SHORT COMMUNICATION
Efficacy of anthelmintic drugs to control Fasciola hepatica in dairy
cattle in Peru
Eficacia de fármacos antihelmínticos para el control de Fasciola hepatica en ganado lechero en Perú
Eficácia de medicamentos anti-helmínticos no controle da Fasciola hepatica em bovinos leiteiros no Peru
Juan Rojas-Moncada1 ; Luz Saldaña1 ; Víctor Urteaga1 ; Roxana Vergara1 ;
Anthony Rojas1 ; Severino Torrel1 ; César Murga-Moreno2,3 ; Luis Vargas-Rocha1,3* .
1Laboratorio de Parasitología Veterinaria y Enfermedades Parasitarias, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av.
Atahualpa 1050, 06003 Cajamarca, Perú.
2Laboratorio de Inmunología e Investigación, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av. Atahualpa 1050, 06003 Cajamarca,
Perú
3Círculo de Estudios e Investigación en Ciencias Veterinarias - CEICIVET, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av.
Atahualpa 1050, 06003 Cajamarca, Perú.
To cite this article:
Rojas-Moncada J, Saldaña L, Urteaga V, Vergara R, Rojas A, Torrel S, Murga-Moreno C, Vargas-Rocha L. Efficacy of anthelmintic
drugs to control Fasciola hepatica in dairy cattle in Peru. Rev Colomb Cienc Pecu 2024; 37(2):101–112. https://doi.org/10.17533/
udea.rccp.v37n2a2
Abstract
Background: Decreasing antiparasitic efficacy of triclabendazole for controlling Fasciola hepatica in dairy cows in the
Cajamarca Valley (Peru) has been reported. Objective: To determine the efficacy of four anthelmintic agents across a broader
area of Cajamarca province. Methods: Four livestock farms were selected from three provinces in the Cajamarca region. Within
each farm, 60 female cattle naturally infected with F. hepatica were chosen. Each farm was divided into four homogeneous groups
based on individual animals and parasite burden. The groups were: triclabendazole (12 mg/kg of BW, VO), clorsulon/ivermectin
(2 mg/kg and 0.2 mg/kg of BW, SC, respectively), closantel (10 mg/kg of BW, VO), and nitroxynil (10 mg/kg of BW, SC). Efficacy
was determined following WAAVP guidelines by measuring the reduction in trematode egg shedding on day 30 post-dosing.
Results: Triclabendazole demonstrated insufficient activity through FERCT and CPCR assessments across all four farms. The
clorsulon/ivermectin and closantel groups exhibited high efficacy in all farms, while nitroxynil showed varying efficacy results
in both types of analysis. Conclusions: Triclabendazole exhibited insufficient activity against F. hepatica. Clorsulon/ivermectin,
closantel, and nitroxynil are viable alternatives with promising outcomes for controlling this trematode in the evaluated provinces.
Received: November 23, 2022. Accepted: September 8, 2023
*Corresponding author. Av. Atahualpa Nº 1050. Facultad de Ciencias Veterinarias - Campus UNC. CEP 060003. Cajamarca, Peru:
E-mail: lvargasr17_1@unc.edu.pe
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License, which permits unrestricted reuse,
distribution, and reproduction in any medium, provided the original work is properly cited.
eISSN: 2256-2958 Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112
https://doi.org/10.17533/udea.rccp.v37n2a2
© 2024 Universidad de Antioquia. Publicado por Universidad de Antioquia, Colombia.
Efficacy of anthelmintic drugs to control Fasciola hepatica in dairy
cattle in Peru
Eficacia de fármacos antihelmínticos para el control de Fasciola hepatica en ganado lechero en Perú
Eficácia de medicamentos anti-helmínticos no controle da Fasciola hepatica em bovinos leiteiros no Peru
Juan Rojas-Moncada1 ; Luz Saldaña1 ; Víctor Urteaga1 ; Roxana Vergara1 ;
Anthony Rojas1 ; Severino Torrel1 ; César Murga-Moreno2,3 ; Luis Vargas-Rocha1,3* .
1Laboratorio de Parasitología Veterinaria y Enfermedades Parasitarias, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av.
Atahualpa 1050, 06003 Cajamarca, Perú.
2Laboratorio de Inmunología e Investigación, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av. Atahualpa 1050, 06003 Cajamarca,
Perú
3Círculo de Estudios e Investigación en Ciencias Veterinarias - CEICIVET, Facultad de Ciencias Veterinarias, Universidad Nacional de Cajamarca, Av.
Atahualpa 1050, 06003 Cajamarca, Perú.
To cite this article:
Rojas-Moncada J, Saldaña L, Urteaga V, Vergara R, Rojas A, Torrel S, Murga-Moreno C, Vargas-Rocha L. Efficacy of anthelmintic
drugs to control Fasciola hepatica in dairy cattle in Peru. Rev Colomb Cienc Pecu 2024; 37(2):101–112. https://doi.org/10.17533/
udea.rccp.v37n2a2
Abstract
Background: Decreasing antiparasitic efficacy of triclabendazole for controlling Fasciola hepatica in dairy cows in the
Cajamarca Valley (Peru) has been reported. Objective: To determine the efficacy of four anthelmintic agents across a broader
area of Cajamarca province. Methods: Four livestock farms were selected from three provinces in the Cajamarca region. Within
each farm, 60 female cattle naturally infected with F. hepatica were chosen. Each farm was divided into four homogeneous groups
based on individual animals and parasite burden. The groups were: triclabendazole (12 mg/kg of BW, VO), clorsulon/ivermectin
(2 mg/kg and 0.2 mg/kg of BW, SC, respectively), closantel (10 mg/kg of BW, VO), and nitroxynil (10 mg/kg of BW, SC). Efficacy
was determined following WAAVP guidelines by measuring the reduction in trematode egg shedding on day 30 post-dosing.
Results: Triclabendazole demonstrated insufficient activity through FERCT and CPCR assessments across all four farms. The
clorsulon/ivermectin and closantel groups exhibited high efficacy in all farms, while nitroxynil showed varying efficacy results
in both types of analysis. Conclusions: Triclabendazole exhibited insufficient activity against F. hepatica. Clorsulon/ivermectin,
closantel, and nitroxynil are viable alternatives with promising outcomes for controlling this trematode in the evaluated provinces.
Received: November 23, 2022. Accepted: September 8, 2023
*Corresponding author. Av. Atahualpa Nº 1050. Facultad de Ciencias Veterinarias - Campus UNC. CEP 060003. Cajamarca, Peru:
E-mail: lvargasr17_1@unc.edu.pe
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License, which permits unrestricted reuse,
distribution, and reproduction in any medium, provided the original work is properly cited.
eISSN: 2256-2958 Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112
https://doi.org/10.17533/udea.rccp.v37n2a2
© 2024 Universidad de Antioquia. Publicado por Universidad de Antioquia, Colombia.
Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112102
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
Keywords: antiparasitic drugs; dairy cattle; bovine; Fasciola hepatica; fascioliasis; farm; parasitology, trematode.
Resumen
Antecedentes: Se ha reportado una disminución de la eficacia antiparasitaria del triclabendazol en el control deFasciola hepatica
en vacas lecheras en el valle de Cajamarca, Perú. Objetivo: Determinar la eficacia antihelmíntica de cuatro antiparasitarios en un
área más amplia de la provincia de Cajamarca. Métodos: Se seleccionaron cuatro predios ganaderos de tres provincias de la región
Cajamarca. En cada predio se seleccionaron 60 hembras bovinas infectadas naturalmente por F. hepatica. Cada predio se dividió
en cuatro grupos homogéneos según los individuos y la carga parasitaria. Los grupos fueron: triclabendazol (12 mg/kg de PV, VO),
clorsulon/ivermectina (2 mg/kg y 0,2 mg/kg de PV, SC, respectivamente), closantel (10 mg/kg de PV, VO), y nitroxinil (10 mg/kg de
PV, SC). La eficacia se determinó siguiendo las directrices de la WAAVP al medir la reducción en puesta de huevos de trematodos el
día 30 posdosificación. Resultados: Por FERCT y CPCR, el triclabendazol fue insuficientemente activo en las cuatro explotaciones.
