HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Doucet, E. Articles by Joanisse, D. R Search for Related Content PubMed PubMed Citation Articles by Doucet, E. Articles by Joanisse, D. R Agricola Articles by Doucet, E. Articles by Joanisse, D. R

Skeletal muscle enzymes as predictors of 24-h energy metabolism in reduced-obese persons^1,2,3,4

¹ From the School of Human Kinetics, University of Ottawa (ED); the Division of Kinesiology, Laval University, Québec (AT, J-AS, and DRJ); and the Laval Hospital Research Centre, Québec (DRJ).

² J-AS is deceased.

³ Supported by Servier Canada.

⁴ Address reprint requests to E Doucet, School of Human Kinetics, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5. E-mail: edoucet{at}uottawa.ca.

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Background: Little is known about the effects of weight loss on the relation between skeletal muscle enzymes and energy metabolism.

Objective: This study was performed retrospectively to investigate the relation between skeletal muscle enzymes and 24-h energy metabolism in obese persons before and after weight loss.

Design: Ten women and 9 men [with body mass indexes (in kg/m²) > 30] underwent a 15-wk weight-loss program (-700 kcal/d). Body weight and composition, 24-h energy metabolism (whole-body indirect calorimetry), and maximal activities of phosphofructokinase (EC 2.7.1.11), creatine kinase (CK; EC 2.7.3.2), citrate synthase (CS; EC 4.1.3.7), 3-hydroxyacyl-CoA dehydrogenase (HADH; EC 1.1.1.35), and cytochrome-c oxidase (COX; EC 1.9.3.1) were determined from biopsy samples of the vastus lateralis taken before and after weight loss.

Results: Before weight loss, fat-free mass (FFM) was the only predictor of 24-h energy expenditure (R² = 0.70, P < 0.001), whereas the cumulative variance in sleeping metabolic rate explained by FFM and fat mass (FM) was 83% (P < 0.001). After weight loss, CS (r = 0.45, P = 0.05) and COX (r = 0.65, P < 0.01) were significantly associated with 24-h energy expenditure, whereas CK (r = 0.53, P < 0.05), CS (r = 0.45, P < 0.05), COX (r = 0.64, P < 0.01), and HADH (r = 0.45, P = 0.05) were all significant correlates of sleeping metabolic rate. After weight loss, FFM, FM, and COX explained 84% (P < 0.01) of the variance in 24-h energy expenditure, whereas FFM, FM, and CK all contributed to the cumulative variance in sleeping metabolic rate explained by this model (R² = 0.82, P < 0.05).

Conclusion: Maximal activities of key skeletal muscle enzymes contribute to the variability in 24-h energy metabolism in reduced-obese persons.

Key Words: Obesity • weight loss • energy expenditure • skeletal muscle enzymes

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
The fact that energy expenditure (EE) is related to body weight and even more closely to fat-free mass (FFM) is well recognized (1). Evidence also supports the independent contribution of fat mass (FM) to the variance in EE (2, 3). In this sense, it is not surprising that changes in body weight and composition induce proportional changes in EE (3). Despite this, it is now becoming apparent that factors other than body composition per se can influence the changes in EE that occur in response to weight loss. In fact, it has been reported that the variations in EE that occur in response to body weight loss are greater than what would be expected from the corresponding changes in body weight and composition (4, 5) and that formerly obese subjects typically have lower EEs than do never-obese control subjects (6, 7). Factors such as changes in leptin (8), thyroid hormones (9), catecholamine excretion (9), sympathetic nervous system activity (10), and even organochlorine compounds (11) may all contribute to the variability in the changes in EE that occur in response to fluctuations in body weight.

