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Use of food waste as fish feeds: effects of prebiotic fibers (inulin and mannanoligosaccharide) on growth and non-specific immunity of grass carp (Ctenopharyngodon idella)

Environmental Science and Pollution Research volume 22, pages 17663–17671 (2015)Cite this article

Abstract

The effects of inulin and mannanoligosaccharide (MOS) on the growth performance and non-specific immunity of grass carp were studied. Two doses of prebiotic fiber with 0.2 or 2 % of the fibers are being mixed into fish feed pellets. Fish growth as well as selected non-specific immune parameters of grass carp were tested in a feeding trial, which lasted for 8 weeks. Fish was fed at 2.5 % body mass per day. INU02, INU2, and MOS2 significantly improved relative weight gain, specific growth rate, protein efficiency ratio, and food conversion ratio of grass carp fed with food waste-based diet. In terms of non-specific immune response, grass carp showed significant improvement in all three tested parameters (total serum immunoglobin, bactericidal activity, and anti-protease activity). Adding 2 % of inulin (INU2) into food waste diets seemed to be more preferable than other supplemented experimental diets (INU02, MOS02, MOS2), as it could promote growth of grass carp as well as improving the non-specific immune systems of grass carp.

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References

  • Abidov AA, Mirismailov MI (1979) In: Tretyakova NM (ed) Influence of vaccination on some factors of natural resistance. Medizina, Tashkent

  • Anderson DP, Siwicki AK (1995) Basic haematology and serology for fish health programmes. In: Shariff M, Arthur JR, Subasinghe RP (eds) Disease in Asian aquaculture. Manila, Philippines

    Google Scholar 

  • AOAC (2002) Official methods of analysis of AOAC international, 17th edn. 1st revision, Gaithersburg

    Google Scholar 

  • Apostolopoulos V, McKenzie IF (2001) Role of the mannose receptor in the immune response. Curr Mol Med 1:469–74

    Article  CAS  Google Scholar 

  • Attia YA, Al-Hamid AA, Ibrahim MS, Al-Harthi MA, Bovera F, Elnaggar AS (2014) Productive performance, biochemical and hematological traits of broiler chickens supplemented with propolis, bee pollen, and mannan oligosaccharides continuously or intermittently. Livest Sci 164:87–95

    Article  Google Scholar 

  • Attia YA, Hamed RS, El-Hamid AA, Shahba HA, Bovera F (2015a) Effect of inulin and mannanoligosaccharides in comparison to zinc-bacitracin on growing performance, nutrient digestibility and hematological profiles of growing rabbits. Anim Product Sci 55:80–86

    Article  CAS  Google Scholar 

  • Attia YA, Hamed RS, El-Hamid AE, Al-Harthi MA, Shahba HA, Bovera F (2015b) Performance, blood profile, carcass and meat traits and tissue morphology in growing rabbits fed mannanoligosaccharides and zinc-bacitracin continuously or intermittently. Anim Sci Paper Rep 33(1):85–101

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Burr G, Hume M, Ricke S, Nisbet D, Gatlin D III (2010) In vitro and in vivo evaluation of the prebiotics GroBiotic®-A, inulin, mannanoligosaccharide, and galactooligosaccharide on the digestive microbiota and performance of hybrid striped bass (Morone chrysops × Morone saxatilis). Microb Ecol 59:187–198

    Article  CAS  Google Scholar 

  • Casali P, Schettino EM (1996) Structure and function of natural antibodies. Curr Top Microbiol Immunol 210:167–179

    CAS  Google Scholar 

  • Causey JL, Slain JL, Tangled BC, Meyer PD (1998) Stimulation of human immune system by inulin in vitro. Proceeding of Danone Conference on Probiotics and Immunity, Bonn, Germany

  • Cerezuela R, Cuesta A, Meseguer J, Ángeles EM (2008) Effects of inulin on gilthead seabream (Sparus aurata L.) innate immune parameters. Fish Shellfish Immunol 24:663–668

    Article  CAS  Google Scholar 

  • CFS (2006a) Malachite green and nitrofurans residues found in turbot imported from the mainland. Center for Food Safety, Food and Environmental Hygiene Department, Hong Kong, Food alert for 2006

    Google Scholar 

  • CFS (2006b) Eel products with malachite green seized. Center for Food Safety, Food and Environmental Hygiene Department, Hong Kong, Press release

    Google Scholar 

  • CFS (2006c) Malachite green and nitrofurans residues found in freshwater fish imported from the mainland. Center for Food Safety, Food and Environmental Hygiene Department, Hong Kong, Food alert for 2006

