0021-972X/00/$03.00/0
The Journal of Clinical Endocrinology & Metabolism
Copyright © 2000 by The Endocrine Society
Vol. 85, No. 12
Printed in U.S.A.
Energy Economy Hampers Body Weight Loss after
Gastric Bypass
E. BOBBIONI-HARSCH, P. MOREL, O. HUBER, F. ASSIMACOPOULOS-JEANNET,
G. CHASSOT, T. LEHMANN, M. VOLERY, AND A. GOLAY
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
ABSTRACT
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) neg-
E
atively 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. (J Clin Endocrinol Metab 85: 4695– 4700, 2000)
NERGY-SPARING MECHANISMS have been more and
more convincingly demonstrated to occur in both
obese (1– 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 – 8); on the other hand,
the amount of energy spared averaged 10 –15% according to
different studies (6 –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 Rouxen-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.
Received February 29, 2000. Revision received August 1, 2000. Accepted September 6, 2000.
Address correspondence and requests for reprints to: Dr. E. BobbioniHarsch, Division of Therapeutic Education for Chronic Diseases, Geneva
University Hospital, 1211 Geneva 14, Switzerland.
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
Materials and Methods
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BOBBIONI-HARSCH ET AL.
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:
pREE 共kcal/day兲 ⫽ 64.5 ⫹ 29.5 ⫻ FFM
The deviation from pREE (kcal/day) was calculated for each patient
at each time point as:
Dev from pREE ⫽ mREE ⫺ pREE
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.Req. ⫽ 1.3 ⫻ mREE
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
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
FIG. 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.
TABLE 1. Modifications of mREE and pREE measured before
and, 3, 6, and 12 months after Roux-en-Y gastric bypass
mREE (kcal/day)
pREE (kcal/day)
Basal
3 Months
6 Months
12 Months
1823 ⫾ 45
1818 ⫾ 52
1585 ⫾ 39
1625 ⫾ 42
1529 ⫾ 34
1538 ⫾ 34
1475 ⫾ 34
1465 ⫾ 36
ANOVA for repeated measurements. Effect of time: f ⫽ 125, P ⬍
0.0001; mREE vs. pREE: f ⫽ 0.52, P ⫽ 0.48, not significant.
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.).
Table 4 shows the evolutive modifications of substrate
oxidative patterns, adjusted by the changes in FFM. ANOVA
for repeated measurements showed a significant effect of
time on the modification of lipids (P ⬍ 0.002), glucose (P ⬍
0.02), and protein (0.02) oxidation rates. The substrates’ utilization returned to the basal values, 12 months after surgery.
When expressed as AUC, fat utilization showed a significant
(r2 ⫽ 0.48, P ⬍ 0.001) positive relationship with the extent of
En.Eco. (Fig. 3A) and a significant (r2 ⫽ 44, P ⬍ 0.002)
negative relationship with En.In. (Fig. 3B). When analyzed by
multiple regression (Table 3), En.Eco. and En.In. remained
significantly and independently related to lipid oxidation
AUC (P ⬍ 0.01 for En.Eco. and P ⬍ 0.02 for En.In.; r2 ⫽ 0.65).
As indicated in Table 5, plasma glucose, insulin, and leptin
levels were reduced after surgery, whereas FFAs were transiently increased. ANOVA for repeated measurements
showed a significant effect of time on the modifications of all
ENERGY ECONOMY HAMPERS BODY WEIGHT LOSS
these parameters. Table 6 indicates that, in a multiple regression analysis, leptin plasma levels, as measured before
surgery, were significantly (P ⬍ 0.01) negatively linked to
En.Eco., independently from both preoperative fat mass and
postoperative lipid oxidation. Preoperative insulin plasma
levels were not significantly linked to En.Eco.
Discussion
Body weight loss induced by Roux-en-Y gastric bypass is
influenced by two factors acting in opposite sense: on one
hand, the drastic reduction of En.In. promotes weight loss,
whereas the individual capability to spare energy hampers
this process. This is demonstrated by the significant relation
that links body weight loss to En.In. (positively) as well as to
En.Eco. (negatively). To our knowledge, this is the first report
demonstrating that energy-sparing mechanisms directly impair body weight loss process. When expressed as mean
values, mREE does not significantly differ from pREE. It
should be noted that, in our study, FFM was measured by
bioelectrical impedance, a method that has been reported to
overestimate FFM loss during body weight reduction (23,
24). An overestimation of FFM loss could, therefore, have led
4697
to an underestimation of the deviation from pREE and, by the
consequence, of En.Eco. More importantly, one of the main
characteristics of energy-sparing capacity is the large individual variability of its extent, as shown by the values of
En.Eco. AUC. This variability, already described by us (8)
and other groups (6, 7) explain why, when expressed as a
mean value, mREE does not significantly differ from pREE.
