Storage conditions and postharvest practices lead to aflatoxin contamination in maize in two counties (Makueni and Baringo) in Kenya

Hannah Mugure Kamano; Michael Wandayi Okoth; Wambui-Kogi Makau; Patrick Kuloba; Nduhiu Gitahi

doi:10.1515/opag-2021-0054

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Storage conditions and postharvest practices lead to aflatoxin contamination in maize in two counties (Makueni and Baringo) in Kenya

Hannah Mugure Kamano , Michael Wandayi Okoth , Wambui-Kogi Makau , Patrick Kuloba and Nduhiu Gitahi

Published/Copyright: November 30, 2022

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From the journal Open Agriculture Volume 7 Issue 1

Abstract

Aflatoxins are known to cause devastating acute and chronic effects in humans and animals. The objective of the study was to determine the influence of postharvest practices and storage conditions on aflatoxin contamination in maize in two counties. Aflatoxin levels in 144 maize samples from different maize storage conditions were determined. While sampling, a structured questionnaire was also administered to evaluate farmer’s postharvest practices. Makueni County had the highest percentage of aflatoxin positive samples with up to 174 ppb attributed to the long storage under unfavourable conditions. On the other hand, Baringo County had lower positivity associated with the harvesting season at the time of sample collection. The type of storage condition had a significant effect on the extent of contamination and accounted for 11% of the variation (R ² = 0.11). Gunny bags were the most common type of storage condition and had the highest level of contamination in both the counties. Metallic bins had the lowest level of contamination. Aflatoxin G1 and G2 were predominant in samples from Baringo County, while aflatoxin B1 and B2 were predominant in samples from Makueni County. The study concluded that the type of storage condition significantly contributes to the aflatoxin contamination in the stored maize. Proper drying of maize to the recommended moisture content and subsequent storage in hermetic structures will reduce the cases of aflatoxin contamination.

Keywords: aflatoxin; storage conditions; postharvest practices; maize; Kenya

1 Introduction

Globally, maize also referred to as “corn” has the highest production and is utilised in food, feed and fuel. It is the most preferred cereal grain in Southern and Eastern Africa, Central America and Mexico [1]. In Africa, maize is regarded as a cash crop and in most cases, the highest quality is set aside for export or sale to milling companies, whilst the poor quality is left behind for home consumption, preparation of local brews or sold in the informal markets [2]. In Kenya, maize is grown in both large and small farms and is the most important food security crop. In 2019, 95% of the 3,800 thousand tonnes of maize was utilised for subsistence needs [3,4]. According to the World Health Organisation statistics, Kenya is ranked among the countries with the highest maize consumption (171 g/person/day). Maize is prone to aflatoxin contamination that leads to huge losses threatening the country’s breadbasket [1]. In fact, for the last four decades Kenya has been documented as one of the leading countries with the most severe and highest incidence of human aflatoxin exposure in the world. In 2004, an outbreak in the Eastern part of the country led to 125 deaths and 317 cases of infection. There were other outbreaks that followed in the year 2005 and 2006 due to fluctuating weather patterns [5,6,7]. Aflatoxin contamination in maize is a common occurrence in Kenya especially in specific counties in the Eastern and North rift parts of the country [8,9]. It has been linked to the growing cases of cancer in the counties [10]. In 2010, the Kenyan government declared over 2.3 million bags of maize unfit for human consumption due to the high levels of aflatoxins [11]. One of the most studied mycotoxins in the world is aflatoxin, which is a toxic metabolite produced by aflatoxigenic fungi particularly Aspergillus flavus, Aspergillus parasitucus and the more rare Aspergillus nomius [12,13]. Aflatoxins contaminate food and feed across the value chain including maize grains, peanuts, cereals and animal feeds among others. Across the globe, a huge population is chronically exposed to aflatoxins [14].

For instance, aflatoxin M1 was detected in samples of breast milk in Ghana, Kenya, Nigeria and Sierra Leone [15,16]. In Benin, 99% of the children had the highest level of aflatoxin biomarkers ever observed in humans indicating a very high exposure level [17]. Several studies have also intuited a close interaction of chronic exposure to mycotoxins with retarded growth, suppressed immunity, malnutrition and diseases such as malaria and HIV/AIDS. Acute exposure to aflatoxin contamination has been associated with liver failure, hepatitis and even death in some instances [2,18,19,20,21,22,23]. Aflatoxin exposure has also been linked to infertility according to a study carried out in Benin [24].

