Content uploaded by Ahmed Abd El-Hady
Author content
All content in this area was uploaded by Ahmed Abd El-Hady on May 28, 2021
Content may be subject to copyright.
Egypt. Poult. Sci. Vol. (40) (III): (613-629)(2020) (2008-1108)
Egyptian Poultry Science Journal
http://www.epsj.journals.ekb.eg/
ISSN: 1110-5623 (Print) – 2090-0570 (Online)
INFLUENCE OF SUPPLEMENTARY RED BEETROOTS OR
BETAINE DIETARY ON PRODUCTIVE PERFORMANCE, BLOOD
PROFILES AND ECONOMIC EFFICIENCY OF GROWING
RABBITS
Aboelfadl M. A., F. N. K. Soliman, O. A. Elghalid and A. M. Abd El-Hady*
Fac. of Agric. (El-Shatby), Poult. Prod. Dep. Alexandria Uni., Alexandria 21545, Egypt
*Correspondence author: A. M. Abd El-Hady Email:ahmed75atta@yahoo.com
Received: 08/08/2020
Accepted: 01 /09/2020
ABSTRACT: The present study aimed to investigate the effect of dried red beetroots
and commercial betaine on blood hematology, lipid profile and immunity status of
growing rabbits. A total of 150, unsexed Alexandria line weaned rabbits, at 4 weeks of
age were randomly divided into five groups (30 rabbits each). Rabbits in the first group
were fed the control diet, while those in groups 2nd, 3rd, 4th and 5th were fed on 0.5 %,
1.0 % of dried red beet, 0.1% and 0.2% of commercial betaine, respectively for 5
weeks. Data revealed that treatment groups with dried red beetroots and commercial
betaine recorded the higher live body weight at 9 weeks of age, body weight gain, feed
consumption from 4 to 9 weeks and improved feed conversion and mortality rate
compared to control group. Red blood cells, hemoglobin and packed cell volume was
increased significantly compared to control group. All treatments and increasing red
beetroots and betaine levels resulted in high in white blood cells, lymphocyte, total
protein, globulin and high density lipoprotein levels compared to control, but, total
lipids, cholesterol, triglyceride and low density lipoprotein values decreased
significantly. Liver enzymes and kidney function levels were improved in treatment
groups compared to the control group. With dried red beetroots physiological status of
growing rabbits was showed an enhanced compared to commercial betaine. The results
of economic efficiency indicated that the Alexandria growing rabbit fed 0.5% dried red
beetroots has highest relative economic efficiency compared to control, 3nd, 4rd and 5th
(108.10, 103.47, 104.72 and 98.79%, respectively). These findings revealed that 0.5 kg/
100 kg diet may exert beneficial effects on productive performance, hematology
parameters, lipid profile and economic efficiency properties of growing rabbits.
Keywords: Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
Aboelfadl M. A. et al.
INTRODUCTION
Plant-derived supplements are used to
maintain the growth performance of
livestock animals (Ashour et al., 2014).
The use of diets rich in natural
antioxidants as a means of removing
excessive free radicals from the animal’s
body (Li et al., 2018), and for normal
physiological processes in animals (Lee
et al., 2017), is becoming popular/
essential. Red beet is a rich source of
polyphenols together with the betaine
(Bet), demonstrating a high antioxidant
effect and radical scavenging capacity,
which possess many health positive
effects (Nestora et al., 2016). Therefore,
Hussein et al. (2016) suggested the use of
new by–products of processed sugar to be
included in poultry diets to enhance
growth performance in areas where an
abundance of this sugar mill by-product is
available.
The Bet has the potential to improve
nutrient digestibility by supporting the
broilers growth, since it stimulate cell
proliferation in the intestinal tissue, the
enlarged gut wall epithelium which
provide an increase surface for nutrient
absorption and then affects the body
weight (Ratriyanto et al., 2009). Also, Bet
supplementation significantly improved
feed conversion ratio (FCR) in rabbits
(Hayam Abo EL-Maaty et al., 2017),
broiler chickens (Chand et al., 2017) and
ducks (Wang et al., 2004). However,
Sakomura et al. (2013) found that
different studied Bet supplementations
did not significantly affect feed
consumption (FC) and FCR of broiler
chickens.
El-Shinnawy (2015) evaluated the
influence of supplementing Bet to broiler
diets containing adequate concentration
of methionine, found that
supplementation with Bet led to
significant increases in serum
concentrations of total protein and
globulin. Due to its special molecular
structure, Bet is also an efficient methyl
donor. The trans-methylation of Bet is
used in many biochemical pathways
including the methionine–homocysteine
cycle and the biosynthesis of carnitine
and phospholipids (Figueroa et al., 2018).
Thus, Bet plays an important role in lipid
metabolism including decrease of hepatic
triglyceride accumulation (Xu et al.,
2015). In general, dietary Bet may affect
the levels of cholesterol in plasma and
different tissues of animal bodies.
Most of the studies on red beets have
been directed to human health features, as
well as the studies of Bet directed to its
advantages in preventing chicken heat
stress. Therefore, the objectives of this
study was to evaluate the effects of
adding two sources of antioxidants dried
red beetroot and commercial betaine to
the diet of growing Alexandria rabbits
line on productive performance, blood
characteristics and economic efficiency.
MATERIALS AND METHODS
The present study was carried out at the
Poultry Research Center, Faculty of
Agriculture, Alexandria University,
during the period from March to April
2017 .
Animal care
All animal care procedures were
approved by the Institutional Animal
Care and Use Committee in AU-IACUC,
Alexandria University, Egypt. Authors
adhere the procedures imposed on the
animals have been implemented in
accordance with Directive 2010/63/EU of
the European Parliament and of the
Council of 22 September 2010 on the
protection of animals used for scientific
purposes. Authors also adhere to the EU
regulations on feed legislation, the
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
‘Regulation (EC) No 767/2009 of the
European Parliament and of the Council
of 13 July 2009 on the placing on the
market and use of feed.
Dried red beetroots
Dried red beetroots (RBR) harvested 7-8
month were washed with tap water,
chopped into small pieces and then dried
at solar energy for 3 days. The dried
material was reduced into powder form as
far as possible and powdered using a lab
grinder and stored at 4°C till use (Rabeh,
2015). The practical nutrition analysis of
RBR was found in Table 1.
