Skip to main content

Advertisement

SpringerLink
Log in

Accumulation and clearance of tissue residues and health status of Nile tilapia Oreochromis niloticus (L.) juveniles as influenced by the extended oral oxytetracycline-dosing

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

Abstract

Antibiotics are considered an important primary therapy for bacterial diseases in aquaculture. This study evaluated the influence of oral administration of oxytetracycline (OTC) on feed intake, growth, mortality, residue accumulation and clearance, and histopathological changes in the vital organs of six groups of Nile tilapia Oreochromis niloticus when fed at 0–10 times the therapeutic dose (1×: 80 mg/kg biomass/day) for 10 and 20 consecutive days. The feed intake was reduced only slightly, viz., 2% in 10-day and 4.25% in 20-day dosing trials at 1× dose compared to control. While in other groups, an OTC-dose-dependent reduction in feed intake up to 31.25% was noted. The fish of the 0.5× and 1× groups recorded significantly high biomass, while the other OTC-dosed groups recorded significantly lower biomass than the control. The fold change in biomass between the control and 1× groups was insignificant. Dose-dependent mortalities were recorded in OTC-dosed fish in 10-day (1.67–6.67%) and 20-day (3.33–8.33%) trials. The OTC concentration in fish muscle established a dose- and time-response relationship. The OTC residue levels in muscle even on day 20 OTC-dosing were lower than the maximum residue limit (MRL) permitted by Codex Alimentarius (200 ng/g). On day 23 post OTC-dosing, the residue levels were traces to <10 μg/g in all groups, except the 10× group. The OTC-dosing caused mild to moderate pathological changes in the gills, liver and kidney of O. niloticus and the fish were able to mount adaptive biological responses to overcome the stress with time.

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
Fig. 3

Similar content being viewed by others

Data availability

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Anonymous (2006) Residues of veterinary drugs in foods. Joint FAO/WHO Food Standards Programme, 29th Session. Codex Alimentarius Commission, Geneva, Switzerland

    Google Scholar 

  • Anonymous (2010a) Commission Regulation (EU) No 37/2010 of 22 December 2009 on pharmacologically active substances and their classification regarding maximum residue limits in foodstuffs of animal origin. Off J Eur Union L15:1–72

    Google Scholar 

  • Anonymous (2010b) Administrative maximum residue limits (AMRLs) and maximum residue limits (MRLs) set by Canada. Drugs and Health Products, Canada. http://www.hc-sc.gc.ca/dhp-mps/vet/mrl-lmr/mrl-lmr_versus_new-nouveau-eng.php

  • Anonymous (2011) Maximum residue limits (MRLs) list of agricultural chemicals in foods. The Japan Food Chemical Research Foundation. http://m5.ws001.squarestart.ne.jp/foundation/search.html.

  • Baldissera MD, Souza CF, Júnior GB, Verdi CM, Moreira KLS, da Rocha MIUM, da Veiga ML, Santos RCV, Vizzotto BS, Baldisserotto B (2017) Aeromonas caviae alters the cytosolic and mitochondrial creatine kinase activities in experimentally infected silver catfish: Impairment on renal bioenergetics. Microb Pathog 110:439–443. https://doi.org/10.1016/j.micpath.2017.07.031

    Article  CAS  Google Scholar 

  • Bowker J, Burbank D, Bowman MP, Wandelear N (2015) Efficacy of AQUAFLOR® (50% Florfenicol) to control mortality in Chinook salmon diagnosed with bacterial kidney disease (2014). United States Fish and Wildlife Service, Aquatic Animal Drug Approval Partnership, Drug Research Information Bulletin No. 45:1–3

    Google Scholar 

  • Boyd CE (1979) Water quality in warm water fish ponds. Auburn University, Alabama, Alabama Agriculture Experiment Station

    Google Scholar 

  • Carraschi SP, da Cruz C, Machado Neto JG, Ignácio NF, Barbuio R, Machado MR (2012) Histopathological biomarkers in pacu (Piaractus mesopotamicus) infected with Aeromonas hydrophila and treated with antibiotics. Ecotoxicol Environ Saf 83:115–120. https://doi.org/10.1016/j.ecoenv.2012.06.016

