A Review of Zophobas Morio: Chemical, Nutritional and Functional

39 A review of Zophobas morio: chemical, “ nutritional and functional characteristics

Rhaissa Coelho Andrade UFBA

Janaína de Carvalho Alves UFBA

Mariana Nougalli Roselino UFBA

10.37885/210203200 ABSTRACT

With the increase in population and the growing demand for protein, new food alternatives with less environmental impacts are being studied, such as edible insects. The objective was to carry out an integrative bibliographic review regarding the chemical, nutritional and functional characteristics of the insect Zophobas morio. For this, the descriptors were used: Zophobas morio, nutritional composition, chemical composition, functional food, probiotics and Lactobacillus to search five databases (Pubmed, Web of Science, Scopus, Capes and SciElo), which after reading and selection, resulted in 11 articles. This reduced number of articles is due to the fact that, even today, this species of insect is little studied. In this review, it was possible to condense the main results described in the literature regarding the dry matter, crude protein, fat, oleic acid, ash, iron and calcium parameters of Zophobas morio. Among these results, attention is drawn to the protein content of the insect, since studies have shown that comparing it to other food sources, such as meat, it is noted that the insect flour is quite superior, having about 45g of protein for every 100g of flour. The values found for lipids were between 14.25 and 43.64g / 100g. In the case of iron content, the values found were from 1.65mg to 9.15mg / 100g. For calcium, the content remained between 17.7mg and 60mg / 100g. Thus, flour from the insect Zophobas morio can be a potential sustainable food source, alone or associated with other foods.

Palavras-chave: Zophobas Morio, Nutritional Composition, Mealworm, Entomology.

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 534 INTRODUCTION

The high population growth has required more livestock systems to satisfy this great demand, however the available areas are limited. Furthermore, these systems cause se- rious environmental problems such as deforestation, soil erosion, desertification, impacts on biodiversity and water pollution, going in the opposite direction to sustainability (VAN HUIS; OONINCX, 2017). According to data from Embrapa, in 2018, about 30.2% of the total areas of Brazil are reserved for use by farmers. Considering the size of the country, a large portion of it is destined to economic activities of soil degradation, which directly impact the environment and tend to grow, according to the population increase already foreseen (EMBRAPA TERRITORIAL, 2020). An interesting alternative that can mitigate this process is the adoption of alternative sources of proteins, such as edible insects. There are more than 2000 species of edible insects (JONGEMA, 2015), consumed in more than 100 countries and predominantly in Africa, Asia and Latin America (DURST et al., 2010). Despite facing great cultural barriers, mainly in westernized societies, many of these insects are sources of proteins, fats and minerals, besides to bringing less environmental impacts, since they emit considerably less greenhouse gases and do not necessarily require terrestrial activities with impact on the soil (VAN HUIS et al., 2013). Studies that provide nutritional information about the types of insects that are viable for consumption are still scarce, such as Zophobas morio. This species belongs to the order Coleptera, which includes beetles, being, in the case of this species, known as dark beetles (KULMA et al., 2020). The first data on nutritional composition of Zophobas morio were presented by Barker et al. (1998), later other researchers also dedicated themselves to the study of this insect (KULMA et al., 2020; KUNTADI; ADALINA; MAHARANI, 2018; SOARES ARAÚJO et al., 2019). Thus, the objective of this work was to carry out a bibliographic review regarding the nutritional, chemical and functional characteristics of the edible insect Zophobas morio. As well as discussing the environmental implications and future perspectives on the consumption of this and other insects in isolation and/or associated with probiotic microorganisms.

METHODS

This study is an integrative review based on scientific articles rescued between September and October 2020, in the databases – PubMed, SciElo, Scopus, Web of Science and Capes periodic. The search strategy was made from the combination of descriptors: “Zophobas morio”, “giant mealworm larvae”, “larva de lagarta gigante”, “food”, “alimento”,

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 Avanços em Ciência e Tecnologia de Alimentos - Volume 3 534 535 “functional”, “functional”, “nutritional composition”, “composição nutricional”, “chemical composition”, “composição química”, “probiotic”, “probióticos”, “Lactobacillus”, “lactobacilos”. Articles published between 1998 and 2020 were selected. In addition, as an inclusion criterion articles in the English and Portuguese languages, original, and related to the insect Zophobas morio were considered. Articles not found in full, cases of duplicity, review articles, dissertations, theses or even cases where the study did not present data regarding the insect Zophobas morio were excluded. After the search, the titles and summary of each reference were read, where some articles have already been discarded. Subsequently, the full articles were read for evaluation. With a detailed reading of the texts, it was possible to identify the relevance of the studies, hypotheses or objectives, and according to the pre-established criteria, a total of 11 articles were included. Then, critical analyzes of the studies and records were performed, collecting information considered relevant. Details regarding these described steps are presented in the flowchart of Figure 1.

