International Livestock Research Institute Food safety landscape analysis: The maize value chain in Kenya June 2020 i © 2020 International Livestock Research Institute (ILRI) ILRI thanks all donors and organizations which globally support its work through their contributions to the CGIAR Trust Fund This publication is copyrighted by the International Livestock Research Institute (ILRI). It is licensed for use under the Creative Commons Attribution 4.0 International Licence. To view this licence, visit https://creativecommons.org/licenses/by/4.0. Unless otherwise noted, you are free to share (copy and redistribute the material in any medium or format), adapt (remix, transform and build upon the material) for any purpose, even commercially, under the following conditions: ATTRIBUTION. The work must be attributed, but not in any way that suggests endorsement by ILRI or the author(s). NOTICE: For any reuse or distribution, the licence terms of this work must be made clear to others. Any of the above conditions can be waived if permission is obtained from the copyright holder. Nothing in this licence impairs or restricts the author’s moral rights. Fair dealing and other rights are in no way affected by the above. The parts used must not misrepresent the meaning of the publication. ILRI would appreciate being sent a copy of any materials in which text, photos etc. have been used. Written by Erastus Kang’ethe, Florence Mutua, Kristina Roesel and Delia Grace Editing and formatting: Tezira Lore Citation: Kang’ethe, E., Mutua, F., Roesel, K. and Grace, D. 2020. Food safety landscape analysis: The maize value chain in Kenya. Nairobi, Kenya: ILRI. ii Contents List of figures ................................................................................................................................................... iii List of tables ..................................................................................................................................................... iii Abbreviations and acronyms ............................................................................................................................. iv Executive summary ........................................................................................................................................... v Introduction ..................................................................................................................................................... 1 Maize standards ............................................................................................................................................... 2 Maize trade ..................................................................................................................................................... 3 Value chain actors ............................................................................................................................................. 3 Input suppliers ................................................................................................................................................. 4 Farmers ......................................................................................................................................................... 4 Marketers ....................................................................................................................................................... 5 Assemblers ................................................................................................................................................ 5 Wholesale traders...................................................................................................................................... 5 Dis-assemblers .......................................................................................................................................... 5 Millers ........................................................................................................................................................... 5 Supermarkets ................................................................................................................................................... 6 Consumers ...................................................................................................................................................... 6 Food safety hazards along the maize value chain ................................................................................................. 6 Aflatoxins ...................................................................................................................................................... 6 Fumonisins ..................................................................................................................................................... 8 Impacts of aflatoxin and fumonisin contamination .............................................................................................. 8 Public health impacts ......................................................................................................................................... 8 Economic impacts............................................................................................................................................ 10 Food safety concerns at nodes along the value chain......................................................................................... 10 Drying ......................................................................................................................................................... 10 Shelling (threshing) .......................................................................................................................................... 10 Sorting ......................................................................................................................................................... 11 Storage ......................................................................................................................................................... 11 Use of pesticides ..................................................................................................................................... 11 Use of other preservatives ....................................................................................................................... 11 Warehouse receipting system .................................................................................................................. 11 Trading ........................................................................................................................................................ 