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RESEARCH ARTICLE
INTRODUCTION
Essential amino acids required by cats are supplied by dietary protein. Cats,
like other monogastric species, need 10 a-amino acids provided in the diet. Besides
these 10 amino acids, cats have a dietary requirement for taurine (TAU), a b-amino
sulfur-containing amino acid. The cat’s requirement for dietary TAU is largely the
result of the need for TAU conjugates in bile salts and its low efficiency in the hepatic
synthesis of TAU from methionine and cystine [NRC, 1986].
TAU deficiencies have been sporadically reported in captive nondomestic
felids. A species-specific sensitivity to TAU depletion in leopard cats (Felis
bengalensis) was documented [Howard et al., 1987] as was a TAU-responsive
therapy in a snow leopard [Panthera unica; Burton et al., 1988]. In 1995, a TAU
study reported dietary and plasma values from eight healthy sand cats [Felis
margarita; Crissey et al., 1997]. A 1-year study conducted in 1997–1998 reported
circulating plasma TAU concentrations in adult cheetahs (Acinonyx jubatus; n 5 12)
fed a commercial product, or whole prey-based diets [Bechert et al., 2002]. This
information is useful and reminds us of the importance of TAU in zoo carnivore
diets, but is not easily interpreted owing to differences in carnivore feeding strategies
among zoos along with differences in bioavailability and variability of TAU in
dietary ingredients.
Current recommendations for dietary allowances of TAU in adult domestic cat
diets—400 mg/kg (0.04%) for dry highly digestible purified diet, 1,000 mg/kg (0.1%)
for dry expanded diets, and 1,700 mg/kg (0.17–0.2%) in canned diets (all expressed
on a dry matter [DM] basis) [AAFCO, 2006; NRC, 2006]—can be met by including
0.1% TAU in dry products, and 0.2% (DM) in canned diets. Canned diets require
higher concentrations of TAU as a result of an increased microbial cleavage of
taurocholic acid in the lower small intestine and its subsequent metabolic
destruction. This does not seem to be true when a purified diet or a dry expanded
diet is fed [Hickman et al., 1990; Kim et al., 1996a,b]. Nevertheless, dry cat foods
containing rice bran and whole rice also can result in decreased plasma and whole
blood TAU concentrations. It seems that the high fat diet increases bile secretion and
the rice fiber increases the fecal excretion of bile acids, increasing the need for dietary
TAU to prevent the development of TAU deficiency [Stratton-Phelps et al., 2002].
Whole prey items such as rodents, poultry, or rabbits are offered on a regular
or periodic basis instead of (or in addition to) commercial diets to increase dietary
diversity for captive felids [Allen et al., 1996; Mellen et al., 1998]. This strategy may
either increase or decrease dietary TAU content unintentionally owing to TAU
content of the prey and the effect of the prey on microbial growth and destruction of
TAU within the intestine of the felids [Hickman et al., 1990; Kim et al., 1996a,b].
The minimum concentration of TAU in the diet to prevent clinical signs of
TAU deficiency defines the minimum requirement. Individual domestic felines vary
greatly in their capacity to regulate TAU metabolism and cope with diets containing
less than optimal TAU [Ruessheim, 2000]. When a diet is marginal in TAU, not all
cats consuming the diet manifest clinical signs of a deficiency that usually includes
cardiomyopathy and progressive retinal atrophy. Minimum dietary TAU concen-
trations high enough to prevent eye defects (0.05%) in cats still may not be adequate
for successful reproduction [Dierenfeld, 1989]. Sturman and Messing [1992] reported
that the reproductive performance was slightly better in queens fed a diet containing
considerably higher concentration of TAU (0.2% DM) than that required to prevent
eye lesions or dilated cardiomyopathy (0.05%).
This article contains information for evaluating normal TAU reference values
in zoo felids consuming quality diets. Various commercial feeds were analyzed for
TAU content, including common milk replacers as well as limited maternal milk
samples, and relationships correlating dietary and circulating concentrations of this
nutrient are documented in healthy nondomestic felids.