Commercial Betaine
The commercial source of chemical Bet
used in the present experiments was
"Betafen". Betafin® natural betaine is
extracted from sustainable sugar beet
molasses and vinasses (fermented
molasses) using a patented
chromatographic separation process.
Alexandria rabbit line
Alexandria line is a synthetic paternal
rabbit line which was established and
progressing at the nucleus breeding rabbit
unit of the Poultry Research Center,
Alexandria University, Egypt. This line
was originated by crossing a V-line with
a Baladi Black rabbits (El-Raffa et al.,
2005). The line is being individually
selected for daily gain between weaning
(28d) and slaughter (63d).
Experimental design
A total of 150 weaned unsexed
Alexandria line rabbits, aged four weeks
and averaged 610 g body weight, were
randomly allocated into five experimental
groups each of 30 rabbits. Each group
was further subdivided into 10 replicates
of 3 rabbits each. All rabbits were nearly
similar in live body weight in treatments,
fed ad libitum until marketing at 63 days
of age and water was accessible all the
time. Rabbits in the control were fed a
basal diet without supplementation, while
those in groups 2nd, 3rd, 4th and 5th were
fed a basal diet containing dried red beet
at levels of 0.5 % and 1.0 % or Bet at
levels of 0.1% and 0.2%, respectively. All
experimental groups were fed the basal
diet was formulated to cover all essential
nutrient needs of growing rabbits (NRC,
1994), containing 17.27% crude protein
and digestible energy 2640 kcal/kg.
Housing and management
Growing rabbits were housed in well-
ventilated open system rabbitry made of
galvanized (50×45×40 cm) wire cages
with gridded wire floor to completely
separate rabbits from excreta. All rabbits
were kept under the same managerial,
hygienic and environmental conditions, at
controlled average range of ambient
temperature 20 - 23 °C, relative humidity
60–73 % and day-light length during the
five weeks of the experimental period
(March to the end of April) 10 h 24 min
to 11 h 46 min.
All cages were provided with manual
feeders and accessible clean fresh water
through an automated system of nipple
drinkers. Cages properly cleaned and
disinfected regularly. After each kindling,
urine and feces were dropped from cages
on the building floor were collected every
day morning and removed outside the
house .
Data collected
Individual rabbit live body weights (BW),
body weight gain (BWG), FC and FCR
for the experimental period were recorded
at the start and end of the experimental
period. The dead rabbits were recorded
during the whole experimental period for
each treatment, and then the mortality
rate (MR) was calculated as number of
dead rabbits at the end of the experiment
to the number of rabbits the beginning of
the study. About 3 ml of blood samples
Aboelfadl M. A. et al.
were collected between 8.00 – 9.00 h a.m.
at 63 days of age from the marginal ear
vein into vacationer tubes with or without
containing K3-EDTA (1 mg/ml).
Coagulated and non-coagulated blood
samples after centrifuged at 4000 rpm for
15 minutes and the clear serum and
plasma were separated and stored frozen
at -20°C until biochemical analysis. Fresh
blood samples were analyzed shortly after
collection for hematological parameters.
Counts of red blood cells (RBCs
106/mm3) and WBCs (103/mm3),
hemoglobin (Hb) concentration (g/dl) and
packed cell volume (PCV %) were
determined and its differential counts
lymphocyte (L), neutrophils (N) and the
ratio between them (N/L) according to
(Feldman et al., 2000).
Plasma total protein and albumin (AL,
g/dl) measured using special kits
delivered from sentinel CH Milano, Italy
by means of spectrophotometer
(Beckman DU-530, Germany). With the
difference between total protein and AL
the blood globulin (GL) level (g/dl) was
calculated as fibrinogen usually contains
a small fraction. AL per GL ratio was
calculated by divided Al per GL. Serum
concentration of total lipids (TL),
cholesterol (Chol), triglyceride (TG), high
density lipoprotein (HDL) and low
density lipoprotein (LDL) (mg/dl) were
assessed calorimetrically using
commercial kits (Biosystems S.A. Costa
Brava, Barcelona, Spain). The
transaminase enzymes activities of serum
aspartate amino transferase (AST),
alanine amino transferase (ALT) and
alkaline phosphatase (ALP) levels were
determined by calorimetric method.
Serum creatinine and uric acid were
assayed by a colorimetric method using
commercial kits of Sclavo Diagnostics
Company (Kite Italia S.P.A.).
Economic efficiency
Economic efficiency of production was
calculated from the input-output analysis
of the money, based on the differences in
both growth rate and feeding costs. The
value of the economic efficiency was
calculated as the net revenue per unit of
total feed costs. The prices of
experimental diets and live body weight
were calculated according to the prices of
the local Egyptian market at the time of
experiment in 2018, according to the
formula of (Riad et al., 2010).
Net Revenue = Total Revenue - Total
feed cost
Economic efficiency = Net Revenue /
Total feed cost x 100
Relative economic efficiency (%)
affecting the control treatment = 100%
Statistical analysis
The statistical analyses were carried out
using a completely randomized design.
Data were analyzed by analysis of
variance using the general liner model
procedure (SAS, 2004). Data on the traits
studied were subjected to analysis of
variance using the following model: Yijk=
μ + Ti + Yj + eijk in which Yijk i is each
dependent variable under study, µ is the
overall mean, Ti is the fixed effect of the
ith treatments of red beet (i from 1 to 2),
Yj is the fixed effect of the jth treatments
of commercial betaine (j from 1 to 2) and
eijk is the random residue error. Duncan’s
multiple range tests was used to detect
any significant differences among the
experimental means (Duncan, 1955). The
statistical significance was accepted at P≤
0.05.
RESULTS AND DISCUSSIONS
Productive performance
The results in table 2 showed that showed
significant differences in control vs.
treatments comparison for 9-week BW
(P≤0.01) by 5.35 % and 4-9-week BWG
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
(P≤0.001) by 8.27 %, while it is
insignificant (P≥0.05) in the other
comparisons (RBR 0.5% vs. RBR 1%,
Bet 0.1% vs. Bet 0.2% and RBR vs. Bet).
The RBR and Bet treatments have
significantly higher BW and BWG
compared to corresponding values of
control group. Although there are no
significant (P≥0.05) differences, the
increase of both experimental antioxidant
sources level has slight positive effect on
the final BW and BWG of growing rabbits.
Also, the comparison of dried RBR vs.
Bet showed enhancer effect on BW and
BWG in favor of dried RBR.
