Skip to main content
SpringerLink
Log in

The immune modulatory effect of oregano (Origanum vulgare L.) essential oil on Tilapia zillii following intraperitoneal infection with Vibrio anguillarum

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

The current study aimed to evaluate the possible effect of Origanum essential oil on innate immune parameters as well as the hematological profiles of Tilapia zillii following challenge with Vibrio anguillarum. Fifty-four of Tilapia zillii weighing 180 ± 10.2 g were randomly distributed into three identical closed recirculating seawater systems. The study included three groups (G1, G2, and G3) repeated in triplicates. Fish of the first two groups were fed on a basal diet without herbs, whereas fish of the last group were fed on a basal diet supplemented with Origanum essential oil at concentration 1 g kg−1 for 15 days. Subsequently, fish of G2 and G3 subjected to a peritoneal inflammation by intraperitoneally injecting V. anguillarum (5.5 × 105 CFU mL−1), whereas fish of G1 injected with saline and served as control. Fish of all groups were then sampled at 4, 12, and 24 h post injection. No mortalities were observed in both basal and Origanum fed groups. However, some specimens of fish fed basal diet showed dorsal fin erosions, eroded mouth, and detached skin. Although the kinetics of RBCs, WBCs, Hb, and differential leukocyte values remained unchanged in fish fed different diets at the beginning of the trial, significant increases in those values were observed in fish fed Origanum essential oil at 12 and 24 h post injection. Similarly, an augmentation of plasma proteases, antiproteases, and lysozyme activities were recorded in fish fed Origanum essential oil at the same particular sampling points. A significant enhancement in plasma bactericidal capacity was only recorded in fish fed Origanum essential oil at 12 and 24 h post challenge compared to those fed basal diet. In conclusion, Origanum essential oil had a pronounced influence on the innate immunity and increased the fish resistance to V. anguillarum. These data gave insight into the potential use of Origanum in prophylactic strategies against threatening pathogens.

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

Similar content being viewed by others

References

  • Adam K, Sivropoulou A, Kokkini S, Lanaras T, Arsenakis M (1998) Antifungal activities of Origanum vulgare subsp. hirtum, Mentha spicata, Lavandula angustifolia, and Salvia fruticosa essential oils against human pathogenic fungi. J Agric Food Chem 46:1739–1745

    Article  CAS  Google Scholar 

  • Afonso A, Lousada S, Silva J, Ellis AE, Silva MT (1998) Neutrophil and macrophage responses to inflammation in the peritoneal cavity of rainbow trout Oncorhynchus mykiss. A light and electron microscopic cytochemical study. Dis Aquat Org 34:27–37

    Article  PubMed  CAS  Google Scholar 

  • Alcaide E (2003) Numerical taxonomy of Vibrionaceae isolated from cultured amberjack (Serioladumerili) and surrounding water. Curr Microbiol 46:184–189

    Article  PubMed  CAS  Google Scholar 

  • Aligiannis N, Kalpoutzakis E, Mitaku S, Chinou IB (2001) Composition and antimicrobial activity of the essential oils of two Origanum spp. J Agric Food Chem 49:4168–4170

    Article  PubMed  CAS  Google Scholar 

  • Athanassopoulou F, Yiagnisis M, Bitchava K (2010) Use of oregano essential oil for the control of parasite and microbial diseases of Mediterranean fish. Proceedings of the WAVMA International Aquatic Veterinary Conference Page 13 of 52

  • Avci H, Lu SB, Cagirgan H (2012) Pathological and immunohistochemical investigations in rainbow trout (Oncorhynchus mykiss Walbaum, 1792) experimentally infected with Vibrio anguillarum. Rev Med Vet 163:31–39

    Google Scholar 

  • Balfry SK, Shariff M, Iwama GK (1997) Strain differences in non-specific immunity of tilapia Oreochromis niloticus following challenge with Vibrio parahaemolyticus. Dis Aquat Org 30:77–80

    Article  Google Scholar 

  • Barton GM (2008) A calculated response: control of inflammation by the innate immune system. J Clin Invest 118:413–420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Baumann P, Furniss AL (1994) Vibrionaceae. In: Hensel WR (ed) Bergey’s manual of determinative bacteriology. William and Wilkins, Baltimore

    Google Scholar 

  • Bayne CJ, Gerwick L (2001) The acute phase response and innate immunity of fish. Dev Comp Immunol 25:725–743

    Article  PubMed  CAS  Google Scholar 

  • Botsoglou NA, Florou-Paneri P, Christaki E, Fletouris DJ, Spais AB (2002) Effect of dietary oregano essential oil on performance of chickens and on iron-induced lipid oxidation of breast, thigh and abdominal fat tissues. Br Poult Sci 43:223–230

