Journal of Animal Science and Biotechnology
Research

Contamination of aflatoxin B1, deoxynivalenol and zearalenone in feeds in China from 2021 to 2024

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Abstract

Background

This study was carried out to investigate the individual and combined contamination of aflatoxin B1(AFB1), deoxynivalenol (DON), and zearalenone (ZEN) in feeds in China between 2021 and 2024. A total of 23,003 feed samples, including 17,489 feedstuff samples and 5,514 complete feed samples, were collected from different provinces of China for mycotoxin analysis.

Results

The analyzed mycotoxins displayed considerably high contamination in the feed samples, with the individual contamination of AFB1, DON, and ZEN were 20.0%–100%, 33.3%–100%, and 85.0%–100%, respectively. The average concentrations of AFB1, DON, and ZEN were 1.2–728.7 μg/kg, 106–8,634.8 μg/kg, and 18.1–3,341.6 μg/kg, respectively. Notably, the rates over China’s safety standards for AFB1, DON, and ZEN in raw ingredients were 9.7%, 2.7%, and 15.7%, respectively. Meanwhile, 3.5%, 1.1%, and 8.7% of analyzed complete feeds exceeded China’s safety standards for AFB1, DON, and ZEN, respectively. Moreover, the co-contamination rates of AFB1, DON, and ZEN in more than 70% of raw ingredients and 87.5% of complete feed products were 60.0%–100% and 61.5%–100%, respectively.

Conclusion

This study reveals that the feeds in China have commonly been contaminated with AFB1, DON, and ZEN alone and their combination during the past four years. These findings highlight the significance of monitoring mycotoxin contaminant levels in domestic animal feed and the importance of carrying out feed administration and remediation strategies for mycotoxin control.

Background

Mycotoxins are naturally occurring toxic secondary metabolites of fungi, primarily produced by five genera, including Aspergillus, Alternaria, Claviceps, Fusarium, and Penicillium [1,2,3,4]. As of the latest research, over 500 mycotoxins have been identified, posing a significant threat to human and animal health [5]. Among the most prevalent mycotoxins found in agricultural commodities are aflatoxin B1 (AFB1), deoxynivalenol (DON), and zearalenone (ZEN) [6,7,8]. AFB1, produced mainly by Aspergillus, is the most toxic mycotoxin, exhibiting hepatotoxic, carcinogenic, mutagenic, and teratogenic properties in various animal species [9,10,11,12,13,14]. Both DON and ZEN are primarily produced by Fusarium [15,16,17]. DON, a type B trichothecene, can induce anorexia, vomiting, and intestinal and immune system disorders in multiple species by inhibiting DNA, RNA, and protein synthesis [18,19,20,21,22]. ZEN is an estrogenic mycotoxin as it competes with 17β-estradiol for estrogen receptor binding, and can induce reproductive and fertility disorders [23,24,25,26,27].

Since mycotoxins in feed can negatively affect animal health, but can also threaten human health when converted into animal products, many countries have established safety standards for these toxins in feed and feed ingredients. For example, the European Commission set the maximum levels of AFB1, DON, and ZEN at 5–20, 900, and 250 μg/kg, respectively, in feed ingredients and complete feed [28, 29]. In 2017, General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China released the latest version of safety standards (GB 13078–2017) for AFB1, DON, and ZEN; which are 10–20, 1,000–5,000 and 100–250 μg/kg, respectively, for feedstuffs and complete feeds [7, 30].

However, current global warming and climate change are making corn, wheat and other crops more susceptible to fungal colonization, and mycotoxin contamination [31,32,33]. Thus, it will be important to monitor mycotoxin levels in livestock feed ingredients well into the future to maintain animal health and ensure the safety of human food products. There are several climatic regions across China, especially the warm or humid conditions of the Yangtze, Yellow River basins and northeast region and their numerous rainfall events, are favorable for mold growth and mycotoxin production in crops, which is increasing crop susceptibility to fungal infection [34,35,36]. Therefore, monitoring mycotoxin concentrations in the feedstuffs and complete feeds from these and other regions across China is essential to prevent farm animal exposure to mycotoxins and to ensure feed and food safety. Thus, the current study was conducted to investigate and renew the individual and combined contamination of AFB1, DON, and ZEN in more than 23,000 feedstuffs and complete feeds collected from different regions of China during the past 4 years.

