Abstract
Aflatoxins are one of the major mycotoxins contaminating food and feed. This study analyses 14 years of notifications on aflatoxins (2010–2023) from the European Union’s Rapid Alert System for Food and Feed (RASFF) to assess contamination risk based on notification counts and the reported aflatoxin levels. The distribution of food and feed in notifications indicates that peanuts (34.4%), pistachios (17.3%) and figs (12.5%) have the highest contamination risk. Among major food–origin combinations, significant differences in the distributions of aflatoxin levels suggest the influence of country-specific factors on contamination patterns. The data also revealed a distinct seasonal peak in notifications on figs from Türkiye in the last quarter of the year, as well as rising trends in median aflatoxin levels over 14 years for figs from Türkiye and pistachios from Iran, with each having a fivefold increase in median levels from 2010 to 2023.
Keywords: aflatoxins, mycotoxins, RASFF notifications, food recalls
1. Introduction
Mycotoxins are the toxic secondary metabolites of fungi [1]. Aflatoxins are a group of 15 to 20 closely related mycotoxins produced by various species of fungi in the genus Aspergillus. The two major species responsible for aflatoxin production in food crops are A. flavus and A. parasiticus [2]. Aflatoxins are carcinogens known to target the liver and are associated with many serious health conditions [3]. The most common forms of aflatoxins are aflatoxin B1, B2, G1 and G2 (denoted as AFB1, AFB2, AFG1 and AFG2, respectively, in this paper). As seen on a chromatographic plate under ultraviolet light, the abbreviations B and G indicate the colours blue and green, and the numbers 1 and 2 indicate the relative migration distance of the compounds [2]. Global food recall data indicate that aflatoxins B and G are found in a wide variety of food and animal feed, especially peanuts, tree nuts, dried fruits, cereal grains, seeds, peppers and spices.
Aflatoxin M1 (AFM1), a metabolic product of AFB1, is found in animal tissues and fluids. When lactating humans and animals feed on food and feed contaminated with AFB1, AFB1 may potentially be converted to AFM1 and excreted in the milk. The conversion of AFB1 to AFM1 is influenced by factors such as genetics, the milking process and environmental conditions [4]. Although there are far fewer recalls globally of food products contaminated with AFM1 compared to recalls due to AFB1, AFM1 in dairy products is a particular concern because infants and young children consume milk daily. It is also known that other forms of aflatoxins, including AFB1 and AFG1, can contaminate dairy products (and human milk) [5]. The International Agency for Research on Cancer (IARC) classifies both AFB1 and AFM1 as Group 1 carcinogens [4].
Examining global food recall records provides valuable insights into how aflatoxins contaminate food supply chains worldwide. The European Union’s Rapid Alert System for Food and Feed (RASFF) provides one of the most comprehensive collections of data on food recalls in the world. Launched in 1979, RASFF enables fast exchange of information on health risks related to food and feed among member countries [6]. Other than countries in the EU, RASFF member countries include countries from the European Economic Area (Iceland, Liechtenstein and Norway), Switzerland and the European Food Safety Authority (EFSA). The number of yearly notifications posted by RASFF has grown from less than 500 notifications in 2000 to more than 4600 notifications in 2023.
Much research on RASFF data has been published in recent years, including analyses of notifications on mycotoxins in specific food [7] and notifications on aflatoxins in food from specific countries of origin [8]. However, prior research on RASFF notifications has largely overlooked the reported aflatoxin levels. By analysing 14 years of RASFF notifications on aflatoxins (2010–2023), the objectives of this study are to identify the food and feed with the highest contamination risk, compare the distributions of the reported aflatoxin levels across major food–origin combinations, and discover temporal trends in notification counts and median aflatoxin levels of food–origins.
2. Materials and Methods
2.1. RASFF Notification Data
Every RASFF notification from 2020 to 2023 has an individual web page that can be viewed on the internet and is searchable from a web portal called RASFF Window [9]. The data are also available for download in Excel and CSV formats from RASFF Window. The downloaded dataset contains a subset of information shown on the web page of each notification. As data on the reported aflatoxin levels are not found in the dataset, we scraped the web page of each notification on aflatoxins to obtain the data.
Pre-2020 notifications, except the few which have been updated since 2020, are not searchable from RASFF Window and are not available for viewing on the internet. Older data from 1979 to 2019 are available for download from the EU’s European Data Portal [10]. Similar to the 2020–2023 dataset, this pre-2020 dataset contains a subset of the complete information in each notification. However, it includes data on the reported aflatoxin levels.