High level of aflatoxins in stored maize is fuelled by various factors such as fungal load, insect infestation, environmental factors (climate, humidity, temperature, O₂, CO₂), preharvest and most importantly poor postharvest practices by farmers [25,26]. If harvesting is done during a rainy season, this may predispose the maize to humid conditions that may facilitate growth of aflatoxigenic fungi during storage due to the increased moisture content in the maize [27]. The type of storage condition and postharvest practices usually influence the state of the grain after storage and is paramount is ensuring the integrity of the maize. This research sought to investigate the influence of type of storage condition and postharvest practices on aflatoxin contamination in Makueni and Baringo Counties.

2 Materials and methods

2.1 Study sites

Makueni and Baringo Counties were purposively selected due to numerous reported and unreported cases of aflatoxicosis [28,29,30]. Makueni County is located within the lower midland agro-ecological zones LM2, LM3, LM4 and LM5. Annually, it receives between 200–1,200 mm rainfall also characterised by sporadic droughts which results in crop failure [29].

Baringo County on the other hand is divided into three agro ecological zones: highlands, midlands and lowlands (Figure 1). Over 80% of the population depends on maize as the main food and cash crop with most of them being farmers [31]. The aflatoxin analysis work was carried out at the Mycotoxin Research Centre located at the Department of Public Health, Pharmacology and Toxicology (PHPT) of the University of Nairobi, Kenya.

Figure 1

Map of the study areas (Makueni and Baringo Counties, Kenya).

2.2 Sample collection and preparation

A total of 144 maize samples (1 kg each) were randomly collected from 4 different types of storage conditions in Makueni and Baringo Counties. These included gunny bags, metallic bins, open storage and PICS (Purdue Improved Crop Storage) bags; 36 samples from each storage condition. Each sample was homogenised before the analysis began. Milling was done using a knife mill (Grindomix GM 200, Germany) before further analysis. The mill was thoroughly cleaned and dried using paper towels after every mill to avoid cross contamination between samples.

2.3 Determination of postharvest practices

While sampling, a questionnaire was also administered with the purpose of relating the postharvest practices to the aflatoxin content of samples collected from each farmer. They included mode of harvesting, drying, shelling, preservation, grading and sorting, disposal of contaminated grain and storage practices.

2.4 Aflatoxin analysis

2.4.1 Enzyme-linked immunosorbent assay (ELISA) for total aflatoxin

Screening of samples was carried out using the competitive enzyme-linked immunoassay for quantitative detection of aflatoxin B1, B2, G1 and G2 (10). The aflatoxin kits (HELICA Total Aflatoxin Assay) were sourced from the United States (Helica biosystems Inc). The samples were prepared according to the manufacturer’s recommendations. All the reagents were brought to room temperature before use. Five gram of the ground maize samples were mixed with 25 mL of 70% methanol. The ratio of the sample to extraction solvent used was 1:5 (w/v). The extracted sample was thereafter mixed with 200 µL of HRP conjugated aflatoxin. 100 µL of each standard and sample was then added to appropriate mixing well containing conjugate and mixed 3 times. 100 µL of the mixture was then transferred to a corresponding antibody coated microtiter well and incubated for 15 min at room temperature. The well contents were then discarded into a discard basin and the micro wells were washed five times by filling each well with phosphate buffered saline (PBS) and Tween wash buffer. Absorbent towels were used to dry the wells (face down) before introduction of 100 µL of substrate reagent. Finally, 120 µL of stop solution was added to each micro well. The optical density of each micro well was read using a spectrophotometer – model type – 355, manufactured by Thermo Fisher Scientific (Shanghai, China). The readings were taken using a 450 nm filter. The limit of detection of the kits was 20 ppb. Samples that had more than 20 ppb were further diluted with 70% methanol and retested to obtain the accurate total aflatoxin level.

