Integrated peanut aflatoxin management for increase income and nutrition in Northern Ghana

Aflatoxins contamination in peanut seeds remains a major challenge in Ghana. This study evaluated aflatoxin levels in peanut samples from farmer storage units, and participatory on-farm research trials. In all, 240 respondents were covered from six main producing districts in northern Ghana through a multi-stage sampling approach. Samples were analysed for total aflatoxins using the indirect Enzyme Linked Immunosorbent Assay technique. Overall, total aflatoxins in the farmer stored nuts showed wide variations across communities and districts. At 20 ppm permissible level, 92.9% of samples (n = 240) from farmer stored peanuts and 98.7% of samples (n = 150) from the on-farm demonstrations were classified as safe at 4–8 weeks after harvest. Therefore, sustainable reduction of aflatoxins to safe limits is possible through greater collaboration among the value chain actors. Low-cost good agricultural practices within the remit of the growers should be prioritized alongside public awareness programmes. Subjects: Agriculture & Environmental Sciences; Botany; Food Science & Technology


ABOUT THE AUTHOR
The Author, Issah Sugri, is an early carrier Research Scientist with the Upper East Region Farming System Research Group of the CSIR-Savanna Agriculture Research Institute based at Manga in the Bawku Municipal, Ghana. The group mandate is to analyze the farming systems of the region with the view to generating appropriate innovations that would improve the livelihood of the people. His research focuses on improving postharvest handling, storage and processing to reduce postharvest losses to conserve the already scarce food resources of the area. Specific emphasis is placed on low-cost storage methods, postharvest handling, postharvest physiology, grain storage and food quality management. My other schedules include providing training and technical support to farmers, farmer groups and other agricultural service providers in aspects of postharvest techniques and management.

PUBLIC INTEREST STATEMENT
Many farm families in northern Ghana consider peanut as the most important grain legume. Generally, about 80% of Ghanaians consume peanut or peanut products at least once a week. However, aflatoxins contamination remains a major food safety concern in peanut-basedfoods. Aflatoxins are highly toxic chemical poisons produced by the fungus Aspergillus flavus in certain food crops. The toxins can suppress the immune system, growth and cause liver disease and death in severe cases. Women, children and the poor are more vulnerable. However, public awareness of the health effects of aflatoxins is low. From this study, 93-99% of peanut samples were classified as safe for human use at 2 months after harvest. However, if peanut is stored for long period the level of contamination may rise. Therefore farmers, processors and traders need to adopt good practices to maintain quality during storage and handling.

Introduction
In Ghana, peanut (Arachis hypogeae L, Fabaceae) production plays an important role in the livelihoods of particularly women farmers in the rural communities (Carlberg, Kostandini, & Dankyi, 2014). Peanut is an important cash crop and component of diet, particularly protein source for many rural households. Although the crop is grown throughout the country, the most important production areas are the three regions of northern Ghana. In these regions, about 20% of farmers consider peanut among their two most important crops. National per capita peanut consumption is estimated at 0.61 kg/week (Awuah, 2000). Informal small-scale processing into paste, oil and cake is widespread particularly among rural women; providing vital source of livelihoods (Shanahan, Carlsson-Kanyama, Offei-Ansah, Ekstrom, & Potapova, 2003). Farmers cultivate peanut on small scales, both in pure stands and in crop mixtures with other cereals (Naab et al., 2005).
Aflatoxins contamination in peanut seeds remains a major challenge in most parts of Africa (Florkowski & Kolavalli, 2013). The fungi responsible for the production of toxins are mainly Aspergillus flavus and A. parasiticus and A. nomius (Waliyar et al., 2008). Ingestion of higher doses of aflatoxin can result in acute aflatoxicosis, which manifests as hepatotoxicity and fulminant liver failure and death in severe cases (Richard & Abbas, 2008). Close to 60-85% of smallholder farmers in developing countries are not protected by commercial food safety regulations (Wild, 2007). They often lack the capacity to protect crops against aflatoxin contamination, and awareness about risk of aflatoxin is poor. A report by International Institute of Tropical Agriculture (IITA Report, 2013) suggests that aflatoxins contamination in maize and peanut remains a major non-tariff barrier to international trade since agricultural products that exceed the permissible levels (4-15 ppb) are banned. About $1.2 billion in commerce is lost annually due to aflatoxins contamination; with African economies losing $450 million each year (IITA Report, 2013).
In Ghana, some studies have been conducted on perception, prevalence and health risk related to aflatoxins in maize and peanut (Florkowski & Kolavalli, 2013;Jolly et al., 2006;Shuaib et al., 2012;Sugri et al., 2015). Albeit, most of such have concentrated on prevalence, consumer risk and perception surveys; such studies are often fragmented and covering only a few zones. Jolly et al. (2006) found high levels of aflatoxin B 1 (AF-B 1 ) albumin adducts in blood and aflatoxin M 1 (AF-M 1 ) metabolite in urine of consumers in major peanut and maize consuming regions. Another study on aflatoxin B 1 -Lysine (AF-ALB) adduct levels among pregnant women showed high levels as well (Shuaib et al., 2012). Higher socioeconomic status, namely, higher education and income, small household size, being employed or having a flush toilet were inversely associated with aflatoxin levels (Jolly et al., 2006;Shuaib et al., 2012). Aflatoxin analysis in peanut products showed higher level (288.9 ppb) in rejected kernels which consist of discoloured, mouldy or split peanuts sorted out of a batch of raw peanuts. Among the processed products, high contamination was recorded in peanut paste (42.5 ppb) and kulikuli (76.91 ppb) (Florkowski and Kolavalli (2013).
This study evaluated aflatoxin levels in peanut samples from farmer storage units, and participatory on-farm research trials.

