Skip to main content
SpringerLink
Log in

Development of pelleted feed containing probiotic Lactobacillus rhamnosus GG and Jerusalem artichoke for Nile Tilapia and its biocompatibility studies

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Growth performance and immune systems of tilapias could be improved by Lactobacillus rhamnosus GG (LGG) and Jerusalem artichoke. This research aimed to determine the effects of Jerusalem artichoke on LGG viability after drying and pelleting and their subsequent exposure to simulated gastrointestinal conditions. Fresh LGG cells were added into wall material solutions, including alginate (AL), alginate + milk powder (AM), and alginate + milk powder + Jerusalem artichoke at different concentrations (AMJ). The solutions were then spray dried to obtain LGG powders. The powder with the highest cell number was then selected to mix with tilapia feed mash and pelleted using a nonthermal feed extruder to obtain pelleted feed containing LGG and Jerusalem artichoke. The LGG viability spray dried powders and pelleted feed were analyzed for their cell counts after drying and after exposure to simulated gastrointestinal conditions. The result showed that the number of viable cells in AMJ was significantly higher than AM and AL after drying. The number of viable cells under both simulated gastric and bile salt fluids was improved with the increasing of Jerusalem artichoke concentrations. The number of viable cells after pelleting process could be maintained. LGG in the pelleted feed could also survive under the simulated gastric and bile salt conditions. The study indicates that JA enhanced LGG viability after drying and exposure to simulated gastrointestinal conditions. The pelleted feed containing LGG and Jerusalem artichoke could be applied in tilapia farming, providing convenience to the farmers, and valuable effects to the fish.

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

Similar content being viewed by others

References

  • Aliyu-A A, Aliyu-Paiko M, Abafi J, Abdul-Malik A, Adamu K, King M (2019) Fermentation of feed ingredients as potential strategy to improve health status and reduce opportunistic pathogens in fish farming. Asian J Biotechnol Bioresour Technol 5:1–17

    Google Scholar 

  • Alvarado-Reveles O, Fernández-Michel S, Jiménez-Flores R, Cueto-Wong C, Vázquez-Moreno L, Montfort GR-C (2019) Survival and goat milk acidifying activity of Lactobacillus rhamnosus GG encapsulated with agave fructans in a buttermilk protein matrix. Probiotics Antimicro 11(4):1340–1347. https://doi.org/10.1007/s12602-018-9475-y

    Article  CAS  Google Scholar 

  • Amal M, Zamri-Saad M (2011) Streptococcosis in tilapia (Oreochromis niloticus): a review. Pertanika J Trop Agric Sci 34(2):195–206

    Google Scholar 

  • Anal AK, Singh H (2007) Recent advances in microencapsulation of probiotics for industrial applications and targeted delivery. Trends Food Sci Technol 18(5):240–251

    Article  CAS  Google Scholar 

  • Atia A, Gomaa A, Fliss I, Beyssac E, Garrait G, Subirade M (2016) A prebiotic matrix for encapsulation of probiotics: physicochemical and microbiological study. J Microencapsul 33(1):89–101. https://doi.org/10.3109/02652048.2015.1134688

    Article  CAS  PubMed  Google Scholar 

  • Bhujel RC (2013) On-farm feed management practices for nile tilapia (Oreochromis niloticus) in thailand, On-farm feeding and feed management in aquaculture. FAO Fisheries and Aquaculture Technical Paper No. 038, Rome, Italy.

  • Boonanuntanasarn S, Tiengtam N, Pitaksong T, Piromyou P, Teaumroong N (2018) Effects of dietary inulin and jerusalem artichoke (Helianthus tuberosus) on intestinal microbiota community and morphology of nile tilapia (Oreochromis niloticus) fingerlings. Aquac Nutr 24(2):712–722

    Article  CAS  Google Scholar 

  • Bustos AY, de Valdez GF, Fadda S, Taranto MP (2018) New insights into bacterial bile resistance mechanisms: the role of bile salt hydrolase and its impact on human health. Food Res Int 112:250–262

    Article  CAS  Google Scholar 

  • Cook MT, Tzortzis G, Charalampopoulos D, Khutoryanskiy VV (2012) Microencapsulation of probiotics for gastrointestinal delivery. J Control Release 162(1):56–67

