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Growth performance, immune-physiological variables and disease resistance of common carp (Cyprinus carpio) orally subjected to different concentrations of Lactobacillus plantarum

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Abstract

Nowadays, probiotics are among the most attractive food supplements for promoting animal’s growth and health condition with the aim of increasing production and lowering losses. Four hundred and eighty fish weighing 31.8 ± 2.6 g were randomly divided into four groups each in triplicates. Groups 1 to 3 were fed with commercial carp feed containing 0.7, 0.5, and 0.3 g (1.2 × 106, 0.9 × 106, and 0.56 × 106 cfu/g feed) probiotic Lactobacillus plantarum per kilogram feed for 80 days at 26 ± 1 °C, respectively. Group 4 received normal feed and was considered as control 1. Growth factors and some immunophysiological parameters were assessed on days 0, 20, 40, 60, and 80 of the trail. An overall increase in growth factors of probiotic-treated groups was seen, and final weight and condition factor of groups 1 and 2 were higher than control group (p ≤ 0.05). The highest specific growth rate and best feed conversion ratio were obtained in group 1. Red blood cell (RBC) count, hematocrit, and hemoglobin in probiotic groups were higher than control 1, but differences were significant for group 1 (p ≤ 0.05). White blood cell (WBC) count significantly increased in groups 1 and 2 compared to other groups (p < 0.05). Respiratory burst activity significantly increased in all probiotic fed groups with the highest level recorded in group 1 (p ≤ 0.05). Complement and lysozyme activities were significantly higher in group 1 followed by group 2 than both group 3 and control 1 (p ≤ 0.05). Also, serum bactericidal activity was significantly higher in group 1 than other groups (p ≤ 0.05). Serum total protein and immunoglobulin were higher in probiotic groups than control 1. No significant changes were seen in serum level of aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (ALP), and lactate dehydrogenase (LDH) among all groups. After challenging fish with virulent strain of Aeromonas hydrophila, the lowest mortality was obtained in groups 1 and 2, respectively (p ≤ 0.05). These data clearly show that application of probiotic L. plantarum in carp feed can not only improve the growth variables and immunophysiological responses of fish but also increase the fish disease resistance to motile Aeromonas septicemia caused by Aeromonas hydrophila. However, these positive improvements are dose dependent.

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References

  • Abd El-Rhman AM, Khattab YA, Shalaby AM (2009) Micrococcus Luteus and Pseudomonas species as probiotics for promoting the growth performance and health of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 27(2):175–180

    Article  PubMed  Google Scholar 

  • Aderfemo OK (2007) Haematological profile of Clarias gariepinus (Burchell, 1822) exposed to lead. Turkish J Fish Aquat Sci 7:163–169

    Google Scholar 

  • Al-Dohail MA, Hashim R, Aliyu-Paiko M (2009) Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African catfish (Clarias gariepinus, Burchell 1822) fingerling. Aquac Res 40:1642–1652

    Article  Google Scholar 

  • Aly SM, Abdel-Galil Ahmed Y, Abdel-Aziz Ghareeb A, Mohamed MF (2008) Studies on Bacillus subtilis and Lactobacillus acidophilus, as potential probiotics, on the immune response and resistance of Tilapia nilotica (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 25(1):128–136

    Article  CAS  PubMed  Google Scholar 

  • Andani HRR, Tukmechi A, Meshkini S, Sheikhzadeh N (2012) Antagonistic activity of two potential probiotic bacteria from fish intestines and investigation of their effects on growth performance and immune response in rainbow trout (Oncorhynchus mykiss). J Appl Ichthyol 28(5):728–734

    Article  Google Scholar 

  • Anderson DP, Siwicki AK (1994) Duration of protection against Aeromonas salmonicida in brook trout immunostimulated with glucan or chitosan by injection and immersion. Prog Fish Cult 56:258–261

    Article  Google Scholar 

  • Austin B, Austin DA (2012) Bacterial fish pathogens: disease of farmed and wild fish. Springer, Dordrecht

