Aflatoxin in Chinese Commodities: History
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Subjects: Agriculture, Dairy & Animal Science
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FIREW Tafesse

Aflatoxins (AFs) are secondary metabolites that represent serious threats to human and animal health. They are mainly produced by strains of the saprophytic fungus Aspergillus flavus, which are abundantly distributed across agricultural commodities. 

  • aflatoxins
  • Aspergillus flavus
  • occurrence
  • atoxigenic strains
  • biocontrol
  • China
  • hepatocellular carcinoma

1. Introduction

Aflatoxins (AFs) are secondary metabolites produced by members of three distinctive sections of the genus Aspergillus: section Flavi, section Ochraceorosei, and section Nidulantes [1]. Members of section Flavi are the most common and widespread producers of AFs. The most commonly known AF producing Aspergillus fungi are A. flavus and A. parasiticus. A. parasiticus appears to be more adapted to a soil environment, being prominent in peanuts, whereas A. flavus seems adapted to the aerial and foliar environment, being dominant in corn, cottonseed, and tree nuts. Thus, it is known to be the most frequently encountered producer of AFs in agricultural products because of its widespread distribution [2][3].
Plant debris, decaying wood, animal silage, dead insects, and animal carcasses are the main organic nutrient sources of A. flavus as this fungus is saprophytic in nature [4]. Although it occurs predominantly in aerial and foliar environments [5], it can even reside on human organs. For example, recent studies reported its presence in tracheal aspirates of patients infected with COVID-19 [6][7].
Aspergillus fungi can grow and proliferate almost everywhere in the world under variable climatic conditions that range from arid to tropical moist to temperate [8][9]. A. flavus requires temperatures ranging from 25 °C to 33 °C and water activity of >0.98 for active growth [10]. However, it can still grow at temperatures between 30 °C and 40 °C [11]. Thus, it occurs in all major cereal, peanut, tree nut, and cotton seed growing areas that experience high temperatures [5].
Aspergillus species produce different types of AFs, including the potent parent toxins AFB1, AFB2, AFG1, and AFG2 under natural conditions. Moreover, they generate other metabolites (AFB2a, AFG2a, AFGM1, AGM2, AFM1, aflatoxicol (R0), parasiticol (B3), and aspertoxin) [12]. Crop soils are the primary source of A. flavus, which means that important food crops can be invaded in the field and subsequent AF contamination can occur when the plants are under stress due to factors such as high soil and/or air temperature, high relative humidity, drought, or insect attacks [13][14]. AFs are generally carcinogenic [15][16], can suppress immunity [17][18], and can lead to growth impairment in children [19][20] and AFB1 is the most potent and frequently occurring AF [21]. A. flavus strains are also known to produce cyclopiazonic acid (CPA) [22], which is an indole tetramic acid that was originally discovered in peanuts as a fungal metabolite [23]. AFs and CPA commonly occur as co-contaminants and result in substantial economic losses [24][25].
Asia and Africa are the continents most affected by AF contamination. China is among the countries with a high prevalence of AFs in different agricultural products targeted for both domestic consumption and export. Studies have reported higher levels of AF contamination in crops from the southern part of China (such as Guangdong Province) compared with other regions [26][27].

2. Reports of AF Distribution in Different Commodities in China

Mycotoxin contamination is a prevailing problem in China, and it is complicated by China’s export of several agricultural products to the EU and the USA. Several studies have reported the presence of AFs in agricultural products such as cereals, peanuts, spices, milk, and animal feeds that originate from China. Several Chinese medicines have also been found to contain mycotoxigenic fungi as well as their toxins. AF contamination reported in different commodities from China from 2001 to 2020 is summarized in the tables below.

