Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-02T20:08:20.239Z Has data issue: false hasContentIssue false
  • English
  • Français

Efficacy of flukicides on Fasciola gigantica, a food-borne zoonotic helminth affecting livestock in Bangladesh

Published online by Cambridge University Press:  10 May 2022

Mohammad Manjurul Hasan ,
Babul Chandra Roy ,
Hiranmoy Biswas ,
Moizur Rahman ,
Anisuzzaman Anisuzzaman Open the ORCID record for Anisuzzaman Anisuzzaman [Opens in a new window] ,
Mohammad Zahangir Alam Open the ORCID record for Mohammad Zahangir Alam [Opens in a new window]  and
Md. Hasanuzzaman Talukder Open the ORCID record for Md. Hasanuzzaman Talukder [Opens in a new window]
Mohammad Manjurul Hasan*
Affiliation:
Department of Parasitology, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh Department of Livestock Services, Dhaka, Bangladesh
Babul Chandra Roy
Affiliation:
Department of Parasitology, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
Hiranmoy Biswas
Affiliation:
Department of Parasitology, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh Department of Livestock Services, Dhaka, Bangladesh
Moizur Rahman
Affiliation:
Faculty of Veterinary and Animal Sciences, University of Rajshahi, Rajshahi 6205, Bangladesh
Anisuzzaman Anisuzzaman
Affiliation:
Department of Parasitology, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
Mohammad Zahangir Alam
Affiliation:
Department of Parasitology, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
Md. Hasanuzzaman Talukder*
Affiliation:
Department of Parasitology, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh
*
Author for correspondence: Md. Hasanuzzaman Talukder, E-mail: [email protected]
Author for correspondence: Md. Hasanuzzaman Talukder, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Fasciola gigantica, the causative agent of tropical fasciolosis, is a food-borne zoonotic trematode that affects around 80% livestock of Bangladesh. Triclabendazole (TCBZ), nitroxynil (NTON) and oxyclozanide (OCZN) are frequently used against fascioliasis; however, the current status of potency of these flukicides was unknown. In this study, in vitro efficacy of TCBZ, NTON and OCZN at various concentrations on F. gigantica has been evaluated by relative motility (RM), morphological distortions of apical cone through an inverted microscope, architectural and ultra-structural changes through histopathological and scanning electron microscopy (SEM). It is observed that TCBZ, NTON and OCZN at higher concentrations significantly (P < 0.05) reduced RM of the flukes compared to untreated control. NTON at 150 μg mL−1 was the most potent to reduce the motility within 4 h whereas TCBZ and OCZN were much delayed. Histopathological changes showed swollen, extensive cracking, numerous vacuoles and splitting of the tegument surrounding the spines; spine dislodged from its socket in treated flukes compared to untreated worms. Histopathological changes were more conspicuous at higher doses of TCBZ, NTON and OCZN. SEM has shown the disruption of the apical cone, apart from swelling of the tegument on the ventral surface corrugation and disruption of the ventral apical cone. All these changes indicate that NTON is the most potent in killing flukes in vitro among the tested flukicides and suggest the presence of TCBZ-resistant fluke populations in Bangladesh. It is imperative to explore the in vivo effects of these flukicides and subsequently their molecular mechanisms.

