Aflatoxin Occurrence in Global Cereal and Animal Feed

1. Global Aflatoxin Occurrence

Aflatoxin B₁ (AFB₁) is the most prevalent and toxic among more than 18 types of aflatoxins presently identified [1]. The prevailing weather is an essential determinant of aflatoxin contamination, with dry and hot weather, and exceptionally prolonged droughts, predisposing crops to aflatoxin contamination [2]. Various research [1,3,4] reported that the most prevalent regions of aflatoxins in the world are South Asia, Sub-Saharan Africa, and Southeast Asia. A global mycotoxin survey for 10 years (from 2008 to 2017) [3] indicated that the prevalence of AFB₁ was 82.2%, 76%, and 57.4% in South Asian, Sub-Saharan African, and Southeast Asian samples, respectively. Besides, Sub-Saharan samples detected the highest median concentration (23 μg/kg) of AFB₁-positive samples globally. A worldwide investigation in 2018 [5] indicated that approximately 37% of corn was contaminated with aflatoxins in Asia, 19% in South and Central America, 18% in Europe, and 9% in North America. The average aflatoxin concentration in positive samples was the highest in Asia (42 μg/kg), followed by North America (36 μg/kg) and South and Central America (11 μg/kg). Asia and North America had aflatoxin concentrations above the Food and Drug Administration (FDA) maximal level for positive feed samples (20 μg/kg). A global survey in 2019 reported that samples from the Middle East and North Africa (MENA) had the highest mean concentration of 42 μg/kg, while corn samples from Asia, MENA, as well as South and Central America, had aflatoxin contamination rates of 31%, 37%, and 21%, respectively. Notably, corn samples from Asia had a 31% occurrence, with a mean concentration among positive samples of 43 μg/kg. The most commonly detected mycotoxin with aflatoxins is fumonisins (FUM) in feed ingredient and animal feed samples [3,6]. Co-occurrence of AFB₁ and FUM was detected in 22% and 24% of the finished feed and maize samples, respectively [3].

Table 1. Regions with the top three highest occurrences of aflatoxins in the grain and balanced feed in the global investigations. (Reorganizing data form [3,7])

2. Asia

2.1. East Asia

Aflatoxin B₁ was detected in a lower fraction of East Asian samples (17.1%) than in South Asia and Southeast Asia but at a relatively high median concentration of 10 μg/kg compared to other regions worldwide from 2008 to 2017 [3]. Accordingly, 10.2% and 6.6% of the samples exceeded the lowest (5 μg/kg) and highest (20 μg/kg) European Union (EU) regulatory limit for AFB₁ in feed, respectively [8]. In maize from East Asia, the mean concentration of AFB₁ was higher in 2017 than in previous years [3]. This may be due to a higher temperature during the approximate silking period of maize (July) in the core Chinese maize growing areas in 2017 compared to 2013 to 2016 [3]. Recent reports showed that AFB₁ occurrence remained at a high level (16% to 19%) in the raw material and finished feed samples from China and Taiwan between 2020 and 2022 [7,9,10]. The same reports indicated that other East Asian countries had significantly lower AFB₁ prevalence (2%). This phenomenon meant that aflatoxin contamination in East Asia may mainly come from China and Taiwan as indicated in the previous report.

2.2. South Asia

Similar to ochratoxin A (OTA), South Asia is the most severely contaminated area of aflatoxins in the world for the long term. A 2-year survey (from 2005 to 2007) [11] on different poultry feed samples in Pakistan detected aflatoxins (10.8 μg/kg to 39.2 μg/kg) in layer and broiler starter feed. Among them, 40% of samples contained aflatoxins above 20 μg/kg (maximum tolerable levels for poultry). From 2008 to 2017 [3], AFB₁ was detected in 82.2% of samples from South Asia, which was the highest prevalence of positive samples found in any region. Furthermore, AFB₁ reached a high median concentration of 20 μg/kg. Accordingly, high fractions of samples, i.e., 61.1% and 41.1%, did not comply with the lowest and highest EU regulatory limits for AFB₁ in feed, respectively. Until recent years [7,9,10], AFB₁ prevalence in South Asian cereal and animal feed remained the highest globally, at 77%, 82%, and 85% in 2020, 2021, and 2022, respectively [7,9,10].