    Book  Google Scholar 

  • Azza MM (2009) Antagonism of Aeromonas hydrophila by propolis and its effect on the performance of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 27(3):454–459

    Article  Google Scholar 

  • Balcázar JL, Id B, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114:173–186

    Article  PubMed  Google Scholar 

  • Balcázar JL, Vendrell D, de Blas I, Ruiz-Zarzuela I, Muzquiz JL, Girones O (2008) Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture 278:188–191

    Article  Google Scholar 

  • Berk P, Korenblat K (2016) Approach to the patient with jaundice or abnormal liver tests. In: Goldman L, Schafer AI (eds) Goldman-Cecil Medicine, 25th edn. Elsevier Saunders, Philadelphia chapter 147

    Google Scholar 

  • Brata O (1993) Veterinary clinical immunology laboratory, vol Vol 2. Bar- Lab Inc, Blacksburg, pp 24–25 Section 3

    Google Scholar 

  • Cerezuela R, Guardiola FA, Meseguer J, Esteban M (2012) Increases in immune parameters by inulin and Bacillus subtilis dietary administration to gilthead seabream (Sparus aurata L.) did not correlate with disease resistance to Photobacterium damselae. Fish Shellfish Immunol 32(6):1032–1040

    Article  CAS  PubMed  Google Scholar 

  • Chi C, Jiang B, Yu XB, Liu TQ, Xia L, Wang GX (2014) Effects of three strains of intestinal autochthonous bacteria and their extracellular products on the immune response and disease resistance of common carp, Cyprinus carpio. Fish Shellfish Immunol 36(1):9–18

    Article  CAS  PubMed  Google Scholar 

  • Corona-Hernandez RI, Álvarez-Parrilla E, Lizardi-Mendoza J, Islas-Rubio AR, Rosa L, Wall-Medrano A (2013) Structural stability and viability of microencapsulated probiotic bacteria: a review. Compr Rev Food Sci Food Saf 12(6):614–628

    Article  CAS  Google Scholar 

  • Das A, Nakhro K, Chowdhury S, Kamilya D (2013) Effects of potential probiotic Bacillus amyloliquifaciens FPTB16 on systemic and cutaneous mucosal immune responses and disease resistance of catla (Catla catla). Fish Shellfish Immunol 35(5):1547–1553

    Article  CAS  PubMed  Google Scholar 

  • Feldman BF, Zinkl JG, Jain NC (2000) Schalm’s Veterinary hematology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1120–1124

    Google Scholar 

  • Ghosh K, Sen SK, Ray AK (2004) Supplementation of lactobacillus acidophilus in compound diets for Labeo rohita fingerlings. Indian J Fish 51(4):521–526

    Google Scholar 

  • Giri SS, Sukumaran V, Oviya M (2013) Potential probiotic Lactobacillus plantarum VSG3 improves the growth, immunity, and disease resistance of tropical freshwater fish, Labeo rohita. Fish Shellfish Immunol 34(2):660–666

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Gupta P, Dhawan A (2014) Dietary supplementation of probiotics affects growth, immune response and disease resistance of Cyprinus carpio fry. Fish Shellfish Immunol 41(2):113–119

    Article  CAS  PubMed  Google Scholar 

  • Harikrishnan R, Rani MN, Balasundaram C (2003) Hematological and biochemical parameters in common carp, Cyprinus carpio, following herbal treatment for Aeromonas hydrophila infection. Aquaculture 221:41–50

    Article  Google Scholar 

  • Iman MKA, Wafaa TA, Elham SA, Mohammad MNA, Kawther E, Osama MS, Gamal AI, Zeinab IS, Hoda SE (2013) Evaluation of Lactobacillus plantarum as a probiotic in aquaculture: emphasis on growth performance and innate immunity. J Appl Sci Res 9(1):572–582

    Google Scholar 

  • Irianto A, Austin B (2002) Probiotics in aquaculture. J Fish Dis 25:633–642

    Article  Google Scholar 

  • Jiang HF, Liu XL, Chang YQ, Liu MT, Wang GX (2013) Effects of dietary supplementation of probiotic Shewanella colwelliana WA64, Shewanella olleyana WA65 on the innate immunity and disease resistance of abalone, Haliotis discus hannai Ino. Fish Shellfish Immunol 35(1):86–91

