Journal of Nutrition LabDiet, Your World of Nutritional Answers

Home Help [Feedback] [For Subscribers] [Archive] [Search] [Contents]
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Villaverde, C.
Right arrow Articles by Fascetti, A. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Villaverde, C.
Right arrow Articles by Fascetti, A. J.
© 2008 American Society for Nutrition J. Nutr. 138:856-860, May 2008

Nutrient Physiology, Metabolism, and Nutrient-Nutrient Interactions

Energy Restriction Results in a Mass-Adjusted Decrease in Energy Expenditure in Cats That Is Maintained after Weight Regain1,2

Cecilia Villaverde, Jon J. Ramsey, Alice S. Green, Danny K. Asami, Seung Yoo and Andrea J. Fascetti*

Department of Molecular Biosciences, School of Veterinary Medicine, University of California, Davis, CA 95616-8741

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


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Dietary energy restriction (ER) is used to treat obesity in cats but it is often unsuccessful. The purpose of this study was to determine whether ER results in a sustained decrease in mass-adjusted energy expenditure (EE) that may oppose weight loss and promote weight regain. EE and body composition were measured in 10 adult neutered cats at 3 time points: baseline (obese cats), during weight loss (40% ER), and following weight regain. The cats started with a body weight (BW) of 6.1 ± 0.30 kg, body condition score (BCS) of 7.6 ± 0.14 (on a 9-point scale), and fat body mass (FM) of 38 ± 1.0% of BW. After weight loss, BW was 5.0 ± 0.19 kg, BCS was 5.5 ± 0.07 kg, and FM was 31 ± 1.6% (P < 0.01). After weight regain, BW was 6.2 ± 0.30 kg, BCS was 7.7 ± 0.16, and FM was 42 ± 1.8% (P < 0.01). Total EE decreased from 1258 ± 33.7 kJ/d to 1025 ± 39.6 kJ/d during weight loss (P < 0.001). After weight regain, EE was still lower than baseline (1103 ± 41.5 kJ/d, P < 0.001). Energy intake (EI) at baseline (1337 ± 50.6 kJ/d) was higher than EI after weight loss and regain (1217 ± 61.2 kJ/d), resulting in no differences in energy balance (78 ± 30.4 and 104 ± 35.4 kJ/d, respectively, P = 0.581). These results support the hypothesis that ER results in a mass-adjusted decrease in EE in cats that is maintained after weight regain.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
Obesity, resulting from an imbalance between energy expenditure (EE)3 and energy intake (EI), is believed to be the most common nutritional problem of cats in Western countries (1). The prevalence of overweight and obese cats in the United States has been estimated to be between 25 (2) and 35% (3). Spaying and neutering is strongly associated with obesity (2–5) and increased efforts toward sterilization may have the unintended effect of contributing to its development. Obesity has also been linked to a high incidence of health problems in cats, such as diabetes mellitus; dermatologic, orthopedic, and oral diseases; hepatic lipidosis; urinary tract infections; and an increased anesthetic risk (1,3,6). For these reasons, treatment of obesity is of great importance in veterinary medicine. The primary treatment for obesity is energy restriction (ER) sufficient to cause a negative energy balance and promote weight loss. However, ER in the clinical setting is often unsuccessful. Even when successful, many cats eventually regain the lost weight. Subsequent weight gain may be due to a lack of owner compliance. However, there is evidence in other species such as humans, rodents, monkeys, and dogs that ER may result in a decrease in EE higher than expected by the decreased body mass (7–10). This decreased EE can oppose further weight loss and may promote weight regain once ER is stopped. The objective of this study was to assess the effect of ER and subsequent weight regain on total EE in adult gonadectomized cats.


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Cats and diet. Ten adult (median age 2.0 y, range 1.9 to 2.2 y at the beginning of the experiment), specific pathogen free, domestic short-hair cats owned by the University of California were used in this study. Four cats were castrated males and 6 were spayed females. A 9-point body condition score (BCS) system was used (11), where a score of 5 was considered ideal, a score >5 and ≤7 was considered overweight, and a score >7 was considered obese. Cats with a BCS of at least 6.5 were included in the experiment. The cats were individually housed in a light (14-h-light/10-h-dark cycle) and temperature (18–24°C) controlled facility at the University of California, Davis, in an enriched environment (perches, rotating toys, and scratching poles) and were brushed and socialized twice a day. Fresh water was available at all times. This study was approved by the Animal Care and Use Committee at the University of California, Davis and by the WALTHAM Ethics Committee.

