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© 2006 American Society for Nutrition J. Nutr. 136:2525-2533, October 2006

Nutrition and Disease

Low Plasma Taurine Concentration in Newfoundland Dogs is Associated with Low Plasma Methionine and Cyst(e)ine Concentrations and Low Taurine Synthesis1

Robert C. Backus2,*, Kwang Suk Ko3, Andrea J. Fascetti3, Mark D. Kittleson4, Kristin A. MacDonald4, David J. Maggs5, John R. Berg6 and Quinton R. Rogers3

2 Department of Veterinary Medicine and Surgery, College of Veterinary Medicine, University of Missouri-Columbia, Columbia MO 65211; and 3 Department of Molecular Biosciences, 4 Department of Medicine and Epidemiology, 5 Department of Surgical and Radiological Sciences, and 6 Department of Chemistry, University of California, Davis, CA 95616

* To whom correspondence should be addressed. E-mail: backusr{at}missouri.edu.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Although taurine is not dietarily essential for dogs, taurine deficiency and dilated cardiomyopathy (DCM) are sporadically reported in large-breed dogs. Taurine status and husbandry were examined in 216 privately owned Newfoundlands, a giant dog breed with high incidence of idiopathic DCM (1.3–2.5%). Plasma taurine concentration was positively correlated (P < 0.01) with plasma cyst(e)ine (r = 0.37) and methionine (r = 0.35) concentrations and was similar across age, sex, neutering status, body weight, and body-condition scores. Plasma taurine concentration was low (≤40 µmol/L) in 8% of dogs. Dogs with low plasma taurine were older, less active, had more medical problems and treatments, and had lower plasma albumin, cyst(e)ine, tryptophan, and {alpha}-amino-n-butyric acid concentrations than the other dogs (P < 0.05). Of 9 taurine-deficient, clinically evaluated dogs, 3 had DCM that was reversed by taurine supplementation and 1 had retinal degeneration. When given a diet apparently adequate in sulfur amino acids (5.4 g/kg) for 3 wk, 6 Newfoundlands (52.5 ± 2.3 kg, 3.5–7 y), compared with 6 Beagles (13.2 ± 2.3 kg, 5.5 y), had lower (P < 0.01) concentrations of plasma taurine (49 ± 16 vs. 97 ± 25 µmol/L) and cyst(e)ine and blood glutathione, lower (P < 0.01) de novo taurine synthesis (59 ± 15 vs. 124 ± 27 mg · kg–0.75 · d–1), and greater (P < 0.05) fecal bile acid excretion (1.7 ± 0.2 vs. 1.4 ± 0.2 µmol/g). Newfoundlands would appear to have a higher dietary sulfur amino acid requirement than Beagles, a model breed used in nutrient requirement determinations.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Nutrition has a recognized role in the development and progression of heart diseases. Unfortunately, the underlying mechanisms of many nutritional influences are not well understood (1). Recently, dilated cardiomyopathy (DCM),7 reportedly induced by diet, has been observed in privately owned adult dogs of varying genetic backgrounds (2–4). Common findings in affected dogs are large body size, very low blood taurine concentration, and maintenance on a lamb meal and rice-containing commercial diet. Dilated cardiomyopathy is among the most common of acquired heart diseases in dogs (5). Although still primarily a disease without a known cause, several etiologies have been proposed, including heritable genetic mutations, viral infections, immune-mediated disorders, arrhythmias, toxins, and nutritional deficiencies. Inadequate provision of dietary taurine will eventually result in systemic taurine deficiency in all cats and development of DCM in a high percentage of cats (6). A requirement for dietary taurine is not generally recognized in dogs. Like many species, dogs appear able to synthesize taurine from dietary methionine and cyst(e)ine in amounts sufficient to meet tissue needs (7).

The sulfur amino acid content of commercial diets given to dogs with taurine deficiency is reported to be well in excess of recommended dietary allowances (8). Nonetheless, methionine supplementation increases plasma taurine concentration in taurine-deficient dogs (3). Based on current knowledge of taurine metabolism, diet-induced taurine deficiency has several possible causes, including 1) insufficient synthesis of taurine (9), 2) extraordinary loss of taurine or its precursors in urine (10), 3) accelerated gastrointestinal loss of taurine in bile acid conjugates (11), and 4) low dietary concentrations and poor bioavailability of sulfur amino acids (3,12,13).

Until recently, taurine-deficient DCM in dogs has been mostly reported in one breed of small body size, American Cocker Spaniels (14). Although dietary taurine supplementation improves cardiac function in these dogs, the cause of taurine deficiency is unknown. Recent observations of taurine deficiency in unrelated large-breed but not small-breed dogs indicate that body size may be a contributing factor to the deficiency. Tôrres (15) has shown that plasma and skeletal muscle taurine concentrations are substantially lower in mongrels of large body size (36.0 ± 1.8 kg) than smaller Beagles (12.0 ± 0.5 kg) when the dogs are given the same diet. As a result, Tôrres et al. (16) suggested that dietary sulfur amino acid requirement of dogs scales disproportionately with metabolizable energy (ME) requirement.