METHODS
Two samples of maternal milk were collected from zoo felids from the San
Francisco Zoological Garden. An anesthetized female fishing cat (Prionailurus
viverrinus) was sampled the day the kittens were born, and a female lion (Panthera
leo) 48 hr after delivery. The fishing cat and possibly the lion milk samples are likely
colostrum. In each case, milk was expressed from all four quadrants without
oxytocin. The fishing cat sample yielded roughly 2.0 ml, and the lion milk sample was
o1.0 ml. The samples were kept frozen at 701C for 2 years until transferred to the
Amino Acid Laboratory (University of California, Davis) for TAU analysis. The
samples were stored in sterile vials and kept frozen at 151C until evaluated.
Over a 5-year period, a total of nine frozen commercial horsemeat meat-based
diets from three manufacturers were analyzed, along with one canned zoo feline diet,
two dry feline diets, and two liquid milk replacers commonly used in hand-rearing
zoo felids. Additionally, the TAU content of five jars of human baby foods (strained
meat and broth), whole herring and bottled clam juice were analyzed. Frozen food
samples were stored at 151C in airtight containers until analysis at the Amino Acid
Laboratory.
Lithium heparinized plasma (1.0–2.0 ml) and whole blood (1.0–2.0 ml) samples
were obtained opportunistically from healthy zoo felids (n 5 29) between 2000 and
2006 from animal collections at San Francisco Zoological Gardens (n 5 15), San
Francisco, CA, Safari West Wildlife Reserve (n 5 4), Santa Rosa, CA, S&R
Productions (n 5 5), Las Vegas, NV, and Six Flags Discovery Kingdom (n 5 5),
Vallejo, CA.
Samples were obtained from Bengal tigers (Panthera tigris tigris) ranging in age
from 6 months to 13 years (n 5 5 samples), a 14-year-old Siberian tiger (Panthera
tigris altaicia; n 5 1 sample), lions (P. leo) ranging in age from 2 days to 9 years
(n 5 8 samples), cheetahs, from 2 to 9.5 months in age (n 5 4 samples), fishing cats
(P. viverrinus) ranging from 4.5 months to 5.3 years of age (n 5 7 samples), leopards
(P. pardus) 6–9 months of age (n 5 2 samples), a 9–month-old cougar (Puma
concolor; n 5 1 sample), and a serval (Leptailurus serval) 5.5 years of age (n 5 1
sample). Samples were either submitted directly to the Amino Acid Laboratory or
stored at 701C at San Francisco Zoological Gardens until transferred to the
laboratory.
TAU Analysis Methodology
On the day of analyses, an equal volume of 0.24 mol/5 sulfosalicyclic acid was
added to plasma to precipitate plasma proteins. After centrifugation the supernatant
was prepared with an internal standard (norleucine) and the equivalent of 40 or 20 ml
of plasma was injected onto the ion exchange column. The quantity of each amino
acid was determined colorimetrically using ninhydrin for color development (Model
6300 Amino Acid Analyzer, Beckman Instruments, Palo Alto, CA or Biochrom Ltd,
Cambridge).
Individual weekly diet histories (ingredients and amounts) were reviewed using
Zootrition software (St. Louis Zoo, St. Louis, MO) based on diets offered at the time
of the blood collection, and concurrent total dietary TAU concentration was
calculated for each cat. In cases where feeding strategies had frequent modifications,
blood concentrations were correlated with the average dietary TAU concentration
for the 3 months before sampling.
