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Article

Drying Methods for Black Soldier Fly (Hermetia illucens) Larvae as a Feed Ingredient for Pigs Affect In Vitro Nutrient Disappearance

by
Junghyun Oh
1,
Hansol Kim
1,
Kwanho Park
2 and
Beob Gyun Kim
1,*
1
Department of Animal Science, Konkuk University, Seoul 05029, Republic of Korea
2
Industrial Insect and Sericulture Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Republic of Korea
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(10), 1792; https://doi.org/10.3390/agriculture14101792
Submission received: 15 August 2024 / Revised: 11 September 2024 / Accepted: 10 October 2024 / Published: 12 October 2024
(This article belongs to the Section Farm Animal Production)
Browse Figure
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Abstract

:
The objective of the present research was to determine the nutrient utilization of full-fat black soldier fly larvae (Hermetia illucens; BSFL), which were processed by various drying methods, using in vitro procedures for pigs. Four sources of BSFL were prepared using various drying methods: (1) hot-air drying at 65 °C for 24 h; (2) microwave drying at 700 W for 5 min, three times; (3) freeze drying at −40 °C for 72 h; (4) infrared drying at medium infrared region (ranged from 2.0 to 6.0 μm) and at 95 °C for 12 min. In vitro ileal disappearance (IVID) of nutrients in the BSFL was measured using a procedure simulating the nutrient digestion and absorption in the stomach and small intestine of pigs. In vitro total tract disappearance (IVTTD) of nutrients in the BSFL was also measured using a procedure that simulated the total intestine of pigs. The contents of dry matter, ether extract, and crude protein in the dried-BSFL ranged from 94.6 to 96.8%, 49.2 to 52.8%, and 30.0 to 36.8%, respectively, on an as-is basis. Microwave drying resulted in a greater (p < 0.05) IVID of dry matter in BSFL, compared with the freeze drying or infrared drying method, which caused the least IVID of dry matter. Hot air-dried BSFL, microwave-dried BSFL, and freeze-dried BSFL had a greater (p < 0.05) IVID of crude protein and a greater (p < 0.05) IVTTD of dry matter and organic matter, compared with infrared-dried BSFL. In conclusion, the hot-air drying, microwave drying, and freeze drying of full-fat black soldier fly larvae resulted in fairly comparable and relatively high nutrient digestibility based on the present in vitro study for pigs. However, the infrared drying method impaired nutrient utilization of full-fat black soldier fly larvae for pigs.

1. Introduction

Insect-derived feed ingredients have been proposed as a promising alternative protein source due to the ability of insects to be efficiently reared on lower-quality feed ingredients and their high nutritional value [1,2,3]. The use of black soldier fly larvae (Hermetia illucens; BSFL) has increased due to their high protein and fat contents [1,4,5,6]. Additionally, BSFL are relatively easy to rear because they can consume a wide range of agro-food industry waste and contain a well-balanced amino acid (AA) profile, compared with plant-derived protein sources such as soybean meal [4,7].
The BSFL oil is notably rich in saturated fatty acids, particularly lauric acid (C12:0), which exhibits antimicrobial and anti-inflammatory properties in the small intestine of pigs, along with its metabolites [8,9,10]. However, the defatting process can negatively impact the bioavailability of protein and AA in animal feeds due to heat or acid treatment [11]. In addition, the oil in full-fat BSFL has advantageous effects on pigs [2], and the defatting procedure is costly. Therefore, full-fat BSFL have been widely utilized.
Various drying methods, using a drying oven, microwave, or freeze dryer to inhibit bacterial and fungal growth, are available; they extend the shelf life of insect-derived products [6,12,13]. These drying methods potentially change the chemical composition and physico-chemical properties of BSFL [14], which eventually influence nutrient digestibility [15]. However, the literature on the nutritional value of full-fat BSFL under various drying methods is insufficient. In vitro procedures mimic the digestion in the gastrointestinal tract of pigs [16,17], and in vitro nutrient utilization is highly correlated with in vivo nutrient digestibility [18]. Thus, in vitro methods have been employed to measure nutrient utilization by pigs [19,20]. Additionally, the in vitro procedure has been used to determine the nutritional value of BSFL-derived feed ingredients for non-ruminants [4,5,6,13]. Therefore, nutrient utilization of full-fat BSFL dried by various methods was measured using in vitro procedures for pigs.