Skeletal muscle is important in the regulation of EE (12) and constitutes an important site for the utilization of both carbohydrates and lipids (13). Because the synthesis and resynthesis of ATP within skeletal muscle is the result of 5 energy-generating pathways, ie, glycolysis, ß-oxidation, the citric acid cycle, the respiration chain, and high-energy phosphate metabolism, and because there are rate-limiting enzymes in each of these pathways, it could be speculated that these enzymes influence EE. Along these lines, it has been shown that the maximal activities of hydroxyacyl-CoA dehydrogenase (HADH; EC 1.1.1.35) and phosphofructokinase (PFK; EC 2.7.1.11) in skeletal muscle contribute independently to the variability in 24-h EE and fat oxidation in weight-stable humans (14).

Another interesting issue pertains to the effects of body weight loss on these key enzymes. Whereas some investigators have reported that weight loss does not significantly decrease skeletal muscle enzyme activity (15, 16), others have shown otherwise (17, 18). As such, the effects of weight loss on the activity of key skeletal muscle enzymes remain to be clarified. Because of the considerable interindividual variability in the response of these enzymes to weight loss and because of their crucial role in the resynthesis of ATP, changes in the activities of key skeletal muscle enzymes brought about by weight loss may contribute to the variance in EE observed in reduced-obese persons. This also remains to be determined.

We thus hypothesized that interindividual differences in the decrease in key enzymes involved in EE might be partly responsible for the changes in energy metabolism that occur in response to weight loss. More precisely, the maximal activities of key skeletal muscle enzymes (determined from biopsies of the vastus lateralis) were correlated with variables of 24-h energy metabolism before and after weight loss and with the changes brought about by the intervention in obese men and women. A secondary objective of this study was to clarify the effects of body weight loss on changes in the activities of key skeletal muscle enzymes.

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Twenty-six subjects (14 men and 12 women) volunteered to participate in this whole-body calorimeter substudy. The subjects were recruited from a larger group of 46 subjects who underwent weight loss by drug therapy (60 mg fenfluramine/d) or placebo treatment coupled to nonmacronutrient-specific energy restriction (-700 kcal/d) for 15 wk, as previously described (8). Of the 26 subjects who accepted to participate in this substudy (9 from the placebo group and 17 from the fenfluramine group), 19 subjects (9 men and 10 women, 7 from the placebo group and 12 from the fenfluramine group) completed the weight-loss program, and their data are analyzed in the present article. The subjects gave their written consent to participate in this study, which received the approval of the Laval University Medical Ethics Committee.

After the suspension of fenfluramine and dexfenfluramine because of a potential association with disturbances in cardiac valvular function (19), all subjects (including those in the placebo group) underwent an echocardiogram. After this assessment, a detailed analysis of cardiac valvular function was performed by cardiologists, who detected no abnormalities in response to the use of fenfluramine under the conditions described in this study (20).

Anthropometric measurements
Body weight was measured on a standard beam scale, and body density was determined by hydrodensitometry (21). The closed-circuit helium dilution method was used to assess residual lung volume (22). The Siri formula (23) was used to estimate the percentage of body fat from body density, whereas FM and FFM were estimated from the derived percentage of body fat and total body weight.

Muscle biopsies
Muscle samples were obtained 3 wk before the start of the weight-loss intervention and 4–6 wk after the end of the energy restriction. Both pre- and post-weight-loss muscle samples were obtained in a state of weight stability. Subjects who were recruited to participate in this study had been weight stable (body weight variation < 2 kg) for 6 mo before being randomly assigned to a study group. As well, between 2 to 4 wk elapsed between the end of the intervention and the post-weight-loss measurements. Subjects were instructed to maintain weight stability during this period, and their mean body weight change was 0.8 ± 2.3 kg (from 92.0 ± 12.2 kg at the end of the intervention to 91.2 ± 12.3 kg at the time of measurement; NS). Biopsy samples were taken from the middle region of the vastus lateralis (15 cm above the patella) and 2 cm away from the fascia by the use of the percutaneous needle biopsy technique described by Evans et al (24) and regularly used in our laboratory (25). Muscle samples were divided into 2 parts: one was frozen in liquid nitrogen for subsequent determination of muscle enzyme activities and the other was trimmed, mounted, and frozen in isopentane, cooled on liquid nitrogen, and stored at -80 °C for histochemical analysis.

