Open Access CAAS Agricultural Journals Czech Journal of Animal Science

Inclusion of Hermetia illucens larvae reared on fish offal to the diet of broiler quails: Effect on immunity and caecal microbial populations

Daniela Pasottoorcid , Liesel van Emmenes, Marco Cullere, Valerio Giaccone, Elsje Pieterse, Louwrens Christiaan Hoffman, Antonella Dalle Zotte

https://doi.org/10.17221/60/2020-CJASCitation:Pasotto D., van Emmenes L., Cullere M., Giaccone V., Pieterse E., Hoffman L.C., Dalle Zotte A. (2020): Inclusion of Hermetia illucens larvae reared on fish offal to the diet of broiler quails: Effect on immunity and caecal microbial populations. Czech J. Anim. Sci., 65: 213-223.
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Hermetia illucens (black soldier fly, BSF) larvae meal has shown to be a good protein source in monogastric animal diets, but published data regarding its immunomodulatory properties is limited. For this purpose, a study has been conducted to evaluate the effects of larvae meal on selected immune parameters and caecal bacterial counts of broiler quails. Hermetia illucens larvae were reared on two substrates (100% chicken feed, BSF-M, or 50% chicken feed + 50% fish offal, BSF-F) in order to manipulate the fatty acid profile of larvae meal by increasing the long-chain omega-3 (n-3) polyunsaturated fatty acids which are known for their immunomodulatory properties. For immunological purposes, a total of 60 birds were randomly allocated to three dietary treatment groups (n = 20/treatment): control quail diet (CON), or quail diets including 10% of BSF-F or BSF-M larvae meal. Blood was collected 27 and 37 days after the trial commenced to determine the humoral immune response, serum lysozyme concentrations, serum bactericidal activity and protein fractions of the serum. The dietary inclusion of BSF-M meal resulted in an increased secondary humoral immune response compared to the CON treatment group (P < 0.01). Quails in the BSF-F treatment had significantly higher serum lysozyme activity compared to quails in the CON and BSF-M treatment group. Both larvae meals significantly increased cell-mediated immunity on day 37 (P < 0.001) but they had no effect on serum bactericidal activity. Both larvae meal sources resulted in higher α2-globulin levels on both sampling days, whereas γ-globulin levels were significantly lower in quails with the BSF-F treatment on day 27. Dietary treatments had no significant effect on caecal bacterial counts. In conclusion, the present study showed that the larvae meal had immunostimulatory effects in quails, but the rearing substrate of larvae strongly influenced the immunostimulatory properties of the larvae meal.

Keywords:

insect meal; black soldier fly; humoral immunity; cellular immunity; lysozyme; bactericidal activity; serum protein

References:
Agazzi A, Cattaneo D, Dell’Orto V, Moroni P, Bonizzi L, Pasotto D, Bronzo V, Savoini G. Effect of administration of fish oil on aspects of cell-mediated immune response in periparturient dairy goats. Small Rumin Res. 2004 Oct;55(1-3):77-83.  https://doi.org/10.1016/j.smallrumres.2004.02.007
 
Ai H, Wang F, Zhang N, Zhang L, Lei C. Antiviral, immunomodulatory, and free radical scavenging activities of a protein-enriched fraction from the larvae of the housefly, Musca domestica. J Insect Sci. 2013 Jan;13(1):112-28.  https://doi.org/10.1673/031.013.11201
 
Baker PE, Fahey JV, Munck A. Prostaglandin inhibition of T-cell proliferation is mediated at two levels. Cell Immunol. 1981 Jun;61(1):52-61. https://doi.org/10.1016/0008-8749(81)90353-1
 
Borrelli L, Coretti L, Dipineto L, Bovera F, Menna F, Chiariotti L, Nizza A, Lembo F, Fioretti A. Insect-based diet, a promising nutritional source, modulates gut microbiota composition and SCFAs production in laying hens. Sci Rep. 2017 Nov;7(1):1-11. https://doi.org/10.1038/s41598-017-16560-6
 