Los grupos de clorsulon/ivermectina y closantel fueron altamente eficaces en todas las explotaciones y, finalmente, el nitroxinil
mostró eficacia variada en ambos tipos de análisis. Conclusiones: El triclabendazol es insuficientemente activo frente a F. hepatica.
Clorsulon/ivermectina, closantel, y nitroxinil presentan buenos resultados en el control de este trematodo en las provincias evaluadas.
Palabras clave: bovino; fascioliasis; Fasciola hepatica; ganado lechero; medicamentos antiparasitarios; parasitología;
trematodo.
Resumo
Antecedentes: Foi relatada uma diminuição na eficácia antiparasitária do triclabendazol no controle da Fasciola hepatica em
vacas leiteiras no Vale de Cajamarca, Peru. Objetivo: Determinar a eficácia anti-helmíntica de quatro antiparasitários em uma área
maior da província de Cajamarca. Métodos: Foram selecionadas quatro propriedades pecuárias de três províncias da região de
Cajamarca. Em cada propriedade, foram escolhidas 60 fêmeas bovinas naturalmente infectadas porF. hepatica; cada propriedade foi
dividida em quatro grupos homogêneos com base nos animais individuais e na carga parasitária. Os grupos incluíram: triclabendazol
(12 mg/kg kg de PV, VO), clorsulon/ivermectina (2 mg/kg e 0,2 mg/kg de PV, SC, respectivamente), closantel (10 mg/kg de PV, VO)
e nitroxinil (10 mg/kg de PV, SC). A eficácia foi determinada seguindo as diretrizes da WAAVP ao medir a redução na excreção de
ovos de trematódeos no dia 30 pós-dosagem. Resultados: Por meio das avaliações FERCT e CPCR, o triclabendazol demonstrou
atividade insuficiente em todas as quatro propriedades. Os grupos de clorsulon/ivermectina e closantel exibiram alta eficácia em
todas as propriedades, enquanto o nitroxinil apresentou resultados de eficácia variados em ambos os tipos de análise.Conclusões:
O triclabendazol apresentou atividade insuficiente contra F. hepatica. Clorsulon/ivermectina, closantel e nitroxinil são alternativas
viáveis com resultados promissores para o controle desse trematódeo nas províncias avaliadas.
Palavras-chave: bovino; fasciolíase; Fasciola hepatica; gado leiteiro; medicamentos antiparasitários; parasitologia,
trematódeo.
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
Keywords: antiparasitic drugs; dairy cattle; bovine; Fasciola hepatica; fascioliasis; farm; parasitology, trematode.
Resumen
Antecedentes: Se ha reportado una disminución de la eficacia antiparasitaria del triclabendazol en el control deFasciola hepatica
en vacas lecheras en el valle de Cajamarca, Perú. Objetivo: Determinar la eficacia antihelmíntica de cuatro antiparasitarios en un
área más amplia de la provincia de Cajamarca. Métodos: Se seleccionaron cuatro predios ganaderos de tres provincias de la región
Cajamarca. En cada predio se seleccionaron 60 hembras bovinas infectadas naturalmente por F. hepatica. Cada predio se dividió
en cuatro grupos homogéneos según los individuos y la carga parasitaria. Los grupos fueron: triclabendazol (12 mg/kg de PV, VO),
clorsulon/ivermectina (2 mg/kg y 0,2 mg/kg de PV, SC, respectivamente), closantel (10 mg/kg de PV, VO), y nitroxinil (10 mg/kg de
PV, SC). La eficacia se determinó siguiendo las directrices de la WAAVP al medir la reducción en puesta de huevos de trematodos el
día 30 posdosificación. Resultados: Por FERCT y CPCR, el triclabendazol fue insuficientemente activo en las cuatro explotaciones.
Los grupos de clorsulon/ivermectina y closantel fueron altamente eficaces en todas las explotaciones y, finalmente, el nitroxinil
mostró eficacia variada en ambos tipos de análisis. Conclusiones: El triclabendazol es insuficientemente activo frente a F. hepatica.
Clorsulon/ivermectina, closantel, y nitroxinil presentan buenos resultados en el control de este trematodo en las provincias evaluadas.
Palabras clave: bovino; fascioliasis; Fasciola hepatica; ganado lechero; medicamentos antiparasitarios; parasitología;
trematodo.
Resumo
Antecedentes: Foi relatada uma diminuição na eficácia antiparasitária do triclabendazol no controle da Fasciola hepatica em
vacas leiteiras no Vale de Cajamarca, Peru. Objetivo: Determinar a eficácia anti-helmíntica de quatro antiparasitários em uma área
maior da província de Cajamarca. Métodos: Foram selecionadas quatro propriedades pecuárias de três províncias da região de
Cajamarca. Em cada propriedade, foram escolhidas 60 fêmeas bovinas naturalmente infectadas porF. hepatica; cada propriedade foi
dividida em quatro grupos homogêneos com base nos animais individuais e na carga parasitária. Os grupos incluíram: triclabendazol
(12 mg/kg kg de PV, VO), clorsulon/ivermectina (2 mg/kg e 0,2 mg/kg de PV, SC, respectivamente), closantel (10 mg/kg de PV, VO)
e nitroxinil (10 mg/kg de PV, SC). A eficácia foi determinada seguindo as diretrizes da WAAVP ao medir a redução na excreção de
ovos de trematódeos no dia 30 pós-dosagem. Resultados: Por meio das avaliações FERCT e CPCR, o triclabendazol demonstrou
atividade insuficiente em todas as quatro propriedades. Os grupos de clorsulon/ivermectina e closantel exibiram alta eficácia em
todas as propriedades, enquanto o nitroxinil apresentou resultados de eficácia variados em ambos os tipos de análise.Conclusões:
O triclabendazol apresentou atividade insuficiente contra F. hepatica. Clorsulon/ivermectina, closantel e nitroxinil são alternativas
viáveis com resultados promissores para o controle desse trematódeo nas províncias avaliadas.
Palavras-chave: bovino; fasciolíase; Fasciola hepatica; gado leiteiro; medicamentos antiparasitários; parasitologia,
trematódeo.
103Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
Introduction
The trematode Fasciola hepatica has been
reported in multiple countries worldwide to exhibit
resistance to triclabendazole, which has long been
the preferred drug for combating fascioliasis in
both animals and humans (Cabada et al., 2016;
McMahon et al., 2016; Ramadan et al., 2019).
Additionally, instances of resistance in specific
regions have also been documented against
albendazole (Sanabria et al., 2013; Novobilský et
al., 2016; Ceballos et al., 2019), as well as closantel
(Novobilský and Höglund, 2015), and rafoxanide
(Rapic et al., 1988; Elitok et al., 2006).
Association of metabolites with comparable
activity and distinct mechanisms of action
becomes imperative when pharmacological
principles alone do not exhibit efficacy. This
approach broadens the spectrum of activity of
individual drugs, facilitating the treatment of
mixed parasitosis or parasites belonging to the
same phylum. Furthermore, such combinations can
potentially delay the development of resistance to
anthelmintics (Bartram et al., 2012). Incorporation
of active principles with differing mechanisms of
action from diverse chemical groups enhances the
likelihood of achieving synergistic effects (Geary
et al., 2012). Consequently, triclabendazole
-the primary fasciolicide of choice- has been
combined with various anthelmintics, including
clorsulon, ivermectin, levamisole, luxabendazole,
moxidectin, nitroxynil, oxfendazole, oxyclozanide,
among others. Such combinations have
demonstrated improved efficacy (Fairweather
and Boray, 1999; Geurden et al., 2012; Martínez-
Valladares et al., 2014; Khan et al., 2017).
The World Association for the Advancement of
Veterinary Parasitology (WAAVP) recommends
methods and techniques for assessing antiparasitic
efficacy. In controlled trials, efficacy is determined
by comparing the number of live parasites in
treated animals with that in untreated controls.
