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Application potential of albendazole as an aquatic animal drug based on its safety, efficacy, and residue profiles

  • Min Ji Kim (Pesticide and Veterinary Drug Residues Division, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Ji Young Kim (Pesticide and Veterinary Drug Residues Division, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Dong Woo Shin (Pesticide and Veterinary Drug Residues Division, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety) ;
  • Mi Ok Eom (Pesticide and Veterinary Drug Residues Division, National Institute of Food and Drug Safety Evaluation, Ministry of Food and Drug Safety)
  • Received : 2024.01.23
  • Accepted : 2024.04.25
  • Published : 2024.10.15

Abstract

The number of available drugs for treating aquatic animals is insufficient, given the occurrence of a variety of parasites and difficulties in developing appropriate treatments, such as vaccines or immunostimulants. Consequently, repurposing livestock drugs for treating aquatic animals is a viable alternative. Several studies have demonstrated that albendazole (ABZ) is a good anthelmintic for humans and animals such as ruminants, poultry, and honeybees. Therefore, we investigated the toxicological studies, metabolic and residue depletion studies, and efficacy trials of ABZ in aquatic animals to identify its application potential as a drug for aquatic animals. ABZ was depleted within 24 h in the muscle tissues of hybrid striped bass, rainbow trout, and tilapia. In muscle tissue with adhering skin obtained from tilapia and largemouth bass, a significant quantity of the amino-sulfone metabolite of ABZ (ABZ-SO2NH2) was present, while no ABZ-SO2NH2 was detected in hybrid striped bass, channel catfish, and patinga. Fish exposed only to high doses of ABZ showed reduced red blood cell counts and hemoglobin levels and increased lymphocytes. Such signs of toxicity have also been observed in human patients and animal studies. At a dose of 100 mg/L, ABZ showed 100% efficacy in eels. In addition, albendazole sulfoxide (ABZSO) demonstrated efficacies of 96.1% and 100% in pirapatinga and ray-finned fish, respectively, at a dose 500 mg/L. ABZ was also highly effective in treating an intracellular parasite E. hepatopenaei in white shrimp. The application of ABZ in aquatic animals under the low-dose and short-term conditions is considered a reasonable solution to manage parasite infections. The types and residual periods of degradation products differed among fish species, suggesting dissimilar metabolic pathways. With a high demand for new alternative veterinary drugs in aquaculture by fish farmers, this review offers important evidence for considering the use of ABZ in Korean farmed fish, taking food safety issues into account.

Keywords

Acknowledgement

The authors sincerely express their gratitude to the editors and peer reviewers of Toxicological research. Their comments and suggestions have enriched the manuscript and produced a better and more balanced account of the research.