Throughout the study, all cats were fed the same batch of a commercial, nutritionally complete and balanced extruded dry-type diet (Adult Fit 32, Royal Canin USA).4 The diet contained 320 g/kg crude protein, 150 g/kg crude fat, 74 g/kg crude fiber, and 90 g/kg of water. The manufacturer calculated metabolizable energy (ME) content of the diet was determined using the proximate analysis and provided 16.7, 37.6, and 16.7 kJ/g from protein, fat, and carbohydrate, respectively. The calculated ME of the diet was 15.9 kJ/g and this value was used for EI calculations. This diet provided 35% of the energy from protein, 36% from fat, and 29% from carbohydrates. This diet was formulated to meet the nutritional recommendations established by the Association of American Feed Control Officials (12) cat food nutrient profiles for maintenance.

    Study design. The experiment was divided into 3 phases (Fig. 1). In the first phase [obese (O)], all the cats consumed the diet ad libitum for 3 mo, at which time their body weights (BW) and food intakes were stable. During the 2nd phase [active weight loss (WL)], the cats were fed ~60% of their previously measured EI to achieve weight loss until they reached a BCS of 5.5. This phase's measurements were made during active weight loss (the cats were not stabilized at their reduced BW). In the 3rd phase [weight regain (WR)], the cats consumed the diet ad libitum, allowing them to gain weight. This phase ended when each of the cats had reached a stable BW and stable food intake for a minimum of 3 wk. Food intake was determined daily by weighing the food bowls prior to and after feeding. EI was determined by multiplying the food intake by the energy density of the diet. Because the energy density was estimated from the chemical analysis of the food (and not measured), EI is an estimation. EI was compared with calculated maintenance energy requirements (MER) by using the following equations obtained from the 2006 edition of the Nutrient Requirements of Cats by the NRC: MER (kJ) = 418 x BW (kg)0.67 for lean cats and MER (kJ) = 543 x BW (kg)0.4 for obese cats (13). Body weight was measured weekly. The same investigator (A.J.F.) assessed body condition once per month during the study. At the end of each phase, daily EE and body composition were determined and a 24-h urine collection completed.


Figure 1
View larger version (7K):
[in this window]
[in a new window]

  		FIGURE 1  BW evolution of 1 experimental cat during O, WL, and WR phases of the study.

 
    Indirect calorimetry. Total daily EE measurements were conducted by whole-body indirect respiration calorimetry at the conclusion of each phase. The calorimetry chamber measured 0.60 x 0.60 x 0.76 m with a Plexiglas window in front. All cats were introduced to the chamber at least 1 mo prior to the measurements for at least 3 consecutive days to acclimate them to the environment. We observed behavior and recorded food intake during this period. The chamber was maintained at room temperature (23°C) by fans blowing over condenser coils circulating chilled water. Calorimetry measurements began at 0800 and concluded at 2000. Total daily EE was measured at least twice for each cat to ensure repeatability and the cats were under supervision for the entire measurement period. Food and water were available at all times. We completed several 24-h test runs to verify that EE did not differ between daytime and nighttime in cats. Therefore, data obtained by 12-h runs were extrapolated to 24 h.

An open-circuit, flow-through design was used for the calorimetry chamber. Room air was drawn through the chamber at 6 L/min and we controlled and measured flow rate with a mass flow controller (Flowkit 100, Sable Systems). Samples of room and chamber air were dried by a Peltier condenser (PC-4, Sable Systems). Pressure was equalized on calibration and sample channels using independent pressure gauges. Oxygen content was measured by a paramagnetic analyzer (Rosemount Analytical) and CO2 content was measured by an infrared analyzer (AEI Technologies). We checked the calorimeter calibration weekly using an ethyl alcohol recovery. Sample gas, reference gas (1.90% CO2), and room air were continually cycled through the analyzers using a multiposition microelectric valve actuator (Vici Valco Instruments) controlled by data acquisition software (LabVIEW, National Instruments). Data from the mass flow meter and gas analyzers were collected using a data acquisition system (National Instruments) with a PC using LabVIEW software (National Instruments). We calculated EE using the Weir equation (14).

