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Department of Animal Science,
*
Veterinary Medicine Resource Services and
California Animal Health and Food Safety Laboratory, University of California, Davis, CA
3To whom correspondence should be addressed. E-mail: kcklasing{at}ucdavis.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • Psittacine • protein toxicity • adaptation • maintenance • amino acid catabolism • cockatiels
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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,2)
. For example, omnivorous species such as
chickens, Japanese quail, rats, pigs and humans are capable of up- or
down-regulating enzymes for amino acid catabolism and are able to
utilize diets with either a very low or very high protein content
(3
4
5
6
7)
. In contrast, nonomnivorous species often
specialize on a narrow range of food items of very uniform nutritional
content. For example, faunivorous (animal matter–eaters) species such
as barn owls, vultures, alligators, trout and cats select high
protein:low carbohydrate food items (protein specialists) and have
little capability to regulate their amino acid and carbohydrate
metabolizing pathways (8
9
10
11
12)
. Granivorous (grain-eaters),
frugivorous (fruit-eaters) and nectarivorous (nectar-eaters) species
select low protein:high carbohydrate foods (carbohydrate specialists).
In contrast to faunivores, these species have low requirements for
dietary amino acids and appear to be able to conserve amino acids by
tight regulation of amino acid catabolism (13)
. Analogous
to the poor metabolic adaptations by faunivores, it might be expected
that carbohydrate specialists would have a poor capacity to adapt to
high protein diets. However, the metabolic plasticity of carbohydrate
selectors has received very little attention. For this reason, we
tested the capacity of cockatiels, an avian granivore, to adapt to high
protein diets. In their native areas of Australia, wild cockatiels
select seeds with 8.8–14% crude protein
(CP)4
and consume little or no animal matter (14)
. Furthermore,
the popular literature is rife with anecdotes of protein intolerance by
this species. The purpose of this experiment was to determine the effect of high dietary protein on the health of adult cockatiels at maintenance, as well as to examine the ability of these birds to adapt metabolically to high protein diets. To assess the possibility of protein toxicity, we examined the maintenance of body weight and composition, deposition of uric acid precipitates in organs and joints, and the development of pathology in kidney and liver. Metabolic adaptation was assessed by changes in amino acid and carbohydrate metabolizing enzymes in the liver and kidney as well as serum metabolite concentrations.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Adult male cockatiels (n = 26; UC Davis cockatiel
colony), 2–3 y of age, with average body weight of 93 g, were
housed individually in 0.3 x 0.3 x 0.6 m3 wire
cages at 24°C under a 12-h light: 12-h dark lighting schedule.
Cockatiels were randomly assigned to one of four dietary treatments,
which were isocaloric and contained either 11% CP (n
= 6), 20% CP (n = 7), 35% CP
(n = 6) or 70% CP (n = 7)
(Table 1
). Diets were formulated for identical acid-base balance, calculated
as meq (Na + K + Ca - P - Cl). Diets were mixed, 
50%
water was added and diets were then pelleted through a commercial
sausage grinder (Hollymatic model # GMG 180A, Countryside, IL) with a
5-mm diameter die. Pelleted diets were crumbled by hand to 12–15 mm
length, and then dried overnight at 55°C. All diets were stored at
4°C before use. Birds were acclimated to the 11% CP diet for 1 mo.
After this acclimation period, birds assigned to the higher protein
diets were switched to their assigned experimental diets over a period
of several weeks to prevent acute protein toxicity. Birds assigned to
20, 35 or 70% CP were initially switched to 20% CP. One week later,
birds assigned to 35 or 70% CP were switched to 35% CP, and so on,
until all birds were being fed their assigned experimental diet (d 1 of
the experiment). Cockatiels consumed the experimental diets ad libitum
for 11 mo and had free access to deionized water. After 10 mo of
consuming the experimental diets, water intake was measured using
100-mL water bottles, graduated in 1-mL increments, with a 1.5-cm
drinking surface (BioServe Frenchtown, NJ). The University of
California at Davis Animal Care and Use Committee approved all animal
protocols.
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All birds were weighed at the onset of the trial and monthly
thereafter. Feed was not withdrawn before the time of weighing,
bleeding or necropsy. Blood (1 mL) was taken from the jugular at the
onset and termination of the experiment and twice in between, on d 34
and 178. Freshly drawn blood was used to make a blood smear and drawn
into a hematocrit tube. The remaining blood was allowed to clot for
3 h and serum was frozen until analysis. After 11 mo of consuming
the experimental diets, all birds were killed by isoflurane (Merial
Animal Health, Iselin, NJ) anesthesia followed by isoflurane overdose.
