Prebiotics in aquaculture: a review

A prebiotic is a non-digestible food ingredient that beneficially affects the host by selectively stimulating the growth and/or the activity of one or a limited number of bacteria in the colon. Despite the potential benefits to health and performance as noted in various terrestrial animals, the use of prebiotics in the farming of fish and shellfish has been less investigated. The studies of prebiotics in fish and shellfish have investigated the following parameters: effect on growth, feed conversion, gut microbiota, cell damage/morphology, resistance against pathogenic bacteria and innate immune parameters such as alternative complement activity (ACH50), lysozyme activity, natural haemagglutination activity, respiratory burst, superoxide dismutase activity and phagocytic activity. This review discusses the results from these studies and the methods used. If the use of prebiotics leads to health responses becoming more clearly manifested in fish and shellfish, then prebiotics might have the potential to increase the efficiency and sustainability of aquaculture production. However, large gaps of knowledge exist. To fully conclude on the effects of adding prebiotics in fish diets, more research efforts are needed to provide the aquaculture industry, the scientific community, the regulatory bodies and the general public with the necessary information and tools.

[1]  Y. Chan,et al.  Xylooligosaccharides and fructooligosaccharides affect the intestinal microbiota and precancerous colonic lesion development in rats. , 2004, The Journal of nutrition.

[2]  T. Mayhew,et al.  The effect of dietary inulin on aerobic bacteria associated with hindgut of Arctic charr (Salvelinus alpinus L.) , 2006 .

[3]  M. Xia,et al.  Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. , 2003, Poultry science.

[4]  T. S. Manning,et al.  Microbial-gut interactions in health and disease. Prebiotics. , 2004, Best practice & research. Clinical gastroenterology.

[5]  J. Bøgwald,et al.  Beta-glucans as conductors of immune symphonies. , 2008, Fish & shellfish immunology.

[6]  P. Shi,et al.  The Effects of Dietary Yeast Culture or Short‐chain Fructo‐oligosaccharides on the Intestinal Autochthonous Bacterial Communities in Juvenile Hybrid Tilapia, Oreochromis niloticus♀×Oreochromis aureus♂ , 2009 .

[7]  S. Denev,et al.  Effect of a mannan oligosaccharide on the growth performance and immune status of rainbow trout (Oncorhynchus mykiss) , 2007, Aquaculture International.

[8]  P. Sorgeloos,et al.  A Review of the Functionality of Probiotics in the Larviculture Food Chain , 2007, Marine Biotechnology.

[9]  C. Ross,et al.  Effects of supplemental fat on growth performance and quality of beef from steers fed corn finishing diets. , 2007, Journal of animal science.

[10]  P. Iji,et al.  Effects of mannanoligosaccharide and fructooligosaccharide on the response of broilers to pathogenic Escherichia coli challenge , 2008, British poultry science.

[11]  Peng Li,et al.  Evaluation of the prebiotic GroBiotic®-A and brewers yeast as dietary supplements for sub-adult hybrid striped bass (Morone chrysops×M. saxatilis) challenged in situ with Mycobacterium marinum , 2005 .

[12]  M. Roberfroid,et al.  Experimental evidences on the potential of prebiotic fructans to reduce the risk of colon cancer , 2002, British Journal of Nutrition.

[13]  L. Morelli,et al.  FAO Technical meeting on prebiotics. , 2008, Journal of clinical gastroenterology.

[14]  W. Verstraete,et al.  Probiotic Bacteria as Biological Control Agents in Aquaculture , 2000, Microbiology and Molecular Biology Reviews.

[15]  F. Gatesoupe Updating the Importance of Lactic Acid Bacteria in Fish Farming: Natural Occurrence and Probiotic Treatments , 2007, Journal of Molecular Microbiology and Biotechnology.

[16]  L. Gram,et al.  Chapter 17 Prospects of fish probiotics , 2005 .

[17]  J. Parajó,et al.  Xylooligosaccharides: manufacture and applications , 2000 .

[18]  S. Yang,et al.  Novel products and new technologies for use of a familiar carbohydrate, milk lactose. , 1995, Journal of dairy science.

[19]  T. Mayhew,et al.  Histological changes in intestine of Atlantic salmon (Salmo salar L.) following in vitro exposure to pathogenic and probiotic bacterial strains , 2007, Cell and Tissue Research.

[20]  D. Day,et al.  Isomaltooligosaccharide increases cecal Bifidobacterium population in young broiler chickens. , 2005, Poultry science.