11 Processing...................................................................................................................................................... 11 Interventions to reduce aflatoxin and fumonisin contamination ........................................................................ 12 References ...................................................................................................................................................... 14 iii List of figures Figure 1: Agro-ecological map of Kenya showing the major maize-growing locations. ....................................... 1 Figure 2: Maize production trends, 2000–2017. ................................................................................................. 1 Figure 3: Maize yield per hectare in selected countries in eastern and southern Africa. ........................................ 2 Figure 4: Historical timeline of major agricultural production shocks in Kenya, 1980–2012. ............................... 2 Figure 5: Maize marketing channels. ................................................................................................................. 4 List of tables Table 1: East African Standard for maize grains (EAS 2:2013) ............................................................................. 3 Table 2: Maize imports and exports in Kenya, 2014–2018 ................................................................................. 3 Table 3: Levels of aflatoxin in maize and maize products in Kenya ..................................................................... 7 Table 4: Levels of fumonisin in maize and maize products in Kenya ................................................................... 8 Table 5: Reported aflatoxin poisoning cases in Kenya, 1960–2010 ..................................................................... 9 Table 6: Mycotoxins in maize and their health effects ........................................................................................ 9 Table 7: Potential food safety interventions in the maize value chain ................................................................ 13 iv Abbreviations and acronyms AOAC Association of Official Analytical Chemists CIMMYT International Maize and Wheat Improvement Center EAC East African Community ELISA enzyme-linked immunosorbent assay FAO Food and Agriculture Organization of the United Nations FAOSTAT Food and Agriculture Organization Corporate Statistical Database ha hectare(s) IARC International Agency for Research on Cancer IITA International Institute of Tropical Agriculture ILRI International Livestock Research Institute ISO International Organization for Standardization KEBS Kenya Bureau of Standards KES Kenya shillings kg kilogram(s) KNBS Kenya National Bureau of Statistics NCPB National Cereals and Produce Board NGO non-governmental organization ppb parts per billion ppm parts per million UNEP United Nations Environment Programme USD United States dollars WHO World Health Organization v Executive summary Maize is the main staple food in Kenya; per capita consumption is 98 kg per year. As it is the most important crop in the country’s strategic food reserve, failure of the maize crop has a significant impact on national food security. Foodborne hazards in the maize value chain contribute to food loss are a threat to public health and trade. Analysis of the maize value chain landscape is needed to understand the practices which may lead to pre- and post-harvest losses and affect food safety. It also helps to identify areas along the value chain where interventions are needed to make the sub-sector sustainable. This review discusses various practices that can increase the risk of maize contamination, recognizing that pre- harvest practices may have an impact on the post-harvest safety of maize. Mycotoxins, especially aflatoxins and fumonisins, are the most important foodborne hazards in the maize value chain and can occur in maize both before and after harvest. Aflatoxins are known to cause liver cancer and are associated with stunting, immunosuppression and teratogenic effects. Fumonisins are associated with oesophageal cancer. The cost of managing aflatoxin and fumonisin contamination of maize is higher for public health compared to trade. Another concern is insecticide contamination of maize from the use of chemicals to prevent damage by insect pests during storage; however, no studies have been carried out to show the effects of insecticide residues on humans. Contamination can occur at any level along the value chain. Therefore, interventions to prevent and control contamination and improve food safety should take a value chain approach from farm to consumer. Capacity building has the potential to influence behaviour change and improve food handling practices. 1 Introduction In Kenya, maize crop occupies 48.5% of arable land (FAOSTAT 2019) and accounts for 0.3% of the world’s maize production. Maize supplies about 365 kilocalories per 100 grams and accounts for 35% of the total caloric intake (FAOSTAT 2019). Maize is the staple crop in Kenya, contributing up to 3% of the agricultural gross domestic product and 21% of the total value of primary agricultural commodities. It is grown in six agro- ecological zones: highland tropical, moist transitional, dry transitional, moist mid-altitude, dry mid-altitude and lowland tropical (Figure 1). Source: Ouma and De Groote (2011) Figure 1: Agro-ecological map of Kenya showing the major maize-growing locations. Smallholder farmers account for 70% of the country’s maize production. Production fluctuates despite increased maize acreage mainly because of unfavourable weather (in rain-fed areas) and high costs of seeds and fertilizers (Figure 2). Source: FAOSTAT (2019) Figure 2: Maize production trends, 2000–2017. 