Selected Edible Insects and Their Products in Traditional Medicine, Food and Pharmaceutical Industries in Africa: Utilisation and Prospects Selected Edible Insects and Their Products in Traditional Medicine, Food and Pharmaceutical Industries in Africa: Utilisation and Prospects

Edible insects are a widely exploited food source by many indigenous populations in most regions of the world. Edible insects have been used as food in sub-Saharan Africa, being a good source of protein and essential amino acid. Historically, they are important contrib- utors to improving food and nutrition security, particularly for people who suffer from malnutrition due to protein deficiency. Africa is the continent with the highest number of records (19 countries), followed by the USA (5 countries) and Asia (5 countries). The species used for food and as feed include Hodotermitidae, Kalotermitidae, Rhinotermitidae and Termitidae . Insects, such as termites, are also eaten raw directly on emergence from the holes. Species used in traditional popular medicine include Hodotermitidae and Termitidae . They are used in the treatment of various diseases that affect humans such as influenza, asthma, bronchitis, whooping cough, sinusitis, tonsillitis and hoarseness.


Overview on edible insects in sub-Saharan Africa
Insects have been consumed for generations in many regions of the world, a practice that has increased in popularity in recent years [1][2][3][4][5][6]. More than 2.5 billion people, mainly in Africa and Asia, commonly consume insects [7]. The use of termites was registered in 29 countries over three continents. Africa is the continent with the highest number of records (19 countries), followed by the USA (5 countries) and Asia (5 countries). Throughout the world, a large portion of the human population consumes insects as a regular part of their diet. Insects' consumption, called Entomophagy, has played an important role in the history of human nutrition in Africa [8]. Currently, edible insects are gaining much attention for their high nutritional value and environmental advantages over meat production [9]. Their short life cycles, low space requirements, efficient nutrient conversion rates and lower greenhouse gas production render insects to be, in principle, an excellent alternative to meat [5]. It is postulated that termites contain high-quality nutrients including highly digestible proteins [10], as well as minerals, which are more bioavailable than minerals from plant foods [11]. Crickets in particular are believed to have higher quality animal protein than some conventional sources, such as fish, and are more affordable among poor communities [12]. Currently, attention is being drawn to this valuable traditional food resource, which if tapped or exploited could contribute to a more sustainable solution for malnutrition in sub-Saharan Africa. It is estimated that insects form part of the traditional diets of at least two billion people. Thousands of edible species have been identified [13][14][15]. More than 1900 species have reportedly been used as food [16,17]. Insects deliver a host of ecological services that are fundamental to human survival. Termites are eusocial insects belonging to the family Isoptera that play a major role in the tropical ecosystem (Figure 1).
In general, insects are important in plant reproduction, waste bio-conversion and in biocontrol of harmful pest species leading to a variety of valuable food and non-food products used in applications such as maggot therapy [1]. They are used as collection items and ornaments and in movies, visual arts and literature. Globally, the most commonly consumed insects are beetles (Coleoptera, 31%), caterpillars (Lepidoptera, 18%) and bees, wasps and ants (Hymenoptera, 14%), grasshoppers, locusts and crickets (Orthoptera, 13%), cicadas, leafhoppers, planthoppers, scale insects and true bugs (Hemiptera, 10%), termites (Isoptera, 3%), dragonflies (Odonata, 3%), flies (Diptera, 2%) and other orders (5%) (Figure 2). The importance of insects as a food source for human is not surprising, since this is the group with the highest number of species in nature, thereby representing significant biomass [19]. Considered as important natural resources, insects are in many ways a basic component of the diets of humans and other animals [20] and have played an important role as a source of medicinal resources [21][22][23][24].
By 2050, the global population is estimated to be nine billion people and could possibly lead to a global food demand increase of up to 70% compared with our current food requirements [25]. Invariably, conventional sources of protein may not be sufficient for the global human population; hence, alternative sources such as insects will be required.