The results of dried RBR are in
agreement with the finding of Hayam
Abo EL-Maaty et al. (2017) who made
different sugar beet tops (SBT)
substitution in rabbit diets was produced
positive effects on growth performance
although feed intake was higher than that
of the control group. However, El-Taweel
(2010) diet did not found that BWG
influences by different studied sugar beet
pulp (SBP) substitutions in rabbit diets.
Moreover, Abedo et al. (2012) showed
that total and daily BWG were
significantly decreased with SBP
substitutions diets and both values were
progressively lowered with the diet
contained 50% SBP of corn diet.
The results of Bet are in agreement with
the finding of Hassan et al. (2011) and
Abd El-Moniem et al. (2016) who
showed significant enhancer effect of
dietary Bet on BW and BWG of NZW
growing male rabbits. Also, Abd El-
Azeem et al. (2019) found that daily
BWG during 5-13 weeks of age was
significantly increased in NZW growing
male rabbits fed Bet supplemented diets
(750 and 1500 mg/kg) compared to
control group (33.28, 35.76 and 30.17g,
respectively).
The RBR and Bet treatments have
significantly higher 4-9weeks FC by
3.09% and better FCR by 5.23%
compared to corresponding values of
control treatment. Although there are no
significant differences, the increase of
beetroot level increase the 4-9weeks FC,
while the results of 4-9weeks FCR found
to be improved with the increase of RBR
level while opposite trend was found with
Bet. The RBR was useful to improve FCR
more than Bet.
The present results of dried RBR are in
agreement with the finding of Shehata
and Bahgat (2006) who reported that SBP
in diets increased FC for growing rabbits
when 25% of whole diet was replaced by
SBP. Hayam Abo EL-Maaty et al. (2017)
found that replacing alfalfa hay with SBT
(0, 20 and 30%) of NZW rabbits during
6-12 weeks of age increased significantly
FC than that of control group and FCR
value was improved significantly. Also,
El-Taweel (2010) showed slight FC
increase by different studied SBP
substitutions in rabbit diets. However,
Aboul-Ela and Reda (2016) reported that
SBP reduced FC of rabbits. Considering
rabbit FCR trait, the SBP substitution has
improved FCR as showed by Abedo et al.
(2012) and Aboul-Ela and Reda (2016).
In contrary, Shehata and Bahgat (2006)
and El-Taweel (2010) found that SBP
substitutions rabbit diets improved FCR.
In regard to Bet supplementation, Hassan
et al. (2011) showed that NZW growing
male rabbits fed Bet supplementation
(750 and 1000 mg Bet/kg) increased
significantly FC compared to control
group. However, Abd El-Azeem et al.
(2019) found that FC of NZW growing
male rabbits not significant affected by
different dietary supplementation include
Bet. They indicated that FCR and
economic efficiency recorded the best
Aboelfadl M. A. et al.
results with rabbits fed 1500 mg Bet /kg
in their diet.
The results showed significant differences
in control vs. treatments comparison for
4-9weeks mortality rate (P≤0.05), while it
is insignificant in the other studied
comparisons (Table 1). The RBR and Bet
treatments have significantly better MR
value by 50% compared to control
treatment value (3.33 and 6.67%,
respectively). The both antioxidant
sources and their levels had no effect on
MR of growing rabbits.
In respect of RBR, the results are in
agreement with the findings of Aboul-Ela
and Reda (2016) and Hayam Abo EL-
Maaty et al. (2018) who showed that the
inclusion of SBP in rabbit diets by
different levels improved viability of the
fattening rabbits.
The good performance of rabbits shown
in the present study may be due to the
phytochemicals present in RBR and Bet
properties which have direct or indirect
effects on animal metabolism, likely by
making modification of animal
metabolism in favor to increase their
positive performance (Valenzuela-
Grijalva et al., 2017). In addition, the use
of diets rich in natural antioxidants as a
means of eliminating excessive free
radicals from the animal’s body and then
alleviation of high-temperature negative
effects on animal production is becoming
popular (Li et al., 2018).
Blood Constituents
Hematological parameters
The results of erythorcytic parameters
(Table 3) showed highly significant
differences in control vs. treatments
comparison for RBC's (P≤0.01), Hb
(P≤0.001) and PCV (P≤0.01) values. The
RBR and Bet treatments have
significantly higher RBC's, Hb and PCV
values by 17.23, 8.04 and 8.28 %,
respectively compared to corresponding
values of control treatment. The results
found to be insignificant for the three
erythrocytes parameters between RBE
treatments and Bet treatments. In regard
to RBR vs. Bet comparison, showed
positive significant effect only on RBC's
(P≤0.001) and PCV % (P≤0.05) values, in
favor to dried RBR by 14.67 and 4.60 %,
respectively compared to Bet treatments.
The present results of leukocytes
parameters (Table 3) showed significant
differences in control vs. treatments
comparison for WBCs (P≤0.05), L
(P≤0.01), N (P≤0.01) and N/L ratio
(P≤0.01) values, while it is insignificant
in the other studied comparisons. The
RBR and Bet treatments have significant
higher WBC's and L values by 13.18 and
16.02 %, respectively and significant
lower N and N/L ratio values by 12.36
and 23.31 %, respectively compared to
corresponding values of control
treatment.
The hematological values obtained in the
present results across the treatments were
within the normal range for rabbit's blood
(NseAbasi Etim et al., 2014). Abd El-
Azeem et al. (2019) showed that RBCs,
Hb, Haematocrit, WBCs and L
parameters of NZW growing male rabbits
did not significant affected by different
dietary supplementation include Bet.
Blood biochemical parameters
The results of studied protein profile traits
(Table 4) showed significant differences
in control vs. treatments comparison for
only total protein (P≤0.01) value, while it
is insignificant in the other studied
comparisons for Al, GL and AL/GL ratio.
The RBR and Bet treatments have
significant higher total protein value by
9.16 % compared to corresponding value
of control treatment. In respect of Al, GL
and AL/GL ratio values, the results
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
showed insignificant differences within
all studied comparisons.
The values of plasma protein profile of
growing rabbits in the present study are
within the range of reference values
reported for healthy rabbits in previous
studies (NseAbasi Etim et al., 2014).
Hassan et al. (2011) found that serum
total protein and GL values were
significantly increased due to dietary Bet,
however AL value was not affected.