    Google Scholar 

  • Che TM (2010) Effects of mannan oligosaccharide on immune function and disease resistance in pigs. Dissertation, University of Illinois at Urbana-Champaign

  • Cheng Z, Mo WY, Man YB, Lam CL, Choi WM, Nie XP, Liu YH, Wong MH (2014a) Environmental mercury concentrations in cultured low-trophic-level fish using food waste-based diets. Environ Sci Pollut Res. doi:10.1007/s11356-014-3333-6

    Google Scholar 

  • Cheng Z, Mo WY, Man YB, Nie XP, Li KB, Wong MH (2014b) Replacing fish meal by food waste in feed pellets to culture lower trophic level fish containing acceptable levels of organochlorine pesticides: health risk assessments. Environ Int 73:22–27

    Article  CAS  Google Scholar 

  • Das BK, Pradhan J, Sahu S (2009) The effect of Euglena viridis on immune response of rohu, Labeo rohita (Ham.). Fish Shellfish Immunol 26:871–876

    Article  CAS  Google Scholar 

  • Dimitroglou A, Merrifield DL, Moate R, Davies SJ, Spring P, Sweetman J, Bradley G (2009) Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum). J Anim Sci 87:3226–3234

    Article  CAS  Google Scholar 

  • Ferrara E, Gustinelli A, Fioravanti ML, Restucci B, Quaglio F, Marono S, Piccolo G (2015) Histological and micro/macro morphological evaluation of intestine in sharpsnout sea bream (Diplodus puntazzo) fed soybean meal based diets added with MOS and inulin as prebiotics. Aquacult Int. doi:10.1007/s10499-015-9902-y

    Google Scholar 

  • Furukawa A, Tsukahara H (1996) On the acid digestion method for the determination of chromic oxide as an index substance in the study of digestibility of fish feed. Bull Jpn Soc Sci Fish 32:502–506

    Article  Google Scholar 

  • Gonzalez R, Matsiota P, Torchy C, De Kinkelin P, Avrameas S (1989) Natural anti-TNP antibodies from rainbow trout interfere with viral infection in vitro. Immunol Res 140:675–684

    Article  CAS  Google Scholar 

  • Grisdale-Helland B, Helland SJ, Gatlin DM III (2008) The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar). Aquaculture 283:163–167

    Article  CAS  Google Scholar 

  • He S, Xu G, Wu Y, Weng H, Xie H (2003) Effects of IMO and FOS on the growth performance and non-specific immunity in hybrid tilapia. Chinese Feed 23:14–15 [In Chinese]

    Google Scholar 

  • Hjelmeland K (1983) Proteinase inhibitors in the muscle and serum of cod (Gadus morhua). Isolation and characterization. Comp Biochem Physiol B: Comp Biochem 76:365–372

    Google Scholar 

  • HKEPD (2014) Problems & solutions: food waste challenge. http://www.epd.gov.hk/epd/english/environmentinhk/waste/prob_solutions/food_waste_challenge.html. Assessed 22 December 2014

  • Holland MCH, Lambris JD (2002) The complement system in teleosts. Fish Shellfish Immunol 12:399–420

    Article  CAS  Google Scholar 

  • Ibrahem MD, Fathi M, Mesalhy S, Abd El-Aty AD (2010) Effect of dietary supplementation of inulin and vitamin C on the growth, hematology, innate immunity, and resistance of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 29:41–246

    Article  CAS  Google Scholar 

  • Kaleeswaran B, Ilavenil S, Ravikumar S (2011) Growth response, feed conversion ratio and antiprotease activity of Cynodon dactylon (L.) mixed diet in Catla catla (Ham.). J Anim Vet Adv 10:511–517

    Article  CAS  Google Scholar 

  • Kolman H (2001) The humoral effects of epin in Siberian sturgeon (Acipenser baeri Brandt). Archives Polish Fish 9:61–69

    Google Scholar 

  • Mahious AS, Gatesoupe FJ, Hervi M, Metailler R, Ollevier F (2006) Effect of dietary inulin and oligosaccharides as prebiotics for weaning turbot, Psetta maxima (Linnaeus, C. 1758). Aquacult Int 14:219–229

    Article  CAS  Google Scholar 

  • Meyer D (2008) Prebiotic dietary fibres and the immune system. Agro Food Industry 19:12–15

