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Management and mitigation of health risks associated with the occurrence of mycotoxins along the maize value chain in two counties in Kenya

Management and mitigation of health risks associated with the occurrence of mycotoxins along the... Aflatoxins and fumonisins are two mycotoxins that are prevalent in cereals. Both toxins have associated and causal health effects in humans and livestock. Once formed in the substrates, the toxins are not easily destroyed. The preferred mitigation is to prevent contamination of the cereals and animal source foods. In this paper we set out to examine the practices of the farmers in two counties (Nandi and Makueni) in Kenya which exacerbates aflatoxin contamination and the government steps to address the issue in the agriculture and livestock sectors. The practices identified in Nandi and Makueni, respectively, included seed varieties where 19.3% and 56% are using local varieties; use of soil amendments where 5.8% and 181 % are not using any amendments; crop rotation where 54.6% and 60.5% are not practicing crop rotation; 22.7% and 37.5% are using wrong drying methods; and 53% and 77.1% are using poor threshing methods. The Kenya government is subsidizing fertilizers, seeds, increasing areas under irrigation, and providing extension services to build capacity of farmers to mitigate aflatoxin contamination. The paper examines also the cultural practices in land preparation, tillage, crop rotation, drying, sorting at farm, and proper storage as better alternative practices for easy adoption that would, if adopted, lead to a decrease in aflatoxin and fumonisin contamination and therefore reduce household exposure. Good agricultural practices should be a prerequisite for the adoption of other aflatoxin control technologies. Key words: Aflatoxins; Fumonisins; Contamination; Maize value chains; Mitigations; Kenya. fatality of 39.4% (Lewis et al., 2005). Subsequent outbreaks have Introduction also resulted in loss of life. Aflatoxins and fumonisins are the major Kenya has had a problem with mycotoxicosis as evidenced by the fungal toxins that contaminate and have been detected in cereals in 2004/2005 aflatoxin outbreak, which resulted in the high case © The Author(s) 2017. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Management and mitigation of mycotoxin along maize value chain, 2017, Vol. 1, No. 4 269 Kenya (Mutiga et al., 2015). In addition to acute toxicity that leads barley growing. Makueni falls within the lower midland agroeco- to loss of life in case of aflatoxins, chronic exposure to the toxins logical zones LM3, LM4, and LM5. It receives between 200 and has been associated with public health concerns and food security. 1200 mm of rainfall per year, which is unreliable at times with fre- Chronic exposure of humans to aflatoxins has been associated quent droughts resulting in crop failures. with immunosuppression (Williams et  al., 2004) and carcinogens causing liver cancer (Wu et  al., 2011). International Agency for Data collection tools Research on Cancer (IARC) estimates that liver cancer incidences A questionnaire was administered to heads or their spouses of in Kenya associated with aflatoxin are 8.5 and 4.9/100 000 cases selected households in Nandi and Makueni. The questionnaire for males and females, respectively (Wu et  al., 2011). There is no sought to capture data on agricultural practices (use of soil amend- direct causal relationship between aflatoxin exposure and stunting ments, seed varieties, crop rotation, harvesting, threshing, drying, in children but a high correlation between the two has been estab- sorting, and storage) during the maize cropping season. lished (Gong et  al., 2004; Leroy, 2013). It has been estimated that Data relating to use, disposal of moldy grains, and health risk per- 25% of the world’s grains are contaminated with aflatoxins (CAST, ceptions associated with consumption of moldy maize were obtained 2003), which would cause a serious world food security threat if by asking the respondents what they used to determine that the maize the contaminated grains are removed from the food supply chain. was spoilt or moldy. In this regard, the researchers gave respond- Fumonisins have been suspected risk factors for human disease such ent women (women are responsible for family food preparation. as esophageal cancer (Marasas, 2001; Wakhisi et  al., 2005) and Determining what is safe for family meals is their responsibility and neural tube defects (Meismer et al., 2006). While a causal relation- were best suited to give information) during the questionnaire admin- ship in human disease is unproven, fumonisins are recognized causes istration a handful of maize that had good and moldy grains. They of equine leukoencephalomalacia (Kellerman, 1990), toxic feed syn- were asked to sort out the good and the bad ones. After the exercise, drome in poultry, and porcine pulmonary edema syndrome in swine they were asked to explain what criteria they used to sort out the (Ross et al., 1993; Norred and Voss, 1994). maize. They too were asked what was the minimum level or type of Mitigation of aflatoxin and fumonisin contamination can be spoilage that would allow consumption of moldy or spoilt grains; the targeted to preharvest and post-harvest periods to prevent plant methods they used to dispose of spoilt or moldy grains; the percep- infection and grain contamination. During preharvest, good agricul- tion of health risks associated with feeding animals with moldy grains; tural practices reduce the vulnerability of crops to fungal infection and whether they considered milk from animals fed moldy grains to (Munkvold, 2003). Post-harvest practices help to prevent mycotoxin be safe. development in the grains. Other mitigation technologies include bio- The data collected through questionnaire were triangulated by logical control (Cotty, 1994) and use of enterosorbents and chemo- group discussions that employed a discussion guide with county reception to prevent absorption of the toxins in exposed individuals extension officers. Three workshops were held with county exten- (Kensler et al., 2013; Miller et al., 2014). This paper investigates the sion officers, which captured the role of the central and county extent to which farmers are adopting good agricultural (cultural) governments in the management of the aflatoxin and fumonisin con- management practices which are known to mitigate aflatoxin and tamination through group discussions on whether they considered fumonisin contamination of cereals at pre-harvest and post-harvest the problem worth mitigating and the measures they would adopt to period in the two counties of Makueni and Nandi, Kenya. control the problem in the counties. Results and discussion Materials and methods Good agricultural practices Site and household selection Five hundred and forty-one questionnaires were administered; for The counties Nandi and Makueni in Kenya were purposively which 280 respondents were from Makueni and 261 from Nandi. selected based on history of human acute aflatoxicosis in Makueni The study evaluated a number of agricultural practices as shown in (Lewis et  al., 2005)) and high incidences of esophageal cancer in Table 1. Nandi (Wakhisi et al., 2005). At the county level, a team consisting of the researchers, veterinary, agriculture extension, and health offic- Land preparation ers selected three subcounties that best fitted the criteria of high dairy production and maize growing activities. At the subcounty and ward During the preharvest stage in a maize cropping season, farmers in level, the extension officers selected the ward and the sublocation, Nandi were better than their counterparts in Makueni in adopting respectively, that best fitted the same criteria. With the assistance good agricultural practices. Adoption of good practices along the of village elders (managers), the households that had dairy animals food value chain has been proposed as the best way to reduce levels (cattle or goats); grew maize, sorghum, and/or millet; had a child of fungal toxins in the food supply (Clarke and Fattori, 2013). This below 5 years or the