https://doi.org/10.52973/rcfcv-e33308
Received: 19/08/2023 Accepted: 11/09/2023 Published: 29/09/2023
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Revista Científica, FCV-LUZ / Vol. XXXIII, rcfcv-e33308
ABSTRACT
In Algeria, sheep farming is still largely traditional, and ewes are
subject to various pathologies, particularly parasitic diseases
leading to reproductive failure and production losses. To assess
the inuence of internal parasites (helminths and protozoa) and their
interaction with the different phases of reproduction and season
on hematological parameters, fecal and blood samples (n = 89) were
taken from ewes during the period from the end of gestation to 3
months after parturition, two weeks apart. Animals were reared
under a traditional pasture–based farming system in a Region of
Northeastern Algeria characterized by a Mediterranean climate.
Parasitic coproscopy results showed the consistent presence of
digestive strongyles, Strongyloides, Trichuris ovis, Moniezia spp.,
Fasciola hepatica, and Coccidia. Hematological parameters, mainly
hematocrit (HCT), hemoglobin (HGB), and erythrocytes (RBC), showed
lower levels in anemic ewes throughout the study period. These
hematological effects became signicantly prevalent in 91% of the
animals (P<0.05) during the third month postpartum (p.p.). The use of
a mixed–effects model conrmed the signicant hematological effect
(P<0.05) of internal parasitism, which was amplied signicantly by
its interaction with the reproduction stage for HCT and RBC (P<0.01).
Monitoring of blood biological constants in ewes during the critical
reproductive stages seems to provide valuable data to improve their
welfare and resistance to potential internal parasites.
Key words: Ewes; hematology; internal parasites; peripartum
RESUMEN
En Argelia, la ganadería ovina sigue siendo en gran medida tradicional,
y las ovejas están sujetas a diversas patologías, en particular
enfermedades parasitarias que provocan fallos reproductivos y
pérdidas de producción. Para evaluar la inuencia de los parásitos
internos (helmintos y protozoos) y su interacción con las diferentes
fases de la reproducción y la estación del año sobre los parámetros
hematológicos, se tomaron muestras fecales y sanguíneas (n = 89) de
ovejas durante el periodo comprendido entre el nal de la gestación
y 3 meses después del parto, con un intervalo de dos semanas. Los
animales se criaban en un sistema tradicional de pastoreo en una
región del noreste de Argelia caracterizada por un clima mediterráneo.
Los resultados de la coproscopía parasitaria mostraron la presencia
constante de estróngilos digestivos, Strongyloides, Trichuris
ovis, Moniezia spp., Fasciola hepatica y Coccidia. Los parámetros
hematológicos, principalmente hematocrito (HCT), hemoglobina
(HGB) y eritrocitos (RBC), mostraron niveles más bajos en las
ovejas anémicas durante todo el periodo de estudio. Estos efectos
hematológicos se hicieron signicativamente incidentes en el 91 % de
los animales (P<0,05) durante el tercer mes posparto (p.p.). El uso de
un modelo de efectos mixtos conrmó el efecto signicativo (P<0,05)
del parasitismo interno en el estado hematológico, que se amplicó
signicativamente por su interacción con la fase de reproducción
para el HCT y el RBC (P<0,01). La monitorización de las constantes
biológicas sanguíneas de las ovejas durante las fases reproductivas
críticas parece aportar datos valiosos para mejorar su bienestar y su
resistencia a posibles parásitos internos.
Palabras clave: Ovejas; hematología; parásitos internos; periparto
Changes in hematological status depending on reproductive stage of ewes
naturally infected with internal parasites in North–Eastern Algeria
Cambios en el estado hematológico en función de la fase reproductiva de ovejas
infectadas naturalmente por parásitos internos en el noreste de Argelia
Ahmed Hadef
1,2
* , Souad Righi
1
, Abdelbasset Ghouar
3
1
Chadli Bendjedid University of El–Tarf, Faculty of Nature and Life Sciences, Department of Veterinary Sciences. El–Tarf, Algeria.
