The canine species encompasses dogs of widely varying body weight and size. It is possible that morphologic variation is associated with anatomic and physiologic differences; previous studies1,2 of food tolerance in dogs have revealed that, fed the same dry diet, dogs of large and giant breeds have higher fecal moisture content and greater frequency of soft feces, compared with dogs of small breeds. One of the primary functions of the large intestine is to dehydrate luminal contents and store the residue prior to its elimination as feces. Therefore, it is possible that differences in fecal characteristics may result from physiologic differences in the large intestine of dogs of small versus large breeds.
The efficiency of absorption of salt and water and the fermentative processes is dependent, to a large extent, on colonic motility.3 The finding that reduction in LITT decreases the capacity for electrolyte and water absorption and results in elimination of loose and watery feces has been reported in nonhealthy dogs4,5 and humans.6,7 In contrast, longer transit time of contents in the large intestine promotes fermentation,8 and the impact of colonic fermentation on fecal quality has been reported.9,10
Although a relationship between body size and gastric emptying time11 or OCTT12 has not been reported, there is a positive correlation between body size and TTT and negative correlations exist between those variables and fecal quality.13 Those results suggest that differences in transit time associated with body size would be mainly attributable to differences in large intestinal variables. To our knowledge, an association between body size and LITT in healthy dogs has not been determined.
Previous studies14,15 have investigated colonic motility and propulsion in dogs, but those studies dealt with colonic transit in terms of acceleration or deceleration, and none expressed results as a function of LITT. Studies have been published in which values of LITT in healthy dogs were determined by use of noninvasive direct16 and indirect17 methods, but results were independent of body size. The objectives of the study reported here were to assess the minimum and mean LITT in healthy dogs of various sizes and determine whether fecal variables were related to LITT.
Materials and Methods
Dogs—Twenty-four female dogs were selected to represent a range of breed sizes as follows: 6 Miniature Poodles (mean ± SD body weight, 3.8 ± 1.0 kg; height at the shoulder [ie, floor to top of scapula], 30.3 ± 2.0 cm), 6 Standard Schnauzers (12.9 ± 2.1 kg; 43.9 ± 1.0 cm), 6 Giant Schnauzers (23.9 ± 2.8 kg; 58.5 ± 1.9 cm), and 6 Great Danes (51.5 ± 2.1 kg; 78.5 ± 0.5 cm). Dogs were housed at the National Veterinary School of Nantes in closed indoor and outdoor runs for the duration of the study and were exercised outdoors for 1 hour once daily. No dogs had a history of previous gastrointestinal disease, and all had been vaccinated and dewormed before enrollment in the study. All dogs underwent a thorough physical examination. Dogs were housed and treated according to the French Ministry of Agriculture and Fisheries regulations for animal welfare. The experimental protocol adhered to European Union guidelines and was approved by the Animal Use and Care Advisory Committee of Nantes Veterinary School. Dogs had been used in a previous study13 of TTT.
Diet—Dogs were fed a dry diet (Appendix). Before commencement of the experiment, dogs were deprived of food for at least 16 hours prior to being offered the first marked meal. Water was freely available for TTT measurements. For OCTT measurements, water was withheld during the first 6 hours after the test meal was given. Each dog received the amount of food necessary to meet daily caloric needs (calculated as 132 kcal/kg of body weight0.75 per day)18 Dogs were fed twice daily to increase the number of defecations and permit more accurate calculation of TTT. All food and markers were ingested by the dogs.
Calculation of transit timesLITT—The LITT was calculated as the difference between TTT and OCTT. Minimum and mean LITTs were calculated as the difference between minimum and mean values for TTT and OCTT, respectively.
