Urinary recovery of orally administered chromium 51–labeled EDTA, lactulose, rhamnose, d-xylose, 3-O-methyl-d-glucose, and sucrose in healthy adult male Beagles

Rafael Frias Central Animal Laboratory, University of Turku, 20520, Turku, Finland.
Department of Equine and Small Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, FI-00014 Helsinki, Finland.

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Jörg M. Steiner Department of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843.

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David A. Williams Department of Small Animal Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843.

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Satu Sankari Department of Equine and Small Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, FI-00014 Helsinki, Finland.

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Elias Westermarck Department of Equine and Small Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, FI-00014 Helsinki, Finland.

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Abstract

Objective—To provide values for gastrointestinal permeability and absorptive function tests (GIPFTs) with chromium 51 (51Cr)-labeled EDTA, lactulose, rhamnose, d-xylose, 3-O-methyl-d-glucose, and sucrose in Beagles and to evaluate potential correlations between markers.

Animals—19 healthy adult male Beagles.

Procedures—A test solution containing 3.7 MBq of 51Cr-labeled EDTA, 2 g of lactulose, 2 g of rhamnose, 2 g of d-xylose, 1 g of 3-O-methyl-d-glucose, and 8 g of sucrose was administered intragastrically to each dog. Urinary recovery of each probe was determined 6 hours after administration.

Results—Mean ± SD (range) percentage urinary recovery was 6.3 ± 1.6% (4.3% to 9.7%) for 51Cr-labeled EDTA, 3.3 ± 1.1% (1.7% to 5.3%) for lactulose, 25.5 ± 5.0% (16.7% to 36.9%) for rhamnose, and 58.8% ± 11.0% (40.1% to 87.8%) for 3-O-methyl-d-glucose. Mean (range) recovery ratio was 0.25 ± 0.06 (0.17 to 0.37) for 51Cr-labeled EDTA to rhamnose, 0.13 ± 0.04 (0.08 to 0.23) for lactulose to rhamnose, and 0.73 ± 0.09 (0.60 to 0.90) for d-xylose to 3-O-methyl-d-glucose. Median (range) percentage urinary recovery was 40.3% (31.6% to 62.7%) for d-xylose and 0% (0% to 0.8%) for sucrose.

Conclusions and Clinical Relevance—Reference values in healthy adult male Beagles for 6 of the most commonly used GIPFT markers were determined. The correlation between results for 51Cr-labeled EDTA and lactulose was not as prominent as that reported for humans and cats; thus, investigators should be cautious in the use and interpretation of GIPFTs performed with sugar probes in dogs with suspected intestinal dysbiosis.

Abstract

Objective—To provide values for gastrointestinal permeability and absorptive function tests (GIPFTs) with chromium 51 (51Cr)-labeled EDTA, lactulose, rhamnose, d-xylose, 3-O-methyl-d-glucose, and sucrose in Beagles and to evaluate potential correlations between markers.

Animals—19 healthy adult male Beagles.

Procedures—A test solution containing 3.7 MBq of 51Cr-labeled EDTA, 2 g of lactulose, 2 g of rhamnose, 2 g of d-xylose, 1 g of 3-O-methyl-d-glucose, and 8 g of sucrose was administered intragastrically to each dog. Urinary recovery of each probe was determined 6 hours after administration.

Results—Mean ± SD (range) percentage urinary recovery was 6.3 ± 1.6% (4.3% to 9.7%) for 51Cr-labeled EDTA, 3.3 ± 1.1% (1.7% to 5.3%) for lactulose, 25.5 ± 5.0% (16.7% to 36.9%) for rhamnose, and 58.8% ± 11.0% (40.1% to 87.8%) for 3-O-methyl-d-glucose. Mean (range) recovery ratio was 0.25 ± 0.06 (0.17 to 0.37) for 51Cr-labeled EDTA to rhamnose, 0.13 ± 0.04 (0.08 to 0.23) for lactulose to rhamnose, and 0.73 ± 0.09 (0.60 to 0.90) for d-xylose to 3-O-methyl-d-glucose. Median (range) percentage urinary recovery was 40.3% (31.6% to 62.7%) for d-xylose and 0% (0% to 0.8%) for sucrose.