Kidney, liver, hock joint and pericardium were immediately dissected
from the birds. One kidney and one liver lobe were flash-frozen
between two aluminum plates in liquid N and stored at -60°C before
enzymatic analysis. All other tissues were fixed in 10% buffered
formalin for histopathologic analysis. The breast was removed, weighed
and returned to the bird of origin. Birds were then weighed and
freeze-dried at a shelf temperature of 30°C (Virtis
Freeze Drier, Model # 50 SRC, Gardiner, NY) for 24 h for moisture
determination. Subsequently, all birds were placed in soxhlet units for
lipid extraction using a modified AOAC procedure (15)
.
Birds were extracted for 7 d with petroleum ether, followed by
3 d with acetone. Birds were then dried overnight at 55°C,
weighed, and lipid content was calculated by difference.
Analysis of blood samples.
Hematocrit tubes were centrifuged in a microcapillary
centrifuge (International Equipment, Needham, MA), and hematocrit
values were determined using a microcapillary reader (International
Equipment). Blood smears were stained with hematoxylin-eosin and
examined microscopically for total leukocyte number, as well as
monocyte, lymphocyte, basophil, heterophil and eosinophil number. Serum
samples were analyzed by standard methods for clinical chemistry
parameters (Clinical Chemistry Laboratory, UC Davis, Veterinary Medical
Teaching Hospital) including cholesterol, creatine kinase, lactate
dehydrogenase, uric acid, urea N, calcium, albumin, globulin, glucose
and total protein. In addition, serum samples were analyzed for plasma
amino acid concentration by HPLC as described by Bidlingmeyer et al.
(16)
.
Postmortem examination and histopathology.
Birds were examined for visual evidence of visceral, articular or renal gout. Any other gross abnormalities were also noted. Kidney, liver and pericardium were fixed in 10% buffered neutral formalin and processed for histopathology. Livers sections were graded from one to five with least severely affected livers (rare, single vacuolated cell-small granulomas) receiving a grade of one and most severely affected livers (numerous, large lipogranulomas) receiving a grade of five. Kidney sections were graded similarly on the basis of the frequency and size of inflammatory or degenerative foci, with grade one denoting the least severely affected and grade five the most severely affected.
Tissue enzyme activities.
Enzymatic activity in liver and kidney samples was analyzed as
described previously by Myers and Klasing (11)
. Briefly,
tissue samples were prepared for enzyme analysis by placing them on dry
ice and breaking them into pieces no larger than 6–7 mm across in a
-20°C cold room. Tissue samples were weighed into test tubes and 9
parts of ice-cold 0.14 mol/L KCl were added for alanine
aminotransferase (ALT; EC 2.6.1.2), aspartate aminotransferase (AST; EC
2.6.1.1) and pyruvate kinase (PK; EC 2.7.1.40). For phosphoenolpyruvate
carboxykinase (PEPCK; EC 4.1.1.31) assays, 9 parts of ice-cold
deionized water were added. Samples were homogenized on ice with a
Polytron (Brinkmann Instruments, Westbury, NY) twice at
half-maximum power for 15 s. Homogenates were centrifuged for
30 min at 14,000 x g in a 5 oC cold
room in an Eppendorf centrifuge (Brinkmann). For glucokinase (GK; EC
2.7.1.1) assay, 1 part liver was added to 5 parts 0.15 mol/L KCl, 0.005
mol/L sodium EDTA and 5 mmol/L MgCl2, pH 7.0, then
homogenized with a Teflon pestle twice for 15 s. The homogenate
was centrifuged (Sorvall RC 100, DuPont, Wilmington, DE) for 1 h
at 105,000 x g at 4°C, and the supernatant was
assayed for GK activity as previously described (17)
. The
assays for ALT and AST were according to procedures described by Segal
and Matsuzawa (18)
; arginase (EC 3.5.3.1) was according to
Tamir and Ratner (19)
and PEPCK and FBP were according to
Opie and Newsholme (20)
. Enzyme activity was measured in a
multicell thermostatically controlled spectrophotometer (Shimadzu,
Kyoto, Japan) and was expressed as substrate consumed per minute per
milligram of protein. Protein was determined by Coomassie dye binding
using a protein assay kit (# 5656; Sigma, St. Louis, MO).
