https://doi.org/10.52973/rcfcv-e34369
Received: 19/12/2023 Accepted: 15/02/2024 Published: 12/06/2024
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Revista Científica, FCV-LUZ / Vol. XXXIV, rcfcv-e34369
ABSTRACT
The aim of this study was to investigate the effects of different
stocking densities on oxidative stress, some hematological and
biochemical blood parameters in New Zealand rabbits, and to
determine the ideal cage area where rabbits can live without being
stressed. A total of 36 1–month–old mixed sex New Zealand weaned
rabbits were selected for the study. The rabbits were placed in cages
at different densities of stocking. Experimental groups were 1 rabbit
per cage (C
1
), 2 rabbits per cage (C
2
) and 3 rabbits per cage (C
3
). There
eosinophlis, basophlis, AST, ALT, trigliseride, cholesterol, HDL and
LDL parameters (P>0.05). C
2
group had lower count of PLT comparing
C
1
and C
3
groups. C
1
P<0.05).
P>0.05). C
2
group had the lowest
value in terms of SOD (P<0.05). In conclusion C
2
group was determined
more advantageous in terms of breeding and welfare, since C
1
group
does not support social needs of the animals and C
3
group leads
to increased stress levels due to reduced individual space and
restricted movement.
Key words:
RESUMEN
El propósito de este estudio fue investigar los efectos de diferentes
densidades de población en conejos de Nueva Zelanda sobre el estrés
oxidativo, así como algunos parámetros sanguíneos hematológicos
y bioquímicos, con el objetivo de determinar el área ideal de la jaula
donde los conejos puedan vivir sin estar estresados. Se utilizaron
un total de 36 conejos destetados de Nueva Zelanda, con una edad
de 1 mes, como material animal. Estos conejos fueron distribuidos
en jaulas con diferentes densidades de población, siendo los grupos
experimentales: 1 conejo (C1), 2 conejos (C2) y 3 conejos (C3) por
P>0,05). Sin
embargo, se encontró que el grupo C2 presentaba un recuento más
bajo de plaquetas (PLT) en comparación con el grupo C1 y el grupo
P<0,05).
En cuanto a los parámetros de estrés oxidativo, no se observaron
TAS (P>0,05). No obstante, el grupo C2 presentó el valor más bajo en
términos de actividad de la superóxido dismutasa (SOD) (P<0,05). En
conclusión, se determinó que la densidad de población representada
por el grupo C2 era más ventajosa en términos de reproducción y
bienestar animal. Esto se debió a que el grupo C1 no satisfacía las
necesidades sociales de los animales, mientras que el grupo C3
conducía a niveles más altos de estrés debido al espacio individual
reducido y al movimiento restringido.
Palabras clave:
Haematological, biochemical and oxidative stress parameters of
New Zealand rabbits housed at different stocking densities
Parámetros hematológicos, bioquímicos y de estrés oxidativo de conejos de
Nueva Zelanda mantenidos en diferentes densidades de población
Büşra Yaranoğlu
1
* , Mustafa Hilmi Yaranoğlu
2
, Saliha Uysal
3
, Adnan Adil Hişmioğullari
3
1
Balikesir University, Faculty of Veterinary Medicine, Department of Animal Husbandry. Balikesir, Türkiye.
2
Balikesir University, Research Center for Experimental Animal Breeding. Balikesir, Türkiye.
3
Balikesir University, Faculty of Medicine, Department of Medical Biochemistry. Balikesir, Türkiye.
*Corresponding author: busrayaranoglu@balikesir.edu.tr
Rabbit Blood Parameters at different stocking densities / Yaranoğlu et al. __________________________________________________________
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INTRODUCTION
suspended in plasma and plays a fundamental role in maintaining
biochemical parameters serve as valuable indicators of the health
and function of internal organs and systems [1, 2, 3].
Stress is a biological response in the form of anatomical,
physiological and behavioral changes that threaten the homeostasis.
Animals experience varying degrees of both psychological and
physiological stress at different stages of their lives. To mitigate
the risk of excessive stress, it is crucial to employ objective measures
for identifying its causative factors. Properly managing an animal's
exposure to stress factors not only has a positive impact on their
productivity but also enhances overall welfare [4].
