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OPEN ACCESS Asian Journal of Animal and Veterinary Advances
ISSN 1683-9919
DOI: 10.3923/ajava.2017.31.37
Research Article
Effect of Varying Levels of Protein and Energy in Pre-stater Feeds
on Pectoralis Muscle Development of Kampung Super Chicks
(Gallus gallus gallus)
3U.E. Puspita, 1R.T. Utomo, 3A.B.I. Perdamaian, 3I. Lesmana, 3H. Arijuddin, 2Y. Erwanto, 3B.S. Daryono and
1H.T.S.G. Saragih
1Animal and Structure Laboratory, Faculty of Biology, Universitas Gadjah Mada, Jalan Teknika Selatan, Sekip Utara, Sleman,
55281 Yogyakarta, Indonesia
2Animal Product Technology Laboratory, Faculty of Animal Husbandry, Universitas Gadjah Mada, Jalan Fauna No. 3, Bulaksumur, Sleman,
55281 Yogyakarta, Indonesia
3Genetics and Breeding Laboratory, Faculty of Biology, Universitas Gadjah Mada, Jalan Teknika Selatan, Sekip Utara, Sleman,
55281 Yogyakarta, Indonesia
Abstract
Objectives: This study was performed to examine effect of varying level of protein and energy in pre-starter feed for 7 days old chicks
on pectoralis muscle development of kampung super chicks. Materials and Methods: Fourthy kampung super day old chicks were
fed pre-starter diet during the experimental period and were divided into four groups. The control group chicks were not fed for the first
3 days post-hatch and continued with a standard pre-starter diet to 7 days old. The second group was chicks with pre-starter type A diet
with 20.19% of protein and 3300 kcal kgG1 of Metabolism Energy (ME) for the first day post-hatch to 7 days old. The 3rd group was treated
with pre-starter diet type B for the first day post-hatch to 7 days old with protein level 21.84% and 3100 kcal kgG1 of ME and the last group
was given pre-starter diet type C with with protein level 21.13% and 2800 kcal kgG1 of ME for the first day post-hatch to 7 days post-hatch.
The parameters measured were body weight, pectoralis thoracicus weight, muscle area, cross-sectional area of myofibers and the number
of Proliferating Cell Nuclear Antigen (PCNA)-positive nuclei. The data were analyzed using one way ANOVA, followed by Tukey tests.
Results: The results showed that groups 4 had lower body weight, pectoralis thoracicus weight, muscle area, cross-sectional of myofibers
area and number of PCNA-positive nuclei compared to group 2 and 3 (p <0.05) which proved that early post-hatch feed in kampung super
chicks was important to body weight and pectoralis muscle development. Conclusion: It was concluded from the study that diet with
21.84% of protein and 3100 kcal kgG1 of ME in 7 days old chicks promised optimum performance and pectoralis muscle development for
kampung super chicks.
Key words: Kampung super chicks, muscle development, PCNA-positive nuclei, prestarter diet, protein and energy level, weight of pectoralis thoracicus
muscle
Received: October 10, 2016 Accepted: November 16, 2016 Published: December 15, 2016
Citation: U.E. Puspita, R.T. Utomo, A.B.I. Perdamaian, I. Lesmana, H. Arijuddin, Y. Erwanto, B.S. Daryono and H.T.S.G. Saragih, 2017. Effect of varying levels
of protein and energy in pre-stater feeds on pectoralis muscle development of kampung super chicks (
Gallus gallus gallus
). Asian J. Anim. Vet. Adv.,
12: 31-37.
Corresponding Author: H.T.S.G. Saragih, Animal and Structure Laboratory, Faculty of Biology, Universitas Gadjah Mada, Jalan Teknika Selatan, Sekip Utara,
Sleman, 55281 Yogyakarta, Indonesia
Copyright: © 2017 U.E. Puspita
et al
. This is an open access article distributed under the terms of the creative commons attribution License, which permits
unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.
Competing Interest: The authors have declared that no competing interest exists.
Data Availability: All relevant data are within the paper and its supporting information files.
