https://doi.org/10.52973/rcfcv-e34318
Received: 08/09/2023 Accepted: 04/11/2023 Published: 13/01/2024
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Revista Científica, FCV-LUZ / Vol. XXXIV, rcfcv-e34318
ABSTRACT
Gonadectomy is a widely used method in reproductive health
management, and behavior disorder therapies of domestic animals.
Anemia and its development, one of the complications of surgical
castration, which has been done so much recently in shelter dogs and
dogs kept at home, has been investigated in male Kangal shepherd
dogs. In castrated male Kangal shepherd dogs was to investigate
the relationship between gonadectomy and oxidant and antioxidant
levels, Iron (Fe) concentrations, unsaturated iron binding capacity
(UIBC) and some blood parameters (RBC, HGB, HCT, MCV, RDW, MCHC).
Blood samples were taken from 20 adult Kangal dogs brought to
a clinic before castration (Day 0) and on the 1st, 3rd and 7th days.
Some biochemical analyzes and blood parameters were evaluated
in the blood samples taken. For this purpose, serum total oxidant–
antioxidant capacity (TAC–TOC), Iron (Fe) concentrations, unsaturated
iron binding capacity (UIBC) and some blood parameters (RBC, HGB,
HCT, MCV, RDW, MCHC) were examined. In this study, it was evaluated
the relationship between gonadectomy and oxidant–antioxidant
capacity and Fe metabolism at some serum parameters in male dogs.
After the orchidectomy operation, a remarkable decrease in clinical
and statistical blood parameters was observed. As a result of this
study, in the analysis of blood parameters, a severe picture of anemia
was observed. It was determined an important role in erythropoiesis,
with orchidectomy. The statistical difference in blood parameters
(P<0.05) was indicative of this.
Key words: Antioxidant; Kangal shepherd dog; iron; oxidative
stress; hematology
RESUMEN
La gonadectomía es un método ampliamente utilizado en el
manejo de la salud reproductiva y en las terapias de trastornos
del comportamiento de los animales domésticos. La anemia y su
desarrollo corporal, son una de las complicaciones de la castración
quirúrgica, que tanto se ha hecho recientemente en perros de refugio
y en perros mantenidos en casa, se ha investigado en perros pastores
Kangal machos. En perros pastores Kangal machos castrados se
investigó la relación entre la gonadectomía y los niveles de oxidantes
y antioxidantes, las concentraciones de hierro (Fe), la capacidad de
unión al hierro insaturado (UIBC) y algunos parámetros sanguíneos
(RBC, HGB, HCT, MCV, RDW, MCHC). Se tomaron muestras de sangre
de 20 perros Kangal adultos traídos a una clínica antes de la castración
(día 0) y en los días 1, 3 y 7. En las muestras de sangre tomadas se
evaluaron algunos análisis bioquímicos y parámetros sanguíneos. Para
ello, se examinaron la capacidad oxidante–antioxidante total en suero
(TAC–TOC), las concentraciones de hierro (Fe), la capacidad de unión al
hierro insaturado (UIBC) y algunos parámetros sanguíneos (RBC, HGB,
HCT, MCV, RDW, MCHC). En este estudio, se evaluó la relación entre la
gonadectomía y la capacidad oxidante–antioxidante y el metabolismo
del Fe en algunos parámetros séricos en perros machos. Tras la
operación de orquidectomía se observó una notable disminución de
los parámetros sanguíneos clínicos y estadísticos. Como resultado
de este estudio, en el análisis de parámetros sanguíneos se observó
un cuadro severo de anemia. Se determinó un papel importante en
la eritropoyesis, con orquidectomía. La diferencia estadística en los
parámetros sanguíneos (P<0,05) fue indicativa de esto.
Palabras clave: Antioxidante; perro pastor Kangal; hierro; estrés
oxidative; hematología
Evaluation of hematological parameters, oxidative stress, Iron and
unsaturated Iron binding capacity levels in Kangal shepherd dogs, before
and after orchiectomy
Evaluación de parámetros hematológicos, estrés oxidativo, niveles de capacidad de unión de
hierro y hierro insaturado en perros pastores Kangal, antes y después de la orquiectomía
Ibrahım Yurdakul
1
, Barıs Atalay Uslu
2
*
1
Sivas Cumhuriyet University, Faculty of Veterinary Medicine, Department of Surgery. Sivas, Türkiye.