The OCTT was assessed by use of the sulfasalazine-sulfapyridine method, as described.12 Each dog's weight was recorded before each experiment, and 120 mg of a combined sulfasalazine-sulfapyrine powdera/kg of body weight (equal to 90 mg of sulfasalazine/kg) was mixed with the morning meal. Meals were ingested within 3 minutes in all instances. On the day of the test, an indwelling IV catheter was placed in the cephalic vein of each dog. Four milliliters of blood was collected before and every 30 minutes after the test meal for the first 6 hours and then every 2 hours until 30 hours after consumption of the test meal. In Miniature Poodles, 2.5 mL of blood was collected every 30 minutes for the first 4 hours and then every 2 hours until 30 hours after test meal consumption. Samples were collected in tubes containing sodium heparin as an anticoagulant, and plasma was obtained by centrifuging samples at 2,000 × g for 10 minutes. Samples were stored at −20°C until analysis.
Total concentrations of sulfapyridine (ie, free sulfapyridine and acetylated or glucuronidated metabolites) in plasma were measured by use of spectrophotometryb according to a described method.19 Concentrations of sulfapyridine in plasma were calculated by means of a calibration curve constructed from a plasma sample to which a known amount of sulfapyridine had been added. Ten plasma dilutions were made to cover the range of concentrations from 0.1 to 40 μg/mL. The standard curve was linear (r = 0.998). The detection limit of the assay was 0.2 μg/mL. Minimum OCTT was defined as the time from ingestion of the meal to the time when the total sulfapyridine concentration was detected in plasma (ie, ≥ 0.2 μg/mL). Mean OCTT was measured from plasma sulfapyridine concentrations obtained over 30 hours. For each dog, mean OCTT was calculated from the cumulative concentration curve as the time for 50% of the total plasma sulfapyridine to be recovered (Figure 1).
Plasma profile (A) of sulfapyridine (SP) concentration measured during the 30-hour period after oral administration of sulfasalazine in 24 dogs. The cumulative sulfapyridine concentration curve (B) was used to determine mean OCTT, which was defined as the time required for 50% of the total plasma sulfapyridine to be recovered.
Citation: American Journal of Veterinary Research 67, 2; 10.2460/ajvr.67.2.342
TTT—Dogs were placed in individual metabolism cages equipped with fecal collection trays for 5 consecutive days. Chromium oxide and ferric oxide (used as nondigestible, nonabsorbable, and safe markers) were alternately used (1 marker/d during 4 days) to determine minimum TTT. Chromium oxide (Cr2O3; green) and Fe3O4 (black) were mixed with the meal in a sufficient amount to be clearly seen in voided feces (150, 250, and 500 mg and 1 g of Cr2O3 and 1, 2, 3, and 4 g of Fe3O4 for Miniature Poodles, Standard Schnauzers, Giant Schnauzers, and Great Danes, respectively). The minimum TTT was estimated as the time from ingestion of the test meal to the time of detection of the first colored feces. For each dog, minimum TTT was expressed as the mean of the 4 values (ie, 2 values for each marker).