Activities of skeletal muscle enzymes
Muscle samples were kept at -80 °C until assayed for maximal enzyme activities. Small pieces of the muscle sample (10 mg) were homogenized in a glass-glass homogenizer with 39 volumes of ice-cold extracting medium (0.1 mol Na-K-phosphate/L, 2 mmol EDTA/L, pH 7.2), and maximal enzyme activities were measured as previously described (26). Key enzymes were chosen to represent every major energy-yielding pathway. PFK was chosen for glycolysis, citrate synthase (CS; EC 4.1.3.7) for the citric acid cycle, cytochrome-c oxidase (COX; EC 1.9.3.1) for the respiration chain, HADH for ß-oxidation, and creatine kinase (CK; EC 2.7.3.2) for high-energy phosphate metabolism. The ratio of PFK to CS (PFK:CS) was also used as an indicator of the glycolysis to aerobic oxidation capacity. Maximal enzyme activities are expressed as micromoles of substrate consumed per minute per gram of tissue (µmol • min^-1 • g^-1). The intraindividual reproducibility for these measurements was reported previously (27).

Twenty-four–hour whole-room indirect calorimetric measurements
Twenty-four–hour EE and sleeping metabolic rate (SMR) were measured by using a whole-body calorimeter. The testing protocol and the reproducibility of measurements in the respiratory chamber were previously reported (28). Subjects were fed a mixed diet (food quotient = 0.85) ad libitum during their stay in the calorimeter (29). SMR was calculated as the mean of 2 consecutive hours representing the lowest values of EE obtained during sleep and then extrapolated over 24 h. Because EE and substrate oxidation are influenced by the state of energy balance, and because a slightly greater positive energy balance was observed before weight loss, energy metabolism variables were adjusted for energy balance [energy intake (kcal) - energy expenditure], and regression analyses were performed on residual scores.

Statistical analysis
JMP software (version 3.1.6.2; SAS Institute Inc, Cary, NC) was used for all analyses. Two-way analysis of variance [considering treatment (placebo or fenfluramine) and sex (male or female) as the between-subject factors] for repeated measures (considering time as the within-subject factor) was performed for all dependent variables. No significant effects of treatment (drug compared with placebo) and no interactions between sex and treatment, time and treatment, or sex and treatment and time were observed for any of the variables reported here. Partial correlation analyses (adjusted for sex, FM, and FFM) were performed between maximal activities of skeletal enzymes and 24-h energy metabolism variables (adjusted for energy balance) before and after body weight loss and for the changes in these variables (after weight loss - before weight loss). Stepwise multiple regression analyses were then performed to identify predictors of 24-h energy metabolism before and after weight loss and for the changes in these variables (after weight loss - before weight loss). Variables entered in these models included maximal activities of PFK, CK, CS, HADH, and COX; PFK:CS; sex; and body composition (FM and FFM). Probability to enter the models was set at P 0.05. Data are expressed as means ± SDs, and effects were considered significant at P 0.05.

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
The characteristics of the subjects before and after the weight-loss program are presented in Table 1. A significant effect of time was observed for body weight (-9%; P < 0.001), FM (-19.4%; P < 0.001), and body mass index. Although FFM was slightly reduced in response to this program, this difference was not significant. The men and women did not differ significantly in age (44.1 ± 2.0 compared with 39.8 ± 1.9 y, respectively; P = 0.14).

Table 2

Table 3

Table 4

Tables 5–7

View this table: [in this window] [in a new window]   TABLE 7 . Stepwise multiple regression analysis for predictors of change () in 24-h energy metabolism before body weight loss1

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 
The main finding of the present study was that maximal activities of key skeletal muscle enzymes become independent predictors of 24-h energy metabolism after body weight loss. In addition, the present results support previous reports that an 10% weight loss is not sufficient to significantly alter the oxidative potential of skeletal muscle.

