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25 Nov 2011
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access type Open Access

Hermetia illucens fat affects the gastrointestinal tract selected microbial populations, their activity, and the immune status of broiler chickens

Published Online: 17 Sep 2021
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Journal Details
License
Format
Journal
First Published
25 Nov 2011
Publication timeframe
4 times per year
Languages
English
Abstract

The present study investigated the effect of Hermetia illucens larvae (BSFL) fat, derived using supercritical CO2 extraction and added to broiler chickens’ diets as a partial (50%) or total replacement for commonly used soybean oil, on the gastrointestinal tract (GIT) microbial population, its activity, and selected physiological and immune traits. A total of 576 one-dayold female Ross 308 chicks were randomly assigned to 3 dietary treatments with 16 replicates each. The following treatments were applied: SO – 100% soybean oil, BSFL50 – a mixture of BSFL and soybean oils in a 50:50 ratio, and BSFL100 – 100% BSFL fat. Digesta samples from the crop, jejunum and ceca were collected for further analyses, i.e., pH measurements, fluorescent in situ hybridization, and short-chain fatty acid (SCFA) concentrations. Additionally, the selected plasma biochemical parameters and immunological traits were assessed. In general, the implementation of BSFL fat in broilers’ diets resulted in increased proliferation of potentially pathogenic bacterial populations in the crop, such as Enterobacteriaceae, BacteroidesPrevotella cluster, and Clostridium perfringens. Furthermore, BSFL100 enhanced microbial activity via total SCFA production and lowered the pH in this segment. However, no detrimental effects were observed in terms of other GIT segments, i.e., the jejunal and cecal microecosystems. The strongest impact on reduction of select components of the microbial population in the cecum was observed with the BSFL50 treatment for potentially pathogenic bacteria such as Enterobacteriaceae, BacteroidesPrevotella cluster, while commensal populations were also limited, i.e., Bacillus spp., C.leptum subgroup, and C.coccoidesEubacteriumrectale cluster. Additionally, BSFL100 reduced the cholesterol concentration in the blood, while both experimental treatments decreased the ALT level. In conclusion, due to the insufficient release of lauric acid from the BSFL fat in the crop, an adverse shift in the microbiota can be noted. However, a positive suppressive effect on the select components of the cecal microbiota, as well as improvement of liver health suggests implying the BSFL fat in broiler nutrition.

Keywords

Alzawqari M., Moghaddam H.N., Kermanshahi H., Raji A.R. (2011). The effect of desiccated ox bile supplementation on performance, fat digestibility, gut morphology and blood chemistry of broiler chickens fed tallow diets. J. Appl. Anim Res., 39: 169–174.Search in Google Scholar

Aviagen. (2018). Ross Broiler Management Handbook. Aviagen Limited Newbridge Midlothian EH28 8SZ, Scotland, UK.Search in Google Scholar

Baltić B., Ćirić J., Šefer D., Radovanović A., Đorđević J., Glišić M., Bošković M., Baltić M.Ž., Đorđević V., Marković R. (2018). Effect of dietary dupplementation with medium chain fatty acids on growth performance, intestinal histomorphology, lipid profile and intestinal microflora of broiler chickens. S. Afr. J. Anim. Sci., 48: 885–896.Search in Google Scholar

Baltić B., Starčević M., Đorđević J., Mrdović B., Marković R. (2017). Importance of medium chain fatty acids in animal nutrition. In: IOP Conference Series: Earth Env. Sci., IOP Publishing, 85: 12048.Search in Google Scholar

Barragan-Fonseca K.B., Gort G., Dicke M., van Loon J.J.A. (2019). Effects of dietary protein and carbohydrate on life-history traits and body protein and fat contents of the black soldier fly Hermetia illucens. Physiol. Entomol., 44: 148–159.Search in Google Scholar

Belghit I., Liland N.S., Waagbø R., Biancarosa I., Pelusio N., Li Y., Krogdahl Å., Lock E-J. (2018). Potential of insect-based diets for Atlantic salmon (Salmo salar). Aquaculture, 491: 72–81.Search in Google Scholar

Benzertiha A., Kierończyk B., Rawski M., Kołodziejski P., Bryszak M., Józefiak D. (2019). Insect oil as an alternative to palm oil and poultry fat in broiler chicken nutrition. Animals, 9: 116.Search in Google Scholar

