Applied Sciences

http://wjst.wu.ac.th https://doi.org/10.48048/wjst.2021.10522

Effect of Dietary Protein Level during Estrus Cycle:

Nutrient Digestibility, Quality of Embryo and Pregnancy Rate by
Embryo Transfer in Thai Crossbred Goats during Hot Season
Juggrid JUGSUMRIT1, Chalermpon YUANGKLANG2,*, Kraisit VASUPEN2,
Benya SAENMAHAYAK2 and Chantira WONGNEN3
1
Nakhonratchasima A.I and Biotechnology Research Center, Nakhon Ratchasima 30130, Thailand
2
Rajamagala University of Technology Isan, Nakhon Ratchasima Campus,
Nakhon Ratchasima 30000, Thailand
3
School of Agricultural Technology, Walailak University, Nakhon Si Thammarat 80160, Thailand

(*Corresponding Author’s e-mail: chayua@hotmail.com)

Received: 5 June 2020, Revised: 11 November 2020, Accepted: 22 December 2020

Abstract
Tis study aimed to evaluate the embryo quality and embryo transfer rate of Thai crossbred goats fed
different levels of protein in total mixed rations (TMR) during the hot season. Twenty-four non- pregnant
Thai crossbred goats with an average body weight of 26±5.9 kg were assigned with a random complete
block design (RCBD). Dietary treatments contained 8, 13, and 18 % crude protein (CP) in TMR. The
feeding trial lasted for 42 days. Does (female goat) were scheduled to determine embryo quality by
surgical laparotomy and flushing. At the end of the feeding trial, the digestion trial was conducted by the
total collection method for a 5-day period. The results showed that the average total feed intake and feed
conversion ratio did not differ among all treatments (p ˃ 0.05), however, digestible protein intake had
increased from 70.39, 79.77 to 89.11 g/d in 8, 13, and 18 % CP group, respectively. Increasing CP levels
in TMR resulted in linearly increased goat final body weight (30.25, 28.75, and 32.00 kg), weight gain
(3.00, 4.00, and 4.25 kg), and average daily gain (ADG) (87.84, 114.87 and 121.63 g/d). Embryo quality
(1, 1, and 3.5 morular follicle state) and pregnancy of embryo transfer rate (25, 25, and 50 %) of the
animal received CP level at 8 and 13 % less than that 18 %. These results indicated that dietary protein
level during program superovulation regimen affected the good quality of an embryo and the pregnancy
rate in an embryo transfer in Thai crossbred goats.
Keywords: Embryo, Goats, Nutrition, Pregnancy rate, Reproduction, Superovulation

Introduction
Goat farming is practiced worldwide, with goat products having a favorable image [1,2]. The
number of goats has increased globally, even in countries with high and intermediate incomes, despite
major changes in agriculture due to industrial mergers, globalization, and technological advances in
developed countries [3,4]. There are 30 million heads of cashmere goats around the world [5]. Goat
production is one of the key elements contributing to the economy of farmers living in the arid and semi-
arid regions. [6,7]. The most important goat breeding continents are Asia and Africa [8]. In developing
countries, 96 % of the milk and meat producing goat populations are found and 4 % are found in
developed countries [9]. Increasing meat production using scientific, accurate, and precise selective
programs are one of the most important goals for the genetic improvement of goats [10]. This can be done
by identifying the genetic reproductive and productive traits of animals [11-13]. Moreover, ruminant
production is primarily based on locally available feed resources. Goat production is one of the most