It was intriguing to observe that the relation between EE and enzymatic activity emerged only after body weight loss because Zurlo et al (14) showed previously that 24-h energy metabolism was independently associated with some key enzymes in a cross-sectional study of 14 weight-stable men and women. In the present study, we observed no such associations before body weight loss. Although it is speculative, it is nonetheless possible that the increased gradient of substrate associated with obesity homogenizes the variance in the enzymatic profile, thus blurring such relations. In addition, even if no significant changes in the enzymatic profile had been observed after weight loss, some persons did indeed display a marked decrease in maximal activities, thus making the relation between EE and the enzymatic activity of skeletal muscle more apparent. Some results partly support this idea. It was shown that postobese women have lower maximal activities of key skeletal muscle enzymes than do normal-weight subjects (30) and that formerly obese subjects typically have lower resting energy expenditure values than do matched lean control subjects (6, 7).

It is obvious that we cannot conclude a causal relation from this design. Nonetheless, these results suggest that marked variations in the enzymatic profile of skeletal muscle can contribute to the variability in 24-h energy metabolism in reduced-obese men and women. It could be concluded that the reduction in EE associated with the reduction in body weight results in a decrease in key enzymatic activities. The decrease in skeletal muscle activity could in turn be interpreted as a result of the decrease in EE and not as a causative factor. It is clear that we cannot disregard this possibility, and that it might partially explain the associations between skeletal enzyme activity and 24-h energy metabolism during and after weight loss. Nonetheless, we tend to believe that other factors could affect enzymatic activities after weight loss. Recent results from our group have highlighted the possibility that the rise in plasma organochlorine concentration that results from weight loss is independently associated with changes in the enzymatic profile of skeletal muscle (31). This factor and others could thus contribute to a more pronounced decrease in the enzymatic activity of skeletal muscle in some persons that could in turn introduce large interindividual variability in energy metabolism in reduced-obese persons.

Contrasting results exist in terms of the effects of body weight loss on the maximal activity of key oxidative enzymes. Whereas some researchers have shown no changes in the activities of HADH and CS (15, 16), others have shown a significant decrease in COX and HADH in response to a weight-loss program (17, 18). These differences might be partly explained by the greater decrease in body weight (-15%) in the studies by Kelley et al (17) and Simoneau et al (18), and it might only be under such circumstances that changes in key enzyme activities occur in a greater proportion of subjects. In the present study, as in others in which a similar amount of body weight loss was observed (15, 16), no significant reduction in key enzyme activities was observed after weight loss, even if some trends were noted for most enzymes.

We were unable to show any consistent relations between the enzymatic profile of skeletal muscle and whole-body RQ (an indicator of substrate partitioning), either before or after body weight loss. Our results agree with those of Blaak et al (15), who reported no significant associations between changes in HADH and CS and changes in resting fat oxidation, even though they found evidence of a relation between variations in cystolic fatty acid binding protein and changes in resting fat oxidation during weight loss. In contrast, Zurlo et al (14) reported that HADH was negatively associated with 24-h RQ. One of the characteristics of the latter report was that lean, weight-stable humans were measured during energy balance. Because the obese subjects in the present study were measured while in positive energy balance, and because the RQ is responsive to this situation (32), it is possible that the association was blurred by this condition, even if a statistical correction was applied to take this factor into account. Another important aspect that must be discussed is that although whole-body RQ is not systematically different between lean and obese persons, leg RQ, as measured by arteriovenous differences in oxygen and carbon dioxide values, is considerably higher in obese persons and this difference persists even after body weight loss (17). These observations could complicate the comparison of the effects of skeletal muscle enzyme activity on substrate oxidation between lean and obese persons. In any event, the association between oxidative potential and whole-body fat oxidation, if any, will need to be investigated further.

