Journal of Applied Animal Research
ISSN: 0971-2119 (Print) 0974-1844 (Online) Journal homepage: https://www.tandfonline.com/loi/taar20
The dietary valine requirement for rainbow trout,
Oncorhynchus mykiss, can be estimated by plasma
free valine and ammonia concentrations after
dorsal aorta cannulation
Jun-Young Bae , Gunhyun Park , Hyeonho Yun , Silas S.O. Hung & Sungchul C.
Bai
To cite this article: Jun-Young Bae , Gunhyun Park , Hyeonho Yun , Silas S.O. Hung & Sungchul
C. Bai (2012) The dietary valine requirement for rainbow trout, Oncorhynchus�mykiss, can be
estimated by plasma free valine and ammonia concentrations after dorsal aorta cannulation,
Journal of Applied Animal Research, 40:1, 73-79, DOI: 10.1080/09712119.2011.628395
To link to this article: https://doi.org/10.1080/09712119.2011.628395
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Journal of Applied Animal Research,
Vol. 40, No. 1, March 2012, 7379
The dietary valine requirement for rainbow trout, Oncorhynchus mykiss, can be estimated by
plasma free valine and ammonia concentrations after dorsal aorta cannulation
Jun-Young Baea, Gunhyun Parka, Hyeonho Yuna, Silas S.O. Hungb and Sungchul C. Baia*
a
Department of Marine Bio-materials and Aquaculture/Feeds and Foods Nutrition Research Center, Pukyong National
University, Busan, Korea; bDepartment of Animal Science, University of California, Davis, CA, USA
(Received 26 July 2011; final version received 27 September 2011)
This study was carried out to evaluate the dietary valine requirement by measuring means of the plasma free
valine and ammonia concentrations in rainbow trout, Oncorhynchus mykiss, after dorsal aorta cannulation. A
total of 35 fish averaging 49897.2 g (initial body weight, mean9SD) were randomly distributed into seven
groups with five fish in each group. After 48 h of feed deprivation, each group was fed one of seven L-amino acid
based diets containing graded levels of valine (0.45, 0.95, 1.20, 1.45, 1.70, 1.95 or 2.45% of diet, dry matter basis)
by intubation at 1% body weight. Blood samples were taken at 0, 5 and 24 h after intubation. Post-prandial
plasma free valine concentrations (PPval, 5 h after intubation) and post-absorptive free valine concentrations
(PAval, 24 h after intubation) of fish fed diets containing 1.45% or more valine were significantly higher than
those of fish fed diets containing 1.20% or less valine (PB0.05). Post-prandial plasma ammonia concentrations
(PPA, 5 h after intubation) remained low or constant from fish fed diets containing 0.451.45% valine, but
increased linearly from fish fed diets containing 1.452.45% valine. Post-absorptive plasma ammonia
concentrations in the present study were not significantly different among the groups. Broken-line model
analyses on PPval, PAval and PPA indicated that the dietary valine requirements of rainbow trout was between
1.41 (3.85) and 1.50% (4.10) of diet (% of dietary protein on a dry matter basis).
Keywords: valine; rainbow trout; plasma; ammonia; dorsal aorta cannulation
1. Introduction
Valine is a branched-chain amino acid along with
isoleucine and leucine, which are not synthesised in
animals; so it must be ingested, usually as valine or
valine containing proteins. Valine plays very important roles in certain biochemical reactions and in the
growth of monogastric and preruminant terrestrial
animals. It is involved in protein synthesis, synthesis
of the amine neurotransmitters serotonin and the
catecholamines dopamine and norepinephrine, which
are derived from the aromatic amino acids tryptophan, phenylalanine, and tyrosine, the production of
energy and the compartmentalisation of glutamate
(Fernstrom 2005). Valine deficiency resulted in poor
feed conversion and growth recession in some fish
species such as catla, Catla catla (Ravi and Devaraj
1991), milkfish, Chanos chanos (Borlongan and
Coloso 1993) and Indian major carp, Labeo rohita
(Murthy and Varghese 1997). So, it is important to
determine the valine requirements of cultured fish
species for normal growth and feed utilisation. Dietary valine requirements have been estimated for
commonly cultured species of fish, and wide variations of 2.54.0% of dietary protein have been
reported (Wilson 2002).
