Iron and zinc concentrations in insects compared with livestock animals

Analyses of both Fe and Zn concentrations in the same edible insect species showed Fe contents ranging between 4 and 62 mg/100 g DM and Zn contents between 9 and 27 mg/100 g DM for eleven edible species that are mass-produced and six species that are collected from nature (Table 1). Fe content reported for the termite Macrotermes subhyalinus Rambur (Isoptera: Termitidae) is an outlier, causing the range for Fe contents to be wider than for Zn contents.

Table 1 Protein, iron and zinc content for a selection of insect species consumed by humans (Mean values and standard deviations where available)

* The first eleven species are globally mass-reared; the last six species are collected from nature.

Comparing three commonly mass-reared insect species with common livestock species shows that the Fe and Zn concentrations in yellow mealworms, Tenebrio molitor L. (Coleoptera: Tenebrionidae) are higher than for chicken and pork, but lower than for beef (Fig. 1). However, both African migratory locusts, Locusta migratoria L. (Orthoptera: Acrididae), and house crickets, Acheta domesticus L. (Orthoptera: Gryllidae), contain similar amounts of Zn and higher amounts of Fe, compared with chicken, pork and beef.

Fig. 1 Iron (a) and zinc (b) content on a DM basis in meat from conventional production animals (beef (); pork (); chicken ()) and in three insect species (yellow mealworm Tenebrio molitor L. (), house cricket Acheta domesticus L. () and African migratory locust Locusta migratoria L. ()). Data for conventional meat were adapted from the US Department of Agriculture (USDA) food database (USDA National Nutrient Database for Standard Reference, release 28; Agricultural Research Service, USDA, Nutrient Data Laboratory; http://www.ars.usda.gov/nea/bhnrc/ndl, selecting data on meat only (excluding pure fat and organs)) reporting both iron and zinc concentrations. Insect data were adapted from references⁽ Reference Barker, Fitzpatrick and Dierenfeld ^{19 ,} Reference Finke ^{20 ,} Reference Oonincx and Van der Poel ^{21 ,} Reference Zielińska, Baraniak and Karaś ^{22 ,} Reference Finke ^{25 )}. Values are means, with standard deviations represented by vertical bars.

More detailed examination of the Fe, Zn and crude protein contents of insects reveals significant correlations between Fe and Zn contents (Spearman’s ρ=0·592; P<0·001; n 48), and between Fe and Zn contents and body crude protein content (Spearman’s ρ=0·443; P=0·002; n 48; and ρ=0·693; P<0·001; n 48 for Fe and Zn, respectively; Fig. 2). Factors that contribute to differences in Fe and Zn concentrations are species (Table 1), developmental stage and diet⁽ Reference Finke and Oonincx ^{18 )}.

Fig. 2 Scatter plots of iron content, zinc content (both expressed as mg/100 g DM) and crude protein content (% DM) of sixteen of the seventeen insect species listed in Table 1. Data for Macrotermes subhyalinus were considered outliers and have been excluded. (a) Iron content (mg/100 g DM) plotted against zinc content (mg/100 g DM) (Spearman’s ρ=0·592; P<0·001; n 48). (b) Iron content plotted against crude protein content (Spearman’s ρ=0·443; P=0·002; n 48). (c) Zinc content plotted against crude protein content (ρ=0·693; P<0·001; n 48).

Biochemical forms of iron and zinc in insects

As for humans, dietary Fe and Zn are essential for proper physiological functioning of insects, fulfilling roles in DNA synthesis, oxidation, cuticle biosynthesis and acting as a cofactor in a variety of enzymes⁽ Reference Locke and Nichol ^{35 ,} Reference Vallee and Falchuk ^{36 )}. Transferrin and ferritin are two major proteins involved in Fe metabolism in insects, both having multiple functions. Transferrin is an Fe transporter, it might act as an antibiotic agent and it can be a vitellogenic protein⁽ Reference Nichol, Law and Winzerling ^{37 )}. Ferritin functions in Fe transport and storage and is present in the endoplasmatic reticulum, nuclear envelope and mitochondria of gut and fat body cells in particular, and extracellularly in the haemolymph⁽ Reference Pham and Winzerling ^{38 ,} Reference Nichol and Locke ^{39 )}. Multiple studies investigating the transport mechanisms of Zn in insects have focused on Zn transporters in the model species Drosophila melanogaster. Thus far, two families of Zn transporters have been identified, ten dZip and seven dZnT proteins⁽ Reference Lye, Richards and Dechen ^{40 )}. These transporters are homologues to the human Zip (SLC39) and ZnT (SLC30) family members and are responsible for cellular influx and efflux, respectively. Zn transporters can be found ubiquitously or accumulated in specific organs/regions of the gastrointestinal tract, for example, the expression of dZip1 in the midgut and dZnT35C in the Malpighian tubules of D. melanogaster ⁽ Reference Lye, Richards and Dechen ^{40 –} Reference Qin, Wang and Zhou ^{42 )} that have roles in the absorption and excretion of Zn. Much less information is available on Zn storage in insects. Zn is present throughout the gastrointestinal tract of D. melanogaster with accumulation regions in the posterior midgut, the crop and the Malpighian tubules⁽ Reference Jones, de Jonge and James ^{43 )}. As most information on the physiological functions of Fe and Zn in insects stems from research on D. melanogaster, it remains to be investigated whether the information is representative for the edible insect species which are the focus of the present review. Some differences in Fe metabolism between different insect orders have been demonstrated, showing different allocations of ferritin in midgut cells⁽ Reference Nichol and Locke ^{39 )}.