Keywords

BangladeshFasciola giganticaflukicidesfood-borne trematodein vitroscanning electron microscopy
Type
Research Article
Information
Parasitology , Volume 149 , Special Issue 10: Foodborne Trematodes – time to rise from neglected status , September 2022 , pp. 1339 - 1348
Check for updates
Copyright
Copyright © Department of Parasitology, Bangladesh Agricultural University, 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aghayan, S, Gevorgian, H, Ebi, D, Atoyan, HA, Addy, F, Mackenstedt, U, Romig, T and Wassermann, M (2019) Fasciola spp. in Armenia: genetic diversity in a global context. Veterinary Parasitology 268, 21–31.CrossRefGoogle Scholar
Ahasan, SA, Valero, MA, Chowdhury, EH, Islam, MT, Islam, MR, Mondal, MMH, Peixoto, RV, Berinde, L, Panova, M and Mas-Coma, S (2016) CIAS detection of Fasciola hepatica/F. gigantica intermediate forms in bovines from Bangladesh. Acta Parasitologica 61, 267–277.CrossRefGoogle ScholarPubMed
Aktaruzzaman, M, Mohamed, Z, Naim-Ul-Alam, M, Siddiqul Islam, M and Howlader, MR (2015) Evaluation of anthelmintic efficacy of triclabendazole, nitroxynil and albendazole against naturally acquired fascioliasis in cattle of Bangladesh with special reference to its residual effect. International Journal of Pharmacology and Toxicology 3, 1–4.CrossRefGoogle Scholar
Amin, MR and Samad, MA (1988) Clinico-therapeutic studies on bovine fascioliasis. Bangladesh Veterinarian 5, 20–22.Google Scholar
Anderson, HR and Fairweather, I (1988) Fasciola hepatica: scanning electron microscopic observations of juvenile flukes following treatment in vitro with the deacetylated (amine) metabolite of diamphenethide (DAMD). International Journal for Parasitology 18, 827–837.CrossRefGoogle ScholarPubMed
Anderson, HR and Fairweather, I (1995) Fasciola hepatica: ultrastructural changes to the tegument of juvenile flukes following incubation in vitro with the deacetylated (amine) metabolite of diamphencthide. International Journal for Parasitology 25, 319–333.CrossRefGoogle Scholar
Anuracpreeda, P, Chankaew, K, Puttarak, P, Koedrith, P, Chawengkirttikul, R, Panyarachun, B, Ngamniyom, A, Chanchai, S and Sobhon, P (2016) The anthelmintic effects of the ethanol extract of Terminalia catappa L. leaves against the ruminant gut parasite, Fischoederius cobboldi. Parasitology 143, 421.CrossRefGoogle ScholarPubMed
Arafa, WM, Shokeir, KM and Khateib, AM (2015) Comparing an in vivo egg reduction test and in vitro egg hatching assay for different anthelmintics against Fasciola species, in cattle. Veterinary Parasitology 214, 152–158.CrossRefGoogle Scholar
Bennett, JL and Köhler, P (1987) Fasciola hepatica: action in vitro of triclabendazole on immature and adult stages. Experimental Parasitology 63, 49–57.CrossRefGoogle ScholarPubMed
Boray, JC and Happich, FA (1968) Standardised chemotherapeutical tests for immature and mature Fasciola hepática infections in sheep. Australian Veterinary Journal 44, 72–78.CrossRefGoogle ScholarPubMed
Buchanan, J, Fairweather, I, Brennan, G, Trudgett, A and Hoey, E (2003) Fasciola hepatica: surface and internal tegumental changes induced by treatment in vitro with the sulphoxide metabolite of albendazole (‘Valbazen’). Parasitology 126, 141.CrossRefGoogle ScholarPubMed
Chang, ACG and Flores, MJC (2015) Morphology and viability of adult Fasciola gigantica (giant liver flukes) from Philippine carabaos (Bubalus bubalis) upon in vitro exposure to lead. Asian Pacific Journal of Tropical Biomedicine 5, 493–496.CrossRefGoogle Scholar
Charlier, J, Duchateau, L, Claerebout, E, Williams, D and Vercruysse, J (2007) Associations between anti-Fasciola hepatica antibody levels in bulk-tank milk samples and production parameters in dairy herds. Preventive Veterinary Medicine 78, 57–66.CrossRefGoogle ScholarPubMed