2.4.2 High performance liquid chromatography (HPLC) analysis

Confirmatory test for the ELISA positive samples were carried using HPLC analysis. The respective standards for each aflatoxin were prepared accordingly [32]. Evira method was used for determination of aflatoxins B1, B2, G1 and G2 (Romer Labs). This involved extraction, filtration, clean up, elution and drying. Extraction of the aflatoxins was done by adding 5 g ground maize sample to 25 mL of 70% methanol and shaking for 2 h followed by filtration using filter paper (Whatman No.1). Cleaning was done by taking 9 mL of the mixture and drying using nitrogen to <0.5 mL. This was then diluted to 10 mL using PBS, and 1 mL of the mixture was passed through immunoaffinity columns placed on vacuum manifold. This was then washed with 2 mL × 10 mL water. Derivatization was carried out followed by drying the elute using a nitrogen stream. 200 µL of trifluoro acetic acid was then added, vortexed for 1 min and incubated for 30 min away from light. The sample was then filtered using a 0.2 µm membrane filter (GHP) before injection into the HPLC machine (Nexera UHPLC Shimadzu – Japan). The type of column used for the analysis was Nova-Pak C18 4 µm × 150 mm (Water Corp – Ireland). The following operating conditions were observed during the process: run time – 30 min; injection volume – 10 µL; column temperature – 35°C; velocity – 1.0 mL/min). Aflatoxins were analysed as their trifluoro acetic acid derivatives and identified according to their retention times. Quantification was done by use of external standard curves.

2.5 Data analysis

Data entered in Microsoft Excel spread sheets were analysed with R software (version 4.0.3). Mean values and standard deviations were calculated from duplicate sample readings. A one-way ANOVA was used to compare mean values of the aflatoxin levels from the different storage conditions. The mean values were separated using Tukey’s honestly significant difference (HSD) method. Independent variables with a p value < 0.05 were considered statistically significant to the outcome variable. Model selection was based on the Akaike Information Criteria (AIC) method [33].

3 Results

3.1 Results of ELISA analysis

Makueni County had the highest percentage of positive samples. The levels of contamination ranged between 0.3 and 174 ppb (Table 1). The location of the sub-county as to being local or urban did not influence the level of aflatoxin contamination in the maize grain. There was no significant difference between the mean values of the aflatoxin levels between the sub counties (P = 0.39) and also comparing the two counties (P = 0.60). However, more than half of the samples collected from Wote (urban, 59.1%) and Kisau Kiteta (rural, 68%) sub-counties were above the Kenya regulatory limit and World Health Organisation statistics/FAO maximum limit allowed in food of 10 ppb [34].

Table 1

Summary of mean total aflatoxin levels of maize (ELISA) from Makueni and Baringo Counties

County	Sub-county	Locality	% positive (exceeding 10 ppb)	Range (ppb)
Makueni	Wote	Urban	59.1	0.3–100
	Kako Woiya	Rural	24.0	2–172
	Kisau Kiteta	Rural	68.0	0.2–105
Baringo	Baringo Central	Urban	14.3	4–160
	Baringo North	Rural	45.5	6–171
	Baringo South	Rural	42.9	2–166
	Eldama Ravine	Rural	16.7	3–174

P = 0.39.

Four models were explored to determine which factors had the largest effect on the level of aflatoxin contamination in the maize grain. The main effects of locality and the type of storage (Model 1) were chosen as they accounted for up to 81% of the variation (Table 2).

Table 2

Model selection for analysis of storage data

	AICc value	AICc delta	AICc weight
Model 1	7 1481.29	0.00	0.81
Model 2	9 1484.61	3.32	0.15
Model 3	3 1488.46	7.17	0.02
Model 4	6 1489.86	8.57	0.01

Model selection based on AIC: Model 1 – locality + type of storage; Model 2 – locality × type of storage; Model 3 – locality and Model 4 – type of storage.

The type of storage had a significant effect (p < 0.001) on the extent of contamination and accounted for 11% of the variation (R ² = 0.11). Gunny bags had the highest level of contamination in both counties. Metallic bins on the other hand had the lowest level of contamination. The mean level of contamination was 3.8 and 47.3 ppb for metallic bins and gunny bags, respectively. There was a similarity in the levels observed in maize samples collected from PICS bags, metallic bins and in open storage (Figure 2).

