Black Soldier Fly (Hermetia Illucens) Larvae Protein Derivatives: Potential to Promote Animal Health.

[en] European legislation permits the inclusion of insect proteins in pet and aquaculture diets. Black soldier fly larvae (BSF) are one of the most actively produced species due to their low environmental impact and nutritional characteristics. BSF protein derivatives (proteins and protein hydrolysates) contain a substantial amount of low molecular weight peptides that are known to possess antioxidant potential. In this study, the in vitro antioxidant potential of commercial BSF proteins and protein hydrolysates was investigated for (1) radical scavenging activity, (2) myeloperoxidase activity modulation, and (3) neutrophil response modulation. Chickenmeal and fishmeal are commonly used in pet food and aquaculture formulations. Hence, both were used as industrial benchmarks during this study. The results indicate that fishmeal and chickenmeal are ineffective at suppressing the oxidative damage caused by neutrophil response and myeloperoxidase activity. Fishmeal and chickenmeal even exhibit pro-oxidant behavior in some of the models used during this study. On the other hand, it was found that BSF protein derivatives could be effective in protecting against the cellular damage resulting from neutrophil and myeloperoxidase activities. The outcomes of this study indicate that BSF protein derivatives could be potentially included in pet food and aquaculture feed formulations as health-promoting ingredients.

Disciplines :

Food science

Author, co-author :

Mouithys-Mickalad, Ange ; Université de Liège - ULiège > Centre de l'oxygène : Recherche et développement (C.O.R.D.)

Schmitt, Eric

Dalim, Monika

Franck, Thierry ; Université de Liège - ULiège > Centre de l'oxygène : Recherche et développement (C.O.R.D.)

Tome, Nuria Martin

van Spankeren, Michel

Serteyn, Didier ; Université de Liège - ULiège > Dép. clinique des animaux de compagnie et des équidés (DCA) > Anesthésiologie gén. et pathologie chirurg. des grds animaux

Paul, Aman

Language :

English

Title :

Black Soldier Fly (Hermetia Illucens) Larvae Protein Derivatives: Potential to Promote Animal Health.

Publication date :

2020

Journal title :

Animals

eISSN :

2076-2615

Publisher :

MDPI AG, Switzerland

Volume :

