Nutritional Composition of Edible Insects Consumed in Africa: A Systematic Review

Edible insects are an important protein rich natural resource that can contribute to resilient food security. Edible insects not only play an important role in traditional diets, but are also an excellent source of protein in traditional dishes in Africa. We systematically searched Web-of-Science and Google Scholar from year 2000–2019 for studies on the consumption of insects and their nutritional composition in Africa, resulting in 98 eligible papers, listing 212 edible insect species from eight orders. These insects were rich in protein, fats, and fibre. The highest protein content was reported for Lepidoptera (range: 20–80%). Coleoptera had the highest carbohydrate content (7–54%), while Lepidoptera had the highest fat content (10–50%). Considering the excellent source of nutrition, and potential socio-economic benefits, from edible insects, they can contribute strongly to improved food security, and rural development in developing countries. In addition, edible insects can be used as a sustainable food source to combat food shortages in the future, for example, providing resilience during times of drought or other climate stressors.


Introduction
Consumption of insects has recently received more attention because of their promising potential for contributing to livelihoods and mitigating food security problems around the world [1][2][3]. Food security problems are caused by an enormous increase in the global human population, which is estimated to increase to approximately 9 billion people by 2050 [1], resulting in a 70% increase in food demand, and an increase in food prices [1,4,5]. The increase in food prices will prompt the search for cheap alternative sustainable protein sources [1]. Entomophagy, which refers to the consumption of insects by humans, is an environmentally friendly approach to increasing food for consumption, and contributing to food security across the world [2,[5][6][7].
Edible insects might be a solution to food shortages, owing to their promising potential in contributing to livelihoods and mitigating food security problems around the world [1][2][3]. Insects are consumed as food in Thailand [8,9], China [10,11], Mexico [12][13][14][15], Latin America [16], Japan [17], and Africa [18]. According to van Huis [1], approximately 2 billion people worldwide regularly consume insects as part of their diets. The consumption of insects is not a new phenomenon, as it dates back to before the development of agriculture when humans relied on gathering plants and hunting wild animals [4,11,19].
Edible insects have played a very important traditional role in nutritious diets in various countries in Africa [18,20]. In addition, edible insects are an important natural resource that is used as a coping strategy, particularly in months of food shortage [21][22][23]. Unfavourable climatic conditions experienced in Africa affect small scale animal husbandry and reduce animal protein production, so diets are then supplemented with edible insect protein [22]. Edible insects provide significant socio-economic and ecological benefits for developing countries [24,25]. Approximately 500 species of edible insects are

Search Strategy
To explore the diversity and nutritional status of edible insects in Africa, we followed the PRISMA guidelines for a systematic review. Peer-reviewed literature was obtained using the Thomson Reuters' Web of Science database (https://apps.webofknowledge.com) and google scholar (https: //scholar.google.co.za/) looking for publications that researched entomophagy in Africa, edible insects, diversity, nutrient content of edible insects, and consumption of insects. To source information, the following key words and phrases were used, "entomophagy", "edible insects", "diversity of edible insects", "entomophagy in Africa", "edible insects in eastern Africa", "edible insects in north Africa", "edible insects in western Africa", "edible insects in Central Africa", "edible insects in southern Africa" and "nutrient content of edible insects". We also screened references included in selected articles in order to identify studies that might be relevant but did not appear in our search. We limited the search to literature published from 2000 to 2019. We started in the year 2000 because it was a starting point where most researchers began investigating the use of edible insects as a food source and as a solution to combat food insecurity problems [33,34].

Data Collection
Data from the selected articles were independently screened and extracted by a single author (Z.T.H). The search result was done by reading the title and abstract of the retrieved papers to determine if the article was relevant to the study. Once it was determined that the article was relevant, the full text of the selected articles was further analysed to extract relevant information. The information that was collected and extracted after full text reading from each article included year, study area and country, study insect species, reported nutrient composition of insects, consumption stage of an insect, main research findings, and conclusions. Collected articles were categorised by country and insect order.

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Original research articles and review papers focusing on entomophagy, nutrient composition of single or multiple edible insect species. • Articles published in English.

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Articles of work done in African countries.

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Articles that reported nutrient composition of edible insects.

Exclusion Criteria
• Conference papers, editorial material, book chapters • Articles on insect rearing and farming.

Data Quality
To evaluate the quality of studies included in this systematic review, we assessed quality based on the following criteria: (1) A clear food description (scientific name(s) of insects studied or genus), (2) a clear description on the part of the insects used for analysis, e.g., whole, head, abdomen, indication of geographic origin of the insects, and the country where it is used as food in Africa, (3) analytical method used, number of analytical samples, (4) clear indication of whether the nutritional composition was based on the dry weight. Studies were included if they meet all the above criteria.