However, in clinical trials involving live animals,
efficacy is ascertained by comparing fecal egg
count of treated animals to that of the same
untreated animals shortly before or at the time of
treatment and within a period not less than 3 weeks
later (Wood et al., 1995).
Similar to many regions worldwide, Cajamarca
serves as a prominent cattle-raising area where dairy
cattle breeds like Holstein Friesian, Brown Swiss,
and Jersey are extensively reared. Nonetheless,
numerous provinces within Cajamarca are marked
by endemic fascioliasis, affecting both animals
and humans (Cornejo et al., 2010; Rodríguez-
Ulloa et al., 2018; Torrel et al., 2023). This
scenario has prompted prolonged anthelmintic
usage, ultimately leading to the emergence of
anthelmintic resistance due to persistent use
of the same active ingredient. This situation is
exemplified by triclabendazole, specifically within
the Cajamarca district's valley, impacting dairy
cattle (Ortiz et al., 2013). However, this condition
is unknown in other provinces, where evaluation
of alternative fasciolicides has been unexplored.
Thus, the present study assessed the efficacy of
four chemical products, namely triclabendazole,
nitroxynil, clorsulon/ivermectin, and closantel in
four cattle farms within the Cajamarca provinces
-Cajamarca, San Marcos, and San Miguel.
Materials and Methods
Ethical considerations
Farm owners were informed and gave written
authorization for the use of their animals. In
addition, all procedures were in accordance with
the European ethical regulations for the use of
animals in scientific research (European Directive
2010/63/EU).
Location
The study was conducted in four cattle farms
located in three provinces of the Cajamarca region:
Cajamarca (P-I and P-II), San Marcos (P-III), and
San Miguel (P-IV) (Figure 1). Processing and
diagnostic tests were performed at Laboratorio
de Parasitología Veterinaria y Enfermedades
Parasitarias, Facultad de Ciencias Veterinarias of
Universidad Nacional de Cajamarca, Perú.
Experimental design
A cross-sectional study was conducted were
initial sampling included all the animals within
the farms, aiming to confirm positive cases and
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
Introduction
The trematode Fasciola hepatica has been
reported in multiple countries worldwide to exhibit
resistance to triclabendazole, which has long been
the preferred drug for combating fascioliasis in
both animals and humans (Cabada et al., 2016;
McMahon et al., 2016; Ramadan et al., 2019).
Additionally, instances of resistance in specific
regions have also been documented against
albendazole (Sanabria et al., 2013; Novobilský et
al., 2016; Ceballos et al., 2019), as well as closantel
(Novobilský and Höglund, 2015), and rafoxanide
(Rapic et al., 1988; Elitok et al., 2006).
Association of metabolites with comparable
activity and distinct mechanisms of action
becomes imperative when pharmacological
principles alone do not exhibit efficacy. This
approach broadens the spectrum of activity of
individual drugs, facilitating the treatment of
mixed parasitosis or parasites belonging to the
same phylum. Furthermore, such combinations can
potentially delay the development of resistance to
anthelmintics (Bartram et al., 2012). Incorporation
of active principles with differing mechanisms of
action from diverse chemical groups enhances the
likelihood of achieving synergistic effects (Geary
et al., 2012). Consequently, triclabendazole
-the primary fasciolicide of choice- has been
combined with various anthelmintics, including
clorsulon, ivermectin, levamisole, luxabendazole,
moxidectin, nitroxynil, oxfendazole, oxyclozanide,
among others. Such combinations have
demonstrated improved efficacy (Fairweather
and Boray, 1999; Geurden et al., 2012; Martínez-
Valladares et al., 2014; Khan et al., 2017).
The World Association for the Advancement of
Veterinary Parasitology (WAAVP) recommends
methods and techniques for assessing antiparasitic
efficacy. In controlled trials, efficacy is determined
by comparing the number of live parasites in
treated animals with that in untreated controls.
However, in clinical trials involving live animals,
efficacy is ascertained by comparing fecal egg
count of treated animals to that of the same
untreated animals shortly before or at the time of
treatment and within a period not less than 3 weeks
later (Wood et al., 1995).
Similar to many regions worldwide, Cajamarca
serves as a prominent cattle-raising area where dairy
cattle breeds like Holstein Friesian, Brown Swiss,
and Jersey are extensively reared. Nonetheless,
numerous provinces within Cajamarca are marked
by endemic fascioliasis, affecting both animals
and humans (Cornejo et al., 2010; Rodríguez-
Ulloa et al., 2018; Torrel et al., 2023). This
scenario has prompted prolonged anthelmintic
usage, ultimately leading to the emergence of
anthelmintic resistance due to persistent use
of the same active ingredient. This situation is
exemplified by triclabendazole, specifically within
the Cajamarca district's valley, impacting dairy
cattle (Ortiz et al., 2013). However, this condition
is unknown in other provinces, where evaluation
of alternative fasciolicides has been unexplored.
Thus, the present study assessed the efficacy of
four chemical products, namely triclabendazole,
nitroxynil, clorsulon/ivermectin, and closantel in
four cattle farms within the Cajamarca provinces
-Cajamarca, San Marcos, and San Miguel.
Materials and Methods
Ethical considerations
Farm owners were informed and gave written
authorization for the use of their animals. In
addition, all procedures were in accordance with
the European ethical regulations for the use of
animals in scientific research (European Directive
2010/63/EU).
Location
The study was conducted in four cattle farms
located in three provinces of the Cajamarca region:
Cajamarca (P-I and P-II), San Marcos (P-III), and
San Miguel (P-IV) (Figure 1). Processing and
diagnostic tests were performed at Laboratorio
de Parasitología Veterinaria y Enfermedades
Parasitarias, Facultad de Ciencias Veterinarias of
Universidad Nacional de Cajamarca, Perú.
Experimental design
A cross-sectional study was conducted were
initial sampling included all the animals within
the farms, aiming to confirm positive cases and
Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112104
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
prevalence rates. From this, a cohort of 60 female
cows, each exceeding eight months of age, was
meticulously chosen. These cows were positive
for presence of F. hepatica eggs in fecal matter,
with a parasite load equal to or exceeding 1 egg
per gram of feces (EPG). The selection process
involved animals naturally infected within each
farm; specifically, Jersey cows in the first farm and
Holstein cows in the remaining three. Furthermore,
the selected cows had not been subjected to
anthelmintic administration during four months.
They were maintained under similar conditions in
terms of management and feeding, in an extensive
breeding system.
conical-bottomed tube. This amalgamation was
sieved into a 250 mL glass beaker, completing the
volume with running water. The solution was then
left to rest for 30 min. Subsequently, two-thirds
of the supernatant was decanted and replenished
with water for an identical resting period. This
sequence was repeated until the supernatant
exhibited apparent clarity. The ultimate sediment
was augmented with two drops of methylene blue
and placed within a Petri dish for examination
using a stereomicroscope (3X, 4X increases).
Three days after obtaining the
coproparasitological outcomes four groups were
constituted per farm, each with the same number
of individuals (n = 15). Each of these groups
underwent administration of an antiparasitic agent.
The composition of these groups was structured
as follows: triclabendazole at a dose of 12 mg/
kg of BW, VO (Bilevon® 12%, Bayer S.A. Lab.
CIFARMA S.A., Peru); clorsulon at 2 mg/kg of
BW, SC, and ivermectin at 0.2 mg/kg of BW,
SC (Ivomec® F, Boehringer Ingelheim Animal
Health do Brasil Ltda, Brazil); closantel at 10
mg/kg of BW, VO (Fasintel®10, Quimtia, Peru);
and nitroxinil at 10 mg/kg of BW, SC (Nitromic
34%, Lab. Microsules Uruguay S.A., Uruguay).
The volume administered was calculated by
multiplying animal live weight by therapeutic dose
of each active ingredient, and then dividing by the
concentration of the product. Administration of
clorsulon in conjunction with ivermectin did not
intend to link these two substances; rather, it was
due to absence of a commercially available product
in the local market with solely the clorsulon active
ingredient.
