Veterinary Parasitology 229 (2016) 73–75

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Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar

Short communication

Ivermectin failure in the control of Oxyuris equi in a herd of ponies in

France
Guillaume Sallé a,∗ , Jacques Cortet a , Christine Koch a , Thierry Gascogne b , Fabrice Reigner b
, Jacques Cabaret a
a
UMR1282 ISP, INRA, Université de Tours, 37380, Nouzilly, France
b
UE1297 Physiologie Animale de l’Orfrasière, INRA, 37380, Nouzilly, France

a r t i c l e i n f o a b s t r a c t

Article history: Drug resistance in equine gastro-intestinal parasitic nematodes has been reported throughout the world.
Received 16 August 2016 While the focus is usually put on cyathostomins, observations of macrocylic lactone failure against Oxyuris
Received in revised form equi have accumulated over the last decade. Here we report the failure of ivermectin in the control of O.
26 September 2016
equi in an experimental Welsh pony herd.
Accepted 28 September 2016
In a first trial, 6 ponies previously drenched with moxidectin and showing patent O. equi infections
were administered ivermectin and subsequently monitored for O. equi egg excretion over one month. This
Keywords:
trial demonstrated a failure of ivermectin to control O. equi egg excretion as half of ponies demonstrated
Oxyuris equi
Horse
recurrent egg excretion in the peri-anal region during 21 days after treatment.
Nematode One year later, six female Welsh ponies drenched with moxidectin demonstrated signs of itching and
Ivermectin scratching in their peri-anal region with worms being found transiently in fecal materials three weeks
Moxidectin later. Ponies were allocated to three treatment groups, i.e. ivermectin, pyrantel embonate and fenben-
Macrocyclic lactone dazole and monitored for egg excretion over five weeks. Fenbendazole and pyrantel embonate broke
ivermectin suboptimal efficacy as soon as 8 and 14 days respectively after treatment, while egg excretion
remained constant throughout the 41-day long trial in the ivermectin-treated ponies.
This is the first report of ivermectin failure against O. equi in France. In the absence of critical efficacy
test, it remains unclear whether true resistance is at stake or if these observations confound a constitutive
suboptimal efficacy of ivermectin against O. equi.
© 2016 Elsevier B.V. All rights reserved.

1. Introduction
Equids usually harbor a wide community of parasitic species.
Among these, Strongylus spp. currently seems to be under control
whereas focus tend to be put on cyathostomins whose resistance
level to commercially available anthelmintics has been increas-
ing over the past decades (Matthews, 2014). These reports have
urged the implementation of targeted selective treatment based on
fecal egg counts to alleviate drug selection pressure put on these
parasitic communities (Nielsen et al., 2014).
However, this strategy also seems to favor the re-emergence of
other parasites that cannot be detected by fecal egg counting, either
because of their long pre-patent period like Strongylus spp. (Nielsen
et al., 2012). O. equi is a clade III parasitic nematode (Blaxter, 2011)
that lives in colon of equids (Enigk, 1949). Larval stages usually
occupy ventral colon for about 2 months, before evolving into
∗ Corresponding author at: INRA Val de Loire, Secteur 2, 37380 Nouzilly, France.
E-mail address: Guillaume.Salle@tours.inra.fr (G. Sallé).
adult worms in approximately 100 days and migrating into the
dorsal colon (Enigk, 1949). After mating, females migrate to the
anus where they deposit sticky clumps of eggs enclosing 8000 to
60,000 eggs (Enigk, 1949). Pathogenicity of this species ranges from
mild (larval stages) to absent (adults) but the fluids secreted along
with eggs by female worms cause pruritus and damage to the tail
(Reinemeyer and Nielsen, 2014; Wolf et al., 2014).
Despite the demonstrated efficacy of available anthelmintics for
controlling O. equi (Colglazier et al., 1977; Reinemeyer et al., 2010;
Xiao et al., 1994), recent reports have indicated a suboptimal effi-
cacy of macrocyclic lactones against this species (Felippelli et al.,
2015; Schankova et al., 2013; Wolf et al., 2014). Our laboratory
has been involved in the monitoring of an experimental herd of
Welsh ponies under targeted selective treatment (Sallé et al., 2015).
Over the last two years, breeders noticed an increased occurrence of
O. equi during routine trans-rectal ultrasonography for monitoring
ovarian activity (F. Reigner, personal communication). In addition,
two consecutive reports of continuous itching after ivermectin and
moxidectin treatments in 2014 and 2015 respectively have led to

http://dx.doi.org/10.1016/j.vetpar.2016.09.020
0304-4017/© 2016 Elsevier B.V. All rights reserved.
74 G. Sallé et al. / Veterinary Parasitology 229 (2016) 73–75

