https://doi.org/10.52973/rcfcv-e34438
Received: 05/04/2024 Accepted: 10/06/2024 Published: 31/08/2024
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Revista Científica, FCV-LUZ / Vol. XXXIV, rcfcv-e34438
ABSTRACT
The objective of the essay was to determine the inuence of protein–
energy supplementation on the gastrointestinal nematode population
during spring rise in ewes and their offspring as a non–chemical
alternative in Integrated Parasite Control. One hundred twenty six
Corriedale ewes were divided into two groups, one supplemented with
protein–energy blocks from one month before lambing until weaning
and the other without supplementation. Every 17 days, faecal matter
was randomly collected from 20 ewes and 20 lambs from both groups.
Modied McMaster and coproculture were performed, estimating the
pathogenicity index for each gender. Lambs´ weight at birth, marking
and weaning were recorded and the daily weight gains from birth to
marking and from marking to weaning were calculated. Eggs count per
gram of faeces were higher (P<0.05) in the non–supplemented group
and their lambs. The predominant genus in dams and lambs were
Haemonchus contortus and Trichostongylus spp. The pathogenicity
index in the non–supplemented dams was higher than 1 from the
faecal egg count increase. The lamb body weights and average daily
gains were higher in those lambs born to the supplemented dam
group (P<0.05). In conclusion, the supplementation contributed to
the non–chemical control of the most prevalent gastrointestinal
nematode in periparturient ewes, H. contortus, and environmental
contamination for lambs at the dam foot.
Key words: Supplementation; sheep; lamb; gastrointestinal nematode
RESUMEN
El objetivo del ensayo fue determinar la influencia de la
suplementación proteico–energética sobre la población de nematodos
gastrointestinales durante el alza de lactación en ovejas y sus corderos
como alternativa no química en el Control Integrado de Parásitos. Se
dividieron 126 ovejas Corriedale en dos grupos, uno fue suplementado
con bloques proteico–energéticos desde un mes antes del parto
hasta el momento del destete y el otro grupo permaneció durante el
mismo período sin suplementación. Cada 17 días se recogió materia
fecal de 20 ovejas y 20 corderos de ambos grupos elegidos al azar. A
estas muestras se les realizó las técnicas de McMaster modicado y
coprocultivo, estimándose además el índice de patogenicidad para
cada género. Se registró el peso de los corderos al nacimiento, en
el momento de la realización de la marca de propiedad en la oreja y
al destete. Se calculó la ganancia diaria de peso entre el nacimiento
y el momento de la marcación en la oreja y entre este último y el
destete. El contaje de huevos por gramo de materia fecal fue mayor
(P<0,05) en el grupo no suplementado y en sus corderos. Los géneros
predominantes en las madres y en los corderos fueron Haemonchus
contortus y Trichostongylus spp. El índice de patogenicidad en las
madres no suplementadas fue superior a 1 debido al aumento del
recuento de huevos en materia fecal. El peso vivo y la ganancia media
diaria de los corderos fueron mayores en los corderos nacidos del
grupo de madres suplementadas (P<0,05). En conclusión, los bloques
proteico–energéticos contribuyeron al control no químico de H.
contortus (alza de lactación), retrasando dos semanas su presentación,
además, con la disminución signicativa del pico de huevos en materia
fecal, la contaminación ambiental de los corderos al pie de la madre
disminuyó, lo que resultó en un recuento de huevos en materia fecal
signicativamente más bajo y en corderos con mayor peso vivo al
nacer y ganancia media diaria. Trichostrongylus spp. Fue el segundo
con mayor índice de patogenicidad.
Palabras clave: Suplementación; ovinos; corderos; nematodos
gastrointestinales
Effect of supplementation on estimated parasite load in periparturient
ewes and their offspring
Efecto de la suplementación sobre la carga parasitaria estimada
en ovejas en periparto y su descendencia
María Soledad Valledor–Echegaray
1
, Luis Cal–Pereyra
2
, Karina Neimaur
3
*
1
Universidad de la República, Facultad de Veterinaria, Departamento de Patobiología. Unidad Académica Parasitología Veterinaria. Montevideo, Uruguay.
