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This
study was aimed to determine hemato-biochemical changes, the oxidants
biomarkers including malondialdehyde (MDA), nitric oxide (NO) and to evaluate
the total antioxidant capacity (TAC) and Glutathione peroxidase (GPX) as
antioxidants in pneumonic sheep. This study was conducted on a total of adult
twenty sheep including sheep suffered from pneumonia (n=10) and healthy sheep
were confirmed by physical examination (n=10). Blood and tissue samples were
collected from the diseased and healthy sheep during field study, for
hematological, biochemical analysis and determine the oxidant/antioxidant in
blood and tissues. The results showed statistically significant increased MDA
and NO and reduced TAC and GPX in pneumonic sheep than healthy ones
(P<0.01). Red blood cells (RBCS), total
leukocytic counts (TLC), Alanine Aminotransferase (ALT) and Aspartate
Aminotransferase (AST) were significantly increased in diseased group compared to control ones
(P<0.05). Young age pneumonic sheep<2 years old were more likely to have
elevated MDA and decreased TAC than old ones (P<0.05). It was concluded that
reduced concentrations of TAC and GPX and elevated MDA and NO could suggest
sever oxidative stress in pneumonic sheep. Moreover, oxidative stress was more
associated with young age pneumonic sheep.
Keywords: Sheep, Malondialdehyde, Nitric
oxide, Total antioxidant capacity, Glutathione peroxidase, Pneumonia
INTRODUCTION
Sheep
are small ruminants that have specific properties rather than other livestock
resources. They are more acclimatized to various ranges
of environment, have short generation cycles and
reproductive rate which lead to high production efficiency and impoverished
people can buy them with less cost [1].
Pneumonia is multifactorial disease which
always involves a combination of infectious causes as well as predisposing
environmental and managerial factors [2]. Pneumonia is a respiratory disease
resulted from an inflammatory response of the bronchioles and alveoli in the
lungs to any causative agents; this is lead to consolidation of the lung
tissue. It is a common disease of sheep in all sheep-producing countries [3,4].
Oxidative
stress is an imbalance between free radical production and radical-removal
mechanism resulting from increased production of pro-oxidants and/or a decrease
in antioxidant status in the body [5]. Free radicals, which include reactive oxygen
species (ROS) and reactive nitrogen species (RNS), are reactive chemical
products that may result in oxidative damage by affecting macromolecules like
lipids, carbohydrates, proteins and nucleic acids [6]. Antioxidant is the first
defense mechanism against free radicals and has a major role in prevention the
hazard effects of oxidants in organs as lung, kidney [7].
Lipid peroxidation is a major factor involved
in cellular damage and is used as oxidative stress marker in body fluids, cells and tissues.
Lipid peroxides are not stable compound and when rapidly dissociated to form
reactive carbonyl compounds. Polyunsaturated fatty acid peroxides generate
malondialdehyde during the decomposition
[8].
Nitric oxide is generated
by different cells in the lung and plays
a crucial physiological
role in regulating pulmonary
The
antioxidants consider the first defensive line in the body against free
radicals includes some antioxidant enzymes such as superoxide dismutase (SOD),
catalase (CAT), glutathione peroxidase (GPX), glutathione reductase (GR)
[14,15]. Antioxidants have a vital role in
preventing or repairing the damage caused by reactive oxygen species (ROS), in
addition to regulation of redox-sensitive signaling pathways [16]. The neutralization process of
hydrogen peroxide and organic peroxides is usually obtained by glutathione
peroxidase activity [17].
The
cumulative action of all the antioxidants can be indicated by measurement of
TAC level in plasma and body fluids, thus providing an integrated parameter
rather than the single sum of measurable antioxidants [18].
The aim of the present study were to focus on
the possible effect of pneumonia on oxidants and antioxidants markers in
addition to alteration in hematological and biochemical dynamics in
hospitalized pneumonic sheep.
MATERIAL AND METHODS
Animal’s criteria
A completely
randomized field study was carried out on a total of 20 adult female sheep aged
between 1-3 years old were collected in different seasons throughout the year
and were divided into two main groups according to their body condition score
(BCS), their general inspection and physical examination. Group 1:
Included 10 apparently healthy sheep showed no clinical signs of diseases and
free from external and internal parasites. The body condition score (BCS) of
this group was ≥ 3 and act as a control group [19,20]. Group 2: Included
10 diseased sheep admitted to veterinary clinics at different area at Menofya
Governorate suffered from general debility, poor health conditions included
signs of anemia, emaciation, dehydration, cough, in appetence, nasal discharge and harsh
vesicular sound and confirmed by physical examination and their BCS was <3
[19,20]. Furthermore,
hospitalized pneumonic sheep was categorized based on their age into pneumonic
sheep >2 years (n=12) and <2 years (n=8).
