Keywords

3.1 Introduction

Recently, the entire universe has encountered a major challenge of food security and protection as part of the major difficulties affecting the entire population of the world. Food safety and security are primarily defined by (i) adequate availability of food; (ii) quality, nutritional, and cultural use of food for healthy life, and (iii) access to safe food (Nazhand et al. 2020). Factors connected to food scarcity, insecurity, and nutritional imbalance not only affect human health and well-being but also play key roles in the economic, political, and social outlook of a society. In respect to the foremost point, pre-harvest and post-harvest losses due to the contamination of mycotoxin are reported as one of the main factors causing insecurity of food since these substances occur along most food chains from farm to fork (Udomkun et al. 2017).

In the 1960s, more than hundreds of deaths were reported in Turkey due to the consumption of groundnut meal which was infected by mold, which brought about the advent and discovery of aflatoxins. A toxin secreted by two fungi, which are Aspergillus flavus and Aspergillus parasiticus, in several cultivars of agricultural crops is known as aflatoxin (Khlangwiset et al. 2011). Aflatoxins are groups of highly toxic secondary metabolic products of some Aspergillus spp. such as Aspergillus flavus, Aspergillus parasiticus, Aspergillus nomius, Aspergillus fumigatus, and Aspergillus tamari, though they are also produced by species such as Emericella spp. Aflatoxins are reported in feeds and foods during germination, cultivation, and storage stage. Both fungus (Aspergillus flavus and Aspergillus parasiticus) are predominant in crops, especially in groundnut, tree nuts, oil seeds, and maize, and in subtropical and tropical areas throughout the world (Khlangwiset et al. 2011). A study has shown that groundnuts are vulnerable and susceptible agricultural crops to aflatoxin contamination due to their relatively high moisture content, cultivation methods, and storage process which favored mold attack (Wu 2006). Furthermore, due to conducive social and environmental conditions, most countries which are developing and underdeveloped experience more cases of aflatoxin contamination in foods on a frequent basis (Ismail et al. 2015; Wu 2006).

More than 5 billion individuals are at risk of chronic exposure to aflatoxins, mostly in the developing countries. The tolerance level of the plant varieties to change in climate, rainfall pattern and drought, framing practices, and insect damage are factors that influence aflatoxin production by fungi. As earlier stated, the fungal contamination can occur during post-cultivation activities and crops such as groundnut and maize are highly vulnerable to Aspergillus attack due to the high level of consumption (Khlangwiset et al. 2011; Strosnider et al. 2006). Aflatoxins are of several types, but the popular ones are aflatoxin B1 (AFB1), aflatoxin B2 (AFB), aflatoxin G1 (AFG1), and aflatoxin G2. AFG2, are capable of poisoning the body through respiratory, mucous, or cutaneous pathways, which prompt excess activation of inflammatory response, while aflatoxin M1 (AFM1) and aflatoxin M2 (AFM2 ) are found in milk and are the hydroxylated metabolites of AFB1 and AFB2 (Kumar et al. 2017). The level of toxicity of the aflatoxins increases in the order G2, B2, G1, and B1. Aflatoxins are known to be cancerous, mutagenic, and teratogenous in nature to humans and animals (Galvano et al. 1996). The International Agency for Research on Cancer (IARC) has categorized aflatoxins B1 (AFB1) as a group 1 carcinogen (“carcinogenic to humans”) (Wu et al. 2009). The chain of transmission of aflatoxins from fungi to humans is shown in Fig. 3.1.

Fig. 3.1
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Transmission chain of aflatoxin from fungi to humans. (Source: Kumar et al. 2017)

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3.2 World Population Growth and Food Production Level

