Food Control 138 (2022) 108968 Contents lists available at ScienceDirect Food Control journal homepage: www.elsevier.com/locate/foodcont Occurrence and postharvest strategies to help mitigate aflatoxins and fumonisins in maize and their co-exposure to consumers in Mexico and Central America Sylvanus Odjo, Amos Emitati Alakonya, Aldo Rosales-Nolasco, Aide L. Molina, Carlos Muñoz, Natalia Palacios-Rojas * International Maize and Wheat Improvement Center (CIMMYT), Carretera México-Veracruz Km. 45, C.P. 56237, El Batán, Texcoco, Estado de México, Mexico A R T I C L E I N F O A B S T R A C T Keywords: Maize is the main dietary cereal in Mexico and Central America, with annual per capita consumption between Nixtamalization 25.5 and 116.34 kg. Unfortunately, maize is highly susceptible to fungal infestation in the field, either through Tortillas systemic infections or wounds caused by farm equipment, birds or insects. Field infestations can be exacerbated Mycotoxins by bad postharvest handling practices. Proliferation of fungi on maize grains can alter physical appearance, taste Food processing and chemical composition, including accumulation of toxic fungal metabolites known as mycotoxins. Such metabolites can also be found in other crops that are also essential in the diet of the population in this region, including beans, rice and chili peppers. Maize grown in Mexico and Central America is mainly contaminated by mycotoxins belonging to the aflatoxins (AFs) and fumonisins (FBs) groups, produced by the fungi Aspergillus and Fusarium, respectively. These myco- toxins are of public health concern because they can induce negative health impacts including cancer in humans and animals. AFs and FBs levels of up to 2630 and 3861 μg/kg, respectively, have been reported in the region between 2017 and 2021. These levels are more than 380 times higher than established maximum levels. Pre- and post-harvest strategies can help mitigate mycotoxin contamination of grain. Pre-harvest AFs and FBs management strategies include the use of tolerant germplasm, good agronomic management, and biological control. Post-harvest strategies include all practices from harvest until consumption. This review examines AFs and FBs predisposing factors, prevalence, and co-occurrence in Mexico and Central America. We discuss common post-harvest practices, and recommended practices to reduce mycotoxin contamination, including optimum grain drying (to decrease moisture content below 14%); grain sorting (with the potential to reduce AFs and FBs levels by 40–95%); use of grain conditioning agents, grain quality- management, and hermetic storage technologies and optimization of storage conditions. The effects of grain processing, including baking, roasting, popping, and nixtamalization on reducing AFs and FBs (15–80% for AFs, 17–100% for FBs) are also reviewed. This review highlights the widespread mycotoxin contamination problem and the urgent need for new research paradigms to inform mycotoxin mitigation strategies in the region. 1. Introduction Mexico and Central American countries mainly consume maize in the form of tortillas and related nixtamalized maize-based food products Maize is the third most important food crop in the world after wheat (Table 1). Nixtamalization is a traditional cooking method in which and rice, but the first in annual production by volume. The average daily maize is cooked and steeped in an alkaline solution (Escalante-Aburto, consumption of maize products by Mexican and Central American Mariscal-Moreno, Santiago-Ramos, & Ponce-García, 2020). populations is 319 g and 282 g respectively. These intakes provide During the growth of the maize plant and during postharvest activ- approximately 986 kcal and 25.4 g of protein for Mexicans and 888 kcal ities, kernels may get colonized by an array of fungi, some of them and 22.9 g of protein for Central Americans (FAOSTAT, 2021). People in producing low molecular-weight secondary metabolites known as * Corresponding author. E-mail address: n.palacios@cgiar.org (N. Palacios-Rojas). https://doi.org/10.1016/j.foodcont.2022.108968 Received 3 August 2021; Received in revised form 11 March 2022; Accepted 14 March 2022 Available online 25 March 2022 0956-7135/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 mycotoxins. Maize is generally susceptible to infection by fungal genera In the past 10 years, AFs outbreaks have been witnessed in regions like Aspergillus, Fusarium and Penicillium where they can produce such as East Africa and India. On the contrary, no AF or any other different symptoms in the kernels and plants or remain symptomless mycotoxin outbreaks have been reported in Mexico or countries in (Fig. 1; Table 2). Members of these genera produce mycotoxin groups Central America (Kumar et al., 2017; Mahuku et al., 2019). However, such as aflatoxins (AFs), fumonisins (FBs), deoxynivalenol (DON), and scientific reports in countries of this region during the same period other trichothecenes and zearalenone (ZEN) (Munkvold, Arias, Taschl, indicate that mycotoxin contamination in grain is an emerging concern. & Gruber-Dorninger, 2019). The risk of infection and subsequent For instance, according to the BIOMIN mycotoxin survey data on maize, contamination with mycotoxins increases when the crops grow under other cereals and finished products intended for feed from Latin America abiotic stress such as high temperature or drought. Several other crops, between 2017 and 2021 there is rampant exposure to 4 main mycotoxins including beans, wheat, rice, chili peppers and peanuts that are also part AF, FB, DON and ZEN. During this period up to 27% of samples analyzed of the Mexican and Central American diet are affected by mycotoxins tested positive to AF with lowest positive annual average value of 4 (Bandyopadhyay et al., 2016; Costa et al., 2019; Telles, Kupski, & μg/kg and a maximum of 3861 μg/kg. Comparatively FB were detected Furlong, 2017; Voth-Gaeddert, Stoker, Torres, & Oerther, 2020). In fact, in up to 90% of samples analyzed with the lowest positive average of maize-based products are commonly consumed with beans and chilies 1390 μg/g and a maximum detected level of 21883 μg/kg. DON was and are the bases of the diet, especially in rural areas (Table 1). detected in up to 82% of total samples analyzed with the lowest average Direct exposure by humans and animals to mycotoxins through of 340 μg/kg in positive samples and the maximum detectable level of consumption of contaminated food and feed can result in toxic health 26 320 μg/kg. Finally, ZEN was detected in up to 60% of samples effects (Alshannaq & Yu, 2017; Martínez Padrón, Hernández Delgado, analyzed during the period where it returned the lowest positive average Reyes Méndez, & Vázquez Carrillo, 2013). If maize is a dietary staple, as of 53 μg/kg and maximum detectable level of 4948 μg/kg. It is impor- is the case in the region, the contamination could translate to high-level tant to note that the total average exposure factor which is the proba- chronic or acute exposure. In Mexico and Central America, the effects bility that one would be exposed to one or more mycotoxins was 79% are more chronic, while in parts of Africa like Kenya, Tanzania, Nigeria with an annual exposure risk range of between 70 and 87% within the 5 or in Asia, e.g., in India, both chronic and acute exposure have been years (Table 3, https://www.biomin.net/. Accessed on November 24, reported (Granados-Chinchilla et al., 2017; Kumar, Mahato, Kamle, 2021). Other recent independent studies in the region have also revealed Mohanta, & Kang, 2017; Mahuku et al., 2019; Morales-Moo et al., 2020; high incidence of mycotoxins in food and feed in the region has Voth-Gaeddert et al., 2020). Mycotoxins therefore pose a threat to food increased exposure to both humans and animals, with negative health, safety, food security and international trade (WHO, 2021). physical development and nutritional implications Table 1 Mexico and Central America main diet crops consumed, processing method and aflatoxin regulations. Country Crop Amount Common food AFB1 limits/regulations Reference consumed (kg/ processing methodsb person/year)a Guatemala Maize 87.25 Nixtamalization, 20 μg/kg in maize grain/COGUANOR COGUANOR (1982) roasting, boiling NGO 43 047 Beans 12.12 Boiling 20 μg/kg/FAO FAO (2004) Rice 5.66 Boiling Mexico Maize 116.34 Nixtamalization 20 μg/kg in maize grains/NMX-FF-034- NMX-FF-034-1995 (1995); NMX-FF-034/1-SCFI-2002 SCFI 1995; NMX-FF-034/1-SCFI-2002; (2002); NMX-FF-034/2-SCFI-2003 (2003); Norma Oficial NMX-FF-034/2–2003; NOM-188-SSA1- Mexicana NOM-188-SSA1-2002 (2002); 2002 Normal Oficial Mexicana NOM-247-SSA1-2008 (2008) 12 μg/kg in maize flour, tortilla and other nixtamalized products/NOM-247- SSA1-2008 Beans 10.38 Boiling No specific information found Chili 18.4 None (consumed 30 μg/kg (proposed by CODEX (Fresh and fresh), roasting, drying Alimentarius Commission)6 dried) Rice 5.64 Boiling 20 μg/kg/NOM-188-SSA1-2002 Costa Rica Maize 10.77 Nixtamalization 20 μg/kg/Decreto 27980-S based on Decreto Ejecutivo: 27980 (1999) Codex Alimentarius7 Beans 10.08 Boiling 20 μg/kg/Decreto 27980-S based on Codex Alimentarius7 Rice 45.69 Boiling 20 μg/kg/Decreto 27980-S based on Codex Alimentarius7 El Maize 70.03 Nixtamalization 20 μg/kg/FAO FAO (2004) Salvador Beans 17.32 Boiling 20 μg/kg/FAO Rice 10.53 Boiling 