Recent results have shown that skeletal muscle ultrastructure and metabolism can play a significant role in the fat deposition observed in response to prolonged positive energy balance. Persons with an increased proportion of type 1 fibers have a lesser FM gain at the end of 100 d of overfeeding, whereas persons with a high ratio of PFK to oxoglutarate dehydrogenase seem predisposed to greater fat deposition under such conditions (33). Although it remains to be determined whether this is also the case for body weight and fat regain after prolonged negative energy balance, these latter results suggest that the role of skeletal muscle in the regulation of energy balance is robust enough to potentiate or attenuate the effects of positive energy balance on body fat gain.

The role of physical activity as a possible therapeutic agent favoring weight maintenance after weight loss has received much attention (34). More specifically, persons who weekly expend large amounts of energy (2800 kcal/wk) through vigorous physical activity can remain weight stable after weight loss (35). Beyond the contribution of this amount of EE to the maintenance of energy balance in a reduced-obese state, it is also possible that part of the effects of vigorous exercise in the maintenance of weight stability are exerted through effects on the oxidative potential of skeletal muscle. Indeed, previous results showed that high-intensity intermittent training induces a greater weight loss than does a continuous aerobic-type exercise regimen, despite the lower energy cost of the higher-intensity exercise program (36). The authors of that study concluded that part of this effect may be attributed to the effects of this program on the oxidative potential. We can only give a partial answer to this question. We previously showed that EE is increased in reduced-obese men after an 18-wk exercise regimen (37). Moreover, by the end of the exercise follow-up in 6 of these men, the activities of HADH, CS, and COX had increased by 14% (P = 0.08), 56% (P < 0.05), and 37% (P < 0.01), respectively. Unfortunately, because too few subjects were sampled for both biopsies and calorimetric measurements at that time, we were unable to corroborate these observations with correlation analyses. Although it is clear that more studies will be needed to confirm this hypothesis, it is possible that physical activity favors weight maintenance through its probable effects on the oxidative potential of skeletal muscle in some persons.

In summary, the results of the present study suggest that changes in the activities of key skeletal muscle enzymes after weight loss may be sufficient to complicate the maintenance of energy balance in some reduced-obese persons. Future studies will be needed to investigate whether an altered skeletal muscle enzyme profile after weight loss predisposes to weight regain and whether the effects of a physical activity program favor body weight maintenance partially through effects on these enzymes.

	ACKNOWLEDGMENTS

 
AT and J-AS were involved in the study design, ED and DRJ carried out the data collection, ED and DRJ analyzed the data, and ED wrote the paper. None of the authors had any financial interests linked to this article.

