, it gets absorbed by the mammary glands and secreted in the milk of mammals. AFM1_, therefore, contaminates milk and dairy products such as cheese and yogurt due to its capacity to stay intact during milk pasteurization, treatment, and fermentation [18]. AFM1 is less toxic than AFB1 and possess 2–10% of its carcinogenic potency [19]. Nevertheless, AFM1 is capable of binding to DNA leading eventually to hepatocellular carcinoma. The findings of many studies that discussed the carcinogenicity of AFM1 led to its reclassification as carcinogenic to human (group 1) by the IARC in 2002 after it was for long classified as possibly carcinogenic to humans (group 2B) [16]. AFM1 presents a particular risk for infants and children due to the vulnerability of their immune systems, their low body weights, and their high consumption of milk.

Figure 3.

AFM1 chemical structure.

1.2 Health effects of AFs

Aflatoxins’ presence is recognized as a global food safety concern by the World Health Organization since they exhibit several toxic effects on animals and humans. The diseases caused by exposure to aflatoxins are referred to as “aflatoxicosis” that could be acute or chronic. The toxic effects exhibited by AFs depend on several factors such as age, gender, intake dosage, exposure duration, and nutritional status. Acute aflatoxicosis is prevalent when individuals are exposed to food contaminated with high doses of AFs and its symptoms include abdominal pain, vomiting, diarrhea, pulmonary edema, cerebral edema, anorexia, fatty liver, jaundice, depression, and photosensitivity [20]. Acute poisoning is more prevalent in developing countries due to the increased risk of contamination of staple food, lack of food security, absence of AF awareness, and lack of regulatory limits. For example, in Eastern Kenia in 2004, acute liver failure was diagnosed in 317 individuals of which 125 people died later due to acute aflatoxicosis caused by consuming contaminated home-grown maize [21]. Acute aflatoxicosis presents a risk to animals, as well, due to their exposure to AFs through contaminated feed, and the susceptibility varies among different species. Acute aflatoxicosis in animals lead to several complications including decreased weight gain, reduction in egg or milk production, decreased feed conversion, and increased vulnerability to infectious diseases [20].

Chronic aflatoxicosis, on the other hand, is caused by being exposed to low doses of AFs for an extended period and results in immune suppression and cancer. The liver is the primary target organ for AFs and chronic consumption could lead to liver cancer, especially when coupled with hepatitis B and/or C virus since those viruses interact synergistically with AF causing an increased risk of hepatocellular carcinoma (HCC) [21]. Many toxicological studies demonstrated the carcinogenicity of AFs in many species including mice, rats, hamsters, monkeys, and ducks. AFs have been demonstrated as mutagenic compounds that can alter DNA leading to changes in chromosomes and mutations in genetic codes [22]. Enough evidence, therefore, lead to the classification of AFs as “group 1 carcinogen to humans” by the IARC [16]. AFs can also lead to other liver diseases such as cirrhosis and hepatomegaly [21]. Additionally, chronic exposure to AFs have been shown to affect immunity through decreased antibody production, reduced cell-mediated immunity, and decreased resistance to fungal, bacterial, and parasitic secondary infection [20, 21]. AFs exposure may also lead to low birth weights since exposure can occur in the uterus through a trans-placental pathway. Impaired child growth can be also caused by being exposed to AFs, especially since exposure is higher in children due to their low body weights which leads to more toxic effects. For example, a follow-up study in Benin showed that there was a strong negative correlation between aflatoxin-albumin adducts and height increase in children over 8 months period [23, 24]. Similarly, in the Gambia, a follow-up study demonstrated a strong effect of AF exposure during pregnancy on the infant’s growth rate during their first year of life [24, 25].

2. The Mediterranean region

2.1 Region and climate

The Mediterranean is an intercontinental sea located between Europe, North Africa, and Western Asia [26]. Its surface area covers around 2.5 million km² and is surrounded by a total of 22 countries including Lebanon, Cyprus, Egypt, Morocco, Spain, Italy, France, etc. [27, 28].

The Mediterranean climate is characterized by mild wet winters and warm dry sunny summers with temperature and humidity variations among different countries [28]. The sea itself is surrounded by vast land areas and acts as a heat reservoir and a source of moisture for them [28]. The climate in the North and South Mediterranean differs mainly due to the fact that the former includes countries with a west coastal climate (e.g. Spain, Turkey, Cyprus) while the latter includes countries with a subtropical desert climate (e.g. Morocco, Syria) [28, 29]. The summer duration range from 2 to 7 months starting from North to South region.

2.2 Agricultural sector

Agriculture in the Mediterranean countries plays a crucial role in the economy as it provides a main source of income and employment, and ensures food security in the region. Around 28% of the Mediterranean land is devoted to agriculture with discrepancies between different countries depending on economic development, industrialization, urbanization, etc. [30].

Agriculture in the Mediterranean basin depends on irrigation, especially in the long hot dry summer seasons. Precipitation across the region is also subject to high inter-annual and seasonal variations, therefore, making it essential for farmers to provide irrigation to maintain crop diversification and assure high quality and yields of crops. Generally, around 21% of cultivated agricultural lands in the area are irrigated, with the main irrigation system being surface irrigation despite its low efficiency.