2 Maize yield per hectare in Kenya is low: 1,440 to 1,836 kg compared to 5,751 kg globally and 2,070 kg elsewhere in Africa (FAOSTAT 2019). In eastern and southern Africa, South Africa has the highest maize yield per hectare (an estimate of 6,399 kg/ha was reported in 2017) (Figure 3). Source: FAOSTAT (2019) Figure 3: Maize yield per hectare in selected countries in eastern and southern Africa. Kenya experiences extreme rainfall events twice every three years. The country has also faced severe droughts in the last decade as well as variable year-on-year rainfall. This, together with high dependence on rain-fed agriculture, makes Kenya particularly vulnerable to food insecurity (Figure 4). Extreme weather can have a profound impact on crop and livestock production. In addition, the global financial and economic crisis, high food and fuel prices and a tense and at times uncertain political environment in recent years have repeatedly disrupted agricultural supply chains and markets, jeopardizing growth and the sector’s ability to provide food security and reduce poverty (D’Alessandro et al. 2015). Source: D’Alessandro et al. (2015) Figure 4: Historical timeline of major agricultural production shocks in Kenya, 1980–2012. The country consumes about 270 million kg every month (Kang’ethe 2011). The per capita consumption of maize in Kenya is 98–103 kg (compared to 73, 52 and 31 kg in Tanzania, Ethiopia and Uganda, respectively) (CIMMYT 2015). Maize standards The East African Community has a standard for maize grain in the region (Table 1). The standard, EAS 2:2013, specifies the acceptable limits of characteristics including foreign matter, damaged grains, moisture and mycotoxins. The standard has been adopted by the Kenya Bureau of Standards (KEBS) to evaluate the suitability 3 of maize for consumption in the country (KEBS 2019). The Government of Kenya has set limits for aflatoxins in food and feed to reduce exposure. The legal limit of total aflatoxin in cereals is 10 parts per billion (ppb), whereas that of aflatoxin B1 is 5 ppb. The total aflatoxin limit in feed is 10 ppb. Table 1: East African Standard for maize grains (EAS 2:2013) Characteristic Maximum limit Testing method Grade 1 Grade 2 Grade 3 Foreign matter (% by weight) 0.5 1.0 1.5 ISO 605 Inorganic matter (%by weight) 0.25 0.5 0.75 ISO 605 Broken kernels (% by weight) 2.0 4.0 6.0 ISO 605 Pest-damaged grains (% by weight) 1.0 3.0 5.0 ISO 605 Rotten and diseased grains (% by weight) 2.0 4.0 5.0 ISO 605 Discoloured grains (% by weight) 0.5 1.0 1.5 ISO 605 Moisture (% by weight) 13.5 13.5 13.5 ISO 711/712 Immature or shrivelled grains (% by weight) 1.0 2.0 3.0 ISO 605 Filth (% by weight) 0.1 0.1 0.1 ISO 605 Total defective grains (% by weight) 3.2 7.0 8.5 ISO 16050 Total aflatoxin (B1 + B2 + G1 + G2) (ppb) 10 10 10 ISO 16050 Aflatoxin B1 (ppb) 5 5 5 AOAC 2001.04 Fumonisin (ppm) 2 2 2 AOAC 2001.04 AF: aflatoxin; ppb: parts per billion; ppm: parts per million; ISO: International Organization for Standardization; AOAC: Association of Official Analytical Chemists The parameter ‘Total defective grains’ is not the sum total of the individual defects; it is limited to 70% of the sum total of individual defects. Source: EAC (2013) Maize trade Depending on the year, Africa generally accounts for 1.5–3.5% of global maize exports. In 2013, the value of the continent’s maize flour exports was about 20.1% of global exports. Between 2004 and 2013, the value of the continent’s maize flour exports increased by close to 400% (FAOSTAT 2019). In the last decade, Kenya experienced heightened food insecurity, dependence on imports and emergency humanitarian assistance. The large deficit is met through import of maize from other countries. Imports are allowed when supply cannot meet the internal demand and are meant to bridge the gap and stabilize market prices. The amount of maize that is imported fluctuates depending on the weather. However, aside from the weather, maize imports have increased to keep up with local consumption patterns, increasing from 2.9% to over 12% between 1970 and 1991 (Kang’ethe 2011). Significant increases in maize imports were observed between 2014 and 2018 (Table 2). With the country’s population being about 46 million in 2020, the demand for maize is likely to be over 5 million metric tonnes. Based on the prevailing rates of maize production, the maize deficit is projected to be around 1.2 million metric tonnes in 2020 (Kang’ethe 2011). With increased reliance on imports, it is likely that foreign exchange reserves and resources earmarked for development will be diverted to procure food for Kenyans. Table 2: Maize imports and exports in Kenya, 2014–2018 Year Quantity (tonnes) Value (KES million) Imports Exports Imports Exports 2014 458,940.1 1,667.6 9,308.5 323.6 2015 490,023.7 2,006.9 8,378.3 312.3 2016 148,558.1 3,191.5 3,636.6 510.8 2017 1,327,971.1 5,419.7 40,265.0 766.4 2018 529,558.3 2,673.3 12,008.4 513.8 Source: KNBS (2019) Value chain actors The maize value chain in Kenya is complex and involves many players including input suppliers, farmers, marketers and consumers (Figure 5). Within these broad categories, there are numerous sub-players that integrate either horizontally or vertically. This integration complicates food safety along the value chain due to different practices among the players. 4 Source: Modified from Kirimi et al. (2011) Figure 5: Maize marketing channels. Input suppliers The Eastern Africa Grain Council is a regional organization of grain value chain stakeholders. Its membership includes farmers, traders, millers and service providers such as banks, warehouse operators and input suppliers from the East African Community (EAC) and the Common Market for Eastern and Southern Africa. Extension service providers are responsible for delivering extension services including dissemination of appropriate technologies (Tiongco 2011). Farmers About 96% of farming households grow maize mostly for home consumption with the surplus sold to assemblers. On average, 45% of household-grown maize is sold (Kirimi et al., 2011). Most rural households own small farms (less than five acres) and are therefore unable to produce enough maize to meet their own needs, forcing them to buy maize. About 18% of farmers sell and buy maize within the same year (Kirimi et al. 2011); the majority are unable to meet their maize needs throughout the year. Only 20% sell maize and these are mainly large-scale farmers. Medium-scale farmers produce medium volumes on 5–20 acres of land. Large-scale farmers produce large volumes on more than 30 acres of land and sell their grain to the National Cereals and Produce Board (NCPB) and large commercial millers (Tiongco 2011). Farm practices such as land preparation, choice of seeds, planting, harvesting, drying, storage and shelling can influence the occurrence of foodborne hazards like aflatoxins. 