Formula

The respiratory quotient (RQ) was calculated as the ratio of the volume of CO2 produced to the volume of O2 consumed. A food quotient (FQ) (15) of 0.84 was calculated from the proportions of protein, fat, and carbohydrates in the diet (on an energy basis).

    Urinary nitrogen. After the 12-h run, the cats spent 12 additional hours in the chamber to collect urine for a 24-h period. Sufficient hydrochloric acid (5N) was added to the samples to reach a final pH < 3. After measuring total urine volume, we took 2 50-mL subsamples and froze them at –20°C until analysis. Nitrogen concentration was measured by the Agriculture and Natural Resources Analytical Lab of the University of California, Davis, using the Total Kjeldahl Nitrogen method (16).

    Body composition. At the conclusion of the calorimetry run for each phase, fat body mass (FM) and lean body mass (LBM) of the cats was measured using an isotope dilution procedure as described by Backus et al. (17), with the following modifications: the dose (0.4 g/kg) of D2O (Cambridge Isotope Laboratories) was given subcutaneously instead of i.v. and the equilibration period was extended to 3 h. We withheld food for 24 h and water for 2 h before and during the period of isotopic equilibration. Blood (3 mL) was obtained from the jugular vein and collected in tubes with no additives (Vacutainer tubes; BD) and was kept at room temperature for 30 min before centrifugation (2817 x g; 10 min) to separate the serum, which was stored at –20°C until analysis.

    Statistical analysis. Data obtained for BW, BCS, body composition, EI, and EE followed a longitudinal design with 3 phases of measurement (O, WL, and WR) and was analyzed by a mixed models approach using the MIXED procedure of SAS (version 9.1) (18). The basic model included only time as a classification factor. To assess the effect of body mass on EE, BW and LBM were included in the model as covariates. We conducted post hoc tests on least square means using Tukey's multiple comparison adjustment for all analyses. The REG (regression) procedure was used to perform simple linear regression analysis. Differences were considered significant at P < 0.05. Unless otherwise indicated, data in the text are presented as means ± SEM.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
    BW and composition. BCS and percent FM were positively correlated (P < 0.001), with a correlation coefficient of 0.76 and a CV of 15.1%. The cats lost 17 ± 1.3% of their initial BW during ER, which lasted 19.8 ± 2.03 wk, ranging from 12 to 29 wk. The weekly weight loss rate was 0.96 ± 0.052% BW. Cats starting at a higher BW needed more time to achieve a BCS of 5.5 (P < 0.01; r = 0.80; CV = 19.4%). The cats lost 10% LBM and 30% FM during the weight-loss process. The percentage of LBM was higher in cats at the WL phase than in cats at the O phase due to the higher loss of FM relative to LBM (Table 1). The composition of the weight lost was 72 ± 5.6% FM and 28 ± 5.4% LBM.


View this table:
[in this window]
[in a new window]

  		TABLE 1 BW and body composition of cats prior to and following weight loss and after weight regain1

 
The cats regained weight in 14.1 ± 1.36 wk. The maximum rate of weight gain (5.4 ± 0.42%/wk) occurred immediately after starting ad libitum consumption (median time, 1 wk; range, 1–2 wk). The rate of weight gain was 1.51 ± 0.112% of BW/wk. After weight regain, the cats returned to their initial BW and BCS; however, the cats had 10.5% more FM and 6.5% less LBM at the completion of the WR phase than at baseline (O phase; P < 0.001).

    EI and EE. Approximately 60% of each cat's baseline EI was offered during the WL phase. The energy fed during WL was the equivalent to 67 ± 2.2% of the calculated MER for obese cats according to the NRC (13) and also equivalent to 61 ± 2.0% of the calculated MER for ideal BW (13).

When the cats consumed the diet ad libitum after WL, their EI increased rapidly (peaking at a median time of 1 wk; range, 1–4 wk), surpassing baseline levels (1770 ± 81.1 kJ/d; P < 0.001), but then slowly decreased until food intake stabilized, which was at the same time that BW stabilized. At that time, EI during WR was lower than EI at baseline (Table 2; O phase; P < 0.001).