2
Sivas Cumhuriyet University, Faculty of Veterinary Medicine, Department of Reproduction and Articial Insemination. Sivas, Türkiye.
*Corresponding Author: atalayuslu@hotmail.com
Effect of castration over hematological parameters in shepherd dogs / Yurdakul and Uslu _________________________________________
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INTRODUCTION
Gonadectomy is a widely used method in reproductive health
management, and behavior disorder therapies of domestic animals.
It is referred to as castration in male mammalians that is the ending
of most functions of external and internal reproductive organs by
either extirpation or removing of testes from the body, or the closing
of the canal system. Some of its positive effects can be count such
as being more resistant to cancer and the immune system diseases
compared to non–sterilized dogs [1]. However, negative major effects
(obesity, infection, trauma, vascular diseases, and anemia) that are
linked to castration should not be missed [2]. Anemia and decrease of
hemoglobin levels have been shown by numerous studies as triggering
effects for the majority of these negative effects [3].
Anemia is when the erythrocytes that carry the oxygen needed
by the body are less than normal or the oxygen carrying capacity
of the erythrocytes is low [4]. The low erythrocyte production in
the organism is under the inuence of many factors. One of them,
Testosterone has a stimulating role in erythrocyte production [5].
It has been reported that a decrease in Testosterone production
associated with bilateral orchidectomy may result in normocytic
anemia in men [6]. Post–orchiectomy anemia is thought to be related
to the hypothesis of this study and to the hypo–androgenic state.
Another key player in erythrocyte production, Fe is an essential
element because of its necessity for the normal function of
erythrocyte production, oxidative metabolism, and immune system
[7]. Its deciency affects erythrocyte status as a prominent effect by
increasing oxidative stress [8]. As a result of this, increased oxidative
stress causes lipid peroxidation in the cell membrane of erythrocytes
and anemia occurs with broken erythrocytes imperiously [9]. On the
parallel perspective, there is a close relationship between Fe and
Testosterone. The Testosterone works with a negative feedback
mechanism that mediates the production of erythrocytes. It
enhances not only Fe absorption but also inhibits the production of
Testosterone to protect Fe homeostasis when excessive amounts of
iron are involved in the body [10]. There is a great balance between
Testosterone, OS and Fe parameters in male dogs. An imbalance in
any of these parameters is thought to occur as a result of sterilization.
The aim of this study was to investigate the relationship between
blood parameters and Fe, UIBC, TAC and TOC in some male dogs
after castration.
MATERIAL AND METHODS
Animal material
A total of 20 male dogs of same species and weights (20–30 kg,
PNR, İstanbul, Turkey) were used in the study. Dogs were at the age
of 2–5 years and brought to the clinics of Sivas Cumhuriyet University
Veterinary Faculty Animal Hospital, Sivas, Turkey, by their owners.
Dogs (Canis lupus familiaris) that undergoing castration operation
were kept in the clinic for 7 days for post–operative care with the
permission of the animal owners. During the study, daily care was
performed according to the asepsis rules of the operation area to
avoid postoperative infection formation. At the end of the day 7, the
animals were delivered to the animal owners in good health.
The permission of the Sivas Cumhuriyet University Animal
Experiments Local Ethics Committee was taken for this study design
(Permission date and number: April 9, 2018, and 155).
Operation
Dogs had been fasted and not allowed to access water pre–
operation overnight. Afterward, they were sedated with Xylazine HCl
(1.0 mg·kg
-1
, Alfazyne 2%, Ege Vet, Turkey) and Ketamine (1.0 mg·kg
-1
,
Alfamine, Ege Vet, Turkey) intramuscularly. Dogs were placed on a
surgical table in lateral recumbency, xed, and surgical sites were
shaved. Lidocaine HCl (6.0 mg·kg
-1
, Jetokain, Adeka, Turkey) was
administered to the testicles and incision site.
