Edible insects as a means to address global malnutrition and food insecurity issues

Edible insects as a means to address global malnutrition and food insecurity issues Although unconventional in the USA, entomophagy, or the practice of consuming insects, can provide a nutritious relief to many malnourished people in developing countries. Edible insects are part of numerous traditional diets found in over 113 countries, including those in Asia, Africa, and South America. Currently, there are 2 billion people consuming over 2000 recorded edible insects. Many of these worldwide insects contain amounts of protein, fat, vitamins, and minerals comparable to commonly eaten livestock. With the popularity of crickets in both developing and developed countries and the nutrient density of locusts, these insects were of particular interest. Rice flour, made from a major food crop around the world, was used as an effective vehicle to deliver these insect ingredients. The use of inexpensive single-screw cold-forming extrusion technology, due to its capability of high production rate yet low capital and operating costs, was employed in making insect-fortified products. The feasibility of incorporating edible insect flours from cricket and locust in an extruded rice product has been demonstrated to be successful with acceptable shelf stability and sensory characteristics. Nutritionally, the insect rice products developed were energy dense (high fat content) and as an excellent source of protein. They also contained considerable amounts of dietary fibre and iron. Sensory evaluations involving 120 untrained panelists–suggested cricket formulations were well accepted compared with locust formulations. There is a positive outlook on the overall acceptance of entomphagy even in developed countries. As a staple food providing 20% of the world’s dietary energy and consumed by over 1 billion people, rice is an ideal vehicle to deliver nutrients carried by edible insects. The incorporation of insect flours in processed foods such as extruded rice products can greatly promote the consumer acceptance by disguising the ‘yuck’ factor associated with intact insects. Keywords: edible insect; food security; malnutrition; consumer acceptance; extruded rice. nutritional benefits. They offer plenty of calories, protein, fat, vita- Introduction mins, and minerals, depending on their species, metamorphic stage, Whether from a perspective of developing or developed countries, and diet. the entire global population is in need of alternative food sources. Although still widely unconventional, developed countries have People living in developing nations, including those countries in also begun considering entomophagy as a means to support our Sub-Saharan Africa or South Asia, are often found to be danger- ever-growing populations. In fact, the United Nation’s Food and ously malnourished. With beef and chicken being difficult to come Agriculture Organization (FAO) projects the world population by, they have been enjoying edible insects as a dietary resource for approaching to 9 billion by 2050. As the numbers swell, natural generations. This is because edible insects actually contain several © The Author(s) 2018. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 18 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 resources such as land and water are being rapidly degraded. Edible Madagascar has been facing political unrest, consequently putting insects, with their high feed conversion efficiency and fecundity, as the country into further economic distress and leaving almost 80% well as their minimal space for rearing, certainly represent as an of the population in poverty (Central Intelligence Agency 2014, advantageous solution for present and future food insecurity. UNICEF). Yet another tragedy is the recent locust plague of 2013. Even so, the ‘yuck’ or ‘disgust’ factor is not so easily elimi- As the infestation continues, more food crops and livestock grazing nated from today’s cultures. Despite its health benefits, perhaps lands could be destroyed, deepening on the suffering of the Malagasy the unappealing nature of entomophagy is in the consumption of people (FAO, 2009). With these outstanding issues, 53% of rural the whole insect. With that, the obscure incorporation of this food households have been reported to not consume enough food to source through the utilization of insect flours is considered. maintain an active and healthy life (UNICEF, 2001). Ongoing studies within our research group at California State Consisting mostly of rice, vegetables, and tubers, the Malagasy Polytechnic University, Pomona have demonstrated the feasibility of diet involves the consumption of these foods about 4 to 6 times a the obscure incorporation and fortification of a major food staple, week. Since rice is the product with the largest production quan- such as rice, by utilizing edible insect flour as a value-adding ingredi- tity, this is clearly reflected in their diet as it is also the number one ent. By removing the original form of the insect and incorporating its commodity available for consumption (FAO, 2014). Yet, proteins, flour into a food matrix that is widely consumed around the world, from both vegetables and animals, are seldom eaten, at an estimated we aim to provide an innovative solution for food insecurity and rate of 1 to 2 times a week (WFP and UNICEF, 2011). Fat, a major malnutrition, especially in developing countries. Furthermore, the source of calories, has also been demonstrated to be low in their hidden form of the edible insect is designed to reduce the ‘yuck’ fac- diets (FAO, 2010). Indeed, the main staple meal in Africa consists tor and increase the acceptance of entomophagy. Rice flour has been mainly of cereal grains, such as rice, sorghum, millet, maize, fonio, specifically chosen to be the vehicle based on the consideration that and tef (Filli et  al., 2014). These foods, being composed mostly of the nutrients carried by the edible insect will supplement the nutri- carbohydrates (rice 80%, sorghum 74%, and maize 78%), are not tional composition of rice. The two main ingredients are combined a major source of protein, and together with the scarce availability in different ratios to form a dough mass, which can be processed of animal protein, the Malagasy people lack the necessary macronu- through an economically feasible, cold-forming extrusion technol- trients for healthy living (Wu Leung, 1968). Moreover, the WFP and ogy. Through this production method, a final rice product containing UNICEF (2011) reports only 20% or less of the surveyed children to optimal addition level of insect flours has been developed, and the have received foods rich in vitamins and minerals, sources of which measurements of its physicochemical properties, nutrient profile, and include fruits and vegetables, legumes, nuts, and dairy products. consumer acceptability via sensory evaluations have been completed. Overall, 84% of households experience inadequate amounts of food While the measurements of organoleptic and nutritional properties or cash every year (WFP and UNICEF, 2011). of the insect rice product have been reported in a separate original Malnourishment occurring in early childhood and if untreated research article, published with the Journal of Insects as Food and results in life-threatening consequences. Chronic malnutrition will Feed (JIFF-S-17-00032) (Tao et  al., 2017), the results of consumer lead to irreversible stunting and has been reported to be the most acceptance study are summarized in this review article. important risk factor for illness and death from diseases (WFP, 2015; Muller et al., 2005). Approximately 150 million children worldwide do not consume the required amounts of energy or nutrients for Food Insecurity and Malnutrition growth and development, with more than half (52%) of these chil- dren residing in South Asia and almost a quarter (21%) living in Although not as widespread in the USA, food insecurity remains a Sub-Saharan Africa (UNICEF, 2001). serious and prevailing issue for much of the world. There is an esti- mated 805 million people who are without enough food to main- tain a healthy and active lifestyle, according to the World Food Nutrient Content of Edible Insects Programme (WFP, 2015). Developing countries, especially those in South Asia and Sub-Saharan Africa, have the highest rates of hun- Interestingly, although perhaps not surprisingly, entomophagy is ger. Although Asia contains the largest population of hungry peo- especially practised in developing nations. Countries in South Asia, ple, about two-thirds of the total, Africa has the highest prevalence where more than 40% of the population is chronically malnour- (WFP, 2015). ished, have already long accepted entomophagy as part of their While many developing countries are facing food insecurity culture. For instance, countries such as India and Lao People’s today, Madagascar, for example, is in an especially delicate state. Democratic Republic have identified 24 and 21 edible insect species, Madagascar is one of the 10 countries with the highest occurrences respectively. Collectively, Africa has been reported to have some 246 of chronic malnutrition (UNICEF, 2013). With at least 50% of the species of edible insects. Countries within this continent that exhibit population moderately or severely malnourished, food insecurity more severe rates of chronic malnutrition, such as Madagascar or remains a critical concern in this nation. In 2013 alone, 4 million Zambia, possess 22 to 33 species (Ramos-Elorduy et  al., 1997). people faced hunger as almost one-third of the population was bur- These insects are consumed for their comparable levels of energy dened with food insecurity (WFP and UNICEF, 2011). Causes of and nutrients, although the levels may vary depending on species their struggle are numerous and difficult to resolve. Deforestation type, metamorphic stage, habitat, and diet. For instance, a study con- by slashing and burning, a largely unsustainable agricultural pro- ducted in Thailand demonstrated that 100 g of insects (fresh weight) cess, has resulted in soil erosion and even rice field destruction (a had comparable, if not more, calories than that of equal weights of major staple) (UNICEF, 2001). The fragility of the environment has commonly eaten livestock, excluding pork (Sirimungkararat et  al., left very few farmers with enough land to cultivate (UNICEF, 2001). 2010). Ramos-Elorduy et al. (1997) reported that of 78 insect species Furthermore, as agriculture accounts for more than one-fourth of found in Mexico, the caloric content ranged 293–762 kJ per 100 g of the country’s GDP and 80% of employment, much of the population dry matter. Specifically, migratory locusts (Locusta migratoria), the has become vulnerable to food insecurity. In addition, since 2009, species of which are currently plaguing Madagascar, were discovered Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 19 to have calories varying in the range of 598–816 kJ per 100  g of underprivileged do turn to edible insects for sustenance since other fresh weight in a study conducted in the Netherlands (Oonincx and forms of livestock are either unavailable or expensive, the tradition van der Poel, 2011). Moreover, besides the caloric value, these ani- of consuming edible insects is not always a tactic for survival. Banjo mals can provide crucial macronutrients as well. and others (2006) reported edible insects being included in a planned Likewise to the evidence supporting the caloric value of edible diet throughout the year and not solely as an emergency food sup- insects, it also suggested that insects are considered to be a substan- ply. A  collective group of people in South Africa called Pedis, for tial source of protein. Certain insects found in China were reported instance, value insect meals, such as those derived from caterpillars, with higher protein contents than those in most plants and com- even more so than beef as the latter sales decrease during caterpillar mercial meat, fowl, and eggs (Xiaoming et al., 2010). In the study, harvesting seasons (Womeni et  al., 2009). Palm weevils, especially 11 orders of insects were analysed with results of protein contents the larvae form of R.  phoenicis, have been a part of a traditional ranging from a low 13% to a high 77% (dry weight basis). Other African diet for centuries and are, like the locusts there, prepared researchers reported a range of 37%–54% protein content in eight by frying (DeFoliart, 1993; Banjo et al., 2006). Besides