20 μg/kg/FAO Honduras Maize 77.96 Nixtamalization 1 μg/kg/FAO FAO (2004) Beans 12.05 Boiling 1 μg/kg/FAO Rice 14.42 Boiling No specific information found Nicaragua Maize 68.5 Nixtamalization No specific information found Beans 21.4 Boiling No specific information found Rice 43.3 Boiling No specific information found Panama Maize 25.5 Dehulled and pre- No specific information found cooked Beans 1.8 Boiling No specific information found Rice 66.4 Boiling 0 μg/kg/DGNTI-COPANIT-75-2002/ DGNTI-COPANIT-75-2002 (2002); DGNTI-COPANIT-74- DGNTI-COPANIT-74-2003 2003 (2003) a FAOSTAT (2021). b INCAP (2007) 2 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 Fig. 1. Summary of actions to mitigate mycotoxin contamination in the maize value chain. Upper panel refer to actions in the smallholder farming system. Lower panel are action at the large-scale farming system. Table 2 Fungi causing ear rot in maize, associated mycotoxin health effects and incidence in Mexico and Central America. Common Scientific Mycotoxin Effects on human and animal Symptoms on Coloration of Favorable Mexican CA countries name of name health maize ears fungi on conditions states with with high fungi infected for ear high incidence incidence maize kernels infection Aspergillus Aspergillus Aflatoxin (B1, B2, Carcinogenic, low Start at tip of Powdery Drought and Tamaulipas, Guatemala, flavus G1, G2) immunological response can be open olive-green/ heat stress Campeche, Honduras, Aspergillus lethal. yellow Sonora Panamá. parasiticus Fusarium Fusarium Fumonisin (B1, Linked to esophagus cancer, Can be White Poor soil Sinaloa, All CA verticillioides B2) pulmonary edema, symptomless or fertility, Jalisco and countries Fusarium immunosuppression, subfertility cracked kernels Warm and Guanajuato proliferatum and poor nutrient retention. or with white dry weather stripes Pink Warm and humid weather Gibberella Fusarium Zearalenone Follicular growth disorder, Start on the ear Red Cold and wet Toluca and Honduras graminareum (ZEA) ovulation, atresia, hyper tip Estado de and Costa Deoxynivalenol estrogenic syndromes, inhibition México Rica (DON) of protein synthesis, acute temporary nausea, vomiting, diarrhea, abdominal pain, headache, dizziness, and fever. Diplodia Stenocarpella Diploidiatoxin Liver dysfunction, loss in body Start on the ear Brown Warm and Chiapas and Belice and maydis weight and feed intake. base wet Guerrero Honduras Penicillium Penicillium. Ochratoxin A Necrotic renal tubules, periportal Start in ear at Blue/green Warm and – – verrucosum liver cells, immunosuppression, milky stage humid damage to the embryo and induction of cancer. Nigrospora Nigrospora None reported None Start on the Black High – – oryzae kernel tip moisture in storage Sources: CABI, 2019; CIMMYT. 2004; Groopman et al., 2021; IARC. 2012; Martínez Padrón et al., 2013; Mendoza et al., 2018; Morales-Rodríguez et al., 2007. 3 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 Table 3 Summary of occurrence of aflatoxin, fumonisin, deoxynivalenol and zearalenone levels (μg/kg) in general cereals and finished product (2017, 2018 and 2021) and maize only (2019 and 2020) in Latin America as reported by Biomin. Mycotoxin 2017a 2018a 2019b 2020b 20211c % of Average % of Average % of Average % of Average % of Average positive mycotoxin positive mycotoxin positive mycotoxin positive mycotoxin positive mycotoxin samples levels to samples levels to samples levels to samples levels to samples levels to (total no. maximum (total no. maximum (total no. maximum (total no. maximum (total no. maximum of samples level detected of samples level of samples level detected of samples level of samples level analyzed) in μg/kg analyzed) detected in analyzed) in μg/kg analyzed) detected in analyzed) detected in μg/kg μg/kg μg/kg Aflatoxin 23 (N = 8–1336 27 (N = 8–402 21 (N = 4–1264 12 (N = 4–179 8 (N = 7–2630 6943) 6023) 4091) 3839) 3861) Fumonisin 75 (N = 2992–218883 72 (N = 2184–72100 90 (N = 1700–170300 84 (N = 1390–56000 73 (N = 1489–64000 5500) 5465) 3304) 3577) 3528) Deoxynivalenol 82 (N = 919–12802 67(N = 1008–24880 56 (N = 340–5600 49 (N = 350–6330 68 (N = 581–4710 4849) 5107) 2608) 2568) 3380) Zearalenone 51 (N = 113–3553 48 (N = 130–520 27 (N = 53–2487 28 (N = 60–4948 25 (N = 82–3469 6030) 5276) 3472) 10511) 3467) Total exposure 80 70 84 87 74 risk Source: https://www.biomin.net/accessed on November 24, 2021. a Denotes that mycotoxin data reported during the year are for all samples analyzed from the region including individual cereals like maize, wheat and oats as well as finished feed. b Denotes that mycotoxin data reported during the year are for maize grain samples. c Data only covers January to September months of the year 2021. (Granados-Chinchilla et al., 2017; Groopman et al., 2021; Marimón to stress conditions or tolerant to the fungi, and appropriate agronomic Sibaja et al., 2021; Morales-Moo et al., 2020; Voth-Gaeddert et al., 2019, management, including sowing date, adequate fertilization, crop rota- 2020). For instance, increased AFs exposure is linked to liver cancer and tion, insect control and the use of biological control agents like non-alcoholic cirrhosis incidence in the region. These two health con- competitive non toxigenic strains (Mahuku et al., 2019; Martínez Padrón ditions are among the top 10 causes of death in Mexico and Central et al., 2013; Moral et al., 2020). Temperature and moisture control America. The frequency of stomach and colorectal cancer is also during storage and transportation can guarantee low water activity in increasing, while the incidence of growth stunting and micronutrient kernels and are critical postharvest factors that can reduce mycotoxin deficiency remains high despite concerted efforts to combat these accumulation. Processing and biotransformation are among other (Alvarez-Banuelos, Carvajal-Moreno, Mendez-Ramirez, & Rojo-Callejas, postharvest strategies used to mitigate consumer exposure to myco- 2015; Ponce-Garcia, Palacios-Rojas, Serna-Saldivar, & Garcia-Lara, toxins (Li et al., 2020; Villers, 2014). 2021; J. W. Smith et al., 2017; Voth-Gaeddert et al., 2020; htt This review discusses postharvest physical and processing strategies ps://www.healthdata.org/results/country-profiles. Accessed on that can be adopted to reduce AF and FB incidence in the context of January 19, 2022). Additionally, intestinal microbiome has been asso- Mexico and Central America. This paper identifies and discusses some ciated with child stunting and AF exposure. Voth-Gaeddert et al. (2019) knowledge gaps that need to be addressed as part of several mycotoxin- have recently added more evidence by assessing microbial differences related integrated actions that can help combat food safety issues, for children in Guatemala, grouped by height, age, diarrhea and AF malnutrition and food insecurity in the region related to mycotoxins. exposure. They found that children with a diet with more than 10 ng/kg of body weight/day had about 24 times higher odds of having a dys- 2. Occurrence of mycotoxins in Mexico and Central America biotic intestinal microbiome. The intake of milk and its derivatives as well as an increase in animal Grain production in Mexico and in Central America is characterized protein sources in the region has exacerbated secondary exposure to by a variety of agricultural systems, from smallholders growing land- various mycotoxins, especially AFs and FBs (Biomin, 2020; Carva- races in rain-fed conditions mainly for self-consumption and local niche jal-Moreno, Vargas-Ortiz, Hernández-Camarillo, Ruiz-Velasco, & markets, to large-scale, market-oriented farming with high inputs and Rojo-Callejas, 2019; Granados-Chinchilla et al., 2017; Marimón Sibaja improved germplasm (Logrieco et al., 2021). Regardless of the farming et al., 2021). Dairy products are considered to be an important part of system, one particular disease complex associated with maize deterio- human diet in the region. However, when AFB1 is ingested by animals ration and mycotoxin accumulation is generically referred to as maize through contaminated feed, this mycotoxin undergoes biotransforma- ear rot fungi, which produce mycotoxins in symptomatic or asymp- tion into aflatoxin M1 (AFM1) that is excreted in milk or eggs (Anfossi, tomatic grains (Ortiz et al., 2018). Ear rot pathogens can enter maize Di Nardo, Giovannoli, Passini, & Baggiani, 2015; Wochner, kernels through wounds caused by insects, through the silk, or system- Becker-Algeri, Colla, Badiale-Furlong, & Drunkler, 2017). AFM1 is ically from the stalk (Jones, Payne, & Leonard, 1980; Munkvold, McGee, potent but slightly less risky than AFB1. FB1 do not undergo any & Carlton, 1997; Murillo-Williams & Munkvold, 2008). The most com- biotransformation they are therefore equally potent as when consumed mon insects linked to Aspergillus flavus and Fusarium verticillioides in- through feed and food (Fink-Gremmels, 2008). This can therefore lead to fections are fall armyworm (Spodoptera frugiperda), corn earworm double human exposure when primary dietary food sources and animal (Helicoverpa zea), European corn borer (Ostrinia nubilalis) and maize feeds are contaminated. weevil (Sitophilus zeamais) (Haidukowski, Farinós, & Patiño, 2021; The mitigation of mycotoxin exposure is a multi-dimensional issue Hutchison et al., 2010; Lussenhop & Wicklow, 1990). that goes