View this table:
[in this window]
[in a new window]

  		TABLE 2 EI, EE, energy balance, and RQ of cats prior to and following weight loss and after weight regain1

 
Compared with baseline (O phase), EE decreased during the WL phase and EE remained low during the WR phase (P < 0.001). These results did not change when either BW (P < 0.05) or LBM (P < 0.01) were included in the statistical analysis. EE differed from EI during the O and WR phases (P < 0.05), where a slight positive energy balance was observed. Energy balance did not differ between the O and WR phases, because the lower EE in WR was accompanied by a lower EI. As expected, energy balance was negative during WL (Table 2).

The ratio of EE during the O phase to the EE during the WL phase correlated well with the number of weeks necessary for the cats to regain their initial BW during the WR phase (P < 0.05; r = 0.62; CV = 22.6%). The greater the decrease in EE during the WL phase compared with baseline, the faster the cats gained weight during the WR phase. The EI:EE ratio during the O phase was 1.06 ± 0.036 and did not differ from the WR phase. The ratio of EE:calculated MER for obese cats (13) was 1.13 ± 0.022 in the O phase but was lower in the WR phase (0.98 ± 0.023; P < 0.001).

The RQ did not differ between the 2 obese states (O and WR) and was similar to the FQ (Table 2). These values should be similar in cats that are either at or near energy balance. During the WL phase, the RQ was lower compared with the 2 obese states (O and WR; P < 0.05) and the FQ.


   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
This study assessed the effect of ER and subsequent free feeding on BW, body composition, and EE in gonadectomized, obese cats. Weight loss was achieved by restricting EI to 60% of measured EI determined at baseline (O phase). During the WL phase, the EI was also equivalent to 60% of the calculated MER for ideal BW using the equations in the NRC (13), assuming the BW at the end of the WL phase was ideal. The cats lost weight at a weekly rate of 1% of BW. The degree of ER and rate of weight loss was similar to previous studies that used different methods to calculate the amount of ER. In those studies, ER ranged between 60 (19,20) and 66% (21) of MER and the weight loss rates ranged between 0.8 (20) and 1.6% (19,21) BW/wk.

Initial body fat in the obese cats from our experiment (38% of BW) was in agreement with other studies: 36% of BW for Butterwick et al. (20) and 44% of BW for Nguyen et al. (21). The mean body fat content in our cats following WL was 31% of BW, which was slightly higher than the 28% of BW previously reported (20,21). These differences could be partially related to the different methodologies used to measure body fat (9). The percentage of body fat in normal weight cats reported in 2 previous studies was 15–20% of BW (22) and 24% of BW (23). Most of the cats at the end of the WL phase in our study had a body fat content higher than those values. This finding could be explained by the fact that the endpoint for the WL phase of our study was a BCS of 5.5, which is slightly greater than the ideal BCS (5).

The degree of ER and the protein intake, among other factors, are thought to affect the composition of weight loss in humans (24). The composition of weight loss in our study differs from the Butterwick (20) study (90.5% FM and 8.2% LBM) and may be due to the lower protein content in our diet (35 vs. 39% on an ME basis). Our diet still provided the necessary nutrient amounts to the cats on a metabolic BW basis when restricted by 40% compared with the minimum requirements established by the NRC (13), but more protein may have promoted better preservation of muscle mass. True nutrient requirements during weight loss in cats are unknown, so it is possible that the diet may have been marginal during this phase, because it was not formulated specifically for weight loss. However, no obvious nutritional deficiencies were observed. The composition of weight loss in this study was comparable to that found by Nguyen et al. (21) (24% LBM and 76% FM) despite the higher protein content (47–53% ME) of their diet. The greater rate of weight loss in that study may have promoted the loss of LBM, as demonstrated in other species (10,25).

To our knowledge, there are no published studies in cats assessing the effect of weight regain on body composition. The cats in this study returned to their initial BW and BCS after consuming the diet ad libitum. However, body fat content of cats at the end of the WR phase was higher than during the O phase. Dulloo et al. (26) found similar results in nonobese humans subject to starvation. Because it took longer to deposit LBM than FM, the authors hypothesized that compensatory hyperphagia did not stop until LBM reached original levels. Similarly, LBM did not differ between O and WR phases. However, not all studies support this hypothesis (27) and studies in rodents have shown conflicting results (28–30).