Conclusions and Clinical Relevance—Reference values in healthy adult male Beagles for 6 of the most commonly used GIPFT markers were determined. The correlation between results for 51Cr-labeled EDTA and lactulose was not as prominent as that reported for humans and cats; thus, investigators should be cautious in the use and interpretation of GIPFTs performed with sugar probes in dogs with suspected intestinal dysbiosis.

Gastrointestinal permeability tests have been used to noninvasively assess mucosal damage in humans and several other animal species, including dogs, in clinical and research settings. These tests have been considered valuable for use in the diagnosis of primary intestinal defects and also for monitoring improvement in the intestinal barrier after treatment. Furthermore, information obtained with gastrointestinal permeability tests may be complemented with results of absorptive function tests, which provide information on the small intestinal absorptive capacity.1,2 In dogs, GIPFTs can be performed by simultaneous oral administration of specific markers and quantification of their subsequent concentrations or percentage recoveries in blood or urine.3–7 In general, 51Cr-labeled EDTA is considered the optimal intestinal permeability marker, specifically because it is easy to measure and cannot be degraded by intestinal bacteria. However, a combination of disaccharide and monosaccharide probes is currently used more commonly because use of the sugar probes avoids exposure to radioactivity. Lactulose and 51Cr-labeled EDTA have similar molecular weights and cross-sectional diameters. They are considered comparable intestinal permeability markers because evidence has suggested that their route of permeation through the intestinal wall is the same (ie, via intercellular junctions) and their urinary recovery after concurrent ingestion is virtually analogous in humans and cats.8–10 Currently, the 5 most frequently used sugar probes for assessing canine gastrointestinal permeability and absorptive function are sucrose (gastric permeability), lactulose and rhamnose (intestinal permeability), and d-xylose and 3-O-methyl-d-glucose (intestinal absorptive function). Reference values for these sugars generally are obtained from healthy control dogs of various breeds.1,7

Beagles are the most frequently used dogs in biomedical research. They have been widely used in a variety of testing programs,11 especially in projects that require assessment of intestinal mucosal damage. Assessment of this damage typically is based on the interpretation of tissue specimens collected via invasive methods such as surgery or endoscopy.12 However, Beagles in experimental settings may benefit from non-invasive assessment of gastrointestinal integrity and absorptive capacity by use of tests such as GIPFTs. In contrast to histologic examination, these tests provide information on both morphological and functional aspects of the gastrointestinal tract, and they comply with the proposed guiding research principles of reduction and refinement.13

Analysis of evidence appears to indicate species- and breed-specific differences in GIPFT results in dogs5,14 and cats9 as well as interracial differences in humans.15,16 In addition, clear effects of age and body size on intestinal permeability have been reported in healthy dogs,17 and diet, sexual status, and other environmental factors, including subclinical disease, have been suggested to alter, at least to some extent, the bioavailability of orally administered drugs.18 If all these factors were to affect the recoveries of the markers used for GIPFTs in dogs, specific reference values might be warranted for frequently used GIPFT markers according to breed, age, sexual status, diet, feeding status, and housing conditions. Moreover, this is particularly important in dogs (such as Beagles) intended for use in experiments because they can be used to control variation and thus reduce the future use of animals in research.

The purpose of the study reported here was to determine the percentage urinary recovery of 51Cr-labeled EDTA, lactulose, rhamnose, d-xylose, 3-O-methyl-d-glucose, and sucrose after oral administration to healthy adult purpose-bred male Beagles housed and maintained under standard laboratory conditions. We also sought to investigate correlations in these dogs between 51Cr-labeled EDTA and the 5 sugar markers most commonly used for assessing canine gastrointestinal permeability and absorptive function.

