Abstract
The objective of this work was to develop a food additive for the sex reversal of Nile tilapia (Oreochromis niloticus) based on a simple oil in water (O/W) nanoemulsion with testosterone propionate for incorporation into commercial feed. Oil screening and evaluation of the organoleptic and physicochemical characteristics were carried out to determine the best formulation. A palatability test was also performed. Sex reversal test was assayed using 5 experimental groups: negative control — macerated feed without hormone; free testosterone — macerated feed with 60 mg/kg of testosterone propionate diluted in ethanol; and macerated feed with testosterone propionate nanoemulsion at a concentration of 30, 60, and 90 mg/kg. Stable nanoemulsions (size 76–210 nm) with testosterone propionate were produced. All nanoemulsion-added feed was palatable to tilapia. We obtained sex reversal values of ≈65, 75, and 72% in the groups of 30, 60, and 90 mg/kg, respectively. We can conclude that the nanoemulsion showed promising results; it is capable of inducing sex reversal in tilapia, is suitable as a commercial product, and has the potential to promote safety for rural staff and reduce the environmental impact of hormones.
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The data and material used in this study are available from the corresponding author on request.
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References
Abo-Al-Ela HG (2018) Hormones and fish monosex farming: a spotlight on immunity. Fish Shellfish Immunol 72:23–30. https://doi.org/10.1016/j.fsi.2017.10.038
Anton N, Vandamme TE (2011) Nano-emulsions and micro-emulsions: clarifications of the critical differences. Pharm Res 28:978–985. https://doi.org/10.1007/s11095-010-0309-1
ANVISA. Agência Nacional de Vigilância Sanitária. Guia de estabilidade de produtos cosméticos (2004) Brasília: ANVISA, 52p
Caddeo C, Teskac K, Sinico C, Kristl J (2008) Effect of resveratrol incorporated in liposomes on proliferation and UV-B protection of cells. Int J Pharm 363(1–2):183–191. https://doi.org/10.1016/j.ijpharm.2008.07.024
Cadena PG, Pereira MA, Cordeiro RBS, Cavalcanti IMF, Barros Neto B, Pimentel MCCB, Lima Filho JL, Silva VL, Santos-Magalhães NS (2013) Nanoencapsulation of quercetin and resveratrol into elastic liposomes. Biochim Biophys Acta-Biomembr 1828:309–316. https://doi.org/10.1016/j.bbamem.2012.10.022
Celik I, Guner Y, Celik P (2011) Effect of orally-administered 17α-methyltestosterone at different doses on the sex reversal of Nile tilapia (Oreochromis niloticus, Linnaeus 1758). J Anim Vet Adv 10(7):853–857. https://doi.org/10.3923/javaa.2011.853.857
Damasceno GAB, Silva RMAC, Fernandes Otrosky EA, Langassner SMZ, Ferrari M (2016) Use of Opuntia ficus-indica (L.) Mill extracts from Brazilian Caatinga as an alternative of natural moisturizer in cosmetic formulations. Braz. J Pharm Sci 52(3):459–470. https://doi.org/10.1590/S1984-82502016000300012
Danaei M, Dehghankhold M, Ataei S, Davarani FH, Javanmard R, Dokhani A, Khorasani S, Mozafari MR (2018) Impact of particle size and polydispersity index on the clinical applications of lipidic nanocarrier systems. Pharmaceutics 10(2):57. https://doi.org/10.3390/pharmaceutics10020057
Dar AH, Rashid N, Majid I, Hussain S, Dar MA (2019) Nanotechnology interventions in aquaculture and seafood preservation. Crit Rev Food 60(3):1–10. https://doi.org/10.1080/10408398.2019.1617232
Dergal NB, Scippo ML, Degand G, Gennotte V, Mélard C, Abi-Ayad SE (2016) Monitoring of 17α-methyltestosterone residues in tilapia’s (Oreochromis niloticus) flesh and experimental water after its sex reversal. Int J Biosci 9(6):101–113. https://doi.org/10.12692/ijb/9.6.101-113
