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. 2021 Jan 3;58(12):4587–4597. doi: 10.1007/s13197-020-04946-w

Sensory attributes and meat quality of broiler chickens fed with mealworm (Tenebrio molitor)

Amir Reza Shaviklo 1, Amir Hossein Alizadeh-Ghamsari 2,✉, Seyed Abdullah Hosseini 2
PMCID: PMC8479021  PMID: 34629523

Abstract

The influence of mealworm (MW) as a dietary protein source on the quality and sensory characteristics of the broiler meat was evaluated. 400 day-old male broilers were randomly distributed into 4 groups using a completely randomized design. Each group was replicated 5 times with 20 birds per replicate. Dietary feeds were included 4 levels of MW (0, 1, 2, and 3%) and fed from 1 to 24 days of age. Chickens took a normal diet (without MW) from 25 to 42 days of age. On days 24 and 42, four birds from each replicate were slaughtered and eviscerated. Sensory attributes were carried out on raw carcass and cooked breast meat using a quantitative descriptive analysis method. Proximate analysis, Water Holding Capacity (WHC), pH, Total Volatile Base Nitrogen (TVB-N), and texture analysis were also done on chicken breast meat. On day 24, significant differences were observed between control and birds fed with MW in terms of fat, ash, pH, TVB-N, WHC, and lightness of carcass. The highest TVB-N (35.50 ml/100 g N), and the lowest WHC (71.60%) were observed in bird received 3% MW. The control had better sensory attributes than those fed with MW in terms of skin color, meat color, abdominal cavity odor, and texture. On day 42, no significant difference was observed in sensory attributes of carcass and chicken meat except for juiciness. Dietary inclusion of MW up to 3% may be appropriate and sensory attributes and meat quality of broilers may adversely be influenced in higher levels.

Keywords: Sensory, Broiler, Mealworm, Carcass, Meat quality, Protein source

Introduction

In recent years, the animal farming industry has grown very fast and among them, broiler chickens are the most abundant domestic species used for poultry meat production (Khan et al. 2018). This industry is also facing major challenges such as high costs and limited feedstuffs mainly protein sources like soybean and fishmeal. Therefore, there is a need to look for alternative cheaper and easily available animal feed protein ingredients (Choi et al. 2018).

These challenges may, however, be overcome by using insects as a protein source in broiler diets (Khan et al. 2018; Dabbou et al. 2019). Palatability of insect meal by poultry and other animal species has been reported and found that it can replace 25–100% of soybean or fishmeal in poultry feeds (Makkar et al. 2014) without compromising bird performance (Van Huis et al. 2012).

The mealworm (MW) (Tenebrio molitor) of dark beetle larvae contains a great deal of protein, fat, amino acid, and minerals (Makkar et al. 2014). Despite widely reporting of MW in poultry diet, there is not any published work precisely evaluating sensory attributes and meat quality of broiler chicken fed with MW based diets, and the optimal level of application. Therefore, this study reports sensory attributes of MW and investigates its effect on sensory characteristics of fresh carcass and cooked breast meat using Quality Index Method (QIM), together with Quantitative Descriptive Analysis (QDA) method and Principal Component Analysis (PCA) and on some quality indexes of chicken slaughtered on 24 and 42 days of age. The results could be useful for the commercial application of MW in formulating broilers feed.

Material and methods

Birds and husbandry

This study was conducted in the research poultry house of the Animal Science Research Institute of Iran (ASRI, Karaj, Iran). The animal ethics committee of ASRI approved all the experimental procedures. A total number of 400 day-old Ross 308 male broiler chicks were obtained from a local hatchery (Sadeghi Co., Karaj, Iran). The broilers were randomly distributed into 4 groups using a completely randomized design. Each group was replicated 5 times with 20 birds per replicate. A total of 20 pens were used for the experiment. Each pen had 3 m3 spaces, with wood shaving covered floor. The initial temperature of the house was kept at 32 ± 2 °C and gently reduced (2.5 °C/week) to have a stable temperature of 20–22 °C at 28 days of age. During the study, relative humidity and lighting regime were maintained in 50–60% and 23:1 h of light: darkness, respectively. The birds had continual access to feed and water during the experiment.

Mealworm (Tenebrio molitor) meal was obtained from Hafez Hayat Javdan Company (Karaj, Iran). Dietary treatments were included 4 levels of MW [(0 as control), 1, 2 and 3%] in the main feed mix (Table 1). All diets were formulated to contain a similar amount of energy and protein and meet or exceed Ross 308 requirements and fed from 1 to 24 days of age (Aviagen 2019). Birds received a normal diet (without MW) from 25 to 42 days of age.