In animal production, the stress level is one of the important criteria
various factors, and it is recommended to analyze a combination of
criteria, including productivity levels, behavioral characteristics, and
physiological parameters (hematological, enzymatic, and hormonal),
in order to accurately identify the causes of stress. This integrated
approach enables a comprehensive understanding of the factors
impacting animal welfare and facilitates effective strategies for stress
management in animal production systems [5, 6, 7].
Ovuru and Ekweozor [8] emphasized that blood data was a very
important indicator in understanding whether animals were adapted
to the environment in which they were raised. Environmental
changes can induce stress in animals, leading to alterations in
blood parameters as a result of physiological responses to these
valuable insights into the adaptive capacity of animals and helps in
understanding how they respond to and cope with changes in their
surroundings. This emphasizes the role of blood analysis as a key tool
in assessing the overall welfare and adaptability of animals to their
environment. New Zealand rabbit (Oryctolagus cuniculus) stands out
with its short generation interval, high fertility rate and short gestation
period. Indeed, rabbits serve a dual role as both laboratory animals
commonly used in experimental studies and important farm animals
recommended for breeding. One of the key factors contributing to
of omega–3 fatty acids, polyunsaturated fatty acids, and essential
amino acids. In terms of the superior properties of the meat, it is
among the functional foods whose importance has been increasing
in the health sector in recent years [9, 10].
The establishment of standard conditions in laboratory animal
breeding is important for the uniformity and reliability of the
results to be obtained at the end of the study. In this respect, it is
necessary to provide animals convenient environment that meet their
requirements in which they can adapt without geting stressed. At
the same time, animals that adapt to different conditions easily and
remain unaffected by the environmental changes contribute to the
enhanced reliability of study results. Providing a suitable and stress–
free environment not only promotes the welfare of laboratory animals
but also plays a vital role in obtaining accurate and reproducible
2, 11, 12].
Increasing the quantity of animals raised per unit area in farm
animal decrease. Commercial enterprises often strive to maximize
is crucial to recognize that higher animal stocking density, especially
the animals. This heightened stress can potentially lead to more
frequent occurrences of aggressive and dominant behaviors among
the animals [13, 14].
The ideal cage size for rabbits should provide enough width for
the animal to stretch its body and stand straight simultaneously In
addition, it should be taken into account that young rabbits need more
space due to their rapid movements and higher activity This ensures
that the living environment accommodates their natural behaviors
and allows for proper physical development. Providing adequate
space in cages is not only essential for the rabbits' welfare but also
contributes to their overall health and well–being [15].
The study aimed to investigate the effects of different stocking
densities on oxidative stress, some hematological and biochemical
blood parameters in New Zealand rabbits. Additionally, the study
aimed to identify the optimal cage area that allows rabbits to live
sought to contribute valuable insights into the relationship between
stocking density and the physiological welfare of New Zealand rabbits,
ultimately aiming to inform practices that promote a healthier and
less stressful living environment.
MATERIAL AND METHODS
Ethical statement
Experiments Local Ethics Committee (2020/4–19).
Experimental design and animals
old New Zealand rabbits were used in the study. The weaned rabbits
were separated from their mothers, placed into experimental cages and
the study was started. Each rabbit was assigned a number, and each
rabbit was randomly transferred to the experimental cages according
to the simple random selection method. The low sexual dimorphism
and the early age of rabbits justify the standard practice of mixed
sex rearing of females and males in intensive commercial farms and
laboratories. The research period was lasted 2 months. During this
period, a commercial ration was prepared in accordance with the
needs of the rabbits was given ad libitum and provide water in drinkers
at all times of experiment. Animals were fed an experimental ration
appropriate for their energy and protein requirements. Ingrediants and
chemical composition of the experimental diet were shown
Housing conditions of the rabbits
Animals were placed in stainless steel racks with plastic suspension
cages at different stocking densities. The cages in which the animals
housed were standard and their dimensions were 71.3 × 71.6 × 47.6 cm
(width×depth×height). Experimental groups were 1 rabbit per cage
(C
1
), 2 rabbits per cage (C
2
) and 3 rabbits (C
3
FIGURE 1. C
1
(1 rabbit / cage group)
FIGURE 2. C
2
(2 rabbits / cage group)
FIGURE 3. C
3
(3 rabbits / cage group)
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TABLE I
Ingredients and chemical composition of the experimental diet
Ingredients (%)
Barley 20.75
Corn 18.00
Wheat Bran 14.00
Soybean meal 18.50
Yeast 0.20
Alfalfa our 25.00
Methionine 0.15
Phytase 0.10
L–lysine 0.20
By–pass fat 1.50
Vitamin and mineral mixture
1
1.60
Chemical composition (%)
Dry matter 94.20
Crude protein 19.35
NDF 31.45
ADF 14.55
ADL 1.02
Ether extract 4.45
Starch 19.50
Ash 9.68
Digestible energy (kcal·kg
-1
) 2,850
NDF: Neutral Detergent Fiber; ADF: Acid Detergent Fiber; ADL: Acid Detergent Lignin.
