A Scoping Review of Mycotoxin Contamination of Maize and Other Grains in South Africa

Despite global legislative and regulatory efforts to enhance food safety, mycotoxins remain a recurring challenge (1) in staple foods such as maize and other locally produced cereals (2) in South Africa. The country is regarded as “a food secure nation”, however, Statistics South Africa (3) and the South African National Health and Nutrition Examination Survey (SANHANES-1) indicated a high level of food insecurity at household level (4). This situation is common with maize (Zea mays), the main staple household food and animal feed (5) in the country. Like many other food commodities, maize produced for human and animal consumption should be safe and supplied in sufficient quantities (1). Therefore, fungal infections and the production of associated secondary metabolites, e.g., mycotoxins, have profound effects on maize farming and downstream activities (1).

Mycotoxin-producing fungi belong mainly to the genera Aspergillus, Alternaria, Claviceps, Fusarium, Penicillium, and Stachybotrys, which are common contaminants of maize (2, 6). Some mycotoxins are immunosuppressive, carcinogenic, nephrotoxic, and neurotoxic in both animals and humans (1, 7-9). For example, according to Grace et al. (10), over 9000 cases of liver cancer per annum, stunting, and immune suppressions in children (11) have been associated with AF exposures. Primarily, mycotoxin effects vary based on the type of mycotoxin, level, and duration of exposure as well as age, sex, and health status of exposed individuals (12). Direct exposure is mainly through ingestion of contaminated food or inhalation of fungal spores and dust particles containing the toxin (13). Indirectly, mycotoxins are consumed via the dermal or maternal (umbilical cord and breast milk) route (13), and cereals together with nuts are reported as the major source of dietary exposure to mycotoxins (14).

Several outbreaks of mycotoxicosis among humans and animals have been reported in South Africa. In 2001, in a primary school nutrition programme (PSNP) in the Eastern Cape, children were hospitalized after consumption of peanut butter highly contaminated with aflatoxins (AFs) (15). In another mycotoxin-related disease outbreak, Arnot et al. (16) reported the death of over 220 dogs in the Gauteng province after the consumption of pet food contaminated with high concentrations of AF. Similarly, nephropathy in pigs was reported in South Africa, with a combination of ochratoxin A (OTA) and FB1 having concentration levels of 67 - 251 µg/kg and 5021 - 5289 µg/kg, respectively, as well as penicillic acid (PA) at 149 - 251 µg/kg (17). Mycotoxins have, therefore, been considered as significant contaminants of food, which carry a high burden (both in morbidity and mortality) in South Africa (17-19).

Studies conducted in South Africa showed that FB is the most common mycotoxin group affecting maize and maize products (20-23). Other mycotoxins, including AFs, OTs, zearalenone (ZEA), and trichothecenes, are also common, though recovered at low concentrations (24, 25). Favorable climatic conditions are likely to increase fungal colonization that causes increased quantities of mycotoxins in maize and other foodstuffs (2, 26), which in turn exacerbate health and economic consequences.

This scoping review summarizes available data on mycotoxin contamination of maize, maize-based products, and other cereals. The aim is for understanding, informing, and enhancing protection against fungal contamination in South Africa, responsible for producing these products in sub-Saharan Africa.

This study describes the type of grains, particularly maize and products associated with mycotoxin contamination, the province where the cereals were obtained as well as the type and concentration of mycotoxins. Mycotoxins in maize and other cereals were confirmed in eight provinces (Table 1). These metabolites included deoxynivalenol (DON), nivalenol (NIV), FB, AF, ZEA, OTA, and patulin (PAT). The most common group of mycotoxins found across all investigated provinces was FB, followed by the AF. Maize only was confirmed to be affected by five (FB, AF, DON, OTA, ZEA) of the mycotoxin identified in South Africa. In a recent research on the South African perspective on the mycotoxin status of commercial maize and wheat crop annually produced, AFB1 was seldom present in commercial maize. In the same report, DON and FB were the most prevalent mycotoxins in all provinces that produce white and yellow maize (29).

This scoping review highlights the importance of mycotoxin contamination and that it remains a serious concern for producers and consumers of maize and related cereal food products in the country. The high prevalence of mycotoxigenic fungi can be attributed to the limitations related to storage, particularly in urban areas. As shown in Table 1, maize is a major source of human dietary exposure to mycotoxins in South Africa, with implications in Africa, since the country is a major supplier to other countries on the African continent. Only a few studies have reported contamination of other cereals such as wheat (Triticum aestivum), barley (Hordeum vulgare), and sorghum (Sorghum bicolor) in this country, which can be attributed to these foods not commonly consumed in most parts of South Africa.