2.2. Data Processing and Analysis
The reported levels required careful cleaning to ensure accuracy. Units of measurement were removed, and commas used in decimal values were replaced by decimal points. In many notifications, multiple levels were reported, indicating multiple samples collected or multiple lab tests performed. Due to recording errors and the inconsistent format of the reported results, it was not clear in a small number of notifications if a reported value referred to AFB1 or the sum of AFB1, AFB2, AFG1 and AFG2. For cases reported in 2020–2023 notifications, we manually checked the web page of each notification. If there was no clear indication on the web page, we assumed the value to be the AFB1 level. Most reported levels also indicate the uncertainty in measurement (e.g., 8.9 ± 2.3). These were all removed. Notifications with ambiguously recorded levels were excluded from this study.
Some notifications had multiple countries of origin. These notifications were on food or feed processed or packaged in one country using raw commodities produced in another country. Although contamination may occur during processing or packaging, we took the origin to be the country of production of the raw commodity.
All data processing and analysis were performed using programs written in Python version 3.8.8. Medians were calculated using the median function in NumPy version 1.20.1. The Kruskal–Wallis H test [11] and the Mann–Whitney U test [12] from SciPy version 1.6.2 were used for tests of differences in the distributions of aflatoxin levels of food origins. Significance levels were adjusted using the Bonferroni correction where appropriate. All charts were plotted using Microsoft Power BI version 2.129.905.0.
3. Results
Before studying the reported aflatoxin levels, it is informative to investigate the prevalence of aflatoxin contamination in food and feed. The distribution of food and feed in notifications on aflatoxins from 2010 to 2023 provides an estimation of the risk of aflatoxin contamination in food or feed commodities. For dairy products, we present the reported AFM1 levels in notifications from 2010 to 2023. For other food products, we present and analyse the reported AFB1, AFB2, AFG1 and AFG2 levels in notifications from 2020 to 2023.
3.1. RASFF Notifications by Mycotoxin Type (2010–2023)
The EU has established maximum limits for six major mycotoxins (aflatoxins, ochratoxin A, deoxynivalenol, fumonisins, patulin and zearalenone) and their associated food commodities [13]. Many of the food commodities in notifications on aflatoxins have established maximum limits. Table 1 shows the number of notifications by mycotoxin type from 2010 to 2023.
Table 1.
Number of notifications on mycotoxins (2010–2023). Data used with permission from Refs. [9,10]. 2025, European Commission.
| Mycotoxin | Number of Notifications |
|---|---|
| Aflatoxins | 6363 |
| Ochratoxin A | 674 |
| Aflatoxins and Ochratoxin A | 71 |
| Deoxynivalenol | 60 |
| Fumonisins | 48 |
| Patulin | 20 |
| Zearalenone | 8 |
| Aflatoxins and Fumonisins | 6 |
| Deoxynivalenol and Zearalenone | 6 |
| Ochratoxin A and Deoxynivalenol | 2 |
| Aflatoxins and Tenuazonic Acid | 1 |
| Aflatoxins and Zearalenone | 1 |
| Deoxynivalenol and Fumonisins | 1 |
| Other mycotoxins 1 | 16 |
| Total | 7277 |
1 Citrinin, Lolitrem B, Alternariol, Tenuazonic Acid, T-2, HT-2.
There were 7277 notifications on mycotoxins, of which 6442 (88.5%) concerned aflatoxins. In 79 notifications on aflatoxins, other mycotoxins were also detected. Aflatoxins and ochratoxin A were both reported in 71 notifications, contaminating fruits (dates, figs, etc.), nuts (peanuts, pistachios), cereal grains (corn, rice), spices (chili peppers, nutmegs, paprika, etc.) and melon seeds. Aflatoxins and fumonisins were both reported in six notifications on corn. Aflatoxins and zearalenone were both reported in one notification on rice. Aflatoxins and tenuazonic acid were both reported in one notification on dried figs.
Other mycotoxins (other than aflatoxins and ochratoxin A) were detected in a small basket of food types. Deoxynivalenol was detected in cereal grains (corn, wheat, etc.); fumonisins were detected in corn and peanuts; zearalenone was detected in rice and wheat; patulin was detected in apple juice and paste; and alternaria mycotoxins (alternariol, tenuazonic acid) were detected in tomato products.
3.2. Distribution of Food and Feed in RASFF Notifications on Aflatoxins (2010–2023)
Figure 1 shows the yearly number of notifications in ten food and feed categories from 2010 to 2023: animal feed, dairy products, fruits, cereal grains, seeds, peppers and spices, peanuts, pistachios, other tree nuts and other food. Pistachios are presented separately from other tree nuts due to the large number of notifications. The last category (“other food”) contains mainly processed products made from multiple raw commodities. We observe rising trends (2014–2018, 2020–2022) and falling trends (2010–2013, 2018–2020) in the yearly number of notifications.
Figure 1.