Scope of study
The survey was conducted in six districts, comprising of three districts each in Upper East and Upper West Regions of Ghana, from November to December 2013. The research tools employed included field surveys, focus group discussions and key informant interviews. A multistage sampling approach targeting main producing districts, communities and households was adopted in selecting the respondents. In all, 240 respondents from 24 communities were covered using structured questionnaire. Information captured included demographic and socio-economic factors; cropping systems and scale of production; postharvest operations; integrated pest management strategies; farmers' knowledge of aflatoxins; and challenges in peanut storage. Focus group discussions were carried out with different gender groups using a checklist designed to capture all relevant information.

Sampling and sample analysis
Peanut samples (240 each weighing ~ 0.5-1 kg) were obtained from farmer storage units: granaries, barns, bags and silos of the respondents. Sampling was conducted in November to December, 2013; approximately 4-8 weeks after harvest. To ensure that samples are representative of the entire batch, triplicate samples were obtained from the proximal, mid and distal points of storage bags, whereas the same procedure was followed at the upper, middle and bottom points of nuts stored in granaries and barns. The samples were then reduced to working samples through the coning and quartering method. The samples were analysed for total aflatoxins at the Plant Pathology Laboratory of ICRISAT, Mali, using the indirect Enzyme Linked Immunosorbent Assay (ELISA) technique.

Participatory on-farm evaluation
The participatory on-farm evaluation assessed the performance of 10 peanut genotypes consisting of 8 aflatoxin resistant lines from ICRISAT-Mali, and 2 local checks from Ghana. Field trials were established at Tingoli, Sambligo and Nyagli in the Northern, Upper East and Upper West Regions, respectively in year 2014 and 2015. All experiments were established between 2nd and 3rd weeks of July and harvesting was done in the 3rd and 4th week of October in both years. At each location, the genotypes were evaluated using researcher-managed "mother trials" and farmer-managed "baby trials". Two farmer field schools were organized at the maximum vegetative growth and harvesting stages for selected farmers from communities. The participants were schooled on good agricultural practices (GAP) in peanut production and aflatoxin management. At harvesting, GAP massages focused on prompt harvesting, quick drying, sorting, storage and processing methods. Also, participatory variety selection was done to enable farmers identify genotypes they preferred as well as traits that are critical to end-users.

Data analysis
The socio-demographic data was analyzed using Statistical Package for Social Sciences (SPSS 16). Data sets on aflatoxin levels were subjected to Analysis of Variance (ANOVA) to determine significant differences among samples by using GenStat (9th Edition) statistical package. The agronomic data sets were analyzed as a randomized complete block design with genotypes over years and locations. Differences between treatment means were separated by Fischer Least Significant Difference at 5% level of probability. Descriptive statistics involving frequencies, minimum, maximum, mean and range were employed in reporting.

