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Evaluating the nutritional content of an insect-fortified food for the child complementary diet in Ghana

BMC Nutrition volume 6, Article number: 7 (2020) Cite this article

Abstract

Background

Due to rising food insecurity, natural resource scarcity, population growth, and the cost of and demand for animal proteins, insects as food have emerged as a relevant topic. This study examines the nutrient content of the palm weevil larva (Rhynchophorus phoenicis), a traditionally consumed edible insect called akokono in Ghana, and assesses its potential as an animal-source, complementary food.

Methods

Akokono in two “unmixed” forms (raw, roasted) and one “mixed” form (akokono-groundnut paste) were evaluated for their macronutrient, micronutrient, amino acid, and fatty acid profiles.

Results

Nutrient analyses revealed that a 32 g (2 tbsp.) serving of akokono-groundnut paste, compared to recommended daily allowances or adequate intakes (infant 7–12 months; child 1–3 years), is a rich source of protein (99%; 84%), minerals [copper (102%; 66%), magnesium (54%; 51%), zinc (37%; 37%)], B-vitamins [niacin (63%; 42%), riboflavin (26%; 20%), folate (40%; 21%)], Vitamin E (a-tocopherol) (440%; 366%), and linoleic acid (165%; 108%). Feed experiments indicated that substituting palm pith, the typical larval diet, for pito mash, a local beer production by-product, increased the carbohydrate, potassium, calcium, sodium, and zinc content of raw akokono. Akokono-groundnut paste meets (within 10%) or exceeds the levels of essential amino acids specified by the Institute of Medicine criteria for animal-source foods, except for lysine.

Conclusions

Pairing akokono with other local foods (e.g., potatoes, soybeans) can enhance its lysine content and create a more complete dietary amino acid profile. The promotion of akokono as a complementary food could play an important role in nutrition interventions targeting children in Ghana.

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Background

Maternal and child undernutrition remains pervasive in low- and middle-income countries (LMICs) and together constitutes the leading underlying cause of child morbidity and mortality [1]. Against a backdrop of global trends such as urbanization, growing populations, and rising incomes, the global food system faces the looming challenge of meeting the world’s evolving nutritional needs [2]. Animal-source foods (ASFs) are important components of diverse diets, providing protein and essential micronutrients that promote growth and development. Increasing evidence points to the positive impact of animal-source proteins on linear growth and physical and cognitive development in children [3,4,5,6,7]. The World Health Organization recommends that children 6 to 23 months of age consume ASFs daily [8]. Yet, ASFs are often costly and remain out of reach for many low-income households [5]. The global demand for ASFs in many LMICs is expected to rise substantially over the coming decades [9]. It is projected that current livestock production practices will be unable to sustainably meet this growing demand [10, 11]. Thus, edible insects are emerging as a potential avenue to sustainably improve nutrition.

Insects as food

Entomophagy, the consumption of insects as food, is a long-standing practice in many cultures around the world and has played a role in the history of human nutrition. The Food and Agriculture Organization estimates that approximately 2 billion people worldwide consume insects as part of their diets, [12] and Jongema [13] has documented over 2000 species of edible insects consumed globally. In comparison to traditional livestock, edible insect production has the potential to positively contribute to environmental sustainability due to lower resource requirements, feed-conversion rates, and greenhouse gas emissions [14, 15].

In the context of locally-sourced diets in LMICs, where the burden of malnutrition is highest, edible insects can contribute essential nutrients necessary to augment dietary quality and diversity among individuals who primarily consume cereal-based foods [16]. However, the nutritional profiles of edible insects indicate substantial variability both between and within species [17, 18] and comprehensive analyses of both macronutrient and micronutrient content are lacking [19].

The Ghanaian context

Malnutrition remains a pressing concern in Ghana, where one-fifth (19%) of children under five suffer from chronic malnutrition (stunting), 5% suffer from acute malnutrition (wasting), and two-thirds (66%) of children between 6 and 59 months of age are anemic [20]. The typical complementary diet of Ghanaian children 6 to 23 months is composed of grains, fruits and vegetables, roots and tubers, and some animal products; only 13% of children of this age met the criteria for a minimally acceptable diet [20].

In Ghana, edible insects are already included in certain traditional diets. In a countrywide survey of 2000 individuals, almost one-third reported consuming edible insects, the most common being the palm weevil larva (Rhynchophoris phoenicis) [21]. Palm weevil larvae, known locally as akokono in Ghana, are consumed across regions of Africa, Asia, and Latin America [12]. In Ghana, the akokono typically feed on the pith of palm trees that are felled for harvesting palm wine and, when farmed, can be available year round [22, 23]. When harvested for food, akokono is typically fried, roasted as a kebab, or boiled in a soup (personal communication with Aspire Food Group, June 2017). According to a recent study, akokono was largely perceived to be an acceptable complementary food source by caregivers in the Brong-Ahafo Region of Ghana [22].

Previous studies investigating the nutritional composition of palm weevil larvae have typically reported high protein, fat, and mineral content, but there is variability between studies [16, 24,25,26,27,28,29,30,31]. This variability may be explained by a number of factors, including differences in insect habitat, geographic location, developmental stage, and feed composition, as well as the study measurement methods [17]. To our knowledge, no studies to date have examined the nutritional profile of the palm weevil larva in Ghana.

Purpose

We hypothesize that the consumption of akokono could help infants and young children meet essential amino acid [32] and micronutrient requirements and offset the need for daily consumption of traditional ASFs. The purpose of this study is to examine the nutrient profile of akokono (raw, roasted) to characterize the potential of this insect as an ingredient in complementary foods. We aimed to evaluate akokono and akokono-fortified foods as alternatives to conventional ASFs and examine the composition of their nutrient profiles based on feed type.