Figure 3.2 shows the increasing rate of population growth among the ten most populous countries around the world. These countries include China, India, The United States of America, Indonesia, Pakistan, Brazil, Nigeria, Bangladesh, Russia, and Mexico. China emerges as the most populous country in the world with 1,439,323,776 people followed by India and the United States of America with 1,380,004,385 and 331,002,651 people, respectively. As the world population increases, the demand, supply, and consumption rates of food produce such as cereals, legumes, oilseed, and vegetables increase which indicate that population growth is directly proportional to demand. Planting and cultivation of major cereal crops such as rice, maize, and wheat have also increased tremendously across the world. For example, the amount of cultivated rice, maize, and wheat has increased in multiple folds between 1968 and 2018 (Fig. 3.3). This increase is necessary in order to meet the frequent population growth and high consumption level of food worldwide. This continuous increase in the trend of all crops is essential in order to mitigate the threat to food security. Different factors such as water use, pest infestation, efficiency of fertilizer use, production costs, government support, and change in farming systems have a major impact on crop production (Chang 1993). In 2016, the Food and Agriculture Organization (FAO) of the United Nations set the seventh sustainable developmental goal which is aimed to reduce hunger in different parts of the world by 2030. This may be difficult to achieve due to the advent of several threats which include environmental and abiotic stress such as drought and submergence and biotic stress such as pest, diseases, and fungi, especially aflatoxins that are having a massive effect on food production particularly cereals which are particularly vulnerable to the mycotoxins.

Fig. 3.2
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Increasing population growth. (Source: Population by Country (2020) (Worldometers 2020))

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Fig. 3.3
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World cereal production rate. (Source: FAOSTAT 2020)

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3.3 Occurrence of Aflatoxins in Feed and Food

The World Health Organization has declared aflatoxin as a threat to food security worldwide (Ali 2019). The presence of aflatoxin has been noticed in many food commodities and in animal feed. Certain crops and feeds which are predominately affected by aflatoxins include cereals (rice, corn, wheat, barley), oil seeds (groundnut, peanuts, almonds, pistachios, and other tree nuts), spices, fig, dried fruits, milk and dairy products, and other foods of animal origin (meat, offal, eggs).

3.3.1 Occurrence of Aflatoxins in Cereals

Cereals and their derivatives are the world’s primary foodstuffs for human consumption. Grains of cereal crops such as barley, wheat, sorghum, and corn are prone to aflatoxin accretion, as a result of the presence of aflatoxigenic fungus. Aflatoxin complication which occurs in nature, especially in corn and rice, has become more severe due to frequent change in technological advancement in the agriculture sector. The problem of aflatoxin encountered in cereals is not confined to a particular climatic condition or geographical location of a place. Toxins occur in cereal crops at different stages such as on the field, in storage, on the seed, and in the entire plant (Filazi and Sireli 2013). It was reported that out of all the cereal crops tested for different types of aflatoxins, about 36.7% were infected. The degree of fungal growth and aflatoxin infection in cereals depends on multiple factors such as moisture content, temperature, types of soil, and mode of storage (Mahato et al. 2019). Table 3.1 highlights the occurrence of aflatoxin in cereal crops around the world.

Table 3.1 The occurrence of aflatoxins in cereals
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Rice is the main cereal grain for half of the world’s population followed by wheat, accounting for more than 19% of daily calories. Asia is considered the continent with the highest rice production and consumption. Rice is usually planted and harvested in a subtropical area under a hot and humid climatic condition which enhances the growth of fungus and the secretion of secondary metabolites. Rice may be infected with fungus-producing aflatoxins when the environment is conducive for their growth on the field, during cultivation, handling, and storage. Several studies have documented the occurrence of aflatoxins in rice which is highly predominant in many Asian countries (Ali 2019). Besides other mycotoxins, AFB1 has been reported to have invaded rice in several countries such as China, the United Kingdom, the United States of America, India, Malaysia, Nepal, Iran, Pakistan, the Philippines, and Egypt (Mahato et al. 2019). The adverse consequences of this form of fungal attack include grain and/or husk discoloration, loss of viability, loss of quality, and contamination with toxins (Filazi and Sireli 2013). The high rate of invasion or occurrence of aflatoxins in rice and its derivatives has highlighted the significance of stringent control of this dietary staple food globally (Ali 2019).