Africa, this insects found in Thailand (Raksakantong et  al., 2010). In spite of insect has also been appreciated across other tropical regions includ- these variations in protein content, edible insects overall demon- ing Latin America and Asia (DeFoliart, 1993). In Mexico, investi- strate to be an exceptionally good source of protein. While this gators reported exceptional consumer acceptance for their maize macronutrient is often difficult to obtain in developing countries and flour tortillas supplemented with ground yellow mealworm larvae so is lacking from their daily diets, edible insects are relatively more (Tenebrio molitor) (Aguilar-Miranda et  al., 2002). The practice of available than other meats, demonstrating yet again its worth as a eating insects can also be found in the East. Lethocerus indicus, or solution for reducing global food insecurity. giant water bug, is a particularly popular insect consumed through- Furthermore, while malnutrition is not limited to protein defi- out several Asian countries such as Thailand, Laos, Vietnam, and ciencies but includes the overall lack of caloric intake, populations Cambodia (Kiatbenjakul et al., 2015). Its odour provides a flavour within developing countries could also benefit from energy dense profile that is essential for consumer acceptance of food products foods provided by edible insects (DeFoliart, 1992). Energy intake such as chili pastes or fish sauces. As entomophagy is practised can be greatly enhanced, to an extent, with higher levels of fat, like around the world, a novel edible insect product has certain potential those potentially found in edible insects. In a study lead by Womeni for being accepted and enjoyed. and others (2009), six insects from Cameroon of Sub-Saharan Africa were analysed to determine their lipid contents and essential fatty Nutritional Variability of Edible Insects acid profiles. Results showed that not only were these insects an excellent source of fat, ranging from 9.12% to 67.25% (dry weight However, it is important to note that while promising, edible insects basis), but also that they were rich in polyunsaturated fatty acids. are still highly variable between/within species and metamorphic These types of fats, along with monounsaturated fats, have been stages. When comparing the amount of energy found between edible widely accepted to offer more nutritional benefits and should be insects in previously cited studies, these values varied by hundreds used to replace the intake of saturated fatty acids (Yang et al., 2012; of calories per gram (Ramos-Elorduy et al., 1997; Oonincx and van Enos et  al., 2014). Furthermore, the polyunsaturated fats included der Poel, 2011). Protein content had differences as great as 64%, essential fatty acids, such as linoleic (omega-6) and linolenic (omega- whereas fat had variations as high as 44% (Womeni et  al., 2009; 3) acids (Womeni et  al., 2009). Comparable findings were demon- Raksakantong et  al., 2010; Xiaoming et  al., 2010). It could be strated in Thailand as well, varying between 0.34% and 23.98% of easily discerned from these values that the benefits of each edible total fat content depending on the species of insects (Raksakantong insect species can vary significantly. In addition, analogous to shell- et al., 2010). Thus, edible insects have the potential to be an excep- fish or prawns, the type of habitat and diet of these insects can also tional source for energy and macronutrients. change their flavour and even their nutritive values (Ramos-Elorduy Micronutrients, on the other hand, are just as essential for a et al., 1997; Klasing et al., 2000; Finke, 2003; Raksakantong et al., healthy life. A major concern for developing countries is iron intake 2010; Oonincx and van der Poel, 2011; Nowak et  al., 2016). As as its deficiency is the world’s most common and widespread nutri- grasshoppers (Zonocerus variegatus) in Nigeria were fed with bran, tional disorder (WHO, 2014). Many of the insects safe for con- which contains more fatty acids than that of corn, these insects sumption contain abundant levels of iron that often exceed other demonstrated almost doubled protein levels (Ademolu et al., 2010). commonly eaten animals. For instance, edible insects such as the In yet another study, migratory locusts were fed with three differ- popular palm weevils (Rhynchophorus phoenicis) or mopane cat- ent diets, consisting either solely of grass, mixed grass and wheat erpillars (Imbrasia belina), both species found in Africa, can pro- bran, or combination of grass, wheat bran, and carrots (Oonincx vide 12 and 31 mg of iron per 100 g of weight, respectively (Banjo and van der Poel, 2011). The investigators found the wheat bran et al., 2006). Chicken and beef, on the other hand, provide only 1.2 diets reduced the protein content and increased the fat content of and 3 mg of iron, respectively (Sirimungkararat et al., 2010). Zinc, the locusts, whereas the addition of carrots further enhanced the fat another mineral important for growth and development, can be gen- content and provided greater levels of β-carotene. Hence, although erally found in most insects. For example, it has been reported that entomophagy has been revealed with great potential to be an extra- the aforementioned palm weevil larvae contain 26.5 mg per 100 g ordinary resource for relieving global food insecurity and malnutri- (Bukkens, 2005). tion, it is essential to obtain complete nutritional profiles in order to determine the actual nourishment available in the finished product. Entomophagy—More Than Survival Environmental and Economic Impacts The overall nutritional value of edible insects presents them to be a remarkable alternative for alleviating the food insecurity and mal- While developing countries are currently facing the burden of food nutrition in developing countries. Although it could be said that the insecurity, the FAO (2009) predicts that the global population will Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 20 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 increase to 9 billion by 2050. As the world population proliferates, many declined touching those insects to their lips. The concept of the demand for food and feed will escalate along with it, subse- food neophobia, the fear of trying new or novel food products, has quently requiring food production to increase by 70% (FAO, 2009). been suggested as the reason for this rejection (Megido et al., 2014). With the current state of the environment, and as it continues to This concept is explained by Rozin and Fallon (1980) to be a dismis- degrade, there is a call to conserve natural resources such as land sal due to distaste for the organoleptic qualities, fear of danger to the and water. Evidently, rearing insects requires remarkably less land body, or disgust stemming from a prior impression of what the prod- than farming other categories of livestock. Oonincx and de Boer uct is or of its origin. While either of these three explanations or the (2012) discovered that to produce 1 kg of edible protein, mealworms combination thereof may be understandable, perhaps the neopho- (T.  molitor) required only 10% of the land that is needed for beef bia of entomophagy could be lifted. Lobster, once considered ‘junk’ production. Although this difference may not be as dramatic when food in the 17th and 18th centuries, was established to be cruel and compared with pork or chicken production, mealworm farming still unusual punishment for feeding to servants and prisoners more than requires 29%–50% less arable land. Due to their obvious smaller twice a week (Greenlaw, 2002; Crowley, 2015). Today, lobster is size, edible insects also have the potential to be farmed vertically, regarded as a fine dining food, depicted as a pleasure enjoyed by thereby requiring no additional land clearing to advance produc- consumers with high incomes. Another interesting example is the tion (van Huis et  al., 2013). Greenhouse gases, including carbon history of the ever popular sushi dish, the California roll. When first dioxide, methane, and nitrous oxide, are also produced at a lesser introduced in Los Angeles, Ichiro Mashita, the sushi chef of Tokyo rate by insects such as crickets (Acheta domesticus) and mealworms Kaikan, innovatively substituted the toro (fatty tuna) with avoca- (T. molitor). When compared with pigs and cattle, the difference is dos as it had a similar texture but was more familiar to Americans. by a factor of about 100 (Oonincx et al., 2010). Furthermore, the He also placed the nori inside the rice as this too was an unusual manure produced from common livestock also contaminates the sur- ingredient (Crowley, 2015). Presently, California rolls have become face and groundwater while releasing ammonia and acidifying the an icon of sushi and are enjoyed all across the globe. Whatever the land (van Huis et  al., 2013). Although pigs have demonstrated to cause of the prior neophobia, lobster and the California roll have produce ammonia at a rate of 10 times or greater than crickets and had their status momentously and positively changed. Edible insects mealworms, the quantity produced by cattle is undoubtedly even less have the same potential. Megido and others (2014) suggest that the favourable (Oonincx et al., 2010). promotion of knowledge and acceptance of edible insects will begin As land becomes scarce, the water supply is equally threatened. with the understanding of the relationship between insects and shell- The FAO (2013) predicts that by 2025, two-thirds of the world will fish, as they are simply arthropods of the land and sea, respectively. be under stress due to water shortages. When evaluated against Correspondingly, increasing the frequency of positive exposures and the quantity required to produce 1  kg of grain protein, 100 times tasting trials would also be effective. more water is required to produce the same weight of animal pro- tein, especially as water is necessary for forage and feed produc- Edible Insect Fortification in Rice Flour via tion (Chapagain and Hoekstra, 2003). Although assessments for Extrusion T echnology the quantity of water required for farming edible insect is currently unavailable, the results are likely in favourable directions, in parallel What is also proposed for increasing acceptability is the form of the with that of greenhouse gas and ammonia emissions. edible insect ingredient. While traditional cooking methods such as In addition to the heavy usage of land and water, farming live- roasting or frying are frequently used to prepare tastier or more pal- stock also requires feed, which in turn requires further land clear- atable dishes, the insects often remain whole, especially in tropical ing. Alternatively, insects are cold-blooded and so only require feed regions (van Huis et al., 2013). Instead, edible insects can be made for energy and warmth. Studies have shown that to produce 1  kg into granular or paste forms that may result in improved acceptabil- of livestock weight, at least 2.5  kg of feed is required for poultry ity. While in a paste or powder form, they can be incorporated into meat, 5 kg for pork, and 10 kg for beef (Smil, 2002). Edible insects, other foods. For instance, in Thailand and other South Asian coun- such as crickets (A. domesticus), require only 1.7 kg to produce the tries, ground giant water bugs (L. indicus) are an essential ingredient same weight (Collavo et al., 2005). In addition, only a percentage of in chili paste and fish sauces (Kiatbenjakul et  al., 2015). Although this livestock weight is edible, consequently reducing the actual pro- the chili paste is used as an ingredient in dishes, the current study duction and availability of meat protein and other nutrients. While suggests that the fortification of a main staple food could be more chicken and pork provide 55% of edible weight, beef only provides effective as the ultimate vehicle for delivering valuable nutrients 40% (Nakagaki and DeFoliart, 1991). Crickets (A. domesticus) con- offered by edible insects. versely offer 80% of its live weight for consumption, making its feed Rice is a staple food for more than half of the world’s popula- conversion efficiency exceptionally high. Furthermore, insects in gen- tion, especially in developing countries (IRIN, 2010; USDA, 2012). eral reproduce more rapidly and in greater quantities. For instance, It provides 20% of world’s dietary energy and supports the liveli- the same aforementioned cricket species can lay 1200–1500 eggs hood of more than 1 billion people (FAO, 2004; IRIN, 