References

  1. OECD, FAO (2023) OECD-FAO agricultural outlook 2023-2032. OCED iLibarary. https://www.fao.org/documents/card/en/c/cc6361en. Accessed 6 July 2023
  2. Du Y, Hu X, Miao L, Chen J (2022) Current status and development prospects of aquatic vaccines. Front Immunol 13:1040336. https://doi.org/10.3389/fmmu.2022.1040336
  3. Mondal H, Thomas J (2022) A review on the recent advances and application of vaccines against fish pathogens in aquaculture. Aquacult Int 30:1971-2000. https://doi.org/10.1007/s10499-022-00884-w
  4. Nowak BF (2007) Parasitic diseases in marine cage culture-an example of experimental evolution of parasites? Int J Parasitol 37:581-588. https://doi.org/10.1016/j.ijpara.2007.01.003
  5. Shivam S, El-Matbouli M, Kumar G (2021) Development of fish parasite vaccines in the OMICs Era: progress and opportunities. Vaccines 9:179. https://doi.org/10.3390/vaccines9020179
  6. Karvonen A, Rintamaki P, Jokela J, Valtonen ET (2010) Increasing water temperature and disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases. Int J Parasitol 40:1483-1488. https://doi.org/10.1016/j.ijpara.2010.04.015
  7. Pulkkinen K, Ketola T, Laakso J, Mappes J, Sundberg LR (2022) Rich resource environment of fish farms facilitates phenotypic variation and virulence in an opportunistic fish pathogen. Evol Appl 15:417-428. https://doi.org/10.1111/eva.13355
  8. Pinto N, Naik MG, Naveen Kumar BT, Shankar KM, Rakesh K, Abhiman PB, Sathish RP, Ramesh KS (2023) Oxytetracycline efficacy and preliminary establishment of pharmacokinetic residues in tropical fish, Catla catla (Hamilton, 1822). Aquaculture 571:739481. https://doi.org/10.1016/j.aquaculture.2023.739481
  9. The European Agency for the Evaluation of Medicinal Products (EMEA) (2004) Albendazole (summary report 3). EMEA/MRL/865/03-FINAL. The European Medicines Agency, London. https://www.ema.europa.eu/en/documents/mrl-report/albendazole-summary-report-3-committee-veterinary-medicinal-products_en.pdf. Accessed June 2004
  10. Shaikh B, Rummel N, Gieseker C, Serfing S, Reimschuessel R (2003) Metabolism and residue depletion of albendazole and its metabolites in rainbow trout, tilapia and Atlantic salmon after oral administration. J Vet Pharmacol Ther 26:421-427. https://doi.org/10.1046/j.0140-7783.2003.00534.x
  11. Shaikh B, Rummel N, Gieseker C, Cheely CS, Reimschuessel R (2009) Residue depletion of albendazole and its metabolites in the muscle tissue of large mouth and hybrid striped bass after oral administration. J Chromatogr A 1216:8173-8176. https://doi.org/10.1016/j.chroma.2009.04.009
  12. Busatto Z, Goncalves de Franca W, Cyrino JEP, Paschoal JAR (2017) Assessment of elimination profle of albendazole residues in fish. Food Addit Contam 35:77-85. https://doi.org/10.1080/19440049.2017.1400186
  13. Buchmann K, Bjerregaard J (1990) Comparative efcacies of commercially available benzimidazoles against Pseudodactylogyrus infestations in eels. Dis Aquat Org 9:117-120 https://doi.org/10.3354/dao009117
  14. Carlsson G, Patring J, Ulleras E, Oskarsson A (2011) Developmental toxicity of albendazole and its three main metabolites in zebrafish embryos. Reprod Toxicol 32:129-137. https://doi.org/10.1016/j.reprotox.2011.05.015
  15. Kang YJ, Kim DS, Kim KH (2013) Evaluation of treatment efficacy of doxycycline and albendazole against scuticociliatosis in olive founder (Paralichthys olivaceus). Aquaculture 416:192-195. https://doi.org/10.1016/j.aquaculture.2013.09.017
  16. Nwani CD, Odo GE, Nwadinigwe AO, Onyeke CC, Atama CI, Ngwu G, Oluah SN, Ukonze JA, Ezeibe BCA (2016) Shortterm effects of albendazole on the oxidative stress markers and hematological parameters in tissues of African Catfsh Clarias gariepinus. J Aquat Anim Health 28:222-228. https://doi.org/10.1080/08997659.2016.1194908
  17. Mykola Z, Inna K, Liudmyla C (2018) Evaluation of the toxic effect of nandrolone and albendazole on fish according to the morphological parameters of blood. ScienceRise Biol Sci 1:4-8. https://doi.org/10.15587/2519-8025.2018.123900
  18. Negreiros LP, Souza EX, Lima TA, Tavares-Dias M (2022) Albendazole is effective for controlling monogenean parasites of the gills of Piaractus brachypomus (Serrasalmidae) and Megaleporinus macrocephalus (Anostomidae). Rev Bras Parasitol Vet 31:e010322. https://doi.org/10.1590/S1984-29612022057
  19. Subash P, Uma A, Ahilan B, Kannan SS (2023) In vivo and in silico investigations on the efficacy of albendazole against Enterocytozoon hepatopenaei (EHP) infecting Penaeus vannamei. Aquaculture 575:739801. https://doi.org/10.1016/j.aquaculture.2023.739801