2. Materials and Methods

2.1. Dried Full-Fat BSFL Preparation

The BSFL were raised for 15 days at 26 °C and 40% relative humidity. Food waste containing 74.9% moisture, 3.3% crude protein (CP), 0.7% ether extract (EE), and 20.1% carbohydrate was provided to the BSFL five times during the entire growth period. On day 15, the BSFL were washed and harvested by freezing at −20 °C to avoid exposure to heat for killing. The frozen BSFL were kept in the freezer for approximately 10 days before drying. As presented in Figure 1, the harvested BSFL were dried by four different drying methods: (1) hot-air drying using a drying oven (DS-80-3O; Dasol Scientific Co., Ltd., Hwaseong, Republic of Korea) at 65 °C for 24 h; (2) microwave drying (MR-M207WB; Samsung Electronics Co., Ltd., Suwon, Republic of Korea) at 700 W for 5 min, three times; (3) freeze drying (APV020XXX144; Ilshinbiobase Co., Ltd., Dongducheon, Republic of Korea) at −40 °C for 72 h; (4) infrared drying (HKD-LAB; Korea Energy Technology, Seoul, Republic of Korea) at medium infrared region ranging from 2.0 to 6.0 μm and at 95 °C for 12 min. The dried full-fat BSFL were finely ground (<1 mm) for the in vitro assays.

2.2. Two-Step In Vitro Procedure

An in vitro digestion procedure mimicking the digestion in the stomach and small intestine of pigs was conducted to measure in vitro ileal disappearance (IVID) of dry matter (DM) and CP in the four sources of dried full-fat BSFL [6,16,18]. In the first step, 1 g of dried full-fat BSFL was placed into a 100-mL conical flask. Sodium phosphate buffer (0.1 M) was adjusted to pH 6.0, and 25 mL of the buffer was added to the flask. We prepared 10 mL of 0.2 M HCl, which was adjusted to pH 0.7 and also added to the flask. The pH of the solution in the flask was adjusted to 2.0 using 1 M HCl or 1 M NaOH solution to mimic the environment of the stomach of pigs. To simulate the excretion of digestive enzymes in the stomach, 1 mL of pepsin solution (10 mg/mL) originating from pig gastric mucosa (≥250 units pepsin/mg solid, P7000; Sigma-Aldrich, St. Louis, MO, USA) was also added. Chloramphenicol (C0378; Sigma-Aldrich, St. Louis, MO, USA) was dissolved with ethanol (5 g/L ethanol), and 0.5 mL of the solution was added to inhibit microbial growth. The conical flasks containing the digesta solution were capped with a silicone stopper, placed in an electronically controlled shaking incubator (LSI-3016R; Daihan Labtech, Namyangju, Republic of Korea), and incubated for 6 h at 39 °C and 125 rpm. Following the incubation, the second step, mimicking the digestion in the small intestine of pigs, proceeded. Initially, 10 mL phosphate buffer solution (0.2 M) was adjusted to pH 6.8, and 5 mL of NaOH solution (0.6 M) were added to the digesta solution in the flasks. Using HCl (1 M) or NaOH (1 M), the pH of the digesta solution was adjusted to 6.8. To simulate the excretion of digestive enzymes in the small intestine, 1 mL pancreatin solution (50 mg/mL) originating from pig pancreas (4 × USP, P1750; Sigma-Aldrich, St. Louis, MO, USA) was added to the conical flask. Then, the conical flasks were placed in the electronically controlled shaking incubator (LSI-3016R; Daihan Labtech, Namyangju, Republic of Korea) and incubated for 18 h at 39 °C and 125 rpm. Following the incubation, each flask was added with 5 mL of sulfosalicylic (20%) acid and left at room temperature for 30 min to precipitate undigested proteins. Then, the undigested residues from dried full-fat BSFL were filtered using filter crucibles (Filter Crucibles CFE Por. 2; Robu, Hattert, Germany) that had been dried and weighed in advance. In each crucible, 0.5 g of Celite (Daejung Co. Ltd., Siheung, Republic of Korea) was placed to prevent the potential plugging of the filter pores with the residues. The flask was rinsed twice with 1% sulfosalicylic acid solution to remove all undigested materials from the flask. For further filtering of lipids, each filter crucible was added with 10 mL of ethanol (95%) and 10 mL of acetone (99.5%) two times. The filter crucibles containing unfiltered residues were dried for 24 h at 80 °C. Then, the crucibles were placed in a desiccator for cooling for 1 h, and the cooled filter crucibles with undigested residues were weighed for the calculation of IVID of DM in the dried full-fat BSFL. The residues were collected from the filter crucibles to determine CP concentrations and calculate IVID of CP in the dried full-fat BSFL. The IVID values for blanks were also estimated to correct the DM and CP contents in the residues that did not originate from the dried full-fat BSFL but from the pepsin and pancreatin added during the digestion procedure [21]. For each source of dried full-fat BSFL, three replicates were performed.