    Article  PubMed  Google Scholar 

  • Khattab YA, Shalaby AM, Abdel-Rhman A (2005) Use of probiotic bacteria as growth promoters, antibacterial and their effects on physiological parameters of Oreochromis niloticus. In: Proceedings of international symposium on Nile Tilapia in aquaculture, 7: 156–165

  • Kongnum K, Hongpattarakere T (2012) Effect of Lactobacillus plantarum isolated from digestive tract of wild shrimp on growth and survival of white shrimp (Litopenaeus vannamei) challenged with Vibrio harveyi. Fish Shellfish Immunol 32(1):170–177

    Article  PubMed  Google Scholar 

  • Kumar R, Mukherjee SC, Prasad KP, Pal AK (2006) Evaluation of Bacillus subtilis as a probiotic to Indian major carp, Labeo rohita. Aquac Res 37:1215–1221

    Article  Google Scholar 

  • Lara-Flores M (2011) The use of probiotic in aquaculture: an overview. Int Res J Microbiol 2(12):471–478

    Google Scholar 

  • Marzouk MS, Moustafa MM, Mohamed NM (2008) Evaluation of Immunomodulatory Effects of Some Probiotics on Cultured Oreochromis niloticus. 8th International Symposium on Tilapia in Aquaculture, Cairo, Egypt

  • Merrifield DL, Dimitroglou A, Bradley G, Baker RTM, Davies SJ (2010) Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) I. Effects on growth performance, feed utilization, intestinal microbiota and related health criteria. Aquac Nutr 16:504–510

    Article  CAS  Google Scholar 

  • Misra CK, Das BK, Mukherjee SC, Pattnaik P (2006) Effect of multiple injections of beta-glucan on non-specific immune response and disease resistance in Labeo rohita fingerlings. Fish Shellfish Immunol 20(3):305–319

    Article  CAS  PubMed  Google Scholar 

  • Mocanu M, Cristea V, Dediu L, Bocioc E, Grecu RI, Ion S, Vasilean I (2010) The effect of probiotic diet on growth and hematology parameters of rainbow trout (Onchorhynchus mykiss, Walbaum 1792). Lucrari Stiintifice-Sera Zootheniie 59:258–263

    Google Scholar 

  • Mohammadian T, Alishahi M, Tabandeh MR, Ghorbanpoor M, Gharibi D, Tollabi M, Rohanizade S (2016) Probiotic effects of Lactobacillus plantarum and L. delbrueckii ssp. bulguricus on some immune-related parameters in Barbus grypus. Aquac Int 24(1):225–242

    Article  Google Scholar 

  • Mohapatra S, Chakraborty T, Prusty AK, Das P, Paniprasad K, Mohanta KN (2012) Use of different microbial probiotics in the diet of rohu, Labeo rohita fingerlings: effects on growth, nutrient digestibility and retention, digestive enzyme activities and intestinal microflora. Aquac Nutr 18(1):1–11

    Article  CAS  Google Scholar 

  • Nayak SK (2010) Probiotics and immunity: a fish perspective. Fish Shellfish Immunol 29(1):2–14

    Article  CAS  PubMed  Google Scholar 

  • Nayak SK, Swain P, Mukherjee SC (2007) Effect of dietary supplementation of probiotic and vitamin C on the immune response of Indian major carp, Labeo rohita (ham). Fish Shellfish Immunol 23(4):892–896

    Article  CAS  PubMed  Google Scholar 

  • Nayak SK, Swain P, Nanda PK, Dash S, Shukla S, Meher PK, Maiti NK (2008) Effect of endotoxin on the immunity of Indian major carp, Labeo rohita. Fish Shellfish Immunol 24(4):394–399