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popular ruminant animals due to its advantages in high reproductive performance and small land for
rearing. Goats are fed based on both natural forages and agricultural by-products. The does are small
ruminants which have a high potential to utilize low-quality roughage and can adjust well and consume
natural feedstuffs, most goats are raised in public fields alongside roads by smallholder farmers with an
average number of 26.3 head per household [14]. Thailand is located in the tropical region where high
temperature and high moisture contents can be met. Heat stress is well known to influence animal
production and reproduction. The heat stress demonstrates less the pregnancy rate in goats and has been
thought to be associated with early embryonic death. In vitro cultures have been more used for the
evaluation of effects of heat stress on oocytes, fertilization, preimplantation, and embryonic development
[15]. Nutrition is one of the most important and controllable management factors influencing
reproductions [16]. The effect of dietary protein on reproduction is complex, lacking protein intake
reduced reproductive performance [17]. More recently it has been found that reproductive performance
may be impaired if a protein is fed in amounts that greatly exceed the animal’s requirements. Over-
feeding of either as protein or urea has been associated with decreased pregnancy rates in female dairy
and beef cattle [18,19]. It appears that exposure to high levels of ammonia or urea may impair the
maturation of oocyte and subsequent fertilization or maturation of developing embryos. However,
supplying adequate energy for the excretion of excess ammonia or urea may prevent decreases in fertility
in dry cows or heifers [20]. Besides, not all studies have observed negative effects of elevated blood urea
nitrogen (BUN) concentrations on embryo quality or pregnancy rate [21]. Overfeeding protein during the
breeding season and early gestation, particularly if the ruminants receives an inadequate supply of energy
may be associated with decreased fertility [22]. This decrease fertility may result from decreased uterine
pH during the luteal phase of the estrous cycle in cattle fed high levels of degradable protein. The
interaction between nutrition and reproduction has long been known to have important implications for
reproductive performance [19].
The objectives of the present study were to investigate the effect of feeding diets that contained
different levels of crude protein (CP) during the estrus cycle on the quality embryos in program
superovulation of Thai crossbred goats and productive performance.

Materials and methods

Animal ethics
The experiment was performed under the ethical regulations of Rajmangala University of
Technology Isan. This study was conducted at the Rajamangala University of Technology Isan, Nakhon
Ratchasima, Thailand.

Animal management and experimental design

Twenty-four Thai crossbred goats with non-pregnant and pass 2nd cycling of estrus, approximately 2
- 4 years of age, with average body weight (BW) of 26±5.9 kg. All goats were kept in individual cages of
1×1.5 m2 and received the vaccine against foot and mouth disease (FMD), brucellosis test, and anti-
internal and external worm were injected to ensure the vitamin sufficiency and a worm-free condition,
respectively, before the experiment started. The animals were randomly assigned according to
Randomized Complete Block Design (RCBD) with 4 blocks (initial body weight and age). The feeding
trial lasted for 42 days and 15 days of an adjustment period.

Experimental feed and feeding

Dietary treatments were the different levels of CP content in TMR, which were 8, 13, and 18 % CP,
Feed ingredients of experimental are presented in Table 1. Goats were ad libitum fed twice daily at 08.00
and 16.00 and clean water was freely accessed. Feed refusals were measured and sampled daily at 07.30
on the next day.
At the end of the experimental period, all animals were used for a digestibility trial that was
conducted using the total collection method for a 5-day period. Feeds, feed refusals, and feces were
weighed and then 10 % of feed refusals and feces were sub-sampled each day. Composites of feeds, feed

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refusals, and feces were sub-sampled approximately 500 g from each goat. Samples were dried at 65 ºC
for 24 h and ground to pass a 1 mm screen using Wiley mill. The samples were stored at −21 ºC pending
further chemical analysis. The proximate chemical composition of feeds, feed refusals, and feces samples
contents of feeds were analyzed by a method described by AOAC [23].
The does were initially weighed at the beginning of the experiment and weighed monthly
throughout the experimental period. At the end of the experimental period, the average weight of the
individual animal was also recorded.

Table 1 Composition of concentrate in total mixed rations used in the experiment.