Issue :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 28 April 2021

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Bibliography

Paul, A.; Frederich, M.; Uyttenbroeck, R.; Hatt, S.; Malik, P.; Lebecque, S.; Hamaidia, M.; Miazek, K.; Goffin, D.; Willems, L.; et al. Grasshoppers as a food source? A review. Biotechnol. Agron. Soc. Environ. 2016, 20, 337–352.
Paul, A.; Frederich, M.; Uyttenbroeck, R.; Malik, P.; Filocco, S.; Richel, A.; Heuskin, S.; Alabi, T.; Megido, R.C.; Franck, T.; et al. Nutritional composition and rearing potential of the meadow grasshopper (Chorthippus parallelus Zetterstedt). J. Asia-Pac. Entomol. 2016, 19, 1111–1116, doi:10.1016/j.aspen.2016.09.012.
Paul, A.; Frederich, M.; Megido, R.C.; Alabi, T.; Malik, P.; Uyttenbroeck, R.; Francis, F.; Blecker, C.; Haubruge, E.; Lognay, G.; et al. Insect fatty acids: A comparison of lipids from three Orthopterans and Tenebrio molitor L. larvae. J. Asia-Pac. Entomol. 2017, 20, 337–340, doi:10.1016/j.aspen.2017.02.001.
IPIFF. Promoting Insects for Human Consumption & Animal Feed—IPIFF. Available online: http://ipiff.org/(accessed on 5 February 2020).
Gasco, L.; Gai, F.; Maricchiolo, G.; Genovese, L.; Ragonese, S.; Bottari, T.; Caruso, G. Fishmeal Alternative Protein Sources for Aquaculture Feeds. In Feeds for the Aquaculture Sector: Current Situation and Alternative Sources; Gasco, L., Gai, F., Maricchiolo, G., Genovese, L., Ragonese, S., Bottari, T., Caruso, G., Eds.; SpringerBriefs in Molecular Science; Springer International Publishing: Cham, Switzerland, 2018; pp. 1–28, ISBN 978-3-319-77941-6.
Deng, P.; Utterback, P.L.; Parsons, C.M.; Hancock, L.; Swanson, K.S. Chemical composition, true nutrient digestibility, and true metabolizable energy of novel pet food protein sources using the precision-fed cecectomized rooster assay. J. Anim. Sci. 2016, 94, 3335–3342, doi:10.2527/jas.2016-0473.
Star, L.; Arsiwalla, T.; Molist, F.; Leushuis, R.; Dalim, M.; Paul, A. Gradual Provision of Live Black Soldier Fly (Hermetia illucens) Larvae to Older Laying Hens: Effect on Production Performance, Egg Quality, Feather Condition and Behavior. Animals 2020, 10, 216, doi:10.3390/ani10020216.
Schmitt, E.; Belghit, I.; Johansen, J.; Leushuis, R.; Lock, E.J.; Melsen, D.; Kathirampatti Ramasamy Shanmugam, R.; Van Loon, J.; Paul, A. Growth and Safety Assessment of Feed Streams for Black Soldier Fly Larvae: A Case Study with Aquaculture Sludge. Animals 2019, 9, 189, doi:10.3390/ani9040189.
Belghit, I.; Liland, N.S.; Gjesdal, P.; Biancarosa, I.; Menchetti, E.; Li, Y.; Waagbø, R.; Krogdahl, Å.; Lock, E.J. Black soldier fly larvae meal can replace fish meal in diets of sea-water phase Atlantic salmon (Salmo salar). Aquaculture 2018, doi:10.1016/j.aquaculture.2018.12.032.
Belghit, I.; Waagbø, R.; Lock, E.J.; Liland, N.S. Insect-based diets high in lauric acid reduce liver lipids in freshwater Atlantic salmon. Aquac. Nutr. 2019, 25, 343–357, doi:10.1111/anu.12860.
Li, Y.; Kortner, T.M.; Chikwati, E.M.; Munang’andu, H.M.; Lock, E.J.; Krogdahl, Å. Gut health and vaccination response in pre-smolt Atlantic salmon (Salmo salar) fed black soldier fly (Hermetia illucens) larvae meal. Fish Shellfish Immunol. 2018, 86, 1106–1113, doi:10.1016/j.fsi.2018.12.057.
Bosch, G.; Zhang, S.; Oonincx, D.G.A.B.; Hendriks, W.H. Protein quality of insects as potential ingredients for dog and cat foods. J. Nutr. Sci. 2014, 3, doi:10.1017/jns.2014.23.
Meyer, L.F.; Kolln, M.; Kamphues, J. Dog food containing insects? Studies on compound feed with larvae of the black soldier fly as the main protein source. Kleintierpraxis 2019, 64, 124–135, doi:10.2377/0023-2076- 64-124.
Head, E.; Rofina, J.; Zicker, S. Oxidative Stress, Aging, and Central Nervous System Disease in the Canine Model of Human Brain Aging. Vet. Clin. N. Am. 2008, 38, 167–178, doi:10.1016/j.cvsm.2007.10.002.
Blier, P. Fish Health: An Oxidative Stress Perspective. Fish Aquac. J. 2014, 5, 1–2.