2.3. Three-Step In Vitro Procedure

To simulate the digestion and absorption of nutrients in the entire gastrointestinal tract of a pig, in vitro total tract disappearance (IVTTD) of nutrients was measured using 3-step procedure. The first and second steps, mimicking the stomach and small intestine, respectively, were identical to the IVID procedure, excluding the sample weight, enzyme concentration, and incubation time. In the IVTTD procedure, 0.5 g sample of dried full-fat BSFL was used. The concentration of pepsin solution for step 1 of digestion was increased to 25 mg/mL, and the concentration of pancreatic solution for step 2 of digestion was increased to 100 mg/mL. In the IVTTD procedure, the incubation periods for the first 2 steps were shortened to 2 and 4 h, respectively. In step 3, which mimicked the fermentation of the hindgut of pigs, 10 mL of ethylenediaminetetraacetic acid solution (0.2 M) was added to digesta solution in the conical flask. Then, the pH in the flask was adjusted to 4.8 by using acetic acid (30%) or NaOH (1 M). A multi-enzyme product (V2010, Viscozyme®; Sigma-Aldrich, St. Louis, MO, USA) 0.5 mL was added to the flask to mimic microbial enzyme secretions. The conical flasks containing the digesta solution were capped with a silicone stopper and incubated in a shaking incubator (LSI-3016R; Daihan Labtech, Namyangju, Republic of Korea) for 18 h at 39 °C and 125 rpm. Following the incubation, the undigested residues from dried full-fat BSFL were filtered as described for the IVID method. Then, the flask containing undigested residues was dried for 6 h at 130 °C and weighed for the calculation of IVTTD of DM in dried full-fat BSFL samples. Additionally, the ash content in the undigested residues remaining in the filter crucible was determined for the calculation of IVTTD of organic matter (OM) in dried full-fat BSFL samples. To correct the DM and OM amounts in the residues that were not originated from the dried full-fat BSFL, a blank was included [15].

2.4. Chemical Analyses

Dry matter concentrations in the four sources of dried full-fat BSFL and undigested residues from the in vitro procedure were determined [22]. All ingredients were analyzed for gross energy (Parr 6400, Parr Instruments, Moline, IL, USA). The CP (method 990.03) and OM (method 942.05) in the dried full-fat BSFL and undigested residues from the in vitro procedure were also determined [23]. The concentrations of EE (method 920.39), ash (method 942.05), and acid detergent fiber (ADF; method 973.18) in the dried full-fat BSFL were also determined [23]. Chitin concentrations in the dried full-fat BSFL were calculated by subtracting ADF-linked protein from ash-free ADF [24]. The chemical analyses were conducted in duplicate.

