Zearalenone Investigation in Cereals and Complete Feed around the World

1. Global Zearalenone Occurrence

Zearalenone (ZEN) is a mycotoxin produced mainly by fungi belonging to the genus Fusarium in cereal and complete feeds [1]. It is frequently implicated in reproductive disorders of economic animals [2]. Zearalenone contamination levels vary distinctly by region, country, and climate and this mycotoxin is commonly found contaminating cereals in cool temperatures and high humidity [3]. Many surveys revealed a potential interaction between ZEN concentrations in grains and balanced feed and the rainfall that occurred in a given year [4,5]. For instance, due to its severe wet climate conditions, there was an extreme 100% positive rate of ZEN in Serbia's corn in 2014 [6,7]. Overall, global surveys from the early days to the present indicate that ZEN is one of the top three mycotoxins with the highest pollution rate in all regions of the world except South Asia [8]. But even in South Asia, the positive rate of ZEN is as high as more than 20% (or even 40% in 2021 [9]), and ZEN has not become the top three mycotoxins with an increased occurrence rate because aflatoxin (AF, about 80%), fumonisins (FUMs, about 70%), and ochratoxin (OTA, about 67%) have the more severe contaminated condition than ZEN for many years in this area. Based on previous global survey results (from 2008 to 2017) [8], grain and balanced feeds from East Asia, Sub-Saharan Africa, and South America have the highest positive rate of ZEN compared to other regions. However, the areas with the worst ZEN contamination in the cereals and complete feed around the world are changed to China and Taiwan, the Middle East and North Africa, and Central Europe in 2021 [9] because of the rainstorms caused by climate change [10]. Zearalenone contamination is specific to common feed ingredients used in livestock animal feed ingredients, occurring in 45% of all samples of feed ingredients and animal feed as well as 55 μg/kg median concentration among the positive samples, classified by sample type, corn (44%), corn-DDGS (75%), soybean grains (36%), soybean meal (61%), wheat (33%), and barley (20%), respectively [8]. Meanwhile, ZEN is the most prevalent mycotoxin in soybean grains and meals. Besides, some studies have reported the presence of ZEN in pasture grasses and grass silage [8,11]. However, levels are usually lower than reported in maize, cereal silages, and straws, where ZEN has been regularly observed.

Table 1. Regions with the top three highest occurrence of zearalenone in the grain and balanced feed in the global investigations.  

2. Asia

2.1 East Asia

In raw materials and finished feed samples from East Asia, ZEN was the most prevalent (58.2%) and the second highest median concentration (90 μg/kg) than in samples from any other region around the world from 2008 to 2017 [8]. It is worth noting that raw materials and finished feed from East Asia exceeded EU standards more than all other regions of the world because 27.3 and 1.3% of samples exceeded the lowest (100 μg/kg) and highest (2,000 μg/kg) EU guidance value for ZEN, respectively. However, the prevalence of ZEN significantly decreased to 36% in crop and compound feed in the 2021 global survey [9], perhaps because the 2021 survey listed China and Taiwan independently instead of being included in the calculation of East Asia. In 2021, ZEN occurrence in feed ingredients and animal feed was as high as 79% in China and Taiwan, which was the most contaminated region in the world.

2.2 South Asia

South Asia had the lowest positive rate (19.6%) of ZEN compared to other regions, according to the previous ten-year global survey (from 2008 to 2017) [8]. The median concentration of ZEN was 37 μg/kg, and only 2% of feed ingredient and animal feed samples exceeded the lowest levels of EU guidance values. However, in 2018, India's local market survey [12] indicated that 84% of corn, rice, wheat, and oat samples were contaminated with ZEN, with 33% exceeding the EU permissible limit. Besides, by 2021, ZEN was still not the top three most contaminated mycotoxins, but its occurrence had risen sharply to 40% because AF (82%), FUM (74%), and OTA (73%) contaminations were more severe than ZEN in the feed ingredients and compound feed from South Asia [9]. Due to climate change, South Asia should be the hardest hit region of Fusarium mycotoxins such as FUM, deoxynivalenol (DON), and ZEN along with China and Taiwan; hence, the local livestock industry needs to pay more attention to tracking mycotoxin concentrations in cereal and animal feed as well as choosing effective mycotoxin degraded agents.

2.3 Southeast Asia

In a previous global survey (from 2008 to 2017) [8], ZEN was the third most prevalent mycotoxin in raw materials and animal feed in Southeast Asia at a positive rate of 45.9% and a median concentration of 45.9 μg/kg. In 2021 [9], the third highest occurring mycotoxin was still ZEN, but its prevalence had significantly decreased to only 37% compared to previous records.