Protein level (%)

Ingredients
8 13 18
Corn silage 40 40 40
Soybean meal 1.20 8.40 15.00
Cassava chip 33.60 28.20 20.40
Corn meal 7.20 6.00 6.00
Rice bran 7.20 6.00 6.00
Dried Brewers grains 7.20 8.70 9.00
Urea 0.60 0.90 1.80
Molasses 2.40 1.20 1.20
Salt 0.18 0.18 0.18
Sulfur 0.30 0.30 0.30
Premix 0.12 0.12 0.12
Total 100 100 100
Metabolizable energy (Mcal) 2.62 2.65 2.64

Program of superovulation and synchronization

After the feeding trial experiment, goats were induced into superovulation and synchronized estrus
using 1 protocol for each of the 3 treatments. Twelve goats to select the method applied for
superovulation (donor) and twelve goats to select the method applied for synchronization (recipient). In
the donor group, the controlled internal drug release device, CIDR-G (EAZI-Breed TM CIDR®, Pfizer,
Auckland, New Zealand) containing 0.3 g progesterone was used as the intravaginal progesterone
delivery system. Day 0 was designated as the day of CIDR-G insertion and concurrently 125 μg
cloprostenol (Estroplan®, Parnell Laboratories (AUST) Pty. Ltd., Alexandria, NSW, Australia) was
administered intramuscularly, inserted with CIDR-G for 12 days, then injected intramuscularly with FSH
120 IU twice daily (6, 5 and 4 mg per injection on day 9, 10 and 11, respectively), injected prostaglandin
F2α (PG) 125 ug, GnRH 150 IU, removed CIDR-G on d 12 and inseminated with frozen semen TAI at 48,
56 and 72 h after CIDR-G removal. All treated animals were exposed to vasectomized bucks 1 day before
CIDR-G removal to stimulate estrus. Laparotomy surgery after TAI on d 7. In the recipient group, the
does were administered with control intravaginal drug release (CIDR-G) for 12 days, injected PG 125 ug,
GnRH 150 IU, and removed CIDR-G on d 12. Laparotomy surgery was performed after estrus on d 7.

Data collection and analysis

Blood samples were collected on the morning of estrus via jugular venipuncture into an EDTA
solution, then immediately centrifuged at 1,500×g for 15 min. Blood plasma samples were harvested and
frozen stored at −20 ºC until assayed of blood urea nitrogen (BUN). Laparotomy surgery was conducted
after TAI on d 9. Goats were injected with 0.075 mg xylazine (Rompun®; L.B.S. Laboratory, Thailand)
and 100 mg ketamine hydrochloride (Ketaset®; Wyeth Animal Health, Canada), and the embryo was
collected and evaluated. After laparotomy was performed, the number of corpus luteam (CL) on each

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ovary was recorded. Each embryo was then flushing and evaluated based on morphology and categorized
as good or poor quality as previously described by [24]. After the end of the embryo transfer, all animals
have used ultrasound scanning at 45 days recheck pregnancy rate in goats.

Statistical analysis
All obtained data were subjected to the Analysis of Variance (ANOVA) according to an RCBD
design. Means were statistically compared using LSD and orthogonal polynomial. The statistical model
was:

Yij =µ +βi +τj +Ɛij

Where Yij was observed variable, µ was the overall mean, βi was the random effect of the ith block, τi was
the fixed effect of the jth treatment (i = 1, 2, 3) and Ɛijk was the residual error.

Results and discussion

Chemical composition of experimental total mixed rations
All experimental diets were provided a similar amount of DM, OM, EE, CP, and Ash to all
treatments (Table 2). As expected, crude protein contents of dietary treatments varied with treatment. In
this study, the diet component was placed to the level at 60:40 of concentrate: forage ratio following the
reports of [25], who found that this ratio significantly improved feed utilization by goats. Intake of dietary
of protein level affected growth performance, in term of final weight in goats. As reported by [26], who
studied the effect of dietary protein level in TMR at 14, 16, 18, and 20 % CP on growth performance of
Korean black goat. The result found that growth performance in Korean black goats was improved by 18
% CP.

Table 2 Chemical composition of dietary protein levels.

