Ochratoxin A Investigation in Cereals and Complete Feed around the World

1. Global Ochratoxin A Occurrence

Ochratoxins are secondary metabolites of fungi produced by the Aspergillus and Penicillium genera [1]. Ochratoxin A (OTA) is the most common and toxic ochratoxins [2]. Ochratoxin A is produced by A. ochraceus and P. verrucosumand is found in several agricultural crops such as wheat and corn [3]. It is especially in the countries with hot and wet climatic conditions (in particular, the Middle East and North Africa, Sub-Saharan Africa, and South Asia) that A. ochraceus is endemic [4]. Thus, corn and wheat, the basic feed ingredients of the populations of these countries, are often contaminated by OTA. However, countries of Eastern Europe, characterized by low temperatures, are especially contaminated by OTA where its production is due to a different species belonging to P. verrucosum [5], which can explain the fact that these countries are more contaminated with OTA-producing Penicillium species than Aspergillus ones. A global ten-year survey with over 700,000 cereal and animal feed samples collected from 100 countries detected that OTA occurred in 15% of the samples [6]. The wide occurrence of OTA and its high thermal stability make the eradication of OTA from the food chain very difficult [7]. The mycotoxin most commonly detected together with OTA is fumonisins (FUM) in feed ingredients and animal feed samples [6] because a majority of A. niger can produce FUM and OTA simultaneously which is confirmed by recent research [8]. Co-occurrence of OTA and FUM was detected in 17% and 4% of the finished feed and maize samples, respectively [6].

Table 1. Regions with the top three highest occurrences of ochratoxin A in the grain and balanced feed in the global investigations.  (Reorganizing data form [6,9])

2. Asia

2.1 East Asia

Ochratoxin A is not one of the most prevalent mycotoxins in East Asian feed ingredients and animal feed. A ten-year survey (between 2008 and 2017) [6] indicated that the prevalence and median value of OTA were 14.1% and 2.9 μg/kg in East Asian cereal and complete feed samples, respectively. In 2022 [9], East Asian grain and balanced feed had significantly lower OTA prevalence (2%) compared to the previous ten-year survey which was researched by the same company. A recent report showed that OTA occurrence remained significantly high (about 30%) in the raw material and finished feed samples from China and Taiwan between 2020 and 2022 [9-11]. Although OTA prevalence in China and Taiwan was the second highest around the world compared to other regions, it was not one of the most serious common mycotoxins in this area. Because Fusarium mycotoxin contamination in China and Taiwan is much more serious than OTA, this means China and Taiwan have been the hardest-hit areas for mycotoxin contamination in recent years  [9-11]. 

2.2 South Asia 

South Asia is the most severely contaminated area of OTA in the world for the long term. From 2008 to 2017 [6], OTA was detected in 60.4% of the samples with a median value of 4.6 μg/kg, the highest percentage of positive samples detected in any dataset. However, nearly all samples (99.6%) complied with the most stringent European Union (EU) guidance value for OTA in feed (50 μg/kg) [12]. In contrast, Pakistan research in 2013 indicated that 37.5% of silage samples reached a maximum concentration of 169 μg/kg OTA, which is higher than the lowest guidance levels set by the European Commission proposed for OTA [12,13]. Until recent years, OTA prevalence in South Asia remained relatively high compared to other regions in the world, at 74%, 73%, and 77% in 2020 [10], 2021 [11], and 2022 [9], respectively. Besides, a survey pointed out that barley, oats, wheat, and maize grown in Indian countries have been particularly susceptible to OTA contamination in recent years [14]. South Asia is one of the few regions where OTA prevalence has continued to increase for years  [9-11].

2.3 Southeast Asia 

In the DSM global survey (from 2008 to 2017) [6], OTA was not one of the most prevalent mycotoxins in animal feed in Southeast Asia at a positive rate of 15.2% and a median concentration of 3 μg/kg. However, a more recent report indicated that maize grains collected from farmers and traditional markets in the Kupang region of Indonesia were found to contain OTA at 20.38 and 20.39 μg/kg, respectively [15,16]. Ochratoxin A remained a relatively low occurrence (10%) compared to Aflatoxin B₁ (AFB₁) and other Fusarium mycotoxins last year [9]. 

2.4 Central Asia

Between 2008 and 2017 [6], OTA was the fourth most frequently occurring mycotoxin in the cereal and animal feed of Central Asia, with a positive rate and median concentration of 13.3% and 22 μg/kg, respectively. Besides, the median value of OTA in grains and complete feed in this region was the highest level among all regions in the world. However, the newest survey mentioned that OTA occurrence significantly dropped to 0% in Central Asia in 2022 [9].