El-Ekiaby WT (2019) Basil oil nanoemulsion formulation and its antimicrobial activity against fish pathogen and enhance disease resistance against Aeromonas hydrophila in cultured Nile tilapia. Egypt J Aquat Res 9(4):13–33. https://doi.org/10.21608/EJA.2019.18567.1007
Essa EA, Elebyary TT, Abdelquader MM, El-Maghraby GM, Elkordy AA (2021) Smart liquids for oral controlled drug release: an overview of alginate and non-alginate based systems. J Drug Deliv Sci Technol 61:102211. https://doi.org/10.1016/j.jddst.2020.102211
FAO - Organização das Nações Unidas para a Agricultura e Alimentação. Cultured Aquatic Species Information Programme Oreochromis niloticus (Linnaeus, 1758) (2019). Publishing FAO.org. https://www.fao.org/fishery/affris/species-profiles/nile-tilapia/nile-tilapia-home/en/. Acessed 10 October 2019
Frange RCC, Garcia MTJ (2009) Desenvolvimento de emulsões óleo de oliva/água: avaliação da estabilidade física. Rev Ciênc Farm Básica Apl, 30(3): 263–271. ISSN 1808–4532
Fujimura K, Okada N (2007) Development of the embryo, larva and early juvenile of Nile tilapia Oreochromis niloticus (Pisces: Cichlidae). Developmental Staging System. Develop Growth Differ 49:301–324. https://doi.org/10.1111/j.1440-169X.2007.00926.x
Golan M, Levavi-Silvan B (2014) Artificial masculinization in tilapia involves androgen receptor activation. Gen Comp Endocrinol 207:50–55. https://doi.org/10.1016/j.ygcen.2014.04.026
Grisham DR, Nanda V (2020) Zeta potential prediction from protein structure in general aqueous electrolyte solutions. Langmuir 36:13799–13803. https://doi.org/10.1021/acs.langmuir.0c02031
Habibah AN, Sharifia AR, Wesselsa S, Wiltingb J, Hoerstgen-Schwarka G, Holtza W (2021) Growth and gonadal development of female Nile tilapia (Oreochromis niloticus) exposed to sex reversing thermal treatment. Aquaculture 531:735865. https://doi.org/10.1016/j.aquaculture.2020.735865
Hansen KMS, Andersen HR (2012) Energy effectiveness of direct UV and UV/H2O2 treatment of estrogenic chemicals in biologically treated sewage. Int J Photoenergy, 1 – 9. https://doi.org/10.1155/2012/270320
ICH. (2003) “Stability testing of new drug substances” from https://www.ema.europa.eu/en/ich-q1a-r2-stability-testing-new-drug-substances-drug-products. Accessed 5 Aug 2022
Joshi HD, Tiwari VK, Gupta S, Sharma R, Lakra WS, Sahoo U (2019) Application of nanotechnology for the production of masculinized tilapia, Oreochromis niloticus (Linnaeus, 1758). Aquaculture 511:1921–1925. https://doi.org/10.1016/j.aquaculture.2019.734206
Jung J, Kang J, Choi J, WooPark J (2020) Chronic toxicity of endocrine disrupting chemicals used in plastic products in Korean resident species: implications for aquatic ecological risk assessment. Ecotoxicol Environ Saf, 192. https://doi.org/10.1016/j.ecoenv.2020.110309
Kubtza F (2006) Questões freqüentes dos produtores sobre a qualidade dos alevinos de tilapia, Publishing Panorama Aquicultura. https://panoramadaaquicultura.com.br/questoes-frequentes-dos-produtores-sobre-a-qualidade-dos-alevinos-de-tilapia/. Acessed 20 July 2021
LENS.ORG (2021) Publishing lens.org. http://www.lens.org, Acessed 15 June 2021
Macintosh DJ, Little DC (1995) Nile tilapia (Oreochromis niloticus). In: BROMAGE, N.R.; ROBERTS, R.J. (Ed.). Broodstock management and egg and larval quality. Oxford: Blackwell Science p. 277–320
Ministério da Agricultura, Pecuária e Abastecimento – MAPA (2006) “Normativa N°49, 22 dez de 2006” from: https://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=visualizarAtoPortalMapa&chave=643062246. Accessed 15 Sept 2019.
McClements DJ, Jafari SM (2018). General aspects of nanoemulsions and their formulation. Nanoemulsions. Nanoemulsins: Formulation, Applications, and Characterization (Ed.), 3–20
PEIXE BR (2021). “Anuário PEIXE BR da Piscicultura” - Associação Brasileira de Piscicultura from https://www.peixebr.com.br/anuario-2021/. Accessed 20 Feb 2022.
