https://doi.org/10.52973/rcfcv-e33260
Received: 14/04/2023 Accepted: 08/05/2023 Published: 15/05/2023
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ABSTRACT
The aim of this study was to investigate complete blood indices
[neutrophil-to-lymphocyte ratio (NLR), monocyte-to-lymphocyte
ratio (MLR), platelet-to-lymphocyte ratio (PLR) and mean platelet
volume/platelet count ratio (MPV/PLT)] and thiols (native and
thiol) in cats undergoing ovariohysterectomy (OHE). The study
sample comprised a total of 10 female cats of mixed breeds.
Ovariohysterectomy operation was performed under Ketamine/
Xylazine anesthesia with the appropriate technique. Blood samples
were collected from the cephalic vein pre-OHE and post-OHE at
2 h, 24 h, and 7 d. Total and native thiol levels in the serum were
analyzed using a colorimetric technique, and whole blood analysis
was carried out using anticoagulant tubes. White Blood Cell (WBC)
and neutrophil increased signicantly at 2 h post-OHE, peaked at
24 h post-OHE, then returned to baseline levels by 7 d (P<0.001). The
lymphocyte and thiols decreased at 2 h, 24 h, and 7 d post-OHE, and
the lowest lymphocyte count was observed at 24 h (P<0.001). The
lowest monocyte count was observed on d 7 post-OHE (P<0.001). NLR
increased signicantly 2 h after OHE, peaked at 24 h after OHE, and
remained high on d 7 (P<0.001). MLR increased at 2 h, peaked at 24
h, then returned to baseline levels on d 7 (P<0.001). PLR increased
gradually and peaked at 24 h and on d 7 (P<0.001). MPV/PLT after
OHE was statistically lowest on d 7 (P<0.05). A negative correlation
was determined between NLR, MLR, PLR, and thiols (P<0.001). In
conclusion, thiols and complete blood indices (NLR, MLR, and PLR)
may be important in the assessment of inammation and stress
responses after OHE in cats.
Key words: Monocyte-to-lymphocyte ratio; neutrophil-to-lymphocyte
ratio; platelet-to-lymphocyte ratio; ovariohysterectomy
RESUMEN
El objetivo de este estudio fue investigar los índices sanguíneos
completos [proporción de neutrólos a linfocitos (NLR), proporción
de monocitos a linfocitos (MLR), proporción de plaquetas a linfocitos
(PLR) y proporción media de volumen de plaquetas/recuento de
plaquetas (MPV/PLT)] y tioles (nativos y tiol) en gatas sometidas
a ovariohisterectomía (OHE). La muestra del estudio estuvo
compuesta por un total de 10 gatas de razas mixtas. La operación de
ovariohisterectomía se realizó bajo anestesia con ketamina/xilazina
con la técnica adecuada. Se recogieron muestras de sangre de la
vena cefálica antes de la OHE y después de la OHE a las 2 h, 24 h y 7d.
Los niveles de tiol total y nativo en el suero se analizaron mediante
una técnica colorimétrica, y el análisis de sangre total se realizó
utilizando tubos con anticoagulante. Los glóbulos blancos (WBC) y
los neutrólos aumentaron signicativamente a las 2 h posteriores
a la OHE, alcanzaron su punto máximo a las 24 h posteriores a la
OHE y luego regresaron a los niveles iniciales a los 7 d (P<0,001). Los
linfocitos y tioles disminuyeron a las 2 h, 24 h y 7 d después de la OHE,
y el recuento de linfocitos más bajo se observó a las 24 h (P<0,001).
El recuento de monocitos más bajo se observó el d 7 después de la
OHE (P<0,001). NLR aumentó signicativamente 2 h después de OHE,
alcanzó su punto máximo a las 24 h después de OHE y permaneció
alto el d 7 (P<0,001). MLR aumentó a las 2 h, alcanzó su punto máximo
a las 24 h y luego volvió a los niveles de referencia el d 7 (P<0,001).
PLR aumentó gradualmente y alcanzó su punto máximo a las 24 h
y el d 7 (P<0,001). MPV/PLT después de OHE fue estadísticamente
más bajo en el d 7 (P<0,05). Se determinó una correlación negativa
entre NLR, MLR, PLR y tioles (P<0,001). En conclusión, los tioles y los
índices de sangre completa (NLR, MLR y PLR) pueden ser importantes
en la evaluación de las respuestas de inamación y estrés después
de la OHE en las gatas.