	REFERENCES

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C. Determinants of 24-hour energy expenditure in man. Methods and results using a respiratory chamber. J Clin Invest 1986;78:1568–78.
2. Ferraro R, Ravussin E. Fat mass in predicting resting metabolic rate. Am J Clin Nutr 1992;56:460–1.[Medline]
3. Dionne I, Despres JP, Bouchard C, Tremblay A. Gender difference in the effect of body composition on energy metabolism. Int J Obes Relat Metab Disord 1999;23:312–9.[Medline]
4. 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]
5. Doucet E, St-Pierre S, Alméras N, Després J-P, Bouchard C, Tremblay A. Evidence for the existence of adaptive thermogenesis during weight loss. Br J Nutr 2001;85:715–23.[Medline]
6. Astrup A, Buemann B, Toubro S, Ranneries C, Raben A. Low resting metabolic rate in subjects predisposed to obesity: a role for thyroid status. Am J Clin Nutr 1996;63:879–83.[Abstract/Free Full Text]
7. Astrup A, Gotzsche PC, van de Werken K, et al. Meta-analysis of resting metabolic rate in formerly obese subjects. Am J Clin Nutr 1999;69:1117–22.[Abstract/Free Full Text]
8. Doucet E, St Pierre S, Alméras N, Mauriège P, Richard D, Tremblay A. Changes in energy expenditure and substrate oxidation resulting from weight loss in obese men and women: is there an important contribution of leptin? J Clin Endocrinol Metab 2000;85:1550–6.[Abstract/Free Full Text]
9. Rosenbaum M, Hirsch J, Murphy E, Leibel RL. Effects of changes in body weight on carbohydrate metabolism, catecholamine excretion, and thyroid function. Am J Clin Nutr 2000;71:1421–32.[Abstract/Free Full Text]
10. Aronne LJ, Mackintosh R, Rosenbaum M, Leibel RL, Hirsch J. Autonomic nervous system activity in weight gain and weight loss. Am J Physiol 1995;269:R222–5.
11. Pelletier C, Doucet E, Imbeault P, Tremblay A. Associations between weight loss-induced changes in plasma organochlorine concentrations, serum T(3) concentration, and resting metabolic rate. Toxicol Sci 2002;67:46–51.[Abstract/Free Full Text]
12. Zurlo F, Larson K, Bogardus C, Ravussin E. Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 1990;86:1423–7.
13. Kelley DE, Reilly JP, Veneman T, Mandarino LJ. Effects of insulin on skeletal muscle glucose storage, oxidation, and glycolysis in humans. Am J Physiol 1990;258:E923–9.
14. Zurlo F, Nemeth PM, Choksi RM, Sesodia S, Ravussin E. Whole-body energy metabolism and skeletal muscle biochemical characteristics. Metabolism 1994;43:481–6.[Medline]
15. Blaak EE, Glatz JF, Saris WH. Increase in skeletal muscle fatty acid binding protein (FABPC) content is directly related to weight loss and to changes in fat oxidation following a very low calorie diet. Diabetologia 2001;44:2013–7.[Medline]
16. Kempen KP, Saris WH, Kuipers H, Glatz JF, Van Der Vusse GJ. Skeletal muscle metabolic characteristics before and after energy restriction in human obesity: fibre type, enzymatic beta-oxidative capacity and fatty acid-binding protein content. Eur J Clin Invest 1998;28:1030–7.[Medline]
17. Kelley DE, Goodpaster B, Wing RR, Simoneau JA. Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 1999;277:E1130–41.
18. Simoneau JA, Veerkamp JH, Turcotte LP, Kelley DE. Markers of capacity to utilize fatty acids in human skeletal muscle: relation to insulin resistance and obesity and effects of weight loss. FASEB J 1999;13:2051–60.[Abstract/Free Full Text]
19. Weissman NJ, Tighe JFJ, Gottdiener JS, Gwynne JT. An assessment of heart-valve abnormalities in obese patients taking dexfenfluramine, sustained-release dexfenfluramine, or placebo. Sustained-Release Dexfenfluramine Study Group. N Engl J Med 1998;10:725–32.
20. Prud’homme D, Langlais M, Samson MP, et al. Lack of major cardiac valvular abnormalities in asymptomatic obese men and women following a 3-month fenfluramine or dexfenfluramine treatment. Int J Obes Relat Metab Disord 1999;23:S175 (abstr).
21. Behnke AR, Wilmore JH. Evaluation and regulation of body build and composition. Englewood Cliffs, NJ: Prentice-Hall, 1974:20–37.
22. Meneely EA, Kaltreider NL. Volume of the lung determined by helium dilution. J Clin Invest 1949;28:129–39.
23. Siri WE. The gross composition of the body. Adv Biol Med Physiol 1956;4:239–80.
24. Evans WJ, Phinney SD, Young VR. Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc 1982;14:101–2.[Medline]
25. Simoneau JA, Bouchard C. Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 1989;257:E567–72.
26. Simoneau JA, Lortie G, Boulay MR, Thibault MC, Bouchard C. Repeatability of fibre type and enzyme activity measurements in human skeletal muscle. Clin Physiol 1986;6:347–56.[Medline]
27. Gauthier JM, Theriault R, Theriault G, Gelinas Y, Simoneau JA. Electrical stimulation-induced changes in skeletal muscle enzymes of men and women. Med Sci Sports Exerc 1992;24:1252–6.[Medline]
28. White MD, Bouchard G, Buemann B, et al. Reproducibility of 24-h energy expenditure and macronutrient oxidation rates in an indirect calorimeter. J Appl Physiol 1996;80:133–9.[Abstract/Free Full Text]
29. Doucet E, St-Pierre S, Alméras N, Tremblay A. Relation between appetite ratings before and after a standard meal and estimates of daily energy intake in obese and reduced obese individuals. Appetite 2003;40:137–43.[Medline]
30. Raben A, Mygind E, Astrup A. Lower activity of oxidative key enzymes and smaller fiber areas in skeletal muscle of postobese women. Am J Physiol 1998;275:E487–94.
31. Imbeault P, Tremblay A, Simoneau JA, Joanisse DR. Weight loss-induced rise in plasma pollutant is associated with reduced skeletal muscle oxidative capacity. Am J Physiol 2002;282:E574–9.
32. Weyer C, Vozarova B, Ravussin E, Tataranni PA. Changes in energy metabolism in response to 48 h of overfeeding and fasting in Caucasians and Pima Indians. Int J Obes Relat Metab Disord 2001;25:593–600.[Medline]
33. Sun G, Ukkola O, Rankinen T, Joanisse DR, Bouchard C. Skeletal muscle characteristics predict body fat gain in response to overfeeding in never-obese young men. Metabolism 2002;51:451–6.[Medline]
34. Fogelholm M, Kukkonen-Harjula K. Does physical activity prevent weight gain—a systematic review. Obes Rev 2000;1:95–111.[Medline]
35. McGuire MT, Wing RR, Klem ML, Seagle HM, Hill JO. Long-term maintenance of weight loss: do people who lose weight through various weight loss methods use different behaviors to maintain their weight? Int J Obes Relat Metab Disord 1998;22:572–7.[Medline]
36. Tremblay A, Simoneau JA, Bouchard C. Impact of exercise intensity on body fatness and skeletal muscle metabolism. Metabolism 1994;43:814–8.[Medline]
37. Doucet E, Imbeault P, Alméras N, Tremblay A. Physical activity and low-fat diet: is it enough to maintain weight stability in the reduced-obese individual following weight loss by drug therapy and energy restriction? Obes Res 1999;7:323–33.[Medline]

