Skip to main content
Log in

Ziziphus mauritiana supplementation of Nile tilapia (Oreochromis niloticus) diet for improvement of immune response to Aeromonas hydrophila infection

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

This study evaluated the effectiveness of dietary Ziziphus mauritiana leaf powder (ZLP) to control Aeromonas hydrophila infection in Nile tilapia and reduce damage to vital immune organs. Four experimental groups were fed a diet supplemented with ZLP at concentrations of 0, 5, 10, and 20 g/kg (w/w) for 6 weeks. At the end of the feeding trial, all groups were intraperitoneally injected with pathogenic A. hydrophila. It was found that Z. mauritiana significantly (P < 0.05) upregulated (lysozyme, interleukin 1 beta) and superoxide dismutase gene expressions as well as improved the activity of serum lysozyme and liver antioxidant enzymes. The fish that were fed a ZLP-supplemented diet also exhibited significantly higher survival rates after A. hydrophila challenge than those that were fed a ZLP-free diet (P < 0.05). Supplementation of 10 g/kg ZLP most effectively reduced the histopathological alterations caused by A. hydrophila challenge in the liver, spleen, kidney, and muscle of the fish. In conclusion, ZLP can be effective in controlling A. hydrophila infection in Nile tilapia (particularly at a concentration of 10 g/kg) through enhancement of its immune and antioxidant status.

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

Access this article

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
Fig. 9

Similar content being viewed by others

References

  • Abd El-Gawad EA, El Asely AM, Soror EI, Abbass AA, Austin B (2020) Effect of dietary Moringa oleifera leaf on the immune response and control of Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus) fry. Aquac Int 28(1):389–402. https://doi.org/10.1007/s10499-019-00469-0

    Article  CAS  Google Scholar 

  • Abdallah EM, Elsharkawy ER, Ed-dra A (2016) Biological activities of methanolic leaf extract of Ziziphus mauritiana. Biosci Biotech Res Comm 9(4):605–614

    Article  Google Scholar 

  • Abdulameer YS, Husain F, Al-cekal SHA (2017) Efficacy of Ziziphus mauritiana leaves extract as antibiotic alternatives in broiler chicken. J Entomol Zool Studies 5(5):742–746

    Google Scholar 

  • Ahmadifar E, Sheikhzadeh N, Roshanaei K, Dargahid N, Faggio C (2019) Can dietary ginger (Zingiber officinale) alter biochemical and immunological parameters and gene expression related to growth, immunity and antioxidant system in zebrafish (Danio rerio)? Aquaculture 507:341–348. https://doi.org/10.1016/j.aquaculture.2019.04.049

    Article  CAS  Google Scholar 

  • AL-Marzooq MA (2014) Phenolic compounds of Napek leave (Ziziphus spina-christi L.) as natural antioxidants. J Food Nutr Sci 2(5):207–214

    CAS  Google Scholar 

  • Amin A, El Asely A, Abd El-Naby AS, Samir F, El-Ashram A, Sudhakaran R, Dawood MAO (2019) Growth performance, intestinal histomorphology and growth-related gene expression in response to dietary Ziziphus mauritiana in Nile tilapia (Oreochromis niloticus). Aquaculture 512:734301. https://doi.org/10.1016/j.aquaculture.2019.734301

    Article  CAS  Google Scholar 

  • AOAC (1990) The Official Methods of Analyses Association of Official Analytical Chemists International (15th edition), Association of Official Analytical Chemists, Arlington, VA, 2220, USA

  • Ardo’ L, Yin G, Xu P, Var’adi L, Szigeti G, Jeney Z, Jeney G (2008) Chinese herbs (Astragalus membranaceus and Lonicera japonica) and boron enhance the non-specific immune response of Nile tilapia (Oreochromis niloticus) and resistance against Aeromonas hydrophila. Aquaculture 275:26–33. https://doi.org/10.1016/j.aquaculture.2007.12.022

    Article  CAS  Google Scholar 

  • Awad E, Awaad AS (2017) Role of medicinal plants on growth performance and immune status in fish. Fish Shellfish Immunol 67:40–54. https://doi.org/10.1016/j.fsi.2017

