Effects of Microencapsulated Saccharomyces cerevisiae on Growth, Hematological Indices, Blood Chemical, and Immune Parameters and Intestinal Morphology in Striped Catfish, Pangasianodon hypophthalmus

  • Surintorn Boonanuntanasarn
  • Khanittha Ditthab
  • Araya Jangprai
  • Chatsirin Nakharuthai


This study investigated the effects of dietary probiotic Saccharomyces cerevisiae in the striped catfish, Pangasianodon hypophthalmus, which is an important aquaculture species. Freeze-dried microencapsulated probiotic S. cerevisiae with guar gum was performed and used for fish feed supplementation. Striped catfish were fed for 120 days with one of three experimental diets: basal diet (control), basal diet supplemented with 106-CFU S. cerevisiae g−1 diet (S. cerevisiae 106), and basal diet supplemented with 108-CFU S. cerevisiae g−1 diet (S. cerevisiae 108). The S. cerevisiae-supplemented diets significantly improved growth performance including growth rate and feed conversion ratio over 120 days of culture period (P < 0.05). The rate of survival was similar in all experimental groups. Supplementation with S. cerevisiae did not significantly affect whole body proximate composition (P > 0.05). In addition, probiotic S. cerevisiae had no effects on hematological indices and blood chemistry values (glucose, cholesterol, triglycerides, protein, albumin, blood urea nitrogen, chloride, calcium, magnesium, iron, and phosphorus) (P > 0.05). However, dietary S. cerevisiae led to increases in humoral immune parameters including total immunoglobulin, lysozyme, and alternative complement activities (P < 0.05). Dietary S. cerevisiae led to increase intestinal villus height in the anterior part of intestine (P < 0.05). Taken together, while the dietary S. cerevisiae had no detectable effects on hematological indices and several metabolic indicators, significant beneficial probiotic effects were observed on rates of growth, feed conversion ratio, and immune parameters.


Saccharomyces cerevisiae Striped catfish Pangasianodon hypophthalmus Probiotic Diet Hematology Immune Intestinal morphology 



Dr. Sirilux Chaijamrus is greatly thanked for the valuable advice of microencapsulation methodology. We thank Mr. Sunai Plymee (SUT Farm) for maintaining the fish throughout this work.

Funding Information

This study was supported by grants from the Suranaree University of Technology (SUT), the Office of the Higher Education Commission, the Higher Education Research Promotion and the National Research University Project of Thailand, and the National Research Council of Thailand (SUT3-303-59-24-18).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Approval

All animal manipulations were performed in accordance with the ethical principles and guideline for the use of animals (National Research Council of Thailand) and approved by the Suranaree University of Technology Laboratory Animal Use Monitoring Committee.