*Corresponding author. Email: scbai@pknu.ac.kr
ISSN 0971-2119 print/ISSN 0974-1844 online
# 2012 Taylor & Francis
http://dx.doi.org/10.1080/09712119.2011.628395
http://www.tandfonline.com
The above requirements were determined by
feeding trials. Feeding trials are expensive and last
for several weeks or months before appreciable
responses are observed. Determination of amino
acid requirements by measuring plasma amino acid
and ammonia concentrations on the other hand lasts
for just a week, with insignificant labour and material
costs. This method has been employed in several
species and results are similar to those obtained by
feeding trials (Cowey 1995; Ok 2002). Hence, it is
advisable that this procedure be confirmed in important species so that they could be employed in
determination of yet undetermined amino acid or
other nutrient requirements in those species.
Plasma free amino acid (PFAA) concentrations
were used to investigate amino acid metabolism and
to evaluate the quality of dietary protein in rainbow
trout, Oncorhynchus mykiss (Nose 1972; Walton and
Wilson 1986; Schuhmacher et al. 1997), carp,
Cyprinus carpio (Plakas et al. 1980; Dabrowski
1982) and Atlantic salmon, Salmo salar (Espe et al.
1993; Sunde et al. 2003). Evaluation of PFAA
concentrations has led to the discovery of genetic
defects of amino acid metabolism as a result of
primary renal or liver disease and the effects of amino
74
J.-Y. Bae et al.
acid deficiencies, imbalances and toxicities on amino
acid metabolism (Park et al. 2005). The relationships
between the concentration of PFAA and intake of
dietary amino acids have been investigated by several
researchers (Plakas et al. 1980; Murai et al. 1987; Bai
et al. 2003). PFAA of fish fed graded levels of the
amino acid tested has been used in several experiments in an attempt to confirm requirement values
assessed by growth. Although the effects of dietary
protein or amino acid mixtures on PFAA concentrations in rainbow trout, O. mykiss (Murai et al. 1987;
Schuhmacher et al. 1997; Vermeirssen et al. 1997),
and sea bass, Dicentrarchus labrax (Thebault et al.
1985), have been reported, the complete dose response relationships for amino acids have not been
investigated. In our previous studies, requirements for
dietary essential amino acids such as arginine,
methionine, lysine and threonine were obtained in
rainbow trout, O. mykiss, by using surgically modified methods in our laboratory (Ok et al. 2001; Ok
2002; Park et al. 2005).
As a part of our studies on essential amino acid
requirements of rainbow trout, the purpose of the
present study was to estimate the dietary valine
requirement based on the plasma free valine and
ammonia concentrations in dorsal aorta cannulated
rainbow trout, O. mykiss.
2. Materials and methods
2.1. Experimental fish
Rainbow trout, O. mykiss, averaging 49397.2 g
(initial body weight, mean9SD) were obtained
from Ewhajung trout farm in Sangju, Korea. Seven
net cages (1.31.3 1.3 m) were placed in a flowthrough concrete raceway with a water flow rate of 60
L min 1. Fish were then fed a commercial rainbow
trout diet (Woo-sung Feed Co. Ltd., Daejon, Korea)
for 72 h until the fish recovered from the dorsal aorta
cannulation operation. Supplemental aeration was
also provided to maintain the dissolved oxygen at
6.790.5 mg L 1, and water temperature was maintained at 1590.38C.
2.2. Preparation of experimental diets
A basal diet containing 36.6% crude protein (29.6%
crystalline amino acids mixture, 5% casein and 2%
gelatin) was formulated by the modification of Kim
(1997). Seven experimental diets were formulated to
contain graded levels of valine (0.45, 0.95, 1.20, 1.45,
1.70, 1.95 or 2.45% of diet, on a dry matter basis)
based on the basal diet. Equal amounts of aspartic
acid and glutamic acid by weight were substituted for
the graded amounts of valine in the basal diet to
maintain the seven experimental diets isonitrogenous.
