Skip to main content

Advertisement

SpringerLink
Log in

Meta-analyses indicate that dietary probiotics significantly improve growth, immune response, and disease resistance in tilapia

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Aquaculture is expanding globally, but intensive rearing conditions can cause diseases due to microbial infections leading to financial losses. Probiotics can be used in tilapia farming instead of antibiotics to improve fish health, growth and are environmentally friendly. We provide a synthesis (meta-analysis) of empirical findings to increase statistical power and produce strong evidence for well-informed decision-making with respect to the use of pro, pre, and synbiotics in tilapia culture. In this meta-analysis, we investigated the effects of dietary probiotics on the immune response modulation and resistance of tilapia against common diseases. A systematic search was performed, and the data from 67 studies were included for review and meta-analysis. Pre-challenge, dietary probiotics led to a significant increase (p < 0.001) in the weight gain and specific growth rate, a significant decrease (p < 0.001) in the feed conversion ratio, but a non-significant increase in survival (p > 0.05). However, probiotics significantly (p < 0.001) enhanced innate immunity based on serum lysozyme, phagocytotic activity, and phagocytotic index, while disease resistance (survival) of tilapia against pathogenic challenge was also significantly (p < 0.001) enhanced. From this study, three categories of probiotics were identified such as single-strain probiotics (SSP), multi-strain probiotics (MSP), and symbiotics (S). The use of synbiotics (probiotics + prebiotics) showed the best effect compared to other probiotic categories, however, more research is needed to ascertain the superiority of synbiotics over other categories. This study concluded that probiotics generally contribute significantly to the growth, immunity, and disease resistance of tilapia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

Most of the associated data can be found in the manuscript. However, any other required data would be provided upon reasonable request from the corresponding author.

References

  • Abarike ED, Cai J, Lu Y et al (2018a) Effects of a commercial probiotic BS containing Bacillus subtilis and Bacillus licheniformis on growth, immune response and disease resistance in Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 82:229–238. https://doi.org/10.1016/j.fsi.2018.08.037

    Article  CAS  PubMed  Google Scholar 

  • Abarike ED, Jian J, Tang J et al (2018b) Influence of traditional Chinese medicine and Bacillus species (TCMBS) on growth, immune response and disease resistance in Nile tilapia, Oreochromis niloticus. Aquac Res 49:2366–2375. https://doi.org/10.1111/are.13691

    Article  CAS  Google Scholar 

  • Abass DA, Obirikorang KA, Campion BB et al (2018) Dietary supplementation of yeast (Saccharomyces cerevisiae) improves growth, stress tolerance, and disease resistance in juvenile Nile tilapia (Oreochromis niloticus). Aquacult Int 26:843–855. https://doi.org/10.1007/S10499-018-0255-1

    Article  CAS  Google Scholar 

  • Abd El-Rhman AM, Khattab YAE, Shalaby AME (2009) Micrococcus luteus and Pseudomonas species as probiotics for promoting the growth performance and health of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 27:175–180. https://doi.org/10.1016/j.fsi.2009.03.020

    Article  PubMed  Google Scholar 

  • Abdel-Tawwab M (2012) Interactive effects of dietary protein and live bakery yeast, Saccharomyces cerevisiae on growth performance of Nile tilapia, Oreochromis niloticus (L.) fry and their challenge against Aeromonas hydrophila infection. Aquacult Int 20:317–331. https://doi.org/10.1007/s10499-011-9462-8

    Article  CAS  Google Scholar 

  • Abomughaid MM (2020) Isolation and Identification of Some Probiotic Bacteria and Their Potential Role in Improving Immune Response and Resistance of Nile Tilapia (Oreochromis niloticus) in Comparison with a Commercial Product. Int J Microbiol 2020:8865456. https://doi.org/10.1155/2020/8865456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abou-El-Atta ME, Abdel-Tawwab M, Abdel-Razek N, Abdelhakim TMN (2019) Effects of dietary probiotic Lactobacillus plantarum and whey protein concentrate on the productive parameters, immunity response and susceptibility of Nile tilapia, Oreochromis niloticus (L.), to Aeromonas sobria infection. Aquac Nutr 25:1367–1377. https://doi.org/10.1111/anu.12957

    Article  CAS  Google Scholar 

  • Abu-Elala N, Marzouk M, Moustafa M (2013) Use of different Saccharomyces cerevisiae biotic forms as immune-modulator and growth promoter for Oreochromis niloticus challenged with some fish pathogens. Int J Vet Sci Med 1:21–29. https://doi.org/10.1016/j.ijvsm.2013.05.001

    Article  Google Scholar 

  • Addo S, Carrias AA, Williams MA et al (2016) Effects of Bacillus subtilis strains on growth, immune parameters, and Streptococcus iniae susceptibility in Nile Tilapia, Oreochromis niloticus. Wiley Online Library 48:257–267. https://doi.org/10.1111/jwas.12380

    Article  CAS  Google Scholar 

  • Addo S, Carrias AA, Williams MA et al (2017) Effects of Bacillus subtilis strains and the prebiotic Previda® on growth, immune parameters and susceptibility to Aeromonas hydrophila infection in Nile tilapia, Oreochromis niloticus. Aquac Res 48:4798–4810. https://doi.org/10.1111/are.13300

    Article  CAS  Google Scholar 

  • Ahn E, Kang H (2018) Introduction to systematic review and meta-analysis. Korean J Anesthesiol 71. https://doi.org/10.4097/kjae.2018.71.2.103