Bort W. Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics. FASEB J. 1992 Jan;6(1):3345-53. https://doi.org/10.1096/fasebj.6.15.1281457
 
Bovera F, Piccolo G, Gasco L, Marono S, Loponte R, Vassalotti G, Mastellone V, Lombardi P, Attia YA, Nizza A. Yellow mealworm larvae (Tenebrio molitor, L.) as a possible alternative to soybean meal in broiler diets. Br Poult Sci. 2015 Oct;56(8):569-75. https://doi.org/10.1080/00071668.2015.1080815
 
Calder PC. Fatty acids and inflammation: The cutting edge between food and pharma. Eur J Pharmacol. 2011 Sep;68(1):50-8.  https://doi.org/10.1016/j.ejphar.2011.05.085
 
Calder PC. Immunomodulation by omega-3 fatty acids. Prostaglandins, Leukot Essent Fatty Acids. 2007 Nov-Dec;77(5-6):327-35.  https://doi.org/10.1016/j.plefa.2007.10.015
 
Corrier DE, DeLoach JR. Evaluation of cell-mediated, cutaneous basophil hypersensitivity in young chickens by an interdigital skin test. Poult Sci. 1990 Mar;69(3):403-8. https://doi.org/10.3382/ps.0690403
 
Cray C, Zaias J, Altman NH. Acute phase response in animals: A review. Comp Med. 2009 Dec;59(6):517-26.
 
Crespo R, Shivaprasad HL. Interpretation of laboratory results and values. In: Greenacre CB, Morishita TY, editors. Backyard poultry medicine and surgery: A guide for veterinary practitioners. USA: Wiley-Blackwell; 2014. p. 283-96.
 
Cullere M, Tasoniero G, Giaccone V, Miotti-Scapin R, Claeys E, De Smet S, Dalle Zotte A. Black soldier fly as dietary protein source for broiler quails: Apparent digestibility, excreta microbial load, feed choice, performance, carcass and meat traits. Animal. 2016 Dec;10(12):1923-30.  https://doi.org/10.1017/S1751731116001270
 
Cullere M, Woods MJ, van Emmenes L, Pieterse E, Hoffman LC, Dalle Zotte A. Hermetia illucens Larvae reared on different substrates in broiler quail diets: Effect on physicochemical and sensory quality of the quail meat. Animals. 2019 Aug 2;9(8):525.  https://doi.org/10.3390/ani9080525
 
Ebeid T, Fayoud A, Abou El-Soud S, Eid Y, El-Habbak M. The effect of omega-3 enriched meat production on lipid peroxidation, antioxidative status, immune response and tibia bone characteristics in Japanese quail. Czech J Anim Sci. 2011 Jul;56(7):314-24. https://doi.org/10.17221/1293-CJAS
 
Fritsche KL, Cassity NA, Huang SC. Effect of dietary fat source on antibody production and lymphocyte proliferation in chickens. Poult Sci. 1991 Mar;70(3):611-7. https://doi.org/10.3382/ps.0700611
 
Guo Y, Chen S, Xia Z, Yuan J. Effects of different types of polyunsaturated fatty acids on immune function and PGE2 synthesis by peripheral blood leukocytes of laying hens. Anim Feed Sci Technol. 2004 Oct;116(3-4):249-58. https://doi.org/10.1016/j.anifeedsci.2004.07.011
 
ISO − International Organisation for Standardisation. Animal feeding stuffs, animal products and faeces or urine. Determination of gross calorific value – bomb calorimetric method. ISO 9831. ISO, Geneva, Switzerland. 1998.
 