Table 1.

Feed ingredients and nutrient compositions of experimental diets

Item Days 1–10 Days 11–24 Days
25–42
mealworm (%) mealworm (%)
0 1 2 3 0 1 2 3
Ingredients (g/kg)
Maize grain 538.8 538.6 538.1 542.0 576.9 576.4 584.8 580.2 649.0
Soybean meal (44% crude protein) 396.5 386.5 377.4 365.4 357.0 345.0 332.1 320 283.9
Soybean oil 20.0 18.0 18.0 16.0 25.0 24.0 20.5 21.0 28.1
Mealworm – 10.0 20.0 30.0 – 10.0 20.0 30.0 –
Limestone 10.1 12.1 12.0 12.0 10.5 11.5 10.8 11.5 11.5
Dicalcium phosphate 17.8 18.0 18.0 18.0 15.0 15.0 14.5 15.0 15.6
Sodium chloride 2.1 2.1 2.1 2.1 2.1 2.1 2.1 2.5 2.0
Bicarbonate sodium 2.5 2.5 2.5 2.5 2.7 3.0 2.5 2.7 2.1
Vitamin-mineral premixa 5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0 5.0
DL- Methionine 99% 3.7 3.7 3.6 3.7 3.2 3.2 3.1 3.2 1.8
L- Lysine HCL 2.7 2.7 2.5 2.5 1.8 2.0 1.8 2.0 1.0
L- Threonine 0.8 0.8 0.8 0.8 0.8 0.8 0.8 0.8 –
Washed sand (inert filler) – – – – – 2.0 2.0 6.0 –
Nutrient compositionb
Metabolizable energy (MJ/kg) 12.2 12.2 12.2 12.2 12.6 12.6 12.6 12.6 12.8
Crude protein (g/kg) 223.1 223.5 223.9 224.1 207.4 207.6 207.6 207.5 180.1
Calcium (g/kg) 9.9 10.2 10.2 10.2 9.1 9.3 9.1 9.2 8.7
Available phosphorus (g/kg) 4.9 5.0 5.0 5.0 4.4 4.5 4.4 4.5 4.0
Sodium (g/kg) 1.6 1.6 1.6 1.7 1.7 1.8 1.7 1.8 1.6
Lysine (g/kg) 14.5 14.5 14.4 14.4 12.8 12.9 12.8 12.8 10.3
Methionine + Cystine (g/kg) 10.6 10.6 10.6 10.6 9.8 9.8 9.7 9.7 8.1
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aTo provide vitamins and minerals per kilogram of diet: vitamin A, 18,000 IU; vitamin D3,4000 IU; vitamin E, 36 mg; vitamin K3, 5 mg; vitamin B12, 1.6 mg; thiamine, 2.97 mg; riboflavin, 7.5 mg; niacin, 57 mg; pyridoxine, 4.45 mg; biotin, 0.18 mg; folic acid, 1.9 mg; pantothenic acid, 17.8 mg; ethoxyquin, 0.125 mg; cyanocobalamin, 0.02 mg; choline chloride, 487.5 mg; Fe-sulfate, 40.5 mg; Zn-sulfate, 84 mg; Mn-sulfate, 160 mg; iodine (calcium iodate), 1.26 mg; Cu-sulfate, 20 mg; and selenium (sodium selenite), 0.31 mg

bDetermined by ingredient analysis, then results used for calculation the nutritional compositions of diets

On day 24 and 42, four birds from each replicate were slaughtered and eviscerated. The carcass of each slaughtered bird was used for sensory evaluation and breast meat samples were used for physicochemical and sensory assessment, too. Each breast was halved, and each half breast was labelled, packaged in polyethylene bags and stored at − 40 °C until analysis.

Proximate analysis, pH and TVB-N

Proximate analysis including crude lipid, crude protein, moisture, and ash contents were determined using standard method, (AOAC 2000). Steam distillation and titration methods were used to measure total volatile basic nitrogen (TVB-N) (Ariyawansa 2000). A digital pH meter (Knick-Portamess 913 pH, Berlin, Germany) was applied to measure the pH of chicken breast meat (Swatland 2008).

Warner-Bratzle (WB) shear force

The Warner-Bratzle (WB) shear force of the cooked chicken breast meat was determined using a TA.XT plus texture analyzer (Stable Micro Systems, Surrey, UK) following the method described by Zhuang and Savage (2009) with some modifications. The chicken breast meat was cut to 100 mm2 (10 × 10 mm) pieces with 10 mm thickness. Three samples from each treatment were sheared by a standard knife blade (68 mm wide × 72 mm long × 3 mm thick), for a penetration depth of 20 mm to the samples. Three shear force values were reported for each breast meat by the use of texture analyzer software.