Protein levels (%)

Chemical composition
8 13 18
DM 50.48 51.29 50.93
----------------% (DM)--------------------
OM 94.05 93.30 93.55
CP 8.81 13.97 18.29
EE 3.40 3.40 3.28
NDF 37.03 41.21 45.28
ADF 27.10 26.91 27.24
Ash 5.95 6.70 6.45

Effect of dietary protein level on feed intake and growth characteristics of goats
The effects of CP level in TMR on body weight gain, growth performance characteristics, and dry
matter intake of Thai crossbred goats are presented in Table 3. The average daily gain (ADG) of all
treatment was varied from 87.84 to 121.63 g during the experimental period. Dry matter intake (DM) of
13 and 18 % CP (4.00 and 4.25 %BW) were higher than 8 % CP group (3.00 %BW) but did not
significantly differ (p > 0.05) by dietary protein levels in TMR. The result of this study was consistent to
the report of [27], who found that there was no effect of different levels of CP in diets on DMI of either
Boer-Spanish crossbred or Spanish kids. This was, however, in contrast to the report of [28], who found
that increasing dietary levels of CP in diet had increased levels of DMI. It is possible that the difference in
feed ingredients and animal breed resulted in this dissimilarity. As expected, increased levels of dietary

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protein level in TMR resulted in significantly increased CPI and digestible crude protein intake (DCPI) of
the animals. Increasing CP levels in TMR (8, 13, and 18 %) led to a linearly increased goat’s final body
weight and ADG. Growth performances of Thai indigenous goats from this study are consistent with the
performance of goats reported by [29], who reported that Saanen kids fed the minimum dietary CP levels
had the lowest ADG and the ADG significantly increased when the kids fed diets with higher levels of CP
diets. Furthermore, [30] reported that both Thai indigenous and crossbred kids received more CP resulted
in higher growth rates. Similarly, [31] found that the significant responses of final body weight, weight
gain, and ADG of Thai indigenous x Anglo-Nubian crossbred to increasing levels of dietary CP linearly.
This finding indicated that Thai indigenous goat responded well to the amount of CP intake.

Table 3 Effect of dietary protein levels on intake and growth characteristics of goats.

Protein Levels (%) Contrast

Item SEM
8 13 18 Linear Quadratic
Initial weight (Kg) 27.00 24.50 27.00
Final weight (Kg) 30.25 28.75 32.00
ADG, g/d 87.84c 114.87b 121.63a 2.12 * *
FCR 10.94 10.31 10.92 0.67 ns ns
Feed intake,
g DM/d 944 1,165 1,309 137.38 ns ns
% BW 3.00 4.00 4.25 0.46 ns ns
g/kgBW0.75 72.76 95.25 94.88 9.34 ns ns
a,b,c
Mean with different superscript within the same row are statistically different (p < 0.05), SEM =
standard error of the means, ns = non-significant (p ˃ 0.05), * = p < 0.05

Nutrients digestibility
Nutrients digestibility of dietary treatments in Thai crossbred goats is shown in Table 4. DM, OM,
and ADF digestibility of 18 % CP (78.07, 80.45 and 54.19 %, respectively) were highest, however, those
were not significantly different (p > 0.05) goats from 8 % (72.02, 73.51 and 45.37 %, respectively) and 13
% CP group (71.33, 73.80 and 41.55 %, respectively). Moreover, CP and NDF digestibility was
significantly affected (p < 0.05) by dietary protein levels, with quadratically increased (p < 0.01)
according to increase inclusion levels of CP in TMR. Protein and NDF utilization levels increased due to
improvement in the efficiency of microbial capture of the available N supply. Our finding was consistent
with the report of [29]. These authors found that goats fed with diet ad libitum (54.2 g/BW0.75/d, DMI)
had CP digestibility of 80.8 %, and the CP digestibility was significantly decreased when the goats were
fed with a lower amount of feed or CP. This study was consistent with the report of [28], who reported
that Saanen kids with diet CP levels ad libitum had CP digestibility of 80.8 % and the CP digestibility
was significantly decreased when the goats were fed with a lower amount of feed or CP. NDF
digestibility was improved (p < 0.05) in goats fed 18 % CP compared with goats fed 8.0 and 13 % CP. It
implied that more protein available for microbial growth in the rumen, enhancing the degradation of
nutrients including fiber content. The data from [32] reported that microbial growth is strongly positively
related to voluntary feed intake, increasing the level of feed intake increased the digestible of organic
matter in the rumen and supplied more nutrients for microbial crude protein synthesis (MCP). The
literature states that the most microbial population in the rumen are fibrolytic and have the high
proteolytic capacity [33], then improved CP and NDF digestibility in the high protein diet group.

