https://doi.org/10.52973/rcfcv-e34340
Received: 19/10/2023 Accepted: 04/03/2024 Published: 12/06/2024
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Revista Científica, FCV-LUZ / Vol. XXXIV, rcfcv-e34340
ABSTRACT
The physiological process of birth can cause stress in animals because
it affects many mechanisms. The aim of this study was to determine
the effect of the type of birth on the Nesfatin–1 level and to explain
the relationship with oxidative stress parameters in Awassi breed
sheep. The study included a total of 60 sheep with a singleton birth in
3 groups: as Group 1 (n:20) including animals that had a normal birth,
Group 2 (n:20) that had a dicult birth (dystocia), and Group 3 (n:20)
including sheep that gave birth by caesarean section. Blood samples
were taken from the sheep in all the groups within 10 min of the birth,
for the measurement of Nesfatin–1, total antioxidant capacity (TAS),
and total oxidant capacity (TOS). The data obtained were examined
with One–Way Variance Analysis, and relationships between the
data with the Pearson test. Statistically signicant differences were
determined between the groups in respect of Nesfatin–1, TAS, TOS,
and oxidative stress index (OSI) levels (P<0.001). The Nesfatin–1, TOS,
and OSI levels were determined to be lowest in the normal birth group
and highest in the caesarean birth group (P<0.001). The TAS level was
highest in the normal birth group and lowest in the caesarean birth
group (P<0.001). A signicant negative correlation was determined
between Nesfatin–1 and TAS (r=-0.932, P<0.001), and a signicant
positive correlation was determined between Nesfatin–1 and TOS,
and between Nesfatin–1 and OSI (r=0.957, P<0.001; r=0.960, P<0.001,
respectively). These results demonstrated a signicant difference in
Nesfatin–1 level according to the type of birth. Therefore, Nesfatin–1
could be a new biomarker in the determination of oxidative stress in
sheep according to the type of birth, and it was concluded that one of
the interventions that would decrease oxidative stress after dystocia
and caesarean births would be to provide an increase in endogenous
Nesfatin–1 because of its antioxidative property.
Key words: Nesfatin–1; oxidative stress; dystocia; caesarean
section; sheep
RESUMEN
El proceso siológico del nacimiento puede provocar estrés en los
animales porque afecta a muchos mecanismos. El objetivo de este
estudio fue determinar el efecto del modo de nacimiento sobre
el nivel de Nesfatin–1 y explicar la relación con los parámetros de
estrés oxidativo en ovejas de raza Awassi. El estudio incluyó un
total de 60 ovejas con un parto único en 3 grupos: Grupo 1 (n:20)
que incluye animales que tuvieron un parto normal, Grupo 2 (n:20)
que tuvo un parto difícil (distocia) y Grupo 3. (n:20) incluyendo ovejas
que dieron a luz por cesárea. Se tomaron muestras de sangre de las
ovejas en todos los grupos dentro de los 10 minutos posteriores al
nacimiento, para medir la Nesfatina–1, la capacidad antioxidante total
(TAS) y la capacidad oxidante total (TOS). Los datos obtenidos fueron
examinados con Análisis de Varianza Unidireccional y las relaciones
entre los datos con la prueba de Pearson. Se determinaron diferencias
estadísticamente signicativas entre los grupos con respecto a los
niveles de Nesfatin–1, TAS, TOS y el índice de estrés oxidativo (OSI)
(P<0,001). Se determinó que los niveles de Nesfatin–1, TOS y OSI eran
más bajos en el grupo de parto normal y más altos en el grupo de
parto por cesárea (P<0,001). El nivel de TAS fue más alto en el grupo
de parto normal y más bajo en el grupo de parto por cesárea (P<0,001).