from the field to the plate. Strategies to mitigate mycotoxins AFs and FBs are the primary mycotoxins occurring in maize in include pre- and postharvest actions as well as health, agricultural and Mexico and Central America (Table 2). A. flavus, Aspergillus nomius and trade regulations. During the pre-harvest period, common preventive Aspergillus parasiticus are the main producers of AFs, while Fusarium measures include the use of appropriate crop varieties that are adapted verticillioides, Fusarium proliferatum and Fusarium subglutinans are the 4 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 main producers of FBs (Morales-Rodríguez, Yañez-Morales, Silva-Rojas, operations that provoke grain contamination by fungi (for example lack García-de-Los-Santos, & Guzmán-de-Peña, 2007; Rosa Junior et al., of hygiene) and their subsequent development (for example moisture 2019; Vaamonde, Patriarca, Fernández Pinto, Comerio, & Degrossi, content and temperature during storage, may lead to the production of 2003). Fusarium graminearum and Fusarium culmorum produce DON mycotoxins (Fig. 1). High temperatures in the food processing result in while F. graminearum, F. culmorum, Fusarium cerealis and Fusarium the formation of FB analogues such as N-carboxymethyl-fumonisin B1 or equiseti produce ZEN (Thapa, Horgan, White, & Walls, 2021). Other ear N-deoxy-D-fructose-1-yl-fumonisin B1. Compared to AFs, FBs are more rot fungi include Stenocarpella maydis, Nigrospora oryzae, Macrospora prone to destruction through different food processing methods. How- phaseoli and Penicillium spp., which develop mainly when climate con- ever, the health effects of the resulting FB analogues are currently not ditions are warm and humid (Table 2). well understood (Bryła, Roszko, Szymczyk, Jędrzejczak, & Obiedziński, The symptoms of different ear rot fungi differ between species 2016; Fandohan et al., 2005; Ponce-García, Serna-Saldivar, & (Table 2). Fusarium ear rot symptoms are characterized by scattered tufts Garcia-Lara, 2018). of mold on the ears ranging from white to pink and are accompanied by As a result of the co-colonization of maize by the above complex of starburst patterns on the kernels. Aspergillus ear rot appears as green- ear rot fungi, in addition to AFs and FBs, maize is also commonly pre- yellow spores and is commonly observed after hot, dry weather in the disposed to ochratoxins, trichothecenes and zearalenone. AFs and FBs post-pollination period. Drought-stressed maize plants such as those co-occur in maize more frequently, posing an array of health risks to growing in non-irrigated fields and pivot corners are vulnerable to these communities that consume maize as a staple diet (Smith, Madec, Coton, pathogens (CIMMYT, 2004). & Hymery, 2016). The potential for co-exposure of consumers to both AFs were first identified in the 1960s and are mainly produced by AFs and FBs is likely to occur due to the Mesoamerican diet and the A. flavus, A. parasiticus and A. nomius. The group consists of 18 chemical potential of Aspergillus and Fusarium to contaminate the staple, maize structures derived from difuranocoumarin with a coumarin nucleus- (Lee & Ryu, 2017). Thus, co-exposure can exacerbate the health and based bifuran group and a lactone ring or a pentanone ring (Richard, nutritional risks associated with the two mycotoxins, and concern is 2008). The most commonly occurring AFs are AFB1, B2, G1, G2, M1, growing since the current regulations and risk assessment guidelines are and M2. A. flavus produces AFs, including aflatoxins type B (AFBs), mainly based on toxicity studies that focus on individual mycotoxins which are considered to be the most carcinogenic and hepatocarcino- (Lee & Ryu, 2017; Torres et al., 2015). The health and nutritional impact genic. The International Agency for Research on Cancer (IARC) groups of the interaction of AF and FB mycotoxins in food and diets must be a AFB1, B2, G1, G2 and M1 as carcinogenic to humans and therefore subject of study. classified as Group 1. AFM2 is considered to be potentially carcinogenic The maximum AFB1 limits for maize, beans and rice is 20 μg/kg in to humans hence classified as group 2B (IARC, 2002). FBs are a group of most countries in the region including Guatemala, Mexico, Costa Rica El 28 structurally related mycotoxins produced by F. verticillioides, Salvador and Nicaragua. Honduras is the most stringent in the region F. proliferatum, F. nygamai, Alternaria alternata f. sp. Lycopersici and with maximum limits of 1 μg/kg for both maize and beans. Mexico is the A. niger. FBs are divided into four subtypes (Dall’Asta, Galaverna, et al., only country in the region with maximum level for AF for chili at 30 μg/ 2009; Upadhaya, Park, & Ha, 2010; Wan Norhasima, Abdulamir, Abu kg and with specific limits for grain and maize food products (Table 1). It Bakar, Son, & Norhafniza, 2009). The most studied FB subtypes are B1, must be noted that Mexico and the Central America countries do not B2 and B3. FBs have been associated with esophageal cancer, pulmonary have official regulations regarding FBs maximum limits. Even for the edema, immunosuppression, subfertility, increase in permeability to AFB1 levels there was reliance on secondary data sources like Codex pathogens, and reduction in nutrient absorption at the intestinal barrier Alimentaries Commission reports, FAO reports and U.S. Food and Drug level; IARC classifies FBs as potentially carcinogenic group 2B carcino- Administration (FDA) reports to obtain mycotoxin guidelines for Central gens (IARC, 2002; Braun & Wink, 2018). America countries (Table 1). Another concern is the high DON and ZEN Further, mechanical damage, or biotic damage by insects or birds level that call for urgent regulation. Clearly, the different maximum predisposes maize to colonization by fungi. Through 2020 regional permissible mycotoxin levels in the region need to be documented and if surveys, FBs were found to occur at high levels in Mexico and Central possible harmonized by the respective regulatory government organi- America (Biomin, 2020). FB structure is similar to that of sphingolipids: zations for easy cross border trading. sphinganine and sphingosine. They have a free amino group in C2 that inhibits ceramide synthase (sphinganine and sphingosine N-acyl- 3. Postharvest grain handling transferase), an important enzyme in the pathway of sphingolipid biosynthesis. The result is increased cytotoxicity (Sharma, He, & 3.1. Grain drying Sharma, 2004; Voss, Smith, & Haschek, 2007). Fumonisin B1 (FB1) is the most prevalent at 70% and its effects can be either acute or chronic In order to halt fungal development and the production of myco- in humans. Although the factors responsible for FB accumulation are not toxins during grain transportation and storage, it is necessary to lower well understood, high FB levels in raw maize have been associated with grain moisture after harvest. Large-scale, artificial drying is done for heat and drought conditions with high humidity periods just before 7–10 days at 40 ◦C but the drying temperature can be over 100 ◦C pollination. The optimum temperature for the growth of F. verticillioides depending on the end-use, for example for feed (Bala, 2016). A moisture and the production of FB1 is 25–30 ◦C (Bruns, 2003; Fandohan, Hell, content of 12–14% is recommended for a safe storage, which corre- Marasas, & Wingfield, 2003; F. M.; Liu, Chen, Fu, & Shih, 2005). The sponds to an equilibrium relative humidity of 65% (Bradford et al., presence of Fusarium graminearum reduces the production of FBs by 2018). However, higher temperatures can affect seed germination and F. verticillioides (Fandohan et al., 2003). Further, nutrient deficiencies, grain quality can deteriorate with high-speed and high-temperature especially of phosphorus, calcium and potassium, increase plant sus- drying by leading to a reduction in protein content, an increase in sus- ceptibility to fungal attack. Hybrids grown out of their adaptive range ceptibility to breakage, and an increase in hairline fractures (called and with no innate Fusarium resistance are also more susceptible to FB stress cracks) in the endosperm. Subsequently, broken grains or grains accumulation (Headrick & Pataky, 1991; Shelby, White, & Bauske, with an increased number of stress cracks are more susceptible to insect 1994). and fungal damage during storage (Hawkins, Windham, & Williams, As fungal AFs and FBs enter into the postharvest system, different 2005). factors may contribute to their accumulation or reduction, starting from Capacity for artificial drying is limited and the most common prac- drying in the field and harvesting and continuing through other post- tice in Mexico and other Central American countries is field drying to a harvest activities including drying, sorting, and processing (Fig. 1). moisture level of between 14% and 18%. In a smallholder farming sys- Whether it is a smallholder or large-scale farming system, conditions and tem, farmers use a variety of practices for field drying, including drying 5 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 cobs and plants in their natural position, cutting the plants at maturation small-scale farming, the effect of grain cleaning varies depending on the and leaving in the field in pyramidal-shaped stacks, or doubling the cobs level of contamination in