Apart from rice, sorghum is a popular and staple food for most countries. Sorghum is planted in severe environmental conditions, whereby most other crops will not flourish or germinate well. Increasing and improving the production level, easy accessibility, adequate storage, and process of this crop will significantly reduce the threat to food security and increase the nutritional level of the crop. Usually, sorghum is cultivated as fast as possible in order to allow the germination of other crops on the same field. In some cases, the cultivation of sorghum is done when there is a change in climatic conditions such as flooding, high rainfall, and hurricanes, thereby increasing the moisture content of the harvested crop which stimulates the growth of mycotoxin-producing fungus (Filazi and Sireli 2013).

3.3.2 Occurrence of Aflatoxins in Oil Seeds

Oil seed crops mainly include seed of flowers, soybeans, canola, safflower, rapeseed, peanuts, flaxseed, mustard seeds, and cotton seeds, used for different purposes such as cooking oil production, protein feed for animals, and commercial applications. Castor beans and sesame are other forms of known oil seeds. Following the removal of oil from the seeds, the remnants are a good source of protein, particularly for livestock meal, which includes press or oil cake (Filazi and Sireli 2013). The crop and its derivatives are mostly eaten as snacks, and some of its ingredients are included in a normal human meal. Being aware of mycotoxin’s existence has led to an increasing concern about their existence in edible materials. Oil seed crops are considered as a possible substrate for the secondary metabolites by a fungus, particularly the induction of aflatoxin by toxigenic strains of Aspergillus flavus and Aspergillus parasiticus (Kershaw 1982). Peanut’s moisture content is one of the major factors which trigger the growth of fungus and production of aflatoxins. The presence of a suitable climatic condition enhances fungal growth, thereby promoting a high risk of liver cancer (Kamika and Takoy 2011).

Aspergillus parasiticus regularly attack young plants of peanuts in a systemic manner as a seedling from the seed, soil, and spread to the entire plant although the leaves and petioles are less affected compared to the stems and roots which experienced severe infection (Klich 2007). Aflatoxin infection are observed in tree nuts which include walnuts, pistachios, and almonds, although at a minimal rate as compared with cottonseed and corn, nevertheless the situation is worrisome to the producer due to (i) high unit value of the crop and (ii) the crop are mostly bought by the European markets which impose a significant limit as compared to other nations. The infection of peanuts by aflatoxins due to the attack of either A. flavus or A. parasiticus is a major concern in tropical semi-arid areas where plants are mainly rain-fed, while the contamination of peanuts by aflatoxins does not in any way reduce the harvested yield. However, accumulation of a high amount of aflatoxins induced by the fungus in the nut could threaten the well-being of the mankind and animals’ health (Filazi and Sireli 2013). Aflatoxin occurrence in oil seeds in different regions around the world is highlighted in Table 3.2.

Table 3.2 The occurrence of aflatoxins in oil seeds
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3.3.3 Occurrence of Aflatoxins in Spices

For many decades, spices have been utilized as fragrance, color, and preservatives for beverages, food, and flavor. In regard to the world commercial value, the most important spices include black pepper (Piper nigrum L.), chili (Capsicum annuum L.), nutmeg (Myristica fragrans), cumin (Cuminum cyminum), cinnamon (Cinnamomum), ginger (Zingiber officinale), turmeric (Curcuma longa), cloves (Syzygium aromaticum), and coriander (Coriandrum sativum) (Ozbey and Kabak 2012). Chili (Capsicum annuum L.) is among the spices which have gained popularity around the world, and it is mostly eaten as a food ingredient, especially in Southeast Asia and Latin America due to its taste, pungency, color, and flavor (Jalili and Jinap 2012). Due to its drying and processing method, climatic and environmental changes such as temperature, relative humidity, and insect and pest attack, spices tend to be highly infected by toxigenic and two mycotoxins which include aflatoxins (AFs) and ochratoxin A (OTA) (Ozbey and Kabak 2012). It was reported that several cultivars of spices such as black pepper, cardamom, cinnamon, clove, cumin, coriander, and ginger are contaminated with aflatoxins in various regions (Mahato et al. 2019). Contamination of spices with Fusarium and Alternaria alternata was observed in fresh and sun-dried pepper (Iqbal et al. 2011). Fungal infection such as mold infection in spices can be witnessed at different stages which include the time of crop production in the field, after harvest and during storage as well as when conditions are suitable for the growth (Filazi and Sireli 2013). After harvest, sun-drying is a popular practice in certain countries around the world, which requires the pepper being spread out on the soil in a single layer. Hot pepper is contaminated with A. flavus and A. niger during storage. During storage, infection of spices with A. flavus consequently producing aflatoxins is regarded as one of the most severe problems threatening food security globally (Iqbal et al. 2011). Previous aflatoxin occurrence in spices across the world is being highlighted in Table 3.3.