    Article  CAS  PubMed  Google Scholar 

  • Nikoskelainen S, Salminene S, Bylund G, Ouwehand AC (2001) Characterization of the properties of human- and dairy-derived probiotics for prevention of infectious diseases in fish. Appl Environ Microbiol 67:2430–2435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parthasarathy R, Ravi D (2011) Probiotic bacteria as growth promoter and biocontrol agent against Aeromonas hydrophila in Catla catla (Hamilton, 1822). Indian J Fish 58(3):87–93

    Google Scholar 

  • Pirarat N, Pinpimai K, Endo M, Katagiri T, Ponpornpisit A, Chansue N, Maita M (2011) Modulation of intestinal morphology and immunity in Nile tilapia (Oreochromis niloticus) by Lactobacillus rhamnosus GG. Res Vet Sci 91(3):92–97

    Article  Google Scholar 

  • Rajikkannu M, Natarajan N, Santhanam P, Deivasigamani B, Ilamathi J, Janani S (2015) Effect of probiotics on the haematological parameters of Indian major carp (Labeo rohita). Int j fish aquat stud 2(5):105–109

    Google Scholar 

  • Ramos MA, Weber B, Gonçalves JF, Santos GA, Rema P, Ozorio ROA (2013) Dietary probiotic supplementation modulated gut microbiota and improved growth of juvenile rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A Mol Integr Physiol 166:302–307

    Article  CAS  PubMed  Google Scholar 

  • Reed LV, Muench H (1938) A simple method of estimating fifty percent end points. Am J Hyg 27:493–497

    Google Scholar 

  • Reitman S, Frankel S (1957) A colorimetric method for the determination of serum glutamic oxaloacitic and glutamic pyruvic transaminases. Am J Clin Path 28:56–63

    Article  CAS  PubMed  Google Scholar 

  • Renuka KP, Venkateshwarlu M, Naik AR (2014) Effect of probiotic (Lactobacillus acidophilus) on Haematological parameters of Catla catla (Hamilton). Int J Curr Microbiol App Sci 3(8):326–335

    Google Scholar 

  • Reyes-Becerril M, Ascencio-Valle F, Macias ME, Maldonado M, Rojas M, Esteba MA (2012) Effects of marine silages enriched with Lactobacillus sakei 5-4 on haematoimmunological and growth response in Pacific red snapper (Lutjanus peru) exposed to Aeromonas veronii. Fish Shellfish Immunol 33(4):984–992

    Article  CAS  PubMed  Google Scholar 

  • Rollo A, Sulpizio R, Nardi M, Silvi S, Orpianesi C, Caggiano M, Cresci A, Carnevali O (2006) Live microbial feed supplement in aquaculture for improvement of stress tolerance. Fish Physiol Biochem 32(2):167–177

    Article  CAS  Google Scholar 

  • Sahoo P, Mahapatra KD, Saha JN, Barat A, Sahoo M, Mohanty BR, Gjerde B, Odegård J, Rye M, Salte R (2008) Family association between immune parameters and resistance to Aeromonas hydrophila infection in the Indian major carp, Labeo rohita. Fish Shellfish Immunol 25(1):163–169

    Article  CAS  PubMed  Google Scholar 

  • Sahu MK, Swarnakumar N, Sivakumar K, Thangaradjou T, Kannan L (2008) Probiotics in aquaculture: importance and future perspectives. Indian J Microbiol 48:299–308

    Article  PubMed  PubMed Central  Google Scholar 

  • Schaperclaus W, Kulow H, Schreckenbach K (1991) Hematological and serological technique. In: Kothekar VS (ed) Fish disease. Oxonian Press, New Delhi, pp 71–108

    Google Scholar 

  • Sharifuzzaman S, Austin B (2009) Influence of probiotic feeding duration on disease resistance and immune parameters in rainbow trout. Fish Shellfish Immunol 27(3):440–445

    Article  CAS  PubMed  Google Scholar 

  • Shelby RA, Lim C, Yildirim-Aksoy M, Delaney MA (2006) Effects of probiotic supplements on disease resistance and immune response of young Nile tilapia. Oreochromis niloticus. J Appl Aquaculture 18:22–34