Bioavailability of iron and zinc in insect-derived food

Nutrient bioavailability refers to the proportion of a nutrient that is absorbed from the diet and used for normal body functions⁽ Reference Hurrell and Egli ^{44 ,} Reference Aggett ^{45 )} and is governed by host-related and food-related factors such as the food matrix and the chemical form of the nutrient in question. Internal factors may include age, sex, nutrient status and life stage (for example, pregnancy). Nutrient bioavailability depends on different processes, including release of the nutrient from the physico-chemical food matrix; effects of digestive enzymes in the intestine; binding and uptake by the intestinal mucosa; transfer across the gut wall to the blood or lymphatic circulation; systemic distribution; systemic deposition; metabolic and functional use; and excretion via urine or faeces⁽ Reference Aggett ^{45 )}.

In vertebrates, Fe is usually found in muscles in the form of myoglobin and Hb. However, the primary form of haem-Fe in insects is found in cytochromes. It is presumed that the bioavailability of cytochrome haem-Fe is similar to that of myoglobin and Hb⁽ Reference Locke and Nichol ^{35 )}. Fe in insects is predominantly present as the non-haem molecules ferritin and holoferritin. Because ferritin functions as a storage protein for Fe, each molecule is capable of containing thousands of Fe atoms, typically in the ferrous state, which increases their bioavailability. Insect ferritin has not yet been well characterised, although it is known to differ from the ferritin found in vertebrates⁽ Reference Nichol and Locke ^{39 )}. Phyto-ferritin, present in legumes such as soya, appears to be better bioavailable than Fe in the form of reduced salts⁽ Reference Beard, Dawson and Piñero ^{46 –} Reference Lönnerdal, Bryant and Liu ^{51 )}. This is explained by protection of Fe from ANF, such as phytates, oxalates and tannins, by the protein complex. Although much of the diet-derived ferritin may not reach the intestinal absorption site intact, due to destruction during cooking and gastric digestion⁽ Reference Hoppler, Schönbächler and Meile ^{52 )}, the suggestion of a separate transporter for phyto-ferritin in human cells indicates that there is an absorption potential⁽ Reference San Martin, Garri and Pizarro ^{53 )}. Even if only a small fraction of the original amount reaches the absorption site, it can have a tremendous impact due to the large number of Fe atoms present in ferritin proteins.

Bioaccessibility (in vitro solubility or dialysability of a nutrient)⁽ Reference Holst and Williamson ^{54 )} of micronutrients present in various species of edible insects has not been widely studied but is expected to follow trends of meat, fish and poultry. However, the non-haem-Fe present in most edible insects may be poorly soluble under intestinal conditions and may also be affected by other components of the diet⁽ Reference Hurrell and Egli ^{44 )}. Furthermore, the impact of known enhancers and inhibitors of nutrient bioavailability on (micro)nutrients present in edible insects is not known. Examples of nutrient enhancers include the ‘meat factor’ present in meat, fish and poultry thought to be a result of muscle protein, which enhances absorption of Fe from all foods⁽ Reference Hurrell and Egli ^{44 )}. Protein (more specifically: amino acids such as histidine and methionine) is known to enhance non-haem-Fe and Zn absorption⁽ Reference Hurrell and Egli ^{44 ,} Reference Lönnerdal ^{55 )}; therefore, insects with a high protein content might promote the uptake of these minerals.