Benzertiha A., Kierończyk B., Rawski M., Mikołajczak Z., Urbański A., Nogowski L., Józefiak D. (2020). Insect fat in animal nutrition: a review. Ann. Anim. Sci., 20: 1217–1240.Search in Google Scholar

Caligiani A., Marseglia A., Sorci A., Bonzanini F., Lolli V., Maistrello L., Sforza S. (2019). Influence of the killing method of the black soldier fly on its lipid composition. Food Res. Int., 116: 276–282.Search in Google Scholar

Canibe N., Højberg O., Badsberg J. H., Jensen B.B. (2007). Effect of feeding fermented liquid feed and fermented grain on gastrointestinal ecology and growth performance in piglets. J. Anim. Sci., 85: 2959–2971.Search in Google Scholar

Costantini L., Molinari R., Farinon B., Merendino N. (2017). Impact of omega-3 fatty acids on the gut microbiota. Int. J. Mol. Sci., 18: 2645.Search in Google Scholar

Cullere M., Schiavone A., Dabbou S., Gasco L., Dalle Zotte A. (2019). Meat quality and sensory traits of finisher broiler chickens fed with black soldier fly (Hermetia illucens L.) larvae fat as alternative fat source. Animals, 9: 1–15.Search in Google Scholar

Dabbou S., Ferrocino I., Gasco L., Schiavone A., Trocino A., Xiccato G., Lajusticia A.C.B., Maione S., Soglia D., Biasato I. (2020). Antimicrobial effects of black soldier fly and yellow mealworm fats and their impact on gut microbiota of growing rabbits. Animals, 10: 1292.Search in Google Scholar

Dabbou S., Lauwaerts A., Ferrocino I., Biasato I., Sirri F., Zampiga M., Bergagna S., Pagliasso G., Gariglio M., Colombino E. (2021). Modified black soldier fly larva fat in broiler diet: effects on performance, carcass traits, blood parameters, histomorphological features and gut microbiota. Animals, 11: 1837.Search in Google Scholar

Dalle Zotte A., Cullere M., Martins C., Alves S.P., Freire J.P.B., Falcão-e-Cunha L., Bessa R.J.B. (2018). Incorporation of black soldier fly (Hermetia illucens L.) larvae fat or extruded linseed in diets of growing rabbits and their effects on meat quality traits including detailed fatty acid composition. Meat Sci., 146: 50–58.Search in Google Scholar

Dumas A, Raggi T., Barkhouse J., Lewis E., Weltzien E. (2018). The oil fraction and partially defatted meal of black soldier fly larvae (Hermetia illucens) affect differently growth performance, feed efficiency, nutrient deposition, blood glucose and lipid digestibility of rainbow trout (Oncorhynchus mykiss). Aquaculture, 492: 24–34.Search in Google Scholar

Ewald N., Vidakovic A., Langeland M., Kiessling A., Sampels S., Lalander C. (2020). Fatty acid composition of black soldier fly larvae (Hermetia illucens) – possibilities and limitations for modification through diet. Waste Manage, 102: 40–47.Search in Google Scholar

Fallani M., Rigottier-Gois L., Aguilera M., Bridonneau C., Collignon A., Edwards C.A., Corthier G., Doré J. (2006). Clostridium difficile and Clostridium perfringens species detected in infant faecal microbiota using 16S rRNA targeted probes. J. Microbiol. Meth., 67: 150–161.Search in Google Scholar

Feng W., Xiong H., Wang W., Duan X., Yang T., Wu C., Yang F., Xiong J., Wang T., Wang C. (2019). Energy consumption analysis of lipid extraction from black soldier fly biomass. Energy, 185: 1076–1085.Search in Google Scholar

Franks A.H., Harmsen H.J.M., Raangs G.C., Jansen G.J., Schut F., Welling G.W. (1998). Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol., 64: 3336–3345.Search in Google Scholar

Gasco L., Dabbou S., Gai F., Brugiapaglia A., Schiavone A., Birolo M., Xiccato G., Trocino A. (2019). Quality and consumer acceptance of meat from rabbits fed diets in which soybean oil is replaced with black soldier fly and yellow mealworm fats. Animals, 9: 629.Search in Google Scholar

Hejdysz M., Kaczmarek S., Józefiak D., Jamroz D., Rutkowski A. (2018). Effect of different medium chain fatty acids, calcium butyrate, and salinomycin on performance, nutrient utilization, and fermentation products in gastrointestinal tracts of broiler chickens. J. Anim. Plant Sci., 28: 377–387.Search in Google Scholar