1
Supplied per kg diet: 13,000 IU vitamin A; 1200 IU vitamin D3; 75 mg vitamin E; 2
mg vitamin B
1
; 6 mg vitamin B
2
; 3 mg vitamin B
6
; 0.02 mg vitamin B
12
; 0.3 mg Co; 8
mg Cu; 27 mg Fe; 19 mg Mn; 44 mg Zn; 0.07 mg Se
allocated for each rabbit was determined as 0.43 m
2
for the group of
1 rabbit housed in the cage, 0.21 m
2
for the group of 2 rabbits housed
in the cage and 0.14 m
2
for the group of 3 rabbits housed in the cage
(FIGS. 1, 2 and 3).
Analysis of haematologic, biochemical and oxidative stress parameters
(mean corpuscular hemoglobin concentration) were calculated from
the measured blood parameters. The formulas were given in
Serum AST (aspartate aminotransferase), ALT (alanine aminotransferase),
triglyceride, total cholesterol, HDL (high density lipoptotein) and LDL (low
density lipoptotein) levels were analyzed by spectrophotometric method
Serum SOD (superoxide dismutase) activity (Elabscience Cat. No: E–
1–1–1672).
Rabbit Blood Parameters at different stocking densities / Yaranoğlu et al. __________________________________________________________
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Statistical analysis
in SPSS software version 25 [16]. Cage stocking density was the
were compared by Tukey test. P<0.05 was considered si
RESULTS AND DISCUSSION
In the study, the research focused on investigating the effects
of various stocking densities on oxidative stress, hematological,
parameters serve as crucial indicators, offering insights into the
infections or damage to visceral organs. The examination of these
parameters is essential for comprehensively understanding the
physiological responses and overall health status of the rabbits under
different stocking densities [17].
P>0.05). C
1
group
P<0.05) and differences between C
2
and C
3
2
group had lower count of PLT
comparing C
1
and C
3
groups (P<0.01).
by stress, age, gender, season and breed [18, 19]. HCT rate under 30%
of anemia [19
parameters. This lack of variation may be attributed to the similarity in
rabbit body weights and ages across the groups [11]. At the same time,
1].
It was seen that there was no problem in terms of oxygen and carbon
under stressful conditions, the animals demonstrated resilience in
et al. [20
stocking density groups. Abdel Hamid [21] didn’t report any differences
et al. [22] reported
4 rabbits reared per cage group had the lowest values among stocking
density groups. Another study, involving Californian and crossbred
rabbits housed at different densities found that the group with 20
rabbits·m
-2
-2
and 12 rabbits·m
-2
had higher values [21]. Omar et al. [12] informed
-2
group had the lowest value compared with
8 rabbits·m
-2
and 16 rabbits·m
-2
differences between 8 rabbits·m
-2
and 16 rabbits·m
-2
groups.
to make evaluation of different haematological situations in the body
role in the diagnosis of anemic conditions [23, 24]. In the study,
highest in 1 rabbit reared per cage group in the study and an increase
et al.
[12
et al. [25
et al. [22]
reported that 1 rabbit reared per cage group had the highest value of
4 rabbits reared per cage groups had lower values than this value.
values than 5 rabbits reared per cage and 7 rabbits reared per cage
groups for New Zealand rabbits [20]. In a different study conducted
California rabbits, 2 rabbits reared per cage group had the highest
cage group had the lowest values [22].
PLT cells have important roles in maintaining homeostasis,
response. An increase or activation of the number is associated with
a high thrombotic risk, while a decrease may be due to heredity or
permanent damage [26]. In the study 1 rabbit reared per cage group
had higher PLT values compared with 2 rabbits reared per cage group.