    Article  CAS  PubMed  Google Scholar 

  • Awad E, Awaad AS, Esteban MA (2015) Effects of dihydroquercetin obtained from deodar (Cedrus deodara) on immune status of gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 43:43–50. https://doi.org/10.1016/j.fsi.2014.12.009

    Article  CAS  PubMed  Google Scholar 

  • Awad E, Austin D, Lyndon A, Awaad A (2019) Possible effect of hala extract (Pandanus tectorius) on immune status, anti-tumour and resistance to Yersinia ruckeri infection in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immun 87:620–626. https://doi.org/10.1016/j.fsi.2019.02.012

    Article  CAS  Google Scholar 

  • Bancroft J, Stevens A, Turner D (1996) Theory and practice of histological techniques, 4th edn. Churchill Living Stone, New York

    Google Scholar 

  • Barreto RE, Gontijo AMMC, Alves-de-Lima RO, Raymundi VC, Pinhal D, Reyes et al (2007) MS222 does not induce primary DNA damage in fish. Aquac Int 15:163–168. https://doi.org/10.1007/s10499-007-9073-6

    Article  CAS  Google Scholar 

  • Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 1999:25–34

    Article  Google Scholar 

  • Brunetti C, Di Ferdinando M, Fini A, Pollastri S, Tattini M (2013) Flavonoids as antioxidants and developmental regulators: relative significance in plants and humans. Int J Mol Sci 14:3540–3555. https://doi.org/10.3390/ijms14023540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camargo MMP, Martinez CBR (2007) Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotropic Ichthyol 5:327–336. https://doi.org/10.1590/S1679-62252007000300013

    Article  Google Scholar 

  • Chatterjee A, Roy D, Patnaik E, Nongthomba U (2016) Muscles provide protection during microbial infection by activating innate immune response pathways in Drosophila and zebrafish. Dis Model Mech 9:697–705. https://doi.org/10.1242/dmm.022665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cipriano RC, Bullock GL, Pyle SW (1984) Aeromonas hydrophila and motile Aeromonad septicemias of fish. United States Fish and Wildlife Service, Washington, DC

    Google Scholar 

  • Dawood MA, Koshio S, Esteban MÁ (2018a) Beneficial roles of feed additives as immunostimulants in aquaculture: a review. Rev Aquac 10(4):950–974. https://doi.org/10.1111/raq.12209

    Article  Google Scholar 

  • Dawood MA, Koshio S, Abdel-Daim MM, Van Doan H (2018b) Probiotic application for sustainable aquaculture. Rev Aquac 11(3):907–924. https://doi.org/10.1111/raq.12272

    Article  Google Scholar 

  • Dawood MA, Magouz FI, Salem MF, Abdel-Daim HA (2019a) Modulation of digestive enzyme activity, blood health, oxidative responses and growth-related gene expression in GIFT by heat-killed Lactobacillus plantarum (L-137). Aquaculture 505:127–136. https://doi.org/10.1016/j.aquaculture.2019.02.053

    Article  CAS  Google Scholar 

  • Dawood MA, Eweedah NM, Moustafa Moustafa E, Shahin MG (2019b) Effects of feeding regimen of dietary Aspergillus oryzae on the growth performance, intestinal morphometry and blood profile of Nile tilapia (Oreochromis niloticus). Aquac Nutr 25:1063–1072. https://doi.org/10.1111/anu.12923

    Article  CAS  Google Scholar 

  • Dkhil MA, Kassab RB, Al-Quraishy S, Abdel-Daim MM, Zrieq R, Abdel Moneim AE (2018) Ziziphus spina-christi (L.) leaf extract alleviates myocardial and renal dysfunction associated with sepsis in mice. Biomed Pharmacother 102:64–75. https://doi.org/10.1016/j.biopha.2018.03.032