Pereira MA, Rebouças JS, Ferraz-Carvalho RS, Redín II, Guerra PV, Gamazo C, Brodskyn CI, Irache JM, Santos-Magalhães NS (2018) Poly (anhydride) nanoparticles containing cashew nut proteins can induce a strong Th1 and Treg imune response after oral administration. Eur J Pharm Biopharm 127:51–60. https://doi.org/10.1016/j.ejpb.2018.02.011
Popma TJ, Lovshin L (1996) “Wordwide prospects for commercial production of tilápia” Internacional Center for Aquaculture and Aquatic Environments. from: https://aurora.auburn.edu/handle/11200/4157. Accessed 2 Aug 2022
Riquelme N, Zuniga RN, Arancibia C (2019) Physical stability of nanoemulsions with emulsifier mixtures: replacement of Tween 80 with Quillaja saponin. Food Sci Technol 111:760–766. https://doi.org/10.1016/j.lwt.2019.05.067
Sifakis S, Androutsopoulos VP, Tsatsakis AM, Spandidos DA (2017) Human exposure to endocrine disrupting chemicals: effects on the male and female reproductive systems. Environ Toxicol Pharmacol 51:56–70. https://doi.org/10.1016/j.etap.2017.02.024
Singh A, Castillo HA, Brown J, Kaslin J, Dwyer KM, Gibert Y (2019) High glucose levels affect retinal patterning during zebrafish embryogenesis. Nature 9:4121. https://doi.org/10.1038/s41598-019-41009-3
Swathy JS, Mishra P, Thomas J, Mukherjee A, Chandrasekaran N (2018) Antimicrobial potency of high-energy emulsified black pepper oil nanoemulsion against aquaculture pathogen. Aquaculture 491:210–220. https://doi.org/10.1016/j.aquaculture.2018.03.045
Tao W, Chen J, Tan D, Yang J, Sun L, Wei J, Conte MA, Kocher TD, Wang D (2018) Transcriptome display during tilapia sex determination and differentiation as revealed by RNA-seq analysis. BMC Genomics 19:363. https://doi.org/10.1186/s12864-018-4756-0
Vidal LVO, Albinati RCB, Albinati ACL, Lira AD, Almeida TR, Santos GB (2008) Eugenol como anestésico para a tilápia-do-nilo. Pesqui Agropecu Bras 43:1069–1074. https://doi.org/10.1590/S0100-204X2008000800017
Zanardi MF, Koberstein TCRD, Urbinati EC, Fagundes M, Santos MA, Mataqueiro MI (2011) Concentrações de hormônio na carcaça de tilápias-do-Nilo e maturação precoce após reversão sexual. R Bras Zootec 30(1):7–11. https://doi.org/10.1590/S1516-35982011000100002
Zanoni MA, Leal TV, Caetano Filho M, Oliveira CAL, Ribeiro RP (2013) Inversão sexual de alevinos de tilápias do Nilo (Oreochromis niloticus) variedade Supreme, submetidos a diferentes temperaturas durante fase de diferenciação sexual. Semin Cienc Agrar 34(1):455–466. https://doi.org/10.5433/1679-0359.2013v34n1p455
Acknowledgements
The authors would like to thank the Universidade Federal de Pernambuco for the availability of Laboratórios Associados em Rede de Nanotecnologia (LARNano), and all the members involved in this research.
Funding
The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior — CAPES, for the scholarship to Amanda R. Santos-Magnabosco, Ester I. D. Quinova, and Jadson F. Silva; CNPq (National Council for Scientific and Technological Development) for the PIBITI scholarship for Matheus V. V. Melo and DT-2 productivity scholarship (Process 310401/2017–8) for Pabyton G. Cadena; and Universidade Federal Rural de Pernambuco (Call 015/2018) and Serviço Brasileiro de Apoio às Micro e Pequenas Empresas (SEBRAE) (Catalisa ICT No. 29083*198) for the financial support.
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Details of each author with their contribution in this paper: Amanda Rodrigues dos Santos Magnabosco — conceptualization, methodology, validation, formal analysis, investigation, data curation, writing — original draft, writing — review and editing, and visualization; Ester Inácio Damião Quinova — investigation and data curation; Matheus Victor Viana de Melo — investigation and data curation; Paulo Eduardo da Silva Bastos — investigation; Thamiris Pinheiro Santos — investigation; Ivanildo Inácio da Silva Júnior — investigation; André Lucas Corrêa de Andrade — formal analysis and data curation; Renata Meireles Oliveira Padilha — investigation and writing — original draft; Jadson Freitas da Silva — investigation; Fabrício Bezerra de Sá — investigation; Marília Ribeiro Sales Cadena — supervision, project administration, writing — original draft, and writing — review and editing; and Pabyton Gonçalves Cadena — conceptualization, methodology, validation, formal analysis, resources, data curation, writing — original draft, writing — review and editing, visualization, supervision, project administration, and funding acquisition. All authors read and approved the final manuscript.
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All protocols presented in this study were submitted and approved by the Ethics Committee on the Use of Animals of Universidade Federal Rural de Pernambuco — UFRPE, protocol number 117/2019.
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The research reported in this manuscript is part of a patent (BR102020004629-2) in the course of the process.
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dos Santos Magnabosco, A.R., Quinova, E.I.D., de Melo, M.V.V. et al. Testosterone nanoemulsion produced masculinized Nile tilapia (Oreochromis niloticus). Fish Physiol Biochem 48, 1449–1462 (2022). https://doi.org/10.1007/s10695-022-01156-3
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DOI: https://doi.org/10.1007/s10695-022-01156-3