Yearly number of notifications by food and feed commodity type (2010–2023). Data used with permission from Refs. [9,10]. 2025, European Commission.
Table 2 shows the number of notifications for food and feed in two separate periods (2010–2019 and 2020–2023). From 2010 to 2023, there were a total of 6442 notifications on aflatoxins, of which 498 notifications were on animal feed. The two most common raw materials in animal feed were peanuts (384 notifications) and corn (59). Other feed materials were sunflower seeds (19), rice (7) and a variety of other commodities (29), such as millet, sorghum, soybeans, cottonseeds and coconuts.
Table 2.
Number of aflatoxin notifications for food and feed (2010–2023). Data used with permission from Refs. [9,10]. 2025, European Commission.
| Category | Commodity or Product | Number of Notifications 2010–2019 |
Number of Notifications 2020–2023 |
Total |
|---|---|---|---|---|
| Animal feed | Peanut feed | 343 | 41 | 384 |
| Corn feed | 49 | 10 | 59 | |
| Sunflower feed | 15 | 4 | 19 | |
| Rice feed | 4 | 3 | 7 | |
| Others (compound feed, etc.) | 21 | 8 | 29 | |
| Dairy products |
Cheese | 3 | 1 | 4 |
| Milk, other products | 10 | 1 | 11 | |
| Fruits | Figs | 603 | 202 | 805 |
| Dates | 2 | 8 | 10 | |
| Mulberries | 0 | 3 | 3 | |
| Cereal grains | Rice | 67 | 91 | 158 |
| Corn | 30 | 15 | 45 | |
| Millet | 2 | 4 | 6 | |
| Buckwheat | 1 | 3 | 4 | |
| Wheat | 0 | 2 | 2 | |
| Barley | 1 | 0 | 1 | |
| Spelt | 0 | 1 | 1 | |
| Seeds | Melon seeds | 77 | 21 | 98 |
| Apricot kernels | 14 | 2 | 16 | |
| Sesame seeds | 3 | 7 | 10 | |
| Ogbono seeds | 7 | 2 | 9 | |
| Sunflower seeds | 7 | 1 | 8 | |
| Chia seeds | 6 | 1 | 7 | |
| Lotus seeds | 1 | 1 | 2 | |
| Flaxseeds | 0 | 1 | 1 | |
| Peppers and spices | Peppers | 247 | 33 | 280 |
| Nutmegs | 123 | 28 | 151 | |
| Ginger | 27 | 4 | 31 | |
| Turmeric | 13 | 7 | 20 | |
| Paprika | 15 | 1 | 16 | |
| Peppercorns (black, white) | 1 | 2 | 3 | |
| Cumin | 2 | 0 | 2 | |
| Mixed spices | 76 | 17 | 93 | |
| Peanuts and tree nuts | Peanuts | 1683 | 536 | 2219 |
| Pistachios | 842 | 273 | 1115 | |
| Hazelnuts | 315 | 91 | 406 | |
| Almonds | 149 | 57 | 206 | |
| Brazil nuts | 24 | 7 | 31 | |
| Chestnuts | 8 | 1 | 9 | |
| Cashew nuts | 5 | 2 | 7 | |
| Walnuts | 6 | 1 | 7 | |
| Pecans | 5 | 0 | 5 | |
| Pine nuts | 5 | 0 | 5 | |
| Mixed nuts or unspecified | 15 | 2 | 17 | |
| Other food | Processed products | 85 | 27 | 112 |
| Vegetables | 7 | 1 | 8 | |
| Total | - | 4919 | 1523 | 6442 |
The top three food commodity types were peanuts (2219), tree nuts (1808) and fruits (818 notifications, of which 805 notifications were on figs). Peanuts and peanut products had the most notifications every year. There were 70 notifications on peanut butter and peanut paste, and 14 notifications on peanut powder and peanut flour.
Aflatoxins contaminated nine different tree nuts, but 95.5% of the notifications on tree nuts concerned pistachios, almonds and hazelnuts. Pistachio was the leading tree nut, with 1115 notifications. The number of notifications on other tree nuts varied significantly, led by hazelnuts (406), almonds (206) and Brazil nuts (31). The other types of tree nuts (chestnuts, cashew nuts, walnuts, pecans and pine nuts) had less than 10 notifications each. There were 17 notifications on mixed or unspecified nuts.
RASFF data indicate that dried fruits such as dried figs, dried dates and raisins are particularly vulnerable to aflatoxin contamination. Of the 805 notifications on figs, 783 notifications were specified as dried figs, and 13 notifications were on fig paste. Other than figs, the only other types of fruits were dates (10) and mulberries (3). Seven notifications on dates concerned processed dates (dried, pitted, diced or in syrup form).