Palabras clave: Proporción de monocitos a linfocitos; proporción
de neutrólos a linfocitos; proporción de plaquetas
a linfocitos; ovariohisterectomia
Investigation of changes in serum thiols and neutrophil-to-lymphocyte
ratio, monocyte-to-lymphocyte ratio, platelet-to-lymphocyte ratio, and
mean platelet volume/platelet count ratio indices in cats undergoing
ovariohysterectomy
Investigación de los cambios en los tioles séricos y la proporción de neutrólos a linfocitos, la
proporción de monocitos a linfocitos, la proporción de plaquetas a linfocitos y los índices promedio
de volumen de plaquetas/recuento de plaquetas en gatas sometidas a ovariohisterectomía
Tuğra Akkuş
1
* , Mehmet Eki̇ci̇
2
1
Harran University, Faculty of Veterinary Medicine, Department of Veterinary Obstetrics and Gynaecology. Sanliurfa, Turkey.
2
Sivas Cumhuriyet University, Faculty of Veterinary Medicine, Department of Veterinary Physiology. Sivas, Turkey.
*Corresponding author: tugraakkus08@hotmail.com
Serum thiols and complete blood indices in cats undergoing OHE / Akkuş and Ekİcİ _______________________________________________
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INTRODUCTION
Surgical sterilization (ovariohysterectomy, OHE) is the most widely
practiced and chosen procedure for controlling the pet population [1].
Ovariohysterectomy in small animal veterinary surgery includes the
removal of sex hormone-producing organs and the uterus, and the
most important reasons include preventing unwanted pregnancies,
reducing the risk of developing mammary tumors, pyometra, and
eliminating estrus and related problems [2]. Surgical stress results
from psychological stress, tissue damage and circulatory changes,
anesthetic agents, and complications before, during, and after surgery,
including sepsis. Surgery-related stress responses stimulate the
sympathoadrenal medullary and hypothalamic-pituitary-adrenal axis,
which results in post-traumatic endocrine and immunomodulatory
alterations [3, 4]. The stress response is a physiological response to
trauma or surgery and is generally considered to be proportional to
the degree of surgical trauma [5].
The evaluation of hematological characteristics is an important
tool that can be used as an effective and sensitive index to monitor
physiological and pathological changes in animals. Analysis of blood
indices has proven to be a valuable approach to analyze the health
status of animals and these indices provide reliable information
about health and stress status [6]. Hematological biomarkers such
as neutrophil, lymphocyte and neutrophil/lymphocyte percentage in
humans and animals are widely used for the evaluation of inammation
and stress response [7, 8].
Oxidative stress is a phenomenon caused by an imbalance between
the production and accumulation of reactive oxygen species (ROS),
and trauma from a surgical procedure can contribute to oxidative
stress [9]. Under increased oxidative stress, thiol levels decrease to
neutralize ROS, and in this condition, the sulfhydryl groups of thiols play
an important role [10]. During oxidative stress, reversible formation of
disulde bonds between protein thiols and low molecular weight thiols
is observed. These bonds can be reduced back to thiols to maintain
thiol/disulde homeostasis [11]. It is well known that the extracellular
space has a relatively more oxidized redox state than the interior of the
cell under physiological conditions. The extracellular supply of thiols is
critical for maintaining the redox state of the extracellular space [12].
Protein–SH groups are important circulating antioxidant defences
[13]. During surgery, the extracellular redox state may change, and
the sulfhydryl group of thiols may undergo oxidation reactions. From a
review of literature, no study could be found that has investigated the
effect of OHE on plasma thiol/disulde levels in domestic cats (Felis
catus). The aim of this study was to determine the ratio of serum thiol
levels and complete blood indices neutrophil/lymphocyte ratio (NLR),
monocyte/lymphocyte ratio (MLR), platelet/lymphocyte ratio (PLR)
and mean platelet volume/platelet count (MPV/PLT) in domestic cats
undergoing OHE and to reveal the correlation between them.