2.1. Cereals Crops

Cereals, mainly, maize, sorghum, wheat, and rice, are the most AF-vulnerable crops. A number of authors in different countries, mainly Africa and Asia, have reported AF contamination of these crops. Table 1 lists AF contamination reported in different cereal and cereal-based food products. The main food items reported to contain AFs were maize, wheat, oats, and rice and their processed products, which were collected from almost all parts of the country. The majority of the food samples tested positive for AFs. The prevalence and incidence of AF contamination are generally higher in maize.
Table 1. Aflatoxin contamination in cereal and cereal-based foods reported in China.
Province Crops Origin Period Test Detection Limit (µg/kg) Mycotoxin Total Samples Incidences (%) Range of Positive Samples/Maximum Value (µg/kg) Mean ± SEM of Positive Samples/Mean (μg/kg) Level of Contamination above Chinese Regulatory Limit (%) (µg/kg) References
Liaoning Maize Farmer stores 2003 HPLC   AFs 73 97 - 0.99 All < 20 [28]
Whole grain rice 16 100 - 3.87
Brown rice 37 97 - 0.88
Heilongjiang Rice Farmer stores, granaries, and markets 2009–2011 DLLME
HPLC		   AFs 62 69 0.033–0.17 0.062 ± 0.042 All < 20 [29]
Liaoning 30 96.7 ND ND
Jilin 59 40 0.030–0.98 0.12 ± 0.25
Guangdong 138 53 0.19–4.1 0.44 ± 0.90
Guangxi 67 81 0.032–21 1.3 ± 3.7
Hainan 14 93 0.032–0.71 10.23 ± 0.32
Heilongjiang LOQ = 0.009 AFB1 62 69.3 0.033–0.14 0.058 ± 0.034
Liaoning 30 97 <LOQ <LOQ
Jilin 59 39 0.030–0.90 0.11 ± 0.23
Guangdong 138 73 0.030–3.7 0.41 ± 0.81
Guangxi 67 53 0.032–20 1.2 ± 3.4
Hainan 14 93 0.032–0.66 0.21 ± 0.30
Heilongjiang LOQ = 0.006 AFB2 62 14.5 0.022 0.022
Liaoning 30 6.6 <LOQ <LOQ
Jilin 59 6.5 0.086 0.086
Guangdong 138 13 0.020–0.47 0.11 ± 0.15
Guangxi 67 37.3 0.029–1.6 0.19 ± 0.36
Hainan 14 14.3 0.051 0.051
Shandong Province (Huantai County) Maize Individual households 2010 ELISA 0.1 AFB1 31 100 0.4–2.2     [30]
Rice 9 100 0.1–1.2
Wheat flour 9 100 0.3–0.9
Jiangsu Province (Huaian City) Maize 43 100 1.2–136.8
Rice 10 100 0.2–0.7
Wheat flour 7 100 0.1–0.3
Guangxi Zhuang Autonomous (Fusui County) Maize 34 100 1.0–50.0
Rice 10 100 0.3–1.4
Wheat flour - - -
Eight regions (Chongqing, Fujian, Guangdong, Guangxi, Hubei, Jiangsu, Shanghai, Zhejiang) Maize Local food markets 2007 HPLC 0.012 ;B1
0.008; B2;
0.036;G1		 AFs 74 52 0.02–1098.36     [31]
AFB1 74 46 0.14–970.32 23.91 above 20
AFB2 74 41 0.02–128.04  
AFG1 74 9 0.36–4.76
Rice AFs 84 23 0.15–3.88
AFB1 84 16 0.15–3.22
AFB2 84 3 0.06–0.24
AFG1 84 7 0.36–1.59
Yangtze Delta region (Hangzhou, Ningbo, Shanghai, Suzhou and Wuxi cities) Rice, wheat, maize, oats, soya bean Supermarkets and wholesale markets 2010 IAC-fluorometer 1 AFs 76 14.5 1.1–35.0 6.9 4.0 beyond Chinese (20) and 6.6 beyond EU(4) [32]
1 AFB1 76 14.5 1.0–32.2 6.6 4 beyond Chinese limit (20) and 9.2 beyond EU limit (2)
Hangzhou Cereal based infant food Supermarkets 2012 UPLC-MS/MS 0.001 AFB1 30 6.6 0.016–0.024     [33]
0.001 AFB2 0 ND
0.002 AFG1 0 ND
0.006 AFG2 0 ND
0.008 AFM1 0 ND
0.004 AFM2 0 ND
Chongzuo County and Guilin suburbs, Guangxi autonomous region Maize Individual households 1998 HPLC 1 AFB1 40 45 9–2496 460 ± 732 76% AFB1positive samples above Chinese limit (20) [34]
2.5 AFB2 35 11–320 82 ± 102
10 AFG1 22.5 12–21 15 ± 3
10 AFG2 0 ND ND
Taiwan Coffee, red yeast rice and maize Local stores 2013 ELISA 1–2 AFB1 36 55.5 1.7–234.0   30% are beyond the Taiwan limit (15) [35]
Eleven districts of Guangzhou Rice and rice products Household supply retail shops 2015–2017 HPLC 0.1 AFB1 490 1.42 0.28–1.00 0.13 ± 0.001   [36]
Wheat and wheat products 436 1.4 0.28–1.46 0.13 ± 0.001
339 0.9 1.50–6.30 0.17 ± 0.001
Maize and maize products
Guangxi ; Zhuqing Village, Fusui, Maize Households 1999 ELISA - AFB1 30 76.7 0.4–128.1 23.7 ± 6.6 30% beyond (20) [37]
Rice 30 23.3 0.3–2.0 1.1 ± 0.3  
Shigatze Prefecture of Tibet Autonomous Region Barley Farms 1998 CD-ELISA   AFs 25 4 0.0 - 0.04   [38]