Recently, the in vitro solubility and availability of Fe and Zn from various insect species (grasshopper, cricket, mealworms and buffalo worms) have been compared with those from sirloin beef using a Caco-2 cell model. It was found that Fe and Zn solubility was significantly higher from the insect samples than from beef, but bioaccessibility of Fe (measured as the ferritin concentration in Caco-2 cells) was more diverse, with the highest response for buffalo worms (Alphitobius diaperinus Panzer; Coleoptera: Tenebrionidae), followed by beef, yellow mealworms, cornfield grasshoppers (Sphenarium purpurascens Charp.; Orthoptera: Pyrgomorphidae), and two-spotted crickets (Gryllus bimaculatus Geer; Orthoptera: Gryllidae)⁽ Reference Latunde-Dada, Yang and Vera Aviles ^{56 )}. In the same study by Latunde-Dada et al. ⁽ Reference Latunde-Dada, Yang and Vera Aviles ^{56 )}, it was shown that the addition of insects to wheat flour (1:1) was superior to beef in increasing Fe and Zn solubility in the composite mixtures.

Based on the above, it is likely that the addition of insects to current starch-based diets, exemplary for individuals living in many low- and middle-income countries (LMIC), will provide additional Fe and Zn, that could potentially fill the requirement gap, and maybe increase the bioavailability of native and fortification Fe in the starchy foods. As an example, a complementary feeding cereal enriched with locally derived dried caterpillars showed a small increment in Hb concentrations in infants and children in the DRC Congo⁽ Reference Bauserman, Lokangaka and Gado ^{57 )}. A better understanding of the bioavailability of Fe and Zn from insects may help to improve the design of such a strategy. In addition, good bioavailability of Fe and Zn will also mean that insects are a valuable food item for consumers in other parts of the world, including Europe and North America.

Anti-nutritional factors

ANF are compounds that interfere with the absorption of one or more nutrients from human food, animal feed or water⁽ Reference Atwood, Cammack and Atwood ^{58 )}. Diets laden with ANF such as phytic acid can cause micronutrient malnutrition by reducing the bioavailability of micronutrients such as Fe and Zn. In many LMIC, micronutrient malnutrition is further exacerbated by the consumption of monotonous staple food-based diets which contain enough energy to ease hunger pangs but not enough micronutrients. In addition, the staple foods are usually high in ANF.

An important ANF reducing Fe and Zn absorption is phytic acid, which is the storage form of P in grains, nuts and legumes. When chelated to a mineral in the seed, phytic acid is known as phytate. Phytic acid is highly abundant in some plant foods (wholegrain cereals, pulses, seeds, nuts) and it binds minerals such as Fe, Zn and Ca, thereby decreasing their bioavailability⁽ Reference Schlemmer, Frølich and Prieto ^{59 )}. This is because it forms soluble or insoluble complexes that cannot be absorbed⁽ Reference Zhou and Erdman ^{60 )}. Similarly, other inhibitors of nutrient absorption may bind the nutrient, render the nutrient insoluble, or compete for the same uptake system. The latter has been observed in the interaction between Ca and non-haem-Fe, especially when Ca and/or Fe supplements are used outside the meal setting⁽ Reference Gibson ^{61 )}.

Phytic acid content varies greatly among plants due to the type/species of seed, environmental condition, climate and soil quality⁽ Reference Schlemmer, Frølich and Prieto ^{59 )}. In grains, phytic acid is primarily found in the bran while in legumes it is found in the cotyledon layer⁽ Reference Schlemmer, Frølich and Prieto ^{59 )}. With the exception of phytic acid, the extent to which other ANF such as polyphenols and tannins affect the bioavailability of Fe and Zn in humans is not clearly established. Management and control of dietary inhibitors and enhancers is critical. For example, the bioavailability of non-haem-Fe, such as that found in plant foods, eggs and milk, is inhibited by phytates but may be enhanced by vitamin C. Practical ways to reduce dietary inhibitors and increase Fe absorption also include fermentation, germination, malting and adopting food fortification practices, i.e. dietary modification strategies to either include in a meal foods that can promote the absorption of a micronutrient or to exclude foods that inhibit its absorption. Whether Zn and the biochemical form of Fe present in edible insects are affected by ANF is a critical consideration worth further research because cereal-based staple foods are consumed in the same meal as the insects.

Nutrient bioavailability also responds to systemic factors such as deficiency of a nutrient or changes in the physiological state, for example during pregnancy⁽ Reference Gibson ^{61 )}. This may result in the up-regulation or down-regulation of the absorption of a nutrient. Similarly, infections and inflammation may reduce the absorptive capacity of the gut⁽ Reference Lynch ^{62 )}. It is important to know the bioavailability of nutrients such as Fe, Zn, folate, Ca, Mg and vitamin A in order to translate their physiological requirements into actual dietary requirements⁽ Reference Gibson ^{61 )}.