  1. 1.
    Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66:365–378CrossRefGoogle Scholar
  2. 2.
    Verschuere L, Rombaut G, Sorgeloos P, Verstraete W (2000) Probiotics bacteria as biological control agents in aquaculture. Microbiol Mol Biol Rev 64:655–671CrossRefGoogle Scholar
  3. 3.
    FAO/WHO (2016) Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria, Cordoba, ArgentinaGoogle Scholar
  4. 4.
    Salinas I, Cuesta, Alberto, Esteban MA, Meseguer J (2005) Dietary administration of Lactobacillus delbrueckii and Bacillus subtilis, single or combinated, on gilthead seabream cellular innate immune responses. Fish Shellfish Immunol 19:67–77Google Scholar
  5. 5.
    Balcazar JL, Rojas-Luna T, Cunningham DP (2007) Effect of the addition of four potential probiotic strains on the survival of Pacific white shrimp (Litopenaeus vannamei) following immersion challenge with Vibrio parahaemolyticus. J Invertebr Pathol 96:147–150CrossRefGoogle Scholar
  6. 6.
    Wongsasak U, Chaijamrus S, Kumkhong S, Boonanuntanasarn S (2015) Effects of dietary supplementation with β-glucan and synbiotics on immune gene expression and immune parameters under ammonia stress in Pacific white shrimp. Aquaculture 436:179–187CrossRefGoogle Scholar
  7. 7.
    Boonanuntanasarn S, Wongsasak U, Pitaksong T, Chaijamrus S (2016) Effects of dietary supplementation with β-glucan and synbiotics on growth, haemolymph chemistry, and intestinal microbiota and morphology in the Pacific white shrimp. Aquac Nutr 22:837–845CrossRefGoogle Scholar
  8. 8.
    Tovar-Ramírez D, Zambonino J, Cahu C, Gatesoupe FJ, Vázquez-Juárez R, Lésel R (2002) Effect of live yeast incorporation in compound diet on digestive enzyme activity in sea bass (Dicentrarchus labrax) larvae. Aquaculture 204:113–123CrossRefGoogle Scholar
  9. 9.
    Wang YB, Xu ZR (2006) Effect of probiotics for common carp (Cyprinus carpio) based on growth performance and digestive enzyme activities. Anim Feed Sci Tech 127:283–292CrossRefGoogle Scholar
  10. 10.
    Askarian F, kousha A, Salma W, Ringo E (2011) The effect of lactic acid bacteria administration on growth, digestive enzyme activity and gut microbiota in Persian sturgeon (acipenser persicus) and beluga (Huso huso) fry. Aquac Nutr 17:488–497CrossRefGoogle Scholar
  11. 11.
    Austin B, Baudet E, Stobie M (1992) Inhibition of bacterial fish pathogens by Tetraselmis suecica. J Fish Dis 15:55–61CrossRefGoogle Scholar
  12. 12.
    Barnes ME, Durben DJ, Reeves SG, Sanders R (2006) Dietary yeast culture supplementation improves initial rearing of Mc Conaughy strain rainbow trout. Aquac Nutr 12:388–394CrossRefGoogle Scholar
  13. 13.
    Reyes-Becerril M, Salinas I, Cuesta A, Meseguer J, Tovar-Ramirez D, Ascencio-Valle F, Esteban MA (2008) Oral delivery of live yeast Debaryomyces hansenii modulates the main innate immune parameters and the expression of immune-relevant genes in the gilthead seabream (Sparus aurata L.) Fish Shellfish Immunol 25:731–739CrossRefGoogle Scholar
  14. 14.
    Nayak SK (2011) Biology of Eukaryotic Probiotics. M.-T. Liong (ed.), Probiotics Microbiology Monographs 21, Springer, Verlag Berlin, HeidelbergGoogle Scholar
  15. 15.
    Gatesoupe FJ (2007) Live yeasts in the gut: natural occurrence, dietary introduction, and their effects on fish health and development. Aquaculture 267:20–30CrossRefGoogle Scholar
  16. 16.
    Blackburn AS, Avery SV (2003) Genome-wide screening of Saccharomyces cerevisiae to identify genes required for antibiotic insusceptibility of eukaryotes. Antimicrob Agents Chemother 47:676–681CrossRefGoogle Scholar
  17. 17.
    Verraes C, Boxstael SV, Meervenne EV, Coillie EV, Butaye P, Catry B, Schaetzen MA, Huffel XA, Imberechts H, Dierick K, Daube G, Saegerman C, Block JD, Dewulf J, Herman L (2013) Antimicrobial resistance in the food chain: a review. Int J Environ Res Public Health 10:2643–2669CrossRefGoogle Scholar
  18. 18.
    Kourelis A, Kotzamanidis C, Litopoulou-Tzanetaki E, Scouras ZG, Tzanetakis N, Yiangou M (2010) Preliminary probiotic selection of dairy and human yeast strains. J Biol Res 13:93–104Google Scholar
  19. 19.
    Taoka Y, Maeda H, Jo JY, Kim SM, Park S, Yoshikawa T, Sakata T (2006) Use of live and dead probiotic cells in tilapia Oreochromis niloticus. Fish Sci 72:755–766CrossRefGoogle Scholar
  20. 20.
    Waché Y, Auffray F, Gatesoupe FJ, Zambonino J, Gayet V, Labbé L, Quentel C (2006) Cross effects of the strain of dietary Saccharomyces cerevisiae and rearing conditions on the onset of intestinal microbiota and digestive enzymes in rainbow trout, Onchorhynchus mykiss, fry. Aquaculture 258:470–478CrossRefGoogle Scholar