Kurchaeva et al. (2019) noted that total
protein was increased of growing rabbits
fed girasole beet pulp from 45 to 120
days, by 8.52 and 6.54%. However,
Abedo et al. (2012) found that blood total
protein of NZW rabbits was decreased
significantly with diets contained SBP
(25 or 50%). Also, the current results
were higher than the corresponding
values of Sara Sherif et al. (2019) who
reported slight lower protein profile
values (total protein, AL and GL) values
in their control groups for NZW rabbits at
14 weeks of age. While, Hayam Abo El-
Maaty et al. (2017) who observed that
feeding the SBT-containing diets did not
alter plasma concentrations of total
protein and AL of 12 weeks old NZW
rabbits compared with the control group.
But rabbits fed the diet containing the
highest level of SBT (30%) exhibited
significantly higher blood plasma level of
GL than that of their control counterparts.
In the present results of studied lipids
profile traits (Table 4) showed significant
differences in control vs. treatments
comparison for TL (TL, P≤0.05), Chol
(Chol, P≤0.05), TG (TG, P≤0.05), LDL
(P≤0.01) and HDL (P≤0.01) values. The
RBR and Bet treatments have significant
higher HDL value by 19.62 %, and
significant lower TL, Chol, TG and LDL
values by 9.09, 12.10, 10.27 and 19.10 %,
respectively compared to corresponding
values of control group. The results of all
of lipids profile traits showed
insignificant differences in other studied
comparisons (RBR 0.5% vs. RBR 1%,
Bet 0.1% vs. Bet 0.2% and RBR vs. Bet).
In general, the level of studied lipids
profile parameters are within the
corresponding reference values in
literature for healthy rabbits (Kaneko,
1989 and Belabbas et al., 2019).
However, the current results were higher
than the corresponding values of Sara
Sherif et al. (2019) who reported lower
TG (61.62 and 61.88 mg/dL ,
respectively), Chol (78.50 and 79.84
mg/dL, respectively) and HDL (24.93 and
28.11 mg/dL , respectively) values in
their control groups for NZW rabbits at
14 weeks of age.
The current lipid profile values are in line
with the finding of Abedo et al. (2012)
found that blood serum TG and Chol
values of NZW growing rabbits were
decreased (P≤0.01) with diets contained
SBP (25 or 50%). Oloruntola et al. (2016)
with rabbits, recorded reduction of serum
Chol level with diets containing 50 or 100
g/kg alchornea leaf meal. However,
Hayam Abo El-Maaty et al. (2018)
showed insignificant effects the plasma
concentrations of TL and Chol values in
examined rabbit fed SBT at levels 0.0, 20
or 30%.
While, Hassan et al. (2011) showed that
serum TL level of NZW growing male
rabbits fed 0, 250, 500, 750 and 1000 mg
Bet/kg diet treatments was significantly
increased due to dietary Bet (2.67, 3.22,
3.36, 3.40 and 3.29 mg/dL, respectively),
while Chol values was not affected
(ranged between 89.90 and 91.24 mg/dL).
The red beetroots phytochemicals
contained Saponins (Mroczek et al.,
2012), were linked to the reduction of
cholesterol uptake in the gut (Yilkal,
Aboelfadl M. A. et al.
2015). On the other hand, Bet has been
shown to regulate hepatic Chol
metabolism. Earlier studies reported
significant roles of Bet as improving
growth performance and fat metabolism
(Saeed et al., 2017).
The results of liver function indicators
(Table 5) showed significant differences
in control vs. treatments comparison for
AST (P≤0.01), ALT (P≤0.01) and ALP
(P≤0.05) activities. The RBR and Bet
treatments have significant higher ALP
activity by 16.20%, and significant lower
AST and ALT values by 17.04 and
18.85%, respectively compared to
corresponding activities of control group.
In respect of both level comparisons, the
effect was insignificant for all studied
indicators. However, the RBR vs. Bet
comparison showed highly significant
(P≤0.01) effect on only AST activity,
since rabbits fed RBR groups have lower
AST activity compared to those fed Bet
treatments (36.17 and 42.20 U/L,
respectively).
Abedo et al. (2012) found that liver ALT
and AST were insignificantly influenced
by feeding SBP diets (25 or 50%) of
NZW rabbits. Hayam Abo EL-Maaty et
al. (2018) concluded that NZW rabbits
fed SBT at different levels (0.0, 20 or
30%) in their diets did not alter plasma
concentrations of AST and ALT activities
at 12weeks of age. Hassan et al. (2011)
found that serum ALP level in the NZW
growing male rabbits fed 0, 250, 500, 750
and 1000 mg Bet/kg diet treatments were
significantly decreased due to dietary Bet
(22.50, 18.63, 16.00, 14.33 and 13.70
IU/l, , respectively). Compared to the
present results, the findings of Sara Sherif
et al. (2019) were higher for AST (52.10
and 65.10 U/l, respectively) and lower
ALT (12.65 and 15.69 U/l, respectively)
values in their control groups for NZW
rabbits at 14 weeks of age.
Serum enzymes activity (AST and ALT)
may be adversely affected by factors such
as muscular injury, rupture of organs,
nutritional status, physical activity,
hemolysis, treatment, and conservation of
plasma samples, and their levels in blood
can increase. These enzymes can be an
important diagnostic tool in veterinary
medicine (Harr, 2002).
The highly significant AST and ALT
enzyme activities found in the present
study (Table 4) could be indicate that the
Bet treatments (T4 and T5) of higher
AST and ALT values compared to both
beetroot treatments (T2 and T3) changed
tissue development and modifications of
studied rabbits as attributed by high
serum enzyme activity, as illustrated by
Moniello et al. (2005) in their study with
broiler chickens. On the other wards, the
Bet treatments increased the liver enzyme
activities while beetroot treatments
decrease them.
The results of kidney function indicators
(Table 5) showed highly significant
(P≤0.001) differences in control vs.
treatments comparison for creatinine
value, while it is insignificant for uric
acid value. The RBR and Bet treatments
have lower significant creatinine by 22.77
% and insignificant uric acid values
compared to corresponding values of
control group. In respect of both level
comparisons, the effect was insignificant
for both studied indicators. However, the
RBR vs. Bet comparison showed
significant effect (P≤0.05) on only
creatinine value, since rabbits fed Bet
treatments have significant lower
creatinine value compared to those fed
RBR treatments (0.74 and 0.82 mg/dL,
respectively).
