Skip to main content

Advertisement

Log in

Human food safety and environmental hazards associated with the use of methyltestosterone and other steroids in production of all-male tilapia

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In recent years, all-male cultures of Nile tilapia (Oreochromis niloticus) have been the most preferred mode of production in aquaculture industry. All-male individuals achieve higher somatic growth rate and shut high energy losses associated with gonadal development and reproduction. The economic advantages of culturing all-male tilapia have led to the development of procedures for producing unisex cultures, using 17α-methyltestosterone (MT). Despite widespread use of the MT in tilapia farming, the implications of hormone treatment in relation to human health and the environment have raised a number of concerns in the scientific community. In this review, the hormonal application processes, economic and ecological significance of MT, food safety and residual MT, comparative uses of steroids in aquaculture, animal husbandry, and medicine have been briefly reviewed for regulatory guidelines, and finally, future research perspectives have been addressed. The review can be used as policy-making guidelines in aquaculture framework development as can be emphasized in African continent, among others. The most important conclusion to draw is that the quantity of MT used in conventional practice is large compared to the actual dose required for sex reversal, fish produced are safe for human consumptions, and the environmental hazards should be further emphasized.

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.

Similar content being viewed by others

References

  • Abdelhamid AM, Mehrim AI, Salem FI, Yosuf HAE (2009) All-Male Monosex Nile Tilapia (Oreochromis niloticus), Pros and Cons. Egyp J BasicAppl Sci 8:41–57

    Google Scholar 

  • Arnon S, Dahan O, Elhanany S, Cohen K, Pankratov I, Gross A, Ronen Z, Baram S, Shore LS (2008) Transport of testosterone and estrogen from dairy-farm waste lagoons to groundwater. Environ Sci Technol 42:5521–5526

    Article  CAS  Google Scholar 

  • Bandelj E, van den Heuvel MR, Leusch FDL, Shannon N, Taylor S, McCarthy LH (2006) Determination of the androgenic potency of whole effluents using mosquitofish and trout bioassays. Aquat Toxicol 80:237–248

    Article  CAS  Google Scholar 

  • Barbara LM (2009). Drug-Induced Fish: Hormone Causes Tilapia to Undergo Sex Change. NaturalNews. http://www.naturalnews.com/026006_fish_tilapia_testosterone.html. Accecced 13/01/2015

  • Barber LB, Lee KE, Swackhamer DL, Schoenfuss HL (2007) Reproductive responses of male fathead minnows exposed to wastewater treatment plant effluent, effluent treated with XAD8 resin, and an environmentally relevant mixture of alkylphenol compounds. Aquat Toxicol 82:36–46

    Article  CAS  Google Scholar 

  • Beardmore JA, Mair GC, Lewis RI (2001) Monosex male production in finfish as exemplified by tilapia: applications, problems, and prospects. Aquaculture 197:283–301

    Article  Google Scholar 

  • Bhatti HN, Khera RA (2012) Biological transformations of steroidal compounds: A review. Steroids 77:1267–1290

    Article  CAS  Google Scholar 

  • Bhowmik BB, Sa B, Mukherjee A (2006) Preparation and in-vitro characterization of slow release testosterone nanocapsules in alginates. Acta Pharma Zagreb 56:417

    CAS  Google Scholar 

  • Biswas S, Shapiro C, Kranz W, Mader T, Shelton D, Snow D, Bartelt-Hunt S, Tarkalson D, van Donk S, Zhang T (2013) Current knowledge on the environmental fate, potential impact, and management of growth-promoting steroids used in the US beef cattle industry. J Soil Water Conserv 68:325–336

    Article  Google Scholar 

  • Brown KH, Schultz IR, Cloud J, Nagler JJ (2008) Aneuploid sperm formation in rainbow trout exposed to the environmental estrogen 17α-ethynylestradiol. Proc Natl Acad Sci 105:19786–19791

    Article  CAS  Google Scholar 

  • Cagauan AG, Baleta FN, Abucay JS (2004) Sex reversal of nile tilapia, (Oreochromis niloticus) by egg immersion technique: The effect of hormone concentration and immersion time. Sixth International Symposium on Tilapia in Aquaculture. 12-16 September 2004. Manila, Philippines. pp.127–136

  • Cai K, Phillips DH, Elliott C, Van der Heiden E, Scippo M, Muller M, Connolly L (2010) Removal of Androgens and Estrogens from Water by Reactive Materials. Journal of Water Resource and Protection. 2: 990-993. doi:10.4236/jwarp.2010.211118