2
Badji Mokhtar University of Annaba, Faculty of Medicine, Laboratory of Development and Control of Hospital Pharmaceutical Preparations. Annaba, Algeria.
3
Frères Mentouri Constantine I University, Institute of Veterinary Sciences. Constantine, Algeria.
*Corresponding author: hadef–ahmed@univ–eltarf.dz
FIGURE 1. Study sampling design for coproscopic examination and blood
parameters assessment
Hematological effects of the reproductive stage–internal parasitism interaction in ewes / Hadef et al. _____________________________
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INTRODUCTION
Sheep (Ovis aries) play a key role in the Algerian agricultural
economy due to their dominant proportion in the National herd (78%)
with approximately 29.4 million head, including 18.4 million ewes in
2019 as reported by the Algerian Ministry of Agriculture and Rural
Development [1]. Sheep farming is subject to considerable pathology,
including those related to the presence of internal parasites that
cause high mortality, decreased production, and signicant overall
economic losses [2, 3, 4].
In the Algerian Coastal Region characterized by a Mediterranean
climate, contrary to the steppe area with a semiarid climate [5, 6, 7],
the internal parasitism of sheep is not well documented. Its study
mainly involves surveys in slaughterhouses [8]. In North Africa,
internal parasites develop under common climatic conditions and
it has been suggested that some of their variants, such as the
trematode Fasciola hepatica, have a common origin and spread in
three Mediterranean Countries (Algeria, Tunisia, and Spain) due to
movements of infected animals [9].
Hematology of infected animals is a very sensitive indicator of the
degree of parasite–induced lesions, particularly liver lesions, which
disrupt metabolic processes vital to the normal health and optimal
productivity of the animals [10, 11]. The assessment of hematological
data in sheep is an essential complement to the detection of the
presence of parasites [12, 13]. Furthermore, blood loss generated
by parasites can lead to anemia and promote hematological and
biochemical alterations if acute [14].
The present study aims to investigate, in a traditional Algerian
breeding system, the hematological effects of some potential internal
parasites that develop in the Mediterranean climate in ewes at critical
stages of reproduction.
MATERIALS AND METHODS
Study area
The present study was carried out in El–Tarf Province, a littoral
Region located in North–Eastern Algeria with a Mediterranean climate
(36°75’N; 7°93’E) during the rainy months of the year (from October to
April). The temperature varies throughout the year between 10° and
36°C, with average annual precipitation of about 600 mm. According
to the Köppen–Geiger classication, the climate is Csa [15].
Animals
Fourteen ewes of autochthon breeds (Ouled–Djellal and Berber
breeds), aged between 2 and 5 years from a private farm maintained
under traditional and semi–intensive management systems were ear–
tagged. The ewes were weekly monitored at different reproductive
stages (late pregnancy, early, and mid–lactation). The ewes pasture
daily but on rainy days, they were fed with hay and straw and
supplemented intermittently with concentrate when available.
The deworming was indiscriminately performed by a Veterinary
practitioner in response to the owner’s request. From the second
month postpartum and following the death of two ewes, the number of
subjects followed was reduced to twelve. This resulted in the missing
values indicated below in the statistical description.
Blood samples and hematological parameters measurement
For each ewe, the hematological status was established from
Ethylenediaminetetraacetic acid (EDTA) –blood samples (10 mL)
collected at 8:00 am once during the antepartum (AP), one to three
weeks before lambing, and twice a month from the parturition to the
3rd month postpartum (FIG. 1).