5 Marketers Assemblers Assemblers are the first commercial purchasers of maize from the field. They buy maize directly from several farmers, bulk it to capture economies of scale in transport to local markets and then sell it to wholesalers and retailers and sometimes directly to consumers (Figure 5). In some cases, they also act as purchasing agents of large commercial millers. They account for about 55% of sales by farmers (Kirimi et al. 2011). These traders do not store their grain but instead offload and sell it quickly to large-scale traders for fear of their capital being tied up in inventory. They make small profit margins ranging from KES 400–500 per 90-kg bag (Kirimi et al. 2011). External traders travel long distances on trucks, vehicles and donkeys to purchase maize from farmers not within their vicinity. Chamberlain and Jayne (2009) observed that the intensity of assemblers in Kenya increased over time as the distance between farmers and assemblers decreased from 0.9 km to 0.7 km. Wholesale traders Wholesale traders buy maize from assemblers in bulk, store and fumigate it and then sell it to retailers or millers. They usually buy maize from surplus areas and sell it to deficit areas and in large marketplaces (Tiongco 2011). They command about 23% of the market (Kirimi et al. 2011). The NCPB is a cereal purchasing, marketing and price regulatory agency that ensures a year-round supply of cereals for the nation. It purchases maize from large- scale farmers, co-operatives and wholesalers. The NCPB commands 1.5% of the maize market in Kenya. In addition to being the major buyer of maize in Kenya, it owns advanced storage facilities that are open for renting by farmers (Kirimi et al. 2011). Dis-assemblers Dis-assemblers are maize trader who buy maize mainly from large wholesalers in deficit areas and break down the volumes for re-sale to small-scale retailers and consumers. Dis-assemblers are usually local traders who raise their initial capital from either salaried employment or from their involvement in other business activities (Kang’ethe 2011). Primary and secondary traders are local maize traders who buy maize from large wholesalers and assemblers and sell it to smaller-scale retailers and consumers. Secondary traders are also retailers in small marketplaces from where maize is stocked and sold in small volumes (Tiongco 2011). Millers Milling of maize is the main form of its value addition. Globally, processing of maize occurs either as dry or wet milling. The main dry milling products include maize flour (for making maize meal, bread and pancake mixes, infant foods, biscuits and porridge), fine meal flaking grits (for making ready-to-eat breakfast cereal cornflakes), coarse and medium grits (for cereal products and snack foods) and fine grits (for brewing). Wet milling products include corn starch (which can be processed into a variety of products such as baked products and candies), corn syrup (which is mainly used in confectioneries and bakery and dairy products), high fructose syrup, dextrose and corn oil (Kang’ethe 2011; Tiongco 2011). Maize is also used to process oil and by-products for animal feed. The most predominant form of maize processing is dry milling to make maize meal, flour and maize grits. The average extraction rate among medium to large industrial millers is 80% for grade 1 and 95% for grade 2, implying that 2.5 kg of maize are needed to produce 2 kg of flour. Millers are characterized based on the technology used, available employed capital, packaging technique used and source of maize. There are large-scale and small-scale millers in the value chain. Formal commercial or large-scale millers deal with large volumes of maize and package their own maize. These millers are capital intensive and use roller milling technology that produces a more refined meal. They purchase maize from wholesalers, NCPB stores and large farmers (Tiongco 2011). Small-scale millers depend on maize that comes directly from farmers and process it into whole maize meal (posho). They use a simple hammer milling technology where both the germ and bran are milled together with the kernel to produce flour. These posho millers are divided into small- scale millers that are involved in custom milling and large-scale millers who have higher production, packaging and retailing capacities. They also stock maize for resale to consumers (Tiongco 2011). The NCPB estimates the total national maize milling capacity at 1.77 million metric tonnes per year. Data from the Cereal Millers Association indicate that the combined maize milling capacity of medium to large maize millers and micro to small maize millers (posho millers) is in the order of 1.62 million metric tonnes per year. Of this amount, the association estimates that 19 of the medium to large millers have a combined milling capacity of about 1.41 million metric tonnes per year or 85–90% of total national maize milling capacity. The association also estimates that posho millers have a combined milling capacity of about 0.21 million metric tonnes per year or about 10–15% of total national maize milling capacity (Kang’ethe 2011). 6 Supermarkets Two leading supermarkets were visited and products containing maize were sought from the shelves. The products were both imported (from France, Germany, the United Arab Emirates and the United Kingdom) and locally processed. The products identified as containing maize included popcorn (eight brands), cornflakes (five brands), corn chips (six brands), tortillas (four brands), biscuits (three brands) and maize flour (eight brands). Consumers Consumers in urban areas purchase their maize from open-air markets. They buy maize meal from supermarkets and kiosks. Consumers in rural areas get maize from farm stores, open-air markets and kiosks, and buy their maize meal from posho millers, supermarkets and kiosks (Tiongco 2011). Food safety hazards along the maize value chain Mycotoxins and pesticides are the main food safety hazards along the maize value chain. Mycotoxins are a group of secondary fungal metabolites produced by certain fungal species under special conditions of temperature, humidity and moisture. The mycotoxins of major concern in maize are aflatoxins and fumonisins. Aflatoxins Aflatoxins are a group of mycotoxins produced primarily by strains of Aspergillus, i.e. Aspergillus flavus Link, A. parasiticus Speare, A. nomius Kurtzman, Horn and Hesseltine, and A. tamarii Kita, and Emericella spp. (Muthomi et al. 2012). While all these species produce aflatoxins, it is A. flavus that frequently colonizes maize and produces high amounts of aflatoxin contaminating the grain (Mutegi et al. 2012). The aflatoxins are grouped into aflatoxin B1, aflatoxin B2, aflatoxin G1 and aflatoxin G2 (IARC 1993) based on the colour they produce under ultraviolet radiation (B for blue and G for green). Naturally, different strains produce aflatoxins and other mycotoxins. Aflatoxin B1 is the most abundant of the aflatoxins produced and the most toxic (Probst et al. 2011). Based on a study in Nandi, Kenya by Nyongesa et al. (2015), four fungal genera colonize maize in the region: Aspergillus, Fusarium, Penicillium and Trichoderma. Five sections of Aspergillus (section Flavi, section Nigri, section Fumigati, section Circumdati and section Clavati)have been identified from maize and soil samples. Aspergillus section Flavi was the most predominant followed by section Nigri. Two other sections (section Nidulantes and section Candidi) were identified from samples of soil from Kaptumo (Nyongesa et al. 2015). Although A. flavus is the most toxigenic, the strain has been shown to produce two types of sclerotia. Those that produce large sclerotia (the L type) are not as toxigenic as those that produce small sclerotia (the S type); the difference is in the amount produced by the two types (Okoth et al. 2012). Sirma et al. (2016) tested maize samples from different agro-ecological zones for aflatoxin. Those with aflatoxin levels exceeding the regulatory limit of 10 ppb were from the humid and sub-humid zones (17–20% of samples), temperate zones (22–25.4%) and the semi-arid region of Isiolo (20%). Table 3 summarizes the status of aflatoxin contamination of maize and maize products in Kenya, based on findings from previous studies. 