Received: 15/07/2024 Accepted: 05/10/2024 Published: 06/01/2025 1 of 6
https://doi.org/10.52973/rcfcv-e35491 RevistaCientíca,FCV-LUZ/Vol.XXXV
ABSTRACT
Equine parascarosis is a Worldwide endoparasitosis, caused by
Parascaris spp., affecting mainly younger horses. This disease is
considered as the most pathogenic parasitosis of young horses.
In Algeria, no knowledge of the resistance of Parascaris spp. to
Ivermectin is published. For this reason, the present study aims
to evaluate the frequency of Parascaris spp. and the anthelmintic
efcacy of Ivermectin and Fenbendazole against this parasite
in a foal population in Tiaret, Algeria. Ninety–one foals were
examined for the presence of Parascaris spp. from two stud farms.
Among the positive, thirty–two faols were treated with Ivermectin
formulations (Ivoral® and Eqvalan®) and Fenbendazole (Funcur®)
at their recommended dosages. Fecal egg count reduction testing
(FECRT) was used to determine the efcacy of each anthelmintic.
Parascaris spp. was detected in 61 foals (67.03%). Decreased
efcacy (reduction of Parascaris spp. fecal egg counts by less than
90%) was found for the two Ivermectin formulations (46.45% for
Ivoral® and 70.29% for Eqvalan®). Nevertheless, fenbendazole
showed 100% efcacy in all foals sampled in this study. These rst
data indicate that Ivermectin–resistant Parascaris spp. populations
are present on horse farms in Algeria. Findings from this study
can be used to create a more sustainable approach for parasite
control programs.
Key words: Parascaris spp.; foals; frequency; ivermectin;
resistance; Tiaret
RESUMEN
La parascarosis equina es una endoparsitosis mundial, causada
por Parascaris spp., que afecta principalmente a caballos
jóvenes, siendo esta enfermedad parasitaria más patógena de
los potros. En Argelia no se tiene conocimiento de la resistencia
de Parascaris spp. la ivermectina. Por esta razón, el presente
estudio tiene como objetivo evaluar la frecuencia de Parascaris
spp. y la ecacia antihelmíntica de Ivermectina y Fenbendazol
contra este parásito en una población de potros en Tiaret, Argelia.
Se examinaron noventa y un potros para detectar la presencia
de Parascaris spp. procedentes de dos ganaderías. Entre los
positivos, treinta y dos potros fueron tratados con formulaciones
de Ivermectina (Ivoral® y Eqvalan®) y Fenbendazol (Funcur®) en
sus dosis recomendadas. Se utilizó la prueba de reducción del
recuento de huevos en heces (FECRT) para determinar la ecacia
de cada antihelmíntico. Parascaris spp. se detectó en 61 potros
(67,03 %). Se encontró una ecacia disminuida (reducción del
recuento de huevos fecales de Parascaris spp. en menos del 90 %)
para las dos formulaciones de ivermectina (46,45 % para Ivoral®
y 70,29 % para Eqvalan®). Sin embargo, el fenbendazol mostró
una ecacia del 100 % en todos los animales de un año incluidos
en la muestra de este estudio. Estos primeros datos indican que
existen poblaciones de Parascaris spp. resistentes a la ivermectina
en granjas de caballos en Argelia. Los hallazgos de este estudio
se pueden utilizar para crear un enfoque más sostenible para los
programas de control de parásitos.
Palabras clave: Parascaris spp.; potros; frecuencia; ivermectina;
resistencia; Tiaret
First report of ivermectin resistance in natural infected Foals by
Parascaris spp. in Tiaret, Algeria
Primer informe de resistencia a ivermectina en potros infectados
de forma natural por Parascaris spp. en Tiaret, Argelia
Selles Sidi Mohammed Ammar
1,2
, Ait Amrane Amar
1,2
, Kouidri Mokhtaria
1,3
* , Belhamiti Belkacem Tahar
1,2
,
Belmedjahad Mustapha
4
, Bouchentouf Keltoum
5
, Kadi Marwa
5
, Mihoubi Amel
5
1
University of Tiaret, Laboratory of research on local animal products. Tiaret, Algeria.
2
University of Tiaret, Veterinary Sciences Institute. Tiaret, Algeria.
3
University of Tiaret, Farm animal reproduction laboratory. Tiaret, Algeria.
4
Chaou Chaoua National Stud. Tiaret, Algeria.
5
University of Tiaret, Nature and Life Sciences Faculty. Tiaret, Algeria.