RESULTS
Milk Taurine Analyses
Table 1 summarizes published TAU milk values in various species and results
from this survey. The maternal milk sample from the fishing cat contained
approximately 1/6 the concentration of TAU (58.4 mg/L) when compared to a
domestic cat at a stage of lactation 45 days after birth (Table 1). TAU
concentration in the weekly diet for this female averaged 0.14–0.19% (DM basis)
during the pregnancy, based on a diet of approximately 95% whole prey and 5%
frozen commercial chopped horsemeat diet. The maternal milk sample collected
from the lion showed a higher concentration, at 165 mg/L or approximately 1/2 of
the concentration expected in domestic cat milk. This lion’s sample was collected
from mammary glands that had been stimulated previously by nursing cubs;
therefore the lion milk may reflect a transition between colostrum and milk, whereas
the sample collected from the fishing cat was undoubtedly colostrum. The lion diet
was estimated to contain 0.18% TAU (DM), with a weekly diet comprising
approximately 6.0 kg (40%) dressed rabbit with fur and 9.0 kg (60%) of a
commercial carnivore diet containing 0.21% TAU.
TABLE 2. Continued
Year g/kg g/kg % TAU
sampled Reference (as-fed basis) (DM basis) (DM basis)
TABLE 2. Continued
Year g/kg g/kg % TAU
sampled Reference (as-fed basis) (DM basis) (DM basis)
Except where noted, all assays conducted at the Amino Acid Laboratory, University of
California, Davis.
TAU, taurine.
1, Bechert et al. [2002]; 2, Clum et al. [1996]; 3, Dierenfeld [1993]; 4, Dierenfeld et al. [2002]; 5,
Huxtable and Lippincott [1982]; 6, Nebraska Packing Inc. [unpublished data]; 7, Roudebush
et al. [2000]; 8, Spitze et al. [2003].
a
Dallas Crown, Inc., Kaufman, TX.
b
Central Nebraska Packing Inc., North Platte, NE.
c
Toronto Zoo Carnivore diets-Miliken Meat Products, Scarborough, Ontario, Canada.
d
Iams Co., Dayton, Ohio.
e
Mazuri Purina Mills, LLC St. Louis, MO.
f
PetAg Inc., Hampshire, IL.
g
ZuPreem Premium Nutritional Products, Inc., Shawnee, KS.
h
Beechnut Nutrition Corp, St Louis, MO.
i
Gerber Products Company, Fremont, MI.
j
Snow’s/Doxsee, Inc, Cape May, NJ.
k
North Bay Meat Co., Rohnert Park, CA.
Liquid Esbilac (Pet Ag, Inc., Hampshire, IL), a canine milk replacer, contained
15.0 mg/L TAU, and liquid KMR (Pet Ag, Inc.) a kitten milk replacer, contained
65.0 mg/L. On a DM basis, the KMR contained less (0.033%) than the expected
value of 0.05%. Esbilac is not expected to contain a significant amount of TAU.
Poultry-based human baby foods (chicken and turkey strained meats and
broth) are particularly high in TAU (0.40–0.97% DM) when compared to beef and
lamb-based products (0.08–0.22% DM).
Raw seafood is an exceptional source of TAU as noted in clam juice, mackerel,
and herring (1.39, 0.90, and 0.49%, respectively). Whole prey items were widely
variable in TAU content with rat containing 1.57% DM. Unsupplemented meat cuts
(beef, chicken, and horse) contained marginal to deficient TAU concentrations
(0.10% DM).
Plasma and Blood
No significant differences in plasma or whole blood TAU concentrations were
found with regard to sex or age in cats in this survey (see Table 3). Younger animals
are expected to be at the higher range of normal. Selective data review within the
range for Bengal tiger showed 6-month-old Bengal tigers (n 5 3) with a lower plasma
TAU concentration than other species/subspecies when consuming diets estimated to
contain 0.14–0.18% TAU. The Bengal tiger cub plasma values were 88.7721.3 and
whole blood values 388744.2.1 nmol/ml compared to both a Siberian tiger with
plasma 183 and whole blood 443 nmol/ml, and fishing cats (plasma 153.3758.6 and
TABLE 3. Plasma, whole blood, dietary taurine concentrations (mean7SD, range) for
nondomestic felids sampled from four zoological institutions in the USA
TAU, taurine.
a,b
Differences in superscripts in a column are significant (Po0.05).
c
www.vetmed.ucdavis.edu/vmb/aal/aal.html.
whole blood 524.0775.3 nmol/ml; n 5 7). TAU in the diets of these latter animals
averaged 0.30% DM. Species differences were not significant (P40.05; Table 3).
