T-2 Toxin Investigation in Cereals and Complete Feed Around the World

1. Introduction

Trichothecenes are one of the most toxic and prevalent mycotoxins produced by Fusarium species [1]. Trichothecenes are divided into four categories (A-D) based on their substitution patterns. T-2 toxin (T-2) and its metabolite (HT-2 toxin, HT-2) are representative members of type-A trichothecenes and are considered to have the most potent acute toxicity among trichothecenes [2]. Once ingested from contaminated feeds, T-2 can threaten the health of animals, leading to T-2 toxicosis. T-2 toxin causes extensive toxic effects in animals, such as feed refusal, growth retardation, reproductive ability reduction, immunosuppression, dermatitis, and organ necrosis (especially in the digestive tract) [1,3]. 

T-2 toxin is produced mainly by Fusarium graminearum and F. poae [4]. It occurs typically in crops such as rice, maize, wheat, barley, oat, and animal feeds and can reach up to hundreds of μg/kg [5]. A warm and humid climate facilitates Fusarium infection in plants [6]. On the other hand, inadequate and improper handling, carrying, and storage conditions of grain with high moisture can be principal causes of T-2 contamination. Although T-2 and deoxynivalenol (DON) belong to the trichothecenes and have common mycotoxigenic strains (F. graminearum), the toxin-producing temperatures of type A and B trichothecenes are different [2]. T-2-toxin is generated between 0 ℃ and 32 ℃, and the optimal temperature for toxin production (6 ℃ to 12 ℃) is comparatively low with DON [7]. T-2 toxin-producing fungi can synthesize mycotoxin under freezing conditions in fields and storage places [8]. A two-year survey in Northern Spain showed a preference for type A trichothecenes (T-2) in the cooler regions and Type B trichothecenes (DON) in the warmer areas [9]. 

Table 1. Regions with the top three highest occurrences of T-2 toxin in the grain and balanced feed in the global investigations (organized data from [10,11]).

2. Asia

2.1 East Asia

The monsoonal climate in East Asia brings hot and rainy summers, as well as mild winters, making T-2 production not much than other Fusarium mycotoxins [12]. T-2 toxin is the least prevalent mycotoxin in the East Asian dataset, with 11% of positive samples and a median concentration of 16 μg/kg in the DSM survey from 2008 to 2017 [11]. T-2 toxin occurrence decreased yearly due to global warming, and by 2022 [10], East Asian raw materials and balanced feeds did not detect T-2.

2.2. South Asia

In the past, mycotoxin control mainly focused on aflatoxin B₁ (AFB₁), fumonisin (FUM), and DON in South Asia due to the warm climate. Between 2008 and 2017 [11], South Asia was the least T-2-contaminated region globally, with an occurrence rate of only 0.9% and a median concentration of 13 μg/kg. However, in 2020 and 2021 [13,14], T-2 occurrence rose sharply to 33% because of extreme global climate change. Surprisingly, in 2022 [10], the T-2 positive rate in South Asian grain and balanced feed reached an extremely high 72%, even surpassing that of 44% in Eastern Europe, which has had the highest T-2 occurrence in the world for an extended period [11]. In South Asian crops and compound feed, current mycotoxin control has seen some differences; thus, feed mills and farmers should focus instead on AFB₁, ochratoxin A (OTA), and T-2 [10].

2.3. Southeast Asia

Throughout the year, Southeast Asia is hot and humid, which is improper for T-2 production, making Southeast Asia becomes one of the areas where T-2 is the top less prevalent mycotoxin in the world [15]. From 2008 to 2017 [11], approximately 2.7% of raw materials and finished feed were contaminated with T-2 at a median concentration of 26 μg/kg. The positive rate of T-2 has not changed much between these years in Southeast Asian cereals and compound feed, and its occurrence was not exceeded 4% since 2020 [10,13,14].

2.4. Central Asia

Similar to Southeast Asia, Central Asia is one of the areas where T-2 is not prevalent. Between 2008 and 2017 [11], only 6.7% of the grain and balanced feed samples were contaminated with T-2 at the median level of 25 μg/kg. A global survey indicated that T-2 was not detected in the raw materials and finished feed samples from Southeast Asia in 2022 [10].