Materials and Methods

Animals—Nineteen sexually intact male adult purebred purpose-bred Beagles were obtained from an approved commercial laboratory animal vendora for use in the study. The dogs were allowed to acclimatize for 1 month prior to the onset of the study. All dogs were housed at the laboratory dog facilities of the Faculty of Veterinary Medicine at the University of Helsinki in indoor pens; dogs were allowed in outdoor runs for approximately 4 hours daily. The dogs were exposed to natural and artificial light (from 7:00 am to 4:00 pm), and the indoor environmental temperature was maintained at 15° to 24°C. Throughout the study, dogs were fed a diet that consisted of a commercial canned food formulated for dogsb (dogs were fed twice daily [1.5 cans/dog/d]). Water was freely available at all times. At the beginning of the study, dogs were between 11 and 40 months of age (mean, 18 months) and had a body weight between 12.4 and 17.0 kg (mean, 14.9 kg). Health status of the dogs was determined via physical examinations, and blood samples were obtained from each dog for routine hematologic and biochemical assessment. Prior to the study, the dogs were treated with fenbendazolec (50 mg/kg, PO, q 24 h for 3 consecutive days), and fecal samples were subsequently collected for endoparasite examination.

The experimental protocol was approved by the Ethics Committee for Animal Experiments of the University of Helsinki. The dogs were cared for and used in experiments in accordance with the prevailing Finnish legislation and the Council of Europe Convention ETS 123 on the use of vertebrate animals for scientific purposes.

GIPFT—In all dogs, GPIFTs were performed by use of 51Cr-labeled EDTA, lactulose, rhamnose, d-xylose, 3-O-methyl-d-glucose, and sucrose. On the morning of the experiment, 2 fresh test solutions that consisted of distilled water containing 3.7 MBq of 51Cr-labeled EDTAd/50 mL and a mixture of 2 g of lactulose, 2 g of rhamnose, 2 g of d-xylose, 1 g of 3-O-methyl-d-glucose, and 8 g of sucrose in 200 mL were prepared and administered to each dog. For subsequent radioactivity measurements, a 1-mL aliquot of the solution containing 51Cr-labeled EDTA was retained as a counting standard; the aliquot was further diluted (1:50).

Food was withheld the night before and throughout the study, but water was freely available at all times. After food was withheld overnight, the body weight of each dog was measured and a baseline blood sample was collected from each dog. Each dog was sedated with medetomidinee (25 μg/kg, IM), and the urinary bladder then was emptied by use of a urinary catheter. All dogs then received the 51Cr-labeled EDTA solution, which was followed immediately by the sugar solution; both solutions were administered via intragastric gavage. To reverse the sedative effects of medetomidine, atipamezolef (100 μg/kg, IM) was injected, and the dogs were then placed in metabolic cages for a 6-hour period during which urine was collected. After the urine collection was complete, medetomidinee (25 μg/kg, IM) was again administered to each dog and the urine in each bladder was collected by use of a urinary catheter. The urine collected from the metabolic cage and urinary bladder of each dog was pooled; total urine volume was determined and recorded for subsequent tests. Two 2-mL aliquots of the pooled urine of each dog were retained, one of which was used for radioactivity measurement and the other of which was stored at −20°C until transported on dry ice to a laboratoryg for analysis.

Analysis of sugar concentrations was performed by use of high-performance liquid chromatography in accordance with a method reported elsewhere.19 The measurement of 51Cr-labeled EDTA concentrations was performed at the University of Helsinki Central Laboratory of the Department of Clinical Veterinary Sciences. The gamma-ray emission from the aliquot of the counting standard and each urine sample was concurrently counted for 10 minutes by use of a gamma counterh during the same evening as the experiment. The amount of 51Cr-labeled EDTA in urine as a percentage of the orally ingested test solution was calculated by use of the following equation:

article image

where CPM is the counts per minute, the first 50 represents the dilution factor, and the second 50 represents the total volume of the test solution.

Statistical analysis—The Shapiro-Wilk test was used to test for normality of the distribution of each variable. Normally distributed variables were expressed as mean ± SD and range, and other variables were expressed as median and range. The Pearson correlation coefficient was used to measure associations between pairs of probe markers that both had a normal distribution, whereas Spearman rank correlation coefficients were calculated if 1 or both of the probe markers were not normally distributed. Values of P < 0.05 were considered significant. Statistical analysis was performed by use of a commercial software program.i

Results

All dogs were assessed as healthy on the basis of results of physical examination and hematologic and serum biochemical analysis. Analysis of BUN and SUN concentrations suggested physiologically normal renal function in all dogs. Carrier-mediated absorption in the proximal and distal portions of the small intestine was considered to be physiologically normal as determined on the basis of serum concentrations of folate and cobalamin. Exocrine pancreatic function was considered physiologically normal on the basis of serum trypsin-like immunoreactivity concentrations. Results of examination for fecal endoparasitic ova were negative for all dogs.

