Efficacy of anthelminthic control programs against natural muellerius capillaris infection in sheep in the north-west of spain. effect on blood gases and ph in venous blood samples
Efficacy of anthElminthic control programs against natural
Muellerius capillaris infEction in shEEp in thE north-wEst of spain.
EffEct on blood gasEs and ph in vEnous blood samplEs
LóPez C.M., Cienfuegos s., DaCaL V., Vázquez L., PanaDeRo R., feRnánDez g., Díaz P.,
Lago n., Díez-baÑos P. & MoRRonDo M.P.*
Efficacité dE différEnts anthElminthiquEs vis-à-vis dE
l’infEction naturEllE par Muellerius capillaris
d’ovins dans lE nord-
The field efficacy of a single dose treatment against natural
ouEst dE l’EspagnE. EffEts sur lEs gaz du sang Et lE ph vEinEux
infection using different anthelmintic drugs, extensively
L’efficacité sur le terrain d’un traitement à dose unique par différents
employed in ovine parasite control programs in Galicia
anthelminthiques vis-à-vis de l’infection naturelle par
(N.W. Spain), and the effect of protostrongylid infection on ovine
d’ovins en Galice (Espagne), ainsi que l’effet de cette infection sur
respiratory functions, were evaluated. Five groups (n = 5) of ewes
la fonction respiratoire de ces ovins ont été évalués. Cinq groupes
were used in this study; animals were treated with injectable
(n = 5) de brebis ont été utilisées dans cette étude. Les animaux ont
ivermectin (0.2 mg/kg), levamisole (7.5 mg/kg) and albendazole
été traités soit avec de l’ivermectine injectable (0,2 mg/kg), soit du
(5 mg/kg) and monitored at 0, 7, 21, 42 and 63 days post-
lévamisole (7,5 mg/kg), soit de l’albendazole (5 mg/kg), et la
treatment (d.p.t.) by enumeration of the lungworm larvae per gram
charge parasitaire a été mesurée à 0, 7, 21, 42 et 63 jours post-
of faeces (l.p.g.) and determination of gas tension and pH in
traitement (j.p.t.) par la détermination du nombre de larves par
venous blood using an i-Stat portable clinical analyzer. No
gramme de fèces (l.p.g.) et par la mesure de la pO2, de la pCO2
statistical difference was found either in larval elimination between
et du pH dans le sang veineux à l’aide d’un i-Stat analyseur
untreated and treated groups or in the reduction in larval counts in
clinique mobile. Aucune différence statistique n’a été retrouvée pour
all of the treated groups. A significant increase in partial oxygen
ce qui concerne le nombre de larves présentes entre groupes traités
tension (pO2) and saturation (sO2) between day 0 and 7 p.t. was
et non traités. Des augmentations significatives de la pression
observed in all treated animals. These values decreased
significantly at day 21 to previous levels. There were no statistical
2) et de la saturation (SO2) entre les jours 0
et 7 p.t. ont été observées chez tous les animaux traités. Au-delà de
differences in blood gases between uninfected and treated groups.
21 j.p.t., ces valeurs sont revenues aux valeurs d’avant traitement.
We can conclude that under Galician field conditions, parasitic
Nous pouvons conclure que, dans des conditions réelles en Galice,
control programs are not totally effective against M. capillaris
les programmes de contrôle des parasites ne sont pas efficaces
contre l’infection par
sheep, Muel erius capil aris
, treatment, field efficacy, blood gases.
MOTS CLÉS : ovins,
Muellerius capillaris, traitment, efficacité sur le terrain, gaz
in galicia (north-west of spain) sheep are raised protostrongylid infection is not very common in sheep,
mainly in a semiextensive husbandry system. in this
Valero et al.
(1992) and berrag & Cabaret (1996) found
region, mild temperatures and environmental humi-
that heavy infections decreased carcass weights,
dity are optimal for the survival of many important
increased levels of mortality and impaired pulmonary
livestock parasites, such as small lungworms (Protos-
trongylidae). Neostrongylus linearis
, Muellerius capil
in this study the field efficacy of three anthelmintic drugs
laris, Cystocaulus ocreatus
(albendazole, levamisole and ivermectin) against M.
the species parasitizing sheep in galicia (Díez-baños et
natural infection, using protocols extensively
, 1994), although a recent extensive survey carried
used in ovine parasite control programs, was evaluated,
out by Cienfuegos et al.,
(2007) have shown Muellerius
together with the effect of natural infection by M. capil
as the most frequent lungworm, with 98.2 %
and the subsequent effect of treatment over pulmo-
prevalence over the rest of the species and a mean of
nary gas exchange under natural conditions.
larval shedding of 67.4 ± 297.7 larvae per gram of faeces (lpg). although clinical disease associated with
* Parasitology and Parasitic Diseases. animal Health Department.