Key messages

  • Akokono is a good source of several essential nutrients including protein, fat, zinc, and B-vitamins that are important for child growth and development.

  • Combining akokono with local groundnuts can improve the amino acid and vitamin profiles of the nut-based food.

  • Substituting the traditional feed substrate of palm pith with pito mash improves both the macronutrient and micronutrient profile of akokono.

  • Optimizing the nutrient content of this insect via manipulation of feed substrate is an area in need of further research.

  • Akokono has the potential to improve child health and nutrition outcomes and can be incorporated into nutrition interventions.

Methods

We examined the nutrient profile of akokono in two “unmixed” forms: raw and roasted. Additionally, three “mixed” akokono products were developed at the Kwame Nkrumah University of Science and Technology (KNUST): akokono flour, akokono-yam biscuit, and akokono-groundnut paste. The akokono-groundnut paste was chosen by the lead food technologist as the most promising food product for further testing and development as a potential child complementary food. Macronutrient composition, amino acid profile, fatty acid profile, mineral, and vitamin tests were conducted on these three forms of akokono as described below. Additionally, we measured the macronutrient and mineral composition of raw akokono fed two different types of feed materials, pito mash and palm pith, as well as that of the feed materials themselves.

Macronutrient composition, amino acid profile, fatty acid profile, and mineral tests (except for iron) were conducted at KNUST in Ghana (described below). All tests conducted at KNUST represent the mean of duplicate analysis. Eurofins Scientific performed all the vitamin tests and examined the iron content of raw akokono, roasted akokono, and akokono-groundnut paste; the Eurofins results represent the mean of triplicate analysis (described below). KNUST used identical macronutrient and mineral testing procedures on the akokono and the feed materials (pito mash, palm pith).

Preparation

The akokono were bred in a warehouse in the Ashanti Region, fed with palm pith and sugar water, and procured from the Aspire Food Group facility in Kumasi. At the time of testing, akokono were between 28 and 35 days old (same development stage). Roasted samples were prepared by first pan-frying the akokono for 5 min followed by dry roasting at low heat for 15 min. Using a recipe created at the KNUST food technology laboratory, the akokono-groundnut paste was produced by mixing and then milling dry-roasted akokono (30%) together with local groundnuts (70%) and adding a small amount of canola oil (2 mL oil per 100 g paste) to improve the organoleptic properties of the final product. Finally, KNUST tested the akokono-groundnut paste to assess shelf-life stability, microbial safety, and chemical deterioration of the product at 0, 7, and 14 days as required by the Ghana Food and Drugs Authority (FDA). The safety data satisfied the Ghana Standards Authority (GSA) requirements for similar groundnut-based products (data not presented herein) [33]. To test the feed materials, palm pith was harvested from purchased felled palm trees in the Ashanti Region, and the pito mash, a by-product of local pito (beer) brewing, was purchased from a local market.

Proximate (macronutrient) analysis

AOAC standard methods [34] were used to determine the proximate composition (moisture, ash, crude fat, protein, and fiber) of the akokono samples in duplicate. Significant differences between the macronutrient contents of the three forms of akokono were analyzed using one-way ANOVAs.

Amino acid profile

The amino acid content was determined by first digesting the sample for 24 h at 110 °C using 37% HCl. Pre-column derivatization was done using o-phthalaldehyde 3-mercaptopropionic acid and 9-fluroenylmethyl chloroformate according to the method described by Schwarz, Roberts, & Pasquali [35]. An aliquot of 100 μL was injected into a Shimadzu high-performance liquid chromatography (HPLC) fitted with a Shimadzu 10AxL Fluorescence detector.

Mobile phase A was composed of 40 mM CH3COONa at pH 7.8 and mobile phase B composed of CH3CN: CH3OH: H2O (45:45:10 v/v/v) at a flow rate of 1 ml/min, passed through a Phenomenex column (3.5 μm, 4.6 mm ID, 15 cm) at 40 °C with run time of 60 min at the following wavelengths: Exitation: 340 nm; Emission: 450 nm.

A gradient elution program was used as described herein: 0 to 10 min (20% mobile phase B), 10 to 20 min (50% mobile phase B), 20 to 30 min (60% mobile phase B), 30 to 35 min (80% mobile phase B), 35 to 40 min (100% mobile phase B), and 40 to 60 min (20% mobile phase B). Samples were analyzed in duplicate, and results expressed as g amino acid per 100 g total amino acids.

Fatty acid profiles

The triglyceride profile was determined by HPLC. The analysis was carried out using a HPLC (Infinity Series 1260, Aligent Technologies, Germany) fitted with an auto sampler and a Refractive Index Detector. The Hypersil ODS C-18 column at ambient temperature was used with mobile phase of Acetonitrile: Acetone (37.5:62.5) at flow rate of 1.5. The elution program was isocratic. The purpose of this analysis was to characterize the fatty acid composition. Using mole ratio, the concentration of each component fatty acid was calculated for each triglyceride [36]. All samples were analyzed in duplicate.

Mineral analysis

The mineral analysis of iron, calcium, magnesium, zinc, and copper was conducted with atomic absorption spectroscopy [37]. The samples were dry-ashed in a muffle furnace at 550 °C for 6 h. The minerals were extracted from ash with 20 mL of 2.50% HCl and heated in a steam bath to reduce the volume to 8.0 mL, which was transferred quantitatively to a 50 mL volumetric flask and diluted to volume using deionized water. The extracts were stored in dry, clean plastic sample bottles, and the mineral concentrations were determined using an atomic absorption spectrophotometer. Potassium was determined with the flame photometric method [38] using a low temperature direct reading single channel emission flame photometer. Significant differences between the mineral contents of the three forms of akokono were analyzed using one-way ANOVAs.

