Deoxynivalenol Toxicosis In Economic Animal Production

1. Introduction

Contamination of mycotoxin in feed causes issues in livestock production processes by reducing growth performance [1]. The most frequently found mycotoxin in feed and feedstuffs is deoxynivalenol (DON) which result in an economic loss of billions of dollars [2]. Deoxynivalenol is trichothecene most commonly detected in toxicologically relevant concentrations for farm animals, and this mycotoxin is mainly produced by Fusarium culmorum and Fusarium graminearum, with more than 60% of feedstuffs testing positive for it [3,4]. Corn, barley, oat, and wheat are the grains affected mainly by DON, due to the fact that Fusarium spp. are the most prevalent DON-producing fungi in East Asia, Northern Europe, and Central Europe [5]. Feed contaminated by DON leads to decreased feed uptake, while high DON levels may lead to vomiting, thus DON is also called “vomitoxin” [6]. The presence of DON in animal feed is practically unavoidable because it is a thermostable compound and also is able to resist low pH levels [7]. Therefore, DON and its metabolite deepoxy deoxynivalenol (DOM-1) readily enter the food chain, causing food poisoning in humans and animals [8]. Several outbreaks of acute human and animal gastrointestinal disorders, including nausea, vomiting, diarrhea, and gastrointestinal discomfort, have also been reported in entire world [9]. Many global surveys indicated DON often co-occurs with other Fusarium mycotoxins, mainly zearalenone (ZEN) and fumonisins (FUM) in raw materials and finished feeds and present the synergistic or additive toxicity in animals [10,11].

2. Toxicities on Animal Production

Monogastric livestock, including swine and poultry, are particularly vulnerable to mycotoxins because of the high percentage of cereals in their diet and because they lack a rumen with a microbiota able to degrade mycotoxins before their intestinal absorption [12]. The gastrointestinal tract (GIT) is the first physiologic barrier against feed contaminants, as well as the first target for toxicants [12]. Deoxynivalenol exerts its toxicity mainly in the GIT of animals which provokes a reduction in the integrity of the intestinal barrier and epithelial cell permeability [13]. Consequently, DON induces impairment of GIT function, inhibiting nutrient absorption and increasing intestinal diseases frequency, resulting in reduced animal growth performance and productivity [14]. In addition, DON contamination results in weak offspring, stillbirth, sow abortion, reduced quality and quantity of the produced eggs in poultry, as well as decreased production performance in ruminants [8,15]. Contamination of animal diets with DON can result in significant economic losses for animal production. In economic animals, it was shown that the impact of DON on growth performance is highly variable due to differences in animal species. Swine is the most sensitive animal with acute exposure to DON and commonly has GIT problems such as diarrhea and melena [16]. Chronic exposure to DON can also cause different effects, such as anorexia, vomiting, and reduced body weight gain (BWG) and feed intake (FI), and negatively impacts the immune and nervous systems [17,18]. For pig, with each mg/kg of DON increase in the feed, the growth depression was estimated at about 8%, while broilers showed no response to DON concentrations below 5 mg/kg [19,20]. The metabolic processes of poultry and ruminants make them highly resistant to DON, which is not easy to carry over in milk and eggs, so trace amounts of DON and DOM-1 will only accumulate in these animal products when high concentrations (>10 mg/kg) of DON are supplied for a long term (>3 weeks) [21].

Table 1. The guidance values of the European Union (EU) Commission, United States Food and Drug Administration (FDA), and China for deoxynivalenol concentrations (mg/kg) in complete feed [22-24].

2.1  Swine

Among all livestock species, swine are most susceptible to the toxicity of DON [25]. Males and young pigs are more sensitive to DON toxicity on growth performances than other categories of swine [26]. A high concentration of DON in the short-term or low doses for an extended period cause symptoms such as abdominal distress, salivation, discomfort, diarrhea, vomiting, inflammation, and gastrointestinal bleeding [12,27]. This mycotoxin also has high emetic and anorexic effects resulting in growth suppression [28,29]. The colloquial name of DON is “vomitoxin” due to its substantial emetic effects observed in pigs [30].

The dietary intake of DON is known to reduce the FI and BWG of pigs [12,31]. Pigs start showing reduced growth performance when fed at least 1 to 3 mg/kg of DON [32]. Specifically for naturally contaminated diets, concentrations of 1 to 2 mg/kg of DON reduce the FI and BWG [19]. Previous meta-analyses pointed out that feed containing an average of 1 mg/kg of DON for three weeks resulted in 7.5% FI and 0.285% BWG reduction in growing swine [26,33]. Over 1 mg/kg of DON causes protein synthesis and FI reduction, decreasing BWG and prolonging the period it takes for boars and gilts to reach 110 kg (selling weight) [33]. If DON concentration is further increased in swine feed, complete feed refusal and vomiting are observed at 12 and 20 mg/kg of DON, respectively [12].

It should be noted that DON reduces vaccinal efficacy in pigs because its toxicity inhibits protein synthesis, leading to decreased corresponding antibody production, such as in the vaccinations for swine fever [34], porcine reproductive and respiratory syndrome virus (PRRSV) [6], and parvo [35]. Deoxynivalenol affects the swine vaccination program at all stages; therefore, farmers need to consider whether it is a DON-contamination problem when they find the vaccine ineffective.