MATERIALS AND METHODS
This study was conducted with the permission of Harran University
Animal Experiments Local Ethics Committee (HRU-HADYEK) (decision
no: 2022/006, dated 07/09/2022).
Selection of animals
The cats comprising the study material were taken to Harran
University Veterinary Faculty Animal Hospital with a request for
sterilization by the owner. The study group was formed of a total of 10
domestic cats of various breeds, aged 1-3 years, each weighing 2.75-
3.34 (2.99 ± 0.19) kg, which had never given birth, were healthy with no
signs of disease, had routine care and feeding procedures, complete
vaccinations and parasitic practices, and were housed in similar
conditions. General clinical examinations of the cats were performed
and recorded. The study exclusion criteria were dened as aggression,
cardiac arrhythmia on auscultation, pregnancy, breastfeeding, obesity
(body condition score >7 on a scale of 1 to 9) [14], anemia (hematocrit
<30%), or any symptoms of clinical disease. Access to food and water
was restricted 8-12 h before the operation. Operations of 10 cats were
performed on different d. The average operation time was 15-20 min.
Anesthesia and ovariohysterectomy operation
All cats undergoing OHE were injected intramuscularly (IM) at a
dose of 1 mg·kg
-1
with Xylazine hydrochloride (Rompun 2%®, Bayer) for
sedation. Approximately 10 min later, Ketamine (Ketasol 10%®, Richter
Pharma) was administered IM at a dose of 15 mg·kg
-1
. Premedication
with atropine administration before anesthesia was not performed
due to early awakening and lack of complete induction. The OHE
operation was performed on all cats by the same experienced
veterinarian using the ventral midline approach technique with a 1cm
incision line [15]. No undesirable complications were encountered
in all of the cats during the operation. Vital parameters (respiration
rate, body temperature and pulse rate) were monitored in all the cats
before, during and after the operation (0, 2, 24 h and 7 d).
Collection of blood and plasma samples
A pediatric intravenous cannula (24G, yellow) was placed in the
cephalic vein in the sedated cats to collect the blood samples.
Catheter patency was provided with heparinized saline (20 UI·mL
-1
)
and the catheter was xed to the skin with an elastic bandage. The
blood samples from the cats were taken into vacuum tubes containing
Ethylenediaminetetraacetic acid (K
3
-EDTA), approximately 0.75-1
mL, pre-OHE and post-OHE at 2 h, 24 h, and 7 d. Lactated Ringer's
solution was administered equivalent to the amount of blood taken.
The catheter was removed after blood collection at the postoperative
24th h. First, hematological analyses of the blood samples were
performed with an automatic hemogram device (Mindray BC-30Vet,
Shenzen, China). Then, the blood in the vacuum tubes containing
K
3
-EDTA was centrifuged (NÜVE NF 200, Ankara, Turkey) at 3000
G for 10 min. The extracted plasma samples were stored at –20°C
(Ugur, UED 5175 DTK, Aydin, Turkey) for later analysis. Plasma total
thiol (Cat. No. MT2101N, Rel Assay, Gaziantep, Turkey) and native
thiol (Cat. No. MT2101T, Rel Assay, Gaziantep, Turkey) levels were
determined spectrophotometrically (Molecular Device SpectraMax
M5 Plate Reader, Pleasanton, CA, USA) using a commercial kit (FIG. 1).
Statistical analysis
Data analyses were performed using GraphPad Prism 8.00
software (GraphPad Software, San Diego, CA, USA). The normal
distribution of the data was conrmed with the Shapiro-Wilk test.
The repeated measures One-way ANOVA test followed by Tukey's
multiple comparisons test was used to evaluate differences in
analytes between different sampling time-points in all the cats that
underwent OHE. The results were expressed as mean ± standard
deviation (SD) values. Correlations of NLR, MLR, and PLR with Total
thiol and native thiol were examined using Spearman correlation
analysis. A value of P<0.05 was considered statistically signicant.