Table 1 were given either fenbendazole (Panacur Equine Guard ® , Inter-

Sampled ponies with corresponding anthelmintic treatment history.
vet, Angers, France, 7.5 mg/kg), pyrantel embonate (Strongid® ,
Start of the experiment IDa Last treatment Trial groupc Zoetis, Paris, France, 6.6 mg/ kg bodyweight) or ivermectin
(date;drug)b (Hippomectin® , Le Vet, Oudewater, The Netherlands, 0.2 mg/kg
July 07, 2014 MW329 10.04.2014; IVM IVM bodyweight). Anthelmitic dosis was adjusted according to individ-
MW483 10.04.2014; IVM IVM ual pony’s weight determined with a scale on the day of treatment.
MW517 10.04.2014; IVM IVM After treatment, each pony was monitored weekly by peri-anal
W600 10.04.2014; IVM IVM
W603 10.04.2014; IVM IVM
adhesive tape sampling over five consecutive weeks. Fecal sam-
W653 10.04.2014; IVM IVM ples were visually inspected on the day before treatment and 24 h
later to look for adult worms.
April 16, 2015 W661 05.03.2015; MOX FBZ
W552 05.03.2015; MOX FBZ
W660 05.03.2015; MOX IVM 2.3. Parasitological measure
W602 19.03.2015; MOX IVM
W663 22.03.2015; MOX PYR A semi-quantitative assessment of O. equi egg burden was per-
W588 11.02.2015; MOX PYR
formed by applying one adhesive tape (7 × 2 cm) in the peri-anal
a
Animal identification number, MW stands for Welsh pony stallion and W for region of each poney, subsequently put on a glass slide observed
Welsh pony mare.
b
with an optical microscope ((×40 magnification). According to the
IVM: Ivermectin; MOX: Moxidectin.
c
IVM: Ivermectin; FBZ: Fenbendazole; PYR: Pyrantel embonate. observed excretion of eggs, four categories were defined: 0, no
egg found on the slide; 1, egg found on 1 field of observation; 2,
eggs found on several field of observation; 3, eggs found in every
a controlled test of efficacy based on scotch tests. This is the first
field of observation. Perianal region was thoroughly washed and
report of a lack of efficacy of ivermectin against O. equi in France.
rinse thrice with a povidone-iodine soap (Vétédine® savon, Véto-
quinol, Paris, France) every day after application of the adhesive
2. Materials and methods tape. Visual inspection of fecal material was performed by succes-
sively washing 200 g of fecal material through sieves with 250 ␮m
2.1. Monitoring of ivermectin efficacy (2014) and 32 ␮m aperture. This monitoring has been performed weekly
from day 0 to 21 day after drenching in 2014 and on day 0 and 24 h
In 2014, three female Welsh ponies monitored for ovarian activ- later in 2015.
ity on June 30 showed visible O. equi in their feces (Table 1). Their
last ivermectin drench (0.2 mg/kg bodyweight Hippomectin® , Le 3. Results
Vet, Oudewater, The Netherlands) had been given more than two
months earlier (April 10, 2014). In addition, three Welsh stallions 3.1. Ivermectin did not prevent continuous eggs excretion
showed recurrent tail pruritus.
After an initial assessment of their O. equi egg load with an Results of the daily assessment of the O. equi eggs load are pro-
adhesive tape (see Section 2.3), ponies were given an oral dose of vided in Table 2. Only one female pony (W603) did show parasitic
ivermectin (0.2 mg/kg bodyweight Hippomectin® , Le Vet, Oudewa- egg on every day of sampling (Table 2). Two additional individuals
ter, The Netherlands). Daily monitoring of O. equi egg presence in (MW517 and W600) also exhibited a consistent egg load with less
peri-anal region was subsequently performed during 21 days after than 6 days without any eggs being recovered (Table 2). Other indi-
drenching. viduals (MW329, MW483 and W653) showed eggs up to the first
five consecutive days after drenching, with erratic egg appearance
2.2. Controlled evaluation of efficacy of available anthelmintics found on a single occasion, i.e. eight and 17 days after treatment for
(2015) MW329 and W653 respectively (Table 2).

In 2015, six female Welsh ponies demonstrated signs of itching
and scratching in their peri-anal region with worms being found
transiently in fecal materials. These ponies had been drenched no
later than three weeks earlier (Table 1) with a combination of praz-
iquantel and moxidectin (2.5 mg/kg and 400 ␮g/kg bodyweight
respectively, Equest pramox ® , Zoetis, Paris, France).
Following the clinical observations, these six ponies were ran-
domly allocated to three treatment groups by using the sample()
function of the R program (www.R-project.org). These groups
3.2. Pyrantel embonate and fenbendazole broke ivermectin
suboptimal efficacy
Results from the controlled drug test are provided in Table 3.
Worms have been collected in the feces of the pyrantel-treated
group up to 24 h after treatment, and one out of the two ponies
in both fenbendazole- and ivermectin-treated groups (Table 3).
Ivermectin drenching did not resolve the O. equi egg excretion
as eggs were collected throughout the 41-day long trial for one

Table 2
Semi-quantitative assessment of O. equi eggs excretion on four female Welsh ponies after IVM treatment.

