Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T11:36:49.418Z Has data issue: false hasContentIssue false

Evaluation of anthelmintic drugs against egg development of rumen flukes recovered from cattle raised in the humid tropics of Mexico

Published online by Cambridge University Press:  10 August 2020

R. González-Garduño
Affiliation:
Unidad Regional Universitaria Sursureste, Universidad Autónoma Chapingo, Km 7.5 Carr. Teapa-Vicente Guerrero, Teapa, Tabasco, Mexico
D.O. Ortiz-Pérez
Affiliation:
Facultad De Medicina Veterinaria y Zootecnia, Extensión Pichucalco, Universidad Autónoma de Chiapas, Libramiento de la Ciudad, Boulevard Universitario S/N. Col, Napaná, Chiapas, Mexico
L. Alegría-Jiménez
Affiliation:
Facultad De Medicina Veterinaria y Zootecnia, Extensión Pichucalco, Universidad Autónoma de Chiapas, Libramiento de la Ciudad, Boulevard Universitario S/N. Col, Napaná, Chiapas, Mexico
O.M. Torres-Chable*
Affiliation:
Laboratorio de Enfermedades Tropicales y Transmitidas por Vectores, División Académica de Ciencias Agropecuarias, Universidad Juárez Autónoma de Tabasco, Km. 25, Carretera Villahermosa-Teapa, R/a La Huasteca 2a Seccion, CP, 86298Villahermosa, Tabasco, Mexico
A.A. Cruz-Tamayo
Affiliation:
Escuela Superior de Ciencias Agropecuarias, Universidad Autónoma de Campeche, Campeche, Mexico
C.V. Zaragoza-Vera
Affiliation:
Laboratorio de Enfermedades Tropicales y Transmitidas por Vectores, División Académica de Ciencias Agropecuarias, Universidad Juárez Autónoma de Tabasco, Km. 25, Carretera Villahermosa-Teapa, R/a La Huasteca 2a Seccion, CP, 86298Villahermosa, Tabasco, Mexico
*
Author for correspondence: O.M. Torres-Chable, E-mail: oswaldo.torres@ujat.mx

Abstract

Paramphistomosis is a parasitic disease endemic in ruminants nearly worldwide. In the present study, an in vitro screening of the main anthelmintics used in Mexico was carried out to determine the mean lethal dose for rumen fluke eggs from cattle in a humid, warm region. Rumen flukes were obtained from cattle slaughtered in the states of Tabasco and Chiapas in Mexico. Eggs were collected using a 37-μm sieve and quantified. Then, an in vitro incubation study was performed: 100 eggs were placed into the wells of polystyrene microtiter plates. Anthelmintic products were tested on the eggs at concentrations ranging from 0.0015 to 3.0 mg/ml for rafoxanide, 0.0025 to 10.20 mg/ml for nitroxinil and 0.0015 to 3 mg/ml for closantel to determine the median lethal dose (LD50) and maximum lethal dose (LD99). A control group (water) was included in each plate. Three different species of rumen flukes (Calicophoron brothriophoron, Calicophoron clavula and Paramphistomum cervi) belonging to five isolates were identified. Nitroxinil had the highest efficacy against rumen fluke eggs, with an LD50 of 0.11 to 65 μg/ml, whereas rafoxanide showed the lowest efficacy with an LD50 ranging from 500 to 1713 μg/ml. Closantel showed high variability in the LD50 among the different analysed isolates (17 to 122 μg/ml). The evaluated flukicidal drugs presented differential efficacy against the development of rumen fluke eggs. The efficacy of the drugs will vary depending on the geographical area of origin of the animals.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. 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