2
Universidad de la República, Facultad de Veterinaria, Departamento de Patobiología, Unidad Académica Patología. Montevideo, Uruguay.
3
Universidad de la República, Facultad de Veterinaria, Departamento de Producción Animal y Salud de los Sistemas Productivos,
Unidad Académica Ovinos, Lanas y Caprinos. Libertad, San José, Uruguay.
*Corresponding autor: kneimaur@gmail.com
Ewe suplementation and spring rise / Valledor-Echegaray et al. ____________________________________________________________________
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INTRODUCTION
Sheep (Ovis aries) production faces different daily challenges,
and parasitosis is one of the most important [1]. Among them,
gastrointestinal nematodes (GIN) are the main ones, and, in Uruguay,
the genus diagnosed are Haemonchus contortus (43%), Trichostrongylus
axei (12%), Nematodirus spp. (11%) and Trichostrongylus spp. (26%) [2].
The incidence of the different GIN is determined by their pathogenic
potential (PP), biotic potential (BP), and the number of parasites
present, and all of them make the Pathogenicity Index (PI) vary [3].
GIN reduce voluntary intake by 10%, generating a body weight (BW)
reduction of 33% in adult animals [4] and of 23.6% in the rearing [1].
Moreover, if infection occurs before the lambs are one month old,
there is no effect on their body condition score (CS) [4, 5].
Adult sheep have immunity to GIN that allows them to perform
productively [6], while lambs (3–6 months) do not eliminate their rst
infection, generating parasitic disease where Trichostrongylus spp.
produces acquired and specic immunity faster than H. contortus
[1]. The response of sheep to a parasitic challenge depends on age
and nutritional status level [7, 8, 9, 10, 11, 12, 13, 14], and frequency
of challenges and genetic factors [15]. Despite this power of
response, in breeding ewes, immune weakening occurs in the period
immediately after lambing, known as “spring rise” [16, 17, 18, 19, 20]. This
epidemiological phenomenon is measurable through the signicant
increase in egg elimination per gram of faeces (EPG) of GIN. In addition,
it allows massive contamination of the paddock and acts as a source
for susceptible lambs before weaning [2, 18]. In Corriedale sheep, the
spring rise has been determined between the sixth and eighth week
postpartum in Uruguay [21] and United Kingdom [22]. In Australian
Merino ewes, this phenomenon coincided with peak milk production
(2–4 weeks postpartum) [23].
Increases in prolactin levels associated with parturition and lactation
have been shown to have a suppressive effect on the immune system,
reducing IgA levels, which favours increased fertility of H. contortus and,
therefore, of EPG [24]. Immunorelaxation also occurs due to increased
energy and protein requirements in postpartum and lactation [9]. In
addition, at 2 to 3 weeks postpartum, the emergence of hypobiotic
larvae (L4) of H. contortus from the mucosa is another critical factor in
spring rise [1]. Pastures have higher parasite loads due to this increase
in faecal egg counts (FEC), which is more marked when lambing takes
place in spring [19, 25, 26].
The lamb is subjected to two sources of parasitic infectation, one
being the dam herself and the other due to residual ingestion of
infesting larvae (L3) from previous grazing [27, 28].
The emergence and development of anthelmintic resistance (AR) in
sheep, mainly Trichostrongylus spp. and H. contortus was generated by
the exclusive use of anthelmintics as the sole control measure [29, 30].
However, changes in nutritional management in sheep can inuence
GIN behaviour [7, 8, 9, 10, 11 ,12, 30]. Donaldson et al. [25] indicated
that the increase in EPG that occurs in peripartum in Coopworth
ewes and the environmental contamination produced from this EPG
can be reduced by protein supplementation to ewes from the month
before lambing. Nutritional protein supplementation benets the
immune response in sheep [1, 13, 14, 31], although Provenza et al. [32]
indicated that protein supplementation without an energy source
could generate adverse effects due to excess ammonia.
Therefore, this research aimed to determine the influence of
protein–energy supplementation on the GIN population at spring
rise in ewes and their offspring as a non–chemical alternative in
Integrated Parasite Control (IPC).