Formulation and amino acid composition of the
experimental diet are shown in Tables 1 and 2,
respectively. The ingredient mixtures without oil
were stored at 808C until used and the diets were
prepared by adding fish oil (10% of diet) and water
(diet plus 0.4 parts of distilled water per diet) before
intubation.
2.3. Dorsal aorta cannulation and intubation (forcefeeding)
Rainbow trout were anaesthetised with 200 mg L 1
3-aminobenzoic acid ethyl ester methanesulfonate
(MS-222; Sigma Chemical Company, St. Louis,
MO, USA) for 35 min, placed on a V-shape table,
and their gills were irrigated continuously with 168C
water containing 100 mg L 1 of MS-222 during the
operation. A 50-cm-long cannula (Clay Adams PE 50
tubing, Parsippany, NJ, USA) with a bubble of about
56 cm on one end was washed with the heparinized
Cortland saline solution; a 13-gauge needle was used
to pierce a hole on the right nostrum of fish (ventral
side up) as an exit for the cannula. A 19-gauge needle
was used to bore a small hole in the roof of the mouth
at the mid-line behind the third gill arc at a 308 angle,
and a piano wire was inserted into the PE 50 tubing as
a guide. The proper insertion was verified by the
observation of a slow blood flow after the wire was
withdrawn from the cannula. A 3 mL syringe with a
23-gauge needle was used to remove air and blood
clot, and the cannula was flushed with the heparinized saline solution. The cannula was sutured
behind the bubble on the roof of the mouth, led out
from the right nostrum, plugged with a colour head
pin, and sutured at the dorsal fin (Ok et al. 2001; Bai
et al. 2003; Park et al. 2005). Thirty five dorsal aorta
cannulated rainbow trout were randomly distributed
into seven groups of five fish per group and fed one of
the seven experimental diets per group. After 24 h
feed deprivation, the fish were anaesthetized with 200
mg L 1 of MS-222 and fed the experimental diet by
the stomach intubation method using a 3 ml syringe.
2.4. Sample collection and analysis
Five fish per group were anaesthetised with 200 mg
L 1 MS-222 and blood was sampled using a 3 ml
syringe from each fish at 0, 5 and 24 h after
intubation of the experimental diets. Plasma samples
were prepared by centrifugation at 3000 g for 10
min at room temperature. For deproteinization,
plasma samples were mixed with a 10% 5-sulphosalicylic acid solution in the ratio of 4:1 (v/v), cooled on
75
Journal of Applied Animal Research
Table 1. Composition of the experimental diets (% of dry matter basis).a
Experimental diet (graded valine level, % in diet)
Ingredients
EAAb
NEAAc
Caseind
Gelatined
Dextrind
Dextrosed
A-Cellulosed
Fish oile
Other ingredientsf
L-valineg
Aspartic acidg
Glutamic acidg
Total
Diet 1
(0.45)
0.10
4.23
4.57
100
Diet 2
(0.95)
0.60
3.98
4.32
100
Diet 3
(1.20)
Diet 4
(1.45)
Diet 5
(1.70)
Diet 6
(1.95)
Diet 7
(2.45)
0.85
3.85
4.19
100
15.27
5.47
5.00
2.00
27.97
5.00
8.20
10.00
12.20
1.10
3.73
4.07
100
1.35
3.60
3.94
100
1.60
3.48
3.82
100
2.10
3.23
3.57
100
a
Diets were neutralised with NaOH to give a final pH of 6.6.
EAA, essential amino acids (gram per 100 g diet): arginine, 1.924; histidine, 0.725; isoleucine, 1.674; leucine, 2.702; lysine, 1.904; methionine,
1.030; cystine, 0.172; phenylalanine, 1.742; tyrosine, 1.335; threonine, 1.601; tryptophan,0.462 (Ajinomoto, Tokyo, Japan).
c
NEEA, Non-essential amino acids (gram per 100 g diet): alanine, 1.741; glycine, 0.758; proline, 0.568; serine, 2.398 (Ajinomoto, Tokyo,
Japan).
d
United States Biochemical (USB), Cleveland, OH, USA.
e
Ewha Oil Company, Busan, Korea.