Methods

Sample collection and preparation

A total of 23,003 feed samples were collected from 2021 to 2024 from either companies or livestock farms in different regions of China. There were 17,489 feedstuff samples including 7,018 corn, 1,558 dried distillers grains with solubles (DDGS), 1,608 corn gluten meal, 968 corn germ meal, 42 corn bran, 1,734 wheat, 845 wheat flour, 340 wheat bran, 169 wheat middlings, 44 wheat germ, 2,558 peanut meal, 58 cottonseed meal, 49 soybean meal, 82 brown rice, 24 rice bran, 20 rice bran meal, 36 sorghum, 182 distiller's grains, 80 corn sugar residue, 33 sugar residue, 27 nucleotide residue, 14 cottonseed protein, along with 5,514 complete feed samples including 658 pig feed, 4,814 poultry feed and 42 ruminant feed. These feed samples were primarily collected from the provinces of Anhui, Beijing, Chongqing, Fujian, Guangdong, Guangxi, Gansu, Henan, Hebei, Hunan, Hubei, Heilongjiang, Inner Mongolia, Jiangsu, Jiangxi, Jilin, Liaoning, Ningxia, Shandong, Sichuan, Shanxi, and Zhejiang by the feed companies. Since few feed samples with insufficient quantity, 11,826, 14,812, and 8,794 samples were analyzed for AFB1, DON, and ZEN, respectively. The feed samples were stored in sealing bags at −20 °C before analysis.

Extraction and quantified of AFB1, DON and ZEN

The extraction and quantified of AFB1, DON, and ZEN from the feed samples collected between 2021 and 2024 were performed as previously described [7, 35,36,37,38,39]. Briefly, 5 g of the mashed feed samples were mixed with a 25-mL solution of ethanol:water (50:50, v/v), blended using a commercial blender at high speed for 3 min, centrifuged at 4,200 r/min for 10 min, filtrated and collected the filtrate. The quantification of AFB1, DON, and ZEN were performed with commercially available test kits purchased from TRUTHERS Biotechnology Co., Ltd. (Tianjin, China) according to their operating instructions. Specially, the quantum dot fluorescence immunochromatographic assay were used to detection. The mycotoxins in the sample bind to the specific antibodies labeled with quantum dots, inhibiting the binding between the antibodies and the mycotoxin-BSA conjugate on the detection line (T line), resulting in changes in the fluorescence value of the T line. The content of mycotoxins is calculated by the high and low fluorescence value signals of the T line. The limit of detection (LOD) for AFB1, DON and ZEN set at 1.0 μg/kg, 100 μg/kg and 10 μg/kg, respectively.

Statistical analysis

All the data were analyzed by Microsoft Excel 2019 (Microsoft Corporation, Redmond, USA) and expressed as means, median, maximum, or percentages.

Results

Contamination of AFB1 in feeds

A total of 11,826 feed samples, including 8,442 feedstuffs and 3,384 complete feeds, were collected between 2021 to 2024 for analysis of AFB1 (Table 1). AFB1 was detected in 20.0%–100% of feedstuff and complete feeds, with the average levels ranging from 1.2 to 728.7 μg/kg. The highest median concentration of AFB1 was 770 μg/kg in wheat bran from the 2024 harvest, followed by 390 μg/kg in complete pig feed and 185.2 μg/kg in corn sugar residue from the 2024 harvest. The maximum levels of AFB1 were 4,490 μg/kg in DDGS harvested in 2024, followed by 2,380 μg/kg in wheat and 1,720 μg/kg in corn harvested in 2024. Among all the analyzed feedstuff samples, 819 raw feed ingredient samples (accounting for 9.7%) were contaminated with AFB1 at concentrations exceeding China’s safety standard. Notably, 74 samples of complete pig feed and 43 samples of complete poultry feed, which account for 2.2% and 1.3% of all the analyzed complete feed samples, were contaminated with AFB1 at levels exceeding the Chinese safety standard concentrations.

Table 1 AFB1 concentrations in feedsa
Full size table

Contamination of DON in feeds

In total, 14,812 feed samples, including 11,527 feedstuff and 3,285 complete feeds, were collected between 2021 to 2024 for analysis of DON (Table 2). DON was detected in 33.3%–100% of feedstuff and complete feeds, with the average levels ranging from 106 to 8,634.8 μg/kg. The highest median concentration of DON was 9,762 μg/kg in corn bran from the 2021 harvest, followed by 7,177 μg/kg and 4,840 μg/kg in corn germ meal from the 2023 and 2022 harvests. The maximum levels of DON were 84,000 μg/kg in wheat flour harvested in 2023, followed by 53,860 μg/kg in corn harvested in 2023 and 34,800 μg/kg in corn germ meal harvested in 2022. Among all the analyzed feedstuff samples, 316 raw feed ingredient samples (accounting for 2.7%) were contaminated with DON at concentrations over 5,000 μg/kg. Notably, the content of DON in corn germ meal and DDGS harvested between 2021 to 2024 exceeded the standard by 9.1%–69.5% and 2.6%–21.2%. Additionally, 24 samples of complete pig feed, 7 samples of complete poultry feed, and 4 samples of complete ruminant feed were contaminated with DON at levels exceeding the Chinese safety standard concentrations, which accounted for 4.6%, 0.3% and 13.3% of complete feeds samples of the same category analyzed, respectively.