Operations were performed with an open castration method
by using a scrotal incision. In the scrotal approach to castration,
the scrotum was covered with a sterile fenestrated drape so that
the testicles were visible. A single thick incision was made on the
ventral surface of the testicle through the skin and subcutaneous
tissue, just lateral to the median raphe, approximately one–third of
the length of the testicle. After tying knots 4 times with absorbable
2/0 suture material to create complete hemostasis around both the
ductus deferens and the vascular cord, the cord was cut. The same
procedure was applied to the remaining testicle. After the testicles
were removed, the scrotum was closed with a non–absorbable 3/0
synthetic monolament suture so that it did not close completely.
After surgery, the area was cleaned and an e–collar was applied to
prevent the dog from licking or tackling the wound. Postoperative
analgesia was provided with 0.3 mg·kg
-1
Meloxicam (Anaflex®,
Hektaş, Turkey) administered SC for 3 days. Additionally, all dogs
were administered Procaine Penicillin G (20,000 IU·kg
-1
IM) for 7 days
after surgery.
Collection of blood samples
Blood samples were collected from all the dogs ve times during the
experiment. Blood samples were taken on the day 0 (as control), 1st,
3rd and 7th days before surgery. Blood samples were taken into 5mL
sterile tubes without anticoagulants from the dogs' Vena cephalica
antebrachii. Samples were kept at room temperature for 30 min,
then centrifuged (Nüve NF 800, Nüve Laboratory & Sterilization
Technology,Turkey) at 3000 G·15 min
-1
. The sera obtained were stored
at -20 °C (Haier, DW–86L828S, China) until analysis.
Hematology
After all clinical examinations, 5 mL of blood samples were taken
from the Vena cephalica antebrachi of the dogs to the tubes with
anticoagulant and without anticoagulant once before castration. In
the blood samples with Ethylenediaminetetraacetic acid (EDTA) the
levels of erythrocyte (RBC), hemoglobin (HGB), hematocrits (HCT),
mean corpuscular volume (MCV), red cell distribution width (RDW) and
mean corpuscular hemoglobin concentration (MCHC) were determined
by a hematological analyzer (BC2800 Vet hematology analyzer, Mindray
Bio–Medical Electronics Co. Ltd., Nanshan, Shenzhen, Chine).
Serum biochemical analysis
Serum total antioxidant capacity (TAC, Rel Assay Diagnostics
kit; Mega Tıp, Gaziantep, Turkey) and total oxidant (TOC, Rel Assay
Diagnostics kit; Mega Tıp, Gaziantep, Turkey) capacity levels were
determined according to the procedure of manufacturers’ directories.
The optical density was determined using a microplate reader
(Multiskan GO, Thermo Scientic, USA). Serum Fe and unsaturated
iron–binding capacity (UIBC) levels were determined using an auto–
analyzer (Abbot C8000–USA) using commercial kits.
FIGURE 1. Serum TAC (mmol Trolox equivalent·L
-1
), TOC (µmol H
2
O
2
Eq·L unit
-1
), Fe
(ng·mL
-1
) and UIBC (µg·dL
-1
) levels in the pre and post castrated dogs (Mean ± SEM)
_____________________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIV, rcfcv-e34318
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Statistical analysis
The sample size was determined as 20 dogs as a result of the power
analysis before starting the study. In the power analysis, type 1 error
probability (α), power (1–β) and effect size (f) were taken 0.05, 0.80
and 0.40, respectively. G * Power Version 3.1.9.2 statistical program
was used for power analysis.
Descriptive statistics for each variable were calculated and
presented as “Mean ± Standard Error of Mean”. Before performing
the statistical analysis, data were examined with the Shapiro–Wilk test
for normality assumptions. To test the differences in each parameter
between time sampling, the Friedman test was used for repeated
measures. The relationship between parameters was analyzed
with the Spearman correlation coecient. For all analyses, SPSS®
22.0 (IBM, New York, USA) for Windows was used and P<0.05 was
considered as signicant.