Sampling and analysis
At a third visit on day 30 post-dosing,
fecal samples were extracted with the same
procedure conducted during the first visit, and
coproparasitological analyses were performed
again by rapid sedimentation, and the Fecal Egg
Count Reduction Test (FERCT) was applied.
Fecal samples were obtained using the identical
procedure as employed during the initial sampling.
Subsequently, coproparasitological analyses
Figure 1. Location of the study.
Early in the morning (6:00 h) cows were
weighted using bovine-specific metric tape tailored
for the Jersey/Holstein breed. Simultaneously,
fecal samples (approximately 100 g each) were
directly retrieved from the rectum using veterinary
obstetrical gloves. These samples underwent
processing on the same day, employing the
Rapid Sedimentation Technique as outlined by
Lumbreras et al. (1962). Briefly, a homogenization
procedure was employed by mixing four grams
fecal matter with 40 mL running water within a
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
prevalence rates. From this, a cohort of 60 female
cows, each exceeding eight months of age, was
meticulously chosen. These cows were positive
for presence of F. hepatica eggs in fecal matter,
with a parasite load equal to or exceeding 1 egg
per gram of feces (EPG). The selection process
involved animals naturally infected within each
farm; specifically, Jersey cows in the first farm and
Holstein cows in the remaining three. Furthermore,
the selected cows had not been subjected to
anthelmintic administration during four months.
They were maintained under similar conditions in
terms of management and feeding, in an extensive
breeding system.
conical-bottomed tube. This amalgamation was
sieved into a 250 mL glass beaker, completing the
volume with running water. The solution was then
left to rest for 30 min. Subsequently, two-thirds
of the supernatant was decanted and replenished
with water for an identical resting period. This
sequence was repeated until the supernatant
exhibited apparent clarity. The ultimate sediment
was augmented with two drops of methylene blue
and placed within a Petri dish for examination
using a stereomicroscope (3X, 4X increases).
Three days after obtaining the
coproparasitological outcomes four groups were
constituted per farm, each with the same number
of individuals (n = 15). Each of these groups
underwent administration of an antiparasitic agent.
The composition of these groups was structured
as follows: triclabendazole at a dose of 12 mg/
kg of BW, VO (Bilevon® 12%, Bayer S.A. Lab.
CIFARMA S.A., Peru); clorsulon at 2 mg/kg of
BW, SC, and ivermectin at 0.2 mg/kg of BW,
SC (Ivomec® F, Boehringer Ingelheim Animal
Health do Brasil Ltda, Brazil); closantel at 10
mg/kg of BW, VO (Fasintel®10, Quimtia, Peru);
and nitroxinil at 10 mg/kg of BW, SC (Nitromic
34%, Lab. Microsules Uruguay S.A., Uruguay).
The volume administered was calculated by
multiplying animal live weight by therapeutic dose
of each active ingredient, and then dividing by the
concentration of the product. Administration of
clorsulon in conjunction with ivermectin did not
intend to link these two substances; rather, it was
due to absence of a commercially available product
in the local market with solely the clorsulon active
ingredient.
Sampling and analysis
At a third visit on day 30 post-dosing,
fecal samples were extracted with the same
procedure conducted during the first visit, and
coproparasitological analyses were performed
again by rapid sedimentation, and the Fecal Egg
Count Reduction Test (FERCT) was applied.
Fecal samples were obtained using the identical
procedure as employed during the initial sampling.
Subsequently, coproparasitological analyses
Figure 1. Location of the study.
Early in the morning (6:00 h) cows were
weighted using bovine-specific metric tape tailored
for the Jersey/Holstein breed. Simultaneously,
fecal samples (approximately 100 g each) were
directly retrieved from the rectum using veterinary
obstetrical gloves. These samples underwent
processing on the same day, employing the
Rapid Sedimentation Technique as outlined by
Lumbreras et al. (1962). Briefly, a homogenization
procedure was employed by mixing four grams
fecal matter with 40 mL running water within a
105Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
were reiterated utilizing the rapid sedimentation
technique, resulting in the quantification of fecal
egg count (FEC) which was expressed in eggs per
gram (EPG).
Consequently, the anthelmintic effectiveness of
each medication was assessed in accordance with
the protocols stipulated by the WAAVP, employing
the formulation for a fecal egg count reduction test
(FECRT): %reduction = [(X̅ FEC day 0 - X̅ FEC
day 30) / X̅ FEC day 0] x 100, where X̅ represents
the arithmetic mean. Categorization of product
efficacy was defined as highly effective (>98%),
effective (90-98%), moderately effective (80 -
89%), and insufficiently active (<80%) (Wood et
al., 1995). Simultaneously, the percentage of cattle
positive by coprology reduction (CPCR) was also
determined.
To establish more precisely the efficacy of
flukicides in clinical trials involving F. hepatica,
the WAAVP recommends calculating the FEC
of treated animals over a period not less than
3 wk and comparing it to the FEC of the same
animals prior to treatment or at the exact dosing
time. This time frame is justified by the biological
cycle of the trematode. In the early immature
stage (1-4 wk), the trematode is migrating to the
parenchyma, in the late immature stage (6-8 wk),
it is in the prepatent period within the biliary
duct, and in the mature stage (12-14 wk) it resides
in the biliary ducts (Wood et al., 1995). In other
words, immature parasites do not mature and
produce eggs within 30 d, which could introduce
bias during the analysis.
The Wilcoxon test (for paired samples)
was employed using the IBM SPSS Statistics
27.0.1 software to assess whether a statistical
difference exists between EPG on day 0 and
day 30. Differences or similarities in egg count
between day 0 and day 30, as well as efficacies
among the antiparasitic groups within each farm,
were analyzed using the Kruskal-Wallis statistic.
Following this test, the Mann-Whitney U test
was employed to identify distinct groups within
each farm in cases where the Kruskal-Walli’s test
detected statistical differences.
Results
Through FERCT and CPCR assessments,
triclabendazole demonstrated insufficient activity
across all farms. The clorsulon/ivermectin and
closantel groups exhibited high efficacy in all
farms, while nitroxynil showed varying efficacy
results in both types of analysis (Table 1).
Discussion
According to the WAAVP, in clinical trials
conducted on animals naturally infected with
F. hepatica the control period must extend for
at least 21 d (Wood et al., 1995) because adult
flukes could be dying and yet continue to release
eggs, or the eggs stored in the bile duct could be
eliminated. Upon reaching the 30-d mark -as in the
present study- it is assured that adult trematodes
have either died or become infertile as a result
of the antiparasitic treatments. Furthermore, the
possibility of a juvenile parasite developing into
an adult and initiating egg laying within a 30-d
timeframe is not likely. If any juvenile worm were
to migrate to the bile ducts, it would perish due
to the early blood consumption induced by the
administered drugs. If it were to survive, it would
take between two to three months to reach sexual
maturity and commence egg production.
Although the WAAVP envisions studies on
antiparasitic efficacy with control groups, it was
not feasible in the present study since livestock
farmers in the Cajamarca Valley follow a health
calendar that entails three to four mandatory
deworming treatments per year. They strictly
adhere to this schedule and do not allow their
animals to exceed these intervals, even though
they do not perform diagnostic studies to confirm
parasitic infections. If, for any reason, they detect
that their animals are confirmed to have parasites,
they become distressed and do not cooperate in
establishing a control group, making it difficult to
conduct comprehensive studies including control
groups. Therefore, working with control groups is
nearly impossible in this location unless the study
involves the use of the researchers’ own animals.
Nonetheless, clinical studies comparing fecal egg
counts between post-treatment and pre-treatment
stages yield satisfactory results.
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
were reiterated utilizing the rapid sedimentation
technique, resulting in the quantification of fecal
egg count (FEC) which was expressed in eggs per
gram (EPG).