    Article  CAS  Google Scholar 

  • Chen J, Sun R, Pan C-G, Sun Y, Mai B-X, Li QX (2020) Antibiotics and food safety in aquaculture. J Agric Food Chem. 68(43):11908–11919. https://doi.org/10.1021/acs.jafc.0c03996

    Article  CAS  Google Scholar 

  • CPCSEA (2018) Compendium of CPCSEA 2018. Committee for the purpose of control and supervision of experiments on animals. Animal Welfare Division, Ministry of Environment Forest and Climate Change, Government of India, New Delhi, 202p

    Google Scholar 

  • Dibner JJ, Richards JD (2005) Antibiotic growth promoters in agriculture: history and mode of action. Poult Sci 84:634–643. https://doi.org/10.1093/ps/84.4.634

    Article  CAS  Google Scholar 

  • Elia AC, Ciccotelli V, Pacini N, Dorr AJM, Gili M, Natali M, Gasco L, Prearo M, Abete MC (2014) Transferability of oxytetracycline (OTC) from feed to carp muscle and evaluation of the antibiotic effects on antioxidant systems in liver and kidney. Fish Physiol Biochem 40:1055–1068. https://doi.org/10.1007/s10695-013-9905-4

    Article  CAS  Google Scholar 

  • European Commission (2002) Council Regulation (EEC) No 2002/657/EC. Commission decision of 12 August 2002 implementing Council Directive 96/23/EC concerning the performance of analytical methods and the interpretation of results. Off J Eur Comm Notified under document number C.

  • Fairgrieve WT, Masada CL, McAuley WC, Peterson ME, Myers MS, Strom MS (2005) Accumulation and clearance of orally administered erythromycin and its derivative, azithromycin, in juvenile fall Chinook salmon Oncorhynchus tshawytscha. Dis Aquat Org 64:99–106. https://doi.org/10.3354/dao064099

    Article  CAS  Google Scholar 

  • FAO (2020) The state of world fisheries and aquaculture 2020. Sustainability in Action. Rome. https://doi.org/10.4060/ca9229en

  • Gaikowski MP, Wolf JC, Schleis SM, Gingerich WH (2003) Safety of oxytetracycline (Terramycin TM-100F) administered in feed to hybrid striped bass, walleyes, and yellow perch. J Aquat Anim Health 15:274–286. https://doi.org/10.1577/H03-042.1

    Article  Google Scholar 

  • Gaikowski MP, Wolf JC, Schleis SM, Tuomari D, Endri SRG (2013) Safety of florfenicol administered in feed to tilapia (Oreochromis sp.). Toxicol Pathol 41:639–652. https://doi.org/10.1177/0192623312463986

    Article  CAS  Google Scholar 

  • Granados-Chinchilla F, Rodríguez C (2017) Tetracyclines in food and feeding stuffs: from regulation to analytical methods, bacterial resistance, and environmental and health implications. J Anal Methods Chem 2017:1–24. https://doi.org/10.1155/2017/1315497

    Article  CAS  Google Scholar 

  • Guardiola FA, Cerezuela R, Meseguer J, Esteban MA (2012) Modulation of the immune parameters and expression of genes of gilthead seabream (Sparus aurata L.) by dietary administration of oxytetracycline. Aquaculture 334–337:51–57. https://doi.org/10.1016/j.aquaculture.2012.01.003

  • Hernández SP (2005) Responsible use of antimicrobials in aquaculture. FAO Fisheries Technical Paper no 469, FAO, Rome, 97pp.

  • Julinta RB, Abraham TJ, Roy A, Singha J, Dash G, Mali P, Nagesh TS, Sar TK, Patil PK, Kumar KA (2019a) Effect of oxytetracycline-dosing on the growth, safety and intestinal histology of Nile tilapia, Oreochromis niloticus (L.) juveniles. Int J Curr Microbiol Appl Sci 8:2708–2724. 10.20546/ijcmas. 2019.808.313

  • Julinta RB, Abraham TJ, Roy A, Singha J, Boda S, Patil PK (2019b) Dietary influences of oxytetracycline on the growth and serum biomarkers of Oreochromis niloticus (L.). Ecotoxicol Environ Saf 186:109752. https://doi.org/10.1016/j.ecoenv.2019.109752