This article has been cited by other articles:

				C. Roy, S. Paglialunga, A. Fisette, P. Schrauwen, E. Moonen-Kornips, J. St-Onge, M. K. Hesselink, D. Richard, D. R. Joanisse, and K. Cianflone Shift in metabolic fuel in acylation-stimulating protein-deficient mice following a high-fat diet Am J Physiol Endocrinol Metab, June 1, 2008; 294(6): E1051 - E1059. [Abstract] [Full Text] [PDF]

				L. Metz, J. Mercier, A. Tremblay, N. Almeras, and D. R. Joanisse Effect of weight loss on lactate transporter expression in skeletal muscle of obese subjects J Appl Physiol, March 1, 2008; 104(3): 633 - 638. [Abstract] [Full Text] [PDF]

				G. R. Hunter, D. E. Larson-Meyer, B. Sirikul, and B. R. Newcomer Muscle metabolic function and free-living physical activity J Appl Physiol, November 1, 2006; 101(5): 1356 - 1361. [Abstract] [Full Text] [PDF]

				L. M. Brewster, G. A. van Montfrans, A. Luke, A. Adeyemo, H. Kramer, T. Forrester, and R. S. Cooper Blood Pressure, Resting Energy Expenditure, and Creatine Kinase Activity * Response: Blood Pressure, Resting Energy Expenditure, and Creatine Kinase Activity: Hypertension, September 1, 2004; 44(3): e6 - e6. [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Citation Map Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Doucet, E. Articles by Joanisse, D. R Search for Related Content PubMed PubMed Citation Articles by Doucet, E. Articles by Joanisse, D. R Agricola Articles by Doucet, E. Articles by Joanisse, D. R