Figure 1. Flowchart for selecting articles

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 536 RESULTS AND DISCUSSION

Implications of insect consumption as a food alternative

The practice of eating insects is known as entomophagy and has been widespread for millennia, although it is still taboo in many westernized societies. Insects are rich in proteins, good fats, calcium, iron, and in addition, the creation of these, emits considerably less greenhouse gases when compared to most traditional herds, this aspect has positive environmental repercussions, thus, it becomes a viable option to complement food and alleviate problems related to malnutrition (VAN HUIS, 2013). According to the World Health Organization (WHO), millions of people started to compo- se the group of chronic malnourished in the last 5 years, and the countries around the world continue to struggle with multiple forms of malnutrition. Asia remains the continent with the largest number of malnourished people (381 million), followed by Africa, Latin America, and the Caribbean region (FAO, IFAD, UNICEF, WFP and WHO, 2019). Data from Brazilian Institute of Geography and Statics (IBGE) estimate that of the 68,9 million permanent private households in Brazil, 36,7% are experiencing some type of food insecurity. Of this, about 3,1 million are in a situation of severe food insecurity, which is the most severe form of low household access to food, this number being more expressive in rural areas. In the case of the Northeast, severe food insecurity affects 7,1% of households (IBGE, 2020). Take these data into account, it is worth mentioning that, in the majority, the articles evaluated in this study, brought similar approaches regarding the malnutrition of the population and, as the use of alternative foods, for example insects, are a way of work around or mitigate this problem, which, unfortunately, is quite common. A survey carried out by Department of Entomology at the University of Wageningen, in the Netherlands, showed that there are more than 2000 species of insects with potential of human consumption, including the beetles (Coleoptera), caterpillars (Lepidoptera), bees, wasps and ants (Hymenoptera), grasshoppers and crickets (Orthoptera) (JONGEMA, 2015). However, in most western countries, the entomophagy is associated with repulsion and primitive behavior. These insects are often eaten whole, but they also be processed and incorporated in other types of food (VAN HUIS,2013). In 2015, a supermarket chain, also in Netherlands, sold hamburgers and nuggets (produced by Belgian company) that contained about 16% of Lesser mealworm flour, which increases the acceptability of eating edible insects (VAN HUIS, 2016). In addition, there are some cookbooks that teach recipes using insects from all over the world (RAMOS-ELORDUY, 1998) and also available (VAN HUIS, GURP, DICKE, 2014),

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 Avanços em Ciência e Tecnologia de Alimentos - Volume 3 536 537 allowing the population to learn about the use of these insects in the preparation of food and there may be incentives for their consumption. According to what is observed in the literature, to nutritionally analyze these insects, one must observe the entire environment in which they are inserted, because there are influential factors such as: type of feed offered, stage of development, sex, diet, and climatic conditions (OONINCX; DIERENFELD, 2012). Insects can be harvested from the wild or raised in designated areas, usually farms, in which living condition, diet and food quality are controlled. In addition to the feed, leftover vegetables, rice, flowers, and grass are used to feed them. After creation, the insects are slaughtered by freeze-drying, drying in the sun and boiling, in addition to being able to be fried while still alive and eaten (VAN HUIS et al., 2013).

Zophobas morio

The species Zophobas morio belongs to the order Coleptera, which includes beetles, which, in the case of this species, are known as dark beetles (KULMA et al., 2020). Besides to the beetle phase, this insect has the larval phase, which is the most used for analysis. Regarding this species, there are still no data regarding its origin, climatic adaptation and places of greater human consumption. As it is a relatively new subject in the scientific field, in which the analysis of specific insects is still poorly studied, the low number of selected articles that contemplate the analysis of this insect is justified. However, data on nutritional composition compared to other species of edible insects are quite relevant, besides to findings that relate results of supplementation in the diet of these insects (LATNEY et al., 2017) and also comparative in relation to environmental impacts when compared to other types of food traditionally consumed (MIGLIETTA et al., 2015).