    Article  CAS  Google Scholar 

  • Denev S, Beev G, Staykov Y, Moutafchieva R (2009) Microbial ecology of the gastrointestinal tract of fish and the potential application of probiotics and prebiotics in finfish aquaculture. Int Aquat Res 1(1):1–29

    Google Scholar 

  • Doherty S, Gee V, Ross R, Stanton C, Fitzgerald G, Brodkorb A (2011) Development and characterisation of whey protein micro-beads as potential matrices for probiotic protection. Food Hydrocoll 25(6):1604–1617

    Article  CAS  Google Scholar 

  • FAO (2020) The state of world fisheries and aquaculture 2020. Sustainability in action. FAO, Rome, Italy. http://www.fao.org/documents/card/en/c/ca9229en/. Accessed 24 April 2021.

  • Gibson GR, Probert HM, Van Loo J, Rastall RA, Roberfroid MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17(2):259–275

    Article  CAS  Google Scholar 

  • Govind B, Nithyalakshmi V (2011) Influence of prebiotic composition on probiotic survivability in calcium alginate coated synbiotic microcapsules at thermal incubation. Agric Res J 6(5):231–236

    Google Scholar 

  • Hirano J, Yoshida T, Sugiyama T, Koide N, Mori I, Yokochi T (2003) The effect of Lactobacillus rhamnosus on enterohemorrhagic Escherichia coli infection of human intestinal cells in vitro. Med Microbiol 47(6):405–409

    CAS  Google Scholar 

  • Khuenpet K, Jittanit W, Sirisansaneeyakul S, Srichamnong W (2017) Inulin powder production from Jerusalem artichoke (Helianthus tuberosus l.) tuber powder and its application to commercial food products. J Food Process Preserv 41(4):e13097

    Article  Google Scholar 

  • Klahan R, Areechon N, Yoonpundh R, Engkagul A (2009) Characterization and activity of digestive enzymes in different sizes of nile tilapia (Oreochromis niloticus l.). Agric Nat Resour 43(1):143–153

    Google Scholar 

  • Krasaekoopt W, Watcharapoka S (2014) Effect of addition of inulin and galactooligosaccharide on the survival of microencapsulated probiotics in alginate beads coated with chitosan in simulated digestive system, yogurt and fruit juice. LWT 57(2):761–766. https://doi.org/10.1016/j.lwt.2014.01.037

    Article  CAS  Google Scholar 

  • Li L, Wang R, Liang W, Gan X, Huang T, Huang Y, Li J, Shi Y, Chen M, Luo H (2013) Rare serotype occurrence and pfge genotypic diversity of Streptococcus agalactiae isolated from tilapia in china. Vet Microbiol 167(3):719–724. https://doi.org/10.1016/j.vetmic.2013.09.001

    Article  CAS  PubMed  Google Scholar 

  • Lund P, Tramonti A, De Biase D (2014) Coping with low ph: Molecular strategies in neutralophilic bacteria. FEMS Microbiol Rev 38(6):1091–1125. https://doi.org/10.1111/1574-6976.12076

    Article  CAS  PubMed  Google Scholar 

  • Maciel G, Chaves K, Grosso C, Gigante M (2014) Microencapsulation of Lactobacillus acidophilus LA-5 by spray-drying using sweet whey and skim milk as encapsulating materials. J Dairy Sci 97(4):1991–1998

    Article  CAS  Google Scholar 

  • Mille Y, Obert JP, Beney L, Gervais P (2004) New drying process for lactic bacteria based on their dehydration behavior in liquid medium. Biotechnol Bioeng 88(1):71–76

    Article  CAS  Google Scholar 

  • Misra S, Pandey P, Mishra HN (2021) Novel approaches for co-encapsulation of probiotic bacteria with bioactive compounds, their health benefits and functional food product development: a review. Trends Food Sci Technol 109:340–351. https://doi.org/10.1016/j.tifs.2021.01.039

    Article  CAS  Google Scholar 

  • Morrison CM, Wright JR Jr (1999) A study of the histology of the digestive tract of the nile tilapia. J Fish Biol 54(3):597–606. https://doi.org/10.1111/j.1095-8649.1999.tb00638.x