MATERIALS AND METHODS
The trial was conducted at the Experimental Station Nº 1 of the
Facultad de Veterinaria (Canelones, Uruguay, 34°37'28" Latitude;
55°60'27" Longitude) from May to December 2015.
Animals
A total of 126 full–mouths Corriedale ewes, individually identied,
were used. The ewes were selected from a flock of 300 animals,
blocked by age, CS, body weight (BW), tooth and hoof condition, thus
homogenising the sample. The ewes were synchronised in March with
intravaginal sponges containing 160 mg of progesterone (Cronipres®
CO, Biogénesis–Bagó) previous articial insemination [33]. Transrectal
ultrasonography was carried out in May when 126 ewes with single
gestation were selected. Lambing lasted from August 22
nd
to August 31
st
.
During the whole trial, the animals were grazing on natural pasture,
mainly composed by Cynodon dactylon. In February, the ewes were
dosed with Naftalophos 80% (Baymetin, Laboratorio BayerR, Uruguay).
The ewes were supplemented with protein–energy blocks
(Metabolisable Energy = 8.8 MJ·kg
-1
, protein = 15%; Compañía Cibeles
SA.) at a rate of 300 g·day
-1
from August 12
th
to December 9
th
(weaning of
the lambs). An adaptation period of 10 days (d) to feeding with the blocks
was carried out in a small paddock. During this period, one person
was responsible for identifying those ewes that ate the supplement,
making four daily observations of 1 hour. At the end of this period, the
animals were divided into two groups: the supplemented group (GS, n=
54) and the non–supplemented group (GC, n= 72), and were located in a
new paddock, which was divided into equal parts by an electric fence.
Determinations in sheep
From August 12
th
to November 22
nd
, faecal samples were collected
every 17 d from 20 animals (randomly) from both experimental groups.
These were directly obtained from the rectum [34], conditioned and
identied in nylon bags (without air) and transported refrigerated to
the laboratory [34, 35].
Determinations in lambs
From October 7
th
to December 9
th
, faecal samples were taken every 17
d from 20 lambs (randomly) born to dams of both experimental groups
and were obtained and conditioned in the same way as in the dams.
BW was determined in all lambs at birth, at marking (average age:
22 d) and at weaning (average age: 98 d) using a digital scale (Baxtran,
UCS30, Spain). Average daily gain (ADG) for the birth–marking and
marking–weaning periods were calculated.
Laboratory analysis
Faecal samples from ewes and lambs were processed at the
Facultad de Veterinaria Parasitology Laboratory. Modied McMaster
technique was carried out using a McMaster camera (INTA, Argentina)
and a microscopy with 40× sensitivity (Olympus, model CX21, Tokyo,
Japan) [36]. The technique was based on FEC, and the result was
expressed in eggs per gram of faeces (EPG). Coproculture (CL) was
FIGURE 1. Average meteorological records of temperature and rainfall during
the assay
FIGURE 2. Mean EPG of the lambs and their dams from the GS and GC (GS:
supplemented group and GC: control group)
_____________________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIV, rcfcv-e34438
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carried out using Roberts and O’Sullivan technique (modied) [36,
37] and subsequent morphological identication of the L3 obtained
using the Niec´s key [38], counting a minimum of 100 L3, and was
expressed in percentage of each genus.
Pathogenicity index
Based on the EPG and CL and according to the BP of each genus
(H. contortus, 5000–10000 eggs·day
-1
; Trichostrongylus spp., 200
eggs·day
-1
, and Oesophagostomum spp., 3000 eggs·day
-1
), the
probable number of GIN females was estimated according to the
following formula:
%
Nfemales
BP of thegenus
EPGofthe genus gfaecalmatterper d
BW5
º
×
=
^h
!+
The number of males was calculated as 70% of females. The
pathogenicity index (PI) of each of the nematodes was determined
using the following formula:
PI
Theorethical pathogenicityfactor
NfemalesNmales
ºº
=
+
^h
The theoretical pathogenicity factor used was 500 for H. contortus,
4000 for Trichostrogylus spp. and 100 for Oesophagostomum spp.