Effect of food preparation methods on the mineral content of edible insects

The nutrient quality of different foods can be altered by different methods of food processing such as frying and boiling⁽ Reference Severi, Bedogni and Manzieri ^{63 )}. Cooking loss of minerals may be caused by the outflow of minerals from the food materials⁽ Reference Kimura and Itokawa ^{64 )}. These losses can be prevented by various methods such as: (a) eating the boiled food with the soup made using the water/stock of the boiled food; (b) boiling in salted water (up to about 1 % NaCl); (c) avoidance of too long boiling; and (d) using cooking methods that cause a lesser amount of mineral losses, for example, stewing, frying or parching⁽ Reference Kimura and Itokawa ^{64 )}. Most insects are either sautéed, baked, ground into a paste before addition to foods, stewed, boiled or fried. Numerous websites offer recipes for cooking insects⁽ Reference Oaklander ^{65 )}. As is the norm for any food product, consumer education aimed at the retention of nutrients from edible insects before, during and after cooking must be systematically introduced alongside the insect products. So far, the effect of various food preparation methods on the micronutrient/mineral content of various insect sources has not been fully investigated.

Conclusions and implications

The relative contribution of diets rich in edible insects towards solving micronutrient malnutrition needs to be quantified. Preliminary findings suggest that Fe biofortification of staple food crops can be efficacious for improving Fe status⁽ Reference De Moura, Palmer and Finkelstein ^{66 –} Reference King, Brown and Gibson ^{69 )}. Furthermore, although the inclusion of animal foods in the diet can be a good strategy to combat micronutrient malnutrition, this is often not affordable for the individuals suffering from micronutrient malnutrition and thus often is an unsuitable option. The Lancet series on interventions for improvement of maternal and child nutrition identified the need for innovative community-based strategies for scaling up the coverage of nutrition interventions that have the potential to reach especially the poor populations⁽ Reference Bhutta, Das and Rizvi ^{3 )}.

The information on Fe and Zn contents in edible insects is at present still limited and best documented for the species discussed in the present paper which feature in human diets around the world⁽ Reference Jongema ^{70 )} and which are also good sources of protein, fat and dietary fibre⁽ Reference Finke and Oonincx ^{18 )}. Consumption of edible insects is widely practised in parts of Africa, Asia and Latin America. Current estimates are that insects form part of the diet of about 2 billion individuals, in particular in tropical areas of the world⁽ Reference Van Huis, Van Itterbeeck and Klunder ^{71 )}. Therefore, insects are receiving increasing attention for their potential to alleviate the projected protein shortage by 2050⁽ Reference Van Huis, Van Itterbeeck and Klunder ^{71 ,} Reference Van Huis ^{72 )}.

Although the consumption of edible insects has been shown to contribute to protein intake⁽ Reference Lizot ^{73 –} Reference Kitsa ^{77 )}, the contribution of edible insects to the micronutrient pool has not been explored. We postulate that the addition of edible insects to the human diet, either whole, in-part, or processed, will greatly contribute towards the achievement of the ‘zero hunger’ sustainable development goal target, especially because the large majority of the hungry individuals (98 % of 795 million individuals) who also suffer from hidden hunger live in LMIC^{( 78 )} where edible insects are widely accepted.

The global human population is growing rapidly and is expected to reach 9–10 billion individuals by 2050. At present, 70 % of the global agricultural land is used to produce livestock that provide meat and dairy products as favoured protein sources⁽ Reference Van Huis, Van Itterbeeck and Klunder ^{71 )}. Increasing the production of livestock is seriously constrained by the availability of agricultural land and will aggravate climate change⁽ Reference Hedenus, Wirsenius and Johansson ^{79 )}. Insect production requires much less agricultural land per unit protein produced and contributes much less to climate change than livestock⁽ Reference Oonincx and De Boer ^{80 )}.

Regarding bioavailability of Fe and Zn from insect-derived food, only data from an in vitro experiment are available. Although the results are promising, in vivo studies on human subjects are required to quantify the absorption efficiency of Fe and Zn from insect-containing foods. Insects are receiving increased attention primarily due to their high protein content which is favourable for enhancing the uptake of Fe and Zn. Factors that may interfere with Fe and Zn absorption from insects such as processing, preservation, preparation and combinations with other foods need to be addressed in controlled studies to allow full utilisation of the potential of insects as Fe and Zn sources in human diets⁽ Reference Glover and Sexton ^{81 )}.