Values were normally distributed for percentage urinary recovery of 51Cr-labeled EDTA (P = 0.155), lactulose (P = 0.331), rhamnose (P = 0.388), and 3-O-methyl-d-glucose (P = 0.121) and for recovery ratios of 51Cr-labeled EDTA to rhamnose (P = 0.077), lactulose to rhamnose (P = 0.062), and d-xylose to 3-O-methyl-d-glucose (P = 0.181). Values were not normally distributed for percentage urinary recovery of d-xylose (P = 0.035) and sucrose (P < 0.001).

The percentage urinary recovery of the 6 markers used to assess gastrointestinal permeability and absorptive function after simultaneous orogastric administration were calculated. Part of the data on 51Cr-labeled EDTA has been previously reported.20 Mean ± SD percentage urinary recovery of intestinal permeability markers 51Cr-labeled EDTA, lactulose, and rhamnose was 6.3 ± 1.6% (range, 4.3% to 9.7%), 3.3 ± 1.1% (range, 1.7% to 5.3%), and 25.5 ± 5.0% (range, 16.7% to 36.9%), respectively. The median and range percentage urinary recovery of the intestinal absorptive function marker d-xylose was 40.3% and 31.6% to 62.7%. Mean ± SD percentage urinary recovery of 3-O-methyl-d-glucose was 58.8 ± 11.0% (range, 40.1% to 87.8%). For sucrose (gastric permeability marker), the median and range percentage urinary recovery was 0% and 0% to 0.8%. Moreover, the mean ± SD urinary recovery ratio was 0.25 ± 0.06 (range, 0.17 to 0.37) for 51Cr-labeled EDTA to rhamnose, 0.13 ± 0.04 (range, 0.08 to 0.23) for lactulose to rhamnose, and 0.73 ± 0.09 (range, 0.60 to 0.90) for d-xylose to 3-O-methyl-d-glucose. Correlation coefficients and significance were determined for all GIPFT variables evaluated in the study (Table 1).

Table 1—

Correlation coefficients (P values) between variables of GIPFTs evaluated in 19 healthy adult male Beagles.

VariableUrinary recovery of 51Cr-labeled EDTA (%)Urinary recovery of lactulose (%)Urinary recovery of rhamnose (%)51Cr-labeled EDTA-to-rhamnose recovery ratioLactulose-to-rhamnose recovery ratioUrinary recovery of d-xylose (%)Urinary recovery of 3-O-methyl-d-glucose (%)d-xylose-to-3-O-methyl-d-glucose recovery ratioUrinary recovery of sucrose (%)
Urinary recovery of 51Cr-labeled EDTA (%)0.64 (0.003)*0.40 (0.086)*0.73 (< 0.001)*0.51 (0.025)*−0.07 (0.775)0.16 (0.508)*−0.47 (0.040)*0 (1.000)
Urinary recovery of lactulose (%)0.64 (0.003)*0.63 (0.004)*0.20 (0.414)*0.80 (< 0.001)*0.37 (0.115)0.61 (0.006)*−0.29 (0.229)*−0.25 (0.304)
Urinary recovery of rhamnose (%)0.40 (0.086)*0.63 (0.004)*−0.32 (0.189)*0.07 (0.784)*0.63 (0.004)0.90 (< 0.001)*−0.40 (0.094)*−0.21 (0.387)
51Cr-labeled EDTA-to-rhamnose recovery ratio0.73 (< 0.001)*0.20 (0.414)*−0.32 (0.189)*0.50 (0.030)*−0.61 (0.006)−0.49 (0.033)*−0.21 (0.393)*0.29 (0.226)
Lactulose-to-rhamnose recovery ratio0.51 (0.025)*0.80 (< 0.001)*0.07 (0.784)*0.50 (0.030)*0.13 (0.583)0.10 (0.676)*−0.13 (0.606)*−0.26 (0.279)
Urinary recovery of d-xylose (%)−0.07 (0.775)0.37 (0.115)0.63 (0.004)−0.61 (0.006)0.13 (0.583)0.85 (< 0.001)*0.38 (0.111)*−0.67 (0.002)
 Urinary recovery of 3-O-methyl-d-glucose (%)0.16 (0.508)*0.61 (0.006)*0.90 (< 0.001)*−0.49 (0.033)*0.10 (0.676)*0.85 (< 0.001)*−0.07 (0.767)*−0.43 (0.067)
d-xylose-to-3-O-methyl-d-glucose recovery ratio−0.47 (0.040)*−0.29 (0.229)*−0.40 (0.094)*−0.21 (0.393)*−0.13 (0.606)*0.38 (0.111)*−0.07 (0.767)*−0.42 (0.071)
Urinary recovery of sucrose (%)0 (1.000)−0.25 (0.304)−0.21 (0.387)0.29 (0.226)−0.26 (0.279)−0.67 (0.002)−0.43 (0.067)−0.42 (0.071)