the grain and on the percentage of contami- downwards (a practice referred as “folding”, or “doblado” in Spanish) nated grain removed (Pascale et al., 2020). (Tigar, Key, Flores-s, & Vazquez-a, 1994). The same practices are re- Grain integrity, including intact pericarps and embryos as well as ported in Guatemala where farmers complement them with drying in kernel wax content, is reportedly fundamental to reducing fungal farmhouse attics (Mendoza, Sabillón, et al., 2017). In such a system, infection and AFs production (Chen, Brown, Damann, & Cleveland, where farmers have little opportunity to monitor damage during field 2004; Ortega-Beltran & Cotty, 2020). At the household level and during drying, infestation by fungi starts in the field and may be important the wet-nixtamalization process at the industrial level, contaminated depending on the environmental conditions, particularly in humid cli- low-density and damaged maize kernels that are used for tortilla pro- mates (Bradford et al., 2018). Moisture content at harvest such as that duction in Mexico are commonly removed before nixtamalization or commonly found in the western highlands of Guatemala results in the during the steeping stage of the process, because such kernels float in the development of a large microbial community, including a significant nixtamalization liquid (Serna Saldivar & Rooney, 2015). Although amount of Fusarium and Aspergillus mycotoxin-producing molds (Men- flotation is, to some degree, effective in reducing mycotoxin contami- doza, Kok, Stratton, Bianchini, & Hallen-Adams, 2017). Farmers in nation, a significant proportion of mycotoxins can be carried over into Mexico also reported that additional atypical rains during drying can the next steps in the nixtamalization process (Matumba, Van Poucke, increase the development of toxigenic strains of fungi (González Rega- Njumbe Ediage, Jacobs, & De Saeger, 2015). A combination of different lado, Rivers, & Verhulst, 2017, pp. 42–48). sorting methods can be effective, but the use of combined methods Some farmers use motorized shellers that can cause physical damage within the regional context remains to be investigated. to grains and create entry points for fungal spores (Fandohan et al., Ortega-Beltran and Cotty (2020) found lower AFs levels in ground 2003). Some of the common practices recommended for reducing the kernels compared to wounded kernels, suggesting that storing flour risk of AF and FB accumulation during postharvest activities include could be more effective if insect or mechanical damage has occurred harvesting maize with the husk, sun drying on platforms, drying maize during crop growing or harvest. However, as they also point out, this without the husk, and the immediate removal of damaged cobs prior to would not be appropriate for consumers in Mexico and Central America storage (Hell, Cardwell, & Poehling, 2003; Odjo, Burgueño, Rivers, & as most of the maize is used for nixtamalization that uses whole kernels Verhulst, 2020). In addition, the promotion of low-cost drying solutions (Ortega-Beltran & Cotty, 2020; Palacios-Rojas et al., 2020). Addition- like the EasyDryM500 portable dryer developed in Kenya (Walker & ally, storing flour could bring other challenges like limited shelf life due Davies, 2017) or the BAU-STR dryer in Bangladesh have helped reduce to increased rancidity (Goffman & Böhme, 2001). the proliferation of fungi (Saha, Alam, Alam, Kalita, & Harvey, 2017) and could be affordable solutions for Mexico and Central American 3.3. Storage countries. The Mexican norm for maize commercialization sets limits on the In Mexico and Central America, smallholder farmers use a variety of percentage of kernels broken or stress-cracked of between 2 and 7% containers to store their grain, including traditional wooden structures, (NMX-FF-034/2-SCFI-2003, 2003). These limits aim to ensure grain metal containers and polypropylene sacks. But unfortunately, none of quality for optimal processing and grain safety. However, more regu- them sufficiently protect the grain against pest infestation (Giles & Leon, lations and guidance on grain quality in the region could help guarantee 1974; González Regalado et al., 2017, pp. 42–48; Mendoza, Sabillón, a reduction of mycotoxin levels and health impacts. et al., 2017; Tigar et al., 1994). Around 40% of maize can be lost post- harvest in Mexico’s tropical regions (García-Lara, García-Jaimes, & 3.2. Grain sorting Ortíz-Islas, 2020; Odjo et al., 2020). Fungal contamination and myco- toxin development account for part of these losses. Some farmers may Wounded, broken and damaged kernels or kernels with dead em- choose to treat their grain with insecticides, including aluminum bryos accumulate more AFs and FBs, and this can worsen with high phosphine tablets and deodorized malathion, two products authorized temperatures and moisture during the growing, harvesting and storage in Mexico, at doses between 4 and 6 tablets of aluminum phosphide per phases (Ortega-Beltran & Cotty, 2020); additionally, fine material, crop ton of grain and 1% weight-by-weight of deodorized malathion (Odjo residuals and dust within grain batches may contain mycotoxins (Pas- et al., 2020). However, there are farmers that treat their grain at higher cale et al., 2020). Healthy and contaminated kernels have shown sig- doses (1 tablet of aluminum phosphide per 50 kg of grain) (González nificant differences in size, shape and especially density (Pascale et al., Regalado et al., 2017, pp. 42–48) and little is known about the potential 2020). Hand- or mechanical cleaning operations targeting the elimina- effect of the use of these chemicals on the health. Cases of intoxication tion of defective kernels, especially those with off-coloration, germ- or by the use of insecticides are reported, but their use in storage has to be endosperm heat damage, broken kernels, and kernels with visible fungal discouraged, particularly in smallholder conditions (Bernardino or insect damage are known to effectively reduce mycotoxin levels Hernández, Torres Aguilar, Sánchez Cruz, Reyes Velasco, & Zapién during storage (Fandohan et al., 2005; Pascale et al., 2020). In fact, these Martínez, 2019; González Regalado et al., 2017, pp. 42–48; Odjo et al., operations are promoted by health and trade regulatory agencies and 2020; Villa-Manzano, Zamora-López, Huerta-Viera, Vázquez-Solís, & policies (FAO (2004); FDA (2020), Codex Alimentarius, Flores-Robles, 2019). NMX-FF-034/1-SCFI-2002, 2002). Sieves, gravity separators, color Few farmers use currently available hermetic storage technologies sorters or electronic sorters can contribute to reducing from 40 to 95% of like hermetic plastic bags and hermetic metal silos (García-Lara et al., AFs and FBs by removing off-colored and low-density kernels that have 2020; Odjo et al., 2020; Villers, 2014). Aspergillus species and fungi in been damaged by heat, insects, or fungi (Pascale et al., 2020). general are aerobic, and therefore their development and the synthesis At a household level, small farmers in Mexico and Central America of mycotoxins cease when the fungi are exposed to oxygen levels lower that use maize for self-consumption clean the grain manually — a time- than 0.025% of environmental levels. Oxygen can be considered a consuming task that does not guarantee a decrease in AF and FB expo- critical element for the growth, but not for the survival of these fungi. sure. This is because in most cases the discarded grain is given to Likewise, CO2 in concentrations of 20% is known to halt the germination backyard animals whose products are later consumed (Odjo et al., of spores and suppress the synthesis of AFs at levels greater than 10% 2020). In addition, grain sorting might not be done systematically (CAST, 2003). Thus, increased deployment of and training in the use of depending on the food-security context, and damaged grain could high-quality hermetic storage technologies in the region will benefit AFs therefore be mixed with sound grain, as reported by Mendoza, Sabillón, and FBs mitigation strategies (García-Lara et al., 2020; Odjo et al., et al. (2017) in Guatemala. In both large-scale, industrial farming and 2020). 