The data indicate that aflatoxins contaminate a wide range of peppers and spices. Notifications on peppers were predominantly on chili peppers (257). A total of 42 notifications on peppers were specified as dried peppers, and 183 notifications were on peppers in ground or crushed form. A total of 93 notifications on spices were specified as mixed spices. These include common spice mixes such as curry and kebab spices. For individual spice types, there were many notifications on nutmegs (151) and a smaller number of notifications on ginger (31), turmeric (20), paprika (16), black and white peppercorns (3) and cumin (2).
The data indicate that cereal grains are at risk from most mycotoxins. For aflatoxins, rice and corn (including rice flour and corn flour) were the most common cereal grains, with 158 and 45 notifications, respectively. Other cereal grains were millet (6), buckwheat (4), wheat (2), barley (1) and spelt (1).
Eight types of oilseeds and fruit seeds were found in notifications on aflatoxins, led by melon seeds, with 98 notifications. Other seeds were apricot kernels (16), sesame seeds (10), ogbono seeds (9), sunflower seeds (8), chia seeds (7), lotus seeds (2) and flaxseeds (1).
Lastly, there were 120 notifications that we classified as “other food”. These concerned food that does not belong to any of the other nine categories, such as beans and tiger nuts, and prepared or processed food such as sauces, seasonings, snacks and food for infants. Many of these food products contain peanuts, tree nuts, fruits or cereal grains as ingredients.
3.3. AFM1 Levels in Dairy Products (2010–2023)
There were 15 notifications on AFM1 in dairy products from 2010 to 2023: milk (10 notifications), cheese (four) and whey (one) (Table 3). Notably, eight of the notifications on milk were on raw milk. All products originated from Europe (Hungary, Italy, Serbia and Slovenia). The reported levels in 14 notifications on milk and cheese ranged from 0.063 µg/kg to 0.87 µg/kg, all exceeding the EU’s regulatory maximum levels of 0.05 µg/kg (for raw milk, heat-treated milk and milk used for the manufacture of milk-based products) and 0.025 µg/kg (for formula milk) [13].
Table 3.
AFM1 levels in dairy products (2010–2023). Data used with permission from Refs. [9,10]. 2025, European Commission.
| Product | Number of Notifications |
AFM1 (µg/kg) | n 1 | Remarks | ||
|---|---|---|---|---|---|---|
| Median | Min | Max | ||||
| Raw milk | 8 | 0.10 | 0.063 | 0.214 | 6 | No AFM1 results were reported in 5 notifications. |
| Milk | 2 | 0.15 | 0.152 | 0.152 | 1 | |
| Cheese | 4 | 0.24 | 0.07 | 0.87 | 6 | |
| Whey | 1 | - | - | - | 0 | |
| Total | 15 | - | - | - | 13 | |
1 n is the sample size, i.e., the number of levels reported in the notifications.
3.4. AFB1, AFB2, AFG1, AFG2 Levels in Food Commodities (2020–2023)
Considering that the countries of origin of some food commodities imported into Europe may have changed significantly since 2010, the notifications in the most recent years provide more relevant information for assessing current origin-specific risks. We therefore focused our analysis on the levels reported in notifications from 2020 to 2023.
Due to differences in sample sizes (i.e., the number of levels reported) for different food commodities and the presence of extremely high levels in a few samples, we present the median levels (rather than mean levels) for all food commodities. Table 4 presents the median, minimum and maximum levels of AFB1 and the sum of AFB1, AFB2, AFG1 and AFG2 for each food commodity or product.
Table 4.
AFB1, AFB2, AFG1, AFG2 levels in food commodities (2020–2023). Data used with permission from Refs. [9,10]. 2025, European Commission.