Davis, CN, Winters, A, Milic, I, Devitt, A, Cookson, A, Brophy, PM and Morphew, RM (2020) Evidence of sequestration of triclabendazole and associated metabolites by extracellular vesicles of Fasciola hepatica. Scientific Reports 10, 13445.CrossRefGoogle ScholarPubMed
Dawes, B (1966) Experimental fascioliasis: some effects on Fasciola hepatica of treatment of rat hosts with Bithionol (‘Actamer’). Helminthologia 7, 297–307.Google Scholar
Dey, AR, Begum, N, Anisuzzaman, , Alim, MA and Alam, MZ (2020) Multiple anthelmintic resistance in gastrointestinal nematodes of small ruminants in Bangladesh. Parasitology International 77, 102105.CrossRefGoogle ScholarPubMed
Diab, TM, Mansour, HH and Mahmoud, SS (2010) Fasciola gigantica: parasitological and scanning electron microscopy study of the in vitro effects of ivermectin and/or artemether. Experimental Parasitology 124, 279–284.CrossRefGoogle ScholarPubMed
Diyana, JNA, Mahiza, MIN, Latiffah, H, Fazila, SHN, Lokman, IH, Hazfalinda, HN, Chandrawathani, P, Ibitoye, EB and Juriah, K (2020) Occurrence, morphometric, and molecular investigation of cattle and buffalo liver adult fluke in peninsular Malaysia main abattoirs. Journal of Parasitology Research 2020, 5436846.CrossRefGoogle ScholarPubMed
Ebeid, MH, Moustafa, AM, Arnaout, FK, Degheidy, NS, Omer, EA, Shalaby, HA and Abd El-Hamed, AF (2011) In vitro evaluation of anthelmentic efficacy of Balanites egyptiaca on Fasciola gigantica. Benha Veterinary Medical Journal 22, 56–67.Google Scholar
Fairweather, I (2005) Triclabendazole: new skills to unravel an old (ish) enigma. Journal of Helminthology 79, 227–234.CrossRefGoogle ScholarPubMed
Fairweather, I (2009) Triclabendazole progress report, 2005–2009: an advancement of learning? Journal of Helminthology 83, 139–150.CrossRefGoogle ScholarPubMed
Fairweather, I and Boray, JC (1999) Fasciolicides: efficacy, actions, resistance and its management. The Veterinary Journal 158, 81–112.CrossRefGoogle ScholarPubMed
Fairweather, I, Holmes, S and Threadgold, L (1984) Fasciola hepatica: motility response to fasciolicides in vitro. Experimental Parasitology 57, 209–224.CrossRefGoogle ScholarPubMed
Fairweather, I, Anderson, H and Baldwin, T (1987) Fasciola hepatica: tegumental surface alterations following treatment in vitro with the deacetylated (amine) metabolite of diamphenethide. Parasitology Research 73, 99–106.CrossRefGoogle ScholarPubMed
Fairweather, I, Anderson, H and Threadgold, L (1986) Fasciola hepatica: tegumental changes induced in vitro by the deacetylated (amine) metabolite of diamphenethide. Experimental Parasitology 62, 336–348.CrossRefGoogle ScholarPubMed
Fairweather, I, Mcshane, D, Shaw, L, Ellison, S, O'Hagan, N, York, E, Trudgett, A and Brennan, G (2012) Development of an egg hatch assay for the diagnosis of triclabendazole resistance in Fasciola hepatica: proof of concept. Veterinary Parasitology 183, 249–259.CrossRefGoogle ScholarPubMed
Fairweather, I, Brennan, GP, Hanna, REB, Robinson, MW and Skuce, PJ (2020) Drug resistance in liver flukes. International Journal for Parasitology: Drugs and Drug Resistance 12, 39–59.Google ScholarPubMed
Halferty, L, Brennan, GP, Hanna, REB, Edgar, HW, Meaney, MM, McConville, M, Trudgett, A, Hoey, L and Fairweather, I (2008) Tegumental surface changes in juvenile Fasciola hepatica in response to treatment in vivo with triclabendazole. Veterinary Parasitology 155, 49–58.CrossRefGoogle ScholarPubMed