2.2. Peanuts, Pine Nuts, Nuts, Oils, and Other Oil Products

Table 2 lists a variety of AF-contaminated commodities, such as peanuts, walnuts, pine nuts, peanut butter, sesame paste, peanut oil, vegetable oil, sunflower oil, fish oil, and maize oil, that were collected from every part of China.
Table 2. Aflatoxin contamination in peanut, pine nut, walnut, other oil seeds and oil reported in China.
Province Crops Origin of Sample Period Analytical Method Detection Limit (µg/kg) Mycotoxin Total Samples Incidences (%) Range of Positive Samples/Maximum Value (µg/kg) Mean ± SEM of Positive Samples/Mean (μg/kg) Level Contamination above Chinese Regulatory Limit (%) References
Twelve provinces, including Liaoning, Shandong, Henan, Hebei, Jiangsu, Anhui, Jiangxi, Hubei, Hunan, Guangdong, Guangxi, and Fujian Peanut with pod From farm 2011/2012 HPLC 3:1 for LOD AFB1 1040 25 0.01–720 2.13 1% beyond Chinese regulation (20) and 3.7% above EU regulation (2) [39]
Liaoning Peanut From farm and storage 2015 HPLC 0.2 for AFB1; 0.05 for AFB2; 0.2 for AFG1; 0.05 for AFG2 AFB1 408 3.19 0.15–116.64 0.43 ± 6.23 - [26]
AFB2 3.68 0.05–27.36 0.11 ± 1.50
AFG1 0.25 3.61 0.01 ± 0.18
AFG2 0.74 0.27–1.15 0.00 ± 0.06
Total AF 4.90 0.05–144.00 0.55 ± 7.80
Henan AFB1 1190 19.00 0.06–483.00 7.57 ± 41.12
AFB2 11.68 0.01–61.50 0.82 ± 4.67
AFG1 1.18 0.33–460.00 0.81 ± 15.23
AFG2 4.03 0.05–104.00 0.23 ± 3.33
Total AF 19.00 0.06–1023.2 9.43 ± 54.98
Sichuan AFB1 455 15.60 15.56 ± 86.73 15.56 ± 86.73
AFB2 13.19 2.34 ± 13.40 2.34 ± 13.40
AFG1 0.22 0.07 ± 1.57 0.07 ± 1.57
AFG2 5.27 0.22 ± 1.82 0.22 ± 1.82
Total AF 15.60 18.19 ± 100.38 18.19 ± 100.38
Guangdong AFB1 441 11.56 0.22–341.41 4.73 ± 29.84
AFB2 11.79 0.05–30.38 0.51 ± 2.96
AFG1 0.91 0.50–11.50 0.04 ± 0.57
AFG2 3.17 0.21–5.74 0.06 ± 0.41
Total AF   14.29 0.06–373.69 5.34 ± 32.90
Eight regions (Chongqing, Fujian, Guangdong, Guangxi, Hubei, Jiangsu, Shanghai, Zhejiang) Peanut Local food markets 2007 HPLC - Total AF 65 15 0.03–28.39   Average 27.44 [31]
Walnut 48 31 0.02–1.20
Pine Nut 12 2 0.19–0.25
Peanut AFB1 65 9 0.15–22.39
Walnut 48 21 0.14–0.32
Pine Nut 12 2 0.19–0.23
Peanut AFB2 65 5 0.03–6.00
Walnut 48 12 0.02–0.70
Pine Nut 12 1 0.02
Peanut AFG1 65 4 0.42–11.73
Walnut 48 8 0.36–0.83
Pine Nut 12 0 -
Shandong Province (Huantai County), Jiangsu Province (Huaian City), and Guangxi Zhuang Autonomous (Fusui County) Plant oil Individual households 2010/2011 ELISA 0.1 AFB1 39 100 0.5–114.4   Median level is 52.3 beyond the Chinese standard 10 [30]
Peanut 17 100 0.1–0.7    
Hebei Province Shijiazhuang Edible oil (peanut, blended,
soybean, maize,
sunflower, fish oil)		 Local markets 2011 LC–MS/MS   AFB1 40 32.5 0.14–2.72     [40]
AFB2 12.5 0.15–0.36  
AFG1 7.5 0.01–0.02  
Baoding AFB1 18 22.2 0.16–1.88  
AFB2 5.56 0–0.18  
Tangshan AFG1 0 -  
AFB1 18 27.8 0.15–0.45  
AFB2 0 -  
AFG1 0 -  
Beijing, Shanghai, Changchun, Chengdu, Shijiazhuang, and Zhengzhou Peanut butter Retail markets 2007 LC 1 AFT 50 82 0.77–70.64 8.51 39% for total AFs set by EU (4)
37% AFB1 set by EU (2)
and 2% AFB1 exceed the Chinese regulations (20);		 [41]
0.15 AFB1 0.39–68.51 6.12
6
AFB2 0–5.52 0.67
AFG1 0–21.22 2
AFG2 0–6.36 0.4
Sesame paste 1 AFT 50 37 0.54–56.89 6.75 24% beyond the limits total AFs of EU (4)
19% and 32% of sesame AFB1 exceed Chinese (5) and European Union (EU) (2)
0.15 AFB1 0.39–20.45 4.31
AFB2 0–4.92 0.63
AFG1 0–26.28 1.44
AFG2 0–5.75 0.37
Eleven districts of Guangzhou Nuts Household supply retail shops 2015–2017 HPLC 0.1 AFB1 96 3.1 0.62–1.37 0.14 ± 0.001   [36]
Vegetable oil 365 38.9 0.26–283.0 6.32 ± 25.99
Commercial vegetable oil 269 25 0.35–7.30 0.67 ± 1.81
Home-made peanut oil 96 75.5 0.26–283.0 38.74 ± 47.45 The mean Is 7 times larger that the Chinese maximum limit (5)
21 provinces, autonomous regions and municipalities Nuts Local markets and supermarkets 2018 UPLC LOD; 0.05–1.00;
LOQ; 0.10–5.00		 AFB1 133 3.8 1.3–40.7 9.3 ± 0.28   [42]
AFB2 15 0.2–1.2 1.9 ± 0.02
AFG1 ND ND ND
AFG2 2.3 1.1–1.6 1.3 ± 0.02
Guangxi; Zhuqing Village, Fusui, Peanut Households 2013 ELISA - AFB1 30 66.7 0.1–52.5 7.8 ± 3.2   [37]
Yangtze Delta region (Hangzhou, Ningbo, Shanghai, Suzhou and Wuxi cities) Peanut, soya bean, and oil. Supermarkets and wholesale markets   IAC-fluorometer 1 AFs 76 14.5 1.1–35.0 6.9 4.0 [32]