RESULTS AND DISCUSSION
Descriptive statistics (Mean ± Standard Error of Mean) of serum and
blood parameters in relation to castration in male dogs are presented
in TABLES I and II, and FIG. 1. Serum TAC (P=0.494), TOC (P=0.668), Fe
(P=0.187) and UIBC (P=0.229) values showed a non–signicant (P>0.05)
difference over time and non –signicant correlations between each other
except Day 0; TAC and TOC levels (r=0.0842, P=0.002) [TABLE II, FIG. 1].
It is well known that Testosterone has anabolic and androgenic
effects on the organism. While anabolic activity plays an important
role in the development of muscles, androgenic effect responses
development of primary (growth and development of reproductive
organs, the continuation of spermatogenesis) and secondary
(sex characteristics, thickening of the voice, rate of gain, feed
conversation, and the development of somebody regions, among
others) [11]. Additionally, Testosterone has been reported to
reduce development and growth, increase stress levels, suppress
the immune system, and increase the risk of death [12]. For this
purpose, it is important that analyze the effects of the absence of
Testosterone on various body parameters to evaluate the pros and
cons of gonadectomy. In this study, it was evaluated the relationship
between gonadectomy and oxidant–antioxidant capacity and Fe
metabolism at some serum parameters in male dogs.
After the orchidectomy operation, a remarkable decrease in
clinical and statistical blood parameters was observed [TABLE III].
It is thought that a sudden androgen decline occurs with orchiectomy
and blood production is disrupted as a result. Among the main factors
reported by researchers for erythropoiesis, androgens are of great
importance [13]. Hematological parameters [14], which have been
determined to be decreased with many disease states, have been
associated with the use of androgenic steroids in athletes [15]. The
hypothesis of the current study is that a decrease in hemoglobin
concentration follows the apparent androgen deprivation that occurs
after castration. It is clear from measurements that blood parameters
tend to drop suddenly after Day 1.
Surgical procedures performed on any part of the body cause
undesirable changes in normal body homeostasis, and even
surgical traumas increase the TOC level alone [16]. In dogs, after an
ovariectomy operation [17], an increase was determined in plasma
TOC levels on the rst post–operation day, which indicated that the
oxidative stress because of anesthesia and surgical trauma. In another
study, lipid peroxidation levels were found high on the rst day after
the operation and lipid peroxidation levels were low on Days 3, 5,
and 7 [18]. Contrary to previous studies performed by Mahalingam
et al. [18] and Lee and Kim [17], the obtained results showed relative
stability in levels of TOC. TOC and TAC levels on post–operation 1.
Day was similar to pre–operation levels. Except Day 0, a signicant
difference could not be found between serum TAC and TOC levels
was found (P>0.05), [TABLE II]. Besides, when the serum TAC levels
were examined in terms of the time change [TABLE I, FIG. 1], it was
determined that there was not a signicant difference (P>0.05).
Similarly, it was determined that the changes in serum TOC levels over
time are not signicant (P>0,643) [TABLE I, FIG. 1]. These unexpected
oxidative and anti–oxidative status stability could be highly related
to the dicult determination of post–operative conditions on intra
and extracellular inammatory response mechanisms from blood
samples [3, 16, 17].
Environmental factors, various diseases, and stress can alter
the results of the anti–oxidative status of the organism [19]. Stress
consists of three stages, alarm, reaction, and exhaustion stages.
Oxidative stress could affect by this complexity of stress [20, 21].
The results of the present study showed no difference over time and
they followed a stable line. This phenomenon could be explained by
stress caused by operation, injection, or collection of blood samples.