3. Europe

3.1. Eastern Europe

Eastern Europe is classified as having a humid continental climate, which features warm to hot summers and cold winters; therefore, trichothecenes are prevalent in raw materials and compound feed from Eastern Europe [16]. T-2 toxin and deoxynivalenol were detected in 48.2% and 59.9% of the samples. From 2008 to 2017 [11], Eastern Europe recorded the worst T-2 contamination in the world. During this period, T-2 and DON median levels were 21 μg/kg and 153 μg/kg in cereals and balanced feed collected from Eastern Europe. To this day, Eastern Europe still has the highest prevalence of T-2 in the world. T-2 toxin occurrence remained at over 40% in feed ingredients and animal feed from this region for nearly three years  [10,13,14]. Farmers and feed mills importing oats, barley, and wheat from Eastern Europe must regularly analyze the T-2 level in these cereals to ensure animal health.

3.2. Northern Europe

An early study of the United Kingdom oats between 2002 and 2005 observed a higher mean concentration of T-2 and HT-2 than had previously been reported in any cereal class worldwide [17]. From 2008 to 2017 [11], an investigation indicated that trichothecenes were prevalent in feed ingredients and animal feed. T-2 toxin and deoxynivalenol were detected in 74.2% and 30.3% of the samples. Besides this, T-2 exhibited a median concentration of 34 μg/kg, the highest median concentration obtained for any region. It should be noted that Northern Europe demonstrated the third-highest T-2 occurrence rate worldwide in this ten-year survey. The results remained the same in the DSM's global survey for 2020 and 2021 [13,14], with the positive rates hovering at 36% and 44%, respectively. However, in 2022 [10], Northern European crops and balanced feed exhibited lower T-2 occurrence at a 30% positive rate, and this area was relegated to fourth place due to a sharp rise in T-2 contamination in South Asia as well as the Middle East and North Africa (MENA).

3.3. Central Europe

Similar to Eastern Europe, Central Europe is also classified as a humid continental climate, which features warm summers and cold winters, making Central Europe has been one of the regions with the highest T-2 occurrence from the past to the present [18]. Previous research indicated that T-2 was detected at a 90% positive rate with an average concentration of 13 μg/kg from 2003 to 2004 in Slovakia [19]. Between 2008 and 2017 [11], 30.7% of the Central European feed ingredients and animal feed were found to be contaminated with T-2 at a median level of 11 μg/kg. It is worth noting that Central Europe was the second most prevalent T-2 region compared to other regions in the world during this period. In 2020 and 2021 [13,14], feed ingredients and animal feed from this region still remained at about 30% of the positive rate, which is still among the most contaminated in all regions of the world. According to a survey in Poland in 2020 [20], 76% to 88% of local animal feed ingredients were contaminated with T-2 with a maximum concentration of 31 to 51 μg/kg. In 2022 [10], the T-2 occurrence rate slightly decreased to 24% in Central Europe.

3.4. Southern Europe

Compared to other regions of Europe, Southern Europe is an exceptional area where T-2 is not one of the top three prevalent mycotoxins. However, T-2 occurrence was still higher than in other regions of the world, with a 23.1% positive rate in cereals and complete feed at a median value of 96 μg/kg from 2008 to 2017 [11]. Another previous investigation reported that the positivity rates for the sum of T-2 and HT-2 in barley samples ranged from 22% to 53% in Italy from 2011 to 2014 [21]. Since 2020  [10,13,14], T-2 occurrence has decreased year by year to 8% in Southern Europe.

4. America

4.1. North America

In feed ingredients and animal feed from North America, T-2 is not one of the most prevalent mycotoxins. The United States is the main export country of corn, wheat, and soybean for global animal feed, and the maximum level of T-2 in these feed ingredients does not exceed the European Union (EU) regulations of 500 μg/kg [22]. According to DSM's global survey, T-2 prevalence was only 3.9% at the median concentration of 29 μg/kg in this region between 2008 and 2017 [11]. A 2022 investigation [10] indicated only 2% T-2 occurrence in North American grain and balanced feed; among them, no T-2 was detected in American wheat.  

4.2. Central America 

Similar to North America, in Central American raw materials and finished feed samples, T-2 contamination is not a severe problem from the past to the present. According to DSM's global survey, T-2 prevalence was only 4.1% at the median concentration of 3.1 μg/kg in this region from 2008 to 2017 [11]. A 2022 survey [10] by the same company showed 0% T-2 occurrence in Central American grain and balanced feed as well. Ventanco's survey results in 2021 [23] showed similar results that T-2 prevalence was only 1.5% at the average concentration of 21.1 μg/kg in this region.