2.5. Calculations

The IVID and IVTTD of DM were calculated [18]:
IVID and IVTTD of DM (%) = [DMBSFL − (DMresidue − DMblank)]/DMBSFL × 100
where DMBSFL (g) is the amount of dried full-fat BSFL on a DM basis that was placed in the conical flask for in vitro procedures, DMresidue (g) is the amount of DM residue remaining in the filter crucible after the in vitro procedures, and DMblank (g) is the amount of DM residue in the blank estimated after the in vitro digestion [21]. The DMblank represents the residues that do not originate from the dried full-fat BSFL sample in addition to Celite. Following the 2-step procedure for IVID, the residues and Celite in the crucible were collected, weighed, and determined for CP for the calculation of IVID of CP [15]:
IVID of CP (%) = [(DMBSFL × CPBSFL) − (DMresidue × CPresidue) + (DMblank × CPblank)]/(DMBSFL × CPBSFL) × 100
where CPBSFL, CPresidue, and CPblank are the CP concentrations (%) in the dried full-fat BSFL, the undigested residue remaining in the filter crucible after the 2-step procedure, and blank, respectively, expressed on a DM basis.
After the 3-step procedures, the residues plus Celite remaining in the filter crucible were collected, weighed, and determined for OM for the calculation of IVTTD of OM [15]:
IVTTD of OM (%) = [(DMBSFL × OMBSFL) − (DMresidue × OMresidue) + (DMblank × OMblank)]/(DMBSFL × OMBSFL) × 100
where OMBSFL, OMresidue, and OMblank are the OM concentration (%) in the dried full-fat BSFL, the undigested residue remaining in the filter crucible after the 3-step in vitro procedures, and blank, respectively, expressed on a DM basis.

2.6. Statistical Analyses

The experimental data were analyzed employing the GLM procedure of SAS (SAS Inst. Inc., Cary, NC, USA). The drying method for full-fat BSFL was used as a fixed variable in the model. Pairwise comparisons were performed using the PDIFF option with Tukey’s adjustment. The output values from the pairwise comparisons were transformed into letter groupings using a SAS macro developed by Saxton [25]. Each conical flask served as the experimental unit. The statistical significance was declared at p < 0.05.

3. Results

The gross energy in the four sources of dried full-fat BSFL ranged from 6913 to 7080 kcal/kg (as-is basis; Table 1). The concentrations of ash and CP in the dried full-fat BSFL ranged from 3.5 to 3.6% and 30.0 to 36.8%, respectively, on an as-is basis. The EE in the dried full-fat BSFL was from 49.2 to 52.8%, and the chitin was from 1.9 to 3.3%.
Microwave-dried full-fat BSFL had a greater (p < 0.05) IVID of DM, compared with freeze-dried or infrared-dried full-fat BSFL, with no difference when compared with hot air-dried BSFL (Table 2). Infrared-dried BSFL had the least (p < 0.05) IVID of CP and IVTTD of DM and OM among the four sources of dried full-fat BSFL.