Statistical analysis.
All data were analyzed by a general linear model (SAS Institute, Cary,
NC). Data collected at only one time point (water consumption, enzyme
activities and histopathology) were analyzed by one-way ANOVA for
the effect of dietary treatment. Data collected at multiple time points
throughout the study were analyzed for main effects due to diet and
time and for the interactions of diet and time by two-way ANOVA for
repeated measures. Birds were nested within diets, and the model
accounted for the random variation among birds. The Pdiff procedure of
SAS was used to determine whether mean values were significantly
different at P < 0.05, with Bonferonni adjustment
for 
critical for data analyzed by repeated measures
(21)
. Regression analysis of dietary protein level on
liver enzyme activities and on serum urea and uric acid concentrations
on d 34, 178 and 330 was accomplished using JMP (SAS Institute).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Change in body weight (calculated as body weight at each time point
- initial body weight) was not significantly different for birds
eating 11 or 20% CP (Fig. 1
). There was no consistent change in body weight for birds consuming
35% CP until d 252, at which point 35% CP resulted in a consistent
positive change in body weight compared with birds fed all other diets
(P < 0.05). Birds consuming 70% CP maintained body
weight; however, on d 330, body weight of birds eating 70% CP was
significantly reduced compared with those eating 20 or 35% CP
(P < 0.05). Body composition was also affected by
dietary CP level (Table 2
). Dry matter content was lower in birds fed 35% CP compared with those
fed all other diets (P < 0.05), whereas breast muscle
mass was greater in birds fed 20% CP compared with those fed 70% CP
(P < 0.05). Finally, lipid content, on a wet weight
(Table 2)
or dry matter basis (data not shown), was significantly
greater in birds fed 35% CP compared with all other dietary treatments
(P < 0.05).
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Water intake (Table 2
) was significantly greater in birds
fed 70 or 11% CP compared with those fed 20 or 35% CP (P
< 0.05). The birds were frequently observed for indices of
general health, including posture, feather positioning and integrity,
mobility, feed wastage and consistency of droppings. No
diet-related changes in these variables were noted. There was no
mortality with the exception of one bird fed 11% CP, which died on d
315 of unknown causes. Necropsy revealed no signs of inflammation,
renal dysfunction or other pathology in this bird.
Enzyme activity.
The effect of dietary protein level on the activity of liver and kidney
enzymes is shown in Table 3
. In the liver, glucokinase activity was significantly decreased at
dietary protein concentrations >11% CP (P < 0.05).
PEPCK activity was not affected in the liver, but was significantly
greater in the kidney of birds fed 70% CP compared with those fed 11%
CP (P < 0.05). Liver and kidney ALT and AST activities
generally increased with increasing level of dietary CP, and the
difference was significant (P < 0.05) between 70% CP
and the lower levels. Arginase activity was significantly greater in
birds fed 70% CP compared with those fed 11% CP in the liver, and
compared with those fed all dietary protein levels in the kidney
(P < 0.05). In addition, kidney arginase activity was
greater in birds fed 35% CP compared with those fed 11 or 20% CP
(P < 0.05).
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Serum uric acid concentrations increased linearly with dietary protein
levels (P < 0.001; r2
= 0.60). Uric acid was significantly greater in birds fed 70% CP
(P < 0.05) compared with 11, 20 or 35% CP (Fig. 2A
). In addition, serum urea concentrations increased linearly with
dietary protein levels (P < 0.0002;
r2 = 0.68). Urea was significantly
increased in birds fed 70% CP (P < 0.05) compared
with all other dietary treatments (Fig. 2B
).
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There were no significant differences in any other blood variables due to dietary treatment. Mean values ± SEM for each were as follows: ammonia (µmol/L) = 89 ± 6; cholesterol (mmol/L) = 5.74 ± 0.09; lactate dehydrogenase (IU/L) = 275 ± 17.4; calcium (mmol/L) = 1.40 ± 0.04; albumin (g/L) = 12 ± 0. 2; globulin (g/L) = 9.5 ± 0.1; glucose (mmol/L) = 18.98 ± 0.26; total protein (g/L) = 21 ± 0.3; hematocrit (%) = 41.1 ± 1.0; heterophil (%) = 62.3 ± 0.39; lymphocyte (%) = 36.2 ± 0.45; monocyte (%) = 0.75 ± 0.11; eosinophil (%) = 0.25% ± 0.05; and basophil (%) = 1.7 ± 0.14.