Asian J. Anim. Vet. Adv., 12 (1): 31-37, 2017
INTRODUCTION
Early post-hatch feeding until the 14 days old which is
called pre-starter feeding on broiler chicks is known to have
significant effect on chicken development especially on body
mass gain, pectoralis muscle size and small intestine
development1-3. Protein and energy from the diet are essential
for chickens, including the pre-starter phase. Energy is needed
to maintain the body function while protein is needed for
tissue maintenance. Protein is needed for energy production
but the protein source on the other hand is relatively more
expensive because in some countries it has to be imported
fr o m o t he r c o un t ri es 4. As kn o wn o n b r oi l er , pr o te i n a n d e n er g y
necessity between temperate zone and tropical zone have
different values5. High energy formulated in broiler pre-starter
feed is leading to waste because the excessed energy will be
converted to extra deposition of fat. The proper nutrient
portion in the feed is important to ensure the maximum needs
of each nutrient6. The ratio between energy and protein for
broilers pre-starters is between 138-140. Furthermore, the
optimum feed formulation in Iran contained 2900 kcal kgG1
energy and 21% Crude Protein (CP) for broiler in pre-starter
period7.
Chicken muscle development is used as an indicator of
chicken meat quality. Pectoralis muscle is one of skeletal
muscle which is located on thorax. It is used as chicken
development parameter because it is reported contained low
fat and has lower rate of post-mortem acidification8.
Embryogenesis and post-hatch period are very crucial phase
in chicken development, including pectoralis muscle
development9, 10. Muscle development in avian species occurs
in 2 distinctive periods. Firstly, during the embryonic phase,
the myofiber number (MFN) is established when a large
number of precursor cells are committed to the expression of
muscle-specific genes. Secondly, during the post-hatch
period, the hypertrophy of the muscle occurs, mainly by
accretion of protein and nuclei resulted from the proliferation
and fusion of satellite cells11. New born chick skeletal muscle
growth did not show an increase in myofiber number but did
in myofiber size, which happened because DNA duplication
was not followed by cell division. The increase in DNA
coincident with myofiber growth occurs through the
donation of nuclei from the mitotically active satellite cells
population1,12, that lies between the myofiber basal lamina
and the sarcolemma13. Development of pectoralis muscle in
post-hatch phase needs appropriate nutrient portion in its
feed9,10, including an appropriate ratio between protein and
energy14.
Developing chicken using cross-breeding is now a trend
in Indonesia, between broiler or layer hen with local roaster for
instance, for the taste of Indonesian local chicken is still the
most favorite one. The advantage from this breeding is the
production of fast growing chicken with Indonesian local
chicken meat taste. The study of body weight of chicken
needs the informations about both the skeleton and muscle
development. Retnoaji
et al
.15 reported the osteogenesis of
hybrid chicken derived from crossbreeding between
Indonesian local chicken (Pelung) and broilers. But until
recently, no study on histological muscle development was
conducted.
Kampung super chicken or commonly called as "Kamper"
is one of the most desirable strain in chicken breeding.
Kampung super chicken is resulted from cross-breeding of
Lohman brown-type hen and Indonesian Pelung chicken. This
strain is started to be developed due to the high consumer
interest of local chicken meat but in opposite, its production
number decrease every year. This phenomenon is caused by
the low development rate of local chicken and the
reproduction rate of the hens is also low. Kampung super
chickens appearence is similar to Indonesian chicken but it
has higher gain mass rate. Kampung super chicken can reach
1 kg in weight on the 3rd month of nursing16.
The aim of this study was to investigate the effect of
different level of protein and energy in pre-starter feed on
pectoralis thoracicus muscle performance of kampung super
chicks.
MATERIALS AND METHODS
Birds and housing: All procedures involving animals were
approved by the Universitas Gadjah Mada, Indonesia
Institutional Animal Care and Use Committee. In conducting
the research, fourthy day old chicks were divided into four
groups. All chickens were housed with semi-intensive system
and kept under standard management conditions. Water was
provided
ad libitum
durin g the e xperime ntal period for
7 days.
Every group was fed by different type of feed. Type A feed
consisted of 21.84% protein and 3200 kcal kgG1 ME, type B
feed consisted of 20.19% protein and 3300 kcal kgG1 ME and
type C feed consisted of 21.13% protein and 2800 kcal kgG1.
The feed types were chosen by the ratio between ME and
protein which were higher, equal and lower than the
reference7.
Experimental design used, which were the offspring of
kampung super chicken were divided into 4 groups.