*Corresponding author: mokhtariakouidri@yahoo.fr
Resistance to Ivermectin by Parascaris spp. in Tiaret, Algeria / Ammar et al._________________________________________________________
2 of 6 3 of 6
INTRODUCTION
Internal parasitic infections are Worldwide pathologies in foals
and young horses [1, 2]. Although Strongylus spp. in particular
Strongylus vulgaris is rare nowadays in horses (Equus caballus)
given the routine deworming programs on farms [3]. Ascarids
(Parascaris spp.), are common and ubiquitous equine parasite
[4], and are considered the most pathogenic parasite in young
horses, especially in foals [3, 5, 6]. It is a nematode belonging
to the family Ascarididae [6]. Two species of Parascaris have
been described, P. equorum and P. univalens [7], these are
morphologically indistinguishable and are seldom distinguished
[8]. In adult horses, infection is generally rare and less intense
because protective immunity against P. equorum starts to develop
at 6 months of age–old [6]. Parascaris infection manifests as nasal
discharge and coughing [9], slow growth, weight loss, cough, and
colic [8, 10, 11]. When worm burdens are numerous, adult ascarids
cause intestinal obstruction, intussusception, or even rupture [6].
Several studies have shown that few compounds are approved
for the treatment of roundworms in various countries [3, 6,
12]. These drugs are the primary means of controlling internal
parasites in horses, and their use can have benecial effects on
the growth and performance of horses [13]. Three classes of
drugs are used for the control of ascarids: benzimidazole (e.g.,
fenbendazole, oxibendazole), tetrahydro pyrimidine (e.g., pyrantel),
and macrocyclic lactones (e.g., ivermectin, moxidectin) [3, 4, 6,
12, 14, 15]. The nematocidal and larvicidal activity as well as the
effect on target migrating larval stages of macrocyclic lactones
make these drugs frequently used in foals and young horses [6].
Nevertheless, the extensive use of anthelmintic drugs has led to
the development of anthelmintic resistance in several parasites of
veterinary importance [11]. This resistance in intestinal nematodes
of horses is considered a global problem [16].
In the last decades, the anthelmintic resistance has made the
control of ascarids more difcult mainly due to the decrease in the
activity of ivermectin (IVM), which was initially very active on these
parasites [3]. Likewise, has allowed the emergence of Parascaris
populations resistant to all major classes of anthelmintics in many
countries [17].
The resistance of Parascaris spp. to ivermectin was reported for
the rst time in the Netherlands by Boersema et al. [18]. Since,
several studies have mentioned this resistance to ivermectin in
various parts of the world [2, 10, 14, 17, 19, 20, 21, 22, 23, 24].
In Algeria, the only anthelmintic resistance data refer to the study
by Kouidri and Selles [25] on the resistance of intestinal strongyles
to benzimidazoles in foals, but since then and to our knowledge, no
additional data has been published on the resistance of Parascaris
spp. to ivermectin. This study aimed to evaluate the frequency of
Parascaris spp. and the Ivermectin and Fenbendazole efcacy
against this parasite in yearling’s population in Tiaret, Algeria.
MATERIAL AND METHODS
Study area
The present study was conducted in the Tiaret area (western
Algeria), from November 2019 to February 2020. Tiaret is located
340 km from the capital Algiers in the north–west of Algeria at
the latitude of 35°15' N and longitude of 1°26' E. Climatologically,
this region is a semi–arid area characterized by cold and humid
winter and hot and dry summer. The foals studied belong to the
Chaouchaoua National stud farm and a private farm
Horses
Ninety–one foals (46 colts and 45 llies) aged between six
months to 2 years belonging to two main breeds (Arabian and
Barb) and having not been dewormed at least 8 weeks before the
test was included in this study.
Study design
Collecting samples
Fecal samples were collected from fresh deposits in the bedding
but were always positively associated with a particular horse (care
was taken to remove the surface parts of the dung, which had not
been in contact with the soil). Each fecal sample was placed in a
labeled plastic bag (containing the name, breed, date of birth of
the horse, and date of collection). These samples were transported
to the Parasitology Laboratory of the Veterinary Institute of Tiaret,
Algeria. In general, samples were processed on the same day, or
stored at 4°C in in the refrigerator (Condor, Algeria) until been
processed (not to exceed 4 days) following sampling.
Microscopic examination (Optika, Italy) of the presence of
Parascaris spp. eggs were performed after fecal flotation in the
saturated salt solution. Parasite egg counts were carried out using the
modied McMaster technique [26] 3 g of feces to 42 mL NaCl solution
(specic gravity of 1.2). The nal number of eggs counted in two
chambers was multiplied by 50 to give the EPG egg per gram (EPG).