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
The obtained creatinine and uric acid
values are in line with the findings of
Elwasife et al. (2015) with rabbits. The
present kidney indicators parameter
values are in line with the finding of
Hayam Abo EL-Maaty et al. (2018) who
showed that feeding SBT at levels 0.0, 20
or 30% to replace 50 or 75% of dietary
alfalfa hay did not alter plasma
concentrations of Urea (11.70, 11.73 and
11.63 g/dL, respectively), while
decreased significantly creatinine level in
SBT treatments (1.180, 1.007 and 1.002
mg/100 mL, respectively) of 12-week-old
NZW rabbits. The opposite trend was
found by Abedo et al. (2012) who
showed that blood serum uric acid values
were decreased significantly, while
creatinine values were insignificantly
influenced by feeding SBP diets (25 or
50%) of NZW rabbits.
Generally, the results reflect that the
rabbits fed different studied
supplementations have normal kidney
functions. However, Bet treatments were
more effective than dried RBR treatments
in reducing creatinine values of growing
rabbits.
Economic efficiency
The results of economic efficiency
indicated that the Alexandria growing
rabbit fed 0.5% dried RBR (T2) has
highest economic efficiency compared to
control, T3, T4 and T5 (140.50,
129.97,134.48, 136.10 and 128.40 % ,
respectively), as shown in Table 6. The
corresponding relative economic
efficiency to control value was 108.10,
103.47, 104.72 and 98.79%. These results
suggested the use of one of 0.5% dried
RBR, 1% dried RBR or 0.1% commercial
Bet supplementations in growing rabbit
diets during 4 and 9 weeks of age, with
positive effects on productive
performance. These results also, indicated
that the use of 0.5% dried red beetroots,
which are more available and cheaper,
has higher profitable economical effect
among all studied treatments. The Bet
improves energy efficiency, growth,
economic performance and carcass
quality (Chand et al., 2017). Yusuf et al.
(2018) showed that dietary organic Bet (0
, 1.5 and 3.0 g Bet/kg diet) Arbor Acre
Plus males from 21-42 days of age, Bet is
recommended in finishing male broilers
as production costs were reduced by
3.97–4.37% per kg, respectively. Shimaa
Amer (2018) showed that Bet can be
included in normal energy diets of broiler
chickens by level of 2g/kg diet for
improving the growth performance,
economic value and welfare during the
summer season. Awad (2019) who
indicated that the Cobb 500 broiler chicks
fed 0.75 kg Bet has higher economic
efficiency. CONCLUSION
It was concluded that the supplementation
of dried red beetroots powder and betaine
to the diet could improve growth
performance, lipid profile, liver and
kidney functions indicators in the blood
and economic efficiency of growing
rabbits. Nevertheless, the range for
optimal inclusion of dried red beetroots
0.5 kg/ 100 kg diet has been shown to
have a beneficial impact on the growth
and feed conversion ratio of growing
rabbits. Considering the vast
improvement in growth performance and
economic efficiency, the Inclusion of
dried red beetroots up to 0.5 % of total
diet is recommended.
ACKNOWLEDGEMENTS
The authors wish to thank "nucleus
breeding rabbit unit" of the Poultry
Research Center, Poultry Department,
Faculty of Agriculture, Alexandria
University, Egypt for providing the rabbit
Aboelfadl M. A. et al.
line and part of the laboratory tools,
chemicals and supervising the experiment. This research did not receive
any specific funding.
Table (1): The nutrition analysis of dried red beetroot used in the experiments.
Nutrients
Content
Protein (%)
16.6
Fat (%)
1.67
Fiber (%)
8.88
Ash (%)
17.54
Water (%)
8.47
Total Betalains (mg/100g)
249.76
Betacyanins(mg/100g)
154.72
Betaxanthins (mg/100g)
95.04
Table (2): Means ± standard error of performance traits of Alexandria growing rabbits
fed diets supplemented with different levels of dried red beetroots or commercial
betaine.
Performance Traits
Comparisons
Mortality
rate (%)
FCR
4-9 wk
FC
4-9 wk (g)
BWG
4-9 wk (g)
BW
at 9 wk (g)
6.67
3.02
3648.00
1208.20
1819.87
Control
Treatments
3.33
2.87
3760.58
1308.12
1917.17
0.041
0.010
0.001
0.001
0.003
P-value
*
*
***
***
**
Significance
3.33
2.86
3758.30
1314.00
1922.33
Beet root 0.5%
Beet root 1%
3.33
2.84
3772.90
1328.67
1936.00
0.481
0.753
0.636
0.644
0.735
P-value
NS
NS
NS
NS
NS
Significance
3.33
2.89
3733.00
1290.17
1900.67
Betaine 0.1%
Betaine 0.2%
3.33
2.91
3778.10
1299.63
1909.67
0.585
0.911
0.145
0.765
0.824
P-value
NS
NS
NS
NS
NS
Significance
3.33
2.85
3765.60
1321.33
1929.17
Beet root Betaine
3.33
2.90
3755.55
1294.90
1905.17
0.810
0.231
0.645
0.239
0.401
P-value
NS
NS
NS
NS
NS
Significance
0.20
0.05
20.99
0.239
27.66
SE Mean
Different letters (a-b) in the same column and comparison indicate significant differences (P≤ 0.05).*,
Significant at P≤ 0.05; **, Significant at P≤ 0.01; N.S, not significant.
BW, body weight; BWG, body weight gain; FC, feed consumption; FCR, feed conversion ratio.
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
Table (3): Means ± standard error of Hematological characteristics of Alexandria growing
rabbits fed diets supplemented with different levels of dried red beetroots or commercial
betaine.