Nutritional composition of Zophobas morio

Barker et al. (1998) and Finke (2002) were pioneers in the analysis of the chemical and nutritional composition of the insect Zophobas morio, however, the results presented by them, in all parameters, are very different from other studies included in the review. As a comparison, while more recent studies show an average of 49.7g / 100g for protein, Finke (2002) showed a protein value of 19.7g / 100g. As this is the first published study, the authors have not shown any corroboration with the literature or possible implications regarding these results. It is known that there are many factors that can interfere with the nutritional composition of insects, however, these researchers also did not present much information about them, as well as about the methodologies used in the analyzes.

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 538 Thus, in the table below, the main results found in the literature will be presented, ob- serving values of dry matter, crude protein, fat, ash, oleic acid, iron and calcium of the insect Zophobas morio. In addition, still in Table 1, the other species of insects that were also studied by the referred researchers have been listed.

Table 1. Nutritional composition of the Zophobas morio according to studies.

Development Dry matter Crude *Oleic Other species analyzed Authors Fat Ash Fe Ca stage (DM) protein acid in the study Adámková et 46 ± 1.0 35 ± 0.1 Tenebrio molitor; Gryllus Larval - - 35.7 ± 0.3 - - al. (2017) (g/100g) (g/100g) assimilis Gryllus sp.; Tenebrio Kuntandi, Ada- 49.96 28.98 3.41 3.19 24.82 molitor; Bombyx mori; lina, Maharani. Larval - - (g/100g) (g/100g) (g/100g) (mg/100g) (mg/100g) Valanga nigricornis; (2018) Nomadacris succincta Kulma et al. 43.9 ± 3.0 48.1 ± 0.6 34 ± 1.8 0.7 ± 0.1 Larval 27.75 ± 0.90 - - Blaberus craniifer (2020) (g/100g) (g/100g) (g/100g) (g/100g)

31.94 ± Soares Araújo 35.42 46.80 ± 1.78 43.64 ± 0.47 8.17 ± 0.06 2.27 ± 0.2 Larval 38.00 ± 0.06 5.48 Gryllus assimilis et al. (2019) (g/100g) (g/100g) (g/100g) (g/100g) (mg/100g) (mg/100g)

Mlček et al. 47.9±0.6 39.4±0.1 39.1±0.4 Larval - 32.4±0.01 - - Tenebrio molitor (2019) (g/100g) (g/100g) (g/100g)

Blatta lateralis; Eubla- berus distanti; Grom- Oonincx and phadorhina portentosa; 38.21±1.61 68.05±0.62 14.25±1.15 6.16±1.85 9.15±0.79 60.00±0.01 Dierenfeld, Beetle - Drosophila melano- (g/100g) (g/100g) (g/100g) (g/100g) (mg/100g) (mg/100g) (2012) gaster; Microcentrum rhombifolium; Tenebrio molitor; Porcellio scaber

*(% of total fatty acids)

Dry matter

The determination of dry matter is the starting point for food analysis, since the conser- vation of the product may depend on the moisture content present in the material. Moisture is eliminated from the sample by drying in an oven with forced air circulation and temperatures above 100ºC. After this process, gravimetric determination is made with the residue remaining after drying (SILVA and QUEIROZ, 2002). Although some articles do not bring a quantity of dry matter for each 100g of the insect, all analyzes of the studies were made from the analysis of the dry matter of Zophobas morio, since, when comparing the nutritional value, it is necessary to take into consideration the respective dry matter contents (SILVA and QUEIROZ, 2002).

