Introduction

Poultry farming is one of the most important agricultural sub-sectors in many countries, which is supported by the governments and the private sectors with the aim of providing the meat and eggs for consumers (Michalak and Mahrose 2020). Reducing feed costs is a major concern for poultry meat and egg producers. Therefore, the need to find sustainable alternatives for poultry feeding is very important (Etemadian et al. 2021). In recent years, increasing interest in using insect-derived (ID) and marine-based (MB) feeds for animal nutrition has led to increase research studies in this field. On the other hand, the world population will exceed 9 billion people by the year 2050. Accordingly, food security and environmental problems will be among the most significant issues of that time. Therefore, in the near future, the demand for this type of animal feeds will increase significantly (Khan et al. 2018). The ID and MB ingredients are rich in valuable proteins, amino acids, fatty acids and energy, vitamins and minerals. Therefore, they will be suitable resources for animal nutrition. Replacing corn and soybeans with these compounds in poultry diet requires not only the evaluation of poultry performance and carcass characteristics, but also the sensory quality of the produced meat and eggs (Shaviklo et al. 2021a, b).

Although nutritional value is very important in the acceptance of a foodstuff, but its sensory quality is a priority for continuous buying and consumption of the product (Meilgaard et al. 2015). The sensory properties of feedstuffs affect the sensory quality of animal products such as meat and eggs, and in this context, it is necessary to know sensory attributes of feed ingredients. Providing such data are required before the introduction of food products to the market or when using new ingredients in livestock farming (Shaviklo et al. 2021a, b). The odor and flavor of fish and seaweed, bitterness, rancidity etc. are the sensory characteristics of the MB products that are used as animal feed. The ID ingredients have unique sensory attributes like chickpeas odor and flavor in mealworm powder (Shaviklo et al. 2021a).

The sensory characteristics of poultry meat and eggs are influenced by various factors including the genetics of birds, the farming system, the animal diet and the age of birds at slaughter (Al-Marzooqi et al. 2010). It is obvious that the use of the ID and MB products in poultry feed may cause significant changes in the approximate analysis and composition of meat fatty acids (Gasco et al. 2016) and sensory attributes of the poultry products (Shaviklo et al., 2021a,b).

To date, most of the published studies on using ID and MB ingredients in feeding poultries have focused mainly on growth performance, safety, and feed composition and utilization. However, sensory evaluation in considerable published studies has not been performed carefully. Therefore, the main purpose of this study is to provide a systematic review of research, using the following methodology, on ID and MB ingredients as they affect sensory attributes of poultry meat and eggs at different levels of inclusion. This study also tries to emphasize the importance of applying standard-based sensory evaluation in animal, including poultry nutrition studies when formulating new feed materials.

Research design and methodology

A systematic literature review that is based on synthesis methodology and described by Heyn et al. (2019) was carried out. Accordingly, the adapted methodology consisted following five important and distinct phases:

Study objective—There are conflicting reports regarding the use of ID & MD ingredients and their effects on the sensory properties of poultry meat and eggs. Therefore, the objective of this study was to compile and review literature on the subject and draw a clear conclusion from studies.

Literature search—Google Scholar database was searched for all available and updated literature from 1960–2022 on the use of ID & MD feed products for poultry farming and their influences on the sensory quality of meat and eggs. The relevant articles were compiled.

Data screening—Compiled articles were screened and only articles whose research methods of sensory evaluation were in line with standard methods were selected for reviewing.

Review—Each study was reviewed for synthesis. The research methods and outcomes of the studies were extracted. Accordingly, they were critically evaluated with complete impartiality.

Presenting the results: Factors affecting sensory quality of food products were defined. The ID and MD ingredients and their application in poultry diet were introduced. The sensory attributes of poultry meat and eggs fed with these compounds were discussed. Two summary tables were well-organized, to report the inclusion levels, avian species, farming period, sensory method, sample preparation and the sensory results which will help the readers to understand the topic clearly.

Factors affecting sensory evaluation results

Panelists’ selection and their training

The most important tool in product development and food quality control is establishment of an efficient sensory evaluation team. The objective of a study defines how to select and train the panelists, and this affects success or failure of the sensory assessment. The training of assessors and their experience is very effective in the ability to understand sensory differences or similarities. Therefore, if a similar sample is presented for sensory evaluation between two groups of trained and untrained assessments, having different results is not unexpected (Meilgaard et al. 2015). International Organization for Standardization (ISO) has issued relevant standards for sensory evaluation. ISO (8589: 2007) presents general guidance for the design of test rooms (ISO 2007) and ISO (8596:2012) describes general guidelines on how to select, train and monitor assessor’s performance which is recommended to be applied for food sensory analysis (ISO, 8596:2012).