Leukocytic parameters
Erythorcytic parameters
Comparisons
N/L
ratio
Neutrophils
(%)
Lymphocyte
(%)
WBC's
(103/cmm3)
PCV
(%)
Hb
(g/dL)
RBC's
(106/cmm3)
1.63
55.20
33.96
5.84
32.48
10.32
4.12
Control
Treatments
1.25
48.38
39.40
6.61
35.17
11.15
4.83
0.001
0.007
0.005
0.028
0.004
0.001
0.001
P-value
**
**
**
*
**
***
**
Significance
1.36
50.26
36.96
6.44
35.60
11.20
5.08
Beet root 0.5%
Beet root 1%
1.25
49.50
39.80
6.62
36.32
11.32
5.24
0.361
0.796
0.212
0.674
0.500
0.465
0.469
P-value
NS
NS
NS
NS
NS
NS
NS
Significance
1.24
48.00
38.90
6.50
33.78
11.02
4.49
Betaine 0.1%
Betaine 0.2%
1.10
45.76
41.96
6.90
34.98
11.06
4.51
0.288
0.449
0.180
0.429
0.265
0.806
1.000
P-value
NS
NS
NS
NS
NS
NS
NS
Significance
1.32
49.88
38.38
6.53
35.96
11.26
5.16
Beet root
Betaine
1.17
46.88
40.43
6.70
34.38
11.04
4.50
0.114
0.159
0.203
0.509
0.045
0.068
0.001
P-value
NS
NS
NS
NS
*
NS
***
Significance
0.09
1.98
1.50
0.29
0.71
0.10
0.15
SE Mean
Different letters (a-b) in the same column and comparison indicate significant differences (P≤ 0.05).*,
Significant at P≤ 0.05; **, Significant at P≤ 0.01; N.S, not significant.
RBCs, red blood cells; Hb, hemoglobin; PCV, packed cell volume; WBCs, white blood cells
differentiation; N/ L ratio, Neutrophils/ Lymphocyte ratio.
Aboelfadl M. A. et al.
Table (4): Means ± standard error of protein and lipids profile (mg/dl) of Alexandria growing
rabbits fed diets supplemented with different levels of dried red beetroots or commercial betaine.
Comparisons
Protein profile
Lipids profile (mg/dl)
TP
(g/dL)
AL
(g/dL)
GL
(g/dL)
AL/GL
ratio
TL
(mg/ dL)
Chol
(mg/ dL)
TG
(mg/ dL)
LDL
(mg/
dL)
HDL
(mg/ dL)
Control
Treatments
6.55
3.63
2.92
1.24
267.50
103.25
118.00
29.58
40.78
7.15
3.78
3.37
1.12
243.19
90.76
105.88
23.93
48.78
P-value
0.003
0.343
0.112
0.419
0.012
0.017
0.050
0.005
0.005
Significance
**
NS
NS
NS
*
*
*
**
**
Beet root 0.5%
Beet root 1%
7.24
3.88
3.36
1.15
239.50
91.00
105.75
21.58
51.03
7.27
3.95
3.32
1.19
235.25
83.75
100.75
23.88
49.73
P-value
0.881
0.722
0.906
0.904
0.700
0.235
0.497
0.308
0.682
Significance
NS
NS
NS
NS
NS
NS
NS
NS
NS
Betaine 0.1%
Betaine 0.2%
7.03
3.61
3.42
1.06
254.25
95.25
110.00
26.12
46.33
7.05
3.68
3.37
1.09
243.75
93.00
107.00
24.15
48.03
P-value
0.927
0.740
0.889
0.877
0.347
0.706
0.682
0.381
0.593
Significance
NS
NS
NS
NS
NS
NS
NS
NS
NS
Beet root
Betaine
7.25
3.91
3.34
1.17
237.38
87.38
103.25
22.73
50.38
7.04
3.65
3.40
1.07
249.00
94.13
108.50
25.13
47.18
P-value
0.183
0.078
0.815
0.499
0.149
0.124
0.318
0.140
0.166
Significance
NS
NS
NS
NS
NS
NS
NS
NS
NS
SE Mean
0.14
0.13
0.19
0.09
6.93
3.87
4.31
1.40
1.86
Different letters (a-b) in the same column and comparison indicate significant differences (P≤ 0.05).
*, Significant at P≤ 0.05; **, Significant at P≤ 0.01; N.S, not significant.
TP, total protein; AL, albumin; GL, globulin; AL/GL, Albumin/ Globulin; TL, total lipid; Chol,
cholesterol; TG, triglyceride; LDL, low density lipoprotein; HDL, high density lipoprotein.
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
Table (5): Means ± standard error of blood liver and kidney indicators of Alexandria
growing rabbits fed diets supplemented with different levels of dried red beetroots or
commercial betaine.
Comparisons
AST
(U/L)
ALT
(U/L)
ALP
(U/L)
Creatinine
(mg/dL)
Uric acid
(mg/dL)
Control
Treatments
47.24
29.81
95.00
1.01
3.02
39.19
24.19
110.39
0.78
2.84
P-value
0.002
0.006
0.011
0.000
0.410
Significance
**
**
*
***
NS
Beet root 0.5%
Beet root 1%
37.55
23.62
115.03
0.83
2.91
34.80
21.99
111.13
0.82
2.87
P-value
0.314
0.478
0.571
0.806
0.888
Significance
NS
NS
NS
NS
NS
Betaine 0.1%
Betaine 0.2%
42.36
25.22
107.30
0.74
2.82
42.03
25.94
108.10
0.75
2.77
P-value
0.904
0.751
0.907
0.883
0.851
Significance
NS
NS
NS
NS
NS
Beet root
Betaine
36.17
22.80
113.08
0.82
2.89
42.20
25.58
107.70
0.74
2.80
P-value
0.006
0.098
0.277
0.044
0.620
Significance
**
NS
NS
*
NS
SE Mean
1.70
0.87
2.44
0.03
0.08
Different letters (a-b) in the same column and comparison indicate significant differences (P≤
0.05). *, Significant at P≤ 0.05; **, Significant at P≤ 0.01; N.S, not significant.
AST, Aspartate Transaminase; ALT, Alanine aminotransferase; ALP, Alkaline phosphatase.
Table (6): Economic efficiency of the experimental Alexandria growing rabbits as affected by
different supplementations level of dried red beetroots or commercial betaine during 4 and 9
weeks of age.
Items
Experimental treatments
Cont
rol
Dried red beetroot
Commercial betaine
0.5kg/100Kg
(0.5%)
1 kg/100Kg
(1.0 %)
0.1 kg/100kg
0.1%
0.1 kg/100kg
0.2%
Feed
Total intake (kg/rabbit)
3.65
3.76
3.77
3.73
3.78
Price/kg (L.E)
4.80
4.90
5.00
4.94
5.08
Total feed cost (L.E)
17.52
18.42
18.85
18.43
19.20
Meat
Weight gain (kg/rabbit)
1.185
1.31
1.30
1.28
1.29
Price/kg (L.E)
34
34
34
34
34
Total Revenue (L.E)
40.29
44.30
44.20
43.52
43.86
Net Revenue (L.E)
22.77
25.88
25.35
25.09
24.66
Economic efficiency
129.97
140.50
134.48
136.10
128.40
Relative economic efficiency (%)
100
108.10
103.47
104.72
98.79
The price of red beetroot algae is about 24.0 LE, betaine is 140.0 LE in 2020.