  • Carroll ME, Lynch WJ, Roth ME, Morgan AD, Cosgrove KP (2004) Sex and estrogen influence drug abuse. Trends Pharmacol Sci 25:273–279

    Article  CAS  Google Scholar 

  • Casey FX, Hakk H, Šimunek J, Larsen GL (2004) Fate and transport of testosterone in agricultural soils. Environ Sci Technol 38:790–798

    Article  CAS  Google Scholar 

  • Celik I, Guner Y, Celik P (2011) Effect of Orally-Administere d 17α-Methyltestosterone at Different Doses on the Sex Reversal of the Nile Tilapia (Oreochromis niloticus, Linneaus 1758). J Anim Vet Adv 10:853–857

    Article  CAS  Google Scholar 

  • Cepa MMDS, Tavares da Silva EJ, Correia-da-Silva G, Roleira FMF, Teixeira NAA (2008) Synthesis and biochemical studies of 17-substituted androst-3-enes and 3,4-epoxyandrostanes as aromatase inhibitors. Steroids 73:1409–1415

    Article  CAS  Google Scholar 

  • Chakroborty S, Mazumbar D, Chatterji U, Banerjee S (2011) Growth of mixed-sex and monosex Nile tilapia in different culture systems. Turk J Fish Aquat Sci 11:133–140

    Google Scholar 

  • Clemens HP, Inslee T (1968) The Production of Unisexual Broods by Tilapia mossambica Sex-reversed with Methyl Testosterone. Trans Am Fish Soc 97:18–21

    Article  Google Scholar 

  • Cotter AG, Powderly WG (2011) Endocrine complications of human immunodeficiency virus infection: hypogonadism, bone disease and tenofovir-related toxicity. Best Pract Res Clin Endocrinol Metab 25:501–515

    Article  CAS  Google Scholar 

  • Curtis LR, Diren FT, Hurley MD, Seim WK, Tubb RA (1991) Disposition and elimination of 17α-methyltestosterone in Nile tilapia (Oreochromis niloticus). Aquaculture 99:193–201

    Article  CAS  Google Scholar 

  • Dan NC, Little DC (2000) The culture performance of monosex and mixed-sex new-season and overwintered fry in three strains of Nile tilapia (Oreochromis niloticus) in northern Vietnam. Aquaculture 184:221–231

    Article  Google Scholar 

  • de Ziegler D, Fanchin R (2000) Progesterone and progestins: applications in gynecology. Steroids 65:671–679

    Article  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364

    Article  CAS  Google Scholar 

  • El-Greisy ZA, El-Gamal AE (2012) Monosex production of tilapia, (Oreochromis niloticus) using different doses of 17α-methyltestosterone with respect to the degree of sex stability after one year of treatment. Egyp J Aquat Res 38:59–66

    Article  Google Scholar 

  • El-Sayed A-FM, Abdel-Aziz E-SH, Abdel-Ghani HM (2012) Effects of phytoestrogens on sex reversal of Nile tilapia (Oreochromis niloticus) larvae fed diets treated with 17α-Methyltestosterone. Aquaculture 360–361:58–63

    Article  Google Scholar 

  • Falutz J (2011) Growth hormone and HIV infection: Contribution to disease manifestations and clinical implications. Best Pract Res Clin Endocrinol Metab 25:517–529

    Article  CAS  Google Scholar 

  • Gaikowski MP, Mushtaq M, Cassidy P, Meinertz JR, Schleis SM, Sweeney D, Endris RG (2010) Depletion of florfenicol amine, marker residue of florfenicol, from the edible fillet of tilapia (Oreochromis niloticus x O. niloticus and O. niloticus x O. aureus) following florfenicol administration in feed. Aquaculture 301:1–6

    Article  CAS  Google Scholar 

  • Gale WL, Fitzpatrick MS, Lucero M, Contreras-Sánchez WM, Schreck BC (1999) Masculinization of Nile tilapia (Oreochromis niloticus) by immersion in androgens. Aquaculture 178:349–357

    Article  CAS  Google Scholar 

  • Golan M, Levavi-Sivan B (2014) Artificial masculinization in tilapia involves androgen receptor activation. Gen Comp Endocrinol 207:50–55

