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Natural products as functional food ingredients for Nile tilapia challenged with Aeromonas hydrophila

Abstract

Functional foods employ ingredients whose purpose is not necessarily to supply a possible nutritional deficiency, but rather to offer benefits to human and animal health. In this context, the present study aimed to investigate the use of oregano essential oil (OEO) and ethanolic extract of propolis (EEP) as functional foods for Nile tilapia challenged with Aeromonas hydrophila. Healthy fingerlings (7.67 ± 0.86 g of mean initial weight) distributed in 60-L aquariums were used in the experiment, maintaining good water quality. The treatments consisted of 2.22 g of EEP kg feed−1 (treatment 2), 0.5% OEO feed−1 (treatment 3), and one control feed (treatment 1), with seven replications. After 30 days of feeding, the animals were subjected to sanitary challenges and observed for 15 days. Zootechnical, survival, and immunological parameters were analyzed, and the variability of intestinal microorganisms was evaluated through denaturing gradient gel electrophoresis (DGGE). The results of this study showed that tilapia fed with feed containing OEO or EEP significantly improved growth parameters compared with the control group, obtaining respective mean values for the control treatment, EEP and OEO: final weight (20.38 ± 1.6b; 23.15 ± 2.07a; 24.31 ± 1.43a), weight gain (12.66 ± 1.67b; 15.5 ± 2.04a; 16.65 ± 1.45a), and body condition (1.66 ± 0.06b; 1.8 ± 0.12a; 1.82 ± 0.11 The). In addition, the addition of OEO effectively improved carcass traits as well as apparent feed conversion (1.91 ± 0.19b; 1.69 ± 0.22ab; 1.45 ± 0.22a) and feed efficiency (0.56 ± 0.05b; 0.63 ± 0.07ab; 0.73 ± 0.13a) compared with the control group (P < 0.05). The two natural additives showed no significant effect on fish immunity, survival parameters after challenge, and hepatosomatic index. However, they presented an effect as growth promoters and on the intestinal microbiome; in the latter, there was an increase in diversity when compared with the control group. It may be concluded that OEO and EEP natural additives can act as growth promoters.

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Abbreviations

CEUA:

Ethics Committee on Animal Use

CIRPA:

Integrated Center for Fishery Resources and Aquaculture

EEP:

Ethanolic extract of propolis

OEO:

Oregano essential oil

References

  1. Abdel-Latif HM, Khalil RH (2014) Evaluation of two phytobiotics, Spirulina platensis and Origanum vulgare extract on growth, serum antioxidant activities and resistance of Nile tilapia (Oreochromis niloticus) to pathogenic Vibrio alginolyticus. Int J Fish Aquat Stud 1:250–255

  2. Abd-El-Rhman AM (2009) Antagonism of Aeromonas hydrophila by propolis and its effect on the performance of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 27(3):454–459

  3. Açıkgöz Z, Yücel B, Altan Ö (2005) The effects of propolis supplementation on broiler performance and feed digestibility. Arch Geflügelk 69(3):117–122

  4. Amarante F (2011) A composição química e atividade antimicrobiana do estrato etanólico de própolis frente a isolados de Staphylococcus spp., obtidos de mastite bovina. Dissertation, Universidade Federal do Vale do São Francisco

  5. Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils–a review. Food Chem Toxicol 46(2):446–475

  6. Balcázar JL, De Blas I, Ruiz-Zarzuela I, Cunningham D, Vendrell D, Múzquiz JL (2006) The role of probiotics in aquaculture. Vet Microbiol 114(3–4):173–186

  7. Bampidis VA, Christodoulou V, Florou-Paneri P, Christaki E, Chatzopoulou PS, Tsiligianni T, Spais AB (2005) Effect of dietary dried oregano leaves on growth performance, carcase characteristics and serum cholesterol of female early maturing turkeys. Br Poult Sci 46(5):595–601

  8. Barbosa MH, Bonato Zuffi F, Maruxo HB, Ruyz Jorge LL (2009) Ação terapêutica da própolis em lesões cutâneas. Acta paul enferm, 22(3)

  9. Busatta C, Mossi AJ, Rodrigues MRA, Cansian RL, Oliveira JVD (2007) Evaluation of Origanum vulgare essential oil as antimicrobial agent in sausage. Braz J Microbiol 38(4):610–616

  10. Canbolat O, Karabulut A (2010) Effect of urea and oregano oil supplementation on growth performance and carcass characteristics of lamb fed diets containing different amounts of energy and protein. Turk J Vet Anim Sci 34(2):119–128