Mean TTT was simultaneously measured by recording the whole-intestine transit time of small plastic beads.20 Briefly, 20 plastic beadsc of known color were given with the morning meal for 3 consecutive days (yellow on day 1, blue on day 2, and orange on day 3). The beads were 2 mm in diameter and had a specific gravity of approximately 1.3. To improve the rate of ingestion, each bead was incorporated into kibbles perforated with a 1.5-mm drill bit. All feces were collected for 5 days, strained through a sieve, and washed, and the number of beads was recorded. Few defecations occur during the night (ie, only 5.8% of total fecal output), and dogs defecate in the early morning (around 7:00 AM) or just after the meal (8:30 AM).13 For this reason, dogs were monitored every 15 minutes from 6:30 AM to 11:00 PM each day. Feces passed outside this period of monitoring and beads that took 96 hours or more to appear were not used in the calculation of mean TTT. Mean TTT was calculated according to the following equation:
where xi is the number of beads of 1 color in the ith fecal sample; ti is the time interval from ingestion of the beads until the ith fecal sample; and i is the number of defecations from 1 to n, n being the last defecation containing beads of 1 predetermined color.21
Fecal variables—Fecal scores for each dog were recorded daily during the week preceding each experimental period. Feces were graded on a scale from 1 to 5. A grade of 1 represented dry, crumbly feces, and a grade of 5 represented diarrhea. Grade 2 represented feces that were well formed, easy to pick up, and left no mark. Grade 3 represented feces of good quality that were slightly moist and less well formed than grade 2 feces. Grade 3 feces left a mark when removed from a dry surface. Grade 4 feces were moist and poorly formed with a consistency of putty or porridge. Feces were scored by the same person throughout the study. Mean fecal moisture was measured during the same week. Fresh fecal samples from each dog were collected for 7 days, pooled, and subjected to assessment of water content by weighing before and after freeze-drying.d
Statistical analysis—Statistical softwaree was used to evaluate associations between body weight and OCTT, LITT, TTT, and fecal variables within each breed by use of ANOVA. Results were expressed as mean ± SD, and values of P < 0.05 were considered significant. If the tested effect was significant, differences among mean values were assessed by use of the Fisher least significant difference test (matrix of pairwise comparison probabilities). Linear regression analysis was performed to assess the relationships, within each breed, between body weight or height at the shoulder and the fecal variables; and among weight, height at the shoulder, and fecal variables and OCTT, LITT, and TTT. For linear regression, normality of data was tested by use of the Durbin-Watson test.
Results
Fecal variables—Scores were significantly higher (corresponding to looser fecal consistency) in Giant Schnauzers and Great Danes, compared with Miniature Poodles and Standard Schnauzers (Figure 2). Fecal moisture was significantly higher in Great Danes, compared with the other breeds. The associations between body size and fecal variables were confirmed by significant positive correlations between fecal scores and body weight (r = 0.79; P < 0.001) or height at the shoulder (r = 0.87; P< 0.001) as well as between fecal water content and body weight (r = 0.63; P = 0.009) or height at the shoulder (r = 0.61; P = 0.002).
Mean ± SD fecal scores (left vertical axis) and values for moisture content (right vertical axis [%]) in Miniature Poodles (MP), Standard Schnauzers (SS), Giant Schnauzers (GS), and Great Danes (GD; 6 dogs each).a-c Significant (P < 0.05) difference among breeds for the same variable (ie, fecal moisture content or fecal score).
Citation: American Journal of Veterinary Research 67, 2; 10.2460/ajvr.67.2.342
Transit times—Transit times (OCTT, LITT, and TTT) were summarized for each breed (Table 1). Mean TTT data have been published.13 Minimum and mean OCTTs were not significantly different between small and large breeds. For all 24 dogs, minimum and mean OCTTs were 2.6 ± 0.7 hours and 14.5 ± 2.4 hours, respectively. There was no significant association between body size and minimum TTT (17.6 ± 8.1 hours for all 24 dogs). Despite a longer mean TTT in Giant Schnauzers, compared with the other breeds, a significant association was detected between body size and mean TTT, with positive correlations between mean TTT and height at the shoulder (r = 0.68; P < 0.001) or body weight (r = 0.57; P = 0.004). Results revealed a significant association between body size and LITT. Positive correlations were detected between mean LITT and height at the shoulder (r = 0.69; P < 0.001; Figure 3), where mean LITT (hours) = (0.47 × height at the shoulder [cm]) − 0.54, as well as between mean LITT and body weight (r = 0.58; P = 0.003), where mean LITT (hours) = (0.39 × body weight [kg]) + 15. Consequently, a strong association between mean TTT and mean LITT was observed, and the corresponding linear regression equation was as follows: mean LITT (hours) = (0.95 × mean TTT [hours]) − 12.6 (r = 0.98; P < 0.001).