  • Akhter N, Wu B, Memon AM, Mohsin M (2015) Probiotics and prebiotics associated with aquaculture: A review. Fish Shellfish Immunol 45:733–741

    Article  CAS  PubMed  Google Scholar 

  • Aly SM, Abdel-Galil AY, Abdel-Aziz GA, Mohamed MF (2008a) 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 25:128–136. https://doi.org/10.1016/j.fsi.2008.03.013

    Article  CAS  PubMed  Google Scholar 

  • Aly SM, Mohamed MF, John G (2008b) Effect of probiotics on the survival, growth and challenge infection in Tilapia nilotica (Oreochromis niloticus). Aquac Res 39:647–656. https://doi.org/10.1111/j.1365-2109.2008.01932.x

    Article  CAS  Google Scholar 

  • Ammar A, Abd El-Galil S, Mohamed B, Gharib A (2022) Immunological, biochemical and growth performance studies on Nile Tilapia supplemented with probiotic, green tea and clove oil. J Adv Vet Res 12:753–759. https://www.advetresearch.com/index.php/AVR/article/view/1093. Accessed 24 Feb 2023

  • Amphan S, Unajak S, Printrakoon C, Areechon N (2019) Feeding-regimen of β-glucan to enhance innate immunity and disease resistance of Nile tilapia, Oreochromis niloticus Linn., against Aeromonas hydrophila and Flavobacterium columnare. Fish Shellfish Immunol 87:120–128. https://doi.org/10.1016/j.fsi.2018.12.062

    Article  CAS  PubMed  Google Scholar 

  • Awad LZ, El-Mahallawy HS, Abdelnaeim NS et al (2022) Role of dietary Spirulina platensis and betaine supplementation on growth, hematological, serum biochemical parameters, antioxidant status, immune responses, and disease resistance in Nile tilapia. Fish Shellfish Immunol 126:122–130. https://doi.org/10.1016/j.fsi.2022.05.040

    Article  CAS  PubMed  Google Scholar 

  • Ayoub HF, Abdelghany MF, El-Sayed AEKB (2019) Effects of diatoms amphora coffeaeformis on growth parameters, non specific immunity and protection of the nile tilapia (Oreochromis niloticus) to aeromonas hydrophila infection. Egypt J Aquat Biol Fish 23:413–426. https://doi.org/10.21608/EJABF.2019.37466

  • Banu MR, Akter S, Islam MR et al (2020) Probiotic yeast enhanced growth performance and disease resistance in freshwater catfish gulsa tengra. Mystus Cavasius Aquac Rep 16:100237. https://doi.org/10.1016/j.aqrep.2019.100237

    Article  Google Scholar 

  • Basri L, Nor R, Salleh A et al (2020) Co-infections of tilapia lake virus, aeromonas hydrophila and Streptococcus agalactiae in farmed red hybrid tilapia. Animals 10:2141. https://doi.org/10.3390/ani10112141

    Article  PubMed  PubMed Central  Google Scholar 

  • Bocamdé TJ, Marie KP, François ZN et al (2020) Improvement of the growth performance, innate immunity and disease resistance of nile tilapia (Oreochromis niloticus) against vibrio parahaemolyticus 1T1 following dietary application of the probiotic strain Lactobacillus plantarum 1KMT. J Adv Biol Biotechnol 23:27–39. https://doi.org/10.9734/jabb/2020/v23i730167

    Article  CAS  Google Scholar 

  • Butt UD, Lin N, Akhter N et al (2021) Overview of the latest developments in the role of probiotics, prebiotics and synbiotics in shrimp aquaculture. Fish Shellfish Immunol 114:263–281

    Article  CAS  PubMed  Google Scholar 

  • Büyükdeveci ME, Cengizler İ, Balcázar JL, Demirkale İ (2023) Effects of two host-associated probiotics Bacillus mojavensis B191 and Bacillus subtilis MRS11 on growth performance, intestinal morphology, expression of immune-related genes and disease resistance of Nile tilapia (Oreochromis niloticus) against Streptococcus iniae. Dev Comp Immunol 138:104553. https://doi.org/10.1016/j.dci.2022.104553

    Article  CAS  Google Scholar 

  • Camargo-dos-Santos B, Rossi VS, Gonçalves BB et al (2021) The impact of catch-and-release on feeding responses and aggressive behavior in Nile tilapia (Oreochromis niloticus). Mar Freshw Behav Physiol 54:133–148. https://doi.org/10.1080/10236244.2021.1953380

    Article  Google Scholar 

  • Cavalcante RB, Telli GS, Tachibana L et al (2020) Probiotics, prebiotics and synbiotics for Nile tilapia: growth performance and protection against Aeromonas hydrophila infection. Aquac Rep 17:100343. https://doi.org/10.1016/j.aqrep.2020.100343

    Article  Google Scholar 

  • Chaudhari A, Dwivedi MK (2022) The concept of probiotics, prebiotics, postbiotics, synbiotics, nutribiotics, and pharmabiotics. In: Dwivedi MK, Sankaranarayanani N, Amaresan N, Kemp HE (eds) Probiotics in the prevention and management of human diseases, 1st edn. Elsevier, Amsterdam, pp 1–11

    Google Scholar 

  • Chen J, Fan Z, Tan D et al (2018) A review of genetic advances related to sex control and manipulation in Tilapia. J World Aquac Soc 49:277–291