2010). It is within 30 days (Patton, 1978). Insects also reach their adult stages regularly consumed and composes a great portion of the diets in much quicker than their livestock counterparts and so are capable of both developing and developed countries. The overall percent of reproduction sooner. dietary energy supplied by rice for Asia, Africa, and South America has been reported to be about 30%, 10%, and 10%, respectively (FAO, 2004). Specifically, developing countries such as Bangladesh, Getting Over the ‘Yuck’ Factor Laos People’s Democratic Republic, and Indonesia have more than However, despite the undeniable benefits for consuming and rearing half of their dietary energy supplied by rice. Other than energy (363 edible insects, this does not deter from the ‘yuck’ or ‘disgust’ factor. calories/100 g), rice is also a good source of thiamin, riboflavin, nia- A study conducted by Rozin and others (1999) revealed that despite cin, and amino acids such as glutamic and aspartic acid (FAO, 2004). American students being willing to touch insects with their hands, While rice lacks lysine, edible insects such as caterpillars (Gynanisa Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 21 maja), grasshoppers (Ruspolia differens), and winged termites per 100 g, crickets can offer 125 kcals, 15 g protein, 6.3 g fat, 41 mg (Macrotermes falciger) can complement this essential amino acid iron, and 75 mg calcium as well as other benefits (Sirimungkararat (Siulapwa et al., 2014). et al., 2010). Crowley (2015) stated that crickets provide 15% more To obtain rice, the grain is milled to remove the outer husk and iron than spinach, two times more protein than beef, and equal bran layer. During this process, broken rice is produced and can be quantity of vitamin B12 as salmon. Locusts, while currently not as used to create rice flour. Our research group has conducted a study available as crickets in the market, are superior in nutrient density. to determine the feasibility of combining an edible insect flour ingre- They can offer 598–816 kcal, 13–28  g protein, and 8–20  mg iron dient with rice flour for the fortification of a staple food (Tao, 2016). per 100 g (Oonincx and van der Poel, 2011; van Huis et al., 2013). The successful results from this study would first extend the yield Inclusion of locust may also provide a solution to present or future of rice harvest and create an additional economic prospect for this infestations, as these insects often occur in swarms. Despite being milling byproduct (Qian and Zhang, 2013) and second improve the viewed as pests, locusts are popular as fried dishes in countries such acceptability of a nutrient dense ingredient such as edible insects for as Thailand and Madagascar. general consumers. Brown rice flour was used as the major bulk ingredient for the To create this fortified rice product, extrusion, a method that production of the extruded insect rice. In contrast to white rice flour, is growing in popularity especially in developing countries, was brown rice flour is more nutritious and also provides the colour employed. Extrusion is a continuous process that combines cooking, background to disguise the intrinsic dark colour from edible insects. mixing, shaping, and forming (Fellows, 2009). The process begins Brown rice flour offers an additional 18% protein, 48% dietary by the raw materials, typically in granular form, being fed into the fibre, 82% iron, and 67% zinc compared with its white colour coun- barrel where water is added to convert the dry ingredients to a semi- terpart (USDA, 2015—National Nutrient Database for Standard moist dough mass that is processed further. As the screw within the Reference, Release 27). In general, white rice is also inferior in its barrel kneads the mixture, it becomes plasticized with a desirable supply of vitamins and minerals when compared with brown rice. rheological property suitable for extrusion. The screw pushes the Formulation development began at a 5% (dry weight basis) add- dough mass out of the die holes where it expands and cools rap- ition level of insect flour in the extruded rice formulation and was idly, forming the shape set by the type of die plate used. This type of then increased to 10% and 15%. Concerns for the increasing add- technology can generate a remarkable number of products, ranging ition levels of edible insect ingredients included an intensified aroma from cereals, pasta, soup and beverage bases, hot dogs and sausages, and taste, which, although may be familiar in other dishes, is not processed cheese, and chewing gum (Fellows, 2009). currently associated with rice. Regardless, the protein fortification of Action towards promoting the application of extrusion tech- insect flour to a product such as brown rice was certainly advanta- nology has already been set forth. ExtruAfrica, an initiative of the geous. For instance, by referencing the certificate of analysis (COA) Center of Excellence in Advanced Manufacturing at the North-West provided by the vendor of the cricket flour, we predicted that a 15% University in South Africa, encourages the extrusion method through insect flour formulation would theoretically increase the protein conferences and training workshops. The first seminar was first content by 8.5–9 g of protein per 100 g of insect rice. Together with held in 2011 and continues on (ExtruAfrica, 2015). Filli and oth- the protein content originally in existence with brown rice flour (3 g ers (2014) suggest extrusion technology to be a key to adding value protein per 40 g serving), 100 g of the insect rice would provide an to agricultural commodities to reduce food insecurity in developing estimated 13.5–14.6  g of protein or 26%–29% of the daily value countries. Staple cereal grains, including rice, have yielded positive (DV) of protein. results. In fact, several investigators have already made considerable A preliminary study confirmed that there were no major differ - progress in creating products that incorporate indigenous materials ences observed from both the extrusion process and the physical and through extrusion applications (Filli et  al., 2014) while increasing organoleptic properties of the extruded rice particles when incorpo- nutrient density (Obatolu, 2002). Moreover, utilization of extrusion rating 5% cricket flour in the brown rice formulation; however, the technology will also offer potential employment and an improved incorporation of 10% and 15% resulted in apparent difficulty to livelihood for local citizens. the extrusion operation and observable differences in particle shape, size, and organoleptic properties. Therefore, the study later focused on the formulation development using higher addition levels (10% Consumer Acceptance of Insect Fortified, or 15%) of either cricket or locust flour. A total of four formulations Extruded Rice Product were developed: 10% cricket rice (10CR), 15% cricket (15CR), As detailed experimental design and laboratory measurements are 10% locust (10LR), and 15% locust (15LR). presented in a separate research article published  by Journal of To determine the acceptability of the insect rice product, a panel Insects as Food and Feed (JIFF-S-17-00032) (Tao et al., 2017), this of 120 untrained participants were recruited via convenience sam- review article will mainly report the outcomes from a consumer pling. Panelists were required to be without shellfish allergies, con- acceptability study. sumers of brown rice, and between the ages of 18–65 years old. It To make the extruded insect rice product, two edible insect flours was heavily stressed that those with shellfish allergies were unable to were chosen, derived from cricket and locust, respectively. Both partake in the study as an allergy to shellfish was likely to produce insects are enjoyed by many populations around the world. Crickets a similar reaction to land insects. It was also encouraged that the are commonly consumed in Thailand, where there are 20 000 regis- participants were either familiar with or enjoyed brown rice as this tered cricket farmers (van Huis et al., 2013; Dunkel 2015) as well was the base of the products. With the questionnaire being an affect- as other Asian countries such as Lao People’s Democratic Republic ive sensory test, it was essential that the panel be users of this prod- and Cambodia (van Huis et al., 2013). They are also making their uct. The age range of the participants was determined as a means way into the US market as they are appearing in commercially pro- to exclude minors and those with a higher risk of compromised duced products such as energy bars from Chapul (Colorado) and immune systems. Another prerequisite for participants was that they ‘Chirps’ (cricket chips) from Six Foods (Boston, MA). Nutritionally, were willing to consume edible insects. Thus, participants knew that Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 22 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 the products to be tasted contained such an ingredient. Although any further education at the time. For instance, there were no choices the ‘yuck’ factor remains a major issue in entomophagy, those who for completing a 2- or 4-year degree while currently in the work- unknowingly consumed edible insect products could become ser- place and not continuing any education. There was also no option iously distraught after learning what they’ve tasted. Hence, despite for those who were still in school but past their 4th year of college. the potential bias that may occur from having this information, it With that, there may be some inflation within the data for the groups was in the best interest of the participants that they were informed stating to be within their 1st–4th year in college (Figure 4). that the products contained edible insects. Perception of Entomophagy Sensory Panel Demographics Several inquiries pertaining to the concept of entomophagy were To profile the sensory panel, a demographics survey was included in asked in a separate survey within the questionnaire. These questions the questionnaire and the age, gender, ethnicity, and the highest level and their responses are displayed in Figures 5–8. As mentioned, two of education were asked (Figures 1–4). of the largest ethnicity groups within the sample population were With recruitment taking place on the university campus, it was Latinos and Asians. In Mexico, ‘escamoles’, or black ant larva, are no surprise that the majority of the panel was in their early 20s, fairly popular dishes and can cost $25 or more per plate (Aguilar- about 76% (Figure  1). Only 6% of the panel was 35  years old or Miranda et al., 2002; Premalatha et al., 2011). ‘Ahuahutle’ is a famed above. It was also found that the ratio of men-to-women panelists was almost 50:50, with only 10% more females to males (Figure 3). In a previous study conducted in Belgium, a similar ratio was found in their sensory evaluation with mealworms (T. molitor) and crickets (A. domesticus) (Megido et al., 2014). These similarities may suggest that either entomophobia or lack thereof holds no discrimination against gender, although this may require further analysis of the data to confirm this proposition. In terms of ethnicity, there were a greater number of Latinos and Asians, together making up almost 70% of the sample population (Figure 2), which may simply be reflective of the campus population. An issue, found only after surveys were con- ducted, was in the options available for the education-level question. There was no option for participants to identify themselves as per- sons who have graduated from their bachelors but were not pursuing Figure 3. Gender of sensory panel. Figure 1. Age of sensory panel. Figure 4. Education level of sensory panel. Figure 2. Ethnicity of sensory panel. Figure 5. Familiarity with entomophagy. Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 23 While entomophagy is unquestionably strong within Latin America, countries in Asia also share this tradition. The giant water bug, as aforementioned, is a prominent edible insect used in mul- tiple dishes for its unique flavour in Thailand and other South Asian countries (Sirimungkararat et al., 2010; van Huis et al., 2013; Kiatbenjakul et  al., 2015). While silkworms are farmed for silk production, their pupae are also prized delicacies in China, Japan, Thailand, and Vietnam (Sirimungkararat et  al., 2010; van Huis et al., 2013). In Korea, rice-field grasshoppers are consumed as side dishes or snacks (van Huis et al., 2013). Considering that about 70% of the participants were self-reported to have cultural or ethnical background from countries where entomophagy is such a widely practice custom, it seemed appropriate that at least these many par- Figure 6. Experience with entomophagy. ticipants were familiar with the practice of consuming edible insects (Figure  5). Furthermore, as the said countries are all regarded as developing nations, the data collected from the sensory evaluation study could be somewhat extrapolated to provide indications of con- sumer acceptance of such insect products in those countries within Latin American and Asia, although domestic Latin Americans and Asian Americans may practice unique dietary habits that are more or less different from the customs found in their mother nations. Thus, despite the present investigation being unable to reach those currently living in countries such as Mexico or Laos People’s Democratic Republic, the results could still offer some implications for such products being implemented in developing countries in the future, although these generalizations may be fairly limited. Figure 7. Future willingness to consume edible insects. Together, the 82% of panelists being familiar with entomophagy and the 73% of participants declaring a high probability of consum- ing edible insects in the future (Figure 7), which pointed towards a positive trend. In a separate study, Tuorila and others (1994) found a positive relationship between pleasurable first experiences with a novel food and the likelihood of future consumption. As more than 50% of the free-response comments included a statement of their enjoyment and/or support of the current study and its products, this certainly presents a progression towards the future applications of edible insects in the market, even in developed nations. Although it was required that participants be willing to consume edible insects to taste the samples, it cannot be completely assumed that the partici- pants would have chosen to eat edible insects after this experience. Figure 8. Future willingness to purchase edible insect products. This is clear within the 6% who reported that they probably would not or definitely would not consume edible insects in the future. This unwillingness could imply that there was some other incentive for their participation in this particular project. This could include some potential extra credit offered by their professors or even the peer pressure from friends and classmates. Even so, the majority of the participants were willing to con- sume edible insects in the future. While 73% reported positively in this inquiry, only 42% were able to say that they had con- sumed edible insects before their involvement in the current study (Figure 6). With more participants (58%) never having previously consumed edible insects, this is certainly a positive outcome of the study. It demonstrates the eagerness of a population to at least try edible insects. Even more dramatic are the findings from the Figure 9 Perception of edible insects in the diet. Belgium study by Megido and others (2014). In this particular sur- vey, the researchers found that although 46.6% of the participants Mexican caviar that is composed of some seven different species of reported some negative attitude towards entomophagy, an even Hemiptera (true bugs) (DeFoliart, 1992; Aguilar-Miranda et  al., greater number of respondents, 77%, were willing to consume 2002; van Huis et  al., 2013). A  perhaps even more famous food, edible insects. The novelty, and perhaps curiosity, of entomophagy especially in Oaxaca, Mexico, is ‘chapulines’, or grasshoppers, and is may be even more powerful than the ‘yuck’ factor. Progress is being consumed as street food (van Huis et al., 2013). This particular dish made towards the acceptance of entomophagy, much like sushi and can be found in many Mexican restaurants in the USA. lobster in the USA. Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 24 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 On the other hand, when taking into account the willingness to several panelists stated that consuming whole insects was a bit off- purchase edible insect products in the future, there seems to be some putting but suggested that if the flavour was suitable, they would be disparity. Although people stated that they would probably and def- more likely to enjoy the product. This comment about flavour being initely consume edible insects in the future, the results from Figure 8 able to better allow the acceptance of a product was also reflected show that they may not actually purchase these insect products. It in the actual sensory evaluation on four attributes including colour, is proposed that this is somewhat correlated with the fact that the aroma, taste (flavour), and texture (mouthfeel), as presented with majority of the panel is college students with limited finances, where more details in the separate article published by Journal of Insects as money is only spent on items that are absolutely essential or worth Food and Feed (Tao et al., 2017). the expense. As mentioned in the free response portions of the ques- tionnaire, knowing of the nutritional and environmental benefits of Summary of Sensory Evaluation consuming and farming edible insects would likely provide enough Besides the four attributes being considered by the panelists based on information for these consumers to make a decision towards pur- a 5-point ‘Just About Right’ (JAR) scale, participants were also asked chasing edible insect products in the future. to rank the four insect rice formulations on overall liking based on a An inquiry pertaining to the opinion of how edible insects should 7-point hedonic scale from 1 = dislike extremely to 7 = like extremely. be placed in the diet was also included in the survey. Participants Among the four sensory attributes, colour and aroma were not the were asked to select as many choices as they felt that described their key factors blocking participants’ acceptance of the insect rice prod- opinions. Perceptions of edible insects in the diet are displayed by ucts, whereas flavour (taste) and texture (mouthfeel) were significant the percentage of the sensory panel who selected those choices. This in differentiating the panel’s overall liking between two insect flours particular survey question had multiple selections and participants (cricket vs. locust) and two addition levels (10% vs. 15%) employed were asked to select all that applied (Figure 9). in the rice formulations. Of the flour insect rice formulations, lower When considering the marketing of edible insect products, the insect formulations, e.g. 10CR and 10LR, were observed to be more results from Figure  9 suggested that edible insects are most often parallel to market brown rice in flavour and mouthfeel, whereas the preferred to be consumed as a snack (22%), appetizer (19%), and rice products made with cricket flour (10CR and 15CR) were more side dish (19%). Edible insects being perceived most as a snack could preferred over those made with locust flour (10LR and 15LR) in be related to their small sizes or, in general, that snacking is on the all sensory attributes, except the colour. This is because locust flour rise. In fact, in 2014, the number of in-between snacks increased to featured a ‘golden brown’ colour shade to the rice products, whereas 2.8 with more than half of adults consuming three or more snacks the incorporation of cricket flour resulted in some ‘greyness’ to the per day (Wyatt, 2014). In a previous study, although ‘snack’ was not extruded rice particles. included as an option in the survey, edible insects were primarily Even so, flavour remained an important component to the distinguished as an appetizer. Investigators suggest that this also be acceptability of the insect products as several participants mentioned due to the small size and original form of the food (Megido et al., that a suitable flavour could positively sway the overall opinion of 2014). With edible insects being perceived as fourth as a main entrée a product. Multiple criticisms made by the panel recommended that (17%) in the current research, this implies that this source of protein the acceptability of the products would be greatly improved if served is primarily viewed as only supplementary and not yet as a main alongside other foods or seasoned, such as with salt or soy sauce. As source of meat, such as those from beef or chicken. Edible insects aforementioned, the study conducted by Megido and others (2014) were even less identified as a main entrée if it were left in its whole involving sensory evaluation on mealworms (T. molitor) and crickets form and as a dessert. While people generally do not consume their (A.  domesticus), where these insects were prepared in a variety of meat as whole animals, this is no surprise to be the same for insects. ways including baked, boiled, a crushed mix of both insects, meal- Even with shellfish, such as with shrimp, many consumers may pre- worms flavoured with vanilla, and mealworms with chocolate. It was fer to have the head removed before consuming. Moreover, as edible found that the most accepted form of preparation was with choc- insects are not particularly sweet, it is unlikely that edible insects olate, followed by flavoured with paprika, and then baked. Although would be perceived as dessert unless people were familiar with the each mealworm was crispy in texture, the investigators advocate the chocolate-covered insects or insect lollipops already available on the flavour to be the factor in preference (Megido et al., 2014). market. Even so, comparing these results with the response pertain- By being a rice product, these insect formulations do have the ing to the panels’ personal accounts with entomophagy, it was also advantage of being versatile in their formulation and preparation. derived that a few previous experiences with edible insect candies Indeed, one of the research assistants in our group took it upon him- were not positive ones. With these negative experiences, it seemed self to create a kimchi fried insect rice dish that was very much well appropriate that the ‘dessert’ option was not as highly selected even received by the other investigators in the group. While this sensory with the familiarity of edible insects as candies. evaluation reveals some introductory indication of how this product As mentioned, personal accounts of entomophagy were included would be fairly accepted in a developed country, such as the USA, as a free response question in the survey (Tao, 2016). A total of 50 the insect rice has the potential of being further developed to include people out of the 120 panelists provided their own encounters with flavours from herbs, spices, etc. Another potential ingredient afore- edible insects. Of these experiences, there were an unanticipated mentioned is the introduction of cocoa powder. Relating the col- number of accounts where the insect was intact. These foods were our observed in 10LR, which was with a toasted brown hue, many mostly roasted, fried, or seasoned products and were implied to be participants expected it to be much more flavourful than actually consumed as snacks, appetizers, or side dishes. About 20% of the experienced. In utilizing cocoa powder, and presenting the succeed- experiences were either in Mexico or in Mexican restaurants and ing outcome as a chocolate product, this could reduce the misleading involved grasshoppers. However, an overwhelming majority of the nature of the brown colour derived from the locust flour. Besides experiences was with crickets (86%) and was followed by worms some colour matching/masking, the cocoa powder may provide (i.e. such as mealworms, maggots, or silkworms) being the second some improved flavouring as a chocolate ingredient. The possibility most consumed insect (32%). While some enjoyed their experiences, Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 25 for the research and development of this insect rice into a marketable References product is seemingly boundless. Ademolu, K. O., Idowu, A. B., Olatunde, G. O. (2010). Nutritional value assessment of variegated grasshopper, Zonocerus variegatus (L.) (Acridoidea: Pygomorphidae), during post-embryonic development. Conclusion African Entomology, 18: 360–364. Aguilar-Miranda, E. 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(2010). rated/polyunsaturated fatty acids reduces the expression of adiponectin in Edible products from eri and mulberry silkworms in Thailand. In: Durst rats fed a high-fat diet. Nutrition Research (New York, N.Y.), 32: 285–291. Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Food Quality and Safety Oxford University Press