Consequently, the anthelmintic effectiveness of
each medication was assessed in accordance with
the protocols stipulated by the WAAVP, employing
the formulation for a fecal egg count reduction test
(FECRT): %reduction = [(X̅ FEC day 0 - X̅ FEC
day 30) / X̅ FEC day 0] x 100, where X̅ represents
the arithmetic mean. Categorization of product
efficacy was defined as highly effective (>98%),
effective (90-98%), moderately effective (80 -
89%), and insufficiently active (<80%) (Wood et
al., 1995). Simultaneously, the percentage of cattle
positive by coprology reduction (CPCR) was also
determined.
To establish more precisely the efficacy of
flukicides in clinical trials involving F. hepatica,
the WAAVP recommends calculating the FEC
of treated animals over a period not less than
3 wk and comparing it to the FEC of the same
animals prior to treatment or at the exact dosing
time. This time frame is justified by the biological
cycle of the trematode. In the early immature
stage (1-4 wk), the trematode is migrating to the
parenchyma, in the late immature stage (6-8 wk),
it is in the prepatent period within the biliary
duct, and in the mature stage (12-14 wk) it resides
in the biliary ducts (Wood et al., 1995). In other
words, immature parasites do not mature and
produce eggs within 30 d, which could introduce
bias during the analysis.
The Wilcoxon test (for paired samples)
was employed using the IBM SPSS Statistics
27.0.1 software to assess whether a statistical
difference exists between EPG on day 0 and
day 30. Differences or similarities in egg count
between day 0 and day 30, as well as efficacies
among the antiparasitic groups within each farm,
were analyzed using the Kruskal-Wallis statistic.
Following this test, the Mann-Whitney U test
was employed to identify distinct groups within
each farm in cases where the Kruskal-Walli’s test
detected statistical differences.
Results
Through FERCT and CPCR assessments,
triclabendazole demonstrated insufficient activity
across all farms. The clorsulon/ivermectin and
closantel groups exhibited high efficacy in all
farms, while nitroxynil showed varying efficacy
results in both types of analysis (Table 1).
Discussion
According to the WAAVP, in clinical trials
conducted on animals naturally infected with
F. hepatica the control period must extend for
at least 21 d (Wood et al., 1995) because adult
flukes could be dying and yet continue to release
eggs, or the eggs stored in the bile duct could be
eliminated. Upon reaching the 30-d mark -as in the
present study- it is assured that adult trematodes
have either died or become infertile as a result
of the antiparasitic treatments. Furthermore, the
possibility of a juvenile parasite developing into
an adult and initiating egg laying within a 30-d
timeframe is not likely. If any juvenile worm were
to migrate to the bile ducts, it would perish due
to the early blood consumption induced by the
administered drugs. If it were to survive, it would
take between two to three months to reach sexual
maturity and commence egg production.
Although the WAAVP envisions studies on
antiparasitic efficacy with control groups, it was
not feasible in the present study since livestock
farmers in the Cajamarca Valley follow a health
calendar that entails three to four mandatory
deworming treatments per year. They strictly
adhere to this schedule and do not allow their
animals to exceed these intervals, even though
they do not perform diagnostic studies to confirm
parasitic infections. If, for any reason, they detect
that their animals are confirmed to have parasites,
they become distressed and do not cooperate in
establishing a control group, making it difficult to
conduct comprehensive studies including control
groups. Therefore, working with control groups is
nearly impossible in this location unless the study
involves the use of the researchers’ own animals.
Nonetheless, clinical studies comparing fecal egg
counts between post-treatment and pre-treatment
stages yield satisfactory results.
Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112
106
https://doi.org/10.17533/udea.rccp.v37n2a2
Anthelmintic drugs for fascioliasis in cattle
Table 1. Anthelmintic efficacy against F. hepatica within naturally infected cattle across three provinces within Cajamarca region.
Province Prevalence
(% ± 95%CI)
Drug n FERCT CPCR
x̄ EPG ± 95%CI
(day 0)
x̄ EPG ± 95%CI
(day 30)
%Efficacy ±
95%CI
Condition %Efficacy ±
95%CI
Condition
Cajamarca: P-I 80/117
(68.38 ± 8.43)
Triclabendazole 15 6.53 ± 3.62ax 2.47 ± 1.32b 62.24 ± 9.60x IA 33.33 ± 23.86x IA
Clorsulon/Ivermectin 15 6.27 ± 3.03ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 5.93 ± 3.74ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 7.13 ± 2.82ax 0.07 ± 0.13b 99.07 ± 1.82z HE 93.33 ± 12.63z E
Cajamarca: P-II 62/76
(81.58 ± 8.72)
Triclabendazole 15 7.93 ± 5.78ax 6.47 ± 5.65b 18.49 ± 6.98x IA 20 ± 20.24x IA
Clorsulon/Ivermectin 15 7.4 ± 3.17ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 7.8 ± 3.99ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 9.13 ± 3.73ax 0.06 ± 0.13b 99.27 ± 1.43z HE 93.33 ± 12.63z E
San Marcos:
P-III
65/95
(68.42 ± 9.35)
Triclabendazole 15 6.13 ± 3.44ax 3.07 ± 2.50b 50.00 ± 10.22x IA 26.67 ± 22.38x IA
Clorsulon/Ivermectin 15 8.13 ± 3.49ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 7.07 ± 3.63ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 5.73 ± 2.92ax 0.4 ± 0.32b 93.02 ± 5.39z E 66.67 ± 23.86x IA
San Miguel:
P-IV
69/124
(55.65 ± 8.74)
Triclabendazole 15 18.47 ± 5.01ax 16 ± 5.43a 13.36 ± 4.30x IA 0.00 ± 0.00x IA
Clorsulon/Ivermectin 15 20.07 ± 5.71ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 19.13 ± 7.81ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 18.07 ± 8.08ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ±0.00y HE
*EPG: Eggs per gram o feces
a,bDistinct letters within the same row indicate statistical differences in EPG counts between day 0 and day 30 (Wilcoxon test, p<0.05).
x,y,zDistinct letters within the same column within each farm indicate statistical differences in efficacies (Kruskal-Wallis + Mann-Whitney U post hoc, p<0.05).
Dosage: Triclabendazole 12 mg/kg, clorsulon 2 mg/kg, closantel 10 mg/kg, nitroxynil 10 mg/kg, ivermectin 0.2 mg/kg.
Categorization: Insufficiently active (IA), effective (E), and highly effective (HE).
106
https://doi.org/10.17533/udea.rccp.v37n2a2
Anthelmintic drugs for fascioliasis in cattle
Table 1. Anthelmintic efficacy against F. hepatica within naturally infected cattle across three provinces within Cajamarca region.
Province Prevalence
(% ± 95%CI)
Drug n FERCT CPCR
x̄ EPG ± 95%CI
(day 0)
x̄ EPG ± 95%CI
(day 30)
%Efficacy ±
95%CI
Condition %Efficacy ±
95%CI
Condition
Cajamarca: P-I 80/117
(68.38 ± 8.43)
Triclabendazole 15 6.53 ± 3.62ax 2.47 ± 1.32b 62.24 ± 9.60x IA 33.33 ± 23.86x IA
Clorsulon/Ivermectin 15 6.27 ± 3.03ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 5.93 ± 3.74ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 7.13 ± 2.82ax 0.07 ± 0.13b 99.07 ± 1.82z HE 93.33 ± 12.63z E
Cajamarca: P-II 62/76
(81.58 ± 8.72)
Triclabendazole 15 7.93 ± 5.78ax 6.47 ± 5.65b 18.49 ± 6.98x IA 20 ± 20.24x IA
Clorsulon/Ivermectin 15 7.4 ± 3.17ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 7.8 ± 3.99ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 9.13 ± 3.73ax 0.06 ± 0.13b 99.27 ± 1.43z HE 93.33 ± 12.63z E
San Marcos:
P-III
65/95
(68.42 ± 9.35)
Triclabendazole 15 6.13 ± 3.44ax 3.07 ± 2.50b 50.00 ± 10.22x IA 26.67 ± 22.38x IA
Clorsulon/Ivermectin 15 8.13 ± 3.49ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 7.07 ± 3.63ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 5.73 ± 2.92ax 0.4 ± 0.32b 93.02 ± 5.39z E 66.67 ± 23.86x IA
San Miguel:
P-IV
69/124
(55.65 ± 8.74)
Triclabendazole 15 18.47 ± 5.01ax 16 ± 5.43a 13.36 ± 4.30x IA 0.00 ± 0.00x IA
Clorsulon/Ivermectin 15 20.07 ± 5.71ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Closantel 15 19.13 ± 7.81ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ± 0.00y HE
Nitroxynil 15 18.07 ± 8.08ax 0.00 ± 0.00b 100 ± 0.00y HE 100 ±0.00y HE
*EPG: Eggs per gram o feces
a,bDistinct letters within the same row indicate statistical differences in EPG counts between day 0 and day 30 (Wilcoxon test, p<0.05).
x,y,zDistinct letters within the same column within each farm indicate statistical differences in efficacies (Kruskal-Wallis + Mann-Whitney U post hoc, p<0.05).