2.3. Chinese Herbal Medicines (CHMs), Spices, Tea, Fruits, and Vegetables

In China, the maximum limits in herbs are 5 µg/kg and 10 μg/kg, respectively [43]. CHMs that have maximum limits for AFs in China are as follows: Jujubae Fructus, Hirudo, Pheretima, Myristicae Semen, Scorpio, Cassiae Semen, Hordei Fructus Germinatus, Polygalae Radix, Citri Reticulatae Pericarpium, Qutisqualis Fructus, Platycladi Semen, Sterculiae Lychnophorae Semen, Nelumbinis Semen, Persicae Semen, Scolopendra, Arecae Semen, Ziziphi Spinosae Semen, Bombyx Batryticatus, and Coicis Semen [43]. EU countries have also established stringent standards, such as commission regulation (EC) No. 165/2010, which sets the maximum limits of AFB1 for dried fruits and spices in the range of 2 to 5 μg/kg and total AFs between 4 and 10 μg/kg. Table 3 summarizes updated data for AF contamination in herbal medicines, spices, fruits, and vegetables in China.
Table 3. Aflatoxin contamination in Chinese herbal medicine, spices, tea, fruits and vegetables reported in China.
Province Product Origin of the Sample Study Year Analytical Method Mycotoxin Detection Limit (µg/kg) Total Samples (n) Incidences (%) Range of Positive Samples/Maximum Value (µg/kg) Mean ± SEM of Positive Samples/Mean (μg/kg) Level Contamination above Chinese Regulatory Limit (%) References
Eleven districts of Guangzhou Tea Household supply retail shops 2019/2020 HPLC AFB1 0.1 128 17.9 0.25~4.0 0.36 ± 0.62   [36]
Anhui, Fujian, Gansu, Guangdong, Guizhou, Hubei, Shanxi, Xinjiang, Yunnan, Zhejiang Traditional Chinese medicines (TCM) Herbal market 2019/2020 HPLC AFB1 0.012–1.3 48 70.8 0.12–3.05   All < 5 [44]
AFB2 0.43–0.5   AFB1 limit 2–10, AF’s ; 4–20 (Chinese AFB1 ≤ 5 ; AFs ≤ 10)
AFG1 ND–0.85  
AFG2 0.87–2.11  
China TCM Regulated enterprises 2011 UHPLC/MS/MS AF’s LOD; 0.01–1.56 60 40 0.2–19.5     [45][46]
AFB1 1.2–9.8
AFB2 0.2–7.1
AFG1 0.6–2.5
AFG2 0.2–4.8
Chongqing China TCM Local markets and
drug stores		 2015 UPLC-MS/MS AF’s LOD; 0.008–0.022 22 63 0.2–7.5   18.2 exceeded the maximum limit set by EU (4) [47]
AFB1 0.2–4.8
AFB2 0.1–2.3
AFG1 0.1–0.8
AFG2 0.1–0.2
Zhejiang TCM Regulated enterprises 2009/2010 (UHPLC–MS/MS AFB1 LOD; 0.01–1.56 30 68.8 - 1.40   [48]
AFB2 50.0 1.27
AFG1 43.8 0.50
AFG2 43.8 0.94
AFM1 6.6 0.7
Beijing Ginger Local markets 2013/2014 UHPLC-FLR AFB1 0.005–0.2 30 5/30 0.3–1.38 0.073   [49]
AFB2 30 ND -  
AFG1 30 ND -  
AFG2   30 ND -  
Hebei province and Guangxi provinces Chinese yam, American ginseng, Ginseng, Notoginseng, Astragalus, Polygala, Bupleurum, Liquorice Markets 2013 UPLC-MS/MS AFB1 LOD ≤ 0.05 and LOQ ≤ 0.1 48 35.4 ND-13.3   14.58 exceed 5 [50]
AFB2 2 ND-8.2    
AFs 37.5 ND-21.5   8.33 exceed 10
Shanghai Pistachios Markets 2014–2015 LC-MS/MS AFB1 0.03 25 4 ND-0.8 0.8 - [51]
AFB2 0.2 0 ND ND
AFG1 0.2 0 ND ND
AFG2 0.3 0 ND ND
Dried longans AFB1 0.1 28 0 ND ND
AFB2 0.1 3.6 ND-0.2 0.2
AFG1 0.2 0 ND ND
AFG2 0.3 0 ND ND
Raisins AFB1 0.1 32 0 ND ND
AFB2 0.3 0 ND ND
AFG1 0.3 0 ND ND
AFG2 0.3 0 ND ND
Dried dates AFB1 0.1 40 0 ND ND
AFB2 0.1 0 ND ND
AFG1 0.3 0 ND ND
AFG2 0.3 0 ND ND
21 provinces, autonomous regions and municipalities Dried jujube Local markets and supermarkets 2018 UPLC-MS/MS AFB1 LOD; 0.05–1.00
and LOQ; 0.10–5.00		 35 0 ND ND   [42]
AFB2 0 ND ND
AFG1 8.6 0.2–0.6 0.4 ± 0.03
AFG2 2.9 0.4 0.4 ± 0.06
Raisins AFB1 30 0 ND ND
AFB2 0 ND ND
AFG1 0 ND ND
AFG2 20 0.5–1.4 0.9 ± 0.02
Dried figs AFB1 20 15 1.8–384.1 129.5 ± 0.68
AFB2 5 2.5 2.5 ± 0.21
AFG1 15 0.4–17.8 5.9 ± 0.33
AFG2 15 0.6–1.2 0.9 ± 0.05
Dried longans AFB1 15 ND ND ND
AFB2 6.7 0.7 0.7 ± 0.01
AFG1 ND ND ND
AFG2 40 0.1–2.9 1.5 ± 0.07