2.3. Southeast Asia

Aflatoxin B₁ was prevalent in feed ingredients and complete feed samples from Southeast Asia. A global investigation from 2008 to 2017 [3] indicated that 57.4% of the samples were at a median concentration of 10 μg/kg, and that 37.9% and 20.9% of the samples did not comply with the lowest and highest EU regulatory limits for AFB₁, respectively. Aflatoxin B₁ concentrations in Southeast Asian maize were exceptionally high between 2008 and 2011 and in 2017. These higher AFB₁ levels may reflect the relatively high rainfall these years leading up to harvest. About 60% of Southeast Asian samples were contaminated with aflatoxins with an average concentration of 43 μg/kg in another survey between 2009 and 2010 [12]. Until 2022 [7], Southeast Asian cereal and complete feed were still detected at a relatively high AFB₁ positive rate of 57%. Although AFB₁ prevalence in Southeast Asia is relatively higher than in other regions worldwide, it was not the most prevalent mycotoxin in this area because FUM contamination is much more severe than that of AFB₁.

2.4. Central Asia

Between 2008 and 2017 [3], AFB₁ was the less prevalent mycotoxin in the cereal and animal feed of Central Asia, with a positive rate and median concentration of 7.1% and 1.4 μg/kg, respectively. Besides, the median value of AFB₁ in grains and complete feed in this region was the lowest level among all regions in the world. The global survey mentioned that Central Asian grain and balanced feed samples did not detect AFB₁ in 2022 [7].

3. Europe

3.1. Eastern Europe

Between 2008 and 2017 [3], Eastern European crop and complete feed samples had a 17% positive rate at a median concentration of 3.4 μg/kg for AFB₁.  In 2013, high concentrations of aflatoxin M₁ (AFB₁ metabolite) were found in the raw milk of a few dairy farms in the Netherlands [13]. Although these cases were found in Western Europe, after tracing the source, they found that these high concentrations were caused by AFB₁-contaminated maize from Eastern Europe that was processed into compound feed, which was fed to dairy cows. In the current climatic conditions, Eastern European countries in which maize cultivation is common, i.e., Russia and Romania, show a low probability of aflatoxin occurrence [14]. In the past three years (from 2020 to 2022) [7,9,10], AFB₁ occurrence was maintained at only 3%, which was much lower than that of other common mycotoxins in the same region.

3.2. Northern Europe

Due to climatic conditions, the AFB₁ occurrence (5.9 % positive rate) in Northern Europe was the lowest globally from 2008 to 2017 [3]. The median value of Northern European crop and compound feed samples was 3.1 μg/kg during this period. In 2022 [7], AFB₁ occurrence in Northern European grain and balanced feed significantly dropped to only a 2% positive rate. Northern European countries are generally in the safe zone regarding aflatoxin contamination. Occasionally there are a few samples or on-site cases with high concentrations of aflatoxins, but the source of raw materials is traced to other regions in Europe. Local grains have almost no aflatoxin contamination issues.

3.3. Central Europe

The samples from Central Europe showed a high percentage of around 30% positive samples of aflatoxin contamination from 2004 to 2011 [15]. However, another report indicated that AFB₁ occurrence significantly dropped to 12.7% at a low median concentration of 1.6 g/kg between 2008 and 2017 [3]. In the recent three years (between 2020 and 2022) [7,9,10], AFB₁ positive rate (8% to 14%) had no apparent changes in Central European samples compared to the previous report from 2008 to 2017. However, according to the forecasts for recent research [16], extreme drought situations will become more prevalent on the northern shores of the western Mediterranean, in countries such as Croatia, which can increase the frequency of Aspergillus spp. and aflatoxin contamination.

3.4. Southern Europe

Aflatoxin B₁ contamination of maize grown in Southern European countries has been reported in recent years [13,17]. Hot and dry conditions necessary for A. flavus infestation of maize mainly prevail in Europe below 45 North latitude [14]. According to the global survey from 2008 to 2017 [3], The prevalence of AFB₁ (28.9%) was higher in samples from Southern Europe than in samples from the other European regions. The median concentration of Southern European samples was 2.1 μg/kg, and the concentration of 2.1% of the positive samples exceeded the highest EU maximum level for AFB₁ in feed. In 2022 [7], AFB₁ occurrence significantly decreased to 16%. However, AFB₁ contamination of crops in Southern Europe should continue to be monitored closely, as occasionally elevated levels occur.