  11. Cascón A, Yugueros J, Temprano A, Sánchez M, Hernanz C, Luengo JM, Naharro G (2000) A major secreted elastase is essential for pathogenicity of Aeromonas hydrophila. Infect Immun 68(6):3233–3241

  12. Chu WH (2006) Adjuvant effect of propolis on immunisation by inactivated Aeromonas hydrophila in carp (Carassius auratus gibelio). Fish Shellfish Immunol 21(1):113–117

  13. Citarasu T (2010) Herbal biomedicines: a new opportunity for aquaculture industry. Aquac Int 18(3):403–414

  14. Costa AB (2003) Caracterização de bactérias do complexo Aeromonas isoladas de peixes de água doce e sua atividade patogênica. Thesis, Universidade de São Paulo

  15. Costa MM, Oliveira STL, Balen RE, Bueno Junior G, Baldan LT, Silva LCR, Santos LD (2013) Brown seaweed meal to Nile tilapia fingerlings. Arch Zootec 62(237):101–109

  16. Deng J, An Q, Bi B, Wang Q, Kong L, Tao L, Zhang X (2011) Effect of ethanolic extract of propolis on growth performance and plasma biochemical parameters of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 37(4):959–967

  17. Denli M, Cankaya S, Silici S, Okan F, Uluocak AN (2005) Effect of dietary addition of Turkish propolis on the growth performance, carcass characteristics and serum variables of quail (Coturnix coturnix japonica). Asian Australas J Anim Sci 18(6):848–854

  18. Ekren S, Yerlikaya O, Tokul HE, Akpınar A, Accedil M (2013) Chemical composition, antimicrobial activity and antioxidant capacity of some medicinal and aromatic plant extracts. Afr J Microbiol Res 7(5):383–388

  19. Ellis AE (1990) Lysozyme assays. Tech fish immunol 1:101–103

  20. Ferreira PMF, da Silva NL, Coelho Dias D, da Veiga Moreira DM, Lúcia SA, de Freitas D, Sampaio Zuanon JA (2014) Essential oregano oil as a growth promoter for the yellowtail tetra, Astyanax altiparanae. J World Aquacult Soc 45(1):28–34

  21. Ferreira PM, Caldas DW, Salaro AL, Sartori SS, Oliveira JM, Cardoso AJ, Zuanon JA (2016) Intestinal and liver morphometry of the yellow tail tetra (Astyanax altiparanae) fed with oregano oil. An Acad Bras Cienc 88(2):911–922

  22. Food and Agriculture Organization of the United Nations – FAO (2010) El estado mundial de la pesca y la acuicultura. Roma: Subdivisión de Políticas y Apoyo en Materia de Publicación Electrónica. Rome

  23. Fracalossi DM, Cyrino JEP (2013) Nutriaqua: nutrição e alimentação de espécies de interesse para a aquicultura brasileira. Florianópolis, SC: Sociedade Brasileira de Aquicultura e Biologia Aquática

  24. Ghatak S, Agarwal RK, Bhilegaonkar KN (2007) Species identification of clinically important Aeromonas spp. by restriction fragment length polymorphism of 16S rDNA. Lett Appl Microbiol 44(5):550–554

  25. Guardabassi L, Jensen LB, Kruse H (2009) Guia de antimicrobianos em veterinária. Artmed Editora

  26. Hong JC, Steiner T, Aufy A, Lien TF (2012) Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers. Livest Sci 144(3):253–262

  27. IBGE – Instituto Brasileiro de Geografia e Estatística. (2016) Pesquisa pecuária municipal. Rio de Janeiro: IBGE, 2016.

  28. Kashkooli OB, Dorcheh EE, Mahboobi-Soofiani N, Samie A (2011) Long-term effects of propolis on serum biochemical parameters of rainbow trout (Oncorhynchus mykiss). Ecotoxicol Environ Saf 74(3):315–318

  29. Keya Sen (2005) Development of a rapid identification method for species by multiplex-PCR. Can J Microbiol 51(11):957–966

  30. Kubitza F (2003) Qualidade da água no cultivo de peixes e camarões. Gráfica Editora Degaspari, Jundiaí

  31. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RT, Bøgwald J, Ringø E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquacult 302(1–2):1–18

  32. Meurer F, Matiuzzi da Costa M, De Barros DAD, de Oliveira LTS, Paixão D, Santana P (2009) Brown propolis extract in feed as a growth promoter of Nile tilapia (Oreochromis niloticus, Linnaeus 1758) fingerlings. Aquac Res 40(5):603–608

  33. Obach A, Quentel C, Baudin Laurencin F (1993) Effects of alpha-tocopherol and dietary oxidized fish oil on the immune response of sea bass Dicentrarchus labrax. Dis Aquat Org 15:175–185