2.4. Animal Feed and Dairy Products

Table 4 lists AFs that were detected in feeds and dairy products collected from different parts of China and shows that the prevalence of AFs in both feedstuffs and dairy products is high. However, the levels of most of these toxins are far below China’s maximum limits for feeds and dairy products.
Table 4. Aflatoxin contamination of animal feeds, and dairy products reported in China.
Province Product Year Origin of the Sample Analytical Method Mycotoxin Detection Limit (µg/kg) Total Samples (n) Incidences (%) Range of Positive Samples/Maximum Value (µg/kg) Mean ± SEM of Positive Samples/Mean (μg/kg) Level Contamination above Chinese Regulatory Limit (%) (µg/kg or L) References
Ten provinces
(Heilongjiang,
Inner Mongolia Beijing, Tianjin Ningxia,
Hebei, Shanxi,
Shandong, North
Shanghai,
Guangdong, South)		 Dairy cow feeds 2013 Dairy farms HPLC AFB1   200 42 0.05–3.53 0.31 <10 [52]
AFB2   200 36 0.03–0.84 0.14 -
AFB1 + AFB2   200 24.5 0.05–3.53 0.34 -
Milk Dairy farms ELISA AFM1 0.005 200 32.5% 5.2–59.6 ng/L 0.0153 <0.5
Beijing Feed and feedstuffs 2012 Animal farms HPLC AFB1 - 22 50 59 6.0 <Chinese limit [53]
AFB2 9.1 12 0.6
AFG1 4.5 0.5 0.0
AFG2 9.1 0.5 0.0
31 provinces Yoghurt 2013 Retail store and supermarkets ELISA AFM1 0.05 μg/kg 178 4.49 - 27.10 <0.5 [54]
Milk 0.005 μg/kg 233 48.07 - 21.49 <0.5
Tangshan region of China Milk 2012–2014 Milk stations HPLC-MS/MS AFM1   530 52.8% 10–200 ng/L 73.0 ng/L <0.5 [55]
China Feed   Company and livestock farms Eu-Nano-TRFIA Total AFs 0.16 μg/kg 397 78.3% 0.50–145.30 μg/kg     [56]
Northern China Raw milk 2019/2020 Shops, distributors, farms ELISA AFM1 - 84   10–430 ng/L 110 ng/kg 34.5% exceeds EU limits [57]
Commercial milk AFM1 69    
Total mixed rations (TMR) HPLC AFB1 0.03 μg/kg 22   30–370 ng/L 4.16 μg/kg 31.8% exceeds EU limits
Central China Feed 2016/2017   HPLC AFB1 0.03 μg/kg 174 35.1%     2.3% (30) [58]
UHT milk ELISA AFM1 0.005 μg/kg 111 73.6% - 100.0 ng/L All below 0.5
Pasteurized milk ELISA AFM1 131 -
China (Beijing and Shanghai) UHT milk 2010 super-
markets		 ELISA AFM1 - 153 54.9% 0.006–0.160 mg/L - All below 0.5 [59]
Pasteurized milk - 26 96.2% 0.023–0.154 mg/L - 20.3% of UHT milk samples and 65.4% of pasteurized milk samples exceed the EU limit