    Article  Google Scholar 

  • Mouriño J, Do Nascimento Vieira F, Jatobá A, Da Silva B, Jesus G, Seiffert W, Martins M (2012) Effect of dietary supplementation of inulin and w. Cibaria on haemato-immunological parameters of hybrid surubim (Pseudoplatystoma sp). Aquac Nutr 18(1):73–80

    Article  Google Scholar 

  • Neira I, Engle CR, Ngugi C (2009) Economic and risk analysis of tilapia production in kenya. J Appl Aquac 21(2):73–95. https://doi.org/10.1080/10454430902892842

    Article  Google Scholar 

  • Phrompanya P, Saenphet K, Saenphet S (2019) Comparative histochemical study of the gastrointestinal tracts of the nile tilapia (Oreochromis niloticus) and the hybrid catfish (clarias batrachus x clarias gariepinus). Acta Histochem 121(3):261–267. https://doi.org/10.1016/j.acthis.2019.01.003

    Article  CAS  PubMed  Google Scholar 

  • Pirarat N, Pinpimai K, Rodkhum C, Chansue N, Ooi EL, Katagiri T, Maita M (2015) Viability and morphological evaluation of alginate-encapsulated Lactobacillus rhamnosus GG under simulated tilapia gastrointestinal conditions and its effect on growth performance, intestinal morphology and protection against streptococcus agalactiae. Anim Feed Sci Technol 207:93–103. https://doi.org/10.1016/j.anifeedsci.2015.03.002

    Article  CAS  Google Scholar 

  • Rezvankhah A, Emam-Djomeh Z, Askari G (2020) Encapsulation and delivery of bioactive compounds using spray and freeze-drying techniques: a review. Dry Technol 38(1–2):235–258. https://doi.org/10.1080/07373937.2019.1653906

    Article  CAS  Google Scholar 

  • Rodrigues FJ, Cedran MF, Bicas JL, Sato HH (2020) Encapsulated probiotic cells: Relevant techniques, natural sources as encapsulating materials and food applications—a narrative review. Food Res Int 137:109682. https://doi.org/10.1016/j.foodres.2020.109682

    Article  CAS  PubMed  Google Scholar 

  • Romano N, Mobili P, Zuñiga-Hansen ME, Gómez-Zavaglia A (2018) Physico-chemical and structural properties of crystalline inulin explain the stability of Lactobacillus plantarum during spray-drying and storage. Food Res Int 113:167–174. https://doi.org/10.1016/j.foodres.2018.07.007

    Article  CAS  PubMed  Google Scholar 

  • Shah NP (2000) Probiotic bacteria: selective enumeration and survival in dairy foods. J Dairy Sci 83(4):894–907. https://doi.org/10.3168/jds.S0022-0302(00)74953-8

    Article  CAS  PubMed  Google Scholar 

  • Sirimanapong W, Thompson KD, Shinn AP, Adams A, Withyachumnarnkul B (2018) Streptococcus agalactiae infection kills red tilapia with chronic francisella noatunensis infection more rapidly than the fish without the infection. Fish Shellfish Immunol 81:221–232. https://doi.org/10.1016/j.fsi.2018.07.022

    Article  PubMed  Google Scholar 

  • Sivakumar K, Rama MS, Janani R, Muthupriya P, Magesh R (2020) Effect of probiotic dietary on growth performances and feed utilization of cyprinus carpio fingerlings. Bull Pure Appl Sci Zool 39(2):463

    Article  Google Scholar 

  • Smith BJ, Smith SA, Tengjaroenkul B, Lawrence TA (2000) Gross morphology and topography of the adult intestinal tract of the tilapian fish (Oreochromis niloticus). Cells Tissues Organs 166(3):294–303. https://doi.org/10.1159/000016743

    Article  CAS  PubMed  Google Scholar 

  • Su Y, Zheng X, Zhao Q, Fu N, Xiong H, Wu WD, Chen XD (2019) Spray drying of Lactobacillus rhamnosus GG with calcium-containing protectant for enhanced viability. Powder Technol 358:87–94. https://doi.org/10.1016/j.powtec.2018.09.082