32
Asian J. Anim. Vet. Adv., 12 (1): 31-37, 2017
Fig. 1: Schematic of pectoralis thoracicus muscle which was
still attached to the bone. Samples of muscle were
taken by lateral cutting with dash orientation (----) then
histological process to count area of myofiber. Sign
solid orientation (-) was used to measure size of muscle
area and tissues cutting for counting area of myofiber17
Each group consisted of 10 DOCs. The first group was the
control group with no feed for the first 3 days post-hatch as
the control group to convinve that the pre-starter feed is
crucial for the weight gain and then it was continued with a
standard pre-starter diet to 7 days post-hatch, which was the
same feed as the type B feed. The type B feed was chosen for
the frist group for it had the middle ratio of protein and ME as
reported in the previous study7. Group 2 members were given
type A pre-starter feed for 7 days post-hatch. Group 3
members were given type B feed for 7 days post-hatch.
Group 4 members were given type C pre-starter feed for
7 days post-hatch. The feeds were provided
ad libitum
du ri ng
the experiment period. The DOCs weight were measured on
the 0, 3rd and 7th days old and then the left side of Pectoralis
Thoracicus (PT) was measured to observe the muscles weight
of PT and then the right side of PT was used to count the area
width of PT with ott-planimeter (Fig. 1).
Myofiber measurement: The myofiber diameter was
measured using micrometer software after histological
preparation done. The measurement was conducted by
counting 5 view area of fasciculus myofiber of every sample of
each group. The histological preparation process was done by
cutting the PT muscles into smaller pieces about 3×3 mm
wide and then fixated in neutral buffer formaline. After fixation
step, the next step was dehydration using alcohol ranging
from 70% to absolute alcohol. Clearing process or
dealcoholization was done using toluol. Afterward, infiltration
was conducted by using paraffin and the muscle samples are
embedded in paraffin blocks. Paraffin blocks then were cut
using rotary microtome with 5 mm of coupes thickness and
then affixed on microscope glass. The next step is
deparaffination and rehydration with xylene and alcohol18.
For immunohistochemical analysis pectoral muscle from
5 individuals was studied. The tissues were fixed in formalin
buffer saline solution embedded in Paraplast (Sigma Aldrich).
They were cut into transversal slices of 5 µm thickness using a
microtome (Leica RM 2265, Leica Microsystems). Tissue
sections were dewaxed with xylene and rehydrated.
Endogenous peroxidase was blocked with a 3% solution of
H2O2. Immunohistochemical analyses were performed using
EnVision+System-HRP (DAB) used for mouse primary
antibodies (Abcam) according to the procedures described by
the manufacturer. Proliferating nuclei cells were identified via
immunohistochemistry using monoclonal mouse antichicken
antibodies at a 1:100 dilution (Abcam) directed against PCNA.
The sections were incubated with the primary antibodies
for 1 h at room temperature and then incubated
with 3.3-diaminobenzidine (DAB)+substrate-chromogen
(DAKO kit), resulting in a brown-coloured precipitate at the
antigen site. The number of PCNA-positive nuclei was
estimated as PCNA-positive cells per 100 nuclei of myofiber.
Furthermore, the number of PCNA-positive nuclei per 100
nuclei of myofiber, within one fasciculus of muscle fibres was
counted, using cross sectional image of pectoral muscle19.
Data analysis: Data of chicken body weight, muscle weight of
PT, area of PT, myofiber area and PCNA-positive nuclei were
analyzed using oneway ANOVA and Tukey-test at significance
level of 5% in SPSS 13.0 software20.
RESULTS
Proximate test: The feed used in this study was pre-starter
feed which was given from post-hatch days until 7th days old.