Heuel M., Sandrock C., Leiber F., Mathys A., Gold M., Zurbrügg C., Gangnat I.D.M., Kreuzer M., Terranova M. (2021). Black soldier fly larvae meal and fat can completely replace soybean cake and oil in diets for laying hens. Poultry Sci., 100: 101034.Search in Google Scholar

van Heugten E., Martinez G., McComb A., Koutsos E. (2019). 285 Black soldier fly (Hermetia illucens) larvae oil improves growth performance of nursery pigs. J. Anim. Sci., 97(Supplement 3): 118.Search in Google Scholar

Jackowski J., Hurej M., Rój E., Poplonski J., Kosny L., Huszcza E. (2015). Antifeedant activity of xanthohumol and supercritical carbon dioxide extract of spent hops against stored product pests. B. Entomol. Res., 105: 456.Search in Google Scholar

Józefiak D., Kierończyk B., Rawski M., Hejdysz M., Rutkowski A., Engberg R.M., Højberg O. (2014). Clostridium perfringens challenge and dietary fat type affect broiler chicken performance and fermentation in the gastrointestinal tract. Animal, 8: 912–922.Search in Google Scholar

Józefiak D., Świątkiewicz S., Kierończyk B., Rawski M., Długosz J., Engberg R.M., Højberg O. (2016). Clostridium perfringens challenge and dietary fat type modifies performance, microbiota composition and histomorphology of the broiler chicken gastrointestinal tract. Eur. Poultry Sci., 80.Search in Google Scholar

Józefiak D., Józefiak A., Kierończyk B., Rawski M., Świątkiewicz S., Długosz J., Engberg R.M. (2016). Insects–a natural nutrient source for poultry – a review. Ann. Anim. Sci., 16: 297–313.Search in Google Scholar

Józefiak D., Kierończyk B., Juśkiewicz J., Zduńczyk Z., Rawski M., Długosz J., Sip A., Højberg O. (2013). Dietary nisin modulates the gastrointestinal microbial ecology and enhances growth performance of the broiler chickens. Plos One, 8(12): 1–11.Search in Google Scholar

Kierończyk B., Sassek M., Pruszynska-Oszmalek E., Kolodziejski P., Rawski M., Świątkiewicz S., Józefiak D. (2017). The physiological response of broiler chickens to the dietary supplementation of the bacteriocin nisin and ionophore coccidiostats. Poultry Sci., 96: 4026–4037.Search in Google Scholar

Kierończyk B., Rawski M., Długosz J., Świątkiewicz S., Józefiak D. (2016). Avian crop function – a review. Ann. Anim. Sci., 16: 653–678.Search in Google Scholar

Kierończyk B., Rawski M., Józefiak A., Mazurkiewicz J., Świątkiewicz S., Siwek M., Bednarczyk M., Szumacher-Strabel M., Cieślak A., Benzertiha A., Józefiak D. (2018). Effects of replacing soybean oil with selected insect fats on broilers. Anim. Feed Sci. Tech., 240: 170–183.Search in Google Scholar

Kierończyk B., Sypniewski J., Rawski M., Czekała W., Świątkiewicz S., Józefiak D. (2020). From waste to sustainable feed material: the effect of Hermetia illucens oil on the growth performance, nutrient digestibility, and gastrointestinal tract morphometry of broiler chickens. Ann. Anim. Sci., 20: 157–177.Search in Google Scholar

Kim B., Bang H.T., Jeong J.Y., Kim M., Kim K.H., Chun J.L., Ji S.Y. (2020). Effects of dietary supplementation of black soldier fly (Hermetia illucens) larvae oil on broiler health. J. Poultry Sci., 200070.Search in Google Scholar

Kim S.A., Rhee M.S. (2016). Highly enhanced bactericidal effects of medium chain fatty acids (caprylic, capric, and lauric acid) combined with edible plant essential oils (carvacrol, eugenol, β-resorcylic acid, trans-cinnamaldehyde, thymol, and vanillin) against Escherichia coli O15. Food Control, 60: 447–454.Search in Google Scholar

Kim Y.B., Kim D.H., Jeong S.B., Lee J.W., Kim T.H., Lee H.G., Lee K.W. (2020). Black soldier fly larvae oil as an alternative fat source in broiler nutrition. Poultry Sci., 99: 3133–3143.Search in Google Scholar