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Table 4 Nutrient digestibility (%) of different levels of crude protein in total mixed rations.

Protein Level (%) SEM Contrast

Items
8 13 18 Linear Quadratic
Dry matter 72.02 71.33 78.07 2.61 ns ns
Organic matter 73.51 73.80 80.45 2.55 ns ns
Crude protein 70.39 c 79.77 b 89.11 a 2.37 ** **
Ether extract 83.70 79.35 85.11 2.57 ns ns
NDF 51.08 b 48.89 b 61.60 a 1.93 ns **
ADF 45.37 41.55 54.19 4.43 ns ns
a,b,c
Mean with different superscript within the same row are significantly differed (p < 0.05), SEM =
standard error of the means, ns = non-significant (p ˃ 0.05), ** = p < 0.01
NDF = neutral detergent fiber; ADF = acid detergent fiber

Table 5 Effect of dietary protein level on pH, ammonia nitrogen (NH3-N), and blood urea nitrogen
(BUN) concentration.

Protein level (%) Contrast

Items SEM
8 13 18 Linear Quadratic
pH
0h 7.16 6.96 7.00 0.10 ns ns
2h 6.79 6.46 6.61 0.13 ns ns
4h 6.79 6.57 6.81 0.14 ns ns
Mean 6.91 6.66 6.81 0.11 ns ns
NH3 N (mg%)
0h 6.58 c 7.58 b 9.18 a 0.15 * *
2h 9.77 12.57 14.68 1.27 ns ns
4h 8.12 9.15 8.51 0.39 ns ns
Mean 8.16 b 9.77 ab 10.79 a 0.39 * *
BUN (mg%)
0h 4.00 c 9.50 b 15.50 a 1.07 ** **
2h 6.25 b 13.50 a 19.25 a 1.82 ** **
4h 5.25 c 12.50 b 19.75 a 1.67 ** **
Mean 5.17 c 11.83 b 18.16 a 1.48 ** **
a,b,c
Mean with different superscript within the same row are statistically different (p < 0.05), SEM =
standard error of the means, ns = non-significant (p ˃ 0.05), * = p < 0.05, ** = p < 0.01

Ruminal pH, NH3-N, and BUN

The result of blood metabolization was shown in Table 5, pH in rumen fermentation was not
significantly different between the treatments (6.91, 6.66, and 6.81, respectively). Rumen pH values were
within the physiological range of 6.6 - 7.1 which had no negative effect on bacterial growth. As same as
with BUN, BUN concentrations in this study were in the normal level according to [1], the normal level
of BUN concentration was 10 - 20 mg/dl. However, NH3-N in rumen fermentation metabolites (8.16,
9.77, and 10.79, respectively, p < 0.05) and BUN (5.17, 11.83 and 18.16 mg%, respectively, p < 0.01)
had increased gradually after feeding on 0, 2, and 4 h, and quadratically increased with increasing levels
of CP in the diets. The higher level of NH3-N and BUN in the high protein diet group would relate to
protein degradation in the rumen which is the main reason for the efficient protein utilization in
ruminants. Ammonia-nitrogen is the major products of protein degradation in the rumen that are crucial