Table 2 DON concentrations in feedsa
Full size table

Contamination of ZEN in feeds

A total of 8,794 feed samples, including 6,153 feedstuffs and 2,641 complete feeds, were collected between 2021 and 2024 for analysis of ZEN (Table 3). ZEN was detected in 85.0%–100% of feedstuff and complete feeds, with the average levels ranging from 18.1 to 3,341.6 μg/kg. The highest median concentration of ZEN was 2,566.4 μg/kg in corn gluten meal from the 2024 harvest, followed by 1,824.7 μg/kg in corn bran from the 2021 harvest and 1,424.4 μg/kg in distiller’s grains from the 2024 harvest. The maximum levels of ZEN were 30,154 μg/kg in corn gluten meal harvested in 2022, followed by 10,958 μg/kg in corn harvested in 2022 and 10,345.1 μg/kg in corn gluten meal harvested in 2024. A total of 965 raw feed ingredient samples, which account for 15.7% of all the analyzed feedstuff samples, were contaminated with ZEN at concentrations over the Chinese safety standard concentrations. Additionally, 149 samples of complete pig feed and 82 samples of complete poultry feed, which account for 5.6% and 3.1% of all the analyzed complete feed samples, were contaminated with ZEN at levels exceeding the Chinese safety standard concentrations.

Table 3 ZEN concentrations in feedsa
Full size table

Co-contamination of AFB1, DON and ZEN in feeds

The co-contamination of AFB1, DON, and ZEN in feed samples between 2021–2024 was presented in Table 4. More than 70.0% of analyzed feed ingredient samples had a combined contamination rate of 60.0%–100% for AFB1 + DON, AFB1 + ZEN, DON + ZEN, and AFB1 + DON + ZEN. Notably, except for the complete pig feed collected from 2022, the co-contamination ranges of AFB1 + DON, AFB1 + ZEN, DON + ZEN, along with AFB1 + DON + ZEN in most complete feeds were 61.5%–100%, 76.7%–100%, 66.7%–100%, and 58.3%–100%, respectively.

Table 4 Percentage of AFB1, DON and ZEN co-occurrence in feedsa
Full size table

Discussion

Mycotoxins have been reported to reduce animal performance, threaten human and animal health, as well as bring huge economic loss to the feed and food industry [4]. Thus, it will be important to monitor mycotoxin levels in livestock feed ingredients well into the future to maintain animal health and ensure the safety of human food products. Considering the widespread contamination, the present study was carried out to investigate the individual and combined contamination of the most prevalent and toxic mycotoxins, AFB1, DON, and ZEN in feedstuffs and complete feeds harvested between 2021 and 2024. In general, the analyzed mycotoxins displayed a considerably high occurrence in the analyzed feed samples harvested between 2021 and 2024, ranging from 20.0% to 100%, 33.3% to 100%, and 85.0% to 100% for AFB1, DON, and ZEN, respectively. Additionally, the LOD of the AFB1, DON, and ZEN are relatively high, which might underestimation of the actual exposure risk of these mycotoxins. These results indicated that the mycotoxin contamination of raw materials and complete feeds in China is quite serious.

The average concentration of AFB1 (1.2–728.7 μg/kg) determined in the present study was higher than previously reported concentrations (1.2–27.4 μg/kg) from samples harvested between 2016–2020 [7, 37]. Notably, 9.7% of all the analyzed raw feedstuff samples, especially corn, corn gluten meal, corn germ meal, and peanut meal, with AFB1 exceeded the Chinese safety standard concentration, which is much higher than the previously reported 0.9% of analyzed feedstuff samples with AFB1 exceeded the Chinese safety standard concentration [7, 30, 37]. Furthermore, there were 31.6% and 1.4% of the analyzed complete pig feed and poultry feed respectively contained AFB1, especially in complete pig feeds harvested in 2024, whereas the excess rate was as high as 85.5%. These results are much higher than the previous reports that 1.5% and 1.2% of all the analyzed final products for pig and poultry contained AFB1 over the limitation of Chinese safety standards [7]. The most toxic AFB1 is a frequent contaminant of various commodities, primarily cereals, nuts, and spices, and represents a highly toxic mycotoxin [9, 40, 41], therefore, it is necessary to persist in supervising the levels of AFB1 in the raw feed ingredients and its final products in the future. Additionally, since the safety limitation of AFB1 in European Commission (5–20 μg/kg) is lower than China (10–20 μg/kg), which might restrict the export of these Chinese feedstuffs [28,29,30].