Sensory evaluation methods

Sensory testing can be classified into two areas: analytical or objective and affective or subjective. Analytical testing is applied in the laboratory to reveal similarities or differences between the products by a selected and trained panel. Descriptive and discrimination tests are the most important analytical tests. In affective testing, the consumer’s reactions to sensory attributes of products are assessed using preference or acceptance tests (Meilgaard et al. 2015).

To distinguish differences or similarities of two products, differences or discrimination tests are used. Discrimination experiments generally use large numbers of participants to estimate the proportion of the population that can distinguish between the two products (Stone et al. 2020).

The triangle test is the most widely used test of sensory differentiation. Thresholds in sensory testing are usually expressed as the minimum detectable level of concentration of a substance. These tests are used for training of assessors. Descriptive tests or sensory profiling techniques are applied to determine sensory attributes and their severities. The most widely used descriptive techniques are Quantitative descriptive analysis (QDA) (Meilgaard et al. 2015; Stone et al. 2020). A successful descriptive analysis depends on 3 factors: training and experience of the assessors, designing and conducting the sensory test, and the role of panel leader in establishment and maintenance of a sensory panel (Meilgaard et al. 2015).

Sensory vocabulary

A sensory vocabulary is a list of standard lexicon prepared by a sensory team to determine the sensory attributes of a product, and it is used in the training of the assessors and for sample evaluation, too. The preparation of the vocabulary is one of the basic steps in descriptive sensory analysis (Meilgaard et al. 2015). To create a vocabulary, sensory assessors evaluate samples that, as far as possible, represent the entire product. They define terms to describe each sensory property of the samples and provide references for better comparison and understanding of the sensory properties. The terms mentioned in the vocabulary should be simple, broad, and complete, and include all product differences. In most cases, assessors also assign a score to each reference standard to determine the intensity of each sensory attribute (Stone et al. 2020). It is as an effective communication tool among different audiences such as assessors, sensory experts, food producers, marketing professionals, and suppliers who may have different perceptions of the correct sensory feature due to differences in perception, knowledge and background (Meilgaard et al. 2015; Stone et al. 2020). Shaviklo et al. (2021b) developed a vocabulary consisting of 17 terms for describing the influence of fish protein hydrolysate-based supplement on the odor, taste and flavor, and texture properties of cooked chicken breast fillets (Table 1). A lexicon for sensory evaluation of chicken eggs prepared by Feng et al. (2020) is presented in Table 2.

Table 1 Vocabulary prepared by Shaviklo et al. (2021b) used for sensory evaluation of cooked chicken breast
Full size table
Table 2 Sensory lexicon defined by Feng et al. (2020) for sensory analysis of chicken eggs
Full size table

The ID products

A high quality protein source for human and animal’s nutrition is insect (Khan et al. 2018). For example, the protein, fat and mineral contents of mealworm larvae was noted 52, 24 and 1% in dry sample, respectively (Zielińska et al. 2015). Zhao et al. (2016) reported that mealworm larvae contained about 32% fat, 5% ash and 51% protein, on a dry weight basis for yellow mealworm (Tenebrio molitor) larvae. They announced that this insect has a good amino acid composition.

Different forms of the ID products are used for animal feeding (Fig. 1). The whole insect powder, insect protein powder and insect oil are frequently used in the animal farming. Insects can be used as a substitute for soybean meal and fishmeal in livestock and poultry feed due to having 30–40% fat and 40–60% protein in dry basis (Khan et al. 2018). Changes in animal feed protein sources from soybean meal and fishmeal to insects lead to more efficient use of natural sources and lead to less greenhouse gas emissions. For these reasons, many researchers have tried to apply insect protein in poultry nutrition. Chickens raised in the wild collect and eat insects at all stages of life indicating that they are evolutionary adapted to feeding insects as a natural part of their nutrition. Therefore, application of insect proteins in the production of livestock and poultry feed and the development of insect breeding systems seems reasonable (Khan et al. 2018). The most important insects used for poultry feeding are: mealworm (MW), housefly (HF), black soldier fly (BSF), earth worm (EW), grasshopper (GH), silk worm pupae (SWP), Cirina forda (westwood), cricket and locust (Khan et al. 2018).