spouse was pregnant at the time were listed. study did not evaluate land tillage practices. However, fungal popu- Based on the population and number of households in the sub- lation densities have been shown to be affected by land preparation location and the households that fitted the criteria, a proportion of methods. Nesci et al. (2006) and Zablotowisc et al. (2007) compared the households was randomly selected for sampling (Martin et  al., the Aspergillus flavus density in land with no tillage and land with 1987), and the household sample size was corrected for finite popu- reduced tillage and found that land with no tillage and medium till- lation according to Daniel (1999). age with grazing had high A. avus fl density compared with land with Nandi falls within the agroecological zones of lower humid deep tillage. This was attributed to high organic matter content in highlands to upper midland and upper highland zones ((LH2, LH3, land with no tillage. Communities in Makueni use oxen ploughs and UM3, and UM4) (Jaetzold et al., 2006). It lies between 1300 to 2500 may not practice deep tillage compared to the communities in Nandi m above sea level and receives about 1200–2000  mm of rain per who use tractors for ploughing after each crop season. Okoth et al. year. Nandi is best suited for tea, dairy activities, maize, wheat, and (2012) found that A. avus fl was the most prevalent contaminant of 270 E. K. Kang’ethe et al., 2017, Vol. 1, No. 4 Table  1. The extent of adoption of good agricultural practices in Use of soil amendments Makueni and Nandi counties. In both counties, majority of the farmers were using fertilizers, fertilizer and animal manure, and animal manure as soil amend- Agricultural practices County ments. Only 17.9% and 6.1% of the farmers in Makueni and Makueni, % (n) Nandi, % (n) Nandi, respectively, were reported not using any soil amendments. The nature and fertility of the soil help to reduce fungal infec- Preharvest tion of crops. The ability of the soil to hold moisture is import- Use of certified seed 44.0 (273) 100 (259) ant. Codex Alimentarius Commission (2004) reported that crops varieties planted on sandy soils were more contaminated with aflatoxins Use of soil amendments 82.1 (280) 93.9 (261) than those planted on loamy soils. Loamy soils have the ability Practice crop rotation 16.4 (280) 25.3 (261) to retain moisture, which reduces moisture stress to the growing Post-harvest crops and therefore prevents fungal infection. In Kenya, farmers Harvesting Stoking 55.4 (280) 49.0 (261) use fertilizer and manure to increase the soil nutrient content to Remove cobs leave 42.5 (280) 48.7 (261) ensure a healthy crop that would resist fungal infection. Manure stovers standing (animal or compost) has the dual role of increasing the organic Drying on canvas 60.7 (280) 72.4 (261) content of the soil and also nutrients, both of which mitigate fun- Shelling gal infection by ensuring healthy crops. Lime application, use of Hand 11.4 (280) 14.6 (261) farm yard manure and cereal crop residues as soil amendments are Machine 11.4 (280) 30.7 (261) effective in reducing A.  avus fl contamination as well as aflatoxin Manual pounding 76.8 (280) 52.1 (261) levels by 50%–90% (Hell and Mutegi, 2011). In Makueni and Use of chemical pre- 77.9 (280) 75.1 (261) Nandi, 81.9% and 79.7% of the farmers, respectively, applied fer- servatives tilizer only as soil amendments while 22% of the farmers in both Storage methods Raised granaries 97.3 (110) 96.0 (126) Nandi and Makueni applied a mixture of fertilizer and manure On pallets in the house 89.6 (144) 60.9 (115) during planting. Failure to use soil amendments results in soils Raised crib 88.0 (25) 100 (13) that are low in organic nutrients with low ability to hold moisture, and this increases the vulnerability of the crops to fungal infection because of water and nutrient stress (Munkvold, 2003). maize in both counties with an incidence of 82.33% and 73.26%, in Nandi and Makueni, respectively. Harvesting and drying During the harvesting period, the methods of harvesting were Certified seeds mainly stoking and removing the cobs and leaving the stovers All the respondents in Nandi planted recommended and certified standing in the field. Fifty percent of farmers, both in Nandi and seeds for the agroecological zones compared to 56% of the farm- Makueni, cut maize stovers with the cobs and stoked them in ers in Makueni who were using local varieties. National and inter- heaps in the field to dry. There was no method that was more pre- national seed producing companies in Kenya had released over 164 ferred by farmers. Such practices expose the crop to proliferation varieties by 2009 (Kang’ethe, 2011). These varieties, though not fun- of fungi and bacteria and contamination with soil, reducing the gal resistant, are tested for pest and disease resistance, drought, and crop’s quality (Mejia and Farruci).The recommended maize-dry- low nitrogen tolerance in addition to being high yielding. They are ing method was either on cob or as shelled grains on canvas. Of ecologically adapted. In Nandi and Makueni, 19.3% and 56% of the farmers, 39.1% and 37.6% in Makueni and Nandi, respect- the farmers were using noncertified local variety seeds, which could ively, were not drying maize on canvas but on cob on ground and be susceptible to fungal infection though they are adapted to local leaving maize to dry in the field on stovers while standing. This conditions as a result of many years of selection. These varieties have practice increases the risk of picking up toxigenic fungal spores very low yields and are not consistent with the government policy of from the soil, thus adding to the risk of aflatoxin production and revitalizing agriculture as a business enterprise (SRA, 2004). accumulation. The moisture level of the grains is an important factor in toxin production. Grains with moisture level above 13% are more prone to aflatoxin contamination than those with Crop rotation lower moisture content. Harvested grains should be dried within The farmers in both counties, 83.6% and 74.7% in Makueni and 24–48 h to moisture content of 13% to reduce risk of aflatoxin Nandi, respectively, were not practicing crop rotation but planted formation (Kaaya and Warren, 2005). maize every season on the same plot. Crop rotation ensures increased soil nutrient by nitrogen fixation by legumes and mitigates nitrogen stress. Aflatoxigenic Aspergillus isolates from soils have been shown Shelling (threshing) to be highest in soils that have maize as the following crop (Abbas Shelling or threshing was mainly done by hand, machine, or manual et  al., 2004). Crop rotation in addition to reducing nutrient and pounding using sticks. Manual pounding (maize put in the sack and nitrogen stress helps to break down the selection of toxigenic fungi beaten with sticks) was the most preferred method; being adopted that would infect the follower crop, therefore reducing the risk of pre- by 76.8% and 75.1% of the respondents in Makueni and Nandi, harvest infection, toxin production, and contamination. Only 21.7% respectively, though it is not the recommended method of shell- of the farmers in both counties practiced crop rotation of maize with ing maize as it results in many damaged kernels. Damaged kernels legumes. Failure to practice crop rotation leads to depletion of soil increase the ease by which fungal hyphae penetrate the kernels. Use nutrients, selects fungal populations that specifically infect maize, of seed varieties that have incomplete husk cover also exposes the therefore increasing the risk of colonization by toxigenic fungi and cobs to damage by birds, which results in similar effects of increasing subsequent aflatoxin contamination (Hell et al., 2010). rate of kernel colonization by toxigenic fungi. Management and mitigation of mycotoxin along maize value chain, 2017, Vol. 1, No. 4 271 Use of preservatives during storage et al., 2005). The advantage of this method is that it reduces toxin concentrations to safe levels without production of toxin degrad- About 25% of the farmers in both counties were not adding any ation products or any reduction in the nutritional value of the