With the exception of the single individuals, species’ means were within normal
reference ranges for TAU for the domestic cat.
Plasma TAU concentrations in this survey were not significantly correlated
with calculated dietary TAU, likely owing to small sample sizes and wide variance
(Fig. 1), but the relationship between dietary and whole blood TAU was significant
(Fig. 2). The various felids were offered a variety of formulated diets ranging from 5
to 100% (primarily) frozen commercial horse-meat-based diets with either
combinations of whole prey, poultry, fish, or supplemented with a dry commercial
feline diet. Calculated TAU content in these varied diets ranged from 0.11 to 0.55%
TAU on a DM basis. None of the diets seemed deficient in TAU based on current
nutrient recommendations.
DISCUSSION
TAU deficiency induces much pathology in cats, such as retinal degeneration,
heart disease, reproductive failure, platelet abnormalities, and developmental
abnormalities [Hayes et al., 1975; Huxtable, 1992]. TAU-responsive retinopathies
have been noted in captive cheetahs [Ofri et al., 1996]. TAU-responsive dilated
cardiomyopathy has also been characterized in exotic felids [Burton et al., 1988] and
350
300
y = 161.97x + 83.26
250
R2 = 0.142 ( P = 0.05)
Plasma Taurine (nmol/ml)
200
150
100
50
0
0 0.1 0.2 0.3 0.4 0.5 0.6
Dietary Taurine (% DM)
domestic cats [Pion et al., 1987, 1989], associated with low plasma TAU
concentrations. Additionally, TAU deficiency has been shown to result in high
incidence of fetal resorption, abortion, stillbirth, and low birth weight of live kittens
at term [Sturman et al., 1986]. TAU-deprived live-born kittens have poor postnatal
survival and slower growth rates than kittens from TAU-supplemented queens
[Sturman et al., 1985b], and TAU-deficient female cats have TAU-deficient milk
[Sturman and Messing, 1991a,b]. Dietary deprivation of TAU in pregnant cats from
approximately 1 week before giving birth is enough to substantially reduce the TAU
concentration in feline milk, but does not necessarily result in any abnormalities in
kittens at birth [Sturman et al., 1985a]. The concentration of TAU in milk of
lactating females was substantially higher in cats fed higher TAU diets [Sturman and
Messing, 1992].
Historically, some hand rearing formulas for zoo felids use either KMR kitten
milk replacer or Esbilac puppy milk replace (both Pet Ag, Inc., Hampshire, IL
60140). KMR has a stated minimum TAU concentration of 0.05% DM [NRC, 1986,
2006], whereas TAU in Esbilac is not reported. McManamon and Hedberg [1993]
anecdotally suggested that supplementing hand-rearing formulas with 250 mg
700
600
500
Whole Blood Taurine (nmol/ml)
400
300
200
y = 428.41x + 310.61
R2 = 0.3243
P < 0.01
100
0
0 0.1 0.2 0.3 0.4 0.5 0.6
Dietary Taurine (% DM)
Fig. 2. Whole blood versus dietary taurine concentrations in zoo felids (n 5 28).
TAU daily (or one teaspoon of clam juice daily) in the first bottle would provide the
required TAU supplement when using a puppy milk replacer without TAU, based
on a treatment protocol for oral administration of purified TAU from
Hoskins [1990]. This study shows the amount of TAU in one teaspoon (5.0 cc) of
clam juice is approximately 85 mg. One tablespoon (15.0 cc) would equal
approximately 250 mg. Adding strained meat human baby food to puppy milk
replacers as part of the weaning diet for zoo carnivores has been suggested in
hand-rearing protocols for two decades [Ewing, 1984; Hedberg, 2002], with no
incidence of TAU deficiency when using chicken meat-based baby food products
reported. Data, however, were limited for assessment of TAU content, so nutritional
adequacy of these diets was difficult to ascertain. Thus, the impetus to evaluate
TAU content started with hand-rearing diet ingredients used for wildlife, and
expanded to milk and diet composition as well as assessment of TAU status and
correlations among circulating blood, plasma, and dietary concentrations of this
essential nutrient.