    Article  Google Scholar 

  • Chen SW, Liu CH, Hu SY (2019) Dietary administration of probiotic Paenibacillus ehimensis NPUST1 with bacteriocin-like activity improves growth performance and immunity against Aeromonas hydrophila and Streptococcus iniae in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 84:695–703. https://doi.org/10.1016/j.fsi.2018.10.059

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Tan X, Padman R (2020) Social determinants of health in electronic health records and their impact on analysis and risk prediction: a systematic review. J Am Med Inform Assoc 27:1764–1773

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawood MAO, Abo-Al-Ela HG, Hasan MT (2020) Modulation of transcriptomic profile in aquatic animals: probiotics, prebiotics and synbiotics scenarios. Fish Shellfish Immunol 97:268–282

    Article  CAS  PubMed  Google Scholar 

  • de Moraes AV, Owatari MS, da Silva E et al (2022) Effects of microencapsulated probiotics-supplemented diet on growth, non-specific immunity, intestinal health and resistance of juvenile Nile tilapia challenged with Aeromonas hydrophila. Anim Feed Sci Technol 287:115286. https://doi.org/10.1016/j.anifeedsci.2022.115286

    Article  CAS  Google Scholar 

  • Dias JAR, Alves LL, Barros FAL et al (2022) Comparative effects of using a single strain probiotic and multi-strain probiotic on the productive performance and disease resistance in Oreochromis niloticus. Aquaculture 550:737855. https://doi.org/10.1016/j.aquaculture.2021.737855

    Article  CAS  Google Scholar 

  • Disner GR, Falcão MAP, Andrade-Barros AI et al (2021) The toxic effects of glyphosate, chlorpyrifos, abamectin, and 2,4-D on animal models: a systematic review of Brazilian studies. Integr Environ Assess Manag 17:507–520

    Article  CAS  PubMed  Google Scholar 

  • Dong HT, Senapin S, Gangnonngiw W, Nguyen VV, Rodkhum C, Debnath PP, Delamare-Deboutteville J, Mohan CV (2020) Experimental infection reveals transmission of tilapia lake virus (TiLV) from tilapia broodstock to their reproductive organs and fertilized eggs. Aquaculture 515:734541

    Article  CAS  Google Scholar 

  • Dowidar M, Abd ElAzeem S, Khater A et al (2018) Improvement of growth performance, immunity and disease resistance in Nile tilapia, Oreochromis niloticus, by using dietary probiotics supplementation. J Anim Sci Vet Med 3:35–46. https://doi.org/10.31248/JASVM2018.076

  • Eissa N, AbouElGheit E (2014) Dietary supplementation impacts of potential non-pathogenic isolates on growth performance, hematological parameters and disease resistance in Nile tilapia (Oreochromis niloticus). J Vet Adv 4:712–719. https://doi.org/10.5455/jva.20141025045451

    Article  Google Scholar 

  • Eissa AE, Attia MM, Elgendy MY et al (2021) Streptococcus, Centrocestus formosanus and Myxobolus tilapiae concurrent infections in farmed Nile tilapia (Oreochromis niloticus). Microb Pathog 158:105084. https://doi.org/10.1016/j.micpath.2021.105084

    Article  CAS  PubMed  Google Scholar 

  • El-Nobi G, Hassanin M, Khalil AA et al (2021) Synbiotic effects of saccharomyces cerevisiae, mannan oligosaccharides, and β-glucan on innate immunity, antioxidant status, and disease resistance of Nile tilapia Oreochromis Niloticus. Antibiotics 10:567. https://doi.org/10.3390/antibiotics10050567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gewaily MS, Shukry M, Abdel-Kader MF et al (2021) Dietary Lactobacillus plantarum relieves Nile tilapia (Oreochromis niloticus) juvenile from oxidative stress, immunosuppression, and inflammation induced by Deltamethrin and Aeromonas hydrophila. Front Mar Sci 8:621558. https://doi.org/10.3389/fmars.2021.621558

    Article  Google Scholar 

  • Gobi N, Vaseeharan B, Chen JC et al (2018) Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish Shellfish Immunol 74:501–508. https://doi.org/10.1016/j.fsi.2017.12.066

    Article  CAS  PubMed  Google Scholar 

  • Gu Q, Yin Y, Yan X et al (2022) Encapsulation of multiple probiotics, synbiotics, or nutrabiotics for improved health effects: A review. Adv Colloid Interface Sci 309:102781

    Article  CAS  PubMed  Google Scholar 

  • Guangxin G, Li K, Zhu Q et al (2022) Improvements of immune genes and intestinal microbiota composition of turbot (Scophthalmus maximus) with dietary oregano oil and probiotics. Aquaculture 547:737442. https://doi.org/10.1016/j.aquaculture.2021.737442

    Article  CAS  Google Scholar 

  • Guimarães MC, Cerezo IM, Fernandez-Alarcon MF et al (2022) Oral Administration of Probiotics (Bacillus subtilis and Lactobacillus plantarum) in Nile Tilapia (Oreochromis niloticus) Vaccinated and Challenged with Streptococcus agalactiae. Fishes 7:211. https://doi.org/10.3390/fishes7040211

    Article  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 41:113–119. https://doi.org/10.1016/j.fsi.2014.08.023

