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Energy Economy Hampers Body Weight Loss after Gastric Bypass

Division of Therapeutic Education for Chronic Diseases (E.B.-H., T.L., A.G.) and Clinic of Digestive Surgery (P.M., O.H., G.C., M.V.), Geneva University Hospital; and Medical Biochemistry Department (F.A.-J.), Geneva Medical School, 1211 Geneva 14, Switzerland

Address correspondence and requests for reprints to: Dr. E. Bobbioni-Harsch, Division of Therapeutic Education for Chronic Diseases, Geneva University Hospital, 1211 Geneva 14, Switzerland.

	Abstract

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The impact of energy economy on body weight loss was investigated in 20 obese women, submitted to Roux-en-Y gastric bypass. Resting energy expenditure (REE), substrate oxidation rates, plasma glucose, free fatty acid, and insulin and leptin levels were measured before and 3, 6, and 12 months after surgery. Predicted REE was obtained from linear regression analysis of REE and fat free mass, in a group of 85 women, whose body mass index ranged between 20 and 60 kg/m². The deviation from predicted REE, calculated as area under the curve (AUC) over the 12-month period for each patient, was considered as the expression of energy economy. Energy economy AUC was significantly (P < 0.005) negatively related to the weight lost during 12 months after surgery.

Energy intake, calculated from self-reported food consumption, was also expressed as AUC. Energy intake AUC showed a significant (P < 0.002) positive correlation with weight loss.

Lipid oxidation rate, also calculated as AUC, significantly correlated, negatively, with energy economy (P < 0.001) and, positively, with energy intake (P < 0.002). Preoperative leptin values were significantly (P < 0.01) linked to individual energy economy capacity.

In conclusion, after Roux-en-Y gastric bypass, energy economy hampers the weight loss process, probably through a low fat oxidation rate.

	Introduction

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ENERGY-SPARING MECHANISMS have been more and more convincingly demonstrated to occur in both obese (1, 2, 3, 4) and normal body weight subjects (5) in response to reduced energy intake (En.In.). Although energy economy (En.Eco.) has been claimed to play a role in frustrating body weight loss efforts, until now no direct evidences of this potential role are available. Furthermore, it is not clear whether En.Eco. occurs in all patients submitted to a reduced En.In. or if it rather depends on intrinsic characteristics of the subjects and/or the degree of energy restriction. This question arises from the observation that, in the literature, a great individual variability in the modifications of energy expenditure has been reported within a group of patients submitted to the same caloric restriction (6, 7, 8); on the other hand, the amount of energy spared averaged 10–15% according to different studies (6, 7, 8, 9, 10), where caloric intake ranged from 300-1000 kcal/day. It would also be important to establish how early En.Eco. takes place and how long it lasts. In fact, although it has been reported that En.Eco. could occur as soon as 3 days after the beginning of a hypocaloric diet (10), it is not clear whether the extent of En.Eco. remains constant or varies along the period of restricted En.In. (i.e. during the phase of active body weight loss). Little is known about the modifications of substrates oxidative patterns underlying En.Eco. Two studies, where these measurements were performed, describe an increase in glucose and a decrease in lipid oxidation; it should be pointed out, however, that in one of these studies body weight loss was obtained by biliopancreatic bypass (4), a surgical procedure inducing malabsorption that mainly concerns lipids (11); in the other study, postobese patients were submitted to a high carbohydrate (55%) weight-maintaining diet (12). Therefore, the described modifications in oxidative patterns could be linked to the surgical procedures and/or to the carbohydrate content of the diet, rather than to the En.Eco. process. This conclusion is suggested by a recent study describing the occurrence of metabolic adaptation after vertical banded gastroplasty (13). In fact, after this restrictive surgical procedure, glucose and protein oxidation were remarkably reduced, whereas fat oxidation was increased.

To contribute to the clarification of some of the above mentioned points, we investigated the metabolic modifications during the phase of active body weight loss induced by Roux-en-Y gastric bypass (14). This procedure, extensively used in the surgical therapy of obesity (15), promotes substantial body weight loss mainly by reduction of En.In. and, differently from biliopancreatic bypass or jejuno-ileal anastomosis, only to a little extent by malabsorption.