Hanna, REB, Mcmahon, C, Ellison, S, Edgar, HW, Kajugu, PE, Gordon, A, Irwin, D, Barley, JP, Malone, FE, Brennan, GP and Fairweather, I (2015) Fasciola hepatica: a comparative survey of adult fluke resistance to triclabendazole, nitroxynil and closantel on selected upland and lowland sheep farms in Northern Ireland using faecal egg counting, coproantigen ELISA testing and fluke histology. Veterinary Parasitology 207, 34–43.CrossRefGoogle ScholarPubMed
Hoque, MN, Begum, N and Nooruddin, M (2003) Albendazole resistance in gastrointestinal nematode parasites of cattle in Bangladesh. Tropical Animal Health and Production 35, 219–222.CrossRefGoogle ScholarPubMed
Ibarra, OF and Jenkins, DC (1984) An in vitro screen for new fasciolicidal agents. Parasitology Research 70, 655–661.Google Scholar
Islam, M and Ripa, RN (2015) Prevalence of fascioliasis in slaughtered goat in Bengal meat abattoir house and its economic impact on business. Journal of Chemical, Biological and Physical Sciences (JCBPS) 5, 2684.Google Scholar
Islam, MA and Samad, MA (1989) Efficacy of commercial fasciolicides against mixed infection of fascioliasis and amphistomiasis in cattle. Bangladesh Veterinarian 6, 27–32.Google Scholar
Islam, KM, Rahman, M, Islam, MS, Adhikary, GN and Rauf, SMA (2014) Epidemiological studies of fascioliasis (Fasciola gigantica) in black Bengal goats. Eurasian Journal of Veterinary Science 30, 152–156.CrossRefGoogle Scholar
Jeyathilakan, N, Murali, K, Anandaraj, A and Abdul Basith, S (2012) In vitro evaluation of anthelmintic property of ethno-veterinary plant extracts against the liver fluke Fasciola gigantica. Journal of Parasitic Diseases 36, 26–30.CrossRefGoogle ScholarPubMed
Jeyathilakan, N, Murali, K, Anandaraj, A and Abdul Basith, S (2010) In vitro evaluation of anthelmintic property of herbal plants against Fasciola gigantica. Indian Journal of Animal Sciences 80, 1070.Google Scholar
Keiser, J and Morson, G (2008) Fasciola hepatica: tegumental alterations in adult flukes following in vitro and in vivo administration of artesunate and artemether. Experimental Parasitology 118, 228–237.CrossRefGoogle ScholarPubMed
Kelley, JM, Elliott, TP, Beddoe, T, Anderson, G, Skuce, P and Spithill, TW (2016) Current threat of triclabendazole resistance in Fasciola hepatica. Trends in Parasitology 32, 458–469.CrossRefGoogle ScholarPubMed
Khan, M, Anisur Rahman, AKM, Ahsan, S, Ehsan, A, Dhand, N and Ward, MP (2017) Bovine fascioliasis risk factors and space-time clusters in Mymensingh, Bangladesh. Veterinary Parasitology: Regional Studies and Reports 9, 104–109.Google ScholarPubMed
Khatun, M, Asaduzzaman, M, Pallab, M and Chakrabartty, P (2015) Risk factor analysis of fascioliasis in two geo-climatic regions of Bangladesh. International Journal of Science and Research 4, 41–43.Google Scholar
Kiuchi, F, Miyashita, N, Tsuda, Y, Kondo, K and Yoshimura, H (1987) Studies on crude drugs effective on visceral larva migrans. I. Identification of larvicidal principles in betel nuts. Chemical and Pharmaceutical Bulletin 35, 2880–2886.CrossRefGoogle ScholarPubMed
Lorsuwannarat, N, Piedrafita, D, Chantree, P, Sansri, V, Songkoomkrong, S, Bantuchai, S, Sangpairot, K, Kueakhai, P, Changklungmoa, N, Chaichanasak, P, Chansela, P and Sobhon, P (2014) The in vitro anthelmintic effects of plumbagin on newly excysted and 4-weeks-old juvenile parasites of Fasciola gigantica. Experimental Parasitology 136, 5–13.CrossRefGoogle ScholarPubMed
Luo, X, Cui, K, Wang, Z, Li, Z, Wu, Z, Huang, W, Zhu, X-Q, Ruan, J, Zhang, W and Liu, Q (2021) High-quality reference genome of Fasciola gigantica: insights into the genomic signatures of transposon-mediated evolution and specific parasitic adaption in tropical regions. PLoS Neglected Tropical Diseases 15, e0009750.CrossRefGoogle ScholarPubMed