food. pesticides during storage. Weevils are notorious pests that attack This could be done manually or by using electronic sorters. Table 2 maize in storage and in the field. They cause mechanical damage that shows that women in both Nandi and Makueni could easily identify disrupts the seed coat and facilitates penetration by fungal inocu- fungal-infected grains that could pose a risk of aflatoxin contam- lum. In addition, they transmit spores from other plants to inoculate ination, while insect and pest damaged kernels increase the rate of already defective kernels (Hussaini et al., 2012). It has been shown fungal penetration and colonization. that insects and other pests create microclimates within the storage bags that increase humidity and favor fungal production of aflatox- ins and contamination of the crop (Makun, 2012). The method of Perceptions of health risks associated with use of storage could increase fungal growth and aflatoxin contamination. spoilt grains A majority of the farmers used the recommended storage methods When asked about health risks associated with feeding animals with apart from 39.1% in Nandi who were storing maize in bags in the moldy feeds, the respondents gave responses which were associated house and on the floor. In the two counties, shelled maize was stored with known effects of aflatoxins in livestock (reduced milk produc- in the house (48.6% of respondents) and in the granary (44.3% tion, reduced milk quality, reduced weight gain, increased susceptibil- of respondents). The type of bags used for storage of maize could ity to diseases, death, loss of appetite, and liver problems) (Table 3). favor mycotoxin accumulation. Polypropylene bags were used by all Respondents in Nandi identified more with effects of chronic afla- farmers, and these have been reported to increase moisture content, toxicosis leading to loss of productivity (low milk production, poor which encourages fungal growth with concomitant production of quality milk, and reduced weight gain) while Makueni respondents aflatoxin (Bulaong, 2002; Mutegi et al., 2013). Fungi are aerobic identified more with effects of acute aflatoxicosis (death, liver prob- micro-organisms, and technolgies have been developed that reduce lems, loss of appetite, and susceptibility to diseases). the oxygen content and increase carbon dioxide content to reduce When they were asked as to how they would dispose of moldy the growth of A. flavus during storage and therefore limit aflatoxin or rotten maize, 59% indicated they will use this as animal feed production. In use, currently in Kenya, are metal silos for the stor- while 15% would use the rotten/moldy maize for making traditional age of small quantities of grains and hermetic improved bags (these brews (changaa and busaa). Feeding moldy or rotten maize to live- bags have a second lining which is impermeable to oxygen and thus stock, if that maize was contaminated with aflatoxins, would lead create anaerobic conditions that inhibit growth of fungal spores and to aflatoxin M1 (AFM1) in milk and eventually expose humans to weevils) based on triple bagging developed for storing cow peas (Ben AFM1. We reported a high proportion of milk contaminated with et al., 2009). AFM1 (96% and 52% of milk samples from Makueni and Nandi, respectively, and 93% of goat milk samples from Makueni (Kangethe Sorting of moldy grains et al., unpublished data). When the respondents were asked if milk A majority of the spouse respondents used the colors they saw from animals fed on moldy/rotten maize was safe for consumption, on moldy grains to determine whether grains were moldy or not. 54.1% considered the milk safe. Of this, 75.1% and 24.9% were Using expert opinion, the colors they give were matched with colors from Nandi and Makueni, respectively. This clearly reveals lack of produced by Aspergillus and Fusarium species when they grew on awareness of the transition of aflatoxins in animal feeds to milk and maize substrate (Table  2). These results show that co-occurrence the risk posed by consuming such contaminated animal products. of Aspergillus and Fusarium species are the major contaminants of Traditional brewing methods do not detoxify the brews if made maize in Makueni and Nandi. Kangethe et  al. (unpublished data) from contaminated foodstuffs. Fumonisins have been detected showed that 60% and 85%; and 55% and 75% of homegrown and in local brews in Botswana (Nkwe et  al., 2012) and South Africa market maize samples in Nandi and Makueni, respectively, were con- (Shephard et al., 2005). Fumonisins and other mycotoxins have been taminated with both aflatoxin and fumonisin. Aspergillus separately detected in Kenyan beers (Mbugua and Gathumbi, 2004). Fifteen per- was five and four times more frequent as a contaminant of maize cent would use these rotten moldy maize to make traditional brews. in Makueni and Nandi, respectively, than Fusarium species. Sorting When the respondents were asked what was the minimum level out physically damaged and infected grains (known from colora- or type of spoilage, when they would still consume moldy/rotten tions, odd shapes, and size) from the intact commodity can result maize, 52.4% replied they would eat despite the level of spoilage. in 40%–80% reduction in aflatoxin levels (Park, 2002; Fandohan Out of this proportion, 57.7% and 42.3% were from Makueni and Table  2. Ability of women to detect spoilt maize using colors seen on spoilt grains and linked to those produced by Aspergillus and Fusarium species growing on maize. County n Criteria for Spoilt a b c Aspergillus and Fusarium (%) Aspergillus (%) Pests/insects damage (%) Others (%) Fusarium (%) Makueni 433 44.6 22.4 19.4 9.2 4.4 Nandi 424 59.9 14.9 9.2 12.5 3.5 Black with red or yellow or brown or maroon or orange, yellow with green or blue. Black, green, black/brown, green/brown. Red, yellow, maroon, red/yellow, and red/purple. Others = Smelling, sprouting, and bitter taste; n = number of respondents in each county; (%) = proportion of respondents who mentioned colors produced by the fungal species. 272 E. K. Kang’ethe et al., 2017, Vol. 1, No. 4 Table  3. Perceptions of health risks associated with feeding ani- weight, treatment costs resulting in income loss); (v) loss of labor mals on moldy maize in Nandi and Makueni. (chronic exposure leads to immunosuppresion with subsequent frequent bouts of illness with many days on sick leave); (vi) afla- Risks to livestock n County toxins and fumonisins are antinutritional and contribute to stunt- ing and wasting in children; and (vii) contaminated foods and feeds Makueni Nandi are condemned and are threat to the country’s food security. They Reduce milk production 15 26.7 73.3 suggested various good agricultural practices as mitigation meas- Reduce milk quality 110 21.9 78.1 ures, as described in Figure 1. The government has adopted various Reduce weight gain 3 66.6 33.3 strategies to mitigate the problem of mycotoxins and food security. Susceptible to diseases 120 64.2 35.8 These include (i) establishment by the government of 1 million acres Death 44 97.7 2.3 under irrigation in Tana Delta under the water master plan 2030 Loss of appetite 8 50.0 50.0 (JICA, 2014) to stop dependence on rain for agriculture in growing Liver problems 7 85.7 14.3 mainly maize (Citing for the reference Uhuru Kenyatta appearing Others 4 75.0 25.0 in the reference list.); (ii) adoption of the East-African harmonized standards on marketed maize, which includes aflatoxin control (KS Nandi, respectively. The reasons given for eating such maize were: if EAS2, 2005); (iii) provision of subsidized agroecologically recom- not all the maize is spoilt, if not bitter, if not so mouldy, if there is a mended and certified seeds and fertilizer to farmers in order to grow slight color change or smell, and if no alternative food was available. more food for home and market; and (iv) as agriculture is a devolved This clearly shows lack of awareness and poverty (population living function, county governments are employing extension officers to below poverty line 47.4% and 64.1% Nandi and Makueni, respec- carry out extension messages in support of farming activities. While tively, CRA, 