Fig. 1
figure 1

Different forms of insects used as feed in animal nutrition

Full size image

Broilers are single-stomach animals and any changes in the chemical composition of their feed can affect the sensory characteristics of their meat positively or negatively (Pieterse et al. 2019). In the use of insects in poultry feed, reports indicate that this ingredient improved the growth and performance of fed chickens. However, the sensory characteristics of insect-fed poultry meat or egg have not been carefully studied (Khan 2018).

In the last 60 years, little published document is available on the influence of feeding insects on the sensory quality of poultry meat. Some authors (Tables 3 and 4) provided important information on how to perform a sensory test, prepare and cook samples and design a liking scale. However, some other articles do not provide specific information about sensory methodology, sample preparation and assessors’ selection and training. They did not publish information about vocabulary designing to define sensory characteristics, how to set up the questionnaire, and whether the test was blind or not.

Table 3 Summary of researches carried out in the recent years reporting the influence of MB and ID ingredients on sensory attributes of poultry meat
Full size table
Table 4 Summary of studies implemented in the recent decades indicating effects of MB and ID ingredients on sensory attributes of poultry eggs
Full size table

Khan et al. (2018) conducted a study comparing the sensory characteristics of fed broiler chicken with different types of insect meal (e.g. mug meal, silkworm meal and mealworm) and concluded that the insect incorporated diet did not change sensory attributes (p > 0.05). Hwangbo et al. (2009) reported that the sensory attributes of chicken meat fed insect meal were not influenced (p > 0.05). Onsongo et al. (2018) also noted that incorporation of black soldier fly (H. illucens) meal in broiler feeding does not influence consumer preference for broiler breast meat consumption because the insect meals application did not alter the odor and flavor of meat (p > 0.05). These results are in line of Pieterse et al. (2019) study. However, chicken breast fillet fed with black soldier fly (H. illucens) had the strongest flavor (p < 0.05) among the treatments (Altmann et al. 2018). The larvae fed meat treatments scored significantly higher (p < 0.05) for juiciness compared to the fishmeal fed treatments. This study also indicated that broilers received larvae meal could have juicier meat (Pieterse et al. 2014).

Feng et al. (1985) studied differences between the meat of broilers fed the corn-ground cricket and corn-soybean meal diet using a triangle test with 26 panelists. No significant difference in the taste of two samples were reported (p > 0.05). Studies carried out on broilers fed several levels of black soldier fly (H. illucens) mealworm (Tenebrio molitor) indicated that there were no significant differences for the chicken meat color (Secci et al. 2018; Pieterse et al. 2019). However, other work (Pieterse et al. 2014) reported that application of black soldier fly (H. illucens) and housefly (Musca domestica) larvae influenced the broilers and quail’s meat color significantly (p < 0.05).

Application of insects in broiler quails and chickens diet did not influence (p > 0.05) sensory properties of the meat (Onsongo et al. 2018; Pieterse et al. 2019). Altmann et al. (2018) instead stated that black soldier fly (H. illucens) fed broiler breast had a strong taste that reduced within storage time (p < 0.05). A higher metallic odor and aftertaste values was reported by Pieterse et al. (2019) for broilers meat fed black soldier fly larvae (p < 0.05). The meat was juicier than chickens fed soybean flour and fish based diet. Khan et al. (2018) revealed that different level of maggot meal, silkworm meal and mealworm did not influence the chicken meat flavor (p < 0.05), but the chickens fed mealworm scored higher tenderness and juiciness values when compared to the other treatments (p < 0.05).

The influence of grasshoppers incorporated feed on sensory properties of chickens farmed in free-range and grassland-based systems were studied (Sun et al. 2013). The results indicated that all breast and thigh meats treatments had the same color and juiciness (p > 0.05), but significant higher scores (p < 0.05) for odor and flavor, chewiness and acceptance and lower scores for tenderness were observed for the chickens fed with grasshoppers compared to the control samples which received a maize-soybean feed.

Bovera et al. (2016) studied incorporation of black soldier fly meal at 29.65% level in broilers chicken diet feeding for 32 days. No significant influence on (p < 0.05) the broiler meat color was reported. Onsongo et al. (2018) reported that inclusion 5–15% black solder fly meal in broilers meat had no effect on odor and flavor (p > 0.05). Altmann (2018) reported the same results. Khan et al. (2018) studied inclusion of 7.8% silkworm (Bombyx mori), 8% housefly (Musca domestica) and 8.1% mealworm (Tenebrio molitor) larvae meal in broiler chicken diet for 35 days and reported that tenderness and juiciness of meat were significantly higher in mealworm group compared to the control and other treatments (p < 0.05).