Vitamin determination

Vitamin a

Vitamin A was released from the sample by alkaline hydrolysis using ethanolic potassium hydroxide solution and extracted three times with hexane:ethylacetate (85:15 volume/volume %). The determination was carried out by normal-phase chromatography (NP-HPLC) with ultraviolet/diode array detector (DAD) at 325 nm (EN 12823–1:2014) [39].

Vitamin B1 (thiamine)

Thiamine was extracted from the sample in an autoclave using acid hydrolysis and quantified by reverse phase chromatography (RP-HPLC) coupled with a fluorescence detector (Ex.: 368 nm, Em.: 440 nm) after post-column oxidation to thiochrome (EN 14122:2006 with modification) [40].

Vitamin B2 (riboflavin)

Riboflavin was extracted from the sample in an autoclave using acid hydrolysis and quantified by RP-HPLC coupled with a fluorescence detector (Ex.: 468 nm, Em 520 nm) (EN 14152:2006 with modification) [41].

Vitamin B3 (niacin)

Niacin was calculated as the sum of nicotinic acid and nicotinamide. The two compounds were extracted from the sample in a mild hydrochloric solution at 100 °C, the pH of the extract was adjusted to pH 4.5 with sodium acetate followed by a filtration.

Vitamin B6

To determine vitamin B6, the European Union reference method for the determination of vitamin B6 in foodstuff (EN 14164–2008) was used with modification [42]. Briefly, the sample was hydrolysed in an autoclave followed by enzymatic dephosphorylation, reacting with glyoxylic acid in the presence of Fe2+ as a catalyst to transform pyridoxamine into pyridoxal, which is then reduced to pyridoxine by the action of sodium borohydride in alkaline medium. Total pyridoxine was quantified by RP-HPLC with a fluorescence detector (Ex: 290 nm, Em: 395 nm).

Folate

Folate was extracted from the sample in an autoclave using a buffer solution, followed by an enzymatic digestion with human plasma and pancreas V, and finally by a second autoclave treatment. After dilution with basal medium containing all required growth nutrients, except folic acid, the growth response of Lactobacillus rhamnosus (ATCC 7469) to extracted folate was measured turbidimetrically and compared to calibration solutions with known concentrations [43].

Vitamin B12

Vitamin B12 was extracted from the sample in an autoclave using a buffered solution. After dilution with basal medium (containing all required growth nutrients except cobalamin) the growth response of Lactobacillus leichmanii (ATCC 7830) to extracted cobalamin was measured turbidimetrically. This was then compared to calibration solutions with known concentrations [44].

Vitamim D3

The samples were saponified in alcoholic potassium hydroxide solution and extracted with hexane: ethylacetate (85:15 v/v%). The extract was concentrated and cleaned up by solid phase extraction (EN 12821:2009) [45]. The amount of vitamin D3 was determined by RP-HPLC with DAD (265 nm).

Vitamin E

Vitamin E was released from the sample by alkaline hydrolysis using ethanolic potassium hydroxide solution and extracted three times with hexane:ethylacetate (85:15 v/v%). Quantification was carried out by NP-HPLC with a fluorescence detector (Ex/EM 290 nm/327 nm) (EN 12822:2014) [46].

Significant differences between the vitamin contents of the three forms of akokono were analyzed using one-way ANOVAs.

Ethics approval and consent to participate

This study was deemed not human subjects research by the PATH Research Determination Committee.

Results

Macronutrients, minerals, and vitamins

Table 1 presents the akokono nutrient content analysis from 100 g wet matter samples. The macronutrient profile of all forms of akokono was slightly more than half (53 to 56%) fat, one-third (32 to 33%) protein, and approximately one tenth (9 to 13%) carbohydrate. The fiber content ranged from 4 to 10%. The akokono-groundnut paste product had a slightly lower fat concentration than the unmixed forms of akokono, and similar protein and higher carbohydrate content.

Table 1 Proximate, mineral, and vitamin profiles of three forms of akokonoǂ
Full size table

In unmixed forms, akokono is richest in magnesium and potassium, followed by calcium, zinc, iron, and copper. When roasted akokono was combined with groundnut paste (and canola oil), the content of all analyzed minerals increased.

Of the vitamins present in akokono, the highest concentrations were observed for vitamin E (α-tocopherol) and niacin. There were small but significant amounts of thiamine, riboflavin, vitamin B6, folate, and vitamin B12 in all akokono samples; vitamin A and vitamin D3 were not present. When roasted akokono was combined with the groundnut paste and canola oil, vitamin E (α-tocopherol) and niacin concentrations increased, and thiamine, riboflavin, folate, vitamin B6 and vitamin B12 decreased. Roasted akokono alone had significantly greater concentrations of thiamine, riboflavin, and vitamin B-12 than when it was combined with groundnut paste and canola oil into a paste.

Table 2 provides a closer examination of the macronutrient and micronutrient contribution of one serving size of akokono-groundnut paste to the child diet. One serving size of two tablespoons (approximately 32 g) of akokono-groundnut paste contains enough protein to satisfy 99% of an infant’s (6 to 12 months) recommended dietary allowance (RDA) and 84% of a child’s (1 to 3 years) RDA. It also provides half (49%) of an infant’s adequate intake (AI) recommendation for fat (AI for children 1 to 3 years not determined). However, the same serving size only provides 7 and 5% of infant and child carbohydrate RDAs, respectively, and 7% of a child’s AI level for fiber (AI for infants not determined). It is a rich source of certain minerals (infant 6 to 12 months, children 1 to 3 years): copper (102% AI, 66% RDA), magnesium (54% AI, 51% RDA), zinc (37% RDA, 37% RDA), potassium (11% AI, 3% AI), iron (4% RDA, 7% RDA), and calcium (5% AI, 2% RDA). The paste also provides B-vitamins (infants 6 to 12 months, children 1 to 3 years): thiamine (13% AI, 8% RDA), niacin (63% AI, 42% RDA), riboflavin (26% AI, 20% RDA), vitamin B6 (22% AI, 13% RDA), folate (40% AI, 21% RDA), and vitamin E (a-tocopherol) (440% AI, 366% RDA).

