Meat quality of poultry fed with diets supplemented with insects: A review

The development of sustainable feed ingredients for monogastric livestock is now also considering insect products. Although the regulation on the use of insect products differs among countries, resulting in restrictions on use in poultry diets, global research is exploring all the strengths and weaknesses of their inclusion. The scientific literature has extensively studied the relationship between insect-containing diet and effects on ante-mortem factors in fish and poultry, however the relationship between insect-containing diet and meat quality has only recently been considered. This review aims to collect the results of the studies that have related the dietary use of some insect species, such as the black soldier fly (Hermetia illucens), the yellow mealworm (Tenebrio molitor) and the silkworm (Bombyx mori), on the physicochemical and sensory traits of poultry meat. The insect source in poultry diets rarely changed the related physicochemical variables or the sensory profile of the meat, whereas the fatty acid (FA) profile was the variable that was most affected, and inclusion of black soldier fly always resulted in meats with a more saturated FA profile, yellow mealworm in a more monounsaturated FA profile, whereas silkworm produced meat with a more unsaturated FA profile, rich in valuable omega-3 FA.


Introduction
Statistics about demographic trends depict that by 2050 the world population should reach 9.1 billion people. This scenario is putting pressure on the search for alternative and sustainable feed resources, and among them insects, for the livestock sector [1]. In addition to the above reason, the use of insects in avian species feeding is supported by the fact that about 80% of birds are reported to include insects in their diets [2]; such birds include chicken (Gallus gallus), turkey (Meleagris gallopavo), guinea fowl (Numida meleagris), quail (Coturnix coturnix), and ostrich (Struthio camelus), which are species of interest for food production in different regions of the world [3,4,5,6].
To exploit their maximum potential as feed ingredients, insects are processed to obtain whole insect meal (full-fat), protein meal (PAPs) which can be defatted or contain some proportion of lipids according to the extraction method, and fat/oil. The fatty acid (FA) profile of insect lipids can be very extreme: two examples are the black soldier fly (Hermetia illucens; BSF) and the silkworm (Bombyx mori; SW). The fat extracted from BSF larvae contains 60-79% saturated fatty acid (SFA). Conversely, the SW chrysalis is very rich in omega-3 PUFA [7], and its oil presents a favourable n-6/n-3 ratio of 0.17 (personal communication). Thus, combining full-fat or partially defatted insect meal from different species could help ensure the best FA profile for animal feed [8]. The amino acid profile also differs between the different species of insects; in the case of the yellow mealworm (Tenebrio molitor; TM) larva, the content of all individual amino acids was found to be higher than that of barley, fish, brewer's yeast, beef/veal, and crustaceans, except for lysine, which was slightly higher in brewer's yeast [9]. Research studies conducted so far have tested a wide range of levels of substitution (5-100%, mainly substitution of fishmeal or soybean meal) or inclusion (0.75-60%) of insect meal, to find the best level, to cover nutrient requirements and to maximise growth and health performance, and product quality from farmed aquatic and terrestrial animals [10].

Insects in poultry feeds and meat quality
The effects of including dietary insect products (larva meal, pre-pupa meal, oil) on the quality of foodproducing terrestrial animals have been studied mainly in poultry. The purpose of this review is to provide updated literature on the use of insect-based products as feed for poultry broilers, detailing the effects on the physico-chemical-sensory quality of the meat obtained. The review will consider the BSF (Hermetia illucens), the TM (Tenebrio molitor), and the SW (Bombyx mori), the first two for the greatest commercial interest in the EU, the third because it is potentially interesting in improving the dietarynutritional value of meat.

Dietary inclusion of black soldier fly (Hermetia illucens) and meat quality
The BSF larva is one of the most commonly used organisms for aquaculture and one of the best studied for both aquaculture and poultry feeding. The BSF larva averagely contains 43.1±5.05 g protein/100 g dry matter (DM), and the amino acid profile is rich in leucine (6.72 g/100 g protein), lysine (6.22±1.08 g/100 g protein), and valine (5.38±0.82 g/100 g protein). Nutritionally important is also its contribution in calcium (24.1±12.8 g/kg DM) and phosphorus (6.01±1.77 g/kg DM) [11]. As aforementioned, the amount of larva fat and its FA profile are extremely variable and depend on the type of substrate. A description of the results obtained on the meat quality of poultry is provided below. Based on numerous studies (Table 1), the BSF as meal or fat in poultry diets has no [12,13,14,15,16,17,18,19,20,21] or limited influence [14,15,20,21,22,23] on physical meat quality (pH, colour, water holding capacity (WHC), shear force) of broiler chicken, quail, Barbary partridge, and Muscovy duck. Similarly, the poultry meat proximate composition also showed variable results, and they do not seem related to the insect meal inclusion level. Differences in meats' nutrient composition were mainly observed as more protein content [15,23], lowered [18] or increased [16,24] essential amino acids, and for enrichment in minerals, like calcium [24], sulphur [22], and copper [13]. In general, the sensory evaluation of poultry meat derived from animals fed diets supplemented with BSF did not differ from that obtained from control diets [14,17,24]. Instead, the BSF inclusion as meal or fat had a major contribution in modifying the FA profile of the lipids in the poultry meat [13,14,15,16,18,20,22,23,24,26,27]. The FA profile of the meat of monogastric animals is in line with the pattern of that of their diet, and the BSF (whatever its form) is rich in SFA, which make up approximately 70% of the total FAME, of which 43% constitutes C12:0 [21]. Therefore, it follows that the proportion of SFA in meat increases as a function of the dietary inclusion level of the BSF. In the majority of cases, this implies a worsening of the n-6/n-3 ratio [16], but either insect defatting or defatting their food substrate might not change [22] or could improve [18] the omega-6/omega-3 ratio. If the FA profile of the meat is changed by the inclusion of the BSF in the poultry diet, changes in the lipid oxidation of the meat is also expected. However, most of the studies did not observe changes in the oxidation of meat lipids in animals fed BSF [13,24,26]. However it is interesting to note that [12] observed a significantly low TBARS value in fresh meat after 7 days of refrigerated storage, and authors attributed it to the improved antioxidant activity (measured through the DPPH radical scavenging activity) of the meat due to the inclusion of the BSF in the diet.