Dosage: Triclabendazole 12 mg/kg, clorsulon 2 mg/kg, closantel 10 mg/kg, nitroxynil 10 mg/kg, ivermectin 0.2 mg/kg.
Categorization: Insufficiently active (IA), effective (E), and highly effective (HE).
107Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
The prevalence of F. hepatica in the farms
ranged from 55.65 ± 8.74% in San Miguel to
81.58 ± 8.72% in Cajamarca. These results are not
novel, as Cajamarca, particularly the Cajamarca
Valley, is recognized as an endemic area for
fasciolosis due to favorable environmental
conditions for the intermediate host and extensive
breeding. Records of trematodes in animals
exist, even predating 1998 (Claxton et al., 1998).
Various districts in Cajamarca have reported
diverse prevalences of F. hepatica in cattle. In
more distant districts from the Cajamarca Valley,
such as Chota, a prevalence of 20.3 ± 4% has
been found, 45.5 ± 5% in Celendín, 50 ± 5% in
San Juan, and in close areas, 80.7 ± 4.1% in La
Encañada, 61.2 ± 5.6% in Los Baños del Inca,
and 49.5 ± 5% in hamlets of the Cajamarca
district (Torrel et al., 2023).
Due to high prevalence of this trematode in
the Cajamarca Valley, livestock farmers have
the habit of deworming their animals against F.
hepatica every three or four months. Due to the
fact that triclabendazole acts on various stages of
the trematode (Cwiklinski and Dalton, 2018), it
has been indiscriminately used for a long time
without technical considerations throughout the
local livestock sector. Reports of its use even
precede 1998 (Claxton et al., 1998). The average
livestock owner does not conduct clinical
efficacy tests of the antiparasitics used. This
responsibility falls on non-professional livestock
personnel who often fail to accurately calculate
therapeutic doses and neglect drug rotation. This
situation is consistent with observations by other
researchers who have mentioned that resistance
tends to develop when the parasite control relies
exclusively on the same active ingredient over
an extended period, with high frequency of
deworming, suboptimal dosing, indiscriminate
use of antiparasitics, lack of drug rotation, and
the absence of comprehensive technical criteria
(Márquez, 2003; Anziani and Fiel, 2015).
Due to these circumstances, triclabendazole
was reported to be inadequately effective in
controlling F. hepatica in dairy cattle within the
Cajamarca Valley as early as 2012. In one farm
(Tartar) 2.8% efficacy was observed; 3.1% in
the second (El Cortijo); and 68% in a third (San
Vicente) (Rojas-Moncada, 2012). A year later
in the same Valley, in a more rigorous study,
triclabendazole achieved 31.05% efficacy on day
14 and 13.63% on day 30 in cattle (Ortiz et al.,
2013). Simultaneously, reports of F. hepatica
resistance to triclabendazole surfaced in other
regions of Peru (Chávez et al., 2012). This
phenomenon has also been observed worldwide
(Olaechea et al., 2011; Brockwell et al., 2013;
Coyne et al., 2020; Kelley et al., 2020). Even at
a concentration of 24 mg/kg, double the usual
dose, satisfactory results have not been achieved
(Romero et al., 2019). Nevertheless, in areas
where its use is not widespread or where its
introduction is recent, triclabendazole maintains
optimal efficacy (Kouadio et al., 2021).
The local livestock owners with better resources
engage in improved livestock management
and receive guidance from veterinarians to
implement strategic antiparasitic administration,
including drug rotation, which might explain the
high efficacy of clorsulon/ivermectin, closantel,
and nitroxinil. Furthermore, these drugs are
relatively new in the local market compared to
triclabendazole. Other researchers have also found
satisfactory efficacy results. Clorsulon has been
used as an alternative to eliminate the adult phase
of parasites resistant to triclabendazole (Elliott et
al., 2015). While closantel has shown excellent
results in the present study and in other regions
(Borgsteede et al., 2008; Nzalawahe et al., 2018;
Bushra et al., 2019), therapeutic failures have also
been reported (Novobilský and Höglund, 2015).
On the other hand, nitroxinil has yielded optimal
results in the therapeutic management of bovine
fascioliasis and represents an alternative in cases
of triclabendazole resistance in cattle (Wood et
al., 1995; Martínez-Valladares et al., 2010).
Several researchers report that antiparasitic
products with efficacy below 90-95% still
hold value, even if not 100% effective, as they
substantially reduce parasite burden or reach
an economic threshold, thus not significantly
impacting animal health and productivity
(Fairweather, 2011; Forbes, 2013). However, in
the present study triclabendazole did not reach
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
The prevalence of F. hepatica in the farms
ranged from 55.65 ± 8.74% in San Miguel to
81.58 ± 8.72% in Cajamarca. These results are not
novel, as Cajamarca, particularly the Cajamarca
Valley, is recognized as an endemic area for
fasciolosis due to favorable environmental
conditions for the intermediate host and extensive
breeding. Records of trematodes in animals
exist, even predating 1998 (Claxton et al., 1998).
Various districts in Cajamarca have reported
diverse prevalences of F. hepatica in cattle. In
more distant districts from the Cajamarca Valley,
such as Chota, a prevalence of 20.3 ± 4% has
been found, 45.5 ± 5% in Celendín, 50 ± 5% in
San Juan, and in close areas, 80.7 ± 4.1% in La
Encañada, 61.2 ± 5.6% in Los Baños del Inca,
and 49.5 ± 5% in hamlets of the Cajamarca
district (Torrel et al., 2023).
Due to high prevalence of this trematode in
the Cajamarca Valley, livestock farmers have
the habit of deworming their animals against F.
hepatica every three or four months. Due to the
fact that triclabendazole acts on various stages of
the trematode (Cwiklinski and Dalton, 2018), it
has been indiscriminately used for a long time
without technical considerations throughout the
local livestock sector. Reports of its use even
precede 1998 (Claxton et al., 1998). The average
livestock owner does not conduct clinical
efficacy tests of the antiparasitics used. This
responsibility falls on non-professional livestock
personnel who often fail to accurately calculate
therapeutic doses and neglect drug rotation. This
situation is consistent with observations by other
researchers who have mentioned that resistance
tends to develop when the parasite control relies
exclusively on the same active ingredient over
an extended period, with high frequency of
deworming, suboptimal dosing, indiscriminate
use of antiparasitics, lack of drug rotation, and
the absence of comprehensive technical criteria
(Márquez, 2003; Anziani and Fiel, 2015).
Due to these circumstances, triclabendazole
was reported to be inadequately effective in
controlling F. hepatica in dairy cattle within the
Cajamarca Valley as early as 2012. In one farm
(Tartar) 2.8% efficacy was observed; 3.1% in
the second (El Cortijo); and 68% in a third (San
Vicente) (Rojas-Moncada, 2012). A year later
in the same Valley, in a more rigorous study,
triclabendazole achieved 31.05% efficacy on day
14 and 13.63% on day 30 in cattle (Ortiz et al.,
2013). Simultaneously, reports of F. hepatica
resistance to triclabendazole surfaced in other
regions of Peru (Chávez et al., 2012). This
phenomenon has also been observed worldwide
(Olaechea et al., 2011; Brockwell et al., 2013;
Coyne et al., 2020; Kelley et al., 2020). Even at
a concentration of 24 mg/kg, double the usual
dose, satisfactory results have not been achieved
(Romero et al., 2019). Nevertheless, in areas
where its use is not widespread or where its
introduction is recent, triclabendazole maintains
optimal efficacy (Kouadio et al., 2021).