The present study evaluated taurine status and husbandry practices in >200 privately owned Newfoundland dogs. Newfoundlands were studied because of their very large body size and propensity for the development of DCM (17). In addition to evaluation of taurine status, comparisons of de novo synthesis rates of taurine, excretion rates of bile acids, and blood and plasma concentrations of amino acids and thiols, including homocysteine, glutathione, and cysteinylglycine, were made between Newfoundland dogs and Beagles of similar age. Beagles were studied because of their historic use in establishing nutrient requirements of dogs (18). Our findings provide evidence of diet-induced taurine deficiency in dogs and associated DCM as well as insight into a probable cause of taurine deficiency observed in large-breed dogs.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Animals. Taurine status was evaluated in Newfoundland dogs at 3 specialty shows (n = 204) and a gathering arranged by a breeder (n = 17) during a 6-mo period (October 2002 to April 2003). The shows were held in Portland, Ore., Ellicottville, N.Y., and Dixon, Calif. Owner interest was the only criterion for participation. Taurine status was determined from concentrations of taurine in cephalic venous blood and plasma. Blood (5 mL) was obtained by venipuncture and was processed and stored for later analyses using previously described methods (19). Plasma was promptly (~15 min) separated from blood by centrifugation (7000 x g for 10 min) and a portion of it (0.5 mL) was immediately extracted 1:1 (v:v) with 60 g/L, 5-sulfosalicylic acid (SSA), and the resulting supernatant was stored frozen (–20°C) for later analysis.

At the time of blood collections, the age, sex, neuter status, body weight, and body-condition scores of dogs were also recorded. Body-condition score was assigned according to a 9-point integer scale (20). Owners completed a questionnaire concerning diet, husbandry, medical condition, and medications. The intensity of dogs' physical activity was categorized by assigning points (1–5) to owner responses to questions regarding housing condition (indoor, outdoor, both, outside mainly for walks and exercise) and activity level (type, duration, and frequency). Follow-up cardiac and ophthalmic examinations were offered to owners of dogs that were identified as having plasma taurine concentrations indicative of taurine deficiency. Findings of the examinations were expected to support the proposal that the dogs were taurine deficient.

To evaluate taurine synthesis, 2 groups of dogs were studied. One group of 6 Newfoundlands, maintained and housed by their owners, consisted of adult (3.5–7 y, 52.5 ± 2.3 kg) sexually intact males (n = 2), orchiectomized males (n = 2), and ovariohysterectomized females (n = 2). The second group of 6 Beagles were all purpose-bred adult (5.5 y, 13.2 ± 2.3 kg) sexually intact males that were individually housed in temperature- and light-controlled runs of the Center for Laboratory Animal Science, University of California, Davis. Husbandry and use of Beagles were reviewed and approved by the University Animal Use and Administrative Advisory Committee. Beagles were maintained in accordance with the NRC Guide for the Care and Use of Laboratory Animals (21).

    Diets. Diets and feeding practices used by owners were identified from questionnaire responses. Owners listed foods and food products, brands, and forms, and they reported duration of food use, meal amounts, and meal frequency. Treats and supplements were also listed. Information on feeding practices was gained from responses to questions regarding the persons responsible for feeding, food storage, feeding environment, and potential for dog's access to unmonitored food sources.

Beagles and Newfoundlands in which taurine synthesis rates were determined were given water continuously and once each day, for 3 wk, a commercial dry-type (extruded) diet (AvoDerm Adult Lamb Meal & Rice Dry Formula, Breeder's Choice Pet Foods) formulated to meet nutrient profiles for all life stages (8). The ME density and methionine plus cyst(e)ine content of the diet were reported to be 15.7 kJ/kg and 5.4 g/kg, respectively (22). Taurine in the diet was determined to be 280 mg/kg by analysis of water extract of the diet (23). Proximate contents of the diet as indicated from the label's guaranteed analysis were (g/kg): crude protein, 200; crude fat, 110; crude fiber, 30; and moisture, 100. Listed ingredients of the diet were lamb meal, brown rice, ground rice, rice bran, chicken fat (preserved with mixed tocopherols and ascorbic acid), flax seed, dehydrated alfalfa meal, dried egg product, avocado oil, lecithin, brewers dried yeast, natural flavoring, monosodium phosphate, choline chloride, rosemary extract, sage extract, ferrous sulfate, dl-{alpha}-tocopheryl acetate, zinc oxide, sodium selenite, manganous oxide, riboflavin supplement (source of vitamin B complex), copper sulfate, zinc methionine, iron proteinate, manganese proteinate, copper proteinate, cobalt proteinate, niacin, vitamin B-12 supplement, vitamin A supplement, calcium pantothenate, d-biotin supplement, pyridoxine hydrochloride, calcium iodate, thiamine mononitrate, folic acid, vitamin D-3 supplement, bromelain, papain, dried bacillus subtilis fermentation product, and dried aspergillus oryzae fermentation product.