    Article  CAS  Google Scholar 

  • Konig J, Muller F, Fromm MF (2013) Transporters and drug-drug interactions: important determinants of drug disposition and effects. Pharmacol Rev 65:944–966. https://doi.org/10.1124/pr.113.007518

    Article  CAS  Google Scholar 

  • Li Z, Zhang W, Lu X, Li J, He B, Jiang H, Wang S, Lu Z, Wang C, Cao J (2012) Reaction temperature alters chorzoxazone metabolism in carp (Cyprinus carpio) hepatic microsomes. Fish Physiol Biochem 38:1225–1231. https://doi.org/10.1007/s10695-012-9605-5

    Article  CAS  Google Scholar 

  • Limbu SM, Zhou L, Sun S-X, Zhang M-L, Du Z-Y (2018) Chronic exposure to low environmental concentrations and legal aquaculture doses of antibiotics cause systemic adverse effects in Nile tilapia and provoke differential human health risk. Environ Int 115:205–219. https://doi.org/10.1016/j.envint.2018.03.034

    Article  CAS  Google Scholar 

  • Limbu SM, Chen L-Q, Zhang M-L, Du Z-Y (2020) A global analysis on the systemic effects of antibiotics in cultured fish and their potential human health risk: a review. Rev Aquac 1–45. 13:1015–1059. https://doi.org/10.1111/raq.12511

  • Mo W, Chen Z, Leung H, Leung A (2017) Application of veterinary antibiotics in China’s aquaculture industry and their potential human health risks. Environ Sci Pollut Res 24:8978–8989. https://doi.org/10.1007/s11356-015-5607-z

    Article  Google Scholar 

  • Nunes B, Antunes SC, Gomes R, Campos JC, Braga MR, Ramos AS, Correia AT (2015) Acute effects of tetracycline exposure in the freshwater fish Gambusia holbrooki: antioxidant effects, neurotoxicity and histological alterations. Arch Environ Contam Toxicol 68:371–381. https://doi.org/10.1007/s00244-014-0101-z

    Article  CAS  Google Scholar 

  • Oliveira R, McDonough S, Ladewig JCL, Soares AMVM, Nogueira AJA, Domingues I (2013) Effects of oxytetracycline and amoxicillin on development and biomarkers activities of zebrafish (Danio rerio). Environ Toxicol Pharmacol 36:903–912. https://doi.org/10.1016/j.etap.2013.07.019

    Article  CAS  Google Scholar 

  • Reda RM, Ibrahim RE, Ahmed EG, El-Bouhy ZM (2013) Effect of oxytetracycline and florfenicol as growth promoters on the health status of cultured Oreochromis niloticus. Egypt J Aquat Res 39:241–248. https://doi.org/10.1016/j.ejar.2013.12.001

    Article  Google Scholar 

  • Reimschuessel R, Ferguson HW (2006) Kidney. In: Ferguson HW (ed) Systemic pathology of fish: a text and atlas of normal tissues in teleosts and their responses in disease. Scotian Press, London, pp 91–118

    Google Scholar 

  • Reimschuessel R, Stewart L, Squibb E, Hirokawa K, Brady T, Brooks D, Shaikh B, Hodsdon C (2005) Fish drug analysis-phish-pharm: a searchable database of pharmacokinetics data in fish. The AAPS J 7:E288–E327. https://doi.org/10.1208/aapsj070230

    Article  CAS  Google Scholar 

  • Rejeki S, Desrina D, Mulyana AR (2005) Chronic effects of detergent surfactant (linear alkylbenzene sulfonate / LAS) on the growth and survival rate of sea bass (Lates calcalifer Bloch) larvae. J Coast Dev 8:207–226

    Google Scholar 

  • Roberts RJ (2012) Fish pathology. John Wiley & Sons, New Delhi

    Book  Google Scholar 

  • Rodrigues S, Antunes SC, Nunes B, Correia AT (2017) Histological alterations in gills and liver of rainbow trout (Oncorhynchus mykiss) after exposure to the antibiotic oxytetracycline. Environ Toxicol Pharmacol 53:164–176. https://doi.org/10.1016/j.etap.2017.05.012