The parasite/host ratio is considered to be in favour of the former
whenever the PI is greater than 1 and in favour of the latter whenever
the PI is less than 1. Furthermore, a PI value of 2 initiates parasitic
symptomatology in sheep [3, 39].
Meteorological records
Daily average records of temperature (ºC) and rainfall (mm) were
taken at the Migues Experimental Station using a meteorological
station (Vantage Vue, Davis Instruments, USA). FIG. 1 shows the
average meteorological records during the trial.
analysis of variance (ANOVA). Live weights of lambs at birth, marking
and weaning, and daily gains in birth–marking and marking–weaning
periods were analysed by ANOVA, determining the effect of treatment
(GS, GC) and sex and their interaction. The signicance level was
P<0.05, and P values between 0.05 and 0.10 were considered as trend.
The statistical package STATA was used for the analysis.
RESULTS AND DISCUSSION
EPG in ewes
As shown in FIG. 2, in the rst sampling, no signicant difference
in the egg count/gram of faecal matter was found (54.3 and 110.4, GS
and GC, respectively). From the second sampling (August 29
th
) until the
last sampling (November 22
nd
), the GC presented signicantly higher
values (P<0.05) than the GS, except in the fth sampling (October 19
th
),
where no signicant difference between treatment groups was found.
Statistical analysis
EPG values obtained were normalised and expressed in logarithm
in base 10. Descriptive statistics (averages ± SEM) of the variables
analysed (EPG, lambs´ body weight, and mean daily gains) were
performed. The effect of treatment (GS, GC) on EPG was determined by
The maximum peak of eggs per gram occurred rst in the GC in the
seventh week postpartum (October 2
nd
; 977.5 EPG). This EPG behaviour
is similar to that described by Crofton [40], who denes this short–
duration phenomenon related to the time of parturition as spring rise.
Furthermore, these results agreed with those reported by Cardozo and
Berdie [21] and Nari and Cardozo [2], who described that the spring
rise occurs between the sixth and eighth week postpartum. Donaldson
et al. [25], Beasley et al. [19] and Mederos et al. [26] further suggested
that this increase is more marked when lambing takes place in spring,
which would coincide with the results of the present trial.
In the GS, the peak of EPG occurred at nine weeks post–lambing
(October 19
th
; 352 EPG), with EPG values lower than in the control group.
At this time, no signicant difference was found between treatment
groups. These results agreed with those reported by Donaldson et al.
[25] who showed that ewes supplemented with protein in peripartum
showed a lower increase in postpartum FEC. These authors found no
evidence of inhibition larval development or GIN egg–laying, which
suggests that the main effect of protein supply to dams would be to
improve resistance at the larval establishment stage of GIN.
FIGURE 3. Image of larval culture. (A): L3 Haemonchus contortus and (B): L3
Trichostrongylus spp.
A
B
TABLE I
Larval culture and Pathogenicity Index of GS and GC dams
August 12
nd
August 29
th
September 15
th
October 2
nd
October 19
th
November 5
th
November 22
nd
GS GC GS GC GS GC GS GC GS GC GS GC GS GC
Larval culture (%)
Haemonchus contortus 40 43 38 45 63 68 57 65 60 66 60 66 88 92
Trichostongylus spp. 38 40 45 38 20 23 13 19 21 19 21 19 8 7
Teladorsagia spp. 7 2 8 6 7 5 15 4 6 4 6 4 0 0
Cooperia spp. 0 0 4 8 5 2 6 7 5 4 5 4 0 0
Oesophagostomum spp. 15 15 5 3 5 2 9 5 8 7 8 7 4 1
IP
Haemonchus contortus 0.1 0.1 0.0 0.1 0.0 0.4 0.2 1.0 0.3 0.8 0.1 0.6 0.2 1.5
Trichostongylus spp. 0.0 0.0 0.1 0.2 0.1 1.1 0.2 0.1 0.2 0.7 0.1 0.6 0.0 0.4
Teladorsagia spp. 0.0 0.1 0.0 0.1 0.0 0.2 0.0 0.3 0.3 0.2 0.0 0.2 0.0 0.0
Cooperia spp. 0.0 0.0 0.0 0.0 0.0 0.2 0.0 0.1 0.1 0.3 0.0 0.1 0.0 0.0
Oesophagostomum spp. 0.0 0.0 0.1 0.3 0.0 0.2 0.1 0.3 0.4 0.5 0.1 0.6 0.0 0.1
Totales 0.1 0.3 0.3 0.6 0.2 2.2 0.5 1.9 1.4 2.5 0.3 2.1 0.2 2.0
GS= supplemented group; GC= control group; IP= Pathogenicity Index
Ewe suplementation and spring rise / Valledor-Echegaray et al. ____________________________________________________________________
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Likewise, de Melo et al. [31], Torres–Acosta et al. [14], and Molento
et al. [13] indicated that protein supplementation improved nutritional
intake and resistance to helminth infection in sheep, thus increasing
the capacity of the animals to resist the adversities of parasitism.