[21]  G. Schaafsma,et al.  Inulin: Fermentation and microbial ecology in the intestinal tract , 1999 .

[22]  A. Kesarcodi-Watson,et al.  Probiotics in aquaculture: The need, principles and mechanisms of action and screening processes , 2008 .

[23]  P. Iji,et al.  Intestinal structure and function of broiler chickens on diets supplemented with a mannan oligosaccharide , 2001 .

[24]  A. Voragen Technological aspects of functional food-related carbohydrates , 1998 .

[25]  R. D. Miles,et al.  Mannanoligosaccharides in Fish Nutrition: Effects of Dietary Supplementation on Growth and Gastrointestinal Villi Structure in Gulf of Mexico Sturgeon , 2003 .

[26]  R. Mosenthin,et al.  A Review of Interactions between Dietary Fiber and the Gastrointestinal Microbiota and Their Consequences on Intestinal Phosphorus Metabolism in Growing Pigs , 2008 .

[27]  J. Nicolas,et al.  Quelles stratégies alternatives aux antibiotiques en aquaculture , 2007 .

[28]  C. Parsons,et al.  The effects of several organic acids on growth performance, nutrient digestibilities, and cecal microbial populations in young chicks. , 2007, Poultry science.

[29]  A. Sapkota,et al.  Aquaculture practices and potential human health risks: current knowledge and future priorities. , 2008, Environment international.

[30]  G. Rumsey,et al.  Dietary intake of immunostimulants by rainbow trout affects non-specific immunity and protection against furunculosis. , 1994, Veterinary immunology and immunopathology.

[31]  Zhou Zhi-gang Effects of Dietary Short Chain Fructo Oligosaccharides on Intestinal Microflora,Mortality and Growth Performance of Oreochromis aureus ♂×O.niloticus♀ , 2007 .

[32]  C. Hauton,et al.  Immunostimulation in crustaceans: does it really protect against infection? , 2003, Fish & shellfish immunology.

[33]  J. Garssen,et al.  Immune-modulatory effects and potential working mechanisms of orally applied nondigestible carbohydrates. , 2007, Critical reviews in immunology.

[34]  C. Grieshop,et al.  Supplemental fructooligosaccharides and mannanoligosaccharides influence immune function, ileal and total tract nutrient digestibilities, microbial populations and concentrations of protein catabolites in the large bowel of dogs. , 2002, The Journal of nutrition.

[35]  T. Mayhew,et al.  Lactic acid bacteria vs. pathogens in the gastrointestinal tract of fish: a review , 2010 .

[36]  Peng Li,et al.  Evaluation of brewers yeast (Saccharomyces cerevisiae) as a feed supplement for hybrid striped bass (Morone chrysops×M. saxatilis) , 2003 .

[37]  D. Gatlin,et al.  The effects of dietary supplementation with mannanoligosaccharide, fructooligosaccharide or galactooligosaccharide on the growth and feed utilization of Atlantic salmon (Salmo salar) , 2008 .

[38]  B. Smedsrød,et al.  Mannose-receptor-mediated clearance of lysosomal alpha-mannosidase in scavenger endothelium of cod endocardium. , 2001, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[39]  T. Wiele,et al.  Dietary Inclusion of Wheat Bran Arabinoxylooligosaccharides Induces Beneficial Nutritional Effects in Chickens , 2008 .

[40]  T. Sako,et al.  Recent progress on research and applications of non-digestible galacto-oligosaccharides , 1999 .

[41]  Joanne L Slavin,et al.  Non-digestible oligosaccharides. , 2000 .

[42]  W. Walker,et al.  Nutritional impact of pre- and probiotics as protective gastrointestinal organisms. , 2002, Annual review of nutrition.

[43]  H. Yamada,et al.  Preparation of a new arabinoxylooligosaccharide from wheat bran hemicellulose and its structure. , 1994, Bioscience, biotechnology, and biochemistry.

[44]  J. Patterson,et al.  Application of prebiotics and probiotics in poultry production. , 2003, Poultry science.

[45]  J. Balcázar,et al.  A review on the interactions between gut microbiota and innate immunity of fish. , 2008, FEMS immunology and medical microbiology.

[46]  Guangyong Zhao,et al.  Effect of dietary isomaltooligosaccharides on nutrient digestibility and concentration of glucose, insulin, cholesterol and triglycerides in serum of growing pigs , 2009 .