Table 2 The nutritional content of one serving** akokono-groundnut paste in comparison to the recommended dietary allowance (RDA) or adequate intake (AI) for children 6–12 months of age and 1–3 years of age
Full size table

Amino acids

Table 3 lists the concentrations of amino acids within two unmixed forms of akokono and the mixed akokono-groundnut paste in comparison to the concentration thresholds listed by the Institute of Medicine (IOM) for ASFs [47]. Concentrations of methionine and cysteine (sulfur amino acids) are examined together since methionine is often the most limiting amino acid in cereal grain-based diets, and cysteine is able to substitute for a portion of methionine’s requirement. Phenylalanine and tyrosine (aromatic amino acids) are also examined together. While both are indispensable to human functions, phenylalanine must be consumed in the diet, but tyrosine can be generated from the hydroxylation of phenylalanine [32]. Roasted akokono meets or exceeds the IOM’s concentration threshold for ASFs for four of the nine essential amino acids (histidine, isoleucine, phenylalanine + tyrosine, and valine), but concentrations of leucine, lysine, methionine + cysteine, threonine, and tryptophan fell short of the IOM threshold level. When akokono was combined with groundnut paste and canola oil, the concentrations of leucine, methionine + cysteine, threonine, and tryptophan increased to within 10% of the IOM threshold level; however, lysine content remained low. The concentrations of histidine, isoleucine, lysine, and phenylalanine + tyrosine were greater in unmixed akokono than the paste product. Akokono is also a source of seven non-essential amino acids, including alanine, arginine, aspartate, glutamate, glycine, proline, and serine (data not presented herein).

Table 3 Amino acid profile of three forms of akokonoa (mg/g protein), compared to the concentration of amino acids required to meet the IOM ASF definition
Full size table

Fatty acids

Table 4 lists the fatty acid compositions of three different forms of akokono. The profiles of raw and roasted akokono respectively showed concentrations of 6.54 and 14.29 g/100 g linoleic acid (n-6 polyunsaturated fatty acid), 14.47 and 7.37 g/100 g oleic acid, 19.95 and 14.97 g/100 g myristic acid, and 19.52 and 13.87 g/100 g palmitic acid. When combined with the groundnut paste and canola oil, fatty acid concentrations (g/100 g akokono) increased compared to roasted akokono for linoleic (omega-6) acid (23.69), stearic acid (1.67), and oleic acid (11.16), while decreasing for myristic and palmitic acids (1.51 and 5.96, respectively). The fatty acid concentration of linoleic acid exceeds the AI levels for infants (165% AI) and children (108% AI). AI levels for oleic acid, myristic acid, and palmitic acid have not been set.

Table 4 Fatty acid compositions of three forms of akokonoa
Full size table

Feed experiment

Table 5 shows the results of the akokono feed experiments. Akokono fed on pito mash had > 10% increased concentrations of carbohydrate, potassium, calcium, sodium, and zinc concentrations in comparison to those fed on palm pith. The protein and iron content remained consistent between the two groups, but the fat content was lower among akokono fed on pito mash. The pito mash itself contained a higher concentration of fat, protein, and all measured elements.

Table 5 Proximate and mineral content of akokono and feed materials
Full size table

Discussion

This study presents the nutritional composition of palm weevil larvae (akokono), edible insects consumed in Ghana, and evaluates their adequacy as a complementary food, both alone and in combination with local groundnuts. We conclude that akokono alone does not provide a complete amino acid profile, but it does offer a significant amount of essential nutrients and can feasibly be integrated into agriculture and nutrition intervention strategies to address upstream determinants of health and nutrition. Furthermore, there is potential to improve the nutrient content of this food by manipulating feed inputs; however, further research in this area is warranted.

Nutrient content

Consistent with existing research, our analysis determined Ghanaian akokono to be a nutrient-rich, high fat, high protein food. Roasted akokono contains adequate amounts of four essential amino acids (histidine, isoleucine, phenylalanine + tyrosine, and valine) but inadequate amounts of five essential amino acids (e.g., leucine, lysine, methionine + cysteine, threonine, tryptophan). Combining akokono with groundnut paste and canola oil favorably affected both the amino acid and fatty acid composition of the food, increasing the ratio of essential to non-essential fatty acids and the ratio of unsaturated to saturated fatty acids (i.e., more linoleic and oleic acid, less myristic and palmitic acid), likely largely due to the composition of canola oil. In comparison to roasted akokono, the paste product had greater concentrations of all minerals analyzed but lower vitamin concentrations (except for vitamin E and niacin).

In contrast to studies examining the nutritional composition of the palm weevil larvae in other African countries, the greatest differences are seen in mineral content, which varies between studies, independent of geography. We hypothesize that the larval diet could be one explanation for the variation between protein, fat, and mineral content. Our feed experiment indicated that the akokono responded to different feed substrates with changes in macronutrient and micronutrient composition. However, multiple studies from Nigeria [26, 29, 30], where the palm weevil larva were fed only raphia palm pith, still observed significant variability in mineral content. Research by Reynolds et al. [48] in Uganda found vast heterogeneity in mineral content between 11 samples of pith from raphia palms, suggesting that nutrient variability among the same type of feed substrate, perhaps due to soil quality, could also contribute to differences in nutrient profiles between different insect samples. Variability may also be linked to the developmental stage of the larvae analyzed [17].