The RQ during the O and WR phases did not differ and was similar to the FQ predicted from the diet composition. This finding confirms that the cats during both obese phases (O and WR) were near energy balance. As expected, the RQ during active WL decreased, reflecting increased fat oxidation from body reserves. The results for energy balance support this explanation, being slightly positive during the O and WR phases, despite a stable BW, and negative during WL. This is likely due to the fact that EI is a calculated, not measured value and that the ME content of the diet may have been slightly overestimated. Also, small differences in food intake and cat activity in the chamber could explain a slightly positive energy balance.

ER resulted in decreased mass-adjusted EE in obese cats. There is evidence in humans (31–33), monkeys (9,34), and rodents (8,35–37) that ER results in decreased EE after accounting for differences in BW and LBM. However, other studies have reported no decrease in mass-adjusted EE with ER (21,38–40). One possible reason for this discrepancy is the different statistical methods used to adjust EE for body mass. Some studies use ratios to adjust for body size, but this approach has been questioned, and regression-based approaches (such as ANCOVA) were recommended for adjusting EE data (41). In support of this conclusion, Arch et al. (42) reviewed the interpretation of indirect respiratory calorimetry measurements in small animals and concluded that LBM should be included when using ANCOVA to analyze EE data. Blanc et al. (9) analyzed data from previous studies in humans, monkeys, and rats using ANCOVA and concluded that ER does result in decreased mass-adjusted EE, similar to our study. Ramsey and Hagopian (43) reviewed the possible mechanisms by which individuals reduce EE when subjected to ER. A passive effect of loss of body mass is implicated, but active metabolic adaptations such as reduced mitochondrial proton leak, changes in ATPase activity, and changes in activity of oxidative pathways have been proposed to occur with sustained ER.

EE and EI during the WR phase was lower than baseline (O phase); however, BW was the same, suggesting an increased efficiency of energy utilization during the WR phase. Cats had a lower LBM during WR compared with baseline, but EE was still lower when LBM was included in the statistical model. This finding suggests that cats that have lost weight have a lower energy requirement than obese cats that have never lost weight. Similar results have been found in dogs (10) and nonobese mice (44) after ER and subsequent weight regain, and in humans, following weight loss due to strenuous exercise and subsequent weight regain (45).

Exercise has been shown to help overcome the EE decrease during ER in humans (46,47). However, the effect of physical activity on EE in cats has not been studied. The cats in this study were groomed/brushed and socialized twice daily. They also had toys, but there was no standardized exercise regime. It is not known if increased physical activity can oppose the decrease in EE that occurs during ER and after weight regain in cats.

In summary, ER results in a mass-adjusted decrease in EE, which is maintained after the cats have regained the lost weight. The lower energy requirement of obese cats in the WL and WR phases has important clinical implications. Commercial weight loss diets contain higher amounts of protein, vitamins, and minerals to compensate for the reduction in EI that occurs during weight loss. Many maintenance diets are formulated to meet nutrient needs in the context of supplying energy requirements. Therefore, it is important to understand that following weight loss, energy needs are likely to be lower compared with predicted or calculated values to avoid situations where deficiencies could potentially occur. Furthermore, owners frequently become impatient considering the time it can often take for their cat to lose weight. Understanding that a metabolic adaptation to ER is contributing to the delay can help with owner compliance and perseverance during the process. Perhaps most importantly, these results underscore the importance of obesity prevention, because weight loss can be very challenging in cats.


   ACKNOWLEDGMENTS
 
The authors thank Debbie Bee for taking care of the cats, Dr. Zengshou Yu for technical assistance, Dr. Denise Elliot from Royal Canin USA, Inc. for donating the experimental diet, and Dr. Edgar G. Manzanilla for his assistance with statistics.