The first aim of this study was to investigate the impact of En.Eco. on body weight reduction process, following Roux-en-Y gastric bypass. The second aim was to characterize the metabolic modifications that could underlie En.Eco., during the active phase of body weight loss.

	Materials and Methods

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A group of 20 obese women [mean age, 38.9 ± 2.5 yr; initial body mass index (BMI), 43.9 ± 1.3 kg/m²] were studied before and 3, 6, and 12 months after Roux-en-Y gastric bypass. According to this surgical procedure (14), a small stomach pouch is first separated from the distal stomach; then, a Y-shaped section of the small intestine is connected to the gastric pouch, to bypass the duodenum and a part of the jejunum. Finally, this bypassed portion of the intestine is attached more distally to the small bowel. The protocol of this study received the approval of the Ethical Committee of the Department of Surgery of the Geneva University Hospital. The patients were informed about the aims of the study and gave their written consent. All the measurements were performed after an overnight fast. Body composition was determined by bioelectrical impedance (16). After urine and blood samples were collected, the patients were placed in a recumbent position with the head in a ventilated hood (Deltatrac; Datex Corp., Helsinki, Finland) to measure V02 consumption and VC02 production, as described previously (17, 18). After a 15-min equilibration period, gas exchanges were measured for 30 min and used to calculate the respiratory quotient and glucose and lipid oxidation rates, according to Lusk (19). Protein oxidation was calculated as 6.235 N, where N is nitrogen excretion (mg/min) in urine. Resting energy expenditure (REE) was calculated from the rates of substrate oxidation. Here, this value will be referred as measured REE (mREE; kcal/day). As reported previously (8), the within individual coefficients of variability were: 6.0% for glucose and 7.4% for lipid oxidation; 1.3% for respiratory quotient; 2.4% for mREE.

Predicted REE (pREE) was calculated according to the equation obtained from linear regression analysis linking mREE and fat free mass (FFM) in a group of 85 women whose REE was measured by indirect calorimetry and FFM by bioelectrical impedance, in conditions of stable body weight. The group had the following characteristics: age, 38 ± 2 yr (range, 18–54); body weight, 105 ± 3 kg (range, 53–168); FFM. 56 ± 1 kg; BMI, 40 ± 1 (range, 20–60).

pREE was calculated as:

The deviation from pREE (kcal/day) was calculated for each patient at each time point as:

The deviation of mREE from pREE indicates the reduction of mREE below the extent that can be accounted for by the reduction in FFM; therefore, this value will be referred as En.Eco. (kcal/day).

En.Eco. was calculated as the area under the curve (AUC), using the values of deviation of mREE from pREE measured in basal conditions and at each postoperative time point. The same procedure was followed to calculate the AUC of lipid, glucose, and protein oxidation rates.

Energy requirement (En.Req., kcal/day) was calculated as:

En.In. (kcal/day) was calculated by a dietician on the basis of food record that each patient was instructed to fulfill during 3 days before each visit. Plasma glucose was enzymatically determined (20) using Automated Glucose Analyzer (Beckman Coulter, Inc., Fullerton CA); plasma free fatty acid (FFA) concentrations were also enzymatically determined (21), using a commercial kit (NEFA kit; WAKO, Neuss, Germany); insulin was measured by RIA (22), as well as leptin (Linco Research, Inc., St. Charles, MO).

Statistical analysis was performed using ANOVA for repeated measurements, simple or multiple regression analysis (Statview 4.5; Abacus Concepts Inc., Berkeley, CA).