The intestine is an important site of DON absorption as it is exposed to contaminated feed. The intestinal epithelium is a frontier barrier to the external environment, including harmful toxins. Both in vivo and in vitro experiments of swine provide evidence that the chronic ingestion of DON, in low doses, alters the small intestine morphology affecting the mucosal epithelial cells and the villi, which reduces nutrition bioavailability and causes the incidence of diseases, including Salmonella typhimurium and porcine epidemic diarrhea virus (PEDV) [36,37].

Although the toxicity of DON in reproductive performance is not as solid and evident as that of ZEN, it still causes reproductive disorders through fetal malformation and sperm viability reduction in boars [25] and sows [38], respectively. Besides, there is a synergistic interaction between DON and ZEN; for instance, studies on piglets showed that neither BWG nor FI was significantly impacted following exposure to either DON or ZEN [10]. Co-exposed piglets showed significantly lower BWG and ADFI, however, indicating that both toxins were acting synergistically to disrupt intestinal functions and cause systemic inflammation [39]. Furthermore, the presence of both DON and ZEN in swine feed together, even at trace levels, can result in hepatotoxicity and nephrotoxicity [40,41].

Table 2. Deoxynivalenol (DON) toxicities on growth performance in swine.

2.2 Poultry

Chickens are less sensitive compared to swine and ruminants. Previous reports [3,46,47] have noted that although feeding poultry feed containing 1 mg/kg of DON for more than five weeks has no apparent influence on FI, BWG, or feed conversion rate, other effects are still observed in the small intestine villus, e.g., villus height, muscular thickness, and villus surface area. A poultry feed diet containing 5 mg/kg of DON for more than three weeks not only changes the relative weights of digestive tract organs but also reduces FI, BWG, egg production, and egg weight [19,20,47]. Andretta et al. [48] have shown that poultry fed higher than 0.8 mg/kg of DON for more than three weeks would cause a decline in body weight by at least 1%. A linear reduction in FI and body weight gain is seen in broiler chickens fed with a diet contaminated with increasing DON concentration [49]. Ducks and geese have more unsaturated fatty acids (UFAs) in their body fat composition than chickens do, making ducks and geese more vulnerable than chickens to being harmed by lipid peroxidation [50]. Consequently, ducks and geese are more sensitive to DON than chickens are. In Peking ducklings, feed refusal was observed after natural contamination of the diet with only 1.2 mg/kg of DON [51], compared to chicken which needs at least 5 mg/kg of DON for FI reduction [20]. Besides, with similar toxicity levels in swine, DON was also shown to suppress the vaccination response to infectious bronchitis virus (IBV) and Newcastle disease virus (NDV) in poultry [52-54]. It should be noted that DON and zearalenone (ZEN) have a synergistic effect also present in poultry. Egg production was negatively affected in laying hens fed a diet containing sorghum that was contaminated with ZEN and DON at levels of 1.1 and 0.3 mg/kg [55], respectively. If layer feed only contains DON, its concentration levels need to reach at least 10 mg/kg to cause a decrease in egg production [21].

Table 3. Deoxynivalenol (DON) toxicities on growth performance in poultry

2.3 Ruminants

The susceptibility of ruminants to DON is significantly lower than that of swine [59]. The fact that the intact ruminal epithelium is a barrier against DON, most of the ingested DON is de-acetylated and de-epoxied by ruminal protozoans and some bacteria before absorption [60]. Ruminants can tolerate extremely high levels of DON for several weeks without negative effects on their growth and lactation performance. Previous research indicated dietary DON concentrations ranging between 3.1 and 3.5 mg/kg did not cause any significant adverse health effects but transiently increased post-prandial ammonia concentrations [61,62]. Similarly, in longer studies with lactating dairy cows, concentrations of up to 12 mg/kg of DON in concentrate (equivalent to 104 mg/cow/day) or 14.6 mg/kg of DON in concentrate (equivalent to 190 mg/cow/day) did not affect FI [63]. No adverse effect of dietary DON on milk yield and composition was observed in most studies. Only one report indicated that first-lactation cows consuming DON-contaminated diets (6.5 mg/kg) tended to produce 13% less milk production than cows consuming clean concentrate [63]. Besides, some field reports likely substantiated the association of DON with poor-performing ruminants because the synergistic effect due to mycotoxin combinations widely co-exist in the ruminant diet in fields, especially of DON and FUM or DON and ZEN. Beef cattle fed a diet contaminated with 1.7 mg/kg of DON combined with 3.5 mg/kg of FUM presented a decreased rumen pH, lower body weight, and poor crude protein digestibility [64]. On the other hand, dairy cows fed diets contaminated with DON (up to 0.9 mg/kg) and FUM (up to 1.3 mg/kg) presented a decrease in their dry matter and neutral detergent fiber digestibility, which in turn negatively influences milk production [65]. In addition, the combination of 1.96 mg/kg of DON and 0.36 mg/kg of ZEN in the diet of lactating cows induced shortened milk yield and decreased fat content in milk [66].

Table 4. Deoxynivalenol (DON) toxicities on growth performance in ruminants

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