    Article  CAS  Google Scholar 

  • Görög S (2011) Advances in the analysis of steroid hormone drugs in pharmaceuticals and environmental samples (2004–2010). J Pharm Biomed Anal 55:728–743

    Article  Google Scholar 

  • Green BW, El Nagdy Z, Hebicha H (2002) Evaluation of Nile tilapia pond management strategies in Egypt. Aquac Res 33:1037–1048

    Article  Google Scholar 

  • Green BW, Teichert-Coddington DR (2000) Human Food Safety and Environmental Assessment of the Use of 17α-Methyltestosterone to Produce Male Tilapia in the United States. J World Aquacult Soc 31:337–357

    Article  Google Scholar 

  • Guerrero RD (1975) Use of Androgens for the Production of All-Male Tilapia aurea (Steindachner). Trans Am Fish Soc 104:342–348

    Article  CAS  Google Scholar 

  • Guerrero RD (2008). Tilapia Sex Reversal. Agriculture Business Week. http://www.agribusinessweek.com/tilapia-sex-reversal/. Accecced 23/08/2013

  • Hasheesh WS, Marie M-AS, Abbas HH, Eshak MG, Zahran EA (2011) An Evaluation of the Effect of 17α-Methyltestosterone Hormone on some Biochemical, Molecular and Histological Changes in the Liver of Nile Tilapia; Oreochromis niloticus. Life Sci J 8:343–358

    Google Scholar 

  • Homklin S, Ong SK, Limpiyakorn T (2011) Biotransformation of 17α-methyltestosterone in sediment under different electron acceptor conditions. Chemosphere 82:1401–1407

    Article  CAS  Google Scholar 

  • Homklin S, Ong SK, Limpiyakorn T (2012) Degradation of 17α-methyltestosterone by Rhodococcus sp. and Nocardioides sp. isolated from a masculinizing pond of Nile tilapia fry. J Hazard Mater 221–222:35–44

    Article  Google Scholar 

  • Homklin S, Ong SK, Ong SK, Limpiyakorn T (2009) Biodegradation of 17a-methyltestosterone and isolation of MT-degrading bacterium from sediment of Nile tilapia masculinization pond. Water Sci Technol 59:261–265

    Article  CAS  Google Scholar 

  • Hornung MW, Jensen KM, Korte JJ, Kahl MD, Durhan EJ, Denny JS, Henry TR, Ankley GT (2004) Mechanistic basis for estrogenic effects in fathead minnow (Pimephales promelas) following exposure to the androgen 17α-methyltestosterone: conversion of 17α-methyltestosterone to 17α-methylestradiol. Aquat Toxicol 66:15–23

    Article  CAS  Google Scholar 

  • Johnstone R, Macintosh DJ, Wright RS (1983) Elimination of orally administered 17α-methyltestosterone by Oreochromis mossambicus (tilapia) and Salmo gairdneri (rainbow trout) juveniles. Aquaculture 35:249–257

    Article  CAS  Google Scholar 

  • Júnior RP, Vargas L, Valentim-Zabott M, Ribeiro RP, da Silva AV, Otutumi LK (2012) Morphometry of white muscle fibers and performance of Nile tilapia (Oreochromis niloticus) fingerlings treated with methyltestosterone or a homeopathic complex. Homeopathy 101:154–158

    Article  Google Scholar 

  • Kang IJ, Yokota H, Oshima Y, Tsuruda Y, Shimasaki Y, Honjo T (2008) The effects of methyltestosterone on the sexual development and reproduction of adult medaka (Oryzias latipes). Aquat Toxicol 87:37–46

    Article  CAS  Google Scholar 

  • Khalil WK, Hasheesh WS, Marie M-AS, Abbas HH, Zahran EA (2011) Assessment the impact of 17α-methyltestosterone hormone on growth, hormone concentration, molecular and histopathological changes in muscles and testis of Nile tilapia; Oreochromis niloticus. Life Sci J 8:329–342

    Google Scholar 

  • Kim I, Yu Z, Xiao B, Huang W (2007) Sorption of male hormones by soils and sediments. Environ Toxicol Chem 26:264–270

    Article  CAS  Google Scholar 

  • Kolodziej EP, Harter T, Sedlak DL (2004) Dairy wastewater, aquaculture, and spawning fish as sources of steroid hormones in the aquatic environment. Environ Sci Technol 38:6377–6384