| Category | Commodity or Product | AFB1 (µg/kg) | Sum of AFB1, AFB2, AFG1 and AFG2 (µg/kg) | ||||||
|---|---|---|---|---|---|---|---|---|---|
| Median | Min | Max | n 1 | Median | Min | Max | n 1 | ||
| Fruits | Figs | 18.0 | 1.0 | 822.0 | 188 | 27.0 | 0.49 | 540.0 | 186 |
| Dates | 3.85 | 2.6 | 70.0 | 12 | 62.0 | 12.0 | 73.0 | 3 | |
| Mulberries | 6.6 | 6.2 | 8.3 | 3 | 9.35 | 9.35 | 9.35 | 1 | |
| Cereal grains | Rice | 6.9 | 0.21 | 48.0 | 102 | 13.5 | 1.4 | 122.5 | 42 |
| Corn | 7.8 | 2.74 | 44.0 | 19 | 9.45 | 5.1 | 49.0 | 12 | |
| Millet | 6.95 | 5.7 | 8.2 | 4 | 8.4 | 6.2 | 9.5 | 4 | |
| Buckwheat | 15.78 | 4.3 | 32.7 | 4 | 17.0 | 6.1 | 38.0 | 4 | |
| Wheat | 8.6 | 8.6 | 8.6 | 1 | 8.6 | 8.6 | 8.6 | 1 | |
| Barley | - | - | - | 0 | - | - | - | 0 | |
| Spelt | 3.7 | 3.7 | 3.7 | 1 | 11.3 | 11.3 | 11.3 | 1 | |
| Seeds | Melon seeds | 10.2 | 3.3 | 79.3 | 16 | 13.05 | 7.9 | 88.2 | 16 |
| Apricot kernels | 58.0 | 9.4 | 80.5 | 4 | 77.35 | 17.7 | 110.0 | 4 | |
| Sesame seeds | 6.7 | 3.9 | 38.0 | 7 | 12.2 | 6.7 | 15.3 | 4 | |
| Ogbono seeds | 12.15 | 9.3 | 15.0 | 2 | 20.85 | 9.7 | 32.0 | 2 | |
| Sunflower seeds | 3.5 | 3.5 | 3.5 | 1 | 9.3 | 9.3 | 9.3 | 1 | |
| Chia seeds | 6.1 | 4.3 | 7.9 | 2 | 10.0 | 10.0 | 10.0 | 1 | |
| Lotus seeds | 12.0 | 12.0 | 12.0 | 1 | - | - | - | 0 | |
| Flaxseeds | 5.9 | 4.1 | 7.7 | 2 | 7.8 | 5.1 | 10.5 | 2 | |
| Peppers and spices | Peppers | 12.6 | 6.9 | 299.0 | 33 | 20.25 | 10.0 | 356.2 | 14 |
| Nutmegs | 22.0 | 7.09 | 170.0 | 33 | 26.8 | 8.6 | 220.0 | 27 | |
| Ginger | 12.8 | 6.7 | 31.0 | 4 | 31.25 | 14.8 | 38.4 | 4 | |
| Turmeric | 10.7 | 9.2 | 15.5 | 7 | 14.9 | 14.9 | 14.9 | 1 | |
| Paprika | 8.3 | 8.3 | 8.3 | 1 | - | - | - | 0 | |
| Peppercorns (black, white) | 12.1 | 9.5 | 14.7 | 2 | 20.1 | 20.1 | 20.1 | 1 | |
| Cumin | - | - | - | 0 | - | - | - | 0 | |
| Mixed spices | 10.0 | 6.6 | 26.8 | 15 | 18.0 | 12.6 | 78.8 | 7 | |
| Peanuts and tree nuts | Peanuts | 12.0 | 0.5 | 407.0 | 631 | 22.0 | 0.6 | 480.0 | 499 |
| Pistachios | 29.9 | 1.7 | 1064.0 | 289 | 34.8 | 3.1 | 1170.0 | 286 | |
| Hazelnuts | 17.4 | 2.8 | 489.2 | 84 | 29.5 | 2.8 | 562.0 | 85 | |
| Almonds | 16.8 | 0.2 | 420.0 | 71 | 23.1 | 2.0 | 466.0 | 67 | |
| Brazil nuts | 15.0 | 7.7 | 80.3 | 6 | 27.5 | 11.1 | 167.0 | 6 | |
| Chestnuts | 4.3 | 4.3 | 4.3 | 1 | 7.7 | 7.7 | 7.7 | 1 | |
| Cashew nuts | 31.7 | 31.7 | 31.7 | 1 | 41.75 | 9.6 | 73.9 | 2 | |
| Walnuts | 31.85 | 3.9 | 59.8 | 2 | 45.1 | 5.1 | 85.1 | 2 | |
| Pecans | - | - | - | 0 | - | - | - | 0 | |
| Pine nuts | - | - | - | 0 | - | - | - | 0 | |
| Mixed nuts or unspecified | 32.2 | 32.2 | 32.2 | 1 | 36.1 | 36.1 | 36.1 | 1 | |
| Other food | Processed products | 13.87 | 0.28 | 139.0 | 26 | 15.4 | 4.3 | 158.0 | 19 |
| Vegetables | 7.8 | 7.8 | 7.8 | 1 | 13.2 | 13.2 | 13.2 | 1 | |
1 n is the sample size, i.e., the number of levels reported in the notifications.
3.5. AFB1, AFB2, AFG1, AFG2 Levels in Food Commodities by Country of Origin (2020–2023)
As the number of notifications and reported levels were very low for many food commodities, we focused on six major food commodities (figs, rice, peanuts, pistachios, hazelnuts and almonds) and their major countries of origins. Table 5 presents the country-specific aflatoxin levels of the six major food commodities. Each food commodity had at least 50 notifications, and each country of origin had at least 10 notifications from 2020 to 2023. Box plots showing the distributions of aflatoxin levels of the food–origins in Table 5 are presented in Figure S1.