    Clinical evaluations. Ophthalmic examinations were conducted by board-certified veterinary ophthalmologists using slit lamp biomicroscopy performed before and after full pharmacologic mydriasis and binocular indirect ophthalmoscopy performed after full pharmacologic mydriasis. Cardiac examinations were conducted without sedation by board-certified veterinary cardiologists using 2-D, M-mode, and color-flow Doppler echocardiography.

    Taurine synthesis. Beagles and Newfoundlands were given the commercial diet in amounts estimated to meet their maintenance ME needs based on body weight [552 x body weight kg0.75, kJ/d, (18)]. After dietary adaptation, body weight and body-condition scores were determined and cephalic venous blood (3 mL) and free-catch urine (≥5 mL) were collected. Subsequently, each dog ingested 14.6 mg/kg of 99 atom percentage of deuterated taurine (H2NCD2CD2SO3H, CDN Isotopes) in a gelatin capsule hidden in a marshmallow. At ~1000 h on the following 5 d, the free-catch urine sampling was repeated. Urine samples were frozen soon after collection. Taurine and creatinine concentrations were determined in urine collected on d 5. Blood samples were processed and stored as described for the taurine status survey. During the urine collection period, all feces were collected for each dog and stored frozen until they were later pooled, blended in aqueous slurry, and their dry matter weight and bile acid content determined. Bile acids were extracted from the feces as described by Porter et al. (24) and bile concentration was determined with a commercial kit (Kit 450A, Trinity Biotech).

    Biochemical analysis. Taurine and other amino acid contents of SSA extracts of blood, plasma, and urine were determined using dedicated amino acid analyzers (System 7300, Beckman Instruments and Biochrom 30, Biochrom) as previously described (25). Because of sample losses during amino acid analyses, amino acid profiles could be determined only in the plasma of 195 dogs. Frozen plasma and blood not treated with SSA were incubated with a reducing agent and the resulting concentrations of cysteine, homocysteine, cysteinylglycine, and glutathione were determined using the method described by Tôrres et al. (19). Concentrations of thiols determined included disulfide forms of thiols that may or may not have been bound to plasma proteins prior to reducing agent exposure. The SSA extraction of plasma was presumed to have oxidized plasma cysteine to cystine (19). Cystine concentration measured in SSA extracts of plasma was designated "free cyst(e)ine" and assumed to include unbound cysteine and cystine occurring in plasma at the time of sampling.

Urine creatinine concentration was determined with a commercial kit (Cold Stable, Pointe Scientific). Plasma albumin concentration was determined with an automated chemistry analyzer (AU440e, Olympus America) by the Veterinary Diagnostic Laboratory, College of Veterinary Medicine, University of Missouri, Columbia, MO.

Enrichment of deuterated taurine in the urine samples was determined by a modification of the method by Fay et al. (26). Modifications were related to analysis of deuterium enrichment in the taurine label using GC-MS (Model 3400 GC equipped with a Model 8200 autosampler coupled to either a Saturn 3 or Finnigan ITS40 ion trap mass spectrometer, Varian Analytical Instruments). Column heating was programmed at 10°C/min from 130 (2.0 min hold) to 260°C (5.0 min hold). MS of deuterated-taurine derivative revealed a unique fragment of 241 m/z. Ratio of amplitudes of fragment signals at 241 and 238 m/z was proportional to deuterium enrichment in analyzed taurine, when the amplitudes of fragment signals were integrated over taurine chromatographic peak duration (usually 7 scans). Integration appeared necessary because of a slight difference between retention times of deuterated and native taurine derivatives.

    Statistical analysis. Normalities of the survey blood and plasma taurine concentrations were evaluated with Shapiro-Wilk tests (version 9.1, SAS Institute). General Linear Models ANOVA and post-hoc least-squared difference analysis were used to determine significance of differences across age tertiles with respect to sex on body weight, body-condition score, blood and plasma taurine concentrations, and plasma thiol concentrations. Student's t tests were used to determine the significance of differences with respect to neutering (neutered vs. intact) and taurine status (plasma taurine concentration ≤40 µmol/L vs. >40 µmol/L). Significance of correlations between biochemical variables was determined with linear regression analysis. Chi-square analysis was used to determine the significance of differences with respect to taurine status on proportions of dogs exposed to variables indicative of feeding practice, husbandry, and medical condition. Unless specified, variance estimates associated with reported means represent SD. Differences with a P < 0.05 were considered significant.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    Survey findings. Blood and plasma taurine concentrations were determined in 216 Newfoundland dogs. Sex distribution, neutering status, and age range among the dogs are shown in Table 1. Body weight and body-condition score of dogs in youngest tertile (<2.2 y) were less (P < 0.05) than those of dogs in older tertiles (Table 1). Body weight of males (57.1 ± 11.9 kg) was greater (P < 0.05) than that of females (49.1 ± 9.2 kg), whereas, body-condition score of males (5.3 ± 0.8) was lower (P < 0.05) than that of females (5.5 ± 0.8). Because few dogs were neutered in the youngest tertile, significance of neutering (orchiectomy and ovariohysterectomy) on body weight, body-condition score, and other study variables was evaluated only in dogs of the older 2 tertiles. Neutered dogs had a body-condition score (5.8 ± 0.9) that was greater (P < 0.05) than that of sexually intact dogs (5.4 ± 0.7). However, these dogs had a body weight (54.0 ± 9.1 kg) that was less (P < 0.05) than that of intact dogs (56.7 ± 8.4 kg).