    Article  CAS  PubMed  Google Scholar 

  • Hamdan AM, El-Sayed AFM, Mahmoud MM (2016) Effects of a novel marine probiotic, Lactobacillus plantarum AH 78, on growth performance and immune response of Nile tilapia (Oreochromis niloticus). J Appl Microbiol 120:1069–1073. https://doi.org/10.1111/jam.13081

    Article  CAS  Google Scholar 

  • Han B, Long WQ, He JY et al (2015) Effects of dietary Bacillus licheniformis on growth performance, immunological parameters, intestinal morphology and resistance of juvenile Nile tilapia (Oreochromis niloticus) to challenge infections. Fish Shellfish Immunol 46:225–231. https://doi.org/10.1016/j.fsi.2015.06.018

    Article  CAS  PubMed  Google Scholar 

  • Hijová E (2022) Synbiotic supplements in the prevention of obesity and obesity-related diseases. Metabolites 12:313

    Article  PubMed  PubMed Central  Google Scholar 

  • Iwashita MKP, Nakandakare IB, Terhune JS et al (2015) Dietary supplementation with Bacillus subtilis, Saccharomyces cerevisiae and Aspergillus oryzae enhance immunity and disease resistance against Aeromonas hydrophila and Streptococcus iniae infection in juvenile tilapia Oreochromis niloticus. Fish Shellfish Immunol 43:60–66. https://doi.org/10.1016/j.fsi.2014.12.008

    Article  CAS  PubMed  Google Scholar 

  • Jose MS, Arun D, Neethu S et al (2023) Probiotic Paenibacillus polymyxa HGA4C and Bacillus licheniformis HGA8B combination improved growth performance, enzymatic profile, gene expression and disease resistance in Oreochromis niloticus. Microb Pathog 174:105951. https://doi.org/10.1016/j.micpath.2022.105951

    Article  CAS  Google Scholar 

  • Junior JAF, Leal CAG, de Oliveira TF et al (2020) Anatomopathological characterization and etiology of lesions on Nile tilapia fillets (Oreochromis niloticus) caused by bacterial pathogens. Aquaculture 526:735387. https://doi.org/10.1016/j.aquaculture.2020.735387

    Article  CAS  Google Scholar 

  • Kaew-On S, Areechon N, Wanchaitanawong P (2016) Effects of Pediococcus pentosaceus PKWA-1 and Bacillus subtilis BA04 on growth performances, immune responses and disease resistance against Aeromonas hydrophila in nile tilapia (Oreochromis niloticus Linn.). Chiang Mai J Sci 43:997–1006

    CAS  Google Scholar 

  • Kavitha M, Raja M, Perumal P (2018) Evaluation of probiotic potential of Bacillus spp. isolated from the digestive tract of freshwater fish Labeo calbasu (Hamilton, 1822). Aquac Rep 11:59–69. https://doi.org/10.1016/j.aqrep.2018.07.001

    Article  Google Scholar 

  • Kerddee P, Dong HT, Chokmangmeepisarn P et al (2020) Simultaneous detection of scale drop disease virus and Flavobacterium columnare from diseased freshwater-reared barramundi Lates calcarifer. Dis Aquat Organ 140:119–128. https://doi.org/10.3354/dao03500

    Article  CAS  PubMed  Google Scholar 

  • Khunrang T, Pooljun C, Wutisutimeethavee S, Direkbusarakom S (2021) Effects of mixed probiotic (Lactobacillus sp. and Saccharomyces cerevisiae) on the growth performance and immune gene expression of tilapia (Oreochromis niloticus) after Streptococcus agalactiae vaccination. Aquac Res 52:3882–3889. https://doi.org/10.1111/are.15232

    Article  CAS  Google Scholar 

  • Kuebutornye F, Abarike ED, Sakyi ME et al (2020a) Modulation of nutrient utilization, growth, and immunity of Nile tilapia, Oreochromis niloticus: the role of probiotics. Aquacult Int 28:277–291

    Article  Google Scholar 

  • Kuebutornye FKA, Wang Z, Lu Y et al (2020b) Effects of three host-associated Bacillus species on mucosal immunity and gut health of Nile tilapia, Oreochromis niloticus and its resistance against Aeromonas hydrophila infection. Fish Shellfish Immunol 97:83–95. https://doi.org/10.1016/j.fsi.2019.12.046

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Roy S, Meena DK, Sarkar UK (2016) Application of probiotics in shrimp aquaculture: importance, mechanisms of action, and methods of administration. Rev Fish Sci Aquacult 24:342–368

    Article  Google Scholar 

  • Li H, Zhou Y, Ling H et al (2019) The effect of dietary supplementation with Clostridium butyricum on the growth performance, immunity, intestinal microbiota and disease resistance of tilapia (Oreochromis niloticus). PLoS One 14:e0223428. https://doi.org/10.1371/journal.pone.0223428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Luo L, Zhou Y et al (2020) Dietary administration of Enterococcus faecalis affects the growth, disease resistance and immune function of tilapia (Oreochromis niloticus). Aquac Rep 18:100440. https://doi.org/10.1016/j.aqrep.2020.100440

    Article  Google Scholar 

  • Liao Q, Zhen Y, Qin Y et al (2022) Effects of dietary Metschnikowia sp. GXUS03 on growth, immunity, gut microbiota and Streptococcus agalactiae resistance of Nile tilapia (Oreochromis niloticus). Aquac Res 53:1918–1927. https://doi.org/10.1111/are.15720