The local livestock owners with better resources
engage in improved livestock management
and receive guidance from veterinarians to
implement strategic antiparasitic administration,
including drug rotation, which might explain the
high efficacy of clorsulon/ivermectin, closantel,
and nitroxinil. Furthermore, these drugs are
relatively new in the local market compared to
triclabendazole. Other researchers have also found
satisfactory efficacy results. Clorsulon has been
used as an alternative to eliminate the adult phase
of parasites resistant to triclabendazole (Elliott et
al., 2015). While closantel has shown excellent
results in the present study and in other regions
(Borgsteede et al., 2008; Nzalawahe et al., 2018;
Bushra et al., 2019), therapeutic failures have also
been reported (Novobilský and Höglund, 2015).
On the other hand, nitroxinil has yielded optimal
results in the therapeutic management of bovine
fascioliasis and represents an alternative in cases
of triclabendazole resistance in cattle (Wood et
al., 1995; Martínez-Valladares et al., 2010).
Several researchers report that antiparasitic
products with efficacy below 90-95% still
hold value, even if not 100% effective, as they
substantially reduce parasite burden or reach
an economic threshold, thus not significantly
impacting animal health and productivity
(Fairweather, 2011; Forbes, 2013). However, in
the present study triclabendazole did not reach
Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112108
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
even 20% efficacy; hence, its use should be
ceased to avoid unnecessary losses, given that the
cost of bovine fasciolosis infection can be quite
high, manifesting as decreased fertility, reduced
weight gain, diminished milk production, liver
condemnations, and poor carcass performance
(Schweizer et al., 2005; Sariözkan and Yalçın,
2011; Charlier et al., 2012; Fanke et al., 2017).
Therefore, control schemes must be cost-effective,
and drug administration should be judicious,
accompanied by regular clinical efficacy
studies. Nevertheless, controlling F. hepatica
requires an integrated approach considering the
epidemiological triad. For instance, cattle are less
infected with F. hepatica in sprinkler-irrigated
pastures, in contrast to flood-irrigated pastures,
which is a common practice in Cajamarca (Torrel-
Pajares et al., 2023).
Although emphasis is being placed on current
techniques for evaluating F. hepatica resistance
and several diagnostic methods are available,
recommended guidelines and standardized
protocols are lacking (Fairweather et al., 2020).
Molecular techniques can be employed to
identify molecular markers of resistance, along
with simpler methods such as the controlled
efficacy test (CET), fecal egg count/reduction
test (FEC/FECRT), coproantigen reduction test
(CRT), and egg hatching assay (EHA). The CRT
has proven to be a solid alternative to FECRT
for evaluating triclabendazole resistance of F.
hepatica in cattle, and its use involves employing
an ELISA kit (Brockwell et al., 2013). However,
the CRT and other techniques entail higher costs
compared to FECRT, which can be implemented
in basic laboratories and field settings, accessible
to most professionals with non-sophisticated and
cost-effective technology. Nonetheless, further
studies comparing these techniques are necessary
to define the best method for assessing drug
resistance of F. hepatica.
In conclusion, triclabendazole is insufficiently
effective against F. hepatica. Antiparasitics based
on clorsulon/ivermectin, closantel or nitroxinil
show good results for controlling the trematode in
the studied zones of Cajamarca region. However,
they should be carefully used -including rotation
and regular clinical evaluations- to prevent
antiparasitic resistance.
Declarations
Acknowledgments
We are grateful to the farm managers where
the study was conducted for allowing us to use
their animals.
Funding
This research did not receive any specific
grant from funding agencies in the public,
commercial, or not-for-profit sectors.
Conflict of interest
The authors declare that they have no known
financial interests or personal relationships that
could have influenced the work presented in this
article.
Author contributions
JRM and ST conceptualized, designed the
methodology, supervised and managed the
research. LS, VU, RV, and AR Executed and
carried out field and laboratory work. LV-R and
CM-M contributed to the software, validation,
data curation and writing-preparation of the
original drafts. All authors collaborated in the
visualization, writing-revising and editing of
the manuscript. All authors approved the final
manuscript and accepted responsibility for its
content.
Use of artificial intelligence (AI)
No AI or AI-assisted technologies were used
during the preparation of this work.
References
Anziani OS, Fiel CA. Resistencia a los
antihelmínticos en nematodos que parasitan a
los rumiantes en la Argentina. RIA Rev Investig
Agropecu 2015; 41(1):34–46.
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
even 20% efficacy; hence, its use should be
ceased to avoid unnecessary losses, given that the
cost of bovine fasciolosis infection can be quite
high, manifesting as decreased fertility, reduced
weight gain, diminished milk production, liver
condemnations, and poor carcass performance
(Schweizer et al., 2005; Sariözkan and Yalçın,
2011; Charlier et al., 2012; Fanke et al., 2017).
Therefore, control schemes must be cost-effective,
and drug administration should be judicious,
accompanied by regular clinical efficacy
studies. Nevertheless, controlling F. hepatica
requires an integrated approach considering the
epidemiological triad. For instance, cattle are less
infected with F. hepatica in sprinkler-irrigated
pastures, in contrast to flood-irrigated pastures,
which is a common practice in Cajamarca (Torrel-
Pajares et al., 2023).
Although emphasis is being placed on current
techniques for evaluating F. hepatica resistance
and several diagnostic methods are available,
recommended guidelines and standardized
protocols are lacking (Fairweather et al., 2020).
Molecular techniques can be employed to
identify molecular markers of resistance, along
with simpler methods such as the controlled
efficacy test (CET), fecal egg count/reduction
test (FEC/FECRT), coproantigen reduction test
(CRT), and egg hatching assay (EHA). The CRT
has proven to be a solid alternative to FECRT
for evaluating triclabendazole resistance of F.
hepatica in cattle, and its use involves employing
an ELISA kit (Brockwell et al., 2013). However,
the CRT and other techniques entail higher costs
compared to FECRT, which can be implemented
in basic laboratories and field settings, accessible
to most professionals with non-sophisticated and
cost-effective technology. Nonetheless, further
studies comparing these techniques are necessary
to define the best method for assessing drug
resistance of F. hepatica.
In conclusion, triclabendazole is insufficiently
effective against F. hepatica. Antiparasitics based
on clorsulon/ivermectin, closantel or nitroxinil
show good results for controlling the trematode in
the studied zones of Cajamarca region. However,
they should be carefully used -including rotation
and regular clinical evaluations- to prevent
antiparasitic resistance.
Declarations
Acknowledgments
We are grateful to the farm managers where
the study was conducted for allowing us to use
their animals.
Funding
This research did not receive any specific
grant from funding agencies in the public,
commercial, or not-for-profit sectors.
Conflict of interest
The authors declare that they have no known
financial interests or personal relationships that
could have influenced the work presented in this
article.
Author contributions
JRM and ST conceptualized, designed the
methodology, supervised and managed the
research. LS, VU, RV, and AR Executed and
carried out field and laboratory work. LV-R and
CM-M contributed to the software, validation,
data curation and writing-preparation of the
original drafts. All authors collaborated in the
visualization, writing-revising and editing of
the manuscript. All authors approved the final
manuscript and accepted responsibility for its
content.
Use of artificial intelligence (AI)
No AI or AI-assisted technologies were used
during the preparation of this work.
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los rumiantes en la Argentina. RIA Rev Investig
Agropecu 2015; 41(1):34–46.
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https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
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gastrointestinal nematodes and liver fluke in
cattle. Vet Parasitol 2008; 155(3–4):235–241.
https://doi.org/10.1016/j.vetpar.2008.05.004
Brockwell YM, Elliott TP, Anderson GR, Stanton
R, Spithill TW, Sangster NC. Confirmation of
Fasciola hepatica resistant to triclabendazole in
naturally infected Australian beef and dairy cattle.