Table 3.3 Occurrence of aflatoxins in spices
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3.3.4 Occurrence of Aflatoxin in Milk and Dairy Products

Milk is a highly nutritious food consisting of several nutrients which are crucial for the development and maintenance of human well-being. The health status of people in a given population is often reflected in the condition of their food-producing ecosystems. In addition, enforcing food legislation may be directly connected to the amount and quality of foods available. Therefore, consumers in developing nations, in particular the rural inhabitants, are faced with food security and animal safety problems as they rely on foods grown locally (Iqbal et al. 2015). When breastfeeding mammals such as sheep, goats, and cows consumed foods which are contaminated with aflatoxin B1 (AFB1) and B2 (AFB2), these metabolites are transformed to aflatoxins M1 (AFM1) and M2 (AFM2) (Filazi et al. 2010). The quantity of AFM1 in milk is directly proportional to the quantity of AFB1 present in feed ingested by animals. AFM1 infection of milk is posing a real threat to the human health, both in adults and infants, but it is more severe in infants due to high dependence on milk for their daily nutrition (Offiah and Adesiyun 2007).

Around 1–2% of AFB1 present in animals’ feed are converted to AFM1 in milk although this varies from one animal to another, day to day, and depending on the type of milk consumed. When the consumption of AFB1 has ceased, the concentration in milk reduces after 72 h to a level which cannot be detected (Filazi et al. 2010), but can be detected between 12 and 24 h of intake, and the bulk of AFB1 and AFB2 consumed by mammals are expelled from the body through feces and urine, but a few are bio-transformed in the liver and discharged simultaneously with milk in the form of AFM1 and AFM2, respectively (Filazi and Sireli 2013).

Occurrence of AFM1 in milk and dairy products has been reported in many countries (Table 3.4). The existence of aflatoxin M1 (AFM1) in both dairy products and milk is a serious concern throughout the world, but it is more severe in developing nations (Iqbal et al. 2015), due to its carcinogenic, teratogenic, and mutagenic nature, which can lead to acute and chronic illness in humans and animals (Offiah and Adesiyun 2007). Contamination of milk with AFM1 has been experienced in several countries. Different factors contribute to contamination of milk with AFM1 such as change in climatic and environmental condition, change in feeding and agricultural practices, and the quality and safety control system of the food business operators in accordance with the different legislations. For instance, the Po valley (a province in Italy) which is the producer of almost all the milk consumed in the country, is regarded as the most susceptible region to AFM1 due to its climatic conditions. AFM1 can withstand heat deactivation process such as sterilization and pasteurization during food processing. So, cheese or any other products made from contaminated raw milk automatically contain AFM1 (Serraino et al. 2019). To guard clients, mainly kids, from infected milk and dairy products, numerous nations have mounted regulation to adjust the levels of AFB1 in feeds and AFM1 in milk and cheese. The European Union limits for AFM1 in milk and cheese are 50 ng/L and 250 ng/kg, respectively (Filazi et al. 2010).

Table 3.4 The Occurrence of aflatoxins in milk and dairy products
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3.4 Aflatoxin Safety Regulation

In order to control the level of aflatoxins intake in food, the European Union in 2007 set a safe limit for total aflatoxins and aflatoxins B1 to be 4 μg/kg and 2 μg/kg accordingly for human consumption, where as in 2010 it was reviewed that the safe limit was set at 5 μg/kg and 10 μg/kg for aflatoxins B1 and total aflatoxins, respectively. This has helped mitigate the level of aflatoxin in consumable agricultural commodities in Europe. Moreover, several other countries such as Taiwan, Canada, and the United States of America have set their safe limit at 10 μg/kg, 15 μg/kg, and 20 μg/kg, respectively (Ali 2019). The lowest safe limit for AFB1 was at 1 μg/kg in Switzerland (Creppy 2002) and Bosnia and Herzegovina (Alessandra et al. 2011), while in Japan aflatoxins must be absent in crops for human consumption (Dadzie et al. 2019). Furthermore, in developed countries mentioned earlier, apart from the imposition of strict rules and regulation, other factors such as high rate of literacy and awareness among farmers and consumers, technological advancement both during processing and at storage stage has been associated with the low level of aflatoxins in such nations (Ismail et al. 2018).