4. Discussion

The nutrient utilization of BSFL may be different depending on the drying method; however, limited information is available on the effects of drying procedures on the nutrient digestibility of black soldier fly larva-derived feed ingredients. In vitro procedures can fairly accurately estimate the digestibility of nutrients in feed ingredients for swine diets [1,16]. In the present work, thus, the utilization of nutrients in full-fat BSFL dried by various methods was determined using in vitro procedures for pigs.
Both full-fat and defatted BSFL are widely used as feed ingredients for pigs. In the present study, full-fat BSFL that did not undergo a defatting process were employed. The use of full-fat BSFL reduces nutrient variation due to oil extraction efficiency [1]. The defatting process can decrease the nutritional value of insect-derived feed ingredients as the high temperatures during the defatting procedure can degrade AA and increase chitin concentrations [26]. In addition, full-fat BSFL are a better source of net energy for growing pigs due to their higher concentrations of EE and energy efficiency [10].
The digestibility of insect-derived products is influenced by various factors, including insect species [27], rearing substrate [4], age [1], and processing methods [28] such as those involving time and temperature conditions [5,6,28]. These factors may be confounded with the effects of drying methods on nutrient digestibility in full-fat BSFL. Therefore, we employed the full-fat BSFL grown under the same environment and fed the same feeds to determine the influence of various drying methods on nutrient digestibility independent of other factors.
The hot-air drying, microwave drying, freeze drying, and infrared drying methods used in the present study are commonly employed in producing insect-derived feed ingredients [6,14,29]. Generally, DM contents are affected by the drying methods used [29]. In the present work, however, the DM contents of the four full-fat BSFL did not largely deviate among the different drying methods (coefficient of variation = 0.96%). We aimed to produce four BSFL as a consistent source of feed ingredients and thus adjusted the drying conditions to achieve approximately 95% DM. The DM contents in the hot air-dried and microwave-dried BSFL were similar to the previous study [6]. However, freeze-dried BSFL had greater DM contents, compared with a previous study [30], which is likely due to the longer drying time in the present study (72 h vs. 24 h). Additionally, infrared-dried BSFL had greater DM contents, compared with the previous study [14]. Drying temperature is one of the main factors that affect DM contents. In our study, the temperature reached up to 95 °C, whereas the temperature only rose to 40 °C in the previous study [14].
The CP concentrations in the dried full-fat BSFL in the present study were lower than those reported in previous studies [7,10]. The greater EE concentration, compared to previous studies, may dilute the CP concentrations, resulting in relatively lower CP concentrations. The different CP concentrations can also be attributed to different rearing conditions, as protein concentrations and AA profiles of BSFL tend to vary depending on their feeds [31] and killing methods [13]. Although the four dried full-fat BSFL were raised under the same environment and provided with the same feeds, the CP concentrations in microwave-dried BSFL and infrared-dried BSFL were less than the others. Microwave drying can denature the protein structure of insects [12], and infrared radiation can disrupt the secondary and tertiary structure bonds of the protein, leading to denaturation [14]. Denatured proteins exhibit a reduction in nitrogen content [32]. Therefore, it appears that microwave-dried BSFL and infrared-dried BSFL undergo denaturation, resulting in lower CP concentrations.
Chitin is present in the exoskeleton of BSFL. Due to the structural similarity between cellulose and chitin, chitin is analyzed as the ADF fraction in various insect sources [1,24]. In our study, the concentrations of chitin in the four dried full-fat BSFL were less than those in previous studies [5,6], likely due to the high fat concentration and dilution effects. In particular, chitin concentrations in the infrared-dried BSFL were greater than the others. However, it is uncertain if chitosonium acetate can be converted to chitin at high temperatures, ranging from 80 to 140 °C [33]. Generally, chitin can be regenerated from a chitosan-acetic acid complex. Therefore, it can be speculated that the relatively high temperature of 95 °C during infrared drying induced a higher chitin concentration in the infrared-dried BSFL.
The in vitro nutrient utilization of full-fat BSFL in the present study was greater than the previously reported values except for the IVID of CP in infrared-dried BSFL [1,5,6]. The greater in vitro nutrient utilization in this work is likely due to the greater EE concentration, compared to previous studies, as the EE from BSFL is more digestible than other nutrients [1]. Additionally, the concentration of chitin in the present study ranges from 1.9 to 3.3%, whereas in a previous study, it was reported as 6.6% in full-fat BSFL [28]. Chitin is not effectively degraded by the digestive enzyme solutions used in the present study and is negatively correlated with nutrient utilization [6,24]. Therefore, excessive chitin content could decrease in vitro nutrient utilization [24]. However, the IVID of CP in infrared-dried BSFL was lower than in the previous studies. It is likely that protein denaturation caused by infrared drying in our study may have negatively affected CP digestibility [14]. Additionally, the relatively greater chitin concentration in infrared-dried BSFL, compared with the other BSFL would be the reason for the lower IVID of CP.
The greater IVTTD of DM in the four dried full-fat BSFL, compared with the IVID of DM is likely due to Viscozyme®, which consists of arabinase, cellulase, β-glucanase, hemicellulase, and xylanase. This complex was employed in the third step of the procedure to simulate nutrient digestion by microbial enzymes in the hindgut of pigs [1]. In the present study, the full-fat BSFL used had greater ADF concentrations. Therefore, the fibers perhaps acted as a substrate for Viscozyme®. Additionally, chitin can be effectively hydrolyzed by the fiber-degrading enzyme (Viscozyme®) due to the resemblance of their degradation pathways [34].

5. Conclusions

The present study determined the nutrient utilization of dried full-fat black soldier fly larvae using in vitro procedures for pigs. Hot air-dried, microwave-dried, and freeze-dried full-fat black soldier fly larvae were better utilized, compared with infrared-dried full-fat black soldier fly larvae for pigs.

Author Contributions

Conceptualization, K.P. and B.G.K.; methodology, J.O. and B.G.K.; formal analysis, J.O.; investigation, J.O., H.K. and K.P.; writing—original draft preparation, J.O.; writing—review and editing, H.K., K.P. and B.G.K.; supervision, B.G.K. All authors have read and agreed to the published version of the manuscript.