Maize is predominantly contaminated by Fusarium spp., especially F. graminearum, F. culmorum, F. verticillioides, F. proliferatum, and F. anthophilum. These are important fungal species that are the principal producers of mycotoxins, including FB, AF, and DON (38, 45). The high prevalence of mycotoxin production in provinces like Kwazulu-Natal, Gauteng, and Free State (Table 1) can be attributed to hot, dry, and humid climates. In this study, FBs (especially FB₁) were the most common mycotoxin, followed by DON and AFs (Table 1). High FB levels was mostly present in home-grown maize.

This was confirmed in the Eastern Cape Province with levels as high as 1.4 × 108 µg/kg (33), followed by Limpopo province with FB levels of 101 – 53863 µg/kg (42). In South Africa, DON contaminates mainly wheat and wheat related products (36). The highest level of DON was recovered from wheat produced in the Eastern Cape Province, with 3750 - 14360 µg/kg (30), though a higher level (18000 µg/kg) was reported with the analyses of combined wheat and wheat-based products collected throughout South Africa (36). Nonetheless, DON toxicity under field conditions has not been reported in the country, although consumption of DON contaminated foods has been linked to outbreaks of human gastroenteritis in India (46) and food poisoning in China (47). DON is also prevalent in maize and home-brewed beer, where it was recovered at 294 and 2340 µg/kg, respectively, particularly in the rural areas of South Africa (22, 44). Limited information is available on AF contamination of different crops in South Africa. Available literature indicates that exposure to this toxin is restricted to maize consumption and few other crops affected by Fusarium species. It may also be directly consumed in other cereals, legumes, and related foodstuffs (31, 36) or indirectly with animal by-products, as summarized in Table 1. Other mycotoxins often encountered in South Africa include ZEA and OTA (17, 36, 38, 39, 44). OTA has been reported in South African traditional home-brewed beer at very high levels, ranging from 876 to 2340 µg/L, with the highest level reported in Kwazulu-Natal (31). This is a product that is consumed almost daily by the local population, and exposure to such high levels of OTA over prolonged period could elicit serious health complications with the human kidney. However, some studies conducted in South Africa have shown OTA levels in cereals within acceptable standards (17, 36, 48). ZEA levels up to 426 µg/L were identified in cereal-based products (44). These levels were noted to be above the maximum level of 100 µg/kg established by the European Commission (49) regulated in unprocessed cereals.

Although mycotoxin occurrences have been reported in cereals in South Africa, very few cases of human mycotoxicosis have been documented. Palanee (50) reported an association between exposure levels to FB₁ and levels in patient's blood as well as brain lesions at Wentworth Hospital’s Neurosurgical Unit of Kwazulu-Natal province. Additionally, consumption of maize with high concentrations of FBs has been linked to increased risk of esophageal carcinoma in South Africa (33). In rural populations of the Eastern Cape Province, where maize and maize-based products are consumed in high volumes, FBs have been implicated in a high incidence of neural tube defects (51, 52). Recently, an association was reported between the AFB₁ and cases of kwashiorkor, marasmus, and underweight in South Africa (2). With the increasing consumption of maize, particularly in rural subsistence farming communities in the country (5), where infrastructure is poor, there is bound to be an increase in mycotoxigenic fungi infections. Contributing factors such as changes in natural conditions (sporadic weather changes) and human activities (increased crop movement) have led to a potential increase in mycotoxin-related health problems.

There are a limited number of reports on the effect of mycotoxins on human and animal health in South Africa, which may be due to the low levels of research on the understanding of the impact of mycotoxins on food safety as well as their associated health consequences. To perform the current scoping review, we reviewed studies and reported published from 1980 to 2020. The findings highlight the economic importance of predominant mycotoxins in maize and other cereals like FBs, AFs, DON, and to a lesser extent, OTA and ZEA (36, 38, 53) in the country.

The methodological approach of the current study was not fully appraised due to the limited number of peer-reviewed articles describing mycotoxin contamination in maize and other cereals in South Africa. Sourcing data from non-academic institutions, particularly when such information was not available online, proved to be difficult. English was used as the search language in the study, as such also limiting the number of articles used for analysis

This study demonstrates high levels of contamination in maize and other cereal products by mycotoxins, notably FBs and AFs. These contaminations are sometimes associated with major health and economic challenges. There is, therefore, a need to increase efforts towards monitoring mycotoxins in food and feed as well as adopting regulatory measures that are effective, sustainable, and scalable in reducing and associated health and economic burden. It is important to empower farmers and other stakeholders to improve on good hygiene and farming practices, particularly at farm and storage levels. Such interventions can limit mycotoxin-associated food contamination, which in turn will translate into declined exposure to these toxic secondary metabolites among humans and animals. This is particularly important as other mycotoxins, especially the emerging ones, can be considered in the regulation of food trade. With changes in global climate scenarios, there may be an increased mycotoxin production, and different or emerging mycotoxins may become important (53-55).