Water holding capacity (WHC)

The WHC was measured by centrifugation using a Biofuge Stratos, Heraeus Instruments (Hanau, Germany). Interval temperature was assigned at 5 °C, speed 1350 rpm, and the time was 5 min. The WHC was noted as the water content remained after centrifugation per g of the dry weight of the sample (Shaviklo et al. 2010a, b):

WHC%=A×B-C/A×B×100 1

where: A = Moisture content of sample before centrifugation (g), B = Sample weight (g), C = Sample weight after centrifugation (g).

Color evaluation

The test sample was cut into 15 mm in thickness or more. The specimens were analysed directly with a CR-200 Chroma Meter (Minolta, Japan) by measuring the values of L* (lightness), a* (red-green colors), and b* (yellow-blue colors). Three sliced pieces were analysed.

Sensory analysis

Sensory attributes of MW powder

The method described by Shaviklo et al. (2012) was used to detect sensory attributes of MW powder. A 5% mealworm solution was prepared and used by an expert panel to detect sensory attributes of MW. Chickpea odor and flavour, bitterness, and astringency were the dominant attributes detected by the panel in the MW solution. Then the results were used for further analysis of chicken carcass and meat.

Sensory evaluation of broiler carcass

A sensory index was designed based on the quality index method (QIM) (Martinsdottir et al. 2001) to analyse the sensory properties of the broilers' carcass treatments (Table 2). An expert panel including 5 (1 female) trained and skillful experts in meat and poultry products was used for sensory assessment. The expert panel evaluated carcass appearance including leg skin color (yellowness/pinkish/darkness), breast skin color (yellowness/pinkish/darkness), abdominal cavity including fat color (yellowness), the odor of fat, fat texture, rancid odor, metallic odor, unusual odor, meat color (leg/breast darkness) and meat texture (thigh and breast).

Table 2.

Sensory index for assessment of fresh chicken carcass

Index Definitions and scales
Appearance
Leg skin color (yellowness) Color intensity. White = 0, yellow = 100
Leg skin color (pinkish) Color intensity. White = 0, pink = 100
Leg skin color (darkness) Color intensity. White = 0, dark = 100
Breast skin color (yellowness) Color intensity. White = 0, yellow = 100
Breast skin color (pinkish) Color intensity. White = 0, pink = 100
Breast skin color (darkness) Color intensity. White = 0, dark = 100
Abdominal cavity
Fat
Fat color (yellowness) Color intensity. White = 0, yellow = 100
Odor of Fat Intensity of chicken odor. None = 0, much = 100
Fat texture After pressing with fingers. Very soft = 0, firm = 100
Odor
Rancid odor Rancid odor can remind oxidation. None = 0, much = 100
Metallic odor Metallic odor can remind iron odor. None = 0, much = 100
Unusual odor Unusual odor like Chickpea. None = 0, much = 100
Meat color
Leg color (darkness) Color intensity. White = 0, dark = 100
Breast color (darkness) Color intensity. White = 0, dark = 100
Meat texture
Thigh After pressing the thigh tissue with the index fingers and thumb, return to the previous state. Irreversible = 0, fast reversible = 100
Breast After pressing the breast tissue with the index fingers and thumb, return to the previous state. Irreversible = 0, fast reversible = 100
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Sensory evaluation of cooked chicken breast

Sensory analysis of cooked chicken breast was performed based on the ISO guidelines (ISO 2007; 2012). Chicken breasts (50 g) from each treatment were placed in a glass jar containing 100 g distilled water separately. Jars were put in hot water and were heated at 65 ± 5 ˚C for 60 m. Sensory evaluation of cooked chicken breast was done by 5 experts. The average age of the assessors was 29 years old and they knew how to apply the Quantitative Descriptive Analysis (QDA) method to evaluate meat products. Assessors were trained in 2 meetings to assess cooked chicken breast using the QDA method (Meilgaard et al. 2007). They determined the different sensory attributes among the samples. A sensory lexicon (Table 3) was adapted from Shaviklo et al. (2010b) to demonstrate the severity of each sensory attribute of the samples. The panel evaluated the samples, using a list of the sensory lexicon and an unstructured scale (from 0 to 100%).

Table 3.

