Insects are a viable protein source for human consumption: from insect protein digestion to postprandial muscle protein synthesis in vivo in humans: a double-blind randomized trial

Wesley J H Hermans, Joan M Senden, Tyler A Churchward-Venne, Kevin J M Paulussen, Cas J Fuchs, Joey S J Smeets, Joop J A van Loon, Lex B Verdijk, Luc J C van Loon, Wesley J H Hermans, Joan M Senden, Tyler A Churchward-Venne, Kevin J M Paulussen, Cas J Fuchs, Joey S J Smeets, Joop J A van Loon, Lex B Verdijk, Luc J C van Loon

Abstract

Background: Insects have recently been identified as a more sustainable protein-dense food source and may represent a viable alternative to conventional animal-derived proteins.

Objectives: We aimed to compare the impacts of ingesting lesser mealworm- and milk-derived protein on protein digestion and amino acid absorption kinetics, postprandial skeletal muscle protein synthesis rates, and the incorporation of dietary protein-derived amino acids into de novo muscle protein at rest and during recovery from exercise in vivo in humans.

Methods: In this double-blind randomized controlled trial, 24 healthy, young men ingested 30 g specifically produced, intrinsically l-[1-13C]-phenylalanine and l-[1-13C]-leucine labeled lesser mealworm- or milk-derived protein after a unilateral bout of resistance-type exercise. Primed continuous l-[ring-2H5]-phenylalanine, l-[ring-3,5-2H2]-tyrosine, and l-[1-13C]-leucine infusions were applied, with frequent collection of blood and muscle tissue samples.

Results: A total of 73% ± 7% and 77% ± 7% of the lesser mealworm and milk protein-derived phenylalanine was released into the circulation during the 5 h postprandial period, respectively, with no significant differences between groups (P < 0.05). Muscle protein synthesis rates increased after both lesser mealworm and milk protein concentrate ingestion from 0.025 ± 0.008%/h to 0.045 ± 0.017%/h and 0.028 ± 0.010%/h to 0.056 ± 0.012%/h at rest and from 0.025 ± 0.012%/h to 0.059 ± 0.015%/h and 0.026 ± 0.009%/h to 0.073 ± 0.020%/h after exercise, respectively (all P < 0.05), with no differences between groups (both P > 0.05). Incorporation of mealworm and milk protein-derived l-[1-13C]-phenylalanine into de novo muscle protein was greater after exercise than at rest (P < 0.05), with no differences between groups (P > 0.05).

Conclusions: Ingestion of a meal-like amount of lesser mealworm-derived protein is followed by rapid protein digestion and amino acid absorption and increases muscle protein synthesis rates both at rest and during recovery from exercise. The postprandial protein handling of lesser mealworm does not differ from ingesting an equivalent amount of milk protein concentrate in vivo in humans.This trial was registered at www.trialregister.nl as NL6897.

Keywords: FSR; intrinsically labeled protein; milk protein; protein metabolism; stable isotopes.

© The Author(s) 2021. Published by Oxford University Press on behalf of the American Society for Nutrition.