    Article  CAS  Google Scholar 

  • Lin YS, Saputra F, Chen YC, Hu SY (2019) Dietary administration of Bacillus amyloliquefaciens R8 reduces hepatic oxidative stress and enhances nutrient metabolism and immunity against Aeromonas hydrophila and Streptococcus agalactiae in zebrafish (Danio rerio). Fish Shellfish Immunol 86:410–419. https://doi.org/10.1016/j.fsi.2018.11.047

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Wang S, Cai Y et al (2017) Dietary administration of Bacillus subtilis HAINUP40 enhances growth, digestive enzyme activities, innate immune responses and disease resistance of tilapia, Oreochromis niloticus. Fish Shellfish Immunol 60:326–333. https://doi.org/10.1016/j.fsi.2016.12.003

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Wen L, Pan X et al (2021) Dietary supplementation of Bacillus subtilis and Enterococcus faecalis can effectively improve the growth performance, immunity, and resistance of tilapia against Streptococcus agalactiae. Aquac Nutr 27:1160–1172. https://doi.org/10.1111/anu.13256

    Article  CAS  Google Scholar 

  • Liu Y, Wang J, Wu C (2022) Modulation of gut microbiota and immune system by probiotics, pre-biotics, and post-biotics. Front Nutr 8:1155

    Article  Google Scholar 

  • Melo-Bolívar JF, Ruiz Pardo RY, Hume ME, Villamil Díaz LM (2021) Multistrain probiotics use in main commercially cultured freshwater fish: a systematic review of evidence. Rev Aquac 13:1758–1780. https://doi.org/10.1111/RAQ.12543

    Article  Google Scholar 

  • Menaga M, Fitzsimmons K (2017) Growth of the tilapia industry in India. World Aquaculture 48:49–52

    Google Scholar 

  • Merrifield DL, Bradley G, Baker RTM, Davies SJ (2010) Probiotic applications for rainbow trout (Oncorhynchus mykiss Walbaum) II. Effects on growth performance, feed utilization, intestinal microbiota and related health criteria postantibiotic treatment. Aquac Nutr 16. https://doi.org/10.1111/j.1365-2095.2009.00688.x

  • Mohamed M, Mahmoud H, Abd-El-Rahman G, Ayyat M (2019) Impacts of commercial probiotics on growth performance, disease resistance and profitability of Nile tilapia (Oreochromis niloticus) under stocking density stress. Zagazig J Agricult Res 46:157–170. https://doi.org/10.21608/zjar.2019.46403

  • Mohammadi G, Rafiee G, Tavabe KR et al (2021) The enrichment of diet with beneficial bacteria (single- or multi- strain) in biofloc system enhanced the water quality, growth performance, immune responses, and disease resistance of Nile tilapia (Oreochromis niloticus). Aquaculture 539:736640. https://doi.org/10.1016/j.aquaculture.2021.736640

    Article  CAS  Google Scholar 

  • Mohammadi G, Hafezieh M, Karimi AA et al (2022) The synergistic effects of plant polysaccharide and Pediococcus acidilactici as a synbiotic additive on growth, antioxidant status, immune response, and resistance of Nile tilapia (Oreochromis niloticus) against Aeromonas hydrophila. Fish Shellfish Immunol 120:304–313. https://doi.org/10.1016/j.fsi.2021.11.028

    Article  CAS  PubMed  Google Scholar 

  • Mousa H, El-Keredy M, Rashed MA (2021) Using lactobacillus acidophilus in fish feed to improve disease resistance and immune status of cultured Nile tilapia. Alex J Vet Sci 70:15–28. https://doi.org/10.5455/ajvs.83913

    Article  Google Scholar 

  • Khaneghah AM, Abhari K, Eş I et al (2020) Interactions between probiotics and pathogenic microorganisms in hosts and foods: A review. Trends in Food Sci Technol 95:205–18. https://doi.org/10.1016/j.tifs.2019.11.022

    Article  CAS  Google Scholar 

  • Moustafa EM, Farrag FA, Dawood MAO et al (2021) Efficacy of Bacillus probiotic mixture on the immunological responses and histopathological changes of Nile tilapia (Oreochromis niloticus, L) challenged with Streptococcus iniae. Aquac Res 52:2205–2219. https://doi.org/10.1111/are.15073

    Article  CAS  Google Scholar 

  • Mugwanya M, Dawood MAO, Kimera F, Sewilam H (2022) Updating the role of probiotics, prebiotics, and synbiotics for tilapia aquaculture as leading candidates for food sustainability: a review. Probiotics Antimicrob Proteins 14:1–28

    Article  Google Scholar 

  • Ng WK, Kim YC, Romano N et al (2014) Effects of dietary probiotics on the growth and feeding efficiency of red hybrid tilapia, Oreochromis sp., and subsequent resistance to Streptococcus agalactiae. J Appl Aquac 26:22–31. https://doi.org/10.1080/10454438.2013.874961

    Article  Google Scholar 

  • Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A (2016) Rayyan-a web and mobile app for systematic reviews. Syst Rev 5:1–10. https://doi.org/10.1186/s13643-016-0384-4

    Article  Google Scholar 

  • Page M, McKenzie J, Bossuyt P, Boutron I (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg 88:105906. https://doi.org/10.1016/j.ijsu.2021.105906

    Article  PubMed  Google Scholar 

  • Palai S, Derecho CMP, Kesh SS, et al (2020) Prebiotics, probiotics, synbiotics and its importance in the management of diseases. Funct Foods Nutraceuticals 173–196. https://doi.org/10.1007/978-3-030-42319-3_10