The treatment was given with varying level of protein and
energy which was designed to accelerate DOCs growth in
7 days post-hatch. At the preliminary study conducted before,
proximate test and bomb calorimetry were done in the
certified laboratory in Animal Hu s ba n dr y Fa c ul t y o f Un i ve r si t as
33
Asian J. Anim. Vet. Adv., 12 (1): 31-37, 2017
Table 1: Proximate test between type A, B and C feed
Code Dry matter Ash Crude protein Crude fat Crude fiber Nitrogen free extract ME (kcal kgG1) Ratio energy: Crude protein
Type A 89.41 6.68 20.19 7.66 2.51 62.95 3300 163.44
Type B 94.42 5.60 21.84 5.48 3.81 63.26 3100 141.94
Type C 88.10 16.95 21.13 4.08 3.25 54.59 2800 132.51
ME: Metabolism energy
Table 2: Average body weight (gram) of kampung super chicks from post-hatch, 3 and 7 days post-hatch
Days N Starved Type A Type B Type C
0 8 32.6±0.6 33.6±0.67 32.0±0.95 32.8±0.73
3 8 28.0±0.44a34.8±0.86b35.2±0.8b31.8±0.73a
7 8 40.0±0.7a53.2±2b54.0±0.54b40.2±1.01a
a,bValues within rows without a common superscript are significantly different (p<0.05). Values are Mean±SE, N: Number of chicks, Type A: Kampung super chicks fed
20.19% protein diet and 3300 kcal kgG1 ME, Type B: Kampung super chicks fed 21.84% protein diet and 3100 kcal kgG1 ME, Type C: Kampung super chicks fed 21.13%
protein diet and 2800 kcal kgG1 ME
Table 3: Average of PT muscle weight (g), PT muscle area (cm2), fasciculus of myofiber area (µm2), area of myofiber (µm2) and PCNA-positive cells kampung super chicks
at 7 days post-hatch
Variables N Starved Type A Type B Type C
Muscle weight 5 0.49±0.06a1.02±0.1b1.15±0.02b0.36±0.02a
Muscle area 5 4.80±0.28a6.12±0.27b5.63±0.20b3.92±0.36a
Fasciculus of myofiber area 5 3036.00±91.96a9545.60±1.43b9737.30±86.9b2401.70±58.8a
Myofiber area 5 32.01±0.48a57.64±0.68b67.64±0.25b41.53±1.09a
PCNA-positive cells 5 0.63±0.02a0.78±0.02b0.79±0.02b0.68±0.01a
a,bValues within rows without a common superscript are significantly different (p<0.05). Values are Mean±SE, N: Number of chicks, Type A: Kampung super chicks fed
20.19% protein diet and 3300 kcal kgG1 ME, Type B: Kampung super chicks fed 21.84% protein diet and 3100 kcal kgG1 ME, Type C: Kampung super chicks fed 21.13%
protein diet and 2800 kcal kgG1 ME
Gadjah Mada (UGM) and Laboratory of Chemistry University
Center of UGM. The analysis (Table 1) showed the level of
protein and energy for type A feed was 20.19% and
3300 kcal kgG1, type B feed was 21.84% and 3100 kcal kgG1
and type C feed was 21.13% and 2800 kcal kgG1. The level of
protein and energy from each group was used to calculate the
ME-protein ratio. From the calculation it was shown that
type A had the highest ratio of ME-protein, type B was at the
middle and type C had the lowest ratio. From this calculation
result, use type B feed for the first group for it had the sam
ratio with optimal ratio of ME-protein reported in the previous
study7.
Body weight: Data on body weight performance during
different of treatment are presented in Table 2. The body
weight performance of kampung super chicks fed with type A
feed containing 20.19% CP and 3300 kcal kgG1 and type B feed
containing 21.84% CP and 3100 kcal kgG1 on the 3rd and
7th days olds was higher compared to type C feed containing
21.13% CP and 2800 kcal kgG1 and starved group (Table 2).
The result showed that pre-starter feed which was given from
day 0 had positive effect compared to the first group which
was delayed to access feed for 3 days.
Pectoralis muscle performance: Pectoralis muscle
performance data was obtained by measuring muscle weight,
muscle area, myofiber area and PCNA-positive cells (PCNA).
The data of pectoralis muscle performance on kampung
super DOCs (Table 3) and area of myofiber (Fig. 2) showed the
result of group 2 which was given with 21.84% protein and
3200 kcal kgG1 ME feed and group 3 containing 20.19% CP and
3300 kcal kgG1 ME feed were significantly different than
group 4 which was given with feed containing 21.13% CP and
2800 kcal kgG1 and the group 1 which was delayed to access
the fee for 3 days (p<0.05). It is shown that the feed which was
given from day 0 gave better effect on muscle performance
than the delayed feed.