2.4 Central Asia

According to the available data (from 2008 to 2017) [8], ZEN were the third most frequently occurring mycotoxins in the cereals and animal feeds of Central Asia, the positive rate and median concentration of ZEN were 23% and 1.3 μg/kg, respectively. The median value of ZEN in grains and complete feed in this region was the lowest level among all regions in the world. From 2015 to 2018, a Turkish local investigation [13] showed that ZEN was found in 4% of wheat, 20% of maize, 55% of paddy rice, and 4% of wheat flour, respectively.

3. Europe

3.1 Eastern Europe

From 2008 to 2017, ZEN was the third most prevalent (42.9%) mycotoxin, followed by DON and T-2 toxin (T-2), and its median concentration was 15 μg/kg in grains and compound feeds collected from Northern Europe [8]. It is worth noting that a 2021 global survey indicated that ZEN surpassed trichothecenes and became the mycotoxin with the highest positive rate (48%) in this region. This change should be due to the fact that the positive rates of DON (from 59.9 to 33%) and T-2 (from 48.2 to 40%) in raw materials and animal feed dropped sharply rather than those of ZEN significantly increased in this area during 2021 [9].

3.2 Northern Europe

Northern and Eastern Europe had similar trends in ZEN positive rates over ten years (from 2008 to 2017) [8], ZEN was the third most prevalent (28.9%) mycotoxin, followed by trichothecenes (DON an T-2), and its median concentration of about 39 μg/kg in grains and compound feeds collected from Northern Europe. Different from Eastern Europe, ZEN still maintained a similar prevalence (28%), and the third highest positive rate followed DON and T-2 in raw materials and animal feed of this area in 2021 [9].

3.3 Central Europe

Zearalenone was the second most prevalent mycotoxin in feed ingredients and animal feed in Central Europe at a positive rate of 45% and a median concentration of 40 μg/kg from 2008 to 2017 [8]. In another study [14], 43% of maize kernels from Poland (2011 and 2012) tested positive for ZEN. Due to torrential rain in July and August 2014 (before and after the main silking period of maize), ZEN concentrations (the average concentration reached about 500 μg/kg) were exceptionally high in harvested corn than in other years. By 2021, the ZEN occurrence rate increased to 50% in cereal and animal feed; however, the positive rate was still ranked second after DON [9].

3.4 Southern Europe

Zearalenone was detected in 36.3% with a median concentration of 44 μg/kg in feed ingredients and animal feed of Southern Europe from 2008 to 2017 [8]. In Serbia, ZEN was detected in 12, 37, 100, and 53% of maize in 2012, 2013, 2014, and 2015, respectively [6,7]. As in Central Europe, the extreme 100% positive rate of ZEN in Serbia's corn in 2014 was due to the severe wet climate conditions that year. Another study [15] showed comparable results that the presence of ZEN in Romanian wheat was elevated with higher amounts of rainfall in 2015 as well. In 2021, the positive rate of ZEN was 34%, similar to those from 2008 to 2017 [9].

4. America

4.1 North America

Zearalenone was the third most prevalent mycotoxin (31.7%) in cereal and complete feed samples from North America in the investigation during the period of from 2008 to 2017 [8]. Zearalenone showed relatively high median concentrations of 102 μg/kg compared to other regions and reached up to 16.8% of the samples exceeded the lowest EU guidance value (100 μg/kg); besides, 0.6% of the positive samples did not comply with the highest guidance values (2,000 μg/kg). Zearalenone prevalence (33%) in grains and balanced feed in 2021 [9] not significantly different from the previous investigation.

4.2 Central America 

In cereals and complete feed of the decade (from 2008 to 2017) global mycotoxin survey from Central America [8], ZEN was the third most prevalent mycotoxin detected in 38.2% of samples at a median concentration of 62 μg/kg. In the 2021 global survey, Zearalenone still was the third most prevalent grain and balanced feed from this region [9]; however, the positive rate had dropped to only 25%. Similar to the DSM study, the 2021 Ventanco survey [16] indicated ZEN was the third most prevalent mycotoxin in Central America but detected up to 42.4% of the samples, and the average value is 120 μg/kg which exceeded the lowest guidance value of the EU (100 μg/kg). It should be noted that raw materials and finished from Costa Rica reached up to 91.41% positive rate of ZEN with an average concentration of 161 μg/kg.  