2011) as the main reasons for consuming overtly spoilt regulation helps to reduce exposure if enforced, grains marketed in or moldy maize. The average estimates of maize lost in Makueni and Kenya should comply with KS EAS2 (2005), which limits the mois- Nandi by being moldy or rotten were 7.5% and 6.8%, respectively. ture content of less than 13%, broken, discolored, rotten, and dis- This translated into KShs 1667 and KShs 2856 per household in eased, pest-damaged grains should be less than 4% and aflatoxin Makueni and Nandi per season, respectively. It is imperative that concentrations less than 5 ppb for aflatoxin B1 (AFB1) and 10 ppb such losses are controlled to increase food security and reduce expo- for total aflatoxins. Ninety percent of the rural households in Kenya sure at households. grow maize, and the maize production is dominated by small-scale Kenya has relied heavily on creating awareness among the farmers who produce 75% of the overall maize yield (Kang’ethe, farming communities on ways to mitigate preharvest and post- 2011). Smallholder farmers depend more on homegrown maize harvest problems that exacerbate aflatoxin and fumonisin pro- for household consumption and less on market-purchased grains. duction. This approach is hampered by the shortage of extension They would be less affected by the demands of aflatoxin content officers in the field. The ratio of extension officers to the farmers regulation and would continue to be prone to aflatoxin exposure in the country is about 1:5000 (GFRAS, 2017). Bandyopadhyay through consumption of homegrown maize if mitigation steps are et  al., (2008) using a nominal group discussion technique iden- not adopted. tified and prioritized communication (knowledge) as an impor - Although it may appear as if the majority of the farmers are tant barrier to farmers and consumers understanding the risks of adopting good agricultural practices (Table 1) that would additively mycotoxins in their food and especially low-grade exposure and help to control the negative effects of mycotoxin exposure, the real- their long-term effects. ity is that this proportion is very large but the effects are minimal A majority of the households in Nandi and Makueni do not because what is done is not done properly and consistently. When understand that if maize is moldy, it could be a risk to health and the proportion of those that were not practicing crop rotation and could be contaminated with aflatoxins and fumonisins. Equally, had samples that were positive for aflatoxin were compared to the if households in Makueni were to intensify the adoption of good proportion of homegrown maize that was positive for aflatoxins, agricultural practices, this could bring down the proportions and this differed significantly (χ   =  6.82, df  =  1, P  =  0.009) between level of contamination and points to the need to create awareness Makueni and Nandi. Significant differences were also observed in at the household level on the causes of contamination of cereals and the proportions of households who did not use soil amendments animal source foods with aflatoxins and fumonisins and mitigation (χ   =  10.27, df  =  1, P  =  0.001), shelled their maize manually by measures to reduce exposure to mycotoxins. pounding (χ   =  4.44, df  =  1, P  =  0.04), and did not use chemicals as preservatives (χ   =  6.82, df  =  1, P  =  0.009). This indicates that Government contribution to good agricultural an increase in the use of good agricultural practices of crop rota- practices tion, application of soil amendments, a reduction on pounding The 200 officers from the county governments (from health, agricul- while shelling, and the adoption of chemical use as preservatives in ture, and county administration) who attended the three workshops, Makueni will significantly bring down the proportions of the posi- one in Nandi and two in Makueni, said that the problem of myco- tive samples for aflatoxins and fumonisins closer to those witnessed toxins is serious and required mitigation. The reasons indicated were in Nandi. However, a comparison of the proportions of the maize that the two mycotoxins: (i) are carcinogens, mutagens and terato- dried on the ground and no canvas to the proportions of positive gens, (ii) result in deaths when they occur and cause psychosocial samples for aflatoxins did not differ significantly (χ  = 2.68, df = 1, problems and put a greater burden on the households that are living P = 0.10) between Makueni and Nandi. This may not be singly the below the poverty line; (iii) are associated with loss of production result of better adoption of agricultural practices, but other factors (reduced milk and egg production, poor quality of animal source like nature of aflatoxigenic A. avus fl found in Makueni and Nandi products, and reduced weight gain); (iv) increase production costs may be contributing to the better effects of good agricultural prac- (increased susceptibility to diseases, takes longer to reach market tices in Nandi compared to Makueni (Okoth et al., 2012). Management and mitigation of mycotoxin along maize value chain, 2017, Vol. 1, No. 4 273 Figure 1. Good agricultural and husbandry practices recommended by policy teams from National and County governments of Nandi and Makueni to mitigate aflatoxins and fumonisins at household level. Waliyar et  al. (2013) reported that good agricultural practices in Ben, D., Liem, P., Dao, N., Gummert, M., Rickman, J. (2009). Effect of her- metic storage in the super bag on seed quality and milled rice quality groundnut production, for instance application of farmyard manure, of different varieties in Bac Lieu, Vietnam. International Rice Research reduces aflatoxins during the preharvest period by 42% while combination Notes, 31(2). Retrieved 12 February 2010, http://www.philjol.info/index. with lime application results in aflatoxin reduction of 84%. Post-harvest php/IRRN/article/view/1138/1035. good agricultural practices were found to reduce aflatoxin contamina- Bulaong, S. S. P. (2002). Fungal population, aflatoxin and free fatty acid con- tion by 66%–88% depending on the location. The authors advocate that tents of peanuts packed in different bag types. Biotropia 19: 1–25. good agricultural practices are the bare basic minimum (prerequisites) on CAST. (2003). Mycotoxins: Risks in plant, animal and human systems. Task which other technologies can build to substantially reduce aflatoxin and force report No.139 Council for Agricultural Science and Technology. fumonisin preharvest and post-harvest contamination. Ames, Iowa, USA. CRA, Commission on Revenue Allocation, Kenya. (2011). Kenya County Fact Sheet. Government Printers, Kenya. Acknowledgements Codex Alimentarius Commission. (2004). Code of practice for the prevention and reduction of aflatoxins contamination in peanuts. Retrieved 13 May The authors wish to thank the Ministry for Foreign Affairs of Finland for 2011. http://www.codexalimentarius.net/download/standards/10084/ providing financial assistance that enabled this study (MFA 24819801); the CXC_055_2004e. pdf. communities in Nandi and Makueni for allowing us to carry out the study Cotty, P.J. (1994). Influence of field application of an Atoxigenic strain of and Government officers in both counties for their facilitation. The views Aspergillus flavus on the population of A. flavus infecting cotton bolls expressed in this paper are not necessarily those of the funding agency or and on aflatoxin content of cotton seed. Phytopathology 84: 1270–1277. institutions taking part in the study, but those of the authors. Clarke, R., Fattori, V. (2013). Codex standards: A global tool for aflatoxins management. In: Unnevehr L., Grace D. (eds.). Aflatoxins: Finding solu- Conflict of interest statement. 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Management and mitigation of health risks associated with the occurrence of mycotoxins along the maize value chain in two counties in Kenya

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Oxford University Press
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© The Author(s) 2017. Published by Oxford University Press on behalf of Zhejiang University Press.