We found that one serving (approximately 32 g) of akokono-groundnut paste provided 6% of the infant (6 to 12 months) iron RDA and 9% of the child (1 to 3 years) iron RDA. However, akokono is a potential source of highly bioavailable iron. Heme-iron is present in insect cytochromes [49] and ferrous iron is carried by holoferritin molecules in the vacuolar system and hemolymph [50]. Both forms have greater bioavailability than the ferric iron most prevalent in non-heme source foods [51], and the absence of iron-binding plant origin compounds [52] could be advantageous for the absorption of iron from akokono. The properties of insect iron may explain results from previous studies, including a trial which found that caterpillar fortified cereal improved hemoglobin levels, ferritin levels, and anemia prevalence among 18-month-old infants, [53] and an in-vitro study that showed iron bioavailability of several insect species to be comparable with that of sirloin beef [54]. It is plausible that similar benefits could extend to akokono presupposing that their underlying biology is largely the same as that of other insects.

Adequacy as a complementary food

In many low-resource settings, women and children are deficient in iron, zinc, and vitamin A, and often subsist on diets low in protein and essential fatty acids. The nutrient profile of akokono can augment the intakes of certain micronutrients and macronutrients that play important roles in development and immunity. At the same time, concentrations of these nutrients may be dependent on insect feed and rearing practices. Opportunities to optimize the nutrient content of this food is an area in need of further research.

Based on our findings, akokono does not meet all the requirements to be classified as an alternative ASF; however, it still holds promise as a component of the complementary diet to help meet nutritional requirements. Pairing akokono-groundnut paste with lysine-rich foods can provide a complete protein profile. For example, potatoes and soybeans are two locally produced foods that are high in lysine. Additionally, it is also significant that the akokono-groundnut paste product meets the GSA requirements for commercial peanut butter products and can be safely consumed without refrigeration for 14 days (data not included). This suggests that the akokono-groundnut paste could be consumed in settings that lack electricity, without any added risk relative to other commercial peanut butter products in Ghana.

Policies on insects as food

In Ghana, akokono has historically been harvested from palm trees; however, this practice has fallen out of favor among younger generations [22]. Recent efforts to stimulate the market have initiated the reintroduction of edible insects into the modern food supply in Ghana by way of microfarming. Forest foods can provide healthy additions to household diets and household microfarming can generate additional income; thus, opportunities for incorporating forest foods into nutrition policy and health intervention strategies should be further explored [55].

However, policies and legislation on insects as food are currently lacking on both national and international levels. While some institutions and policies, such as Ghana’s FDA, do focus on food standards in Ghana, legislation is generally broad and does not offer guidelines specific to insects. Although unprocessed akokono is recognized as a safe, local, traditional food that has been consumed for generations, GSA certification is required for all processed akokono-based products. Building quality control mechanisms and risk mitigation strategies can help to inform the standards enforced and upheld by the Ghana FDA and the GSA to ensure food safety. There is a great need for unifying regulations and efforts focusing on the production and sale of insects for human consumption, both in Ghana and internationally—particularly given their low environmental impact and potential to improve human nutrition.

Limitations

This study investigated the macronutrient and micronutrient content of a small sample of domestically microfarmed akokono. Future research, including studies with larger sample sizes and those testing akokono harvested from the wild, is needed to confirm our results. In addition, further research into different feed inputs and their associated impact on the insect’s nutrient profile will continue to support both optimal insect nutrient content as well as inform low-environmental impact production efforts. Further analyses comparing the nutrient profile of akokono-fortified groundnut paste to that of groundnut paste alone may also provide additional insights. Acceptability studies, such as the one conducted by Bauserman et al., [56] are also warranted to further investigate consumer perceptions of akokono-fortified commercial food products.

In addition to further characterizing the nutrient profiles of akokono and akokono-fortified foods, clinical research is also needed to determine the impacts of these foods on human health and nutrition outcomes. For example, Bauserman and colleagues [53] evaluated the efficacy of a caterpillar cereal on stunting and anemia in the Democratic Republic of the Congo.

Finally, it was a limitation of this study that we did not investigate the digestibility of protein from akokono, nor did we examine micronutrient bioavailability. Although information on insect protein quality is limited, several studies have calculated Protein Digestibility Corrected Amino Acid Scores for various insect species [57, 58]. As such, insect protein quality and digestibility is an important area for future inquiry, particularly given the role of protein quality in early growth [59].

Conclusion

Although there is no one-size-fits-all solution to malnutrition, it is important that we continue to examine traditional practices—such as entomophagy—and their implications for human and planetary health. In this paper, we conclude that the promotion and uptake of akokono as a complementary food could address nutritional inadequacies in the Ghanaian diet. Further, our feed experiment demonstrates the potential for using recycled by-products as novel feed inputs to reduce the environmental impact of production and manipulate insect nutrient profiles. Implemented properly, nutrition and policy interventions involving akokono could also incorporate nutrition-sensitive strategies centered around women-led micro-farming to generate supplemental income while improving food security.

Availability of data and materials

All data generated or analyzed during this study are included in this published article [and its supplementary information files].

Abbreviations

AI:

Adequate Intake

ASF:

Animal-source food

DAD:

Diode array detector

FDA:

Food and drug authority

GSA:

Ghana standards authority

HPLC:

High-performance liquid chromatography

IOM:

Institute of medicine

KNUST:

Kwame Nkrumah University of Science and Technology

LMIC:

Low- and middle-income country

LOQ:

Limit of quantitation

ND:

Not determined

NP:

Normal-phase

RDA:

Recommended dietary allowance

RP:

Reverse phase

References

  1. Black R, Victora C, Walker S, Bhutta Z, Christian P, Onis MD, et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet. 2013 Aug 03;382(9890):427–51.