Se determinó una correlación negativa signicativa entre Nesfatin–1
y TAS (r =-0,932, P<0,001), y una correlación positiva signicativa
entre Nesfatin–1 y TOS, y entre Nesfatin–1 y OSI (r =0,957, P<0,001;
r=0,960, P<0,001, respectivamente). Estos resultados demostraron
una diferencia signicativa en el nivel de Nesfatin–1 según el modo de
nacimiento. Por tanto, Nesfatin–1 podría ser un nuevo biomarcador
en la determinación del estrés oxidativo en ovejas según el modo
de nacimiento, y se concluyó que una de las intervenciones que
disminuirían el estrés oxidativo tras distocia y partos por cesárea
sería proporcionar un aumento en Nesfatin–1 endógeno debido a su
propiedad antioxidante.
Palabras clave: Nesfatin–1; estrés oxidativo; distocia, cesárea;
oveja
An evaluation of Nesfatin–1 levels in Awassi sheep according to
the type of birth
Una evaluación de los niveles de Nesfatin–1 en ovejas Awassi según el tipo de parto
Tuğra Akkuş , Ömer Yaprakci*
Harran University, Faculty of Veterinary Medicine, Department of Veterinary Obstetrics and Gynecology. Sanliurfa, Türkiye.
*Corresponding author: yaprakciomer275@gmail.com
FIGURE 1. Study design for evaluation of Nesfatin–1 levels in Awassi sheep
according to the type of birth
Nesfatin-1 level according to type of birth / Akkuş and Yaprakci ____________________________________________________________________
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INTRODUCTION
Birth is the process of the removal of the fetus together with uids
and membranes of the offspring from the maternal organism at the end
of pregnancy, which is specic to the species [1]. Dystocia is dened as
a life–threatening condition for both mother and newborn due to birth
not having occurred in a certain time and that cannot occur without
some kind of intervention [2]. Dystocia may be of fetal or maternal origin
[3, 4]. and causes severe decreases in reproductive performance and
puerperal infections. It is also of great importance that there may be
complications that can result in the death of the offspring and even
the mother [3, 5, 6]. A caesarean section operation is a laparotomy
method to remove the fetus by making an incision in the abdominal
wall and uterus, which is used when vaginal route delivery is high risk
or not possible. This is widely used in all living creatures in cases of
dystocia, where the mother, fetus, or both are at risk [6].
Oxidative stress develops when there is an imbalance in cells
because of an increase in free radicals or a decrease in antioxidants.
There is a series of special mechanisms that keep this stress under
control. When these mechanisms remain insucient, oxidative
damage occurs [7]. When the antioxidant systems are inadequate
against oxidative stress, the progression of oxidative damage can
cause damage to proteins, lipids, carbohydrates, and Deoxyribonucleic
acid (DNA) in cells, resulting in cell dysfunction [8, 9]. Organs and
tissues with a high metabolism rate and high energy demands,
primarily the muscles, heart, liver, brain, and skin, are affected by
high levels of oxidative stress [10].
Nesfatin–1, which was discovered in 2006, is a 9.7 kDa peptide
formed of 82 amino acids and is effective in the physiological
control of feeding behaviour. It plays a role in body weight control by
suppressing the peristaltic activity of the digestive system, ultimately
reducing food intake [11]. Non–esteried fatty acid/nucleon binder–2
(NUCB2) is the precursor of Nesfatin–1 [12]. Previous studies have
shown that Nesfatin–1 has vital power in the suppression of energy
intake through signals coming from peripheral tissues in the brain
[13] and is protective against serious metabolic disorders [14].
Biochemical, immunohistochemical, physiological, pathological, and
pharmacological studies related to Nesfatin–1 have focused more on
humans and some animal species to date [15]. Recent studies have
shown antioxidant, anti–inammatory, and anti–apoptotic effects of
Nesfatin–1 in different diseases [16, 17].
The aim of this study was to determine the effect of the type of
birth on the Nesfatin–1 level in Awassi breed sheep, and to investigate
the correlations between Nesfatin–1 and oxidative stress parameters.
There is no previous study in the literature that has evaluated
Nesfatin–1 in sheep according to the type of birth, and therefore
this study can be considered to contribute to the literature.
MATERIALS AND METHODS
Approval for this study was granted by the Animal Experiments
Local Ethics Committee of Harran University (HRÜ–HADYEK) (decision
no: 2023/005).