    Article  CAS  PubMed  Google Scholar 

  • El Asely AM, Amin RA, El-Habashi NM (2012) Effect of dietary administration of Echinacea purpurea on immune responses, histopathological alteration and microbial safety in Nile tilapia (Oreochromis niloticus) infected with Aeromonas hydrophila. Proceedings of the 5th Global Fisheries and Aquaculture Research Conference. Giza: Faculty of Agriculture, Cairo University, 2012:100-114

  • El Asely AM, Abbass AA, Austin B (2014) Honey bee pollen improves growth, immunity and protection of Nile tilapia (Oreochromis niloticus) against infection with Aeromonas hydrophila. Fish Shellfish Immun 40(2):500–506. https://doi.org/10.1016/j.fsi.2014.07.017

    Article  CAS  Google Scholar 

  • Elaloui M, Laamouri A, Ennajah A, Cerny M, Mathieu C, Vilarem G, Chaar H, Hasnaoui B (2016) Phytoconstituents of leaf extracts of Ziziphus jujuba Mill. plants harvested in Tunisia. Ind Crop Prod 83:133–139. https://doi.org/10.1016/j.indcrop.2015.11.029

    Article  CAS  Google Scholar 

  • Engstad RE, Robertsen B, Frivold E (1992) Yeast glucan induces increase in lysozyme and complement-mediated haemolytic activity in Atlantic salmon blood. Fish Shellfish Immunol 2:287–297. https://doi.org/10.1016/S1050-4648(06)80033-1

    Article  Google Scholar 

  • Fernandes DC, Eto SF, Funnicelli MIG, Fernandes CC, Charlie-Silva I, Belo MAA, Pizauro JM (2019) Immunoglobulin Y in the diagnosis of Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus). Aquaculture 500:576–585. https://doi.org/10.1016/j.aquaculture.2018.10.045

    Article  CAS  Google Scholar 

  • Gabriel NN, Qiang J, Ma XY, He J, Xu P, Liu K (2015) Dietary Aloe vera improves plasma lipid profile, antioxidant, and hepatoprotective enzyme activities in GIFT-tilapia (Oreochromis niloticus) after Streptococcus iniae challenge. Fish Physiol Biochem 41:1321–1332. https://doi.org/10.1007/s10695-015-0088-z

    Article  CAS  PubMed  Google Scholar 

  • Gobi N, Ramya C, Vaseeharan, Malaikozhundan B, Vijayakumar SK, Murugan G, Benelli (2016) Oreochromis mossambicus diet supplementation with Psidium guajava leaf extracts enhance growth, immune, antioxidant response and resistance to Aeromonas hydrophila. Fish Shellfish Immunol 58:572–583. https://doi.org/10.1016/j.fsi.2016.09.062

    Article  CAS  PubMed  Google Scholar 

  • Gröner F, Ziková A, Kloas W (2015) Effects of the pharmaceuticals diclofenac and metoprolol on gene expression levels of enzymes of biotransformation, excretion pathways and estrogenicity in primary hepatocytes of Nile tilapia (Oreochromis niloticus). Comp Biochem Physiol C 167:51–57. https://doi.org/10.1016/j.cbpc.2014.09.003

    Article  CAS  Google Scholar 

  • Hassaan MS, Mohammady EY, Soaudy MR, El-Garhy HAS, Moustafa MMA, Mohamed SA, El-Haroun ER (2019) Effect of Silybum marianum seeds as a feed additive on growth performance, serum biochemical indices, antioxidant status, and gene expression of Nile tilapia, Oreochromis niloticus (L.) fingerlings. Aquaculture 509:178–187

    Article  CAS  Google Scholar 

  • Hoseinifar SH, Khodadadian Zou H, Paknejad H, Ahmadifar E, Van Doan H (2018) Non-specific immune responses and intestinal immunity of common carp (Cyprinus carpio) fed Jujube (Ziziphus jujube) fruit extract. Aquac Res 49(9):2995–3003. https://doi.org/10.1111/are.13759

    Article  CAS  Google Scholar 

  • Jiang WD, Hu K, Liu Y, Jiang J, Wu P, Zhao J, Zhang YA, Zhou XQ, Feng L (2016) Dietary myo-inositol modulates immunity through antioxidant activity and the Nrf2 and E2F4/cyclin signalling factors in the head kidney and spleen following infection of juvenile fish with Aeromonas hydrophila. Fish Shellfish Immun 49:374–386