Minimum and mean OCTT, LITT, and TTT for Miniature Poodles, Standard Schnauzers, Giant Schnauzers, and Great Danes (n = 6 dogs each).
| Transit time | Miniature Poodle | |||
|---|---|---|---|---|
| OCTT (h) | ||||
| Minimum | 2.3 ± 0.2a | 2.7 ± 0.2a | 2.7 ± 0.4a | 2.8 ± 0.3a |
| Mean | 13.8 ± 0.8a | 14.3 ± 1.0a | 15.7 ± 1.3a | 14.0 ± 1.1a |
| LITT (h) | ||||
| Minimum | 3.6 ± 0.6a | 17.6 ± 1.1b,c | 21.8 ± 2.6c | 16.8 ± 1.7b |
| Mean | 9.1 ± 1.1a | 18.5 ± 3.0b | 39.4 ± 1.6c | 29.3 ± 1.3d |
| TTT (h) | ||||
| Minimum | 6.0 ± 0.5a | 20.3 ± 1.2b,c | 24.5 ± 2.6c | 19.6 ± 1.6b |
| Mean | 22.9 ± 0.9a | 32.8 ± 2.7b | 55.1 ± 1.3c | 43.3 ± 0.4d |
Values are mean ± SD.
Significant (P < 0.05) difference among breeds.
Relationships between mean LITT and height at the shoulder in 24 healthy dogs.
Citation: American Journal of Veterinary Research 67, 2; 10.2460/ajvr.67.2.342
Correlation between transit times and fecal variables—Fecal scores were related to TTT (r = 0.72 and 0.75 for minimum and mean TTT, respectively; P < 0.001) and LITT (r = 0.70 and 0.73 for minimum and mean LITT, respectively; P < 0.001; Figure 4), whereas there was no significant correlation between fecal moisture and TTT or LITT.
Relationships between mean LITT and fecal score in 24 healthy dogs.
Citation: American Journal of Veterinary Research 67, 2; 10.2460/ajvr.67.2.342
Discussion
Given the close relationship between transit time and major colonic functions,3,8 it is of interest to study LITT in healthy dogs. Although dogs have been widely used in experimental studies14,15 of colonic motility and transit, there is a lack of data on LITT in dogs, especially regarding the relationship between body size and LITT. Measurements of LITT obtained by use of noninvasive methods in dogs fed a commercial dry diet have been reported.16,17 In 1 study,16 LITT was measured in 10 Collie-cross dogs. Abdominal radiographs were obtained at 2-hour intervals, and the mean residence time of radiopaque markers in the large intestine was calculated. In another study,17 an indirect method was used to estimate LITT as the difference between TTT and OCTT in Beagles. Total transit time was assessed by use of recovery of ingested colored plastic beads in feces, and OCTT was assessed by the detection of sulfapyridine in blood after oral administration of sulfasalazine.
In the present study, the same noninvasive indirect method was used to evaluate the association between body size and LITT in healthy dogs. Markers used in the determination of TTT (beads) and OCTT (sulfasalazine) are safe and nontoxic. The methods are not associated with exposure to ionizing radiation and do not require specialized equipment or expense. Time of detection of sulfapyridine in plasma has been validated by direct comparison with results obtained by use of nuclear scintigraphy.22 In a previous study12 of the same dogs at 60 weeks of age, minimum OCTT was determined from blood samples collected over 6 hours. No relationship between body size and minimum OCTT (from 2.2 ± 0.5 hours for Miniature Poodles to 2.7 ± 0.6 hours for Great Danes) was detected in healthy dogs. The authors questioned whether detection of the first marker to reach the colon was sufficiently sensitive for detecting differences among dogs of various body sizes. In the present study, a similar minimum OCTT of 2.6 ± 0.7 hours was observed for all 24 dogs, confirming the repeatability of the method and indicating that there was no association between age and minimum OCTT (dogs were from 5.5 to 6 years old in the present study). There was no association between body size and mean OCTT, as assessed from the curve of plasma sulfapyridine concentrations over 30 hours (from 13.8 ± 0.8 hours in Miniature Poodles to 15.7 ± 1.3 hours in Giant Schnauzers). These results suggested that mean OCTT for movement of half the meal through the ileocecal valve was 14.5 ± 2.4 hours.