Table 5.
AFB1, AFB2, AFG1, AFG2 levels of major food–origins (2020–2023). Data used with permission from Refs. [9,10]. 2025, European Commission.
| Commodity | Country of Origin | No. of Notifications |
AFB1 (µg/kg) | Sum of AFB1, AFB2, AFG1 and AFG2 (µg/kg) | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Median | Min | Max | n 1 | Median | Min | Max | n 1 | |||
| Figs | Türkiye | 192 | 17.8 | 1.0 | 822.0 | 178 | 27.5 | 0.49 | 540.0 | 176 |
| Rice | Pakistan | 66 | 7.2 | 0.5 | 48.0 | 73 | 13.5 | 1.4 | 122.5 | 38 |
| India | 10 | 4.2 | 3.0 | 24.0 | 11 | 27.0 | 27.0 | 27.0 | 1 | |
| Peanuts | USA | 128 | 11.6 | 0.5 | 407.0 | 136 | 20.0 | 3.2 | 480.0 | 103 |
| Egypt | 115 | 25.5 | 3.32 | 320.0 | 146 | 34.4 | 0.6 | 370.0 | 133 | |
| Argentina | 100 | 6.45 | 2.1 | 110.0 | 116 | 13.0 | 2.4 | 140.0 | 85 | |
| India | 89 | 11.5 | 2.82 | 260.0 | 104 | 22.0 | 4.5 | 270.0 | 73 | |
| China | 25 | 12.2 | 2.4 | 107.7 | 29 | 24.0 | 4.3 | 122.9 | 25 | |
| Bolivia | 19 | 23.0 | 4.1 | 300.0 | 28 | 59.55 | 8.6 | 350.0 | 22 | |
| Pistachios | Iran | 111 | 35.55 | 9.7 | 1064.0 | 116 | 42.36 | 13.0 | 1170.0 | 114 |
| Türkiye | 74 | 25.04 | 1.7 | 225.0 | 75 | 27.5 | 3.1 | 309.0 | 76 | |
| USA | 68 | 29.7 | 7.9 | 240.0 | 78 | 33.05 | 8.7 | 260.0 | 78 | |
| Hazelnuts | Georgia | 57 | 18.02 | 5.9 | 489.2 | 50 | 31.6 | 12.2 | 562.0 | 53 |
| Azerbaijan | 21 | 28.5 | 6.9 | 320.0 | 22 | 44.25 | 11.01 | 370.0 | 22 | |
| Türkiye | 12 | 8.3 | 2.8 | 46.0 | 11 | 20.3 | 2.8 | 51.0 | 9 | |
| Almonds | USA | 25 | 16.8 | 0.2 | 277.0 | 29 | 24.0 | 13.2 | 302.0 | 24 |
| Australia | 17 | 14.7 | 0.5 | 50.0 | 29 | 21.4 | 2.0 | 125.0 | 25 | |
1 n is the sample size, i.e., the number of levels reported in the notifications.
Tests of differences in the distributions of aflatoxin levels of the food–origins indicate significant differences. The results of the Kruskal–Wallis H tests for peanuts, pistachios and hazelnuts (each with more than two major countries of origins) are presented in Tables S1 and S2. The results of the Mann–Whitney U tests for pairwise comparisons are presented in Tables S3 and S4. Non-transitive inconsistencies in the test results are possibly due to unequal sample sizes and outliers.
3.6. Trends in AFB1, AFB2, AFG1, AFG2 Levels of Food-Origins (2010–2023)
We plotted the yearly median levels from 2010 to 2023 for the food–origins in Table 5 to study long-term trends in aflatoxin levels. The plots for figs from Türkiye and pistachios from Iran show rising trends over 14 years (Figure 2). For both food–origins, there were fivefold increases in median levels from 2010 to 2023.
Figure 2.
(a) Yearly median levels for figs from Türkiye (2010–2023); (b) yearly median levels for pistachios from Iran (2010–2023). Data used with permission from Refs. [9,10]. 2025, European Commission.
For figs from Türkiye (Figure 2a), the median AFB1 increased from 4.2 µg/kg in 2010 (sample size n = 83) to 23.3 µg/kg in 2023 (n = 25), while the median sum of AFB1, AFB2, AFG1 and AFG2 increased from 7.7 µg/kg in 2010 (n = 76) to 39.2 µg/kg in 2023 (n = 30).