  • Panase A, Thirabunyanon M, Promya J, Chitmanat C (2023) Influences of Bacillus subtilis and fructooligosaccharide on growth performances, immune responses, and disease resistance of Nile tilapia. Oreochromis Niloticus Front Vet Sci 9:109468. https://doi.org/10.3389/fvets.2022.1094681

    Article  Google Scholar 

  • Pauzi NA, Mohamad N, Azzam-Sayuti M, Yasin ISM, Saad MZ, Nasruddin NS, Azmai MNA (2020) Antibiotic susceptibility and pathogenicity of Aeromonas hydrophila isolated from red hybrid tilapia (Oreochromis niloticus × Oreochromis mossambicus) in Malaysia. Vet World 13(10):2166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prabu E, Rajagopalsamy CBT, Ahilan B et al (2019) Tilapia – an excellent candidate species for world aquaculture: a review. Annu Res Rev Biol 31:1–14. https://doi.org/10.9734/arrb/2019/v31i330052

    Article  CAS  Google Scholar 

  • Pujari R, Banerjee G (2021) Impact of prebiotics on immune response: from the bench to the clinic. Immunol Cell Biol 99:255–273

    Article  CAS  PubMed  Google Scholar 

  • Reverter M, Tapissier-Bontemps N, Sarter S et al (2021) Moving towards more sustainable aquaculture practices: a meta-analysis on the potential of plant-enriched diets to improve fish growth, immunity and disease resistance. Rev Aquac 13:537–555

    Article  Google Scholar 

  • Rohani MF, Islam SM, Hossain MK et al (2022) Probiotics, prebiotics and synbiotics improved the functionality of aquafeed: Upgrading growth, reproduction, immunity and disease resistance in fish. Fish Shellfish Immunol 120:569–589

    Article  CAS  PubMed  Google Scholar 

  • Rose EC, Odle J, Blikslager AT, Ziegler AL (2021) Probiotics, prebiotics and epithelial tight junctions: a promising approach to modulate intestinal barrier function. Int J Mol Sci 22:6729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai M, Yoshida T, Atsuta S, Kobayashi M (1995) Enhancement of resistance to vibriosis in rainbow trout, Oncorhynchus mykiss (Walbaum), by oral administration of Clostridium butyricum bacterin. J Fish Dis 18:187–190. https://doi.org/10.1111/j.1365-2761.1995.tb00276.x

    Article  Google Scholar 

  • Samson JS, Choresca CH, Quiazon KMA (2022) Probiotic effect of Bacillus spp. isolated from African nightcrawler (Eudrilus eugeniae) on the performance of Nile Tilapia (Oreochromis niloticus L.). Arch Microbiol 204:235. https://doi.org/10.1007/s00203-022-02856-3

  • Santos G, Libanori M, Pereira S, Ferrarezi J (2023) Probiotic mix of Bacillus spp. and benzoic organic acid as growth promoter against Streptococcus agalactiae in Nile tilapia. Aquaculture 566:739212. https://doi.org/10.1016/j.aquaculture.2022.739212

  • Saputra F, Shiu Y, Chen Y, Puspitasari A (2016) Dietary supplementation with xylanase-expressing B. áamyloliquefaciens R8 improves growth performance and enhances immunity against Aeromonas. Fish Shellfish Immunol 58:379–405. https://doi.org/10.1016/j.fsi.2016.09.046

  • Sayed S, Zakaria A, Mohamed G (2011) Use of probiotics as growth promoter, anti-bacterial and their effects on the physiological parameters and immune response of Oreochromis niloticus Lin. J Arab Aquacult Soc 6:201–222

    Google Scholar 

  • Selim KM, Reda RM (2015) Improvement of immunity and disease resistance in the Nile tilapia, Oreochromis niloticus, by dietary supplementation with Bacillus amyloliquefaciens. Fish Shellfish Immunol 44:496–503. https://doi.org/10.1016/j.fsi.2015.03.004

    Article  CAS  PubMed  Google Scholar 

  • Sewaka M, Trullas C, Chotiko A et al (2019) Efficacy of synbiotic Jerusalem artichoke and Lactobacillus rhamnosus GG-supplemented diets on growth performance, serum biochemical parameters, intestinal morphology, immune parameters and protection against Aeromonas veronii in juvenile red tilapia (Oreochromis spp.). Fish Shellfish Immunol 86:260–268. https://doi.org/10.1016/j.fsi.2018.11.026

    Article  CAS  PubMed  Google Scholar 

  • Sharifuzzaman SM, Austin B (2009) Influence of probiotic feeding duration on disease resistance and immune parameters in rainbow trout. Fish Shellfish Immunol 27:440–445. https://doi.org/10.1016/j.fsi.2009.06.010

    Article  CAS  PubMed  Google Scholar 

  • Shelby RA, Lim C, Yildirim-Aksoy M, Delaney MA (2006) Effects of probiotic diet supplements on disease resistance and immune response of young Nile tilapia, Oreochromis niloticus. J Appl Aquac 18:23–34. https://doi.org/10.1300/J028v18n02_02

    Article  Google Scholar 

  • Sherif AH, Gouda MY, Al-Sokary ET, Elseify MM (2021) Lactobacillus plantarum enhances immunity of Nile tilapia Oreochromis niloticus challenged with Edwardsiella tarda. Aquac Res 52:1001–1012. https://doi.org/10.1111/are.14955