The average levels of DON in feeds ranged from 106 to 8,634.8 μg/kg in this study, which is relatively higher than the previously reported range of 364.5–4,381.5 μg/kg in the feeds collected in China between 2013 and 2020 [7, 34, 37]. The maximum value of DON in feedstuffs in the current study is 84,000 μg/kg, which is at least 39 times higher than the values in all the reported areas [42]. There are 2.7% of the analyzed raw feed ingredients with DON exceeded China’s safety standard, especially as much as corn (9.1%–69.5%) and DDGS (2.6%–21.2%), which are much higher than the previously reported in 2013–2020 [7, 37]. Although only 4.6% of the complete pig feed samples exceeded the Chinese safety standard concentration, 0.3% of the complete poultry feed samples and 13.3% of the complete ruminant feed samples contaminated DON over the limitation of Chinese safety standard. These divergences could be attributed to the fact that the analyzed feed samples were randomly collected from different regions, and weather varies in these areas during the harvest period [7, 34, 35, 37, 43]. Taken together, these findings remind us that we need to be cognizant of the potential for contamination of feed ingredients, especially corn, DDGS, corn gluten meal, and corn germ meal, which were relatively severely contaminated by DON. In addition, since the safety limitation of DON in European Commission (900 μg/kg) is lower than China (1,000–5,000 μg/kg), which might restrict the export of these Chinese feedstuffs [28,29,30].

The occurrence of ZEN (85.0%–100%) in the analyzed feeds in this study was lower than previously study (96.9%–100%) from harvests in 2018–2020, but it was higher than feed samples (50.0%–100%) collected from 2013 to 2017 [7, 34, 35]. Meanwhile, in the current study, the average concentration of ZEN (18.1–3341.6 μg/kg) was relatively higher than previously reported results (48.1–326.8 μg/kg and 0–729.2 μg/kg) from harvests between 2013 and 2020 [7, 34, 35]. These differences might be due to the number of feed samples, different sampling areas, and different weather conditions during harvest. Notably, 15.7% of analyzed feedstuff samples, mainly including corn and its by-products, as well as 8.7% of analyzed complete feed samples (complete pig feed and complete poultry feed), were contaminated with ZEN at concentrations that exceeded the Chinese safety standards. These findings were much higher than previously reported, where 0.5% and 1.9% of all the analyzed feedstuffs and complete feed samples, respectively, were shown to be contaminated with ZEN exceeding the regulatory limits [7].

The co-occurrence and interaction between two or more mycotoxins were regularly found, and results suggested that co-contaminates can exhibit stronger toxic effects on animals when compared to each mycotoxin [44,45,46,47]. It is worth noting that the co-contamination of AFB1, DON, and ZEN, can exert additive and synergistic toxic effects on animal health and production [48]. In the present study, the co-contamination of mycotoxins in all analyzed feeds harvested in 2021–2024 was quietly universal, with more than 20% of feedstuff samples and 15.2% of complete feeds containing 2 or more mycotoxins. Notably, DDGS, corn gluten meal, corm germ meal, distiller’s grains, complete pig feed, and complete poultry feed were more than 70% co-contaminated with AFB1, DON, and ZEN. These results were similar to previous studies that mycotoxin contamination is a widespread issue in the livestock and poultry industry [48,49,50,51,52]. The present feed safety regulations do not consider the potential toxicity of co-contamination of mycotoxins and their combined toxicity on animal health and production may be underestimated. Therefore, the combined toxicity of these mycotoxins warrants further study, which might further reduce thresholds of the regulatory limits for mycotoxins. Although how to set the regulatory limits for mycotoxins under their co-contamination is very complicate, it still might be very important to consider it when new regulatory frameworks for mycotoxins are plan in the future.

Conclusion

In summary, the mycotoxin survey of 23,003 samples collected from different areas of China from 2021 to 2024 indicated that mycotoxins are ubiquitously present in feeds. Generally, 9.7%, 2.7%, and 15.7% of analyzed raw feed ingredients collected between 2021 and 2024 were contaminated with AFB1, DON, and ZEN by exceeding the Chinese safety standards, respectively. Meanwhile, 3.4%, 1.1% and 8.7% of analyzed complete feeds exceeded China’s safety standards for AFB1, DON and ZEN, respectively. Moreover, it is worth noting that co-occurrence ≥ 2 mycotoxins were quite common in all analyzed feed samples. The co-contamination rates of the three mycotoxins (AFB1, DON and ZEN) in more than 70% of analyzed feed samples were 60.0%–100%. Taken together, these results remind us that, 1) the serious situation of mycotoxin contamination in feed requires strict supervision, 2) it is desperately necessary to constant monitoring and continue research effort on the prevention and mitigation of co-contamination of mycotoxin due to a considerable number of feed samples containing more than one mycotoxin, and 3) suitable and targeted strategies controlling mycotoxin occurrence and toxicity need to be researched and applied.

Data Availability

The datasets used and/or analyzed during the current study are publicly available.