    Article  PubMed  CAS  Google Scholar 

  • Chelladurai G, Veni T, Mohanraj J, Nagarajan R (2014) Effect of herbal extracts supplemented diets on non-specific immunity and resistance to Aeromonas hydrophila in Indian catfish (Mystus montanus). J Zool Biosci Res 1:10–14

    Google Scholar 

  • Ching CYY (2008) Improving aquaculture production through better health and disease prevention the natural way. Feed Tech Up 3:4–10

    Google Scholar 

  • Costas B, Rêgo PCNP, Simões I, Marques JF, Castro-Cunha M, Afonso A (2013) Cellular and humoral immune responses of Senegalese sole, Solea senegalensis (Kaup), following challenge with two Photobacterium damselae subsp. piscicida strains from different geographical origins. J Fish Dis 36:543–553

    Article  PubMed  CAS  Google Scholar 

  • Davison W, Franklin CE, Mckenzie JC, Carey PW (1993) The effects of chronic exposure to the water soluble fraction of fuel oil on an Antarctic fish Pagothenia borchgkevinki. Comp Biochem Physiol C Comp Pharmacol 104:67–70

    Article  Google Scholar 

  • Diler O, Gormez O, Diler I, Metin S (2016) Effect of oregano (Origanum onites L.) essential oil on growth, lysozyme and antioxidant activity and resistance against Lactococcus garvieae in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquac Nutr doi: https://doi.org/10.1111/anu.12451

  • Drăgan SR, Gergen II, Socaciu C (2008) Alimentaţia funcţională cu componente bioactive naturale în sindromul metabolic. Eurostampa p, 200-202,160–161, 314

  • Eissa IAM, Aly SM, Derwa HI, Fawzy A (2017) Studies on vibriosis among some marine fishes in Lake Temsah. SCVMJ XXII:1–18

    Google Scholar 

  • Ekici S, Diler O, Didinen BI, Kubilay A (2011) Antibacterial effect of some medicinal plant essential oils against bacterial fish pathogens. Kafkas Univ Vet Fac Res 17:47–54

    Google Scholar 

  • Ellis AE (1999) Immunity to bacteria in fish. Fish Shellfish Immunol 9:291–308

    Article  Google Scholar 

  • Fagbenro OA (2001) Feedstuff digestibility in culturable freshwater fish species in Nigeria. Proceedings of the First National Symposium on Fish Nutrition and Fish Feed Technology in Nigeria, pp.26–37 (A.A. Eyo, ed.). Fisheries Society of Nigeria (FISON) and Nigerian Institute for Oceanography and Marine Research (NIOMR), Lagos, Nigeria

  • FAO (2014) The state of world fisheries and aquaculture in opportunities and challenges, F.a.A.O.o.t.U. Nations, Editor Rome p. 223

  • Galina J, Yin G, Ardó L, Jeney Z (2009) The use of immunostimulating herbs in fish. An overview of research. Fish Physiol Biochem 35:669–676

    Article  PubMed  CAS  Google Scholar 

  • Garcia F, Pilarski F, Onaka EM, Moraes FR, Martins ML (2007) Hematology of Piaractus mesopotamicus fed diets supplemented with vitamins C and E, challenged by Aeromonas hydrophila. Aquaculture 271:39–46

    Article  CAS  Google Scholar 

  • Gonzalez SF, Osorio CR, Santos Y (2003) Development of a PCR-based method for the detection of Listonella anguillarum in fish tissues and blood samples. Dis Aquat Org 55:109–115

    Article  PubMed  CAS  Google Scholar 

  • Gopalakannan A, Arul V (2006) Immunomodulatory effects of dietary intake of chitin, chitosan and levamisole on the immune system of Cyprinus carpio and control of Aeromonas hydrophila infection in ponds. Aquaculture 255:179–187

    Article  CAS  Google Scholar 

  • Grimble RF (2009) Basics in clinical nutrition: immune nutrition—nutrients which influence immunity: effect and mechanism of action. E Spen Eur E J Clin Nutr Metab 4:10–13

    Article  Google Scholar 

  • Harikrishnan R, Balasundaram C, Heo MS (2011) Impact of plant products on innate and adaptive immune system of cultured finfish. Aquaculture 317:1–15

    Article  CAS  Google Scholar 

  • Harikrishnan R, Balasundaram C, Heo MS (2012) Effect of Inonotus obliquus enriched diet on hematology, immune response, and disease protection in kelp grouper, Epinephelus bruneus against Vibrio harveyi. Aquaculture 344:48–53

    Article  CAS  Google Scholar 

  • Harikrishnan R, Nisha Rani M, 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 

