The discrete incidence of ochratoxins and aflatoxins in foodstuff is quite common in cereals and is a worldwide problem during pre-and post-harvest stages 56. However, the concomitant occurrence of these mycotoxins has not been researched adequately in Africa. In this study, a range of 0-97.51 µg/kg (mean 48.76 µg/kg) of ochratoxins was obtained and were comparable to other previous studies globally. Nalle et al 57 reported a mean value of 20.385 µg/kg in corn grains and corn products from different sources in West Timor, Indonesia. Kamala et al 58 reported a range of 16–73 µg/kg OTA concentration in maize samples from Tanzania. Values of ranges 0.12–0.59 µg/kg and 1.70–19.5 µg/kg have been reported by Kara et al 59 in cereal flour samples from Turkey and by De Giromalo et al 60 for cereals from Italy respectively, Again, Temba et al 61 also reported levels of 19.5 µg/kg. Veldman et al 62 demonstrated a total of 16.7% of maize samples originating from Holland contaminated by OTA with an average level of 73 µg/kg. From Brazil, Sekiyama et al 63 recorded levels between the range of 0–64 µg/kg.
Greater quantities of ochratoxins have been reported in maize from other studies worldwide. Recently, ul Hassan 64 reported ochratoxins (OTA) levels that ranged from 2.14–214 µg/kg which was detected in 71% of commercially grown maize samples in Pakistan. Makun et al 65 reported that samples of maize showed the highest levels of OTA were in the range of ND to 139.2 µg/kg in Nigeria.
Conversely, Iram et al 66 did not detect ochratoxins in maize samples obtained from Punjab, Pakistan. Adebajo et al 67 also detected OTA in corn-based snacks in Nigeria only at toxicologically significant levels. The co-occurrence of different mycotoxins in one commodity created by fungal genera is common 68. The permissible limit of OTA recognized by FAO/WHO Joint Committee Experts on Food Additives is 100 ng/kg/week and 14ng/kg/day, whereas European Food Safety re-established 120 ng/kg of OTA, which is nearly 17.1 ng/kg 47.
Ochratoxins have been implicated in a variety of adverse health effects both in humans and in animals suggested to be reaching from renal, neuro-, immuno-, and embryo-toxicity to muta- or teratogenicity 69. OTA was proven as a renal carcinogen in rodents 70, nevertheless its transferability to humans is still not clear 71. Its carcinogenicity has been adopted to be related with genetic changes leading to a new assessment so that OTA can also be considered as genotoxic/mutagenic 72. The high presence of OTA might be attributed to other fungal species that have not yet been explored or due to other pieces.
Aflatoxins levels recorded in this study was in the range of 0-441.02 µg/kg which is within the range of values reported by Adebajo et al 67 for values between the ranges 25–770 ppb, 15-1070 ppb, and 10–160 ppb for corn, corn cake, and corn roll snack respectively in Nigeria.
Recently, Kortei et al 2 also reported aflatoxins levels of range 0-445.01 µg/kg from maize samples obtained from different agro-ecological zones across Ghana. Aflatoxin quantities of 692 and 945 ng g− 1 from maize samples obtained from Fumesua and Ejura in Ghana respectively by 73. From Eastern and Central Kenya, Lewis et al74 reported greater quantities of aflatoxin > 1000 ppb in maize samples from contamination due to aflatoxin of commercial maize products during an outbreak of acute aflatoxicosis. Dadzie et al 73 recorded Total aflatoxins levels in the samples per community were in the range of below limit of detection (LOD) to 692 ng/g, 23 ng/g, 945 ng/g, and 112 ng/g for Fumesua, Wenchi, Ejura, and Akomadan, respectively.
Lower aflatoxin levels have been reported in other studies. de Souza et al 75 reported quantities as low as 0–16 in Brazilian maize and maize-based foods. Total aflatoxin values of 50.234, 70.102, and 30.943 ng/g were, respectively obtained from three composite samples taken from the Ejura market was reported by 76. Danso et al77 reported aflatoxin levels of 2.9–3.4 ppb in all markets in the minor season maize samples, but levels ranging from 38.2 to 64.0 ppb were found in the major season samples. Total aflatoxin levels of 82.9 ppb, 48.9 ppb, and 48.9 ppb were recorded for maize samples stored in polypropylene sack, hermetic bags, and local crib respectively by 78.
The variation in contamination levels could be attributed to speckled infection levels of the toxigenic fungus genera, Aspergillus (esp. flavus) owing to their ubiquitous nature, infect maize grains on the field even before harvest 79,80. Ghana is reliant on rain-fed agriculture which is coupled with high temperatures and unavailability of regular rains, the crop is left under stress which predisposes the crop to fungal invasion 81 during the growth cycle. This may explain the presence of aflatoxins on maize grains before storage.
There were significant correlations between AFtotal and OTA. Likewise, AFB1 and AFtotal in this study. These observations corroborate the findings of some previous researchers 63,64,66,82. The co-existence of two or more fungi and their subsequent mycotoxins production in an environment suggests a possible non-antagonistic metabolites interaction additionally, the probable effect of combined exposure to aflatoxins with other mycotoxins in foodstuffs could be additive or antagonistic.