Animal selection and experiment protocol
This study was conducted between February and March 2022 at
the Obstetrics and Gynaecology Clinic of Harran University Veterinary
Faculty Animal Hospital, located in the Eyyubiye district of Şanlıurfa
Province, southeast Türkiye, at an altitude of 517 m, 37.11974 latitude
and 38.81990 longitude (average temperature (°C): 6.35, average
monthly total rainfall (mm): 65.35) [18]. The animal sample comprised
60 Awassi sheep, aged 2–4 years, each weighing mean 55.24 ± 1.22
kg, with a body condition score ranging from 2–3 (1=Extremely weak,
5=Obese) (2.56 ± 0.06), which had previously given birth at least once,
and had no genital system conditions.
The 60 sheep were separated into 3 groups as Group 1 (n:20)
including animals that had a normal birth, Group 2 (n:20) those that
had a dicult birth (dystocia), and Group 3 (n:20) including sheep
that gave birth by caesarean section. Dystocia was dened as a
dicult delivery which exceeded 90 min in total, or when there was
no progression for 30 min after rupture of the fetal membranes [19].
For sheep that could not deliver despite interventions, a caesarean
section operation was performed.
Blood sample collection and laboratory analysis
Blood samples were taken from the vena jugularis of the ewes in
all the groups within 10 min of the birth of the offspring. The blood
samples were centrifuged (NÜVE NF 200, Ankara, Turkey) at 3000 G
or 10 min to obtain serum samples, which were then stored at -20°C
until the day of analysis. To determine the serum Nesfatin–1 levels
of the sheep in all the groups, a commercial kit was used (Sheep
Nesfatin E0095Sh, ELISA Kit – NES BT–LAB kit.). The serum TAS and
TOS levels were examined using commercial kits (Total Antioxidant
Status, NN21117A, Rel Assay Diagnostics, Mega Tıp, Gaziantep, Türkiye,
and Total Oxidant Status NN211290, Rel Assay Diagnostics, Mega Tıp,
Gaziantep, Türkiye) and were determined spectrophotometrically at
660nm for TAS and at 530 nm for TOS (Molecular Device SpectraMax
M5 Plate Reader, Pleasanton, CA, USA) FIGURE 1. The oxidative stress
index (OSI) was calculated as the ratio of the TAS and TOS levels [20].
Statistical analysis
Data obtained in the study were analyzed statistically using
Statistical Package for the Social Sciences (SPSS Statistics for
Windows) [21] software. Conformity of variables to normal distribution
was assessed using visual (histogram and Q–Q Graphs) and analytical
methods (Shapiro–Wilk tests). Descriptive analyses were stated as
mean ± standard error (SEM) values for variables showing normal
distribution. As the relevant data showed normal distribution, One–
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Way Variance Analysis was applied in the comparisons of the groups.
Correlations of the data and statistical signicance were determined
with the Pearson test. The total error margin for statistical signicance
was determined as 5%.
RESULTS AND DISCUSSION
The Nesfatin–1 levels and oxidative stress parameters according to the
type of birth are presented in TABLE I. Statistically signicant differences
were determined between the groups in respect of Nesfatin–1, TAS,
TOS, and OSI levels (P<0.001). The Nesfatin–1, TOS, and OSI levels were
determined to be lowest in the normal birth group and highest in the
caesarean birth group (P<0.001). The TAS level was highest in the normal
birth group and lowest in the caesarean birth group (P<0.001). Signicant
correlations were determined between the Nesfatin–1 level and oxidative
stress parameters (P<0.01). There was seen to be a signicant negative
correlation between Nesfatin–1 and TAS (r=–0.932, P<0.001), and a
signicant positive correlation was determined between Nesfatin–1 and
TOS, and between Nesfatin–1 and OSI (r=0.957, P<0.001; r=0.960, P<0.001,
respectively). There was also determined to be a signicant negative
correlation between TAS and TOS (r= –0.967, P<0.001) and between TAS
and OSI (r=–0.994, P<0.001), and a signicant positive correlation between
TOS and OSI (r=0.981, P<0.001) TABLE II.