Mas-Coma, S (2003) Adaptation capacities of Fasciola hepatica and their relationships with human fascioliasis: from below sea level up to the very high altitude. Taxonomy, Ecology and Evolution of Metazoan Parasites 2, 81–123.Google Scholar
Mas-Coma, MS, Esteban, JG and Bargues, MD (1999) Epidemiology of human fascioliasis: a review and proposed new classification. Bulletin of the World Health Organization 77, 340–346.Google ScholarPubMed
Mas-Coma, S, Bargues, MD and Valero, MA (2005) Fascioliasis and other plant-borne trematode zoonoses. International Journal for Parasitology 35, 1255–1278.CrossRefGoogle ScholarPubMed
Mckinstry, B, Fairweather, I, Brennan, GP and Forbes, AB (2003) Fasciola hepatica: tegumental surface alterations following treatment in vivo and in vitro with nitroxynil (Trodax). Parasitology Research 91, 251–263.CrossRefGoogle ScholarPubMed
Mckinstry, B, Brennan, GP, Halferty, L, Forbes, AB and Fairweather, I (2007) Ultrastructural changes induced in the tegument and gut of Fasciola hepatica following in vivo and in vitro drug treatment with nitroxynil (Trodax). Parasitology Research 101, 929–941.CrossRefGoogle ScholarPubMed
Meaney, M, Fairweather, I, Brennan, G, Ramasamy, P and Subramanian, P (2002) Fasciola gigantica: tegumental surface alterations following treatment in vitro with the sulphoxide metabolite of triclabendazole. Parasitology Research 88, 315–325.CrossRefGoogle ScholarPubMed
Meaney, M, Fairweather, I, Bernnan, GP, Mcdowell, LSL and Forbes, AB (2003) Fasciola hepatica: effects of the fasciolicide clorsulon in vitro and in vivo on the tegument surface, and a comparison of the effects on young- and old-mature flukes. Parasitology Research 91, 238–250.CrossRefGoogle Scholar
Mehmood, K, Zhang, H, Sabir, AJ, Abbas, RZ, Ijaz, M, Durrani, AZ, Saleem, MH, Ur Rehman, M, Iqbal, MK, Wang, Y, Ahmad, HI, Abbas, T, Hussain, R, Ghori, MT, Ali, S, Khan, AU and Li, J (2017) A review on epidemiology, global prevalence and economical losses of fasciolosis in ruminants. Microbial Pathogenesis 109, 253–262.CrossRefGoogle ScholarPubMed
Mohanta, UK, Ichikawa-Seki, M, Shoriki, T, Katakura, K and Itagaki, T (2014) Characteristics and molecular phylogeny of Fasciola flukes from Bangladesh, determined based on spermatogenesis and nuclear and mitochondrial DNA analyses. Parasitology Research 113, 2493–2501.CrossRefGoogle ScholarPubMed
Novobilský, A and Höglund, J (2015) First report of closantel treatment failure against Fasciola hepatica in cattle. International Journal for Parasitology: Drugs and Drug Resistance 5, 172–177.Google ScholarPubMed
Omran, E and Ahmad, N (2015) Effect of nitroxynil (fasciolid) on adult Fasciola gigantica and Fasciola hepatica in infected cows. Parasitologists United Journal 8, 107–114.CrossRefGoogle Scholar
Opio, LG, Abdelfattah, EM, Terry, J, Odongo, S and Okello, E (2021) Prevalence of fascioliasis and associated economic losses in cattle slaughtered at lira municipality abattoir in northern Uganda. Animals 11, 681.CrossRefGoogle ScholarPubMed
Rahman, AKMA, Islam, SKS, Talukder, MH, Hassan, MK, Dhand, NK and Ward, MP (2017) Fascioliasis risk factors and space-time clusters in domestic ruminants in Bangladesh. Parasites & Vectors 10, 228.CrossRefGoogle ScholarPubMed
Rapic, D, Dzakula, N, Sakar, D and Richards, RJ (1988) Comparative efficacy of triclabendazole, nitroxynil and rafoxanide against immature and mature Fasciola hepatica in naturally infected cattle. The Veterinary Record 122, 59–62.CrossRefGoogle ScholarPubMed