Correlations were considered significant at values of P < 0.05.

Correlation was calculated by use of Pearson rank coefficients.

Correlation was calculated by use of Spearman rank coefficients.

— = Not applicable.

Discussion

In the study reported here, the percentage urinary recovery of 51Cr-labeled EDTA for urine samples collected during a 6-hour period in healthy adult male Beagles ranged from 4.3% to 9.7%. In other studies21 on healthy Beagles, the mean percentage urinary recovery of 51Cr-labeled EDTA for urine samples collected during a 24-hour period ranged between 17.3% and 37.6%,21 and the percentage urinary recovery for urine samples collected during a 6-hour period ranged between 3.8% and 34.2%.6 The high variation in test results in those earlier studies may be explained by the inclusion of both pubertal and adult dogs of both sexes that were fed both canned and dry foods. In addition, some of those dogs in earlier investigations were affected by small intestinal dysbiosis (formerly ascribed as small intestinal bacterial overgrowth).6,21 To our knowledge, the study reported here was the first in which the 51Cr-labeled EDTA-to-rhamnose recovery ratio has been determined in dogs.

We found that the urinary lactulose-to-rhamnose recovery ratio for samples collected during a 6-hour period in healthy adult male Beagles ranged from 0.08 to 0.23. As expected, our ranges were considerably different from, but in agreement with, results of other investigations that used healthy dogs of a number of breeds, ages, and sizes, including Irish Setters (0.03 to 0.18),5 Greyhounds (0.19 to 0.34),14 Viszlas (0.07 to 0.26),14 mixed-breed dogs (0.08 to 0.34),14 adult Miniature Poodles (0.14 to 0.21),17 adult Standard Schnauzers (0.13 to 0.26),17 adult Giant Schnauzers (0.17 to 0.32),17 adult Great Danes (0.26 to 0.42),17 and Beagles (0.05 to 0.15).j The findings for the present study, together with those of previous studies, are consistent with the theory that there are effects of breed, age, and body size and possibly diet on intestinal permeability in dogs.

The urinary d-xylose–to–3-O-methyl-d-glucose recovery ratio ranged from 0.60 to 0.90 in urine samples collected during a 6-hour period in healthy adult male Beagles in the present study, which was consistent with results of similar studies on a group of Beagles (0.40 to 0.59)19,j and in other breeds, including adult Miniature Poodles (0.52 to 0.65),21 adult Standard Schnauzers (0.51 to 0.68),17 adult Giant Schnauzers (0.54 to 0.62),17 and adult Great Danes (0.56 to 0.62).17 Findings from the present study are in agreement with those of another study,17 which suggested that in contrast to the apparent morphological differences, the carrier-mediated mechanisms that allow intestinal absorption are similar among adult dogs of different breeds.

Studies in humans (r = 0.98; P = 0.001) and cats (r = 0.85; P = 0.03) have revealed a correlation between 51Cr-labeled EDTA and lactulose concentrations when compared as single markers8,9 or as ratios to rhamnose concentrations (r = 0.97; P = 0.002).9 However, analysis of the data from the present study suggested that the correlation between the percentage urinary recovery of 51Cr-labeled EDTA and lactulose after their concurrent oral administration in Beagles when compared as single markers (r = 0.64; P = 0.003) or as ratios to rhamnose (r = 0.50; P = 0.030) was not as prominent as previously determined in humans and cats. The lower correlation between these 2 markers in the dogs of the present study may be explained by the possible partial metabolization or breakdown of the sugar probes (eg, lactulose metabolism by resident intestinal bacteria).