6 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 Regarding large-scale storage systems, data on the management of mineral bioavailability (Awuor et al., 2017). Despite the high prevalence warehouses and the occurrence of mycotoxin contamination in Mexico of AF-contaminated foods in Mexico and Central American countries, and Central America is scarce. A study conducted in Mexico has, how- the use of adsorbents in foods is currently prohibited because they bind ever, reported that most grain warehouses have minimal or no equip- essential micronutrients. The supplementation of nixtamalized masa — ment, which may have a significant impact on the standards of quality a coarse-ground, cohesive corn dough — with adsorbents to selectively management including mycotoxin contamination (Ortiz Rosales, Ram- bind AFs in tortillas and related products has not been the subject of írez Abarca, González Elías, & Velázquez Monter, 2015). The training research. and application of a quality management system such as the SLAM Mexico and Central America are recognized for their biological di- (Sanitation, Loading, Aeration, and Monitoring) strategy (Mason & versity, and pre-Columbian civilizations used aromatic and medicinal Woloshuk, 2010) or the HACCP (Hazard Analysis and Critical Control plants in their daily activities. Some of these plants have been used as Points) approach can help in minimizing mycotoxin occurrence in these food additives due to the essential oils they contain that have insecti- warehouses. Most of these warehouses rely on aluminum phosphine cidal and repellent effects against insects, antimicrobial effects against tablets for control, but postharvest pests resistant to phosphine have fungi, and anti-aflatoxigenic properties (Palma-Tenango, been reported in the region (Afful, Elliott, Nayak, & Phillips, 2018). The Miguel-Chávez, & Soto-Hernández, 2017; Pöll, 2005). Essential oils use of ozone may be an alternative and has been successfully used to from aromatic plants are widely accepted because of their relatively low reduce AFs elsewhere. Maeba, Takamoto, Kamimura, and Miura (1988) adverse effects (rare allergic reactions), high volatility and biodegrad- determined the inactivation of the mutagenic activities of AFs via ozo- ability. Rangel-Fajardo, Tucuch-Haas, Burgos-Díaz, Gómez-Montiel, & nolysis. However, their results showed that AFB2 and AFG2 were more Basto-Barbudo, 2020 and Hernández-Cruz et al. (2019) have demon- resistant to degradation (34.3 mg/L over 50–60 min) compared to AFB1 strated that ground dry leaves of the Mexican tea plant Dysphania and AFG1 (1.1 mg/L over 5 min). Luo et al. (2014) determined that the ambrosioides, and essentials oils from Porophyllum linaria can control AFB1 degradation rate increased with ozone concentration and the damage caused by the maize weevil due to their terpene compounds, maize kernels’ treatment time. Kernel moisture content had a negative which may in turn limit fungal infestation. Juárez, Hernández, Bach, correlation with the degradation rate. Ozone application for at least 40 Sánchez-Arreola, and Bach (2015) reported the antifungal activity of min degraded fungi and reduced AFB1 by up to 88%. To our knowledge, essential oils extracted from Agastache Mexicana ssp. xolocotziana the use of ozone-treated maize in Mexico or Central America countries is against fungal strains including A. flavus isolated from stored grain. very limited but it might be an alternative for the future. Extracts from Buddleja perfoliate and Pelargonium graveolens have also shown the same potential (Juárez, Bach, Sánchez-Arreola, Bach, & 3.4. Grain conditioning agents, adsorbents and other food and feed Hernández, 2016). However, data on the use of these aromatic plants by additives smallholder farmers are scare, and a diagnostic made in Mexico has shown that only 1% of farmers surveyed use this strategy to protect their Farmers in Mexico and Central America may also use grain- grain during storage (González Regalado et al., 2017, pp. 42–48). Even conditioning agents, other than chemical insecticides, that potentially though recent research has shown that the use of these plant extracts has have an insecticidal effect and are used in combination with poly- no significant effect on product quality (Juárez, Bach, Bárcenas-Pozos, & propylene bags or any other non-hermetic containers. For example, Hernández, 2021), their suitability for generalized use has yet to be smallholder farmers in this region may use inert dusts as conditioning proven, given the potential effects on sensory quality of the food prod- agents to control pests. This category of adjuvants includes diatom- ucts, risk to the products’ forms, and the method’s practicality at large eceaous earth, limestone, clays, zeolites, ash, sand and is considered as scale. Generally Regarded As Safe (GRAS) additive in food and feed. by the U. Few farmers use currently available hermetic storage technologies S. Food and Drug Administration (Subramanyam & Roesli, 2000). The like hermetic plastic bags and hermetic metal silos (García-Lara et al., use of lime during storage was reported by the ancient Aztecs and is still 2020; Odjo et al., 2020; Villers, 2014). Mycotoxigenic fungi, including, used today in Mexico and Central America (Golob, 1997; González Aspergillus spp. are aerobic, and therefore their development and the Regalado et al., 2017, pp. 42–48). While inert dusts seem to be a synthesis of mycotoxins cease when the fungi are exposed to oxygen non-toxic solution to the problem of insect control, their effectiveness in levels lower than 0.025% of environmental levels. Oxygen can be minimizing losses, which depends on relative humidity and tempera- considered a critical element for the growth, but not for the survival of ture, can be reduced in tropical conditions (Odjo et al., 2020). Data on these fungi. Likewise, CO2 in concentrations of 20% is known to halt the the use of lime on AFs and FBs levels are scarce, however. But the effects germination of spores and suppress the synthesis of AFs at levels greater of similar conditioning agents on mycotoxins have been investigated than 10% (CAST, 2003). Thus, increased deployment of and training in elsewhere. Some studies have shown that the synthetic zeolite NaA the use of high-quality hermetic storage technologies in the region will (sodium aluminum silicate) is not effective in binding aflatoxin B1 benefit AF and FB mitigation strategies (García-Lara et al., 2020; Odjo (AFB1) in feed in comparison with bentonites (Vekiru et al., 2015). The et al., 2020). mechanism of the interaction between hydrated sodium-calcium Regarding large-scale storage systems, data on the management of aluminosilicate clay and AFB1 is the chelation of the toxin carbonyl warehouses and the occurrence of mycotoxin contamination in Mexico groups with metal ions or metal surface sites at a low pH. Bentonites are and Central America is scarce. A study conducted in Mexico has, how- widely accepted, low-cost binding materials with a high specific surface ever, reported that most grain warehouses have minimal or no equip- area for reducing the toxic effects of AFB1. Moreover, they improve the ment, which may have a significant impact on the standards of quality palatability and durability of supplemented feed. Bentonites containing management including mycotoxin contamination (Ortiz Rosales et al., cis-vacant smectite, C2 trans-vacant smectite, and clinoptilolite con- 2015). The application of a quality management system such as the taining zeolite Z08 have been successfully tested. However, the effec- SLAM (Sanitation, Loading, Aeration, and Monitoring) strategy (Mason tiveness of bentonites depends on the chemical batch and source of & Woloshuk, 2010) or the HACCP (Hazard Analysis and Critical Control extraction (geological deposit), dose, and AF loads in the feed to be Points) approach can help in minimizing mycotoxin occurrence in these treated (Magnoli et al., 2008; Vekiru et al., 2015). A clinical trial tested warehouses. Most of these warehouses rely on aluminum phosphine the oral ingestion of calcium montmorillonite clay capsules or the same tablets for control, but postharvest pests resistant to phosphine have adsorbent supplemented directly to the diet. The study concluded that been reported in the region (Afful et al., 2018). The use of ozone may be the clay effectively reduced AFs without detrimental effect in terms of an alternative and has been successfully used to reduce AFs elsewhere. palatability and food acceptability. However, further studies are needed Maeba et al. (1988) determined the inactivation of the mutagenic ac- to determine if these adsorbents cause side effects, especially in essential tivities of AFs via ozonolysis. However, their results showed that AFB2 7 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 and AFG2 were more resistant to degradation (34.3 mg/L over 50–60 Fig. 2 depicts the most common processes used in Mexico and Central min) compared to AFB1 and AFG1 (1.1 mg/L over 5 min). Luo et al. America to transform maize kernels into dishes. Thermal processes are (2014) determined that the AFB1 degradation rate increased with ozone the most common ones, including both dry heating (baking, roasting, concentration and the maize kernels’ treatment time. Kernel moisture popping) and wet-heating (lime-cooking and the subsequent baking, content had a negative correlation with the degradation rate. Ozone frying, steaming processes). Ranges of reductions in AF and FB areas are application for at least 40 min degraded fungi and reduced AFB1 by up to also included in this figure. These ranges are based on several reports 88%. To our knowledge, the use of ozone-treated maize in Mexico or analyzed by Schaarschmidt and Fauhl-Hassek (2021) and specific ref- Central America countries is null or very limited and it may be an erences for Mexican and Central American food products described in alternative for the future. more detailed below. 