Group treatments
Thirty–tow foals infected by Parascaris spp. (with a number of
eggs per gram of fecal matter greater than or equal to 100) were
divided into three groups and received anthelmintic treatments
respectively: Gr01: twelve foals : Ivoral (Ivermectin 0.8 mg·ml
-1
,
0.32 mg·kg
-1
in oral suspension, Algeria), Gr 02 seven foals: Eqvalan
(Ivermectin 18,7 mg·g
-1
oral paste, 1.07 g of dough per 100 kg of
live weight, France) and Gr 03: thirteen foals Funcur (Fenbendazole
2.5%, 10 mg·kg
-1
in oral suspension, Algeria). The weight was
estimated by the Zoometric tape (Virbac, France), which allows
us to indicate the weight in kg using the chest measurement. The
oral solutions were administered using an applicator gun.
Fecal egg count reduction test (%)
The efcacy of treatment was evaluated based on the reduction
between pre–and post–treatment FEC (Fecal egg count) for each
horse separately and on the arithmetic mean reduction between
pre–and post–treatment FEC per treatment. To perform a FEC
Reduction Test (FECRT) a fecal egg count should be performed on
day (d) 0 and again on d 14. FECRT (%) was calculated according
Resistance to Ivermectin by Parascaris spp. in Tiaret, Algeria / Ammar et al._________________________________________________________
___________________________________________________________________________________________________Revista Cientica, FCV-LUZ / Vol. XXXV
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to the American Association of Equine (AAEP) Parasite Control
Guidelines [27]. Using the equation below, the FECR (%) for each
horse in the group was calculated individually. The formula used
to calculate FECRT (%):
FECRT %
^ h
=
Egg Reduction (%)
=
EPG Pre
-
Treatment
^ h
EPG Pre
-
Treatment
^ h
-
EPG 14 days Post
-
Treatment
^ h
#
100
While equine–specic criteria are yet to be established to dene
the presence of resistance, the AAEP Parasite Control Guidelines
[27] recommend using a reduction of mean fecal egg count < 95%.
When fecal egg counts increased for an individual horse after
treatment, the percentage FECRT was considered to be zero to
avoid negative percentages.
RESULTS AND DISCUSSION
Parascaris spp. was detected in 61 yearlings with a prevalence
of 67.03% (61/91). In the present study, the frequency was higher
than 53% reported in Saudi Arabia by Alanazi et al. [17] and 58.3%
in Australia noticed by Armstrong et al. [14]. Likewise, this rate is
high than those cited by Aromaa et al. [1] and Näreaho et al. [28]
in Finland with rates of 11.5% and 21%, respectively. The same
is high compared to that suggested by Laugier et al. [6] in France
at 30.5% and Studziska et al. [10] in Poland at 40%. A lower
rate (6.3%) was observed by Scala et al. [12] in Italy. Othman
and Alzuheir [29] mentioned a lower prevalence rate (15.6%) in
West Bank Palestine. However, these same authors noted a high
prevalence in Jericho city with a rate of 70%. This higher rate
of infection in the present study might be due to the number of
analyzed samples that were lower than the other studies. Often,
the foals of the current study grazed in open fields, this can
contaminate the grazing environment and consequently ensures
the infection or reinfection of sensitive animals.
In this study, only 32 foals were used to determine FECRT. The
foals considered in this study had EPG levels with a minimum of
100 and a maximum of 10100 and their mean fecal egg count
varied between groups from 566.67 to 2800.
TABLE I shows the summary of the results of FECRT. The FECRT
values on day 14 (D14) in each treatment group were 46.74%,
70.29%, and 100% (groups treated with Ivoral, Eqvalan, and
Funcur, respectively).
This is the rst report of Parascaris spp. resistance to Ivermectin
in Algeria. The FECRT showed that at two weeks post–treatment,
the efciency percentages were much lower than 95% (46.45%
and 70.29% for Ivoral and Eqvalan, respectively). Our detected
FECR values suggest resistance to Ivermectin. Previous studies
have described a decrease in the efcacy of Ivermectin in different
parts of the world including Europe [2, 5, 6, 10, 18, 19, 20, 21,
28, 30, 31, 32, 33, 34], North America [24, 30, 35, 36], Australia
and New Zealand [14, 37, 38] and in Arab Gulf States [17]. Several
factors can cause the development of resistance to Ivermectin
among them we can mention the use of Ivermectin in mares, which
yields a high content of this molecule in their milk secretions and
consequently a sub–optimal exposure of parasite populations.
