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,3
* Centre for Feline Nutrition, Institute of Food, Nutrition, and Human Health, and Institute of Veterinary, Animal, and Biomedical Sciences, Massey University, Palmerston North, New Zealand, and ** WALTHAM Centre for Pet Nutrition, Waltham-on-the-Wolds, Leicestershire, LE14 4RT, UK
3 To whom correspondence should be addressed. E-mail: c.e.ugarte{at}massey.ac.nz.
KEY WORDS: • cats • inflammatory bowel disease • fecal grade • fecal osmolar gap • breath hydrogen
By definition, carbohydrate tolerance is the ability to consume dietary carbohydrates without adverse effect or injury. Carbohydrate malassimilation and intolerance are suspected to be common complications of gastrointestinal disease (1) and can result in osmotic diarrhea, bacterial overgrowth, and ill thrift in cats (2).
The pathophysiology of carbohydrate malabsorption in feline gastrointestinal disease is poorly understood. Carbohydrate malabsorption may occur in inflammatory bowel disease (IBD)4 because of the adverse effects of inflammation on digestive enzymes (3) or due to inflammatory infiltrates acting as a nutrient diffusion barrier (4).
The widespread use of commercial diets, the large amount of carbohydrates they contain [many commercial dry cat foods contain at least 40% carbohydrate (5)], and the frequent changes in the formulation of these diets suggest that handling of dietary carbohydrates by cats with gastrointestinal inflammation warrants study. Furthermore, the peculiarities of the digestion, absorption, and metabolism of carbohydrates by cats (6–8) may make cats with gastrointestinal disease more vulnerable than other species to carbohydrate maldigestion and malabsorption.
The above observations suggest that optimizing the digestibility and utilization of dietary carbohydrates might improve the outcome of dietary management of feline IBD. Furthermore, improved carbohydrate assimilation might improve the utilization of other macronutrients, specifically, protein (9).
Carbohydrate malabsorption in the small intestine has been difficult to measure in clinical patients, because the malabsorbed carbohydrates are fermented in the colon (10,11). However, the breath-hydrogen technique takes advantage of this process and allows not only identification but also semiquantification of carbohydrate malabsorption (12,13).
The objective of this study was to compare the absorption and tolerance to four different sources of starch, namely, corn, rice, barley, and tapioca, by healthy cats and cats diagnosed with IBD. Malassimilation was evaluated by the breath-hydrogen method. In addition, fecal characteristics (grade, water content, and osmolar gap) were studied to understand how well they indicate the presence of carbohydrate malabsorption and how important the tested sources of dietary carbohydrates are in producing lower-grade feces in cats.
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MATERIALS AND METHODS |
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 TOP MATERIALS AND METHODS RESULTSDISCUSSIONLITERATURE CITED |
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The test diets were provided by the WALTHAM Centre for Pet Nutrition. All diets contained chicken as the principal source of protein and either tapioca, maize, barley, or rice as the principal carbohydrate. Gelatinization of the starch in all diets occurred during canning. Diets were isocaloric and very similar in macronutrient composition [protein, 25.3–28.7% of metabolizable energy (% ME), fat, 48.9–52.9% ME; and nitrogen-free extract, 18.4–25.8% ME]. A negative control of boiled chicken flesh was also used; this contained virtually no carbohydrate and a higher level of protein (64% ME).
Animals
Fifteen healthy control cats and seven cats diagnosed with IBD were used for this study. Control cats were provided by the Centre for Feline Nutrition at Massey University and lived in a colony situation. The cats in the IBD group were referred to the Massey Veterinary Teaching Hospital for chronic diarrhea, vomiting, weight loss, or other signs of gastrointestinal disease. They were diagnosed with IBD by way of an exhaustive standardized diagnostic protocol and were housed at the hospital for the whole length of the trial.
Allocation of treatments
A crossover trial design was chosen to compare the carbohydrates. The cats were fed 75% of their energy requirements (70 x body weight = kcal ME/d) during the trial to encourage voluntary consumption of the entire meal and decrease variability of food intake between cats, which could have confounded the results. On d 1, the cats were fed boiled chicken flesh. On d 2 of the trial, the first of a sequence of carbohydrate-containing diets was fed. Each of the different carbohydrate diets was fed for 2 d without a washout period between consecutive diets. On the second day of each carbohydrate diet, a breath-hydrogen test was performed. Chromic oxide was added and manually mixed with the diets [1/8 teaspoon (0.625 mL) per feeding bowl] in stages 2 and 4 (d 2, 3, 6, and 7 of the trial), independently of the dietary carbohydrate being tested, with the sole purpose of allowing us to recognize from which diet each stool was derived.