DISCUSSION
The body weight in group 2 and 3 showed significant
difference compared to groups 1 and 4 since the proportion
of nutrients included the good ratios of protein and energy in
type A and type B feed. The results were in line with the data
that reported that in Asia, which is tropical zone, the
proportion value of protein and energy needed by broiler
chicken in starter phase7 is 138. Another study also stated that
the ideal ratio of energy and protein for 1-10 days old
broilers21 is 137. In addition, according to the body weight
gain data in type A and B feed groups, it could be explained
that chickens in early development have very high trypsin and
other protease enzymes. Therefore, the intestinal absorption
34
Asian J. Anim. Vet. Adv., 12 (1): 31-37, 2017
Fig. 2(a-d): Histological microscopy of myofiber area and PCNA-positive nuclei pectoralis muscle kampung super chicks,
(a) Control group, (b) Type A feed group, (c) Type B feed group and (d) Type C feed group. It is clearly showed that the
myofiber area, myonuclei (yellow arrow) and PCNA-positive nuclei (red arrow) of group B and C are larger and increase
than the control and type D groups. Magnification 40x100
of amino acids, in this case lysine is better in younger chicks
than the older ones. After they reach 3 weeks of age, the
digestive enzymes activities will decrease22,23. However, the
results of the present study did not agree with the previous
study which reported that the optimum performance for
broiler chickens at pre-starter phase with low ME and high CP
diets24.
It showed that type C, which has protein and energy of
21.13% and 2800 kcal kgG1 could not increase the body
weight of kampung super chicks
.
It might be caused by the
level of protein and energy was not balance so that the ratio
between protein level and energy was too high, which
became uneffective for body mass gain in chicks. High ratio
between protein and ME in chicken feed would cause low
mass gain because of the limited chicken ability to fulfill their
protein-energy needs25. The results were also in line with the
study which stated that feeding broilers with low CP feed
failed to support growth performance25.
Another study conducted by Van Emous
et al
.26 using
broilers chicks reported that the chicks which were fed with
the medium and low crude protein diet showed a higher feed
intake between days 18 and 27 and during the total growth
period, compared to the chicks which were fed with high
crude protein. Male broilers which were fed with low crude
protein had higher breast meat yield than male broilers which
were fed with high crude protein, while breast meat yield of
female broilers was not affected by dietary protein levels. This
experiment showed that a higher growth pattern during the
rearing period influenced the fertility, decreased embryonic
mortality and improved offspring performance in young
breeders, on the other hand decreasing the dietary protein
level did not affect those traits. The study of varying dietary
levels of energy and protein on Vanaraja chicken revealed that
feed containing 19 and 21% CP with 3000 kcal kgG1 ME
showed significantly higher body weight and FCR and it also
indicated better immune response against new castle
disease27.
35
(c)
(a) (b)
(d)
Asian J. Anim. Vet. Adv., 12 (1): 31-37, 2017
Body weight for starved group was lower than the
group 1 and 2. It showed that pre-starter feeding is important
to DOC development in the future
1,2. After the growth
response test, a surgery was conducted to measure PT muscle
performance, including muscle weight, muscle area width and
area of myofiber. The surgery was conducted after growth
response observation has been finished to confirm nutrient
absorption in the formation of muscle. Pectoralis muscle was
chosen because of its bigger mass compared to other
muscles. Pectoralis muscle development is commonly used as
an indicator of chicken husbandry success.
Performance of PT muscle was related to body weight
and it is indicated that formulation used in groups 2 and 3
induced muscle development rather than lipid deposition. It
was because the nutrient components in type A and type B
feeds were sufficient which could improve muscle
development during early age. The results were also in line
with the report which stated that the low protein and high
energy feed for broilers might influence the breast muscle
characteristic28. Post-hatch muscle development was
conducted by the increase of new nuclei number from
progenitor satellite cells of muscle in muscle fibers29. Good
proportion feed on this stage is very essential because the
stimulation of the proliferation of satellite cells, the
incorporation satellite into myofibers and muscle growth
highly occur on this stage30. Pectoralis muscle development
with type C feed treatment did not show positive result on
chickens growth. This was the result of incapability of nutrient
compositions in type C to improve the muscle development.
Unbalancing ratio between protein and energy in chicken
feed can disturb its muscle development14. The starved group
showed delayed pectoralis muscle development compared
to group 1 and 2. It proved that pre-starter feeding had
important effect to pectoralis muscle development19.
To understand molecular mechanism of increasing
number of muscles nuclei, proliferating cells were identified
by
immunohistochemistry methods, using antibodies directed
against proliferating cell nuclear antigen. Levels of PCNA are
excellent markers of cell proliferation state for analysis the
regulatory proteins cell cycle24. The PCNA-a protein molecule,
which is found in nucleus is involved in regulation of
polymerase delta (δ) and polymerase DNA. The peak
concentration of PCNA protein is observed in nucleus during
the interphase of cell cycle (G1, S, G2) and it is declining during
G0 phase and division of cells31.