Postmortem and histopathology.
No evidence of visceral, articular or renal gout was found in any of
the birds at necropsy. One bird fed 70% CP showed breast muscle
atrophy and dark intestinal contents with excess gas formation. No
other gross lesions were found in any of the treatment groups. There
was no evidence of substantive renal pathology due to dietary treatment
(Table 4
). Sixteen of 25 birds had lesions in the kidneys; these were
characterized by infrequent foci of mild interstitial mononuclear
inflammatory cell infiltrates, and 12 of these birds also had focal or
infrequent multifocal mild tubular dilatation with occasional tubular
luminal mineral concretions. Renal changes were considered background
changes and not related to dietary protein levels because four of the
five birds fed low protein diets had lesions in the kidneys. In
general, lesions in the kidneys of most birds were mild when present
and likely not clinically important (Fig. 3A
).
|
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; Fig. 3B
, C
, D
). Single vacuolated cells were intimately
associated with the sinusoidal and perisinusoidal space and were likely
Ito cells (vitamin A–storing cells, fat storing cells, lipocytes,
stellate cells). Only one bird had hepatocellular micro- and
macrovesicular lipidosis. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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23
24)
]. Therefore, an 11% CP diet was chosen as the
control. A 20% CP diet was included in this experiment because this
level is often supplied in commercial diets used for breeding, growth
and maintenance. The high dietary protein levels of 35 and 70% CP were
chosen to ensure that if there was a limit to up-regulation of
enzyme activity or nitrogen excretion in cockatiels, a protein toxicity
would be reached.
Excess levels of dietary amino acids cause decreased food intake,
muscle deposition and body weight in chickens and rats
(25)
. In the present experiment, body weight and breast
muscle size were maintained by 11, 20 and 70% CP, whereas 35% CP
caused a significant increase in body weight, accompanied by an
increase in whole-body lipid content. These data indicate that
levels of CP well above expected maintenance requirements did not cause
overt protein toxicity. An increase in fat deposition at high levels of
dietary protein (35%) was surprising; lipid accretion may be due to
increased energy consumption or to a shift in metabolic priorities.
However, the fact that breast muscle weight of these birds was similar
to that of the 11 and 20% CP treatment groups argues in favor of
increased energy intake and not a change in the partitioning of dietary
energy toward fat storage at the expense of other tissue types.
Water intake was significantly greater in birds fed 70 and 11% CP
compared with 20 or 35% CP. Additional water for the excretion of
nitrogen end products may be responsible for increased water
consumption by birds eating 70% CP. In the case of the increase by
cockatiels eating 11% CP, an explanation is less clear. However, in
growing broiler chickens, levels of dietary protein below NRC
recommendations (17% CP) resulted in a significant increase in water
intake (26)
. A mechanism for this change in water intake
has yet to be proposed.
Liver and kidney enzymes involved in amino acid catabolism generally
increased with increasing protein level, which has been demonstrated in
the omnivorous chicken and quail (4
5
6
7
,27)
. These data
suggest that cockatiels are able to up-regulate enzymes for amino
acid catabolism in a manner similar to that of omnivores. Cockatiels
were also able to adapt to low dietary glucose levels as indicated by
maintenance of serum glucose and altered activity of kidney PEPCK and
liver glucokinase. Because cockatiels have evolved consuming low
protein, high carbohydrate diets, the ability to catabolize high levels
of dietary protein and to use amino acids for glucose synthesis could
indicate that these activities are retained for other purposes.
Increases in the rate of amino acid catabolism and gluconeogenesis are
also important in acute starvation and the catabolic response to
infection or trauma (28)
, and it may be that these are the
primary reasons for the retention of metabolic plasticity.
Kidney arginase and serum urea concentrations increased with increasing
dietary protein. These data are in contrast to work done in growing
broiler chickens, which demonstrated that a twofold increase in protein
level above dietary requirements did not increase blood urea levels
(4)
. However, in the present experiment, assuming a
maintenance CP requirement of 11%, a sixfold increase in dietary
protein was tested. This substantial increase may account for
differences in urea N data. Traditionally, blood urea is considered to
have little clinical importance in avian species; however, it has been
suggested that this variable may be useful to detect early renal
failure (29)
. In the case of these cockatiels, high
concentrations of blood urea N were not associated with renal
pathology, but were correlated with dietary protein concentration.