	Results

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As shown in Fig. 1, body weight progressively declined from 116.8 ± 4.0 before surgery to 79.7 ± 3.1 kg 12 months later. The total body weight loss ranged from 18.6–58.8 kg. FFM also decreased from 59.3 ± 1.8 to 49.2 ± 1.2 kg; one year after surgery, FFM reduction represented 32.1 ± 1.2% of the total weight loss. mREE (Table 1) significantly declined over the study period from 1823 ± 45 to 1475 ± 34 kcal/day. pREE (Table 1) also progressively declined after surgery. ANOVA for repeated measurements showed a significant (P < 0.0001) effect of time for both mREE and pREE. When expressed as a mean value, mREE did not significantly differ from pREE either in basal or in postoperative conditions (ANOVA for repeated measurements, P = 0.48). However, the extent and the evolutive pattern of mREE reduction largely varied from one subject to another. For this reason, En.Eco. AUC (kcal/day) was calculated for each patient, over the 12-month period, as indicated in Materials and Methods. As shown in Fig. 2A, a significant (r² = 0.37, P < 0.005) negative relationship linked En.Eco. AUC and the amount of weight lost during the same period. Self-reported En.In. (kcal/day) is shown in Table 2. When calculated as AUC (Fig. 2B), En.In. was significantly (r² = 43, P < 0.002) positively related to body weight reduction. A multiple regression analysis (Table 3) showed that En.Eco. and En.In. were significantly and independently related to body weight loss (r² = 0.56; P < 0.05 for En.Eco.; P < 0.02 for En.In.).

View larger version (10K): [in this window] [in a new window]   Figure 1. Modifications of body weight (1 ) and FFM (m) after Roux-en-Y gastric bypass. ANOVA for repeated measurements: effect of time. Body weight: f = 203, P < 0.0001; FFM: f = 102, P < 0.0001.

View larger version (22K): [in this window] [in a new window]   Figure 2. A, Relationship between energy economy, expressed as AUC, and the amount of weight (kg) lost during the 12-month study period (r2 = 0.37, P < 0.005). B, Relationship between energy intake AUC and the amount of weight (kg) lost during the 12-month study period (r2 = 0.43, P < 0.002).

View larger version (23K): [in this window] [in a new window]   Figure 3. A, Relationship between energy economy, expressed as AUC, and the lipid oxidation rate AUC, during the 12-month study period (r2 = 0.48, P < 0.001). B, Relationship between energy intake AUC and the lipid oxidation rate AUC, during the 12-month study period (r2 = 0.44, P < 0.002).

	Discussion

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In normal body weight subjects, Dulloo and Jacquet (25) found that the extent of En.Eco. was positively correlated to the amount of fat reserves lost during a 24-week period of semistarvation. The authors, therefore, suggest that the reduction of REE below the FFM loss was a consequence of body fat depletion and interpreted this phenomenon as a physiological, survival-aimed mechanism. In contrast to Dullo and Jacquet (25), we observe a significant negative correlation between En.Eco. and body weight loss: in other terms, the largest En.Eco., the smallest weight reduction. This may indicate that En.Eco. is activated sooner in obese than in lean subjects. In fact, assuming that metabolic adaptation takes place very soon after the beginning of the caloric restriction, that could explain why, in obese subjects, En.Eco. becomes a determinant factor (and not a consequence) of body weight loss. This hypothesis is supported by the results from Fricker et al. (10), who have demonstrated a very early occurrence (within 3 days) of En.Eco. in obese subjects submitted to caloric restriction.

Contrary to our results, Flancbaum et al. (26) reported an increase of mREE compared with pREE following gastric bypass-induced body weight loss. These contrasting results could be attributed to several reasons because of, for instance, the different calculation of the deviation from pREE. In fact, in the study by Flancbaum et al. (26), pREE was calculated by the Harris-Benedict formula. Furthermore, pREE so obtained was lowered by 15–30% because of the decrease of REE, in conditions of restricted En.In. This, of course, makes the occurrence of metabolic adaptation difficult to detect. Finally, it should be noted that, also in our study, a third of the patients showed a mREE higher than the pREE: a different composition of the study groups could also have contributed to the contrasting results.

En.In. was calculated on the basis of anamnestic data of food consumption, which is known to be underreported, particularly by obese subjects (27). This is the case also in our study group, as indicated in preoperative conditions, by the discrepancy (18%) between caloric intake and En.Req. (Table 2). Therefore, postoperative En.In. could also be underestimated. However, it is well established that underreport increases with increasing food intake (27); it is, therefore, reasonable to think that underreport should be less pronounced in the postoperative period, when En.In. is drastically reduced. Furthermore, the significant relationship linking both body weight loss and lipid oxidation AUC to En.In. (Figs. 2B and 3B) clearly supports the reliability of caloric intake results, despite the inaccuracy of a calculation based on anamnestic data. Finally, the values of caloric intake obtained in our study are consistent with the ones reported by several other groups, in comparable experimental conditions (28, 29, 30, 31).