Funding

The authors are grateful for the support by the National Institute of Agricultural Sciences, Rural Development Administration, Republic of Korea (PJ015818).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data presented in the current work are available.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 14 01792 g001
Figure 1. Four sources of dried full-fat black soldier fly larvae were prepared by performing one of the following: (1) hot-air drying for 24 h at 65 °C; (2) microwave drying for 5 min at 700 W, three times; (3) freeze drying for 72 h at −40 °C; (4) infrared drying for 12 min at medium infrared region ranging from 2.0 to 6.0 μm and at 95 °C.
Figure 1. Four sources of dried full-fat black soldier fly larvae were prepared by performing one of the following: (1) hot-air drying for 24 h at 65 °C; (2) microwave drying for 5 min at 700 W, three times; (3) freeze drying for 72 h at −40 °C; (4) infrared drying for 12 min at medium infrared region ranging from 2.0 to 6.0 μm and at 95 °C.
Agriculture 14 01792 g001
Table 1. Chemical composition of full-fat black soldier fly larvae (BSFL) dried by various methods.
Table 1. Chemical composition of full-fat black soldier fly larvae (BSFL) dried by various methods.
Item, % As-IsHot Air-
Dried BSFL		Microwave-
Dried BSFL		Freeze-
Dried BSFL		Infrared-
Dried BSFL
Dry matter95.895.496.894.6
Gross energy, kcal/kg7080696969806913
Crude protein 34.131.636.830.0
Ether extract52.852.249.250.6
Ash3.63.53.63.5
Acid detergent fiber6.45.65.99.1
Chitin 12.21.91.93.3
1 Chitin (%) = ash-free acid detergent fiber (%) − acid detergent fiber-linked protein (%).
Table 2. In vitro disappearance (%) of nutrients in full-fat black soldier fly larvae (BSFL) dried by various methods 1.
Table 2. In vitro disappearance (%) of nutrients in full-fat black soldier fly larvae (BSFL) dried by various methods 1.
ItemHot Air-Dried BSFLMicrowave-Dried BSFLFreeze-Dried BSFLInfrared-Dried BSFLSEMp-Value
In vitro ileal disappearance
Dry matter91.5 ab92.1 a90.3 b86.3 c0.4<0.001
Crude protein89.3 a88.2 a87.4 a74.4 b0.5<0.001
In vitro total tract disappearance
Dry matter93.0 a92.6 a91.6 a86.4 b0.3<0.001
Organic matter91.5 a92.0 a91.0 a85.7 b0.3<0.001
SEM, standard error of the means. 1 Each mean value represents data from 3 dried full-fat BSFL samples. a–c Means for the same measurement lacking a common superscript letter are different (p < 0.05).
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MDPI and ACS Style

Oh, J.; Kim, H.; Park, K.; Kim, B.G. Drying Methods for Black Soldier Fly (Hermetia illucens) Larvae as a Feed Ingredient for Pigs Affect In Vitro Nutrient Disappearance. Agriculture 2024, 14, 1792. https://doi.org/10.3390/agriculture14101792

AMA Style

Oh J, Kim H, Park K, Kim BG. Drying Methods for Black Soldier Fly (Hermetia illucens) Larvae as a Feed Ingredient for Pigs Affect In Vitro Nutrient Disappearance. Agriculture. 2024; 14(10):1792. https://doi.org/10.3390/agriculture14101792

Chicago/Turabian Style

Oh, Junghyun, Hansol Kim, Kwanho Park, and Beob Gyun Kim. 2024. "Drying Methods for Black Soldier Fly (Hermetia illucens) Larvae as a Feed Ingredient for Pigs Affect In Vitro Nutrient Disappearance" Agriculture 14, no. 10: 1792. https://doi.org/10.3390/agriculture14101792

APA Style

Oh, J., Kim, H., Park, K., & Kim, B. G. (2024). Drying Methods for Black Soldier Fly (Hermetia illucens) Larvae as a Feed Ingredient for Pigs Affect In Vitro Nutrient Disappearance. Agriculture, 14(10), 1792. https://doi.org/10.3390/agriculture14101792

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