Egg breed, breeding systems, and diets supplementation are factors influencing sensory attributes of egg (Zeweil et al. 2019). Al-Qazzaz et al. (2016) noted that an increase in black soldier fly application in laying hens, improved the shape and sensory attributes of obtained eggs compared to the control samples (p < 0.05). Incorporating more than 7.5%, fat free black soldier fly larvae in the corn-soybean diet for broilers from 19–27 weeks of age could increase egg yolk color intensity and eggshell thickness significantly (p < 0.05) as revealed by Mwaniki et al. (2018). However, a significant decrease (p < 0.05) in egg yolk color intensity of the free-range laying hens received black soldier fly larvae meal was noted (Ruhnke et al. 2018).

Secci et al. (2018) studied the influence of incorporating 17% black soldier fly larvae meal on laying hens fed 147 days and reported that it was contributed with the redder yolks (p < 0.05). It was in agreement with the work of Mwaniki et al. (2018) who applied 5 and 7.5% black soldier fly larvae meal in 182 days feeding in laying hen. Ruhnke et al. (2018) used 15% black soldier fly larvae meal in free-range laying hen for 12 weeks and reported that it decreased yolk color significantly (p < 0.05).

Dalle Zotte et al. (2019) incorporated 10 and 15% defatted black soldier fly larvae meal in laying quails for 6 weeks and reported that these levels of ingredients did not influence the sensory attributes of eggs significantly (p < 0.05). In another study (Bejaei and Cheng 2020) applied full fat dried black soldier fly larvae to feed brown layer pullets for 17 weeks. Inclusion levels (10 and 18%) did not change the sensory quality of eggs (p > 0.05), but the intensity of orange color was lower than the control treatment (p < 0.05).

The MB products

Fishery and aquaculture processing by-products include the rest of the raw materials of fish and marine crustaceans that are created after processing (filleting, canning, and packaging). These compounds are very nutritious and are commonly used to produce fishmeal and oil, fish protein hydrolysate (FPH) and silage to feed animals. However, these by-products are not fully utilized and this leads to economic and environmental problems in disposing of them. The proximate analysis and nutritional value of fishery by-products is considerable, and depends on different aquatic species (Etemadian et al. 2021). Different fish products are used in animal farming. Figure 2 illustrates the schematic processing methods of these products.

Fig. 2
figure 2

Schematic processing methods of marine based ingredients

Full size image

Fishmeal and oil

Fishmeal is a ground brown powder, which obtained after cooking of whole fish/ fish by-products, then dewatering or pressing, drying and milling. In countries where fishmeal is the cheapest animal protein, its use in poultry feed at the highest possible level is economically viable if the level of inclusion do not change the sensory quality of meat and eggs (Onsongo et al. 2018). Egg fortification with fish oil can influence sensory attributes, which affect consumer liking or preference (Fraeye et al. 2012). The severity of some adverse sensory characteristics such as fishy odor and sourness increases in the yolk as the amount of fishmeal and oil in the diet increases (Lawlor et al. 2010). Accordingly, to prevent fish odor and flavor in the product, it is suggested to use less than 1% fish oil and 12% fishmeal in the poultry diet (Leskanich, and Noble 1997).

FPH

The FPH is a product of breakdown of proteins that contains a mixture of polypeptides, peptides and amino acids. Enzymatic hydrolysis is one of the most important methods used for this purpose. FPH is a balanced amino acid and has a high level of essential amino acids that are extracted from various species of fish. This product can be included in poultry diet as an alternative to fish and soymeal. In addition, FPH improve protein digestibility. Commercial products of FPH are in powder, paste and liquids. The FPH is a valuable source of protein in human food and animal feed, especially for chickens (Etemadian et al. 2021).

Fish silage, a chemical treated form of FPH is a stable semi-liquid product that requires less investment and technology for manufacturing. It is a good substitute of fishmeal or soybean flour as a source of animal protein in regions where there are low-cost fish or sufficient fish processing by-products (Al-Marzooqi et al. 2010). Qiao et al. (2002) reported that using fish silage improves the growth efficiency of broilers, but sensory panelists recognized the unpleasant fish flavor in poultry meat fed 30% fish silage (p < 0.05). As it was mentioned, fish oil is the most important factor affecting sensory attributes of animals including chicken meat. Residues of fat in FPH including fish silage can may adversely influence the meat sensory quality (Ramírez et al. 2013). However, carcass discoloration is observed when fish products exceed the desired levels in the poultry diet (p < 0.05). In general, up to 20.5 of soybean meal can be substituted with fish silage in chicken nutrition without influencing the performance and sensory quality of the meat (Al-Marzooqi et al. 2010).