Ali, Q, Rashid, I, Shabbir, MZ, Akbar, H, Shahzad, K, Ashraf, K and Chaudhry, U (2018) First genetic evidence for the presence of the rumen fluke Paramphistomum epiclitum in Pakistan. Parasitology International 67(5), 533537.CrossRefGoogle ScholarPubMed
Arias, MSS, Sanchís, M, Francisco, I, et al. (2013) The efficacy of four anthelmintics against Calicophoron daubneyi in naturally infected dairy cattle. Veterinary Parasitology 197, 126129.CrossRefGoogle ScholarPubMed
Canevari, J, Ceballos, L, Sanabria, R, et al. (2014) Testing albendazole resistance in Fasciola hepatica: validation of an egg hatch test with isolates from South America and the United Kingdom. Journal of Helminthology 88, 286292.CrossRefGoogle ScholarPubMed
Cauquil, L, Hüe, T, Hurlin, JC, Mitchell, G, Searle, K, Skuce, P and Zadoks, R (2016) Prevalence and sequence-based identity of rumen fluke in cattle and deer in New Caledonia. PLoS ONE 11(4), 115.CrossRefGoogle ScholarPubMed
Chryssafidis, AL, Fu, Y, De Waal, T and Mulcahy, G (2015) Standardisation of egg-viability assays for Fasciola hepatica and Calicophoron daubneyi: a tool for evaluating new technologies of parasite control. Veterinary Parasitology 210(1–2), 2531.CrossRefGoogle ScholarPubMed
CONAGUA (2019) Servicio Meteorológico Nacional. Normales climatológicas. Resúmenes mensuales de temperatura y lluvia. https://smn.conagua.gob.mx/es/climatologia/temperaturas-y-lluvias/resumenes-mensuales-de-temperaturas-y-lluvias (accesed on March 20, 2019).Google Scholar
Eduardo, SL (1982) The taxonomy of the family Paramphistomidae Fischoeder, 1901 with special reference to the morphology of species occurring in ruminants. I. General considerations. Systematic Parasitology 4(1), 757.CrossRefGoogle Scholar
Fairweather, I, McShane, DD, Shaw, L, Ellison, SE, O'Hagan, NT, York, EA, Trudgett, A and Brennan, GP (2012) Development of an egg hatch assay for the diagnosis of triclabendazole resistance in Fasciola hepatica: proof of concept. Veterinary Parasitology 183(3–4), 249259.CrossRefGoogle Scholar
Ferreras, MC, González-lanza, C, Pérez, V, et al. (2014) Calicophoron daubneyi (Paramphistomidae) in slaughtered cattle in Castilla y León (Spain). Veterinary Parasitology 199(3–4), 268271.CrossRefGoogle Scholar
Fuertes, M, Pérez, V, Benavides, J, González-Lanza, MC, Mezo, M, González-Warleta, M and Ferreras, MC (2015) Pathological changes in cattle naturally infected by Calicophoron daubneyi adult flukes. Veterinary Parasitology 209(3–4), 188196.CrossRefGoogle ScholarPubMed
González-Garduño, R, Hernández-Hernández, JC, Ortiz-Pérez, DO and Torres-Hernández, G (2019) Hematological performance of cattle infected by trematodes in a humid warm climate of Mexico. Pastos y Forrajes 42(3), 185188.Google Scholar
González-Warleta, M, Lladosa, S, Castro-Hermida, JA, Martínez-Ibeas, AM, Conesa, D, Muñoz, F, López-Quílez, A, Manga-González, Y and Mezo, M (2013) Bovine paramphistomosis in Galicia (Spain): prevalence, intensity, aetiology and geospatial distribution of the infection. Veterinary Parasitology 191(3–4), 252263.CrossRefGoogle ScholarPubMed
Huson, KM, Oliver, NAM and Robinson, MW (2017) Paramphistomosis of ruminants: an emerging parasitic disease in Europe. Trends in Parasitology 33(11), 836844.CrossRefGoogle ScholarPubMed
Jones, RA, Brophy, PM, Mitchell, ES and Williams, HW (2017) Rumen fluke (Calicophoron daubneyi) on Welsh farms: prevalence, risk factors and observations on co-infection with Fasciola hepatica. Parasitology 144(2), 237247.CrossRefGoogle ScholarPubMed
Khedri, J, Radfar, MH, Borji, H and Mirzaei, M (2015) Prevalence and intensity of Paramphistomum spp. in cattle from south-eastern Iran. Iranian Journal of Parasitology 10(2), 268272.Google ScholarPubMed
Malrait, K, Verschave, S, Skuce, P, Van Loo, H, Vercruysse, J and Charlier, J (2015) Novel insights into the pathogenic importance, diagnosis and treatment of the rumen fluke (Calicophoron daubneyi) in cattle. Veterinary Parasitology 207(1–2), 134139.CrossRefGoogle ScholarPubMed
Millar, M, Colloff, A and Scholes, S (2012) Disease associated with immature paramphistome infection. Veterinary Record 171, 509510.Google ScholarPubMed
Nikander, S and Saari, S (2007) Notable seasonal variation observed in the morphology of the reindeer rumen fluke (Paramphistomum leydeni) in Finland. Rangifer 27(1), 4757.Google Scholar
Novobilský, A, Amaya Solis, N, Skarin, M and Höglund, J (2016) Assessment of flukicide efficacy against Fasciola hepatica in sheep in Sweden in the absence of a standardised test. International Journal for Parasitology: Drugs and Drug Resistance 6(3), 141147.Google ScholarPubMed