The observed increase in the level of PLT could be associated with
oxidative stress and cardiovascular diseases [27]. The lower value
of 2 rabbits reared per cage group suggested that the animals in 1
rabbit reared per cage group could be stressed, as the increase in
this value for the 3 rabbits reared per cage group supported this
opinion. Trocino et al. [28] reported that rabbits housed individual
cages had the highest level of fear comparing with collective cages.
less stressful condition. The fact that 2 rabbits reared per cage group
had lower values in terms of PLT parameter showed that this group
might not have experienced stress and adapted to the situation in
TABLE II
The formulas of the calculated blood parameters in New Zealand rabbits
Test Formula
HCT (RBC × MCV) / 10
MCH (HGB / RBC) × 10
MCHC (HGB / HCT) × 100
HCT Hematocrit; MCH: Mean Corpuscular Hemoglobin; MCHC: Mean Corpuscular
Hemoglobin Concentration
TABLE III
Mean erythrogram parameters in dierent stocking
density of New Zealand rabbits
Blood Parameters C
1
(n=12) C
2
(n=12) C
3
(n=12) SEM P
RBC, 10
3
cell·µL
-1
6.04 6.34 6.17 0.09 –
HGB, g·dL
-1
13.46 13.81 13.64 0.20 –
HCT, % 40.48 42.32 41.89 0.63 –
MCV, fL 66.92 66.80 67.24 0.35 –
MCH, pg 22.27 21.80 22.13 0.13 –
MCHC, g·dL
-1
33.29
a
32.63
b
32.52
b
0.14 *
PLT, 10
3
cell·µL
-1
364.33
a
212.42
b
297.33
a
20.79 **
C
1
: 1 rabbit per cage, C
2
: 2 rabbits per cage C
3
: 3 rabbits per cage. RBC: Red Blood Cell;
HGB: Hemoglobin; HCT Hematocrit; MCV: Mean Corpuscular Volume; MCH: Mean
Corpuscular Hemoglobin. MCHC: Mean Corpuscular Hemoglobin Concentration;
PLT: Platelet. SEM: Standard error of mean. –:
P>0.05; *: P<0.05; **: P<0.01.
a,b
: Values
within a row with dierent superscript dier signicantly at
P<0.05
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et al. [29] reported that while 2 rabbits reared per cage group had the
per cage groups had highest PLT values in New Zealand rabbits.
Leucogram parameters in different stocking density of New Zealand
lymphocytes, monocytes, eosinophils and basophils (P>0.05).
stocking density groups to the count of monocytes, eosinophils,
basophils [12] and lymphocytes [21].
rabbits·m
-2
group in terms of lymphocyte count. It has been reported
that the values in 12 rabbits·m
-2
and 8 rabbits·m
-2
groups continued
to decrease and the lowest value was in the 8 rabbits·m
-2
group [21].
value as the stocking density increased [20]. It was reported that
4 rabbits reared per cage group had the highest values in terms of
reared per cage groups had lower values and reported that there
and 5 rabbits reared per cage groups [34].
different stocking density groups in terms of AST, ALT, triglyceride,
cholesterol, HDL and LDL (P>0.05).
TABLE IV
Mean leucogram parameters in dierent stocking
density of New Zealand rabbits
Blood Parameters C
1
(n=12) C
2
(n=12) C
3
(n=12) SEM P
WBC, 10
3
cell·µL
-1
9.23 9.63 8.06 0,45 –
Neutrophils, % 25.85 23.18 19.40 1,84 –
Lymphocytes, % 68.06 70.19 76.93 2,06 –
Monocytes, % 4.10 3.03 1.81 0,49 –
Eosinophils, % 0.65 0.75 0.69 0,10 –
Basophils, % 1.28 2.86 1.17 0,74 –
C
1
: 1 rabbit per cage, C
2
: 2 rabbits per cage C
3
: 3 rabbits per cage. WBC: White Blood
Cell; SEM: Standard error of mean. –:
P>0.05
TABLE V
Mean biochemical parameters in dierent stocking
density of New Zealand rabbits
Blood Parameters C
1
(n=12) C
2
(n=12) C
3
(n=12) SEM P
AST, U·L
-1
15.67 15.92 21.67 2.16 –
ALT, U·L
-1
27.83 38.00 48.83 5.03 –
Triglyceride, mg·dL
-1
87.83 97.42 84.58 4.86 –
Cholesterol, mg·dL
-1
106.00 78.33 97.50 6.93 –
HDL, mg·dL
-1
36.50 30.58 35.83 1.85 –
LDL, mg·dL
-1
68.17 47.75 60.92 5.17 –
C
1
: 1 rabbit per cage, C
2
: 2 rabbits per cage C
3
: 3 rabbits per cage. AST: Aspartate
aminotransferase; ALT: Alanine aminotransferase; HDL: High density lipoptotein; LDL:
Low density lipoptotein; SEM: Standard error of mean. –:
P>0.05
count was generally associated with a microbial infection or presence
2
to 15–30 indicated that the rabbit may be under stress conditions [1].