Larouche J., Deschamps M.-H., Saucier L., Lebeuf Y., Doyen A., Vandenberg G.W. (2019). Effects of killing methods on lipid oxidation, colour and microbial load of black soldier fly (Hermetia illucens) larvae. Animals, 9: 182.Search in Google Scholar

Li S., Ji H., Zhang B., Tian J., Zhou J., Yu H. (2016). Influence of black soldier fly (Hermetia illucens) larvae oil on growth performance, body composition, tissue fatty acid composition and lipid deposition in juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture, 465: 43–52.Search in Google Scholar

Lieberman S., Enig M.G., Preuss H.G. (2006). A review of monolaurin and lauric acid: natural virucidal and bactericidal agents. Altern. Complem. Ther., 12: 310–314.Search in Google Scholar

Lin C.-W., Huang T.-W., Peng Y.-J., Lin Y.-Y., Mersmann H.J., Ding S.-T. (2021). A novel chicken model of fatty liver disease induced by high cholesterol and low choline diets. Poultry Sci., 100: 100869.Search in Google Scholar

Mai H.C., Dao N.D., Lam T.D., Nguyen B.V., Nguyen D.C., Bach L.G. (2019). Purification process, physicochemical properties, and fatty acid composition of black soldier fly (Hermetia illucens Linnaeus) larvae oil. J. Am. Oil Chem. Soc., 96: 1303–1311.Search in Google Scholar

Mailund T. (2019). Manipulating data frames: dplyr. In: R Data Science Quick Reference, 109–60. Springer.Search in Google Scholar

Manz W., Szewzyk U., Ericsson P., Amann R., Schleifer K.H., Stenström T.A. (1993). In situ identification of bacteria in drinking water and adjoining biofilms by hybridization with 16S and 23S rRNA-directed fluorescent oligonucleotide probes. Appl. Environ. Microb., 59: 2293–2298.Search in Google Scholar

Melis R., Braca A., Mulas G., Sanna R., Spada S., Serra G., Fadda M.L., Roggio T., Uzzau S., Anedda R. (2018). Effect of freezing and drying processes on the molecular traits of edible yellow mealworm. Innov. Food Sci. Emerg., 48: 138–149.Search in Google Scholar

Mendiburu F.D., Simon R. (2015). Agricolae-ten years of an open source statistical tool for experiments in breeding, agriculture and biology. Peer J. Pre Prints, 3:e1404v1.Search in Google Scholar

Mentang F., Maita M., Ushio H., Ohshima T. (2011). Efficacy of silkworm (Bombyx mori L.) chrysalis oil as a lipid source in adult wistar rats. Food Chem., 127: 899–904.Search in Google Scholar

Moscoviz R., Trably E., Bernet N. (2016). Consistent 1,3-propanediol production from glycerol in mixed culture fermentation over a wide range of pH. Biotech. Biofuels, 9: 32.Search in Google Scholar

Neijat M., Habtewold J., Li S., Jing M., House J.D. (2020). Effect of dietary n-3 polyunsaturated fatty acids on the composition of cecal microbiome of Lohmann hens. Prostag. Leukotr. Ess., 162: 102182.Search in Google Scholar

Ogle D.H. (2016). Introductory Fisheries Analyses with R. Vol. 32. CRC Press.Search in Google Scholar

Poorghasemi M., Alireza S., Qotbi A.A.A., Laudadio V., Tufarelli V. (2013). Influence of dietary fat source on growth performance responses and carcass traits of broiler chicks. Asian Austral. J. Anim., 26: 705.Search in Google Scholar

Purschke B., Stegmann T., Schreiner M., Jäger H. (2017). Pilot‐scale supercritical CO2 extraction of edible insect oil from Tenebrio molitor L. larvae–influence of extraction conditions on kinetics, defatting performance and compositional properties. Eur. J. Lipid Sci. Tech., 119: 1600134.Search in Google Scholar

Rasco D. (2020). An R Companion for Applied Statistics I: Basic Bivariate Techniques. SAGE Publications, Thousand Oaks, CA, USA.Search in Google Scholar

Rawski M., Kierończyk B., Długosz J., Świątkiewicz S., Józefiak D. (2016). Dietary probiotics affect gastrointestinal microbiota, histological structure and shell mineralization in turtles. Plos One, 11(2): e0147859.Search in Google Scholar

Revelle W. (2017). An Introduction to the Psych Package: Part I: Data Entry and Data Description. Retrieved from https://personality-project.org/r/psych/intro.pdf.Search in Google Scholar