3. Europe

3.1 Eastern Europe 

Ochratoxin A has been endemic in Eastern Europe. A survey between 1991 and 1998 [17] pointed out that the average concentration of OTA of Hungarian soybean, maize, and rye was 350, 320, and 250 μg/kg, respectively. Average contamination in other feeds, such as wheat, barley, oat, triticale, and sunflower, was lower than 200 μg/kg. Furthermore, another ten-year survey indicated that OTA showed a relatively high prevalence of 36.4% with a median concentration of 3.6 μg/kg in Eastern European feed ingredients and animal feed from 2008 to 2017 [6]. At that time, Eastern Europe recorded the second highest OTA contamination in the world. For nearly three years [9-11], OTA contamination decreased year by year in Eastern European crop and compound feed samples, presenting an occurrence rate of only 19% until 2022. Due to these reasons, OTA prevalence in Eastern Europe is still higher than its occurrence in most regions of the world, but OTA has become one of the less threatening mycotoxins in this region. In 2022 [9], wheat from Russia was detected with 6% OTA occurrence at a median value and a maximum value of 22 and 119 μg/kg, respectively. It should be noted that the maximum value has exceeded the lowest guidance value for OTA in feed in the EU. 

3.2 Northern Europe 

Due to climatic factors, the OTA contamination (8.1% positive rate) in Northern Europe was relatively less than in other European regions. Northern Europe had the lowest median concentration (1.9 μg/kg) in the world from 2008 to 2017 [6]. In 2022 [9], Northern European crops and balanced feed significantly dropped OTA occurrence to only a 2% positive rate. However, some Nordic countries are exceptions. It is found that barley, oats, wheat, and maize grown in Scandinavian and Balkan countries are particularly susceptible to OTA contamination [18,19]. 

3.3 Central Europe 

In Germany, a study analyzed samples of grains between 1991 and 1993, stored for different durations, and reported that about 54% of the samples had OTA, and in 2% the levels of OTA were above 3 μg/kg [20]. Between 2008 and 2017 [6], OTA was detected at an 11.9% positive rate at a median value of 2.8 μg/kg in Central European cereal and complete feed samples. In 2022 [9], Central European samples were not detected with OTA.

3.4 Southern Europe

Southern Europe has been one area with have a high OTA prevalence. A study carried out in Spain found extremely high levels of OTA in a reduced number of samples (1%) of maize (up to 225 μg/kg) and barley (up to 90 μg/kg) in 2007 [21]. A global ten-year survey (between 2008 and 2017) [6] indicated that Southern European crops and animal feed samples were detected at a 21.2% positive rate at a median concentration of 2.6 μg/kg, this high occurrence made Southern Europe become the fourth-highest prevalent region of OTA contamination. In recent years  [9-11], OTA prevalence remained at 15-20% in this region’s samples. However, OTA occurrence significantly dropped to only 5% in Southern European crops and compound feed in 2022 [9].

4. Americas

4.1 North America 

In feed ingredients and animal feed from North America, OTA is not a prevalent mycotoxin from then till now. According to a previous survey, OTA positive rate was only 4.3% at the median value of 2.4 μg/kg in this region from 2008 to 2017 [6]. The latest investigation indicated that OTA prevalence (2%) remained a low trend in North American cereal and compound feed samples [9]. The United States is the main export country of corn, wheat, and soybean for global animal feed ingredients, and the maximum level of OTA in these raw materials did not exceed the EU regulations of 50 μg/kg in 2022 [9]. However, it should be noted that 50% of the United States corn samples in 2022 had OTA contaminated phenomenon [9], its occurrence in the United States even was higher than its occurrence in Russia's wheat (6%), on the contrary, its maximum level in the United States (16 μg/kg) was far below than its level in Russia (119 μg/kg).

5.2 Central America 

Notably, a ten-year (from 2008 to 2017) study [6] indicated that Central America was the least OTA-contaminated region in the world. In grain and balanced feed from Central America, OTA was only 3.8% positive samples at 2.5 μg/kg of median concentration because the climatic conditions in this area are not suitable for OTA production. In 2021 [11] and 2022 [9], OTA occurrence remained at 5% in raw materials and compound feed samples in DSM’s global survey. On the other hand, Ventanco's survey in 2021 [22] presented different results that OTA occurrence reached up to 25.4% at the average concentration of 3.3 μg/kg in Central America. However, OTA-contaminated samples were mainly collected from Mexico (38.3%), and feed ingredient and animal feed samples from Costa Rica were not detected in OTA.