Abbreviations

  • AFB1 :: Aflatoxin B1
  • DDGS:: Dried distillers grains with solubles
  • DON:: Deoxynivalenol
  • LOD:: Limit of detection
  • ZEN:: Zearalenone

References

  1. 1.Greeff-Laubscher MR, Beukes I, Marais GJ, Jacobs K. Mycotoxin production by three different toxigenic fungi genera on formulated abalone feed and the effect of an aquatic environment on fumonisins. Mycology. 2019;11(2).(2019)105–17.: 105.
    10.1080/21501203.2019.1604575
    Article|CAS|PubMed|Google Scholar
  2. 2.Ruan ML, Wang J, Xia ZY, Li XW, Zhang B, Wang GL, et al. An integrated mycotoxin-mitigating agent can effectively mitigate the combined toxicity of AFB1, DON and OTA on the production performance, liver and oviduct health in broiler breeder hens. Food Chem Toxicol. 2023;182.(2023)114159.: 114159.
    10.1016/j.fct.2023.114159
    Article|CAS|PubMed|Google Scholar
  3. 3.Liu M, Zhao L, Gong G, Zhang L, Shi L, Dai J, et al. Invited review.(2022)remediation strategies for mycotoxin control in feed.J Anim Sci Biotechnol.: 19.
    10.1186/s40104-021-00661-4
    Article|CAS|PubMed|Google Scholar
  4. 4.Hao W, Li A, Wang J, An G, Guan S. Mycotoxin contamination of feeds and raw materials in China in year 2021. Front Vet Sci. 2022;9.(2021)929904.: 929904.
    10.3389/fvets.2022.929904
    Article|CAS|PubMed|Google Scholar
  5. 5.Haque MA, Wang Y, Shen Z, Li X, Saleemi MK, He C. Mycotoxin contamination and control strategy in human, domestic animal and poultry.(2020)a review.Microb Pathog.: 104095.
    10.1016/j.micpath.2020.104095
    Article|CAS|PubMed|Google Scholar
  6. 6.Zhang Z, Nie D, Fan K, Yang J, Guo W, Meng J, et al. A systematic review of plant-conjugated masked mycotoxins.(2020)Occurrence, toxicology, and metabolism.Crit Rev Food Sci Nutr.: 1523.
    10.1080/10408398.2019.1578944
    Article|CAS|PubMed|Google Scholar
  7. 7.Zhao L, Zhang L, Xu Z, Liu X, Chen L, Dai J, et al. Occurrence of aflatoxin B1, deoxynivalenol and zearalenone in feeds in China during 2018–2020. J Anim Sci Biotechnol. 2021;12.(2018)74.: 74.
    Article|CAS|PubMed|Google Scholar
  8. 8.Deng J, Huang JC, Xu ZJ, Liu Y, Karrow NA, Liu M, et al. Remediation strategies for mycotoxins in animal feed. Toxins (Basel). 2023;15(9).(2023)513.: 513.
    10.3390/toxins15090513
    Article|CAS|PubMed|Google Scholar
  9. 9.Deng J, Yang JC, Feng Y, Xu ZJ, Kuča K, Liu M, et al. AP-1 and SP1 trans-activate the expression of hepatic CYP1A1 and CYP2A6 in the bioactivation of AFB1in chicken. Sci China Life Sci. 2024;67(7).(2024)1468–78.: 1468.
    10.1007/s11427-023-2512-6
    Article|CAS|PubMed|Google Scholar
  10. 10.Sun LH, Zhang NY, Zhu MK, Zhao L, Zhou JC, Qi DS. Prevention of aflatoxin B1 hepatoxicity by dietary selenium is associated with inhibition of cytochromeP450 isozymes and up-regulation of 6 selenoprotein genes in chick liver. J Nutr. 2016;146.(2016)655–61.: 655.
    10.3945/jn.115.224626
    Article|CAS|PubMed|Google Scholar
  11. 11.Deng J, Zhao L, Zhang NY, Karrow NA, Krumm CS, Qi DS, et al. Aflatoxin B1 metabolism.(2018)regulation by phase i and ii metabolizing enzymes and chemoprotective agents.Mutat Res Rev Mutat Res.: 79.
    10.1016/j.mrrev.2018.10.002
    Article|CAS|PubMed|Google Scholar
  12. 12.Mo YX, Ruan ML, Wang J, Liu Y, Wu YY, Wang GL, et al. Mitigating the adverse effects of aflatoxin B1 in LMH, IPEC-J2 and 3D4/21 cells by a novel integrated agent. Food Chem Toxicol. 2023;178.(2023)113907.: 113907.
    10.1016/j.fct.2023.113907
    Article|CAS|PubMed|Google Scholar
  13. 13.Zhao L, Feng Y, Xu ZJ, Zhang NY, Zhang WP, Zuo G, et al. Selenium mitigated aflatoxin B1-induced cardiotoxicity with potential regulation of 4 selenoproteins and ferroptosis signaling in chicks. Food Chem Toxicol. 2021;154.(2021)112320.: 112320.
    10.1016/j.fct.2021.112320