Lexicon for sensory attributes of cooked chicken breast (

adapted from Shaviklo et al. 2010a, b)

Sensory attribute Scale (0–100) Definitions
Odor
Chickpea none|much Odor of chickpea
Earth none|much Odor of clay
Rancid none|much Rancid odor remind of oxidised oil, fermentation, etc
Flavor/Taste
Chickpea none|much Flavor of chickpea
Bitterness none|much Taste of bitterness
Astringency none|much Astringency
Rancid none|much Rancid flavor
Chicken none|much Intensity of taste similar to chicken soup
Texture
Softness firm|soft Softness in the first bite
Elasticity little|much When chewing rubbery, springy
Juiciness dry|juicy When chewing: Dry (sample draws liquid from mouth), Juicy (Samples give away liquid)
Acceptance
Liking none|much How do you like it?
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All samples were randomly coded with 3 digit numbers and gave to the assessors in a separate tray in separate stands. The arrangements of sample presentation to the panellists were quite randomized in duplicate. The water was used between the assessments to cleanse the palate. Individual score sheets were provided and during the evaluation, the panellists recorded the severity of every sensory attribute of cooked chicken breast samples, by marking on an unstructured 15 cm line scale with 2 notations at the ends (low and much). Five panellists evaluated each sensory attributes of the samples at the 2 sessions (5 evaluations × 2 sessions). Therefore, the reported sensory values were the mean of 10 evaluations for every attribute.

Statistical analysis

PanelCheck software (V1.3.2, Matforsk, Ås, Norway) was used to monitor the performance of the assessors and to analyse sensory data. Multivariate comparison of sensory attributes of samples also performed applying the Unscrambler@ statistical program (V9.7, CAMO, Ås, Norway). Analysis of variance was carried out using the statistical program NCSS 2007 (NCSS, Statistical Software, Kaysville, UT) for the statistical analysis of physicochemical results. The results were presented as a mean ± standard deviation. The significance of difference was determined at the 5% level.

Results and discussion

Physicochemical properties

Birds slaughtered on 24 days of age

Control and broilers fed with 1, 2 and 3% MW had the same protein (21.04–21.64%), fat (1.67–1.84%), and moisture content (74.81–75.22%) in breast meat. Control and broilers fed with 1% MW had the highest ash content (2.07, 1.92%) followed by the broilers fed with 2% MW (1.60%). The lowest ash content was observed for the broilers fed with 3% MW (1.18%). Significant differences were reported for pH, ash, TVB-N, and WHC of chicken slathered on day 24. The effect of the different levels of MW in chicken diets on chicken meat pH is found by the difference in the initial pH value. Control treatment and broilers fed with 1% MW had the highest pH (6.06). Broilers fed with 2 and 3% MW had the same pH (5.78, 5.96) and the lowest pH value. The formation of TVB-N was increased in the broilers fed with MW. The highest TVB-N value was reported for the broilers fed with 3% MW (35.50 mg N/100 g) followed by birds received 1 and 2% MW (32.00–33.00 mg N/100 g). The lowest TVB-N value was seen for the control treatment (30.50 mg N/100 g). The highest WHC was seen for the control (76.12%) and broilers fed with 1% MW (76.62%) followed by the broiler fed with 2% MW (73.93%). The broiler received 3% MW had the lowest WHC (71.60%) among the treatments (Table 4).

Table 4.

Proximate analysis (%), pH, TVBN (mg N/100 g), WHC (%) and cook loos (%) of chicken fed by different level of MW

Treatment Protein Fat Ash Moisture pH TVB-N WHC
Chicken fed 24 days by different level of MW
C 21.04 ± 1.48 1.71 ± 0.69 2.07a ± 0.13 75.16 ± 0.40 6.06a ± 0.01 30.50c ± 2.95 76.12 a ± 0.30
M1 21.43 ± 1.18 1.84 ± 0.99 1.92a ± 0.49 74.81 ± 0.29 6.06a ± 0.01 32.00b ± 2.07 76.62 a ± 0.59
M2 21.50 ± 1.28 1.67 ± 0.48 1.60b ± 0.14 75.22 ± 0.72 5.78b ± 0.01 33.00b ± 2.83 73.93 b ± 0.64
M3 21.64 ± 2.65 1.77 ± 0.56 1.18c ± 0.42 75.00 ± 0.94 5.96b ± 0.13 35.50a ± 3.54 71.60c ± 0.40
Sig NS NS p < 0.05 NS p < 0.05 p < 0.05 p < 0.05
Chicken fed 24 days by different level of MW and 18 days without MW
C 21.48 ± 1.18 2.52a ± 0.28 1.38b ± 0.99 74.63 ± 0.17 6.13 ± 0.09a 29.30 ± 0.42 57.32a ± 0.01
M1 21.38 ± 0.19 1.55b ± 0.02 1.43b ± 0.64 74.64 ± 0.09 5.72 ± 0.01b 28.55 ± 0.71 54.06b ± 0.09
M2 22.12 ± 0.31 1.41b ± 0.42 1.55a ± 0.65 74.92 ± 0.75 5.86 ± 0.06b 30.51 ± 0.71 53.65b ± 0.42
M3 22.25 ± 0.73 1.24c ± 0.70 1.75a ± 0.55 74.80 ± 0.19 5.76 ± 0.07b 29.55 ± 0.71 52.05b ± 0.07
Sig NS p < 0.05 p < 0.05 NS p < 0.05 NS p < 0.05
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Values are mean of 3 analyses. C control sample, M1 chicken fed with 1% MW, M2 chicken fed with 2% MW, M3 chicken fed with 3% MW. NS not significant