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2399-1399
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2399-1402
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10.1093/fqsafe/fyx025
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Abstract

Aflatoxins and fumonisins are two mycotoxins that are prevalent in cereals. Both toxins have associated and causal health effects in humans and livestock. Once formed in the substrates, the toxins are not easily destroyed. The preferred mitigation is to prevent contamination of the cereals and animal source foods. In this paper we set out to examine the practices of the farmers in two counties (Nandi and Makueni) in Kenya which exacerbates aflatoxin contamination and the government steps to address the issue in the agriculture and livestock sectors. The practices identified in Nandi and Makueni, respectively, included seed varieties where 19.3% and 56% are using local varieties; use of soil amendments where 5.8% and 181 % are not using any amendments; crop rotation where 54.6% and 60.5% are not practicing crop rotation; 22.7% and 37.5% are using wrong drying methods; and 53% and 77.1% are using poor threshing methods. The Kenya government is subsidizing fertilizers, seeds, increasing areas under irrigation, and providing extension services to build capacity of farmers to mitigate aflatoxin contamination. The paper examines also the cultural practices in land preparation, tillage, crop rotation, drying, sorting at farm, and proper storage as better alternative practices for easy adoption that would, if adopted, lead to a decrease in aflatoxin and fumonisin contamination and therefore reduce household exposure. Good agricultural practices should be a prerequisite for the adoption of other aflatoxin control technologies. Key words: Aflatoxins; Fumonisins; Contamination; Maize value chains; Mitigations; Kenya. fatality of 39.4% (Lewis et al., 2005). Subsequent outbreaks have Introduction also resulted in loss of life. Aflatoxins and fumonisins are the major Kenya has had a problem with mycotoxicosis as evidenced by the fungal toxins that contaminate and have been detected in cereals in 2004/2005 aflatoxin outbreak, which resulted in the high case © The Author(s) 2017. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Management and mitigation of mycotoxin along maize value chain, 2017, Vol. 1, No. 4 269 Kenya (Mutiga et al., 2015). In addition to acute toxicity that leads barley growing. Makueni falls within the lower midland agroeco- to loss of life in case of aflatoxins, chronic exposure to the toxins logical zones LM3, LM4, and LM5. It receives between 200 and has been associated with public health concerns and food security. 1200 mm of rainfall per year, which is unreliable at times with fre- Chronic exposure of humans to aflatoxins has been associated quent droughts resulting in crop failures. with immunosuppression (Williams et  al., 2004) and carcinogens causing liver cancer (Wu et  al., 2011). International Agency for Data collection tools Research on Cancer (IARC) estimates that liver cancer incidences A questionnaire was administered to heads or their spouses of in Kenya associated with aflatoxin are 8.5 and 4.9/100 000 cases selected households in Nandi and Makueni. The questionnaire for males and females, respectively (Wu et  al., 2011). There is no sought to capture data on agricultural practices (use of soil amend- direct causal relationship between aflatoxin exposure and stunting ments, seed varieties, crop rotation, harvesting, threshing, drying, in children but a high correlation between the two has been estab- sorting, and storage) during the maize cropping season. lished (Gong et  al., 2004; Leroy, 2013). It has been estimated that Data relating to use, disposal of moldy grains, and health risk per- 25% of the world’s grains are contaminated with aflatoxins (CAST, ceptions associated with consumption of moldy maize were obtained 2003), which would cause a serious world food security threat if by asking the respondents what they used to determine that the maize the contaminated grains are removed from the food supply chain. was spoilt or moldy. In this regard, the researchers gave respond- Fumonisins have been suspected risk factors for human disease such ent women (women are responsible for family food preparation. as esophageal cancer (Marasas, 2001; Wakhisi et  al., 2005) and Determining what is safe for family meals is their responsibility and neural tube defects (Meismer et al., 2006). While a causal relation- were best suited to give information) during the questionnaire admin- ship in human disease is unproven, fumonisins are recognized causes istration a handful of maize that had good and moldy grains. They of equine leukoencephalomalacia (Kellerman, 1990), toxic feed syn- were asked to sort out the good and the bad ones. After the exercise, drome in poultry, and porcine pulmonary edema syndrome in swine they were asked to explain what criteria they used to sort out the (Ross et al., 1993; Norred and Voss, 1994). maize. They too were asked what was the minimum level or type of Mitigation of aflatoxin and fumonisin contamination can be spoilage that would allow consumption of moldy or spoilt grains; the targeted to preharvest and post-harvest periods to prevent plant methods they used to dispose of spoilt or moldy grains; the percep- infection and grain contamination. During preharvest, good agricul- tion of health risks associated with feeding animals with moldy grains; tural practices reduce the vulnerability of crops to fungal infection and whether they considered milk from animals fed moldy grains to (Munkvold, 2003). Post-harvest practices help to prevent mycotoxin be safe. development in the grains. Other mitigation technologies include bio- The data collected through questionnaire were triangulated by logical control (Cotty, 1994) and use of enterosorbents and chemo- group discussions that employed a discussion guide with county reception to prevent absorption of the toxins in exposed individuals extension officers. Three workshops were held with county exten- (Kensler et al., 2013; Miller et al., 2014). This paper investigates the sion officers, which captured the role of the central and county extent to which farmers are adopting good agricultural (cultural) governments in the management of the aflatoxin and fumonisin con- management practices which are known to mitigate aflatoxin and tamination through group discussions on whether they considered fumonisin contamination of cereals at pre-harvest and post-harvest the problem worth mitigating and the measures they would adopt to period in the two counties of Makueni and Nandi, Kenya. control the problem in the counties. Results and discussion Materials and methods Good agricultural practices Site and household selection Five hundred and forty-one questionnaires were administered; for The counties Nandi and Makueni in Kenya were purposively which 280 respondents were from Makueni and 261 from Nandi. selected based on history of human acute aflatoxicosis in Makueni The study evaluated a number of agricultural practices as shown in (Lewis et  al., 2005)) and high incidences of esophageal cancer in Table 1. Nandi (Wakhisi et al., 2005). At the county level, a team consisting of the researchers, veterinary, agriculture extension, and health offic- Land preparation ers selected three subcounties that best fitted the criteria of high dairy production and maize growing activities. At the subcounty and ward During the preharvest stage in a maize cropping season, farmers in level, the extension officers selected the ward and the