At variance with our observation, Imperato et al 82 reported that among food products analyzed in Italy, dried vine fruits were mainly contaminated with OTA and less with AFs. Discovered from pertinent literature, there is an inverse correlation between AFB1 and OTA. To buttress this claim, 83 observed, no AFB1 was found in dried vine fruits, while OTA was detected at high levels. In addition, Dimitrokallis et al 84 reported that OTA inhibits AFB1 production by Aspergillus species in a related study.
The different categorizations of the biosphere (agro-ecological zones) presage different growth conditions for the proliferation of fungi. Brzonkalik et al 85 as well Garcia et al 86 emphasized mycotoxin production is dependent on species or/and strain, which is affected by the growth substrate and environmental conditions. de Souza et al75 and Kortei et al 88 also explained co-existence of fungal strains on a substrate can affect both the level of mycotoxin production and the toxicity of the contaminated grains resulting in additive and synergistic effects when tested Nonetheless, data on multiple mixtures is very rare 87.
The relatively high aflatoxin (AF) and ochratoxin (OTA) concentrations in maize grains suggested favorable environmental conditions for the growth of these fungi 88,89. 90 noted that Penicillium spp. grow well between 0–30°C and have been found to produce ochratoxin A this may explain the high incidence of this mycotoxin. Furthermore, Magan et al 89 also emphasized fungal contamination in cereals is influenced by two main factors. Firstly, by initial high moisture content in crops or late harvesting of crops in rural areas, and secondly, the lack or poor storage facilities characterized by poor ventilation, high temperatures, and humidity.
Regular monitoring and pre-and post-harvest control measures can be used to control mycotoxins by enhancing the resistance of the crop against incursive fungi through plant breeding or genetic engineering which are laborious and time-consuming. Effective, sustainable, and universally applicable pre-harvest intervention strategies are needed. Proper field management practices such as the use of resistant varieties, timely planting, fertilizer application, weed control, insect control, and avoiding drought and nutritional stress could reduce mycotoxins 91. Other options are the biological control by using non-toxigenic strains to competitively displace toxigenic fungi 92.
Risk assessment.
Kuiper-Goodman 93 highlighted that risk estimations are computed to envisage the adverse health implications of mycotoxin exposure and guide food regulators to set limits for these toxins in foodstuffs.
Risk assessment results obtained in this study were comparable to published findings of Blanckson and Mills 94 as they reported Total aflatoxins EDI values of range 0.005–1.054 µgkg-¹bwd-¹ and 0.004–0.838 µgkg-¹bwd-¹ for infants and young children respectively in infant cereal-based formula and were risky for children to consume in Ghana.
The Estimated Daily Intakes (EDI) of the total aflatoxins in the maize samples recorded by Kortei et al 2 were 109.7, 58.8, 33.08, and 25.2 µg Kg bw− 1 day− 1 for infants, children, adolescents, and adults with Margin of Exposure (MOE) values of 4.73, 8.79, 15.63 and 20.51 respectively.
Exposure assessment carried out by Omari and Anyebuno 95 showed that the minimum and maximum daily AFs exposures were 0.044 and 2.805 µg/kg bw/d, respectively for weanimix (infant complementary food prepared from maize) from rural households; these rates for complementary food purchased from urban shops were 0.014 and 0.55 µg/kg bw/d, respectively. The chances of liver cancer development would increase to 0.6 per year if infants were fed on complementary food prepared in rural households with a minimum AF level of 7.9 µg/kg.
In Guangzhou China, Zhang et al 96 reported EDI values of range 0.02–0.04 respectively for the age ranges of 3–6, 7–17, 18–59, and above 60 yrs for maize and products. All their computed MOE values were below the safe threshold of 10,000 and so risk analysis results showed that most of the lower bound MOE values ranged from 10 to 100, indicating a concern for risk management. Age-group analysis suggested close attention is paid to the 3 ~ 6 years of age group, whose MOE value was the lowest. Their results reflected those preschool children might have the highest risk of being exposed to AF. Their results agreed with our findings.
The MOE values (995–860 at mean and 336 at 95th percentile exposure) and cancer potency estimates, based on the current exposure levels indicated a potential health concern for Turkish adults was reported by 97. Li et al 98 pointed from a Chinese survey data, that the average daily intake of AFB1 from maize in the high-risk area was 184.1 µg, and the probable daily intake is estimated to be 3.68 µg kg− 1 bw day− 1.
Chun et al 99 estimated excess cancer risk values to liver cancer incidence by ingestion of these foods for AFB1 were calculated to be 5.78 × 10− 6 for individuals negative for hepatitis B and 1.48 x 10− 4 mg kg− 1 bw day− 1 for individuals positive for hepatitis B in Korea.
Various interventions have been established to combat aflatoxin biosynthesis and accumulation, ranging from preharvest to dietary interventions. Simply avoiding or reducing consumption of foods that are frequently contaminated with aflatoxin has shown effectiveness in reducing liver cancer mortality in one population 100.
Advocacy on the strict compliance to good agricultural practice (GAP), good manufacturing practice (GMP) as well as good hygiene practice (GHP) which are critical ingredients to alleviate the formation of aflatoxins in the field as well as during storage of foodstuffs, must be strengthened. By impeding the aflatoxins formation in foods, there is the protection of both public health and the prevention of economic losses. Monitoring foods prone to fungal infection and the presence of mycotoxins regularly is cautious to assess the public level of awareness.