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  		TABLE 1 Taurine status survey findings by age, sex, and neuter status for body weight and body-condition score1

 
Taurine concentrations in blood and plasma varied widely but were normally distributed (Fig. 1). Taurine concentration in blood was 226 ± 57 µmol/L, whereas in plasma it was 81.1 ± 34.9 µmol/L. Owners of 7 dogs reported that taurine was given as a supplement. Among these dogs, taurine concentrations in blood and plasma were 294 ± 85 and 137 ± 77 µmol/L, respectively. Observations from these dogs were not considered in other analyses. Approximately 8% (n = 18) of dogs had a plasma taurine concentration ≤40 µmol/L. Taurine findings were grouped by age tertile and evaluated across groups (Table 2). Blood taurine concentration in dogs in the youngest tertile was slightly greater (P < 0.05) than the concentration in dogs of older tertiles. Concentration of taurine in plasma did not differ among age groups. Blood and plasma taurine concentrations did not differ between neutered and intact dogs.


Figure 1
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  		Figure 1  Frequency histogram of blood and plasma taurine concentrations found in Newfoundland dogs (n = 216) during a 6-mo period. Bars represent number of dogs with taurine concentrations within the range indicated on the x-axis.

 

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  		TABLE 2 Taurine status survey findings by age for concentrations of plasma and blood taurine, cysteine, homocysteine, cysteinylglycine, and glutathione1

 
Concentrations of plasma thiols, with the exception of homocysteine, differed slightly across age tertiles (Table 2). Plasma glutathione and cysteinylglycine concentrations in the youngest tertile were greater (P < 0.05) than concentrations of these thiols in older tertiles. Plasma cysteine and free cyst(e)ine concentrations in dogs of the youngest tertile were less than (P < 0.05) that in dogs of the oldest tertile, but did not differ from that in middle-age tertile dogs. Males had a higher (P < 0.05) plasma cysteine concentration than females, but there was no difference between sexes for free cyst(e)ine concentration. Plasma cysteine and free cyst(e)ine concentrations were positively correlated (P < 0.01), but the CV was only 0.47 (Fig. 2). Plasma free cyst(e)ine concentration was 20 ± 6% of the plasma total cysteine concentration.


Figure 2
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  		Figure 2  Relation between plasma concentrations of free cyst(e)ine (f-Cys) and cysteine (Cys) and free cyst(e)ine and methionine (Met) in Newfoundland dogs surveyed for their taurine status. Plotted points are observations in individual dogs. Plotted lines are derived from linear regression analysis of f-Cys observations on Cys and Met observations (Cys = 1.3 x f-Cys + 98 µmol/L, P < 0.01, r = 0.46; Met = 0.62 x f-Cys + 45 µmol/L, P < 0.01, r = 0.33).

 
Plasma taurine concentration was weakly positively correlated (P < 0.01, r = 0.24) with plasma cysteine concentration and more strongly positively correlated with plasma concentrations of free cyst(e)ine (P < 0.01, r = 0.37) and methionine (P < 0.01, r = 0.34) (Fig. 3). Plasma methionine concentration was positively correlated with plasma concentration of free cyst(e)ine (P < 0.01, r = 0.33) (Fig. 2), but did not correlate (P < 0.08, r = 0.14) with cysteine. Other significant correlations were not found between assayed thiols and taurine concentrations in plasma. Plasma homocysteine concentration was very weakly positively correlated (P < 0.01, r = 0.24) with plasma methionine concentration and very weakly negatively correlated (P < 0.02, r = 0.20) with blood taurine concentration. Plasma glutathione concentration was positively correlated (P < 0.01, r = 0.35) with plasma cysteinylglycine but did not correlate with plasma concentrations of methionine, cysteine, or free cyst(e)ine.