    Article  CAS  Google Scholar 

  • Tiengtam N, Paengkoum P, Sirivoharn S, Phonsiri K, Boonanuntanasarn S (2017) The effects of dietary inulin and Jerusalem artichoke (Helianthus tuberosus) tuber on the growth performance, haematological, blood chemical and immune parameters of nile tilapia (Oreochromis niloticus) fingerlings. Aquac Res 48(10):5280–5288

    Article  CAS  Google Scholar 

  • Wang J, Huang S, Fu N, Jeantet R, Chen XD (2016a) Thermal aggregation of calcium-fortified skim milk enhances probiotic protection during convective droplet drying. J Agric Food Chem 64(30):6003–6010

    Article  CAS  Google Scholar 

  • Wang L, Yu X, Xu H, Aguilar ZP, Wei H (2016b) Effect of skim milk coated inulin-alginate encapsulation beads on viability and gene expression of Lactobacillus plantarum during freeze-drying. LWT 68:8–13. https://doi.org/10.1016/j.lwt.2015.12.001

    Article  CAS  Google Scholar 

  • Xavier dos Santos D, Casazza AA, Aliakbarian B, Bedani R, Saad SMI, Perego P (2019) Improved probiotic survival to in vitro gastrointestinal stress in a mousse containing Lactobacillus acidophilus LA-5 microencapsulated with inulin by spray drying. LWT 99:404–410. https://doi.org/10.1016/j.lwt.2018.10.010

    Article  CAS  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(3–4):283–292

    Article  Google Scholar 

  • Yi M, Wang M, Li Z, Liu Z, Song C, Zhang D, Gao F, Ke X, Cao J, Lu M (2019) An investigation into the effects of streptococcus agalactiae on the 5-ht system and the behavior of gift tilapia (oreochromis niloticus). Aquac Rep 15:100232. https://doi.org/10.1016/j.aqrep.2019.100232

    Article  Google Scholar 

  • Ying D, Schwander S, Weerakkody R, Sanguansri L, Gantenbein-Demarchi C, Augustin MA (2013) Microencapsulated lactobacillus rhamnosus gg in whey protein and resistant starch matrices: Probiotic survival in fruit juice. J Funct Foods 5(1):98–105. https://doi.org/10.1016/j.jff.2012.08.009

    Article  CAS  Google Scholar 

  • Yuan Y, Yuan Y, Dai Y, Gong Y (2017) Economic profitability of tilapia farming in china. Aquac Int 25(3):1253–1264. https://doi.org/10.1007/s10499-017-0111-8

    Article  Google Scholar 

  • Zheng X, Fu N, Huang S, Jeantet R, Chen XD (2016) Exploring the protective effects of calcium-containing carrier against drying-induced cellular injuries of probiotics using single droplet drying technique. Food Res Int 90:226–234

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by Thailand Research Fund (MRG6080108).

Author information

Authors and Affiliations

  1. Division of Biology, Faculty of Science and Technology, Rajamangala University of Technology Thanyaburi, Pathum Thani, 12110, Thailand

    Unchaleeporn Sribounoy

  2. Department of Pathology, Faculty of Veterinary Science, Chulalongkorn University, Bangkok, 10330, Thailand

    Nopadon Pirarat

  3. Department of Food Science and Technology, The University of Georgia, Griffin, GA, 30223, USA

    Kevin Mis Solval

  4. School of Nutrition and Food Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA, 70803, USA

    Subramaniam Sathivel

  5. Division of Food Science and Technology Management, Faculty of Science and Technology, Rajamangala University of Technology Thanyaburi, Pathum Thani, 12110, Thailand

    Arranee Chotiko

Authors
  1. Unchaleeporn Sribounoy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nopadon Pirarat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kevin Mis Solval
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Subramaniam Sathivel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arranee Chotiko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arranee Chotiko.

Ethics declarations

Conflict of interest

The authors declared that there were no potential conflicts of interest with respect to authorship or research publication of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sribounoy, U., Pirarat, N., Solval, K.M. et al. Development of pelleted feed containing probiotic Lactobacillus rhamnosus GG and Jerusalem artichoke for Nile Tilapia and its biocompatibility studies. 3 Biotech 11, 279 (2021). https://doi.org/10.1007/s13205-021-02829-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-021-02829-1

Keywords

Search

Navigation