Tsumbu, C.N.; Deby-Dupont, G.; Tits, M.; Angenot, L.; Frederich, M.; Kohnen, S.; Mouithys-Mickalad, A.; Serteyn, D.; Franck, T. Polyphenol content and modulatory activities of some tropical dietary plant extracts on the oxidant activities of neutrophils and myeloperoxidase. Int. J. Mol. Sci. 2012, 13, 628–650, doi:10.3390/ijms13010628.
Paul, A. Field Border Flowering Strips As a Source of Valuable Compounds. PhD Thesis, Gembloux Agro- Bio Tech University of Liège, Gembloux, Belgique, 2017.
Lobo, V.; Patil, A.; Phatak, A.; Chandra, N. Free radicals, antioxidants and functional foods: Impact on human health. Pharm. Rev. 2010, 4, 118–126, doi:10.4103/0973-7847.70902.
Elias, R.J.; Kellerby, S.S.; Decker, E.A. Antioxidant Activity of Proteins and Peptides. Crit. Rev. Food Sci. Nutr. 2008, 48, 430–441, doi:10.1080/10408390701425615.
Zielińska, E.; Karaś, M.; Jakubczyk, A. Antioxidant activity of predigested protein obtained from a range of farmed edible insects. Int. J. Food Sci. Technol. 2017, 52, 306–312, doi:10.1111/ijfs.13282.
Zielińska, E.; Baraniak, B.; Karaś, M. Antioxidant and Anti-Inflammatory Activities of Hydrolysates and Peptide Fractions Obtained by Enzymatic Hydrolysis of Selected Heat-Treated Edible Insects. Nutrients 2017, 9, 970, doi:10.3390/nu9090970.
Zielińska, E.; Baraniak, B.; Karaś, M. Identification of antioxidant and anti-inflammatory peptides obtained by simulated gastrointestinal digestion of three edible insects species (Gryllodes sigillatus, Tenebrio molitor, Schistocerca gragaria). Int. J. Food Sci. Technol. 2018, 53, 2542–2551, doi:10.1111/ijfs.13848.
Vercruysse, L.; Smagghe, G.; Herregods, G.; Van Camp, J. ACE Inhibitory Activity in Enzymatic Hydrolysates of Insect Protein. J. Agric. Food Chem. 2005, 53, 5207–5211, doi:10.1021/jf050337q.
Paul, A. EU Patent Application: N2023838—Hydrolysate of Water Soluble Insect Proteins.
Arsiwalla, T.; Aarts, K.W.P. United States Patent Application: 0150223508—Method to Convert Insects or Worms into Nutrient Streams and Compositions Obtained Thereby A1. Available online: https://patents.google.com/patent/US20150223508A1/en (accessed on 27 March 2020).
Zhu, D.; Huang, X.; Tu, F.; Wang, C.; Yang, F. Preparation, antioxidant activity evaluation, and identification of antioxidant peptide from black soldier fly (Hermetia illucens L.) larvae. J. Food Biochem. 2020, e13186, doi:10.1111/jfbc.13186.
Firmansyah, M.; Abduh, M.Y. Production of protein hydrolysate containing antioxidant activity from Hermetia illucens. Heliyon 2019, 5, e02005, doi:10.1016/j.heliyon.2019.e02005.
Smith, P.K.; Krohn, R.I.; Hermanson, G.T.; Mallia, A.K.; Gartner, F.H.; Provenzano, M.D.; Fujimoto, E.K.; Goeke, N.M.; Olson, B.J.; Klenk, D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150, 76–85, doi:10.1016/0003-2697(85)90442-7.
Brand-Williams, W.; Cuvelier, M.E.; Berset, C. Use of a free radical method to evaluate antioxidant activity. LWT 1995, 28, 25–30, doi:10.1016/S0023-6438(95)80008-5.
Arnao, M.B.; Cano, A.; Acosta, M. The hydrophilic and lipophilic contribution to total antioxidant activity. Food Chem. 2001, 73, 239–244, doi:10.1016/S0308-8146(00)00324-1.
Franck, T.; Kohnen, S.; Boudjeltia, K.Z.; Van Antwerpen, P.; Bosseloir, A.; Niesten, A.; Gach, O.; Nys, M.; Deby-Dupont, G.; Serteyn, D. A new easy method for specific measurement of active myeloperoxidase in human biological fluids and tissue extracts. Talanta 2009, 80, 723–729, doi:10.1016/j.talanta.2009.07.052.
Zhang, H.; Holden-Wiltse, J.; Wang, J.; Liang, H. A Strategy to Model Nonmonotonic Dose-Response Curve and Estimate IC50. PLoS ONE 2013, 8, e69301, doi:10.1371/journal.pone.0069301.
R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2017.
Chang, S.K.C.; Zhang, Y. Protein Analysis. In Food Analysis; Nielsen, S.S., Ed.; Food Science Text Series; Springer International Publishing: Cham, Switzerland, 2017; pp. 315–331, ISBN 978-3-319-45776-5.
Makkar, H.P.S.; Tran, G.; Heuzé, V.; Ankers, P. State-of-the-art on use of insects as animal feed. Anim. Feed Sci. Technol. 2014, 197, 1–33, doi:10.1016/j.anifeedsci.2014.07.008.