Chromium oxide has been used to assess mean TTT in veterinary species.5,23 Analysis of chromium oxide in fecal samples typically requires storage of samples and batch analysis, with an inherent delay in the acquisition of data. Therefore, we used chromium oxide only as a colored marker for determination of minimum TTT. Results were in agreement with values (20.6 ± 5.0 hours) reported in a study5 of 8 dogs weighing from 10 to 30 kg and fed a dry food. In that study, the authors designated the minimum whole-intestine transit time as the interval between the time of ingestion of colored plastic beads and the appearance of the first bead in feces.
The method used in the present study to measure mean TTT involved the recovery from feces of small plastic beads. The bead markers were inexpensive, easy to count in fecal material, and enabled rapid acquisition of data. This method of calculating transit time was first described by Cummings and Wiggins20 in 1976. The beads do not affect the transit of ingesta, and the method has been validated by means of direct comparison with results obtained with the chromium oxide technique.5 The beads used were similar in dimension and density to the pellets used in previous studies.17,21 The main drawback with the use of beads lies in determining the exact timing of each defecation. Some authors5 have used video cameras to monitor dogs during the study. In our study, few dogs defecated during the night and monitoring was conducted every 15 minutes from 6:30 AM to 11:00 PM; defecations occurring outside this period were not taken into account. There was no significant difference between the mean TTTs calculated with and without beads passed from 11:00 PM to 6:30 AM. Although all feces were collected during 5 days, markers that took > 96 hours to pass were not included in calculations. As has been reported,13 Giant Schnauzers had the longest TTT. Although the dogs in our study had been habituated to metabolism cages since they were puppies, Giant Schnauzers seemed less at ease than did Miniature Poodles, Standard Schnauzers, and Great Danes. Therefore, considering that the method used in this study depended heavily on the time of defecation, it is possible that Giant Schnauzers retained their feces when in the metabolism cages. This would explain the longer TTT in those dogs and illustrates the chief drawback of use of this method. Nevertheless, for each breed, low SDs were detected, compared with results of other studies,5,16 and a positive correlation was detected between height at the shoulder and mean TTT. Measurements of TTT in numerous dogs of various breeds would be required to determine if this finding in Giant Schnauzers is truly a breed-specific difference.
In the present study, water was freely available so that a more normal feeding environment would be simulated, but water intake was not recorded. To the best of our knowledge, water intake was not taken into account in the measurement of colonic transit time in previous studies16,17,21,24 in dogs and humans. The potential influence of water intake on OCTT, TTT, and LITT is unknown.
Minimum and mean LITTs were calculated from the difference between the minimum and mean values for TTT and OCTT. A significant association between body size was found for mean LITT, as well as a correlation between height at the shoulder and mean LITT. Stronger correlations were detected between minimum or mean LITT and height at the shoulder, compared with body weight. Nevertheless, the correlation observed between mean LITT and body weight is in agreement with results of a previous study.17 When the same indirect method of measurement was used, a mean LITT of 17.5 ± 5.2 hours was determined for Beagles that weighed 12.2 ± 1.1 kg and a mean LITT of 19.8 hours was calculated for the same body weight value. A minimum LITT of 12.0 ± 7.1 hours was observed in 10 Collie-cross dogs with a mean body weight of 20.2 kg, and a minimum LITT of 14.4 hours was calculated from the same value for body weight.16 In that study, successive radiographs were obtained after radiopaque markers were ingested by nonanesthetized dogs and the colonic residence time was determined from the time of first entry of markers into the proximal portion of the colon to the time at which 90% of radiopaque markers had left the colon and entered the rectum. With this method, fecal recovery of markers was not taken into account and minimum LITT was determined without consideration of the time at which the dog defecated. The similarity between values for minimum LITT in that study and the values calculated from our equation may indicate that conscious withholding of defecation did not appear to be a limiting factor in determining TTT (and LITT) as measured by the recovery of indigestible markers in feces.