f
Other ingredients include: carboxymethyl cellulose, 1.00% (United States Biochemical); Ca(H2PO4)2H2O, 3.00%; choline bitartrate, 1.20%
(United States Biochemical), vitamin mixture, 3.00% & mineral mixture, 4.00% (Bae et al. 2010).
g
Ajinomoto, Tokyo, Japan.
b
ice for 30 min and re-centrifuged. The protein-free
supernatant was dissolved in pH 2.2 lithium citrate
sample dilution buffer in the ratio of 1:1 (v/v), and the
samples were stored at 808C until analysis. PFAAs
were quantified using an S433 amino acid analyzer
(Sykam, Gilching, Germany) using the ninhydrin
method. Plasma ammonia concentrations were analysed using the Berthelot reaction (Sigma).
Table 2. Amino acid composition of the experimental diet (% of dry matter basis).
From casein and gelatin
From crystalline amino acids
Totala
EAA
Arginine
Histidine
Isoleucine
Leucine
Lysine
Methionine
Cystine
Phenylalanine
Tyrosine
Threonine
Tryptophan
Valine
0.353
0.194
0.252
0.493
0.502
0.152
0.019
0.271
0.270
0.221
0.065
0.350
1.924
0.725
1.674
2.702
1.904
1.030
0.172
1.742
1.335
1.601
0.462
0.000b
2.277
0.919
1.926
3.195
2.406
1.182
0.191
2.013
1.605
1.822
0.527
0.350
NEAA
Alanine
Aspartic acid
Glycine
Glutamic acid
Proline
Serine
0.345
0.483
0.538
1.298
0.790
0.374
1.741
4.280
0.758
4.616
0.568
2.398
2.086
4.763
1.296
5.914
1.358
2.772
Amino acids
a
The amino acid profile was simulated with that of 35% whole chicken egg protein (Robinson et al. 1981).
Seven experimental diets were formulated to have graded levels of valine (0.45, 0.95, 1.20, 1.45, 1.70, 1.95 or 2.45%) equal amount of aspartic
acid and glutamic acid by weight were substituted for the proper amounts of valine in the basal diet.
b
76
J.-Y. Bae et al.
2.5. Statistical analysis
Data were subjected to one way analysis of variance
test using Statistix 3.1 (Analytical Software, St Paul,
MN, USA). When a significant treatment effect was
observed, a Least Significant Difference test was used
to compare means. Treatment effects were considered
significant at P B0.05. The breakpoints for postprandial plasma free valine concentrations (PPval),
post-absorptive free valine concentrations (PAval)
and post-prandial plasma ammonia concentrations
(PPA) were estimated by using the broken line model
of Robbins et al. (1979).
3. Results
3.1. Plasma free valine concentrations
Results of PPval (5 h after intubation) and PAval (24
h after intubation) in dorsal aorta cannulated rainbow trout force-fed with diets containing seven
graded levels of valine are summarised in Table 3.
PAval of fish fed diets containing 1.45% or more
valine were significantly higher than those of fish fed
diets containing 1.20% or less valine (PB0.05). There
were no significant differences in PPval among fish
fed diets containing 1.45% or more valine (P 0.05).
Broken-line model analyses on the basis of PPval as
shown in Figure 1 indicated that the dietary valine
requirement of trout could be 1.47% (4.02) of diet (%
dietary protein on a dry matter basis).
Post-absorptive plasma free valine concentrations
of fish fed diets containing 1.45% or more valine were
significantly higher than those of fish fed diets
containing 1.20% or less valine (P B0.05). Postabsorptive plasma free valine concentration of fish
fed the diet containing 2.45% valine was significantly
higher than that of fish fed the diet containing 1.95%
valine (P B0.05), but these were not significantly
different among fish fed diets containing 1.45 and
1.70% valine (P 0.05). Broken-line model analyses
on the basis of PAval in Figure 2 indicated that the
dietary valine requirement of trout could be 1.50%
(4.10) of diet (% dietary protein on a dry matter
basis).