Aboelfadl M. A. et al.
REFERENCES
Abd El-Azeem, A.; Ahmed, E.; Al-
Sagheer, A. A.; Daader, A. H.;
Bassiony, S. M. 2019. Effect of
dietary supplementation with betaine,
thyme oil and their mixtures on
productive performance of growing
rabbits. Zagazig Journal of
Agricultural Research, 46(3): 815-828.
Abd El-Moniem, E. A.; Daader, A. H.;
Al-Sagheer, A. A.; Gabr, H. A. 2016.
Effect of vitamin C, vitamin E or
betaine addition on alleviation of heat
stress impacts on growing
rabbits. Zagazig Journal Agriculture
Research. 43(5):1601-1613.
Abedo, A. A.; El-Badawi, A. Y.;
Hassan, A. A. 2012. Sugar beet pulp
as an energetic feed in growing rabbit
diets. Egyptian Journal Nutrition and
Feeds. 15(3): 513-522.
Aboul-Ela, S. S.; Reda, F. M. 2016.
Influence of partial and total
substitution yellow corn grains with
sugar beet pulp on growing rabbits
performance. Zagazig Journal
Agriculture Research. 4(6A).
Ashour, E. A.; Alagawany, M.; Reda,
F. M.; Abd El-Hack, M. E. 2014.
Effect of supplementation of Yucca
schidigera extract to growing rabbit
diets on growth performance, carcass
characteristics, serum biochemistry
and liver oxidative status. Asian
Journal of Animal Veterinary
Advanced. 9(11): 732-742.
Awad, M. A. 2019. Effects of betaine
chloride on performance,
physiological and carcass
characteristics in diet of broiler
chickens under the environmental
conditions of Egypt. Msc. Thesis,
Poultry production, Faculty of
Agriculture, Alexandria University.
Belabbas, R.; María de la Luz García;
Hacina Ainbaziz; Nadia Benali; Ali
Berbar, A.; Zoubeida Boumahdi;
María José Argente 2019. Growth
performances, carcass traits, meat
quality and blood metabolic
parameters in rabbits of local Algerian
population and synthetic line.
Veterinary World. 12: 55- 62
Chand, N.; Naz, S.; Maris, H.; Khan,
R. U.; Khan, S.; Qureshi, M. S.
2017. Effect of betaine
supplementation on the performance
and immune response of heat stressed
broilers. Pakistan Journal Zoology.
49(5): 1857-1862.
Duncan, D. B. 1955. Multiple Rang and
Multiple F-Test Biometrics. 11:1-42.
El-Raffa, A. M.; Youssef, Y. K.; Iraqi,
M. M.; Khalil, M. H.; García, M. L.;
Bselga, M. 2005. Developing rabbit
lines for meat production in Egypt and
Saudi Arabia: Overview, synthesizing
plan, descriptive performance and
future prospects. In Proc.: The 4th
International Conference on Rabbit
Production in hot climates. Genetics
Section N4. Sharm El-Sheik, Egypt,
24-27 February. ERSA.
El-Shinnawy, A. M. 2015. Effect of
betaine supplementation to methionine
adequate diet on growth performance,
carcass characteristics, some blood
parameters and economic efficiency of
broilers. Journal of Animal and
Poultry Production. 6(1): 27-41.
El-Taweel, A. A. F. 2010. Studies on
using sugar beet pulp in rabbit diets.
MSC. Thesis, Faculty of Agriculture,
Zagazig University, Egypt.
Elwasife, K.; Abdel Aziz, I.; Shabat,
M.; Shahwan, O.; El Hamidi, A.
2015. Effects of noise on rabbit’s
blood. European Journal Biophysics,
3(2): 10-13
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
Feldman, U.; Curdt, W.; Landi,
E.; Wilhelm, K. 2000. Identification
of spectral lines in the 500-1600 å wave
length range of highly ionized Ne, Na,
Mg, Ar, K, Ca, Ti, Cr, Mn, Fe, Co, and
Ni emitted by flares (Te ≥ × 106 K) and
their potential use in plasma
diagnostics. The Astrophysical
Journal, 544:508-521.
Figueroa, S.; Ciria, G.; Elisa, M.;
Valenzuela, S. 2018. Glycine betaine
rather than acting only as an osmolyte
also plays a role as regulator in cellular
metabolism. Biochimie. 147, 89–97.
doi: 10.1016/j.biochi.2018.01.002
Harr, K. E. 2002. Clinical chemistry of
companion avian species: A Review.
Veterinary Clinical Pathology. 31,
140-151
Hassan, R. A.; Ebeid, T. A.; Abd El-
Lateif, A. I.; Ismail, N. B. 2011.
Effect of dietary betaine
supplementation on growth, carcass
and immunity of New Zealand White
rabbits under high ambient
temperature. Livestock Science.
135:103–109
Hayam, M. A. Abo EL-Maaty; Sara
Kh. Sherif; Lina S. A. Foda 2017.
Efficiency of Utilization of Sugar Beet
Tops Hay and Prebiotic in Diets of
Growing Rabbits. Asian Journal of
Animal and Veterinary Advances, 12
(2): 71-79
Hayam, M. A. Abo El-Maaty; Sara Kh.
Sherif; Lina S. A. Foda 2018. Dietary
Sugar Beet Tops and Prebiotic Effect
on Nutrient Digestibility, Caecal
Activity and Organ Histology of
Weaning Rabbits. Journal Agriculture
Science. 10(3): 162-177
Hussein, A. S.; Al Ghurair, J.; John, P.
G. K. ; Habib, H. M.; Sulaiman, M.
2016. Graded levels of sugar syrup in
broiler rations and its effect on growth
performance and blood biochemical
parameters. Animal Nutrition, 3: 1-6
Kaneko, J. J. 1989. Clinical
biochemistry of domestic animals.
Academic Press, New York.
Kurchaeva, E. E., Vostroilov, A. V.;
Artemov, E. S.; Maksimov, I. V.