Figure 3
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  		Figure 3  Relation between plasma concentrations of free cyst(e)ine (f-Cys) and taurine and plasma concentrations of methionine (Met) and taurine in Newfoundland dogs surveyed for their taurine status. Plotted points are observations in individual dogs. Plotted lines are derived from linear regression analyses of taurine observations on f-Cys and Met observations (taurine = 0.10 x f-Cys + 17 µmol/L, P < 0.01, r = 0.37; taurine = 0.20 x Met + 46 µmol/L, P < 0.01, r = 0.34).

 
Blood and plasma taurine observations were grouped in quartiles by concentration (Fig. 4). Albumin concentration was determined in samples of plasma from dogs of the lowest plasma taurine concentration quartile. For comparison purposes, albumin concentration was determined in an equivalent number (n = 17) of randomly selected samples of plasma from the second quartile that had a taurine concentration in the mid range of the quartile (73 to 79 µmol/L). Albumin concentration in plasma of the lowest quartile (270 ± 50 g/L) was less (P < 0.02) than that of the second quartile (310 ± 20 g/L).


Figure 4
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  		Figure 4  Population quartile concentrations of taurine determined in blood and plasma from Newfoundland dogs (n = 216) and dogs of varying body size and genetic backgrounds (n = 131 [38]). Values are means ± SEM.

 
Dogs with plasma taurine concentrations ≤40 µmol/L compared with dogs having greater plasma taurine concentrations had lower blood taurine concentrations (P < 0.01) and lower concentrations of plasma cysteine (P < 0.02), free cyst(e)ine (P < 0.03), tryptophan (P < 0.01), and {alpha}-amino-n-butyric acid (P < 0.01) (Table 3 and Fig. 5). Plasma concentrations of other thiols and amino acids assayed did not differ between dogs with plasma taurine concentrations ≤40 µmol/L and dogs with greater taurine concentrations.


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  		TABLE 3 Comparison of survey observations between Newfoundland dogs with plasma taurine concentrations that are low (≤40 µmol/L) and dogs with reputedly adequate plasma taurine concentrations (>40 µmol/L)1

 

Figure 5
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  		Figure 5  Plasma amino acid concentrations in Newfoundland dogs with plasma taurine concentrations ≤ 40 µmol/L (n = 11) and in dogs with greater plasma taurine concentrations (n = 145). Values are means ± SD. *Different from dogs with plasma taurine >40 µmol/L, P < 0.05. Nonstandard abbreviations for {alpha}-amino-n-butyric acid, cyst(e)ine, and hydroxyproline are AABA, half-Cys, and HO-Pro, respectively.

 
Dogs with plasma taurine concentrations ≤40 µmol/L were older (P < 0.05), less active (P < 0.03), had more (P < 0.03) active medical problems (59 vs. 33%), and received more (P < 0.02) medications than dogs with greater plasma taurine concentrations (Table 3). Body weights and body-condition scores of dogs with plasma taurine concentrations ≤40 µmol/L did not differ from those in dogs with greater plasma taurine concentrations. For observations related to husbandry, significant differences between these groups were not found. Descriptions of medical problems were so varied that evaluations of problems with respect to taurine status were not conducted. Medical problems could be categorized to involve joint, bone, and muscle (21.4%), integument (21.4%), heart (17.9%), thyroid gland (6.0%), eye (6.0%), and other tissues and organs (21.4%).

The foods given to dogs varied in type, amount, and duration of use prior to the survey. They included commercially prepared dry (extruded), canned, and frozen diets, home-prepared diets, treats, and nutritional supplements. Most (93%) dogs received one or more commercial diet as a principal food source. Dry and canned diets were given to 88 and 39% of the dogs, respectively. Only 38% received a single commercial diet (43 different diets). The large variation in food sources precluded analysis of the influence of diet on taurine status.

The use of one or more supplements was reported in 86% of dogs. Of supplements, 56% appeared to have ingredients or labels intended for the prevention or treatment of joint diseases (chondroitin, glucosamine, "MSM," "Glycoflex," "Cosequin," "Move Free"). The proportion of dogs given such supplements tended to differ (P < 0.09) between dogs with plasma taurine ≤40 µmol/L (73%) and dogs with a greater plasma taurine concentration (50%).

    Clinical evaluations. Of dogs with plasma taurine concentrations ≤40 µmol/L, 9 were presented for cardiac and ophthalmic evaluations. Heart murmur, arrhythmia, valvular insufficiency, and overt clinical signs of heart failure were not observed. Three dogs had ventricular dimensions and shortening fractions (< 22%) consistent with DCM (27) (Fig. 6). These dogs were given 1 g of taurine twice each day and a follow-up cardiac evaluation ≥4 mo after taurine supplementation. Minor dietary modification to increase protein and sulfur amino acid intake was recommended for 1 of 3 dogs because of owner-reported cystinuria and observed low plasma albumin concentration (21 g/L). On re-evaluation, shortening fractions of the dogs substantially increased (P < 0.01) from a mean of 15 ± 14 to 37 ± 6%.