4. America

4.1. North America

Aflatoxin B₁ is not commonly found in North American grains, but occasionally these samples are detected in extremely high concentrations. According to a previous survey, AFB₁ positive rate was 10.5% at the median value of 8.7 μg/kg in this region from 2008 to 2017 [3]. However, the record-breaking heat and drought in 2012 resulted in atypically high aflatoxin concentrations of the feeds from the southern Corn Belt States in the US. Especially in Texas, 60% of corn was contaminated with aflatoxin levels greater than 20 μg/kg in the same year [18]. The latest investigation [7] indicated that AFB₁ prevalence remained a low trend (only 5%) in North American cereal and compound feed samples. However, it should be noted that these samples detected an extremely high average level (70 μg/kg) of AFB₁, which exceeded the EU regulations of 20 μg/kg in 2022. In contrast, American wheat did not detect AFB₁ occurrence.

5.2. Central America

In grain and balanced feed from Central America, AFB₁ was only 8.6% positive samples at 3.9 μg/kg of median concentration because the climatic conditions in this area are not suitable for AFB₁ production [3]. In 2021 and 2022 [7,10], AFB₁ occurrence remained at low fractions of 8% and 12% in raw materials and compound feed samples in DSM’s global survey. Unlike the results of the DSM’s survey, Ventanco's survey in 2021 [19] presented different results that aflatoxin occurrence reached up to 69.7% at the average concentration of 4.33 μg/kg in Central America. The occurrence and average concentration of aflatoxins were 65.5% and 71.9%, as well as 3 μg/kg and 5 μg/kg in grain and balanced feed samples from Costa Rica and Mexico.

5.3. South America

It should be noted, compared to North and Central America, AFB₁ was detected in high prevalence (32.5%) in South American cereal and animal feed samples, but the median concentration of only 3.2 μg/kg, which was lower than that of North America (8.7 μg/kg) from 2008 to 2017 [3].  In nearly three-year surveys conducted by the same company, AFB₁ occurrence remained at 25% in 2022 in South American feed ingredients and animal feed samples. Argentine soybean and corn had a relatively high contaminated occurrence (73% and 33%), but the average concentration presented a moderate level (both 3 μg/kg) in 2022 [7]. Although AFB₁ prevalence in South America was relatively high (the fourth highest occurrence in the world) compared to most areas of the world, it was the second mildest common mycotoxin (only more prevalent than OTA) in this area. Vetanco’s survey in 2021 [19] mentioned a different result, stating that aflatoxin prevalence reached to 68% of the positive rate at 6.33 μg/kg of average concentration in South American cereals and complete feed. Notably, the same investigation indicated that the average value of aflatoxins of raw materials and complete feed from Uruguay, Ecuador, and Argentina reached up to 92.4%, 87.3%, and 74.7%, respectively. The average value of samples from all tested South American countries exceeded the lowest limit levels for aflatoxins in the EU.

Table 2. Occurrence and concentration of aflatoxins in Latin America (modified from [19]) 

5. Africa

5.1. Middle East and North Africa

The high temperature and humidity in MENA generally lead to Aspergillus proliferation. Therefore, MENA has had AFB₁-contaminated issues in local grain, feed ingredients, and animal feed. A global 10-year survey (between 2008 and 2017) [3] presented that the crop and animal feed samples of MENA detected a 22.2% positive rate at a median concentration of 2.4 μg/kg, the high occurrence indicated MENA was the sixth-highest prevalent region of AFB₁ contamination. A Sudan local survey in 2009 [20] indicated that a total of 64.3% of animal feed (average value of 130.6 μg/kg) and 87.5% of manufactured animal rations (54.4 μg/kg to 579.9 μg/kg) were contaminated with aflatoxins. An investigation observed that AFB₁ concentrations in the finished feed of Mauritius were significantly higher in 2011 than that in previous years [7]. Aflatoxin B₁ positive rates in raw materials and finished feed from MENA significantly increased to 38%, making MENA the fourth-highest AFB₁-contaminated area in the world in 2022 [7].