  21. 21.
    Essa MA, Mabrouk HA, Mohamed RA, Michael FR (2011) Evaluating different additive levels of yeast, Saccharomyces cerevisiae, on the growth and production performances of a hybrid of two populations of Egyptian African catfish, Clarias gariepinus. Aquaculture 320:137–141CrossRefGoogle Scholar
  22. 22.
    FAO (1879) Cultured aquatic species information programme. January 1, 2018
  23. 23.
    Shori AB (2017) Microencapsulation improved probiotics survival during gastric transit. HAYATI J Biosci 24:1–5CrossRefGoogle Scholar
  24. 24.
    Cook MT, Tzortzis G, Charalampopoulos D, Khutoryanskiy VV (2012) Microencapsulation of probiotics for gastrointestinal delivery. J Control Release 162:56–67CrossRefGoogle Scholar
  25. 25.
    Ditthab K, Boonanuntanasarn S (2016) Microencapsulation of Saccharomyces cerevisiae and its effects on fish intestinal microbiota. In Proceedings of the First International Conference on Tropical Animal Science and Production (TASP 2016). July 26–29, 2016, Bangkok, ThailandGoogle Scholar
  26. 26.
    Brinker A, Reiter R (2011) Fish meal replacement by plant protein substitution and guar gum addition in trout feed. Part I: effects on feed utilization and fish quality. Aquaculture 310:350–360CrossRefGoogle Scholar
  27. 27.
    Leenhouwers JI, Adjei-boateng D, Verreth JAJ, Schrama JW (2006) Digesta viscosity, nutrient digestibility and organ weights in African catfish (Clarias gariepinus) fed diets supplemented with different levels of a soluble non-starch polysaccharide. Aquac Nutr 12:111–116CrossRefGoogle Scholar
  28. 28.
    AOAC (1990) Association of Official Analytical Chemists. Official methods of analysis of the Association of Official Analytical Chemists, Vol. 1, 14th edn. AOAC, Arlington, VA, USAGoogle Scholar
  29. 29.
    Voigt GJ (2000) Hematology techniques and concepts for veterinary technicians. Iowa State University Press, Ames, p 139Google Scholar
  30. 30.
    Trinder P (1969) Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann Clin Biochem 6:24–27CrossRefGoogle Scholar
  31. 31.
    Flegg HM (1973) An investigation of determination of serum cholesterol by an enzymatic method. Ann Clin Biochem 10:79–84CrossRefGoogle Scholar
  32. 32.
    Bucolo G, David H (1973) Quantitative determination of serum triglycerides by the use of enzymes. Clin Chem 19:476–482Google Scholar
  33. 33.
    Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–766Google Scholar
  34. 34.
    Doumas BT, Watson WA, Biggs HG (1971) Albumin standards and the measurement of serum albumin with bromcresol green. Clin Chim Acta 31:87–96CrossRefGoogle Scholar
  35. 35.
    Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974CrossRefGoogle Scholar
  36. 36.
    Hamilton RH (1966) A direct photometric method for chloride in biological fluids, employing mercuric thiocyanate and perchloric acid. Clin Chem 11:1–17Google Scholar
  37. 37.
    Moorehead WR, Biggs HG (1974) 2-Amino-2-methyl-1-propanol as the alkalizing agent in an improved continuous-flow cresolphthalein complexone procedure for calcium in serum. Clin Chem 20:1458–1460Google Scholar
  38. 38.
    Siwicki AK, Anderson DP, Rumsey GL (1994) Dietary intake of immunostimulants by rainbow trout affect non-specific immunity and protection against furunculosis. Vet Immunol Immunopathol 41:125–139CrossRefGoogle Scholar
  39. 39.
    Pitaksong T, Kupittayanant P, Boonanuntanasarn S (2013) The effects of vitamins C and E on the growth, tissue accumulation and prophylactic response to thermal and acidic stress of hybrid catfish. Aquac Nutr 19:148–162CrossRefGoogle Scholar
  40. 40.
    Boonanuntanasarn S, Khaomek P, Pitaksong T, Hua Y (2014) The effects of the supplementation of activated charcoal on the growth, health status and fillet composition-odor of Nile tilapia (Oreochromis niloticus) before harvesting. Aquacult Int 22:1417–1436CrossRefGoogle Scholar
  41. 41.
    Piccolo G, Bovera F, Lombardi P, Mastellone V, Nizza S, Meo CD, Marono S, Nizz A (2015) Effect of Lactobacillus plantarum on growth performance and hematological traits of European sea bass (Dicentrarchus labrax). Aquacult Int 23:1025–1032CrossRefGoogle Scholar
  42. 42.
    Abdel-Tawwab M, Abdel-Rahman AM, Ismael NEM (2008) Evaluation of commercial live bakers’ yeast, Saccharomyces cerevisiae as a growth and immunity promoter for fry Nile tilapia, Oreochromis niloticus (L.) challenged in situ with Aeromonas hydrophila. Aquaculture 280:185–189CrossRefGoogle Scholar