Figure 2

Aflatoxin levels of maize stored in different types of storages.

Metallic bins and PICS bags had lower levels of aflatoxin contamination in the stored maize as compared to gunny bags and open storage. Metallic bins and PICS bags are forms of hermetic storage. Hermetic storage has been found to be very effective against the Aspergillus spp. which produce aflatoxin in conducive environments [35,36]. Effectiveness of improved drying and storage practices of maize was studied in Senegal. The study concluded that hermetic storage greatly improved the integrity of the stored maize by extending storage period by 3–4 months [37]. Proper postharvest management and practices are promising ways of reducing or even completely eliminating aflatoxin contamination of maize [38,39]. Harvesting for instance by 97.9% of farmers was by stacking maize in heaps (Table 3). This is a stage where aflatoxin contamination can easily occur especially if the maize is left in the field for a long period before drying. Infection of maize by Aspergillus spp. begins in the field and therefore control strategies also need to begin at preharvest [40,41]. Erratic rains that are common in this region are possible cause of aflatoxin contamination of the maize during harvest. Timely harvesting is also critical to prevent contamination. A study on the effect of delayed harvesting of maize after maturity revealed that the aflatoxin contamination increased by 4–7 folds after 3–4 weeks [42]. Drying of maize on a tarpaulin/canvas was practiced by over 50% of the farmers in both counties. Interesting to note was that 47.1% of farmers in Makueni County dried maize on the ground and this is associated with the high levels of positivity in the samples. Drying of maize on the ground is highly discouraged as the soil contains the toxigenic strains responsible for aflatoxin contamination. Shelling was mainly by hand (38.2%) and pounding manually in gunny bags (47.1%) in Makueni County.

Table 3

Association of postharvest practices with aflatoxin contamination

		Makueni	Baringo	p-value (R ², df)
Postharvest practices		Yes (%)	Yes (%)	p-value (R ², df)
Harvesting	Maize stovers stacked in heaps	77.9	97.9	0.73 (0.001,114)
	Maize cob removed while stovers are standing	22.1	2.1
Drying	Drying maize on the ground	47.1	11.8	0.32 (0.081, 107)
	Drying maize on a tarpaulin mat/canvas	51.5	76.5
	Open store	0.0	3.9
	Left to dry in the field	1.5	0.0
Shelling	By hand	38.2	6.3	0.88 (0.052, 104)
	Using a machine (Sheller)	14.7	85.4
	Pounding manually in gunny bags	47.1	8.3
Preservation	Using insecticides (actellic)	76.5	79.2	0.05 (0.065, 112)
	Using ash	2.9	0.0
	None	20.6	20.8
Grading and sorting	Grading based on colour and size	32.4	23.0	0.37 (0.007, 114)
	Grading to improve quality	22.1	33.4
	No grading	45.5	43.6
Disposal	Feeding livestock	29.4	56.3	0.57 (0.002, 114)
	Throw away	35.3	23.0
	Consume in different forms	36.8	58.3
	Sell in markets	5.9	23.0
	Destroy	36.8	16.7
	Give away	0.0	12.5
Storage	Store bags on wooden pallets	86.8	58.3	0.23 (0.012, 114)
	Store on the ground	13.2	41.7

The farmers in Baringo County mainly employed the use of a mechanised sheller. The use of the appropriate shelling methods to reduce grain damage, control of insects in the store, sorting to remove damaged grain and use of clean, well-aerated stores are recommended as a good postharvest practices [43,44]. When the grain is damaged, it is more prone to aflatoxin contamination. This could also be a contributing factor to the high positivity of samples from Makueni County as pounding of the maize grain in the gunny bags makes it prone to aflatoxin contamination by the spoilage fungi. Some of the farmers did not dispose the contaminated maize as recommended but rather used it in various ways. The larger proportion of farmers used it to make alternative products such as local alcoholic-based beverages (busaa and chang’aa) and some fed it to livestock. Still another group sold it in local markets after blending with “clean” or uncontaminated maize grain.