    Article  CAS  Google Scholar 

  • Romero J, Feijoó CG, Navarrete P (2012) Antibiotics in aquaculture – use, abuse and alternatives. In: Carvalho E, David GS, Silva RJ (eds.) Health and Environment in Aquaculture. ISBN: 978-953-51-0497-1, InTech, pp. 159–199. https://www.intechopen.com/books/health-and-environment-in-aquaculture/antibiotics-in-aquaculture-use-abuse-and-alternatives

  • Sanchez-Martinez JG, Perez-Castaneda R, Rabago-Castro JL, Aguire-Guzman G, Vazquez-Sauceda ML (2008) A preliminary study on the effects on growth, condition, and feeding indexes in channel catfish, Ictalurus punctatus, after the prophylactic use of potassium permanganate and oxytetracycline. J World Aquacult Soc 39:664–670. https://doi.org/10.1111/j.1749-7345.2008.00195.x

    Article  Google Scholar 

  • Seely JC, Hard GC, Blankenship B (2018) Kidney. In: Suttie A (ed) Boorman’s pathology of the rat, 2nd edn. Academic Press, USA, pp 125–166. https://doi.org/10.1016/B978-0-12-391448-4.00011-3

    Chapter  Google Scholar 

  • Senarat S, Kettratad J, Poolprasert P, Yenchum W, Jiraungkoorskul W (2015) Histopathological finding of liver and kidney tissues of the yellow mystus, Hemibagrus filamentus (Fang and Chaux, 1949), from the Tapee River, Thailand. Songklanakarin J Sci Technol 37:1–5 https://rdo.psu.ac.th/sjstweb/journal/37-1/37-1-1.pdf

    Google Scholar 

  • Shiogiri NS, Ikefuti CV, Carraschi SP, da Cruz C, Fernandes MN (2016) Effects of azithromycin on tilapia (Oreochromis niloticus): health status evaluation using biochemical, physiological and morphological biomarkers. Aquac Res 48:1–15. https://doi.org/10.1111/are.13191

    Article  CAS  Google Scholar 

  • Straus DL, Bowker JD, Bowman MP, Carty D, Mitchell AJ, Farmer BD (2012) Safety of aquaflor-medicated feed to sunshine bass. N Am J Aquacult 74:1–7. https://doi.org/10.1080/15222055.2011.630262

    Article  Google Scholar 

  • Svobodova Z, Sudova E, Nepejchalova L, Červinka S, Vykusova B, Modra H, Kolářová J (2006) Effects of oxytetracycline containing feed on pond ecosystem and health of carp (Cyprinus carpio L.). Acta Vet Brno 75:571–577. https://doi.org/10.2754/avb200675040571

    Article  CAS  Google Scholar 

  • Toften H, Jobling M (1997) Feed intake and growth of Atlantic salmon, Salmo salar L., fed diets supplemented with oxytetracycline and squid extract. Aquac Nutr 3:145–151. https://doi.org/10.1046/j.1365-2095.1997.00081.x

    Article  CAS  Google Scholar 

  • Trushenski JT, Aardsma MP, Barry KJ, Bowker JD, Jackson CJ, Jakaitis M, McClure RL, Rombenso AN (2018) Oxytetracycline does not cause growth promotion in finfish. J Anim Sci 96:1667–1677. https://doi.org/10.1093/jas/sky120

    Article  Google Scholar 

  • USFWS (2015) Approved drugs for use in aquaculture, second ed. U.S. Fish and Wildlife Service’s Aquatic Animal Drug Approval Partnership Program, American Fisheries Society’s Fish Culture and Fish Health Sections, Association of Fish and Wildlife Agencies, and Fisheries and Water Resources Policy Committee’s Drug Approval Working Group.