FIGURE 1. Study design
FIGURE 2. Heart rate, respiration, and temperature changes in cats undergoing OHE. *P<0.05, **P<0.01, and ***P<0.001 indicates signicance between
0 h and other time-points. #
P<0.05 and ###P <0.001 indicates signicance between 2 h and other time-points (24 h)
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RESULTS AND DISCUSSION
Heart rate, respiration, and temperature were signicantly reduced
at 2 h following OHE in all the cats (P<0.05). At 24 h and 7 d after OHE,
these physiological parameters reached their normal values and
were statistically signicantly higher than at 2 h (P<0.05) (FIG. 2). No
statistically signicant difference was determined before and after
OHE in the RBC, Hb, Hct, MCV, MCHC, PLT, and MPV values (P>0.05)
(FIG. 3). The WBC and neutrophil counts increased signicantly
at 2 h and peaked at 24 h after OHE (P<0.001), with no signicant
difference seen between 0 hr and 7 d (P>0.05). The lymphocyte count
decreased signicantly at 2 h, 24 h, and 7 d after OHE, and the lowest
lymphocyte value was observed at 24 h (P<0.001). Statistically, the
lowest monocyte count was observed on d 7 after OHE (P<0.001).
The eosinophil count gradually increased after OHE and the highest
eosinophil level was observed on d 7 (FIG. 4).
FIGURE 3. RBC, Hb, Hct, MCV, MCHC, PLT, and MPV concentration changes in cats undergoing OHE
FIGURE 4. WBC, neutrophil, lymphocyte, monocyte, eosinophil concentration changes in cats undergoing OHE. **
P<0.01 and ***P<0.001 indicates
signicance between 0 hr and other time-points. #
P<0.05, ##P<0.01 and ###P<0.001 indicates signicance between 2 h and other time-points (24 h).
ααα
P<0.001 indicates signicance between 24 h and 7 d
Serum thiols and complete blood indices in cats undergoing OHE / Akkuş and Ekİcİ _______________________________________________
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FIGURE 5. The hematological indices (NLR, MLR, PLR, and MPV/PLT) changes in cats undergoing OHE. *P<0.05, **P<0.01 and ***P<0.001 indicates
signicance between 0 hr and other time-points. ###
P<0.001 indicates signicance between 2 h and other time-points (24 h). ααP<0.01 and
ααα
P<0.001 indicates signicance between 24 h and 7 d
FIGURE 6. The serum total and native thiol concentration changes in cats undergoing OHE. ***P<0.001 indicates signicance between 0 hr and other
time-points. ###
P<0.001 indicates signicance between 2 h and other time-points (24 h and 7 d). ααα P<0.001 indicates signicance between 24 h and 7 d
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The hematological indices (NLR, MLR, PLR, and MPV/PLT) are shown
in FIG. 4. NLR increased signicantly at 2hrs, peaked at 24 h after
OHE (P<0.001) and remained signicantly higher on d 7 after OHE
(P<0.001). After OHE, MLR increased signicantly at 2 h, peaked at 24
h (P<0.001) and returned to the pre-OHE value on the 7th d (P>0.05).
The PLR increased signicantly at each time-point (P<0.01), showing
a signicant peak at 24 h and 7 d after OHE (P<0.001). The MPV/PLT
value after OHE was statistically lowest on the 7th d (P<0.05) (FIG. 5).
Total and native thiol counts were signicantly reduced at 2 h, 24
h, and 7 d after OHE (P<0.001). The lowest serum total and native thiol
levels were determined at 24 h after OHE (P<0.001) (FIG. 6).
The correlations between the hematological indices (NLR, MLR,
PLR, and MPV/PLT) and thiols (total and native thiol) are shown in
FIG.7. A very strong positive correlation was determined between
native and total thiol (r=0.978, P<0.001). A very strong negative
correlation was determined between NLR and total (r=-0.913, P<0.001)
and native (r=-0.915, P<0.001) thiol. A strong negative correlation
was determined between MLR and total (r=-0.719, P<0.001) and
native (r=-0.737, P<0.001) thiol. A moderate negative correlation
was determined between PLR and total (r=-0.639, P<0.001) and native
(r=-0.671, P<0.001) thiol. No correlation was determined between
MPV/PLT and total and native thiol (P>0.05).