It is interesting to note that, both in our previous study (8)
and in the present one, patients were submitted to a same
reducing weight therapy: in the former case a dietary restriction of 1000 kcal/day (8), and in the latter case a Rouxen-Y gastric bypass. This suggests that En.Eco. is independent from the treatment adopted to reduce body weight.
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 diffiTABLE 3. Multiple regression analyses
Independent variables
FIG. 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).
Dependent variable: body weight loss
Energy economy AUC
Energy intake AUC
r2 ⫽ 0.56
Dependent variable: lipid oxidation AUC
Energy economy AUC
Energy intake AUC
r2 ⫽ 0.65
Coefficient
P
⫺0.03
0.03
⬍0.05
⬍0.02
0.002
⫺0.001
⬍0.01
⬍0.02
TABLE 2. Energy balance evaluated before and 3, 6, and 12 months after Roux-en-Y gastric bypass
Energy intake (kcal/day)
Energy requirements (kcal/day)
Energy deficit (kcal/day)
a
Basal
3 Months
6 Months
12 Months
1945 ⫾ 83
2369 ⫾ 58
⫺424 ⫾ 85a
897 ⫾ 67
2060 ⫾ 58
⫺1162 ⫾ 85
1090 ⫾ 82
1989 ⫾ 43
⫺898 ⫾ 90
1265 ⫾ 49
1915 ⫾ 45
⫺650 ⫾ 73
This value has been considered as the degree of underreport of self-recorded energy intake.
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BOBBIONI-HARSCH ET AL.
TABLE 4. Substrate oxidation rates measured before and 3, 6, and 12 months after Roux-en-Y gastric bypass
Lipid oxidation (mg/min䡠kg FFM)
Glucose oxidation (mg/min䡠kg FFM)
Protein oxidation (mg/min䡠kg FFM)
Basal
3 Months
6 Months
12 Months
1.35 ⫾ 0.09
1.28 ⫾ 0.19
1.00 ⫾ 0.09
1.74 ⫾ 0.06
0.55 ⫾ 0.15
0.68 ⫾ 0.09
1.62 ⫾ 0.09
0.85 ⫾ 016
0.76 ⫾ 0.09
1.38 ⫾ 0.11
1.13 ⫾ 0.21
1.13 ⫾ 0.18
ANOVA for repeated measurements: effect of time. Lipid oxidation: f ⫽ 5.7, P ⬍ 0.002; glucose oxidation: f ⫽ 4.0, P ⬍ 0.02; protein oxidation:
f ⫽ 3.7, P ⬍ 0.02.
FIG. 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).
cult 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 –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
ENERGY ECONOMY HAMPERS BODY WEIGHT LOSS
4699
TABLE 5. Substrates and hormones plasma levels measured before and 3, 6, and 12 months after Roux-en-Y gastric bypass
Glucose (mmol/L)
FFA (mg/L)
Insulin (pmol/L)
Leptin (ng/mL)
Basal
3 Months
6 Months
12 Months
6.0 ⫾ 0.9
154 ⫾ 13
169 ⫾ 34
64 ⫾ 6
4.9 ⫾ 0.4
177 ⫾ 13
76 ⫾ 9
24 ⫾ 4
4.7 ⫾ 0.1
141 ⫾ 14
60 ⫾ 7
19 ⫾ 3
4.2 ⫾ 0.1
120 ⫾ 10
52 ⫾ 3
15 ⫾ 2
ANOVA for repeated measurements: effect of time. Glucose: f ⫽ 44, P ⬍ 0.01; FFA: f ⫽ 4.8, P ⬍ 0.005; insulin: f ⫽ 15.9, P ⬍ 0.0001; leptin:
f ⫽ 79.3, P ⬍ 0.0001.
TABLE 6. Multiple regression analysis of various parameters
influencing energy economy capacity
4.
Independent variables
Coefficient
P
Dependent variable: energy economy AUC
Preoperative leptin
Preoperative FM
Preoperative insulin
Lipid oxidation AUC
⫺3.2
2.7
⫺68.4
233.5
⬍0.01
0.08
0.06
⬍0.0001
5.
6.
7.
r ⫽ 0.70.
2
8.
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.
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