Edible insects as a means to address global malnutrition and food insecurity issues

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Abstract

Although unconventional in the USA, entomophagy, or the practice of consuming insects, can provide a nutritious relief to many malnourished people in developing countries. Edible insects are part of numerous traditional diets found in over 113 countries, including those in Asia, Africa, and South America. Currently, there are 2 billion people consuming over 2000 recorded edible insects. Many of these worldwide insects contain amounts of protein, fat, vitamins, and minerals comparable to commonly eaten livestock. With the popularity of crickets in both developing and developed countries and the nutrient density of locusts, these insects were of particular interest. Rice flour, made from a major food crop around the world, was used as an effective vehicle to deliver these insect ingredients. The use of inexpensive single-screw cold-forming extrusion technology, due to its capability of high production rate yet low capital and operating costs, was employed in making insect-fortified products. The feasibility of incorporating edible insect flours from cricket and locust in an extruded rice product has been demonstrated to be successful with acceptable shelf stability and sensory characteristics. Nutritionally, the insect rice products developed were energy dense (high fat content) and as an excellent source of protein. They also contained considerable amounts of dietary fibre and iron. Sensory evaluations involving 120 untrained panelists–suggested cricket formulations were well accepted compared with locust formulations. There is a positive outlook on the overall acceptance of entomphagy even in developed countries. As a staple food providing 20% of the world’s dietary energy and consumed by over 1 billion people, rice is an ideal vehicle to deliver nutrients carried by edible insects. The incorporation of insect flours in processed foods such as extruded rice products can greatly promote the consumer acceptance by disguising the ‘yuck’ factor associated with intact insects. Keywords: edible insect; food security; malnutrition; consumer acceptance; extruded rice. nutritional benefits. They offer plenty of calories, protein, fat, vita- Introduction mins, and minerals, depending on their species, metamorphic stage, Whether from a perspective of developing or developed countries, and diet. the entire global population is in need of alternative food sources. Although still widely unconventional, developed countries have People living in developing nations, including those countries in also begun considering entomophagy as a means to support our Sub-Saharan Africa or South Asia, are often found to be danger- ever-growing populations. In fact, the United Nation’s Food and ously malnourished. With beef and chicken being difficult to come Agriculture Organization (FAO) projects the world population by, they have been enjoying edible insects as a dietary resource for approaching to 9 billion by 2050. As the numbers swell, natural generations. This is because edible insects actually contain several © The Author(s) 2018. Published by Oxford University Press on behalf of Zhejiang University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 18 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 resources such as land and water are being rapidly degraded. Edible Madagascar has been facing political unrest, consequently putting insects, with their high feed conversion efficiency and fecundity, as the country into further economic distress and leaving almost 80% well as their minimal space for rearing, certainly represent as an of the population in poverty (Central Intelligence Agency 2014, advantageous solution for present and future food insecurity. UNICEF). Yet another tragedy is the recent locust plague of 2013. Even so, the ‘yuck’ or ‘disgust’ factor is not so easily elimi- As the infestation continues, more food crops and livestock grazing nated from today’s cultures. Despite its health benefits, perhaps lands could be destroyed, deepening on the suffering of the Malagasy the unappealing nature of entomophagy is in the consumption of people (FAO, 2009). With these outstanding issues, 53% of rural the whole insect. With that, the obscure incorporation of this food households have been reported to not consume enough food to source through the utilization of insect flours is considered. maintain an active and healthy life (UNICEF, 2001). Ongoing studies within our research group at California State Consisting mostly of rice, vegetables, and tubers, the Malagasy Polytechnic University, Pomona have demonstrated the feasibility of diet involves the consumption of these foods about 4 to 6 times a the obscure incorporation and fortification of a major food staple, week. Since rice is the product with the largest production quan- such as rice, by utilizing edible insect flour as a value-adding ingredi- tity, this is clearly reflected in their diet as it is also the number one ent. By removing the original form of the insect and incorporating its commodity available for consumption (FAO, 2014). Yet, proteins, flour into a food matrix that is widely consumed around the world, from both vegetables and animals, are seldom eaten, at an estimated we aim to provide an innovative solution for food insecurity and rate of 1 to 2 times a week (WFP and UNICEF, 2011). Fat, a major malnutrition, especially in developing countries. Furthermore, the source of calories, has also been demonstrated to be low in their hidden form of the edible insect is designed to reduce the ‘yuck’ fac- diets (FAO, 2010). Indeed, the main staple meal in Africa consists tor and increase the acceptance of entomophagy. Rice flour has been mainly of cereal grains, such as rice, sorghum, millet, maize, fonio, specifically chosen to be the vehicle based on the consideration that and tef (Filli et  al., 2014). These foods, being composed mostly of the nutrients carried by the edible insect will supplement the nutri- carbohydrates (rice 80%, sorghum 74%, and maize 78%), are not tional composition of rice. The two main ingredients are combined a major source of protein, and together with the scarce availability in different ratios to form a dough mass, which can be processed of animal protein, the Malagasy people lack the necessary macronu- through an economically feasible, cold-forming extrusion technol- trients for healthy living (Wu Leung, 1968). Moreover, the WFP and ogy. Through this production method, a final rice product containing UNICEF (2011) reports only 20% or less of the surveyed children to optimal addition level of insect flours has been developed, and the have received foods rich in vitamins and minerals, sources of which measurements of its physicochemical properties, nutrient profile, and include fruits and vegetables, legumes, nuts, and dairy products. consumer acceptability via sensory evaluations have been completed. Overall, 84% of households experience inadequate amounts of food While the measurements of organoleptic and nutritional properties or cash every year (WFP and UNICEF, 2011). of the insect rice product have been reported in a separate original Malnourishment occurring in early childhood and if untreated research article, published with the Journal of Insects as Food and results in life-threatening consequences. Chronic malnutrition will Feed (JIFF-S-17-00032) (Tao et  al., 2017), the results of consumer lead to irreversible stunting and has been reported to be the most acceptance study are summarized in this review article. important risk factor for illness and death from diseases (WFP, 2015; Muller et al., 2005). Approximately 150 million children worldwide do not consume the required amounts of energy or nutrients for Food Insecurity and Malnutrition growth and development, with more than half (52%) of these chil- dren residing in South Asia and almost a quarter (21%) living in Although not as widespread in the USA, food insecurity remains a Sub-Saharan Africa (UNICEF, 2001). serious and prevailing issue for much of the world. There is an esti- mated 805 million people who are without enough food to main- tain a healthy and active lifestyle, according to the World Food Nutrient Content of Edible Insects Programme (WFP, 2015). Developing countries, especially those in South Asia and Sub-Saharan Africa, have the highest rates of hun- Interestingly, although perhaps not surprisingly, entomophagy is ger. Although Asia contains the largest population of hungry peo- especially practised in developing nations. Countries in South Asia, ple, about two-thirds of the total, Africa has the highest prevalence where more than 40% of the population is chronically malnour- (WFP, 2015). ished, have already long accepted entomophagy as part of their While many developing countries are facing food insecurity culture. For instance, countries such as India and Lao People’s today, Madagascar, for example, is in an especially delicate state. Democratic Republic have identified 24 and 21 edible insect species, Madagascar is one of the 10 countries with the highest occurrences respectively. Collectively, Africa has been reported to have some 246 of chronic malnutrition (UNICEF, 2013). With at least 50% of the species of edible insects. Countries within this continent that exhibit population moderately or severely malnourished, food insecurity more severe rates of chronic malnutrition, such as Madagascar or remains a critical concern in this nation. In 2013 alone, 4 million Zambia, possess 22 to 33 species (Ramos-Elorduy et  al., 1997). people faced hunger as almost one-third of the population was bur- These insects are consumed for their comparable levels of energy dened with food insecurity (WFP and UNICEF, 2011). Causes of and nutrients, although the levels may vary depending on species their struggle are numerous and difficult to resolve. Deforestation type, metamorphic stage, habitat, and diet. For instance, a study con- by slashing and burning, a largely unsustainable agricultural pro- ducted in Thailand demonstrated that 100 g of insects (fresh weight) cess, has resulted in soil erosion and even rice field destruction (a had comparable, if not more, calories than that of equal weights of major staple) (UNICEF, 2001). The fragility of the environment has commonly eaten livestock, excluding pork (Sirimungkararat et  al., left very few farmers with enough land to cultivate (UNICEF, 2001). 2010). Ramos-Elorduy et al. (1997) reported that of 78 insect species Furthermore, as agriculture accounts for more than one-fourth of found in Mexico, the caloric content ranged 293–762 kJ per 100 g of the country’s GDP and 80% of employment, much of the population dry matter. Specifically, migratory locusts (Locusta migratoria), the has become vulnerable to food insecurity. In addition, since 2009, species of which are currently plaguing Madagascar, were discovered Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 19 to have calories varying in the range of 598–816 kJ per 100  g of underprivileged do turn to edible insects for sustenance since other fresh weight in a study conducted in the Netherlands (Oonincx and forms of livestock are either unavailable or expensive, the tradition van der Poel, 2011). Moreover, besides the caloric value, these ani- of consuming edible insects is not always a tactic for survival. Banjo mals can provide crucial macronutrients as well. and others (2006) reported edible insects being included in a planned Likewise to the evidence supporting the caloric value of edible diet throughout the year and not solely as an emergency food sup- insects, it also suggested that insects are considered to be a substan- ply. A  collective group of people in South Africa called Pedis, for tial source of protein. Certain insects found in China were reported instance, value insect meals, such as those derived from caterpillars, with higher protein contents than those in most plants and com- even more so than beef as the latter sales decrease during caterpillar mercial meat, fowl, and eggs (Xiaoming et al., 2010). In the study, harvesting seasons (Womeni et  al., 2009). Palm weevils, especially 11 orders of insects were analysed with results of protein contents the larvae form of R.  phoenicis, have been a part of a traditional ranging from a low 13% to a high 77% (dry weight basis). Other African diet for centuries and are, like the locusts