To the best of the knowledge, this is the first study to have
thoroughly investigated the responses of thiols (total and native)
and hematological indices (NLR, MLR, PLR, and MPV/PLT) in cats
undergoing OHE. After OHE, The measurement of thiols is a novel
method that could help to quantify oxidative stress in post-surgical
patients, the leukogram in the hemogram was the most affected
hematological parameter, but no change was observed in the
FIGURE 7. The correlation between hematological indices (NLR, MLR, PLR, and MPV/PLT) and thiols (native and total) in cats undergoing OHE
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erythrogram. While NLR, MLR, and PLR were the most affected in
hematological indices, negligible changes were seen in MPV/PLT.
After OHE, total and native thiol plasma concentrations decreased
dramatically in the rst 24 h, and showed lower levels than before
OHE even at one week after OHE.
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The results of this study showed that the vital parameters of heart
rate, respiration, and temperature were depressed at 2 h post-OHE
and then returned to normal after the recovery phase. In the study,
anesthesia was provided with Ketamine, a centrally effective
N-methyl-D-aspartate (NMDA) antagonist, and xylazine, an alpha 2
adrenergic receptor agonist. The suppression of all vital parameters
at 2 h post-OHE shows that the depth of pharmacological action of
the anesthetics continued. With the return of vital values to normal
levels in the following h the effect of the anesthetics was seen to
have disappeared. Numerous studies that have used various surgical
procedures and anesthesia regimens to assess the alterations in
hematochemical parameters in OHE bitches have reported varying
results [16]. Intraoperative blood loss of less than 15% of blood
volume is not anticipated to result in clinical symptoms in non-anemic
human patients, although the loss of less than 30% of intraoperative
blood volume has been proposed as a red cell transfusion trigger in
otherwise healthy people [17].
Dogs (Canis lupus familiaris) and cats have been reported to be
more likely to develop hospital-acquired anemia when cumulative
phlebotomy volumes exceed 3% of their total blood volume and when
undergoing surgery [18]. No difference in RBC, Hb, Hct, MCV, MCHC,
PLT and MPV values was determined in the current study, which was
consistent with the ndings of a previous study of OHE in cats [19].
This can be attributed to the fact that the OHE surgery performed
was minimally invasive with minimal bleeding.
OHE is an intrusive operation with postoperative pain ranging from
mild to severe [5, 20]. Surgical trauma induces a stress reaction
and increases muscle activity because of injury to superficial
nerve terminals, which stimulates the corticotropic releasing
hormone (CRH). Following hypothalamic activation, CRH promotes
adrenocorticotropin hormone (ACTH) and causes the adrenal
gland to produce cortisol [21]. As a result of tissue damage, organ
manipulation, and inammation, OHE is well known to produce pain
and stress. In a previous study, 2 h after OHE, dogs had considerably
greater peak plasma cortisol levels [22]. Neutrophils migrate from
the neutrophil pool to the circulating neutrophil pool in response to
cortisol, although this can also be augmented by neutrophil release
from the bone marrow storage pool and decreased migration of
neutrophils to tissues [23]. It has been reported that neutrophilia
and lymphocytopenia are seen in dogs undergoing OHE [24]. Another
study of dogs showed that OHE led to stress leukogram such as
leukocytosis, neutrophilia, lymphocytopenia, and eosinopenia [25].
However, in a recent study of cats, neutrophilia and lymphocytopenia
were observed on the 2nd d after OHE, and eosinophilia on the 10thd
[19]. In the current study, leukocytosis with neutrophilia started to
appear at 2 h after OHE and peaked at 24 h, but then returned to
the baseline level. However, lymphocytopenia, monocytopenia, and
interestingly eosinophilia was noted in the cats after OHE in the
current study. This may have been due to circulating stress hormones
originating from OHE.
NLR, PLR, MLR, and MPV/PLT are biomarkers of systemic
inammatory response, which are potentially diagnostic [26, 27].
There is a growing amount of evidence indicating the potential utility
of these indexes in veterinary care. Previous research in veterinary
medicine has associated increased NLR with canine sepsis [26], dogs
with chronic enteropathy [28], feline hypertrophic cardiomyopathy
[29], and tumor size in cats [30]. Recently, ndings have been reported
proving that NLR can be an effective stress and inammation marker
in cats undergoing OHE [19]. In the current study, NLR increased in
the rst two h following OHE, peaked in the next 24 h, and then started
to decline on the 7
th
d to the pre-OHE level.