sublocation, Nandi were better than their counterparts in Makueni in adopting respectively, that best fitted the same criteria. With the assistance good agricultural practices. Adoption of good practices along the of village elders (managers), the households that had dairy animals food value chain has been proposed as the best way to reduce levels (cattle or goats); grew maize, sorghum, and/or millet; had a child of fungal toxins in the food supply (Clarke and Fattori, 2013). This below 5 years or the spouse was pregnant at the time were listed. study did not evaluate land tillage practices. However, fungal popu- Based on the population and number of households in the sub- lation densities have been shown to be affected by land preparation location and the households that fitted the criteria, a proportion of methods. Nesci et al. (2006) and Zablotowisc et al. (2007) compared the households was randomly selected for sampling (Martin et  al., the Aspergillus flavus density in land with no tillage and land with 1987), and the household sample size was corrected for finite popu- reduced tillage and found that land with no tillage and medium till- lation according to Daniel (1999). age with grazing had high A. avus fl density compared with land with Nandi falls within the agroecological zones of lower humid deep tillage. This was attributed to high organic matter content in highlands to upper midland and upper highland zones ((LH2, LH3, land with no tillage. Communities in Makueni use oxen ploughs and UM3, and UM4) (Jaetzold et al., 2006). It lies between 1300 to 2500 may not practice deep tillage compared to the communities in Nandi m above sea level and receives about 1200–2000  mm of rain per who use tractors for ploughing after each crop season. Okoth et al. year. Nandi is best suited for tea, dairy activities, maize, wheat, and (2012) found that A. avus fl was the most prevalent contaminant of 270 E. K. Kang’ethe et al., 2017, Vol. 1, No. 4 Table  1. The extent of adoption of good agricultural practices in Use of soil amendments Makueni and Nandi counties. In both counties, majority of the farmers were using fertilizers, fertilizer and animal manure, and animal manure as soil amend- Agricultural practices County ments. Only 17.9% and 6.1% of the farmers in Makueni and Makueni, % (n) Nandi, % (n) Nandi, respectively, were reported not using any soil amendments. The nature and fertility of the soil help to reduce fungal infec- Preharvest tion of crops. The ability of the soil to hold moisture is import- Use of certified seed 44.0 (273) 100 (259) ant. Codex Alimentarius Commission (2004) reported that crops varieties planted on sandy soils were more contaminated with aflatoxins Use of soil amendments 82.1 (280) 93.9 (261) than those planted on loamy soils. Loamy soils have the ability Practice crop rotation 16.4 (280) 25.3 (261) to retain moisture, which reduces moisture stress to the growing Post-harvest crops and therefore prevents fungal infection. In Kenya, farmers Harvesting Stoking 55.4 (280) 49.0 (261) use fertilizer and manure to increase the soil nutrient content to Remove cobs leave 42.5 (280) 48.7 (261) ensure a healthy crop that would resist fungal infection. Manure stovers standing (animal or compost) has the dual role of increasing the organic Drying on canvas 60.7 (280) 72.4 (261) content of the soil and also nutrients, both of which mitigate fun- Shelling gal infection by ensuring healthy crops. Lime application, use of Hand 11.4 (280) 14.6 (261) farm yard manure and cereal crop residues as soil amendments are Machine 11.4 (280) 30.7 (261) effective in reducing A.  avus fl contamination as well as aflatoxin Manual pounding 76.8 (280) 52.1 (261) levels by 50%–90% (Hell and Mutegi, 2011). In Makueni and Use of chemical pre- 77.9 (280) 75.1 (261) Nandi, 81.9% and 79.7% of the farmers, respectively, applied fer- servatives tilizer only as soil amendments while 22% of the farmers in both Storage methods Raised granaries 97.3 (110) 96.0 (126) Nandi and Makueni applied a mixture of fertilizer and manure On pallets in the house 89.6 (144) 60.9 (115) during planting. Failure to use soil amendments results in soils Raised crib 88.0 (25) 100 (13) that are low in organic nutrients with low ability to hold moisture, and this increases the vulnerability of the crops to fungal infection because of water and nutrient stress (Munkvold, 2003). maize in both counties with an incidence of 82.33% and 73.26%, in Nandi and Makueni, respectively. Harvesting and drying During the harvesting period, the methods of harvesting were Certified seeds mainly stoking and removing the cobs and leaving the stovers All the respondents in Nandi planted recommended and certified standing in the field. Fifty percent of farmers, both in Nandi and seeds for the agroecological zones compared to 56% of the farm- Makueni, cut maize stovers with the cobs and stoked them in ers in Makueni who were using local varieties. National and inter- heaps in the field to dry. There was no method that was more pre- national seed producing companies in Kenya had released over 164 ferred by farmers. Such practices expose the crop to proliferation varieties by 2009 (Kang’ethe, 2011). These varieties, though not fun- of fungi and bacteria and contamination with soil, reducing the gal resistant, are tested for pest and disease resistance, drought, and crop’s quality (Mejia and Farruci).The recommended maize-dry- low nitrogen tolerance in addition to being high yielding. They are ing method was either on cob or as shelled grains on canvas. Of ecologically adapted. In Nandi and Makueni, 19.3% and 56% of the farmers, 39.1% and 37.6% in Makueni and Nandi, respect- the farmers were using noncertified local variety seeds, which could ively, were not drying maize on canvas but on cob on ground and be susceptible to fungal infection though they are adapted to local leaving maize to dry in the field on stovers while standing. This conditions as a result of many years of selection. These varieties have practice increases the risk of picking up toxigenic fungal spores very low yields and are not consistent with the government policy of from the soil, thus adding to the risk of aflatoxin production and revitalizing agriculture as a business enterprise (SRA, 2004). accumulation. The moisture level of the grains is an important factor in toxin production. Grains with moisture level above 13% are more prone to aflatoxin contamination than those with Crop rotation lower moisture content. Harvested grains should be dried within The farmers in both counties, 83.6% and 74.7% in Makueni and 24–48 h to moisture content of 13% to reduce risk of aflatoxin Nandi, respectively, were not practicing crop rotation but planted formation (Kaaya and Warren, 2005). maize every season on the same plot. Crop rotation ensures increased soil nutrient by nitrogen fixation by legumes and mitigates nitrogen stress. Aflatoxigenic Aspergillus isolates from soils have been shown Shelling (threshing) to be highest in soils that have maize as the following crop (Abbas Shelling or threshing was mainly done by hand, machine, or manual et  al., 2004). Crop rotation in addition to reducing nutrient and pounding using sticks. Manual pounding (maize put in the sack and nitrogen stress helps to break down the selection of toxigenic fungi beaten with sticks) was the most preferred method; being adopted that would infect the follower crop, therefore reducing the risk of pre- by 76.8% and 75.1% of the respondents in Makueni and Nandi, harvest infection, toxin production, and contamination. Only 21.7% respectively, though it is not the recommended method of