Clinical information
The clinical history of sheep was obtained
from their owners. Physical examination, serum biochemistry and hemogram were
determined for all sheep. Body condition scoring in sheep is determined by
estimation of muscle and amount of fat cover the lumbar processes scaled on a
scoring system of ‘0’ to ‘5’, The BCS of an animal is evaluated by the
palpation of the lumbar region, specifically on and around the backbone
(spinous and transverse processes) in the loin area, immediately behind the
last rib and above the kidneys to detect the degree of sharpness or roundness
[19,20].
Samplings
Blood samples: Two blood
samples were collected from jugular vein of each sheep using sterile syringe
.The first one was collected in dry clean labeled test tube contain
anticoagulant,
Ethylene diamine tetra acetic acid (EDTA) for complete blood count (CBC) and The
second sample collected in dry clean centrifuge tube and kept in sloping
position without agitation till coagulation. The clotted samples centrifuged at
3000 rpm for 10 min for separation a clear non-hemolysed serum for biochemical
analysis. Sera were kept in deep freezer at -20°C till biochemical analysis.
Tissue samples: Lung
tissue samples were collected before dissection, the tissue samples were perfused with a phosphate
buffered saline solution with pH 7.4 containing 0.16 mg/ml heparin to remove
any red blood cells then the tissues were homogenized in 5-10 ml cold buffer
(i.e., 100 mM potassium phosphate, pH 7.0, containing 2 mM EDTA) per gram
tissue and centrifuged at 4,000 rpm for 15 min at 4°C till obtaining the
supernatant. These are for determination of glutathione peroxidase activity and
nitric oxide.
Hematological
and biochemical measurements
Hematological
examinations included Complete Blood Count (CBC), Red Blood Cells Count (RBCs),
Packed Cell Volume (PCV), Hemoglobin (Hb), Mean Corpuscle Volume (MCV), Mean
Corpuscle Hemoglobin (MCH), Mean Corpuscle Hemoglobin Concentration (MCHC),
Total Leukocytic Count (TLC) and differential Leucocytic Count (DLC)were
carried out on apparently healthy and diseased sheep according to methods
described by Meyer et al. [21].
Total protein,
albumin, ALT and AST were measured in serum by UV-colorimetric
spectrophotometric method using special kits according to Doumas [22] and Reitman and Frankel [23], respectively. Globulin was calculated by subtraction of albumin
value from total protein value and then A/G ratio was calculated by dividing
albumin on globulin concentrations [24].
Determination of oxidants
and antioxidants status
MDA in serum samples was measured by using a
special kit in which MDA reacts directly with thiobarbituric acid at optimum pH
(3.5) to produce a red color that was measured spectrophotometrically [25]. NO
in tissue samples was measured by using a special kit [26]. Total antioxidant
capacity was determined according to the method of using a special kit in which
a Fe-EDTA complex reacts with hydrogen peroxide by a Fenton-type reaction,
leading to the formation of hydroxyl radicals that degrade benzoate, followed
by release of thiobarbituric acid reactive substances [27]. GSH activity was
evaluated by using special kit at which Glutathione peroxidase catalysis the
oxidation of glutathione by cumene hydroperoxide. In the presence of
glutathione reductase and NADPH, the oxidized glutathione is immediately
converted to the reduced form with a concomitant oxidation of NADPH to NADP+.
The decrease in absorbance at 340 nm was measured [28].
STATISTICAL
ANALYSIS
Data from healthy and diseased sheep were
compared by means of independent t test by using the statistical package for
social science (SPSS) for windows (Version 16.0; SPSS Inc., Chicago, Ill.).
Results were expressed as the mean ± standard error (SEM), Significance was set
at P<0.05. Univariate analysis was done based on age of hospitalized sheep
with reference to 5-95% confidence interval from healthy sheep. Receiver
operating curve (ROC) was determined using GraphPad Prism 8.
RESULTS AND DISCUSSION
The mean value of RBCs, PCV and TLC were
significantly increased in diseased pneumonic sheep than healthy ones
(P<0.05; Table 1). We have also
shown that serum total protein and albumin concentrations were significantly
increased in pneumonic sheep rather than healthy group as demonstrated in Table 1 (P<0.05). Our findings were
agreed with the results that obtained by Maina et al. [29]
and this due to that
diseased sheep could be exposed to dehydration that accompanied by loss of
fluid [29]. TLC was significantly increased in pneumonic sheep which is similar
to a previous study that reported by Maina et al. [29]
and Chirkena et al.