4. Grain processing 4.1. Baking, roasting and popping During food processing, mycotoxins can be redistributed, degraded, Baked maize products in the region include maize bread, a diverse modified, bind or be released from the food matrixes. Mycotoxin content array of maize cookies (semitas, coricos, pemoles, gorditas, polvorones can also be altered by dilution or concentration effects due to moisture totopos, tlayudas, etc.) and flat bread prepared with decorticated maize changes or when different ingredients are mixed (Schaarschmidt & (arepas, consumed in Panama). Some of these products are consumed Fauhl-Hassek, 2021). Thus, the stability of mycotoxins is affected by sporadically, during special festivities, at a specific time of the year, or in moisture, heating regime, type of cereal/food matrix, pH levels and even specific towns/areas (Fernández Suárez, Morales Chávez, & Gálvez external forces like pressure or shear forces. Meal composition can also Mariscal, 2013; Guzzon et al., 2021). The average reduction in AFs contribute to lowering the bioaccessibility and bioavailability of my- during baking ranges from 15 to 50% and to about 70% for FBs (See- cotoxins (Lin, Hu, Zhang, Xia, & Zhang, 2019). AF are more stable than nappa & Nyagahungu, 1982); the degree of variation depends on the FBs. FB are heat stable up to 100 ◦C, although significant decrease of temperature and length of baking, as well as the presence of other in- detectable FBs has been reported. Chemical degradation of FBs occurs gredients. To our knowledge, however, there is no report on concen- via Maillard-type reactions at high temperature or hydrolysis of FBs also trations of AFs or FBs in baked maize products in Mexico and Central occurs in the presence of alkali (Ponce-García et al., 2018). Moreover, in American countries. the past decade or so, the presence of FBs bound to proteins or other food Maize kernels are commonly toasted, milled, and mixed with sugar components as well as FBs physical entrapment into the structure of cane and cinnamon or other flavors. This flour is consumed directly or macromolecular components like starch and proteins have been diluted in water or milk (atole) (Guzzon et al., 2021). Roasting can have demonstrated, as well as its implication in the accuracy of FBs moni- a stronger effect on the degradation of mycotoxins, because normally toring in food products (Dall’ Asta et al., 2009). temperatures are higher, at a higher surface to volume ratio and Fig. 2. Percentages of reported losses of AFs and FBs in food products derived from common maize processing methods used in Mexico and Central America. 8 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 therefore a higher internal temperature. About 30–100% reduction in & Rooney, 2015). The hydrolyzed pericarp, the partial removal of the FBs and 40–80% reduction in AFs have been found in dry heating impact germ and the leaching of FBs and AFs into the cooking liquid are the studies on mycotoxins (Schaarschmidt & Fauhl-Hassek, 2021). main mechanisms responsible for the significant reduction of these Méndez-Albores, De Jesús-Flores et al. (2004)monitored the fate of AFs harmful metabolites (Odukoya et al., 2021; Schaarschmidt & in spiked maize kernels toasted and boiled to prepare atole and found Fauhl-Hassek, 2019; Serna Saldivar & Rooney, 2015). During the nix- that the toasting led to about 30% reduction in AFB1, while a further tamalization, the alkaline treatment remove two tricarballylic acid side moderate reduction occurred during the boiling step. chains from the 20-carbon backbone of FB1 resulting in the formation of Popping maize kernels by heating at 220–230 ◦C leads to a reduction hydrolyzed fumonisin B1 (HFB1) (Hartl & Humpf, 1999). Dom- of around 50% in AFB1, independently of whether the kernels are brink-Kurtzman and Dvorak (1999) and Voss, Poling, Meredith, Bacon, spiked, inoculated with the fungi, or naturally contaminated (Rehana & and Saunders (2001) described the fate of FB1 and hydrolyzed FB1 Basappa, 1990). Recent surveillance of popcorn maize samples collected during the nixtamalization and commercial processing of fried tortilla in 30 different places in the city of Veracruz found that about 47% of the chips, respectively, and found that more the 80% of those mycotoxins samples had significant levels of AFs, indicating that the popping process were lost in the process, especially during the nixtamalization and was not enough to remove the AFs, and that it is therefore important to rinsing steps. Although HFB1 has greater cytotoxicity than FB1, it is less ensure that the grain to be processed is clean (Morales-Moo et al., 2020). toxic in vivo (Hopmans & Murphy, 1993; Park, Scott, Lau, & Lewis, D’Ovidio, Trucksess, Devries, and Bean (2007) analyzed FBs in popcorn 2004). Voss, Ryu, Jackson, Riley, and Gelineau-Van Waes (2017) from the optical reject stream that contained about 1 ppm of FBs. After monitored the effectiveness of extrusion and nixtamalization methods popping in a microwave oven, a 67–92% reduction in the FBs was by rat-feeding bioassays and found that neither FB1 nor the HFB1 caused observed. neural tube effects in experimental mice and suggested that extrusion and nixtamalization reduce the potential toxicity of FB1 contaminated 4.2. Alkaline-cooking or the nixtamalization process maize. AFs have also been found to be reduced through nixtamalization: the Nixtamalization or alkaline-cooking is a Mesoamerican ancient reported AFB1 reductions range from 28% to 98%, depending on the technique for transforming maize into hundreds of different food dishes level of AF contamination, the nixtamalization process used, and the (Palacios-Rojas et al., 2020). The traditional and industrial methods degree to which the nixtamalized kernels were contaminated prior to the used today consist mainly of cooking maize kernels in a lime solution processing (Fig. 2). A steeping time longer than 6h, a calcium hydroxide (calcium hydroxide) for about 30–40 min, followed by overnight concentration higher than 1%, and an intense grain-washing step will steeping for 8–16 h. The lime-cooked grains are washed to remove impact the final content of mycotoxins in the food products excess lime and then stone-ground to transform them into masa. The (Guzmán-De-Peña, 2010; Palacios-Rojas, unpublished data). In the resulting masa is formed into tortilla discs that are baked in continuous nixtamalization process, the grain cooking at 90 ◦C and the very high pH gas-fired ovens, although it is thought that about 300 other food prod- (12–14), the degradation of AFs is induced by the hydrolytic cleavage of ucts are derived from such dough (Palacios-Rojas et al., 2020). After the lactone ring of AFs, which is followed by decarboxylation lime-cooking, other processes like baking, frying and steaming are used (Schaarschmidt & Fauhl-Hassek, 2019). However, if the processing to prepare the final dishes (Fernández Suárez et al., 2013). In Fig. 2 the conditions are not optimal to induce the decarboxylation, the cleavage incidence on the AFs and FBs in some of the most popular nixtamalized of the lactone ring can be reversed at the lower pH during the human food products is summarized. Tortillas are considered the most common digestion process (Méndez-Albores, Arámbula-Villa et al., 2004; Moc- staple food in Mexico and Guatemala. They are also highly consumed in tezuma-Zárate et al., 2015; Price & Jorgensen, 1985). The fact that AF El Salvador, Honduras and Costa Rica (Table 1). On average, Mexicans adducts have been found in tortilla consumers might indicate that in rural and urban areas consume 79.5 and 56.7 kg of tortillas each year, reactivation of the AF ring is taking place, or that not all AFs were fully respectively (CEDRSSA, 2014). These amounts are equivalent to seven detoxified during the nixtamalization process, Their effect and accu- and five tortillas daily, which supply 477 and 340 kcal, respectively. In mulation can also be exacerbated by the amount of tortillas and of other addition to tortillas, several other food products including sopes, tla- products potentially contaminated with AFs that are commonly coyos, salbutes, chalupas, etc are prepared by baking the nixtamalized consumed with nixtamalized tortillas as part of the daily diet, including dough. Nixtamalized dough is also baked and fried to produce chips or beans, chili peppers or rice (Table 1) (Kroker-Lobos et al., 2019). totopos, chilaquiles, etc., or it can be steamed to make tamales, a very Alternative methods to the traditional nixtamalization have been common breakfast dish in Mexico and Central American countries. developed and studied, particularly because of the drawbacks of tradi- Atoles, a popular drink, also given to children as weaning food, can be tional nixtamalization, such as long steeping times leading to more en- prepared by diluting the nixtamalized dough with water or milk ergy expenditure, and the high production of cooking liquids to contain (Fernández Suárez et al., 2013; Guzzon et al., 2021; Martorell, 2020). the polluting residues (Escalante-Aburto et al., 2020). More Cooking time and temperature, lime concentration, steeping time, ecologically-friendly methods, such as microwaving and the use of other and intensity of the washing step vary from household to household, salts instead of calcium hydroxide, have also been tested for their impact within each country, and among the Mesoamerican countries. Industrial on AFs. In tortillas processed with traditional nixtamalization, the total production of nixtamalized dry milling flour is accomplished by the AF degradation rate was 92%. In tortillas created through the ecological sorting and removal of damaged kernels, lime-cooking, nixtamal process, degradation rates were between 61% and 78% washing, grinding, drying, sieving, regrinding coarse particles, re- (Méndez-Albores, Villa, et