Therefore, it could be used as a non–chemical control method for
parasitosis, as indicated by Castells et al. [1], stating that a high
nutritional level would benet the health of the sheep, improving
the immune response.
EPG in lambs
In the rst two samplings, no signicant differences were found
between treatment groups in egg counts/gram of faecal matter.
In the third sampling (November 22
nd
), lambs born to GC dams had
signicantly higher EPG values than those born to GS dams (245.3 and
40 EPG, respectively; P<0.05). In the last sampling, the EPG values
of lambs born to GC dams continued to be signicantly higher (272.2
and 45.7, respectively; P<0.05) (FIG. 2). The EPG peaks presented
by both experimental groups would generate an increase of L3 in
the pastures, which can be ingested by susceptible animals (lambs)
[2]. Castells et al. [1] indicated that environmental contamination
generated by H. contortus and its high BP would be the primary source
of infection for the lamb at the foot of the dam. This result would
coincide with those of the present trial, as the lambs born to the GC
had signicantly higher EPG values than those born to the GS from
the third sampling onwards, which continued until the end of the trial.
According to Castells et al. [1], lambs would be susceptible at rst
contact with this L3 as they have a less developed immune system.
Larval culture in ewes and lambs
Concerning larval culture in dams, the predominant GIN genus
was H. contortus, followed by Trichostongylus spp. (FIG. 3), while
Teladorsagia spp., Cooperia spp. and Oesophagostomum spp. genus
were present in percentages lower than 10% (TABLE I). This coincided
with those reported by Nari and Cardozo [2] and Castells et al. [6],
which indicate that the predominant genus were H. contortus and
Trichostrongylus spp.
In the lambs the predominant genus were H. contortus and
Trichostongylus spp. In addition, 10% of Oesophagostomum spp. was
present in the November 22
nd
sampling. In this category, the genus of GIN
identied was in agreement with the results obtained in Uruguay by Nari
and Cardozo [2], Castells et al. [6], Valledor [41] and de Melo et al. [31],
who also diagnosed Oesophagostomum spp. as the third prevalent genus.
In both categories, H. contortus was the GIN genus that started to be
identied in late winter, when temperatures began to rise. These results
agreed with Castells et al. [1], van Dk et al. [42] and McMahon et al. [43],
who described this nematode as the most prevalent in warm climates
(autumn and spring, with mild temperatures and the presence of rainfall),
when its BP was expressed at its highest level (5000–10000 eggs·d
-1
) [1].