Proteins

The main protein sources most consumed are meat, eggs, fish and dairy products, having predominant role in this sector. With rapid population growth in the developing world, there has

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 Avanços em Ciência e Tecnologia de Alimentos - Volume 3 538 539 been a growing increase in animal protein demands in recent decades (BOLAND et al., 2013). Consequently, the environmental damage intensifies, since it is necessary to use land to rase these animals, occupying and degrading vast agricultural areas (STEINFELD et al., 2006). In this context, alternative protein sources are inserted, such as edible insects, which can be produced with less environmental impacts and provide satisfactory protein quantities (VAN HUIS, 2015). A recent study compared the protein content of conventional animal sources with that of insects and found that the protein content of the species analyzed (Zophobas morio e Gryllus assimilis) are higher than that of chicken, beef, pork and fish (SOARES ARAÚJO et al., 2019). In addition, another positive aspect concerns the high digestibility of proteins from insects, varying from 77 to 98% (RAMOS-ELORDUY et al., 1997). It is important to analyze this parameter, since it represents the percentage of proteins that are hydrolyzed by protea- ses and actually absorbed by the body in the form of amino acids or any other nitrogenous compound (PIRES et al., 2006). Noteworthy is the result obtained by researchers Oonincx, Dierenfeld (2012), who rea- ched the highest value (68,05g/100g) for crude protein. The insects used in this study were still in the beetle phase, with this, it is understood that the higher crude protein content found may be related to the higher degree of sclerotization, which could negatively influence protein digestibility (FINKE, 2007), since, in the other studies, in which the insects were in the larval phase, the values of crude protein remained between 39.4 to 49.96g/100g. Therefore, based on this result, it can be inferred that, about protein content, the consumption of Zophobas morio should be carried out even in its larval period, given its superiority when related to the beetle phase, since this would negatively impact its digestibility.

Fat

Lipid content is the second most commonly found nutritional component in insects, right after proteins (KUNTADI; ADALINA; MAHARANI, 2018). Besides to providing energy for the body, lipids act as precursors to some types of fat-soluble vitamins and essential fatty acids, and are also important for the sensory characteristics of food (PAUL et al., 2017). Regarding the results found for lipids, it is noted that the study by Oonicx and Dierenfeld (2012) presented the lowest value for this parameter 14.25g / 100g, while the others were between 28.98 to 43.64g / 100g. It is known that as well as for protein, the life stage in which the insect is found (larva or beetle) is a major factor for the analysis of these data (OONINCX; DIERENFELD, 2012) thus, the low values found may be justified this aspect, since the insects used by Oonincx and Dierenfeld (2012) were in the beetle phase.

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 540 It is also important to analyze the proportion of fatty acids in the samples, generally classified as saturated (SFA), monounsaturated (MUFA) and polyunsaturated (PUFA), which makes it possible to assess the quality of the lipids, as shown in Table 2 (KULMA et al., 2020).

Table 2. Fatty acid composition in Zophobas morio (% of total fatty acids).

Authors SFA MUFA PUFA

Kulma et al. (2020) 47.52 ± 1.46 30.79 ± 1.29 21.69 ± 0.21

Soares Araújo et al. (2019) 41.05 42.35 15.7

Mlček et al. (2019) 43 33 24

According to Rumpold and Schi (2013), the fatty acid content in most insects is predominantly composed of unsaturated fatty acids, being the group of PUFAs important for the reduction of cholesterol levels in the body (BINKOSKI et al., 2005). However, in recent studies comparing the percentage of total fatty acids in Zophobas morio with other species, it was noted that the content of saturated fat is considerably higher than that of polyunsaturated fat and relatively equivalent to the content of monounsaturated fat (MLČEK et al., 2019) (SOARES ARAÚJO et al., 2019).

Oleic acid

Figure 2: Description of the Chemical Structure of Oleic Acid.

National Center for Biotechnology Information. PubChem Compound Summary for CID 445639, Oleic acid. https://pubchem.ncbi.nlm.nih.gov/compound/Oleic-acid. Accessed Jan. 11, 2021.

Among the articles analyzed in this study (Table 1), in relation to the fatty acid profile observed in the species, oleic acid is the one with the highest percentage among the total fatty acids. This acid has a double bond between carbons 9 and 10 (Figure 2), and is therefore classified as a monounsaturated fatty acid (MOREIRA; CURI; MANCINI-FILHO, 2002). Regarding the percentage of this acid in the studies, the values did not vary as much, remaining between 27.75 to 39.1% of the total fatty acids. The differences between the cited nutritional values may be due to different conditions of rearing and feeding of these insects (MLČEK et al., 2019) since all studies used gas chromatography with flame ionization de- tector for the analysis.