Figure 6
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  		Figure 6  M-mode echocardiography indices of left ventricular function in Newfoundland dogs (n = 9) with plasma taurine concentrations ≤40 µmol/L (obs). Reported reference ranges (RR) of left ventricular end-diastolic diameter (LVIDd) and left ventricular end-systolic diameter (LVIDs) in healthy controls of a previous study of Newfoundland dogs (27) are plotted with bars indicating range maximums and minimums. The fractional shortening (FS) percentage expected (expd) in the 50th, 90th, and 10th percentile of normal healthy dogs are plotted as a black closed circle and bars above and below the circle, respectively. Indices of 3 dogs with FS % <22 after being given taurine for ≥4 mo are plotted (+ tau) with lines connecting pretreatment indices in the dogs.

 
Two of 9 dogs clinically evaluated had ocular fundus abnormalities. In one dog, which had normal cardiac function, 2 small hypomelanotic regions (1/4 to 1/2 of optic disc diameter) were noted in the nontapetal fundus, and a focal region (1/2 optic of disc diameter) of pigment migration and tapetal hyper-reflectivity was noted in the tapetal fundus. The other dog, which had cystinuria and a low cardiac shortening fraction (12%), had moderate, generalized retinal vascular attenuation and tapetal hyper-reflectivity, and apparent difficulty negotiating a maze under scotopic but not photopic conditions. Fundic findings and maze performance were not notably different 4 mo after taurine supplementation. Ocular anterior segment abnormalities in the 9 evaluated dogs involved lens (nuclear sclerosis; n = 7), eyelids (entropion or ectropion; n = 5), or iris (cysts or atrophy or pupillary reflex abnormalities; n = 3).

    Taurine synthesis. During prefeeding and sample collection periods, each Beagle lost body weight, although all diet food given was consumed. Body weight losses were between 0.4 and 13.7% of prefeeding weights. On study completion, ME intake for each Beagle was calculated and normalized to end metabolic body weight. Mean ME intake among the Beagles was 583 ± 25 kJ · d–1· kg–0.75.

Within the first week of the prefeeding period for the Newfoundlands, some owners reported undesired body weight gain. Concerned owners were instructed to reduce the amount of diet given so that body condition was unchanged. By the end of the study, 4 Newfoundlands had gained weight (+ 3.2 to 7.4%), whereas 2 had lost weight (–1.9%). Weight of food each Newfoundland consumed was determined from the difference in weight between food given and food returned by each owner. Using these differences and end body weights, mean ME intake among the Newfoundlands was calculated to be 421 ± 98 kJ ·d–1· kg–0.75, an amount appreciably lower (P < 0.01) than that found for the Beagles.

Blood and plasma taurine concentrations of Newfoundland dogs were less than those of Beagles by 27 (P < 0.01) and 49% (P < 0.01), respectively (Table 4). Concentrations of blood glutathione and plasma cysteine in Newfoundlands were also less than those in Beagles (P < 0.01). Plasma cysteinylglycine concentration in Newfoundlands was greater (P < 0.01) than that in Beagles. Plasma concentrations of other thiols did not differ between dog groups. The ratio of taurine to creatinine in urine of Newfoundlands (14 ± 10 µmol/mmol) was substantially less (P < 0.05) than that in urine of Beagles (106 ± 58 µmol/mmol).


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  		TABLE 4 Blood and plasma concentrations of taurine and cysteine (Cys), homocysteine (Hcys), cysteinylglycine (Cys-gly) and glutathionine (GSH) in Newfoundland dogs and Beagles given the same diet1

 
Taurine synthesis rate in Newfoundlands was greater (P < 0.01) than that in Beagles (Table 5). However, with normalization to metabolic body weight or estimated liver weight, the taurine synthesis rate in Newfoundlands was less (P < 0.01) than that in Beagles by >50%. Total fecal bile acid excretion and excretion of bile acids/g of fecal dry matter by the Newfoundlands were greater (P < 0.05) than those excretions by the Beagles. Percentage dry matter digestibility did not differ between Newfoundlands (82 ± 4%) and Beagles (83 ± 5%).


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  		TABLE 5 Total de novo taurine synthesis and synthesis normalized by metabolic body weight (MBW) and liver weight (LW) and total fecal bile acid excretion and excretion normalized by weight of fecal dry matter (FDM) in Newfoundland dogs and Beagles given the same diet1

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
The importance of taurine to tissues is evident in functional losses that occur with taurine deficiency. These include reduced or abnormal cardiac contractility, vision, growth, motor function, immunity, and reproduction (28–30). Fortunately, for the purpose of identifying taurine deficiencies in tissues, concentrations of taurine in blood, plasma, and urine reflect taurine concentrations in tissues (31). Unfortunately, the relations between concentrations of taurine in tissues and those in blood, plasma, and urine are not linear, and they vary with the duration of taurine deficiency and the species and tissues studied (32).