    Article  CAS  Google Scholar 

  • Sîrbu E, Dima MF, Tenciu M et al (2022) Effects of dietary supplementation with probiotics and prebiotics on growth, physiological condition, and resistance to pathogens challenge in Nile tilapia (Oreochromis niloticus). Fishes 7:273. https://doi.org/10.3390/fishes7050273

    Article  Google Scholar 

  • Sookchaiyaporn N, Srisapoome P, Unajak S, Areechon N (2020) Efficacy of Bacillus spp. isolated from Nile tilapia Oreochromis niloticus Linn. on its growth and immunity, and control of pathogenic bacteria. Fish Sci 86:353–365. https://doi.org/10.1007/s12562-019-01394-0

    Article  CAS  Google Scholar 

  • Srisapoome P, Areechon N (2017) Efficacy of viable Bacillus pumilus isolated from farmed fish on immune responses and increased disease resistance in Nile tilapia (Oreochromis niloticus): Laboratory and on-farm trials. Fish Shellfish Immunol 67:199–210. https://doi.org/10.1016/j.fsi.2017.06.018

    Article  CAS  PubMed  Google Scholar 

  • Suphoronski SA, de Souza FP, Chideroli RT et al (2021) Effect of enterococcus faecium as a water and/or feed additive on the gut microbiota, hematologic and immunological parameters, and resistance against francisellosis and streptococcosis in Nile tilapia (Oreochromis niloticus). Front Microbiol 12:743957. https://doi.org/10.3389/fmicb.2021.743957

    Article  PubMed  PubMed Central  Google Scholar 

  • Suprayudi MA, Maeda M, Hidayatullah H et al (2017) The positive contributions of PowerLac™ supplementation to the production performance, feed utilization and disease resistance of Nile tilapia Oreochromis niloticus (L.). Aquac Res 48:2145–2156. https://doi.org/10.1111/are.13052

    Article  CAS  Google Scholar 

  • Tachibana L, Telli GS, de Carla Dias D et al (2020) Effect of feeding strategy of probiotic Enterococcus faecium on growth performance, hematologic, biochemical parameters and non-specific immune response of Nile tilapia. Aquac Rep 16:100277. https://doi.org/10.1016/j.aqrep.2020.100277

    Article  Google Scholar 

  • Tan HY, Chen SW, Hu SY (2019) Improvements in the growth performance, immunity, disease resistance, and gut microbiota by the probiotic Rummeliibacillus stabekisii in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immunol 92:265–275. https://doi.org/10.1016/j.fsi.2019.06.027

    Article  CAS  PubMed  Google Scholar 

  • Toledo A, Frizzo L, Signorini M et al (2019) Impact of probiotics on growth performance and shrimp survival: a meta-analysis. Aquaculture 500:196–205

    Article  CAS  Google Scholar 

  • Van Doan H, Hoseinifar SH, Khanongnuch C et al (2018) Host-associated probiotics boosted mucosal and serum immunity, disease resistance and growth performance of Nile tilapia (Oreochromis niloticus). Aquaculture 491:94–100. https://doi.org/10.1016/j.aquaculture.2018.03.019

    Article  Google Scholar 

  • Van Hai N (2015) Research findings from the use of probiotics in tilapia aquaculture: A review. Fish Shellfish Immunol 45(2):592–597. https://doi.org/10.1016/j.fsi.2015.05.026

    Article  CAS  PubMed  Google Scholar 

  • Waiyamitra P, Zoral MA, Saengtienchai A et al (2020) Probiotics modulate tilapia resistance and immune response against tilapia lake virus infection. Pathogens 9:919. https://doi.org/10.3390/pathogens9110919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Lu M (2016) Tilapia polyculture: a global review. Aquac Res 47:2363–2374. https://doi.org/10.1111/are.12708

    Article  Google Scholar 

  • Wang X, Zhang P, Zhang X (2021) Probiotics regulate gut microbiota: an effective method to improve immunity. Molecules 26:6076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Thompson KD, Wangkahart E et al (2023) Strategies to enhance tilapia immunity to improve their health in aquaculture. Rev Aquac 15:41–56. https://doi.org/10.1111/raq.12731

    Article  CAS  Google Scholar 

  • Wu PS, Liu CH, Hu SY (2021) Probiotic bacillus safensis npust1 administration improves growth performance, gut microbiota, and innate immunity against Streptococcus iniae in nile tilapia (Oreochromis niloticus). Microorganisms 9:2494. https://doi.org/10.3390/microorganisms9122494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wuertz S, Schroeder A, Wanka KM (2021) Probiotics in fish nutrition—long-standing household remedy or native nutraceuticals? Water (Switzerland) 13:1348

  • Wulansari F, Prayitno B, Harjuno A, Haditomo C (2019) Study of probiotic candidate bacteria CBL20 for inhibiting of Aeromonas hydrophila with different concentration in Tilapia (Oreochromis niloticus). IOP Conf Ser Earth Environ Sci 246:1–8. https://doi.org/10.1088/1755-1315/246/1/012032

    Article  Google Scholar 

  • Xia Y, Lu M, Chen G et al (2018) Effects of dietary Lactobacillus rhamnosus JCM1136 and Lactococcus lactis subsp. lactis JCM5805 on the growth, intestinal microbiota, morphology, immune response and disease resistance of juvenile Nile tilapia Oreochromis Niloticus. Fish Shellfish Immunol 76:368–379. https://doi.org/10.1016/j.fsi.2018.03.020