4. Health Impacts of AFs in China

Human dietary AF exposure can result in either chronic or acute health risks depending on the extent of exposure. In one remarkable case, 125 Kenyans died between 2004 and 2006 due to acute liver failure after consumption of homegrown maize containing high levels (up to 4400 ppb) of AFs [60][61][62]. Stunted growth, immunosuppressive effects, and cancer are also chronic health complications of AF consumption [17][18][62]. Among the AFs, AFB1 is known to cause liver cancer and, in synergism with the hepatitis B virus (HBV), to increase the possibility of developing chronic liver disease (CLD) or HCC [63][64].
AF parent molecules (like AFB1) are relatively harmless, but the electrophilic intermediates AFBO (B1-8,9-epoxide) that are generated at the predominant AF metabolization site are mutagenic and carcinogenic [65][66]. The major human cytochrome p450 enzymes are responsible for converting AFB1 into two reactive 8,9-epoxide stereoisomers (exo and endo) [62]. Exo-isomers are more toxic and cause the AFB1 to exhibit genotoxic characteristics [67]. The exo-8,9-epoxide has a high binding affinity for DNA, forming AF-DNA adducts, which primarily exist as 8,9-dihydroxy-8-(N7) guanyl-9-hydroxy-AFB1 (AFB1-N7-Gua) adducts. These adducts are primarily responsible for the genotoxic, mutagenic, and carcinogenic properties of AFB1 [21].
Human dietary AF exposure is usually measured using several biomarkers. Biomarkers help to assess AF exposure to more accurately reflect individual intake of AFs, and they are measured in urine or blood serum. The AF albumin adduct (AF-alb) in serum is a valuable biomarker for CLD and HCC due to long-term high AF exposure [68][69][70]. The most commonly used biomarkers are the urinary AFB1-N7-Gua adduct, which is a product of DNA damage, and the metabolites of AFM1 in urine or milk (AFP1, AFB1, AFQ1, AFP1, AFB-N-acetyl-L-cysteine (AFB1-mercapturic acid)) [37][71][72].
In China, studies of AFs and HCC risks have been conducted for more than three decades, with the earliest report dating back to 1989 [73]. That study confirmed the roles of the HBV virus and AFB1 in the rate of primary hepatocellular carcinoma (PHC) in southern Guangxi, China, which was the most PHC-prevalent region in the world. A number of other researchers have reported elevated AF exposure and higher incidences of HCC in different cities/counties of China in the provinces/municipalities of Jiangsu, Guangxi, Guangdong, Shanghai, and Taiwan [37][31][74][75], as regions in the southern parts of China are prone to AF contamination because their humid and warm climate is suitable for the growth and proliferation aflatoxigenic fungi [26][27].
Guangxi Province is a well-studied region of China due to its high rate of HCC morbidity, mortality, and AF exposure. Wang et al. (2001) [37] conducted a study in Zhuqing Village, Fusui County, Gangxi, aimed at determining the correlation between AF exposure, chronic HBV, and HCC cases. In this study, AFB1 contents of the major food items in the area were evaluated, and it was detected in 76.7% of maize (range 0.4–128.1 ppb), 66.7% of cooking oil (range 0.1–52.5 ppb), and 23.3% of rice (range 0.3–2.0 ppb). The mean levels of serum AFB1-albumin adducts in 29 identified HCC groups were >1.2 pmol/mg of albumin at both the beginning and end of the study period, and urinary AFB1 metabolites were detected in 88.9% of samples (range 0.9–3569.7 ng/24 h urine). The study also concluded that HCC accounted for 64% of the total cancer cases in the area.
Another comparative epidemiological study was conducted in China to identify the potential factors modulating AF exposure among three locations: Fusui County and Nanning City in Guangxi Province and Chengdu City in Sichuan Province [74]. These three locations had HCC rates of 92–97, 32–47, and 21 per 100,000 people, respectively. Residents were screened for AF-alb adducts and human papilloma virus (HPV) infection. Higher numbers of HPV-positive people (47%) were found among Fusui residents compared to Nanning (15%) and Chengdu (22%) residents. This suggests a co-effect of HPV infection and AFB1 exposure in the high risk of HCC in the Fusui region.
Taiwan is another province of China that has a high rate of dietary AF exposure and HCC prevalence. Wan et al. (1996) [75] published one of the earliest reports about AF-related HCC cases in Taiwan. They surveyed seven townships, including those with the highest HCC incidence. Detectable concentrations of the AF-alb adduct and urinary AF metabolites were highly correlated with HCC in 56 cases, and the authors concluded that AF exposure was enhancing the risk of HCC associated with HBV. In a similar study designed to elucidate the importance of AF exposure in the etiology of HCC, researchers conducted a community-based cohort epidemiological study in the Taiwan Penghu Islets, where the HCC mortality rate was highest [76]. In this study AF exposure was evaluated in inhabitants (6487) via regular follow-up. AFB1-albumin adducts were detected in 60% of HBsAg-positive HCC cases, and the authors concluded that a higher risk of developing HCC was attributable to both a heavy exposure to AFs and high HPV incidence.
During the last 30 years, changes in China have led to a significant drop in AF-associated HCC prevalence and HCC mortality. This decrease might be due to socioeconomic changes and changes in the consumption pattern of maize, which dramatically decreased among Chinese families from 1980 to 2000 [77]. Additionally, after adoption of the national children’s HBV vaccination program (1980–1990), the prevalence of HCC has dropped significantly. Evidence for this decline comes from a recent cancer registration report showing about an 83% reduction of HCC mortality in Qidong, which was one of the regions with the highest prevalence [78]. The reduction of HCC incidence is also evident in results of a longitudinal (28 year) study that utilized follow-ups of etiological interventions among 1.1 million inhabitants of this area [78]. In this study there was a controlled neonatal HBV vaccination program (1980–1990) and economic reforms beginning in 1980 that were aimed at changing the consumption pattern from maize to rice and wheat. Compared with 1980–1983, the age-specific liver cancer incidence rates in 2005–2008 significantly decreased by 14-fold (ages 20–24), 9-fold (ages 25–29), and 4-fold (ages 30–34). The reduction among 20–24 year-olds might reflect the combined effects of reduced AF exposure and neonatal HBV vaccination, whereas the decreased incidence in the age groups of >25 years may be attributable mainly to a rapid reduction of AF exposure.