    CAS  Google Scholar 

  • Mo WY, Cheng Z, Choi WM, Man YB, Liu Y, Wong MH (2014) Application of food waste based diets in polyculture of low trophic level fish: effects on fish growth, water quality and plankton density. Marine Poll Bull 85:803–809

    Article  CAS  Google Scholar 

  • Ortiz LT, Rebolé A, Velasco S, Rodríguez ML, Treviño J, Tejedor JL, Alzueta C (2013) Effects of inulin and fructooligosaccharides on growth performance, body chemical composition and intestinal microbiota of farmed rainbow trout (Oncorhynchus mykiss). Aquacult Nutr 19:475–482

    Article  CAS  Google Scholar 

  • Piccolo G, Centoducati G, Marono S, Bovera F, Tudisco R, Nizza A (2011) Effects of the partial substitution of fish meal by soy bean meal with or without mannanoligosaccharide and fructooligosaccharide on the growth and feed utilization of sharpsnout seabream, Diplodus puntazzo (Cetti, 1777): preliminary results. Italian J Animal Sci 10:195–199

    Article  CAS  Google Scholar 

  • Piccolo G, Centoducati G, Bovera F, Marrone R, Nizza A (2013) Effects of mannan oligosaccharide and inulin on sharpsnout seabream (Diplodus puntazzo) in the context of partial fish meal substitution by soybean meal. Italian J Animal Sci 12:133–138

    Article  CAS  Google Scholar 

  • Rao YV, Chakrabarti R (2004) Enhanced antiproteases in Labeo rohita fed with diet containing herbal ingredients. Indian J Clin Biochem 19:132–134

    Article  Google Scholar 

  • Reza A, Abdolmajid H, Abbas M, Abdolmohammad AK (2009) Effect of dietary prebiotic inulin on growth performance, intestinal microflora, body composition and hematological parameters of juvenile beluga, Huso huso (Linnaeus, 1758). J World Aquacult Soc 40:771–779

    Article  Google Scholar 

  • Ringø E, Olsen RE, Gifstad TØ, Dalmo RA, Amlund H, HEMRE GI, Bakke AM (2010) Prebiotics in aquaculture: a review. Aquacult Nutr 16:117–136

    Article  CAS  Google Scholar 

  • Sahu S, Das BK, Mishra BK, Pradhan J, Sarangi N (2007) Effect of Allium sativum on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. J Appl Ichthyol 23:80–86

    Article  CAS  Google Scholar 

  • Samrongpan C, Areechon N, Yoonpundh R, Sirsapoome P (2008) Effects of mannan oligosaccharide on growth survival and disease resistance of Nile tilapia (Oreochromis niloticus linnaeus) fry. In 8th International Symposium on Tilapia in Aquaculture (pp. 345–353)

  • Sapkota A, Sapkota AR, Kucharski M, Burke J, McKenzie S, Polly Walker P, Robert Lawrence R (2008) Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int 34:1215–1226

    Article  Google Scholar 

  • Seifert S, Watzl B (2007) Inulin and oligofructose: review of experimental data on immune modulation. J Nutr 137:2563S–2567S

    CAS  Google Scholar 

  • Sharma A, Deo AD, Riteshkumar ST, Chanu TI, Das A (2010) Effect of Withania somnifera (L. Dunal) root as a feed additive on immunological parameters and disease resistance to Aeromonas hydrophila in Labeo rohita (Hamilton) fingerlings. Fish Shellfish Immunol 29:508–512

    Article  CAS  Google Scholar 

  • Silva DG, Cooper PD, Petrovsky N (2004) Inulin-derived adjuvant efficiently promote both Th1 and Th2 immune responses. Immunol Cell Biol 82:611–616

    Article  CAS  Google Scholar 

  • Sinyakov MS, Dror M, Zhevelev HM, Margel S, Avtalion RR (2002) Natural antibodies and their significance in active immunization and protection against a defined pathogen in fish. Vaccine 20:3668–3674

    Article  CAS  Google Scholar 

  • Sivaram V, Babu MM, Immanul G, Murugadass S, Citarasu T, Petermarian M (2004) Growth and immunoresponse of juvenile greasy groupers (Epinephelus tauvina) fed with herbal antibacterial active principle supplemented diets against Vibrio harveyi infections. Aquaculture 237:9–20

    Article  Google Scholar 

  • Sohn KS, Kim MK, Kim JD, Han IK (2000) The role immunostimulants in monogastric animal and fish—review. Asian Australas J Anim Sci 13:1178–1187