  • Helander IM, Alakomi HL, Latva-Kala K, Mattila-Sandholm T, Pol I, Smid EJ, Von Gorris LGM, Wright A (1998) Characterization of the action of selected essential oil components on Gram-negative bacteria. J Agric Food Chem 46:3590–3595

    Article  CAS  Google Scholar 

  • Karousou R, Kokkini S (2003) The genus Origanum (Labiatae) in Crete: distribution and essential oils. Bocconea 16:717–721

    Google Scholar 

  • Karpouhtsis I, Pardali E, Feggou E, Kokkini S, Scouras ZG, Mavragani-Tsipidou P (1998) Insecticidal and genotoxic activities of oregano essential oils. J Agric Food Chem 46:1111–1115

    Article  CAS  Google Scholar 

  • Kocić-Tanackov SD, Dimić GR, Tanackov IJ, Pejin DJ, Mojović LV, Pejin JD (2012) Antifungal activity of oregano (Origanum vulgare L.) extract on the growth of Fusarium and Penicillium species isolated from food. HEM IND 66:33–41

    Article  CAS  Google Scholar 

  • Lamas J, Santos Y, Bruno DW, Toranzo AE, Anadon R (1994) Non-specific cellular responses of rainbow trout Vibrio anguillarum and its extracellular products. J Fish Biol 45:839–854

    Article  Google Scholar 

  • Lambert RJW, Skandamis PN, Coote PJ, Nychas GJE (2001) A study of the minimum inhibitory concentration and mode of action of oregano essential oil, thymol and carvacrol. J Appl Microbiol 91:453–462

    Article  PubMed  CAS  Google Scholar 

  • Lee KK, Liu PC, Chuang WH (2002) Pathogenesis of gastroenteritis caused by Vibrio carchariae in cultured marine fish. J Mar Biotechnol 4:267–277

    Article  CAS  Google Scholar 

  • Li P, Yin YL, Li D, Kim SW, Wu GY (2007) Amino acids and immune function. Br J Nutr 98:237–252

    Article  PubMed  CAS  Google Scholar 

  • Machado M, Azeredo R, Díaz-Rosales P, Afonso A, Peres H, Oliva-Teles A, Costas B (2015) Dietary tryptophan and methionine as modulators of European seabass (Dicentrarchus labrax) immune status and inflammatory response. Fish Shellfish Immunol 42:353–362

    Article  PubMed  CAS  Google Scholar 

  • Muona M, Soivio A (1992) Changes in plasma lysozyme and blood leucocyte levels of hatchery-reared Atlantic salmon (Salmo salar L.) and sea trout (Salmo trutta L.) during parr-smolt transformation. Aquaculture 106:75–87

    Article  CAS  Google Scholar 

  • Neumann NF, Stafford JL, Barreda D, Ainsworth AJ, Belosevic M (2001) Antimicrobial mechanisms of fish phagocytes and their role in host defense. Dev Comp Immunol 25:807–825

    Article  PubMed  CAS  Google Scholar 

  • NRC (1993) Nutrient requirements of fish, National Research Council Washington, DC pp. 114

  • Pourmoghim H, Haghighi M, Rohani MS (2015) Effect of dietary inclusion of Origanum vulgare extract on non-specific immune responses and hematological parameters of rainbow trout (Oncorhynchus mykiss). BEPLS 4:33–39

    Google Scholar 

  • Ran C, Hu J, Liu W, Liu Z, He S, Dan BCT, Diem NN, Ooi EL, Zhou Z (2016) Thymol and carvacrol affect hybrid tilapia through the combination of direct stimulation and an intestinal microbiota-mediated effect: insights from a germ-free zebrafish model–3. J Nutr 146:1132–1140

    Article  PubMed  CAS  Google Scholar 

  • Rattanachaikunsopond P, Phumklachor P (2010) Assessment of synergistic efficacy of carvacrol and cymene against Edwardsiella tarda in vitro and in tilapia (Oreochromis niloticus). Afr J Microbiol Res 4:420–425

    Google Scholar 

  • Roofchaee A, Irani M, Ebrahimzadeh MA, Akbari MR (2013) Effect of dietary oregano (Origanium vulgare L.) essential oil on growth performance, cecal microflora and serum antioxidant activity of broiler chickens. Afr J Biotechnol 10:6177–6183

    Google Scholar 

  • Ross NW, Firth KJ, Wang A, Burka JF, Johnson SC (2000) Changes in hydrolytic enzyme activities of naïve Atlantic salmon Salmo salar skin mucus due to infection with the salmon louse Lepeophtheirus salmonis and cortisol implantation. Dis Aquat Org 41:43–51