   FOOTNOTES
 
1 Supported by the WALTHAM Centre for Pet Nutrition, Leicestershire, UK. C.V. is supported by Fundacio la Caixa and A.S.G. is supported by a National Science Foundation Graduate Fellowship. Back

2 Author disclosures: C. Villaverde, J. J, Ramsey, A. S. Green, D. K. Asami, and S. Yoo, no conflicts of interest; A. J. Fascetti receives research funding from the WALTHAM Centre not related to this study. The School of Veterinary Medicine at the University of California, Davis, receives unrestricted support from WALTHAM for the WALTHAM UCVMC SD Clinical Nutrition Program, but those funds did not contribute to the current research. Back

3 Abbreviations used: BCS, body condition score; BW, body weight; EE, energy expenditure; EI, energy intake; ER, energy restriction; FM, fat body mass; FQ, food quotient; LBM, lean body mass; ME, metabolizable energy MER, maintenance energy requirement; O, obese phase; RQ, respiratory quotient; WL, weight loss phase; WR, weight regain phase. Back

4 Manufactured by Royal Canin USA. The ingredient composition was as follows: Chicken meal, brown rice, corn, corn gluten meal, chicken, chicken fat (naturally preserved with mixed tocopherols, rosemary extract, and citric acid), pea fiber, natural chicken flavor, beet pulp, dried brewers yeast, rice hulls, dried egg powder, salmon oil, salt, calcium sulfate, soya oil, potassium chloride, DL-methionine, choline chloride, brewers yeast extract, L-lysine, sodium tripolyphosphate, taurine, vitamins (dl-alpha-tocopherol, L-ascorbyl-2-polyphosphate, niacin, biotin, riboflavin, d-calcium pantothenate, pyridoxine hydrochlorate, thiamine mononitrate, vitamin B-12 supplement, vitamin A acetate, cholecalciferol supplement, folic acid), trace minerals (zinc proteinate, zinc oxide, ferrous sulfate, copper proteinate, copper sulfate, manganese proteinate, manganous oxide, sodium selenite, calcium iodate), and marigold extract. Back

Manuscript received 27 November 2007. Initial review completed 30 December 2007. Revision accepted 7 February 2008.


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

1. Hand MS, Thatcher CD, Remillard RL, Roudebush P. Small animal clinical nutrition. 4th ed. Topeka (KS): Mark Morris Institute; 2000.

2. Scarlett JM, Donoghue S, Saidla J, Wills J. Overweight cats: prevalence and risk factors. Int J Obes Relat Metab Disord. 1994;18 Suppl 1:S22–8.

3. Lund EM, Armstrong J, Kirk CA, Klausner JS. Prevalence and risk factors for obesity in adult cats from private US veterinary practices. Int J Appl Res Vet Med. 2005;3:88–96.

4. Kanchuk ML, Backus RC, Calvert CC, Morris JG, Rogers QR. Weight gain in gonadectomized normal and lipoprotein lipase-deficient male domestic cats results from increased food intake and not decreased energy expenditure. J Nutr. 2003;133:1866–74.[Abstract/Free Full Text]

5. Backus RC, Cave NJ, Keisler DH. Gonadectomy and high dietary fat but not high dietary carbohydrate induce gains in body weight and fat of domestic cats. Br J Nutr. 2007;98:641–50.[Medline]

6. German AJ. The growing problem of obesity in dogs and cats. J Nutr. 2006;136:S1940–6.[Abstract/Free Full Text]

7. Dulloo AG, Jacquet J, Girardier L. Autoregulation of body composition during weight recovery in human: the Minnesota Experiment revisited. Int J Obes Relat Metab Disord. 1996;20:393–405.[Medline]

8. MacLean PS, Higgins JA, Johnson GC, Fleming-Elder BK, Donahoo WT, Melanson EL, Hill JO. Enhanced metabolic efficiency contributes to weight regain after weight loss in obesity-prone rats. Am J Physiol Regul Integr Comp Physiol. 2004;287:R1306–15.[Abstract/Free Full Text]

9. Blanc S, Schoeller D, Kemnitz J, Weindruch R, Colman R, Newton W, Wink K, Baum S, Ramsey J. Energy expenditure of rhesus monkeys subjected to 11 years of dietary restriction. J Clin Endocrinol Metab. 2003;88:16–23.[Abstract/Free Full Text]

10. Laflamme D, Kuhlman G. The effect of weight loss regimen on subsequent weight maintenance in dogs. Nutr Res. 1995;15:1019–28.

11. Laflamme D. Development and validation of a body condition score system for cats: a clinical tool. Feline Pract. 1997;25:13–8.