    Article|CAS|PubMed|Google Scholar
  14. 14.Zhao L, Deng J, Xu ZJ, Zhang WP, Khalil MM, Karrow NA, et al. Mitigation of aflatoxin B1 hepatoxicity by dietary hedyotis diffusa is associated with activation of NRF2/ARE signaling in chicks. Antioxidants (Basel). 2021;10(6).(2021)878.: 878.
    10.3390/antiox10060878
    Article|CAS|PubMed|Google Scholar
  15. 15.Thapa A, Horgan KA, White B, Walls D. Deoxynivalenol and zearalenone-synergistic or antagonistic agri-food chain co-contaminants? Toxins (Basel). 2021;13(8).(2021)561.: 561.
    10.3390/toxins13080561
    Article|CAS|PubMed|Google Scholar
  16. 16.Kim NY, Kim MO, Shin S, Kwon WS, Kim B, Lee JY, et al. Effect of atractylenolide III on zearalenone-induced Snail1-mediated epithelial-mesenchymal transition in porcine intestinal epithelium. J Anim Sci Biotechnol. 2024;15.(2024)80.: 80.
    10.1186/s40104-024-01038-z
    Article|CAS|PubMed|Google Scholar
  17. 17.Kang TH, Lee SI. Establishment of a chicken intestinal organoid culture system to assess deoxynivalenol-induced damage of the intestinal barrier function. J Anim Sci Biotechnol. 2024;15.(2024)30.: 30.
    10.1186/s40104-023-00976-4
    Article|CAS|PubMed|Google Scholar
  18. 18.Liu M, Zhang L, Mo Y, Li J, Yang J, Wang J, et al. Ferroptosis is involved in deoxynivalenol-induced intestinal damage in pigs. J Anim Sci Biotechnol. 2023;14.(2023)29.: 29.
    10.1186/s40104-023-00841-4
    Article|CAS|PubMed|Google Scholar
  19. 19.Zhang L, Ma R, Zhu MX, Zhang NY, Liu XL, Wang YW, et al. Effect of deoxynivalenol on the porcine acquired immune response and potential remediation by a novel modified HSCAS adsorbent. Food Chem Toxicol. 2020;138.(2020)111187.: 111187.
    10.1016/j.fct.2020.111187
    Article|CAS|PubMed|Google Scholar
  20. 20.Liu AM, Yang YQ, Guo JC, Gao Y, Wu QH, Zhao L, et al. Cytochrome P450 enzymes mediated by DNA methylation is involved in deoxynivalenol-induced hepatoxicity in piglets. Anim Nutr. 2022;9.(2022)269–79.: 269.
    10.1016/j.aninu.2021.11.009
    Article|CAS|PubMed|Google Scholar
  21. 21.Xue Y, Li F, Li R, Zhang X, Guo H, Wang C. Chlorogenic acid alleviates IPEC-J2 pyroptosis induced by deoxynivalenol by inhibiting activation of the NF-κB/NLRP3/caspase-1 pathway. J Anim Sci Biotechnol. 2024;15.(2024)159.: 159.
    10.1186/s40104-024-01119-z
    Article|CAS|PubMed|Google Scholar
  22. 22.Qiu Y, Yang J, Wang L, Yang X, Gao K, Zhu C, et al. Dietary resveratrol attenuation of intestinal inflammation and oxidative damage is linked to the alteration of gut microbiota and butyrate in piglets challenged with deoxynivalenol. J Anim Sci Biotechnol. 2021;12.(2021)71.: 71.
    10.1186/s40104-021-00596-w
    Article|CAS|PubMed|Google Scholar
  23. 23.Shi D, Zhou J, Zhao L, Rong X, Fan Y, Hamid H, et al. Alleviation of mycotoxin biodegradation agent on zearalenone and deoxynivalenol toxicosis in immature gilts. J Anim Sci Biotechnol. 2018;9.(2018)42.: 42.
    10.1186/s40104-018-0255-z
    Article|CAS|PubMed|Google Scholar
  24. 24.Balló A, Busznyákné Székvári K, Czétány P, Márk L, Török A, Szántó Á, et al. Estrogenic and non-estrogenic disruptor effect of zearalenone on male reproduction.(2023)a review.Int J Mol Sci.: 1578.
    10.3390/ijms24021578
    Article|CAS|PubMed|Google Scholar
  25. 25.Zhou J, Zhao L, Huang S, Liu Q, Ao X, Lei Y, et al. Zearalenone toxicosis on reproduction as estrogen receptor selective modulator and alleviation of zearalenone biodegradative agent in pregnant sows. J Anim Sci Biotechnol. 2022;13.(2022)36.: 36.
    10.1186/s40104-022-00686-3
    Article|CAS|PubMed|Google Scholar
  26. 26.Li X, Duan J, Wang S, Cheng J, Chen H, Zhang Z, et al. Isorhamnetin protects porcine oocytes from zearalenone-induced reproductive toxicity through the PI3K/Akt signaling pathway. J Anim Sci Biotechnol. 2023;14.(2023)22.: 22.