As stated above, the feline milk replacer KMR is supplemented with TAU. A
1993 nutrient report for this product lists the TAU content as 0.05% DM, but the
current analysis showed the TAU content to be 0.033% DM. Esbilac, a puppy milk
replacer often used for hand rearing Panthera species [Hedberg, 2002], is not
supplemented with TAU. The analysis for TAU in a can of liquid Esbilac resulted in
a concentration of 0.007% DM. Comparing queen and bitch’s milk TAU
concentrations with the replacers, and assuming maternal milk samples reflect
TAU needed in those replacers, it would seem that the current TAU concentration is
not adequate for felids in the sample of KMR analyzed, and clearly too low in
Esbilac. This may have serious significance for the hand rearing of zoo felids, where
at times Esbilac is used as a substitute milk formula but clearly requires an additional
TAU supplement for use in felids.
The TAU content in the fishing cat milk sample taken in this study was lower
that reported in domestic queen milks (359 mg/L) consuming adequate TAU. This
was unexpected because of the fact that this sample comprised colostrum. Certainly
previous dietary history may have impacted the TAU content of milk, particularly
dietary TAU content and total sulfur amino acids. The calculated diet for this animal
contained slightly less than adequate TAU by comparison with requirements of
domestic cats. It is possible that the variety of whole prey (40% dressed rabbit, 35%
rat and mouse, 17% whole chicken, 5% herring, and 3% day-old chicks) impacted
the available TAU. The lion milk sample was higher in TAU (165 mg/L) but still
below what has been reported as normal for domestic cats. Research has shown that
a TAU-deficient diet can impact the TAU content of the milk from lactating cats,
with TAU concentration in milk of lactating females substantially higher in cats fed
higher TAU diets [Sturman and Messing, 1992]. Conversely the concentration of
TAU in the milk from TAU-deprived mothers is substantially lower than that
in the milk from TAU supplemented mothers [Sturman, 1991; Sturman and
Messing, 1991]. This may have contributed to the low TAU concentration in both
the lion and fishing cat milk reported here, as the dietary TAU content for the fishing
cats was calculated at 0.14–0.19% DM and the lion diet was estimated to contain
0.18% DM.
Researchers at the University of California at Davis fed domestic cats
whole ground rabbit containing apparently adequate TAU content of 0.13%
DM. These cats developed clinical signs consistent with TAU deficiency that
were reversed when the diet was supplemented with TAU. Rabbits were not
skinned, dressed, or cleaned, but rather ground in their entirety. The ground
whole rabbit diet was frozen in smaller batches and thawed before feeding
[Glasgow et al., 2002]. The cats in this study were likely impacted by the digestibility
of the protein; dietary indigestible protein may have an effect on the cat’s gut
microflora that have cholylhydrolase activity, and then destroy the released TAU
[Morris et al., 1994]. This information may have relevance when examining the
feeding strategies for adult African lion and adult fishing cats in our study, as they
were fed rabbits. Adding whole rabbits to the diet of the lions not only may have
lowered the TAU content in the overall diet, it seemed to reduce plasma TAU to
55 nmol/ml as well.
Feeding a mixture of a commercial carnivore diet and a commercial dry feline
diet in a ratio of 9 parts: part 1 (wt: wt ratio) may also have an impact on overall
TAU status. Two types of dry feeds were analyzed and had differing amounts of
TAU (Table 2). The mixed diet of dry cat food and a frozen commercial carnivore
diet provided 0.40% TAU (DM basis) using a product containing rice bran—
Eukanuba chicken and rice kitten dry food (Iams Co., Dayton, Ohio 45414 USA),
seemed to have had an impact on the cheetah’s TAU status, resulting in lower
plasma and whole blood TAU concentrations (10070.0 and 377.5763.5 nmol/ml,
respectively), compared to values from cheetahs fed diets that did not contain rice
bran, where baseline plasma values were approximately double when fed a
formulated diet without the dry component rice bran.