On day 24, no significant difference was observed in meat samples obtained from the MW fed and control group in respect of color and lightness. However, the control group had the highest lightness (57.36). Birds fed with MW had a similar lightness (52.37–55.59). The highest b* value was observed in control and broiler fed with 1% MW (13.13, 13.83). Broilers fed with 2 and 3% MW had a similar b* value (11.31, 12.04).

Birds slaughtered on 42 days of age

All treatment had a similar amount of protein (21.38–22.25%), moisture content (74.63–74.80%), and TVB-N (28.55–30.51 mg N/100 g) values. Significant differences were observed in fat, pH, and WHC values of chicken slaughtered on day 42. The highest pH was observed in the control treatment (6.13). The lowest pH recognized for the birds few with MW (5.72–5.86). The highest fat content was observed in the control (2.52%) followed by the broilers fed with 1 and 2% MW (1.55, 1.42%). The lowest fat content was seen in the birds received 3% MW (1.24%). The highest WHC was seen in control (57.32%). Birds fed with 1, 2 and 3% MW had the lowest WHC (52.05–54.06%) (Table 4).

On day 42, the control group and samples fed with MW for the first 24 days of age showed similar levels of L* (55.42–58.31), a* (11.15–12.68), and b* (12.69–14.47) values in meat samples.

The proximate composition of animal meat is influenced by the diet. Several works reveal contradictory results about the effect of feeding animals with insects on the physical properties of the carcasses (Ng et al. 2001; Belforti et al. 2015; Gasco et al. 2016; Cullere et al. 2016). Biasato et al. (2017) noted that when chickens were fed 1% of MW, the moisture content was significantly increased. In Altmann et al. (2018) work, control, and broilers fed with Hermetia larval had the same amount of protein and moisture contents.

In this study ash content was affected by MW inclusion, with the highest values was found in control after 24 days feeding. But after 18 days of normal feeding, ash content increased in treatments which fed 24 days with 2, 3% MW. Ash indicates muscle mineral content and is associated with the diet compounds and its values usually increase in the high mineral level of diet. However, this decrease in ash content in the first 24 days and increase in the next 18 days can be associated with the incorporation of MW in the diet, which could increase intestinal pH and therefore, reduced the absorption of minerals (Fallah et al. 2016).

In our experiments, feeding broilers with MW decreased fat content. The results were in agreement with the research reported by Sealey et al. (2011) and Belforti et al. (2015). One of the main components of the insect exoskeleton is chitin, a polysaccharide that is similar to cellulose in a plant structure. A beneficial effect of chitin and its de-acetylated derivative is the decline of plasma cholesterol and triglycerides due to its capability to bind dietary fats, thereby decreasing intestinal lipid absorption (Kobayashi and Itoh 1991). The hypolipidemic influence of chitin may also be due to the interruption of the enterohepatic bile acid circulation. These are some of the reasons that may be caused a reduction of fat contents in broilers received MW in the present study.

The initial pH levels were significantly higher in control (Table 4). This is in agreement with Altmann et al. (2018) work who reported the control group having the highest pH values than broilers fed with Hermetia illucens larval. Similarly, Bovera et al. (2016) observed a decline in breast pH of broiler received increasing levels of Hermetia illucens larvae meal. Our results, however, were in contrast with those reported by Bovera et al. (2016), who measured higher pH value of breast muscle in MW-fed quails comparing to the control. On the other hand, Dabbou et al. (2019) reported no difference in breast muscle pH among free-range chickens fed with or without MW. These differences can be ascribable to variation in muscle glycogen contents, birds’ species, genotype, and rearing system (Cullere et al. 2016; Dabbou et al. 2019). This variance also might be due to MW based diets and related metabolism in the digestive tract and presence higher free amino acids (tyrosine, phenylalanine, histidine, lysine, arginine) and releasing amino acids and some other low molecular-weight nitrogenous compounds in treatment fed with MW that could affect the initial pH (Triki et al. 2018).