shell- of the farmers in both counties practiced crop rotation of maize with ing maize as it results in many damaged kernels. Damaged kernels legumes. Failure to practice crop rotation leads to depletion of soil increase the ease by which fungal hyphae penetrate the kernels. Use nutrients, selects fungal populations that specifically infect maize, of seed varieties that have incomplete husk cover also exposes the therefore increasing the risk of colonization by toxigenic fungi and cobs to damage by birds, which results in similar effects of increasing subsequent aflatoxin contamination (Hell et al., 2010). rate of kernel colonization by toxigenic fungi. Management and mitigation of mycotoxin along maize value chain, 2017, Vol. 1, No. 4 271 Use of preservatives during storage et al., 2005). The advantage of this method is that it reduces toxin concentrations to safe levels without production of toxin degrad- About 25% of the farmers in both counties were not adding any ation products or any reduction in the nutritional value of the food. pesticides during storage. Weevils are notorious pests that attack This could be done manually or by using electronic sorters. Table 2 maize in storage and in the field. They cause mechanical damage that shows that women in both Nandi and Makueni could easily identify disrupts the seed coat and facilitates penetration by fungal inocu- fungal-infected grains that could pose a risk of aflatoxin contam- lum. In addition, they transmit spores from other plants to inoculate ination, while insect and pest damaged kernels increase the rate of already defective kernels (Hussaini et al., 2012). It has been shown fungal penetration and colonization. that insects and other pests create microclimates within the storage bags that increase humidity and favor fungal production of aflatox- ins and contamination of the crop (Makun, 2012). The method of Perceptions of health risks associated with use of storage could increase fungal growth and aflatoxin contamination. spoilt grains A majority of the farmers used the recommended storage methods When asked about health risks associated with feeding animals with apart from 39.1% in Nandi who were storing maize in bags in the moldy feeds, the respondents gave responses which were associated house and on the floor. In the two counties, shelled maize was stored with known effects of aflatoxins in livestock (reduced milk produc- in the house (48.6% of respondents) and in the granary (44.3% tion, reduced milk quality, reduced weight gain, increased susceptibil- of respondents). The type of bags used for storage of maize could ity to diseases, death, loss of appetite, and liver problems) (Table 3). favor mycotoxin accumulation. Polypropylene bags were used by all Respondents in Nandi identified more with effects of chronic afla- farmers, and these have been reported to increase moisture content, toxicosis leading to loss of productivity (low milk production, poor which encourages fungal growth with concomitant production of quality milk, and reduced weight gain) while Makueni respondents aflatoxin (Bulaong, 2002; Mutegi et al., 2013). Fungi are aerobic identified more with effects of acute aflatoxicosis (death, liver prob- micro-organisms, and technolgies have been developed that reduce lems, loss of appetite, and susceptibility to diseases). the oxygen content and increase carbon dioxide content to reduce When they were asked as to how they would dispose of moldy the growth of A. flavus during storage and therefore limit aflatoxin or rotten maize, 59% indicated they will use this as animal feed production. In use, currently in Kenya, are metal silos for the stor- while 15% would use the rotten/moldy maize for making traditional age of small quantities of grains and hermetic improved bags (these brews (changaa and busaa). Feeding moldy or rotten maize to live- bags have a second lining which is impermeable to oxygen and thus stock, if that maize was contaminated with aflatoxins, would lead create anaerobic conditions that inhibit growth of fungal spores and to aflatoxin M1 (AFM1) in milk and eventually expose humans to weevils) based on triple bagging developed for storing cow peas (Ben AFM1. We reported a high proportion of milk contaminated with et al., 2009). AFM1 (96% and 52% of milk samples from Makueni and Nandi, respectively, and 93% of goat milk samples from Makueni (Kangethe Sorting of moldy grains et al., unpublished data). When the respondents were asked if milk A majority of the spouse respondents used the colors they saw from animals fed on moldy/rotten maize was safe for consumption, on moldy grains to determine whether grains were moldy or not. 54.1% considered the milk safe. Of this, 75.1% and 24.9% were Using expert opinion, the colors they give were matched with colors from Nandi and Makueni, respectively. This clearly reveals lack of produced by Aspergillus and Fusarium species when they grew on awareness of the transition of aflatoxins in animal feeds to milk and maize substrate (Table  2). These results show that co-occurrence the risk posed by consuming such contaminated animal products. of Aspergillus and Fusarium species are the major contaminants of Traditional brewing methods do not detoxify the brews if made maize in Makueni and Nandi. Kangethe et  al. (unpublished data) from contaminated foodstuffs. Fumonisins have been detected showed that 60% and 85%; and 55% and 75% of homegrown and in local brews in Botswana (Nkwe et  al., 2012) and South Africa market maize samples in Nandi and Makueni, respectively, were con- (Shephard et al., 2005). Fumonisins and other mycotoxins have been taminated with both aflatoxin and fumonisin. Aspergillus separately detected in Kenyan beers (Mbugua and Gathumbi, 2004). Fifteen per- was five and four times more frequent as a contaminant of maize cent would use these rotten moldy maize to make traditional brews. in Makueni and Nandi, respectively, than Fusarium species. Sorting When the respondents were asked what was the minimum level out physically damaged and infected grains (known from colora- or type of spoilage, when they would still consume moldy/rotten tions, odd shapes, and size) from the intact commodity can result maize, 52.4% replied they would eat despite the level of spoilage. in 40%–80% reduction in aflatoxin levels (Park, 2002; Fandohan Out of this proportion, 57.7% and 42.3% were from Makueni and Table  2. Ability of women to detect spoilt maize using colors seen on spoilt grains and linked to those produced by Aspergillus and Fusarium species growing on maize. County n Criteria for Spoilt a b c Aspergillus and Fusarium (%) Aspergillus (%) Pests/insects damage (%) Others (%) Fusarium (%) Makueni 433 44.6 22.4 19.4 9.2 4.4 Nandi 424 59.9 14.9 9.2 12.5 3.5 Black with red or yellow or brown or maroon or orange, yellow with green or blue. Black, green, black/brown, green/brown. Red, yellow, maroon, red/yellow, and red/purple. Others = Smelling, sprouting, and bitter taste; n = number of respondents in each county; (%) = proportion of respondents who mentioned colors produced by the fungal species. 