For pistachios from Iran (Figure 2b), there were sharp increases in median levels from 2010 to 2011 and from 2022 to 2023, resulting in an increase in the median AFB1 from 11.1 µg/kg in 2010 (n = 114) to 57.3 µg/kg in 2023 (n = 23) and in an increase in the median sum of AFB1, AFB2, AFG1 and AFG2 from 12.4 µg/kg in 2010 (n = 113) to 62.6 µg/kg in 2023 (n = 23).
4. Discussion
4.1. Factors Influencing Aflatoxin Production
Aflatoxin production in food and feed is influenced by many factors in the environment of the fungi. Factors shown to enhance or reduce aflatoxin production include the availability of water (which is essential for both fungal growth and aflatoxin production), temperature, radiation, the nutrients in the crop, the presence of bacteria and the presence of many chemical compounds, such as organic solvents and pesticides [2]. Many of these factors affect all stages of the food chain. For instance, dried fruits are at risk during pre-harvest, from the moment the fruit tree bears fruit to post-harvest, when fruits are processed, transported and stored. Likely factors influencing aflatoxin production in dried fruits include the additional time spent in drying and processing the fruits after harvest and the likelihood of longer storage before consumption [14].
Various studies over recent decades [15] have indicated that climate is a factor in aflatoxin production. The Food and Agriculture Organization (FAO) of the United Nations and the European Food Safety Authority (EFSA) have identified aflatoxins as one of the foodborne hazards most likely to be impacted by climate change [16,17].
4.2. Correlation Between Import Quantity and Number of Notifications of Food–Origins
Import quantity tends to correlate with the number of notifications. For example, Türkiye is the largest source of figs for RASFF member countries, accounting for 71.6% of dried fig imports from 2010 to 2023 [18]. This correlated with the large number of notifications on figs from Türkiye (96.1% of notifications on figs from 2010 to 2023). In the last two decades, the import of pistachios from Iran to RASFF member countries fell from 54.1% of total pistachio imports in 2000 to 4.6% in 2023 [18]. Iran accounted for most of the notifications on pistachios before 2009, with over 400 notifications per year from 2003 to 2005. Europe’s reduced dependence on Iran for pistachios correlated with a sharp decrease in notifications on pistachios from Iran after 2005. This reduced the overall number of notifications on pistachios from more than 500 notifications in 2003 to fewer than 100 notifications in most of the years since 2011.
However, a disproportionately large number of notifications on some food–origins suggests underlying country-specific factors influencing aflatoxin contamination. For example, Pakistan was the fourth largest source of rice, accounting for 9.5% of rice imports from 2020 to 2023 [18]. However, there were more notifications on rice from Pakistan (66) than from all other countries of origin combined (25).
4.3. Seasonal Trends in Number of Notifications of Food–Origins
The RASFF data from 2010 to 2023 showed a distinct seasonal trend in the number of notifications on figs from Türkiye (Figure S2), with spikes in notifications during the fourth quarter of most of the years. The plot of the distribution of notification counts by month over 14 years shows low notification counts from February to September, followed by sharp increases from October to January (Figure S3a). This trend may be associated with the yearly growing season of figs, which depends on climate. For Turkish figs, the main yearly harvest occurs around August. Aydin Province in western Türkiye is the dominant region for the production of dried figs [19]. A lag between harvesting and the dates of notifications is expected due to the time required for processing, exporting, sampling and testing of dried figs. We also observed decreasing trends, followed by increases in notifications in the last quarter of the year for pistachios and hazelnuts from Türkiye (Figure S3b,c). For hazelnuts from Georgia (Figure S3d) and Azerbaijan (Figure S3e), where the climate is similar to that of Türkiye, notification counts were also very low during summer months before increasing in the final four months of the year. The similar trends observed for Türkiye, Georgia and Azerbaijan suggest an association between climate and notification counts. The summer conditions in July and August may have an influence on aflatoxin contamination in crops, leading to higher detection rates in the final three to four months of the year.
4.4. Aflatoxin Levels of Food–Origins (2020–2023)
The significant differences in aflatoxin levels between some food–origins suggest that contamination levels may be influenced by country-specific factors. Although climate and other natural environmental factors may be influential, man-made factors related to farming practices and regulatory controls can also have an impact. For example, as the climate of Türkiye and Azerbaijan is quite similar, the significantly higher levels reported for hazelnuts from Azerbaijan could be due to man-made country-specific factors.
Figure 2 shows a rising trend and a fivefold increase in yearly median levels over 14 years for figs from Türkiye and pistachios from Iran. This may be an indication of the increasing risk to the safety of figs and pistachios from Türkiye and Iran, respectively. The EU reviews its food safety regulations for specific country–food–hazards at regular intervals (not exceeding six months) based on RASFF data and other information. It implements temporary changes of official controls and emergency measures for countries showing increasing non-compliance. The measures include increasing the frequency of checks and sampling, requirement of an official certificate from the country of origin proving compliance by stating results of sampling, and suspension of entry into the EU [20]. The EU has implemented these measures for dried figs from Türkiye and pistachios from Iran since 2019 [20,21]. The observed rising trends suggest that the measures have not produced the desired effect.