Int J Parasitol Drugs Drug Resist 2013; 4(1):
48–54. https://doi.org/10.1016/j.ijpddr.2013.11.005
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hepatica research using 'omics' technologies.
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against natural liver fluke infection in cattle. Vet
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org/10.1016/j.vetpar.2005.10.008
Elliott TP, Kelley JM, Rawlin G, Spithill TW.
High prevalence of fasciolosis and evaluation
of drug efficacy against Fasciola hepatica
in dairy cattle in the Maffra and Bairnsdale
districts of Gippsland, Victoria, Australia.
Vet Parasitol 2015; 209(1–2):117–124.
https://doi.org/10.1016/j.vetpar.2015.02.014
Fairweather I, Boray JC. Fasciolicides:
efficacy, actions, resistance and its
management. Vet J 1999;158(2):81–112.
https://doi.org/10.1053/tvjl.1999.0377
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
Bartram DJ, Leathwick DM, Taylor MA, Geur-
den T, Maeder SJ. The role of combination
anthelmintic formulations in the sustainable con-
trol of sheep nematodes. Vet Parasitol 2012;
186(3–4):151–158. https://doi.org/10.1016/j.vet-
par.2011.11.030
Borgsteede FH, Taylor SM, Gaasenbeek CP,
Couper A, Cromie L. The efficacy of an ivermectin/
closantel injection against experimentally
induced infections and field infections with
gastrointestinal nematodes and liver fluke in
cattle. Vet Parasitol 2008; 155(3–4):235–241.
https://doi.org/10.1016/j.vetpar.2008.05.004
Brockwell YM, Elliott TP, Anderson GR, Stanton
R, Spithill TW, Sangster NC. Confirmation of
Fasciola hepatica resistant to triclabendazole in
naturally infected Australian beef and dairy cattle.
Int J Parasitol Drugs Drug Resist 2013; 4(1):
48–54. https://doi.org/10.1016/j.ijpddr.2013.11.005
Bushra M, Shahardar RA, Allaie IM, Wani
ZA. Efficacy of closantel, fenbendazole and
ivermectin against GI helminths of cattle in central
Kashmir. Journal of parasitic diseases: official
organ of the Indian Society for Parasitology
2019; 43(2):289–293. https://doi.org/10.1007/
s12639-019-01091-w
Cabada MM, Lopez M, Cruz M, Delgado JR, Hill
V, White AC Jr. Treatment Failure after Multiple
Courses of Triclabendazole among Patients
with Fascioliasis in Cusco, Peru: A Case Series.
PLoS Negl Trop Dis 2016; 10(1):e0004361.
https://doi.org/10.1371/journal.pntd.0004361
Ceballos L, Canton C, Pruzzo C, Sanabria
R, Moreno L, Sanchis J, Suarez G, Ortiz P,
Fairweather I, Lanusse C, Alvarez L, Martinez-
Valladares M. The egg hatch test: A useful
tool for albendazole resistance diagnosis in
Fasciola hepatica. Vet Parasitol 2019; 271:7–13.
https://doi.org/10.1016/j.vetpar.2019.06.001
Charlier J, Van der Voort M, Hogeveen H,
Vercruysse J. ParaCalc® - A novel tool to evaluate
the economic importance of worm infections on the
dairy farm. Vet Parasitol 2012; 184(2–4):204–211.
https://doi.org/10.1016/j.vetpar.2011.09.008
Chávez A, Sánchez L, Arana C, Suárez F.
Resistencia a antihelmínticos y prevalencia de
fasciolosis bovina en la ganadería lechera de
Jauja, Perú. Rev Inv Vet Perú 2012; 23(1):90–97.
https://doi.org/10.15381/rivep.v23i1.887
Claxton JR, Zambrano H, Ortiz P, Delgado
E, Escurra E, Clarkson MJ. Strategic control
of fasciolosis in the inter-Andean valley of
Cajamarca, Peru. Vet Rec 1998; 143(2):42–45.
https://doi.org/10.1136/vr.143.2.42
Cornejo H, Oblitas F, Cruzado S, Quispe W.
Evaluation of an ELISA test with Fasciola
hepatica metabolic antigen for diagnosis of
human fascioliasis in Cajamarca, Peru. Rev Peru
Med Exp Salud Publica 2010; 27(4):569–574.
https://doi.org/10.17843/rpmesp.2010.274.1529
Coyne LA, Bellet C, Latham SM, Williams D.
Providing information about triclabendazole
resistance status influences farmers to change
liver fluke control practices. Vet Rec 2020;
187(9):357. https://doi.org/10.1136/vr.105890
Cwiklinski K, Dalton JP. Advances in Fasciola
hepatica research using 'omics' technologies.
Int J Parasitol 2018; 48(5):321–331. https://doi.
org/10.1016/j.ijpara.2017.12.001
Elitok B, Elitok OM, Kabu M. Field trial on
comparative efficacy of four fasciolicides
against natural liver fluke infection in cattle. Vet
Parasitol 2006; 135(3–4):279–85. https://doi.
org/10.1016/j.vetpar.2005.10.008
Elliott TP, Kelley JM, Rawlin G, Spithill TW.
High prevalence of fasciolosis and evaluation
of drug efficacy against Fasciola hepatica
in dairy cattle in the Maffra and Bairnsdale
districts of Gippsland, Victoria, Australia.
Vet Parasitol 2015; 209(1–2):117–124.
https://doi.org/10.1016/j.vetpar.2015.02.014
Fairweather I, Boray JC. Fasciolicides:
efficacy, actions, resistance and its
management. Vet J 1999;158(2):81–112.
https://doi.org/10.1053/tvjl.1999.0377
Rev Colomb Cienc Pecu 2024; 37(2, Apr-Jun):101–112110
https://doi.org/10.17533/udea.rccp.v37n2a2Anthelmintic drugs for fascioliasis in cattle
Fairweather I, Brennan GP, Hanna REB, Robin-
son MW, Skuce PJ. Drug resistance in liver flukes.
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vetpar.2017.03.018
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Himmelstjerna G, Maeder S, Holdsworth P,
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org/10.1016/j.vetpar.2012.09.004
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comparative efficacy of a moxidectin plus
triclabendazole pour-on solution against adult
and immature liver fluke, Fasciola hepatica, in
cattle. Vet Parasitol 2012; 189(2–4):227–232.
https://doi.org/10.1016/j.vetpar.2012.04.019
Kelley JM, Rathinasamy V, Elliott TP, Rawlin
G, Beddoe T, Stevenson MA, Spithill TW.
Determination of the prevalence and intensity
of Fasciola hepatica infection in dairy cattle
from six irrigation regions of Victoria, South-
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triclabendazole resistance on three properties.
Vet Parasitol 2020; 277:109019. https://doi.
org/10.1016/j.vetpar.2019.109019
Khan MN, Sajid MS, Rizwan HM, Qudoos A,
Abbas RZ, Riaz M, Khan MK. Comparative
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natural infection of fasciola species in sheep. Pak
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Kouadio JN, Evack JG, AChi LY, Balmer O,
Utzinger J, N'Goan E, Bonfoh B, Hattendorf
J, Zinsstag J. Efficacy of triclabendazole and
albendazole against Fasciola spp. infection in
cattle in Côte d'Ivoire: a randomised blinded
trial. Acta Trop 2021; 222:106039. https://doi.
org/10.1016/j.actatropica.2021.106039
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un procedimiento de sedimentación rápida para
investigar huevos de Fasciola hepatica en las
heces, su evaluación y uso en el campo. Rev Per
Med 1962; 31:167–174.
Márquez D. Resistencia a los antihelmínticos:
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Agropecuaria 2003; 4(1):55–71. https://doi.
org/10.21930/rcta.vol4_num1_art:14
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Rojo-Vázquez FA. Efficacy of an anthelmintic
combination in sheep infected with Fasciola
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