[30] as in acute inflammatory diseases TLC increased especially those
due to bacterial infections. This could be explained tissue injury due to acute
inflammation during bacterial infections stimulate various types of cells to
produce growth factors, cytokines, and other mediators of inflammation that in
turn increase TLC and more production, proliferation, maturation and bone
marrow release of mature and immature neutrophils [31] Additional explanation
for this neutrophilic leukocytosis stress factors to which the animal exposed
during the course of the respiratory diseases that lead to endogenous
production and increase of corticosteroids which play a vital role in
regulation of circulating concentration of leukocytes in moderate and severe
pneumonia [32].
ALT and
AST were increased in
diseased pneumonic sheep rather than control one (P<0.01; Table 1). Similar to findings observed
by El-Deeb
et al. [33] and Donia et al. [34]. This might be due to the changes
in the antioxidant abilities that occurred in liver and in the phospholipid
structure of the cell membrane which lead to high levels of ALT and AST as
markers of liver damage according to Deger et al. [35]. Of interest, serum globulins concentrations were
increased in pneumonic sheep compared to healthy ones. Globulins are serum
protein produced by liver and categorized into α-, β- and γ-globulins in
ruminants which are produced and increased in response to acute inflammation
which is the case of pneumonic sheep of this study suggesting sever oxidative
stress on the liver [36].
The present study showed a significant
increase in the levels of MDA pneumonic sheep when compared to its levels in
the healthy ones (P<0.01; Table 2).
TAC concentrations were inversely correlated with MDA concentrations in
pneumonic sheep (rs=-0.6; P<0.01; Figure
1). Moreover, MDA and NO were associated with severity of disease in
pneumonic sheep (ROC=0.95; P<0.05; Figure
2). Additionally, young age pneumonic sheep <2 years old were more
likely to have increased oxidant MDA (OR= 1.97; 95% CI= 1.02-15.6; P=0.04; Table 3) than old one >2 years old.
The increase in MDA level could be explained by the risk effect of cellular
damage and inflammation which are associated with bronchopneumonia and
broncho-interstitial pneumonia in addition to destruction of epithelial cells
and fibrinous reaction resulted from vascular damage. This clearly clarified
that the measurement of MDA level, is closely linked to the inflammatory
reactions and mechanisms of cellular response [37]. MDA is the best marker of
oxidative stress [38], its level increases during any stressful condition.
The significant increase in NO level in
diseased pneumonic sheep was also found by Yuksek et al. [39]. In case of respiratory diseases, NO played
an important role in the immune system and its consumption is in surge with the
severity of infection in a parallel way [40-47]. Alveolar macrophages are
proven to have major roles for immunity in the lower respiratory tracts and NO
produced by alveolar macrophages has significant roles in respiratory system
infections [48]. Moreover, previous studies clarified that the imbalance between oxidative
compounds and local antioxidant system caused inflammation in the lungs,
increased alveolar capillary leakage and reduce the functions of surfactant
[49-52].
There was a significant decrease in the
concentration of TAC and GPX in diseased pneumonic sheep than healthy ones (P<0.01;
Table 2). Furthermore, we have
documented that young age pneumonic sheep <2 years old were more likely to
have decreased TAC (OR=2.04; 95% CI=1.16-20.4; P=0.02; Table 3). GPX was significant diminished in
lung tissue of hospitalized sheep than healthy ones as recorded by Donia et al.
[34], Jarikre et al
[37] and Nisbet et al. [53]. Significant reductions were observed in
broncho-interstitial pneumonia and bronchopneumonia [37].
Phagocytic cells and
neutrophils are protected by (GSH-Px), from oxidative damage caused by free
radicals, its decreased level shows that the host’s defense system is affected
by oxidative stress and that there is a severe damage of cells of the immune
system [54-57].
CONCLUSION
Reduced
TAC and GPX together with increased MDA and NO concentrations in hospitalized
pneumonic sheep could indicate sever oxidative stress. Elevated MDA and reduced
TAC in young age hospitalized pneumonic sheep suggest more likely oxidative
stress rather than old ones. Pneumonic sheep were associated with alterations
in hemato-biochemical dynamics during course of disease. Addition of
antioxidants therapeutic strategy to routine pneumonia therapy might add value
for enhancing recovery of pneumonic sheep [58-61].
ACKNOWLEDGMENT
Our grateful thanks to all veterinarians and
technicians at The Faculty of Veterinary Medicine, University of Sadat City for
supporting this study.
CONFLICT
OF INTERESTS
No conflict of interests was declared.
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