TABLE I
Reference values of assessed hematological parameters in ewes
Hematological parameters (unit) Range* Mean*
WBC (×10
3
·μL
-1
) 4 – 8 12.0
RBC (×10
6
·μL
-1
) 9 – 15 12.0
HGB (g·dL
-1
) 9 – 15 11.5
HCT (%) 27 – 45 35.0
MCV (v) 28 – 40 34.0
MCH (pg) 8 – 12 10.0
MCHC (%) 31 – 34 32.5
PLT (×10
3
) 800 – 1,100 500.0
*: Reference values reported by Byers–Stacey and Kramer [16]
The hematological indicators monitored were White Blood Cell
count (WBC), erythrocytes parameters mainly Red Blood Cell count
(RBC), Hemoglobin concentration (HGB), Hematocrit (HCT), Mean
Corpuscular Volume (MCV), Mean Corpuscular Hemoglobin (MCH),
Mean Corpuscular Hemoglobin Concentration (MCHC) and platelet
parameters (PLT) using an Auto Hematology Analyzer (BC–5380,
Shenzhen Mindray Bio–medical Electronics Co, Ltd, China). Females
were categorized into anemic and non–anemic groups according to
their hematocrit values lower than the threshold value (27%) reported
by Byers–Stacey and Kramer [16] (TABLE I).
Fecal samples and coproscopic examination
Once during antepartum and fortnightly from lambing to weaning,
fecal samples were collected directly from the rectum of each ewe
in labeled plastic bags (FIG. 1).
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Fecal egg counts (FECs) of internal parasites (gastrointestinal
nematodes, Coccidia, Moniezia, and Fasciola hepatica eggs) were
estimated using the Modied Wisconsin Sugar Flotation (Sheather’s
solution, specic gravity 1.27) [17]. The identication of internal
parasites’ eggs was based on the morphological criteria reported by
Bussiéras and Chermette [18]. For worm burdens and coccidiosis,
the FEC was considered low for less than 10 eggs/oocysts per gram
(EPG/OPG) and moderate for 11 to 50 eggs/oocysts. A high level of
worm burden requiring anthelmintic administration was dened at
a threshold of 50 EPG. According to these FEC levels, females were
assigned to three groups, Low, Moderate, and High levels both for
worm burdens and Eimeria spp. The presence of liver uke eggs in
the fecal sample led us to dene two other ewes’ groups, fasciolosis
“Absence “and “Presence” [17, 19].
Statistical analysis
Statistical analysis was performed with IBM SPSS Statistics 26
software. The mixed–effects model for repeated measurements was
used to measure the model for the hematological variation according
to the anemia status, season (months), and internal parasites eggs
shedding level (FEC level). These factors and their interaction with the
reproductive stage (Time) were considered as xed effects (missing
values were not imputed).
Independent samples t–tests were performed to compare measures
between the two groups at the limit reference values, antepartum,
weeks 2, 4, 6, 8, 10, and 12. Overall within–group variations in measures
across reproductive stages (weeks) were tested using repeated–
measures ANOVA. Furthermore, a chi–squared (χ
2
) test was performed
for comparison between the proportions of the group’s categories.
To compare the distribution of internal parasite parameters (FECs)
across categories of groups, non–parametric tests for independent
samples were used. Anemia and fasciolosis categories via Mann–
Whitney U Test; reproductive stage, season, Worm and Coccidian FEC
levels through Kruskal–Wallis Test for one way ANOVA for k sample.
In addition, Spearman's rho correlation was used to establish the
relationship between these parameters and studied factors. The
threshold value for all these statistical tests was 5%.
RESULTS AND DISCUSSIONS
The micro–coproscopic study made it possible to follow the
evolution of female infection by internal parasites according to the
stage of reproduction and season.
As shown in TABLE II, gastrointestinal nematodes, mainly
strongyles, shed a low number of eggs (< 10 EPG) during most of the
reproductive stages; the only signicant increase in egg shedding
but not exceeding the moderate level of 50 EPG has occurred at the
second week postpartum and no ewes had a high–level FEC.