    Article  PubMed  CAS  Google Scholar 

  • Sahu S, Das BK, Pradhan J, Mohapatra BC, Mishra BK, Sarangi N (2007) Effect of Magnifera indica kernel as a feed additive on immunity and resistance to Aeromonas hydrophila in Labeo rohita fingerlings. Fish Shellfish Immunol 23:109–118

    Article  PubMed  CAS  Google Scholar 

  • Seden MEA, Abbas AE, Ahmed MH (2009) Effect of Origanum vulgare as a feed additive on growth performance, feed utilization and whole body composition of Nile tilapia (Oreochromis niloticus) fingerlings challenged with pathogenic Aeromonas hydrophila. J Agric Sci 34:1683–1695

    Google Scholar 

  • Sivropoulou A, Paranikolaou E, Nikolaou C, Kokkini S, Lanaras T, Arsenakis M (1996) Antimicrobial and cytotoxic activities of Origanum essential oils. J Agric Food Chem 44:1202–1205

    Article  CAS  Google Scholar 

  • Swain P, Dash S, Sahoo PK, Routray P, Sahoo SK, Gupta SD, Meher PK et al (2007) Non-specific immune parameters of brood Indian major carp Labeo rohita and their seasonal variations. Fish Shellfish Immunol 22:38–43

    Article  PubMed  CAS  Google Scholar 

  • Vaseeharan B, Thaya R (2014) Medicinal plant derivatives as immunostimulants: an alternative to chemotherapeutics and antibiotics in aquaculture. Aquac Int 22:1079–1091

    Article  CAS  Google Scholar 

  • Volpatti D, Chiara B, Francesca T, Marco G (2013) Growth parameters, innate immune response and resistance to Listonella anguillarum of D. labrax fed carvacrol supplemented diets. Aquac Res 45:31–44

    Article  CAS  Google Scholar 

  • Wu YR, Gong QF, Fang H, Liang WW, Chen M, He RJ (2013) Effect of Sophora flavescens on non-specific immune response of tilapia (GIFT Oreochromis niloticus) and disease resistance against Streptococcus agalactiae. Fish Shellfish Immunol 34:220–227

    Article  PubMed  CAS  Google Scholar 

  • Yildirim P, Kubilay A, Guney S (2013) In vitro antibacterial activity of some medicinal plants oil against fish pathogens Lactococcus garvieae and Vibrio anguillarum. Yunus Araştırma Bülteni 3:33–37

    Google Scholar 

  • Yilmaz E, Ergün S (2015) Influence of carvacrol on the growth performance, hematological, non-specific immune and serum biochemistry parameters in rainbow trout (Oncorhynchus mykiss). Food Nutr Sci 6:523–531

    CAS  Google Scholar 

  • Yin G, Jeney G, Racz T, Xu P, Jun X, Jeney Z (2006) Effect of two Chinese herbs (Astragalus radix and Scutellaria radix) on non-specific immune response of tilapia, Oreochromis niloticus. Aquaculture 253:39–47

    Article  Google Scholar 

  • Zhang J, Liu X (2002) Study on tetrazolium salt colorimetric assay for growth and survival of bacteria. Wei sheng yan Jiu= J Hyg Res 31:361–363

    Google Scholar 

  • Zheng ZL, Tan JYW, Liu HY, Zhou XH, Xiang X, Wang KY (2009) Evaluation of oregano essential oil (Origanum heracleoticum L.) on growth, antioxidant effect and resistance against Aeromonas hydrophila in channel catfish (Ictalurus punctatus). Aquaculture 292:214–218

    Article  CAS  Google Scholar 

  • Zuo X, Woo PTK (1997) In vivo neutralization of Cryptobia salmositica metallo-protease by α2-macroglobulin in the blood of rainbow trout Oncorhynchus mykiss and in brook charr Salvelinus fontinalis. Dis Aquat Org 29:67–72

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Fish Diseases and Management, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, Egypt

    Mahmoud Abd Elaziz Mabrok

  2. Department of Bacteriology, Immunology and Mycology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, Egypt

    Ali Wahdan

Authors
  1. Mahmoud Abd Elaziz Mabrok
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali Wahdan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mahmoud Abd Elaziz Mabrok.

Ethics declarations

Ethical approval

All the animals were maintained in accordance with the National and International Institutional Guidelines for the Care and Use of Animals for Scientific purposes.

Competing interests

The authors declare that they have no competing interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mabrok, M.A.E., Wahdan, A. The immune modulatory effect of oregano (Origanum vulgare L.) essential oil on Tilapia zillii following intraperitoneal infection with Vibrio anguillarum. Aquacult Int 26, 1147–1160 (2018). https://doi.org/10.1007/s10499-018-0274-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-018-0274-y

Keywords

Search

Navigation