In studies conducted in rats (Rattus norvegicus) [22] and rabbits
(Oryctolagus cuniculus) [23] reported that high levels of Testosterone
TABLE I
Descriptive statistics of serum TAC (mmol Trolox equivalent·L
-1
),
TOC (µmol H
2
O
2
Eq·L unit
-1
), Fe (ng·mL
-1
) and UIBC (µg·dL
-1
)
levels in the pre and post castrated dogs (Mean ± SEM)
Preoperation Postoperation
P–value
Day 0 Day 1 Day 3 Day 7
TAC 1.446 ± 0.084 1.403 ± 0.063 1.502 ± 0.032 1.520 ± 0.059 0.494
TOC 8.590 ± 2.708 8.850 ± 2.257 5.622 ± 1.182 8.115 ± 2.365 0.668
Fe 130.680 ± 12.990 115.520 ± 7.240 101.990 ± 5.900 109.860 ± 10.350 0.187
UIBC 151.320 ± 17.580 168.080 ± 17.490 181.240 ± 18.850 172.400 ± 16.320 0.229
Effect of castration over hematological parameters in shepherd dogs / Yurdakul and Uslu _________________________________________
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TABLE II
Spearman’s correlation coecients (rs), describing the relation between TAC (mmol Trolox equivalent·L
-1
),
TOC (µmol H
2
O
2
Eq·L unit-1), Fe (ng·mL
-1
) and UIBC (µg·dL
-1
) levels in the pre and post castrated dogs
Day 0 TAC TOC Fe UIBC
Spearman’s rho
TAC
Correlation Coecient 1.000
Sig. (2–tailed)
n 10
TOC
Correlation Coecient 0.842** 1.000
Sig. (2–tailed) 0.002
n 10 10
Fe
Correlation Coecient 0.006 0.455 1.000
Sig. (2–tailed) 0.987 0.187
n 10 10 10
UIBC
Correlation Coecient -0.115 -0.430 -0.600 1.000
Sig. (2–tailed) 0.751 0.214 0.067
n 10 10 10 10
Day 1 TAC TOC Fe UIBC
Spearman’s rho
TAC
Correlation Coecient 1.000
Sig. (2–tailed)
n 10
TOC
Correlation Coecient 0.539 1.000
Sig. (2–tailed) 0.108
n 10 10
Fe
Correlation Coecient 0.236 0.370 1.000
Sig. (2–tailed) 0.511 0.293
n 10 10 10
UIBC
Correlation Coecient -0.212 -0.018 -0.297 1.000
Sig. (2–tailed) 0.556 0.960 0.803
n 10 10 10 10
Day 3 TAC TOC Fe UIBC
Spearman’s rho
TAC
Correlation Coecient 1.000
Sig. (2–tailed)
n 10
TOC
Correlation Coecient 0.006 1.000
Sig. (2–tailed) 0.987
n 10 10
Fe
Correlation Coecient 0.164 -0.430 1.000
Sig. (2–tailed) 0.651 0.214
n 10 10 10
UIBC
Correlation Coecient -0.212 -0.018 0.091 1.000
Sig. (2–tailed) 0.556 0.960 0.803
n 10 10 10 10
Day 7 TAC TOC Fe UIBC
Spearman’s rho
TAC
Correlation Coecient 1.000
Sig. (2–tailed)
n 10
TOC
Correlation Coecient -0.018 1.000
Sig. (2–tailed) 0.960
n 10 10
Fe
Correlation Coecient -0.261 0.006 1.000
Sig. (2–tailed) 0.467 0.987
n 10 10 10
UIBC
Correlation Coecient 0.564 0.200 -0.661* 1.000
Sig. (2–tailed 0.090 0.580 0.038
n 10 10 10 10
*: Correlation is signicant at the 0.05 level (2–tailed). **: Correlation is signicant at the 0.01 level (2–tailed)
_____________________________________________________________________________Revista Cientifica, FCV-LUZ / Vol. XXXIV, rcfcv-e34318
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increased oxidation levels in testicular tissues and decreased
antioxidant levels such as SOD, CAT, GSH–Px and GSH. In another
study [21]. that supports this information; It has been reported that
antioxidant levels such as SOD and GSH–Px decreased compared to
the control group, and the reason for the decrease in these antioxidant
levels was that testosterone deciency disrupted antioxidant defense
mechanisms. In this study, similar serum TOC and TAC levels were
assessed at 0th, 1st, 3rd and 7th days. On the post–operation 1st,
3rd and 7th days, decreased serum TOC levels could be interpreted
as a decrease in the risk of OS for the elimination of Testosterone
hormone secretion from testicles, mainly because of the elimination
of the inducing effect of Testosterone on ROS. However, this study
is in a contrast with the results of some studies [11, 12, 24]. The
balance in serum TAC levels (FIG. 1) can be interpreted as a decrease in
oxidative stress because of a decrease in Testosterone concentration
and an increase in the antioxidant defense activities of the cells in
response to harmful effects such as lipid peroxidation/oxidation in
the membranes caused by ROS.