3.2. Plasma ammonia concentrations
Post-prandial plasma ammonia concentrations (PPA,
5 h after intubation) and post-absorptive plasma
ammonia concentrations (PAA, 24 h after intubation)
in rainbow trout force-fed graded levels of dietary
valine are shown in Table 3. Post-prandial plasma
ammonia concentration of fish fed the diet containing
2.45% valine was significantly higher than those of
fish fed diets containing 1.95% or less valine
(P B0.05). Post-prandial plasma ammonia concentrations linearly increased with dietary valine levels from
1.45 to 2.45%. Post-absorptive plasma ammonia
concentrations in the present study were not significantly different among the groups (P 0.05). Brokenline model analyses on the basis of PPA (Figure 3)
indicated that the dietary valine requirement of
rainbow trout could be 1.41% (3.85) of diet (%
dietary protein on a dry matter basis).
4. Discussion
In the present study, the dietary valine requirement
for the rainbow trout based on plasma free valine
concentrations (PPval and PAval) was between 1.47
and 1.50% of the dry diet. This value corresponds to
4.024.10% of the dietary protein on a dry weight
basis. In previous studies, the dietary valine requirements of rainbow trout have been reported to be
1.30% of diet by Ogino (1980) and 1.551.58% of
diet by Rodehutscord et al. (1997) based on dose
Table 3. Plasma post-prandial (5 h after intubation) and post-absorptive (24 h after intubation) valine and ammonia
concentrations (nmol mL 1) of rainbow trout fed graded levels of dietary valine.*
Plasma valine concentrations
Dietary valine level
(%)
0.45
0.95
1.20
1.45
1.70
1.95
2.45
Pooled SEM$
Plasma ammonia concentrations
Post-prandial values
(PPval)
Post-absorptive values
(PAval)
Post-prandial values
(PPA)
Post-absorptive values
(PAA)
123d
357c
487b
608a
617a
593a
649a
72.1
141e
163d
186c
256a,b
250a,b
243b
271a
19.4
121e
148d,e
162d
172d
222c
284b
312a
27.3
105
114
120
107
122
110
116
2.43
*Values are means from groups (n=5) of fish where the means in each column with different superscript letters are significantly different
(PB0.05).
$Pooled standard error of mean: SD/ân.
77
Journal of Applied Animal Research
400
Post prandial plasma ammonia
concentrations (nmol ml–1)
Post prandial plasma free valine
–1
concentrations (nmol ml )
800
600
400
y = 486.1x –98.383
y'= 616.75
R² = 0.9996
200
300
200
y = 139.66x –16.103
y'= 160.67
R² = 0.9006
100
1.41%
1.47%
0
0.0
0.5
1.0
1.5
2.0
2.5
3.0
0
0.0
0.5
1.0
1.5
2.0
2.5
3.0
Dietary valine level (%)
Dietary valine level (%)
Figure 1. Broken line analysis of post-prandial plasma
valine concentrations (nmol mL 1) in rainbow trout fed
graded levels of dietary valine. Values of the X-axis are the
valine levels in the experimental diets. Values are
means9SD of five replicates. Y486.1x 98.383, Y?
616.75, R2 0.9996.
Figure 3. Broken line analysis of post-prandial plasma
ammonia concentrations (nmol mL 1) in rainbow trout fed
graded levels of dietary valine. Values of the X-axis are the
valine levels in the experimental diets. Values are
means9SD of five replicates. Y139.66x 16.103, Y?
160.67, R2 0.9006.
response or protein accretion. Results of the present
study were similar to those reported for Rohu, L.
rohita, 1.50% of diet (Murthy and Varghese 1997).
Somewhat lower requirement values have been reported for other species including 0.71% of diet in
channel catfish, Ictalurus punctatus (Wilson et al.
1980); 0.78% in lake trout, Salvelinus namaycush
(Hughes et al. 1983); 0.78% in Nile tilapia,
Oreochromis niloticus (Santiago and Lovell 1988);
1.20% in chum salmon, Oncorhynchus keta (National
Research Council 1993); 1.30% in Chinook salmon,
Oncorhynchus tshawytscha (Chance et al 1964); 1.42%
in milkfish, C. chanos (Borlongan and Coloso 1993)
and 1.42% in Catla, C. catla (Ravi and Devaraj
1991), while higher levels of valine in diet have been
reported for mrigal, Cirrhinus mrigala, 1.52%
(Ahmed and Khan 2006).