However, in Africa and certain Asian countries, there are no strict safety regulations in place to curb the level of aflatoxins present in food commodities consumed by the population, which may be considered as one of the possible reasons for the presence of the high level of aflatoxins in food products. This has led to major health consequences among the people living in this part of the world. In addition, the presence of suitable environmental condition for aflatoxin development, technological hurdles, high rate of illiteracy among farmers and consumers and lack of awareness, poor storage condition and facilities, and overall high rate of poverty may also be considered as possible reasons for the high level of aflatoxins in Africa and certain Asia nations (Ismail et al. 2018).

3.5 Mycotoxins: Hidden Toxins

Mycotoxins are believed to be a part of the fungal chemical protection system that safeguards them from living creatures such as microorganisms, grazing animals, nematodes, insects, and humans. Mycotoxins can be found in food and several harvested crops and produce through many infection routes, at various phases of production, processing, transport, and storage. Mold and mycotoxin development are affected by numerous biotic and abiotic factors such as relative humidity, fungicides and fertilizers, temperature, insect infestation, kind of substrate and dietary factors, geographical place, genetic requirements, and interaction among the colonizing toxigenic fungal species (Rychlik et al. 2014). Aspergillus, Fusarium, Alternaria, and Penicillium are the most crucial fungal genera that produce mycotoxins which are found in foods and feeds. Mycotoxins which cannot be detected through traditional analytical methods due to modification of their form and structures inside the plants are referred to as masked mycotoxins (Berthiller et al. 2013). Nevertheless, the modified mycotoxins can be returned to their toxic nature during food processing and digestion through the process called hydrolysis. Parts of the altered toxins are found in various forms as complexes together with matrix compounds; for this reason, they can also be known as matrix-associated mycotoxins. Hidden fumonisin in its altered forms was returned to its toxic nature via hydrolysis and was eventually analyzed and determined via LC/MS/MS approach (Mahato et al. 2019). Several of the contemporary issues on the occurrence of masked mycotoxins are reported in different parts of the world including the United States of America, Africa, Europe, and some countries in Asia such as Japan and China. The highest prevalence rate of masked mycotoxins are reported in agricultural products, in particular cereal-based foods, which is threatening and detrimental to both humans and animals’ health (Zhang et al. 2019). Therefore, the determination of masked mycotoxins is an essential part to ensure safety of feed, food, human lives, and animals.

3.6 Conclusion

Aflatoxins (AFs) are toxic secondary metabolites produced by Aspergillus species, which are found in susceptible agricultural products. Aflatoxins can cause substantial economic losses, and they have a detrimental effect on human and animal health. This book chapter summarizes the occurrence, effect, and implications of AF contamination in a wide range of agricultural crops around the world. Contamination of AFs can be found in both tropical and temperate regions of the world. Agricultural crops such as oil seeds, nuts, spices, dried fruit, beans, fruit, and cereals are the most important commodities affected by AFs. Maximum levels of aflatoxins were found in the food commodities of African and Asian countries. Due to the economic importance of AFs, regulations for major mycotoxins in agricultural commodities have been put in place in more than 100 nations, most of which are for aflatoxins, and maximum tolerated levels vary significantly across countries (Filazi and Sireli 2013). The inability to manage and at times even predict production of aflatoxin makes it a unique problem to food security. Although preventing aflatoxin contamination is the best control method, all forms of mycotoxin contamination cannot be avoided. Optimal conditions for post-harvest storage will reduce consumer exposure to most mycotoxins, but detoxification procedures may be needed in certain cases (Reddy et al. 2009).