In this study, serum Fe and UIBC levels were examined also. It
was not found a significant correlation except Day 7 (r= -0.661,
P<0.05) between serum Fe and UIBC levels [TABLE II]. Additionally,
changes of serum Fe and UIBC levels during the time were analyzed
and the relation was similar to other parameters and there was not
a signicant difference (P>0.05) [TABLE II, FIG. 1] also determined.
Fe is a particularly important element because of its necessity for
the normal function of erythrocyte production. There is a close
relationship between Fe and Testosterone. It is working with
Testosterone during the production of erythrocytes by a negative
feedback mechanism [10]. Fe deciency is reduced in Testosterone
deciency and is one of the most important causes of anemia [25].
It has been shown that there is a signicant decrease in erythrocyte
and hemoglobin concentration in the elderly or the littered male
animals, parallel to the decrease in Testosterone level [26]. It has also
been shown that in castrated male animals, blood parameters can
be normalized by the administration of androgens in the presence of
anemia [25, 27]. Because of all these stimuli, serum Fe concentration
is also expected to increase due to the need for absorption and
consumption. Contrary to the work of Shahidi [25], a signicant
decrease in serum levels of Fe was not detected in parallel with the
decrease of Testosterone hormone secreted from testes in this study.
CONCLUSION
As a result, it was determined by measurements that UIBC increased
and Fe ratio decreased due to the sudden decrease in androgens after
orchiectomy. In conditions such as inammation and anemia, serum
Fe level decreases and UIBC increases. The statistical difference in
blood parameters (P<0.05) is an indication of this. Although these
values try to return to normal as the inammation heals in the future,
they will not be able to return due to long–term androgen deciency
and anemia will occur. Orchiectomy–induced anemia is a process
that can be explained by androgens that support the hematopoiesis
mechanism. Although the data obtained in this study prove that
orchiectomy is slightly associated with anemia, the relationship
between orchiectomy and anemia will be revealed more clearly in
future studies with more animals, more parameters and longer periods
of time. In addition, it is thought that different results may occur due
to diculties in determining serum TAC, TOC and Fe levels in dogs,
and the relationships between these parameters can be claried
with clinical observations and longer studies.
ACKNOWLEDGMENT
The authors declare that no funds, grants, or other support were
received during the preparation of this manuscript
Ethical statement
This study was approved by the Sivas Cumhuriyet University Animal
Experiments Local Ethics Board.
Conict of ınterest
The authors declare that they have no conflict of interest.
Statement of Animal Rights all applicable international, national,
and/or institutional guidelines for the care and use of animals
were followed.
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TABLE III
Hematological parameters before and after surgery in castrated dogs
Preoperation Postoperation
Day 0 Day 1 Day 3 Day 7
RBC (×10
12
·L
-1
) 5.6 ± 0.96
a
4.7 ± 0.82 3.0 ± 0.81 3.6 ± 1.73
a
HGB (g·dL
-1
) 14.5 ± 0.97 12.5 ± 1.78
a
9.0 ± 0.94 10.1 ± 1.96
a
HCT(%) 44.9 ± 2.46 40.7 ± 2.45 31.5 ± 4.4 30.4 ± 4.32
MCV(fL) 73.1 ± 3.72
a
59.9 ± 3.6
b
43.0 ± 3.29
ac
51.2 ± 9.44
bc
RDW (%) 14.9 ± 0.73 11.4 ± 1.26 9.4 ± 1.50 9.7 ± 3.02
MCHC (g·dL
-1
) 33.0 ± 1.56
a
22.7 ± 4.57 20.3 ± 2.75 22.1 ± 3.54
a
a,b,c
: There is a statistically signicant dierence (P<0.05) for lines bearing the same letter,
RBC: Erythrocyte, HGB: Hemoglobin, HCT: Hematocrit, MCV: Mean Corpuscular Volume,
RDW: Red Cell Distribution Width, MCHC: Mean Corpuscular Hemoglobin Concentration
Effect of castration over hematological parameters in shepherd dogs / Yurdakul and Uslu _________________________________________
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