Rojas, O.J.; Stein, H.H. Effects of replacing fish, chicken, or poultry by-product meal with fermented soybean meal in diets fed to weanling pigs. Rev. Colomb. Cienc. Pecu. 2015, 28, 22–41.
Li, P.; Wu, G. Composition of amino acids and related nitrogenous nutrients in feedstuffs for animal diets. Amino Acids 2020, 1–20, doi:10.1007/s00726-020-02833-4.
Zou, T.B.; He, T.P.; Li, H.B.; Tang, H.W.; Xia, E.Q. The Structure-Activity Relationship of the Antioxidant Peptides from Natural Proteins. Molecules 2016, 21, 72, doi:10.3390/molecules21010072.
Yang, X.R.; Zhang, L.; Ding, D.G.; Chi, C.F.; Wang, B.; Huo, J.C. Preparation, Identification, and Activity Evaluation of Eight Antioxidant Peptides from Protein Hydrolysate of Hairtail (Trichiurus japonicas) Muscle. Mar Drugs 2019, 17, 23, doi:10.3390/md17010023.
Cai, L.; Wu, X.; Zhang, Y.; Li, X.; Ma, S.; Li, J. Purification and characterization of three antioxidant peptides from protein hydrolysate of grass carp (Ctenopharyngodon idella) skin. J. Funct. Foods 2015, 16, 234–242, doi:10.1016/j.jff.2015.04.042.
Esfandi, R.; Walters, M.E.; Tsopmo, A. Antioxidant properties and potential mechanisms of hydrolyzed proteins and peptides from cereals. Heliyon 2019, 5, doi:10.1016/j.heliyon.2019.e01538.
FAO. The Production of Fish Meal and Oil; FAO: Rome, Italy, 1986.
Diedrich, D.M. For Pet’s Sake, Do Something! Book Two: How to Heal You Sick, Overfed, and Bored Pets with Nutrition, Supplements, Herbs, and Exercise (Mom’s Choice Award Recipient); Two Paws Up Press, Minnesota, USA: 2007; ISBN 978-0-9713812-8-5.
Nygaard, H. Standard Norwegian fishmeal- and Fishoil Process. Heat Treatment Requirements; Nofima: Tromsø, Norway, 2010; p. 30.
Bartosz, G. Food Oxidants and Antioxidants: Chemical, Biological, and Functional Properties; CRC Press, Florida, USA: 2013; ISBN 978-1-4398-8242-9.
Yu, T.Y.; Morton, J.D.; Clerens, S.; Dyer, J.M. Cooking-Induced Protein Modifications in Meat. Compr. Rev. Food Sci. Food Saf. 2017, 16, 141–159, doi:10.1111/1541-4337.12243.
Celi, P.; Gabai, G. Oxidant/Antioxidant Balance in Animal Nutrition and Health: The Role of Protein Oxidation. Front. Vet. Sci. 2015, 2, doi:10.3389/fvets.2015.00048.
Gallegos, M.E.H.; Zannatha, M.M.I.; Osornio, E.G.; Sánchez, A.S.; del Rio, F.A.P. The Activities of Six Exo-and Endopeptidases in the Substantia Nigra, Neostriatum, and Cortex of the Rat Brain. Neurochem. Res. 1999, 24, 1557–1561, doi:10.1023/A:1021156216661.
Perobelli, S.M.; Galvani, R.G.; Gonçalves-Silva, T.; Xavier, C.R.; Nóbrega, A.; Bonomo, A. Plasticity of neutrophils reveals modulatory capacity. Braz. J. Med. Biol. Res. 2015, 48, 665–675, doi:10.1590/1414- 431X20154524.
Swain, S.D.; Rohn, T.T.; Quinn, M.T. Neutrophil Priming in Host Defense: Role of Oxidants as Priming Agents. Antioxid. Redox Signal. 2002, 4, 69–83, doi:10.1089/152308602753625870.
Zholobenko, A.; Mouithys-Mickalad, A.; Modriansky, M.; Serteyn, D.; Franck, T. Polyphenols from Silybum marianum inhibit in vitro the oxidant response of equine neutrophils and myeloperoxidase activity. J. Vet. Pharmacol. Ther. 2016, 39, 592–601, doi:10.1111/jvp.12319.
Yamka, R.M.; Jamikorn, U.; True, A.D.; Harmon, D.L. Evaluation of low-ash poultry meal as a protein source in canine foods. J. Anim. Sci. 2003, 81, 2279–2284, doi:10.2527/2003.8192279x.
Ben Hamed, S.; Tavares Ranzani-Paiva, M.J.; Tachibana, L.; de Carla Dias, D.; Ishikawa, C.M.; Esteban, M.A. Fish pathogen bacteria: Adhesion, parameters influencing virulence and interaction with host cells. Fish Shellfish Immunol. 2018, 80, 550–562, doi:10.1016/j.fsi.2018.06.053.
Washabau, R.J.; Day, M.J. Canine and Feline Gastroenterology—E-Book; Elsevier Health Sciences, Oxford, UK: 2012; ISBN 978-1-4377-0302-3.
Wang, B.; Xie, N.; Li, B. Influence of peptide characteristics on their stability, intestinal transport, and in vitro bioavailability: A review. J. Food Biochem. 2019, 43, e12571, doi:10.1111/jfbc.12571.
Hill, R.W.; Wyse, G.A.; Anderson, M. Animal Physiology, 3rd ed.; Sinauer Associates, Massachusetts, USA: 2013; ISBN 9780878935598.