The Mediterranean region has some unique environmental characteristics that shape its agricultural production. First, its seasonal variation is characterized by rainy mild winters and long hot dry summers. Second, its terrain, in which the presence of coastal plains that support summer agriculture are backed up by low hills or mountains that help provide at sometimes snow water for irrigation in the summer.

Climate patterns also affect agricultural products along the Mediterranean Basin, for example, temperate crops can be cultivated in rainy seasons, while sub-tropical crops can be grown in summer seasons. Several agricultural commodities are produced in the Mediterranean region, first, traditional permanent crops like olives, grapes, fruits, vegetables, and dates. Most of the grapes grown in the Mediterranean region are used for wine production, additionally, grapes are also cultivated for table grapes, currants, and sultanas. Similarly, olives are used to produce olive oil and which amounts to 99% of the world’s output with the main producers being Italy, Spain, and Greece [30]. As for fruits and vegetables, the Mediterranean basin production accounts for approximately 16% and 13% of the world’s fruits and vegetable production, respectively. The Mediterranean region also accounts for 85% of world hazelnut output, 36% of dates, 55% of pulses, etc. [30].

Second, cereals are produced in the region specifically wheat, maize, barley, and rice which contribute to 90% of cereal production [31]. While most of the Mediterranean countries produce cereals, their yields are not enough for local consumption, therefore, most of the countries depend on imports and store cereals for long durations to ensure an adequate and continuous supply. On an overall scale, 16% of total world wheat output is produced in the Mediterranean, with France being the main producer and the only exporter country followed by Turkey, Spain, Italy, and Egypt [30].

2.3 Aflatoxins in the Mediterranean

The climate of the Mediterranean is in general inductive to fungal attacks and mycotoxin production, in addition to other factors, such as prevalence of pests, irrigation systems, droughts, agricultural practices, storage techniques, etc. Generally, the most important mycotoxins in the Mediterranean basin are aflatoxins, ochratoxin A, trichothecenes, and fumonisins with variations in the type and level of each mycotoxin in each country and in different regions [32]. Aflatoxin contamination specifically of dried fruits is most frequent in the southern and eastern parts of the basin including African and Asian countries [32]. Crops such as peanuts, pistachios, and maize are also reported to be contaminated with aflatoxins in the Mediterranean basin [32].

AFM1 is also frequent in Mediterranean countries and has been reported in many studies among different countries due to the presence of AFB1 in the feed either due to field contamination or improper storage practices.

2.4 Aflatoxins regulations in Mediterranean countries

Previous studies done in the Mediterranean region have showed a frequency of aflatoxins contamination specifically AFB1 and AFM1. As a control measure, Mediterranean countries have adopted different regulations while specifically many European countries follow the European Commission legislation (Table 1).

Country	Commodity	AFT (μg/kg)	AFB1 (μg/kg)	AFM1 (μg/l)
Algeria	Cereals	—	10	—
Cyprus	Cereals, pulses, oilseeds, dried fruits, sesame, and their food products	5	—	—
Egypt	Peanuts, oilseeds, cereals, and their products	10	5	—
European Union	All cereals and all products derived from cereals	4	2	—
	Maize and rice to be subjected to sorting or other physical treatment before human consumption	10	5	—
	Groundnuts (peanuts) and other oilseeds and processed products intended for direct human consumption or use as an ingredient in foodstuff	4	2	—
	Almonds and pistachios for direct human consumption or use as an ingredient in foodstuff	10	8	—
	Hazelnuts and Brazil nuts for direct human consumption or use as an ingredient in foodstuff	10	5	—
	Other tree nuts for direct human consumption or use as an ingredient in foodstuff	4	2	—
	Spices	10	5
	Raw milk, heat-treated milk and milk for the manufacture of milk-based products	—	—	0.05
	Infant formula	—	—	0.025
France	Peanuts, pistachios, almonds, and oilseeds	—	1	—
	All cereals	—	5	—
	White wheat flour	—	3	—
	Raw wheat bran	—	10	—
	Whole wheat flour	—	5	—
	All vegetable oils	—	5	—
	Children food products	—	1	—
	Milk	—	—	0.05
	Milk powder	—	—	0.5
	Liquid milk for infants	—	—	0.03
	Milk powder for infants	—	—	0.3
Greece	Dried fruits, peanuts, hazelnuts, walnuts, pistachios, almond, pumpkin seeds, sunflower seeds, pine seeds, apricot seeds, maize,	—	5	—
Italy	All foods	10	5	—
	Spices	40	20	—
Lebanon	Cereals	4	2	—
	Milk	—	—	0.05
Morocco	Cereals and cereal-based products	4	2	—
	Milk	—	—	0.05
Spain	All food for human consumption	10	5	—
Syria	Fluid milk	—	—	0.2
	Powdered milk	—	—	0.05
Tunisia	Cereals	—	2	—
Turkey	All foods	20	5	—
	Infant foods	2	—	—
	Milk and milk products	—	—	0.5

Table 1.

AFT, AFB1, and AFM1 maximum tolerable limits in some Mediterranean countries [33, 34, 35, 36].

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 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 sun-drying 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 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, 56, 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].

Figure 4.

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

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, 61, 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 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.