Dietary inclusion of yellow mealworm (Tenebrio molitor) and meat quality
The yellow mealworm (TM) larva meal is considered a nutritionally suitable substitute for fishmeal and soybean in aquaculture and poultry diets, although its cost is currently too high and it cannot financially compete with standard feed sources. It should be emphasised that the strength of this feedstuff, therefore, lies in the high protein content (Nx6.25: 56-61%), characterised by a high biological value, as it includes all the essential amino acids in favourable proportions. Furthermore, it is a rich source of phosphorus [11] and potassium [9]. The fat (25-30% of TM meal) contains approximately 24% saturated FA, 24% polyunsaturated FA, and 50% monounsaturated FA, resulting in an omega-6/omega-3 ratio of 24 [9]. Contrasting results were obtained for physicochemical traits of meat from chicken broilers, apparently not depending on the inclusion level of TM meal (Table 2). However, the majority of the studies did not observe change in the meat pH, colour, moisture loss, shear force or fatty acid profile [28,29,30]. Instead, [31] observed that WHC, lipid and ash contents, TVB-N and sensory attributes worsened as the level of TM in the diet increased, and the authors partly attributed this trend to the possible presence of oxidised fat in dried insect meal. On the other hand, no other studies, testing higher TM inclusion levels, found adverse effects on sensory traits; on the contrary, [32] observed an improvement in meat juiciness and tenderness. When other poultry species were considered, such as Barbary partridge [20] and quail [33], no substantial differences in the meat physicochemical traits were observed due to the use of moderate to high levels of TM in the diet. Only meat colour changed in both bird species, although with an unclear pattern. The FA profile of the Barbary partridge meat was significantly affected by the dietary TM inclusion, particularly at the higher substitution level (50% of the soybean meal) [20]. FA changes resulted in the reduction of the C18:0 and omega-6/omega-3 ratio and the increase of C14:0, C15:0, C16:1, and C18:1 (P<0.05).

Dietary inclusion of silkworm (Bombyx mori) and meat quality
The silkworm pupa is characterised by high protein content (53.9% in the full-fat meal, 66.7% in the defatted meal), by a variable amount of lipids (29% in the full-fat meal, 9.5% in the defatted meal), the latter able to provide an extremely healthy FA profile (omega-3 FA: 29.5% and 31.5% total FAME, in the full-fat and defatted meal, respectively), suggesting that it is a valuable nutritional ingredient for feed of different monogastric livestock species [7]. Silkworm pupa meal has been successfully included in chicken broiler diet (Table 3), as it produced no effect on colour values, lipid content [34] or on sensory attributes [28,32] of the meat. A slight effect was observed in lipid content (3.56 vs. 4.48% for leg meat of control and treated broilers, respectively) in the study of [28] and in protein and ash contents (however, differences were not coherent with the inclusion level; [34]). Meat pH increased with the SW meal inclusion level, but it did not impair meat colour [34]. The best result for the dietary inclusion of SW pupa meal in chicken diets concerns the FA profile of the meat lipids: the PUFA n-3 increased, and the omega-6/omega-3 ratio decreased with the increase of the dietary SW meal substitution level (P<0.01). The C18:3 n-3 content in breast meat ranged from 6.75 to 15.0 to 28.4 mg/100 g meat, for control, 25% and 50% SW meal inclusion levels, respectively (P<0.05; [34]).

Conclusions
The great economic impulse towards the use of insects as food and feed for ecological-environmental sustainability purposes has generated new companies producing insect meal and derivatives. A flywheel of interest has therefore been generated on several fronts, and the use of these products increasingly requires confirmation of safety and efficacy. In the last five years, much research has been conducted relating to the use of insects for alimentary use. Many of these studies aimed at the feed sector, which, however, has mainly considered the effect of their use on animal ante-mortem variables, whereas the study of the effects on nutritional, rheological and sensory quality of the meat has only intensified significantly in the last two years. This review focused on collecting and describing the results of research conducted so far on the effect of insects as feed on the meat quality of avian species. The results showed different effects, more depending on the insect species used than on the avian species that benefited from them. Overall, no adverse effects were observed on meat quality. Only the meat's FA profile was affected by the insect species included in the diet, suggesting its improvement through manipulation of the insect substrate, or the use of mixtures of insect meal or oil from different insect species.