The results showed increase of percentage of
PCNA-positive cells in chicken pectoralis muscle treated with
type A and B feed, indicating that bigger amount of muscle
cells were present within interphase. Myocytes are
multinuclear fibres, which result from fusion of myoblasts
being in the post-mitotic G1 phase31. The expression of PCNA
is a good marker of satellite cells, which are also precursors of
myofiber, into S phase of cell cycle30. Assuming that an
increase of PCNA-positive cells in the muscles reflects state
when more cells are involved in non-dividing structure of
myotubes, might be suggest improved balance between
hypertrophy to hyperplasia in chicken post-hatch30. The result
from this study revealed that the pre-starter feed which is
given from day 0 showed positive effect on pectoralis muscle
growth and performance and this is in line with the previous
study reported by Modziak
et al
.19.
CONCLUSION
Pre-starter feeding which contained 21.84% protein and
3100 kcal kgG1 metabolism energy fed from the 0 day of
post-hatch is recommended for the kampung super chicken
to support higher growth of pectoralis muscle.
ACKNOWLEDGMENTS
The authors gratefully acknowledge Agricultural Research
and Education Farm Land of Universitas Gadjah Mada
(KP4 UGM) for the permission of land use for chicken breeding.
This study was financially supported by Indonesian Institute of
Science in National Incentive for Research and Innovation
System 2015 (INSINAS LIPI 2015).
REFERENCES
1. Noy, Y. and D. Sklan, 1998. Metabolic responses to early
nutrition. J. Applied Poult. Res., 7: 437-451.
2. Noy, Y. and D. Sklan, 1999. Different types of early feeding
and performance in chicks and poults. J. Applied Poult. Res.,
8: 16-24.
3. Uni, Z., S. Ganot and D. Sklan, 1998. Posthatch development
of mucosal function in the broiler small intestine. Poult. Sci.,
77: 75-82.
4. Kamran, Z., M.A. Mirza, A.U. Haq and S. Mahmood, 2004. Effect
of decreasing dietary protein levels with optimum amino
acids profile on the performance of broilers. Pak. Vet. J.,
24: 165-168.
5. Hoffmann, L., 1987. [Effects of factors of nutrition and
husbandry on the heat production of rats and broilers.
1. Heat production of growing broiler chicks kept in
groups depending on the environmental temperature].
Arch. Tierernahr., 37: 191-213, ( In German).
36
Asian J. Anim. Vet. Adv., 12 (1): 31-37, 2017
6. Holsheimer, J.P. and W.M. Jenson, 1991. Limiting amino acids
in low protein maize-soybean meal diets fed to broiler chicks
from 3 to 7 weeks of age. Br. Poult. Sci., 32: 151-158.
7. Ganjali, H., A.R. Raji and H. Zarghi, 2015. Effect of post hatch
delayed access to feed on performance, GIT physical and
histological development and yolk absorption in young
broiler chicks. Biomed. Pharmacol. J., 8: 945-955.
8. Berri, C., E. Le Bihan-Duval, M. Debut, V. Sante-Lhoutellier and
E. Baeza
et al
., 2007. Consequence of muscle hypertrophy on
characteristics of Pectoralis major muscle and breast meat
quality of broiler chickens. J. Anim. Sci., 85: 2005-2011.
9. Zielinska, M.K., E. Sawosz, A. Chwalibog, T. Ostaszewska,
M. Kamaszewski, M. Grodzik and J. Skomial, 2010.
Nano-nutrition of chicken embryos. Effect of gold and taurine
nanoparticles on muscle development. J. Anim. Feed Sci.,
19: 277-285.
10. Zielinska, M.K., E. Sawosz, M. Grodzik, M. Wierzbicki and
M. Gromadka
et al
., 2011. Effect of heparan sulfate and
gold nanoparticles on muscle development during
embryogenesis. Int. J. Nanomedicine, 6: 3163-3172.
11. Christ, B. and B. Brand-Saberi, 2002. Limb muscle
development. Int. J. Dev. Biol., 46: 905-914.
12. Velleman, S.G., C.S. Coy and D.A. Emmerson, 2014. Effect of
the timing of posthatch feed restrictions on broiler breast
muscle development and muscle transcriptional regulatory
factor gene expression. Poult. Sci., 93: 1484-1494.