Socio-economic importance
The results in Table 1 showed that 33.2% of growers produced up to 3 bags, 42% harvested up to 10 bags and less than 11% harvested more than 25 bags per season. The harvested unshelled peanut was sun-dried for 4-6 sunshine days and stored during the drier months of the year. The dried unshelled peanut was stored in polypropylene (70.4%) and jute bags (20.8%). From the study, only few respondents applied chemicals in anticipation of prolong storage or when insect infestation was noticed during storage. The focus group discussions revealed that peanut production contributed immensely to household income and food security. The crop performs well on poor soils even without fertilizer as well as minimal susceptibility to biological pests. Currently, peanut is produced under rain fed conditions by using cultivars which have been recycled for over three decades now. Early planting from May to June is preferred by farmers in Northern and Upper West Regions. Although, this period usually coincides with terminal and prolong drought which are reportedly associated with occurrence of aflatoxins. Late planting was done from mid-June to late July across all three northern regions. At the harvesting period, pod piercing and sucking bugs invade peanut fields particularly where harvesting to thrashing interval is delayed. Lack of adequate sunshine days and intermittent rainfalls were listed as challenges during drying. Access to market was not a major challenge, however occasional glut, low price at harvest and exploitation by middlemen were recurrent problems to farmers.

Total aflatoxins in stored peanut
Total aflatoxins in stored peanut samples is summarized in Figure 1. Aflatoxin levels ranged from 0.0 to 1,546 ppb with wide variations occurring within and across communities and districts (Table 2). Total aflatoxins was below 20 ppm in 20 communities but some excessive levels of 25.7, 75, 171.5 and 252 ppm were recorded at Baazu, Nimbare, Denegu and Bantanfarigu, respectively. Total aflatoxins in samples from Garu-Tempane and Jirapa districts was significantly higher (p < 0.05) compared to counterpart districts. The overall analysis showed that up to 92.9% of the samples could be classified as safe at permissible level of 20 ppb. Table 3 provides a summary of the field performances of the 10 genotypes across 3 locations. Overall, good seedling establishment was noticed for all genotypes except Nkatie-SARI with extreme low germination rate. Using the number of days to 50% flowering (DFF) stage as a criteria for earliness, all the genotypes can be grouped as early maturing, attaining DFF by 28-32 days after planting (DAP) except Nkatie-SARI, which attained DFF by 37-42 DAP. Yield was generally low (0.266-0.437 t/ha) across the genotypes compared to yield potential of peanut (1.8-2.2 t/ha) in Ghana. However, this could be attributed to late planting of the trial in mid-July since the trials could not be established if the farmers had not planted their farmlands. Significant genotype and environment interaction (p < 0.05) was recorded for pod yield and yield component traits which will be considered in future agronomic evaluations.    The total aflatoxins across locations showed that all 10 genotypes recorded levels of <15 ppb (range of 0.00-38.6 ppb) at 4-8 weeks after harvest (Figure 2). Genotypes: ICGV-94379 (0.6-38.7 ppb), farmer variety (0.92-22.6 ppb) and ICGV-91284 (0.4-19.9 ppb) were quite susceptible compared to their counterparts. Significant (p < 0.05) regional variation was recorded where samples from the Upper East Region recorded higher levels compared to Northern and Upper West Regions. The overall analysis showed that up to 98.7% of the samples could be classified as safe at permissible level of 20 ppb (Table 4).

Gender roles in the value chain
The focus discussions showed that peanut plays enormous role in livelihoods across gender in northern Ghana. All gender (men, women and youth) were involved at all stages of crop production, processing and food preparation (Table 5); although the degree of involvement varied according to task. Women were more involved in seed selection, shelling as well as primary and secondary processing operations. At the utilization stage, women were primarily responsible for processing and value addition activities up to consumption.
Figure 3 presents a model which put emphasis on smallholder actors (growers, traders, processors and consumers) at centre of the chain with associated technical support and market linkage services to support the actors. The model emphasizes on strong linkages among research, extension service, policy, smallholder actors and allied services. To reduce drudgery, the development of small scale equipment such as simple planters, thrashing, shelling and oil pressing machines require some attention. In addition, community level trainings and awareness on the emerging food safety threat of aflatoxins in peanut and peanut products should be put at the fore.