7 Table 3: Levels of aflatoxin in maize and maize products in Kenya Study site Number of samples tested Samples positive for aflatoxin (%) Samples with aflatoxin above acceptable limit (%) Acceptable limit for aflatoxin (ppb)* Method of analysis Reference Makueni 91 65 20 Modified immunoaffinity method based on AOAC method 991.3 Lewis et al. (2005) Kitui 73 62 Machakos 102 34 Thika 76 51 Machakos 20 70 20 Probst et al. (2007) Makueni 37 70 Kitui 38 55 Makueni 104 36 20 100 Immunoaffinity column (AflaTEST; Vicam, Milford, MA, USA) method 977.16 by AOAC Mwihia et al. (2008) Eastern province 144 590 20 USDA/GIPSA certified ELISA (ELISA, Mycochek Strategic Diagnostics Inc, Nevak, DE, USA) Probst et al. (2011) Coast province 18 25 Rift Valley province 13 0 Kitui 30 10 33 10 Low matrix competitive ELISA (Helica Biosystems, Fullerton, California) Gachara (2015) Trans Nzoia 40 58 53 Nakuru 60 83 4 Makueni and Kitui 716 35 20 Immunoaffinity column (AflaTEST; Vicam, Milford, MA, USA) method 977.16 by AOAC Daniel et al. (2011) Nairobi 144 83 Okoth and Kola (2012) Meru Central 150 80 60 10 Low matrix competitive ELISA (Helica Biosystems, Fullerton, California) Mutiga et al. (2014) Mwala 150 85 55 Meru North 150 73 45 Meru South 150 78 43 Mwingi 150 65 58 Kitui 150 73 37 Mbeere 150 61 33 Embu 150 58 31 Machakos 150 50 23 Kathiani 150 46 22 Rachuonyo 104 77 55 10 Low matrix competitive ELISA (Helica Biosystems, Fullerton, California) Mutiga et al. (2015) Homa Bay 113 69 29 Kisii 125 45 9 Bungoma 309 43 3 Trans Nzoia 192 42 4 Uasin Gishu 142 25 6 Korogocho and Dagoretti West 186 95 4 20 Low matrix competitive ELISA (Helica Biosystems, Fullerton, California) Kiarie et al. (2016) Makuyuni 15 33 0 20 Immunoaffinity column (AflaTEST; Vicam, Milford, MA, USA) method 977.16 by AOAC Maina et al. (2016) Kilala 15 93 7 Kwale 20 95 20 5 Low matrix competitive ELISA (Helica Biosystems, Fullerton, California) Sirma et al. (2016) Isiolo 40 50 25 Tharaka Nithi 53 75 17 Kisii 63 78 25 Bungoma 57 72 23 Nandi (home) 272 68 0 10 Competitive ELISA (r- biopharm-Germany) Kang’ethe et al. (2017b) Nandi (market) 42 73 0 Makueni (home) 325 80 25 Makueni (market) 55 91 45 *The acceptable limit of total aflatoxin in maize changed from 20 ppb to 10 ppb; authors used either the Codex Alimentarius (10 ppb) or the United States Food and Drug Administration (20 ppb) standard. ppb: parts per billion; AOAC: Association of Official Analytical Chemists; ELISA: enzyme-linked immunosorbent assay 8 Fumonisins Fumonisins are toxic metabolites produced by Fusarium verticillioides and Fusarium proliferatum (Fandohan 2006). Fumonisins have been identified in corn, corn flour, dried milled maize, dried figs (Karbancioglu-Güler and Heperkan 2009), herbal tea and medicinal plants (Omurtag and Yazicioglu 2004). Six types of fumonisins have been identified: fumonisin B1, B2, B3, B4, A1 and A2 (Burger et al. 2010). The B series fumonisins contain a free amine while the A series fumonisins have an amide. Fumonisin B1 is the most frequent in maize (Ritieni et al. 1997). Contamination of maize with fumonisins mainly occurs before harvest. Fusarium section Verticillioides and section Moniliforme have been identified in Kenya; Fusarium section Verticillioides is predominant in Nandi, Makueni and western Kenya (Kedera et al. 1999; Kang’ethe et al. 2017a). These genera of fungi produce fumonisins that have various harmful effects on humans. A study by Kedera et al. (1999) in western Kenya found 47% of maize samples contained fumonisin (> 100ng/g), with 5% containing fumonisins above the acceptable level in maize for human consumption (1,000 ng/g). In Kisii County, the same study reported fumonisin B1 levels of 3,600–11,600 ng/g. Alakonya et al. (2009) reported fumonisin B1 levels of 22–348 µg/kg in healthy maize. Table 4 summarizes the status of fumonisin contamination in maize and maize products in Kenya, based on findings from previous studies. Table 4: Levels of fumonisin in maize and maize products in Kenya Study site Number of samples tested Samples positive for fumonisin (%) Samples with fumonisin levels above 2 ppm (%) Method of analysis Reference Kitui 42 cELISA (Rindascreen, r-biopharm) Bii et al. (2012) Makueni 44 cELISA (Rindascreen, r-biopharm) Bii et al. (2012) Makueni (home) 285 91.9 28.9 cELISA (Rindascreen, r-biopharm) Kang’ethe et al. (2017a) Makueni (market) 49 94.2 38.2 cELISA (Rindascreen, r-biopharm) Kang’ethe et al. (2017a) Nandi (home) 219 84.2 5.5 cELISA (Rindascreen, r-biopharm) Kang’ethe et al. (2017a) Nandi (market) 40 95.2 7.1 cELISA (Rindascreen, r-biopharm) Kang’ethe et al. (2017a) Western Kenya 197 47 High-performance liquid chromatography Kedera et al. (1999) ppm: parts per million; cELISA: competitive enzyme-linked immunosorbent assay Impacts of aflatoxin and fumonisin contamination Public health impacts Outbreaks of aflatoxin poisoning have occurred in Kenya since 1960 (Table 5). Exposure to aflatoxins has negative effects on animals and humans (Table 6). Aflatoxins were first reported in Kenya in 1960, when 16,000 turkeys died from feeding on aflatoxin-contaminated groundnut feeds (Peers and Linsell 1973). Humans are exposed when they consume contaminated products (cereals, pulses or nuts). In Kenya, aflatoxin exposure ranges between 3.5 and 133 ng/kg body weight per day (assuming 60 kg body weight per individual) (Shephard 2008). Acute toxicity occurs following exposure to high doses of aflatoxins and may lead to death due to liver failure (Lewis et al. 2005). Acute aflatoxicosis outbreaks in humans in Kenya were first described in 1978 and later in 1981, 1982 and 2001 (Muthomi et al. 2012). The 1982 outbreak occurred in Machakos, Makueni and Kitui counties, which are now known as aflatoxin hot spots following outbreaks from 2004 to 2006 (Korir and Bii 2012). The outbreak of 2004 recorded 317 cases of acute aflatoxin poisoning and 125 deaths (Okoth and Kola 2012). Chronic aflatoxin toxicity occurs when small doses are consumed over a long time and