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 Avanços em Ciência e Tecnologia de Alimentos - Volume 3 540 541 Olive oil is an example of a traditionally used food that has a high content of monounsaturated fatty acids, especially oleic, and studies relate the presence of these acids and may be relevant in reducing cardiovascular events, including myocardial infarction and stroke (NOCELLA et al., 2017). Thus, although oleic acid, or omega 9, can be synthesized by the body, the increase in foods rich in this acid in the daily diet can be an interesting alternative.

Extraction of fatty acids

In their study, Ramos-Bueno et al. (2016) analyzed several species of edible insects, including Zophobas morio, in relation to the fatty acid profiles of these insects. The lipids were extracted by ethanol in a degree similar to that of other organic products tested solvents, while the direct methylation of the biomass provided the highest yields. As a result, Zophobas morio showed high percentages of monounsaturated fatty acids, confirming the other data found, in addition to showing high proportions of medium chain fatty acids (RAMOS-BUENO et al., 2016). The extracted fats can be used in the food industry, with applications similar to coconut oil, as confectionery fat, particularly in the preparation of ice cream, in imitation of choco- late and coconut in place of cocoa butter, in industrial soaps, pharmaceuticals, cosmetics, plastics, rubber substitutes, synthetic resins, as well as for obtaining biodiesel (RAMOS- BUENO et al., 2016).

Iron (Fe)

Among other minerals, iron is an inorganic component that makes up the ash content of insects. It is an essential element for almost all living organisms, and participates in several metabolic processes, which include oxygen transport, deoxyribonucleic acid (DNA) synthesis and electron transport. Disorders related to iron metabolism are among the most common diseases in humans, from anemia to iron overload, and possibly degenerative diseases (ABBASPOUR; HURRELL; KELISHADI, 2014). Therefore, it is important that there is control and monitoring of iron levels to maintain a healthy body. According to the Recommended Dietary Intake (RDA), for men over 19 years of age, a daily intake of 8mg/day of Fe is recommended, whereas for women, at the same age, this recommendation rises to 18mg/day of Fe, due to menstruation and other metabolic factors (PADOVANI et al., 2006). Analyzing Table 1, the iron content for 100g of dry matter of the insect Zophobas morio varied from 1.65 to 9.19mg, values significantly higher when compared to the same amount of fresh weight of pork and chicken, 0.83 and 0.76mg / 100g respectively, as shown in Table

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 542 3 (SOARES ARAÚJO et al., 2019). Thus, it is possible to say that the insect’s studied flour may be a potential source of iron.

Table 3.Content of calcium and iron of insect Zophobas morio, expressed as mg/100g dry matter, compared to beef, pork and chicken to fresh weight.

Zophobas Mineral Beef Pork Chicken morio

Iron 2.27 ± 0.2 3.31 0.89 0.76

Calcium 31.94 ± 5.48 5.43 5.87 5.23

Adapted from Soares Araújo et al., 2019.

It is observed that in the study by Oonincx and Dierenfeld (2012), the iron content was distanced from the others, being around 9.19mg / 100g, while in the other studies this value did not exceed the 3.19mg / 100g range. In another study by Oonincx and Van der Poel, (2010) analyzing migratory Locusta, the authors observed that adult insects had higher con- centrations of iron than in previous stages of development. Thus, the use of the beetle phase of the insect Zophobas morio may also have provided higher iron values, since the other studies used the larval phase of the insect for the analyzes.

Calcium (Ca)

Calcium is an important mineral for maintaining bone health and density, in addition to being essential for the normal functioning of nerves and muscles (SOETAN; OLAIYA; OYEWOLE, 2010). According to the Reference Dietary Intake (DRI), the values of Adequate Intake (AI) of Calcium for men and women aged 19 to 50 years is 1000mg/day (PADOVANI et al., 2006). As noted in Table 1, the calcium content values varied widely, ranging from 24.82 to 60mg / 100g, setting low values for the content of this micronutrient. However, these are expected values, since insects are generally poor sources of calcium (LATNEY; CLAYTON, 2014). Despite the low calcium values, shown in Table 1, when the reference rates are analyzed, these values are higher than those found in traditional foods, as shown in Table 3.