there, prepared researchers reported a range of 37%–54% protein content in eight by frying (DeFoliart, 1993; Banjo et al., 2006). Besides Africa, this insects found in Thailand (Raksakantong et  al., 2010). In spite of insect has also been appreciated across other tropical regions includ- these variations in protein content, edible insects overall demon- ing Latin America and Asia (DeFoliart, 1993). In Mexico, investi- strate to be an exceptionally good source of protein. While this gators reported exceptional consumer acceptance for their maize macronutrient is often difficult to obtain in developing countries and flour tortillas supplemented with ground yellow mealworm larvae so is lacking from their daily diets, edible insects are relatively more (Tenebrio molitor) (Aguilar-Miranda et  al., 2002). The practice of available than other meats, demonstrating yet again its worth as a eating insects can also be found in the East. Lethocerus indicus, or solution for reducing global food insecurity. giant water bug, is a particularly popular insect consumed through- Furthermore, while malnutrition is not limited to protein defi- out several Asian countries such as Thailand, Laos, Vietnam, and ciencies but includes the overall lack of caloric intake, populations Cambodia (Kiatbenjakul et al., 2015). Its odour provides a flavour within developing countries could also benefit from energy dense profile that is essential for consumer acceptance of food products foods provided by edible insects (DeFoliart, 1992). Energy intake such as chili pastes or fish sauces. As entomophagy is practised can be greatly enhanced, to an extent, with higher levels of fat, like around the world, a novel edible insect product has certain potential those potentially found in edible insects. In a study lead by Womeni for being accepted and enjoyed. and others (2009), six insects from Cameroon of Sub-Saharan Africa were analysed to determine their lipid contents and essential fatty Nutritional Variability of Edible Insects acid profiles. Results showed that not only were these insects an excellent source of fat, ranging from 9.12% to 67.25% (dry weight However, it is important to note that while promising, edible insects basis), but also that they were rich in polyunsaturated fatty acids. are still highly variable between/within species and metamorphic These types of fats, along with monounsaturated fats, have been stages. When comparing the amount of energy found between edible widely accepted to offer more nutritional benefits and should be insects in previously cited studies, these values varied by hundreds used to replace the intake of saturated fatty acids (Yang et al., 2012; of calories per gram (Ramos-Elorduy et al., 1997; Oonincx and van Enos et  al., 2014). Furthermore, the polyunsaturated fats included der Poel, 2011). Protein content had differences as great as 64%, essential fatty acids, such as linoleic (omega-6) and linolenic (omega- whereas fat had variations as high as 44% (Womeni et  al., 2009; 3) acids (Womeni et  al., 2009). Comparable findings were demon- Raksakantong et  al., 2010; Xiaoming et  al., 2010). It could be strated in Thailand as well, varying between 0.34% and 23.98% of easily discerned from these values that the benefits of each edible total fat content depending on the species of insects (Raksakantong insect species can vary significantly. In addition, analogous to shell- et al., 2010). Thus, edible insects have the potential to be an excep- fish or prawns, the type of habitat and diet of these insects can also tional source for energy and macronutrients. change their flavour and even their nutritive values (Ramos-Elorduy Micronutrients, on the other hand, are just as essential for a et al., 1997; Klasing et al., 2000; Finke, 2003; Raksakantong et al., healthy life. A major concern for developing countries is iron intake 2010; Oonincx and van der Poel, 2011; Nowak et  al., 2016). As as its deficiency is the world’s most common and widespread nutri- grasshoppers (Zonocerus variegatus) in Nigeria were fed with bran, tional disorder (WHO, 2014). Many of the insects safe for con- which contains more fatty acids than that of corn, these insects sumption contain abundant levels of iron that often exceed other demonstrated almost doubled protein levels (Ademolu et al., 2010). commonly eaten animals. For instance, edible insects such as the In yet another study, migratory locusts were fed with three differ- popular palm weevils (Rhynchophorus phoenicis) or mopane cat- ent diets, consisting either solely of grass, mixed grass and wheat erpillars (Imbrasia belina), both species found in Africa, can pro- bran, or combination of grass, wheat bran, and carrots (Oonincx vide 12 and 31 mg of iron per 100 g of weight, respectively (Banjo and van der Poel, 2011). The investigators found the wheat bran et al., 2006). Chicken and beef, on the other hand, provide only 1.2 diets reduced the protein content and increased the fat content of and 3 mg of iron, respectively (Sirimungkararat et al., 2010). Zinc, the locusts, whereas the addition of carrots further enhanced the fat another mineral important for growth and development, can be gen- content and provided greater levels of β-carotene. Hence, although erally found in most insects. For example, it has been reported that entomophagy has been revealed with great potential to be an extra- the aforementioned palm weevil larvae contain 26.5 mg per 100 g ordinary resource for relieving global food insecurity and malnutri- (Bukkens, 2005). tion, it is essential to obtain complete nutritional profiles in order to determine the actual nourishment available in the finished product. Entomophagy—More Than Survival Environmental and Economic Impacts The overall nutritional value of edible insects presents them to be a remarkable alternative for alleviating the food insecurity and mal- While developing countries are currently facing the burden of food nutrition in developing countries. Although it could be said that the insecurity, the FAO (2009) predicts that the global population will Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 20 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 increase to 9 billion by 2050. As the world population proliferates, many declined touching those insects to their lips. The concept of the demand for food and feed will escalate along with it, subse- food neophobia, the fear of trying new or novel food products, has quently requiring food production to increase by 70% (FAO, 2009). been suggested as the reason for this rejection (Megido et al., 2014). With the current state of the environment, and as it continues to This concept is explained by Rozin and Fallon (1980) to be a dismis- degrade, there is a call to conserve natural resources such as land sal due to distaste for the organoleptic qualities, fear of danger to the and water. Evidently, rearing insects requires remarkably less land body, or disgust stemming from a prior impression of what the prod- than farming other categories of livestock. Oonincx and de Boer uct is or of its origin. While either of these three explanations or the (2012) discovered that to produce 1 kg of edible protein, mealworms combination thereof may be understandable, perhaps the neopho- (T.  molitor) required only 10% of the land that is needed for beef bia of entomophagy could be lifted. Lobster, once considered ‘junk’ production. Although this difference may not be as dramatic when food in the 17th and 18th centuries, was established to be cruel and compared with pork or chicken production, mealworm farming still unusual punishment for feeding to servants and prisoners more than requires 29%–50% less arable land. Due to their obvious smaller twice a week (Greenlaw, 2002; Crowley, 2015). Today, lobster is size, edible insects also have the potential to be farmed vertically, regarded as a fine dining food, depicted as a pleasure enjoyed by thereby requiring no additional land clearing to advance produc- consumers with high incomes. Another interesting example is the tion (van Huis et  al., 2013). Greenhouse gases, including carbon history of the ever popular sushi dish, the California roll. When first dioxide, methane, and nitrous oxide, are also produced at a lesser introduced in Los Angeles, Ichiro Mashita, the sushi chef of Tokyo rate by insects such as crickets (Acheta domesticus) and mealworms Kaikan, innovatively substituted the toro (fatty tuna) with avoca- (T. molitor). When compared with pigs and cattle, the difference is dos as it had a similar texture but was more familiar to Americans. by a factor of about 100 (Oonincx et al., 2010). Furthermore, the He also placed the nori inside the rice as this too was an unusual manure produced from common livestock also contaminates the sur- ingredient (Crowley, 2015). Presently, California rolls have become face and groundwater while releasing ammonia and acidifying the an icon of sushi and are enjoyed all across the globe. Whatever the land (van Huis et  al., 2013). Although pigs have demonstrated to cause of the prior neophobia, lobster and the California roll have produce ammonia at a rate of 10 times or greater than crickets and had their status momentously and positively changed. Edible insects mealworms, the quantity produced by cattle is undoubtedly even less have the same potential. Megido and others (2014) suggest that the favourable (Oonincx et al., 2010). promotion of knowledge and acceptance of edible insects will begin As land becomes scarce, the water supply is equally threatened. with the understanding of the relationship between insects and shell- The FAO (2013) predicts that by 2025, two-thirds of the world will fish, as they are simply arthropods of the land and sea, respectively. be under stress due to water shortages. When evaluated against Correspondingly, increasing the frequency of positive exposures and the quantity required to produce 1  kg of grain protein, 100 times tasting trials would also be effective. more water is required to produce the same weight of animal pro- tein, especially as water is necessary for forage and feed produc- Edible Insect Fortification in Rice Flour via tion (Chapagain and Hoekstra, 2003). Although assessments for Extrusion T echnology the quantity of water required for farming edible insect is currently unavailable, the results are likely in favourable directions, in parallel What is also proposed for increasing acceptability is the form of the with that of greenhouse gas and ammonia emissions. edible insect ingredient. While traditional cooking methods such as In addition to the heavy usage of land and water, farming live- roasting or frying are frequently used to prepare tastier or more pal- stock also requires feed, which in turn requires further land clear- atable dishes, the insects often remain whole, especially in tropical ing. Alternatively, insects are cold-blooded and so only require feed regions (van Huis et al., 2013). Instead, edible insects can be made for energy and warmth. Studies have shown that to produce 1  kg into granular or paste forms that may result in improved acceptabil- of livestock weight, at least 2.5  kg of feed is required for poultry ity. While in a paste or powder form, they can be incorporated into meat, 5 kg for pork, and 10 kg for beef (Smil, 2002). Edible insects, other foods. For instance, in Thailand and other South Asian coun- such as crickets (A. domesticus), require only 1.7 kg to produce the tries, ground giant water bugs (L. indicus) are an essential ingredient same weight (Collavo et al., 2005). In addition, only a percentage of in chili paste and fish sauces (Kiatbenjakul et  al., 2015). Although this livestock weight is edible, consequently reducing the actual pro- the chili paste is used as an ingredient in dishes, the current study duction and availability of meat protein and other nutrients. While suggests that the fortification of a main staple food could be more chicken and pork provide 55% of edible weight, beef only provides effective as the ultimate vehicle for delivering valuable nutrients 40% (Nakagaki and DeFoliart, 1991). Crickets (A. domesticus) con- offered by edible insects. versely offer 80% of its live weight for consumption, making its feed Rice is a staple food for more than half of the world’s popula- conversion efficiency exceptionally high. Furthermore, insects in gen- tion, especially in developing countries (IRIN, 2010; USDA, 2012). eral reproduce more rapidly and in greater quantities. For instance, It provides 20% of world’s dietary energy and supports