The association of the level of aflatoxin contamination was also related to the postharvest practices of the farmers. However, none of these postharvest factors investigated in this study significantly contributed to aflatoxin contamination (P > 0.001).

3.2 Results of HPLC analysis

A linearity curve for aflatoxin (AF) B1, B2, G1 and G2 was generated as shown in Figure 3. The average retention times for AFG1 and AFG2 were 6.440 min and 10.497 min, respectively. On the other hand, those of AFB1 and AFB2 were 7.838 min and 13.438 min, respectively (Figures 4 and 5).

Figure 3

Calibration curve for aflatoxin B₁.

Figure 4

Chromatogram of a maize sample from Baringo County observed in Kenya.

Figure 5

Chromatogram of a maize sample from Makueni County.

4 Discussion

The results of the Elisa analysis for the maize samples revealed a high level of contamination of the maize grains in these sub-counties especially those in Makueni County. This may have been due to the long period of storage as the samples were collected at the onset of another planting season. Baringo County, however, experienced lower percentage of samples with maximum permissible limits. This was attributed to the fact that the samples had been fresh from harvest at the time of collection among other factors. The highest and lowest levels of contamination were while using gunny bags and metallic bins, respectively. A similar study on the influence of storage conditions on aflatoxin contamination in wheat and mustard showed a high incidence of Aspergillus flavus and high aflatoxin levels in samples collected from gunny bags [45]. The low levels noted in samples stored in metallic bins and PICS bags can be explained by the integrity of the packing in preventing uptake of moisture by the grain after proper drying. The optimum conditions that favour the development of A. flavus are temperature (86°F), relative humidity (85%) and kernel moisture (18%). When temperatures are below 65°F and kernel moisture ranges between 12 and 13%, the growth of the fungus usually stops. Hermetic storage arrests the further growth of the colonies by curtailing respiration [46]. Gunny bags being plastic in nature allow moisture into the grain and this facilitates spoilage. Sisal bags are recommended for use in place of gunny bags [47]. Proper postharvest management and practices are promising ways of reducing or even completely eliminating aflatoxin contamination of maize. Harvesting for instance by 97.9% of farmers was by stacking maize in heaps. This is a stage where aflatoxin contamination can easily occur, especially, if the maize is left in the field for a long period before drying. Erratic rains that are common in this region are possible cause of aflatoxin contamination of the maize during harvest. Timely harvesting is also critical to prevent contamination.

A study on the effect of delayed harvesting of maize after maturity revealed that the aflatoxin contamination increased by 4–7 folds after 3–4 weeks [42]. Drying of maize on a tarpaulin/canvas was practiced by over 50% of the farmers in both the counties. Interesting to note was 47.1% of farmers in Makueni County dried maize on the ground associated with the high levels of positivity in the samples. Drying of maize on the ground is highly discouraged as the soil contains the atoxigenic strains responsible for aflatoxin contamination. Shelling was mainly by hand (38.2%) and pounding manually in gunny bags (47.1%) in Makueni County. The farmers in Baringo County mainly employed the use of a mechanised sheller. The use of the appropriate shelling methods to reduce grain damage, control of insects in the store, sorting to remove damaged grain and use of clean well-aerated stores are recommended as a good postharvest practices [43,44]. When the grain is damaged, it is more prone to aflatoxin contamination. This could also be a contributing factor to the high positivity of samples from Makueni County as pounding of the maize grain in the gunny bags makes it prone to aflatoxin contamination by the spoilage fungi. Some of the farmers did not dispose the contaminated maize as recommended but rather used it in various ways. The larger proportion of farmers used it to make alternative products such as local alcoholic-based beverages (busaa and chang’aa) and some fed it to livestock. Still another group sold it in local markets after blending with “clean” or uncontaminated maize grain.