Feed conversion and footprint

Insects, for being poikilothermic, do not use metabolic energy to keep their body tem- perature constant, and can invest more energy in growth and reproduction, which results in greater efficiency of feed conversion(VAN BROEKHOVEN et al., 2015). This aspect translates into a lower need for food and water, so that insects present themselves as good food sources when compared to pork, beef and chicken, bringing less environmental impacts (MIGLIETTA et al., 2015).

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 Avanços em Ciência e Tecnologia de Alimentos - Volume 3 542 543 In addition, the edible portion of the insects is considered 100% since the entire animal can be consumed, unlike the other types of food that require specific treatments and cuts for consumption, wasting parts of the food (MIGLIETTA et al., 2015). The study by Miglietta et al. (2015) who analyzed the insect Zophobas morio, pointed out that the water footprint, which corresponds to the volume of fresh water spent per gram of protein, is much smaller in insect larvae than in other foods, as shown in Table 4.

Table 4.The water footprint of food products from animal origin in terms of protein value.

Water Footprint per Unit of Food item Nutritional Value (L/g Protein) Mealworms 23 Pig meat 57

Chicken meat 34

Beef 112 Adapted from Migletta et al., 2015. Analyzing the table, it is noted that beef uses about 5 times more water to produce the same amount of protein that insects can produce, followed by pork and chicken. Thus, in addition to nutritional issues, it is important to note the environmental impact caused by the traditional types of food consumed by the population

Futures perspectives

Food, moreover to being indispensable for growth, reproduction and human health, can also modulate as symbiotic microbial communities present in the digestive tract. The type, quality and origin of foods impact microbe-host interactions, affecting the composition and function of these microbes (MAKKI et al., 2018). Lactobacillus bacteria are examples that make this interaction, being important components of the human microbiota and are present in the respiratory, gastrointestinal and genital tracts, in addition to their strains are used commercially in the production of fermented foods (O’CALLAGHAN; O’TOOLE, 2013). Although no studies have yet been found that analyze the interaction of insect flour with Lactobacillus, some other studies have already demonstrated this possibility. As is the case with the work of Khempaka et al. (2011), who carried out experiments to evaluate the effects of shrimp flour on intestinal microbial populations in broilers, resulting in an increase in the population of Lactobacillus and a decrease in intestinal Escherichia coli and Salmonella cecal (KHEMPAKA; CHITSATCHAPONG; MOLEE, 2011) which opens up possibilities for further studies and research in this area, with other types of flour and hosts. These experiments can also be developed in the laboratory from the plating of bacteria and subsequent supplementation with desired material to analyze whether or not there is an increase in the viability of bacterial cultures. An example of this process was studied by

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 544 Collins et al. (2018), using prebiotics to evaluate the development of Lactobacillus cultures for the maintenance of the vaginal microbiota (COLLINS et al., 2018).

FINAL CONSIDERATIONS

It can be concluded that insects, specifically the species Zophobas morio, have great nutritional potential, in view of their nutritional qualities. However, it is necessary to be aware that some factors such as stage of development, diet and environment can influence their nutritional composition, and therefore they must be considered during cultivation and consumption. Besides that, even today, there are many cultural barriers related to the consumption of insects or alternative food sources, making it necessary means that either through processing or insertion into other foods promote increased acceptance by the consumer. With regard to the environmental impacts for the production of this type of food, they are much smaller when compared to other traditional foods, which brings better future perspectives when thinking about sustainability. It is also important that there is the development of research that studies the interaction of insect flour with microorganisms beneficial to human health, analyzing the -in crease or not of their viability, in order to enable improvements in the microbe-host rela- tionship when necessary.

FINANCING

This project was financed by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) from the program PROPCI/UFBA 01/2020 – PIBIC.

REFERÊNCIAS

1. ABBASPOUR, N.; HURRELL, R.; KELISHADI, R. Review on iron and its importance for human health. Journal of research in medical sciences: the official journal of Isfahan University of Medical Sciences, v. 19, n. 2, p. 164, 2014.

2. ADÁMKOVÁ, A. et al. Nutritional potential of selected insect species reared on the island of Sumatra. International Journal of Environmental Research and Public Health, v. 14, n. 5, p. 521, 2017.