    Article  PubMed  Google Scholar 

  2. International Food Policy Research Institute (US). 2018 Global food policy report. Washington (DC): International Food Policy Research Institute; 2018. p. 150.

    Google Scholar 

  3. Grace D, Dominguez-Salas P, Alonso S, Lannerstad M, Muunda E, Ngwili N, et al. The influence of livestock-derived foods on nutrition during the first 1,000 days of life. Nairobi (KE): ILRI; 2018. p. 82. Report No. 44

    Google Scholar 

  4. Dror DK, Allen LH. The importance of milk and other animal-source foods for children in low-income countries. Food Nutr Bull. 2011;32(3):227–43.

    Article  PubMed  Google Scholar 

  5. Headey D, Hirvonen K, Hoddinott J. Animal sourced foods and child stunting. Am J Agric Econ. 2018;100(5):1302–19.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Iannotti LL, Lutter CK, Stewart CP, Riofrío CA, Malo C, Reinhart G, et al. Eggs in early complementary feeding and child growth: a randomized controlled trial. Pediatrics. 2017;140(1):e20163459.

    Article  PubMed  Google Scholar 

  7. Krebs NF, Mazariegos M, Tshefu A, Bose C, Sami N, Chomba E, et al. Meat consumption is associated with less stunting among toddlers in four diverse low-income settings. Food Nutr Bull. 2011;32(3):185–91.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Dewey K. Guiding principles for complementary feeding of the breastfed child. Pan American Health Organization: Washington (DC); 2003. p. 37.

    Google Scholar 

  9. Alexandratos N, Bruinsma J. World agriculture towards 2030/2050: the 2012 revision. Rome (IT): Food and Agriculture Organization of the United Nations; 2012. p. 146. ESA Working Paper No. 12–03

    Google Scholar 

  10. Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, de Haan C. Livestock’s long shadow: environmental issues and options. Rome (IT): Food and Agriculture Organization of the United Nations; 2006. p. 26.

    Google Scholar 

  11. Wu G, Fanzo J, Miller DD, Pingali P, Post M, Steiner JL, Thalacker-Mercer AE. Production and supply of high-quality food protein for human consumption: sustainability, challenges, and innovations. Ann N Y Acad Sci. 2014;1321:1–19.

    Article  CAS  PubMed  Google Scholar 

  12. Van Huis A, Van Itterbeeck J, Klunder H, Mertens E, Halloran A, Muir G, et al. Edible insects: future prospects for food and feed security. Rome (IT): Food and Agriculture Organization of the United Nations; 2013. p. 187. FAO Forestry Paper No. 171

    Google Scholar 

  13. Jongema, Y. Worldwide list of recorded edible insects. Wageningen (NL): Wageningen University & Research; 2017 [cited 2017 Jun 04]. 100. Available from http://www.wur.nl/en/Expertise-Services/Chair-groups/Plant-Sciences/Laboratory-of-Entomology/Edible-insects/Worldwide-species-list.htm.

  14. Oonincx DG, van Itterbeeck J, Heetkamp MJ, van den Brand H, van Loon JJ, van Huis A. An exploration on greenhouse gas and ammonia production by insect species suitable for animal or human consumption. PLoS One. 2010;5(12):e14445.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Van Huis A, Oonincx DG. The environmental sustainability of insects as food and feed. A review Agron Sustain Dev. 2017;37:43.

    Article  Google Scholar 

  16. Payne C, Scarborough P, Rayner M, Nonaka K. Are edible insects more or less ‘healthy’ than commonly consumed meats? A comparison using two nutrient profiling models developed to combat over- and undernutrition. Eur J Clin Nutr. 2016;70(3):285–91.

    Article  CAS  PubMed  Google Scholar 

  17. Rumpold B, Schlüter O. Nutritional composition and safety aspects of edible insects. Mol Nutr Food Res. 2013 May;57(5):802–23.

    Article  CAS  PubMed  Google Scholar 

  18. Van Huis A. Potential of insects as food and feed in assuring food security. Annu Rev Entomol. 2013 Jan;58:563–83.

    Article  PubMed  CAS  Google Scholar 

  19. Finke MD. Complete nutrient content of four species of feeder insects. Zoo Biol. 2013 Jan;32(1):27–36.

    Article  CAS  PubMed  Google Scholar 

  20. Ghana Statistical Service, Ghana Health Service, ICF International. Ghana demographic and health survey 2014. Rockville (MD): GSS, GHS, and ICF International; 2015. p. 530.

    Google Scholar 

  21. Anankware JP, Osekre EA, Obeng-Ofori D, Khamala CM. Identification and classification of common edible insects in Ghana. Int J Entomol Res. 2016;1(5):33–9.

    Google Scholar 

  22. Laar A, Kotoh A, Parker M, Milani P, Tawiah-Agyemang C, Soor S, et al. An exploration of edible palm weevil larvae (akokono) as a source of nutrition and livelihood: perspectives from Ghanaian stakeholders. Food Nutr Bull. 2017;38(4):455–67.

    Article  PubMed  Google Scholar 

  23. Van Itterbeeck J, van Huis A. Environmental manipulation for edible insect procurement: a historical perspective. J Ethnobiol Ethnomed. 2012;8(1):3.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Banjo AD, Lawal OA, Songonuga EA. The nutritional value of fourteen species of edible insects in southwestern Nigeria. Afr J Biotechnol. 2006;5(3):298–301.