These wide variations observed in the valine
requirements among fish species may be due to the
differences in dietary protein sources, the reference
protein for which amino acid pattern is being
imitated, diet formulation, size and age of fish,
genetic differences, feeding practices and rearing
conditions (Rodehutscord et al. 1997). Zhou et al.
(2007) reported that the dietary lysine requirements of
fish species that have high protein requirements, such
as marine fish and freshwater carnivorous fish, are
higher than those of the species that have low protein
requirements including omnivores and herbivorous
fish. However, the difference in the dietary valine
requirement values listed above indicates that there is
no apparent distinction in food habits or environmental needs which may help to give a clear
classification of dietary valine requirements for various fish species.
The effects of dietary valine intake on PPval and
PAval were dependent on the relative adequacy of the
dietary valine supply, increasing up to the dietary
valine requirement levels with no further increase
above the requirement values. The pattern of postprandial or absorptive plasma free amino acid concentrations of fish fed graded levels of the amino acid
tested has been used in several studies in an attempt to
confirm requirement values assessed by growth
(Wilson et al. 1980; Thebault et al. 1985; Tibaldi
and Tulli 1999). The plasma limiting amino acid
concentration is expected to be low in fish given
Post absorptive plasma free valine
concentrations (nmol ml–1)
300
200
y = 104.9x – 80.274
y'= 237.6
R² = 0.8077
100
1.50%
0
0.0
0.5
1.0
1.5
2.0
2.5
3.0
Dietary valine level (%)
Figure 2. Broken line analysis of post-absorptive plasma
valine concentrations (nmol mL 1) in rainbow trout fed
graded levels of dietary valine. Values of the X-axis are the
valine levels in the experimental diets. Values are
means9SD of five replicates. Y104.9x 80.274, Y?
237.6, R2 0.8077.
78
J.-Y. Bae et al.
sub-requirement levels of the test amino acid, however
when adequate levels are fed the plasma concentration
tends to increase linearly as the dietary concentrations
rise (Cowey 1995). As indicated above, a similar
response was observed in the present study in that a
breakpoint was observed in the plasma concentration
value at 1.07% (PPval) or 0.97% (PAval) dietary
valine.
In the present study, the dietary valine requirement for rainbow trout based on post-prandial
plasma free ammonia concentration (PPA, 5 h after
intubation) could be 1.41% of the dry diet. This value
corresponds to 3.85% of the dietary protein on a dry
weight basis. PPA was significantly affected by the
dietary valine levels. However, PAA (24 h after
intubation) was not affected by the dietary valine
level. PPA remained low and virtually constant, but
increased linearly when dietary valine level was higher
than the requirement level. Similar observations were
reported that PPA was affected in response to dietary
arginine, lysine, methionine and threonine levels in
rainbow trout (Ok 2002). This observation could be
attributed to an increase in net protein synthesis with
the increase in dietary amino acids. The ammonia
excretion is related to the intake of protein (Koshio
et al. 1993) and dietary amino acids balance (Kaushik
et al. 1988). Considering protein and amino acid
metabolism, results of the present study indicated
that the dietary valine requirement in rainbow trout
can be estimated based on PPA. Furthermore, the
results showed that estimated valine requirement
value based on PPA is lower than that based on
PPval and PAval. This relationship between plasma
free valine concentrations and plasma ammonia
concentrations was not observed in this study. Future
studies would look into the cause of the discrepancy
in these values.
In conclusion, broken-line model analyses on the
basis of PPval, PAval and PPA concentrations
indicated that the dietary valine requirements of
rainbow trout could be between 1.41% (3.85) and
1.50% (4.10) of diet (% of dietary protein basis).
Acknowledgements
This research was supported by the funds of the Feeds and
Foods Nutrition Research Center, Korea Sea Grant
Program and Brain Korea 21 Program at Pukyoung
National University, Busan, Korea, Ewhajung trout farm
in Sangju, Korea.
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