    Article  CAS  Google Scholar 

  • Kumar A, Sharma B, Pandey (2012) Assessment of stress in effect to pyrethroid insecticides, λcyhalothrin and cypermethrin, in a freshwater fish, channa punctatus (bloch). Cell Mol Biol 58(1):153–159

    PubMed  Google Scholar 

  • Lie Ø, Evensen Ø, SØrensen A, FrØysadal E (1989) Study on lysozyme activity in some fish species. Dis Aquat Org 6:1–5

    Article  CAS  Google Scholar 

  • Magrone T, Fontana S, Laforgia F, Dragone T, Jirillo E, Passantino L (2016) Administration of a polyphenol-enriched feed to farmed sea bass (Dicentrarchus labrax L.) modulates intestinal and spleen immune responses. Oxidative Med Cell Longev 2016:28–31. https://doi.org/10.1155/2016/2827567

    Article  CAS  Google Scholar 

  • Milla S, Mathieu C, Wang N, Lambert S, Nadzialek S, Massart S, Henrotte E, Douxfils J, Mélard C, Mandiki SN, Kestemont P (2010) Spleen immune status is affected after acute handling stress but not regulated by cortisol in Eurasian perch, Perca fluviatilis. Fish Shellfish Immunol 28(5–6):931–941. https://doi.org/10.1016/j.fsi.2010.02.012

    Article  CAS  PubMed  Google Scholar 

  • Murray AG, Munro LA (2018) The growth of Scottish salmon (Salmo salar) aquaculture 1979–2016 fits a simple two-phase logistic population model. Aquaculture 496:146–152. https://doi.org/10.1016/j.aquaculture.2018.07.023

    Article  Google Scholar 

  • Negm IM, EL Asely AM, Abbass AA (2016) Influence of dietary ginger (Zingiber officinale) on haemato-biochemical parameters, spleen histopathological changes and resistance of Oreochromis niloticus fingerlings to Aeromonas hydrophila infection. Egyptian J Aquacult 6(1):25–45

    Article  Google Scholar 

  • Ostaszewska T, Dabrowski K, Hliwa P, Gomółka P, Kwasek K (2008) Nutritional regulation of intestine morphology in larval cyprinid fish, silver bream (Vimba vimba). Aquac Res 39:1268–1278. https://doi.org/10.1111/j.1365-2109.2008.01989.x

    Article  Google Scholar 

  • Owatari MS, Alves Jesus GF, Brum A, Pereira SA, Lehmann NB, de Pádua PU et al (2018) Sylimarin as hepatic protector and immunomodulator in Nile tilapia during Streptococcus agalactiae infection. Fish Shellfish Immunol 8:565–572. https://doi.org/10.1016/j.fsi.2018.08.061

    Article  CAS  Google Scholar 

  • Preeti T, Shalini T (2014) Ziziphus jujuba: a phytopharmacological review. Int J Res Dev Pharm Life Sci 3:959–966

    CAS  Google Scholar 

  • Rajasekaran S, Ravi K, Sivagnanam K, Subramanian S (2005) Antioxidant effect of Aloevera gel extract in streptozotocin-induced diabetes in rats. Pharmarcoll Report 57:90–96

    Google Scholar 

  • Sarhadi I, Alizadeh E, Ahmadifar E, Adineh H, Dawood MA (2020) Skin mucosal, serum immunity and antioxidant capacity of common carp (Cyprinus carpio) fed artemisia (Artemisia annua). Ann Animal Sci

  • Smith P (2012) 7-Antibiotics in aquaculture: reducing their use and maintaining their efficacy. In: Austin B (ed) Infectious disease in aquaculture. Woodhead Publishing, pp 161–189. https://doi.org/10.1533/9780857095732.2.161

  • Srikanth K, Pereira E, Duarte AC, Ahmad I (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish-a review. Environ Sci Pollut Res 20:2133–2149. https://doi.org/10.1007/s11356-012-1459-y