manifests as stunting in children below five years of age, immunosuppression which lowers immunity to infections, induction of hepatocellular carcinoma, reduced fertility and teratogenic effects (Wu et al. 2014). The risk of hepatocellular carcinoma is increased in people exposed to chronic doses of aflatoxin with concurrent hepatitis B virus infection (Wild and Gong 2009). A study by Ly et al. (2016) in Kenya found 31.5% (n = 1091) exposure to hepatitis B virus, corresponding to an estimated 6.1 million people with past or present infection; of these, about 400,000 people had chronic infection. Wu et al. (2011) estimated the number of liver cancer cases in women and men in Kenya at 4.9 and 8.9 per 100,000, respectively. The estimated incidence of hepatocellular carcinoma attributable to aflatoxin ranged from 0.04 to 1.33 cases per 100,000 in hepatitis-B-negative populations and from 1.05 to 39.9 cases per 100,000 in hepatitis-B-positive populations in Kenya (Hall and Wild 1994; Shephard 2008). The annual 9 global burden of hepatocellular carcinoma cases attributable to aflatoxin exposure in Kenya was estimated to range from 11 to 450 in hepatitis-B-negative populations and from 44 to 2,270 in hepatitis-B-positive populations (Liu and Wu 2010). All domestic animals can be affected by aflatoxins but sensitivity is influenced by several factors including the species of the animal (dogs and chickens are more sensitive than ruminants). Aflatoxin causes reduced feed conversion efficiency, reduced productivity and immunosuppression (Wogan 1973; Richard et al. 1978). In poultry, aflatoxins are associated with liver damage, impaired productivity, decreased egg production, inferior carcass quality and increased susceptibility to disease (Edds and Bortell 1983). Fumonisins are carcinogenic and have been linked to oesophageal cancer (Kimanya 2015) and neural tube defects in the foetus (Missmer et al. 2006). Wakhisi et al. (2005), using hospital data, reported high incidences of oesophageal cancer in patients seeking medical care at the Moi Teaching and Referral Hospital; the incidence was higher in patients from the Nandi community compared to those from other communities. In animals, fumonisins cause leukoencephalomalacia in horses (Marasas et al. 1988), pulmonary oedema in swine (Haschek et al. 2001) and hepatocarcinoma in rats (Gelderblom et al. 1991). Table 5: Reported aflatoxin poisoning cases in Kenya, 1960–2010 Year Subject affected Numbers affected Locality Source of aflatoxin Observed effects Reference 1960 Ducklings 16,000 Settler farm in Rift Valley Contaminated groundnut feed Death Peers and Linsell (1973) 1977 Dogs and poultry Large numbers Nairobi, Mombasa and Eldoret Contaminated products due to poor storage Death FAO and UNEP (1979) 1981 Humans 12 Machakos Contaminated maize Death Ngindu et al. (1982) 1984–85 Poultry Large numbers Poultry farms Contaminated imported maize Death Ngindu et al. (1982) 1988 Humans 3 Meru North Contaminated maize Death; acute effects Autrup et al. (1987) 2001 Humans 3 Meru North Mouldy contaminated maize Death Probst et al. (2007) 2001 Humans 26 Maua Mouldy contaminated maize 16 deaths Probst et al. (2007) 2002 Dogs and poultry Large numbers Coast Contaminated feed Death Njapau et al. (2007) 2003 Humans 6 Thika Mouldy maize Death Onsongo (2004) 2004 Humans 317 Eastern, Central, Makueni, Kitui Contaminated grains Acute poisoning; 125 deaths Lewis et al. (2005) 2005 Humans 75 Machakos, Makueni, Kitui Contaminated maize 75 cases of acute poisoning; 32 deaths Azziz-Baumgartner et al. (2005) 2006 Humans 20 Makueni, Kitui, Machakos Contaminated maize Acute poisoning, 10 deaths Muture and Ogana ( 2005) 2007 Humans 4 Kibwezi, Makueni Contaminated maize 2 deaths Wagacha and Muthomi (2008) 2008 Humans 5 Kibwezi, Kajiado, Mutomo Contaminated maize 3 hospitalizations, 2 deaths Muthomi et al. (2009) 2010 Humans 29 districts in Eastern Kenya Suspected contaminated maize Downward price spiral; breakdown of grain trade; unconfirmed dog cases Muthomi et al. (2010) Source: Kang’ethe (2011) Table 6: Mycotoxins in maize and their health effects Fungus Mycotoxin Health effects Aspergillus flavus and A. parasiticus Aflatoxin B1 Carcinoma, immunosuppression, retarded child growth and development Fusarium verticillioides Fumonisin B1 Oesophageal cancer and neural tube defects leading to abortion Fusarium graminearum Zearalenone Oestrogenic effects in animals not of puberty age Fusarium graminearum Deoxynivalenol Immunosuppression Fusarium verrucosum Ochratoxin Chronic renal disease Source: Mahuku and Nzioki (2011) 10 Economic impacts According to IITA (2013), about 1.2 billion United States dollars (USD) are lost annually worldwide due to aflatoxin contamination; African countries are estimated to contribute about 38% of this loss (which amounts to USD 456 million). In the United States of America, the annual cost of aflatoxin contamination has been estimated at USD 500 million (Wu and Munkvold 2008), with management costs of USD 20 million to USD 50 million per year (Robens and Cardwell 2003). Lubulwa and Davis (1994) reported social costs of USD 1 billion annually associated with aflatoxin contamination in maize and peanuts in Indonesia, Thailand and the Philippines. These costs could be higher if the effects of aflatoxin on product taste, odour, texture and colour, as well as the opportunity cost of forgone crop production (due to soil contamination) and trade, are factored in. Developed countries are increasingly using aflatoxin risk as a non-tariff barrier to trade under the precautionary principle (Otsuki et al. 2001). A reduction of the limit of aflatoxin in cereals, dried fruits and nuts by the European Union from 5 ppb to 4 ppb would cost African countries about USD 670 million dollars in lost earnings per year (Otsuki et al. 2001). Although no study has so far estimated the cost of aflatoxin contamination and management in Kenya, the cost is believed to be high. For instance, Okoth and Kola (2012) found that 120 (83%) of 144 food samples screened for aflatoxin contamination in their study had levels greater than the regulatory limit of 10 ppb. Additionally, at least 207 million kg of maize were found to be unfit for human and livestock consumption and trade during the aflatoxin outbreaks in Kenya in 2004 to 2006 (Atser 2010). Some of this study’s key informants in Kitui County indicated that maize prices dropped from KES 1,800 to KES 900 following an aflatoxin alert in the area in 2009. Apart from the significant monetary costs associated with aflatoxin contamination, aflatoxins disproportionately affect the poor and particularly women. For instance, food-insecure resource-poor households (which are predominantly headed by women) are more