the liveli- the same aforementioned cricket species can lay 1200–1500 eggs hood of more than 1 billion people (FAO, 2004; IRIN, 2010). It is within 30 days (Patton, 1978). Insects also reach their adult stages regularly consumed and composes a great portion of the diets in much quicker than their livestock counterparts and so are capable of both developing and developed countries. The overall percent of reproduction sooner. dietary energy supplied by rice for Asia, Africa, and South America has been reported to be about 30%, 10%, and 10%, respectively (FAO, 2004). Specifically, developing countries such as Bangladesh, Getting Over the ‘Yuck’ Factor Laos People’s Democratic Republic, and Indonesia have more than However, despite the undeniable benefits for consuming and rearing half of their dietary energy supplied by rice. Other than energy (363 edible insects, this does not deter from the ‘yuck’ or ‘disgust’ factor. calories/100 g), rice is also a good source of thiamin, riboflavin, nia- A study conducted by Rozin and others (1999) revealed that despite cin, and amino acids such as glutamic and aspartic acid (FAO, 2004). American students being willing to touch insects with their hands, While rice lacks lysine, edible insects such as caterpillars (Gynanisa Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 21 maja), grasshoppers (Ruspolia differens), and winged termites per 100 g, crickets can offer 125 kcals, 15 g protein, 6.3 g fat, 41 mg (Macrotermes falciger) can complement this essential amino acid iron, and 75 mg calcium as well as other benefits (Sirimungkararat (Siulapwa et al., 2014). et al., 2010). Crowley (2015) stated that crickets provide 15% more To obtain rice, the grain is milled to remove the outer husk and iron than spinach, two times more protein than beef, and equal bran layer. During this process, broken rice is produced and can be quantity of vitamin B12 as salmon. Locusts, while currently not as used to create rice flour. Our research group has conducted a study available as crickets in the market, are superior in nutrient density. to determine the feasibility of combining an edible insect flour ingre- They can offer 598–816 kcal, 13–28  g protein, and 8–20  mg iron dient with rice flour for the fortification of a staple food (Tao, 2016). per 100 g (Oonincx and van der Poel, 2011; van Huis et al., 2013). The successful results from this study would first extend the yield Inclusion of locust may also provide a solution to present or future of rice harvest and create an additional economic prospect for this infestations, as these insects often occur in swarms. Despite being milling byproduct (Qian and Zhang, 2013) and second improve the viewed as pests, locusts are popular as fried dishes in countries such acceptability of a nutrient dense ingredient such as edible insects for as Thailand and Madagascar. general consumers. Brown rice flour was used as the major bulk ingredient for the To create this fortified rice product, extrusion, a method that production of the extruded insect rice. In contrast to white rice flour, is growing in popularity especially in developing countries, was brown rice flour is more nutritious and also provides the colour employed. Extrusion is a continuous process that combines cooking, background to disguise the intrinsic dark colour from edible insects. mixing, shaping, and forming (Fellows, 2009). The process begins Brown rice flour offers an additional 18% protein, 48% dietary by the raw materials, typically in granular form, being fed into the fibre, 82% iron, and 67% zinc compared with its white colour coun- barrel where water is added to convert the dry ingredients to a semi- terpart (USDA, 2015—National Nutrient Database for Standard moist dough mass that is processed further. As the screw within the Reference, Release 27). In general, white rice is also inferior in its barrel kneads the mixture, it becomes plasticized with a desirable supply of vitamins and minerals when compared with brown rice. rheological property suitable for extrusion. The screw pushes the Formulation development began at a 5% (dry weight basis) add- dough mass out of the die holes where it expands and cools rap- ition level of insect flour in the extruded rice formulation and was idly, forming the shape set by the type of die plate used. This type of then increased to 10% and 15%. Concerns for the increasing add- technology can generate a remarkable number of products, ranging ition levels of edible insect ingredients included an intensified aroma from cereals, pasta, soup and beverage bases, hot dogs and sausages, and taste, which, although may be familiar in other dishes, is not processed cheese, and chewing gum (Fellows, 2009). currently associated with rice. Regardless, the protein fortification of Action towards promoting the application of extrusion tech- insect flour to a product such as brown rice was certainly advanta- nology has already been set forth. ExtruAfrica, an initiative of the geous. For instance, by referencing the certificate of analysis (COA) Center of Excellence in Advanced Manufacturing at the North-West provided by the vendor of the cricket flour, we predicted that a 15% University in South Africa, encourages the extrusion method through insect flour formulation would theoretically increase the protein conferences and training workshops. The first seminar was first content by 8.5–9 g of protein per 100 g of insect rice. Together with held in 2011 and continues on (ExtruAfrica, 2015). Filli and oth- the protein content originally in existence with brown rice flour (3 g ers (2014) suggest extrusion technology to be a key to adding value protein per 40 g serving), 100 g of the insect rice would provide an to agricultural commodities to reduce food insecurity in developing estimated 13.5–14.6  g of protein or 26%–29% of the daily value countries. Staple cereal grains, including rice, have yielded positive (DV) of protein. results. In fact, several investigators have already made considerable A preliminary study confirmed that there were no major differ - progress in creating products that incorporate indigenous materials ences observed from both the extrusion process and the physical and through extrusion applications (Filli et  al., 2014) while increasing organoleptic properties of the extruded rice particles when incorpo- nutrient density (Obatolu, 2002). Moreover, utilization of extrusion rating 5% cricket flour in the brown rice formulation; however, the technology will also offer potential employment and an improved incorporation of 10% and 15% resulted in apparent difficulty to livelihood for local citizens. the extrusion operation and observable differences in particle shape, size, and organoleptic properties. Therefore, the study later focused on the formulation development using higher addition levels (10% Consumer Acceptance of Insect Fortified, or 15%) of either cricket or locust flour. A total of four formulations Extruded Rice Product were developed: 10% cricket rice (10CR), 15% cricket (15CR), As detailed experimental design and laboratory measurements are 10% locust (10LR), and 15% locust (15LR). presented in a separate research article published  by Journal of To determine the acceptability of the insect rice product, a panel Insects as Food and Feed (JIFF-S-17-00032) (Tao et al., 2017), this of 120 untrained participants were recruited via convenience sam- review article will mainly report the outcomes from a consumer pling. Panelists were required to be without shellfish allergies, con- acceptability study. sumers of brown rice, and between the ages of 18–65 years old. It To make the extruded insect rice product, two edible insect flours was heavily stressed that those with shellfish allergies were unable to were chosen, derived from cricket and locust, respectively. Both partake in the study as an allergy to shellfish was likely to produce insects are enjoyed by many populations around the world. Crickets a similar reaction to land insects. It was also encouraged that the are commonly consumed in Thailand, where there are 20 000 regis- participants were either familiar with or enjoyed brown rice as this tered cricket farmers (van Huis et al., 2013; Dunkel 2015) as well was the base of the products. With the questionnaire being an affect- as other Asian countries such as Lao People’s Democratic Republic ive sensory test, it was essential that the panel be users of this prod- and Cambodia (van Huis et al., 2013). They are also making their uct. The age range of the participants was determined as a means way into the US market as they are appearing in commercially pro- to exclude minors and those with a higher risk of compromised duced products such as energy bars from Chapul (Colorado) and immune systems. Another prerequisite for participants was that they ‘Chirps’ (cricket chips) from Six Foods (Boston, MA). Nutritionally, were willing to consume edible insects. Thus, participants knew that Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 22 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 the products to be tasted contained such an ingredient. Although any further education at the time. For instance, there were no choices the ‘yuck’ factor remains a major issue in entomophagy, those who for completing a 2- or 4-year degree while currently in the work- unknowingly consumed edible insect products could become ser- place and not continuing any education. There was also no option iously distraught after learning what they’ve tasted. Hence, despite for those who were still in school but past their 4th year of college. the potential bias that may occur from having this information, it With that, there may be some inflation within the data for the groups was in the best interest of the participants that they were informed stating to be within their 1st–4th year in college (Figure 4). that the products contained edible insects. Perception of Entomophagy Sensory Panel Demographics Several inquiries pertaining to the concept of entomophagy were To profile the sensory panel, a demographics survey was included in asked in a separate survey within the questionnaire. These questions the questionnaire and the age, gender, ethnicity, and the highest level and their responses are displayed in Figures 5–8. As mentioned, two of education were asked (Figures 1–4). of the largest ethnicity groups within the sample population were With recruitment taking place on the university campus, it was Latinos and Asians. In Mexico, ‘escamoles’, or black ant larva, are no surprise that the majority of the panel was in their early 20s, fairly popular dishes and can cost $25 or more per plate (Aguilar- about 76% (Figure  1). Only 6% of the panel was 35  years old or Miranda et al., 2002; Premalatha et al., 2011). ‘Ahuahutle’ is a famed above. It was also found that the ratio of men-to-women panelists was almost 50:50, with only 10% more females to males (Figure 3). In a previous study conducted in Belgium, a similar ratio was found in their sensory evaluation with mealworms (T. molitor) and crickets (A. domesticus) (Megido et al., 2014). These similarities may suggest that either entomophobia or lack thereof holds no discrimination against gender, although this may require further analysis of the data to confirm this proposition. In terms of ethnicity, there were a greater number of Latinos and Asians, together making up almost 70% of the sample population (Figure 2), which may simply be reflective of the campus population. An issue, found only after surveys were con- ducted, was in the options available for the education-level question. There was no option for participants to identify themselves as per- sons who have graduated from their bachelors but were not pursuing Figure 3. Gender of sensory panel. Figure 1. Age of sensory panel. Figure 4. Education level of sensory panel. Figure 2. Ethnicity of sensory panel. Figure 5. Familiarity with entomophagy. Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 23 While entomophagy is unquestionably strong within Latin America, countries in Asia also share this tradition. The giant water bug, as aforementioned, is a prominent edible insect used in mul- tiple dishes for its unique flavour in Thailand and other South Asian countries (Sirimungkararat et al., 2010; van Huis et al., 2013; Kiatbenjakul et  al., 2015). While silkworms are farmed for silk production, their pupae are also prized delicacies in China, Japan, Thailand, and Vietnam (Sirimungkararat et  al., 2010; van Huis et al., 2013). In Korea, rice-field grasshoppers are consumed as side dishes or snacks (van Huis et al., 2013). Considering that about 70% of the participants were self-reported to have cultural or ethnical background from countries where entomophagy is such a widely practice custom, it seemed appropriate that at least these many par- Figure 6. Experience with entomophagy. ticipants were familiar with the practice of consuming edible insects (Figure  5). Furthermore, as the said countries are all regarded as developing nations, the data collected from the sensory evaluation study could be somewhat extrapolated to provide indications of con- sumer acceptance of such insect products in those countries within Latin American and Asia, although domestic Latin Americans and Asian Americans may practice unique dietary habits that are more or less different from the customs found in their mother nations. Thus, despite the present investigation being unable to reach those currently living in countries such as Mexico or Laos People’s Democratic Republic, the results could still offer some implications for such products being implemented in developing countries in the future, although these generalizations may be fairly limited. Figure 7. Future willingness to consume edible insects. Together, the 82% of panelists being familiar with entomophagy and the 73% of participants declaring a high probability of consum- ing edible insects in the future (Figure 7), which pointed towards a positive trend. In a separate study, Tuorila and others (1994) found a positive relationship between pleasurable first experiences with a novel food and the likelihood of future consumption. As more than 50% of the free-response comments included a statement of their enjoyment and/or support of the current study and its products, this certainly presents a progression towards the future applications of edible insects in the market, even in developed nations. Although it was required that participants be willing to consume edible insects to taste the samples, it cannot be completely assumed that the partici- pants would have chosen to eat edible insects after this experience. Figure 8. Future willingness to purchase edible insect products. This is clear within the 6% who reported that they probably would not or definitely would not consume edible insects in the future. This unwillingness could imply that there was some other incentive for their participation in this particular project. This could include some potential extra credit offered by their professors or even the peer pressure from friends and classmates. Even so, the majority of the participants were willing to con- sume edible insects in the future. While 73% reported positively in this inquiry, only 42% were able to say that they had con- sumed edible insects before their involvement in the current study (Figure 6). With more participants (58%) never having previously consumed edible insects, this is certainly a positive outcome of the study. It demonstrates the eagerness of a population to at least try edible insects. Even more dramatic are the findings from the Figure 9 Perception of edible insects in the diet. Belgium study by Megido and others (2014). In this particular sur- vey, the researchers found that although 46.6% of the participants Mexican caviar that is composed of some seven different species of reported some negative attitude towards entomophagy, an even Hemiptera (true bugs) (DeFoliart, 1992; Aguilar-Miranda et  al., greater number of respondents, 77%, were willing to consume 2002; van Huis et  al., 2013). A  perhaps even more famous food, edible insects. The novelty, and perhaps curiosity, of entomophagy especially in Oaxaca, Mexico, is ‘chapulines’, or grasshoppers, and is may be even more powerful than the ‘yuck’ factor. Progress is being consumed as street food (van Huis et al., 2013). This particular dish made towards the acceptance of entomophagy, much like sushi and can be found in many Mexican restaurants in the USA. lobster in the USA. Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 24 J. Tao and Y. O. Li, 2018, Vol. 2, No. 1 On the other hand, when taking into account the willingness to several panelists stated that consuming whole insects was a bit off- purchase edible insect products in the future, there seems to be some putting but suggested that if the flavour was suitable, they would be disparity. Although people stated that they would probably and def- more likely to enjoy the product. This comment about flavour being initely consume edible insects in the future, the results from Figure 8 able to better allow the acceptance of a product was also reflected show that they may not actually purchase these insect products. It in the actual sensory evaluation on four attributes including colour, is proposed that this is somewhat correlated with the fact that the aroma, taste (flavour), and texture (mouthfeel), as presented with majority of the panel is college students with limited finances, where more details in the separate article published by Journal of Insects as money is only spent on items that are absolutely essential or worth Food and Feed (Tao et al., 2017). the expense. As mentioned in the free response portions of the ques- tionnaire, knowing of the nutritional and environmental benefits of Summary of Sensory Evaluation consuming and farming edible insects would likely provide enough Besides the four attributes being considered by the panelists based on information for these consumers to make a decision towards pur- a 5-point ‘Just About Right’ (JAR) scale, participants were also asked chasing edible insect products in the future. to rank the four insect rice formulations on overall liking based on a An inquiry pertaining to the opinion of how edible insects should 7-point hedonic scale from 1 = dislike extremely to 7 = like extremely. be placed in the diet was also included in the survey. Participants Among the four sensory attributes, colour and aroma were not the were asked to select as many choices as they felt that described their key factors blocking participants’ acceptance of the insect rice prod- opinions. Perceptions of edible insects in the diet are displayed by ucts, whereas flavour (taste) and texture (mouthfeel) were significant the percentage of the sensory panel who selected those choices. This in differentiating the panel’s overall liking between two insect flours particular survey question had multiple selections and participants (cricket vs. locust) and two addition levels (10% vs. 15%) employed were asked to select all that applied (Figure 9). in the rice formulations. Of the flour insect rice formulations, lower When considering the marketing of edible insect products, the insect formulations, e.g. 10CR and 10LR, were observed to be more results from Figure  9 suggested that edible insects are most often parallel to market brown rice in flavour and mouthfeel, whereas the preferred to be consumed as a snack (22%), appetizer (19%), and rice products made with cricket flour (10CR and 15CR) were more side dish (19%). Edible insects being perceived most as a snack could preferred over those made with locust flour (10LR and 15LR) in be related to their small sizes or, in general, that snacking is on the all sensory attributes, except the colour. This is because locust flour rise. In fact, in 2014, the number of in-between snacks increased to featured a ‘golden brown’ colour shade to the rice products, whereas 2.8 with more than half of adults consuming three or more snacks the incorporation of cricket flour resulted in some ‘greyness’ to the per day (Wyatt, 2014). In a previous study, although ‘snack’ was not extruded rice particles. included as an option in the survey, edible insects were primarily Even so, flavour remained an important component to the distinguished as an appetizer. Investigators suggest that this also be acceptability of the insect products as several participants mentioned due to the small size and original form of the food (Megido et al., that a suitable flavour could positively sway the overall opinion of 2014). With edible insects being perceived as fourth as a main entrée a product. Multiple criticisms made by the panel recommended that (17%) in the current research, this implies that this source of protein the acceptability of the products would be greatly improved if served is primarily viewed as only supplementary and not yet as a main alongside other foods or seasoned, such as with salt or soy sauce. As source of meat, such as those from beef or chicken. Edible insects aforementioned, the study conducted by Megido and others (2014) were even less identified as a main entrée if it were left in its whole involving sensory evaluation on mealworms (T. molitor) and crickets form and as a dessert. While people generally do not consume their (A.  domesticus), where these insects were prepared in a variety of meat as whole animals, this is no surprise to be the same for insects. ways including baked, boiled, a crushed mix of both insects, meal- Even with shellfish, such as with shrimp, many consumers may pre- worms flavoured with vanilla, and mealworms with chocolate. It was fer to have the head removed before consuming. Moreover, as edible found that the most accepted form of preparation was with choc- insects are not particularly sweet, it is unlikely that edible insects olate, followed by flavoured with paprika, and then baked. Although would be perceived as dessert unless people were familiar with the each mealworm was crispy in texture, the investigators advocate the chocolate-covered insects or insect lollipops already available on the flavour to be the factor in preference (Megido et al., 2014). market. Even so, comparing these results with the response pertain- By being a rice product, these insect formulations do have the ing to the panels’ personal accounts with entomophagy, it was also advantage of being versatile in their formulation and preparation. derived that a few previous experiences with edible insect candies Indeed, one of the research assistants in our group took it upon him- were not positive ones. With these negative experiences, it seemed self to create a kimchi fried insect rice dish that was very much well appropriate that the ‘dessert’ option was not as highly selected even received by the other investigators in the group. While this sensory with the familiarity of edible insects as candies. evaluation reveals some introductory indication of how this product As mentioned, personal accounts of entomophagy were included would be fairly accepted in a developed country, such as the USA, as a free response question in the survey (Tao, 2016). A total of 50 the insect rice has the potential of being further developed to include people out of the 120 panelists provided their own encounters with flavours from herbs, spices, etc. Another potential ingredient afore- edible insects. Of these experiences, there were an unanticipated mentioned is the introduction of cocoa powder. Relating the col- number of accounts where the insect was intact. These foods were our observed in 10LR, which was with a toasted brown hue, many mostly roasted, fried, or seasoned products and were implied to be participants expected it to be much more flavourful than actually consumed as snacks, appetizers, or side dishes. About 20% of the experienced. In utilizing cocoa powder, and presenting the succeed- experiences were either in Mexico or in Mexican restaurants and ing outcome as a chocolate product, this could reduce the misleading involved grasshoppers. However, an overwhelming majority of the nature of the brown colour derived from the locust flour. Besides experiences was with crickets (86%) and was followed by worms some colour matching/masking, the cocoa powder may provide (i.e. such as mealworms, maggots, or silkworms) being the second some improved flavouring as a chocolate ingredient. The possibility most consumed insect (32%). While some enjoyed their experiences, Downloaded from https://academic.oup.com/fqs/article-abstract/2/1/17/4911878 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Edible Insects for Malnutrition, 2018, Vol. 2, No. 1 25 for the research and development of this insect rice into a marketable References product is seemingly boundless. Ademolu, K. O., Idowu, A. B., Olatunde, G. O. (2010). Nutritional value assessment of variegated grasshopper, Zonocerus variegatus (L.) (Acridoidea: Pygomorphidae), during post-embryonic development. Conclusion African Entomology, 18: 360–364. Aguilar-Miranda, E. 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