Figures

FIGURE 1
FIGURE 1
Plasma leucine (A), phenylalanine (B), and tyrosine (C) concentrations after ingestion of milk- (MILK; n = 12) or lesser mealworm– (WORM; n = 12) derived protein during 5 h of recovery from a single bout of unilateral exercise in healthy, young men. The dotted line represents the time of protein ingestion. Values represent means ± SDs. Data were analyzed using repeated-measures (Time × Group) ANOVA and separate analyses were performed when a significant interaction was detected. Bonferroni post hoc testing was used to detect differences between groups. Time × Group interactions were observed for plasma leucine, phenylalanine, and tyrosine concentrations (all P < 0.05). *MILK significantly different from WORM (P < 0.05). MILK, 30 g milk protein concentrate; WORM, 30 g lesser mealworm–derived protein.
FIGURE 2
FIGURE 2
Plasma EAA (A), NEAA (B), and TAA (C) concentrations and iAUCs after ingestion of milk- (MILK; n = 12) or lesser mealworm– (WORM; n = 12) derived protein during 5 h of recovery from a single bout of unilateral exercise in healthy, young men. The dotted line represents the time of protein ingestion. Values represent means ± SDs. Data were analyzed using repeated-measures (Time × Group) ANOVA and separate analyses were performed when a significant interaction was detected. Bonferroni post hoc testing was used to detect differences between groups. Time × Group interactions were observed for plasma EAAs, NEAAs, and TAAs (all P < 0.05). *MILK significantly different from WORM (P < 0.05). EAA, essential amino acid; MILK, 30 g milk protein concentrate; NEAA, nonessential amino acid; TAA, total amino acid; WORM, 30 g lesser mealworm–derived protein.
FIGURE 3
FIGURE 3
Exogenous phenylalanine Ra (A), endogenous phenylalanine Ra (B), total phenylalanine Ra (C), and total plasma phenylalanine Rd (D) after ingestion of milk- (MILK; n = 12) or lesser mealworm– (WORM; n = 12) derived protein during 5 h of recovery from a single bout of unilateral exercise in healthy, young men. The dotted line represents the time of protein ingestion. Values represent means ± SDs. Data were analyzed using repeated-measures (Time × Group) ANOVA and separate analyses were performed when a significant interaction was detected. Bonferroni post hoc testing was used to detect differences between groups. Time × Group interactions were observed for exogenous phenylalanine Ra, total phenylalanine Ra, and total phenylalanine Rd (all P < 0.05). *MILK significantly different from WORM (P < 0.05). MILK, 30 g milk protein concentrate; Ra, rate of appearance; Rd, rate of disappearance; WORM, 30 g lesser mealworm–derived protein.
FIGURE 4
FIGURE 4
Dietary protein–derived phenylalanine (expressed as a percentage of total amount of protein-bound phenylalanine ingested) released in the circulation during 5 h after ingestion of milk- (MILK; n = 12) or lesser mealworm– (WORM; n = 12) derived protein in healthy, young men. Values represent means ± SDs. Data were analyzed using an independent t test. MILK, 30 g milk protein concentrate; WORM, 30 g lesser mealworm–derived protein.
FIGURE 5
FIGURE 5
Mixed muscle protein FSRs assessed using l-[ring-2H5]-phenylalanine after ingestion of milk- (MILK; n = 12) or lesser mealworm– (WORM; n = 11) derived protein for both REST and EXERCISE in healthy, young men. Values represent means ± SDs. Data were analyzed using repeated-measures (Time × Leg × Group) ANOVA, and separate analyses were performed when a significant interaction was detected. A Time × Leg × Group interaction was absent (P > 0.05). A Time × Leg interaction was observed (P < 0.05). #Both 0–2 h and 0–5 h postprandial FSR significantly different from basal (P < 0.05); $postprandial FSR in EXERCISE significantly different from REST (P < 0.05). EXERCISE, exercised leg; FSR, fractional synthesis rate; MILK, 30 g milk protein concentrate; REST, rested leg; WORM, 30 g lesser mealworm–derived protein.
FIGURE 6
FIGURE 6
Corrected l-[1-13C]-phenylalanine enrichment in mixed muscle protein over time after ingestion of milk- (MILK; n = 12) or lesser mealworm– (WORM; n = 11) derived protein for both REST and EXERCISE in healthy, young men. Values for the WORM group were multiplied by 0.75 to correct for the difference in enrichment in the MILK (38.3 MPE) and WORM (50.8 MPE) protein. Values represent means ± SDs. Data were analyzed using repeated-measures (Time × Leg × Group) ANOVA, and separate analyses were performed when a significant interaction was detected. A Time × Leg × Group interaction was absent (P > 0.05). A Time × Leg interaction was observed (P < 0.05). +t = 2 h significantly different from t = 0 h (P < 0.05); #t = 5 h significantly different from t = 0 and t = 2 h (P < 0.05); $REST significantly different from EXERCISE for that time point (P < 0.05). EXERCISE, exercised leg; MILK, 30 g milk protein concentrate; MPE, mole percentage excess; REST, rested leg; WORM, 30 g lesser mealworm–derived protein.

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