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for microbial growth and minor rates of ruminal degradation improved efficiency of MCP synthesis due
to the better holding of releasing N by rumen microbes [32]. However, it is proposed that the capture of
rumen degradable protein is not completed, when the ammonia amount is large due to the extensive
degradation of the proteins, the surplus of ammonia is absorbed through the lining of the tract. Later, it is
turned into urea in the liver, to reduce its toxicity to the animal, and lead high amount of BUN. The BUN
may be recycled to the rumen as non-protein nitrogen [33] and leading to a higher level of NH3-N prior
feeding of high CP group (9.18 mg%) than others (6.58 and 7.58 mg%, respectively).

Effect of dietary protein level on pregnancy rate in embryo transfer and quality of an embryo
Laparotomy of the donor was performed at d 7 after AI, then the number of embryos and CL were
recorded. The mean recovery of an embryo in donors fed different protein levels of 8, 13, and 18 % were
10, 5, and 10.25, respectively (p > 0.05). The embryo quality was evaluated by using state of embryo in
goats receiving protein level at 18 % and was significantly higher (p < 0.05) than the goats fed protein
level at 8 % and 13 % as shown in Table 6. In recipients, the result of number (6, 5, and 6, respectively)
and the pregnancy rate in embryo transfer in fed high levels of protein (50 %) were higher than the lower
groups (25 and 25 %, respectively). In females of small ruminant species, nutritional supplementation
stimulates envelopment of the small follicle population [31], growth rate and size of the ovulatory follicle
[34], ovulation rate [35], and litter size [36]. In this research, results belonging to CP level and utilization
in diets, in ruminants, low protein diets resulted in low BUN, whereas high BUN was associated with
high protein diets or excessive protein breakdown. Inadequate protein intake showed a lower BUN
concentration and negative effect on conception rate, fetal reabsorptions, premature parturition, and weak
offspring [37], however, exceeds BUN concentrations has been negatively associated with reduced
conception rates and increased early embryonic death. The effects of urea on embryo quality are likely to
be due to alterations in the oviduct environment or deleterious changes in the follicle, rather than changes
in the uterine environment [38,39]. Depending upon protein quality and composition, serum
concentrations of progesterone may be lowered, the uterine environment altered, and fertility decreased
[40].

Table 6 Effect of dietary protein levels on pregnancy rate in embryo transfer and quality of an embryo.

Protein level (%) Contrast

Item SEM
8 13 18 Linear Quadratic
Donor (n) 4 4 4
Number of CL (n) 10.00 5.00 10.25 1.80 ns ns
Quality of embryos (donor)
Unfertilized Ovum (UFO, n) 7.00 2.75 2.50 1.93 ns ns
Degenerated (n) 1.25 0.75 1.25 0.47 ns ns
Morula 1.00 b 1.00 b 3.50 a 0.55 ns *
Blastocyst 0.75 0.50 3.00 0.84 ns ns
Recipient (n) 4 4 4
Number of total CL (n) 6 5 6
Pregnancy recipient (n) 1 1 2
a,b
Mean with different superscript within the same row are statistically different (p < 0.05), SEM =
standard error of the means, ns = non-significant (p ˃ 0.05), * = p < 0.05

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Conclusions
Average total feed intake was not different, while ADG was significantly different fed level protein
group. However, the fed level 18 % protein-induced compensatory growth on embryo quality, follicular
development greater than 8 and 13 % group. Thus, the results indicated that reproductive management in
pubertal and pre-gestation periods using the different fed level protein regimen affected fertility
improvement in Thai-native crossbreed goats.

Acknowledgments
The authors would like to thank Nakhon Ratchasima A.I. and Biotechnology Research Center and
Nakhon Ratchasima E.T center, and staff members of HHU Phakchong Nakhon Ratchasima. We would
also like to express our sincere thanks to the Rajamagala University of Technology Isan for facilities
support.

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