5.2. Sub-Saharan Africa

Sub-Saharan Africa has been one of the hardest hit regions by aflatoxin contamination. In 2004, there was a massive outbreak in Kenya, among the most significant outbreaks of aflatoxicosis in history, causing at least 125 deaths and 317 cases for humans [21]. Aflatoxin B₁ was detected in 76% of samples from Sub-Saharan Africa at a median concentration of 23 μg/kg, which is the highest median concentration detected in any region from 2008 to 2017 [3]. Consequently, 59.1% and 38.5% of these samples exceeded the lowest and the highest EU regulatory limit for AFB₁ in feed, respectively. Aflatoxin B₁ occurrence remained relatively high in the grain and balanced feed samples from Sub-Saharan Africa in 2021 (38%) and 2022 (45%) [7,10].

5.3. South Africa

South Africa is a leading production and exporter region of African maize [22]. Fortunately, compared to high AFB₁ occurrence in Sub-Saharan Africa, various studies [23-25] pointed out that the incidence of contamination by AFB₁ is considered low in South African feed ingredients and animal feed. From 2008 to 2017 [3], AFB₁ was detected at only a 9% positive rate at a median level of 2.2 μg/kg in South African cereal and complete feed samples. Aflatoxin B₁ prevalence remained a low trend, with only 2%, 4%, and 4% in South African grain and balanced feed samples in 2020, 2021, and 2022, respectively [7,9,10].

6. Oceania

Compared to other continents, Oceania has a moderate level of aflatoxin contamination worldwide. In raw material and finished feed samples from Oceania, AFB₁ was 11.3% of positive samples at 2 μg/kg of median concentration from 2008 to 2017 [3]. Another investigation between 2009 and 2010 indicated similar results, pointing out that 10% of samples were contaminated with an average concentration of 1 μg/kg in Australia and New Zealand [12]. In 2022, AFB₁ contamination was only 7% in crop and compound feed samples [7].