2019. Improvement of rabbit
productivity using probiotics and
herbal supplements. Conference on
Innovations in Agricultural and Rural
development. Earth and
Environmental Science. 341, 012051
doi:10.1088/1755-1315/341/1/012051
Lee, M. T.; Lin, W. C.; Lee, T.
T. 2017. Antioxidant capacity of
phytochemicals and their potential
effects on oxidatus status in animals:
A review. Asian-Australian Journal
Animal Science. 30(3): 299– 308
Li, S.; Zhao, M.; Jiang, T.; Lv, W.;
Gao, S.; Zhou, Y.; Miao Z. 2018.
Growth performance and antioxidant
status of growing rabbits fed on diets
supplemented with Eucommia
ulmoides leaves. World Rabbit
Science. 26: 35-41.
Moniello, G.; Bovera, F.; Solinas, I. L.;
Piccolo, G.; Pinna, W.; Nizza, A.
2005. Effect of age and blood
collection site on the metabolic profile
of Ostriches. South African Journal of
Animal Science, 35: 268-272
Mroczek, A.; Kapusta, I.; Janda, B.;
Janiszowska, W. 2012. Triterpene
saponin content in the roots of red beet
(Beta vulgaris L.) cultivars.
Agriculture Food Chemistry. 60(50):
12397-12402.
Nestora, S.; Merlier, F.; Prost, E.;
Haupt, K.; Rossi, C.; Tse, S. B. B.
2016. Solid-phase extraction of
betanin and isobetanin from beetroot
extracts using a dipicolinic acid
molecularly imprinted polymer.
Aboelfadl M. A. et al.
Journal Chromatography. A, 1465:47–
54
NRC 1994. National Research Council:
Nutrient requirements of poultry:
National Academies Press; 9th rev.
edn. National Academy Press,
Washington DC, USA.
NseAbasi, N. Etim; Mary, E. W.;
Akpabio, U.; Offiong, E. E. A. 2014.
Haematological parameters and factors
affecting their values. Agriculture
Science. 2: 37-47.
Oloruntola, O. D.; Ayodele, S. O.;
Agbede, J. O.; Oloruntola, D. A.;
Ogunsipe, M. H.; Omoniyi, I. S.
2016. Effect of Alchornea cordifolia
leaf meal and enzyme supplementation
on growth, haematological, immune
stimulatory and serum biochemical
response of rabbits. Asian Journal of
Life sciences, 5: 190-195.
Rabeh, N. M. 2015. Effect of red
beetroot (Beta vulgaris L.) and its
fresh juice against carbon tetrachloride
induced hepatotoxicity in rats. World
Applied Sciences Journal, 33(6): 931-
938.doi:10.5829/idosi.wasj.2015.33.06
.260
Ratriyanto, A.; Mosenthin, R.; Bauer,
E.; Eklund, M. 2009. Metabolic,
osmoregulatory and nutritional
functions of betaine in monogastric
animals. Asian-Australasian Journal of
Animal Sciences, 22(10): 1461-1476.
Riad, S. A.; Safaa, H. M.; Mohamed, F.
R.; Siam, S. S.; El-Minshawy, H. A.
2010. Influence of probiotic, prebiotic
and/or yeast supplementation in broiler
diets on the productivity, immune
response and slaughter traits. Journal
of Animal and Poultry
Production. 1(2): 45-60.
Saeed, M.; Babazadeh, D.; Naveed, M.;
Arain, M. A.; Hassan, F. U.; Chao,
S. 2017. Reconsidering betaine as a
natural anti-heat stress agent in poultry
industry: A review. Tropical Animal
Health Production. 49, 1329–1338.
Sakomura, N. K.; Barbosa, N. A. A.;
Longo, F. A.; Silva, E. P. da;
Bonato, M. A.; Fernandes, J. B. K.
2013. Effect of dietary betaine
supplementation on the performance,
carcass yield, and intestinal
morphometrics of broilers submitted to
heat stress. Brazilian Journal Poultry
Science. 15: 105-112.
Sara Kh. Sherif ; Fatma A. Elgohary;
Hayam A. Abo El-Maaty 2019.
Response to β-pro dietary
supplementation in growing rabbits
reared at different stocking densities
under hot environmental conditions.
Egypt Poultry Science Journal. 39(I):
133-151.
SAS 2004. SAS/STAT User's Guide.
Statistics, version 8. Cary, NC: SAS
Institute.
Shehata, S. A.; Bahgat, L. B. 2006.
Effect of sugar beet pulp and molasses
on growth performance of rabbits.
Zagazig Journal Agriculture Research.
33(5): 903-913
Shimaa, A. Amer; Anaam E. Omar;
Wafaa A. M. Mohamed; Heba S. A.
Gharib; Wafaa A. El-Eraky 2018.
Impact of betaine supplementation on
the growth performance, tonic
immobility, and some blood chemistry
of broiler chickens fed normal and low
energy diets during natural summer
stress. Zagazig Veterinary Journal.
46(1): 37-50.
Valenzuela-Grijalva, N. V.; Pinelli-
Saavedra, A.; Muhlia- Almazan, A.;
Domínguez-Díaz, D.; González-Ríos,
H. 2017. Dietary inclusion effects of
phytochemicals as growth promoters
in animal production. Journal Animal
Beetroots; Betaine; Productive performance; Lipid profile; Rabbits
Science Technology. 58: 8.
doi.org/10.1186/s40781-017-0133-9
Wang, Y. Z.; Xu, Z. R.; Feng, G. 2004.
The effect of betaine and DL-
methionine on growth performance
and carcass characteristics in meat
ducks. Animal Feed Science
Technology. 116: 151-159.
Xu, L.; Huang, D.; Hu, Q.; Wu, J.;
Wang, Y.; Feng, J. 2015. Betaine
alleviates hepatic lipid accumulation
via enhancing hepatic lipid export and
fatty acid oxidation in rats fed with a
high-fat diet. Brazilian Journal
Nutrition. 113, 1835–1843.
Yilkal, T. 2015. Important anti-
nutritional substances and inherent
toxicants of feeds. Food Science and
Quality Management. 36: 40-47
Yusuf, M. S.; El Nabtiti, A. A.; Marwa
A. Hassan; Mandour, M. A. 2018.
Supplementary outcomes of betaine on
economic and productive performance,
some biochemical parameters, and
lipoprotein lipase gene expression in
finishing male broilers. International
Journal of Veterinary Science and
Medicine, 6(2): 213–218.
: