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Total dietary fiber composition of diets used for management of obesity and diabetes mellitus in cats Tammy J. Owens, DVM; Jennifer A. Larsen, DVM, PhD; Amy K. Farcas, DVM, MS; Richard W. Nelson, DVM; Philip H. Kass, DVM, MPVM, PhD; Andrea J. Fascetti, VMD, PhD Objective—To determine total dietary fiber (TDF) composition of feline diets used for management of obesity and diabetes mellitus. Design—Cross-sectional survey. Sample—Dry veterinary (n = 10), canned veterinary (12), and canned over-the-counter (3) feline diets. Procedures—Percentage of TDF as insoluble dietary fiber (IDF), high-molecular-weight soluble dietary fiber (HMWSDF), and low-molecular-weight soluble dietary fiber (LMWSDF) was determined. Results—Median measured TDF concentration was greater than reported maximum crude fiber content in dry and canned diets. Median TDF (dry-matter) concentration in dry and canned diets was 12.2% (range, 8.11% to 27.16%) and 13.8% (range, 4.7% to 27.9%), respectively. Dry and canned diets, and diets with and without a source of oligosaccharides in the ingredient list, were not different in energy density or concentrations of TDF, IDF, HMWSDF, or LMWSDF. Similarly, loaf-type (n = 11) and gravy-type (4) canned diets differed only in LMWSDF concentration. Disparities in TDF concentrations among products existed despite a lack of differences among groups. Limited differences in TDF concentration and dietary fiber composition were detected when diets were compared on the basis of carbohydrate concentration. Diets labeled for management of obesity were higher in TDF concentration and lower in energy density than diets for management of diabetes mellitus. Conclusions and Clinical Relevance—Diets provided a range of TDF concentrations with variable concentrations of IDF, HMWSDF, and LMWSDF. Crude fiber concentration was not a reliable indicator of TDF concentration or dietary fiber composition. Because carbohydrate content is calculated as a difference, results suggested that use of crude fiber content would cause overestimation of both carbohydrate and energy content of diets. (J Am Vet Med Assoc 2014;245:99–105)
O
besity is prevalent among the domestic feline population1 and is associated with a 4-fold risk of developing diabetes mellitus.2 Obesity likely plays a primary role in insulin resistance in cats, and glucose intolerance with impaired insulin secretion is associated with weight gain.3 The addition of fiber is a common strategy used in obesity management because cats regulate food intake by volume.4 Diets high in water or fiber reduce both energy density and calorie intake4–6 and may be useful in prevention and treatment of both obesity and diabetes mellitus. Although some studies7–10 suggest that diets with low carbohydrate content and high protein content From the Veterinary Medical Teaching Hospital (Owens), the Departments of Molecular Biosciences (Larsen, Fascetti), Medicine and Epidemiology (Nelson), and Population Health and Reproduction (Kass), School of Veterinary Medicine, and the Department of Animal Science, College of Agriculture and Environmental Sciences (Farcas), University of California-Davis, Davis, CA 95616. Dr. Farcas’s present address is Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104. Supported in part by the Center for Companion Animal Health, School of Veterinary Medicine, University of California-Davis, and by Barbara Smith. Dr. Owens was supported by an educational grant from the Nestlé Purina PetCare Co. Presented in abstract form at the 13th Annual American Academy of Veterinary Nutrition and Research Symposium, Seattle, June 2013. Address correspondence to Dr. Fascetti ([email protected]). JAVMA, Vol 245, No. 1, July 1, 2014
ABBREVIATIONS AAHA AOAC CF GA HMWSDF IDF LMWSDF ME OTC SDF TDF
American Animal Hospital Association Association of Analytical Communities Crude fiber Guaranteed analysis High-molecular-weight soluble dietary fiber Insoluble dietary fiber Low-molecular-weight soluble dietary fiber Metabolizable energy Over-the-counter Soluble dietary fiber Total dietary fiber
may be advantageous in managing feline diabetes mellitus, the fiber types and concentrations of the diets in those studies were not well characterized. Other diets intended to manage feline obesity or diabetes mellitus highlight an increased fiber content in their product guides or marketing materials; however, direct comparison among diets is not possible because TDF (composed of IDF, HMWSDF, and LMWSDF) information is often not provided. Quantification of fiber fractions is valuable, given that the effects of fiber types are not uniform. Fiber supplementation, particularly IDF, may affect nutrient absorption and modulation of postprandial glycemic response,11 whereas short-chain fatty acid Scientific Reports
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production from bacterial fermentation of SDF (eg, inulin and fructooligosaccharides) supports beneficial colonic microbial populations,12–15 which are recognized as having a role in controlling obesity.16 Crude fiber, a required component of the GA of a pet food label, remains the only representation of fiber for most cat foods. The method for CF analysis, developed in 1806, recovers variable fractions of cellulose, hemicellulose, and lignin,17,18 which provides incomplete information on IDF content only. Crude fiber is a poor reflection of TDF, which can vary greatly among diets.17,19 However, traditional laboratory analysis of TDF also has limitations, given that the most commonly used methodology does not detect or quantify LMWSDF (oligosaccharides and most types of resistant starch). Until recently, there was not a practical method to quantify LMWSDF in addition to the IDF and HMWSDF typically measured and reported as TDF. Newer methodology has been recently developed,20,21 but further validation is needed, and widespread use has not yet occurred. As such, reported TDF concentrations may be underestimated depending on the method of measurement used.22 The objective of the study reported here was to determine TDF content as IDF, HMWSDF, and LMWSDF in veterinary therapeutic feline diets labeled for obesity and diabetes mellitus as well as a limited number of OTC canned diets occasionally recommended for feline diabetes mellitus, by means of an updated method of measuring TDF. We hypothesized that measured TDF would be greater than reported maximum CF, that TDF and LMWSDF would be greater in dry diets than in canned diets, and that LMWSDF concentrations would be greater in diets with added oligosaccharides, compared with those without. We further hypothesized that TDF concentration would be lower in low-carbohydrate diets versus other diets and higher in diets primarily recommended for obesity versus those primarily used for diabetes mellitus.
were considered marketed as low-carbohydrate diets if this was either a noted feature on the label or if the diet was included in widely available low-carbohydrate diet lists.23–25 Diets were also compared on the basis of carbohydrate concentrations recommended by the AAHA Diabetes Management Guidelines.26 These guidelines provide medical and nutritional management recommendations that include limiting carbohydrate intake. Carbohydrate concentrations in diets are defined as ultralow if the diet provides < 5% carbohydrate concentration and low if the diet provides 5% to 25% carbohydrate concentration on an ME basis. Carbohydrate concentration on an ME basis was provided in the product guides for all veterinary therapeutic diets. For OTC diets, carbohydrate concentration was estimated with modified Atwater values applied to GA nutrient concentrations and determined by difference:
Materials and Methods
A reference sample was analyzed with each batch of test samples; results of reference samples were within 2 SDs of the reference sample’s mean.
Samples of commercially available, veterinary therapeutic dry and canned feline diets labeled for obesity and diabetes mellitus (Appendix) were donated from the faculty and staff at the University of CaliforniaDavis Veterinary Medical Teaching Hospital or purchased from local veterinary clinics. Samples of commercially available, OTC canned feline diets considered to have low concentrations of carbohydrates and occasionally recommended23–25 in place of the veterinary therapeutic diets for diabetes mellitus were purchased from local retail outlets. Product name, type, lot number, ingredient list, GA, typical analysis (available from 4 manufacturers for 23 diets), energy density, and expiration date were recorded from product labels, product guides, or manufacturer websites. Total dietary fiber (IDF + HMWSDF) was available from 2 manufacturers for 10 diets. This information was provided on a dry-matter basis for 3 diets and on an ME basis for 7 diets (converted to a dry-matter basis on the basis of measured moisture concentrations). Veterinary therapeutic diets were considered marketed as low-carbohydrate diets if they were identified as having a low carbohydrate content in the associated product guide or on the label. Over-the-counter diets 100
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Carbohydrate (%) = 100 – crude protein (%) + CF (%) + crude fat (%) + ash (%) + moisture (%)
Approximately 200 g of each dry sample was placed in a sealed, labeled plastic bag. Canned samples (unopened cans in a quantity sufficient to provide 708 to 935 g of each diet) were labeled. Samples were submitted to a reference laboratorya and analyzed for moisture with a validated modification of AOAC International method 925.0927 for canned diets and AOAC International method 930.1528 for dry diets. The IDF, HMWSDF, and LMWSDF concentrations were determined by AOAC International method 2011.25.29 Total dietary fiber is defined as IDF + HMWSDF + LMWSDF. Soluble dietary fiber is defined as HMWSDF + LMWSDF. For TDF measurements, the reference laboratory provided a measure of uncertainty of 0.66. Measure of uncertainty was calculated as follows for a reference sample:
Statistical analysis—Reported versus measured moisture concentration, reported CF versus measured TDF concentration, and reported TDF versus measured TDF concentration were compared on the basis of Wilcoxon signed rank tests. Dietary groups (canned and dry, market category, carbohydrate concentration, and presence of added oligosaccharides) were compared on the basis of Mann-Whitney tests for differences in energy density and concentrations of TDF, IDF, HMWSDF, and LMWSDF. All data are reported as median and range unless otherwise specified. Linear regression was performed to evaluate the relationship between dietary caloric content (kcal/kg of dry matter) and measured TDF concentration on a dry-matter, as-fed, and ME basis. Commercial software was used for all analyses.b,c Values of P ≤ 0.05 were considered significant. Results Five dry and 2 canned (loaf-type) diets were donated. Five dry and 13 canned (10 loaf-type and 3 gravyJAVMA, Vol 245, No. 1, July 1, 2014
and TDF, IDF, SDF, and LMWSDF concentrations. For all comparisons, no differences in TDF concentration, TDF composition (Table 1), or energy density were found. Of the 15 canned diets analyzed, 11 were loaftype and 4 were gravy-type products; these types differed only in LMWSDF concentration (P = 0.013). Of the diets analyzed, 9 of the dry diets had corresponding canned products. Five had a loaf-type canned version only, 1 had a gravy-type canned version only, and 3 had both a loaf- and gravy-type canned version). Differences in TDF concentrations between dry and canned versions of the same diet varied greatly, with canned versions having greater TDF concentrations than the dry counterpart in 9 of 12 comparisons. Overall, percentage differences in TDF concentration between canned and dry versions ranged from 8.2% to 77.8% on a dry-matter basis. The overall percentage difference in TDF concentration between dry and loaf-type canned diets ranged from 16.3% to 64.3% of the TDF concentration of the dry diet. For the 4 dry diets with gravy-type canned diet counterparts, the percentage difference in TDF concentration ranged from 8.2% to 77.8%, and only one of these gravy-type canned diets had lower TDF concentration, compared with the dry diet. The percentage differences in TDF concentrations between the loaf- and gravy-type canned products for the same diet (n = 3) were 0.7%, 9.8%, and 42.8%. All these percentage differences describe magnitude but not direction of the difference in TDF concentration. Diets marketed as low-carbohydrate diets were not different in TDF, IDF, SDF, and LMWSDF concentrations, compared with diets not marketed this way (Table 2). The only difference was higher energy density on a dry-matter basis in diets marketed as low-carbohydrate diets (median, 4,243 kcal/kg [1,929 kcal/lb]; range, 3,517 to 5,941 kcal/ kg [1.599 to 2,700 kcal/lb] vs 3,764 kcal/kg [1,711 kcal/lb]; range, 3,057 to 4,148 kcal/kg [1,390 to 1,885 kcal/lb]; P = 0.01). Dry diets marketed as low-carbohydrate diets (n = 3) could not be compared with other dry diets (7) because of small group size. However, canned diets marketed as low-carbohydrate diets (n = 7) had significantly (P = 0.015) higher energy density on a dry-matter basis (4,266 kcal/kg [1,939 kcal/lb]; range, 3,517 to 5,941 kcal/kg) as well as lower TDF (8.3%; range, 4.7% to 13.7%) and IDF (3.3%; range, 1.7% to 9.9%), compared with other canned diets (8; 3,800 kcal/kg [1,727 kcal/lb]; range, 3,178 to 4,148 kcal/ kg [1,445 to 1,885 kcal/lb]; 18.9%%; range, 5.7% to 27.9%; 12.4%; range, 3.2% to 25.6%; respectively). When AAHA guidelines26 to categorize diets on the basis of carbohydrate concentration were applied to the
Table 1—Median (range) concentrations (on a percentage dry-matter basis) of TDF, IDF, HMWSDF, and LMWSDF in various categories of veterinary therapeutic dry, veterinary therapeutic canned, and select OTC canned feline diets intended for management of diabetes mellitus and obesity. Category Dry (n = 10) Canned (n = 15) Veterinary therapeutic canned (n = 12) OTC canned (n = 3) Oligosaccharides on label (n = 6 [4 dry and 2 canned]) Without oligosaccharides on label (n = 19 [6 dry and 13 canned]) Canned loaf type (n = 11) Canned gravy type (n = 4)
TDF (%)
IDF (%)
HMWSDF (%)
LMWSDF (%)
12.2 (8.1–27.2) 13.7 (4.7–27.9) 16.2 (5.7–27.9) 5.5 (4.7–8.3) 11.2 (5.7–27.2) 13.0 (4.7–27.9) 13.7 (4.7–27.9) 15.2 (7.4–20.5)
9.1 (4.0–24.3) 9.4 (1.7–25.6) 10.3 (3.2–25.6) 2.7 (1.7–2.8) 7.4 (3.2–24.3) 9.6 (1.7–25.6) 9.9 (1.7–25.6) 9.3 (3.3–12.5)
3.2 (2.1–5.0) 3.7 (1.9–8.2) 3.8 (1.9–8.2) 2.7 (2.1–6.6) 3.8 (2.5–5.1) 3.5 (1.9–8.2) 3.0 (1.9–6.6) 6.1 (3.6–8.2)
2.0 (1.1–3.0) 2.0 (0.5–7.3) 2.1 (0.5–7.3) 1.2 (1.2–5.6) 1.7 (1.3–2.5) 2.1 (0.5–7.3) 1.6 (0.5–5.6)* 4.8 (2.3–7.3)*
*Values are significantly (P = 0.013) different.
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type) diets were purchased. Overall, dry diets were produced by 4 manufacturers and canned diets by 5 manufacturers. Energy density was reported on labels by manufacturers for 10 of 10 dry diets and 13 of 15 canned diets. Energy-density information was available for all diets when requested from the manufacturers. Of these diets, 19 diets (9 dry and 10 canned) had calculated values provided. For the remaining diets (1 dry and 5 canned), the method of energy density determination was not specified, which implies a measured value obtained via digestibility trials.30 Median energy density was 3,808 kcal/kg on a dry-matter basis (range, 3,057 to 5,941 kcal/kg on a dry-matter basis) for all diets. Energy density negatively correlated with TDF on an asfed (r = –0.64; P < 0.001), dry-matter (r = –0.56; P = 0.004), and ME (r = –0.71; P < 0.001) basis for all diets. No diet exceeded the GA for moisture. The median measured moisture concentration on an as-fed basis was 6.2% (range, 4.23% to 8.0%) for dry diets and 76.5% (range, 66.8% to 84.3%) for canned diets. The median difference between reported maximum moisture concentrations and measured concentrations on an as-fed basis was 3.7% (range, 2.1% to 5.0%) for dry diets (P = 0.002) and 2.8% (range, 1.1% to 11.2%) for canned diets (P < 0.001). Median TDF concentration, on a dry-matter basis, was 12.7% (range, 4.7% to 27.9%) for all diets, 12.2% (range, 8.1% to 27.2%) for dry diets, and 13.8% (range, 4.7% to 27.9%) for canned diets. The median difference between reported maximum CF concentration and measured TDF concentration (as TDF – CF) on a dry-matter basis was 6.5% (range, 4.3% to 10.7%) for dry diets (P = 0.002) and 2.2% (range, 0.05% to 8.20%) for canned diets (P < 0.001). Interestingly, several canned diets had a reported maximum CF concentration that was higher than measured IDF or TDF concentrations. The median difference between reported typical and measured TDF concentrations in diets for which that information was available (6 dry and 4 canned diets) was 3.4% (range, 0.8% to 8.4%) on a dry-matter basis (P = 0.002). Dry veterinary therapeutic diets were compared with all canned diets (12 veterinary and 3 OTC diets) and with only canned veterinary therapeutic diets for energy density and TDF, IDF, SDF, and LMWSDF concentrations. Diets with a distinct source of oligosaccharides (fructooligosaccharides, inulin, chicory, or yeast) in the ingredient list (4 dry and 2 canned diets) were compared with those diets without added oligosaccharides (6 dry and 13 canned diets) for energy density
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Table 2—Median (range) TDF, IDF, HMWSDF, and LMWSDF concentrations (on a percentage dry-matter basis) in various categories of veterinary therapeutic dry, veterinary therapeutic canned, and select OTC canned feline diets for management of diabetes mellitus and obesity. Category
TDF (%)
IDF (%)
HMWSDF (%)
LMWSDF (%)
Marketed as low carbohydrate (n = 10 [7 canned and 3 dry]) Dry (n = 3) Canned (n = 7) Not marketed as low carbohydrate (n = 15 [8 canned and 7 dry]) Dry (n = 7) Canned (n = 8) Low carbohydrate by AAHA guidelines (n = 17 [13 canned and 4 dry]) Dry (n = 4) Canned (n = 13) Not low carbohydrate by AAHA guidelines (n = 8 [2 canned and 6 dry]) Dry (n = 6) Canned (n = 2)
9.4 (4.7–13.7) 12.0 (8.1–12.7) 8.3 (4.7–13.7)* 16.7 (5.7–27.9) 12.4 (9.8–27.2) 18.9 (5.7–27.9)* 12.4 (4.7–25.3) 12.2 (8.1–12.7) 13.0 (4.7–25.3) 16.6 (9.8–27.9) 13.5 (9.8–27.2) 16.7–27.9
6.3 (1.7–9.9) 8.7 (4.0–9.6) 3.3 (1.7–9.9)† 12.3 (3.2–25.6) 10.1 (5.0–24.3) 12.4 (3.2–25.6)† 9.1 (1.7–22.3) 9.1 (4.0–10.1) 9.1 (1.7–22.3) 12.6 (5.0–25.6) 10.0 (5.0–24.3) 12.3–25.6
3.5 (1.9–6.6) 3.4 (3.1–4.2) 3.6 (1.9–6.6) 3.5 (2.1–8.2) 2.9 (2.1–5.0) 4.0 (2.3–8.2) 3.6 (1.9–8.2) 3.2 (2.3–4.2) 3.7 (1.9–8.2) 3.2 (2.1–5.0) 3.2 (2.1–5.0) 2.3–4.4
2.3 (0.5–5.6) 2.4 (1.3–3.0) 2.3 (0.5–5.6) 1.9 (0.8–7.3) 1.9 (1.1–2.5) 1.8 (0.8–7.3) 2.1 (0.5–7.3) 2.2 (1.3–3.0) 2.1 (0.5–7.3) 1.6 (0.9–2.5) 1.7 (1.1–2.5) 0.9–1.7
Diets primarily for obesity (n = 12) Dry (n = 5) Canned veterinary therapeutic (n = 7) Diets primarily for diabetes mellitus (n = 13) Dry (n = 5) Canned (n = 8 [5 veterinary and 3 OTC diets#]) Canned veterinary therapeutic (n = 5)
17.0 (5.7–27.9)‡ 12.4 (9.8–27.2) 17.4 (5.7–27.9)¶ 10.5 (4.7–25.3)‡ 12.0 (8.1–16.4) 9.4 (4.7–25.3)¶ 13.0 (7.4–25.3)
11.5 (3.2–25.6)§ 10.2 (6.1–24.5) 12.3 (3.2–25.6) 8.7 (1.7–22.3)§ 8.7 (4.0–13.0) 6.0 (1.7–22.3) 9.4 (3.3–22.3)
3.3 (2.1–8.2) 2.7 (2.1–4.3) 4.4 (2.3–8.2) 3.5 (1.9–6.6) 3.5 (3.1–5.0) 3.3 (1.9–6.6) 3.6 (1.9–4.1)
1.8 (0.9–7.3) 1.6 (1.1–2.1)║ 2.0 (0.9–7.3) 2.3 (0.5–5.6) 2.5 (1.3–3.0)║ 1.7 (0.5–5.6) 2.3 (0.5–3.5)
Values with the same symbol are significantly different. *Values are significantly (P = 0.008) different. †Values are significantly (P = 0.011) different. ‡Values are significantly (P = 0.030) different. §Values are significantly (P = 0.033) different. ║Values are significantly (P = 0.047) different. ¶Values are significantly (P = 0.049) different. #OTC diets were not compared as a separate group because of small sample size.
products assessed in this study, there were no differences in energy density or TDF, IDF, SDF, or LMWSDF concentrations for all diets and for dry diets (Table 2). Canned diets categorized as low-carbohydrate diets by AAHA guidelines could not be compared as a group with other canned diets because only 2 canned diets were not considered low-carbohydrate diets by this criterion. Energy density on a dry-matter basis was significantly (P = 0.034) different between diets labeled primarily for obesity (3,777 kcal/kg [1,717 kcal/lb]; range, 3,057 to 4,148 kcal/kg), compared with diets labeled primarily for diabetes mellitus (4,168 kcal/kg [1,895 kcal/lb]; range, 3,445 to 5,941 kcal/kg [1,566 to 2,700 kcal/lb]). All diets (dry and canned) labeled for obesity differed in both TDF concentration (P = 0.030) and IDF concentration (P = 0.034), compared with all diets labeled for diabetes mellitus (Table 2). When dry diets labeled for obesity were compared with dry diets labeled for diabetes mellitus, they only differed in LMWSDF concentration (P = 0.047), and canned diets in these categories differed only in TDF concentration (P = 0.049). Discussion The goal of this study was to provide practitioners with clarification between CF and TDF and to report the various fiber fractions that compose TDF with methodology that included LMWSDF, in diets intended to treat obesity and diabetes mellitus. A secondary objective was to further define the inherent limitations with the use of CF to estimate the carbohydrate content of feline diets. Diets high in fiber are generally assumed to be lower in energy density because fiber increases food volume yet adds few to no calories.31–33 In this study, we found a negative correlation between energy density of diets and TDF concentration, as expected. Diets used for management of obesity were lower in energy density, compared with those used for diabetes mellitus, likely driven by a difference in both TDF and IDF concentrations. However, differences in energy den102
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sity between diet groups did not always correspond to a difference in fiber content, likely because differences in energy density also depend on other factors such as fat content. The higher measured versus reported TDF concentrations (available for 6 dry and 4 canned diets) may reflect analytic variation (TDF assays performed at different times or different laboratories); however, the most likely reason for this was the use of different assays. The method used to measure TDF concentration in the study was relatively new, compared with other methods, and included measurement of LMWSDF, whereas typical methods do not. Importantly, LMWSDF comprised a median of 16.76% of TDF concentration and 55.88% of SDF concentration on a dry-matter basis for all diets, implying that this percentage of fiber would be underrepresented by traditional methods of measuring TDF. It is ideal to report not only TDF but also IDF and SDF concentrations, given that these fiber fractions have differing physiologic effects. This information was available from manufacturers for only a few of the diets in this study (IDF concentration for 3 dry diets and SDF concentration for 2 of those 3 diets). Although ingredient lists may contain obvious sources of IDF (cellulose), SDF (guar gum, locust bean gum, carrageenan, oat fiber, psyllium seed husk, and fruits), mixed fiber (flax seed or beet pulp), or LMWSDF (fructooligosaccharides, chicory, yeast, and inulin), quantitative information is more useful, given that estimating fiber content and composition of a diet from the ingredient list is not possible. This was supported by the present findings, in that no differences were determined in the concentrations of fiber types between diets with and without an added source of oligosaccharides on the label. This indicates that either oligosaccharides or additional LMWSDF fractions are in other dietary ingredients or that purified oligosaccharides are not added to diets in concentrations that result in significant differences in LMWSDF concentrations. The lack of differences in fiber concentrations among many groups compared in the present study may reflect JAVMA, Vol 245, No. 1, July 1, 2014
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CF and TDF concentrations of each diet included in the present study to estimate the carbohydrate concentration of the diets. Use of CF concentration, rather than TDF concentration, to estimate the carbohydrate concentration on an ME basis resulted in an estimate of carbohydrate concentration that was 21% (range, 3% to 93%) higher for all diets, 35% (range, 3% to 93%) higher for canned diets labeled for diabetes mellitus (5 veterinary and 3 OTC diets), 28% (range, 13% to 45%) higher for dry diets labeled for diabetes mellitus, 12% (range, 8% to 25%) higher for canned diets labeled for obesity, and 17% (range, 13% to 30%) higher for dry diets labeled for obesity. This emphasizes the importance of measurement and use of TDF concentration to more accurately account for fiber when estimating carbohydrate concentration by difference. Crude fiber concentration is currently the only measurement of fiber required on pet food labels, yet results of the present study and past studies17,19,36 indicate that this is an inaccurate reflection of dietary fiber concentration. Considering the range of LMWSDF concentrations in the diets analyzed here (0.5% to 7.3% on a dry-matter basis), additional studies that include larger numbers and broader categories of diets to assess the use of different TDF measurement methodologies are warranted, especially in situations where LMWSDF may make an important contribution to TDF concentration or have a physiologic role in disease management. Categorizing diets on the basis of carbohydrate concentration, regardless of method, provided limited information regarding fiber concentration or composition. Fiber concentration and composition may have an important effect on the efficacy of diets used to manage feline obesity and diabetes mellitus. Different types of fiber likely result in diverse physiologic effects, and additional research to better determine the physiologic effect of fiber concentration and composition is needed. Previous research that did not consider TDF concentration should be reevaluated in light of the present study. Reporting TDF, IDF, SDF, and LMWSDF concentrations is encouraged so that informed and meaningful nutritional recommendations can be made, with better effects on patient outcome. a. b. c.
Eurofins Scientific, Des Moines, Iowa. Microsoft Excel 2007, Microsoft Corp, Redmond, Wash. Stata/IC 12.1, StataCorp LP, College Station, Tex.
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Lund EM, Armstrong PJ, Kirk CK, et al. Prevalence and risk factors for obesity in adult cats from private US veterinary practice. Int J Appl Res Vet Med 2005;3:88–96. Scarlett JM, Donoghue S. Associations between body condition and disease in cats. J Am Vet Med Assoc 1998;212:1725–1731. Backus RC, Cave NJ, Ganjam VK, et al. Age and body weight effects on glucose and insulin tolerance in colony cats maintained since weaning on high dietary carbohydrate. J Anim Physiol Anim Nutr (Berl) 2010;94:e318–e328. Prola L, Dobenecker B, Kienzle E. Interaction between dietary cellulose content and food intake in cats. J Nutr 2006;136:1988S–1990S. Fekete S, Hullar E, Andrasofszky E, et al. Reduction of the energy density of cat foods by increasing their fibre content with a view to nutrients’ digestibility. J Anim Physiol Anim Nutr (Berl) 2001;85:200–204. Wei A, Fascetti AJ, Villaverde C, et al. Effect of water content in a canned food on voluntary food intake and body weight in cats. Am J Vet Res 2011;72:918–923. Frank G, Anderson W, Pazak H, et al. Use of a high-protein diet in the management of feline diabetes. Vet Ther 2001;2:238–246. Scientific Reports
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the low numbers of diets and uneven group distribution in certain categories as well as the wide range of fiber content and type among diets within a given category. Although there were no differences when dry and canned diets were compared as groups, there were notable differences among individual diets, even those made by the same manufacturer for management of the same disease. Canned diets are often assumed to have less fiber than their dry counterparts; however, in the present study, only 3 canned products had lower TDF concentrations, compared with the dry version. Furthermore, percentage differences between canned and dry versions of the same diet ranged from 8.2% to 77.8% (1 to 10.5 g of TDF/100 g of food) on a dry-matter basis. There was also a difference in LMWSDF concentration between loaf- and gravy-type canned foods, despite similar TDF concentration, which could result in differing physiologic effects. These findings reinforce that there can be marked differences in fiber concentration or composition among diets, and understanding these differences is relevant for clinical trial planning and for recommendations for individual cats. Defining diets with low carbohydrate concentration on the basis of either marketing or AAHA guidelines affected group size and distribution, but there were no differences in any fiber type or proportion among groups when AAHA guidelines were used and only limited differences on the basis of marketing categorization, despite a wide range of fiber concentrations among individual diets. It is often assumed that fiber and carbohydrate content are interdependent; however, the results reported here indicated this was not entirely true. In addition, values from the GA or typical analysis are typically used when estimating carbohydrate concentration on an ME basis. Many clinicians and pet owners do not realize that reported carbohydrate concentrations are not determined by laboratory analysis. Rather, carbohydrate concentration is reported as nitrogenfree extract, which is simply calculated by subtracting the percentage of the diet that is protein, fat, ash, moisture, and (usually crude) fiber from 100%. Estimation of both dietary carbohydrate concentration and energy density is inherently inaccurate unless more precise values for other components are used. For example, similar to other reports,19,34 median measured moisture concentrations in all diets analyzed in this study were less than the reported maximum values, and this difference would be falsely attributed to the carbohydrate fraction. More importantly, categorizations of diets on the basis of CF concentration will underreport the TDF concentration and will therefore overestimate the calories contributed by carbohydrates and subsequently the energy density. Considering the historical use of CF concentration to define individual diets as low- or high-fiber diets and to estimate carbohydrate concentration, previous conclusions regarding the efficacy of individual diets used for weight loss or management of diabetes mellitus on the basis of these values may be inaccurate. This is concerning given a recent report35 that veterinarians commonly recommended diet changes for diabetic cats, usually a change to veterinary therapeutic diets marketed for the management of diabetes mellitus in cats or OTC diets categorized as lowcarbohydrate diets. In some cases, the recommendation may be based on inaccurate categorizations, and many diet options may be unnecessarily omitted. The magnitude of this effect can be illustrated if one were to consider use of
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8. 9.
10. 11. 12. 13.
14.
15.
16. 17.
18. 19.
20. 21. 22.
Mazzaferro EM, Greco DS, Turner AS, et al. Treatment of feline diabetes mellitus using an alpha-glucosidase inhibitor and a low-carbohydrate diet. J Feline Med Surg 2003;5:183–189. Bennett N, Greco DS, Peterson ME, et al. Comparison of a low carbohydrate–low fiber diet and a moderate carbohydrate–high fiber diet in the management of feline diabetes mellitus. J Feline Med Surg 2006;8:73–84. Hall TD, Mahoney O, Rozanski EA, et al. Effects of diet on glucose control in cats with diabetes mellitus treated with twice daily insulin glargine. J Feline Med Surg 2009;11:125–130. Nelson RW, Scott-Moncrief JC, Feldman EC, et al. Effect of dietary insoluble fiber on control of glycemia in cats with naturally acquired diabetes mellitus. J Am Vet Med Assoc 2000;216:1082–1088. Roberfroid MB. Introducing inulin-type fructans. Br J Nutr 2005;93:S13–S25. Vickers RJ, Sunvold GD, Kelley RL, et al. Comparison of fermentation of selected fructooligosaccharides and other fiber substrates by canine colonic microflora. Am J Vet Res 2001;62:609–615. Sunvold GD, Fahey GC, Merchen NR, et al. Dietary fiber for cats: in vitro fermentation of selected fiber sources by cat fecal inoculum and in vivo utilization of diets containing selected fiber sources and their blends. J Anim Sci 1995;73:2329–2339. Verbrugghe A, Hesta M, Daminet S, et al. Propionate absorbed from the colon acts as gluconeogenic substrate in a strict carnivore, the domestic cat (Felis catus). J Anim Physiol Anim Nutr (Berl) 2012;96:1054–1064. Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006;444:1027–1031. de-Oliveira LD, Takakura FS, Kienzle E, et al. Fibre analysis and fibre digestibility in pet foods—a comparison of total dietary fibre, neutral and acid detergent fibre and crude fibre. J Anim Physiol Anim Nutr (Berl) 2012;96:895–906. Van Soest PJ, McQueen RW. The chemistry and estimation of fibre. Proc Nutr Soc 1973;32:123–130. Farcas AK, Larsen JA, Fascetti AJ. Evaluation of fiber concentration in dry and canned commercial diets formulated for adult maintenance or all life stages of dogs by use of crude fiber and total dietary fiber methods. J Am Vet Med Assoc 2013;242:936–940. Hollmann J, Themeier H, Neese U, et al. Dietary fibre fractions in cereal foods measured by a new integrated AOAC method. Food Chem 2013;140:586–589. McCleary BV, DeVries JW, Rader JI, et al. Determination of total dietary fiber (CODEX definition) by enzymatic-gravimetric method and liquid chromatography: collaborative study. J AOAC Int 2010;93:221–233. Brunt K. Pitfall in the determination of the dietary fibre content
23. 24. 25. 26. 27.
28.
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30.
31. 32. 33. 34. 35. 36.
and nutritional value of food products. Qual Assur Saf Crops Foods 2009;1:225–230. Feline Diabetes. Diets for diabetic cats. Available at: www.felinediabetes.com/diabetic-cat-diets.htm. Accessed Sep 9, 2013. Binky’s Page. Canned cat food nutritional information from Jan 2000 to Dec 2004. Available at: binkyspage.tripod.com/CanFoodOld.html. Accessed Sep 9, 2013. Binky’s Page. Canned cat food nutritional information updated March 22, 2008. Available at: binkyspage.tripod.com/CanFoodNew.html. Accessed Sep 9, 2013. Rucinsky R, Cook A, Haley S, et al. AAHA diabetes management guidelines for dogs and cats. J Am Anim Hosp Assoc 2010;46:215–224. AOAC official method 925.09 Solids (total) and loss on drying (moisture) in flour vacuum oven method, Chapter 32. In: Latimer GW Jr, ed. Official methods of analysis of AOAC International. 19th ed. Gaithersburg, Md: AOAC International, 2012;2. AOAC official method 930.15. Loss on drying (moisture) for feeds (at 135°C for 2 hours) dry matter on oven drying for feeds (at 135°C for 2 hours), Chapter 4. In: Latimer GW Jr, ed. Official methods of analysis of AOAC International. 19th ed. Gaithersburg, Md: AOAC International, 2012;2. AOAC official method 2011.25. Insoluble, soluble, and total dietary fiber in foods enzymatic-gravimetric-liquid chromatography first action 2011, Chapter 32. In: Latimer GW Jr, ed. Official methods of analysis of AOAC International. 19th ed. Gaithersburg, Md: AOAC International, 2012;31–41. Association of American Feed Control Officials. Regulation PF9. Statements of calorie content. In: 2013 AAFCO official publication. Oxford, Ind: Association of American Feed Control Officials, 2013;130–131. Roberfroid M, Gibson GR, Delzenne N. The biochemistry of oligofructose, a nondigestible fiber: an approach to calculate its caloric value. Nutr Rev 1993;51:137–146. Roberfroid MB. Caloric value of inulin and oligofructose. J Nutr 1999;129:1436S–1437S. Aust L, Dongowski G, Frenz U, et al. Estimation of available energy of dietary fibres by indirect calorimetry in rats. Eur J Nutr 2001;40:23–29. Hill RC, Choate CJ, Scott KC, et al. Comparison of the guaranteed analysis with the measured nutrient composition of commercial pet foods. J Am Vet Med Assoc 2009;234:347–351. Smith JR, Vrono Z, Rapoport GS, et al. A survey of southeastern United States veterinarians’ preferences for managing cats with diabetes mellitus. J Feline Med Surg 2012;14:716–722. Opitz B, Smith PM, Kienzle E, et al. Comparisons of various methods of fiber analysis in pet foods. J Nutr 1998;128:2795S–2797S.
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Feline veterinary dry, veterinary canned, and select OTC canned foods used for management of diabetes mellitus and obesity in cats. Brand
Line
Name
Type
Hill’s
Prescription Diet
m/d Feline Weight Loss-Low Carbohydrate-Glucose Management m/d Feline Weight Loss-Low Carbohydrate-Glucose Management r/d Feline Weight Loss-Low Calorie r/d Feline Weight Loss-Low Calorie w/d Feline Low Fat-Diabetic-Gastrointestinal w/d Feline Low Fat-Diabetic-Gastrointestinal
Dry Loaf Dry Loaf Dry Loaf
Iams
Veterinary Formula
Glucose and Weight Control Plus Optimum Weight Control Weight Loss/Mobility Plus Restricted-Calorie Weight Loss Restricted-Calorie
Dry Dry Loaf
Purina
Veterinary Diets
DM Dietetic Management Feline Formula DM Dietetic Management Feline Formula DM Savory Selects Dietetic Management Feline Formula OM Overweight Management Feline Formula OM Overweight Management Feline Formula OM Savory Selects Overweight Management Feline Formula Tender Beef Feast Classic
Dry Loaf Gravy Dry Loaf Gravy Loaf
Fancy Feast Royal Canin
Veterinary Diet
Diabetic Diabetic Morsels in Gravy Calorie Control Calorie Control Calorie Control Morsels in Gravy Satiety Support Calorie Control CC High Fiber
Dry Gravy Dry Loaf Gravy Dry Loaf
Natura
EVO
95% Venison
Loaf
Wellness
Complete Health
Chicken Formula
Loaf
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Appendix
Total dietary fiber composition of diets used for management of obesity and diabetes mellitus in cats Tammy J. Owens, DVM; Jennifer A. Larsen, DVM, PhD; Amy K. Farcas, DVM, MS; Richard W. Nelson, DVM; Philip H. Kass, DVM, MPVM, PhD; Andrea J. Fascetti, VMD, PhD Objective—To determine total dietary fiber (TDF) composition of feline diets used for management of obesity and diabetes mellitus. Design—Cross-sectional survey. Sample—Dry veterinary (n = 10), canned veterinary (12), and canned over-the-counter (3) feline diets. Procedures—Percentage of TDF as insoluble dietary fiber (IDF), high-molecular-weight soluble dietary fiber (HMWSDF), and low-molecular-weight soluble dietary fiber (LMWSDF) was determined. Results—Median measured TDF concentration was greater than reported maximum crude fiber content in dry and canned diets. Median TDF (dry-matter) concentration in dry and canned diets was 12.2% (range, 8.11% to 27.16%) and 13.8% (range, 4.7% to 27.9%), respectively. Dry and canned diets, and diets with and without a source of oligosaccharides in the ingredient list, were not different in energy density or concentrations of TDF, IDF, HMWSDF, or LMWSDF. Similarly, loaf-type (n = 11) and gravy-type (4) canned diets differed only in LMWSDF concentration. Disparities in TDF concentrations among products existed despite a lack of differences among groups. Limited differences in TDF concentration and dietary fiber composition were detected when diets were compared on the basis of carbohydrate concentration. Diets labeled for management of obesity were higher in TDF concentration and lower in energy density than diets for management of diabetes mellitus. Conclusions and Clinical Relevance—Diets provided a range of TDF concentrations with variable concentrations of IDF, HMWSDF, and LMWSDF. Crude fiber concentration was not a reliable indicator of TDF concentration or dietary fiber composition. Because carbohydrate content is calculated as a difference, results suggested that use of crude fiber content would cause overestimation of both carbohydrate and energy content of diets. (J Am Vet Med Assoc 2014;245:99–105)
O
besity is prevalent among the domestic feline population1 and is associated with a 4-fold risk of developing diabetes mellitus.2 Obesity likely plays a primary role in insulin resistance in cats, and glucose intolerance with impaired insulin secretion is associated with weight gain.3 The addition of fiber is a common strategy used in obesity management because cats regulate food intake by volume.4 Diets high in water or fiber reduce both energy density and calorie intake4–6 and may be useful in prevention and treatment of both obesity and diabetes mellitus. Although some studies7–10 suggest that diets with low carbohydrate content and high protein content From the Veterinary Medical Teaching Hospital (Owens), the Departments of Molecular Biosciences (Larsen, Fascetti), Medicine and Epidemiology (Nelson), and Population Health and Reproduction (Kass), School of Veterinary Medicine, and the Department of Animal Science, College of Agriculture and Environmental Sciences (Farcas), University of California-Davis, Davis, CA 95616. Dr. Farcas’s present address is Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104. Supported in part by the Center for Companion Animal Health, School of Veterinary Medicine, University of California-Davis, and by Barbara Smith. Dr. Owens was supported by an educational grant from the Nestlé Purina PetCare Co. Presented in abstract form at the 13th Annual American Academy of Veterinary Nutrition and Research Symposium, Seattle, June 2013. Address correspondence to Dr. Fascetti ([email protected]). JAVMA, Vol 245, No. 1, July 1, 2014
ABBREVIATIONS AAHA AOAC CF GA HMWSDF IDF LMWSDF ME OTC SDF TDF
American Animal Hospital Association Association of Analytical Communities Crude fiber Guaranteed analysis High-molecular-weight soluble dietary fiber Insoluble dietary fiber Low-molecular-weight soluble dietary fiber Metabolizable energy Over-the-counter Soluble dietary fiber Total dietary fiber
may be advantageous in managing feline diabetes mellitus, the fiber types and concentrations of the diets in those studies were not well characterized. Other diets intended to manage feline obesity or diabetes mellitus highlight an increased fiber content in their product guides or marketing materials; however, direct comparison among diets is not possible because TDF (composed of IDF, HMWSDF, and LMWSDF) information is often not provided. Quantification of fiber fractions is valuable, given that the effects of fiber types are not uniform. Fiber supplementation, particularly IDF, may affect nutrient absorption and modulation of postprandial glycemic response,11 whereas short-chain fatty acid Scientific Reports
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production from bacterial fermentation of SDF (eg, inulin and fructooligosaccharides) supports beneficial colonic microbial populations,12–15 which are recognized as having a role in controlling obesity.16 Crude fiber, a required component of the GA of a pet food label, remains the only representation of fiber for most cat foods. The method for CF analysis, developed in 1806, recovers variable fractions of cellulose, hemicellulose, and lignin,17,18 which provides incomplete information on IDF content only. Crude fiber is a poor reflection of TDF, which can vary greatly among diets.17,19 However, traditional laboratory analysis of TDF also has limitations, given that the most commonly used methodology does not detect or quantify LMWSDF (oligosaccharides and most types of resistant starch). Until recently, there was not a practical method to quantify LMWSDF in addition to the IDF and HMWSDF typically measured and reported as TDF. Newer methodology has been recently developed,20,21 but further validation is needed, and widespread use has not yet occurred. As such, reported TDF concentrations may be underestimated depending on the method of measurement used.22 The objective of the study reported here was to determine TDF content as IDF, HMWSDF, and LMWSDF in veterinary therapeutic feline diets labeled for obesity and diabetes mellitus as well as a limited number of OTC canned diets occasionally recommended for feline diabetes mellitus, by means of an updated method of measuring TDF. We hypothesized that measured TDF would be greater than reported maximum CF, that TDF and LMWSDF would be greater in dry diets than in canned diets, and that LMWSDF concentrations would be greater in diets with added oligosaccharides, compared with those without. We further hypothesized that TDF concentration would be lower in low-carbohydrate diets versus other diets and higher in diets primarily recommended for obesity versus those primarily used for diabetes mellitus.
were considered marketed as low-carbohydrate diets if this was either a noted feature on the label or if the diet was included in widely available low-carbohydrate diet lists.23–25 Diets were also compared on the basis of carbohydrate concentrations recommended by the AAHA Diabetes Management Guidelines.26 These guidelines provide medical and nutritional management recommendations that include limiting carbohydrate intake. Carbohydrate concentrations in diets are defined as ultralow if the diet provides < 5% carbohydrate concentration and low if the diet provides 5% to 25% carbohydrate concentration on an ME basis. Carbohydrate concentration on an ME basis was provided in the product guides for all veterinary therapeutic diets. For OTC diets, carbohydrate concentration was estimated with modified Atwater values applied to GA nutrient concentrations and determined by difference:
Materials and Methods
A reference sample was analyzed with each batch of test samples; results of reference samples were within 2 SDs of the reference sample’s mean.
Samples of commercially available, veterinary therapeutic dry and canned feline diets labeled for obesity and diabetes mellitus (Appendix) were donated from the faculty and staff at the University of CaliforniaDavis Veterinary Medical Teaching Hospital or purchased from local veterinary clinics. Samples of commercially available, OTC canned feline diets considered to have low concentrations of carbohydrates and occasionally recommended23–25 in place of the veterinary therapeutic diets for diabetes mellitus were purchased from local retail outlets. Product name, type, lot number, ingredient list, GA, typical analysis (available from 4 manufacturers for 23 diets), energy density, and expiration date were recorded from product labels, product guides, or manufacturer websites. Total dietary fiber (IDF + HMWSDF) was available from 2 manufacturers for 10 diets. This information was provided on a dry-matter basis for 3 diets and on an ME basis for 7 diets (converted to a dry-matter basis on the basis of measured moisture concentrations). Veterinary therapeutic diets were considered marketed as low-carbohydrate diets if they were identified as having a low carbohydrate content in the associated product guide or on the label. Over-the-counter diets 100
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Carbohydrate (%) = 100 – crude protein (%) + CF (%) + crude fat (%) + ash (%) + moisture (%)
Approximately 200 g of each dry sample was placed in a sealed, labeled plastic bag. Canned samples (unopened cans in a quantity sufficient to provide 708 to 935 g of each diet) were labeled. Samples were submitted to a reference laboratorya and analyzed for moisture with a validated modification of AOAC International method 925.0927 for canned diets and AOAC International method 930.1528 for dry diets. The IDF, HMWSDF, and LMWSDF concentrations were determined by AOAC International method 2011.25.29 Total dietary fiber is defined as IDF + HMWSDF + LMWSDF. Soluble dietary fiber is defined as HMWSDF + LMWSDF. For TDF measurements, the reference laboratory provided a measure of uncertainty of 0.66. Measure of uncertainty was calculated as follows for a reference sample:
Statistical analysis—Reported versus measured moisture concentration, reported CF versus measured TDF concentration, and reported TDF versus measured TDF concentration were compared on the basis of Wilcoxon signed rank tests. Dietary groups (canned and dry, market category, carbohydrate concentration, and presence of added oligosaccharides) were compared on the basis of Mann-Whitney tests for differences in energy density and concentrations of TDF, IDF, HMWSDF, and LMWSDF. All data are reported as median and range unless otherwise specified. Linear regression was performed to evaluate the relationship between dietary caloric content (kcal/kg of dry matter) and measured TDF concentration on a dry-matter, as-fed, and ME basis. Commercial software was used for all analyses.b,c Values of P ≤ 0.05 were considered significant. Results Five dry and 2 canned (loaf-type) diets were donated. Five dry and 13 canned (10 loaf-type and 3 gravyJAVMA, Vol 245, No. 1, July 1, 2014
and TDF, IDF, SDF, and LMWSDF concentrations. For all comparisons, no differences in TDF concentration, TDF composition (Table 1), or energy density were found. Of the 15 canned diets analyzed, 11 were loaftype and 4 were gravy-type products; these types differed only in LMWSDF concentration (P = 0.013). Of the diets analyzed, 9 of the dry diets had corresponding canned products. Five had a loaf-type canned version only, 1 had a gravy-type canned version only, and 3 had both a loaf- and gravy-type canned version). Differences in TDF concentrations between dry and canned versions of the same diet varied greatly, with canned versions having greater TDF concentrations than the dry counterpart in 9 of 12 comparisons. Overall, percentage differences in TDF concentration between canned and dry versions ranged from 8.2% to 77.8% on a dry-matter basis. The overall percentage difference in TDF concentration between dry and loaf-type canned diets ranged from 16.3% to 64.3% of the TDF concentration of the dry diet. For the 4 dry diets with gravy-type canned diet counterparts, the percentage difference in TDF concentration ranged from 8.2% to 77.8%, and only one of these gravy-type canned diets had lower TDF concentration, compared with the dry diet. The percentage differences in TDF concentrations between the loaf- and gravy-type canned products for the same diet (n = 3) were 0.7%, 9.8%, and 42.8%. All these percentage differences describe magnitude but not direction of the difference in TDF concentration. Diets marketed as low-carbohydrate diets were not different in TDF, IDF, SDF, and LMWSDF concentrations, compared with diets not marketed this way (Table 2). The only difference was higher energy density on a dry-matter basis in diets marketed as low-carbohydrate diets (median, 4,243 kcal/kg [1,929 kcal/lb]; range, 3,517 to 5,941 kcal/ kg [1.599 to 2,700 kcal/lb] vs 3,764 kcal/kg [1,711 kcal/lb]; range, 3,057 to 4,148 kcal/kg [1,390 to 1,885 kcal/lb]; P = 0.01). Dry diets marketed as low-carbohydrate diets (n = 3) could not be compared with other dry diets (7) because of small group size. However, canned diets marketed as low-carbohydrate diets (n = 7) had significantly (P = 0.015) higher energy density on a dry-matter basis (4,266 kcal/kg [1,939 kcal/lb]; range, 3,517 to 5,941 kcal/kg) as well as lower TDF (8.3%; range, 4.7% to 13.7%) and IDF (3.3%; range, 1.7% to 9.9%), compared with other canned diets (8; 3,800 kcal/kg [1,727 kcal/lb]; range, 3,178 to 4,148 kcal/ kg [1,445 to 1,885 kcal/lb]; 18.9%%; range, 5.7% to 27.9%; 12.4%; range, 3.2% to 25.6%; respectively). When AAHA guidelines26 to categorize diets on the basis of carbohydrate concentration were applied to the
Table 1—Median (range) concentrations (on a percentage dry-matter basis) of TDF, IDF, HMWSDF, and LMWSDF in various categories of veterinary therapeutic dry, veterinary therapeutic canned, and select OTC canned feline diets intended for management of diabetes mellitus and obesity. Category Dry (n = 10) Canned (n = 15) Veterinary therapeutic canned (n = 12) OTC canned (n = 3) Oligosaccharides on label (n = 6 [4 dry and 2 canned]) Without oligosaccharides on label (n = 19 [6 dry and 13 canned]) Canned loaf type (n = 11) Canned gravy type (n = 4)
TDF (%)
IDF (%)
HMWSDF (%)
LMWSDF (%)
12.2 (8.1–27.2) 13.7 (4.7–27.9) 16.2 (5.7–27.9) 5.5 (4.7–8.3) 11.2 (5.7–27.2) 13.0 (4.7–27.9) 13.7 (4.7–27.9) 15.2 (7.4–20.5)
9.1 (4.0–24.3) 9.4 (1.7–25.6) 10.3 (3.2–25.6) 2.7 (1.7–2.8) 7.4 (3.2–24.3) 9.6 (1.7–25.6) 9.9 (1.7–25.6) 9.3 (3.3–12.5)
3.2 (2.1–5.0) 3.7 (1.9–8.2) 3.8 (1.9–8.2) 2.7 (2.1–6.6) 3.8 (2.5–5.1) 3.5 (1.9–8.2) 3.0 (1.9–6.6) 6.1 (3.6–8.2)
2.0 (1.1–3.0) 2.0 (0.5–7.3) 2.1 (0.5–7.3) 1.2 (1.2–5.6) 1.7 (1.3–2.5) 2.1 (0.5–7.3) 1.6 (0.5–5.6)* 4.8 (2.3–7.3)*
*Values are significantly (P = 0.013) different.
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type) diets were purchased. Overall, dry diets were produced by 4 manufacturers and canned diets by 5 manufacturers. Energy density was reported on labels by manufacturers for 10 of 10 dry diets and 13 of 15 canned diets. Energy-density information was available for all diets when requested from the manufacturers. Of these diets, 19 diets (9 dry and 10 canned) had calculated values provided. For the remaining diets (1 dry and 5 canned), the method of energy density determination was not specified, which implies a measured value obtained via digestibility trials.30 Median energy density was 3,808 kcal/kg on a dry-matter basis (range, 3,057 to 5,941 kcal/kg on a dry-matter basis) for all diets. Energy density negatively correlated with TDF on an asfed (r = –0.64; P < 0.001), dry-matter (r = –0.56; P = 0.004), and ME (r = –0.71; P < 0.001) basis for all diets. No diet exceeded the GA for moisture. The median measured moisture concentration on an as-fed basis was 6.2% (range, 4.23% to 8.0%) for dry diets and 76.5% (range, 66.8% to 84.3%) for canned diets. The median difference between reported maximum moisture concentrations and measured concentrations on an as-fed basis was 3.7% (range, 2.1% to 5.0%) for dry diets (P = 0.002) and 2.8% (range, 1.1% to 11.2%) for canned diets (P < 0.001). Median TDF concentration, on a dry-matter basis, was 12.7% (range, 4.7% to 27.9%) for all diets, 12.2% (range, 8.1% to 27.2%) for dry diets, and 13.8% (range, 4.7% to 27.9%) for canned diets. The median difference between reported maximum CF concentration and measured TDF concentration (as TDF – CF) on a dry-matter basis was 6.5% (range, 4.3% to 10.7%) for dry diets (P = 0.002) and 2.2% (range, 0.05% to 8.20%) for canned diets (P < 0.001). Interestingly, several canned diets had a reported maximum CF concentration that was higher than measured IDF or TDF concentrations. The median difference between reported typical and measured TDF concentrations in diets for which that information was available (6 dry and 4 canned diets) was 3.4% (range, 0.8% to 8.4%) on a dry-matter basis (P = 0.002). Dry veterinary therapeutic diets were compared with all canned diets (12 veterinary and 3 OTC diets) and with only canned veterinary therapeutic diets for energy density and TDF, IDF, SDF, and LMWSDF concentrations. Diets with a distinct source of oligosaccharides (fructooligosaccharides, inulin, chicory, or yeast) in the ingredient list (4 dry and 2 canned diets) were compared with those diets without added oligosaccharides (6 dry and 13 canned diets) for energy density
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Table 2—Median (range) TDF, IDF, HMWSDF, and LMWSDF concentrations (on a percentage dry-matter basis) in various categories of veterinary therapeutic dry, veterinary therapeutic canned, and select OTC canned feline diets for management of diabetes mellitus and obesity. Category
TDF (%)
IDF (%)
HMWSDF (%)
LMWSDF (%)
Marketed as low carbohydrate (n = 10 [7 canned and 3 dry]) Dry (n = 3) Canned (n = 7) Not marketed as low carbohydrate (n = 15 [8 canned and 7 dry]) Dry (n = 7) Canned (n = 8) Low carbohydrate by AAHA guidelines (n = 17 [13 canned and 4 dry]) Dry (n = 4) Canned (n = 13) Not low carbohydrate by AAHA guidelines (n = 8 [2 canned and 6 dry]) Dry (n = 6) Canned (n = 2)
9.4 (4.7–13.7) 12.0 (8.1–12.7) 8.3 (4.7–13.7)* 16.7 (5.7–27.9) 12.4 (9.8–27.2) 18.9 (5.7–27.9)* 12.4 (4.7–25.3) 12.2 (8.1–12.7) 13.0 (4.7–25.3) 16.6 (9.8–27.9) 13.5 (9.8–27.2) 16.7–27.9
6.3 (1.7–9.9) 8.7 (4.0–9.6) 3.3 (1.7–9.9)† 12.3 (3.2–25.6) 10.1 (5.0–24.3) 12.4 (3.2–25.6)† 9.1 (1.7–22.3) 9.1 (4.0–10.1) 9.1 (1.7–22.3) 12.6 (5.0–25.6) 10.0 (5.0–24.3) 12.3–25.6
3.5 (1.9–6.6) 3.4 (3.1–4.2) 3.6 (1.9–6.6) 3.5 (2.1–8.2) 2.9 (2.1–5.0) 4.0 (2.3–8.2) 3.6 (1.9–8.2) 3.2 (2.3–4.2) 3.7 (1.9–8.2) 3.2 (2.1–5.0) 3.2 (2.1–5.0) 2.3–4.4
2.3 (0.5–5.6) 2.4 (1.3–3.0) 2.3 (0.5–5.6) 1.9 (0.8–7.3) 1.9 (1.1–2.5) 1.8 (0.8–7.3) 2.1 (0.5–7.3) 2.2 (1.3–3.0) 2.1 (0.5–7.3) 1.6 (0.9–2.5) 1.7 (1.1–2.5) 0.9–1.7
Diets primarily for obesity (n = 12) Dry (n = 5) Canned veterinary therapeutic (n = 7) Diets primarily for diabetes mellitus (n = 13) Dry (n = 5) Canned (n = 8 [5 veterinary and 3 OTC diets#]) Canned veterinary therapeutic (n = 5)
17.0 (5.7–27.9)‡ 12.4 (9.8–27.2) 17.4 (5.7–27.9)¶ 10.5 (4.7–25.3)‡ 12.0 (8.1–16.4) 9.4 (4.7–25.3)¶ 13.0 (7.4–25.3)
11.5 (3.2–25.6)§ 10.2 (6.1–24.5) 12.3 (3.2–25.6) 8.7 (1.7–22.3)§ 8.7 (4.0–13.0) 6.0 (1.7–22.3) 9.4 (3.3–22.3)
3.3 (2.1–8.2) 2.7 (2.1–4.3) 4.4 (2.3–8.2) 3.5 (1.9–6.6) 3.5 (3.1–5.0) 3.3 (1.9–6.6) 3.6 (1.9–4.1)
1.8 (0.9–7.3) 1.6 (1.1–2.1)║ 2.0 (0.9–7.3) 2.3 (0.5–5.6) 2.5 (1.3–3.0)║ 1.7 (0.5–5.6) 2.3 (0.5–3.5)
Values with the same symbol are significantly different. *Values are significantly (P = 0.008) different. †Values are significantly (P = 0.011) different. ‡Values are significantly (P = 0.030) different. §Values are significantly (P = 0.033) different. ║Values are significantly (P = 0.047) different. ¶Values are significantly (P = 0.049) different. #OTC diets were not compared as a separate group because of small sample size.
products assessed in this study, there were no differences in energy density or TDF, IDF, SDF, or LMWSDF concentrations for all diets and for dry diets (Table 2). Canned diets categorized as low-carbohydrate diets by AAHA guidelines could not be compared as a group with other canned diets because only 2 canned diets were not considered low-carbohydrate diets by this criterion. Energy density on a dry-matter basis was significantly (P = 0.034) different between diets labeled primarily for obesity (3,777 kcal/kg [1,717 kcal/lb]; range, 3,057 to 4,148 kcal/kg), compared with diets labeled primarily for diabetes mellitus (4,168 kcal/kg [1,895 kcal/lb]; range, 3,445 to 5,941 kcal/kg [1,566 to 2,700 kcal/lb]). All diets (dry and canned) labeled for obesity differed in both TDF concentration (P = 0.030) and IDF concentration (P = 0.034), compared with all diets labeled for diabetes mellitus (Table 2). When dry diets labeled for obesity were compared with dry diets labeled for diabetes mellitus, they only differed in LMWSDF concentration (P = 0.047), and canned diets in these categories differed only in TDF concentration (P = 0.049). Discussion The goal of this study was to provide practitioners with clarification between CF and TDF and to report the various fiber fractions that compose TDF with methodology that included LMWSDF, in diets intended to treat obesity and diabetes mellitus. A secondary objective was to further define the inherent limitations with the use of CF to estimate the carbohydrate content of feline diets. Diets high in fiber are generally assumed to be lower in energy density because fiber increases food volume yet adds few to no calories.31–33 In this study, we found a negative correlation between energy density of diets and TDF concentration, as expected. Diets used for management of obesity were lower in energy density, compared with those used for diabetes mellitus, likely driven by a difference in both TDF and IDF concentrations. However, differences in energy den102
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sity between diet groups did not always correspond to a difference in fiber content, likely because differences in energy density also depend on other factors such as fat content. The higher measured versus reported TDF concentrations (available for 6 dry and 4 canned diets) may reflect analytic variation (TDF assays performed at different times or different laboratories); however, the most likely reason for this was the use of different assays. The method used to measure TDF concentration in the study was relatively new, compared with other methods, and included measurement of LMWSDF, whereas typical methods do not. Importantly, LMWSDF comprised a median of 16.76% of TDF concentration and 55.88% of SDF concentration on a dry-matter basis for all diets, implying that this percentage of fiber would be underrepresented by traditional methods of measuring TDF. It is ideal to report not only TDF but also IDF and SDF concentrations, given that these fiber fractions have differing physiologic effects. This information was available from manufacturers for only a few of the diets in this study (IDF concentration for 3 dry diets and SDF concentration for 2 of those 3 diets). Although ingredient lists may contain obvious sources of IDF (cellulose), SDF (guar gum, locust bean gum, carrageenan, oat fiber, psyllium seed husk, and fruits), mixed fiber (flax seed or beet pulp), or LMWSDF (fructooligosaccharides, chicory, yeast, and inulin), quantitative information is more useful, given that estimating fiber content and composition of a diet from the ingredient list is not possible. This was supported by the present findings, in that no differences were determined in the concentrations of fiber types between diets with and without an added source of oligosaccharides on the label. This indicates that either oligosaccharides or additional LMWSDF fractions are in other dietary ingredients or that purified oligosaccharides are not added to diets in concentrations that result in significant differences in LMWSDF concentrations. The lack of differences in fiber concentrations among many groups compared in the present study may reflect JAVMA, Vol 245, No. 1, July 1, 2014
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CF and TDF concentrations of each diet included in the present study to estimate the carbohydrate concentration of the diets. Use of CF concentration, rather than TDF concentration, to estimate the carbohydrate concentration on an ME basis resulted in an estimate of carbohydrate concentration that was 21% (range, 3% to 93%) higher for all diets, 35% (range, 3% to 93%) higher for canned diets labeled for diabetes mellitus (5 veterinary and 3 OTC diets), 28% (range, 13% to 45%) higher for dry diets labeled for diabetes mellitus, 12% (range, 8% to 25%) higher for canned diets labeled for obesity, and 17% (range, 13% to 30%) higher for dry diets labeled for obesity. This emphasizes the importance of measurement and use of TDF concentration to more accurately account for fiber when estimating carbohydrate concentration by difference. Crude fiber concentration is currently the only measurement of fiber required on pet food labels, yet results of the present study and past studies17,19,36 indicate that this is an inaccurate reflection of dietary fiber concentration. Considering the range of LMWSDF concentrations in the diets analyzed here (0.5% to 7.3% on a dry-matter basis), additional studies that include larger numbers and broader categories of diets to assess the use of different TDF measurement methodologies are warranted, especially in situations where LMWSDF may make an important contribution to TDF concentration or have a physiologic role in disease management. Categorizing diets on the basis of carbohydrate concentration, regardless of method, provided limited information regarding fiber concentration or composition. Fiber concentration and composition may have an important effect on the efficacy of diets used to manage feline obesity and diabetes mellitus. Different types of fiber likely result in diverse physiologic effects, and additional research to better determine the physiologic effect of fiber concentration and composition is needed. Previous research that did not consider TDF concentration should be reevaluated in light of the present study. Reporting TDF, IDF, SDF, and LMWSDF concentrations is encouraged so that informed and meaningful nutritional recommendations can be made, with better effects on patient outcome. a. b. c.
Eurofins Scientific, Des Moines, Iowa. Microsoft Excel 2007, Microsoft Corp, Redmond, Wash. Stata/IC 12.1, StataCorp LP, College Station, Tex.
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Lund EM, Armstrong PJ, Kirk CK, et al. Prevalence and risk factors for obesity in adult cats from private US veterinary practice. Int J Appl Res Vet Med 2005;3:88–96. Scarlett JM, Donoghue S. Associations between body condition and disease in cats. J Am Vet Med Assoc 1998;212:1725–1731. Backus RC, Cave NJ, Ganjam VK, et al. Age and body weight effects on glucose and insulin tolerance in colony cats maintained since weaning on high dietary carbohydrate. J Anim Physiol Anim Nutr (Berl) 2010;94:e318–e328. Prola L, Dobenecker B, Kienzle E. Interaction between dietary cellulose content and food intake in cats. J Nutr 2006;136:1988S–1990S. Fekete S, Hullar E, Andrasofszky E, et al. Reduction of the energy density of cat foods by increasing their fibre content with a view to nutrients’ digestibility. J Anim Physiol Anim Nutr (Berl) 2001;85:200–204. Wei A, Fascetti AJ, Villaverde C, et al. Effect of water content in a canned food on voluntary food intake and body weight in cats. Am J Vet Res 2011;72:918–923. Frank G, Anderson W, Pazak H, et al. Use of a high-protein diet in the management of feline diabetes. Vet Ther 2001;2:238–246. Scientific Reports
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the low numbers of diets and uneven group distribution in certain categories as well as the wide range of fiber content and type among diets within a given category. Although there were no differences when dry and canned diets were compared as groups, there were notable differences among individual diets, even those made by the same manufacturer for management of the same disease. Canned diets are often assumed to have less fiber than their dry counterparts; however, in the present study, only 3 canned products had lower TDF concentrations, compared with the dry version. Furthermore, percentage differences between canned and dry versions of the same diet ranged from 8.2% to 77.8% (1 to 10.5 g of TDF/100 g of food) on a dry-matter basis. There was also a difference in LMWSDF concentration between loaf- and gravy-type canned foods, despite similar TDF concentration, which could result in differing physiologic effects. These findings reinforce that there can be marked differences in fiber concentration or composition among diets, and understanding these differences is relevant for clinical trial planning and for recommendations for individual cats. Defining diets with low carbohydrate concentration on the basis of either marketing or AAHA guidelines affected group size and distribution, but there were no differences in any fiber type or proportion among groups when AAHA guidelines were used and only limited differences on the basis of marketing categorization, despite a wide range of fiber concentrations among individual diets. It is often assumed that fiber and carbohydrate content are interdependent; however, the results reported here indicated this was not entirely true. In addition, values from the GA or typical analysis are typically used when estimating carbohydrate concentration on an ME basis. Many clinicians and pet owners do not realize that reported carbohydrate concentrations are not determined by laboratory analysis. Rather, carbohydrate concentration is reported as nitrogenfree extract, which is simply calculated by subtracting the percentage of the diet that is protein, fat, ash, moisture, and (usually crude) fiber from 100%. Estimation of both dietary carbohydrate concentration and energy density is inherently inaccurate unless more precise values for other components are used. For example, similar to other reports,19,34 median measured moisture concentrations in all diets analyzed in this study were less than the reported maximum values, and this difference would be falsely attributed to the carbohydrate fraction. More importantly, categorizations of diets on the basis of CF concentration will underreport the TDF concentration and will therefore overestimate the calories contributed by carbohydrates and subsequently the energy density. Considering the historical use of CF concentration to define individual diets as low- or high-fiber diets and to estimate carbohydrate concentration, previous conclusions regarding the efficacy of individual diets used for weight loss or management of diabetes mellitus on the basis of these values may be inaccurate. This is concerning given a recent report35 that veterinarians commonly recommended diet changes for diabetic cats, usually a change to veterinary therapeutic diets marketed for the management of diabetes mellitus in cats or OTC diets categorized as lowcarbohydrate diets. In some cases, the recommendation may be based on inaccurate categorizations, and many diet options may be unnecessarily omitted. The magnitude of this effect can be illustrated if one were to consider use of
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Mazzaferro EM, Greco DS, Turner AS, et al. Treatment of feline diabetes mellitus using an alpha-glucosidase inhibitor and a low-carbohydrate diet. J Feline Med Surg 2003;5:183–189. Bennett N, Greco DS, Peterson ME, et al. Comparison of a low carbohydrate–low fiber diet and a moderate carbohydrate–high fiber diet in the management of feline diabetes mellitus. J Feline Med Surg 2006;8:73–84. Hall TD, Mahoney O, Rozanski EA, et al. Effects of diet on glucose control in cats with diabetes mellitus treated with twice daily insulin glargine. J Feline Med Surg 2009;11:125–130. Nelson RW, Scott-Moncrief JC, Feldman EC, et al. Effect of dietary insoluble fiber on control of glycemia in cats with naturally acquired diabetes mellitus. J Am Vet Med Assoc 2000;216:1082–1088. Roberfroid MB. Introducing inulin-type fructans. Br J Nutr 2005;93:S13–S25. Vickers RJ, Sunvold GD, Kelley RL, et al. Comparison of fermentation of selected fructooligosaccharides and other fiber substrates by canine colonic microflora. Am J Vet Res 2001;62:609–615. Sunvold GD, Fahey GC, Merchen NR, et al. Dietary fiber for cats: in vitro fermentation of selected fiber sources by cat fecal inoculum and in vivo utilization of diets containing selected fiber sources and their blends. J Anim Sci 1995;73:2329–2339. Verbrugghe A, Hesta M, Daminet S, et al. Propionate absorbed from the colon acts as gluconeogenic substrate in a strict carnivore, the domestic cat (Felis catus). J Anim Physiol Anim Nutr (Berl) 2012;96:1054–1064. Turnbaugh PJ, Ley RE, Mahowald MA, et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006;444:1027–1031. de-Oliveira LD, Takakura FS, Kienzle E, et al. Fibre analysis and fibre digestibility in pet foods—a comparison of total dietary fibre, neutral and acid detergent fibre and crude fibre. J Anim Physiol Anim Nutr (Berl) 2012;96:895–906. Van Soest PJ, McQueen RW. The chemistry and estimation of fibre. Proc Nutr Soc 1973;32:123–130. Farcas AK, Larsen JA, Fascetti AJ. Evaluation of fiber concentration in dry and canned commercial diets formulated for adult maintenance or all life stages of dogs by use of crude fiber and total dietary fiber methods. J Am Vet Med Assoc 2013;242:936–940. Hollmann J, Themeier H, Neese U, et al. Dietary fibre fractions in cereal foods measured by a new integrated AOAC method. Food Chem 2013;140:586–589. McCleary BV, DeVries JW, Rader JI, et al. Determination of total dietary fiber (CODEX definition) by enzymatic-gravimetric method and liquid chromatography: collaborative study. J AOAC Int 2010;93:221–233. Brunt K. Pitfall in the determination of the dietary fibre content
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and nutritional value of food products. Qual Assur Saf Crops Foods 2009;1:225–230. Feline Diabetes. Diets for diabetic cats. Available at: www.felinediabetes.com/diabetic-cat-diets.htm. Accessed Sep 9, 2013. Binky’s Page. Canned cat food nutritional information from Jan 2000 to Dec 2004. Available at: binkyspage.tripod.com/CanFoodOld.html. Accessed Sep 9, 2013. Binky’s Page. Canned cat food nutritional information updated March 22, 2008. Available at: binkyspage.tripod.com/CanFoodNew.html. Accessed Sep 9, 2013. Rucinsky R, Cook A, Haley S, et al. AAHA diabetes management guidelines for dogs and cats. J Am Anim Hosp Assoc 2010;46:215–224. AOAC official method 925.09 Solids (total) and loss on drying (moisture) in flour vacuum oven method, Chapter 32. In: Latimer GW Jr, ed. Official methods of analysis of AOAC International. 19th ed. Gaithersburg, Md: AOAC International, 2012;2. AOAC official method 930.15. Loss on drying (moisture) for feeds (at 135°C for 2 hours) dry matter on oven drying for feeds (at 135°C for 2 hours), Chapter 4. In: Latimer GW Jr, ed. Official methods of analysis of AOAC International. 19th ed. Gaithersburg, Md: AOAC International, 2012;2. AOAC official method 2011.25. Insoluble, soluble, and total dietary fiber in foods enzymatic-gravimetric-liquid chromatography first action 2011, Chapter 32. In: Latimer GW Jr, ed. Official methods of analysis of AOAC International. 19th ed. Gaithersburg, Md: AOAC International, 2012;31–41. Association of American Feed Control Officials. Regulation PF9. Statements of calorie content. In: 2013 AAFCO official publication. Oxford, Ind: Association of American Feed Control Officials, 2013;130–131. Roberfroid M, Gibson GR, Delzenne N. The biochemistry of oligofructose, a nondigestible fiber: an approach to calculate its caloric value. Nutr Rev 1993;51:137–146. Roberfroid MB. Caloric value of inulin and oligofructose. J Nutr 1999;129:1436S–1437S. Aust L, Dongowski G, Frenz U, et al. Estimation of available energy of dietary fibres by indirect calorimetry in rats. Eur J Nutr 2001;40:23–29. Hill RC, Choate CJ, Scott KC, et al. Comparison of the guaranteed analysis with the measured nutrient composition of commercial pet foods. J Am Vet Med Assoc 2009;234:347–351. Smith JR, Vrono Z, Rapoport GS, et al. A survey of southeastern United States veterinarians’ preferences for managing cats with diabetes mellitus. J Feline Med Surg 2012;14:716–722. Opitz B, Smith PM, Kienzle E, et al. Comparisons of various methods of fiber analysis in pet foods. J Nutr 1998;128:2795S–2797S.
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Feline veterinary dry, veterinary canned, and select OTC canned foods used for management of diabetes mellitus and obesity in cats. Brand
Line
Name
Type
Hill’s
Prescription Diet
m/d Feline Weight Loss-Low Carbohydrate-Glucose Management m/d Feline Weight Loss-Low Carbohydrate-Glucose Management r/d Feline Weight Loss-Low Calorie r/d Feline Weight Loss-Low Calorie w/d Feline Low Fat-Diabetic-Gastrointestinal w/d Feline Low Fat-Diabetic-Gastrointestinal
Dry Loaf Dry Loaf Dry Loaf
Iams
Veterinary Formula
Glucose and Weight Control Plus Optimum Weight Control Weight Loss/Mobility Plus Restricted-Calorie Weight Loss Restricted-Calorie
Dry Dry Loaf
Purina
Veterinary Diets
DM Dietetic Management Feline Formula DM Dietetic Management Feline Formula DM Savory Selects Dietetic Management Feline Formula OM Overweight Management Feline Formula OM Overweight Management Feline Formula OM Savory Selects Overweight Management Feline Formula Tender Beef Feast Classic
Dry Loaf Gravy Dry Loaf Gravy Loaf
Fancy Feast Royal Canin
Veterinary Diet
Diabetic Diabetic Morsels in Gravy Calorie Control Calorie Control Calorie Control Morsels in Gravy Satiety Support Calorie Control CC High Fiber
Dry Gravy Dry Loaf Gravy Dry Loaf
Natura
EVO
95% Venison
Loaf
Wellness
Complete Health
Chicken Formula
Loaf
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Appendix