Weak correlations between minimum or mean LITT and height at the shoulder or weight were observed, likely because of the longer TTT in Giant Schnauzers, compared with Great Danes. These equations were used to verify that the results were in agreement with those from previous studies.16,17 We do not believe that the equations enable the prediction of LITT on the basis of height at the shoulder or body weight. However, there was a correlation between mean LITT and mean TTT, a finding that may be useful for prediction of LITT.
Although there was no difference in mean OCTT between small and large dogs, LITT could be estimated from TTT (as proposed5), but independently of body size. In that study,5 colonic transit time accounted for 80% to 90% of whole-intestine transit time in dogs and colonic transit time was estimated indirectly by recording the whole-intestine transit time of small plastic beads. However, in the present study, mean LITT accounted for 58 ± 15% of mean TTT (39 ± 9.4%, 55 ± 13%, 72 ± 5.2%, and 68 ± 4.0% for Miniature Poodles, Standard Schnauzers, Giant Schnauzers, and Great Danes, respectively). Thus, we propose the following linear regression equation, where mean LITT (hours) = (0.95 × mean TTT [hours]) − 12.6.
Results of this study confirmed the predisposition of large dogs to have softer feces, as indicated by the positive correlation between body size and fecal scores or fecal moisture and between body weight and fecal scores or fecal moisture. Despite the longer mean TTT observed in Giant Schnauzers, compared with Great Danes, a relationship was also observed between mean LITT and fecal scores but not between mean LITT and fecal water content. It has been reported2,25 that fecal humidity and consistency are not strictly inversely related.
In previous studies4-7 of diarrhea in humans and dietary sensitivity in dogs, a relationship between a shortened LITT (ie, a higher transit rate) and decreased water absorption, leading to loose and watery feces, has been reported. In our study, mean LITT increased with body size and fecal moisture was not correlated with mean LITT in healthy dogs. Results suggested that time for water absorption in the large intestine is not the limiting factor behind the looser fecal consistency in large dogs, compared with small dogs. Considering that intestinal and colonic lengths should increase with body size and given the positive correlation between LITT and body size, it is probable that the rate of transit of luminal contents through the large intestine does not differ between small and large breeds. However, a prolonged LITT may promote intraluminal fermentation, influencing fecal quality.8-10 The longer large intestinal residence time in large dogs may influence fecal consistency, in part by promoting fermentative activity. Further investigations would be necessary to confirm this hypothesis.
| LITT | Large intestinal transit time |
| OCTT | Orocecal transit time |
| TTT | Total transit time |
Salazopyrine, Pharmacia AB, Uppsala, Sweden.
Spectrophotometer, Jenway Ltd, Essex, UK.
Cofalu Kim'play, La Brede, France.
Flexi-Dry MP, FTS Systems Inc, New York, NY.
Statview 5.0, SAS Institute Inc, Cary, NC.
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Appendix 1
Appendix 1
Nutrient composition of a diet fed to 24 dogs during a study of LITT.
| Nutrients | Amount |
|---|---|
| Dry matter (g/100 g) | 92.4 |
| Crude protein (g/100 g DM) | 24.7 |
| Crude fat (g/100 g DM) | 16.0 |
| Ash (g/100 g DM) | 5.8 |
| Total dietary fiber (g/100 g DM) | 7.7 |
| Metabolizable energy* (kcal/100 g DM) | 402.0 |
Ingredients were dehydrated poultry meat, animal fat, maize gluten, maize, maize flour, dehydrated poultry liver, beet pulp, brew-er’s yeast, vegetable oil, fish oil, minerals, chelated trace-elements, egg powder, taurine, chondroitin sulfate, glucosamine chloride, and vitamins.
Calculated according to National Research Council guide-lines.18