Cultivation
The cultivation of edible insects in sub-Saharan Africa is not common as obtainable in developed economies. Although edible insects are popular in the continent, they are not cultivated and there appears to be no campaign strategies in place. This is attributable to a number of reasons ranging from cultural, behavioural to lack of understanding of nutritional benefits of insects in the continent. Rearing insects may also require minimal land or market introduction efforts, as insects already form part of some local food cultures. A recent study shows that house crickets (Acheta domesticus), common across Africa, are a highly valuable yet neglected source of proteins [12] contributing a viable solution to food security challenges.
Apparently, due to huge local and international demand for insect-based foods, insect farming initiatives seems to have taken off in Africa. Iwuoha [26] highlighted the following initiatives: (i) The McGill Entomophagy Project-in September 2013, the Clinton Global Initiative seems to have awarded a significant prize to a team of student entrepreneurs from the McGill University in Montreal, Canada to fight hunger and nutrition deficiencies in developing regions of the world like Africa by improving diets with insect-based meals. This team, working with researchers and local insect farmers in Thailand, has assessed red palm weevil larva farming practices for possible translation to West Africa where palm weevil larva are eaten, but not farmed; (ii) Prof. Arnold van Huis (Insect Protein for Africa)-a researcher using insects as a sustainable source of protein for Africa-is on a drive to raise 1.5 million Euros in funding to carry out fundamental research of simple insect cultivation methods in Africa and (iii) AgriProtein-a South African business developing insect-based protein feed, extruded oil, and fertilisers since 2009 and has raised $11 million from strategic partners to commercialise and globalise its revolutionary concept.

Cultural and religious considerations
The consumption of insects as food is acceptable and practised by many cultures around the world [18]. Many ethnic groups in 130 countries utilise insects as essential elements of their diet, even in the United States there has been an increasing interest in insect-based food products in recent years [27]. Edible insects are a widely exploited food source by many indigenous populations in most regions of the world [18].
Entomophagy, the consumption of insects, is heavily influenced by cultural and religious practices in many regions of the world [28] and sometimes economic circumstance in some parts of Africa. Historical references to the use of insects for food are currently found in some religious literatures, for example, in the Bible, in Leviticus chapter 11, verse 22 and in Matthew chapter 3, verse 4 [29]. Despite these references, the topic of entomophagy has only very recently started to capture some attention worldwide. In the most developed economy, however, people still view entomophagy with disgust and associate eating insects with primitive behaviour. This attitude has resulted in the neglect of insects in agricultural research.
Edible termites form an important part of the food culture in the Lake Victoria region of East Africa [30,31]. The study of Pambo et al. [32] shows that in Kenya attitudes, subjective norms and behavioural capabilities are considerations in designing food from edible insects (FEI) that are culturally appropriate. Their study proposed FEI as a viable option, given that insects are ubiquitous and that taste, availability/convenience, cost, nutrition, health benefits/risks and disgust factors are major determinants of consumption. Their study was conceptualised to identify potential differences in salient beliefs between participants from western region and those from eastern region, given that consumption of edible insects is popular in the western region. Although Pambo et al. [32] did not find potential differences in salient beliefs regarding insect consumption between two regions in Kenya, differences could exist between countries. Acceptance and popularity of FEI would depend much on campaign, nutrition literacy and other considerations. Kipkoech [12] observed that it took the presence of participants from different countries, continents and cultures, some of whom had tasted cricket before to demystify their consumption as food at a conference reception.