7. References

1. Benkerroum, N. Aflatoxins: Producing-Molds, Structure, Health Issues and Incidence in Southeast Asian and Sub-Saharan African Countries. Int J Environ Res Public Health 2020, 17, doi:10.3390/ijerph17041215.
2. Jiang, Y.; Ogunade, I.M.; Vyas, D.; Adesogan, A.T. Aflatoxin in Dairy Cows: Toxicity, Occurrence in Feedstuffs and Milk and Dietary Mitigation Strategies. Toxins (Basel) 2021, 13, doi:10.3390/toxins13040283.
3. Gruber-Dorninger, C.; Jenkins, T.; Schatzmayr, G. Global Mycotoxin Occurrence in Feed: A Ten-Year Survey. Toxins (Basel) 2019, 11, doi:10.3390/toxins11070375.
4. Siri-Anusornsak, W.; Kolawole, O.; Mahakarnchanakul, W.; Greer, B.; Petchkongkaew, A.; Meneely, J.; Elliott, C.; Vangnai, K. The Occurrence and Co-Occurrence of Regulated, Emerging, and Masked Mycotoxins in Rice Bran and Maize from Southeast Asia. Toxins (Basel) 2022, 14, doi:10.3390/toxins14080567.
5. DSM. Biomin Mycotoxin Survey 2018. 2018.
6. Dersjant-Li, Y.; Verstegen, M.W.; Gerrits, W.J. The impact of low concentrations of aflatoxin, deoxynivalenol or fumonisin in diets on growing pigs and poultry. Nutr Res Rev 2003, 16, 223-239, doi:10.1079/NRR200368.
7. DSM. DSM World Mycotoxin Survey 2022; 2023.
8. Battilani, P.; Toscano, P.; Van der Fels-Klerx, H.J.; Moretti, A.; Camardo Leggieri, M.; Brera, C.; Rortais, A.; Goumperis, T.; Robinson, T. Aflatoxin B1 contamination in maize in Europe increases due to climate change.
9. DSM. DSM World Mycotoxin Survey 2020; 2021.
10. DSM. DSM World Mycotoxin Survey 2021; 2022 
11. M. Shareef, A. Molds and mycotoxins in poultry feeds from farms of potential mycotoxicosis. Iraqi Journal of Veterinary Sciences 2010, 24, 17-25, doi:10.33899/ijvs.2010.5581.
12. Rodrigues, I.; Naehrer, K. Prevalence of mycotoxins in feedstuffs and feed surveyed worldwide in 2009 and 2010. Phytopathologia Mediterranea 2012, 51, 175-192, doi:10.14601/Phytopathol_Mediterr-9693.
13. Focker, M.; van der Fels-Klerx, H.J.; Oude Lansink, A. Financial losses for Dutch stakeholders during the 2013 aflatoxin incident in Maize in Europe. Mycotoxin Res 2021, 37, 193-204, doi:10.1007/s12550-021-00429-9.
14. Battilani, P.; Toscano, P.; Van der Fels-Klerx, H.J.; Moretti, A.; Camardo Leggieri, M.; Brera, C.; Rortais, A.; Goumperis, T.; Robinson, T. Aflatoxin B1 contamination in maize in Europe increases due to climate change. Sci Rep 2016, 6, 24328, doi:10.1038/srep24328.
15. Streit, E.; Naehrer, K.; Rodrigues, I.; Schatzmayr, G. Mycotoxin occurrence in feed and feed raw materials worldwide: long-term analysis with special focus on Europe and Asia. J Sci Food Agric 2013, 93, 2892-2899, doi:10.1002/jsfa.6225.
16. Rouaa, D.; Jean Claude, A.; André El, K. Aflatoxins in the Era of Climate Change: The Mediterranean Experience. In Aflatoxins, Jean Claude, A., Ed. IntechOpen: Rijeka, 2022; 10.5772/intechopen.108534p. Ch. 1.
17. Leggieri, M.C.; Toscano, P.; Battilani, P. Predicted Aflatoxin B1 Increase in Europe Due to Climate Change: Actions and Reactions at Global Level. Toxins 2021, 13, 292.
18. Mitchell, N.J.; Bowers, E.; Hurburgh, C.; Wu, F. Potential economic losses to the US corn industry from aflatoxin contamination. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 2016, 33, 540-550, doi:10.1080/19440049.2016.1138545.
19. Esp. M.V. Bruno Vecchiy, M.M.V.E.M.T. Prevalence in Latin America 2021 Survey; Vetanco: 2022.
20. Elzupir, A.O.; Younis, Y.M.H.; Fadul, M.H.; Elhuss, A.M. Determination of Aflatoxins in Animal Feed in Khartoum State, Sudan. Journal of Animal and Veterinary Advances 2009, 8, 1000-1003, doi:10.3923/javaa.2009.1000.1003.
21. Probst, C.; Njapau, H.; Cotty, P.J. Outbreak of an acute aflatoxicosis in Kenya in 2004: identification of the causal agent. Appl Environ Microbiol 2007, 73, 2762-2764, doi:10.1128/AEM.02370-06.
22. Nji, Q.N.; Babalola, O.O.; Mwanza, M. Aflatoxins in Maize: Can Their Occurrence Be Effectively Managed in Africa in the Face of Climate Change and Food Insecurity? Toxins (Basel) 2022, 14, doi:10.3390/toxins14080574.
23. Meijer, N.; Kleter, G.; de Nijs, M.; Rau, M.L.; Derkx, R.; van der Fels-Klerx, H.J. The aflatoxin situation in Africa: Systematic literature review. Compr Rev Food Sci Food Saf 2021, 20, 2286-2304, doi:10.1111/1541-4337.12731.
24. Misihairabgwi, J.M.; Ezekiel, C.N.; Sulyok, M.; Shephard, G.S.; Krska, R. Mycotoxin contamination of foods in Southern Africa: A 10-year review (2007–2016). Crit Rev Food Sci 2019, 59, 43-58, doi:10.1080/10408398.2017.1357003.
25. Motloung, L.; De Saeger, S.; De Boevre, M.; Detavernier, C.; Audenaert, K.; Adebo, O.A.; Njobeh, P.B. Study on mycotoxin contamination in South African food spices. World Mycotoxin Journal 2018, 11, 401-409, doi:10.3920/wmj2017.2191.