TABLE II
Larval culture and Pathogenicity Index of GS and GC lambs
Oct. 19
th
Nov. 5
th
Nov. 22
nd
Dec. 9
th
GS GC GS GC GS GC GS GC
Larval culture (%)
Haemonchus contortus 55 65 58 64 60 69 75 78
Trichostongylus spp. 15 20 20 19 15 10 12 12
Teladorsagia spp. 18 5 7 4 14 8 0 0
Cooperia spp. 6 7 6 5 4 3 5 3
Oesophagostomum spp. 6 4 9 8 7 10 8 7
IP
Haemonchus contortus 0.01 0.01 0.00 0.01 0.00 0.03 0.00 0.20
Trichostongylus spp. 0.02 0.02 0.00 0.04 0.03 0.03 0.03 0.20
Teladorsagia spp. 0.05 0.05 0.10 0.11 0.08 0.09 0.08 0.50
Cooperia spp. 0.03 0.04 0.10 0.08 0.00 0.24 0.00 0.00
Oesophagostomum spp. 0.05 0.87 0.10 0.11 0.16 0.18 0.16 1.00
Totales 0.15 0.98 0.30 0.35 0.40 0.76 0.21 1.90
Oct= October; Nov.= November; Dec.= December; GS= supplemented group; GC=
control group; IP= Pathogenicity Index
TABLE III
Body weight of the lambs at birth, marking and weaning, average daily gain
between birth and marking and between marking and weaning (Mean ± SEM)
GS GC
Birth (kg) 5.26 ± 0.10
a
4.96 ± 0.08
b
Marking (kg) 10.02 ± 0.37
a
8.82 ± 0.27
b
Weaning (kg) 18.90± 0.48
a
17.11 ± 0.37
b
AGD Birth–marking (g·day
-1
) 240.00 ± 20.00
a
170.00 ± 10.00
b
AGD Marking–weaning (g·day
-1
) 150.00 ± 0.00
a
140.00 ± 0,00
b
BW= body weight; GS= supplemented group; GC= control group; AGD= average daily
gain;
a–b
= P<0.05
_____________________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIV, rcfcv-e34438
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Pathogenicity Index in ewe and lambs
The PI determined in the dams in both experimental groups is
presented in TABLE I. In the GC, the PI higher than 1 coincided with
the beginning of the increase in EPG (September 15
th
) and remained
elevated until the end of the trial (November 22
nd
). On the other hand,
the GS presented a PI above 1 only at the EPG peak (October 19
th
) at
the expense of the sum of the GIN.
The PI in those lambs born to GS dams at no time exceeded the
value of 1, while in the GC, it was higher than 1 in the last sampling
(December 9
th
) (TABLE II).
According to Ueno and Goncalves [44], PI values above 1 favours the
parasite over the host. In the present work, this situation was present
in the GC dams from the EPG peak and maintained until the end of the
trial. However, in the GS, it was only observed at the peak of EPG due to
the addition of the GINs. In lambs, only in the GC last sampling the PI was
higher than 1, and Oesophagostomum spp. was the most prevalent genus.
CONCLUSION
According to the results, the protein–energy blocks contribute to the
non–chemical control of the spring rise phenomenon and environmental
contamination for lambs at the foot of the dam. They signicantly
decreased the peak of EPG and delayed its presentation by two
weeks. Haemonchus contortus was the most prevalent GIN genus, and
Trichostrongylus spp. was the second one with had the highest PI. In
lambs, maternal supplementation also resulted in a signicantly lower
EPG and lambs with higher BW at birth and AGD. Further studies on the
non–chemical control of GIN are required because of its importance
in integrated control and environmental preservation.
Conict of interest
The authors declare that they have no competing interests.
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Body weight in lambs
BW at birth, marking and weaning were signicantly higher in lambs
born to the supplemented dam group (P<0.05). Average daily gains at
birth–marking and marking–weaning periods were also signicantly
higher in lambs born to the GS (P<0.05) (TABLE III). None of the variables
were affected by sex or the interaction between treatment group and
sex. The higher BW at birth, marking and weaning, and higher ADG
obtained in both periods evaluated in lambs born to the supplemented
dams demonstrated that supplementation could be helpful for parasitic
control in susceptible categories. De Melo etal. [31] showed that lambs
born to Ile de France and Dorper/Santa Inês ewes supplemented with
a protein concentrate and deworming treatments from lambing to
weaning obtained lower EPG values and higher daily weight gains
compared to lambs born to unsupplemented control group dams.
Ewe suplementation and spring rise / Valledor-Echegaray et al. ____________________________________________________________________
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the 23
rd
International Conference of the World Association for the
Advacement of Veterinary Parasitology; 2011 Aug. 21–25; Buenos
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