    Article  CAS  Google Scholar 

  • Kolok AS, Sellin MK (2008) The environmental impact of growth-promoting compounds employed by the United States beef cattle industry: history, current knowledge, and future directions. Rev Environ Contam Toxicol 195:1–30

    CAS  Google Scholar 

  • Lange IG, Daxenberger A, Schiffer B, Witters H, Ibarreta D, Meyer HHD (2002) Sex hormones originating from different livestock production systems: fate and potential disrupting activity in the environment. Anal Chim Acta 473:27–37

    Article  CAS  Google Scholar 

  • Linderoth M, Ledesma M, Zebühr Y, Balk L (2006) Sex steroids in the female zebrafish (Danio rerio): Effects of cyproterone acetate and leachate-contaminated sediment extract. Aquat Toxicol 79:192–200

    Article  CAS  Google Scholar 

  • Little DC (2004) Delivering better quality tilapia seed to farmers. Sixth International Symposium on Tilapia in Aquaculture. 12-16 September, 2004. Manila, Philippines. pp.3-17

  • Little DC, Bhujel RC, Pham TA (2003) Advanced nursing of mixed-sex and mono-sex tilapia (Oreochromis niloticus) fry, and its impact on subsequent growth in fertilized ponds. Aquaculture 221:265–276

    Article  Google Scholar 

  • Megbowon I, Mojekwu T (2014) Tilapia Sex Reversal Using Methyl Testosterone (MT) and its Effect on Fish, Man and Environment. Biotechnology 13:213–216

    Article  Google Scholar 

  • Melamed P, Gong Z, Fletcher G, Hew CL (2002) The potential impact of modern biotechnology on fish aquaculture. Aquaculture 204:255–269

    Article  CAS  Google Scholar 

  • Miller VM, Mulvagh SL (2007) Sex steroids and endothelial function: translating basic science to clinical practice. Trends Pharmacol Sci 28:263–270

    Article  CAS  Google Scholar 

  • Moreno-Pérez Ó, Esteva De Antonio I (2012) Clinical practice guidelines for assessment and treatment of transsexualism. SEEN Identity and Sexual Differentiation Group (GIDSEEN). Endocrinol Nutr (English Edition) 59:367–382

    Article  Google Scholar 

  • Ong SK, Chotisukarn P, Limpiyakorn T (2012) Sorption of 17α-Methyltestosterone onto Soils and Sediment. Water Air Soil Pollut 223:3869–3875

    Article  CAS  Google Scholar 

  • Pandian T, Kirankumar S (2003) Recent advances in hormonal induction of sex-reversal in fish. J Appl Aquac 13:205–230

    Article  Google Scholar 

  • Pandian TJ, Sheela SG (1995) Hormonal induction of sex reversal in fish. Aquaculture 138:1–22

    Article  CAS  Google Scholar 

  • Parks LG, LeBlanc GA (1996) Reductions in steroid hormone biotransformation/elimination as a biomarker of pentachlorophenol chronic toxicity. Aquat Toxicol 34:291–303

    Article  CAS  Google Scholar 

  • Passantino A (2012) Steroid hormones in food producing animals: Regulatory situation in Europe. In: Perez-Marin CC (ed) A bird’s-eye view of veterinary medicine, pp.33-50

  • Phelps RP, Popma TJ (2000) Sex reversal of tilapia. World Aquac Soc 2:34–59

    Google Scholar 

  • Quesada-García A, Valdehita A, Fernández-Cruz ML, Leal E, Sánchez E, Martín-Belinchón M, Cerdá-Reverter JM, Navas JM (2012) Assessment of estrogenic and thyrogenic activities in fish feeds. Aquaculture 338–341:172–180

    Article  Google Scholar 

  • Ramírez-Godínez J, Beltrán-Hernández RI, Coronel-Olivares C, Contreras-López E, Quezada-Cruz M and Vázquez-Rodríguez G (2013) Recirculating Systems for Pollution Prevention in Aquaculture Facilities. Journal of Water Resource and Protection. 5: 5–9. dx. doi:10.4236/jwarp.2013.4257A4002.