These changes in the level of nematode egg shedding corresponding
to a periparturient rise were revealed by the second peak observed
during late Autumn–early Winter (November–December) and which
were also reported in North Tunisia [20]. This phenomenon which
began about two weeks before lambing, and continued up to eight
weeks after lambing [21], was assigned to the physiological changes
characterizing the peripartum period. The endocrine and metabolic
effects of this transition period are closely associated with leptin and
cortisol proles in response to the mobilization of fat and protein
reserves on the anti–parasite immune system relaxation of the host
and on worm egg count had been blamed [22].
The level of excretion of Eimeria oocysts was often low, it increased
from the second–week p.p.; its incidence for a moderate level
increased insignicantly in the third month postpartum in 40% of
the animals and its highest level was never reached during the study.
The presence of Fasciola egg in fecal material was observed from
15 days after parturition at the highest prevalence value (TABLE II).
According to the chi–square test, the distribution of groups did not
seem to be wholly affected by the reproductive stage.
Worm eggs have been consistently disposed of at a low level
without ever reaching the high level (TABLE II) except for a signicant
prevalence rise of ewes with moderate EPG in January (66.7%). As
well, an increase in ewes with moderate Eimeria oocysts count and
a signicant presence of Fasciolosis in 61.9% of fecal samples were
observed in January (TABLE II). In the subsequent month (February),
a marked disappearance of ewes shed a moderate level of coccidian
FEC and those excreting Fasciola egg was noted. With the arrival of
Spring, these categories reappeared over time.
Through the overall comparison of the categories, a signicant
seasonal variation in the proportions of the groups was recorded for
the worm’s FEC level (P<0.05) and Fasciolosis (P<0.001).
In the study area, a temperature ranging from 10° to 36°C during
the whole year is considered generally favorable for the development
of trichostrongylid larvae from egg to L3 infective larva [23]. This
climatic–seasonal effect was also veried by the Spring rise in ewes
that shed worm eggs and the Spring reappearance of ewes with
moderate coccidian FEC levels and Fasciola eggs.
The permanent presence of internal helminths during the rainy and
cold seasons (late Autumn and Winter) and the Spring seems related to
the climatic condition of this Mediterranean area, in agreement with
that reported in North Tunisia by Akkari et al. [20]. Under this temperate
climate, the egg count of gastrointestinal helminths showed a gradual
increase from January with a peak in May and June due to the ingestion
of infective larvae during the rainy and cold seasons. Strongylid eggs
were considered cold tolerant, and the succession between low and
higher temperatures could stimulate their hatching [23].
For the Fasciola genus, its presence seems surprising given the
gravity of Sheather’s solution (1.27), which is not the best choice for
demonstrating Fasciola hepatica eggs using the oatation method
[24]. This suggests an incidence of infection by Fasciola which
could have been estimated at higher rates if a solution allowing the
otation of heavy eggs of this trematode had been used. The seasonal
occurrence of this trematode could be related to the life–cycle of its
intermediate host, the freshwater snail Galba truncatula. The natural
infection of this snail was recorded during Winter and Spring from
December (2.3%) to May (4.8–9.3%) in the Algerian Coastal Region
by Mekroud et al. [25].
The results obtained from hematology tests showed a signicant
prevalence of anemia in the studied ock, where 50% of the animals
were anemic throughout the study and reaching 91% (P<0.05) in the third
month postpartum (TABLE II). These results are consistent with those
observed by David et al. [26] where they reported signicant variations
across the gestational period with a decrease in mean corpuscular
volume (MVC) and lowest values of hemoglobin concentration (HGB),
and corpuscular hemoglobin concentration (MCHC) near the birth date.
Hematological effects of the reproductive stage–internal parasitism interaction in ewes / Hadef et al. _____________________________
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Across months of study, anemia that presents the six months of
study (TABLE II) had signicantly decreased to affect 36.8% of the
ock in Winter (December). Subsequently, it continued to increase
until affecting all studied animals as shown by a signicant peak in
March (100%), thus a signicant seasonal variation in the proportions
of anemic and non–anemic ewes was noted (P<0.05).