    Article  CAS  Google Scholar 

  • Steinel NC, Bolnick DI (2017) Melanomacrophage centers as a histological indicator of immune function in fish and other Poikilotherms. Front Immunol 8:827. https://doi.org/10.3389/fimmu.2017.00827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tkachenko H, Kurhaluk N, Andriichuk A, Gasiuk E, Beschasniu S (2014) Oxidative stress biomarkers in liver of sea trout (Salmo trutta m. trutta L.) affected by ulcerative dermal necrosis syndrome. Turk J Fish Aquat Sci 14:391–402. https://doi.org/10.4194/1303-2712-v14_2_09

    Article  Google Scholar 

  • Valenzuela CA, Zuloaga R, Poblete-Morales M, Vera-Tobar T, Mercado L, Avendano-Herrera R, Valdes JA, Molina A (2017) Fish skeletal muscle tissue is an important focus of immune reactions during pathogen infection. Dev Comp Immunol 73:1–9. https://doi.org/10.1016/j.dci.2017.03.004

    Article  CAS  PubMed  Google Scholar 

  • Van Hai N (2015) The use of medicinal plants as immunostimulants in aquaculture. Aquaculture 446:88–96. https://doi.org/10.1016/j.aquaculture.2015.03.014

    Article  CAS  Google Scholar 

  • Wang Y, Branicky R, Noë A, Hekimi S (2018) Superoxide dismutases: dual roles in controlling ROS damage and regulating ROS signaling. J Cell Biol 217(6):1915–1928. https://doi.org/10.1083/jcb.201708007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yengkhom O, Shalini K, Subramani S, Subramani PA, Michael RD (2019) Stimulation of non-specific immunity, gene expression, and disease resistance in Nile Tilapia, Oreochromis niloticus (Linnaeus, 1758), by the methanolic extract of the marine macroalga, Caulerpa scalpelliformis. Vet World 12(2):271–276

    Article  CAS  Google Scholar 

  • Yilmaz E (2019) Effects of dietary anthocyanin on innate immune parameters, gene expression responses, and ammonia resistance of Nile tilapia (Oreochromis niloticus). Fish Shellfish Immune 93:694–702. https://doi.org/10.1016/j.fsi.2019.08.033

    Article  CAS  Google Scholar 

  • Yostawonkul J, Kitiyodom S, Kaewmalun S, Suktham K, Nittayasut N, Khongkow M, Namdee K, Ruktanonchai UR, Rodkhum C, Pirarat N, Surassmo S, Yata T (2019) Bifunctional clove oil nanoparticles for anesthesia and anti-bacterial activity in Nile tilapia (Oreochromis niloticus). Aquaculture 503:589–595. https://doi.org/10.1016/j.aquaculture.2018.12.058

    Article  CAS  Google Scholar 

  • Zahran E, Abd El-Gawad EA, Engy R (2018) Dietary Withania sominefera root confers protective and immunotherapeutic effects against Aeromonas hydrophila infection in Nile tilapia (Oreochromis niloticus). Fish Shellfish Immun 80:641–650. https://doi.org/10.1016/j.fsi.2018.06.009

    Article  CAS  Google Scholar 

  • Zapata A, Diez B, Cejalvo T, Gutierrez-de Frias C, Cortes A (2006) Ontogeny of the immune system of fish. Fish Shellfish Immunol 20:126–136. https://doi.org/10.1016/j.fsi.2004.09.005

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mahmoud A. O. Dawood.

Ethics declarations

Ethical statement

The experimental design was approved by the Central Laboratory for Aquaculture Research (CLAR), Abassa, Egypt (Approval no. 43429), and all procedures followed the guidelines for the care and use of fish.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

El Asely, A., Amin, A., Abd El-Naby, A.S. et al. Ziziphus mauritiana supplementation of Nile tilapia (Oreochromis niloticus) diet for improvement of immune response to Aeromonas hydrophila infection. Fish Physiol Biochem 46, 1561–1575 (2020). https://doi.org/10.1007/s10695-020-00812-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00812-w

Keywords

Navigation