Data Analysis
The methods and data sources used in the included studies were highly heterogeneous and a statistical meta-analysis was not possible. Instead, a more narrative synthesis approach was used, and data from each study were tabulated. We synthesised the results according to study species and mean values of all insect species belonging to the same insect order were calculated and represented in bold, the nutritional composition of consumed species were presented in the table, most consumed species in different countries were presented graphically.

Results and Discussion
A total of 428 papers were identified for potential inclusion; after checking the title and abstract, 300 articles were excluded because they did not meet the inclusion criteria. From here, 128 articles were selected for full-text reading; from these, 29 articles were further excluded because they were not relevant or not conducted in Africa. After reading the full-text, 89 studies met all inclusion criteria, and a further nine articles were identified through screening references and confirming inclusion criteria were met. In total 98 articles were included in a systematic review ( Figure 1). • Articles on insect rearing and farming.

Data Quality
To evaluate the quality of studies included in this systematic review, we assessed quality based on the following criteria: (1) A clear food description (scientific name(s) of insects studied or genus), (2) a clear description on the part of the insects used for analysis, e.g., whole, head, abdomen, indication of geographic origin of the insects, and the country where it is used as food in Africa, (3) analytical method used, number of analytical samples, (4) clear indication of whether the nutritional composition was based on the dry weight. Studies were included if they meet all the above criteria.

Data Analysis
The methods and data sources used in the included studies were highly heterogeneous and a statistical meta-analysis was not possible. Instead, a more narrative synthesis approach was used, and data from each study were tabulated. We synthesised the results according to study species and mean values of all insect species belonging to the same insect order were calculated and represented in bold, the nutritional composition of consumed species were presented in the table, most consumed species in different countries were presented graphically.

Results and Discussion
A total of 428 papers were identified for potential inclusion; after checking the title and abstract, 300 articles were excluded because they did not meet the inclusion criteria. From here, 128 articles were selected for full-text reading; from these, 29 articles were further excluded because they were not relevant or not conducted in Africa. After reading the full-text, 89 studies met all inclusion criteria, and a further nine articles were identified through screening references and confirming inclusion criteria were met. In total 98 articles were included in a systematic review ( Figure 1).

Consumption of Insect Patterns in Africa
For the research articles published since 2000, a total of 212 edible insect species from nine orders were recorded and are potentially consumed in different African countries (Appendix A). Of these, 41% were Lepidoptera, 23% Orthoptera, 15% Coleoptera, 12% Blattodea (including both cockroaches and termites as recently classified), 4% Hemiptera, and Hymenoptera, Diptera, Blattodea, and Mantodea each contributed <1%. Rhynchophorus phoenicis (African palm weevil) and Cirina forda (Pallid emperor moth) were the most studied species in Africa, with 32 publications from 12 countries, and 18 publications from 10 countries, respectively ( Figure 2). Most research has been done in the western African countries, particularly in Nigeria, mainly on Rhynchophorus phoenicis and Cirina forda, which are the most consumed species in West Africa. However, southern African countries (Zimbabwe, South Africa, and Bostwana) have the highest number of consumed species, but little research has been done on nutritional content and consumption patterns of edible insects.

Consumption of Insect Patterns in Africa
For the research articles published since 2000, a total of 212 edible insect species from nine orders were recorded and are potentially consumed in different African countries (Appendix A). Of these, 41% were Lepidoptera, 23% Orthoptera, 15% Coleoptera, 12% Blattodea (including both cockroaches and termites as recently classified), 4% Hemiptera, and Hymenoptera, Diptera, Blattodea, and Mantodea each contributed <1%. Rhynchophorus phoenicis (African palm weevil) and Cirina forda (Pallid emperor moth) were the most studied species in Africa, with 32 publications from 12 countries, and 18 publications from 10 countries, respectively ( Figure 2). Most research has been done in the western African countries, particularly in Nigeria, mainly on Rhynchophorus phoenicis and Cirina forda, which are the most consumed species in West Africa. However, southern African countries (Zimbabwe, South Africa, and Bostwana) have the highest number of consumed species, but little research has been done on nutritional content and consumption patterns of edible insects.

Nutrient Composition of Edible Insects
A compilation of nutrient composition of 54 edible insects based on the dry matter is presented in Table 1. Percentage of fat, protein, moisture, and ash content were calculated based on dry weight of the insect when ready for preparation to eat, noting that, in some cases, the insects had been processed since collecting. The highest protein was reported in Lepidoptera (range: 12-79%) and Orthoptera (12-73%), while the lowest protein content ranging from (0-39%) was reported for Blattodea.