Khatibjoo A, Kermanshahi H, Golian A, Zaghari M. The effect of dietary n-6 : n-3 ratio and sex on broiler breeder immunity. Poult Sci. 2011 Oct;90(10):2209-16.  https://doi.org/10.3382/ps.2011-01373
 
Khempaka S, Chitsatchapong C, Molee W. Effect of chitin and protein constituents in shrimp head meal on growth performance, nutrient digestibility, intestinal microbial populations, volatile fatty acids, and ammonia production in broilers. J Appl Poult Res. 2011 Oct;20(1):1-11.  https://doi.org/10.3382/japr.2010-00162
 
Konieczka P, Barszcz M, Chmielewska N, Cie M, Szlis M, Smulikowska S. Interactive effects of dietary lipids and vitamin E level on performance, blood eicosanoids, and response to mitogen stimulation in broiler chickens of different ages. Poult Sci. 2017 Feb;96(2):359-69. https://doi.org/10.3382/ps/pew219
 
Korver D, Klasing K. Dietary fish oil alters specific and inflammatory immune responses in chicks. J Nutr. 1997 Oct;127(10):2039-46. https://doi.org/10.1093/jn/127.10.2039
 
Magor B. Evolution of effectors and receptors of innate immunity. Dev Comp Immunol. 2001 Oct;25(8-9):651-82. https://doi.org/10.1016/S0145-305X(01)00029-5
 
Makkar HPS, Tran G, Heuze V, Ankers P. State-of-the-art on use of insects as animal feed. Anim Feed Sci and Technol. 2014 Nov;197:1-33. https://doi.org/10.1016/j.anifeedsci.2014.07.008
 
Meylaers K, Clynen E, Daloze D, DeLoof A, Schoofs L. Identification of 1-lysophosphatidylethanolamine (C16:1) as an antimicrobial compound in the housefly, Musca domestica. Insect Biochem Mol Biol. 2004 Jan;34(1):43-9.  https://doi.org/10.1016/j.ibmb.2003.09.001
 
Riera Romo M, Perez-Martinez D, Castillo Ferrer C. Innate immunity in vertebrates: An overview. Immunology. 2016 Feb;148(2):125-39. https://doi.org/10.1111/imm.12597
 
SAS Institute. Statistical Analysis Software for Windows (SAS). Statistics version 9.1.3 ed. Cary, NC, USA: SAS Institute. 2008.
 
Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature. 2007 Jun;447:869-74.  https://doi.org/10.1038/nature05877
 
Spranghers T, Ottoboni M, Klootwijk C, Ovyn A, Deboosere S, De Meulenaer B, Michiels J, Eeckhout M, De Clercq P, De Smet S. Nutritional composition of black soldier fly (Hermetia illucens) prepupae reared on different organic waste substrates. J Sci Food Agric. 2017 Oct;97(8):2594-600. https://doi.org/10.1002/jsfa.8081
 
St-Hilaire S, Cranfill K, McGuire MA, Mosley EE, Tomberlin JK, Newton L, Sealey W, Sheppard C, Irving S. Fish offal recycling by the black soldier fly produces a foodstuff high in omega-3 fatty acids. J World Aquac Soc. 2007 May;38(2):309-13. https://doi.org/10.1111/j.1749-7345.2007.00101.x
 
Starkey PM, Barrett AJ. Evolution of α2-macroglobulin. The demonstration in a variety of vertebrate species of a protein resembling human α2-macroglobulin. Biochem J. 1982 Jul;205(1):91-5. https://doi.org/10.1042/bj2050091
 
Turchini GM, Nichols PD, Barrow C, Sinclair AJ. Jumping on the omega-3 bandwagon: Distinguishing the role of long-chain and short-chain omega-3 fatty acids. Crit Rev Food Sci Nutr. 2012 Jun;52(9):795-803.  https://doi.org/10.1080/10408398.2010.509553
 
Van Leuven F, Cassiman JJ, van den Berghe H. Uptake and degradation of α2-macroglobulin-protease complexes in human cells in culture. Exp Cell Res. 1978 Dec;117(2):273-82. https://doi.org/10.1016/0014-4827(78)90141-6
 
Woods M, Cullere M, van Emmenes L, Vincenzi S, Pieterse E, Hoffman LC, Dalle Zotte A. Hermetia illucens larvae reared on different substrates in broiler quail diets: Effect on apparent digestibility, feed-choice and growth performance. J Insects Food Feed. 2019 Apr;5(2):89-98. https://doi.org/10.3920/JIFF2018.0027
 
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