Robinson, MW, Trudgett, A, Hoey, EM and Fairweather, I (2002) Triclabendazole-resistant Fasciola hepatica:[beta]-tubulin and response to in vitro treatment with triclabendazole. Parasitology 124, 325.CrossRefGoogle ScholarPubMed
Rolfe, PF and Boray, JC (1987) Chemotherapy of paramphistomosis in cattle. Australian Veterinary Journal 64, 328–332.CrossRefGoogle ScholarPubMed
Sabourin, E, Alda, P, Vázquez, A, Hurtrez-Boussès, S and Vittecoq, M (2018) Impact of human activities on fasciolosis transmission. Trends in Parasitology 34, 891–903.CrossRefGoogle ScholarPubMed
Saowakon, N, Tansatit, T, Wanichanon, C, Chanakul, W, Reutrakul, V and Sobhon, P (2009) Fasciola gigantica: anthelmintic effect of the aqueous extract of Artocarpus lakoocha. Experimental Parasitology 122, 289–298.CrossRefGoogle ScholarPubMed
Shafiei, R, Sarkari, B, Sadjjadi, SM, Mowlavi, GR and Moshfe, A (2014) Molecular and morphological characterization of Fasciola spp. isolated from different host species in a newly emerging focus of human fascioliasis in Iran. Veterinary Medicine International 2014, 10–20.CrossRefGoogle Scholar
Shalaby, HA, El Namaky, AH and Kamel, ROA (2009) In vitro effect of artemether and triclabendazole on adult Fasciola gigantica. Veterinary Parasitology 160, 76–82.CrossRefGoogle ScholarPubMed
Shalaby, HA, El Namaky, AH and Kamel, ROA (2016) In vitro tegumental alterations on adult Fasciola gigantica caused by mefloquine. Journal of Parasitic Diseases 40, 145–151.CrossRefGoogle ScholarPubMed
Shareef, PAA, Brennan, GP, Mcveigh, P, Khan, MAH, Morphew, RM, Mousley, A, Marks, NJ, Saifullah, MK, Brophy, PM, Maule, AG and Abidi, SMA (2014) Time-dependent tegumental surface changes in juvenile Fasciola gigantica in response to triclabendazole treatment in goat. Acta Tropica 136, 108–117.CrossRefGoogle ScholarPubMed
Skuce, P and Fairweather, I (1990) The effect of the hydrogen ionophore closantel upon the pharmacology and ultrastructure of the adult liver fluke Fasciola hepatica. Parasitology Research 76, 241–250.CrossRefGoogle ScholarPubMed
Soulsby, EJL (2012) Helminths Arthropods and Protozoa of Domesticated Animals. Eastbourne, UK: Baillière, Tindall & Cassell.Google Scholar
Stitt, AW and Fairweather, I (1993) Fasciola hepatica: tegumental surface changes in adult and juvenile flukes following treatment in vitro with the sulphoxide metabolite of triclabendazole (Fasinex). Parasitology Research 79, 529–536.CrossRefGoogle ScholarPubMed
Stitt, A and Fairweather, I (1994) The effect of the sulphoxide metabolite of triclabendazole (‘Fasinex’) on the tegument of mature and immature stages of the liver fluke, Fasciola hepatica. Parasitology 108, 555–567.CrossRefGoogle ScholarPubMed
Talukder, S, Bhuiyan, M, Hossain, M, Uddin, M, Paul, S and Howlader, M (2010) Pathological investigation of liver fluke infection of slaughtered black Bengal goat in a selected area of Bangladesh. Bangladesh Journal of Veterinary Medicine 8, 35–40.CrossRefGoogle Scholar
Tansatit, T, Sahaphong, S, Riengrojpitak, S, Viyanant, V and Sobhon, P (2012) Fasciola gigantica: the in vitro effects of artesunate as compared to triclabendazole on the 3-weeks-old juvenile. Experimental Parasitology 131, 8–19.CrossRefGoogle ScholarPubMed
Toledo, R and Fried, B (2014) Digenetic Trematodes. New York, NY: Springer.CrossRefGoogle Scholar
Valero, MA, Marcos, MD and Mas-Coma, S (1996) A mathematical model for the ontogeny of Fasciola hepatica in the definitive host. Research and Reviews in Parasitology 56, 13–20.Google Scholar
WHO (1995) Control of Food Borne Trematode Infections. Geneva, Switzerland: WHO.Google Scholar
Zerna, G, Spithill, TW and Beddoe, T (2021) Current status for controlling the overlooked caprine fasciolosis. Animals 11, 1819.CrossRefGoogle ScholarPubMed