4.3. South America

Compared to the low occurrence and trace concentration of T-2 in North America and Central America, their positive rate and median values of T-2 were relatively high, with 21.5% and 31 μg/kg for South American feed ingredients and animal feed, respectively, according to a DSM global survey from 2008 to 2017 [11].  In a nearly three-year survey investigated by the same company  [10,13,14], T-2 occurrence remained within a similar range (25 to 28%) in South American feed ingredients and animal feed. Although T-2 prevalence is much higher in South America than in most areas of the world, it is not one of the most serious mycotoxins in this area. The maximum T-2 concentration in corn and soybean of Argentina and Brazil does not exceed the EU regulations [22], and these countries are the main provider of these raw materials for global animal feed. The mycotoxins in most need of controlled in this area are FUM, zearalenone (ZEN), and DON. Ventanco's survey results in 2021  [23] showed slightly different results, stating a T-2 prevalence of only 4.2% at the average concentration of 33.8 μg/kg in this region. Besides, Uruguay exhibited the most severe T-2 contamination, with a positive rate and average level of T-2 were 33.3% and 98 μg/kg, respectively.

Table 2. Occurrence and concentration of T-2 toxin (T-2) in Latin America (modified from [23]) 

5. Africa

5.1. Middle East and North Africa

The MENA region is particularly vulnerable to climate change. It is one of the hottest and driest regions in the world. For the longest time, the top three prevalent mycotoxins sequentially have been FUM (66.8%), DON (47.8%), and ZEN (44.8%) in MENA. From 2008 to 2017 [11], the feed ingredients and animal feed from this region only had an 8.5% T-2 positive rate with a median concentration of 14 μg/kg. T-2 toxin had been the least noteworthy mycotoxin in MENA in the past. However, similar to South Asia, in 2020 and 2021, T-2 occurrence rose sharply from 15% to 17% because of extreme global climate change. Abnormally, in 2022 [10], the T-2 prevalence in MENA’s grain and balanced feed reached 37%, making MENA the region with the third highest positive rate of T-2 contamination in the world after South Asia and Eastern Europe. All corn kernels from MENA were co-contaminated with at least two mycotoxins. Besides, except for AFB₁, the prevalence of other mycotoxins is among the top three most contaminated areas in the world. All Fusarium mycotoxins are highly abundant, with significant increases in DON and T-2 rates. Because the MENA is expected to become the hardest hit area for all mycotoxins in the future due to extreme temperature changes, prolonged droughts, and sporadic torrential rains, livestock farmers and the feed industry who have crops and animal feed from this area need to track the concentrations of all mycotoxins regularly [24].

5.2 Sub-Saharan Africa

Sub-Saharan Africa has a wide variety of climate zones, including a dry winter season and a wet summer season. Because its winter sees extremely low precipitation, these environmental conditions inhibit T-2 production. Between 2008 and 2017 [11], Sub-Saharan African crops and compound feed detected only a 3% T-2 positive rate with a median value of 3 μg/kg. Unlike the sharp increase in the T-2 positive rate in MENA’s cereals and complete feed, the samples from Sub-Saharan Africa still remained low in T-2 prevalence since 2017. In the last three years  [10,13,14], T-2 occurrence has not exceeded 1% in Sub-Saharan African feed ingredients and animal feeds.

5.3 South Africa

South Africa has both sub-tropical and temperate climate conditions, with an annual temperature between 22°C and 35°C; therefore, T-2 is not a prevalent mycotoxin in South Africa for the reason that the optimal temperature of this mycotoxin production is below 15 °C. From 2008 to 2017 [11], South Africa was one of the top three areas with the lowest T-2 contamination worldwide because T-2 occurrence and median concentration were only detected 1.2% and 4.4 μg/kg in feed ingredient and animal feed samples. Similar to Sub-Saharan Africa, South African grain and balanced feed still remained extremely low in T-2 prevalence in recent years; even since 2020, T-2 was not detected in the samples from the latter region. South Africa, East Asia, Central Asia, and Central America were the regions where T-2 was not detected in raw materials and finished feed in 2022 [10].

6. Oceania

Notably, many studies indicated that Oceania was one of the least T-2-contaminated regions in the world [11,25]. In grain and balanced feed from Oceania, T-2 was only 2% positive samples at 16 μg/kg of median concentration from 2008 to 2017 because the climatic conditions in this area are not suitable for T-2 production [11]. In 2022 [10], T-2 occurrence was only 1% in raw materials and compound feed samples.

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