Consumption
Insects, especially termites, have been used as food in sub-Saharan Africa, Asia, Australia and Latin America ( Table 1). Edible insects consumption has been recently reported in Nigeria [33,34] among which the termites had the highest mean frequency [33].
Some of the insects are eaten raw directly from the emergence hole [35,36]. Although termite harvest begins with the onset of the rains and the swarming of the winged termites, villagers have shown that some termites could be induced to emerge even during the dry seasons,
In many households, termites are a delicacy enjoyed by almost all ethnic communities in western Kenya. They are consumed as part of a meal or as a complete meal with tapioca, bread, roast corn or simply eaten as snack food. Some mothers grind the dried termites into flour and use it as a sprinkle in baby porridge [38]. Termites are also eaten raw directly from the emergence hole [35,36]. Addition of termites to maize resulted in significant increase in β-carotene, niacin, vitamin B6, and B12 content, with significant reduction in thiamine, riboflavin and ascorbic acid content of enriched complementary foods.
The utilisation of insects as a sustainable and secure source of animal-based food for the human diet has continued to increase in popularity in recent years [39]. Many ethnic groups in approximately 130 countries utilise insects as essential elements of their diet. In recent years, in the United States, there has been an increasing interest in insect-based food products [27]. More than 2000 insect species and other small invertebrates are consumed as food by humans and animals alike [40] and used for either self-sufficiency or commercial food products in many parts of the world.
Insects link biodiversity conservation and human nutrition in a way that many other food sources do not. They often contain more protein, fat and carbohydrates than equal amounts of beef or fish, and a higher energy value than soy beans, maize, beef, fish, lentils or other beans [46].

Processing of edible insects
Insects are often consumed whole but can also be processed into granular or paste forms. In most western and eastern African countries, termites are collected during the rainy seasons as they emerge from holes on the ground. In western Kenya, this period is between April and October. They are prepared by blanching in boiling water, dried in the sun before frying in their own fat. Others dipped the crickets into hot water for 1 min and then sun-dried and ground them for use in making porridge, cookies and other sweet delicacies or deep-fry to get crispy crickets that would be eaten whole [12]. Surprisingly, the deep-fried crickets were everyone's favourite because of their delicious aroma and taste.
Several studies have shown that the product preparation affects the willingness to eat insects [47]. However, to date, consumer expectations and preferences towards different aspects of the product preparation have not been investigated, especially in sub-Saharan Africa. Figure 3 shows the processing of mopane worms by frying.
Roasted termites moisture content was very low, while the crude protein, fat, carbohydrate and gross energy content were very high. Banjo et al. [37] stated that there was a significant reduction in moisture content of formulated complementary foods, the level of reduction increasing with increasing level of 10-20% inclusion of termites (p<0.05) with the values increasing with increasing level of inclusion of termites. They also reported significant increase in values of crude protein and fat, ash, total carbohydrates, mineral and gross energy of the formulated maize and sorghum complementary foods (p<0.05). However, they highlighted that some of the increases in value were lower than recommended by FAO/WHO.

Edible insects and bio-economy
Currently, attention is being drawn to this valuable traditional food resource, which if tapped or exploited is likely to be a more sustainable solution for nutrient deficiency. Considering the trajectory of the economy in sub-Saharan Africa, the gathering and farming of insects can offer employment and cash income, either at the household level or in larger, industrialscale operations. In most parts of sub-Saharan Africa and Southeast Asia, the process of insect gathering, rearing and processing into street foods or for sale as chicken and fish feed is easily within reach of small-scale enterprises. With only a few exceptions, international trade in edible insects is insignificant, but border trade is significant. The trade that does exist in developed countries is often driven by demand from immigrant communities or because of the development of niche markets that sell exotic foods.
Some of the poorest people in Africa, living in urban and rural areas, can earn a living by the gathering, cultivation, processing and sale of edible insects. Such activities can improve diets, making available cash income by selling raw and processed insects as street foods or supply junior and high schools where school meals are served to pupils. Insects can be directly and easily collected from nature or farmed with minimal technical or capital expenditure considering the use of basic rearing and harvesting equipment.