12. AAFCO. Official publication. Oxford (IN): Association of American Feed Control Office; 2007.

13. National Research Council. Nutrient requirements of dogs and cats. Washington, DC: National Academies Press; 2006.

14. Weir JBD. New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol (Lond). 1949;109:1–9.[Free Full Text]

15. Westerterp KR. Food quotient, respiratory quotient, and energy balance. Am J Clin Nutr. 1993;57:S759–64.

16. Bremner JM, Mulvaney CS. Nitrogen-total. In: Page AL, editor. Methods of soil analysis. Part 2. Chemical and microbiological properties. 2nd ed. Madison (WI): American Society of Agronomy; 1983. p. 595–624.

17. Backus RC, Havel PJ, Gingerich RL, Rogers QR. Relationship between serum leptin immunoreactivity and body fat mass as estimated by use of a novel gas-phase Fourier transform infrared spectroscopy deuterium dilution method in cats. Am J Vet Res. 2000;61:796–801.[Medline]

18. SAS Institute. SAS. 9.1 ed. Cary (NC): SAS Institute; 2002.

19. Center SA, Harte J, Watrous D, Reynolds A, Watson TD, Markwell PJ, Millington DS, Wood PA, Yeager AE, et al. The clinical and metabolic effects of rapid weight loss in obese pet cats and the influence of supplemental oral L-carnitine. J Vet Intern Med. 2000;14:598–608.[Medline]

20. Butterwick RF, Markwell PJ. Changes in the body composition of cats during weight reduction by controlled dietary energy restriction. Vet Rec. 1996;138:354–7.[Abstract/Free Full Text]

21. Nguyen P, Dumon H, Martin L, Siliart B, Ferrier L, Humbert B, Diez M, Breul S, Biourge V. Weight loss does not influence energy expenditure or leucine metabolism in obese cats. J Nutr. 2002;132:S1649–51.[Abstract/Free Full Text]

22. Stanton CA, Hamar DW, Johnson DE, Fettman MJ. Bioelectrical impedance and zoometry for body-composition analysis in domestic cats. Am J Vet Res. 1992;53:251–7.[Medline]

23. Lauten SD, Cox NR, Baker GH, Painter DJ, Morrison NE, Baker HJ. Body composition of growing and adult cats as measured by use of dual energy X-ray absorptiometry. Comp Med. 2000;50:175–83.[Medline]

24. Prentice AM, Goldberg GR, Jebb SA, Black AE, Murgatroyd PR. Physiological responses to slimming. Proc Nutr Soc. 1991;50:441–58.[Medline]

25. Pasanisi F, Contaldo F, de Simone G, Mancini M. Benefits of sustained moderate weight loss in obesity. Nutr Metab Cardiovasc Dis. 2001;11:401–6.[Medline]

26. Dulloo AG, Jacquet J, Girardier L. Poststarvation hyperphagia and body fat overshooting in humans: a role for feedback signals from lean and fat tissues. Am J Clin Nutr. 1997;65:717–23.[Abstract/Free Full Text]

27. Graci S, Izzo G, Savino S, Cattani L, Lezzi G, Berselli ME, Balzola F, Liuzzi A, Petroni ML. Weight cycling and cardiovascular risk factors in obesity. Int J Obes Relat Metab Disord. 2004;28:65–71.[Medline]

28. Graham B, Chang S, Lin D, Yakubu F, Hill JO. Effect of weight cycling on susceptibility to dietary obesity. Am J Physiol. 1990;259:R1096–102.[Medline]

29. Stein LJ, Stellar E, West DB, Greenwood MR, Foster GD, Feurer I, Brown J, Mullen JL, Brownell KD. Early-onset repeated dieting reduces food intake and body weight but not adiposity in dietary-obese female rats. Physiol Behav. 1992;51:1–6.[Medline]

30. Simpson JA, Wainwright PE, Hoffman-Goetz L, Levesque S. Effects of different weight loss treatments on weight cycling and metabolic measures in male mice. Physiol Behav. 1994;56:197–201.[Medline]

31. Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med. 1995;332:621–8.[Abstract/Free Full Text]

32. Luke A, Schoeller DA. Basal metabolic rate, fat-free mass, and body cell mass during energy restriction. Metabolism. 1992;41:450–6.[Medline]

33. Heilbronn LK, de Jonge L, Frisard MI, DeLany JP, Larson-Meyer DE, Rood J, Nguyen T, Martin CK, Volaufova J, et al. Effect of 6-month calorie restriction on biomarkers of longevity, metabolic adaptation, and oxidative stress in overweight individuals: a randomized controlled trial. JAMA. 2006;295:1539–48.[Abstract/Free Full Text]