Lugo Veterinary faculty. santiago de Compostela university. 27002,
Correspondence: Ceferino M. López.
Tel.: +34-82252231 - fax: +34-82252195.
in March 2008, 25 ewes from Lugo province were
examined twice by means of the baermann-Wetzel
technique (baermann, 1917; Wetzel, 1930) in order
LóPez C.M., Cienfuegos s., DaCaL V. et al.
to confirm a natural pure infection by M. capillaris
sheep grazed pastures around the farms during the day and were housed at night in strawed-floor stables. sheep
Larval elimination was transformed to the logarithm of
included in this study were ewes (> 3 years) that have
the count plus 1 to calculate geometric means. To assure
not received any anthelmintic treatment during the last
homogeneity of sheep groups, larval counts in day 0
year (last treatment March-april 2007).
were compared using Kruskal-Wallis non parametric
The ewes were ranked according to larval shedding analysis. Differences in larval excretion at day 7, 21, 42 before treatment. Within ranks, sheep were randomly
and 63 p.t. were analyzed using Mann-Whitney test to
compare the treated groups with the positive untreated
- group 1 (n = 5), untreated control group.
one. The significance in reduction of larval counts over
- group 2 (n = 5), treated with injectable ivermectin time was tested with friedman non parametric test for 1 % for ovine at the dose rate of 0.2 mg/kg body weight
sc (ivomec®, Merial Ltd. essex, england).
The effect of the treatment over gas tension and pH in
- group 3 (n = 5), treated with levamisole base (hydro-
treated animals was analyzed with repeated measures
chloride) 7.5 % at a dose rate of 7.5 mg/kg b.w. sub-
anoVa. “Repeated” contrast was introduced to deter-
cutaneously administered (Caliermisol®, Laboratorios
mine if measures were significantly different from the
adjacent sample. “simple” contrast was used to compare
- group 4 (n = 5), treated with albendazole 2.5 % at a
between groups measures. all the analysis were realized
dose rate of 5 mg/kg b.w. per os
with sPss, Version 15.0.1, sPss inc., 1989-2006).
industrial Veterinaria s.a., barcelona, spain).
We also included a negative control group, composed by five ewes with no larval elimination in two succes-
sive samplings (group 0).
after treatment, animals were maintained under field conditions, so that reinfections were possible.
The geometric mean of lpg and the statistical signi-
fication between untreated and treated groups
faecal and blood samples were taken before treatment
are shown in Table i. all the animals of the posi-
(day 0), and at 7, 21, 42 and 63 days post-treatment (d.p.t.).
tive control (g1) and treated groups (g2, g3 and g4)
faeces were collected directly from the rectum with plastic
were positive previously to treatment. neither statistical
gloves and were kept cool until being analyzed by the
difference was found between untreated and treated
baermann-Wetzel technique in the same day.
groups during the study nor in the reduction in larval
blood samples were collected from the jugular vein into counts all through the study in all of the treated groups.
Lithium-heparin vacuum tubes (bD Vacutainer®, becton,
all larvae recorded throughout the study were identified
Dickinson and Company) and were immediately ana-
lyzed for blood gas tension and pH, using the i-sTaT portable clinical analyzer (i-sTaT Corporation, east
Windsor, usa). The following parameters were mea-
sured: pH, partial pressures of o2 (po2) and Co2 (pCo2), Results of blood gas tension and pH of infected (g1-g4)
oxygen saturation (so2), bicarbonate concentration and uninfected (g0) groups are shown in Table ii. all
(HCo3), total Co2 (TCo2) and base excess (be – amount treated groups (g2-g4) were considered as a whole
of H+ required to returned blood pH to reference value).
(gT) because of the lack of statistical differences in
* g1: untreated group; g2: ivermectin treated group; g3: levamisole treated group; g4: albendazole treated group.
Table i. – geometric Mean lpg and Median (between brackets) in the different groups of sheep.
anthElminthic control programs against protostrongylids
* Repeated Measures anoVa (Repeated Contrast) p < 0.05 Po2 and so2 7 days vs
0 days and Po2 and so2 21 days vs
Table ii. – arithmetic mean ± standard deviation of pH and blood gas tension of the uninfected (g0), positive control (g1) and all treated groups (gT) measured using the i-sTaT portable clinical analyzer.