    CAS  Google Scholar 

  25. Bukkens SG. The nutritional value of edible insects. Ecol Food Nutr. 1997;36(2–4):287–319.

    Article  Google Scholar 

  26. Ekpo KE, Onigbinde AO. Nutritional potentials of the larva of Rhynchophorus phoenicis (F). Pak J Nutr. 2005;4(5):287–90.

    Article  Google Scholar 

  27. Elemo BO, Elemo GN, Makinde M, Erukainure OL. Chemical evaluation of African palm weevil, Rhychophorus phoenicis, larvae as a food source. J Insect Sci. 2011;11(1):146.

    PubMed  PubMed Central  Google Scholar 

  28. Koffi DM, Cisse M, Koua GA, Niamke SL. Nutritional and functional properties of flour from the palm (Elaeis Guineensis) weevil Rhynchophorus Phoenicis larvae consumed as protein source in south Côte d’Ivoire. The Annals of the University Dunarea de Jos of Galati Fascicle VI –Food Technology. 2016;41(1):9–19.

    Google Scholar 

  29. Okaraonye CC, Ikewuchi JC. Rhynchophorus phoenicis (F) larva meal: nutritional value and health implications. J Biol Sci. 2008;8(7):1221–5.

    Article  CAS  Google Scholar 

  30. Okunowo WO, Olagboye AM, Afolabi LO, Oyedeji AO. Nutritional value of Rhynchophorus phoenicis (F.) larvae, an edible insect in Nigeria. Afr Entomol. 2017;25(1):156–63.

    Article  Google Scholar 

  31. Onyeike EN, Ayalogu EO, Okaraonye CC. (2005). Nutritive value of the larvae of raphia palm beetle (Orcytes rhinoceros) and weevil (Rhyncophorus pheonicis). J Sci Food Agric. 2005;85(11):1822–8.

    Article  CAS  Google Scholar 

  32. World Health Organization. Joint FAO/WHO/UNU Expert Consultation on Protein and Amino Acid Requirements in Human Nutrition. Geneva, Switzerland: WHO technical report series; no. 935; 2002.

    Google Scholar 

  33. Ghana Standards Authority (GH). Fruits, vegetables and derived products—specification for peanut butter and peanut butter crunches. 2nd ed. Accra (GH): Ghana Standards Authority; 2005. Report No.: ICS 67.060, Ref. No. GS 49: 2005.

  34. Helrich K, editor. Official methods of analysis of the Association of Official Analytical Chemists. 15th ed. Arlington: Association of Official Analytical Chemists, Inc.; 1990. p. 771.

    Google Scholar 

  35. Schwarz EL, Roberts WL, Pasquali M. Analysis of plasma amino acids by HPLC with photodiode array and fluorescence detection. Clin Chim Acta. 2005;354(1–2):83–90.

    Article  CAS  PubMed  Google Scholar 

  36. Ortiz EG, Quintero I, Arévalo K. Biodiesel production from three mixes of oils with high free fatty content: quality evaluation and variable analysis. Int J Environ Sci Technol. 2016;13(5):1367–76.

    Article  CAS  Google Scholar 

  37. Lutterodt H. Protocol for AAS Analysis. Central Laboratory of Kwame Nkrumah University of Science and Technology. Kumasi, Ghana: Kwame Nkrumah University of Science and Technology; May. 3 pages

  38. Chapman, H.D., Pratt, P.F. Methods of Analysis for Soils, Plants and Waters. 2nd ed. Determination of minerals by titration method. Berkeley: Division of Agriculture Sciences, University of California; 1982. 169–170.

  39. European Committee for Standardization (BE). Foodstuffs. Determination of vitamin A by high performance liquid chromatography. In: Measurement of all-E-retinol and 13-Z-retinol (EN 12823–1). Brussels (BE): European Committee for Standardization; 2014.

    Google Scholar 

  40. European Committee for Standardization (BE). Foodstuffs. Determination of vitamin B1 by high performance liquid chromatography (EN 14122). Brussels (BE): European Committee for Standardization; 2006.

    Google Scholar 

  41. European Committee for Standardization (BE). Foodstuffs. Determination of vitamin B2 by high performance liquid chromatography (EN 14152). Brussels (BE): European Committee for Standardization; 2006.

    Google Scholar 

  42. European Committee for Standardization (BE). Foodstuffs. Determination of vitamin B6 by high performance liquid chromatography (EN 14164). Brussels (BE): European Committee for Standardization; 2008.

    Google Scholar 

  43. Nordic Committee on Food Analysis (DK). Folate, biologically active. In: Microbiological determination in milk and milk products with Lactobacillus casei (Method no. 11). Lyngby (DK): Nordic Committee on Food Analysis; 1985. Report No. p. 111.

    Google Scholar 

  44. Horowitz W, Latimer GW. Association of Official Analytical Chemists International. Official methods of analysis of AOAC international. 18th ed. AOAC International: Gaithersburg (MD); 2006.

    Google Scholar 

  45. European Committee for Standardization (BE). Foodstuffs. Determination of vitamin D by high performance liquid chromatography. In: Measurement of cholecalciferol (D3) or ergocalciferol (D2) (EN 12821). Brussels (BE): European Committee for Standardization; 2009.

    Google Scholar 

  46. European Committee for Standardization (BE). Foodstuffs. Determination of vitamin E by high performance liquid chromatography. In: Measurement of Α-, Β-, Γ- and Δ-tocopherol (EN 12822). Brussels (BE): European Committee for Standardization; 2014.

    Google Scholar 

  47. Institute of Medicine. Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids. Washington: The National Academies Press; 2005. 1358 p.