This underdosing is a significant factor in the emergence of
drug–resistant isolates [39, 40]. Additionally, the administration
of anthelmintics to foals during their rst month of life and then
in a repeated manner at intervals of less than three months to
reduce environmental contamination from eggs contributes to
the development of resistant ascarid populations [5, 41, 42, 43].
In the present study, intensive use of the Ivoral in the two farms
was found for its low price. Fritzen et al. [44] also reported that
intensive use of Ivermectin appears to be associated with the
development of resistance in Parascaris spp. populations. Whereas,
Pérez et al. [45] noted that plasma levels of Ivermectin can persist
TABLE I
Results of fecal egg count reduction per foal and arithmetic mean following treatments with Ivoral, Eqvalan and Funcur
Yearlings
Ivoral Eqvalan Funcur
EPG1
(0 D)
EPG2
(14 D)
reduction
(%)
EPG1
(0 D)
EPG2
(14 D)
reduction
(%)
EPG1
(0 D)
EPG2
(14 D)
reduction
(%)
1
100 50 50 2950 2500 15.25 850 0 100
2
350 950 0 10100 5250 48.02 1800 0 100
3
1150 50 95.65 5650 1200 78.76 1200 0 100
4
2500 50 98 100 50 50 1600 0 100
5
150 100 33.33 100 0 100 400 0 100
6
150 250 0 150 0 100 100 0 100
7
200 100 50 550 0 100 150 0 100
8
200 50 75 1200 0 100
9
350 100 71.43 350 0 100
10
1200 150 87.5 300 0 100
11
200 300 0 700 0 100
12
250 400 0 450 0 100
13
350 0 100
Mean of EPG
566.67 212.5 62.5 2800 1285.71 54.08 726.92 0 100
Mean of %
46.45 70.29 100
Resistance to Ivermectin by Parascaris spp. in Tiaret, Algeria / Ammar et al._________________________________________________________
4 of 6 5 of 6
for several days or weeks after a single treatment. However, drug
concentrations inevitably decrease over time and newly acquired
parasites during this phase may be exposed to sub–therapeutic
concentrations [41] leading to the development of Ivermectin
resistance by the larvae of Parascaris spp. within 10 weeks of the
prepatent period [18] then the transmission of resistance alleles
to subsequent generations [17].
Schougaard and Nielsen [20] incriminated the transport of horses
between farms or between countries as a factor in the spread of
resistance once detected.
In the present investigation, the FECRT was 100% for Fenbendazole.
This result shows that this product was effective in agreement with
Kaplan et al. [46] and Martin et al. [47] reported that the drug of choice
commonly used to treat Parascaris spp. is fenbendazole. Conflicting
reports regarding the effectiveness of Fenbendazole have been
raised across the world. Some authors still note the effectiveness
of Fenbendazole [21, 22, 36, 47], while other authors have reported
Parascaris spp resistance to this molecule [14, 17, 48, 49].
CONCLUSION
This study detected the presence of Ivermectin resistance in
Parascaris spp. for the rst time in yearlings reared in two farms in
the Tiaret region while these parasitic isolations remain sensitive to
the activity of Fenbendazole. Further research for good knowledge
of the mechanisms involved in the development of resistance
to Ivermectin and regular monitoring of the effectiveness of
anthelmintic against Parascaris spp. and other parasites could
help adopt measures to slow the development of this resistance
and therefore optimize local parasitic control programs.
ACKNOWLEDGMENTS
The authors would like to thank the general direction of scientic
research and technological development (DGRSDT) for their support.
Author Contributions
All authors contributed to the study’s conception and design.
Sampling [Bouchentouf Keltoum], [Kadi Marwa] and [Mihoubi
Amel], Treatment of foals [Belmedjahad Mustapha], Material
preparation [Kouidri Mokhtaria], [Selles Sidi Mohammed Ammar]
and [Belhamiti Belkacem Tahar], data collection and analysis
were performed by [Kouidri Mokhtaria], [Ait Amrane Amar], [Bia
Taha] and [Selles Sidi Mohammed Ammar]. The rst draft of the
manuscript was written by [Selles Sidi Mohammed Ammar] and
all authors commented on previous versions of the manuscript.
All authors read and approved the nal manuscript.
Funding information
The study was not sponsored by any authority
Conflict of interest
The authors declare that there is no conflict of interest in
this study.
Ethical approval
This paper does not contain any studies with human participants
or animals performed by any of the authors.
Data availability
The datasets generated during and/or analyzed during the
current study are available from the corresponding author upon
reasonable request.
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