  • Rolf C, Nieschlag E (1998) Potential adverse effects of long-term testosterone therapy. Bailliere Clin Endocrinol Metab 12:521–534

    Article  CAS  Google Scholar 

  • Rothbard S, Zohar Y, Zmora N, Levavi-Sivan B, Moav B, Yaron Z (1990) Clearance of 17α-ethynyltestosterone from muscle of sex-inversed tilapia hybrids treated for growth enhancement with two doses of the androgen. Aquaculture 89:365–376

    Article  CAS  Google Scholar 

  • Rowell CB, Watts SA, Wibbels T, Hines GA, Mair G (2002) Androgen and Estrogen Metabolism during Sex Differentiation in Mono-Sex Populations of the Nile Tilapia (Oreochromis niloticus). Gen Comp Endocrinol 125:151–162

    Article  CAS  Google Scholar 

  • Seal LJ (2009) Testosterone replacement therapy. Medicine 37:445–449

    Article  Google Scholar 

  • Shore LS, Shemesh M (2003) Naturally produced steroid hormones and their release into the environment. Pure Appl Chem 75:1859–1871

    Article  CAS  Google Scholar 

  • Shors TJ, Miesegaes G (2002) Testosterone in utero and at birth dictates how stressful experience will affect learning in adulthood. Proc Natl Acad Sci 99:13955–13960

    Article  CAS  Google Scholar 

  • Snow DD, Bartelt-Hunt SL, Devivo S, Saunders S, Cassada DA (2009) Detection, occurrence, and fate of emerging contaminants in agricultural environments. Water Environ Res 81:941–958

    Article  CAS  Google Scholar 

  • Soto AM, Calabro JM, Prechtl NV, Yau AY, Orlando EF, Daxenberger A, Kolok AS, Guillette LJ Jr, le Bizec B, Lange IG (2004) Androgenic and estrogenic activity in water bodies receiving cattle feedlot effluent in Eastern Nebraska, vol 112. Environmental health perspectives, USA, p 346

    Google Scholar 

  • Straus DL, Bowker JD, Bowman MP, Carty DG, Mitchell AJ, Farmer BD, Ledbetter CK (2013) Safety of Feed Treated with 17α-Methyltestosterone (17MT) to Larval Nile Tilapia. N Am J Aquac 75:212–219

    Article  Google Scholar 

  • Tuan PA, Little DC, Mair GC (1998) Genotypic effects on comparative growth performance of all-male tilapia Oreochromis niloticus (L.). Aquaculture 159:293–302

    Article  Google Scholar 

  • van Honk J, Schutter DJ, Bos PA, Kruijt A-W, Lentjes EG, Baron-Cohen S (2011) Testosterone administration impairs cognitive empathy in women depending on second-to-fourth digit ratio. Proc Natl Acad Sci 108:3448–3452

    Article  Google Scholar 

  • Vick AM, Hayton WL (2001) Methyltestosterone pharmacolinetics and oral bioavailability in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 52:177–188

    Article  CAS  Google Scholar 

  • Wassermann GJ, Afonso LOB (2002) Validation of the aceto-carmine technique for evaluating phenotypic sex in Nile tilapia (Oreochromis niloticus) fry. Ciênc Rural 32:133–139

    Article  Google Scholar 

  • Yialamas MA, Hayes FJ (2003) Androgens and the ageing male and female. Best Pract Res Clin Endocrinol Metab 17:223–236

    Article  CAS  Google Scholar 

  • Yoo J-W, Lee CH (2006) Drug delivery systems for hormone therapy. J Control Release 112:1–14

    Article  CAS  Google Scholar 

  • Young RB, Latch DE, Mawhinney DB, Nguyen T-H, Davis JC, Borch T (2013) Direct Photodegradation of Androstenedione and Testosterone in Natural Sunlight: Inhibition by Dissolved Organic Matter and Reduction of Endocrine Disrupting Potential. Environ Sci Technol 47:8416–8424

    CAS  Google Scholar 

  • Zheng W, Yates SR, Bradford SA (2007) Analysis of steroid hormones in a typical dairy waste disposal system. Environ Sci Technol 42:530–535

    Article  Google Scholar 

Download references

Acknowledgments

The authors would appreciate the affection and financial support from the Nelson Mandela African Institution of Science and Technology in Arusha, Tanzania, and the Council for Scientific and Industrial Research (SCIR) in Pretoria, South Africa, for hosting the research progress in nanotechnology perspectives of this project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nichrous Mlalila.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mlalila, N., Mahika, C., Kalombo, L. et al. Human food safety and environmental hazards associated with the use of methyltestosterone and other steroids in production of all-male tilapia. Environ Sci Pollut Res 22, 4922–4931 (2015). https://doi.org/10.1007/s11356-015-4133-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4133-3

Keywords

Navigation