    10.1186/s40104-022-00809-w
    Article|CAS|PubMed|Google Scholar
  27. 27.Li X, Zhao L, Fan Y, Jia Y, Sun L, Ma S, et al. Occurrence of mycotoxins in feed ingredients and complete feeds obtained from the Beijing region of China. J Anim Sci Biotechnol. 2014;5.(2014)37.: 37.
    10.1186/2049-1891-5-37
    Article|CAS|PubMed|Google Scholar
  28. 28.European Commission. Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on undesirable substances in animal feed. Off J Eur Commun. 2002;2002(10–22).(2002)16.: 16.
    Article|CAS|PubMed|Google Scholar
  29. 29.European Commission. Commission recommendation of 17 August 2006 on the Presence of deoxynivelenol, zearalenone, ochratoxin A, T−2 and HT-2 and fumonisins in products intended for animal feeding (2006/576/EU). Off J Eur Commun. 2006.(2006)7–9.: 7.
    Article|CAS|PubMed|Google Scholar
  30. 30.Ministry of Agriculture and Rural Affairs of the People's Republic of China. Hygienical standard for feeds: GB 13078–2017. Beijing: Standards Press of China; 2017.
    Article|CAS|PubMed|Google Scholar
  31. 31.Kos J, Anić M, Radić B, Zadravec M, JanićHajnal E, Pleadin J. Climate change-a global threat resulting in increasing mycotoxin occurrence. Foods. 2023;12(14).(2023)2704.: 2704.
    10.3390/foods12142704
    Article|CAS|PubMed|Google Scholar
  32. 32.Cao KX, Deng ZC, Li SJ, Yi D, He X, Yang XJ, et al. Poultry nutrition.(2024)achievement, challenge, and strategy.J Nutr.: 3554.
    10.1016/j.tjnut.2024.10.030
    Article|CAS|PubMed|Google Scholar
  33. 33.Zhang Y, Cao KX, Niu QJ, Deng J, Zhao L, Khalil MM, et al. Alpha-class glutathione S-transferases involved in the detoxification of aflatoxin B1 in ducklings. Food Chem Toxicol. 2023;174.(2023)113682.: 113682.
    10.1016/j.fct.2023.113682
    Article|CAS|PubMed|Google Scholar
  34. 34.Li R, Wang X, Zhou T, Yang D, Wang Q, Zhou Y. Occurrence of four mycotoxins in cereal and oil products in Yangtze Delta region of China and their food safety risks. Food Control. 2014;35(1).(2014)117–22.: 117.
    10.1016/j.foodcont.2013.06.042
    Article|CAS|PubMed|Google Scholar
  35. 35.Liu J, Sun L, Zhang J, Guo J, Chen L, Qi D, et al. Aflatoxin B1, zearalenone and deoxynivalenol in feed ingredients and complete feed from central China. Food Addit Contam Part B. 2016;9(2).(2016)91–7.: 91.
    10.1080/19393210.2016.1139003
    Article|CAS|PubMed|Google Scholar
  36. 36.Li A, Hao W, Guan S, Wang J, An G. Mycotoxin contamination in feeds and feed materials in China in year 2020. Front Vet Sci. 2022;9.(2020)1016528.: 1016528.
    10.3389/fvets.2022.1016528
    Article|CAS|PubMed|Google Scholar
  37. 37.Ma R, Zhang L, Liu M, Su YT, Xie WM, Zhang NY, et al. Individual and combined occurrence of mycotoxins in feed ingredients and complete feeds in China. Toxins (Basel). 2018;10(3).(2018)113.: 113.
    10.3390/toxins10030113
    Article|CAS|PubMed|Google Scholar
  38. 38.Zhao W, Li XW, Dessalegn L, Sun H, Guo LY, Liu M, et al. A study of contamination of T-2 toxin, ochratoxin A and fumonisin in feed ingredients and compound feed in China. Chin J Anim Nutr. 2024;36(4).(2024)2690–8.: 2690.
    Article|CAS|PubMed|Google Scholar
  39. 39.Mousavi Khaneghah A, Fakhri Y, Raeisi S, Armoon B, Sant’Ana AS. Prevalence and concentration of ochratoxin A, zearalenone, deoxynivalenol and total aflatoxin in cereal-based products.(2018)a systematic review and meta-analysis.Food Chem Toxicol.: 830.
    10.1016/j.fct.2018.06.037
    Article|CAS|PubMed|Google Scholar
  40. 40.National Technical Committee on Food Industry of Standardization Administration of China. Determination of zearalenone in food-high performance liquid chromatographic method with immunoaffinity column clean-up: GB 23504–2009. Beijing: Standards Press of China; 2009.
    Article|CAS|PubMed|Google Scholar