The results of non–parametric tests used to compare the distribution
for FEC count of internal parasite species across categories of groups
are presented in TABLE III. Anemia status seems to be related to
changes in the FEC count of Moniezia and Eimeria (P<0.05) but not
to that of another genus of internal parasites (P>0.05). It appears
that egg shedding of the Nematode species, except Trichuris ovis,
as well as that of Moniezia and Fasciola, were signicantly different
between months of study (P<0.01). Among all studies genus of internal
parasites, only Strongyloides FEC was distributed differently across
the reproductive stage (Time), but this did not indicate by signicant
correlation (rs = 0.14, P>0.05).
The presence of Strongyloides and Trichuris eggs in fecal samples
appears generally incidental because of their susceptibility to the
anthelmintics used to treat the more important Nematode species
such as Haemonchus [23]. These could explain the insignicant
seasonal changes in Trichuris egg excretion and the low signicance
of Strongyloides FEC distribution across reproductive stages.
FIG. 2 demonstrates that leucocyte count (WBC) had exceeded the
threshold value (12 × 10
3
cells·μL-1) both in anemic and non–anemic
ewes from week 2 to week 10 p.p. A single signicantly highest value
of WBC in non–anemic ewes was recorded during the weaning period
(week 8) in comparison with a normal value measured at the same
TABLE II
Proportions of internal parasites and anemia categories (frequencies) according to the reproductive stage and season
Factor
Worm FEC level (%) Coccidia FEC level (%) Fasciolosis (%) Anemia Group (%)
Low Moderate High Low Moderate High Absence Presence Anemic Non–anemic
Reproductive
stage (Time)
AP 100 0 0 100 0 0 100 0 64.3 35.7
W2 33.3 44.4 22.2 55.6 44.4 0 44.4 55.6 50 50
W4 83.3 8.3 8.3 50 41.7 8.3 83.3 16.7 57.1 42.9
W6 66.7 33.3 0 77.8 11.1 11.1 55.6 44.4 66.7 33.3
W8 75 25 0 25 58.3 16.7 91.7 8.3 58.3 41.7
W10 60 40 0 40 50 10 50 50 90.9 9.1
W12 66.7 25 8.3 25 50 25 66.7 33.3 50 50
χ
2
13.09 14.41 10.33 5.83
P 0.36 0.28 0.11 0.44
Season
(Months)
OCT 42.9 57.1
NOV 100 0 0 75 25 0 100 0 50 50
DEC 91.7 0 8.3 58.3 16.7 25 83.3 16.7 36.8 63.2
JAN 19 66.7 14.3 33.3 42.9 23.8 38.1 61.9 70.8 29.2
FEB 81.8 18.2 0 36.4 63.6 0 100 0 63.6 36.4
MAR 93.3 6.7 0 53.3 46.7 0 73.3 26.7 100 0
APR 75 25 0 50 50 0 50 50 50 50
χ
2
34.72 14.00 17.96 16.4
P 0.000 0.17 0.003 0.012
TABLE III
Distribution tests for internal parasites FEC following to the studied factors
Factor of grouping
Anemia
Reproductive
stage (Time)
Season (Month)
Test
a
Sig. rs Test
b
Sig. rs Test
b
Sig. rs
Nematode worms 0.59 0.07 0.15 –0.01 0.00* –0.08
Strongyloides 0.46 0.09 0.04* 0.14 0.00* 0.14
Nematodirus 0.35 0.12 0.08 –0.16 0.02* –0.21
Trichuris 0.99 0.00 0.64 –0.10 0.55 –0.13
Moniezia 0.011* 0.32** 0.19 –0.22 0.00* –0.45**
Eimeria 0.026* 0.28* 0.34 0.26* 0.54 –0.01
Fasciola 0.492 –0.09 0.15 0.06 0.00* 0.03
a
: comparison of variables distribution across groups using Mann–Whitney U Test.
b
: comparison of variables distribution across groups using Kruskal Wallis Test. rs:
Spearman's rho correlation with factor of grouping. **: signicant at the 0.01 level.