5.3 South America 

An Argentina report indicated that OTA was present at a mean level of about 25 μg/kg in 38% of the poultry feed samples and in 13% of the pig feed samples with similar levels of toxins from 1999 to 2000 [23]. Previous Brazil research [24,25] from 2005 to 2006 described that corn (44%), animal feed (31%), and distiller’s dried grains with solubles (DDGS, 13%) were contaminated with an average OTA concentration of about 133, 78, and 84 μg/kg, respectively. There was a notable phenomenon in DSM’s global report, similar to North and Central America but slightly different, of OTA being detected in trace amounts (4.9%) in South American cereal and animal feed samples, but its median concentration reached 17 μg/kg, a level which was the second highest in the world from 2008 to 2017 [6]. In nearly three-year surveys conducted by the same company [9-11], OTA occurrence increased year by year and rose to 19% in 2022 in South American feed ingredients and animal feed samples. Although OTA prevalence in South America was relatively high compared to most areas of the world, it was the least serious common mycotoxin in this area. Besides, OTA was not detected in Brazilian corn and soybean samples in 2022 [9]. Vetanco’s survey in 2021 [22] mentioned a different result, stating that OTA prevalence was only 5.9% of the positive rate at 14.5 μg/kg of average concentration in South American cereals and complete feed. It is worth noting that the same investigation indicated that the average value of OTA of raw materials and complete feed from Ecuador (157 μg/kg) exceeded the lowest guidance value of the EU and OTA occurrence reached an extreme high of 61.8%. 

Table 2. Occurrence and concentration of ochratoxin A (OTA) in Latin America (modified from [22]) 

5 Africa

5.1 Middle East and North Africa 

The high temperature and humidity in the Middle East and North Africa generally favor to the proliferation of Aspergillus and Penicillium. Hence, the Middle East and North Africa have been the hardest hit region of OTA and AFB₁contaminated issues. A global ten-year survey (between 2008 and 2017) [6] presented that Middle East and North African crops and animal feed samples were detected 20.3% positive rate at a median concentration of 2.1 μg/kg, the high occurrence indicated the Middle East and North Africa was the fifth highest prevalent region of OTA contamination. Another research pointed out that feed ingredients such as maize, peanut cake, wheat, and other cereals tested in Nigeria were reported to contain OTA at 10 μg/kg in 2018 [26]. Ochratoxin A positive rate in the Middle East and North African raw materials and finished feed remained at 22% and 23% positive rates in 2021 [11] and 2022 [9], respectively. As OTA contamination decreased in Eastern Europe and Sub-Saharan Africa, the Middle East and North Africa grew to become the third-highest OTA-contaminated area in the world last year [9].

5.2 Sub-Saharan Africa 

Similar to the Middle East and North Africa, Sub-Saharan Africa has been the hardest-hit region of OTA contamination issues. From 2008 to 2017 [6], an investigation indicated that OTA was prevalent in feed ingredients and animal feed samples from Sub-Saharan Africa. Ochratoxin A was detected in 31% of the samples with a median value of 7.2 μg/kg. The high OTA-positive rate in local cereals and complete feed made Sub-Saharan Africa the third-highest contaminated region in the world during this period.  However, OTA occurrence in Sub-Saharan African crops and balanced feed significantly decreased to only 5% and 16% positive rates in 2021 [11] and 2022 [9], respectively. Sub-Saharan Africa is no longer an area where OTA is prevalent compared to the past.

5.3 South Africa 

Compared to high OTA occurrence in the Middle East and North Africa as well as Sub-Saharan Africa, much research pointed out that the incidence of contamination by OTA is considered to be low in South Africa. From 2008 to 2017 [6], OTA was detected at only a 5.6% positive rate at a median level of 2.2 μg/kg in South African feed ingredients and animal feed samples. Ochratoxin A prevalence did not exceed 5% in South African cereal and complete feed samples for nearly three years [9-11]. 

7. Oceania 

It is worth noting that many studies indicated that most mycotoxin-contaminated issues in Oceania have been more moderate over the years compared to other regions in the world because of the climatic conditions. Similar to most mycotoxins, Oceania is one of the least OTA-contaminated regions in the world. In raw material and finished feed samples from Oceania, OTA was only 7.5% positive samples at 3.6 μg/kg of median concentration from 2008 to 2017 [6]. In 2022 [9], the occurrence of OTA was only 1% in crop and compound feed samples.

8. References

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