4.3 South America

The previous survey [8] indicated that ZEN was the second most prevalent mycotoxin after FUM in South America, and the positive rate and median value of ZEN were 46.9% and 51 μg/kg for feed ingredients and animal feed from 2008 to 2017, respectively. Besides, South America yielded the third-highest ZEN contamination rates compared to other regions worldwide, and 13.1% of positive samples did not comply with the lowest EU guidance value (100 μg/kg). An analysis of corn meal produced in Brazil found that 78.6% tested positive for ZEN at the concentration range from 15.4 to 72.1 μg/kg in 2016. Another two mycotoxin surveys indicated similar results: the prevalence rate dropped to between 15 and 18% [9,16]. However, the average content increased to between 100 and 177 μg/kg of crop and compound feed from Brazil in 2021. Since Brazil is an essential exporter of corn and soybean meal globally, livestock farmers should pay more attention to the rise of ZEN levels in feed ingredients and animal feed. It is worth noting that, in Ventanco's 2021 survey of mycotoxins in cereals in Latin America, it was shown that, except for Bolivia, the average ZEN value of raw materials and complete feed from other countries exceeded the lowest guidance value of the EU. In terms of positive rate and mean level, the most contaminated countries were Peru (37.1% with 202 μg/kg) and Uruguay (28.57% with 215 μg/kg), respectively.

Table 1 Occurrence and concentration of zearalenone (ZEN) in Latin America (modified from Ventanco 2021 Mycotoxin Survey) 

5. Africa

5.1 Middle East and North Africa

In raw materials and balanced feed from the Middle East and North Africa, ZEN (44.8%) was the third most frequently detected mycotoxin, followed by FUM and DON with a median concentration of 31 μg/kg in previous research from 2008 to 2017 [8]. However, ZEN-positive rates in feed ingredients and animal feed significantly increased to 58% and surpassed DON, which became the second most prevalent mycotoxin in 2021. Compared to previous years (from 2008 to 2017) mycotoxin contaminated issues were general have risen significantly in 2021 [9] ; not only ZEN prevalence increased significantly, but also other Fusarium mycotoxins FUM (from 66.8 to 84%), DON (from 44.8 to 58%), and T-2 (from 8.5 to 15%) raised substantially. This trendy means that the Fusarium spp. contaminated condition in this area is becoming more and more severe due to climate change inducing rapid changes in temperatures and rainfalls in the Middle East and North Africa, the livestock farmers who have crop sources from this area need to pay more attention.

5.2 Sub-Saharan Africa

A decade survey (from 2008 to 2017) indicated ZEN was the third most prevalent mycotoxin detected in 52.2% of positive rate with 38 μg/kg of median concentration in grain and balanced feed from Sub-Saharan Africa, where was the second most severely contaminated region in the world [8]. Compared to previous research, the 2021 study [9] presented the occurrence dramatically dropped to only 27%. High contamination with ZEN in feed ingredients is usually associated with increased rainfall during cereal silking; therefore, decreased positive rate may be because one-third of the world's droughts occur in sub-Saharan Africa, and Ethiopia and Kenya endured one of the worst in at least four decades in 2021 [17].

5.3 South Africa

Fusarium mycotoxins DON, FUM and ZEN were the top three highest occurring in South African crop and compound feed of previous survey (from 2008 to 2017) and yielded positive rates of 63.2, 62.6, and 41.6%, respectively [8]. However, DON prevalence in feed ingredients and animal feeds reached 84%; on the contrary, FUM prevalence decreased to 48%, and ZEN prevalence maintained with 46% in 2021 [9]. 

6. Oceania

From then until now, many surveys have shown that cereals and complete feed in Oceania have had milder mycotoxin-contaminated issues than in other continents [8,18]. Zearalenone was consistently the second or third highest occurring mycotoxin on this continent. Notably, ZEN was detected in a comparatively low fraction of raw materials and finished feed samples (21.5%) but reached the highest median concentration of 105 μg/kg compared to other regions around the world. Accordingly, 11.1% of samples did not comply with the lowest EU guidance value for ZEN in feed, and 0.7% of samples also exceeded the lowest EU guidance. In the 2021 survey [9], feed ingredients and animal feed from Oceania had the similar lowest positive rate of ZEN (16%) compared to other regions. 

7. Co-occurrence

Zearalenone co-occurs with other Fusarium mycotoxins, mainly DON [19]. Because both ZEN and DON are produced by F. graminearum or F. culmorum [20], the ideal moisture and temperature for Fusaria growth are the same, only mycotoxin production temperature is slightly different; cooler environment induce ZEN production [3], on the other hand, temperate regions are better suited for DON production [21]. Rainfall and mild temperatures during the flowering and maturation periods were shown to favor infestation of wheat and maize with F. graminearum and F. culmorum as well as DON and ZEN contamination [8]. A global decade-long survey [8] showed that the co-occurrences of ZEN and DON were detected in 48% of finished feed, 39% in corn, and 28% in wheat, respectively. It should be noted that ZEN and DON were also the most frequently observed mycotoxin combination in wheat.

8. References

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