Food intake and fecal output
Food intake was measured daily. Feces were collected at least three times each day or when seen in the cages, graded 1–5 (1 = liquid feces; 2 = pasty feces with no shape; 3 = soft feces with cylindrical shape; 4 = cylindrical shaped feces, dry appearance, separated in pellets sometimes, can be crushed out of shape; and 5 = cylindrical shaped feces, separated in pellets, difficult to crush out of shape), labeled, and refrigerated. Refrigerated stools were separated into two portions. One portion was used to determine the dry matter and water contents of the feces by oven drying them at 70°C until constant weight was achieved. The second portion of the feces was ultracentrifuged at 48,000 x g at 4°C to obtain fecal fluid (14,15).
The fecal osmolar gap was calculated as follows:
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The value 314 represents the average osmolality of serum in the cat (16). The concentrations of sodium and potassium in the fecal fluid were measured by flame-emission photometry (Corning 400 Flame Photometer) (17,18).
Statistical analysis
Statistical analysis was carried out using SAS software, version 6.12 (19). Data are reported as means ± SEM, and a probability of P < 0.05 was considered significant for all tests. All data were analyzed for normality. Data transformation or nonparametric methods were chosen for the analysis of data that were not normally distributed or had an ordinal or nominal scale. ANOVA for repeated measures with contrasts, nonparametric Friedman test for repeated measures, and Spearman rank correlation were used for statistical analysis. Adjustments for multiple comparisons were used when appropriate (20).
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RESULTS |
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TOPMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The area under the breath-hydrogen curve (AUC) was significantly lower for the chicken-flesh diet than for any of the carbohydrate sources (P = 0.0001). All carbohydrate diets behaved similarly in each group. However, IBD-diagnosed cats showed a significantly higher AUC (P = 0.0001) than the control cats for all diets (AUC values for healthy and IBD cats, respectively, were as follows: for chicken-flesh diet, 42.03 ± 5.06 and 104.89 ± 15.95; corn, 96.68 ± 19.12 and 256.89 ± 55.7; rice, 78.38 ± 8.44 and 272 ± 51.25; barley, 88.58 ± 10.08 and 196.32 ± 36.88; and tapioca, 80.45 ± 9.25 and 234.32 ± 45.36). The breath-hydrogen production peak time of cats in the control group that consumed a tapioca-based diet (P = 0.05) occurred significantly earlier (5 h) than the peak times recorded for the control cats that consumed the other carbohydrate diets (6 h for barley and rice and 7 h for corn and chicken). No significantly different peak times were found between different diets in the IBD group (corn, 8 h, and all other diets, 7 h).
Fecal water content (1 g of feces contained 0.85, 0.79 ± 0.017, 0.77 ± 0.006, 0.68 ± 0.007, and 56 ± 0.01 g of water for feces graded 1–5, respectively) was inversely correlated to stool firmness (r = –0.76). No significant differences were found in fecal grade produced by the different carbohydrate sources in IBD-diagnosed or control cats. A weak correlation coefficient (r = 0.28) was found between breath-hydrogen AUC values and fecal grade. Water content was significantly lower in the stools produced after the cats had consumed chicken flesh when compared with those produced after consumption of any of the carbohydrate diets (P = 0.0001; 0.59 ± 0.03, 0.70 ± 0.013, 0.70 ± 0.014, 0.70 ± 0.012, and 0.70 ± 0.012 for chicken-, corn-, rice-, barley-, and tapioca-based diets, respectively). The number of stools produced when each carbohydrate diet was fed was not different in IBD-diagnosed or control cats when compared as a percentage of the total number of stools for the group (IBD-diagnosed or control cats).
There were no significant differences between the fecal potassium content or the fecal osmolar gap of the cats fed the different carbohydrate diets or between the IBD-diagnosed and control cats. Contrasts showed that overall, when cats ate the rice-based diet, sodium concentration in the fecal fluid was higher than with any other carbohydrate (P = 0.046; 37.70 ± 3.11, 54.34 ± 9.72, 33.71 ± 2.26, and 40.71 ± 2.34 mmol/L of fecal fluid for corn-, rice-, barley-, and tapioca-based diets, respectively), and when cats ate the barley-based diet, fecal sodium levels were lower than when they ate rice (P = 0.007).