34. DeLany JP, Hansen BC, Bodkin NL, Hannah J, Bray GA. Long-term calorie restriction reduces energy expenditure in aging monkeys. J Gerontol A Biol Sci Med Sci. 1999;54:B5–11.[Abstract]

35. Dulloo AG, Girardier L. 24 hour energy expenditure several months after weight loss in the underfed rat: evidence for a chronic increase in whole-body metabolic efficiency. Int J Obes Relat Metab Disord. 1993;17:115–23.[Medline]

36. Gonzales-Pacheco DM, Buss WC, Koehler KM, Woodside WF, Alpert SS. Energy restriction reduces metabolic rate in adult male Fisher-344 rats. J Nutr. 1993;123:90–7.[Abstract/Free Full Text]

37. Santos-Pinto FN, Luz J, Griggio MA. Energy expenditure of rats subjected to long-term food restriction. Int J Food Sci Nutr. 2001;52:193–200.[Medline]

38. Ballor DL. Effect of dietary restriction and/or exercise on 23-h metabolic rate and body composition in female rats. J Appl Physiol. 1991;1991:801–6.

39. Keesey RE, Corbett SW. Adjustments in daily energy expenditure to caloric restriction and weight loss by adult obese and lean Zucker rats. Int J Obes. 1990;14:1079–84.[Medline]

40. McCarter RJ, Palmer J. Energy metabolism and aging: a lifelong study of Fischer 344 rats. Am J Physiol. 1992;263:E448–52.[Medline]

41. Allison DB, Gomez JE, Heshka S, Babbitt RL, Geliebter A, Kreibich K, Heymsfield SB. Decreased resting metabolic rate among persons with Down's Syndrome. Int J Obes Relat Metab Disord. 1995;19:858–61.[Medline]

42. Arch JR, Hislop D, Wang SJ, Speakman JR. Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int J Obes (Lond). 2006;30:1322–31.[Medline]

43. Ramsey JJ, Hagopian K. Energy expenditure and restriction of energy intake: could energy restriction alter energy expenditure in companion animals? J Nutr. 2006;136:S1958–66.[Abstract/Free Full Text]

44. Mahoney LB, Denny CA, Seyfried TN. Caloric restriction in C57BL/6J mice mimics therapeutic fasting in humans. Lipids Health Dis. 2006;5:13.[Medline]

45. Major GC, Doucet E, Trayhurn P, Astrup A, Tremblay A. Clinical significance of adaptive thermogenesis. Int J Obes (Lond). 2007;31:204–12.[Medline]

46. Jakicic JM, Marcus BH, Gallagher KI, Napolitano M, Lang W. Effect of exercise duration and intensity on weight loss in overweight, sedentary women: a randomized trial. JAMA. 2003;290:1323–30.[Abstract/Free Full Text]

47. Tate DF, Jeffery RW, Sherwood NE, Wing RR. Long-term weight losses associated with prescription of higher physical activity goals. Are higher levels of physical activity protective against weight regain? Am J Clin Nutr. 2007;85:954–9.[Abstract/Free Full Text]




This article has been cited by other articles:


Home page
 J. Nutr.Home page
R. S. Vasconcellos, N. C. Borges, K. N. V. Goncalves, J. C. Canola, F. J. A. de Paula, E. B. Malheiros, M. A. Brunetto, and A. C. Carciofi
Protein Intake during Weight Loss Influences the Energy Required for Weight Loss and Maintenance in Cats
J. Nutr., May 1, 2009; 139(5): 855 - 860.
[Abstract] [Full Text] [PDF]

Home page
 J. Nutr.Home page
A. S. Green, J. J. Ramsey, C. Villaverde, D. K. Asami, A. Wei, and A. J. Fascetti
Cats Are Able to Adapt Protein Oxidation to Protein Intake Provided Their Requirement for Dietary Protein Is Met
J. Nutr., June 1, 2008; 138(6): 1053 - 1060.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Villaverde, C.
Right arrow Articles by Fascetti, A. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Villaverde, C.
Right arrow Articles by Fascetti, A. J.

Home Help [Feedback] [For Subscribers] [Archive] [Search] [Contents]
Copyright © 2008 by American Society for Nutrition