  43. 43.
    Chiu CH, Cheng CH, Gua WR, Guu YK, Cheng W (2010) Dietary administration of the probiotic, Saccharomyces cerevisiae P13, enhanced the growth, innate immune responses, and disease resistance of the grouper, Epinephelus coioides. Fish Shellfish Immunol 29:1053–1059CrossRefGoogle Scholar
  44. 44.
    Tovar-Ramirez D, Infante JZ, Cahu C, Gatesoupe FJ, Vázquez-Juárez R (2004) Influence of dietary live yeast on European sea bass (Dicentrarchus labrax) larval development. Aquaculture 234:415–427CrossRefGoogle Scholar
  45. 45.
    Tovar-Ramírez D, Mazurais D, Gatesoupe JF, Quazuguel P, Cahu CL, Zambonino-Infante JZ (2010) Dietary probiotic live yeast modulates antioxidant enzyme activities and gene expression of sea bass (Dicentrarchus labrax) larvae. Aquaculture 300:142–147CrossRefGoogle Scholar
  46. 46.
    Reyes-Becerril M, Tovar-Ramirez D, Ascencio-Valle F, Civera-Cerecedo R, Gracia-Lopez V, Barbosa-Solomieu V, Esteban MA (2011) Effects of dietary supplementation with probiotic live yeast Debaryomyces hansenii on the immune and antioxidant systems of leopard grouper Mycteroperca rosacea infected with Aeromonas hydrophila. Aquac Res 42:1676–1686CrossRefGoogle Scholar
  47. 47.
    Harikrishnan R, Kim MC, Kim JS, Balasundaram C, Heo MS (2011) Immunomodulatory effect of probiotics enriched diets on Uronema marinum infected olive. Fish Shellfish Immunol 30:964–971CrossRefGoogle Scholar
  48. 48.
    Lara-Flores M, Olvera-Novoa MA, Guzman-Mendez BE, Lopez-Madrid W (2003) Use of the bacteria Streptococcus faecium and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture 216:193–201CrossRefGoogle Scholar
  49. 49.
    Aubin J, Gatesoupe FJ, Labbe L, Lebrun L (2005) Trial of probiotics to prevent the vertebral column compression syndrome in rainbow trout (Oncorhynchus mykiss Walbaum). Aquac Res 36:758–767CrossRefGoogle Scholar
  50. 50.
    Dumas A, France J, Bureau D (2010) Modelling growth and body composition in fish nutrition: where have we been and where are we going? Aquac Res 41:161–181CrossRefGoogle Scholar
  51. 51.
    Smith MAK (1981) Estimation of growth potential by measurement of tissue protein synthetic rates in feeding and fasting rainbow trout, Salmo gairdnerii Richardson. J Fish Biol 19:213–220CrossRefGoogle Scholar
  52. 52.
    Reyes-Becerril M, Tovar-Ramírez D, Ascencio-Valle F, Civera-Cerecedo R, Gracia-López V, Barbosa-Solomieu V (2008) Effects of dietary live yeast Debaryomyces hansenii on the immune and antioxidant system in juvenile leopard grouper Mycteroperca rosacea exposed to stress. Aquaculture 280:39–44CrossRefGoogle Scholar
  53. 53.
    Scholz-Ahrens KE, Ade P, Marten B, Weber P, Timm W, Asil Y, Gluer CC, Schrezenmeir J (2007) Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content, and bone structure. J Nutr 137:838–846CrossRefGoogle Scholar
  54. 54.
    Dimitroglou A, Merrifield DL, Carnevali O, Picchietti S, Avella M, Daniels C, Güroy D, Davies SJ (2011) Microbial manipulations to improve fish health and production—a Mediterranean perspective. Fish Shellfish Immunol 30:1–16CrossRefGoogle Scholar
  55. 55.
    Martins FS, Silva AA, Vieira AT, Barbosa FHF, Arantes RME, Teixeira MM, Nicoli JR (2009) Comparative study of Bifidobacterium animalis, Escherichia coli, Lactobacillus casei and Saccharomyces boulardii probiotic properties. Arch Microbiol 191:623–630CrossRefGoogle Scholar
  56. 56.
    Li P, Gatlin DM (2003) Evaluation of brewers yeast (Saccharomyces cerevisiae) as a feed supplement for hybrid striped bass (Morone chrysops × M. saxatilis). Aquaculture 219:681–692CrossRefGoogle Scholar
  57. 57.
    He S, Zhou Z, Meng K, Zhao H, Yao B, Ringo E, Yoon I (2011) Effects of dietary antibiotic growth promoter and Saccharomyces cerevisiae fermentation product on production, intestinal bacterial community, and nonspecific immunity of hybrid tilapia (Oreochromis niloticus female × Oreochromis aureus male). J Animal Sci 89:84–92CrossRefGoogle Scholar
  58. 58.
    Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nature Rev Genet 7:349–359CrossRefGoogle Scholar
  59. 59.
    Tiengtam N, Khempaka S, Paengkoum P, Boonanuntanasarn S (2015) Effects of inulin and Jerusalem artichoke (Helianthus tuberosus) as prebiotic ingredients in the diet of juvenile Nile tilapia (Oreochromis niloticus). Anim Feed Sci Tech 207:120–129CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Animal Production Technology, Institute of Agricultural TechnologySuranaree University of TechnologyNakhon RatchasimaThailand

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