In the present survey of Newfoundland dogs, a wide variation in the taurine concentrations of blood and plasma was observed (Fig. 1). This variation may reflect physiologically important variations in tissue function related to taurine status. Correlative measurements of various tissue taurine concentrations and performance variables of tissues are needed to determine healthy ranges of blood and plasma taurine concentrations in dogs. Kramer et al. (33), in their survey of plasma taurine in dogs with and without heart disease, found that 44 µmol/L was the lowest plasma taurine concentration in healthy dogs. Based on this report, a plasma taurine concentration ≤40 µmol/L was considered low in the present survey. Although selection of 40 µmol/L was arbitrary, a few observations appeared to support the use of this limit. Dogs with a plasma taurine concentration ≤40 µmol/L were less active, had more medical problems, and received more therapeutic medication than dogs with greater plasma taurine concentrations (Table 3). Also, for the 9 dogs that were clinically evaluated, evidence of a myocardial dysfunction reversible by taurine administration was found when plasma taurine concentration was ≤40 µmol/L (Fig. 6). Interpretation of these findings is, unfortunately, confounded by differences age and incidence of neutering. Dogs with a plasma taurine concentration ≤40 µmol/L were older than other dogs surveyed, by a mean of 2 y. Incidence of health problems is expected to increase with age, and physical activity is expected to decrease with age and neutering. Nonetheless, as a group, dogs with a plasma taurine concentration ≤40 µmol/L were only middle aged (5.7 ± 3.7 y) in the lifespan of large-breed dogs (34). Furthermore, significant differences in plasma taurine concentrations were not found between intact and neutered dogs of the survey (Table 1).

Ophthalmic examinations were conducted because of a well-recognized association between taurine deficiency and retinal degeneration in cats (35) and brief reference to cat-like retinal lesions in 3 American Cocker Spaniels with a low plasma taurine concentration (36). Evidence of generalized retinal degeneration was observed in only 1 of the 9 taurine-deficient dogs evaluated. It was not possible to directly attribute the retinal degeneration to taurine deficiency for several reasons. Taurine-deficient retinopathy in cats first causes characteristic ophthalmoscopic changes in the area centralis before progressing to cause generalized retinal degeneration indistinguishable from that caused by many other factors. The cone and ganglion cell-rich area, centralis, is not present in the canine fundus and retinal degeneration in this dog was moderately advanced and lacked any pathognomonic features with respect to cause. This dog's retinal degeneration was consistent with, but not pathognomonic for, inherited progressive retinal atrophy. The disease is recognized commonly in many dog breeds, but prevalence in the Newfoundland breed is not high (37). Although taurine deficiency may have contributed to retinal degeneration in this dog, the present findings indicate that taurine deficiency in Newfoundland dogs is not commonly associated with retinal degeneration.

Plasma taurine concentration was positively correlated with plasma concentrations of methionine, cysteine, and free-cyst(e)ine (Fig. 3). These findings agree with previous observations in dogs (38) and are consistent with methionine and cyst(e)ine utilization for synthesis of taurine. Correlations between plasma concentrations of taurine, methionine, and cyst(e)ine are probably weak for several reasons. Foremost of these may be normal liver homeostasis of methionine and cyst(e)ine, both of which are potentially toxic in excess (39). Also, plasma collections were not synchronized with meals. Stronger correlations would be expected in portal venous plasma collected consistently with respect to meals. Correlations between plasma concentrations of taurine, methionine, and cyst(e)ine may also be weak because dietary taurine concentration, although probably low in commercial dog diets (40), varied independently with dietary sulfur amino acid concentration.

The mean of each quartile of blood and plasma taurine concentration in the Newfoundlands surveyed was lower than corresponding means reported in healthy dogs of a variety of breeds for which mean body size is smaller than that of Newfoundlands (38) (Fig. 4). Lower taurine status of Newfoundlands may be unique to the breed. However, it is consistent with the hypothesis that body size influences the risk for developing taurine deficiency (16). Blood, plasma, and urine taurine concentrations, all indicators of tissue taurine concentrations, were lower in Newfoundlands relative to Beagles (Table 4), even though all dogs were given the same diet.

The difference in taurine status between Newfoundlands and Beagles appears to be well explained by differences in de novo taurine synthesis. On the bases of metabolic body weight and liver weight, the Newfoundlands had less than half of the taurine synthesis rates of Beagles (Table 5). Relative to Beagles, Newfoundlands consumed less food on a metabolic body weight basis to maintain their body weight. This difference agrees with previous findings on ME requirements in dogs (41). As a consequence, Newfoundlands had lower total intakes of methionine and cystine relative to the Beagles. Lower concentrations of plasma cysteine and blood glutathione in Newfoundlands, relative to Beagles, probably reflect lower intakes of methionine and cysteine by the Newfoundlands (Table 4). Similarity of plasma glutathione concentrations between Newfoundlands and Beagles seems inconsistent with differences in sulfur amino acid intake. However, plasma glutathione concentration may be more tightly regulated than plasma cyst(e)ine and blood glutathione concentrations. Erythrocyte glutathione concentration might decline because erythrocyte glutathione is synthesized from cysteine and not acquired from plasma (42). In applying these findings to the interpretation of taurine-status survey observations, it is noteworthy that the small difference in plasma cysteine concentration (14%) between Newfoundlands and Beagles was associated with a much larger difference in taurine synthesis (52%) and plasma taurine concentration (49%). Also of worthwhile note, is that blood glutathione concentration may not be maximal when plasma taurine concentration is >40 µmol/L (Table 4).