3. BARKER, D.; FITZPATRICK, M. P.; DIERENFELD, E. S. Nutrient composition of selected whole invertebrates. Zoo Biology, v. 17, n. 2, p. 123–134, 1 jan. 1998.

4. BINKOSKI, A. E. et al. Balance of unsaturated fatty acids is important to a cholesterol-lowering diet: Comparison of mid-oleic sunflower oil and olive oil on cardiovascular disease risk factors. Journal of the American Dietetic Association, v. 105, n. 7, p. 1080–1086, jul. 2005.

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 Avanços em Ciência e Tecnologia de Alimentos - Volume 3 544 545 5. BOLAND, M. J. et al. The future supply of animal-derived protein for human consumption. Trends in Food Science and Technology, v. 29, n. 1, p. 62–73, 2013.

6. COLLINS, S. L. et al. Promising prebiotic candidate established by evaluation of lactitol, lactulo- se, raffinose, and oligofructose for maintenance of a Lactobacillus-dominated vaginal microbiota. Applied and Environmental Microbiology, v. 84, n. 5, 1 mar. 2018.

7. DURST, P. B. et al. Forest insects as food: humans bite back. RAP publication, 2010. EMBRA- PA TERRITORIAL. Agricultura e preservação ambiental: uma análise do cadastro ambiental rural. Campinas, 2020. Disponível em: < www.embrapa.br/car >. Acesso em: 28 jan. 2021

8. FAO, IFAD, UNICEF, WFP and WHO. The State of Food Security and Nutrition in the World 2019. Safeguarding Against Economic Slowdowns and Downturns. FAO: Roma, 2019.

9. FINKE, M. D. Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biology, v. 21, n. 3, p. 269–285, 2002.

10. FINKE, M. D. Estimate of Chitin in Raw Whole Insects. Zoo Biology, v. 26, n. April, p. 105– 115, 2007.

11. INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. Pesquisa de orçamentos fa- miliares 2017-2018: análise da segurança alimentar no Brasil. [s.l: s.n.].

12. Jongema Y. List of edible insects of the world. 2015, available at http://www.wageningenur.nl/ en/Expertise-Services/Cha ir-groups/Plant-Sciences/Laboratory- of-Entomology/ Edible-insects/ Worldwide-species-list.htm.

13. KHEMPAKA, S.; CHITSATCHAPONG, C.; MOLEE, W. Effect of chitin and protein constituents in shrimp head meal on growth performance, nutrient digestibility, intestinal microbial populations, volatile fatty acids, and ammonia production in broilers. Journal of Applied Poultry Research, v. 20, n. 1, p. 1–11, 1 mar. 2011.

14. KULMA, M. et al. Effect of developmental stage on the nutritional value of edible insects. A case study with Blaberus craniifer and Zophobas morio. Journal of Food Composition and Analysis, v. 92, 1 set. 2020.

15. KUNTADI, K.; ADALINA, Y.; MAHARANI, K. E. NUTRITIONAL COMPOSITIONS OF SIX EDIBLE INSECTS IN JAVA. Indonesian Journal of Forestry Research, v. 5, n. 1, p. 57–68, maio 2018.

16. LATNEY, L.; CLAYTON, L. A. Updates on amphibian nutrition and nutritive value of common feeder insects. Veterinary Clinics: Exotic Animal Practice, v. 17, n. 3, p. 347-367, 2014.

17. LATNEY, L. V. et al. Effects of various diets on the calcium and phosphorus composition of mealworms (Tenebrio molitor larvae) and superworms (Zophobas morio larvae). American Journal of Veterinary Research, v. 78, n. 2, p. 178–185, 1 fev. 2017.

18. MAKKI, K. et al. The impact of dietary fiber on gut microbiota in host health and disease. Cell host & microbe, v. 23, n. 6, p. 705-715, 2018.

19. MIGLIETTA, P. P. et al. Mealworms for food: A water footprint perspective. Water (Switzer- land), v. 7, n. 11, p. 6190–6203, 2015.

20. MLČEK, J. et al. Fat from Tenebrionidae bugs – Sterols content, fatty acid profiles, and cardiovascular risk indexes. Polish Journal of Food and Nutrition Sciences, v. 69, n. 3, p. 247–254, 2019.