  • Watts JE, Schreier HJ, Lanska L, Hale MS (2017) The rising tide of antimicrobial resistance in aquaculture: sources, sinks and solutions. Mar Drugs 15:158. https://doi.org/10.3390/md15060158

    Article  CAS  Google Scholar 

  • Wen Y, Wang Y, Feng YQ (2006) Simultaneous residue monitoring of four tetracycline antibiotics in fish muscle by in-tube solid-phase microextraction coupled with high-performance liquid chromatography. Talanta 70:153–159. https://doi.org/10.1016/j.talanta.2005.11.049

    Article  CAS  Google Scholar 

  • Wilhelm Filho D, Torres MA, Tribess TB, Pedrosa RC, Soares CHL (2001) Influence of season and pollution on the antioxidant defenses of the cichlid fish acará (Geophagus brasiliensis). Braz J Med Biol Res 34:719–726. https://doi.org/10.1590/S0100-879X2001000600004

  • Wolf JC, Baumgartner WA, Blazer VS, Camus AC, Engelhardt JA, Fournie JW, Frasca SJr, Groman DB, Kent ML, Khoo LH, Law JM, Lombardini ED, Ruehl-Fehlert C, Segner HE, Smith SA, Spitsbergen JM, Weber K, Wolfe MJ (2015) Nonlesions, misdiagnoses, missed diagnoses, and other interpretive challenges in fish histopathology studies a guide for investigators, authors, reviewers, and readers. Toxicol Pathol 43:297–325. https://doi.org/10.1177/0192623314540229

  • Yang C, Song G, Lim W (2020) A review of the toxicity in fish exposed to antibiotics. Comp Biochem Physiol C- Toxicol Pharmacol 237:108840. https://doi.org/10.1016/j.cbpc.2020.108840

    Article  CAS  Google Scholar 

  • Zhang Q, Cheng J, Xin Q (2015) Effects of tetracycline on developmental toxicity and molecular responses in zebrafish (Danio rerio) embryos. Ecotoxicology 24:707–719. https://doi.org/10.1007/s10646-015-1417-9

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the Vice Chancellor, West Bengal University of Animal and Fishery Sciences, Kolkata, for providing the necessary infrastructure facility to carry out the work.

Funding

The research work was supported by the Indian Council of Agricultural Research, Government of India, New Delhi, under the All India Network Project on Fish Health (Grant F. No. CIBA/AINP-FH/2015-16 dated 02.06.2015).

Author information

Authors and Affiliations

  1. Department of Aquatic Animal Health, Faculty of Fishery Sciences, West Bengal University of Animal and Fishery Sciences, Chakgaria, Kolkata, West Bengal, 700094, India

    Thangapalam Jawahar Abraham, Anwesha Roy, Roy Beryl Julinta & Jasmine Singha

  2. Aquatic Animal Health and Environment Division, ICAR-Central Institute of Brackishwater Aquaculture, Raja Annamalai Puram, Chennai, Tamil Nadu, 600028, India

    Prasanna Kumar Patil

  3. Fish Processing Division, ICAR-Central Institute of Fisheries Technology, Willingdon Island, Kochi, Kerala, 682029, India

    Edapparambil Krishnappan Nanitha Krishna, Ravindran Rajisha & Kesavan Ashok Kumar

Authors
  1. Thangapalam Jawahar Abraham
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anwesha Roy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roy Beryl Julinta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jasmine Singha
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Prasanna Kumar Patil
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Edapparambil Krishnappan Nanitha Krishna
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ravindran Rajisha
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kesavan Ashok Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TJA and PKP designed the study and contributed to study materials and consumables. AR, JS and RBJ performed the wet laboratory experiments and histopathology and generated the data. EKNK and RR performed the LC-MS/MS analysis. KAK interpreted the LC-MS/MS data. TJA interpreted the statistical data and wrote the manuscript. All authors agreed with the results and conclusions.

Corresponding author

Correspondence to Thangapalam Jawahar Abraham.

Ethics declarations

Ethics approval and consent to participate

All the experimental protocols were as per the guidelines of the Government of India and approved by the Indian Council of Agricultural Research, Government of India, New Delhi (F. No. CIBA/AINP-FH/2015-16 dated 16.7.2015), under the All India Network Project on Fish Health.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests

Additional information

Responsible Editor: Bruno Nunes

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

Abraham, T.J., Roy, A., Julinta, R.B. et al. Accumulation and clearance of tissue residues and health status of Nile tilapia Oreochromis niloticus (L.) juveniles as influenced by the extended oral oxytetracycline-dosing. Environ Sci Pollut Res 28, 55362–55372 (2021). https://doi.org/10.1007/s11356-021-14854-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-14854-x

Keywords

Search

Navigation