The synthesis of taurine, which occurs mostly in liver, has lower priority than the synthesis of either protein or glutathione (39). Hence, taurine status, as reflected in plasma, blood, and urine taurine concentrations, should serve as an early and sensitive indicator of otherwise unapparent declines in protein or glutathione synthesis caused by sulfur amino acid deficiency. For this reason, the practice of adding taurine to dog foods to prevent taurine deficiency may be inappropriate. Sulfur amino acid deficiency for other needs may also be indicated by low taurine status.

Low plasma albumin concentration presently observed in dogs that had plasma taurine concentrations ≤40 µmol/L could have reflected limited sulfur amino acid availability for protein synthesis. However, differences in availability of other amino acids or protein in general could have accounted for plasma albumin observations. For example, plasma tryptophan concentration in dogs with a plasma taurine concentration ≤40 µmol/L were lower than those of other dogs (Fig. 5). The lower tryptophan might have indicated that tryptophan was the first or second amino acid–limiting protein synthesis in taurine-deficient dogs (25). Tryptophan, like methionine and cysteine, is susceptible to destruction by heat processing (43). Taurine deficiency in dogs is suggested to result from reduced sulfur amino acid bioavailability in dietary ingredients that are heat processed, such as rendered meat meals (3,16). Indeed, effects of heat processing on bioavailability are not always evident from a chemical analysis of dietary amino acids (44). All dogs with a plasma taurine concentration ≤40 µmol/L received heat-processed commercial diets as a principal source of their ME intake. Although most of the other dogs surveyed received similar diets, a unique attribute of taurine-deficient dogs may have been their increased sensitivity to low sulfur amino acid bioavailability. A low-maintenance energy requirement, perhaps from inactivity, may have been such an attribute.

Increasing dietary protein content would appear to be appropriate for treating Newfoundlands with taurine deficiency. However, protein quality should be considered.

Studies in cats show that increasing the concentration of poor quality protein in diets increases microbial-mediated, gastrointestinal loss of taurine, probably through inhibition of reabsorption of taurine carried in bile acids (11,45,46). Like cats, dogs can only conjugate bile acids with taurine (47,48). Therefore, increasing dietary protein concentration might accelerate taurine loss more than its synthesis if the protein quality or sulfur amino bioavailability is poor. Greater excretion of fecal bile acids by Newfoundlands relative to Beagles (Table 5) agrees with a previous finding in dogs indicating that bile acid excretion increases with body size (15).

In summary, taurine status and husbandry practices were evaluated in >200 privately owned Newfoundland dogs, a breed of large body size in which idiopathic DCM occurs with high incidence and taurine deficiency has been identified. A substantial number of dogs had a plasma taurine concentration that, from previous studies, is indicative of taurine deficiency. These dogs, evaluated relative to other dogs, were older, less active, and had more medical problems and treatments. Relatively few dogs were presented for later clinical evaluation. Some taurine-deficient dogs had a DCM that was reversed after taurine supplementation. Retinal degeneration similar to that described in cats as a result of taurine deficiency was not observed. Comparisons between a small group of Newfoundlands and an equivalent number of Beagles given the same diet indicated that taurine deficiencies probably result from inadequate taurine synthesis to meet taurine losses. Biochemical comparisons between taurine-deficient and taurine-replete dogs, and correlations between plasma amino acid and thiol concentrations, indicate that low sulfur amino acid intake may account for the low taurine synthesis observed. If Newfoundland dogs are representative of large-breed dogs, future studies should determine whether sulfur amino acid requirement of dogs scales disproportionally with metabolic energy requirement.


   ACKNOWLEDGMENTS
 
The authors thank Dr. Gabrielle Cohen for her assistance with the recruitment of dog owners and the coordination of sample collections.


   FOOTNOTES
 
1 Supported by the American Kennel Club Canine Health Foundation. The contents of this publication are solely the responsibility of the authors and do not represent the view of the foundation. Back

7 Abbreviations used: DCM, dilated cardiomyopathy; ME, metabolizable energy; SSA, 5-sulfosalicylic acid. Back

Manuscript received 11 May 2006. Initial review completed 2 June 2006. Revision accepted 7 July 2006.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 

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