Aflatoxicosis in Economic Animal Production

1. Introduction

Aflatoxins are a group of secondary fungal metabolites, also known as mycotoxins, which are produced primarily by toxigenic strains of the fungi Aspergillus flavus and Aspergillus parasiticus [1]. Aflatoxins are especially problematic in hot and dry climates, which favor mycotoxigenic fungal growth, so regions with these environmental conditions, namely Sub-Saharan Africa and Southeast as well as South Asia, often experience greater contamination [2]. Besides, their prevalence is exacerbated by drought, pests, delayed harvest, insufficient drying, and poor post-harvest handling [3].

Aflatoxins consist of twenty relative polycyclic structures belonging to a class of compounds known as furanocoumarins [4]. There are mainly six different types of aflatoxins: aflatoxin B₁ (AFB₁), aflatoxin B₂ (AFB₂), aflatoxin G₁ (AFG₁), aflatoxins G₂ (AFG₂), aflatoxin M₁ (AFM₁), and aflatoxin M₂ (AFM₂) [5]. Out of these AFB₁, AFB₂, AFG₁, and AFG₂ are found in food crops or their products, while AFM₁ and AFM₂ (metabolite of AFB₁ and AFB₂) are found in the animal by-products such as milk and eggs [1]. Aflatoxin B₁ as the most toxic and prevalent aflatoxins mainly exhibits severe hepatoxicity that not only induces human hepatitis and liver cancer but also inhibits growth performance and reproduction ability in livestock, resulting in negative effects on human and animal health, food security, and economic trade [6,7]. The potential economic losses to the U.S. corn industry by aflatoxin contamination were estimated at between US$52.1 and US$1.68 billion annually [8].

2. Toxicities on Animal Production

The liver is the organ most affected by ingesting aflatoxins because it receives and metabolize aflatoxins from the bloodstream [9,10]. Aflatoxin B₁ has to convert to AFB₁-8,9-exo-epoxide (AFBO) by hepatic enzymes (the cytochrome P450 family) to exert toxicity [11-13]. Aflatoxin B₁ has been characterized as hepatotoxic, teratogenic, carcinogenic, and immunosuppressive [14]. Aflatoxin B₁-contaminated feeds can cause animal poisoning, including growth retardation, liver and kidney damage, oxidative stress, immune inhibition, and increased disease susceptibility, eventually leading to significant economic losses [15,16]. Extremely high concentrations of aflatoxins (over 1,000 μg/kg) cause hepatitis, hepatic necrosis, increased clotting time, and, finally, the death of animals caused by severe hemorrhage [10]. Under prolonged exposure period and low-dose conditions, aflatoxicosis causes hepatic lipidosis, portal fibrosis, and liver tumors [17]. Dietary concentrations cause a 5% reduction in growth rate were estimated at 0.3 mg/kg and 1 mg/kg for aflatoxins for pigs and broilers, respectively [18]. Ruminants have a higher tolerance to aflatoxins than non-ruminants due to rumen microorganisms' biodegradation [19]. Expect for sheep, ruminants do not inhibit growth performance and reproductive trait unless their diets contain extremely high concentrations or long exposure time. If multiple mycotoxins contaminate the feed at the same time, aflatoxins can interact with other mycotoxins, such as fumonisins (FUMs), ochratoxin A (OTA), and T-2 toxin (T-2), producing more severe effects on animal performance than individual mycotoxins [20-22]. Among these mycotoxins, FUMs are the most co-occurring with aflatoxins because they have the same mycotoxigenic fungi, such as A. flavus [23,24].

Table 1. The guidance values of the European Union (EU) Commission, United States Food and Drug Administration (FDA), and China for aflatoxin B₁ concentrations (μg/kg) in complete feed [25-27].

2.1  Swine

Aflatoxin exposure generates the main symptoms in pigs, including lethargy, hypothermia, low growth performance, high mortality, impaired blood coagulation, poor liver and kidney functions, immunosuppression, and increased disease susceptibility [10,28]. Acute aflatoxicosis is uncommon in swine unless the feed contains aflatoxin concentrations beyond 1,000 μg/kg, but it causes severe liver lesions, and signs are a consequence of liver dysfunction, such as hemorrhages, jaundice, and sudden death [29]. Aflatoxins at lower doses are cumulative [30]. Thus, chronic aflatoxicosis is more common in swine due to ingesting of lower amounts of aflatoxins for a prolonged period and is expressed as lower feed intake and growth rate [28].

Previous studies have shown that piglets fed a diet contaminated with 200 μg/kg of aflatoxins decreased growth rate [31]. Other previous research reported that it not only decreased the growth rate of piglets fed a diet contaminated with 280 μg/kg of AFB₁ but also decreased the final body weight and average daily intake [28]. The adverse effect of AFB₁ on growth performance partially results from undereating and decreased nutrient digestibility [28]. Aflatoxin concentrations above 400 μg/kg can cause porcine organ pathological lesions, such as the liver, spleen, lymph node, kidney, uterus, heart, and lungs [10,18]. Furthermore, aflatoxins induce immunosuppression, increasing infectious disease occurrence and decreasing vaccination efficacy [30]. For instance, aflatoxins increase the susceptibility to Brachyspira hyodysenteriae and Erysipelothrix rhusiopathiae [32,33]; besides, these mycotoxins inhibit the vaccination efficacy of E. rhusiopathiae and ovalbumin [9,33].