WHC indicates the maximum level of moisture that muscle proteins can retain and has a direct effect on the color and texture of meat (Shariat Zadeh et al. 2019). In this study, the broiler breast meat with high pH had higher WHC than samples with lower pH. However, it disagrees with the work of Shariat Zadeh et al. (2019) who claimed that WHC was increased in quail’s breast muscle by enhancing the level of MW in the diet. Poultry meat with low pH has low WHC, and consequently cook-loss, drip loss, and shelf-life decrease (Barbut 1993). This may explain why control samples in this study had the highest WHC (Table 4).

The total volatile basic nitrogen (TVB-N) is an indicator of the presence of compounds containing volatile nitrogen in feedstuff to assess the quality of protein products (Ariyawansa 2000). Fallah et al. (2016) stated a clear relationship between TVB-N in broiler chicken feed and TVB-N formation in broiler meat. They reported that the high value of TVB-N in the diet (more than 15 mg/100 g) could increase the TVB-N value of chicken meat. This may explain the high value of TVB-N (28.5–35.5 mg N/100 g) in all treatment of this study in which the highest was observed in treatments fed with MW for 24 days.

Meat color is the result of many physicochemical processes within the muscles (Barbut 1993). The color of breast raw meat is characterized as a pale pink color, while the color of the raw thigh and raw leg meat is considered dark red. A direct influence of pH on quality attributes of meat such as appearance is well known (Fletcher 2002). Meat with a high pH is very dark, and if the color is very light, the pH is low. The color differences in breast meat are basically due to pH influences. Chicken fillet with an initial pH of 5.8 is lighter than normal fillets. Chicken fillet with an initial pH of 6.0 is darker than normal fillets (Allen et al. 1997).

The lightness (L*) of raw and cooked poultry breast meat has a direct correlation with physicochemical characteristics and meat functional properties (Zhuang and Savage 2010). Several researchers have noted that the L* value has a negative correlation with the pH of poultry breast muscle (Barbut 1993).

Unlike the earlier works (Hwangbo et al. 2009; Altmann et al. 2018) which showed insect-based feed had no significant influence on broiler meat color regarding the L*, a*, and b* values; this study indicated a significant difference among control and treatments fed 24 days with MW for lightness (L*) and yellowness (b*). Decreasing yellowness in samples fed with MW is in agreement with the data released by Shariat Zadeh et al. (2019) who reported these values were decreased by increasing the level of MW in the diet of Japanese quails (Coturnix japonica). The variations in broiler breast meat color are because of changes in muscle pH and may be related to MW levels in the diet. Fletcher (2002) reported significant linear relationships between raw meat color and its pH. Meat at pH 6.0 has minimum protein denaturation and translucent appearance.

Texture analysis

On days 24 and 42, the Warner-Bratzle shear force values showed no significant difference among chickens fed with MW for the first 24 days of age (40.39–45.10) and chickens fed further 18 days without MW (49.07–71.97).

Warner-Bratzle shear force was equal among samples after 24 days feeding with MW and 18 days fattening. The results are in agreement with the works of Cullere et al. (2016) who reported MW application did not influence the shear force of broiler quails and Altmann et al. (2018) who used Hermetia meal in poultry diet. Samples (control and treatment fed with Hermetia larval had the same hardness (soft to hard), and tenderness (tender to tough) (Altmann et al. 2018). However, the Warner-Bratzle shear force in samples at day 42 was significantly higher than day 24. Intramuscular fat and meat moisture content can affect broiler meat quality.

Sensory evaluation

Raw samples (chicken carcass)

Significant differences were seen for sensory attributes of raw carcass among birds slaughtered on 24 days of age. Feeding with MW influenced the skin color of the carcass. The highest severity of the yellowness and pinkish of leg and breast skin was found in the control. The darkness of leg and breast skin color was more recognized in the birds fed with 3% MW followed by birds received 2% MW. The control had the lowest severity of darkness in leg and breast skin among the treatments. The same values were observed for the darkness of skinless leg and breast samples. Fat layers in the abdominal cavity of the control had the highest yellowness followed by the broilers fed with 1% mealworm. The highest chicken odor was reported in the abdominal cavity of the control and chickens fed with 1% mealworm. The highest rancidity and unusual odor were found in the abdominal cavity of the birds fed with 3% MW. However, rancidity and unusual odor were the same in control, and birds received 1 and 2% MW. No significant difference was reported in fat texture and chicken leg and breast texture among the treatments. The carcass of birds slaughtered on 42 days of age had similar sensory attributes in all the treatments.