  34. Plumb JA, Hanson LA (2011) Health maintenance and principal microbial diseases of cultured fishes. John Wiley & Sons

  35. 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). Bull Env Pharmacol Life Sci 4:33–39

  36. Purohit MK, Singh SP (2009) Assessment of various methods for extraction of metagenomic DNA from saline habitats of coastal Gujarat (India) to explore molecular diversity. Lett Appl Microbiol 49(3):338–344

  37. Quinn PJ, Carter ME, Markey B, Carter GR (1994) Clinical veterinary medicine. Mosby-Year ed, London, p 648

  38. Ramos AFN, Miranda JD (2007) Propolis: a review of its anti-inflammatory and healing actions. J Venom Anim Toxins incl Trop Dis 13(4):697–710

  39. Rostagno HS, Albino LFT, Donzele JL, Gomes PC, Oliveira RD, Lopes DC, Euclides RF (2005) Composição de alimentos e exigências nutricionais. Tabelas brasileiras para aves e suínos, 2

  40. Santos PG, Santos PA, Bello AR, Freitas-Almeida AC (2011) Association of Aeromonas caviae polar and lateral flagella with biofilm formation. Lett Appl Microbiol 52(1):49–55

  41. Sen K (2005) Development of a rapid identification method for Aeromonas species by multiplex-PCR. Can J Microbiol 51(11):957–966

  42. Talas ZS, Gulhan MF (2009) Effects of various propolis concentrations on biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss). Ecotoxicol Environ Saf 72(7):1994–1998

  43. Tsadik GG, Bart AN (2007) Effects of feeding, stocking density and water-flow rate on fecundity, spawning frequency and egg quality of Nile tilapia, Oreochromis niloticus (L.). Aquaculture 272(1–4):380–388

  44. Tukmechi A, Karimi Rad F, Farrokhi F, Agh N, Jalili R (2014) The effects of short-and long-term diet supplementation with Iranian propolis on the growth and immunity in rainbow trout (Oncorhynchus mykiss). Iran J Vet Res 15(3):250–255

  45. Velotto S, Vitale C, Varricchio E, Crasto A (2011) Effect of propolis on the fish muscular development and histomorphometrical characteristics. Acta Vet Brno 79(4):543–550

  46. Viana PV (2013) Atividade antifúngica do óleo essencial de Origanum vulgare (orégano) sobre fungos oportunistas do gênero Fusarium. Dissertation, Universidade Federal da Paraíba

  47. Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J, Pérez-Álvarez JA (2008) Functional properties of honey, propolis, and royal jelly. J Food Sci 73(9)

  48. Wafaa E, Doaa I, El-Murr A, Rania M (2014) Effects of dietary inclusion of black cumin seeds, green tea and propolis extraction growth parameters, body composition and economic efficiency of Nile tilapia, Oreochromis niloticus. World J Fish Mar Sci 6:447–452

  49. Yonar ME, Yonar SM, Silici S (2011) Protective effect of propolis against oxidative stress and immunosuppression induced by oxytetracycline in rainbow trout (Oncorhynchus mykiss, W.). Fish Shellfish Immunol 31(2):318–325

  50. Zhang G, Gong S, Yu D, Yuan H (2009) Propolis and Herba Epimedii extracts enhance the non-specific immune response and disease resistance of Chinese sucker, Myxocyprinus asiaticus. Fish Shellfish Immunol 26(3):467–472

  51. Zheng ZL, Tan JY, 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(3–4):214–218

  52. Zheng Z, Yingeng W, Qingyin W, Nannan D, Meijie L, Jiangbo Q, Lan W (2012) Study on the immune enhancement of different immunoadjuvants used in the pentavalent vaccine for turbots. Fish Shellfish Immunol 32(3):391–395

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Author information

Correspondence to Gisele Veneroni Gouveia.

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The authors declare that they have no conflict of interest.

Ethical approval

The present experiment was conducted according to protocol no. 0006/160812, approved by the Ethics Committee on Animal Use of the Federal University of São Francisco Valley - CEUA/UNIVASF, January 2013.

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de Oliveira, S.T.L., Soares, R.A.N., de Negreiros Sousa, S.M. et al. Natural products as functional food ingredients for Nile tilapia challenged with Aeromonas hydrophila. Aquacult Int (2020) doi:10.1007/s10499-019-00503-1

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Keywords

  • Bacterial challenge
  • Extract of propolis
  • Fish farming
  • Feed additives
  • Microbiome
  • Oregano essential oil