The restriction of energy supply largely influences lipid oxidation rate, as demonstrated by the correlation between En.In. and lipid oxidation AUC (Fig. 3B), and supported by the increase of fat utilization 3 months after surgery, probably in response to the remarkable reduction of caloric intake. On the other hand, energy-sparing capacity seems also involved in the control of fat reserves utilization, because its extent correlates with the fat oxidation rate (Fig. 3A); this significant relationship persists even when En.In. is taken into account in a multiple regression analysis (Table 3). It is interesting to observe that, 12 months after surgery, lipid oxidation is back to basal values (and in 50% of the subjects below). This occurs despite the patients still being in a phase of negative energy balance, as indicated by the body weight profile. The return of fat oxidation to basal values cannot be attributed to a normalization of the fat mass. In fact, a mean BMI of 30.1 ± 1.2 kg/m² 1 yr after surgery indicates that a large amount of fat reserves are still potentially available to provide body En.Req. The reduction of fat utilization could be the consequence of an active mechanism aimed at sparing energy. This is suggested by our results demonstrating a significant negative correlation between the extent of En.Eco. and the lipid oxidation surface over the study period, independent from the reduction of En.In. (Fig. 3A and Table 3). A defect in the lipid oxidation rate has been described in postobese, weight-stable subjects (32). Our study suggests that a relative defect in fat utilization could occur in some subjects already in the active phase of body weight loss. This relative defect may become absolute when body weight is stabilized. It has been proposed that a low lipid oxidation rate could contribute to the relapse of obesity after body weight stabilization (32). Our data indicate that a low lipid oxidation rate can hamper and/or slow down body weight reduction during the active phase of body weight loss. Glucose and protein oxidation are reduced 3 and 6 months after surgery, and then returns to basal values. Glucose and protein oxidation rates have been reported to be regulated by their own intake (33, 34); that could explain the substantial reduction in the utilization of these substrates observed during the early postoperative phase, when En.In. is the lowest. It is interesting to note that an increase in glucose oxidation has been described, after jejuno-ileal anastomosis (4), already during the phase of active body weight loss. This different result probably depends on the fact that the main consequence of jejuno-ileal anastomosis is lipid malabsorption (35), whereas En.In. is only slightly reduced (36). As a consequence, dietary carbohydrates become the main energetic resource in patients submitted to this surgical procedure. Glucose and insulin plasma levels are remarkably reduced after surgery, this confirming the well documented beneficial effect of surgical therapy of obesity on diabetes and insulin resistance (37, 38). Consistent with our previous results (8), leptin plasma levels, as measured in condition of stable body weight, are significantly (P < 0.01) negatively linked to the capacity to spare energy, when energy supply is reduced. Leptin plays this predictive role independently of the preoperative degree of obesity (i.e. initial FM). On the other hand, leptin does not seem to be involved in the postoperative modifications of lipid oxidation. In fact, leptin maintains its significant negative relationship to energy-sparing capacity even when lipid utilization is taken into account (Table 6).

Preoperative insulin plasma concentration does not show a significant relationship to En.Eco. (Table 6). However, fasting circulating values do not represent a sufficient parameter to rule out insulin from a possible involvement in the development of En.Eco.

In conclusion, this study demonstrates a direct negative effect of En.Eco. on the body weight loss process. Metabolic adaptation hampers body weight loss possibly by influencing lipid oxidation activity and by reducing the caloric deficit. The mechanisms involved in this phenomenon remain to be elucidated. The knowledge of the signals activating and the mechanisms underlying En.Eco. in obese patients, despite the presence of excessive fat reserves, would greatly help our understanding of the physiopathology of obesity. Our study also shows that metabolic adaptation capability largely varies from one individual to another. Therefore, it will be important to better elucidate the reasons of this individual variability to detect the subjects who are more prone to develop En.Eco. and, therefore, to counteract the effect of a body weight reducing therapy.

Received February 29, 2000.

Revised August 1, 2000.

Accepted September 6, 2000.

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