    Article  CAS  PubMed  Google Scholar 

  • Xia Y, Wang M, Gao F et al (2020) Effects of dietary probiotic supplementation on the growth, gut health and disease resistance of juvenile Nile tilapia (Oreochromis niloticus). Animal Nutrition 6:69–79. https://doi.org/10.1016/j.aninu.2019.07.002

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Ding FF, Zhou NN et al (2022) Bacillus amyloliquefaciens protects Nile tilapia against Aeromonas hydrophila infection and alleviates liver inflammation induced by high-carbohydrate diet. Fish Shellfish Immunol 127:836–842. https://doi.org/10.1016/j.fsi.2022.07.033

    Article  CAS  PubMed  Google Scholar 

  • Yousefi M, Naderi Farsani M, Ghafarifarsani H, Raeeszadeh M (2023) Dietary Lactobacillus helveticus and Gum Arabic improves growth indices, digestive enzyme activities, intestinal microbiota, innate immunological parameters, antioxidant capacity, and disease resistance in common carp. Fish Shellfish Immunol 135:108652. https://doi.org/10.1016/j.fsi.2023.108652

    Article  CAS  PubMed  Google Scholar 

  • Yu Y-M, Poon PM-Y, Sharma AA et al (2022) Colonization of Lactobacillus rhamnosus GG in Cirrhinus molitorella (Mud Carp) fingerling: evidence for improving disease resistance and growth performance. Appl Microbiol 2:175–184. https://doi.org/10.3390/applmicrobiol2010012

    Article  Google Scholar 

  • Zawistowska-Rojek A, Tyski S (2022) how to improve health with biological agents—narrative review. Nutrients 14:1700. https://doi.org/10.3390/nu14091700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Lee D, Zhang M, Tippetts B (2016) Object recognition algorithm for the automatic identification and removal of invasive fish. Biosyst Eng 145:67–75. https://doi.org/10.3389/fmicb.2019.02663

    Article  Google Scholar 

  • Zheng ZL, Wang KY, Gatlin DM, Ye JM (2011) Evaluation of the ability of grobiotic ®-a to enhance growth, muscle composition, immune responses, and resistance against Aeromonas hydrophila in nile tilapia, Oreochromis niloticus. J World Aquac Soc 42:549–557. https://doi.org/10.1111/j.1749-7345.2011.00497.x

    Article  Google Scholar 

  • Zhou X, Zhao X, Zhang S, Lin J (2019) Marine ranching construction and management in East China Sea: programs for sustainable fishery and aquaculture. Water (basel) 11:1237

    Google Scholar 

  • Zhu W, Su J (2022) Immune functions of phagocytic blood cells in teleost. Rev Aquac 14:630–646

    Article  Google Scholar 

  • Zhu C, Yu L, Liu W et al (2019) Dietary supplementation with Bacillus subtilis LT3-1 enhance the growth, immunity and disease resistance against Streptococcus agalactiae infection in genetically improved farmed tilapia, Oreochromis niloticus. Aquac Nutr 25:1241–1249. https://doi.org/10.1111/anu.12938

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We appreciate the anonymous reviewers whose comments have helped to improve this manuscript.

Funding

This study was financially supported by the Ministry of Higher Education, Malaysia under the Transdisciplinary Research Grant Scheme (TRGS/1/2019/UPM/02/5) and Higher Institution Centre of Excellence (IBS HICoE; Grant no. 6369100).

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Universiti Putra Malaysia (UPM), 43400, Serdang, Selangor, Malaysia

    Abdulwakil Olawale Saba & Mohammad Noor Amal Azmai

  2. Department of Fisheries, Faculty of Science, Lagos State University, Ojo, Lagos, 102101, Nigeria

    Abdulwakil Olawale Saba

  3. Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia (UPM), 43400, Serdang, Selangor, Malaysia

    Ina Salwany Md Yasin

  4. Aquatic Animal Health and Therapeutics Laboratory, Institute of Bioscience, Universiti Putra Malaysia (UPM), 43400, Serdang, Selangor, Malaysia

    Ina Salwany Md Yasin & Mohammad Noor Amal Azmai

Authors
  1. Abdulwakil Olawale Saba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ina Salwany Md Yasin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammad Noor Amal Azmai
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Abdulwakil Olawale Saba: Conceptualization, Methodology, Data curation, Writing- Original draft preparation. Ina Salwany Md Yasin: Conceptualization, Writing- Reviewing and Editing. Mohammad Noor Amal Azmai: Conceptualization, Methodology, Writing- Reviewing and Editing.

Corresponding author

Correspondence to Abdulwakil Olawale Saba.

Ethics declarations

Ethical approval

This review and meta-analysis is based on publicly available information and requires no form of ethical approval.

Competing interests

The authors declare the absence of any competing interests or personal connections that could potentially affect the results presented in the paper.

Additional information

Handling Editor: Gavin Burnell

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 30 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saba, A.O., Yasin, I.S.M. & Azmai, M.N.A. Meta-analyses indicate that dietary probiotics significantly improve growth, immune response, and disease resistance in tilapia. Aquacult Int (2024). https://doi.org/10.1007/s10499-024-01404-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10499-024-01404-8

Keywords

Search

Navigation