al., 2004). The effects of the calcium sources sieving, classifying and blending to meet specific requirements on the fate of AFs in nixtamalized foods should be explored further. For regarding particle size distribution, water absorption and pH (Serna example, some alternative nixtamalization processes use sources other Saldívar & Perez Carillo, 2016). than calcium hydroxide (lime), such as wood ash, CaCO3, CaSO4, CaCl2, In addition to the nutritional benefits of the nixtamalization process and C6H10CaO6 (Santiago-Ramos et al., 2018). Odukoya et al. (2021) due to the increased intake of calcium, increased niacin bioavailability found a significant reduction of FBs in nixtamalized maize and sorghum and fiber intake, and reduction in phytate (Escalante-Aburto et al., 2020; when using wood ash, calcium hydroxide, sodium hydroxide and po- Palacios-Rojas et al., 2020), nixtamalization contributes to a reduction tassium hydroxide; however, tortilla quality and sensory tests might be in FBs and AFs, mainly due to the physical loss of the pericarp into the important when using different lime sources, especially in a Meso- residual cooking- and steeping-water known as nejayote (cooking american context where the tortilla is part of the culture and consumers liquid). Lime is known to hydrolyze fiber components in maize and can be very knowledgeable about how a nixtamalized tortilla should enhance pericarp detachment from the rest of the kernel (Serna Saldivar taste. 9 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 Nixtamalized extruded maize is used at mid- and large-scale to forms of FBs as well as other hidden mycotoxins like zein-bound zear- produce chips and snacks. Maize-based breakfast cereals are also pro- alenone is important to further assess the nutritional and safety prop- duced by extrusion. This cooking method involves a mixture of in- erties of this technology and measure the mycotoxin exposure risk of the gredients (maize, water, lime, sugars, and/or additives), cooking under consumers (Tan, Zhou, Guo, Zhang, & Ma, 2021; De Girolamo et al., pressure, and shear forces due to the rotating screw and extrusion at very 2016). The development and deployment of cost-effective methodolo- high pressure for moisture reduction and shaping. Schaarschmidt and gies and availability of proper standards could facilitate such monitoring Fauhl-Hassek (2021) have summarized several reports on the effect of at higher scale in the region. extrusion conditions on the mycotoxin levels. In general, extrusion has a high impact on mycotoxin content, but it can vary depending on which 5. Co-exposure to aflatoxins and fumonisins in Mexico and ingredients are included, the extrusion conditions, and the type of Central America mycotoxin (Martinez & Monsalve, 1989; Elias-Orozco, Castellanos-Nava, Gaytán-Martínez, Figueroa-Cárdenas, & Loarca-Piña, The high consumption of tortillas and other nixtamalized, maize- 2002) (Fig. 2). The inactivation of AFB1, AFB1, and AFB1-dihydrodiol in derived products has led to high exposure to AFs and other myco- the extrusion process using lime together with hydrogen peroxide toxins in the region. As presented in Table 1, in Mexico and the Central showed higher elimination of AFB1 than treatments with lime or American region, regulations for AFB1 are different among countries: hydrogen peroxide alone. The extrusion process with 0.3% of lime and regulations are limited to raw grain; they do not exist; or they are not 1.5% of hydrogen peroxide was the most effective at detoxifying maize easily accessed or found. In Mexico, the regulatory limit for maize tor- tortillas. A high level of these reagents negatively affected sensory tillas is 12 μg/kg of total AFs (Norma Oficial Mexicana characteristics such as the taste and aroma of tortillas compared with NOM-187-SSA1/SCFI-2002, 2002). In Guatemala, El Salvador and Costa those produced by traditional nixtamalization (Elias-Orozco et al., Rica, the limit is 20 μg/kg in maize grain, but the regulations do not 2002). Although hydrogen peroxide is a chemical oxidant with high clearly specify the levels for nixtamalized tortillas (Table 1) (COGUA- potential to reduce AFs, it is not allowed in EU countries, but it can be NOR, 1982; FAO, 2004; Food & Drug Administration (FDA), 2020). used in other countries at very low levels. The FDA allows the use of Unless accepted AF levels in crops as well as food products are revised food-grade reagent as an anti-microbial and with a maximum limit of and standardized and regulations are enforced, international develop- 0.001% w/w (Food & Drug Administration (FDA), 2020; Normal Oficial ment efforts to improve food security, nutrition and health are at risk Mexicana NOM-247-SSA1-2008, 2008). (Lizárraga-Paulín, Miranda-Castro, Moreno-Martinez, Torres-Pacheco, The reduction of FBs in extruded maize has been shown in different & Lara-Sagahón, 2013). Equally important is the regulation and moni- studies and can vary from 30 to 90%. As for the AFs, the FBs reduction toring of FB and HFB levels, not only in the maize value chain, but also in depends on level of initial contamination, moisture, temperature, screw other relevant dietary crops in the region. Table 4 summarizes published speed and extrusion die (Castelo, Jackson, Hanna, Reynolds, & Buller- surveillance studies of AFs and FBs in common maize products in Mexico man, 2001; Cortez-Rocha, Trigo-Stockli, Wetzel, & Reed, 2002; Scuda- and Central American countries. Biological and methodological vari- more, Guy, Kelleher, & MacDonald, 2008). In general, lower moisture ability (from sampling to analytical recovering, matrix composition, led to higher reductions of FB and HFB. Katta, Jackson, Sumner, Hanna, moisture) are challenges to consider when comparing data and drawing and Bullerman (1999) and De Girolamo, Solfrizzo, and Visconti (2001) conclusions on mycotoxin exposure (Schaarschmidt & Fauhl-Hassek, have point out, however, that extrusion conditions that led to product 2021). Nevertheless, taking together the mycotoxin surveillance in with acceptable color and expansion not necessarily led to high re- food products and the clinical studies, the risk of exposure to AFs and ductions of FB1. During the applied direct extrusion is where most of the FBs by the Mexican and Central America populations is evident. In some FBs reduction occurs; while in pellet extrusion and frying pellets not of the studies, the levels of AFs and/or FBs seem low or even within the changes or very low reduction can occur (Scudamore et al., 2008). In ranges accepted by the regulations. However, it is important to consider addition to the technical extrusion parameters, the type and amount of that exposure can be exacerbated by the quantity of contaminated food ingredients added in the process, like salt, glucose or other sugars, can that a person is consuming. Although nixtamalization and other food have positive impact in FBs reduction (Bullerman et al., 2008; Jackson processes used in the region could have an impact on reducing AFs and et al., 2011; Scudamore et al., 2008). N-acyl FBs derivatives can be FBs, nothing that is done at postharvest level, including appropriate formed when glucose is added, including N-(carboxymethyl)-fumonisin food-processing conditions, will ensure mycotoxin elimination if grain is B1 (NCM-FB1) and N-(1-deoxy-D-fructos-1-yl)-fumonisin B1 (NDF-FB1) highly contaminated in the field. (Bullerman et al., 2008; Jackson et al., 2011; Ponce-García et al., 2018). Surveys and clinical studies in the region, mainly in Mexico and Seefelder, Hartl, and Humpf (2001) reported very low concentrations of Guatemala, have shown the presence of FB1 in human urinary samples NCM-FB1 in extruded commercial products from Germany and point out (Riley et al., 2012; Torres et al., 2014, 2015; Yun et al., 2008). In the low risk due also to the low toxicity of this FB derivative. To our addition, and as summarized and highlighted by Ponce-Garcia et al. knowledge, detailed monitoring of FBs derivatives is not a common (2021), there is increased evidence of AF abducts found in different practice, especially in the large informal industry of extruded products populations during clinical studies in the region, as well as an increase in that can be found in Mexico and Central American countries. diseases and deaths where the causes are associated with AF exposure, The so called “hidden fumonisins” refer to FBs to noncovalently including hepatocellular carcinoma, cervical cancer, child stunting and matrix-bound derivatives. The use of alkaline hydrolysis procedures has dysbiotic intestinal microbiome (Díaz de León-Martínez et al., 2021; contributed to the determination of hidden FB1 in maize (Dall’Asta, Ponce-Garcia et al., 2021; Voth-Gaeddert et al., 2019). Falavigna, Galaverna, Dossena, & Marchelli, 2010). A very small survey Co-occurrence of FBs and AFs is of great concern given the potential including nixtamalized flour and tortilla chips revealed the of FB1 to modulate AFB1 hepatoxicity (Torres et al., 2015). Co-presence co-occurrence of FBs with partially hydrolyzed FB (PHFB) and HFB (De of FBs and AFs in the same grain has been documented from field to Girolamo, Lattanzio, Schena, Visconti, & Pascale, 2014). De Girolamo, processed food, and co-exposure has been highlighted in clinical studies. Lattanzio, Schena, Visconti, and