The results of this study present important data that will contribute
to the understanding of the effect type of birth on Nesfatin–1 levels
and oxidative stress in Awassi breed sheep. The physiological process
of birth can cause stress in animals because many mechanisms are
affected. It has been stated that a normal birth is a stressful process
and abnormal deliveries (dystocia, caesarean) can contribute further
to the stress of a normal birth [22].
Aerobic exercise has a signicant effect on energy–regulating
hormones such as Nesfatin–1 [23]. Muscle activity induced by aerobic
exercise has been shown to lead to signicant increases in Nesfatin–1
levels in healthy women [24, 25]. In another study the increase in
Nesfatin–1 levels after high–intensity training was shown to be no
different from the increase after moderate intensity training [24].
There has been determined to be a signicant increase in Nesfatin–1
levels as a response to acute maximal intensity and short–term
exercise in normal body weight subjects [26]. The current study is
the rst to have determined the Nesfatin–1 level in sheep according
to the type of birth, and the study results demonstrated signicant
differences in the Nesfatin–1 level according to the type of birth. In
our study, based on the exercise and muscle activity in the above–
mentioned literature; muscle activity due to abdominal and uterine
contractions that occur during birth may cause an increase in the level
of Nesfatin–1 in the circulation. In addition to the change in Nesfatin–1
levels caused by exercise, it may also be because it causes energy
regulation in addition to the mechanical effects.
Experimental studies related to Nesfatin–1 have defined anti–
inflammatory, anti–apoptotic, and anti–oxidative properties of
Nesfatin–1 [27, 28, 29]. Ayada et al. [11] concluded that Nesfatin–1
could play a protective role against ischaemia and reperfusion [11]. It
has also been reported that by reducing apoptosis, inammation, and
oxidative stress, Nesfatin–1 has a cardioprotective effect in conditions
of myocardial damage [16]. Tang et al. [30] reported anti–oxidative and
anti–apoptotic effects of Nesfatin–1 in rats through neuroprotective
effects against subarachnoid bleeding which inhibits apoptosis and
causes brain damage. Özsavci et al. [31] and Kolgaziet et al. [32] stated
that the anti–oxidant effects of Nesfatin–1 could improve stomach
damage, and Jiang et al. [29] showed that the kidneys could be
protected against ischaemia reperfusion damage by reducing the
oxidative expression of Nesfatin–1. In a rat model study by Tamer et al.
[33] Nesfatin–1 was shown to have anti–oxidant, anti–inammatory, and
anti–apoptotic effects on testis dysfunction caused by testis torsion.
Nesfatin–1 was found to protect spermatogenic cells in the rat testes by
reducing proinammatory cytokine expression, suppressed apoptosis,
and degeneration of tubules, and by healing oxidative damage [34].
In our study, the highest level of Nesfatin–1 was determined in the
sheep group that had undergone caesarean section operation in which
the oxidative stress level was highest, and the lowest was in the normal
birth group with the lowest oxidative stress. The reason for this is
thought to be that the increase in Nesfatin–1 level is a defence system
of the body, and the anti–oxidative property of Nesfatin–1 decreases
oxidative stress rapidly and with the least tissue damage. The main
shortcoming of our study is that measurements were not taken at
certain time intervals after birth to clearly see this effect. The anti–
oxidant effect of Nesfatin–1 treatment is shown by the prevention of
over–production of intracellular reactive oxygen species (ROS), thereby
protecting the balance of the oxidant/antioxidant systems, lowering the
levels of lactate dehydrogenase and malondialdehyde, and increasing
levels of superoxide dismutase, catalase, and glutathione [29].