    Article  Google Scholar 

  • Shelby RA, Lim C, Yildirim-Aksoy M, Klesius PH (2007) Effects of probiotic bacteria as dietary supplements on growth and disease resistance in young channel catfish, Ictalurus punctatus (Rafinesque). J Appl Aquaculture 19:81–91

    Article  Google Scholar 

  • Soltani M, Kalbassi MR (2001) Protection of Persian sturgeon (Acipenser persicus) fingerling against Aeromonas hydrophila septicemia using three different antigens. Bull Eur Ass Fish Pathol 21(6):235

    Google Scholar 

  • Son VM, Chang CC, Wu MC, Guu YK, Chiu CH, Cheng W (2009) Dietary administration of the probiotic, Lactobacillus plantarum, enhanced the growth, innate immune responses, and disease resistance of the grouper Epinephelus coioides. Fish Shellfish Immunol 26(5):691–698

    Article  CAS  PubMed  Google Scholar 

  • Standen BT, Rawling MD, Davies SJ, Castex M, Foey A, Gioacchini G, Carnevali O, Merrifield DL (2013) Probiotic Pediococcus acidilactici modulates both localised intestinal- and peripheral-immunity in tilapia (Oreochromis niloticus). Fish Shellfish Immunol 35(4):1097–1104

    Article  CAS  PubMed  Google Scholar 

  • Sun YZ, Yang HL, Ma RL, Song K, Li JS (2012) Effect of Lactococcus lactis and Enterococcus faecium on growth performance, digestive enzymes and immune response of grouper Epinephelus coioides. Aquac Nutr 18(3):281–289

    Article  Google Scholar 

  • Suzer C, Coban D, Kamaci HO, Saka S, Firat K, Otgucuoglu O, Kucuksari H (2008) Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities. Aquaculture 280:140–145

    Article  CAS  Google Scholar 

  • Thrall MA, Weiser G, Allison R, Campbell TW (2004) Veterinary haematology and clinical chemistry. Wiley- Blackwell, Hoboken, pp 277–289

    Google Scholar 

  • Tripathi NK, Latimer KS, Burnley VV (2004) Hematologic reference intervals for koi (Cyprinus carpio), including blood cell morphology, cytochemistry, and ultrastructure. Vet Clin Path 33(2):74–83

    Article  Google Scholar 

  • Uma A, Abraham TJ, Sundararaj V (1999) Effect of a probiotic bacterium, Lactobacillus plantarum on disease resistance of Penaeus indicus larvae. Indian J Fish 46(4):367–373

    Google Scholar 

  • Venkat HK, Narottam PS, Kamal KJ (2004) Effect of feeding lactobacillus-based probiotics on the gut microflora, growth and survival of postlarvae of Macrobrachium rosenbergii (de man). Aquac Res 35:501–507

    Article  Google Scholar 

  • Wang YB, Li JR, Lin J (2008) Probiotics in aquaculture: challenges and outlook. Aquaculture 281:1–4

    Article  Google Scholar 

  • Wiegertjes GF, Stet RM, Parmentier HK, van Muiswinkel WB (1996) Immunogenetics of disease resistance in fish: a comparative approach. Dev Comp Immunol 20(6):365–381

    Article  CAS  PubMed  Google Scholar 

  • Wu S, Wang G, Angert ER, Wang W, Li W, Zou H (2012) Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS One 7:e30440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yanbo W, Zirong X (2006) Effect of probiotics for common carp (Cyprinus carpio) based on growth performance and digestive enzyme activities. Anim Feed Sci Technol 127:283–292

    Article  Google Scholar 

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Acknowledgements

This work was funded by a Grant from Research Council of University of Tehran and Center of Excellence of Aquatic Animal Health, University of Tehran.

We would like to thank Faradaneh Company for supporting and providing us the common carp food.

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Correspondence to Mehdi Soltani.

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Soltani, M., Abdy, E., Alishahi, M. et al. Growth performance, immune-physiological variables and disease resistance of common carp (Cyprinus carpio) orally subjected to different concentrations of Lactobacillus plantarum . Aquacult Int 25, 1913–1933 (2017). https://doi.org/10.1007/s10499-017-0164-8

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