Additionally, among aflatoxins, AFM₁ is the monohydroxylated derivate of dietary AFB₁ formed in the liver and excreted into the milk of lactating sows, and this toxic metabolite can be transmitted from lactating sows to nursing piglets via milk [10]. The growth performance of piglets is permanently stunted, delaying the time to market weight and increasing feeding costs even though they are not exposed to aflatoxins after weaning. Furthermore, the mortality of piglets with aflatoxicosis reaches 20%, characterized by enterocolitis, diarrhea, and a suppressed immune system, leading to decreased resistance to infectious diseases [34]. In addition, several cases of carry-over in swine have been reported for AFB₁ [35,36]. It may occur in the liver, muscles, and adipose tissue. The most toxic mycotoxins commonly found in pork are AFB₁ and OTA [35].

Table 2. Aflatoxin toxicity on production performance in swine.

2.2 Poultry

Poultry aflatoxicosis has been documented for a long time. Aflatoxins were first discovered in the UK in 1960, being confirmed as the causative agent for the outbreak of turkey X diseases, which killed over 100,000 turkeys and other kinds of poultry [39]. The contaminated feeds contain high levels of aflatoxins, causing turkey X diseases with major symptoms of liver necrosis and bile duct hyperplasia [40]. Aflatoxin contamination is still a threat to the poultry industry and has resulted in substantial economic losses to farmers until now because global climate change increases aflatoxins outbreak worldwide [41]. In poultry, adverse effects of aflatoxins include a reduction in growth rate and feed efficiency, a decline in egg production and hatchability, and an increase in susceptibility to infections [42].

Ducklings are the most sensitive poultry species to aflatoxins, followed by turkey poults, broilers, and laying hens, as the ducklings showed 100% mortality at 1 mg/kg AFB₁ [43]. Moreover, with every 0.1 mg/kg increase in dietary AFB₁, cumulative feed intake and body weight gain decrease by approximately 230 g and 169 g per duckling from hatch to the age of 14 days [44]. Ducklings are 5- to 15-fold more sensitive to aflatoxin toxicity than laying hens [45]; therefore, many countries set stricter limits for the former than other poultry species [46,47]. Aflatoxin-contaminated feed affects almost the entire poultry body system, such as interference in bone metabolism resulting in bone strength decline, bone diameter reduction, as well as dressed weight and breast yield decrease [48]. In disease infection, a recent epidemiological study indicated a high correlation between the infection rate of Newcastle disease and aflatoxin contamination status in broilers [49]. In addition, aflatoxins lead to reduced egg production, poor egg quality, and increased mortality in laying hens [42]. Aflatoxin B₁ adversely influences egg quality by decreasing the shell thickness and weight [50]. Besides, aflatoxin residues from poultry can appear in eggs and edible tissue, which raises public health concerns when humans consume these aflatoxin-contaminated products [51].

Table 3. Minimum aflatoxin B₁ concentrations (μg/kg) with major effects in poultry [52-54]

2.3 Ruminant

In general, ruminants, except sheep, are more tolerant to aflatoxins due to rumen microorganisms’ biodegradation [19]. Calves are more susceptible than mature ruminants because the rumen environment of the former does not complete development. In dairy cows, chronic exposure to aflatoxins can reduce growth and lactating performance, impair liver function, compromise immune function, and increase disease susceptibility [55,56]. A previous report [57] indicated that feeding 75 μg/kg AFB₁ of diet dry matter (DM) to dairy cows for 4 weeks reduced milk yield by 2.5 kg and 3.5% fat-corrected milk yield by 1.7 kg. Previous scientists [58,59] observed that consuming 2.5 mg/kg aflatoxins of diet DM for 5 weeks caused liver damage, reduced body weight gain, feed intake, and feed efficiency of growing lambs but had no effects on rumen fermentation. It indicated that the negative impacts of aflatoxins on ruminal growth and lactating performance are due to the systematic toxicity effects, including immunosuppression, rather than direct toxicity to rumen microorganisms [56]. Besides, some recent studies also confirmed the negative impact of aflatoxins on bull spermatozoa, fertilization competence, and preimplantation embryo development in dairy cows [60,61].

When ruminants are fed with a contaminated diet containing AFB₁, the mycotoxin is metabolized to AFM₁ in raw milk [62]. Aflatoxin B₁ and aflatoxin M₁ are stable in heat with carcinogenic, mutagenic, and teratogenic effects in humans and animals [63]. It should be noted that the carcinogenic potency of AFM₁ is almost as high as that of AFB₁, and the toxicological properties are generally comparable [64]. Therefore, many countries have set AFM₁ maximal concentrations in raw milk and milk products to avoid human exposure. The AFM₁ maximum residue level permitted in milk has been set by the European Union (EU) and the United States Food and Drug Administration (FDA) at 50 ng/kg and 500 ng/kg of raw milk, respectively [65].

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