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 546 21. MOREIRA, N. X.; CURI, R.; MANCINI-FILHO, J. Ácidos graxos: uma revisão. Nutrire Rev. Soc. Bras. Aliment. Nutr, p. 105-123, 2002.

22. NOCELLA, C. et al. Extra Virgin Olive Oil and Cardiovascular Diseases: Benefits for Human Health. Endocrine, Metabolic & Immune Disorders - Drug Targets, v. 18, n. 1, 18 dez. 2017.

23. O’CALLAGHAN, J.; O’TOOLE, P. W. Lactobacillus: Host-microbe relationships. Current Topics in Microbiology and Immunology, v. 358, p. 119–154, 2013.

24. OONINCX, D. G. A. B.; VAN DER POEL, A. F. B. Effects of diet on the chemical composition of migratory locusts ( Locusta migratoria ). Zoo Biology, v. 30, n. 1, p. 9-16, 2011.

25. OONINCX, D. G.; DIERENFELD, E. S. An investigation into the chemical composition of alternative invertebrate prey. Zoo biology, v. 31, n. 1, p. 40–54, 2012.

26. PADOVANI, R. M. et al. Dietary Reference Intakes: Application Of Tables In Nutritional Studies [dietary Reference Intakes: Aplicabilidade Das Tabelas Em Estudos Nutricionais]. Revista de Nutrição, 2006.

27. PAUL, A. et al. Insect fatty acids: A comparison of lipids from three Orthopterans and Tenebrio molitor L. larvae. Journal of Asia-Pacific Entomology, v. 20, n. 2, p. 337–340, 1 jun. 2017. PIRES, C. V. et al. Qualidade nutricional e escore químico de aminoácidos de diferentes fontes protéicas. Ciencia e Tecnologia de Alimentos, v. 26, n. 1, p. 179–187, jan. 2006.

28. RAMOS-BUENO, R. P. et al. Fatty acid profiles and cholesterol content of seven insect species assessed by several extraction systems. European Food Research and Technology, v. 242, n. 9, p. 1471–1477, 1 set. 2016.

29. RAMOS-ELORDUY, J. et al. Nutritional value of edible insects from the state of Oaxaca, Mexico. Journal of Food Composition and Analysis, v. 10, n. 2, p. 142–157, 1 jun. 1997.

30. RAMOS-ELORDUY, J.; MENZEL, P. Creepy crawly cuisine: the gourmet guide to edible insects. Inner Traditions/Bear & Co, 1998.

31. SILVA, D. J., QUEIROZ, A. C. Análise de Alimentos. Métodos químicos e biológicos. 3ª edição. Editora UFV. 235p. 2002.

32. SOARES ARAÚJO, R. R. et al. Nutritional composition of insects Gryllus assimilis and Zopho- bas morio: Potential foods harvested in Brazil. Journal of Food Composition and Analysis, v. 76, p. 22–26, 1 mar. 2019.

33. SOETAN, K. O.; OLAIYA, C. O.; OYEWOLE, O. E. The importance of mineral elements for humans, domestic animals and plants: A review. African Journal of Food Science, v. 4, n. 5, p. 200–222, 31 maio 2010.

34. STEINFELD, Henning et al. Livestock’s long shadow: environmental issues and options. Food & Agriculture Org., 2006.

35. VAN BROEKHOVEN, S. et al. Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by- pro- ducts. Journal of Insect Physiology, v. 73, p. 1–10, 1 fev. 2015.

36. VAN HUIS, Arnold et al. Edible insects: future prospects for food and feed security. Food and Agriculture Organization of the United Nations, 2013.

Avanços em Ciência e Tecnologia de Alimentos - Volume 3 Avanços em Ciência e Tecnologia de Alimentos - Volume 3 546 547 37. VAN HUIS, A.; VAN GURP, H.; DICKE, M. The insect cookbook: food for a sustainable planet. Columbia University Press, 2014.

38. VAN HUIS, A. Edible insects contributing to food security? Agriculture & Food Security, v. 4, n. 1, p. 1-9, 2015.

39. VAN HUIS, A.; OONINCX, D. G. A. B. The environmental sustainability of insects as food and feed. A review. Agronomy for Sustainable Development, v. 37, n. 5, p. 1-14, 2017.

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