Nutrient Composition of Edible Insects
A compilation of nutrient composition of 54 edible insects based on the dry matter is presented in Table 1. Percentage of fat, protein, moisture, and ash content were calculated based on dry weight of the insect when ready for preparation to eat, noting that, in some cases, the insects had been processed since collecting. The highest protein was reported in Lepidoptera (range: 12-79%) and Orthoptera (12-73%), while the lowest protein content ranging from (0-39%) was reported for Blattodea. Note the mineral abbreviations are Fe: Iron; Zn: Zinc; Ca: Calcium; P: Phosphorus; Mg: Magnesium. * Source [37]. Mean ± standard deviation of insects belonging to the same insect order are highlighted in bold and species names are in italics.
Edible insects are widely consumed in Africa, and play an important role in nutritious diets. However, the preference and consumption of insects vary with species and orders. Lepidoptera caterpillars were the most consumed order, and they are the most preferred species because of their nutritional value, they are rich in protein, fats, and essential micronutrients [6,54]. In addition, several caterpillar species play an important role in income generation in rural areas in southern Africa, Uganda, and Nigeria [18,22,55].
Studies from western and Central Africa indicated that Rhynchophorus phoenic (palm weevil), and Cirina forda (pallid emperor moth) were the commonly consumed species [18,24,56]. The palm weevil and pallid emperor moth are a delicacy in western and Central Africa, and, in addition, these species were of economic importance in Nigeria, Cameroon, Benin, and Ghana [57]. In southern Africa, the literature indicates that the most consumed or preferred species were Imbrasia belina (mopane worm), Macrotermes natalensis, falciger, and bellicosus (termites) [28,50,58]. While in eastern Africa, the most consumed species were Ruspolia nitidula and differens (grasshoppers), [22,[59][60][61]. Mopane worms, and termites are an important part of food culture in different ethnic groups in southern Africa [18,59]. Moreover, the trade of mopane worms and termites plays an important role in rural food security and income generation, as it provides rural people with household income [28,50,57,58].
Edible insects are a good source of protein content, which ranges from 12-79% of dry matter, which is consistent with studies from China, Germany, and Asia [6,10]. The protein content reported in edible insects is higher than protein found in chicken (43%) or beef (54%) [28,62]. The high protein content found in edible insects could help to combat protein deficiency in Africa. Protein deficiency is a major contributor to human malnutrition [63], and, in Africa, protein deficiency is the most common form of malnutrition, which needs to be addressed to halt starvation [64]. Therefore, including edible insects in daily diets might help reduce malnutrition rates.
Moisture content ranged from 1-7.5%, which is relatively low, such that most edible insects have longer preservation periods, and the risk of microbial deterioration and spoilage is minimal [29,42,65]. Unlike beef or chicken, which are prone to decay (unless refrigerated), edible insects can be stored for longer periods, especially during the dry season when food shortage is higher [42]. However, three caterpillars (Gonimbrasia (Nudaurelia) alopia, Anaphe panda, and Pseudontheraea discrepans) had higher moisture (>60%), meaning they are prone to spoilage and their preservation period is shorter unless processed in some manner. Siulapwa et al. [29] reported similar results, where caterpillars Imbrasia belina and Gynanisa maja had higher moisture content than other species. To increase shelf life, caterpillars are usually degutted, washed in boiling salt water, or roasted before drying in the sun, then packed in large sacks and containers [23,66].
Edible insects contain fat content ranging from 1-67%. The fat content of edible insects are higher in the larval stage. For example, a palm weevil, which is a beetle larva that is consumed as a delicacy in western Africa, contained the highest fat content of 67%. These results are consistent with Bukkens [67], who reported that Lepidopteran caterpillars and palm weevil larvae contain higher fat than any other insect species. Edible insects can be used to provide essential fatty acids required by the human body [10,68]. In addition, fat plays an important role in providing the human body with energy, which means that consuming insects such as Rhynchophorus phoenicis, Imbrasia belina, Anaphe panda, and Brachytrupes membranaceus, may help provide people with energy, thereby reducing malnutrition associated with energy deficiencies in developing countries [4,10,69].
Carbohydrates play a very important role in human nutrition as they are the primary source of energy. Carbohydrates found in edible insects varied from 5-51% [19,70]. Therefore, edible insects can be used as a source of carbohydrates, as they contain relatively high amounts of polysaccharides, which play an important role in enhancing the immune system of the human body [10]. In addition, carbohydrates are an essential nutritive element in the human body [29]. Species such as Oryctes monoceros and Gryllotalpa africana, reported in the current study, contained a high amount of carbohydrates; therefore, edible insects can be included in human diets to provide a good source of carbohydrates [29].
Excellent source of iron and zinc found in some edible insects indicate that edible insects could be used to combat malnutrition deficiencies such as zinc and iron deficiency anemia, which is prevalent in Africa [37]. Species such as Zonocerus variegatus, Pseudacathotermes spinige, and Macrotermes herus contained high iron content of 910, 332, and 161 mg/100 g respectively, which means that these species can be used as a good source of Iron. Zinc content was notably high in insects such as Zonocerous variegatus (29 mg/100 g) and Rhyncophorus phoenicis (26.5 mg/100 g) the Zinc content found in these insects exceed the daily recommended intake of 3.0-14 mg/100 g. Rumpold and Schluter [6] reported that Iron and Zinc content found in edible insects is generally higher than the Zinc and Iron content found in pork, beef, or chicken; therefore, edible insects might be a solution in fighting Iron and Zinc deficiency. Zinc and Iron deficiency are one of the health problems faced by many women of reproductive age and children in developing countries [37]. Therefore, consumption of edible insects might provide a solution to Iron deficiency health problems, such as anemia, reduced physical activity, and maternal mortality [37,71].
Edible insects reported in the current study contained a low amount of Vitamin A, B2, and C. The 100 g dry matter of edible insects reported in this study did not contain enough daily recommended Vitamin A (500-600 mg) or C (45 mg). As such, Chen et al. [10] reported that to meet the daily recommended amount of Vitamin C, insect tea derived from the excrement of insects is an option. This tea contains up to 15.04 mg of Vitamin C per 100 g, and the consumption of 300 mL of insect tea per day makes 45 mg of Vitamin C, which is the daily recommended amount of vitamin C for adults [10]. Contrary to findings reported in this study, Bukkens [67] reported that Vitamin B1, B2, and B3 content found in an edible house fly is richer than the Vitamin B1, B2, and B3 found in chicken, beef, or salmon. In addition, edible crickets contain twice more Vitamin B12 than the beef [69]. Igwe et al. [72] found that Microtermes nigeriensis contain a favourable high source of Niacin, Thiamine, Vitamin A, and C. Vitamins play an important role in human nutrition, as Vitamin C is important for human growth, development, and repair of various body tissues [73]. The excellent source of Vitamins found in some edible insects shows that insects have a great potential of being used as a healthy food supplement for malnourished people, or to prevent malnutrition [24].
There were several limitations to this review, which included studies reported in English only and excluded studies published in other languages used in Africa. There were significant gaps in data available on the nutritional composition of edible insects consumed in Africa. Most publications focused on a single macronutrient content, especially protein, carbohydrates, fats and fibre, and other nutrients, especially minerals, are not included in analyses. In addition, research focused on reporting the nutritional composition of economically important species such as Imbrasia belina, Macrotermes natalensis, bellicosus and falciger, Rhynchophorus phoenics, and Cirina forda. Strengths of this review incudes the robust approach to combine the nutritional composition of consumed insects in Africa, previous studies have focused on documenting the nutritional composition of single, or a group of, insects that are consumed in Africa.
This review reported combined nutritional data of consumed insects in Africa; this information can be useful to policy makers in the health and nutrition sector by including insects in food and nutrition policies. Health officials need to motivate people to include insects in their daily diets, particularly the most vulnerable groups such as elderly people, women, and children, with the aim to improve the quality of life for people. In addition, farming and rearing of insects by the agricultural sector need to be adopted to ensure that insects are easily accessible and available all year even when they are out of season in nature. Insects can be included as an ingredient in other food products such as bread, maize powder, chocolate, and biscuits to overcome discomfort and fear associated with eating whole insects in some groups of people. Future studies are required to research sustainable ways of farming and rearing insects in Africa and the implication that might have on the environment.

Conclusions
Meeting global food demand and halting poverty in Africa are among the greatest challenges, and these challenges are expected to continue if sustainable and innovative measures are not put into place. In 2017, approximately 256 million people were reported to be undernourished in Africa [74]. There is no doubt that Africa is far from achieving Sustainable Development Goal 2, which is to end hunger, achieve food security and improved nutrition, and promote sustainable agriculture by 2030. Edible insects are widely consumed in Africa, and they play an important socio-economic role for rural communities in Africa, by providing nutritious diets (this review), and income opportunities to traders and harvesters [22,75,76]. In addition, edible insects are a traditional delicacy, and are used as an emergency food source during times of food shortage [57]. They are rich in protein, carbohydrates, amino acids, and micronutrients such as Zinc and Iron. This implies that edible insects have a potential of contributing in sustainable diets, while assuring food security, and improving livelihoods of African people.  Acknowledgments: This study forms part of the Sustainable and Healthy Food Systems (SHEFs) supported by the Wellcome Trust's Our Planet, our Health programme (grant number, 205200/Z/16/Z). We would like to thank Alan Dangour for providing constructive comments that helped improve this review. Lastly, we would like to thank the National Research Foundation (NRF) for financial support.

Conflicts of Interest:
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.