Nutraceutical benefits
The nutraceutial benefit of insects is substantial varying as a result of the wide range of edible species. Within the same species, it has been shown that nutritional and medicinal values could differ based on the metamorphic stage of the insect, the habitat, and diet. They are a readily available source of protein (Figure 4), lipids, carbohydrates, certain vitamins, and minerals such as calcium, iron, or zinc ( Table 2). The protein content in insects is high, equivalent to that of fish and meat and is also said to be similar to the one found in a human body, making it easier to be utilised by the body as to compared to plant protein [13]. The energy content of insects is on average comparable to that of meat (on a fresh weight basis) except for pork because of its particularly high-fat content [48].
Dried termites have been reported to be a good source of dietary protein, fat and micronutrients [37,[50][51][52]34]. Adepoju and Omotayo [34] reported termites to be low in anti-nutrients and suggested its possible inclusion in formulating adequate, nutrient-dense complementary foods with nutraceutical benefits. Addition of termites to maize resulted in significant increase in β-carotene, niacin, vitamin B6 and B12 content, with significant reduction (p<0.05) in thiamine, riboflavin and ascorbic acid content [37].
Termites constitute a food source of great nutritional value: high in protein and essential amino acids such as tryptophan, which is generally limiting in the food insects [53].
Termites are rich in minerals and other micronutrients. Essential fatty acids are well represented [54]. In general, heads of termites are better nutritionally featured than thorax and abdomens. Termites are undeniably rich sources of iron and their inclusion in the daily diet could improve iron status and help prevent anaemia in developing countries. Essential vitamins for stimulating metabolic processes and enhancing immune system functions are present in most edible insects such as termites. Booth [54] showed for a whole range of insects that thiamine ranged from 0.1 to 4 mg/100 g of dry matter. Insects contain significant amounts of fibre, as measured by crude fibre, acid detergent fibre and neutral detergent fibre. The most common form of fibre in insects is chitin, an insoluble fibre derived from the exoskeleton [17].
From a utilitarian perspective, termites are commonly used insects in entomotherapeutic practices and traditional popular medicine [20,23,55,56] in the treatment of various diseases ( Table 3) that affect humans, such as influenza, asthma, bronchitis, whooping cough, sinusitis, tonsillitis and hoarseness [57,58]. They have historically been an important source of food that may contribute to improving human diet, particularly for people who suffer from malnutrition due to a deficit of protein [17], as they are considered a nonconventional food with great economic and social importance [3][4][5][6].

Prospects and challenges of edible insects industry
The induction of insect emergence during off seasons by villages [37] gives room for technological application in making insects available all through the year. This is an area that needs investigation as the world looks for alternative, environmentally friendly and cheaper sources of protein foods.
As earlier highlighted, edible termites are a good source of protein and the essential amino acid tryptophan. Many commercial food products are enriched with protein extracted or derived from legumes but insect protein is better in terms of nutritional properties and contains all the essential amino acids ( Table 2). Adepoju and Omotayo [34] reported termites as being low in anti-nutrients and suggested their possible inclusion in formulating adequate, nutrient-dense complementary foods. Moreover, some insects (    [62]. At present, extraction processes for specific food ingredients are too costly and will need to be further developed to render insects profitable and applicable for industrial use in the food and feed sectors.
In the continent, the role of the media, peers and health officials in a FEI intervention need to be given consideration [32]. A theory-based intervention targeting FEI consumption and nutrition literacy, and ultimately increase the intake of FEI among the target population was proposed by Pambo et al. [32].
As stated by Pambo et al. [32], population growth, urbanisation and climate change are among the factors that have created uncertainties and pressures on current global food and economic systems. Insects as food and consumption of foods from edible insects are being promoted as one potential solution to the declining access to protein foods. It has been said by various authors that with the increasing global population, one of the strategies to improve food and nutrition security is to diversify diets using available food sources [25,64,65,46,3,5,12]. However, one of the challenges facing consumption [66] of edible insects is the limited information regarding consumerpsychographic characteristics including attitudes, values, interests and beliefs.

Conclusion and recommendation
Insects abundantly thrive in Africa, given the prevailing tropical climate. As the price of beef, chicken and fish continue to rise across the world, there is a huge opportunity for insects to meet the animal protein needs of human beings and livestock. It is now the view that edible insects have more iron than sirloin beef. One area of challenge in edible insect promotion, consumption and commercialisation is the consumer-psychographic characteristics. Edible insects are a highly nutritious and healthy food source with high fat, protein, vitamin, fibre and mineral content. The consumption of edible insects should be emphasised as this could be one of the sustainable strategies towards the alleviation of poverty, hunger and malnutrition in sub-Saharan Africa.