5. AF Standards in China and Recent Updates

AFs are the most regulated mycotoxins due to their toxicities and health risks, particularly carcinogenicity. Over 100 countries have defined maximum limits for AFs [79][80]. For cereals and nuts, most maximum limits range between 10 and 20 µg/kg, although the EU sets the lowest limit at 4 µg/kg [81]. Most countries set the maximum limits of AFM1 at either 0.05 µg/kg (EU) or 0.5 µg/kg. Currently, the Chinese government also has regulations on the maximum limits of AFs allowed in different foodstuffs. In maize, peanuts, peanut oil, nuts (walnuts, almonds), and dried fruit, the maximum limit of AFB1 is 20 μg/kg, whereas the limit in rice and oils (sesame, rapeseed, soybean, sunflower, flax, maize germ, bran, cottonseed) is 10 μg/kg. In milk and milk products (fresh raw milk, whole milk powder, evaporated milk, sweet condensed milk) and butter the AFM1 limit is 0.5 μg/kg, excluding liquid infant formula [82].
The establishment of mycotoxin legislation and regulations is dynamic both in terms of addressing newly identified toxins and maintaining rigorous limits. For instance, the EU has made the maximum tolerable limits more stringent over time [81][83]. It has been two decades since the Chinese government first imposed national food safety standards on maximum levels of mycotoxins in foods. Mycotoxin food standards were established in China in 2003 for the first time (GB 9676-2003) and considered toxins such as AFB1, AFM1, DON, and patulin, and they were renewed in 2005 (GB2761-2005). In 2011, GB2761-2011 added maximum limits of OTA and ZEN and considered baby foods and other special food groups [84]. In 2017, the Chinese maximum levels of mycotoxins in foods were updated, with a special emphasis on vulnerable groups of society (GB2761-2017). In this version, the maximum limit of AFB1 in infant formula and supplementary foods for infants, young children, and pregnant and lactating woman was set at 0.5 µg/kg. In 2019, GB 2761 lowered the maximum AFM1 limit from 0.5 to 0.2 µg/kg in liquid infant formula, which includes raw milk, pasteurized dairy, sterilized dairy, modified dairy, and fermented dairy. It also added a maximum limit for fumonisins (200 μg/kg) in cereal-based (maize or maize flour) auxiliary foods for infants [85]. Other common AFs (e.g., B2, G1, and G2) are being detected in different foods in China and are known to be carcinogenic, but they and total AFs are not yet regulated.

7. Distribution and Genetic Characteristics of Aspergillus Species in China

The most important fungi responsible for AF contamination in China are the three members of Aspergillus section Flavi: A. flavus, A. parasiticus, and A. nomius [86]. Hence, understanding the distribution and mycotoxin (AFs and CPA) production capacities and the genetic makeup of these fungi is crucial for broader AF management and for designing preharvest and postharvest mitigation strategies. Interest in the distribution of A. flavus across different agro-ecologies, geographical locations, crops, and crop soils has also been increasing in China, due to the possibility of using isolates of atoxigenic A. flavus strains to reduce AF contamination. Thus, several reports describing the nature and distribution of Aspergillus section Flavi in China have been published, and they are summarized in Table 5.
Table 5. Distribution of Aspergillus flavus reported by different authors in China.
Location Product Number of Samples Source Sampling Season Incidences of Fungi, or Aspergillus spp. or Aspergillus Section Flavi Incidences of A. flavus Species Toxin Production of A. flavus Strains Nature Biosynthetic Genes Morphological Nature Reference
Liaoning Province
(Northeast)		 Maize 120 Household stored (1–3 years) 2003 55.8% (Aspergillus section Flavi) 98.5% - - 64%-L
36%-S		 [27]
Guangxi
province		 Maize 89   2016/2017 195 (Aspergillus section Flavi) 98.5% 86.6% (30) were aflatoxin and CPA positive - Fluorescence and pink color observed in carbon added PDA [87]
19 provinces, 1 autonomous region and 1 municipality Peanut, maize, rice - - 2013/2014 724 A.flavus species isolated >95% 32% (229) atoxigenic 10.4% atoxigenic strains found to have lost aflR, fas-1 and aflJ genes 51% S-type (229)
34% L- type (229)15% NS (229)		 [88]
14 provinces Peanut pod 1106   2013 265 Aspergillus spp. 262 (98.9%) 18.8% A.flavus atoxigenic 38.0% atoxigenic strains lost nor-1, ver-1, aflR, omtA genes - [89]
2015 257 Aspergillus spp. 254 (98.8%)  
12 provinces Rice - - - - 127 A.flavus 47(37%) toxigenic - - [90]
Provinces Liaoning Peanut-cropped soils - Field 2013 343 fungi isolated 9 323 76 Atoxigenic [91] 97% of atoxigenic strains lost one of the aflT, nor-1, aflR, hypB genes  
Shandong 73  
Hubei 125  
Guangdong 116  
Different provinces of China Peanut cropped soil - Field - - 56 A.flavus 35 atoxigenic 11 A. flavus isolates had 5 deletion patterns for 12 genes 21 atoxigenic strains were either L- or S-type [92]