*: signicant at the 0.05 level
period in anemic ewes (FIG. 2A). This could be attributed, in the early
postpartum period, to the effect of cortisol which triggers delivery
[27] and afterward to the impact of the parasite infections.
The change in leucocytes number was only influenced by the
interaction of the reproductive stage with Eimeria FEC level (TABLE
IV). This could be related to the release pattern of coccidia which
impairs the immune system and reduces the count of WBC following
FIGURE 2. Hematological parameters (mean ± SD) during the late pregnancy (antepartum) and postpartum weeks in anemic and non–anemic groups. *: signicant
difference at
P<0.05 between non–anemic ewes and those with anemia using “t” test
A
A B
C D
E
G
F
H
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Hematological effects of the reproductive stage–internal parasitism interaction in ewes / Hadef et al. _____________________________
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TABLE IV
F–tests of xed effects of studied factors and interactions of internal parasites FEC levels with
the reproductive stages (time) in the mixed model for hematological parameters
Factors Time Season GIN Cocc. Fasc. Time × GIN Time × Cocc. Time × Fasc.
WBC
F 2.17 2.57 2.51 0.29 0.12 1.35 2.53 0.36
Sig. 0.15 0.06 0.12 0.59 0.73 0.25 0.045 0.70
RBC
F 16.45 11.78 22.56 0.02 0.11 72.70 9.39 15.17
Sig. 0.00 0.00 0.00 0.90 0.74 0.00 0.00 0.00
HGB
F 19.09 6.03 1.74 0.16 8.03 4.43 3.90 2.29
Sig. 0.00 0.00 0.20 0.69 0.01 0.04 0.01 0.11
HCT
F 21.39 11.15 19.67 0.02 0.02 91.01 9.43 14.05
Sig. 0.00 0.00 0.00 0.90 0.89 0.00 0.00 0.00
MCV
F 0.45 8.36 15.25 1.06 11.10 6.71 2.51 9.20
Sig. 0.51 0.00 0.00 0.31 0.00 0.01 0.048 0.00
MCH
F 8.10 12.22 155.48 0.39 8.07 50.41 1.08 31.20
Sig. 0.01 0.00 0.00 0.54 0.01 0.00 0.39 0.00
MCHC
F 1.16 30.44 175.77 0.37 16.18 56.54 0.61 28.49
Sig. 0.29 0.00 0.00 0.55 0.00 0.00 0.69 0.00
PLT
F 9.09 0.65 20.09 0.48 0.77 14.11 4.00 0.10
Sig. 0.01 0.63 0.00 0.50 0.40 0.00 0.01 0.90
Sig.:
P–value of F–test for xed effects which are signicant when P<0.05. Anemia: anemia status; Time: reproductive stages; GIN: gastrointestinal
nematodes FEC levels; Cocc.:
Coccidia FEC levels; Fasc.: Fasciola FEC levels
the infection by digestive strongyles [28] as observed during the
antepartum. During this period, prenatal stress mediated by Cortisol
[29] and hormonal changes such as Progesterone [30] levels may
affect the immune system of pregnant ewes. In addition, it has
reported that relative concentrations of eosinophil were highest in the
blood of pregnant ewes and reduced dramatically upon parturition, as
is characteristic of a stress response [31]. On the contrary, according
to Panousis et al. [32], the reproductive stage of the animals does
not seem to affect WBC.
At each period of sampling, both during late pregnancy, early
postpartum, or weaning except week 10 when most ewes were anemic
(91%), a signicant difference (P<0.05) in red blood cell count (FIG.
2B), hemoglobin concentration as well as hematocrit percentage
(FIG. 2C and FIG. 2D) was noted.