Discussion
Aflatoxin contamination can be minimized during "on-farm" operations by using a combination of agronomic and genetic strategies including control of soil arthropods, nutrient amendments, crop rotation, appropriate plant density and host plant resistance. Postharvest operations such as monitoring of thermal time and kernel moisture content, reducing the cutting to thrashing intervals, quick drying, good crop storage are additional management options (Wright & Cruickshank, 1999). Adjustments of sowing dates and application of gypsum can reduce pre-harvest contamination (Waliyar, Osiru, Sudini, & Njoroge, 2013). The applications of lime or any calcium source fertilizer alone is reported to reduce aflatoxins contamination by 72% compared to farm yard manure (42%) under field conditions, but combined application of both sources reduced aflatoxin contamination up to 84% (Waliyar et al., 2008). Intercropping of zimmu (Allium sativum L._Allium cepa L.) and an antagonistic bacterium Burkholderia sp. strain TNAU-1 for the control of Aspergillus flavus infection and aflatoxin B1 contamination in peanut exhibited some potential (Vijayasamundeeswari, Vijayanandraj, Paranidharan, Samiyappan, & Velazhahan, 2010). Seed treatment at 10 g/kg or soil application at 2.5 kg/ha on 30, 45, 60 days after sowing with the formulation of Burkholderia sp. significantly reduced infection by A. flavus and aflatoxin B1 contamination in kernels. Recently, the effectiveness of biological control involving Aflasafe TM , which uses native strains of A. flavus that do not produce aflatoxins, in the field has been reported (IITA Report, 2013). Aflatoxin contamination in maize and peanut was consistently reduced by 80-90% using aflasafe TM (IITA Report, 2013).
Information dissemination and public awareness including training, fact sheet and radio broadcast in local languages have been suggested (Sugri et al., 2015). Wu and Khlangwiset (2010) suggested awareness and education of farmers, governmental functionaries, and the general public as well as economic incentives to adopt interventions. Ilesanmi and Ilesanmi (2011), recommended the possibility of incorporating awareness into routine health talks to increase level of awareness among Table 5

. Assessment of gender roles in peanut production operations chain in Northern Ghana
Notes: x shows the relative involvement in the task by gender where x: not often involved; xx: often involved and, xxx: most often involved. patients and their families. However, awareness of aflatoxins contamination in food is low in most parts of sub-Sahara Africa. Some reports from Nigeria and Ghana suggest that in spite of several campaigns on the health effects and economic impact of aflatoxins, few agriculturists or health professionals were cognizant of the associated health risk (Ilesanmi & Ilesanmi, 2011;Jolly, Bayard, Awuah, Fialor, & Williams, 2009;Sugri et al., 2015). In some instance the professionals in charge of the allocation of resources to reduce contamination are unaware of its economic and health risks (Hendrickse, 1999). A study in northern Ghana for instance revealed that although 78% of respondent were aware of aflatoxins in maize and peanut a large majority (68.1%) did not perceive it as a major food safety issue (Sugri et al., 2015). Among health workers in Nigeria, it was found that 95% of respondents had previous awareness of aflatoxins, however class room lectures was the common source of information to 56% of respondents (Ilesanmi & Ilesanmi, 2011). They noticed that none of the health workers had ever discussed with their patients about the risk of Aflatoxins in food.

Production operations Description of tasks
This study suggests that at 20 ppm permissible level, 92.9% of samples from farmer stored peanuts and 98.7% of samples from the participatory on-farm experiments were safe for human use at 4-8 weeks after harvest. This trend is similar to earlier study by Florkowski and Kolavalli (2013). They reported that freshly harvested peanuts, even if contaminated, may contain low levels of aflatoxins. However, because peanut is stored after harvest, the level of contamination rises with time and significantly exceeds the permissible limits. Integrated strategies such as resistant genotypes, soil amendments and quite recently Aflasafe TM should be demonstrated to the small-holder growers. Low-cost strategies such as improved seed, clean farm operations, quick drying, sorting and used of improved storage methods, which are within the remit of the smallholder growers should be prioritized during farmer field schools and public awareness programmes. The eight genotypes evaluated showed yields comparable to the two standard checks (Table 3). Given that these are early maturing and possess resistance to aflatoxin, they have been advanced to on-farm evaluations to validate their yield potentials.

Conclusion
From this study, sustainable reduction of aflatoxins to safe limits is possible through greater collaboration among the peanut value chain actors in Ghana. In addition to the good agricultural practices, others actors such as the Food and Drugs Board, the main food regulatory agency in Ghana, should be strengthened to provide periodic testing for aflatoxins in grain markets. Traders and consumers could be trained to use simple testing kits to determine safety levels of grains being traded or consumed. In this regard, the Department of Agriculture and private sector involvement in aspects of providing testing kits, training or initially operating such system would be required. In the interim, intensifying training of frontline actors such as public and private agricultural extension agents and community health workers, to assist in creating awareness of aflatoxins in routine community outreach programmes, should be pursued.