Seaweed

Seaweed is a biologically active compound that can be used to feed poultries. The brown seaweed is mostly used in poultry nutrition. Several species of brown, red and green species are used in livestock feeding. Seaweeds are suggested as feed ingredients because of their high content of micro-and macroelements and they can contribute in the growth and performance of poultries and the quality of produced meat and egg quality (Michalak and Mahrose 2020). Seaweed polysaccharides have probiotic activities and can enhance poultry health and performance and improve egg quality. Seaweed can also be used in laying hens and broilers feed to fortify eggs and chicken meat with omega-3 fatty acids (Zeweil et al. 2019).

Microalgae can partially replace soybean meal, corn, sorghum and mineral salts in poultry diet. The level of seaweed incorporation influences the chicken carcass quality. Significant color changes (p < 0.05) from yellowish to reddish when 5–15% of S. muticum was included in diet was reported (Erum et al. 2017). Athis Kumar (2018) reported that flavor, color, tenderness and juiciness of chicken meat which broilers received 1% or 2% of Sargassum wightii scored the highest sensory liking by the consumers (p > 0.05).

El-Deekx et al. (2009) reported that the breast muscle color was not influenced when male broiler chicken (Ross) which fed 3% of the seaweed by any dietary treatment (p > 0.05). Seaweed at the levels of 15% and 5 and 10% improved the texture of breast and thigh meats significantly (p < 0.05). No significant differences (p > 0.05) in the odor, flavor, juiciness and color of meat was observed (Michalak and Mahrose 2020).

The maximum level of seaweed in the diet of laying hens is 10% (Carrillo-Dominguez et al. 2008). Seaweed carotenoids can increase the pigmentation of egg yolk. Significant increasing (p < 0.05) of the total carotenoids in egg yolks when incorporating brown algae (sargassum dentifebium) at level of 3 and 6% was reported (Michalak and Mahrose 2020). Feeding chickens with seaweed can improve the physical and biochemical quality of eggs. The weight, quality of egg shell, including its thickness and strength are important indexes for poultry farmers as well as consumers. Consumers prefer eggs with golden yolks (El-Deek et al. 2009).

Few studies are available on the use of microalgae oil in the laying hen’s diet, the results of which indicate the effect of this ingredient on the sensory properties of eggs (Feng et al. 2020). However, excessive use of algae has a negative effect on the egg sensory quality (Al-Marzooqi et al. 2010). Carrillo-Dominguez et al. (2008) reported that the application of 10% Macrocystis pyrifera, and Sargassum sinicola and 2% sardine oil to the diet did not influence egg flavor (p > 0.05). In another research, no significant difference (p > 0.05) was detected for eggs flavor produced from the hens received 2.4% marine macroalgae in comparison to the control treatment (Herber-McNeill and van Elswyk 1998). Rendón et al. (2003) revealed that egg flavor was not influenced by the incorporation of post extraction residue from Macrocycstis pyrifera at the level of 5% in poultry feed (p > 0.05). Eggs from laying Japanese quails received dried Ulva fasciata (1.5%) and Sargassum cinereum (3%) in their diet had better physical and sensory quality like egg yolk weight, color index and eggshell thickness (Zeweil et al. 2019).

Conclusions

The ID and MB products show great potential for animal feeding to overcome animal feed shortages and to provide animal proteins. The ID and MB products are good sources of nutrients for poultry feeding that can be partially replaced by soybean meal, corn and fishmeal. However, using such ingredients, in poultry diet, influences the sensory properties of meat and eggs negatively or positively. Researchers have used different ratios of these ingredients in the poultry diet studied and other components of the diet have not been the same in all researches. Therefore, the results of the similar studies cannot be compared. But the levels of using these compounds and perceived sensory attributes can be used as guidelines for other researchers and industry to determine the optimum level of inclusion of such products and using them in a stable manner. Information on metabolism of these products in the poultry’s body and the end products responsible for their effect on sensory quality of meat and egg, is an interesting topic for further research in this field of study. Furthermore, the provided sensory data could be used in the commercial application of the ID and MB ingredients in poultry nutrition.