In the study, it was determined that the housing system did not have
reference values, it might be associated with allergic conditions,
anaphylactic shock or parasite infestations [1, 30, 31].
In accordance with the present findings, some studies have
density groups [12, 21
et al. [20] reported that as the stocking density increased,
et al. [29
count of 4 rabbits reared per cage group was the highest while 2
rabbits reared per cage group had the lowest levels.
seen that the stocking density did not affect these values. Neutrophil,
lymphocyte, monocytes, and basophil counts were within normal
infections [32
neutrophil, lymphocyte, monocyte and eosinophil values examined
between groups. It was reported that high eosinophil value might
be associated with allergic reactions or conditions [33]. In this
regard, allergic reactions may be caused by housing factors due to
between groups in terms of eosinophil values in the study indicates
that there was no allergic situation among the groups. Similar to study
In rabbits, serum biochemical parameters ensure important key
factors about visceral organ damage, particulary in liver and kidneys
[18, 35
of the stocking density groups in terms of AST, ALT, triglyceride,
differences between different stocking density groups in terms of
of the study [12, 15, 34, 36, 37et al. [22], Aboegla et al. [29]
et al. [38] stated that cholesterol and triglyceride
values decreased as the stocking density increased. Contrary to the
the stocking density increased [22, 39]. In terms of HDL, the value
obtained from 3 rabbits reared per cage group was found to be higher
than the value obtained from 2 rabbits reared per cage group [37].
In normal physiological conditions, there exists a delicate equilibrium
within cells and the presence of antioxidants that counteract their
along with the accumulation of superoxide radicals within the cell
or an inadequate endogenous defense system, is referred to as
Rabbit Blood Parameters at different stocking densities / Yaranoğlu et al. __________________________________________________________
6 of 8
the intracellular signaling mechanism by damaging proteins, lipids and
nucleic acids in the cell. Antioxidants fundamentally work to prevent
or delay cell damage by scavenging free radicals in the cell. SOD and
TAS are among the important antioxidants in this context [39].
is a metabolic product of protein occurred during acute ischemic
conditions or oxidative stress due to a decrease in binding capacity
of albumin for transition metals such as iron, cobalt, copper and
nickel [40, 41].
Oxidative stress parameters in different stocking density groups
P>0.05).
C
2
group had the lowest value in terms of SOD (P<0.05). There was no
1
and C
3
groups (P>0.05).
concluded that the C
2
group might be the ideal housing frequency
in terms of cage breeding, where the animals can adapt without
getting stressed, but the individual behaviors and struggle between
the animals should be considered. In future studies, monitoring and
evaluating the behavior of animals in cages and interpreting them
contribute to the literature.
Availability of data and materials
Financial support
2021/040).
Conict of interest
interest.
Author contributions
anuscript.
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TABLE VI
Mean oxidative stress parameters in dierent stocking
density groups of New Zealand rabbits
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1
group
had higher values than C
2
and C
3
groups. As PLT value, C
2
group had
lower values than C
1
and C
3
groups. It was determined that C
2
group
study, it can be said that the C
2
group was more advantageous in
terms of breeding and welfare, since the C
1
group does not support
the social needs of the animals, and thus increases the stress in the
animals, and the animals adapt to these conditions more easily. In
the C
3
group, animals tend to get stressed due to the decrease in
the area per animal and the restriction of movement. In this respect,
it is important to pay attention to the area per unit animal in cage
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