272 E. K. Kang’ethe et al., 2017, Vol. 1, No. 4 Table  3. Perceptions of health risks associated with feeding ani- weight, treatment costs resulting in income loss); (v) loss of labor mals on moldy maize in Nandi and Makueni. (chronic exposure leads to immunosuppresion with subsequent frequent bouts of illness with many days on sick leave); (vi) afla- Risks to livestock n County toxins and fumonisins are antinutritional and contribute to stunt- ing and wasting in children; and (vii) contaminated foods and feeds Makueni Nandi are condemned and are threat to the country’s food security. They Reduce milk production 15 26.7 73.3 suggested various good agricultural practices as mitigation meas- Reduce milk quality 110 21.9 78.1 ures, as described in Figure 1. The government has adopted various Reduce weight gain 3 66.6 33.3 strategies to mitigate the problem of mycotoxins and food security. Susceptible to diseases 120 64.2 35.8 These include (i) establishment by the government of 1 million acres Death 44 97.7 2.3 under irrigation in Tana Delta under the water master plan 2030 Loss of appetite 8 50.0 50.0 (JICA, 2014) to stop dependence on rain for agriculture in growing Liver problems 7 85.7 14.3 mainly maize (Citing for the reference Uhuru Kenyatta appearing Others 4 75.0 25.0 in the reference list.); (ii) adoption of the East-African harmonized standards on marketed maize, which includes aflatoxin control (KS Nandi, respectively. The reasons given for eating such maize were: if EAS2, 2005); (iii) provision of subsidized agroecologically recom- not all the maize is spoilt, if not bitter, if not so mouldy, if there is a mended and certified seeds and fertilizer to farmers in order to grow slight color change or smell, and if no alternative food was available. more food for home and market; and (iv) as agriculture is a devolved This clearly shows lack of awareness and poverty (population living function, county governments are employing extension officers to below poverty line 47.4% and 64.1% Nandi and Makueni, respec- carry out extension messages in support of farming activities. While tively, CRA, 2011) as the main reasons for consuming overtly spoilt regulation helps to reduce exposure if enforced, grains marketed in or moldy maize. The average estimates of maize lost in Makueni and Kenya should comply with KS EAS2 (2005), which limits the mois- Nandi by being moldy or rotten were 7.5% and 6.8%, respectively. ture content of less than 13%, broken, discolored, rotten, and dis- This translated into KShs 1667 and KShs 2856 per household in eased, pest-damaged grains should be less than 4% and aflatoxin Makueni and Nandi per season, respectively. It is imperative that concentrations less than 5 ppb for aflatoxin B1 (AFB1) and 10 ppb such losses are controlled to increase food security and reduce expo- for total aflatoxins. Ninety percent of the rural households in Kenya sure at households. grow maize, and the maize production is dominated by small-scale Kenya has relied heavily on creating awareness among the farmers who produce 75% of the overall maize yield (Kang’ethe, farming communities on ways to mitigate preharvest and post- 2011). Smallholder farmers depend more on homegrown maize harvest problems that exacerbate aflatoxin and fumonisin pro- for household consumption and less on market-purchased grains. duction. This approach is hampered by the shortage of extension They would be less affected by the demands of aflatoxin content officers in the field. The ratio of extension officers to the farmers regulation and would continue to be prone to aflatoxin exposure in the country is about 1:5000 (GFRAS, 2017). Bandyopadhyay through consumption of homegrown maize if mitigation steps are et  al., (2008) using a nominal group discussion technique iden- not adopted. tified and prioritized communication (knowledge) as an impor - Although it may appear as if the majority of the farmers are tant barrier to farmers and consumers understanding the risks of adopting good agricultural practices (Table 1) that would additively mycotoxins in their food and especially low-grade exposure and help to control the negative effects of mycotoxin exposure, the real- their long-term effects. ity is that this proportion is very large but the effects are minimal A majority of the households in Nandi and Makueni do not because what is done is not done properly and consistently. When understand that if maize is moldy, it could be a risk to health and the proportion of those that were not practicing crop rotation and could be contaminated with aflatoxins and fumonisins. Equally, had samples that were positive for aflatoxin were compared to the if households in Makueni were to intensify the adoption of good proportion of homegrown maize that was positive for aflatoxins, agricultural practices, this could bring down the proportions and this differed significantly (χ   =  6.82, df  =  1, P  =  0.009) between level of contamination and points to the need to create awareness Makueni and Nandi. Significant differences were also observed in at the household level on the causes of contamination of cereals and the proportions of households who did not use soil amendments animal source foods with aflatoxins and fumonisins and mitigation (χ   =  10.27, df  =  1, P  =  0.001), shelled their maize manually by measures to reduce exposure to mycotoxins. pounding (χ   =  4.44, df  =  1, P  =  0.04), and did not use chemicals as preservatives (χ   =  6.82, df  =  1, P  =  0.009). This indicates that Government contribution to good agricultural an increase in the use of good agricultural practices of crop rota- practices tion, application of soil amendments, a reduction on pounding The 200 officers from the county governments (from health, agricul- while shelling, and the adoption of chemical use as preservatives in ture, and county administration) who attended the three workshops, Makueni will significantly bring down the proportions of the posi- one in Nandi and two in Makueni, said that the problem of myco- tive samples for aflatoxins and fumonisins closer to those witnessed toxins is serious and required mitigation. The reasons indicated were in Nandi. However, a comparison of the proportions of the maize that the two mycotoxins: (i) are carcinogens, mutagens and terato- dried on the ground and no canvas to the proportions of positive gens, (ii) result in deaths when they occur and cause psychosocial samples for aflatoxins did not differ significantly (χ  = 2.68, df = 1, problems and put a greater burden on the households that are living P = 0.10) between Makueni and Nandi. This may not be singly the below the poverty line; (iii) are associated with loss of production result of better adoption of agricultural practices, but other factors (reduced milk and egg production, poor quality of animal source like nature of aflatoxigenic A. avus fl found in Makueni and Nandi products, and reduced weight gain); (iv) increase production costs may be contributing to the better effects of good agricultural prac- (increased susceptibility to diseases, takes longer to reach market tices in Nandi compared to Makueni (Okoth et al., 2012). Management and mitigation of mycotoxin along maize value chain, 2017, Vol. 1, No. 4 273 Figure 1. Good agricultural and husbandry practices recommended by policy teams from National and County governments of Nandi and Makueni to mitigate aflatoxins and fumonisins at household level. Waliyar et  al. (2013) reported that good agricultural practices in Ben, D., Liem, P., Dao, N., Gummert, M., Rickman, J. (2009). Effect of her- metic storage in the super bag on seed quality and milled rice quality groundnut production, for instance application of farmyard manure, of different varieties in Bac Lieu, Vietnam. International Rice Research reduces aflatoxins during the preharvest period by 42% while combination Notes, 31(2). Retrieved 12 February 2010, http://www.philjol.info/index. with lime application results in aflatoxin reduction of 84%. Post-harvest php/IRRN/article/view/1138/1035. good agricultural practices were found to reduce aflatoxin contamina- Bulaong, S. S. P. (2002). 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