Previous studies support that this may be related to OHE-induced
stress and inammatory status. Related to systemic inammatory
reactive diseases and PLT function and activity, the rise in PLR has
been reported to be caused by an increase in platelet count and a
reduction in lymphocyte count in peripheral blood [31]. Increased
thrombopoietin and cytokine levels during inammation result in
increased megakaryocytes, which stimulate PLT production and
decrease their size [32]. PLT are important in initial hemostasis
because they adhere to the damaged vascular bed induced by
subendothelial collagen exposure [33]. MPV/PLT and PLR indices
have been previously shown to be ineffective as systemic biomarkers
for disease activity in dogs, such as periodontitis and oropharyngeal
cancers [27]. In a previous study, increases in the mean PLT values
were observed in cats after OHE [34], whereas another cat study
showed that PLT, MPV and PLR were not significantly changed
post-OHE [19]. PLR increased following OHE in the current study,
and the MPV/PLT ratio decreased on the 7
th
d post-OHE. In general,
stress-induced hypercortisolemia, followed by platelet release into
blood cells and transient lymphopenia, inuences the degree of PLR
elevation in a variety of proinammatory and prothrombotic states
[31]. MLR is a simple biomarker of the host immune system. Research
has linked a high monocyte count to immune gene upregulation
and the generation of monocyte/macrophage-related cytokines
[35]. Although a previous study showed that monocyte levels did
not change, lymphocytes decreased after OHE in cats [19]. Another
study of domestic dogs in Nigeria reported a decrease in monocyte
levels 2 h after OHE, returning to pre-OHE levels, while decreased
lymphocyte levels were reported [3]. MLR and NLR formed similar
curves in the current study, increasing at 2 h post-OHE, peaking at
24 h, and then reverting to normal on the 7
th
d. OHE-induced stress
and inammation may have contributed to this response.
Native thiols (–SH) and total thiols (–SH+ –SS) are critical for the
detoxication of extracellular and intracellular reactive nitrogen and
oxygen species, which is a crucial component of cellular antioxidant
defences. Importantly, this oversees preservation of the redox state
of protein thiols necessary for deoxyribonucleic acid (DNA) synthesis
and repair [13]. Protein structural and functional alterations are
commonly caused by the loss of thiol groups, which is the principal
molecular process. It has been reported that surgery and trauma
decrease protein synthesis and increase protein catabolism and
oxidation, and these changes are related to the level and duration
of trauma [36]. In a previous study, total thiol was reported to be
a therapeutically relevant indicator of oxidative stress in cats with
pyometra that had undergone elective OHE [37]. In the current study,
it was hypothesized that the body's efforts to detoxify oxidative stress
and the oxygen free radicals generated by surgical trauma would be
the main cause of the greatly reduced thiol levels post-OHE. The
study results showed that natural and total thiol have a very high
negative correlation with NLR, a strong negative correlation with
MLR, and a moderate negative correlation with PLR. However, MPV/
PLT and native and total thiol did not correlate. Although there are
many human studies in the literature to explain the relationship
between thiols and NLR, PLR, and MLR, animal research is limited.
A negative correlation has been previously reported between NLR
and native and total thiol after gunshot injury in humans [38]. Total
thiol and native thiol levels have also been shown to be positively
correlated with lymphocyte levels and negatively correlated with NLR
Serum thiols and complete blood indices in cats undergoing OHE / Akkuş and Ekİcİ _______________________________________________
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and PLR in COVID-19 patients [39]. In a clinical study of patients who
presented at the Emergency Department with ischemic stroke, NLR
values were found to be signicantly higher, and total and native thiols
were signicantly lower [38]. Thiol homeostasis could potentially be
benecial in the inammatory response and negatively correlated
with the degree of inammation.
CONCLUSIONS
The results of this study demonstrated that the whole blood
indices of NLR, MLR, and PLR increased and thiols (native and total)
decreased in cats after OHE, which was related to the inammatory
and stress response. This information indicates that changes in serum
concentrations of thiols as well as NLR, MLR, and PLR are important
in the assessment of inammation and stress response after OHE.
Conict of interests
The authors have read and approved the article, and have no conict
of interests to declare.
ACKNOWLEDGEMENTS
The authors thank the cat owners for their kind co-operation
throughout the study.
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