There was a distinct variation in the levels of aflatoxin B1, B2, G1 and G2 detected in samples from Makueni and Baringo Counties. Aflatoxins B1 and B2 were more predominant in samples from Makueni County, whilst aflatoxins G1 and G2 were more predominant in samples from Baringo County. This can be explained by the strain variation in the two ecological zone. For instance, confirmatory tests on a sample from Kako Woiya, in Makueni County showed a level of 867 ppb and 45 ppb for aflatoxins B1 and B2, respectively (Figure 4). During one of the most severe reported cases in the last 20 years that occurred in 2004 in Makueni County, maize samples were found to have extremely high levels of aflatoxin B [48]. The level of aflatoxin B1 was 4,400 ppb, 440 times the maximum permissible limit of 10 ppb by Kenya Bureau of Standards. On the other hand, a test on a sample from Baringo North revealed a level of 11 ppb and 2 ppb for aflatoxin G1 and G2, respectively (Figure 5). Aspergillus flavus strains can be grouped into two groups based on their morphology: L and S strains. The morphology of the L strains is characterised by numerous conidiospores and sclerotia and are larger in size, up to 400 µm. The S strains, on the other hand, are fewer and are smaller in size. The S strain isolates are not only more stable but also produce higher amounts of aflatoxin as compared to the L strain isolates [49]. Recent studies have revealed a very high presence of the toxigenic A. flavus S strains in Makueni County and the less toxigenic L strains in Nandi County, which is a county that borders Baringo County. All the A. flavus strains isolated from Makueni and Baringo Counties were the S type and L type, respectively The S strains primarily produce the more toxic B toxins, whilst the L strains produce more of the less toxic G toxin [28].

This explains the higher cases of aflatoxicosis reported in (Eastern Kenya) Makueni County as compared to (north rift parts of Kenya) Baringo County. However, the distribution of aflatoxins B1, B2, G1 and G2 between the two counties was relatively the same despite the different geographical locations and environmental conditions. These results are similar to findings of earlier studies in the areas that found a similar pattern of occurrence of A. flavus which eventually produces the B toxins [28]. This similarity was also observed in Nigeria [50].

5 Conclusion

Very high levels of aflatoxin contamination of stored maize occur in Makueni County. Baringo County, on the other hand, has had few cases of aflatoxicosis. The most common aflatoxin in Makueni is aflatoxin B1, which is the most lethal of the aflatoxins usually produced by the S strains of A. flavus. Samples from Baringo County had more of the less lethal toxin, G1 which is characteristic of the L strains predominantly found in the county. Despite the already known dangers of consumption of aflatoxin contaminated maize, farmers still utilise the grain for various purposes. The main uses include use in the manufacture of animal feeds and traditional alcoholic beverages such as “busaa” and “chang’aa.” The type of storage condition also affects the level of contamination in the grain. Based on the levels of aflatoxins in the stored maize, the storage conditions were rated from the best to the worst in the following order: metallic bins – PICS bags – open storage – gunny bags. Hence, implementation of the appropriate postharvest management and practices has a major impact on reducing or even eliminating aflatoxin contamination in maize. There is need for more sensitisation of the farmers at the farm level on hazard analysis critical control points and good agricultural practices to reduce the chances of contamination at the production stage. If better postharvest practices are implemented, then this can almost solve the problem to a large extent. In the case of contaminated maize grain, farmers need to be sensitised on safe disposal instead of the common practices of use in animal feeds as well as in the manufacture of traditional alcoholic beverages. Finally, surveillance and monitoring of the maize along the value chain by the regulatory authorities is important in order to protect the public from consumption of contaminated maize grain.

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Acknowledgments

The authors wish to thank the County Governments of Makueni and Baringo for allowing the study to be carried out in their jurisdiction.

Funding information: This work was funded by the National Drought Management Authority (NDMA) through the financial support of the European Union (EU) – (Project no. NDMA/EDE DRMC/006/2019-2020)
Conflict of interest: The authors state no conflict of interest.
Data availability statement: The datasets generated during and/or analysed during the current study are available in the Zenodo repository, https://zenodo.org/record/4916850#.YMDSv_kzbIU, reference number doi:10.5281/zenodo.4916850.

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Received: 2021-06-17

Revised: 2021-09-11

Accepted: 2021-10-19

Published Online: 2022-11-30

This work is licensed under the Creative Commons Attribution 4.0 International License.

Articles in the same Issue

https://doi.org/10.1515/opag-2021-0054

Keywords for this article

aflatoxin; storage conditions; postharvest practices; maize; Kenya

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