likely to consume contaminated food rather than sell or discard it. Additionally, owing to income constraints, such households may not be able to adopt costly control strategies, thereby reducing crop productivity, particularly if the household is located in an aflatoxin hot spot. Furthermore, although well-intentioned aflatoxin awareness campaigns can reduce prices of aflatoxin contaminated food, they may inadvertently result in direct market losses for the poor; it is unlikely that poor farmers can afford to throw away crops that cannot be sold due to aflatoxin contamination. This leads to more severe health impacts associated with farmers’ consumption of their own low-priced, contaminated food. Food safety concerns at nodes along the value chain Mycotoxin contamination in the maize value chain is associated with both pre- and post- harvest farm practices. In the pre-harvest stage, maize may be colonized by the fungal species due to artisanal farming practices. This review will focus on off-farm practices. Drying Drying of maize is usually done either on the cob or as shelled grains. On-cob drying of maize directly on the ground without a canvas sheet increases the risk of contamination with fungal spores from the soil which may lead to aflatoxin contamination in the stored crop. Kang’ethe et al. (2017a) found that 39.1% of farmers in Makueni County and 37.1% of farmers in Nandi County dried their cobbed maize on the ground without a canvas sheet. Such practices, as observed by Mejía (2003), are likely to lower grain quality and present risks to public health. The expected moisture content in properly dried maize is ≤ 13.5%. Higher moisture levels favour the growth of fungi and make the maize crop more susceptible to aflatoxin contamination if the maize was already colonized by aflatoxigenic mould species. Shelling (threshing) Shelling of maize grains from the cob is achieved by manual shellers, shelling machines or pounding with sticks. Pounding maize with sticks or improperly calibrated shelling machines can damage the grains and make it easier for fungal hyphae to penetrate the grains and cause aflatoxin contamination if conditions are favourable for mould growth. Kang’ethe et al. (2017a) report that 76.1% and 75.1% of respondents in Makueni and Nandi, respectively, pounded maize with sticks. 11 Sorting Sorting of maize can result in a 40–80% reduction in aflatoxin levels (Fandohan et al. 2005). It is commonly done before the grains are cooked but rarely before storage. Kang’ethe et al. (2017a) report that women were able to detect and sort out discoloured grains (which are likely contaminated with moulds), thereby reducing the risk of exposure when the food is consumed. Storage Farmers store maize either as cobs or shelled grains. They use cribs that are well ventilated and raised from the ground to store the maize on the cob. Although there is good air flow, the pre-harvest and harvesting practices will affect the levels of aflatoxin at this stage. In the cribs, the grains are expected to dry and are only threshed when market is assured. When maize is stored as shelled grains, farmers use nylon bags which build up moisture and this exposes the maize to aflatoxin contamination (Mutegi et al. 2013). The bags are on many occasions stored on the ground instead of on pallets. This continues to expose the shelled grains to fungal spores and risk of aflatoxin accumulation (Mutegi et al. 2013). Use of pesticides Pest infestation is a common problem that farmers have to deal with. Several pesticide brands exist in the market and farmers rely on these to control weevils that can damage grains and result in post-harvest losses. Majority of these have pyrethrins as the active compound. They include pirimiphos-methyl, an organophosphate compound mixed with permethrin (a pyrethroid, common name Actellic), malathion (organophosphate), permethrin (pyrethrin), fenitrothion (organophosphate) and fenvalerate (pyrethrin). Aluminium phosphide is commonly used in large warehouses by large-scale traders and millers. Users should observe the recommended withholding periods to make sure the product is safe, in addition to taking safety precautions during application. Organophosphate-based insecticides may leave residues because of their bioaccumulation tendency; however, these are being replaced by organic and synthetic pyrethrins that are thought to have lower environmental and non-target toxicity than organophosphates (Kang’ethe, 2011; Chesang et al. 2016). Although initially thought to have no adverse effects, a study by Chrustek et al. (2018) reports that deltamethrin has adverse effects on fertility, the immune system and cardiovascular and hepatic metabolism; deltamethrin has nephron and hepatotoxic effects while alpha-cypermethrin impairs the immune system and increases glucose and lipid levels in blood. While these effects are new findings, research is needed on the side effects of pyrethrins. Use of other preservatives In a study in Nandi and Makueni, farmers reported using wood ash and hanging maize over fire as local methods of preserving produce (Kang’ethe et al. 2017a). The effectiveness of wood ash in preventing weevil attack, fungal infection and aflatoxin contamination is unknown. However, hanging maize over fire exposes it to smoke that contains antifungal and antibacterial compounds that lengthen the shelf-life of the produce. In addition, the smoke aids in drying the maize. Warehouse receipting system This is a system whereby farmers rent storage space in registered warehouses in which storage practices are optimized to control pests and aflatoxin contamination. Maize from a warehouse receipting system would be traded through a commodity stock exchange with certification that the produce is free from aflatoxin. Kenya’s parliament has not assented to legislation on commodity stock exchange trading; the Bill is in parliament for discussion. Trading This stage of the value chain includes assemblers, dis-assemblers and large-scale or wholesale traders. Here, food safety risks include the use of inappropriate storage bags (polypyrene) instead of sisal or hermetic bags. Polypyrene or nylon bags build up moisture and create a microclimate that favours fungal growth and toxin production. Hermetic bags and silos are effective by creating anaerobic environments which do not favour fungal growth and toxin production (Ben et al. 2006). In the warehouses, the products are fumigated to prevent fungal growth; it is important to maintain the fumigation regime and use recommended products that leave no residue. The effectiveness of fumigation is hampered by the resistance of insects to the active compounds. Processing Maize processors use either wet milling or dry milling. The