Pascale (2016) have also shown the that Mendoza et al. (2018) reported the presence of AFs and FBs in 50% of nixtamalization reduce the number of FBs and PHFBs, converting them the grain samples collected from 25 farmers in Huehuetenango depart- to HFBs. The alkaline process also made available matrix-associated FBs ment in Guatemala, and in 2015, Torres et al. reported FBs and AFs in as it was revealed by the increase of total amount measured in the raw 640 samples collected in 22 departments of Guatemala. Trucksess, maize. Although nixtamalization have advantages in providing safer Dombrink-Kurtzman, Tournas, and White (2002) found both FBs and products in terms of FB contamination, studies at higher/real scale will AFs in incaparina, a mixture of maize and cottonseed flour supplemented be beneficial. In addition, appropriate monitoring of the hydrolyzed with vitamins and minerals and used as a high-protein food supplement, 10 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 Table 4 Surveillance studies on occurrence of aflatoxins and fumonisins in maize products in Mexico and Central America. NR: not reported. Maize Process Country of Fumonisins Aflatoxins Reference product study Incaparina Milling Guatemala n = 8 n = 8 Trucksess et al. (2002) 100% with FB1, FB2, FB3 100% with AFB1, <214 0.2–2.2 μg/g μg/kg 100% with AFB2, <32 μg/ kg Pozol Nixtamalization + Mexico NR n = 111 Méndez-Albores, De Jesús-Flores et al. (2004) boiling 17% with AFB1 and AFB2 <20 μg/kg Popcorn Popping Mexico NR n = 30 Morales-Moo et al. (2020) 40% AFs 0–26 μg/kg AFB1 0–51 μg/kg AFB2 0–46 μg/kg AFG1 0–28 μg/kg AFG2 Tortilla Nixtamalization + Mexico NR n = 37 Palacios-Rojas ( unpublished data) baking 15% with AFB1 >20 μg/kg Tortilla Nixtamalization + Mexico NR n = 50 Rodríguez-Aguilar et al. (2020) baking 4% with AFB1 >12 μg/kg Tortilla Nixtamalization + Mexico n = 64 NR Gilbert Sandoval et al. (2019) baking 98% with FB1 and FB2; FB1 9–1589 ppm; FB2 24–524 μg/g Tortilla Nixtamalization + Mexico n = 120 n = 120 Wall-Martínez et al. (2019) baking 90% with FB1 71% with AFB1 <526 μg/g 0–22 μg/kg Tortilla Nixtamalization + Mexico n = 88 NR Gilbert Sandoval et al. (2019) baking 4% AFB1 >1 μg/g Tortilla Nixtamalization + Mexico NR n = 171 Zuki-Orozco, Batres-Esquivel, Ortiz-Pérez, baking 50% with AFB1 Juárez-Flores, and Díaz-Barriga (2018) 0–287 μg/kg Tortilla Nixtamalization + Mexico NR n = 396 Castillo-Urueta, Carvajal, Méndez, Meza, and Gálvez baking 17% with AFs (2011) 3–385 μg/kg AFB1, AFB2, AFG1, AFG2 Tortilla Nixtamalization + Mexico n = 9 NR Dombrink-Kurtzman and Dvorak (1999) baking 100% with FB1 0.2–1.8 μg/g Tortilla Nixtamalization + Guatemala n = 72 NR Meredith, Torres, De Tejada, Riley, and Merrill (1999) baking 100 with FB1 0.4–11.6 μg/g especially for malnourished children in Guatemala. Wall-Martínez et al. climate-change effect on crop safety is increasing, and therefore actions (2019) also reported the presence of AFs and FBs in tortilla samples in during pre-harvest are essential. At a postharvest level, several options Veracruz, Mexico. Co-exposure to AFs and FBs and the exposure to FB have been explored. Some are more applicable at a lower scale while analogues need much more attention in the field, as do their health others still need further investigation and application in the region. impacts in Mexican and Central America populations (Gilbert Sandoval, However, the creation of awareness, training, and the communication of Wesseling, & Rietjens, 2019; Torres et al., 2015). mycotoxin issues in Mexico and Central America are first steps towards More surveys in the field and of storage and end products are the effectiveness of pre- and postharvest mitigation strategies. If farmers necessary in other countries of the region and should include other and vulnerable populations are aware of the health and nutrition im- mycotoxins and the modified/matrix associated forms. It is also plications of mycotoxin-contaminated grain and crops, they might enact important to explore alternative analytical methods as proposed by or more regularly employ simple practices like kernel cleaning and Chavez, Cheng, and Stasiewicz (2020) that include near infra-red avoid using contaminated kernels to feed livestock. At a country level, reflectance and fluorescence imaging. Other risk-assessment modeling the creation of awareness could also aid in enforcing and monitoring approaches considering simultaneous mycotoxins could also provide regulations. Unfortunately, no, or very limited public information, further and more holistic information for taking measurements and including scientific studies or regulations were found for countries like devising specific mitigation actions (Battilani et al., 2020; N.; Liu et al., El Salvador, Honduras and Nicaragua. Grain integrity and quality are 2021). basic traits that should be considered more in maize production, con- sumption and trade. Hermetic technologies can reduce fungal contam- 6. Conclusions ination and AF production during storage. Several methods to treat contaminated grain have been studied, but their application in the re- Mexican and Central American populations are at a high risk of gion is limited. Some of the main limitations are the potential effects on mycotoxin exposure and especially to AFs and FBs due to the large sensory traits of the food products and the cost and scalability of such intake of products from crops that are prone to high contamination. Pre- technologies. and postharvest mitigation strategies as well as appropriate regulatory The nixtamalization process significantly reduces the amounts of AFs environments could help reduce exposure to the mycotoxins. The and FBs present in products like tortillas and fried snacks due to the 11 S. Odjo et al. F o o d C o n t r o l 138 (2022) 108968 physical removal of these toxins. Given the fact that nixtamalization Bullerman, L. B., Bianchini, A., Hanna, M. A., Jackson, L. S., Jablonski, J., & Ryu, D. contributes to the release of hidden FBs, monitoring of HFB is very (2008). Reduction of fumonisin B1 in corn grits by single-screw extrusion. Journal of Agricultural and Food Chemistry, 56(7), 2400–2405. https://doi.org/10.1021/ relevant. Optimization of nixtamalization guidelines at both the jf0729513. household and industrial level need to be developed, since they may CABI. (2019). Crop protection compendium. Wallingford , UK: CAB International. www. contribute to a decrease in or elimination of AFs and FBs in products. cabi.org/cpc. Carvajal-Moreno, M., Vargas-Ortiz, M., Hernández-Camarillo, E., Ruiz-Velasco, S., & Rojo-Callejas, F. (2019). Presence of unreported carcinogens, Aflatoxins and their Declaration of competing interest hydroxylated metabolites, in industrialized Oaxaca cheese from Mexico City. In Food and chemical toxicology (Vol. 124, pp. 128–138). Elsevier Ltd. https://doi.org/ The authors reported no potential conflict of interest. 10.1016/j.fct.2018.11.046. CAST. (2003). Mycotoxins: Risks in plant, animal, and human systems. Task Force Report. https://www.international-food-safety.com/pdf/Mycotoxins - Risks in Plant, Acknowledgments Animals and Human Systems.pdf. Castelo, M. M., Jackson, L. S., Hanna, M. A., Reynolds, B. H., & Bullerman, L. B. (2001). Loss of fumonisin B1 in extruded and baked corn-based foods with sugars. Food and The authors wish to acknowledge the financial support of MasAgro- Chemical Toxicology, 66, 416–421. Cultivos para México, a program of the Mexican government in collab- Castillo-Urueta, P., Carvajal, M., Méndez, I., Meza, F., & Gálvez, A. (2011). Survey of oration with Grupo Maseca and the CGIAR research program MAIZE aflatoxins in maize tortillas from Mexico City. Food Additives and Contaminants: Part B Surveillance, 4(1), 42–51. https://doi.org/10.1080/19393210.2010.533390. CRP and CCAFS. “CCAFS’ work is supported by CGIAR Fund Donors and CEDRSSA. (2014). Consumo , distribución y producción de alimentos : El caso del through bilateral funding agreements. For details, please visit complejo maiz-tortilla. www.cedrssa.gob.mx. https://ccafs.cgiar.org/donors". We thank partners in the region (Adri- Chavez, R. A., Cheng, X., & Stasiewicz, M. J. (2020). A review of the methodology of analyzing aflatoxin and fumonisin in single corn kernels and the potential impacts of ana Murillo, Manolo Mazariegos, Mario Fuentes, Gabriela Jimenez) for these methods on food security. Foods, 9(3), 297. https://doi.org/10.3390/ sources on mycotoxin regulations in Mexico and Central America. We foods9030297 thank Borlaug fellow, Molly Carrol, and summer student, Diana Laura Chen, Z. Y., Brown, R. L., Damann, K. E., & Cleveland, T. E. (2004). Identification of a maize kernel stress-related protein and its effect on aflatoxin accumulation. Figueroa-Casarrubias, for support in collecting and analyzing commer- Phytopathology, 94(9), 938–945. https://doi.org/10.1094/PHYTO.2004.94.9.938 cial tortillas in the Texcoco area. We appreciate contributions from CIMMYT. (2004). Maize diseases: A guide for field identification (CIMMYT). https://reposi Sergio Serna-Saldivar, Nestor Ponce-Garcia and Silverio Garcia-Lara. We tory.cimmyt.org/xmlui/bitstream/handle/10883/775/78507.pdf?sequence=4&is thank colleagues of communication department at CIMMYT including Allowed=y. COGUANOR. (1982). 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