13. Moss, F.P. and C.P. Leblond, 1971. Satellite cells as the source
of nuclei in muscles of growing rats. Anatomical Record,
170: 421-435.
14. Marcu, A., I. Vacaru-Opris, G. Dumitrescu, A. Marcu and
L.P. Ciochina
et al
., 2013. Effect of diets with different energy
and protein levels on breast muscle characteristics at broiler
chickens. Anim. Sci. Biotechnol., 46: 333-340.
15. Retnoaji, B., R. Wulandari, L. Nurhidayat and B.S. Daryono,
2016. Osteogenesis study of hybrids of Indonesia's native
chicken pelung (
Gallus gallus domesticus
) with broiler
(
Gallus gallus>domesticus
). Asian J. Anim. Vet. Adv.,
11: 498-504.
16. Cahyono, B. and B. Samadi, 2007. The easy ways to raise
hybrid and crossbred chicken as livestock. Pustaka Mina.
Jakarta, pp: 1-6. (Indonesian Version).
17. Scheuermann, G.N., S.F. Bilgili, S. Tuzun and D.R. Mulvaney,
2004. Comparison of chicken genotypes: Myofiber number in
pectoralis muscle and myostatin ontogeny. Poult. Sci.,
83: 1404-1412.
18. Velleman, S.G., C.S. Coy, J.W. Anderson, R.A. Patterson and
K.E. Nestor, 2003. Effect of selection for growth rate and
inheritance on posthatch muscle development in turkeys.
Poult. Sci., 82: 1365-1372.
19. Mozdziak, P.E., T.J. Walsh and D.W. McCoy, 2002. The effect of
early posthatch nutrition on satellite cell mitotic activity.
Poult. Sci., 81: 1703-1708.
20. SPSS., 2006. SPSS 13.0 for Windows. SPSS Inc., Chicago.
21. Nukreaw, R. and C. Bunchasak, 2015. Effect of supplementing
synthetic amino acids in low-protein diet and subsequent
re-feeding on growth performance, serum lipid profile and
chemical body composition of broiler chickens. J. Poult. Sci.,
52: 127-136.
22. Beski, S.S.M., R.A. Swick and P.A. Iji, 2015. Specialized protein
products in broiler chicken nutrition: A review. Anim. Nutr.,
1: 47-53.
23. Zuprizal, 2008. Poultry feed industry in Indonesia:
Overview of the use of macronutrients protein feed. Inaugural
Speech Professorships Universitas Gadjah Mada Yogyakarta,
pp: 10-16. (Indonesian Cersion).
24. Sidadolog, J.P.H. and T. Yuwanta, 2009. Effect of
protein-energi concentration in feed on body weight gain,
energy and protein efficiency in the growth period of
merawang chicken. Anim. Prod., 11: 15-22.
25. Bregendahl, K., J.L. Sell and D.R. Zimmerman, 2002. Effect of
low-protein diets on growth performance and body
composition of broiler chicks. Poult. Sci., 81: 1156-1167.
26. Van Emous, R.A., R.P. Kwakkel, M.M. van Krimpen, H. van den
Brand and W.H. Hendriks, 2015. Effects of growth patterns
and dietary protein levels during rearing of broiler breeders
on fertility, hatchability, embryonic mortality and offspring
performance. Poult. Sci., 94: 681-691.
27. Perween, S., K. Kumar, Chandramoni, S. Kumar, P.K. Singh,
M. Kumar and A. Dey, 2016. Effect of feeding different dietary
levels of energy and protein on growth performance and
immune status of Vanaraja chicken in the tropic. Vet. World,
9: 893-899.
28. Uni, Z. and P. Ferket, 2004. Methods for early nutrition and
their potential. World Poult. Sci. J., 60: 101-111.
29. Johnson, S.E. and R.E. Allen, 1993. Proliferating cell nuclear
antigen (PCNA) is expressed in activated rat skeletal muscle
satellite cells. J. Cell Physiol., 154: 39-43.
30. Paunesku, T., S. Mittal, M. Protic, J. Oryhon, S.V. Korolev,
A. Joachimiak and G.E. Woloschak, 2001. Proliferating cell
nuclear antigen (PCNA): Ringmaster of the genome.
Int. J. Radiat. Biol., 77: 1007-1021.
31. Bischoff, R. and H. Holtzer, 1969. Mitosis and the processes
of differentiation of myogenic cells
in vitro
. J. Cell Biol.,
41: 188-200.
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