Safety, regulatory, and environmental issues related to breeding and international trade of edible insects in Africa

Insect breeding or farming for food and feed is an emerging enterprise that can address the ever-growing demand for protein and curb high unemployment rates in Africa and beyond. However, for the sector to prosper, its value chain needs to be regulated to ensure sustainability and safety for consumers and the environment. Although a few African countries, such as Malawi, Tanzania, Kenya and Uganda, have promulgated standards on the use of insects as food and feed, greater efforts are needed in other countries, and relevant policies governing the sector need to be formulated. All over the globe, attention to the regulation of the edible insect sector is peaking, and more investment in the industry is foreseen. Safety issues such as the identity of insects to be reared, substrate quality and traceability imposed by importing countries will be critical for expansion of the sector. This paper analyses safety, regulatory, and environmental issues related to breeding and international trade of edible insects in Africa and provides case studies and recommendations for sustainable use of insects for food and feed.


Introduction
Eating insects is a part of local culture for at least 2 billion people in about 113 countries (1)(2)(3)(4), and Africa accounts for over 120 million insect eaters (5). Of the 2111 edible insect species known globally (6), around 500 species have been reported in sub-Saharan Africa (7, 8). In Africa, edible insects are mainly collected from the wild for household consumption and informal trade (9-12). Wild harvesting is unsustainable due to the seasonal availability of insects, habitat change and overexploitation (9). Eating or feeding insects to animals is recommended because of their unique nutritional profile, which is 41_1_10_Niassy -pre-print 3/34 equals or exceeds that of conventional foods (13). Insects are an excellent source of protein, fatty acids, vitamins and minerals (14).
Besides traditional entomophagy (the practice of eating insects) in some parts of the world, increasing demand for alternative sources of nutrients for humans and animals has fuelled the need to farm edible insects (2, 5, 15).
Farming edible insects ensures continuous supply and offers alternative and cheaper protein sources compared to soy and fish meals (16,17). Adopting cost-effective technologies for rearing, harvesting, handling, processing, added value, and packaging is a significant game-changer to ensure constant availability of insect proteins and enhance profit margins for farmers and other stakeholders (7, 8). Insects grow faster with high feed conversion efficiency and have less requirements for space and water than many conventional feed species. The carbon footprint of insect farming is much lower than conventional farming (2, 4,18). Insect farming is gender-friendly (15,19,20) and currently, there are nearly 1000 edible insect farms in Africa, with the industry projected to be worth up to US$8 billion by 2030 (5). A recent World Bank report estimates that black soldier fly farming alone has the potential to replace 60 million tons of traditional feed production in Africa annually, leading to 200 million tons of recycled crop waste, 60 million tons of organic fertilizer production, besides creating 15 million jobs (5). Therefore, the use of insects as food and feed may help attain some UN Sustainable Development Goals and the aspirations of the African Union Agenda 2063 (21).
Although insect farming is considered an emerging enterprise in Africa (5, 15,22), critical issues in the production chain need undivided attention if the sector is to prosper. Key among these is safety, and the most debated issues are food hazards commonly associated with edible insects and their by-products. These issues may be related to how the insects have been reared, euthanised, handled, processed and packaged.
Biological agents and chemical contaminants are some major health hazards associated with edible insects (2). Safety issues around insects for food and feed cut across environmental, health, agriculture and trade.
41_1_10_Niassy -pre-print 4/34 Food safety regulations on edible insects are not fully realised in Africa due to a wide range of challenges (23). These challenges include: 1) lack of awareness of food safety on socio-economic matters; 2) lack of established hazard and critical point checklists/systems; 3) limited data and information on health burden, especially food-borne diseases; 4) limited compliance with international agreements on food safety and quality standards; 5) limited enforcement of local, regional and international standards and global best practices; 6) limited resources to support scientific risk analysis and upgrading of food safety regulatory systems; and 7) poor food supply chains and traceability system.
Several authors acknowledged the lack of regulatory frameworks specific to insect farming and their use as food and feed in many countries (18,24,25). There is also a lack of harmonisation to improve policy and strengthen the trading environment, especially market linkages, to reduce constraints along the insect-based value chain (25).
Several regulatory bodies are nominally in charge; however, procedures and the motivation behind these safety measures on food are often unclear, overlooked or fail to capture specific matters that concern the farming of insects as "mini-livestock". The lack of understanding of these regulatory and legislative measures vis-a-vis the diversity of edible insects (which belong to several insect orders with very different lifestyles) hampers the sector. The objective of the present paper is to analyse the regulatory elements that govern safety issues in edible insect farming for national and international trade and provide an overview of legal procedure flow among regions and countries in Africa. The production chain and safety and regulation in relation to the environment and trade are summarized in Fig. 1. resistant bacteria are also of major concern. High levels of microbial pathogens will raise health concerns and consequently affect the consumption and sale of edible insects and insect-based products at a local, national, regional and international scale.  (2).