  41. 41.Zhao L, Feng Y, Deng J, Zhang NY, Zhang WP, Liu XL, et al. Selenium deficiency aggravates aflatoxin B1-induced Immunotoxicity in chick spleen by regulating 6 selenoprotein genes and redox/inflammation/ apoptotic signaling. J Nutr. 2019;149(6).(2019)894–901.: 894.
    10.1093/jn/nxz019
    Article|CAS|PubMed|Google Scholar
  42. 42.Augustin Mihalache O, Torrijos R, Dall’Asta C. Occurrence of mycotoxins in meat alternatives.(2024)dietary exposure, potential health risks, and burden of disease.Environ Int.: 108537.
    10.1016/j.envint.2024.108537
    Article|CAS|PubMed|Google Scholar
  43. 43.Pinotti L, Ottoboni M, Giromini C, Dell’Orto V, Cheli F. Mycotoxin contamination in the EU feed supply chain.(2016)a focus on cereal byproducts.Toxins (Basel).: 45.
    10.3390/toxins8020045
    Article|CAS|PubMed|Google Scholar
  44. 44.Wu L, Li J, Li Y, Li T, He Q, Tang Y, et al. Aflatoxin B1, zearalenone and deoxynivalenol in feed ingredients and complete feed from different province in China. J Anim Sci Biotechnol. 2016;7.(2016)63.: 63.
    10.1186/s40104-016-0122-8
    Article|CAS|PubMed|Google Scholar
  45. 45.Speijers GJ, Speijers MH. Combined toxic effects of mycotoxins. Toxicol Lett. 2004;153(1).(2004)91–8.: 91.
    10.1016/j.toxlet.2004.04.046
    Article|CAS|PubMed|Google Scholar
  46. 46.Smith MC, Madec S, Coton E, Hymery N. Natural co-occurrence of mycotoxins in foods and feeds and their in vitro combined toxicological effects. Toxins (Basel). 2016;8.(2016)94.: 94.
    10.3390/toxins8040094
    Article|CAS|PubMed|Google Scholar
  47. 47.Kochiieru Y, Mankevičienė A, Cesevičienė J, Semaškienė R, Dabkevičius Z, Janavičienė S. The influence of harvesting time and meteorological conditions on the occurrence of Fusarium species and mycotoxin contamination of spring cereals. J Sci Food Agric. 2020;100(7).(2020)2999–3006.: 2999.
    10.1002/jsfa.10330
    Article|CAS|PubMed|Google Scholar
  48. 48.Grenier B, Oswald IP. Mycotoxin co-contamination of food and feed.(2011)meta-analysis of publications describing toxicological interactions.World Mycotoxin J.: 285.
    10.3920/WMJ2011.1281
    Article|CAS|PubMed|Google Scholar
  49. 49.Hao W, Guan S, Li A, Wang J, An G, Hofstetter U, et al. Mycotoxin occurrence in feeds and raw materials in China.(2023)a five-year investigation.Toxins (Basel).: 63.
    10.3390/toxins15010063
    Article|CAS|PubMed|Google Scholar
  50. 50.Chang H, Kim W, Park JH, Kim D, Kim CR, Chung S, et al. The occurrence of zearalenone in South Korean feedstuffs between 2009 and 2016. Toxins (Basel). 2017;9.(2009)223.: 223.
    10.3390/toxins9070223
    Article|CAS|PubMed|Google Scholar
  51. 51.Gruber-Dorninger C, Jenkins T, Schatzmayr G. Global mycotoxin occurrence in feed.(2019)a ten-year survey.Toxins (Basel).: 375.
    10.3390/toxins11070375
    Article|CAS|PubMed|Google Scholar
  52. 52.Gruber-Dorninger C, Jenkins T, Schatzmayr G. Multi-mycotoxin screening of feed and feed raw materials from Africa. World Mycotoxin J. 2018;11.(2018)369–83.: 369.
    10.3920/WMJ2017.2292
    Article|CAS|PubMed|Google Scholar

Acknowledgements

The authors thank Xuewu Li, Juan Wang, Yuli Li, and Dianyi Peng for their technical assistance.

Funding

This project was supported by the Chinese Natural Science Foundation projects (32272915 and 32472949), National Key Research and Development Programs of China (2023YFD1301003), the Fundamental Research Funds for the Central Universities (2662023DKPY002), and Hebei Panshuo Biotechnolog Co., Ltd.

Ethics Declaration

Ethics approval and consent to participate

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Consent for publication

All authors have approved the final manuscript.

Competing interests

The authors declare no conflict of interest.

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