Cooked samples (chicken breast)

Feeding broilers with MW affected sensory attributes of cooked chicken meat on 24 days of age. Significant differences were found for chickpea odor and flavour, juiciness, and acceptance among the treatments. Control had the lowest level of chickpea odor and flavour and the highest was found in the birds fed with 3% MW followed by birds received 2% MW. The control sample was juicier and had the highest acceptance among the treatments. All these defects were overcome after 42 days of rearing period except for juiciness. The treatment fed with 3% MW obtained the lowest score of juiciness. Control and treatments fed with 1 and 2% had a similar score of juiciness. However, all treatments had similar acceptance on day 42.

Multivariate analysis of the data obtained from the feeding period with MW (Fig. 1) and rearing period without MW (Fig. 2) showed that 96% and 98.8% of the variations between the samples were explained in the first two principal components, respectively. The PCA plots revealed the influence of feeding with MW on sensory characteristics of the raw carcass and cooked breast meat (Fig. 1). Two sample groups (control and treatments fed with MW) are quite separated from each other. The control (C) was located on the left side and treatments fed with 1, 2, and 3% MW (M1, M2, M3) are located on the right side of the plot. Attributes located on the left side of the plot indicated that all samples obtained from birds fed with MW had sensory similarities. Chickpea odor and attributes like rancid odor and color change can be observed by the sample groups fed with MW for 24 days. Control samples were further specified by juiciness and acceptance, while the groups fed with MW are more characterized by chickpea odor and flavour, high TVB-N, and low WHC values. The intensity of chickpea odor and flavour were increased in the broilers by a dietary increase of MW as indicated by the arrow, tracking the decreasing quality and sensory changes of the treatments along with PCA plot from lower right part to the upper right part (Fig. 1).

Fig. 1.

Fig. 1

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Principal component analysis (PCA) describing sensory scores of of chicken carcass and cooked chicken breast fed 24 days with MW as evaluated by a trained sensory panel. C control sample, M1 chicken fed with 1% MW, M2 chicken fed with 2% MW, M3 chicken fed with 3% MW. The arrow indicates the influence of MW levels on sensory changes of the samples. Negative attributes like TVBN, rancid odor and unusual odor and flavour were more described by increasing MW levels in the diet

Fig. 2.

Fig. 2

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Principal component analysis (PCA) describing sensory scores of of chicken carcass and cooked chicken breast fed fed 24 day with MW and 18 dayes without MW as evaluated by a trained sensory panel. C control sample, M1 chicken fed with 1% MW, M2 chicken fed with 2% MW, M3 chicken fed with 3% MW

Meanwhile, the PCA also revealed that 18 days of MW withdrawal after 24 days of MW dietary inclusion had ameliorated the effects of MW on sensory attributes of raw carcass and cooked meat except for juiciness (Fig. 2). Two sample groups (control and treatments fed with MW) were still quite separated from each other and control samples were more characterized by juiciness.

Sensory attributes of poultry meat are contributed to the bird nutrition/ diet and it can be better by formulating the feed (Lyon et al. 2004). Takahashi et al. (2012) revealed a significant positive relationship between sensory attributes and arachidonic acid content in broiler chickens’ meat. However, some fatty acids like arachidonic acid can act as a flavour enhancer. Sensory characteristics of broiler chicken meat are very important when using insects as a feed supplement. Odor and flavour of insects are very diverse. They are affected by the insect body and the environment where insects live and the feed that they eat (Makkar et al. 2014). We observed chickpea odor and flavor, bitterness, and astringency as dominant sensory attributes in MW. The odor is an important sensory attribute of meat, which is sensed more easily than taste and flavour, and both affect acceptance of the product (Winiarska-Mieczan et al. 2016).

Sensory index for evaluation of (raw) chicken carcass fed 24 days with MW revealed significant differences for leg/ breast skin color (yellowness, pinkish, darkness), leg/ breast meat color, fat color, and abdominal cavity chicken odor, rancidity odor and unusual odor among all treatments. However, these attributes were not significant for a further 18 days of rearing without MW.

The color of chicken skin/meat depends on the level of protein denaturation, postmortem temperature, and pH, and abundance of pigments soluble in lipids such as carotenoids in the feedstuff and feed sources/additives (Barbut 1993). On the other hand, dried insects as a feed ingredient contain a large amount of oxidized fat that can affect sensory attributes of the final product. This may explain color variation in sample groups (Makkar et al. 2014).