Pesticides residues and toxic, trace metals
Pesticides residues and toxic metals in reared insects can be associated with particular insect species, their source before being reared, sources and type of substrates used and contamination of the rearing unit (2, 39

Other substances
According to FAO (2), edible insects and insect products may contain, accumulate or release noxious substances. These substances include bioaccumulated organic compounds (organic contaminants, plasticisers, and halogenated flame retardants), dioxin-like polychlorinated biphenyls (PCB), spiked levels of mineral oil hydrocarbons and histamines. Other undesirable contaminants such as antimicrobials, allergens and inherent anti-nutritional substances (phytic acids, tannins, saponins, phenolics, thiaminase, cyanogenic glycosides and oxalates) may accumulate in edible insect products during production and processing (2). Poorly processed and packaged edible insect products may contain undesirable objects and hard parts of the insects such as wings, rostrum, stings and spines.

Allergies arising from eating insect-based products
Insects and crustaceans are related members of the phylum Arthropoda.
Since allergic reactions to crustaceans are potentially severe, a cross-41_1_10_Niassy -pre-print 9/34 reactivity and co-sensitisation of the immune system between edible insects, crustaceans and mites pose a potential health concern (43).
Indeed, cases of cross-reactivity/co-sensitisation between edible insects and crustaceans leading to food allergy have been clinically relevant with an unknown underlying molecular mechanism attributed to allergens, specifically arginine kinase (44 and references therein). Food allergy due to consumption of edible insects has been described for silkworms, mealworms, caterpillars, locusts, grasshoppers, cicadas, bees and sago worms (45). There are opportunities for further research on allergies due to eating insects, including diagnostic allergy tests that could lead to the identification of vaccines.

National, regional and international regulatory frameworks for edible insects
As insect farming is gaining prominence, questions on safety are increasingly important. Countries that are known to practise entomophagy lack regulatory policies that would potentially benefit the insects for food and feed sector. These countries rely on a precautionary approach or the World Health Organization (WHO) and Food and Agricultural Organization (FAO) information on insect-based diets (18). Most studies have clearly shown that there are more stringent rules on the use of insects as "novel food and feed ingredients" in countries with no history of entomophagy but have food policies that prioritise food safety (18,46). Country specific regulations have also been formulated in some countries (47). can be considered to be either in "traditional" or "transitioning" stages towards "modernising" food systems. While African countries are in the "transitioning" stages of recognising edible insects as "foodstuffs" or "animal feed", it is expected that most existing food laws and policies would apply to edible insects as well.
Edible insects are not listed in the Codex Alimentarius, which is considered a global problem (53 However, in the case of EU standards, insect species used for food and feed must be reared on a substrate that fulfils certain prescribed safety conditions for insect production (53,56,57). According to the EU, insects used as food and feed should not be reared on waste streams (2, 57); however, insects meant for biomass conversion for economic gains can be reared on waste streams (2). Though EU restrictions are designed to eliminate the risk of prion contamination of the edible insects, they limit their use to close nutrient loops, this is also the case for Africa.

South Africa
In South Africa, four government departments oversee food safety and quality legislation (Table I) (Table II).      Regulatory procedure of the insect production chain and the emergencies in relation to safety in Kenya