Felids in our study group with plasma TAU concentrations o50 nmol/ml were
being offered diets with relatively low normal TAU (r0.21%) concentrations. These
findings are consistent with research in the domestic cat showing that low plasma
values are indicators of low dietary TAU. Individuals vary greatly in their capacity
to regulate TAU metabolism when fed low-TAU diets. When diets were high in
TAU, the plasma concentrations were two to three times higher than corresponding
levels in animals fed low-TAU diets. Six-month-old hand-reared Bengal tigers (n 5 3)
consuming diets estimated to contain 0.14–0.18% TAU also showed low plasma
concentrations of TAU. These cubs received a milk formula low in TAU as well as
Nebraska products low in TAU. The whole blood values were also lower, but never
in a range considered deficient o200 nmol/ml.
Whole blood provides the best assessment of body status while plasma
levels provide a good measure of dietary intake [Hayes, 1988]. Whole blood
concentrations are more closely correlated with skeletal muscle TAU concentrations
than plasma during depletion studies, whereas plasma TAU concentrations seem to
be the most valuable predictor of skeletal muscle TAU concentrations during
repletion. The best clinical method to evaluate the TAU status of the cat is
determination and interpretation of both plasma and whole blood TAU concentra-
tions [Pacioretty et al., 2001]. Early indication of TAU deficiency is evident
when plasma TAU concentration is o40 nmol/ml, or whole blood o200 nmol/ml.
Severe TAU deficiency becomes evident at only 1/5 to 1/10 these concentrations
[Pion et al., 1987].
Although we found no significant differences among species or between sexes
in circulating TAU concentrations measured in this survey, younger animals are
expected to have higher TAU concentrations than older animals. This was noted in
an 8-week-old, mother-reared, ocelot kitten with plasma and whole blood TAU
concentrations of 301 and 760 nmol/ml, respectively [Hedberg unpublished data,
2006]. Circulating TAU is influenced after many hours of food deprivation; however,
this is not enough to cause whole blood to decline significantly though plasma values
may change 1–15%.
One would not necessarily, however, expect a direct correlation between
dietary and plasma concentrations of TAU, except below the requirement to
somewhat above the requirement. When an excess of TAU is present in the diet, the
excess is simply excreted in the urine and the plasma and tissues are held relatively
constant at a high concentration.
One last aspect to consider in evaluating TAU status is the use of products
designed for canids when feeding felids, which is often done for weight management
purposes owing to the lower fat content of canid diets. Canid products are rarely
designed with added TAU, and may thus be deficient when fed as an exclusive
diet to cats. Thus, multiple factors can impact TAU status in zoo felids; total
dietary concentrations, specific products, and even individual ingredients must be
evaluated.
ACKNOWLEDGMENTS
The authors express their gratitude to Pet Ag, Inc. for their generous grant to
support the blood TAU analyses. S&R Productions and the San Francisco
Zoological Gardens also contributed financial support for various blood and
dietary sample analysis. We appreciate assistance from Freeland Dunker, DVM,
Jacqueline Jencek, DVM, Laurie Gage, DVM, Ashley Sansome DVM and
Mike Simon, DVM in obtaining the blood samples for this study. Lynette
Chappell and Melody Hitzhusen of S&R Productions, Sarah Rieback of Safari
West Wildlife Preserve, Barbara Palmer of San Francisco Zoological Gardens
and Eric Calvo of Six Flags Discovery Kingdom were instrumental in supplying
the variety of commercial diets for analysis and supplying individual animal
diet information. Zengshou Yu of the University of California Davis Amino
Acid Laboratory, Dr. Russell Chesney and Andrea Patters of University of
Memphis, Department of Pediatrics provided assistance with research and statistical
analysis. Comments from L. Frank and E. Kuhn improved earlier versions of this
manuscript.
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