8. Atoxigenic A. flavus as AF Biocontrol Agents

Recent developments in the field of mycotoxin prevention have led to renewed interest in seeking effective, feasible, and environmentally friendly control strategies. Biological methods, which basically utilize naturally occurring microorganisms or their enzymes or extracts, have been confirmed to have fewer food safety problems and environmental impacts compared to chemical methods. Biological control methods are also promising because they are very specific for specific toxins. Over the last three decades, numerous investigations have been conducted to explore potential biological control agents (e.g., fungi, bacteria, enzymes, and proteins) that can reduce mycotoxin levels either by inhibiting fungal growth and/or proliferation and subsequent mycotoxin production, or by degrading (transforming) them into harmless metabolic products.
The application of atoxigenic A. flavus is now becoming a widely applicable biocontrol mechanism. The effect is achieved by applying naturally occurring competitive native atoxigenic strains of A. flavus to the soil [93]. Atoxigenic A. flavus strains interfere with the proliferation of indigenous toxigenic strains [13][94][95][96][97]. Atoxigenic strains that are inoculated in the soil have been shown to have a carry-over effect that may inhibit peanut contamination during storage [98], which makes the method more acceptable because it may reduce AF contamination during both preharvest and postharvest. Several countries (USA, Italy, Argentina, Nigeria, Australia, and Thailand) are either developing or already using this native biocontrol agent widely [13][94][95][96][97]. In doing so, they have achieved significant levels of AF reduction (43–98%). Several atoxigenic strains of A. flavus have been patented, registered, and commercialized. In the USA between 2004 and 2008, the atoxigenic A. flavus strains NRRL 21,882 (active component of Afla-guard®) and AF36 (NRRL 18543) were registered and used [99] widely. Strain K49 (NRRL 30797) was also patented by the USDA [100].
In order to develop sustainable AF biocontrol, the population dynamics and genetic stability of A. flavus populations in the field must be carefully examined. Due to the possibility of recombination with toxigenic strains, atoxigenic A. flavus strains could develop the ability to produce AFs [101]. Therefore, it is critical to assess the frequency of such events in agricultural environments where atoxigenic biocontrol A. flavus has been introduced [102]. Analysis of vegetative compatibility groups (VCGs) is critical, as VCGs are a strong barrier to sexual recombination [103]. Atoxigenic biocontrol isolates selected for use should belong to VCGs that contain only atoxigenic strains and have wide distributions [104], as different VCGs are clonal lineages that differ in many characteristics, including AF-producing ability [105].

9. Conclusions and Recommendations

Historically, mycotoxins, especially AFs, were the most prevalent toxins in China. The incidence of HCC cases due to AF exposure was also among the highest in China compared to other countries. Some regions of China are particularly prone to AF contamination due to the climate and geographical location. However, strong Chinese AF regulations, control measures, such as good agricultural and manufacturing practices that include preventive strategies from preharvest to postharvest, policy implementations, and national HBV vaccinations are yielding encouraging results in terms of reduced AF prevalence and exposure risks. Nonetheless, as revealed in some reports reviewed herein, the prevalence of AFs in some agricultural products is still relatively high compared to the national maximum limits. Thus, there is still a need for extensive surveys of AF contamination in food and foodstuffs as well as human biomarker monitoring in order to improve risk management.
Feasible mechanisms to reduce toxic AF levels throughout the food chain, from farm to storage and processing, are needed. The application of native atoxigenic A. flavus as a biocontrol mechanism is currently being used in different countries, as it is easy to use and environmentally friendly. Soil treatment with atoxigenic strains offers the extra advantage in the carry-over effect of reducing AF contamination that occurs during storage. According to several reports from China, several indigenous atoxigenic A. flavus can be used as biocontrol agents. However, little is known about the potential of these native strains at the experimental level or under field conditions. The few existing studies suggest that these native strains show a promising competitive ability to displace toxigenic strains and reduce AF levels [106][107][108]. Thus, there is a need for more studies to characterize and search for potential AF biocontrol strains of A. flavus and to develop formulations and application techniques for these biocontrol strains in the field. Extensive field trials must be conducted across China in areas where potential AF contamination risks are high. Finally, VCG tests should be conducted to ensure genetic stability of atoxigenic strains and to test for their recurrent efficiency.

This entry is adapted from the peer-reviewed paper 10.3390/toxins13100678

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