[47]  E. McLean,et al.  Dietary mannan oligosaccharide enhances salinity tolerance and gut development of larval cobia , 2008 .

[48]  G. Gibson,et al.  Developing a quantitative approach for determining the in vitro prebiotic potential of dietary oligosaccharides. , 2004, FEMS microbiology letters.

[49]  Satoshi Koike,et al.  Molecular ecological analysis of the gastrointestinal microbiota: a review. , 2004, The Journal of nutrition.

[50]  A. Gernat,et al.  Effect of Dietary Mannan Oligosaccharide from Bio-Mos or SAF-Mannan on Live Performance of Broiler Chickens , 2008 .

[51]  T. Storebakken,et al.  Differing nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar) , 2000 .

[52]  H. Sørum Antimicrobial Drug Resistance in Fish Pathogens , 2019, Antimicrobial Resistance in Bacteria of Animal Origin.

[53]  S. Davies,et al.  Improving growth performance and health status of aquaculture stocks in Europe through the use of Bio-Mos®. , 2006 .

[54]  J. Meseguer,et al.  Oral administration of yeast, Saccharomyces cerevisiae, enhances the cellular innate immune response of gilthead seabream (Sparus aurata L.). , 2002, Veterinary immunology and immunopathology.

[55]  A. Easa,et al.  Benefits of probiotics: beyond gastrointestinal health. , 2009 .

[56]  B. Watzl,et al.  Inulin and oligofructose: review of experimental data on immune modulation. , 2007, The Journal of nutrition.

[57]  L. Martínez-Pomares,et al.  Influence of the mannose receptor in host immune responses. , 2009, Immunobiology.

[58]  D. Day,et al.  Efficacy of Leuconostoc mesenteroides (ATCC 13146) isomaltooligosaccharides as a poultry prebiotic. , 2004, Poultry science.

[59]  Solange I. Mussatto,et al.  Non-digestible oligosaccharides: A review , 2007 .

[60]  S. D. De Keersmaecker,et al.  Supporting Probiotic Action Genes and Molecules of Lactobacilli Genes and Molecules of Lactobacilli Supporting Probiotic Action Mechanisms of Health-promoting Effects of Lactobacilli: Probiotic Factors..747 , 2022 .

[61]  Zi-rong Xu,et al.  Effects of Dietary Fructooligosaccharide on Digestive Enzyme Activities, Intestinal Microflora and Morphology of Growing Pigs , 2002 .

[62]  F. Cabello [Antibiotics and aquaculture in Chile: implications for human and animal health]. , 2004, Revista medica de Chile.

[63]  R. Mackie,et al.  Continuous culture selection of bifidobacteria and lactobacilli from human faecal samples using fructooligosaccharide as selective substrate , 1998, Journal of applied microbiology.

[64]  M. Izquierdo,et al.  Immune stimulation and improved infection resistance in European sea bass (Dicentrarchus labrax) fed mannan oligosaccharides. , 2007, Fish & shellfish immunology.

[65]  T. Wiele,et al.  Microbial metabolism and prebiotic potency of arabinoxylan oligosaccharides in the human intestine , 2007 .

[66]  E. Yılmaz,et al.  Effects of dietary mannan oligosaccharides on growth, body composition, and intestine and liver histology of rainbow trout, Oncorhynchus mykiss , 2007 .

[67]  E. Yılmaz,et al.  Effects of Dietary Mannan Oligosaccharides (MOS) on Growth, Body Composition, and Intestine and Liver Histology of the Hybrid Tilapia (Oreoch romis niloticus x O. aureus) , 2007 .

[68]  Å. Krogdahl,et al.  Effects of dietary soyabean meal, inulin and oxytetracycline on intestinal microbiota and epithelial cell stress, apoptosis and proliferation in the teleost Atlantic salmon (Salmo salar L.). , 2007, The British journal of nutrition.

[69]  Baohua Xu,et al.  Effect of prebiotic xylooligosaccharides on growth performances and digestive enzyme activities of allogynogenetic crucian carp (Carassius auratus gibelio) , 2009, Fish Physiology and Biochemistry.

[70]  M. Verstegen,et al.  Fermentation in the large intestine of single-stomached animals and its relationship to animal health , 2001, Nutrition Research Reviews.

[71]  A. S. Diab,et al.  Effects of mannan-oligosaccharide on growth, survival and disease resistance of Nile tilapia (Oreochromis niloticus Linnaeus) fry. , 2008 .