ID J0 J1 J2 J3 J4 J5 J6 J7 J8 J9 J10 J11 J12 J13 J14 J15 J16 J17 J18 J19 J20 J21
MW329 0 2 2 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0
MW483 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
MW517 3 1 3 1 0 0 0 1 1 1 0 1 3 3 3 3 3 2 4 0 3 1
W600 4 1 4 3 3 2 1 2 2 3 1 1 0 0 0 4 1 0 0 2 1 1
W603 2 1 3 1 2 3 2 2 3 2 2 4 2 2 1 4 2 2 2 1 3 1
W653 0 1 1 2 1 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0
Grade of egg excretion is provided for each individual monitored over 21 days after ivermectin drenching. 0: no egg found on the slide; 1: egg found on 1 field of observation;
2: eggs found on several field of observation; 3: eggs found in every field of observation.
 G. Sallé et al. / Veterinary Parasitology 229 (2016) 73–75 75

Table 3
Results of the controlled drug efficacy trial.

No. worms
Egg loadb
ID Treatmenta collectedc
D0 D8 D14 D25 D32 D41 D0 D1
W661 FBZ 3 0 0 0 0 0 0 1
W552 FBZ 1 0 0 0 0 0 0 0
W660 IVM 0 0 1 2 3 1 0 0
W602 IVM 3 4 3 1 3 2 5 0
W663 PYR 0 0 0 0 0 0 1 0
W588 PYR 2 1 0 0 0 0 1 18
a
IVM: Ivermectin; FBZ: Fenbendazole; PYR: Pyrantel embonate.
b
Grade of egg load is provided for each individual monitored over 21 days after ivermectin drenching. 0: no egg found on the slide; 1: egg found on 1 field of observation; 2:
eggs found on several field of observation; 3: eggs found in every field of observation.
c
numbered based on visual inspection of fecal material; only the days when worms have been collected are reported.

individual and from 14 days after treatment onward for the other
(Table 3). On the contrary, no eggs were retrieved from eight and
14 days after treatment with fenbendazole and pyrantel embonate
respectively.
4. Discussion
oping in this species or if this class of molecules is inefficient per se,
both pyrantel embonate and fenbendazole seemed to exert adulti-
cide effect. This stresses the strategic role that fenbendazole still
play in the frame of parasitic nematode control in horses even
if broadened resistance has been described for this molecule in
cyathostomins.

After two recent European cases of macrocyclic lactone ineffi-

cacy against O. equi (Schankova et al., 2013; Wolf et al., 2014),our
study reports the first case of such failure in France. Noticeably and
to our knowledge, this is the first time such a case is reported for
equids under targeted-selective treatment regimen.
In the absence of a critical efficacy test, i.e. worm counting after
drenching and necropsy, it is difficult to draw any conclusion about
drug efficacy. Macrocyclic lactones, though potent against pin-
worms, never reached complete efficacy against them (Reinemeyer
and Nielsen, 2014) and reports of suboptimal efficacy have already
been made in America (Felippelli et al., 2015; Reinemeyer, 2012).
However, a critical test performed in Tennessee after reports of
macrocyclic lactone failure did not show any evidence of resistance
(Reinemeyer et al., 2010), highlighting the difficulty of evaluating
the origin of anthelmintic failure with this species (Reinemeyer,
2012).
In our case and similarly to what has been reported elsewhere
ivermectin could not prevent O. equi egg excretion while both
pyrantel embonate and fenbendazole seemed to exert potent effect.
Indeed, ivermectin treatment was not able to resolve the egg output
in half of the considered ponies in 2014 while the successive admin-
istration of moxidectin and ivermectin one-month apart in 2015
did not eliminate clinical signs. Whether this is due to the use of
generic anthelmintic product or not remains unclear but such sub-
optimal efficacy of generic macrocyclic lactone has been reported
in Brazilian horses (Toscan et al., 2012).
On the opposite, both fenbendazole and pyrantel resulted in
an extinction of peri-anal egg laying in every 2015 pony as soon
as the second sampling and adult worms could be recovered in
both treatment groups. The small number of individuals consid-
ered in this trial did not permit to be conclusive on this point, but
our findings are congruent with other reports (Reinemeyer, 2012).
It also reminds that even if fenbendazole failure against cyathos-
tomin is now widespread and that intermediate level of efficacy are
found for pyrantel (Matthews, 2014), these drugs remain an asset
for the management of non-strongylid gastro-intestinal nematodes
in horses.
5. Conclusion
Acknowledgement
Authors are greatly indebted to the UEPAO team for managing
and taking good care of the ponies.
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This is the first report of macrocyclic lactone failure against O.

equi in France. While it remains unclear whether resistance is devel-