5. Conclusions
Historical RASFF notifications provide quantitative evidence for identifying high-risk food products and prevalent contaminants. Studying long-term trends in RASFF notifications for specific food–origins helps the EU in evidence-based risk assessment and management of food–origins, informing decisions on import controls. The distribution of food and feed in notifications from 2010 to 2023 indicates that certain food commodities (peanuts, pistachios, hazelnuts, almonds, figs, rice, melon seeds, peppers and nutmegs) have a higher risk of aflatoxin contamination. Peanuts, pistachios and figs, with 34.4%, 17.3% and 12.5% of all notifications, respectively, have the highest risk. Significant differences in the distributions of aflatoxin levels between food–origins suggest country-specific factors influencing aflatoxin contamination. RASFF data also revealed a distinct seasonal trend in notifications on figs from Türkiye, with yearly spikes in notifications in the last quarter of most years. A fivefold increase in median levels over 14 years for figs from Türkiye and pistachios from Iran are a concern for the EU, as both countries are major import sources.
Monitoring trends in RASFF notifications and learning from EU’s risk management measures may help countries outside of Europe assess aflatoxin risk and make informed decisions on import sources, particularly small countries that may not be able to conduct enough testing if import quantities are much smaller.
Acknowledgments
The authors would like to thank the European Commission for providing the data required for this research.
Abbreviations
The following abbreviations are used in this manuscript:
| RASFF | Rapid Alert System for Food and Feed |
| EU | European Union |
| EC | European Commission |
| AFM1 | Aflatoxin M1 |
| AFB1 | Aflatoxin B1 |
| AFB2 | Aflatoxin B2 |
| AFG1 | Aflatoxin G1 |
| AFG2 | Aflatoxin G2 |
Supplementary Materials
The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/foods14183250/s1. Table S1: Kruskal–Wallis H test results for comparisons of the distributions of AFB1 levels across food–origins (2020–2023); Table S2: Kruskal–Wallis H test results for comparisons of the distributions of sums of the AFB1, AFB2, AFG1 and AFG2 levels across food–origins (2020–2023); Table S3: Mann–Whitney U test results for pairwise comparisons of the distributions of AFB1 levels across food–origins (2020–2023); Table S4: Mann–Whitney U test results for pairwise comparisons of the distributions of sums of the AFB1, AFB2, AFG1 and AFG2 levels across food–origins (2020–2023); Figure S1: Distributions of aflatoxin levels across food–origins (2020–2023); Figure S2: Quarterly notification counts of figs from Türkiye (2010–2023); Figure S3: Distributions of monthly notification counts by food–origin (2010–2023).
Author Contributions
Conceptualization, R.K., B.E. and K.T.A.; methodology, R.K. and B.E.; software, R.K.; validation, R.K.; formal analysis, R.K.; investigation, R.K.; resources, R.K.; data curation, R.K.; writing—original draft preparation, R.K.; writing—review and editing, R.K., B.E. and K.T.A.; visualization, R.K.; supervision, B.E., K.T.A., J.K. and J.S.H.C.; project administration, K.T.A., J.K. and J.S.H.C.; funding acquisition, K.T.A., J.K. and J.S.H.C. All authors have read and agreed to the published version of the manuscript.
Institutional Review Board Statement
Not applicable.
Informed Consent Statement
Not applicable.
Data Availability Statement
The 2020–2023 RASFF data used in this study are available for download from the RASFF website (https://webgate.ec.europa.eu/rasff-window/screen/search (accessed on 22 May 2025)). Older 2000–2019 data are available for download from the EU’s European Data Portal (https://data.europa.eu/en (accessed on 16 February 2024)). Food trade data are available from the FAOSTAT Food and Agriculture Data website (https://www.fao.org/faostat/en/ (accessed on 26 May 2025)).
Conflicts of Interest
The authors declare no conflicts of interest.
Funding Statement
This research was supported by the Singapore Food Agency.
Footnotes
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The 2020–2023 RASFF data used in this study are available for download from the RASFF website (https://webgate.ec.europa.eu/rasff-window/screen/search (accessed on 22 May 2025)). Older 2000–2019 data are available for download from the EU’s European Data Portal (https://data.europa.eu/en (accessed on 16 February 2024)). Food trade data are available from the FAOSTAT Food and Agriculture Data website (https://www.fao.org/faostat/en/ (accessed on 26 May 2025)).