Rodriguez-Sanchez R., Tres A., Sala R., Guardiola F., Barroeta A.C. (2019). Evolution of lipid classes and fatty acid digestibility along the gastrointestinal tract of broiler chickens fed different fat sources at different ages. Poultry Sci., 98: 1341–1353.Search in Google Scholar

Salzman N.H., de Jong H., Paterson Y., Harmsen H.J.M., Welling G.W., Bos N.A. (2002). Analysis of 16S libraries of mouse gastrointestinal microflora reveals a large new group of mouse intestinal bacteria. Microbiology, 148: 3651–3660.Search in Google Scholar

Schiavone A., Dabbou S., De Marco M., Cullere M., Biasato I., Biasibetti E., Capucchio M.T., Bergagna S., Dezzutto D., Meneguz M., Gai F., Dalle Zotte A., Gasco L. (2018). Black soldier fly larva fat inclusion in finisher broiler chicken diet as an alternative fat source. Animal, 12: 2032–2039.Search in Google Scholar

Schiavone A., Cullere M., De Marco M., Meneguz M., Biasato I., Bergagna S., Dezzutto D., Gai F., Dabbou S., Gasco L. (2017). Partial or total replacement of soybean oil by black soldier fly larvae (Hermetia illucens L.) fat in broiler diets: effect on growth performances, feed choice, blood traits, carcass characteristics and meat quality. Ital. J. Anim. Sci., 16: 93–100.Search in Google Scholar

Schumacker R., Tomek S. (2013). R Fundamentals. In: Understanding statistics using R, Schumacker R., Tomek S. (eds.). Springer New York, USA, pp. 1–10.Search in Google Scholar

Sghir A., Gramet G., Suau A., Rochet V., Pochart P., Dore J. (2000). Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl. Environ. Microbiol., 66: 2263–2266.Search in Google Scholar

Spranghers T., Ottoboni M., Klootwijk C., Ovyn A., Deboosere S., De Meulenaer B., Michiels J., Eeckhout M., De Clercq P., De Smet S. (2017). Nutritional composition of black soldier fly (Hermetia illucens) prepupae reared on different organic waste substrates. J. Sci. Food Agr., 97: 2594–2600.Search in Google Scholar

Sypniewski J., Kierończyk B., Benzertiha A., Mikołajczak Z., Pruszyńska-Oszmałek E., Kołodziejski P., Sassek M., Rawski M., Czekała W., Józefiak D. (2020). Replacement of soybean oil by Hermetia illucens fat in turkey nutrition: effect on performance, digestibility, microbial community, immune and physiological status and final product quality. Brit. Poultry Sci., 61: 294–302.Search in Google Scholar

Tancharoenrat P., Ravindran V., Zaefarian F., Ravindran G. (2013). Influence of age on the apparent metabolisable energy and total tract apparent fat digestibility of different fat sources for broiler chickens. Anim. Feed Sci. Tech., 186: 186–192.Search in Google Scholar

Timbermont L., Lanckriet A., Dewulf J., Nollet N., Schwarzer K., Haesebrouck F., Ducatelle R., Van Immerseel F. (2010). Control of Clostridium perfringens-induced necrotic enteritis in broilers by target-released butyric acid, fatty acids and essential oils. Avian Pathol., 39: 117–121.Search in Google Scholar

Weththasinghe P., Hansen J.Ø., Nøkland D., Lagos L., Rawski M., Øverland M. (2021). Full-Fat black soldier fly larvae (Hermetia illucens) meal and paste in extruded diets for Atlantic salmon (Salmo salar): effect on physical pellet quality, nutrient digestibility, nutrient utilization and growth performances. Aquaculture, 530: 735785.Search in Google Scholar

Xiang M.S.W., Tan J.K., Macia L. (2019). Fatty acids, gut bacteria, and immune cell function. Mol. Nutr. Fats, 151–164.Search in Google Scholar

Zeiger K., Popp J., Becker A., Hankel J., Visscher C., Klein G., Meemken D. (2017). Lauric acid as feed additive – an approach to reducing Campylobacter spp. in broiler meat. Plos One, 12(4): e0175693.Search in Google Scholar

Zeitz J.O., Fennhoff J., Kluge H., Stangl G.I., Eder K. (2015). Effects of dietary fats rich in lauric and myristic acid on performance, intestinal morphology, gut microbes, and meat quality in broilers. Poultry Sci., 94: 2404–2413.Search in Google Scholar

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