    Google Scholar 

  48. Reynolds V, Lloyd AW, Babweteera F, English CJ. Decaying Raphia farinifera palm trees provide a source of sodium for wild chimpanzees in the Budongo forest. Uganda PLoS One. 2009;4(7):e6194.

    Article  PubMed  CAS  Google Scholar 

  49. Locke M, Nichol H. Iron economy in insects: transport, metabolism, and storage. Annu Rev Entomol. 1992 Jan;37:195–215.

    Article  CAS  Google Scholar 

  50. Pham DQ, Winzerling JJ. Insect ferritins: typical or atypical? Biochim Biophys Acta. 2010;1800(8):824–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Santiago P. Ferrous versus ferric oral iron formulations for the treatment of iron deficiency: a clinical overview. ScientificWorldJournal. 2012;2012:846824.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Schumann K, Solomons NW. Perspective: what makes it so difficult to mitigate worldwide anemia prevalence? Adv Nutr. 2017 May 15;8(3):401–8.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Bauserman M, Lokankgaka A, Gado J, Close K, Wallace D, Kodondi K, et al. A cluster-randomized trial determining the efficacy of caterpillar cereal as a locally available and sustainable complementary food to prevent stunting and anaemia. Public Health Nutr. 2015;18(10):1785–92.

    Article  PubMed  Google Scholar 

  54. Latunde-Dada GO, Yang W, Aviles MV. In vitro iron availability from insects and sirloin beef. J Agric Food Chem. 2016;64(44):8420–4.

    Article  CAS  PubMed  Google Scholar 

  55. Fungo R, Muyonga J, Kabehenda M, Kaaya A, Okia CA, Donn P, et al. Contribution of forest foods to dietary intake and their association with household food insecurity: a cross-sectional study in women from rural Cameroon. Public Health Nutr. 2016;19(17):3185–96.

    Article  PubMed  Google Scholar 

  56. Bauserman M, Lokangaka A, Kodondi KK, Gado J, Viera AJ, Bentley ME, et al. Caterpillar cereal as a potential complementary feeding product for infants and young children: nutritional content and acceptability. Matern Child Nutr. 2015;11(4):214–20.

    Article  PubMed  Google Scholar 

  57. Yang Q, Liu S, Sun J, Yu L, Zhang C, Bi J, Yang Z. Nutritional composition and protein quality of the edible beetle Holotrichia parallela. J Insect Sci. 2014;14:139.

    PubMed  PubMed Central  Google Scholar 

  58. Michaelsen KF, Hoppe C, Roos N, Kaestel P, Stougaard M, Lauritzen L, et al. Choices of foods and ingredients for moderately malnourished children 6 months to 5 years of age. Food Nutr Bull. 2009;30(3 Suppl):S343–404.

    Article  PubMed  Google Scholar 

  59. Ghosh S. Protein quality in the first thousand days of life. Food Nutr Bull. 2016;37(Suppl 1):S14–21.

    Article  PubMed  Google Scholar 

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Acknowledgements

We thank Eurofins for conducting components of the analysis.

Funding

This project was supported by a grant from the Bill & Melinda Gates Foundation.

Author information

Authors and Affiliations

  1. PATH, Maternal, Newborn, and Child Health and Nutrition, 2201 Westlake Ave, Suite 200, Seattle, WA, 98121, USA

    Megan E. Parker, Stephanie Zobrist, Chantal Donahue, Connor Edick, Kimberly Mansen & Cyril M. Engmann

  2. Department of Food Science and Technology, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana

    Herman E. Lutterodt & Cyril R. Asiedu

  3. Division of Nutritional Sciences, Cornell University, Ithaca, New York, USA

    Gretel Pelto

  4. Sight and Life Foundation, Kaiseraugst, Switzerland

    Peiman Milani

  5. Aspire Food Group, Kumasi, Ghana

    Shobhita Soor

  6. Department of Population, Family and Reproductive Health, School of Public Health, University of Ghana, Accra, Ghana

    Amos Laar

  7. Department of Global Health, University of Washington, Seattle, Washington, USA

    Cyril M. Engmann

  8. Department of Pediatrics, University of Washington & Seattle Children’s Hospital, Seattle, Washington, USA

    Cyril M. Engmann

Authors
  1. Megan E. Parker
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  3. Herman E. Lutterodt
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  4. Cyril R. Asiedu
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  11. Amos Laar
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  12. Cyril M. Engmann
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Contributions

MEP, HEL, SS, AL, GP and PM made substantial contributions to study concept and design. HEL, CRA, and SS completed data collection and laboratory analysis. MEP, SZ, CRA, CE, KM, and CD interpreted the data and drafted the manuscript. PM, GP, KM, AL, and CME critically revised the manuscript. All authors gave final approval of the version to be published and agreed to be accountable for all aspects of the work.

Corresponding author

Correspondence to Megan E. Parker.

Ethics declarations

Ethics approval and consent to participate

This study was deemed not human subjects research by the PATH Research Determination Committee. Experimentation was only conducted on deceased insects.

Consent for publication

Experimentation was conducted on deceased insects thus consent for publication was not applicable.

Competing interests

SS is a founding member and Chief Impact Officer of Aspire Food Group. Aspire FG commercially farms palm weevil larvae in Ghana and directs a program to empower peri-rural farmers to raise palm weevils locally. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Parker, M.E., Zobrist, S., Lutterodt, H.E. et al. Evaluating the nutritional content of an insect-fortified food for the child complementary diet in Ghana. BMC Nutr 6, 7 (2020). https://doi.org/10.1186/s40795-020-0331-6

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  • DOI: https://doi.org/10.1186/s40795-020-0331-6

Keywords

  • Edible insects
  • Animal-source food
  • Complementary food
  • Nutrient profile
  • Ghana

BMC Nutrition

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