IBD-diagnosed cats that consumed rice showed a higher fecal sodium:potassium ratio than when they consumed tapioca (P = 0.0014) or barley (P = 0.0013) but not corn (P = 0.42). Furthermore, when rice was contrasted with all other carbohydrates, it showed a significantly higher (P = 0.001) fecal sodium:potassium ratio (ratio for rice, 3.60 ± 0.58; for barley, 2.77 ± 0.24; for corn, 3.40 ± 0.38; and for tapioca, 3.31 ± 0.31). Contrasts also showed that overall, when cats consumed the rice diet, they had a significantly higher sodium:potassium fecal ratio than when they consumed a barley-based diet (P = 0.0004) but not when they consumed a corn-based diet (P = 0.11).
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DISCUSSION |
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TOPMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In addition to yielding the lowest levels of breath hydrogen, chicken flesh also produced feces with the lowest fecal water content. However, the consistency (grade) of feces was good on average for all diets, and the fecal grading system used was shown to be consistent and accurate to assess fecal water content. All carbohydrates produced larger breath-hydrogen AUC values in cats with IBD compared with healthy cats, but the higher fermentable carbohydrate load entering the colon did not affect fecal characteristics in these cats. We speculate that this discordance may be due to the very high efficiency by which the feline colon can absorb water and produce feces with high osmolality.
Nutritionally, fermentation is not as efficient as small-intestine absorption at energy recovery (24), but the importance of colonic salvage of dietary energy has been reported in human patients with short-bowel syndrome (25). The long-term effects of carbohydrate malabsorption in cats with IBD and its clinical relevance remain to be studied.
Rice has often been recommended as a good carbohydrate source for cats with gastrointestinal problems because of presumed good digestibility (26). Rice has also been reported to have antisecretory properties (27); however, all other carbohydrates tested in this study produced similar breath-hydrogen AUC values to rice. The differences in breath-hydrogen AUC cannot be directly equated to the grams of starch malabsorbed because of possible differences in the amount of hydrogen produced per gram of carbohydrate from different sources (28). These data suggest that additional research in this field is warranted including differences between canned and dry diets (29).
Despite the presence of normal feces, the feeding of rice increased the concentration of sodium in the fecal fluid of all cats when compared with the other carbohydrates, but especially in cats with a diagnosis of IBD. The increased sodium content in the fecal fluid of cats that consumed rice was highlighted by the fecal sodium:potassium ratio, which was significantly higher than the ratio determined with the other diets. The significance of these findings is not clear; however, they are interesting and may question the purported antisecretory effects of rice in the feline gastrointestinal tract. It is unclear how absorptive and secretory functions relate to electrolytes present in fecal fluid. Rice-based oral rehydration solutions were found to be beneficial in the treatment of cholera and non-cholera diarrhea in humans, although other tested cereals (corn and wheat) were also reported to be beneficial (30). A secretory inhibitory factor was isolated from boiled rice that blocks the secretory response to 3',5'-cyclic-adenosine monophosphate of some cryptal chloride channels (27) and could underpin the beneficial effects of rice in cholera diarrhea. It is unclear whether this rice factor is as effective in any other type of secretory diarrhea or if it survives food processing and appears in normal commercial pet foods that contain rice. However, the presence of sodium at higher concentrations in fecal fluid from stools produced while cats consumed a rice diet than in other stools of similar water content is paradoxical, because sodium absorption drives water absorption in the colon of most mammals studied. Colonic water absorption on a background of sodium secretion was already reported in cats that consumed fermentable fibers (31), which in this instance is equivalent to the presence of malabsorbed fermentable carbohydrates in the colon. Our knowledge of absorptive processes in the colon of the cat is poor and requires additional study before we can make sound conclusions on the effects of malabsorbed carbohydrates in feline gastrointestinal disease.
No significant differences in fecal osmolar gap were found between diets or among the IBD-diagnosed and healthy cats in this study.
Conclusions
Cats with gastrointestinal disease show broad-spectrum subclinical carbohydrate malabsorption but no untoward effects in this situation demonstrating remarkable carbohydrate gastrointestinal tolerance. Fecal grade does not seem to be a reliable measure of dietary carbohydrate malabsorption in cats. Additional investigations into the responses to different carbohydrates by cats with gastrointestinal disease are needed.
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FOOTNOTES |
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2 This study has been generously supported by the WALTHAM Centre for Pet Nutrition, WALTHAM-on-the-Wolds, Leicestershire, UK.
4 Abbreviations used: AUC, area under the curve; IBD, inflammatory bowel disease; % ME, percent of metabolizable energy.
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