Fouad et al. [34] measured TAS levels in Egyptian buffalo (Bubalus
bubalis) according to the type of birth, and higher TAS levels were
determined in the animals with a normal birth compared to the group with
dystocia. In another study, the serum TAS levels of cows with dystocia
were found to be lower, although not at a statistically signicant level,
than those of cows with a normal birth [35]. Kızıl et al. [36] examined the
effects on oxidative stress parameters in cows according to the type of
birth, and determined differences between the normal, dystocia, and
TABLE I
Oxidative parameters and Nesfatin–1 levels in
Awassi sheep according to type of birth
Nesfatin–1 and OSI
status
N
Nesfatin–1 TAS TOS OSI
X
̄
± SEM X
̄
± SEM X
̄
± SEM X
̄
± SEM
Eutocia
(Group 1)
20 5.10 ± 0.10
a
2.00 ± 0.010
a
12.81 ± 0.57
a
6.36 ± 0.04
a
Dystocia
(Group 2)
20 7.20 ± 0.08
b
1.76 ± 0.009
b
16.01 ±0.86
b
9.03 ± 0.06
b
Cesarian Section
(Group 3)
20 10.06 ± 0.10
c
1.57 ± 0.007
c
19.01 ± 0.78
c
12.07 ± 0.08
c
P value
(repeated measures ANOVA)
P=0.000 *** P= 0.000 *** P=0.000 *** P= 0.000 ***
a,b,c
: Dierent letters in the same column indicate a statistically signicant dierence.
***:
P<0.001, ANOVA: Analysis of variance, X
̄
: mean, SEM: Standard error of the mean.
TAS: total antioxidant capacity, TOS: total oxidant capacity, OSI: oxidative stress index
TABLE II
Correlations between Nesfatin–1, TAS, TOS, and OSI
in Awassi sheep according to type of birth
Correlation analysis Nesfatin–1 TAS TOS OSI
Nesfatin–1 r 1
TAS r -0.932** 1
TOS r 0.957** -0.967** 1
OSI r 0.960** -0.981** 0.994** 1
**:
P<0.01, r: correlation coecient, TAS: total antioxidant capacity, TOS: total oxidant
capacity, OSI: oxidative stress index
Nesfatin-1 level according to type of birth / Akkuş and Yaprakci ____________________________________________________________________
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caesarean birth groups. The highest oxidative stress was determined in
the caesarean birth group but the differences were not at a statistically
signicant level. In a study by Akkuş et al. [37] to determine the TAS, TOS,
and OSI values in Aleppo goats according to the type of birth, higher TAS
levels and lower TOS and OSI values were determined in the normal birth
group compared to the dystocia group. In another human clinical study,
Noh et al. [38] reported that antioxidant capacity was higher in patients
who underwent a planned caesarean section delivery compared to those
with a normal vaginal route birth, and both mother and newborn were
exposed to greater oxidative stress during caesarean delivery. In the
current study, differences were seen in the TAS, TOS, and OSI values
according to the type of birth, consistent with the ndings in literature.
Higher TAS values and lower TOS and OSI values were determined
in the normal birth group compared to the dystocia group, and in the
dystocia group, higher TAS values and lower TOS and OSI values were
determined compared to the caesarean group. The reason for this was
thought to be that the contractions occurring in both the skeletal and
uterus muscles during labour increase ROS formation. As a result of the
increased ROS formation, oxidative damage of lipids, proteins, and DNA
has been reported [39]. It has also been shown that oxidative stress is
induced by long–term or shorter–term maximal aerobic exercise [40].
There may be signicant effects of aerobic exercise on oxidative stress
parameters, decreasing antioxidant parameters and increasing oxidant
parameters. All these data lead to the hypothesis that oxidative stress
may be present during normal and dicult births. Although some studies
have shown a great effect of the formation of free radicals in a caesarean
delivery, it is thought that the surgical intervention could contribute to
lipid peroxidation [41].
CONCLUSIONS
In conclusion, the results of this study demonstrated a signicant
difference in the level of Nesfatin–1 according to the type of birth.
Negative correlations were obtained between Nesfatin–1 and total
antioxidant capacity, and positive correlations were obtained between
Nesfatin–1 and total oxidant capacity. Therefore, Nesfatin–1 could be
a new biomarker in the determination of oxidative stress in sheep
according to the type of birth, and it was concluded that one of the
interventions that would decrease oxidative stress after dystocia
and caesarean births would be to provide an increase in endogenous
Nesfatin–1 because of its antioxidative property.
ACKNOWLEDGEMENTS
The authors thank the sheep owners for their kind co–operation
throughout the study.
Conict of interests
The authors have read and approved the article, and have no conict
of interests to declare.
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