  20. Shaikh B, Rummel N, Reimschuessel R (2003) Determination of albendazole and its major metabolites in the muscle tissues of atlantic Salmon, Tilapia, and rainbow trout by high performance liquid chromatography with fluorometric detection. J Agric Food Chem 51:3254-3259. https://doi.org/10.1021/jf021176i
  21. Shaikh B, Rummel N, Gieseker C, Reimschuessel R (2006) Metabolism and depletion of albendazole in the muscle tissue of channel catfish following oral treatment. J Vet Pharmacol Ther 29:525-530. https://doi.org/10.1111/j.1365-2885.2006.00799.x
  22. Yu D, Evans ER, Hasbrouck N, Reimschuessel R, Shaikh B (2012) Residue depletion of albendazole and its metabolites in aquacultured yellow perch (Perca flavescens). J Vet Pharmacol Ther 35:560-562. https://doi.org/10.1111/j.1365-2885.2011.01354.x
  23. Li Z, Chen C, Ai D, Wang C, Li J, Qi Y, Yi W, Shen H, Cao J (2012) Pharmacokinetics and tissue residues of hydrochloric acid albendazole sulfoxide and its metabolites in crucian carp (Carassius auratus) after oral administration. Environ Toxicol Pharmacol 33:197-204. https://doi.org/10.1016/j.etap.2011.12.001
  24. Portela ACV, Silveira JGF, Damaceno MA, da Silva AFB, de Jesus RB, Pilarski F, Gadaj A, Mooney MH, Paschoal JAR (2020) Food safety evaluation for the use of albendazole in fish: residual depletion profile and withdrawal period estimation. Food Addit Contam 37:596-606. https://doi.org/10.1080/19440049.2020.1719285
  25. Pereira Cordeiro R, de Campos A, Braga P, Souza Rocha MJ, Campos Chagas E, Reyes Reyes FG (2021) Depletion study and estimation of the withdrawal period for albendazole in tambaqui (Colossoma macropomum) parasitised by acanthocephalan (Neoechinorhynchus buttnerae) treated with albendazolecontaining feed. Food Addit Contam 38:1883-1896. https://doi.org/10.1080/19440049.2021.1954700
  26. Onaka E, Martins M, Moraes F (2003) Albendazole and praziquantel efficacy against Anacanthorus penilabiatus (Monogenea: Dactylogyridae), gill parasite of Piaractus mesopotamicus (Osteichthyes: Characidae). I. Therapeutic baths. Bol Inst Pesca 29:101-107
  27. Alves CMG, Nogueira JN, Barriga IB, Dos Santos JR, Santos GG, Tavares-Dias M (2019) Albendazole, levamisole and ivermectin are efective against monogeneans of Colossoma macropomum (Pisces: Serrasalmidae). J Fish Dis 42:405-412. https://doi.org/10.1111/jfd.12952
  28. Opatrny L, Snell L, Prichard RW, Maclean J (2005) Death related to albendazole-induced pancytopenia: case report and review. Am J Trop Med Hyg 72:291-294. https://doi.org/10.4269/AJTMH.2005.72.291
  29. Dow GS, O'Hara AJ, Newton SC, Reynoldson JA, Thompson RCA (2000) Plasmodium berghei: the antimalarial activity of albendazole in rats is mediated via effects on the hematopoietic system. Exp Parasitol 94:259-263. https://doi.org/10.1006/expr.2000.4491
  30. Harm TA, Radke SL, Burns LE, Schrunk DE (2022) Enteropathy and bone marrow hypoplasia associated with presumptive albendazole toxicosis in a juvenile Boer goat. J Vet Diagn Invest 34:1015-1019. https://doi.org/10.1177/10406387221121122
  31. Howard LL, Papendick R, Stalis IH, Allen JL, Sutherland-Smith M, Zuba JR, Ward DL, Rideout BA (2002). Fenbendazole and albendazole toxicity in pigeons and doves. J Avian Med Surg 16:203-210. http://www.jstor.org/stable/30133222 https://doi.org/10.1647/1082-6742(2002)016[0203:FAATIP]2.0.CO;2
  32. Gomez-Puerta LA, Carrasco J, Vargas-Calla A, Lopez-Urbina MT, Gonzalez AE (2019) Alopecia a potential adverse side effect of albendazole use in alpacas. Vet Parasitol Reg Stud Rep 17:100297. https://doi.org/10.1016/j.vprsr.2019.100297
  33. Kim JH, Lee C, Jeon HJ, Kim BK, Lee NK, Choi SK, Han JE (2021) First report of Enterocytozoon hepatopenaei infection in Pacific whiteleg shrimp (Litopenaeus vannamei) cultured in Korea. Animals 11:3150. https://doi.org/10.1016/j.aquaculture.2021.737525
  34. Jang GI, Kim SM, Oh YK, Lee SJ, Hong SY, Lee HE, Kwon MG, Kim BS (2022) First report of Enterocytozoon hepato-penaei infection in giant freshwater prawn (Macrobrachium rosenbergii de Man) cultured in the Republic of Korea. Animals 12:3149. https://doi.org/10.3390/ani12223149
  35. Tang KF, Pantoja CR, Redman RM, Han JE, Tran LH, Lightner DV (2015) Development of in situ hybridization and PCR assays for the detection of Enterocytozoon hepatopenaei (EHP), a microsporidian parasite infecting penaeid shrimp. J Invertebr Pathol 130:37-41. https://doi.org/10.1016/j.jip.2015.06.009-