[72]  W. Verstraete,et al.  The intestinal environment in health and disease - recent insights on the potential of intestinal bacteria to influence human health. , 2009, Current pharmaceutical design.

[73]  S Gordon,et al.  Macrophage lectins in host defence. , 2000, Microbes and infection.

[74]  Yoshirô Watanabe An ultrastructural study of intra cellular digestion of horseradish peroxidase by the rectal epithelium cells in larvae of a fresh water cottid fish cottus nozawae , 1984 .

[75]  G. Baeverfjord,et al.  Lactic acid fermentation eliminates indigestible carbohydrates and antinutritional factors in soybean meal for Atlantic salmon (Salmo salar) , 2005 .

[76]  K. Mai,et al.  Dietary probiotic Bacillus OJ and isomaltooligosaccharides influence the intestine microbial populations, immune responses and resistance to white spot syndrome virus in shrimp (Litopenaeus vannamei) , 2009 .

[77]  S. Ricke,et al.  Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture , 2005 .

[78]  H. Smidt,et al.  Influence of dietary components on development of the microbiota in single-stomached species , 2006, Nutrition Research Reviews.

[79]  F. Respondek,et al.  Effects of dietary short-chain fructooligosaccharides on the intestinal microflora of horses subjected to a sudden change in diet. , 2008, Journal of animal science.

[80]  T. Kaneko,et al.  Digestibility characteristics of isomaltooligosaccharides in comparison with several saccharides using the rat jejunum loop method. , 1995, Bioscience, biotechnology, and biochemistry.

[81]  C. Grieshop,et al.  Fructooligosaccharides and Lactobacillus acidophilus modify bowel function and protein catabolites excreted by healthy humans. , 2002, The Journal of nutrition.

[82]  R. Lochmann,et al.  Mortality Rates in Golden Shiners Fed High-Fat Diets with or without a Dairy-Yeast Prebiotic before Challenge with Flavobacterium columnare , 2007 .

[83]  Diego G. Silva,et al.  Inulin‐derived adjuvants efficiently promote both Th1 and Th2 immune responses , 2004, Immunology and cell biology.

[84]  J. Meseguer,et al.  Immunostimulant properties of a cell wall-modified whole Saccharomyces cerevisiae strain administered by diet to seabream (Sparus aurata L.). , 2003, Veterinary immunology and immunopathology.

[85]  L. Fortun-Lamothe,et al.  A review on the interactions between gut microflora and digestive mucosal immunity. Possible ways to improve the health of rabbits , 2007 .

[86]  P. Li,et al.  Dietary supplementation of short-chain fructooligosaccharides influences gastrointestinal microbiota composition and immunity characteristics of Pacific white shrimp, Litopenaeus vannamei, cultured in a recirculating system. , 2007, The Journal of nutrition.

[87]  Peng Li,et al.  Dietary brewers yeast and the prebiotic Grobiotic™AE influence growth performance, immune responses and resistance of hybrid striped bass (Morone chrysops×M. saxatilis) to Streptococcus iniae infection , 2004 .

[88]  J. Balcázar,et al.  The role of probiotics in aquaculture. , 2006, Veterinary microbiology.

[89]  Á. J. Bicudo,et al.  Feeding Dietary Mannan Oligosaccharides to Juvenile Nile Tilapia, Oreochromis niloticus, Has No Effect on Hematological Parameters and Showed Decreased Feed Consumption , 2008 .

[90]  W. H. Neill,et al.  Effects of prebiotics on nutrient digestibility of a soybean-meal-based diet by red drum Sciaenops ocellatus (Linnaeus) , 2008 .

[91]  E. Yılmaz,et al.  Effects of dietary mannan oligosaccharide on growth, body composition and hepatopancreas histology of Penaeus semisulcatus (de Haan 1844) , 2007 .

[92]  P. Klesius,et al.  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 , 2007 .

[93]  J. Meseguer,et al.  Effects of inulin on gilthead seabream (Sparus aurata L.) innate immune parameters. , 2008, Fish & shellfish immunology.

[94]  P. Iji,et al.  Dietary modulation of gut microflora in broiler chickens: a review of the role of six kinds of alternatives to in-feed antibiotics , 2009 .

[95]  J. D. Kim,et al.  The role of immunostimulants in monogastric animal and fish - review. , 2000 .

[96]  G. Gibson Dietary modulation of the human gut microflora using prebiotics , 1998, British Journal of Nutrition.

[97]  G. Reid Probiotics and prebiotics - Progress and challenges , 2008 .