In this study, the scores of chicken odor in raw samples were decreased along with the increased levels of MW powder and the rancid odor was decreased by the increasing level of MW. The former may be related to fatty acid composition, which is directly influencing meat aroma (Gunya et al. 2016) and the latter to the freshness index of the added ingredient in the feed (MW).

Unusual, rancid, and metallic odors are sensory attributes that are unpleasant in meat and influence consumer acceptance negatively (Mahmoud and Buettner 2016). The high scores of rancid and unusual odors were detected in the treatments fed with MW possibly due to peroxidation of polyunsaturated fatty acids in MW which then results in the formation of such attributes (Winiarska-Mieczan et al. 2016). In this study, the metallic odor was not found in broilers' carcasses fed with MW. This differs from the findings of other researchers. Pieterse et al. (2014) reported a metallic odor in breast meat of chickens received feeds containing Musca domestica, larvae meal, fishmeal, or soya bean meal. The different sources of protein applied in their researches as well as the different types and nature of compounds including insects, fishmeal, and plants proteins that had different amounts of unsaturated fatty acids may explain the reason.

Chickpea odor and flavor, juiciness, and acceptance were detected in cooked chicken meat as dominant attributes among the treatments fed with MW during 1–24 days of age. All these defects were overcome after 42 days of farming except for juiciness. According to Khan et al. (2018), the meat of chickens fed with MW was juicy and tender. The intensity of chicken meat flavor depends on the variations in the content of Inosine-50-monophosphate (IMP) (Tang et al. 2009), arachidonic acid, and docosahexaenoic acid (DHA). Also the pH of meat, fatty acid compositions, and compounds derived from lipids “i.e.” the 2-alkenals and aldehydes, are responsible for specific chicken odor and flavor.

Application of MW in chickens’ diet had no influence on chicken flavor in cooked chicken breast. The results disagree with the works of William and Damron (1989) who reported the incorporation of insects in birds’ diet decreased the chicken flavour scores of breast meat. However, these findings are in line with the works by Lyon et al. (2004), Pieterse et al. (2014), and Onsongo et al. (2018) who detected no dietary effect on chicken flavour scores fed with insects. This may be due to the different physicochemical of insect-based diets.

Meat juiciness is influenced by the fat and protein contents of the structure of proteins and feeding programs (Barbanti and Pasquini 2005). The juiciness scores of breast meat were decreased by increasing the level of MW in diet due to decreasing fat contents of MW fed treatments compared to the control. The results differ from the studies carried out by Williams and Damron (1998), Pieterse et al. (2014), and Winiarska- Mieczan et al. (2016) who did not report any influence of insect dietary feed on the breast meat juiciness. In a previous work carried out by Teye et al. (2015) improvement of the meat juiciness by increasing the level of E. foetida increased was reported. These contradictory results might be due to the different sources of protein and fat included in the diets of the chickens used in those studies.

Our results regarding sensory attributes were not in agreement with some earlier studies. For instance, Hwangbo et al. (2009) reported that the sensory characteristic of broiler meat was not affected by the supplementation of insect meal in the diet. The results of another study showed that sensory attributes were not affected by the inclusion of MW in the diet of broilers (Hussain et al. 2017). Onsongo et al. (2018) reported that the incorporation of black soldier fly larvae meal to broiler chickens diet had no influence on odor, flavor, and acceptance of cooked breast meat. Incorporation of MW had no significant effect on sensory characteristics of quails breast muscle (Shariat Zadeh et al. 2019). This disagreement could be due to the use of different insects and livestock, varied feedstuff, or using non-standard sensory evaluation methods. Therefore, it is necessary to pay more attention to the sensory characteristics and their evaluation methods in researches on the application of insects as animal feed.

Conclusion

Feeding broilers with MW (Tenebrio molitor) influenced the sensory attributes of the carcass and chicken meat. Sensory defects were much worse as the level of MW increased in the diet. Birds fed with 3% MW showed the lowest juiciness attributes. In conclusion, the dietary inclusion of MW up to the level of 3% for the first 24 days of broilers’ life may be appropriate for achieving optimum broiler meat quality and sensory attributes. Such characteristics may negatively be affected by higher levels of MW application. Further studies should be accomplished about meat quality and sensory stability changes in broilers fed with MW especially from the marketing point of view.

Acknowledgements

Supports provided by Hafez Hayat Javdan Company (Karaj, Iran) and Animal Science Research Institute of Iran (ASRI) are appreciated.

Compliance with ethical standards

Conflict of interest

Authors declare no conflict of interest.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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