main difference is in the products obtained. In wet milling, the maize grain is separated into its four constituent parts: corn oil, starch, fibre and protein. The maize is first steeped in water at 52–54°C for 40 hours. The steep water is then drained, concentrated and used as animal 12 feed (given its high protein content). The next step is recovery of germ for oil extraction; the residue is used as animal feed protein. This is followed by recovery of starch. Dry milling separates the grain into flour, germ, fine grits and coarse grits; these are processed into human food or animal feed. The grain is tempered by adding water to separate the germ and endosperm. De-germination allows the kernel to break down into germ, pericarp and endosperm. Aspiration is done to separate the pericarp from the mixture of germ and endosperm. Roller/hammer mills grind the different products. The main food safety concern is to make sure the steep water which may contain aflatoxins is disposed of properly and not used in subsequent steps. In dry milling, the whole grain is milled without separation of the kernel parts and water and chemicals which would help to wash out some of the toxins are not applied. If the products of wet or dry milling are not well dried, the moisture content will support mould growth and increase the risk of aflatoxin production and accumulation. Interventions to reduce aflatoxin and fumonisin contamination This review has analysed the maize value chain in Kenya and identified practices or omissions with the potential to cause contamination with aflatoxins and fumonisins. Table 7 indicates potential food safety interventions along the value chain and the appropriate stakeholders to intervene or fund the activities. In each case, research is crucial to identify trade-offs for adoption and upscaling. 13 Table 7: Potential food safety interventions in the maize value chain Level and node of value chain Current practices Recommended best practices Interventions Best suited to intervene Farm Land preparation Limited land tillage Shallow tillage Tilling land before planting Deep tillage using tractors Train farmers on best tillage methods and their benefits in aflatoxin control County government; local non-governmental organizations (NGOs) Application of Aflasafe No application by many farmers Application of Aflasafe Train farmers on the benefits of Aflasafe application County government, NGOs and research organizations Certified seeds Use of local seed varieties Use of recommended certified seeds Train farmers on benefits of certified seeds County government, local NGOs and seed companies Crop rotation and intercropping No seasonal rotation of maize with other crops Failure to intercrop maize with other crops Rotation of maize with other crops Intercropping maize with other crops Train farmers on benefits of intercropping County government, local NGOs Soil amendments Planting maize on sandy soils Failure to use amendments to improve soil fertility Planting maize on loam soils if accessible Use of lime, farmyard manure and cereal crop residues to improve soil fertility Train farmers on best soil amendments and their benefits in aflatoxin control County government, local NGOs and fertilizer companies Harvesting and drying Cutting maize stovers Delayed drying of maize Drying on cob or as shelled grains on canvas Drying maize within 24–48 hours Train farmers on best practices in harvesting and drying County government and local NGOs Shelling (threshing) Pounding maize with sticks Poorly calibrated threshing machines Well calibrated threshing machines Train farmers on best shelling methods and adverse effects of damaged maize grains County government and local NGOs Storage method Storage of maize and bags in the house on the floor Storage of shelled grain in the house Poorly ventilated granaries Use of granaries that are not raised and have no pest control measures Use of inappropriate polypyrene/nylon bags Storage of maize bags on a raised platform in the house Storage of maize in well- ventilated, raised granaries with effective pest control measures Use of hermetic improved bags and metal silos Train farmers on optimal storage of maize (method, bags, design) Invest in improved hermetic bags and metal silos County government and local NGOs Preservatives Failure to use preservatives Failure to observe withholding periods Use of un-approved preservatives (thiamethoxam, imidacloprid and clothianidin) Use of approved and efficient preservatives Observing recommended withholding periods before consumption of maize grains Train farmers on use of approved preservatives, their efficiency and risks posed by banned substances County government, local NGOs and preservative manufacturing companies Sorting of mouldy grains Failure to sort and remove physically damaged and mouldy maize grains Manual sorting of mouldy and damaged grains Use of electric sorters (E- nose) to isolate and remove damaged and mouldy grains Use of ultra-violet detectors to detect and isolate mouldy grains which are removed magnetically Train farmers on identification and sorting of mouldy grains before storage, cooking and milling and the effect of sorting on aflatoxin control County government and local NGOs Marketing and processing Small-scale traders Storage Storage of maize grains in the house on the floor Use of polypropylene bags to store maize Storage of maize on a raised platform Use of hermetic improved bags Train marketers and processors on proper storage of maize and maize products Invest in hermetic improved bags County government and local NGOs Large-scale traders Storage Storage method Preservation Use of poorly designed warehouses Use of polypropylene bags to store maize grains Failure to use approved preservatives Failure to adhere to withholding periods of preservatives Poor fumigation procedures Use of well-designed ventilated warehouses Use of improved hermetic bags for storage Proper use of approved preservatives Adhering to withholding periods of preservatives before consumption of maize Proper fumigation procedures Train processors on design of warehouses, optimal fumigation procedures, use of preservatives and withholding periods for preservatives before consumption of maize Develop and implement fumigation protocols County government, local NGOs Processors Artisanal processing Poor processing techniques to make muthokoi (no soaking, no use of Magadi soda) Proper techniques to make muthokoi (soaking, use of Magadi soda) Train traditional millers on proper techniques to make muthokoi County government and local NGOs Formal processing Poor quality and maintenance of milling equipment Poor calibration of milling equipment Use 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