Ojeda-Robertos, NF, Medina-Reynes, A, Garduza-Arias, G and Rangel-Ruiz, LJ (2014) Dinámica de excreción de huevos de Fasciola hepatica y Paramphistomum spp en ganado bovino de Tabasco. Ecosistemas y Recursos Agropecuarios 1(1), 7380.Google Scholar
Pavan Kumar, C, Syaama Sundar, N and Devi Prasad, V (2016) Outbreak of immature paramphistomosis in nellore jodipi sheep. Journal of Parasitic Disease 40, 533535.CrossRefGoogle ScholarPubMed
Pinedo, V, Chávez, V, Casas, A, Suárez, A, Sánchez, P and Huamán, U (2010) Prevalencia de trematodes de la familia Paramphistomatidae en bovinos del distrito de Yurimaguas, provincia de alto Amazonas. Revista de Investigaciones Veterinarias Del Perú 21(2), 161167.Google Scholar
Ploeger, HW, Ankum, L, Moll, L and Holzhauer, M (2017) Presence and species identity of rumen flukes in cattle and sheep in the Netherlands. Veterinary Parasitology 243, 4246.CrossRefGoogle ScholarPubMed
Rahman, M, Kabir, A, Ahmed, S, et al. (2017) Nitroxynil uncouples oxidative phosphorylation in the cell mitochondria and a drug wherever injectables are preferred over drenching. Bangladesh Journal of Veterinary Medicine 15, 9222308.CrossRefGoogle Scholar
Robles-Pérez, D, Martínez-Pérez, JM, Rojo-Vázquez, FA and Martínez-Valladares, M (2014) Development of an egg hatch assay for the detection of anthelmintic resistance to albendazole in Fasciola hepatica isolated from sheep. Veterinary Parasitology 203(1), 217221.CrossRefGoogle ScholarPubMed
Robles-Pérez, D, Martínez-Pérez, JM, Rojo-Vázquez, FA and Martínez-Valladares, M (2015) Screening anthelmintic resistance to triclabendazole in Fasciola hepatica isolated from sheep by means of an egg hatch assay. BMC Veterinary Research 11, 226.CrossRefGoogle ScholarPubMed
Rojo-Vázquez, F, Meana, A, Valcárcel, F and Martínez-Valladares, M (2012) Update on trematode infections in sheep. Veterinary Parasitology 189(1), 1538.CrossRefGoogle Scholar
Rolfe, PF and Boray, JC (1987) Chemotherapy of paramphistomosis in cattle. Australian Veterinary Journal 64(11), 328332.CrossRefGoogle ScholarPubMed
Rothwell, JT, Lacey, E and Sangster, NC (2000) The binding of closantel to ovine serum albumin, and homogenate fractions of Haemonchus contortus. International Journal for Parasitology 30, 769775.CrossRefGoogle ScholarPubMed
Sanabria, REF and Romero, JR (2008) Review and update of paramphistomosis. Helminthologia 45(2), 6468.CrossRefGoogle Scholar
Sanabria, R, Moreno, L, Alvarez, L, Lanusse, C and Romero, J (2014) Efficacy of oxyclozanide against adult Paramphistomum leydeni in naturally infected sheep. Veterinary Parasitology 206(3–4), 277281.CrossRefGoogle ScholarPubMed
Sanchís, J, Sánchez-Andrade, R, Macchi, MI, Piñeiro, P, Suárez, JL, Cazapal-Monteiro, C and Arias, MS (2013) Infection by Paramphistomidae trematodes in cattle from two agricultural regions in NW Uruguay and NW Spain. Veterinary Parasitology 191(1–2), 165171.CrossRefGoogle ScholarPubMed
Sargison, N, Francis, E, Davison, C, Bronsvoort, BMdC, Handel, I and Mazeri, S (2016) Observations on the biology, epidemiology and economic relevance of rumen flukes (Paramphistomidae) in cattle kept in a temperate environment. Veterinary Parasitology 219, 716.CrossRefGoogle Scholar
SAS (2017) SAS/STAT user's guide (S. Inst., Ed.), release 6, Cary, NC, USA.Google Scholar
Swan, GE (1999) The pharmacology of halogenated salicylanilides and their anthelmintic use in animals: review article. Journal of the South African Veterinary Association 70(2), 6170.CrossRefGoogle Scholar
Tehrani, A, Javanbakht, J, Khani, F, Hassan, MA, Khadivar, F, Dadashi, F, Alimohammadi, S and Amani, A (2015) Prevalence and pathological study of Paramphistomum infection in the small intestine of slaughtered ovine. Journal of Parasitic Diseases 39(1), 100106.CrossRefGoogle ScholarPubMed
Toolan, DP, Mitchell, G, Searle, K, Sheehan, M, Skuce, PJ and Zadoks, RN (2015) Bovine and ovine rumen fluke in Ireland-Prevalence, risk factors and species identity based on passive veterinary surveillance and abattoir findings. Veterinary Parasitology 212(3–4), 168174.CrossRefGoogle ScholarPubMed
Zhang, J-L, Si, H-F, Zhou, X-Z, Shang, X-F, Li, B and Zhang, JY (2019) High prevalence of fasciolosis and evaluation of the efficacy of anthelmintics against Fasciola hepatica in buffaloes in Guangxi, China. International Journal for Parasitology. Parasites and Wildlife 8, 8287.CrossRefGoogle ScholarPubMed