We observed a marked increase in serum levels of uric acid at 70% CP,
indicating that increased uric acid synthesis accompanied increased
amino acid catabolism. However, there were no significant differences
in uric acid levels among the 11, 20 and 35% CP groups. In breeding
parakeets, levels of CP from 13 to 25% did not affect plasma uric acid
concentration (24)
, but higher concentrations of dietary
protein were not tested. In chickens, uric acid synthesis increases
with increasing dietary CP (30)
, and plasma uric acid
concentrations of chickens fed a similarly high CP diet
(31)
are elevated to the same extent that we observed in
cockatiels. In both chickens and cockatiels fed very high protein
diets, uric acid synthesis appears to keep pace with amino acid
catabolism because blood ammonia levels do not rise.
In avian clinical medicine, uric acid concentration is considered to be
indicative of renal function (29)
. Further, many avian
species presenting with high plasma uric acid levels are diagnosed with
gout and renal dysfunction. The cause of these pathologies is often
attributed to protein toxicity (32)
. However, renal
sections in the present experiment showed no evidence of pathology at
either the gross or the histologic level, which suggests that high uric
acid concentrations may be indicative of dietary protein concentration
and not renal damage. In chickens, gout seems to be associated
primarily with a genetic predisposition for the condition; although
high dietary protein aggravates the pathology of the disease, it does
not cause it (33
34)
. These data indicate that
susceptibility to gout is genetic, rather than a result of dietary
protein levels.
In contrast to low lesion severity in kidneys, liver samples had
increasing lesion severity with increasing dietary protein, and lesions
were associated with an increased incidence of lipogranulomas. Rates of
amino acid deamination and uric acid production are higher in liver
than in kidney (35)
. If rates of deamination exceeded the
capacity of uric acid synthesis in the liver, locally high levels of
ammonia might have induced the observed pathology. In humans,
hyperammonemia due to a variety of genetic disorders causes aberrant
hepatic lipid storage (36)
. However, we did not observe
hyperammonemia, and it is not clear whether the changes in liver
histology should be considered an indication of protein toxicity. Serum
chemistry values indicative of liver function (albumin, total protein)
were within normal limits, indicating no severe functional outcome of
the lipidosis. Further research is warranted to evaluate the incidence
of liver lipogranulomas on the basis of dietary protein level.
Finally, the serum concentrations of several amino acids were affected
by dietary crude protein level. In chickens fed an isolated soy
protein–based diet containing 21 or 64% CP, plasma amino acids were
altered in a manner similar to that seen in the present experiment
(31)
. Interestingly, dietary protein levels did not affect
serum arginine concentrations, and this lack of change can be
attributed to the nearly threefold increase in activity of kidney
arginase. This evidence indicates that the granivorous cockatiel is as
capable of disposing of surfeit amino acids as the omnivorous chicken.
On the basis of the data, it seems that cockatiels, a granivorous avian species, are quite capable of adapting to high dietary protein concentrations. To do so, these birds change activity of enzymes for amino acid catabolism, as well as rates of gluconeogenesis. In addition, at high dietary protein concentrations, cockatiels increase uric acid production to excrete excess nitrogen. These data suggest that unlike the lack of metabolic plasticity in faunivorous species, granivores that have evolved consuming low protein diets are able to adapt to changing protein concentration.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported in part by Morris Animal Foundation grant 99AV-01.
4 Abbreviations used: ALT, alanine aminotransferase; AST, aspartate aminotransferase; CP, crude protein; GK, glucokinase; PEPCK, phosphoenolpyruvate carboxykinase; PK, pyruvate kinase; TEAA, total essential amino acids; TNEAA, total nonessential amino acids.
Manuscript received December 18, 2000. Initial review completed February 4, 2001. Revision accepted April 17, 2001.
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E. A. Koutsos, L. A. Tell, L. W. Woods, and K. C. Klasing Adult Cockatiels (Nymphicus hollandicus) at Maintenance Are More Sensitive to Diets Containing Excess Vitamin A Than to Vitamin A-Deficient Diets J. Nutr., June 1, 2003; 133(6): 1898 - 1902. [Abstract] [Full Text] [PDF]
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