larval elimination. using a repeated measures anoVa
Most anthelmintic treatments have shown an important
with “Repeated” contrast, significant increase in partial
lack of efficacy against protostrongylid lungworms, and
in particular against M. capillaris
(bliss & greiner, 1985;
day 0 and day 7 p.t. (f = 7.055; p = 0.019 and f = 7.076,
McCraw & Menzies, 1986; Helle, 1986; Díez-baños et
p = 0.019, respectively) were observed in gT. These
., 1995; Rehbein & Visser, 2002). some of those
values decreased significantly at day 21 (f = 5.003,
authors found that Muellerius
larvae reappeared in fecal
samples in less than 60 days, even in animals under
previous levels. The “simple” contrast did not shown
strict isolation. This reappearance might be explained
statistical differences between treated groups (gT) vs
by immature Muellerius
not affected by anthel-
untreated parasitized control group (g1) or negative
mintic treatment, developing to maturity after destruc-
tion of the original adult population (McCraw & Menzies, 1986, 1988) or by the protection conferred by altered tissue surrounding that lungworm that is more pro-
nounced than in other protostrongylid species (Rehbein & Visser, 2002). Recently, Papadopoulos et al.
and geurden & Vercruysse (2007) have obtained better
one of the treatments that are usually employed results with moxidectin and eprinomectin, respectively, in ovine parasite control programs in galicia
but in those cases larval elimination was studied for a
was completely effective against M. capillaris
short period of time after treatment, giving no time for
Despite a temporary descent in larval elimination
the reappearance of larvae observed in other studies.
detected in all groups, at least one animal were elimi-
in galicia, traditionally parasite control practices in
nating larvae in faeces at every sampling time and most
ovine include a systematic single dose treatment in
of them shed larvae at the end of the study (63 d.p.t.).
spring and/or autumn, mainly with benzimidazoles
LóPez C.M., Cienfuegos s., DaCaL V. et al.
(bzD), that generally it is designed to control gastro-
intestinal nematode infections. However, specific treat-ment for protostrongilyd infections would require higher dosage than these (Richard & Cabaret, 1992) or repeated
The authors thanks to oViCa (galician association
of ovine and caprine breeders) and the veterina-
treatments (McCraw & Menzies, 1986).
rians of the aDsg aCiVo for their collaboration
blood gas tension and pH were obtained from venous
in the realization of this study. This work was supported
samples with a portable clinical analyzer to reproduce
by the research project PgiDiT06Rag26101PR.
the field clinical conditions. Though blood gases and pH are usually measured in arterial blood, according to garcía alarcón et al.
(2003) and Dascombe et al.
(2007) venous values reflect correctly and can be used to eva-
luate the pulmonary gas exchange, particularly when values are used for comparative purposes (Verwaerde
baErmann g. eine einfache Methode zur auffindung von anky-
lostomum-(nematoden)-Larven in erdproben. Geneesk.
The treated group (gT) was not significantly different
, 1917, 57,
from the positive or negative control groups. The differ-
bErrag b. & cabarEt J. impaired pulmonary gas exchange in
ences found by berrag & Cabaret (1996) between infected
ewes naturally infected by small lungworms. Int. J. Parasitol.
and uninfected ewes
were due to the intense level of
infection of the animals that exhibited typical clinical
bliss e.L. & grEinEr E.c. efficacy of fenbendazole and cam-
signs of intense bronchopneumonia. However, in our
bendazole against Muellerius capillaris
in dairy goats. am.
study treated animals increased significantly po
J. Vet. Res.
, 1985, 46,
levels at 7 d.p.t., either because of an improvement of
ciEnfuEgos s., vázquEz l., dacal v., pardo m., fErnándEz g.,
the alveolar ventilation or the local perfusion (berrag &
lago n., panadEro r., morrondo p. & lópEz c. estudio
Cabaret, 1996). in our opinion, the moderate intensity of
preliminar de las nematodosis broncopulmonares en el ganado ovino de galicia. 10th Congreso ibérico de Parasi-
infection of sheep in our study would provoke a slight
chronic airway obstruction that may be compensated by
increasing diaphragmatic force output. The temporary
ascombE b.J., rEaburn p.r.J., sirotic a.c. & coutts a.J. The
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lungs pulling oxygen into the blood, observed as an
íEz-baños P., morrondo-pElayo p., carrillo-gonzálEz b.,
lópEz-sándEz c. & fEiJóo-pEnEla a. Relationship between
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west spain and climatic conditions. J. Helminthol
to treatment, because of either the larval population
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díEz-baños P., morrondo-pElayo p., fEiJóo-pEnEla a., carrillo-
The baermann migration technique is still considered
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the gold standard for the diagnosis of lungworm infec-
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, 2008), there is a need for new
rodríguEz-JiménEz a., hErnándEz-alonso b. & martín-
immunological or molecular tools capable to provide a
montEs m. gasometría venosa frente a gasometría arterial
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