[98]  R. Lochmann,et al.  Preliminary Observations of Mortality Reduction in Stressed, Flavobacterium columnare–Challenged Golden Shiners after Treatment with a Dairy-Yeast Prebiotic , 2008 .

[99]  J. Meseguer,et al.  In vitro studies of Lactobacillus delbrueckii subsp. lactis in Atlantic salmon (Salmo salar L.) foregut: tissue responses and evidence of protection against Aeromonas salmonicida subsp. salmonicida epithelial damage. , 2008, Veterinary microbiology.

[100]  F. Gatesoupe,et al.  Lactic acid bacteria in fish: a review , 1998 .

[101]  D. Burkitt,et al.  Effect of dietary fibre on stools and the transit-times, and its role in the causation of disease. , 1972, Lancet.

[102]  F. Ollevier,et al.  Effect of dietary inulin and oligosaccharides as prebiotics for weaning turbot, Psetta maxima (Linnaeus, C. 1758) , 2006, Aquaculture International.

[103]  K. Clements,et al.  Fermentation in Tropical Marine Herbivorous Fishes , 1995, Physiological Zoology.

[104]  F. Gatesoupe The use of probiotics in aquaculture , 1999 .

[105]  T. Klaenhammer,et al.  Genomics of lactic acid bacteria. , 2009, FEMS microbiology letters.

[106]  Å. Krogdahl,et al.  Capacity for digestive hydrolysis and amino acid absorption in Atlantic salmon (Salmo salar) fed diets with soybean meal or inulin with or without addition of antibiotics , 2006 .

[107]  S. Salminen,et al.  Opportunities for improving the health and nutrition of the human infant by probiotics. , 2008, Nestle Nutrition workshop series. Paediatric programme.

[108]  J. Delcour,et al.  Large‐scale production and characterisation of wheat bran arabinoxylooligosaccharides , 2006 .

[109]  D. Li,et al.  Effects of isomalto-oligosaccharides on broiler performance and intestinal microflora. , 2003, Poultry science.

[110]  Najamuddin,et al.  Gastrointestinal delivery of peptide and protein drugs to aquacultured teleosts , 1999 .

[111]  A. Farzanfar The use of probiotics in shrimp aquaculture. , 2006, FEMS immunology and medical microbiology.

[112]  D. H. Wang,et al.  Enhancement of the resistance of tilapia and grass carp to experimental Aeromonas hydrophila and Edwardsiella tarda infections by several polysaccharides. , 1997, Comparative immunology, microbiology and infectious diseases.

[113]  K. B. Bach Knudsen,et al.  New insight into butyrate metabolism , 2003, Proceedings of the Nutrition Society.

[114]  T. Mayhew,et al.  Damaging effect of dietary inulin on intestinal enterocytes in Arctic charr (Salvelinus alpinus L.) , 2001 .

[115]  T. Mayhew,et al.  Bacterial translocation and pathogenesis in the digestive tract of larvae and fry , 2007 .

[116]  Yanbo Wang,et al.  Probiotics in aquaculture: Challenges and outlook , 2008 .

[117]  T. Mayhew,et al.  Damaging effect of the fish pathogen Aeromonas salmonicida ssp. salmonicida on intestinal enterocytes of Atlantic salmon (Salmo salar L.) , 2004, Cell and Tissue Research.

[118]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[119]  Zong Dai,et al.  A Novel C-Type Lectin from the Shrimp Litopenaeus vannamei Possesses Anti-White Spot Syndrome Virus Activity , 2008, Journal of Virology.

[120]  E. Ringø,et al.  Chapter 10 Pathogenesis and the gastrointestinal tract of growing fish , 2005, Biology of Growing Animals.

[121]  J. L. Greger Nondigestible carbohydrates and mineral bioavailability. , 1999, The Journal of nutrition.

[122]  B. Austin,et al.  Probiotics in aquaculture , 2002 .

[123]  R. Crittenden,et al.  Production, properties and applications of food-grade oligosaccharides , 1996 .

[124]  Zhigang Zhou,et al.  Effects of Dietary Short‐chain Fructooligosaccharides on Intestinal Microflora, Survival, and Growth Performance of Juvenile White Shrimp, Litopenaeus vannamei , 2007 .

[125]  M. Roberfroid,et al.  Dietary fiber, inulin, and oligofructose: a review comparing their physiological effects. , 1993, Critical reviews in food science and nutrition.

[126]  G R Gibson,et al.  Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. , 1995, The Journal of nutrition.