In general, 51Cr-labeled EDTA is considered to be the ideal permeability marker because of its biological inertness. This is especially useful in individuals with an overgrowth of bacteria because the inertness will prevent bacterial degradation of the molecule. It is known that apparently healthy Beagles may have evidence of small intestinal dysbiosis,21 a condition that is consistent with bacterial degradation of saccharides such as lactulose and that may be exacerbated if bacteria that typically colonize the colon are able to colonize the small intestine.22

No significant positive correlation was detected in the present study between the percentage urinary recovery of 51Cr-labeled EDTA and that of the other sugar markers (rhamnose, d-xylose, 3-O-methyl-d-glucose, and sucrose), which is consistent with current knowledge of the GIPFT markers.2 Interestingly, the correlation (r = 0.90; P < 0.001) between rhamnose, a marker reflecting nonmediated transcellular diffusion throughout the small intestine, and 3-O-methyl-d-glucose, a molecule absorbed across the small intestine via a specific carrier-mediated transport system, may indicate that both markers may be absorbed in parallel by the intact mucosa of the small intestines of healthy Beagles. Moreover, the correlation (r = 0.63; P = 0.004) between rhamnose and d-xylose, the intestinal absorption mechanism of which is similar to that of 3-O-methyl-d-glucose but limited to the jejunum, adds support to this suggestion.

It has generally been assumed that the ratio of 2 molecules provides a more reliable index of intestinal damage and dysfunction than does evaluation of single markers alone.2 Nevertheless, the findings for the present study, in which we compared the percentage urinary recovery of 51Cr-labeled EDTA and lactulose with the 51Cr-labeled EDTA-to-rhamnose recovery ratio (r = 0.73; P < 0.001) and lactulose-to-rhamnose recovery ratio (r = 0.80; P < 0.001), suggested that equivalent results were obtained in healthy dogs when a single marker was evaluated or a combination of 2 markers was used as a ratio. However, evaluation of a single marker for the assessment of intestinal absorptive function is not recommended on the basis of the findings of the present study in healthy Beagles.

In the study reported here, we provided data on the percentage urinary recovery of 51Cr-labeled EDTA, lactulose, rhamnose, d-xylose, 3-O-methyl-d-glucose, and sucrose used for GIPFTs in healthy adult male Beagles in a controlled experimental setting. These data add to current information about integrity of the physiologically normal gastrointestinal mucosa and absorptive capacity in this breed. These data could be used in future studies with Beagles. Although there was a significant correlation between the percentage urinary recovery of the intestinal permeability markers 51Cr-labeled EDTA and lactulose, there was a slight discrepancy between results for the present study in dogs and published results for other species. Further studies are needed to clarify this disagreement. Meanwhile, caution is warranted when GIPFT results are obtained via the use of lactulose and other sugar probes, particularly in dogs suspected of having small intestinal dysbiosis.

ABBREVIATIONS

51Cr

Chromium 51

GIPFT

Gastrointestinal permeability and absorptive function test

a.

Harlan-Winkelmann GmbH, Borchen, Germany.

b.

Pedigree, Fortivil 400 g, Waltham, Masterfoods Ltd, Helsinki, Finland.

c.

Axilur, Intervet International, Boxmeer, The Netherlands.

d.

Nycomed Amersham plc, Little Chalfont, Buckinghamshire, England.

e.

Domitor, Orion Pharma Ltd, Turku, Finland.

f.

Antisedan, Orion Pharma Ltd, Turku, Finland.

g.

GI Laboratory, Texas A&M University, College Station, Tex.

h.

LKB-Wallac 1270 Rackgamma II gamma counter, LKB-Wallac, Turku, Finland.

i.

SAS system for Windows, release 9.2, SAS Institute Inc, Cary, NC.

j.

Steiner JM, Cardwell JR, Williams DA. Determination of a control range for a 5-sugar gastrointestinal permeability and mucosal function test in clinically healthy dogs (abstr). J Vet Intern Med 2001;15:311.

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