These parameter values were highest in non–anemic ewes in
comparison with those of anemic ewes. RBC counts were lower
than the minimum limit value (9 × 10
6
cells·μL
-1
) regardless of the
anemic status of the ewes during pregnancy, before or after
parturition and which may be largely due during the gestation period
to the physiological anemia of gestation and combined with other
factors including internal parasitism such as Haemonchus contortus
(hematophagy and leakage of blood from the site of attachment
of parasites) [11, 13, 33]. In contrast, pregnant sheep in a farm
environment with fecal samples consistently negative for nematode
eggs, coccidian oocysts, and adequate diet (good pasture), did not
develop anemia (HCT < 0.27), and the hematology (HCT and HGB) and
protein concentrations (total protein and albumin) were not different
in pregnant or non–pregnant ewes [34].
In the present study, erythrocytes parameters were signicantly
(P<0.01) determined by the reproductive stage, excepting MCV and
MCHC, and the season (TABLE IV). For the red cell indices (MCV, MCH,
MCHC) and platelet parameters (PLT), any signicant difference was
found between anemia groups (P>0.05) except one only marked
increase in anemic ewes during the weaning period for MCH and
MCHC at week 10 and PLT at week 8 p.p (FIG. 2F, FIG. 2G, and FIG. 2H,
respectively). The effect of internal parasites on these parameters
was expressed by the impact of the level of their egg shedding, which
was signicant for that of gastrointestinal nematodes (GIN), excepting
on hemoglobin concentration, but not for that of Eimeria. For that of
Fasciola, it was signicant only for hemoglobin and the red cell indices
(MCV, MCH, and MCHC). The interaction of the reproductive stage with
this indicator of internal parasites burden severity had a signicant
effect on changes in most erythrocytes parameters (P<0.01) excluding
that of interaction with Fasciola FEC level on hemoglobin and that of
interaction with Eimeria oocyst count on MCH and MCHC (P>0.05).
For platelet count variation (TABLE IV), a signicant effect of
individual factors (anemia status and reproductive stage) and the
shedding level of nematode eggs was revealed (P<0.01). In addition,
it appeared to be inuenced by the interaction of the breeding stage
with the level of excretion of GIN eggs and Coccidia (P<0.01) but not
with that of Fasciola (P>0.05). However, this parameter was not
affected by the season or Coccidia and Fasciola FEC levels (P>0.05).
In a study conducted on West African Dwarf sheep reared under a
semi–intensive system, no signicant changes in HCT, RBC, HGB, MCV,
MCH, or MCHC values during the postpartum period (between days 5
and 30 p.p.) were noted [35]. In agreement with the latter ndings,
MCV did not reveal a decrease in values, which goes hand in hand
with the number of red blood cells during the present study. Thus,
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these results are in contrast with those observed by Bezerra etal.
[36] who reported a decrease in MCV during the different stages of
reproduction with a recovery at weaning. However, in the present
study, the interaction of the reproductive stage with the three types
of parasites had a signicant effect on MCV. A similar decrease in the
recorded values of hematological parameters mainly HCT, HGB and
RBC was noted in sheep naturally infected by Fasciola hepatica [37].
CONCLUSIONS
The present study highlighted signicant variation in hematological
parameters in anemic ewes in response to the combined effects of
internal parasitism and the metabolic and endocrine changes involved
in the transition from pregnancy to the postpartum period. Under
the Mediterranean climate favorable to the development of internal
parasites, infections during these critical reproductive periods remain
an important health threat that should be considered and monitored
by biological markers for better ock management. The study could
not determine which species of internal parasites was the main agent
compromising the hematological status of animals, therefore to
select the most effective anthelmintic drug to be used in the control
program. This seems essential from a research perspective to assess
the potential resistance behavior of their infective agents in response
to anthelmintic molecules under the inuence of host–related factors.
Conict of interests
The authors of this study declare that there is no conict of interest
with the publication of this manuscript.
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