    Article  CAS  Google Scholar 

  • Sørensen KK, Tollersrud OK, Evjen G, Smedsrod B (2001) Mannose-receptor-mediated clearance of lysosomal a-mannosidase in scavenger endothelium of cod endocardium. Comp Biochem Physiol A Mol Integr Physiol 129:615–630

    Article  Google Scholar 

  • Sørum H (2006) Antimicrobial drug resistance in fish pathogens. In: Aarestrup FM (ed) Antimicrobial resistance in bacteria of animal origin. ASM Press, Washington

    Google Scholar 

  • Spring P, Wenk C, Dawson KA, Newman KE (2000) The effects of dietary mannan oligosaccharides on cecal parameters and the concentrations of enteric bacteria in the cecae of Salmonella-challenged broiler chicks. Poult Sci 79:205–211

    Article  CAS  Google Scholar 

  • Staykov Y, Spring P, Denev S, Sweetman J (2007) Effect of a mannan oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss). Aquacult Int 15:153–161

    Article  CAS  Google Scholar 

  • Torrecillas S, Makol A, Caballero MJ, Montero D, Robaina L, Real F, Sweetman J (2007) Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol 23:969–981

    Article  CAS  Google Scholar 

  • USAID-HARVEST (2011) Feed conversion ratio—technical bulletin #07. http://www.fintrac.com/cpanelx_pu/cambodia/15_21_9947_13_04_4043_Technical%20Bulletin%207%20-%20Feed%20Conversion%20Ratio%20(English).pdf. Assessed 29 May 2014

  • Wang WS, Wang DH (1997) Enhancement of the resistance of tilapia and grass carp to experimental Aeromonas hydrophila and Edwardsiella tarda infections by several polysaccharides. Comp Immunol Microb 20:261–270

    Article  CAS  Google Scholar 

  • Welker TL, Lim C, Yildirim-Aksoy M, Shelby R, Klesius PH (2007) Immune response and resistance to stress and Edwardsiella ictaluri challenge in channel catfish, Ictalurus punctatus, fed diets containing commercial whole-cell yeast or yeast subcomponents. J World Aquacult Soc 38:24–35

    Article  Google Scholar 

  • Whyte SK (2007) The innate immune response of finfish: a review of current knowledge. Fish Shellfish Immunol 23:1127–1151

    Article  CAS  Google Scholar 

  • Yilmaz E, Genc MA, Genc E (2007) Effects of dietary mannan oligosaccharides on growth, body composition, and intestine and liver histology of rainbow trout, Oncorhynchus mykiss. Isr J Aquacult-Bamid 59:182–188

    Google Scholar 

  • Zhao ZY, Yin ZX, Xu XP et al (2009) A novel C-type lectin from the shrimp Litopenaeus vannamei possesses anti-white spot syndrome virus activity. J Virol 83:347–356

    Article  CAS  Google Scholar 

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Acknowledgments

Financial support from Environment and Conservation Fund (37/2009) of the Hong Kong SAR Government is gratefully acknowledged.

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Affiliations

  1. Consortium on Health, Environment, Education and Research (CHEER) and Department of Science and Environmental Studies, The Hong Kong Institute of Education, Tai Po, Hong Kong, China

    Wing Y. Mo, Wai M. Choi & Ming H. Wong

  2. Croucher Institute for Environmental Sciences and Department of Biology, Hong Kong Baptist University, Hong Kong, China

    Wing Y. Mo, Wai M. Choi, Yu B. Man & Ming H. Wong

  3. College of Resources and Environment, Sichuan Agricultural University, Chengdu, China

    Zhang Cheng

  4. Environmental Science Programs, School of Science, The Hong Kong University of Science and Technology, Hong Kong, China

    Clare H. I. Lun

  5. Department of Civil and Environmental Engineering, The Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, SAR, China

    James T. F. Wong & Xun W. Chen

  6. Division of Life Science, The Hong Kong University of Science and Technology, Hong Kong, China

    Stanley C. K. Lau

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  1. Wing Y. Mo
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  2. Zhang Cheng
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Correspondence to Ming H. Wong.

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Mo, W.Y., Cheng, Z., Choi, W.M. et al. Use of food waste as fish feeds: effects of prebiotic fibers (inulin and mannanoligosaccharide) on growth and non-specific immunity of grass carp (Ctenopharyngodon idella). Environ Sci Pollut Res 22, 17663–17671 (2015). https://doi.org/10.1007/s11356-015-4971-z

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Keywords

  • Diet digestibility
  • Feed conversion ratio
  • Food waste
  • Grass carp
  • Prebiotic fibers
  • Non-specific immunity